J. R. Pluske, J. Le Dividich, M. W. A. Verstegen - Weaning The Pig - Concepts and Consequences - Enfield Pub & Dist Co Inc (2003)

Weaning the pig
Concepts and consequences
Edited by:
J.R. Pluske
J. Le Dividich
M.W.A. Verstegen
Weaning the pig – concepts and consequences
Weaning the pig
concepts and consequences
Edited by:
J.R. Pluske
J. Le Dividich
M.W.A. Verstegen
Wageningen Academic
P u b l i s h e r s
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Contents
1 Introduction 15
J.R. Pluske, J. Le Dividich and M.W.A. Verstegen
2 Growth of the weaned pig 17

I.H. Williams
2.1 Introduction 17
2.2 The potential growth of weaned pigs 17
2.3 Description of growth 18
2.4 The growth check at weaning 19
2.5 Bodyweight at weaning - its importance for post-weaning growth 20
2.6 Can weaning weight be increased by supplementary feeding? 21
2.7 Do pigs stimulated to reach higher weaning weights grow faster
to slaughter? 23
2.8 Do pigs exhibit compensatory growth? 25
2.9 The importance of weight gain in the first week after weaning 26
2.10 Minimising the growth check at weaning 27
2.11 Does minimising the growth check have long-term benefits? 29
2.12 Conclusions 31
References 31
3 Nutritional management of the pig in preparation for weaning 37

R.H. King and J.R. Pluske
3.1 Introduction 37
3.2 The importance of weaning weight to subsequent growth 38
3.3 Nutrient intake before weaning 39
3.3.1 Supplying creep food in lactation 39
3.3.2 Dry creep feed intake 40
3.3.3 Liquid diets to enhance feed intake 41
3.3.4 The effects of gender on nutrient intake of neonatal pigs 43
3.4 The composition of diets offered during lactation 43
3.4.1 Dietary formulation of creep diets 44
3.4.2 Use of flavours in creep/starter diets 45
3.4.3 Presentation of the creep diet 45
3.5 Water for suckling pigs 47
3.6 Conclusions 47
References 48
4 Behavioural changes and adaptations associated with weaning 53

P. Mormède and M. Hay
Summary 53
4.1 Introduction 53
Concepts and consequences 7

Contents
4.2 Neuroendocrine consequences of weaning 54

4.3 The critical role of food 54
4.4 Behaviour 57
4.5 Conclusion 57
References 58
5 Metabolic and endocrine changes around weaning 61

F.R. Dunshea
5.1 Introduction 61
5.2 The post-weaning check 61
5.3 Effect of weaning on metabolism 65
5.3.1 Lipid and carbohydrate metabolism 65
5.3.2 Protein metabolism 67
5.4 Hormonal status 68
5.4.1 Somatotropin and insulin-like growth factor-I 68
5.4.2 Insulin 72
5.4.3 Hypothalamic-pituitary axis 72
5.5 Conclusions 74
References 74
6 Factors affecting the voluntary feed intake of the weaned pig 81

P.H. Brooks and C.A. Tsourgiannis
6.1 Introduction 81
6.2 Feeding behaviour of piglets kept under ‘natural’ or
‘semi-natural’ conditions 81
6.3 Commercial weaning practice - an event rather than a process 86
6.4 Pre-weaning feed and water intake 87
6.5 Relationship between pre-weaning food consumption and
post-weaning growth 91
6.6 Feeding behaviour of the post-weaned pig 94
6.7 Feed and water intake of weaned pigs 96
6.8 The significance of maintaining continuity of food intake
after weaning 99
6.9 The interaction between water and feed intake post weaning 102
6.10 Liquid feeding post-weaning 106
6.11 Conclusions 108
References 109
7 Digestive physiology of the weaned pig 117

H.M. Miller and R.D. Slade
Summary 117
7.1 Introduction 117
7.2 Strategies for adaptation to enteral nutrition in the neonatal pig 118
8 Weaning the pig

Contents
7.2.1 Preparation 118

7.2.2 Implementation I 120
7.2.3 Perspective 1 122
7.3 The weaned pig 122
7.3.1 Commercial weaning 123
7.3.2 Gastrointestinal, pancreatic and hepatic response 123
7.3.3 Small intestine morphological response 124
7.3.4 Small intestine carbohydrase and transporter response 127
7.3.5 Amino acid transport 128
7.4 Regulation of post-weaning adaptation 130
7.4.1 Milk withdrawal 130
7.4.2 Weaning stress 131
7.4.3 Direct dietary effects 132
7.4.4 Indirect dietary effects 134
References 139
8 Diet-mediated modulation of small intestinal integrity in

weaned piglets 145
M.A.M. Vente-Spreeuwenberg and A.C. Beynen
Summary 145
8.2 Small intestinal integrity 147
8.2.1 Small intestinal morphology 148
8.2.2 Mucus production 149
8.2.3 Transepithelial permeability 149
8.2.4 Inflammation 150
8.2.5 Brush border enzyme activity 150
8.2.6 Animal performance 151
8.3 Modulation of small intestinal integrity by luminal nutrition 151
8.3.1 Modulation by route of administration 152
8.3.2 Modulation by level of energy intake 155
8.3.3 Modulation by dietary components 159
8.4 Concluding remarks 185
References 186
9 Interactions between the intestinal microflora, diet and diarrhoea,

and their influences on piglet health in the immediate
post-weaning period 199
D.E. Hopwood and D.J. Hampson
Summary 199
9.1 Changes in intestinal microflora at weaning 199

Contents
9.2 Major enteric diseases at weaning 201

9.3 Post-weaning colibacillosis (PWC) 202
9.4 Factors predisposing to post-weaning colibacillosis at weaning 204
9.4.1 The role of the small intestine 204
9.4.2 The role of the large intestine 205
9.4.3 The specific role of diet 205
9.4.4 The specific role of dietary non-starch polysaccharides in PWC 206
9.5 Conclusions 211
Acknowledgements 212
References 212
10 Aspects of intestinal immunity in the pig around weaning 219

M.R. King, D. Kelly, P.C.H. Morel and J.R. Pluske
10.2 Overview of immune systems 220
10.2.1 Active immunity 220
10.2.2 Passive immunity 223
10.3 The intestinal immune system 224
10.3.1 Intestinal inflammation 227
10.3.2 Oral tolerance 228
10.3.3 Development of intestinal immunity 231
10.4 The effect of weaning on the intestinal immune system 233
10.4.1 Overview of the weaning process 233
10.4.2 Alteration of intestinal morphology 234
10.4.3 Activation of the intestinal immune system 236
10.5 Conclusion 244
References 244
11 Nutritional requirements of the weaned pig 259

M.D. Tokach, S.S. Dritz, R.D. Goodband and J.L. Nelssen
Summary 259
11.2 Importance of pig weight and age 259
11.3 Basis of nutrient specifications for weaner pigs 262
11.3.1 Ingredient selection based on digestive capacity 263
11.4 Nutrient requirements of the weaned pig 264
11.4.1 Energy 264
11.4.2 Amino acids 264
11.4.3 Other approaches to determining a requirement estimate 265
11.4.4 Vitamins 268
11.4.5 Minerals 269
11.4.6 Post-weaning diarrhea and zinc oxide. 270
11.4.7 Organic trace minerals 271
10 Weaning the pig

Contents
11.5 Selection of ingredients for the weaned pig 272

11.5.1 Energy sources 272
11.5.2 Protein sources 275
11.5.3 Non-nutritive Feed additives (eg., antibiotics, enzymes,
organic acids, etc.) 282
11.6 Example of phase feeding program for early weaned pigs 283
11.6.1 SEW diet - weaning to 5 kg 283
11.6.2 Transition diet - 5 to 7 kg 285
11.6.3 Phase 2 - 7 to 11 kg 286
11.6.4 Phase 3 - 11.5 to 23 kg 287
11.7 Importance of management in the success of the nutritional
program 288
11.7.1 Management to encourage feed intake 289
11.7.2 Adjust feeders frequently to minimize feed wastage 289
References 290
12 Intestinal nutrient requirements in weanling pigs 301

D. Burrin and B. Stoll
12.2 Changes in gut physiology during weaning 301
12.2.1 Acute phase 302
12.2.2 Adaptive phase 304
12.3 Intestinal nutrient utilization in young pigs 306
12.3.1 Physiological and cellular basis of gut metabolism 307
12.3.2 Major oxidative fuels 311
12.3.3 Essential amino acid utilization 314
12.3.4 Interactions between nutrition and enteric health and function 320
12.4 Summary and perspectives 324
Acknowledgments 324
References 325
13 Environmental requirements and housing of the weaned pig 337

F. Madec, J. Le Dividich, J.R. Pluske and M.W.A. Verstegen
13.2 Environmental requirements of the weaned pig 338
13.2.1 Events related to weaning that affect thermal requirements 338
13.2.2 Ambient temperature 339
13.2.3 Relative humidity and ventilation 343
13.2.4 Lighting 344
13.2.5 Effects of non-optimal climate on performance 344
13.3 Pen structure 346
13.3.1 Flooring materials 346
13.3.2 Feeders and waterers 346

Contents
13.3.3 Stocking densities 347

13.3.4 Group size 348
13.4 Housing as a cause of poor health of weaned pigs 349
13.4.1 Evidence that housing conditions predispose pigs to digestive
disorders 349
13.4.2 Impact of non-optimal indoor climate on the pig’s health status 350
13.4.3 Multifactorial nature of post-weaning disorders: risk factors
associated with housing and management 351
13.4.4 Integrating the risk factors to improve health 353
13.5 Conclusion 353
References 355
14 Saving and rearing underprivileged and supernumerary piglets,

and improving their health at weaning 361
J. Le Dividich, G.P. Martineau, F. Madec and P. Orgeur
14.2 What are underprivileged and supernumeraries? 362
14.3 Reasons accounting for variation in birthweight and
weaning weight 363
14.3.1 Variation in birth weight 363
14.3.2 Variation in weaning weight 364
14.4 Differences between underprivileged and “normal” piglets 365
14.4.1 Body composition 365
14.4.2 Performance of underprivileged pigs 366
14.5 Management practices to improve survival and growth of the
underprivileged pigs 367
14.5.1 Providing assistance to the underprivileged piglets at birth 368
14.5.2 Cross fostering 369
14.5.3 Split weaning 370
14.5.4 Feeding strategy 370
14.6 Growth potential of underprivileged piglets 371
14.7 Supernumerary piglets 371
14.7.1 Weaning at day 1-3 372
14.7.2 Fostering onto a nurse sow 372
14.7.3 Weaning at one week of age 372
14.8 Management to improve the health of piglets 373
14.8.1 All-in / All-out management system 373
14.8.2 Segregation 374
14.9 Conclusion: the need for research 376
References 377
12 Weaning the pig

Contents
15 Productivity and longevity of weaned sows 385

A. Prunier, N. Soede, H. Quesnel and B. Kemp
15.2 Reproductive causes of culling 385
15.3 Consequences of lactation and weaning on the reproductive
axis 388
15.3.1 Postpartum inhibition 388
15.3.2 Removal of the inhibition of the hypothalamic-pituitary-
ovarian axis at weaning 392
15.4 Variation in reproductive performance: extent and sources of
variation 394
15.4.1 Components of fertility and prolificacy 394
15.4.2 Influence of nutritional factors 394
15.4.3 Influence of lactational characteristics 402
15.4.4 Influence of the physical and social environment 404
15.4.5 Relationships between WEI, litter size and farrowing rate 406
15.5 Conclusion 408
References 409
Conclusions 421
List of authors 422
Index 425

1 Introduction
The weaning age of pigs has been reduced from about 8 weeks of age in the 1950s
and 1960s down to a current average weaning age of 22-26 days of age that is
practiced in many pig-producing countries, although even earlier weaning ages
(< 21 days) are adopted with some systems. The reduction in weaning age
occurred largely because of the productivity increases, both in the growing and
breeding herds, which were achievable. However, the inevitable shift to earlier
weaning ages presented many problems concerning the nutrition, housing, health,
behavioural and environmental requirements of the young pig, as well as having
consequences for the fertility of the sow. These are especially pertinent in systems
where pigs are weaned at less than 21 days of age, such as segregated early weaning
practices. Much research, combined with field experience, has minimized the
stressors encountered at weaning so that good levels of production can be
achieved after weaning.
Nevertheless, changes in the global business of pig production continue to occur

and must be dealt with. Of recent interest, particularly in Europe, has been the
increasing awareness in society with respect to animal welfare, food safety, the
environment, and the ‘quality’ of production, especially with respect to antibiotics
as growth promoters. These (relatively) recent events have instigated a flood of new
research into fields concerning, for example, optimum gut ‘health’ and immune
function that, until recently, have largely been ignored in weaner pig production.
Consequently, issues such as enteric diseases, welfare and the intestinal nutritional
requirements of the weaned pig are under increased scrutiny and attention as
producers, feed manufacturers, scientists and managers attempt to resolve these
new issues. It is also increasingly evident that the events surrounding weaning can
have profound and life-long consequences in both the growing and breeding herds.
Collectively, the process of ‘weaning’ has never been considered as more important
as it is nowadays.
In light of these changes and developments, “Weaning the Pig: Concepts and
Consequences” is timely and has been compiled to provide the reader with an up
to date account of all facets related to the weaning process, including the fate of
the weaned sow. The material in the book covers the following areas associated
with the weaning process: growth of the weaned pig, nutritional management in
preparation for weaning, behavioural changes and adaptations around weaning,
voluntary feed intake, digestive physiology, modulation of small intestinal integrity,
the intestinal microflora and diarrhoeal diseases after weaning, intestinal immunity,
nutritional requirements and intestinal requirements of the weaned pig,
environmental and housing issues after weaning, saving and rearing supernumery
and underprivileged piglets, and productivity and longevity of the weaned sow.

Pluske, Le Dividich and Verstegen
World-renowned experts and specialists from numerous countries have written the
chapters, and are applicable to all people involved in pig production, health and
disease, research, management and extension throughout the world. The information
contained can be used to modify and (or) develop nutritional, environmental,
housing, disease, welfare and management strategies to best handle the weaning
process. Developments in our knowledge may also help to update courses in the
field of pig science and to interest those who teach animal production principles.
John Pluske
Jean Le Dividich
Martin Verstegen
16 Weaning the pig

2 Growth of the weaned pig
I.H. Williams
2.1 Introduction
Pigs are capable of extremely rapid growth after weaning but there are a host of
factors that limit the extent to which this potential is expressed. The weight of the
pig at weaning, its nutrition and growth rate in the immediate post-weaning period,
and the physical, microbiological and psychological environment are all factors
that interact to determine food intake and subsequent growth. The age at weaning
is variable and so weight at weaning can vary two or three fold. In most countries
it is common practice to wean at 3 to 4 weeks when pigs weigh in excess of 6 kg
but, in other countries, particularly North America, weaning pigs before three weeks
of age of age is common. The main reason for early weaning is to reduce the transfer
of disease from the sow but younger, lighter piglets require a higher standard of
management and require better nutrition and more stringent environmental
conditions.
This chapter begins by outlining the young pig’s potential for growth followed by
a simple description of growth and its principles. This is followed by a consideration
of how bodyweight and nutrition impinge on growth. Other factors that limit growth
will be considered in subsequent chapters.
2.2 The potential growth of weaned pigs

Growth rates of 100, 200 and 400 g/d in the first, second and third weeks after
weaning at 21 days have been suggested by Whittemore and Green (2001) as
commercially acceptable targets in the absence of observed clinical disease and overt
stress. However, these growth rates represent substantial underperformance. The
same authors suggest that a healthy pig at 3 weeks of age weighing 5 kg and given
unrestricted food intake in the experimental facility at Edinburgh will grow at 500
g/d, twice the commercial performance.
Yet even this rapid growth may not represent the true growth potential of the young
pig. If piglets are weaned very early in life (1 to 2 days) and given liquid diets based
on cow’s milk, growth rates in excess of 500 g/d can be achieved. For example, Hodge
(1974) removed piglets from the sow when they were 2 days old and fed them ad
libitum on reconstituted cow’s whole milk. Between 10 and 30 days of age his pigs
grew at 571 g/d and between 30 and 50 days of age they grew at 832 g/d. Similar
growth rates for piglets removed from sow at 2 days of age and fed milk have been
demonstrated by Williams (1976) and by Harrell et al. (1993). If similar

Williams
experiments to those of Hodge (1974) were conducted with modern-day genotypes,

piglets might grow even faster on milk and demonstrate a higher potential.
There can be no doubt that the potential for growth of the young pig is extremely
high and is between two and three times that which is commonly observed under
the best commercial conditions. The question is, why is this potential rarely if ever
reached and what can be done to lift performance closer to potential?
2.3 Description of growth

There has been much debate in recent years about the best way to describe growth
because of the interest in modelling growth (Black, 1995). Most models are based
on a prediction of the protein mass and its incrementation, and some defined
relationship between the gain in protein and lipid. Gains in protein and lipid are
summed to give gain in liveweight. If the liveweights of animals that have been
fed ad libitum on high-quality diets throughout life are plotted against time they
produce an “S-shaped” curve, termed a sigmoidal growth curve (Lawrence and
Fowler, 1997). Whittemore and Green (2001) have put forward a compelling
argument that the sigmoid growth in pigs from birth to maturity can best be
described by a Gompertz function:
Daily gain = liveweight * B * ln(weight at maturity/liveweight),
where B is a growth coefficient.
Sigmoidal growth has two main phases. The first is early in life where growth
increases. The second is where growth decreases and finally ceases when animals
reach maturity. These phases are linked at the point of inflection where growth is
linear and this generally occurs at approximately one third of mature body size
(Lawrence and Fowler, 1997). The weaned pig fits into phase one, that of
increasing or accelerating growth.
The Gompertz function requires two parameters, an asymptote or description of

maturity and a growth coefficient, which are not independent of each other. An
increase in one will be accompanied by an increase in the other.
This has some important ramifications for the growth of animals. It means that
animals have predetermined growth paths and that there are large, fast growing
animals and smaller, slower growing animals. It means that a larger genotype or
a pig with a greater propensity for growth will, at any age, be bigger and grow faster
than a smaller genotype.
18 Weaning the pig

Growth of the weaned pig
What the Gompertz function does not describe is the growth check that usually
occurs at weaning and the recovery phase that follows. At weaning it is common
for piglets to lose weight and display negative growth for several days and not recover
their pre-weaning weight for perhaps 7 or even 10 days (Pluske et al., 1995). When
they do begin their recovery phase, do they exhibit any signs of compensation?
That is, do they grow faster than their contemporaries at the same weight who have
not experienced the same check in growth or do they grow at the same rate and
simply take longer to market weight. This will be addressed later in this chapter.
2.4 The growth check at weaning

At weaning the piglet faces three challenges. First, there are major changes to its
food supply. Not only does the piglet have to find its own food from a creep feeder
but the new food is more bulky, is often composed of ingredients that the piglet
has not previously encountered, and it is 88% dry. By contrast, sow’s milk is 80%
water and the dry matter (20%) is composed of protein (30%), fat (40%) and lactose
(25%), but no starch. True digestibilities of fat and lactose are close to 100% and
ileal digestibilities of amino acids are also very high at 92% (Mavromichalis et al.,
2001). Creep feed is less digestible (80 to 90%), often contains a mixture of plant
and animal proteins, contains mostly starch instead of lactose, and has very little
fat relative to sow’s milk. As a consequence the digestive tract of the piglet has to
make a major shift away from digesting fat towards digesting complex carbohydrates.
In addition, it has to cope with a very large increase in dry matter intake if the
growth of the newly-weaned piglet is to be maintained. For example, a piglet growing
at 250 g/d would need to eat about 200 g of dry matter per day from sow’s milk
while consumption of a high-density creep would need to reach at least 300 g/d,
a 50% increase, and even more if lower-quality creep diets are used.
Associated with these changes in the supply of food are alterations of the digestive
tract that may have long-term (one or more weeks) ramifications. When the milk
supply ceases abruptly the structure and function of the digestive tract begins to
change immediately within hours. Villous height reduces, crypt depth increases,
and there is a reduction in the absorptive capacity because the specific activity of
the digestive enzymes, lactase and sucrase, decreases. Poor absorption of nutrients
in the small intestine is often associated with proliferation of enterotoxigenic bacteria
(mainly Escherichia coli) and/or fermentation of less digestible nutrients in the large
intestine (McCracken and Kelly, 1993). Either way, this may lead to diarrhoea.
The second major challenge at weaning for the piglet is to cope with the change
in the physical environment. At weaning litters are generally mixed together into
weaner pools. Having learnt to live in the farrowing pen with its mother and
littermates it now has to learn to live without its mother and face competition with
many more pigs, up to 250. The problem is to design a weaner pen that allows

Williams
individual piglets to find their own comfort zone. Because of the great variation
in food intake it is almost impossible to design an environment where all piglets
will be within their thermoneutral zone. For example, when a piglet increases its
food intake from maintenance to twice maintenance its lower critical temperature
is reduced by 3°C (Close and Stanier, 1984). So there could be a difference of 12°C
in lower critical temperature between a piglet that is not eating compared with one
that is eating at maximum, say 4 times maintenance. If room temperatures are set
to keep the pigs that are eating within their thermoneutral zone then the piglets
not eating will be severely cold stressed. If room temperatures are raised so that
piglets not eating are within their comfort zone, other piglets that are eating are
likely to be heat stressed.
The third challenge at weaning is the psychological stress that accompanies

moving and mixing. Although many workers believe that this depresses growth
the extent of this influence is unknown, but will be considered in a subsequent
chapter.
When all these changes are taken into account it is little wonder that the rate of
growth of the piglet falls after weaning, and the extent of the depression in growth
depends on how rapidly the piglet can adjust to its new circumstances and regain
homeostasis.
2.5 Bodyweight at weaning - its importance for

post-weaning growth
The Gompertz description of growth predicts that a pig of large mature body size
will be larger and grow faster at any given age than a pig of smaller size. Producers
have always known that heavier pigs at birth are heavier at weaning and that heavier
pigs at weaning grow faster after weaning than smaller pigs and, in most instances,
are also heavier at slaughter. So the difference in weight at weaning is not just
maintained but it is magnified as the pig grows because the heavier pigs grow faster
than their lighter counterparts at all ages.
There are several studies that substantiate this view. Birth weight is positively
correlated with weight at weaning (McBride et al., 1965; McConnell et al., 1987;
Cranwell et al., 1995; Dunshea et al., 2003), weight at one week of age is highly
correlated with weaning weight (Miller et al., 1999) and weight at weaning is highly
correlated with post-weaning performance (Miller et al., 1999; Lawler et al., 2002).
There are also several studies where bodyweights at various ages have been
quantified for their influence on subsequent growth to slaughter. Campbell
(1989) analysed the weaning records from a large piggery in Australia and found
that a difference of 1.8 kg between pigs weaned at 25 to 29 days of age (6.14 verses
7.95 kg) increased to 5 kg at 78 days and 10 kg at 150 days. Mahan and Lepine
20 Weaning the pig

(1991) found that pigs with weaning weights of 4.1 to 5.0 kg required 11 to 20
days longer to reach slaughter at 105 kg than piglets with weaning weights of 7.3
to 8.6 kg. More recently, Wolter and Ellis (2001) reached a similar conclusion after
they found that a difference of 1.5 kg (3.9 versus 5.4 kg) in pigs weaned at 3 weeks
of age was translated into a growth difference of 8.6 days at slaughter. In a most
comprehensive study on lifetime and post-weaning determinants of performance
indices of pigs Dunshea et al. (2003) found that a difference in birthweight of 0.37
kg (1.86 vs 1.39 kg) had increased to 1.9 kg (5.22 vs 3.21 kg) by two weeks of age
and 13 kg (107.1 vs 94.3 kg) by 23 weeks of age.
Because of the great importance of bodyweight at weaning, research has focused

on two questions. Can the growth of piglets during lactation be stimulated so that
they are heavier at weaning and, if so, will this larger pig at weaning outperform
a lighter counterpart in growth after weaning?
2.6 Can weaning weight be increased by

supplementary feeding?
The main argument for offering sucking piglets supplementary food from a creep
feeder is that it can satisfy the ever-widening energy gap between the piglet’s energy
requirements and the dwindling supply of milk. Since Harrell et al. (1993) have
calculated that the supply of sows’s milk probably begins to limit growth at about
10 days of age, piglets offered creep should be heavier at weaning and be better
able to withstand the stresses at weaning. In the 1950s and 1960s when it was
common to wean piglets at 8 weeks of age, Lucas and Lodge (1961) demonstrated
the importance of offering creep feed before weaning. They raised weaning weight
from 12 to 20 kg but found that significant consumption of creep did not begin
until the piglets were four weeks or older. As the age of weaning was reduced to
as little as two or three weeks it was thought that creep feeding might become even
more important because of the susceptibility of smaller pigs to adverse
environmental conditions.
However, despite a large number of studies conducted in many parts of the world
the magic formula that encourages creep consumption before the piglets were 3
weeks of age has eluded research workers and producers. Pluske et al. (1995) analysed
the results of several experiments and reached two conclusions. First, that
consumption of creep feed before weaning is highly variable and at best might
contribute approximately 17% of energy intake and, at worst, zero. Perhaps more
baffling is the relatively poor relationship between the amount of creep consumed
and the weight at weaning suggesting that creep feed might be a substitute for rather
than a supplement to sow’s milk. This is exemplified by the work of Toplis et al.
(1999) who introduced creep at 14 days and then weaned the piglets at 24 days.
Piglets receiving no creep weighed 6.9 kg at weaning, those that were offered creep

Williams
in dry form consumed 91 g over the 10 days and were 6.5 kg at weaning, and piglets
offered creep as a gruel (1:2 meal to water) ate 374 g/piglet over the 10 days and
weighed 6.7 kg. So despite consuming sufficient gruel that should have, by
calculation, increased weaning weight by about 5%, no increase could be measured.
A similar example comes from the work of Brown et al. (1999). They coaxed sucking
piglets to drink cow’s whole milk at 12 days of age and measured a mean dry matter
intake of 332 g dry matter/week between 12 and 19 days, an intake that should
have been sufficient to stimulate growth by about 0.4 kg. Yet they found that the
piglets that drank milk were the same bodyweight as the controls at weaning at
19 days.
Growth of piglets during lactation can be stimulated if food is offered in a liquid

form early enough in life, and Reale (1987) was one of the first to demonstrate
this. He offered milk to piglets when they were a week old and, by the time they
had reached a weaning age of four weeks, they weighed 9.6 kg and had grown an
extra 1.8 kg (24% increase in weight) over piglets not receiving supplementary milk.
Similar results have been obtained by Dunshea et al. (1997b), who offered
supplemental milk to piglets at 10 days of age and measured a 10% stimulation
in growth by the time the pigs were 20 days old.
As suggested above, the success of stimulating growth by offering supplementary

milk during lactation probably depends on the age that piglets are offered the milk.
For example, Armstrong and Clawson (1980) offered milk to piglets at three weeks
of age but failed to stimulate growth suggesting perhaps that piglets were too settled
in suckling behaviour to take in extra milk.
Another way to increase weight at weaning is to split wean the litter, a practice where
half the litter is weaned at say 20 days (generally the heavier pigs) leaving the lighter
pigs to remain suckling for an extra week to obtain more milk per piglet. Several
workers have shown that the light piglets that remain with the sow grow faster than
their counterparts that have to compete with their larger littermates (Cox et al.,
1983; Edwards et al., 1985; English et al., 1987; Pluske and Williams, 1996). For
example, Pluske and Williams (1996) split weaned litters at 22 days of age and
demonstrated that the growth rate of light pigs could be increased by 60% in the
following week. When the light piglets in the split-weaned litters were weaned at
29 days they weighed 15% more than their counterparts in the full litters. This
stimulation of growth was brought about by a 50% increase in milk consumption
because the piglets learned to suck multiple teats and there was a longer duration
of sucking during letdown. More milk per piglet and better growth of piglets might
also be achieved by increasing the milk output of the sow through better nutrition
(see a later chapter by R.H. King and J.R. Pluske) or by infusing sows with insulin
(see McCauley et al., 1999).
22 Weaning the pig

The conclusion is that supplementary feeding during lactation can increase

weaning weight if the food is offered early in life in a liquid form. If the supply
of sow’s milk can be increased then weaning weights are likely to be greater. However
dry diets are unlikely to be effective if offered early in life and are only likely to
be of value in situations where piglets are weaned late, for example, at four or five
weeks of age.
Supplementary or creep feeding has been practised for reasons other than simply
increasing the weight at weaning. It has been suggested that exposure to dry food
would allow piglets to learn how to source dry food from a feeder, drink water,
accustom the digestive tract to dry food, induce the necessary enzymes for its
digestion and help prepare the piglet to cope better with many of the potential
allergens contained in plant foods. Evidence that any of these benefits might accrue
if creep feed is offered is also scarce. Pluske et al. (1995) concluded that there was
a modest but non-significant relationship between gain after weaning and creep
intake during suckling. They questioned the value of creep feeding particularly for
early-weaned pigs but suggested that creep feed may still be of some value for pigs
weaned after 3 weeks of age. However, if piglets can be stimulated to eat a reasonable
quantity of creep feed in lactation it may pay dividends after weaning. By feeding
gruel, Toplis et al. (1999) stimulated piglets to eat 374g of creep over 10 days and,
although this did not increase weaning weight, it did stimulate performance after
weaning. Piglets fed gruel grew 150% faster (49 vs 125 g/d) than piglets that ate
no creep in the first week after weaning and 30% faster (317 vs 416 g/d) for 5 weeks
after weaning.
2.7 Do pigs stimulated to reach higher weaning

weights grow faster to slaughter?
The philosophy for stimulating piglets to reach a higher weaning weight is that
they will behave in a similar way to piglets that are naturally heavier at weaning
and grow faster than piglets not stimulated during lactation. Put another way, can
supplementary nutrition during lactation be used to raise a piglet from a lower to
a higher growth curve? If food intake is genetically determined to drive growth that
is also genetically programmed, as it must be, it is most unlikely that a transient
period of higher-than-normal nutrition will alter a long-term food setting in the
hypothalamus. If this is correct the expectation would be that any increase in weight
brought about an increase in growth would, at best, be maintained and, at worst,
disappear with time.
There have been many attempts to increase weaning weight but relatively few
attempts to measure the long-term benefits. Offering piglets dry food from a creep
has mostly been unsuccessful in stimulating growth during lactation but increasing

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the milk available to each piglet by split weaning or offering it as a supplement

has consistently stimulated growth.
Pluske and Williams (1996) increased the growth of light piglets by split weaning
litters at 3 weeks of age. These piglets grew faster than their contemporaries left as
whole litters and weighed 1 kg more at full weaning at 4 weeks (7.7 vs 6.7 kg).
However by nine weeks of age the difference in weight had vanished (19.3 vs 19.3
kg). Edwards et al. (1985) achieved a weight difference of 0.4 kg by split weaning
and noted that post-weaning growth rate was no different between the heavy and
light pigs. Wolter et al. (2002) stimulated the growth of piglets by offering
supplementary milk at 3 days of age. By 3 weeks the supplemented piglets weighed
0.9 kg more (6.6 vs 5.7 kg) than the unsupplemented piglets. This increase in weight
was not translated into a significant increase in post-weaning growth and overall
growth from weaning to 110 kg was almost identical for the supplemented versus
the unsupplemented pigs (827 vs 820 g/d). By contrast Dunshea et al. (1997a) found
that increasing growth rate during suckling had longer-term benefits. They found
that skim milk fed to piglets at 10 days of age increased weaning weight by 0.7 kg
of (7.3 vs 6.6 kg) and that this extra growth was still evident at 42 days (14.7 vs
12.2 kg) and 120 days (64.5 vs 60.6 kg).
Do the data of Dunshea et al. (1997a) suggest that supplementary feeding has
stimulated piglets to a higher growth path? The answer is uncertain but recent data
from Wolter et al. (2002) are helpful in addressing this question. In an elegant
experiment and, to my knowledge the only one of its kind, Wolter et al. (2002)
investigated how weaning weight affected growth to slaughter. They attempted to
measure the importance of weaning weight as a measure of the growth curve versus
weaning weight as consequence of previous nutrition. They separated piglets into
light and heavy at birth and supplemented half the piglets with a milk replacer
beginning at three days of age (Table 2.1). By separating pigs at birth into light
Table 2.1. How birth weight (Heavy vs Light), weaning weight and supplementary milk
in lactation (Milk vs No milk) influence food intake and growth to slaughter (from
Wolter et al., 2002).
Heavy Light Milk No milk
Weight (kg)
Birth 1.83 1.38 1.58 1.58
Weaning (20d) 6.6 5.7 6.6 5.7
Weaning to 110 kg liveweight
Food intake (g/d) 1866 1783 1841 1808
Growth rate (g/d) 851 796 827 820
24 Weaning the pig

and heavy they achieved a weight difference at weaning of 0.9 kg. The same difference
in weight was induced at 20 days by feeding half the piglets supplementary milk.
The pigs that were heavier at weaning because of their birth-weight advantage ate
more food and grew faster (7%) after weaning than their lighter counterparts. By
contrast, the pigs that were heavier at weaning because they were offered
supplementary milk during lactation failed to maintain the advantage and
consumed similar amounts of food as their lighter counterparts. Wolter et al. (2002)
concluded that supplemental milk replacer is unlikely to be an effective strategy
for increasing post-weaning performance.
However, the work of Dunshea et al. (1997a) cannot be ignored and a possible
explanation of their results is that they provided a supplement that allowed pigs
to exhibit compensation, a topic discussed in the next section.
2.8 Do pigs exhibit compensatory growth?

Compensatory or catch-up growth is the growth of an animal fed ad libitum after
a period of nutritional stress, and it is higher than the growth of a genetically-identical
animal in the same environment at the same body weight during normal growth
(Hogg, 1991). Interest in compensatory growth began initially with grazing
animals because in most temperate parts of the world there is an abundance of
food at one time of the year and a scarcity at another. This leads to rapid growth
at one time of the year followed by weight loss at another.
Whether animals exhibit compensatory gain after a period of restriction depends

on several factors including the severity of restriction, the duration of the restriction
and the stage of maturity when the restriction is applied; the younger the animal,
the less likely it is to exhibit compensatory growth. For example, sheep less than
3 months old (Ryan, 1990) and cattle below 4 months old (Morgan, 1972) do
not show compensatory growth. Pigs might be different. McCance (1960) weaned
piglets at 10 days of age and severely restricted their food intake so that they gained
only 2 kg in a year. When allowed to rehabilitate with food offered ad libitum they
grew at high rates and, according to Widdowson and Lister (1991), showed some
signs of compensatory growth despite the young age at which their gross nutritional
insult was imposed.
Despite an exhaustive literature on compensatory growth (see reviews by

O’Donovan, 1984; Ryan, 1990; Hogg, 1991; Lawrence and Fowler, 1997) the
underlying mechanisms remain elusive. The most consistent observations in
compensating animals are that they are more efficient in the initial stages of
rehabilitation and that this may be followed by a higher-than-normal food intake.
The common explanation for increased efficiency involves changes in size and
possibly metabolic activity of the internal organs such as the liver, kidney, and gastro-

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intestinal tract. In a well-nourished animal these organs make up 10 to 15% of

the liveweight and make a disproportionately high contribution to the fasting heat
of production, about 40% (Koong et al., 1983). When nutrition is restricted these
organs reduce in size and possibly metabolic rate and this allows the animal to
conserve energy and function on less. When rehabilitation begins and food becomes
available, these organs take time to build up their size and metabolic rate and, in
the meantime, there is extra energy available for the animal to deposit in body tissues.
Pigs reared under intensive conditions are in a very different situation from grazing
animals and are rarely short of food or specific nutrients except in the early stages
of their growth, that is, before weaning and just after. At weaning the stresses are
often sufficient to reduce food intake to very low levels and growth is often zero
or negative, a situation where compensatory growth might apply. Sow’s milk has
low protein relative to its energy content and is deficient in protein for maximum
lean gain (Campbell and Dunkin, 1982; Williams, 1995). After about 10 days of
lactation the potential intake of milk by the piglets begins to exceed the production
from the sow so growth of the piglets starts to fall below their potential (Harrell
et al., 1993). So the relative deficiency of protein plus the restriction in quantity
of milk that together limit growth represent another situation that might invoke
compensation. Several workers have demonstrated compensatory growth in young
pigs but the most comprehensive experiments are those of Campbell and Dunkin
(1983a, b and c) who have clearly demonstrated that very young pigs will
compensate when deprived of protein or energy or both, and will do so even when
given fixed intakes of food.
In the previous section reference was made to work of Dunshea et al. (1997a) who
supplemented piglets at 10 days of age with skim milk and measured a 0.7 kg
increase in weaning weight which was still evident at 60 kg liveweight. Could it
be that the skim milk allowed the piglets to compensate and return to their pre-
programmed growth curve? Since sow’s milk is known to be deficient in protein
for maximum lean gain, skim milk with its high protein content would make an
excellent supplement to sow’s milk.
2.9 The importance of weight gain in the first week

after weaning
The aim of producers is to encourage piglets to make a smooth transition between
drinking milk from the sow and eating solid feed after weaning with minimal
interruption to growth. The importance of the rate of growth in the first week after
weaning in determining growth to slaughter is shown in calculations made by Pluske
et al. (1995). They analysed data from Pollman (1993) showing that if pigs
maintained weight during the first week after weaning they reached slaughter weight
in 178 days but, if pigs grew at 115 g/d or better in the first week, age at slaughter
26 Weaning the pig

was reduced by 15 days to 163 days. This means that a 0.9 kg weight difference
one week after weaning becomes a 12 kg difference in weight at slaughter.
Similarly, Tokach et al. (1992) showed that pigs gaining 225 g/d were 1.6 kg heavier
at the end of the first week after weaning than pigs that maintained weight and
were 8 kg heavier at slaughter at 156 days.
2.10 Minimising the growth check at weaning

The extent and duration of the interruption or growth check is highly variable. Pluske
et al. (1995) concluded that it often takes pigs two or even three weeks to recover
their energy intake and grow at the same rate as they did before weaning, let alone
grow faster to begin to reach their potential. Minimising the growth check at weaning
depends on the amount of food the piglet can eat. Fowler and Gill (1989) calculated
that if a weaned pig at 21 days of age was to grow at 280 g/d, a growth akin to
growth on the sow, it would need to eat 7.8 MJ of DE. Hence, it would need to
eat 500 g of a starter diet containing 15.5 MJ of DE, an intake that is never seen
under experimental conditions let alone in commercial practice.
Campbell (1989) believes that practical nutrition of the young pig at weaning is
more of an art than a science and has suggested that a dietary regime that is highly
successful and repeatable at a research station may not stand up to the rigours of
commercial practice. Such a comment simply reflects the number of factors that
impinge and interact on the animal at weaning. However there are some general
nutritional principles that have been established as far as nutrition of the young
pig is concerned. High food intake and hence high growth rates with minimal
digestive disturbances can only be achieved consistently when high-density,
highly-digestible diets are used. Starter diets are generally required to ease the
transition from milk (high fat, high lactose) to plant based diets that are much
lower in fat, and contain high non-starch polysaccharides. Such diets generally need
to contain high-quality animal products of milk origin and/or products derived
from blood. The younger the pig is at weaning the more important this becomes
and this is nicely demonstrated in recent data from Dunshea et al. (2002a). They
offered piglets a traditional weaner diet containing wheat (55%), lupins (5%),
soybean meal (5%) meatmeal (6.6%), fish meal (8.3%) skim milk (2%) and blood
meal (2.6%) and whey powder (10%) and weaned them at either 14 or 24 days
of age. The older pigs at weaning coped much better than the younger pigs (Table
2.2) with this sort of diet and gained weight during the first week after weaning
while the younger pigs lost weight.
In the 1970s it was generally regarded that the most profitable time to wean pigs
was between 3 and 5 weeks. During the 1980s this changed and interest was
rekindled in weaning pigs earlier largely because of two findings. The first was the
realisation that sow’s milk begins to impose a limit on the growth of piglets at about

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Table 2.2. Age at weaning and its effect on growth (g/d) after weaning (from Dunshea
et al., 2002a).
Age at weaning (d)
Days after weaning 14 24
0-7 -16 162

7 - 14 187 340
14 - 21 333 460
day 10 of age and, by 3 weeks, the limitation becomes severe enough to reduce
piglet growth.
Second, piglets at two weeks of age are relatively free of disease and, the longer
they stay with the sow, the more disease organisms they are likely to acquire. So
early weaning was thought to be a way of reducing and controlling disease and
overcoming the limitation of milk imposed by the sow.
Successful early weaning requires specialised diets if the growth check at weaning
is to be minimised. In the early 1990s, nutritionists at Kansas State University began
to develop a dietary program for early weaning to ease the transition from sow’s
milk to solid food (see chapter by M. Tokach et al.). The program was based on
feeding piglets as soon as they were weaned with milk products and animal plasma
proteins. Products from porcine blood, particularly porcine plasma, have now been
tested in many studies and seem to be mandatory for diets in North America. It
seems that an inclusion rate of 6% is likely to stimulate food intake of young pigs,
particularly in situations where enteric disease is more prevalent (Coffey and
Cromwell, 2001). The most favoured explanation of the stimulation of food intake
is that it is due to the presence of immunoglobulins and presumably
immunoglobulins of pig origin might be more effective than those derived from
cow’s milk. But, because of the concern about feeding animal proteins to the same
species, there is now interest in looking at other sources of immunoglobulins.
Products from cows are also effective in stimulating food intake and growth. Pluske
et al. (1999) weaned pigs at 4 weeks and found that 5% spray-dried colostrum
stimulated food intake by 12% in the first week after weaning. They increased the
amount to 10% and stimulated food intake by 25%. This extra food intake boosted
growth by 40% and 80% respectively so that pigs on the highest level of colostrum
grew in excess of 200 g/d in the first week after weaning, a very acceptable rate of
growth. King et al. (2001) have also found a 25% stimulation to food intake in
the first week after weaning by adding 6% bovine colostrum. They found a lesser,
28 Weaning the pig

non-significant stimulation with spray-dried bovine plasma. Dunshea et al.

(2002b) have recently compared a number of animal products containing
immunoglobulins and, rather than using spray-dried products from commercial
sources, they freeze-dried their own products to preserve the potency of the
immunoglobulins. They compared porcine and bovine plasma, bovine colostrum
and commercially produced skim milk and found relatively little difference
between the protein sources in the performance of pigs weaned at 14 days. However,
they did point out that their studies were conducted in a ‘clean’ research
environment.
There is little doubt that high-quality animal proteins are far superior at stimulating
growth in early-weaned pigs and even small amounts of plant protein will depress
performance (see Dunshea et al., 2002b; Liu et al., 2001).
Advances in technology have allowed liquid feeding systems to be a viable

commercial option and, as a consequence, there is now interest in using liquid
milk to stimulate food intake and growth. Pluske et al. (1996a) demonstrated that,
given a similar intake, fresh milk obtained from sheep maintained villous height
better than a dry diet based on skim milk powder and fish meal. They found that
villous height could also be maintained with fresh cow’s milk and the more milk
consumed the greater the height of the villi or, alternatively, less villous atrophy
(Pluske et al., 1996b). Maintenance of gut architecture after weaning seems a
prerequisite for high food intake and good growth, particularly for pigs weaned
early in life at two to three weeks of age. So feeding liquid milk or milk replacer
at weaning is perhaps the best way of minimising the growth check. Heo et al. (1999)
almost eliminated the growth check by feeding a liquid milk replacer at weaning,
and they achieved a growth rate of 470 g/d for the first 7 days after weaning pigs
at 14. The pigs were held at 24°C in this experiment. When pigs were kept at 17°C,
and presumably cold stressed, growth was reduced to 340 g/d and, when kept at
32°C and possibly heat stressed, growth was also reduced to 360 g/d. Kim et al.
(2001) have also recorded extremely high growth rates with very young pigs weaned
at 11 days of age and fed diets based on whey proteins (70%), lard (12%) and plasma
proteins (5%) fed either in liquid form or as a dry pellet. Pigs fed the liquid grew
at 380g/d while those fed the pellets grew at 260 g/d for the first 14 days after
weaning.
2.11 Does minimising the growth check have long-

term benefits?
Minimising the growth check at weaning has obvious short-term benefits of faster
turnover in the weaner rooms and reductions in mortality and morbidity but there
are very few studies where long-term benefits for growth have been quantified.
Dunshea et al. (1997a) found that skim milk fed to pigs for one week after weaning

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at 20 days of age increased liveweight by 0.6 kg compared with control animals

offered a dry, conventional starter diet. By the time the pigs had reached 120 days
of age the difference in weight had increased to 3 kg (59 vs 62 kg). Pluske et al.
(1999) fed spray-dried bovine colostrum to pigs and, 14 days after weaning at 4
weeks of age, the weight advantage of the pigs fed colostrum was 1.1 kg. This growth
difference was still evident at slaughter at 83 kg. Kim et al. (2001) induced a difference
in weight of 1.6 kg 14 days after weaning by feeding pigs a milk replacer diet in a
liquid rather than a dry pellet. This difference doubled to 3.3 kg by the time the
pigs reached 150 days of age and about 110 kg. So it seems from the few reports
available that stimulation of growth in the immediate post-weaning period by high-
quality animal proteins has a small but beneficial effect on long-term growth.
There has been some suggestion that stimulating post-weaning growth and
minimising the check is unnecessary because pigs will display compensatory growth
and catch up to their contemporaries who have suffered less of a check. Whang et
al. (2000) addressed this by comparing a 3-phase starter regimen containing high-
quality animal products (skim milk, whey, and plasma protein) with a traditional
starter diet based on corn and soybean with minimal fish meal. Pigs fed animal protein
gained liveweight at 175 g/d while the pigs fed the corn/soybean diet lost 38 g/d,
and this gave a difference in liveweight of 1.5 kg at the end of the first week after
weaning. Animal protein allowed the pigs to gain substantial amounts of body protein
and keep fat losses to a minimum, while the pigs fed plant proteins could only
maintain their body protein and they lost substantial amounts of fat (Table 2.3).
Table 2.3. Change in liveweight, body protein and body fat (g/d) in the first 7 days
after weaning (from Whang et al., 2000).
Diet Liveweight Protein Fat
Animal protein 175 30 -7

Corn/soybean -38 5 -30
Despite these differences created in the first week after weaning the pigs fed the
traditional starter diet compensated and reached the same mass of body protein
(15.4 vs 15.1 kg) as the pigs fed animal protein at 152 days of age although they
did not compensate completely in body fat (25.5 vs 28.1 kg) and were leaner. If
body protein had been lost in the first week after weaning rather than just maintained
it would be interesting to know whether there would have been complete
compensation. Young pigs, particularly after weaning, protect their body protein
and appear to preferentially metabolise fat in times of nutritional shortage.
Whittemore et al. (1978) showed that for the first week after weaning piglets lost
30 Weaning the pig

a modest 6 g/d of bodyweight and this consisted of a large loss of fat (46 g/d) and
gains in both protein (4 g/d) and water (36 g/d). They suggested that young pigs
probably needed to grow at rates of about 200 g/d before they started to
accumulate body fat. Allowing pigs to exhibit compensatory growth might be one
way reducing the cost of starter diets and increasing the efficiency of growth.
2.12 Conclusions
It is suggested that growth and its driver, food intake, are pre-programmed and that
bigger animals at birth are bigger at weaning and bigger at maturity. The
consequence of this is that a larger animal will grow faster than a smaller animal
at any stage of its life. Hence pigs that are heavier at weaning will grow faster than
lighter ones and any weight differences at weaning will be magnified during post-
weaning growth. It seems from most of the evidence that stimulating growth of
piglets during lactation to reach a greater weaning weight is rarely rewarded by a
higher post-weaning growth.
Simple observations on growth rate in the first week after weaning, like the
genetically programmed weight at weaning, suggest that this is also an important
determinant of post-weaning growth, that is, the more rapid the growth the faster
the pig reaches market weight. The normal check in growth that follows weaning
can be minimised and reduced to only a few days by feeding high-quality diets
based on animal proteins. This circumvents the need for the normal mechanisms
of compensatory growth that would otherwise operate and allow animals to catch
up to their normal growth path.
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34 Weaning the pig

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performance and carcass characteristics. Journal of Animal Science 80, 301-308.

3 Nutritional management of the pig in
preparation for weaning
R.H. King and J.R. Pluske
3.1 Introduction
The average weaning age in many of the major pork-producing countries in the
world has declined progressively over the last 20 years owing to the continued
pressure on the pig industry to improve the efficiency of pork production.
Reducing the age at weaning to 18 to 24 days of age, which is the average weaning
age in many countries, has the potential of improving efficiency. This is because
the farrowing interval of sows is reduced (thereby increasing the number of pigs
produced per sow per year) and the risk of disease transfer between sows and piglets
(segregated early weaning systems) is reduced, thereby increasing growth rate and
efficiency in subsequent growth phases. Removing piglets from the sow at an earlier
age also provides opportunities to exploit the enormous growth potential of the
young pig, because it is well established that the sucking piglet, because of limitations
on sow milk yield and milk composition, does not grow to its full genetic potential.
Weaning can be regarded as one of the most critical periods in the modern-day
pork production cycle because it represents a period of adaptation and stress in
response to the simultaneous stressors imposed on pigs at weaning. Pigs are removed
from their mothers, usually mixed with others and moved to a different
environment, and are fed an alien diet that is presented and offered very differently
to sows’ milk that was received during lactation. Consequently, pigs usually suffer
a post-weaning “growth check” for 7-14 days following weaning that is characterised
by low and variable feed intake, poor and variable growth rate, increased
maintenance requirements and increased susceptibility to enteric pathogens to cause
diseases such as post-weaning colibacillosis.
There is now realisation that the weight of the pig at weaning, and indeed at birth,
bears a strong, positive relationship to subsequent growth and weight at some point
in the future. A key performance target in pork production should be maximisation
of weaning weight, because this will have an overall influence on subsequent growth
in the growing and finishing stages. Also of importance is the variation in weaning
weight, and weight in the nursery, grower and finisher phases. Increases in litter
size cause an increase in variation in piglet size, and this includes more piglets in
the less viable category. Limiting weight variation is important for improving a
facility’s utilisation of all-in, all-out systems, and this needs to be balanced against
management strategies aimed at improving piglet growth rate during lactation.

King and Pluske
The influences of sow-and piglet-related characteristics to milk production by the

sow have been the subject of many reviews (eg, Hartmann and Holmes, 1989;
Pettigrew, 1995; Williams, 1995; Le Dividich, 1999), and will not be discussed in
this chapter. To help satisfy the requirements of the piglet to achieve maximum
growth potential and maximum weaning weight, nutrients additional to those
supplied by sow’s milk are often provided to the sucking pig. In addition, the supply
of additional nutrients may also prepare the digestive system of the sucking pigs
to cereal-based solid diets after weaning.
The purpose of this chapter is to discuss some of the management options available
before weaning to ensure that the liveweight of the pig, and perhaps the efficiency
of the gastrointestinal tract, is maximised/optimised at weaning so that the
stressors imposed around weaning will have less impact upon overall efficiency
in the production system.
3.2 The importance of weaning weight to

subsequent growth
The weight of piglets at weaning is one of the most critical factors determining the
subsequent growth performance of pigs, and has been reviewed in chapter 14 (Le
Dividich et al., 2003). Research by Campbell (1990), for example, showed a strong
inverse relationship between weight of pigs at weaning at 28 days of age (W) and
the length of time taken to grow to 20 kg live weight (T), as follows:
T = 52.1 (± 1.69) - 3.39 (± 0.224) W (R2 = 0.85, P < 0.001).
Based upon this equation, pigs that are 1 kg heavier at weaning reach 20 kg over
3 days earlier. Other research using younger pigs (eg, Dritz et al. 1996; Miller et al.
1999) confirms this general relationship. Heavier pigs at weaning seem to continue
their weaning weight advantage to slaughter weight (Mahan and Lepine, 1991; Le
Dividich et al. 2003), and the age at slaughter could be reduced even further by at
least 10 days for a pig that is 1 kg heavier at weaning (Cole and Close, 2001). Because
of the positive relationship between weaning weight and post-weaning growth
performance, any factor that increases piglet weight at weaning should reduce
slaughter age.
Interestingly, data from both commercial and research trials shows consistently that
there is a highly significant (30 to 60% of the total variance) effect of litter from
which the piglet is derived on weaning weight and subsequent post-weaning
performance (Slade and Miller, 1999). This indicates that one or more factors that
occurs prior to weaning is/are having a major influence on both weaning weight
and subsequent growth rate, with both pre-natal and post-natal components having
an effect. Rooke et al. (1998) reported that the relative importance of these events
38 Weaning the pig

Nutritional management of the pig in preparation for weaning
was 3:1 in favour of the pre-natal effects, begging the question of just where exactly
does one begin to investigate the phenomenon of variation in pig weights. Some
authors (Bate, 1991; Braastad, 1998) have presented evidence of in utero effects on
subsequent post-natal behaviour. Nevertheless, maximisation of weaning weight
should remain a goal in pig production because of its relationship to the number
of days it takes a given pig to reach slaughter weight.
3.3 Nutrient intake before weaning

The piglet places an enormous reliance on the sow for its nutritional needs before
weaning, first consuming colostrum in the first 24-36 hours after parturition and
then consuming milk at regular intervals during the day and night until weaning
(Pluske and Dong, 1998). The intake of an ‘adequate’ amount of colostrum before
closure of the small intestine to immunoglobulins is of crucial importance to both
the subsequent survival and performance of the young pig (Le Dividich and Noblet,
1981; Varley, 1992). Coalson and Lecce (1971) considered an intake of 40-60 g
colostrum was necessary for piglets to have normal serum immunoglobulin
concentrations. The provision of colostrum to weaker piglets, or to litters where
the sow is suffering agalactia, is generally used as a key management technique to
increase survival rates, increase weaning weight, and possibly reduce the variation
in weaning weight. Alternatively, practices such as split weaning immediately after
farrowing offer potential to allow a more equitable transfer of colostral
immunoglobulins across the spectrum of weights within a litter (Donovan and Dritz,
1997). Many studies espouse the benefits of colostrum for gut development, as
an energy source for thermoregulation of the newborn piglet, a substrate for protein
synthesis, and as a passive supply of protection against enteric pathogens.
Collectively, these functions are important in establishing the pig during lactation
and, ultimately, after weaning.
3.3.1 Supplying creep food in lactation
Amongst the many pre-weaning influences that can affect the growth and survival
of pigs after weaning, most attention has been directed towards the nutrition of the
young pig. A plethora of studies have examined, and reviewed, the effects of creep
feeding (ie, offering a solid diet) during lactation on weaning weight and performance
thereafter (eg, Pluske et al., 1995). This is based largely on the premise that offering
solid feed before weaning will familiarise, both behaviourally and physiologically,
the young pig to the changes imposed on it simultaneously at weaning.
Traditionally, the sucking piglet has been supplied with creep food for two main
reasons. First, creep food supplies supplemental nutrients that are required to
maintain satisfactory growth rates and achieve heavier weaning weights. Second,
the consumption of creep food is believed to prepare the digestive system of the

King and Pluske
piglet for digestion of complex carbohydrates and protein that will be supplied as
the sole source of nutrients after weaning. However, some research, such as that
of Chapple et al. (1989), found that the variation in amylolytic activity in the
pancreas of piglets was more a function of sow (litter of origin) than of the intake
of solid feed during lactation and immediately after weaning. Similarly, it has been
reported that pepsin and maltase activities could not be related to weaning weight
or creep feeding time (Lindemann et al. 1986; de Passille et al. 1989).
3.3.2 Dry creep feed intake
Evidence to support the notion that supplying pigs with dry creep food during
lactation will improve pre-weaning growth performance is equivocal. Pluske et al.
(1995) reviewed a large number of studies presented in the literature and found
an enormous variation in feed intake of creep-fed piglets, with the contribution
of creep feed to daily energy intake prior to weaning at 21-35 days of age ranging
from 1.2 to 17.4%. Thus the data from the literature demonstrate that intake of
dry creep food during lactation is generally small and variable and unlikely to
significantly influence weaning weight, particularly in piglets weaned at 3 weeks
of age or younger.
Furthermore, growth rate in the immediate period following weaning is often poorly
related to pre-weaning creep food intake (Barnett et al. 1989, Pajor et al. 1991; Fraser
et al. 1994), suggesting that causal links between creep feeding and weight gain
after weaning remain to be demonstrated. Two of the reasons for this are because
creep feed consumption varies so much within litters and between litters. Fraser
et al. (1994), for example, estimated that creep feed intake (associated with creep
feeding behaviour) accounted for only 1-4% of the variation in liveweight gain in
piglets in their first 14 days following a 28-day weaning, even though there were
significant litter effects on the intake of dry feed during lactation.
Nevertheless, some pork producers, especially those weaning later than 21 days of
age, often offer high-quality expensive creep diets to sucking pigs, despite minimal
responses in pre-weaning growth rate, to assist the adaptation to starter diets as
the sole source of nutrients immediately after weaning. In some European
countries such as Sweden and Denmark where weaning age is now 28 days of age
or greater, and the use of growth-promoting antibiotics and antimicrobial agents
such as zinc oxide are banned or strictly regulated, the importance of enhancing
the intake of solid feed before weaning is receiving renewed attention. This is to
take advantage of both a heavier weaning weight and to modulate the gastrointestinal
tract, especially the microflora, to the dietary challenges after weaning. Numerous
recent studies, such as those reported by Toplis et al. (1999) and Blanchard et al.
(2000), show that offering creep feed as a gruel/slurry (1:2 meal to water) may
enhance the consumption of dry matter before weaning.
40 Weaning the pig

3.3.3 Liquid diets to enhance feed intake
In contrast to the equivocal results reported with dry creep feed supplementation
(Pluske et al. 1995), providing sucking piglets with liquid diets would appear to
offer more potential to provide a significant boost to pre-weaning growth rate and
weaning weight (Reale, 1987; Azain et al. 1996), and also performance after weaning
(see Odle and Harrell, 1998, for review). Reale (1987) offered cows’ whole milk
to piglets from 10.00 h each day, adding fresh milk every two hours until 23.00
h, from day 7 to day 28 of lactation. Growth was stimulated by 151 g/day (71%)
in the fourth week of lactation and, from days 7 to 28, by 87 g/day, an amount
that increased weaning weight by 1.8 kg in comparison to controls that were offered
a dry creep feed. Similarly, King et al. (1998) found that piglets offered cows’ liquid
milk from day five of lactation were 1.6 kg heavier at weaning at 28 days of age
than piglets which received no supplemental nutrients. In addition, piglets
appeared to still prefer milk from the sow, as the supply of supplemental milk did
not reduce the amount of milk that the piglet obtained directly from the sow.
The results of a number of studies where sucking piglets were offered milk liquid
diets are shown in Table 3.1. Significant increases in the intakes of nutrients have
been observed when sucking pigs have been offered liquid milk diets compared
to dry creep intakes (Table 3.1). As a result, pre-weaning growth rates are increased
by 11 to 35% (Table 3.1). These results demonstrate the potential benefit of
additional nutrients on weaning weight and a clear benefit of supplemental milk
replacer to increase weaning weight. Although pre-weaning growth rates were
increased to almost 300 g/day, there is still enormous potential for these piglets
to grow faster up until weaning at 21-28 days of age (Hodge, 1974) if further nutrients
are consumed.
The use of a liquid milk replacer not only before weaning, but the supply of liquid
diets during the immediate period after weaning, can further reduce the growth
check and improve the subsequent growth performance of pigs. Kim et a1. (2001)
showed that feeding a starter diet as a liquid rather than in the dry form for the
first 14 days after weaning significantly increased weight at 28 days of age by 1.62
kg. In this study, pigs were weaned at 14 days of age. This growth advantage was
maintained to market weight with no evidence of compensatory gain in the dry-
fed control pigs. However, and in contrast, Lawlor et al. (2002) showed no positive
effects whatsoever on post-weaning gain when a number of dietary interventions
based on liquid feeding were implemented after weaning.
Dunshea et al. (1997) attempted to alleviate the post-weaning growth check by

providing extra milk around the time of weaning. Pigs provided with liquid milk
replacer, in addition to access to dry starter feed, gained 1.2 kg during the first week
after weaning whereas pigs that received only dry starter feed gained 0.4 kg in the

King and Pluske
Table 3.1. Consumption of liquid milk replacer by piglets during lactation and
consequent growth response.
Reference Treatment Lactation Average Pre-weaning Increase in

duration length supplemental growth rate growth rate
of feeding (days) intake over (g/day) (%)
(days) lactation
(g DM/pig/day)
Azain et al. (1996)

Cool season
No replacer 21 21 - 222 -
Replacer 21 21 20.9 247 11
Warm season
Replacer 21 21 66.2 224 35
King et al. (1998)
Replacer 24 28 58.5 297 25
Dunshea et al. (1997b)
Replacer 10 20 48.5 291 30
Campbell (1990)
Replacer 10 28 29.3 264 23
Pluske et al. (1995)1 15.3 28.1 11.8 213.6
1Means figures for dry creep intake in studies reviewed by Pluske et al. (1995).
first week after weaning (Dunshea et al. 1997). Supply of a liquid milk replacer to
piglets both prior to weaning and in the first week after weaning had an additive
effect; pigs that received liquid milk replacer before and after weaning were 10%
heavier at 120 days of age than pigs that were suckled by the sow only and weaned
onto dry starter feed (Dunshea et al. 1997). Much of this improvement was due
to the extra nutrient intake from supplemental milk replacer prior to and
immediately after weaning. The development of liquid feeds and feeding systems
offers the potential to markedly improve the growth performance of piglets both
before weaning and during the immediate period after weaning.
42 Weaning the pig

3.3.4 The effects of gender on nutrient intake of neonatal pigs
An interesting observation by King et al. (1998) was that female piglets grew faster
than their male counterparts prior to weaning when litters were offered supplemental
milk. This was most likely related to greater nutrient intake in the female pigs. Similar
observations of greater growth rates amongst female piglets have been made in the
immediate post-weaning period when pigs were offered either liquid diets
(Dunshea et al. 1997) or dry diets (Bruininx et al. 2001; Dunshea et al. 2001).
In a retrospective analysis of 58 studies conducted at the University of Kentucky,

Cromwell et al. (1996) showed that gilts grew more rapidly over the first few weeks
after weaning. Thus, there does appear to be more sexual dimorphism in young
pigs, and this is often manifested in the immediate post-weaning period if
nutrient intake is high or when supplemental nutrients are provided before weaning.
3.4 The composition of diets offered during

lactation
During the first two or three weeks of life, the piglet’s digestive tract is best suited
to digest lactose, fat and the milk proteins, casein and whey (Pluske and Dong,
1998). The digestive enzymes necessary for the digestion of starch, sugar and non-
milk proteins are present at relatively low levels. Therefore, dry and liquid creep
feeds must be palatable, concentrated and contain ingredients compatible with the
digestive system of the young sucking pig.
Complete creep diets containing cooked or flaked cereals, oils, various milk products
and other highly digestible feedstuffs are often used to stimulate food intake of
piglets prior to weaning to achieve heavier weaning weights and to prepare the piglet
for weaning. Fraser et al. (1994) compared a standard creep diet based primarily
on corn and soybean meal with a complex commercial creep diet containing no
soybean meal, and found that piglets consumed more of the complex creep diet
and were 0.3 kg heavier at weaning at four weeks of age. However, Fraser et al. (1994)
found that these piglets only tended to gain more weight in the week before, and
the two weeks following, weaning. In other studies with 4- or 5-week weaning,
performance of pigs after weaning that have been raised with or without creep
feeding has generally shown small or negligible effects (Okai et al. 1976; Barnett
et al. 1989; Tokach et al. 1990), although English et al. (1980) showed large effects
of pre-weaning creep feed intake on post-weaning performance.
One of the contentious issues associated with creep feeding is to do with the
inclusion of antigenic compounds, such as glycinin and β-conglycinin from
soybean products, in the diet. It has been hypothesised by some researchers that
a short-term exposure to creep feed and low feed consumption may sensitise the

King and Pluske
pig to antigens in certain feed ingredients, eg, soybean meal, beans, such that
exposure of the sensitised pigs to an increased intake of the same dietary antigens
after weaning gives rise to a hypersensitivity response. This, in turn, is believed to
cause post-weaning diarrhoea (eg, Miller et al. 1984; Newby et al. 1985). It is outside
the scope of this chapter to discuss this issue in detail, however numerous authors
have subsequently failed to endorse this hypothesis. For example, Barnett et al.
(1989) examined the effects of feeding a common corn-soybean meal-whey creep-
diet on the immune response and post-weaning performance of pigs weaned at 4
weeks of age. Although creep-fed pigs tended to have higher immune responses
and slightly more severe scouring, both pre-weaning and post-weaning growth
performance of piglets were unaffected by the provision of the creep diet containing
soybean meal. Similarly, Kelly et al. (1990) found that offering creep feed before
weaning failed to affect the prevalence or severity of diarrhoea induced
experimentally by exposure to an enteropathogenic strain of Escherichia coli, and
Sarimento et al. (1990) reported that restricted feeding of a creep diet failed to affect
the incidence of induced diarrhoea and did not induce any morphological
changes characteristic of an allergic reaction in the small intestine. McCracken et
al. (1999) postulated that any effects of soybean antigens on the structure and
function of the small intestine might occur secondarily to the period of starvation
that occurs after weaning.
The reader is directed towards reviews by Dreaù and Lallès (1999) and Bailey et
al. (2001) for further information on this topic. Nevertheless, withholding soybean
meal from the diet of a young pig after weaning, to allow for the negative effects
on gut structure and function that occur post-weaning, and then re-including it
two weeks after weaning, causes the same histological and performance setback
as if the antigens were present in the diet all along (Dritz et al., 1996). In this regard,
commercial practice dictates that soybean meal is included in diets for young pigs
despite the documented physiological, immunological and morphological changes
that occur.
3.4.1 Dietary formulation of creep diets
There is a dearth of data relating to the protein and amino acid requirements of
pigs before 3-4 weeks of age (ARC, 1981). Data from milk-fed pigs have provided
estimates of 0.87 to 0.95 g lysine/MJ gross energy as the nutrient requirements for
pigs averaging 4 kg live weight (Williams, 1976, Auldist et al. 1997). There is little
data on which to base nutrient requirements for solid diets for weaned pigs. NRC
(1998) estimated the minimum dietary requirements of weaned pigs from 3 to 5
kg were 14.2 MJ DE/kg, 18.3g CP/MJ DE and 1.06 g lysine/MJ DE. Similarly, ARC
(1981) provided tentative recommendations of 16 g CP/MJ DE and 1.12 g
lysine/MJ DE for the nutrient requirements of weaned pigs between birth and three
weeks of age.
44 Weaning the pig

These dietary requirements are often used as a guide to develop diet specifications
for supplemental creep diets. However, the emphasis on dietary formulation of creep
diets is more specifically on the choice of palatable and highly digestible protein
and energy sources that promote high feed intake rather than meeting the nutrient
specifications on a least cost basis. Examples of the composition of creep diets
suitable for suckling pigs up until 3-4 weeks of age are shown in Table 3.2 (A.C.
Edwards, personal communication).
3.4.2 Use of flavours in creep/starter diets
Attempts have been made to increase weaning weight and reduce the growth check
of pigs after weaning by using various sweeteners and aromatic compounds to
increase feed consumption, particularly during the first week or two after weaning
(Campbell, 1976; Kornegay, 1977). Gatel and Guion (1990) found that diets
containing monosodium glutamate significantly increased creep food intake,
although the increase was not sufficient to improve weaning weight. However, Clarke
and Batterham (1989) found that creep food intake was low and unaffected by
the supplementation of a creep diet with monosodium glutamate.
Campbell (1976) found that incorporation of a feed flavour into a creep diet failed
to increase creep food consumption or weaning weight. However, Campbell (1976)
also found that pigs that had been weaned from sows given a flavoured diet and
had also been given a flavoured diet after weaning consumed more feed, particularly
in the first two weeks after weaning. King (1979) later confirmed this interaction
for feed intake after weaning, and also demonstrated that when the flavour was
added to the sow diet, it was detected in milk samples collected from those sows.
Madsen (1977) indicated that feed preferences could be transferred from lactating
sows to their litter by incorporating a non-metabolisable substance into both the
lactating sow diet and the diet offered to piglets after weaning. Any positive effects
of feed flavours observed in young pigs are more likely to be due to this
transference of feed preferences via flavours incorporated in sows milk or masking
unacceptable tastes to improve the palatability in the creep diet.
3.4.3 Presentation of the creep diet
One of the most important factors stimulating piglets to eat creep feed is the
freshness of the feed. Piglets should be offered small amounts of feed, at least on
a daily basis, as not only does this ensure that the feed is fresh, but the frequent
arrival of fresh feed stimulates the inherent curiosity of the piglets, thereby
encouraging consumption of creep feed (Pajor et al. 1991).
Creep feed is usually offered to pigs when they are at least one week of age because
they usually show no interest in supplemental dry feed during the first week of

King and Pluske
Table 3.2. Composition of creep diets (g/ kg air dry diet)1.
Weaning age 2 weeks 3-4 weeks
Duration of Feeding 2-4 weeks of age 3-6 weeks of age
Diet 1 2 3 4 5 6
Wheat 390 - - 592 - -

Dehulled oats - 464 - - 616 -
Extruded corn - - 352 - - 579
Soyabean meal 30 - 35 80 80 80
Sugar 30 30 30 20 20 20
Full fat soyabean meal 60 40 119 45 45 79
Meat and bone meal 30 25 30 55 50 42
Fish Meal 50 50 60 70 60 50
Blood Meal 15 20 - 20 20 20
Skim milk powder 200 200 200 - - -
Whey powder 150 150 150 100 100 100
Vegetable oil 38 15 20 10 - -
Dicalcium phosphate 2 2 - - - -
Limestone - - - - 2 5
Lysine -HCL 0.5 0.6 0.2 2.6 2 1.9
D, L-methionine 1.0 0.6 1.0 0.8 0.6 1.0
Threonine 0.7 0.8 0.4 1.0 0.9 0.4
Tryptophan 0.2 0.2 0.2 0.2 0.1 0.1
Mineral/ vitamin premix 2.0 2.0 2.0 2.0 2.0 2.0
Salt - - - 1.0 1.0 2.0
Digestible energy (MJ/ kg) 16.0 16.1 16.1 15.3 15.6 15.6
Crude protein 233 225 236 229 228 230
Lysine 15.9 16.1 16.2 15.0 15.3 15.3
Methionine 5.5 5.1 5.8 4.8 4.6 4.9
Threonine 10.1 10.2 10.2 9.5 9.7 9.7
Calcium 9.4 9.1 9.1 9.2 9.4 9.1
Phosphorus 7.9 7.8 7.6 7.7 7.6 7.3
1Use of cooked cereals and extruded feed ingredients may improve digestibility. In
addition, use of supplements such as organic acids, enzymes and flavours might also
improve digestibility, feed intake and (or) piglet health.
46 Weaning the pig

life. Initially, feed should be offered on the floor of the farrowing crate or in shallow
trays (English et al. 1977). When the litter is obviously consuming the feed, a small
feeder allowing room for several piglets to feed at the same time can be used to
supply the creep diet to the suckling pigs. Appleby et al. (1991) observed that
although provision of fresh food daily compared to three times per day had no
effect on creep food consumption, increasing the number of feeding spaces enhanced
overall creep intake in both the third and fourth week of lactation. It seems that
provision of sufficient feeder space to allow several pigs to feed at once may assist
imitation of feeding behaviour, which is an important factor in the establishment
of feeding behaviour in pigs (Appleby et al. 1991).
3.5 Water for suckling pigs

Water intake by pigs is often taken for granted but is one of the more critical
nutrients, particularly for the sucking pig. Apart from water required to support
the growth of muscle tissue and to clear wastes from the body, young pigs require
water to replace that lost by evaporation and respiration. Under most circumstances
the amount of water consumed via sows’ milk would be more than enough to satisfy
the requirements for tissue deposition and evaporative moisture loss (Fraser et al.
1993). Supplemental water is often available to piglets in farrowing crates, but B.
Jennings (personal communication) showed that deprivation of supplemental water
to suckling piglets had no significant effect on their growth performance to weaning
or in the immediate post-weaning period. Water availability is likely to be only
important for an underfed piglet in a very warm environment or in a piglet suffering
diarrhoea (Fraser et al. 1993).
3.6 Conclusions
The first weeks after weaning are regarded as some of the most crucial in the pork
production cycle because they represent a period of adaptation and stress on the
young pig. There are nutritional strategies that can be implemented before, and
around, weaning to reduce the amount of stress and severity of the growth check
in the immediate post-weaning period. Adequate intake of supplemental nutrients
before weaning can assist in preparing the digestive system of the pig for the digestion
of complex carbohydrates and proteins, and promote greater weight gain and
weaning weight. Responses to this strategy, however, tend to be variable and depend
to a degree on the weaning age. Supplementation of piglets before and around
weaning with liquid milk diets offers the greatest potential to stimulate pre-weaning
growth rate and to eliminate the post-weaning check than usually occurs in
commercial pork production. The development of liquid feeds and feeding
systems offers the potential to prepare the piglet for the weaning process and
markedly improve the performance of the young pig.

King and Pluske
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4 Behavioural changes and adaptations
associated with weaning
P. Mormède and M. Hay
Summary
In modern husbandry, weaning is an abrupt transition between two extremely
different conditions and imposes numerous challenges to piglets: nutritional
(from milk diet to solid food), environmental (temperature, characteristics of the
lodging system), social (separation from the dam, interactions with unknown mates),
and physical (transportation). Therefore, weaning leads to intense taxation of adaptive
processes, both at the behavioural and at the neuroendocrine level. The consequences
of weaning are more intense with earlier ages, although detailed biological data are
still scarce. Several behavioural and biological indices indicate that the welfare of
the piglets may be compromised during this period of intense adaptation.
Experimental data clearly show that the anorexia or, at least, the nutritional deficit
due to the abrupt transition from milk to solid food plays a major role in these
alterations. New experimental approaches have been developed, allowing a detailed
investigation of neuroendocrine changes in urinary excretion of stress hormones
(cortisol and catecholamines), together with the monitoring of behavioural changes
and production traits. Those new approaches should allow more comprehensive
studies of the different factors impinging upon piglets at weaning when nutritional
needs are covered, as well as a better appraisal of the influence of age at weaning.
This knowledge is necessary to adjust weaning procedures to ensure an optimal
production rate without compromising the welfare of the animals.
4.1 Introduction
In natural or seminatural conditions, weaning in the pig is a progressive process
taking place around 12 to 17 weeks (Jensen, 1986; Newberry and Wood-Gush, 1988;
Stolba and Wood-Gush, 1989; Boe, 1991). In modern husbandry, piglets are usually
weaned abruptly at the age of 3-4 weeks. It can occur even earlier with the practice
of segregated early weaning, which allows a better control of some diseases, and
with the use of hyperprolific sows, which leads to an excessive number of piglets
to be raised by the sows (Worobec and Duncan, 1997). Weaning is a period of
important and numerous changes for the young piglets, including: separation from
the dam, reallocation involving mixing with strangers, introduction in a novel
environment and eventually transportation to a distant place in the case of segregated
weaning, the radical change from a milk diet to solid food, and various other changes
in the physical environment (e.g. ambient temperature, nature of the floor, air
quality). Therefore, weaning leads to intense taxation of adaptive processes, both

Mormède and Hay
at the level of behavioural adjustments and neuroendocrine and other biological

systems (Dantzer and Mormède, 1983).
4.2 Neuroendocrine consequences of weaning

Most available neuroendocrine data concern the variation of cortisol in plasma.
Cortisol is a secretion product of the adrenal gland released under stimulation by
the anterior pituitary hormone ACTH that, itself, is under hypothalamic control
(Mormède, 1995). Circulating cortisol levels are very high at delivery, and decrease
sharply immediately after birth and then more slowly during the first weeks of life,
to increase thereafter (Kattesh et al., 1990; Carroll et al., 1998). Adrenal reactivity
to ACTH also decreases during the first post natal weeks (Kanitz et al., 1999). A
transient increase of cortisol levels at weaning has been described in a number of
studies, whatever the age of the piglets, although the change tends to be higher
when the animals are weaned at a younger age (Worsaae and Schmidt, 1980; Dantzer
and Mormède, 1981; Rantzer et al., 1995, 1997; Carroll et al., 1998). Glucocorticoid
receptor levels in the hippocampus were also reduced after weaning, alike after
snaring stress in adults (Kanitz et al., 1998). Although the changes of cortisol level
are widely used as an index of stress, they are not stimulus-specific. It is thus difficult
to dissociate the respective contribution of the various changes associated with
weaning in the activation of the hypothalamic-pituitary-adrenal (HPA) axis. A
number of single factors like fasting (Farmer et al., 1992), maternal deprivation
(Klemcke and Pond, 1991), exposure to novel environments (Mormède and Dantzer,
1978; Désautés et al., 1999), simulated or real transportation (Mormède and Dantzer,
1978; Lamboij and Van Putten, 1993, Perremans et al., 2001), and mixing of animals
(Bradshaw et al., 1996) can all activate the HPA axis and may therefore play a role
in the increase of cortisol levels measured at weaning.
4.3 The critical role of food

One critical change associated with weaning is the shift from sow’s milk to a dry
feed, which induces a period of fasting during the first few days following
weaning. This weaning anorexia has a negative impact on growth and leads to
mobilisation of fat stores, as shown by the sharp increase of circulating free fatty
acid levels (Bark et al., 1996). It may also be involved in the digestive problems
that are frequently encountered after weaning (McCracken et al., 1999). Experimental
data indicate that this period of under-nutrition markedly alters the functioning
of several neuroendocrine systems during the post-weaning period. For instance,
the changes measured in the somatotrophic axis (increased GH and reduced IGF
levels) and in the autonomic nervous system (reduced catecholamine excretion in
urine) are similar to those measured in fasting animals (Carroll et al., 1998; Hay
et al., 2001). These changes may be long lasting, as in the case of weaning at 6 days
of age for instance (Hay et al., 2001) (figure 4.1). Some of the metabolic responses
54 Weaning the pig

Behavioural changes and adaptations associated with weaning
a 10 b
Body weight, kg 70
NE, pg/µg creatinine

8 C
EW 45
6 *** 30
4 *** ***
18
2 *** C **
** 11 EW ***
0
d1 d8 d13 d22 d28 d5 d7 d11 d14 d19
W Age W Age
c 32 *** d
Cortisol, pg/µg creatinine
11.2
EPI, pg/µg creatinine

20 *
6.3
13 3.6
2.0 ***
8
C 1.1 C ***
5 EW 0.6 EW
d5 d7 d11 d14 d19 d5 d7 d11 d14 d19
W W
Age Age
e 100 f 56
C C ***
EW 32 EW
75
NE:EPI ratio
percent
18
50 ** 10
**
* **
25 6 ***
3
0
d5 d6 d7 d8 d12 d20 d5 d7 d11 d14 d19
W Age W Age
Figure 4.1. Consequences of early weaning (EW) on post-natal day 6 (C = control piglets
raised by their dam). EW induced an early and persistent reduction in growth rate, that
did not reach control values until the fourth post-natal week (panel a). EW transiently
increased cortisol excretion in urine (panel c). EW induced an early and profound
reduction in urinary levels of noradrenaline (panel b), that may be a consequence of
starvation, in order to save calories via a reduction of heat production. This
interpretation is supported by the change in thermoregulatory behavior of EW piglets
that spend more time under the infrared lamp (panel e shows the proportion of piglets
located under the infrared lamp, as recorded by scan sampling for 4 h/day). The reduction
of adrenaline excretion in urine was postponed by a few days after EW, but was long-
lasting, as compared to noradrenaline (d), since adrenaline has a major role in the
mobilisation of energy stores. The differential influence of EW on adrenaline and
noradrenaline excretion is better illustrated by the ratio of the urinary content in both
catecholamines (panel f). From Hay et al. (2001), with permission of Elsevier Science.

Mormède and Hay
to weaning can be corrected by milk feeding, which improves the growth rate of
the animals as compared to dry feed (McCracken et al., 1995; Kim et al., 2001).
Indeed, piglets weaned at 2-3 days of age and subsequently fed with a milk replacer
display greater growth rates by day 7-8 of lactation than piglets raised by their dam,
showing that sow milk yield is a limiting factor to piglet growth (Harrell et al., 1993).
The increase of voluntary food intake after weaning by using whole cow’s milk also
improves the mucosal architecture of the small intestine (Pluske et al., 1996).
However, in commercial settings, weanling piglets are usually offered dry food, for
economical reasons. Such a food is not accepted as well as a liquid milk replacer,
and weaning alters average daily feed intake and average daily weight gain, the
magnitude of which is larger with earlier weaning ages. As an example, Leibbrandt
and collaborators showed that increasing weaning age (2, 3 and 4 weeks) resulted
in reduced weight gain depression. All the animals nevertheless reached the same
body weight at 6 weeks of age (Leibbrandt et al., 1975).
Consumption of solid food by suckling piglets increases slowly and becomes

significant only during the fourth week of age. Moreover, large differences among
animals have been reported, and many piglets show no evidence of eating creep
feed at the weaning age of 4 weeks (Barnett et al., 1989; Pajor et al., 1991; Fraser
et al., 1994; Bruininx et al., 2002a). For instance, Bruininx and collaborators (2001)
observed in 4-week piglets that the mean time to initiate feeding after weaning was
15.4 hours, with very large variation among individual piglets, ranging from a very
short time up to four days after weaning. The initial feed intake was only slightly
affected by sex or initial body weight, but occured sooner in animals eating
significant amount of creep feed before weaning. Additionally, the daily weight
gain was improved in those animals during the first weeks after weaning as compared
to their littermates (Bruininx et al., 2002a).
Much effort has been devoted to the development of highly palatable and easily
digestible diet for nursing and weanling piglets, with mixed success. For instance,
in an experiment with piglets weaned at 14-18 days of age, Gardner and
collaborators (2001) compared the efficiency of two diets (a low-quality diet with
a relatively high content of soybean meal and a high-quality diet enriched with
blood plasma and fish meal) with and without addition of milk products. The low
quality - no milk diet was slightly less consumed, but only during the first week
after weaning, and the difference between diets disappeared thereafter. In accordance
with the latter experiment, Lawlor et al. (2002) did not find any significant difference
of feeding postweaning diets as dry pelleted feed, fresh liquid feed, acidified liquid
feed and fermented liquid feed on pig performance from weaning (26 days) to
harvest. Another attempt to increase food intake was made by increasing day length
to 23 h (instead of 8 h). Although this lighting regimen was efficient to increase
56 Weaning the pig

food intake and weight gain during the second week after weaning, no change could
be observed during the first week (Bruininx et al., 2002b).
4.4 Behaviour
The behaviour of early weaned (6-day) piglets, as compared to animals raised by
the dam, is characterised by an increase of vocalisations emitted during the first
few days after weaning, increased restlessness, more aggressive behaviours and belly-
nosing, increased litter cohesion and increased time spent under the heating lamp
(Orgeur et al., 2001). Most of these changes are still visible on day 20, i.e. 2 weeks
after weaning, like some of the neuroendocrine changes (Hay et al., 2001). They
have also been observed at various intensities in piglets weaned at older ages. For
instance, belly-nosing, which consists of reciprocal massages, butting and sucking
bouts, has been repeatedly described in weaned piglets, and its frequency increases
when the age at weaning decreases (Boe, 1993; Worobec et al., 1999). Belly-nosing
has been suggested to be a form of massaging that piglets would normally direct
toward the udder both before and after a bout of suckling (Worobec and Duncan,
1997). However, the fact that it develops progressively over days after weaning and
remains stable thereafter suggests that it may have its own psychobiological
mechanisms and several authors have suggested that it reflects reduced welfare. As
with belly-nosing, the increase of aggressive behaviours after weaning was found
to be more intense when weaning occurred at a younger age (Worsaae and Schmidt,
1980; Orgeur et al., 2001). Aggressive behaviours are normal components of the
behaviour of weaned pigs, but their high level of expression after early weaning
may be part of the same general psychobiological syndrome indicative of altered
welfare, together with belly-nosing and other behavioural changes.
4.5 Conclusion
There is no doubt that weaning is a period of intense stress for piglets, with profound
consequences on growth, physiology, and disease outbursts, which reveal severe
welfare problems. Experimental data clearly show that the anorexia or, at least, the
nutritional deficit due to the abrupt transition between milk and solid food, induces
severe taxation of the adaptive mechanisms of piglets and may be of special relevance
from a welfare point of view. Most of the problem comes from the fact that during
lactation spontaneous intake of dry food remains very low up to 3 weeks of age
and does not become significant until the 4th week, indicating that the appetite
for dry food is very low in younger piglets. The large individual variation suggests
that this trait may be influenced by genetic factors and could therefore respond to
genetic selection. It would be valuable to gain more information on the physiological
changes induced by weaning at different ages. Indeed, most studies have focused
solely on growth performance and behaviour up to now. Recent experiments showed
however that measures of physiological stress, like urinary levels of catecholamines

Mormède and Hay
provide sensitive indications on the adaptation processes occurring at weaning and

on the nature of the constraints imposed to piglets (Hay et al., 2001). Additionally,
it would be interesting to design experiments where nutritional needs are covered,
in order to assess the respective contribution of the other components involved
in the stress of weaning (e.g. separation from the dam, transportation to remote
places, change of the environment, mixing with unknown congeners).
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Farmer, C., D. Petitclerc, G. Pelletier, P. Gaudreau and P. Brazeau, 1992. Carcass composition and
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Behavioural, growth and immune consequences of early weaning in one-week-old Large White
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60 Weaning the pig

5 Metabolic and endocrine changes around
weaning
F.R. Dunshea
5.1 Introduction
One of the major stressors for the weaning pig is the rapid change from a liquid
milk based diet to a solid pelleted cereal-based diet. All this occurs at the same
time as the pigs are introduced into a new environment, mixed with other pigs
and removed from the sow. The combined effect of this transition and these stressors
is that newly weaned pigs often lose considerable weight (up to 10% of live weight)
over the first 2 days post-weaning and may not regain this weight for up to 7 days
post-weaning. These effects are more pronounced in young and small-for-age pigs
(Power et al. 1996). The metabolic and endocrine changes that occur at this time
are equally profound. In this chapter I will discuss the metabolic and endocrine
events that occur after weaning and some of the interventions that have been tried
to reduce this growth check.
5.2 The post-weaning check

Between birth and weaning, sucking pigs grow at approximately 220 g/day (King
et al. 1993), but this growth rate is far below the biological potential of the artificially-
reared pig (Hodge, 1974). For example, pigs weaned at 2-3 days of age and fed
cow’s milk or milk replacer alone until 21 days of age, can achieve growth rates in
excess of 400 g/day (Harrell et al. 1993; Dunshea et al. 2002a). Since the sow
increases milk production over the first two weeks of lactation before reaching a
plateau (Toner et al. 1995), the extent to which milk yield limits piglet growth rate
is exacerbated as lactation advances. For example, from d 21 of lactation, suckling
piglet growth rate decreases, particularly in large litters (Cranwell et al. 1995a;
Dunshea and Walton, 1995). That milk yield constrains piglet growth was
demonstrated by Cranwell et al. (1995). Except for the period immediately after
weaning (27-35 days) pigs exhibited considerably faster growth rate in all post-
weaning periods than they did while on the sow. To accommodate this decline in
nutrient supply, suckling piglets may commence to eat creep feed, or sows feed,
from about three weeks of age. However, the intakes of dry creep feeds are generally
low and unlikely to significantly increase pre-weaning growth rate of pigs (Pluske
et al. 1995). Also, given that in many parts of the world weaning typically occurs
now at 21 d or younger, most piglets have had little opportunity to consume solid
feed. It is little wonder then, that newly-weaned piglets consume very little feed
over the first few days post weaning. The post-weaning check in body weight occurs
in pigs that are heavy- or light-for-age (Figure 5.1; Dunshea et al. 2000a, 2002a,b)

Dunshea
6000 a
Change from weaning weight
5000
4000
3000
(g)
2000
1000
0
-1000
0 2 4 6 8 10 12 14 16
Days post-weaning
6000 b
Change from weaning weight
5000
4000
3000
(g)
2000
1000
0
-1000
0 2 4 6 8 10 12 14 16
Days post-weaning
Figure 5.1. Effect of sex, weaning age and weaning weight on growth in pigs weaned
onto solid diets. Animals were either weaned at between 12 and 17 days (Figure 5.1a)
or 20 and 28 days (Figure 5.1b). Boars are depicted as open symbols and gilts as closed
symbols. Light-, average- and heavy-for age pigs are depicted as triangles, squares or
circles, respectively. Data are collated from a number of studies conducted by the author
(Power et al. 1996; Dunshea, 2001; Dunshea et al 1.999a;2000a,b;2002b,c).
and is greater and lasts longer in early-weaned pigs (Power et al. 1996; Dunshea
et al. 2002b). Collation of data from a number of studies conducted by the author
demonstrate that pigs weaned at greater than 20 days of age take approximately
4 days to return to weaning weight, whereas pigs weaned at less than 17 days of
age may not return to weaning weight until after 7 days post-weaning (Figure 5.1).
The post-weaning check is also greater in boars and barrows than in gilt piglets
(Power et al. 1996; Dunshea et al. 1999a; Dunshea, 2001; Bruininx et al. 2002)
although this difference is only transient in nature.
The reason for the reduction in live weight is the failure of weaned pigs to consume
dry feed. Le Dividich and Seve (2000) collated data from 7 studies on feed intake
62 Weaning the pig

Metabolic and endocrine changes around weaning
immediately before and after weaning. Average milk energy intake prior to
weaning was approximately 1250 kJ/kg0.75/day. On the day after weaning, solid
feed intake was approximately 25% that achieved before weaning. By 1 week post-
weaning solid feed intake had increased but was still only 60-70% of that
consumed prior to weaning. In a very comprehensive study, Bruininx et al. (2001)
investigated the effect of weaning weight on time taken to first consume feed and
found that on average it took approximately 15 h until pigs first consumed dry
food. However, over half (53%) of the pigs had consumed food in the first 4 h
after weaning when the lights were turned off for 12 h. Over the next 12 h of darkness
only a further 3% of pigs commenced feeding. During the following 12 of light a
further 32% of the pigs commenced feeding. These data suggest that although it
can take some considerable time before weaned pigs consume feed there may be
some potential to influence this by changing light patterns (Bruininx et al. 2002).
The low feed intake and growth check immediately after weaning are consistent
with a large number of observations in our laboratory (Power et al. 1996;
Dunshea, 2001; Dunshea et al. 1999a,b; 2000a, b;2002a,b,c).
The low feed intake, and poor or even negative growth rates, can be largely overcome
by feeding the weaned pigs liquid instead of dry diets (Lecce et al. 1979; Odle and
Harrell, 1998). Liquid diets (skim milk) have also been used to supplement dry
post-weaning diets with considerable success especially if the pigs received the same
liquid diet as a supplement prior to weaning (Dunshea et al. 1999a). Growth rates
and DM intakes of up to 240 g/day and 260 g/day respectively, in the 7 days after
weaning, were recorded in pigs supplemented with a liquid diet before and after
weaning compared with growth rates of <30 g/day and DM intakes of up to 88
g/day in pigs that were not supplemented before weaning and then fed a dry diet.
The critical importance of feed intake in the immediate post-weaning period has
been demonstrated recently by Geary and Brooks (1998), who found that there
was a highly significant (P<0.001) relationship between DM intake in the first 7
days post-weaning and 28-day post-weaning weight. For every 10 g/d of extra DM
that a pigs eats in the 7 days post weaning, 174 g of extra body weight will be
accumulated by 28 days post-weaning.
Irrespective of the physical form of the diet another problem that can occur at
weaning, especially in early-weaned pigs, is disease associated with enterotoxigenic
bacterial infection of the gastrointestinal tract. Lecce (1986), a pioneer of artificial
rearing of pigs, observed that while early-weaned pigs can be raised on liquid milk,
“diarrhoea was the nemesis of the artificially reared pig” and remained the
greatest barrier to adoption of these systems on farm. One method of overcoming
this is to use liquid diets that have been fermented by lactic acid bacteria (or
acidified) to reduce the pH of the diet to that which is inhibitory to pathogenic
organisms (Azain et al. 1996; Geary and Brooks, 1998; Dunshea et al. 2000b). Liquid
feeding systems for weaners, however, need not be based on milk or milk replacers

Dunshea
but rather take the form of water and mash meal as is the case for grower-finishers.
For example, Russell et al. (1996) fed weaner pigs either dry commercial pellets
or the same diet as a liquid feed and observed an increase in daily gain, particularly
over the first week after weaning. Thus, daily gain was increased by 110 and 25%
over the first 1 and 4 weeks after weaning, respectively. However, under many pig
production systems there is no opportunity to liquid feed the weaner pig and the
metabolic events that occur at weaning are obligatory.
Despite the fact that there is only a modest change in live weight over the first week
post-weaning, there are quite dramatic changes in the weights of the visceral organs.
In particular, there is an enormous increase in the weight of the large intestine as
this becomes a major site of digestion of the solid feed. Initially, there is a decrease
in the weight of the small intestine (Kelly et al. 1991; Spreeuwenberg et al. 2001)
while the weight of the large intestine increases rapidly (Kelly et al. 1991; Pluske
et al. 2003). For example, Kelly et al. (1991) found that by 3 days post weaning
the small intestine and large intestine were 80 and 141%, of pre-weaning weights
in pigs intragastrically-infused with cereal-based weaner feed. The weight of the
small intestine subsequently increases in mass after the short period of weight loss
and alteration in morphology (Cera et al. 1988). Similarly, we have found that in
both early (14 d) and late (28 d) weaned pigs there is a considerable increase in
the various intestinal components, both in total and relative mass, particularly in
the early-weaned pigs (Pluske et al. 2003, Figure 5.2). There are also quite
dramatic changes in small intestinal histology over this period. For example,
McCracken et al. (1999) found that while there was no effect of weaning on the
villous height on the first day post-weaning, by the second day post-weaning there
300
250
% of weaning weight
200 Body weight

Stomach
150 Small intestine
Large intestine
100 Pancreas
50
0
14 d 28 d 14 d 28 d
7 day post-weaning 14 days post-weaning
Figure 5.2. Effect of weaning age (14 and 28 d of age) and time post -weaning on the
body weight and weight of visceral organs. Data are expressed as a percentage of the
respective weights at weaning. Data are from Pluske et al. 2003.
64 Weaning the pig

was a 65% reduction in villus height. There subsequently follows a period of rapid
hyper-regenerative villus repair (Cera et al. 1988; McCracken et al. 1999;
Spreeuwenberg et al. 2001). In addition to these morphological changes in the gut
there are also quite profound changes in the composition of the carcass as the piglet’s
metabolism adjusts to meet the energetic deficit that occurs at weaning, as well as
the change in substrates that the piglet receives.
5.3 Effect of weaning on metabolism

Prior to weaning, the piglet consumes a liquid milk diet with a high ratio of fat to
protein and with lactose as the predominant source of carbohydrate. The neonatal
pig is born with very little in the way of fat reserves, but because of the high fat content
of sow’s milk, it incorporates much of the pre-formed fat from milk into body lipid
(Mellor and Cockburn, 1986). In addition, the piglet obtains these nutrients every
45-60 minutes (Ellendorff et al. 1982; Auldist et al. 1998; 2000) and so tissues are
receiving substrates at a relatively steady rate and are in an anabolic state. However,
the newly weaned pig suddenly has this source of nutrients removed and unless it
can consume some food, moves into a negative energy balance. This energy deficit
can be exacerbated by the stress of being removed from the sow, mixing, transportation
and change in temperature. All of these factors combine to alter metabolism and
increase energy expenditure in the immediate post-weaning period.
5.3.1 Lipid and carbohydrate metabolism
The weaning-induced fasting results in mobilisation of fat, and to a much lesser

extent glycogen, to provide energy to support life. Classical calorimetry studies
demonstrate that pigs generally mobilise lipid while conserving or even deposit
protein, with the mobilisation of body lipid being exacerbated at temperatures below
the piglets ’lower critical body temperature (Le Dividich et al. 1980; Close and Le
Dividich, 1984; Bruininx et al. 2002). Although not typically measured or reported,
the amount of fat mobilised must be greatest over the first 2-3 days post-weaning,
once the animals have absorbed the nutrients from sow’s milk and before they
consume solid feed. For example, over the period between 1 and 6 days post-weaning
feed intake increased from approximately 50 to 250 g/d while the average rate of
fat mobilisation over the entire period was 20 g fat/d (Bruininx et al. 2002). Total
heat production per day was relatively constant between 1 and 6 d post-weaning
suggesting that most of the fat mobilisation occurred in the immediate couple of
days post-weaning (Bruininx et al. 2002). Indeed, using slaughter balance
techniques, Whittemore et al. (1981) found that over the first 2 d post-weaning
pigs weaned at 21 d of age lost approximately 80 g fat/day, but that this fat loss
progressively decreased over the next 6 d (Figure 5.3). These findings are supported
by other slaughter balance data that show that both the proportionate and
absolute body lipid contents are reduced over at least the first 7 d post-weaning.

Dunshea
80
Tissue gain (g/d)

40
-40
-80
-120
0 2 4 6 8
Days post-weaning
Figure 5.3. Effect of time post -weaning on body fat (open symbols) and protein (closed
symbols) tissue gain. Data are from Whittemore et al. (1981).
Thus, in the study by Zijlstra et al. (1996) total body lipid decreased from
approximately 11.2 to 8.5% of body weight in pigs weaned at 18 d of age. On the
other hand, pigs that remained nursing the sow or were given milk replacer increased
fat deposition by approximately 40 and 60 g/d, thus maintaining a similar
proportionate lipid composition as at weaning at 18 d. Indeed, after weaning pigs
of modern genotypes may not return to the same proportionate body lipid
composition until 17 weeks of age (Dunshea et al. 2001).
Plasma NEFA concentrations, which are directly related to the rate of fatty acid
mobilisation from adipose tissue (Dunshea et al. 1992a), are elevated immediately
after weaning (Bark et al. 1986; Funderburke and Seerley, 1990). Regression
analyses of the mean data of Bark et al. (1986) demonstrate a strong inverse
relationship between feed intake and plasma NEFA (Feed intake (g/d) = -4.2 + 234.9
* 0.998NEFA (µmol/L), n=20, R2 = 0.86, P<0.001) in weaned pigs, as is the case in
ruminants (Dunshea et al. 1988). Thus, in response to the low feed intake that occurs
immediately post-weaning, the newly weaned pig mobilises body fat as NEFA. This
is clearly demonstrated when feed intake and plasma NEFA from the ad libitum-
fed pigs in their study are graphed against days post-weaning (Figure 5.4). In addition,
the rate of lipogenesis in adipose tissue explants obtained from weaned pigs is very
low suggesting that adipose tissue is in a net catabolic state at this time (Fenton et
al. 1990).
Interestingly, even though there is a dramatic reduction in energy intake over the
first few days post-weaning, plasma glucose is reduced only transiently and
slightly (Funderburke and Seerley, 1990) before returning to similar levels to those
observed in suckled animals (Rantzer et al. 1997). These data suggest that there
must be increased glycogen breakdown and/or increased gluconeogenesis in
order to maintain glycemia after weaning. However, liver glycogen stores are relatively
low at weaning (ca. 10 g/pig) and are relatively resistant to depletion after
66 Weaning the pig

300 1400
Plasma NEFA (µmol/L)

250 1200
Feed intake (g/d) 1000
200
800
150
600
100
400
50 200
0 0
1 2 3 4 5 6 7
Time post-weaning (days)
Figure 5.4. Effect of time post -weaning on feed intake (open symbols) and plasma
non-esterified fatty acid (NEFA) concentrations (closed symbols). Data are from Bark
et al. (1986).
weaning (Stanton and Mueller, 1976; Funderburke and Seerley, 1990) suggesting
that gluconeogenesis must be the major source of glucose. Mobilised glycerol is
the most likely source of gluconeogenic substrates rather than amino acids since
whole body protein accretion is maintained in the post-weaning period (see next
section) and plasma urea nitrogen is low in newly-weaned pigs (Pluske, 1995;
McCracken et al. 1995). Plasma glycerol concentrations are not high in the weaned
piglet (Pluske, 1995) possibly because the glycerol is rapidly cleared from the liver
and converted to glucose. As we shall see later, some of the hormonal changes that
occur around weaning orchestrate these necessary adaptations in metabolism.
5.3.2 Protein metabolism
The concept of homeorhesis, as defined as “the partitioning of nutrients towards a

tissue of priority for a particular physiological state” by Bauman and Currie (1980),
is possibly no better illustrated as by the conservation or increase in whole body
protein, particularly in the gut, during the weaning-induced fast and subsequent
undernutrition. In the case of the newly-weaned pig, the tissues of priority are gut
and skeletal muscle protein. Thus, the neonatal pig has an enormous capacity to
deposit protein and the whole-body fractional protein synthesis rate is at its highest
in the first few weeks of life (Young, 1970). In the face of undernutrition the weaned
pig attempts to conserve protein in the gut and to a lesser extent in skeletal muscle
tissue. For example, Ebner et al. (1994) found that during periods of both protein
and energy restriction, the decrease in protein deposition was less in the
gastrointestinal tract than it was in skeletal muscle. Also, calorimetric studies indicate
that whole-body protein balance is positive over the first week after weaning despite
the animals being in negative energy balance (Bruininx et al. 2002). Nevertheless,

Dunshea
the newly weaned pig must be in negative protein balance for at least the first 2
days after weaning since they consume so little food over this period of time.
Extrapolation of the relationship between protein intake and protein balance suggests
that the weaned pig needs to consume 3.1 g protein/kg0.75 (Le Dividich et al. 1980),
or approximately 60 g/d of a typical weaner diet, to remain in zero protein balance.
Using the slaughter balance technique, Whittemore et al. (1981) found that newly-
weaned pigs were in a slight negative protein balance for the first 4 days after weaning
(Figure 5.3). However, there is no doubt that very soon after commencing to consume
solid food the newly-weaned piglet is in positive protein balance and there is a rapid
expansion of the gut and other visceral organs. It is also interesting that the rate at
which protein deposition increases with increasing feed intake is greater at low as
compared to high levels of energy consumption (Close and Stanier, 1984).
Feeding stimulates the fractional rate of protein synthesis and protein accretion
in the small intestine and skeletal muscle of young pigs (Davis et al. 1996; 1997).
While the post-prandial increase in insulin stimulates protein synthesis in skeletal
muscle, insulin does not appear to be the mediator of the increase in intestinal
protein synthesis that occurs after feeding (Davis et al. 2001). Likewise, systemic
elevations of amino acid concentrations, achieved through intravenous infusion,
have little effect on intestinal protein synthesis stimulation (Davis et al. 2002).
Therefore, it appears that the feeding-induced increase in protein synthesis is due
to an increase in amino acid supply via the intestinal lumen rather than via increased
arterial supply of insulin or amino acids. In this context, dietary amino acids make
a greater contribution to small intestinal protein synthesis than circulating amino
acids in fed neonatal pigs (Stoll et al. 1999). As the weaned pig moves from a liquid
milk diet to a period of limited feed consumption followed by a gradual increased
ingestion of a dry complex diet, there are some dramatic changes to intestinal growth
and histology (see above). It is likely that some of the hormonal changes that occur
post-weaning help to conserve gut and body protein.
5.4 Hormonal status

The onset of weaning results in some quite profound hormonal changes, although
it is difficult to separate cause and effect. No doubt many of the changes are in
response to the social and nutritional stress associated with weaning but there are
also overlying developmental changes that likely occur independent of the
weaning process.
5.4.1 Somatotropin and insulin-like growth factor-I
Although porcine somatotropin (pST) increases lean tissue growth and decreases
fat growth in grower and finisher pigs, the response to pST is much less in younger
pigs (Campbell et al. 1991). For example, young weaned pigs (ca. 10.0 kg, age not
68 Weaning the pig

given) did not exhibit any growth response to pST until after at least 10 d of treatment
and even then the response was inconsistent (Harrell et al. 1997). This was despite
elevated plasma IGF-I and insulin levels and reduced plasma urea as a result of
only 5 d with pST treatment (Harrell et al. 1997). Also, pST administration at the
doses used in finisher pigs (0.06 mg/kg) failed to increase plasma IGF-I or growth
in neonatal sucking pigs although there was limited evidence of subsequent growth
responses (Dunshea et al. 1999b). In contrast, Wester et al. (1998) found that a
relatively high dose of exogenous pST (1 mg/kg) increased plasma IGF-I and growth
over the first 7 days of life in artificially-reared pigs. Likewise, Dunshea et al. (2001)
found that relatively high doses of pST could increase lean tissue and decrease fat
deposition in neonatal pigs.
The ontogeny of somatotropin and its receptors in the neonate has been well studied
in a variety of species although data specific to the pig are relatively scarce. In the
young pig plasma ST is very high around parturition, declines rapidly over the first
week of birth, then remains constant until the second week of life before gradually
increasing again over the next 5 weeks and declining once again (Buonomo and
Klindt, 1993; Matteri and Carroll, 1997). ST then gradually declines up to at least
30 weeks of age (Harrell et al. 1997; Klindt and Stone, 1984; Owens et al. 1991).
These patterns of plasma ST concentrations are essentially the same as in vitro basal
and growth hormone releasing hormone-stimulated ST release from cultured
pituitary cells (Matteri and Carroll, 1997). ST receptor mRNA has been found in
the liver of the fetal (Duchamp et al. 1996) and neonatal (Brameld et al. 1995)
pig and it increases over at least the first 20 d of life (Owens et al. 1990). Therefore
it appears that the ST receptor gene is being transcribed but there may be only a
limited number of functional receptors being produced or alternatively, there may
be some functional receptors that are resistant to ST but that may respond to high
doses of exogenous pST. Either of these scenarios would explain why there was
little response to moderate doses of exogenous pST (Dunshea et al. 1999b) whereas
there was modest response to high doses of pST (Wester et al. 1998; Dunshea et
al. 2001) in neonatal pigs.
Weaning itself results in a decrease in plasma IGF-I and a simultaneous increase

in plasma ST (White et al. 1991; Tang et al. 1995; Carroll et al. 1998; Matteri et al.
2000). The study of Matteri et al. (2000) quite clearly demonstrated that the decrease
in IGF-I concentrations was related to the onset of weaning rather than being a
developmental response since animals that remained nursing the sow had much
higher levels of IGF-I than weaned pigs. Also, the decrease in plasma IGF-I occurs
regardless of weaning age, at least between 14 and 35 days (White et al. 1991; Matteri
et al. 2000). Circulating IGF-I does not return to pre-weaning values until 1 to 2
weeks post-weaning at a similar time to when pre-weaning energy intakes are
achieved (Le Dividich and Seve, 2000). Exogenous IGF-I and analogues inhibit pST
secretion in 60 kg growing pigs (Dunaiski et al. 1997), and it is possible that the

Dunshea
increase in pST after weaning is in response to the profound decrease in IGF-I and
subsequent diminution in the inhibitory effects of IGF-I upon pST secretion. The
increase in pST in response to the reduction in feed intake at weaning may occur
in an attempt to conserve gut and skeletal muscle protein. Indeed, the proteins in
the gastrointestinal tract have an enormous turnover and without some conservation
of these organs the gut would reduce in size to a greater extent than it does
immediately after weaning. Interestingly, in weaned pigs fed either a high or low
feed intake, the hepatic ST receptor mRNA was down-regulated whereas it was up-
regulated by a low feed intake in the four muscles examined (longissimus,
rhomboideus, soleus, and cardiac) (Katsumata et al. 2000). In contrast, at 2 d post-
weaning Matteri et al. (2000) did not see any effect of weaning on either skeletal
muscle, adipose tissue or hepatic ST receptor mRNA. However, there were
differences between different weight classes. These adaptations to underfeeding may
explain how skeletal muscle is spared during the weaning-induced negative energy
balance via muscle ST receptor up-regulation and/or elevated circulating pST. Indeed,
the effects of pST on protein metabolism differ between the fed and the fasted state
with pST increasing protein deposition in the fed state via increasing protein
synthesis and decreasing protein degradation and amino acid oxidation (Vann et
al. 2000a), whereas protein loss is minimised during the fasted state via an increase
in protein synthesis and a decrease in amino acid oxidation (Vann et al. 2000b).
Therefore, a number of workers have investigated whether somatotropin or IGF-I
treatment of neonatal and/or weaned pigs can ameliorate the weaning-induced
depression in feed intake and weight gain.
Dunshea et al. (1999b) treated nursing pig with daily pST injections (0.06 mg/kg)
from day 4 until weaning on day 31 and found little effect of pST on daily gain
until the final 3 days of lactation. However, immediate post-weaning growth was
not studied. In a subsequent study, Dunshea et al. (2001) found that pre-weaning
fat and immediate post-weaning lean tissue deposition were decreased with much
higher doses of pST (1.0 mg/kg per day) given from day 1 until weaning on day
21. Previous pST treatment of finisher pigs causes a large (ca. 50%) reduction in
the amount of pST contained in the pituitary (Campbell et al. 1989). Therefore,
it may be possible that pST treatment of neonatal pigs may decrease pituitary pST
production and/or delay the development of somatotrophic activity in the pituitary
(Matteri et al. 1997). A decrease in endogenous pST production in the immediate
post-weaning period may be the cause of the reduced lean tissue deposition in
weaner pigs previously treated with pST and this may limit the applicability of
neonatal pST treatment to improve immediate post-weaning performance. Despite
these findings, it may be worth investigating pST treatment during the weaning
process since daily pST injection partially reversed a dexamethasone-induced
catabolic state in weaned piglets, although the combined pST/IGF-I therapy was
even more efficacious (Ward and Atkinson, 1999). Also, exogenous pST partially
ameliorated fasting induced protein catabolism in older pigs (Vann et al. 2000b).
70 Weaning the pig

Exogenous IGF-I, the putative mediator of pST’s action on lean tissue growth, has
also been investigated as a means of increasing growth of weaned pigs.
Acute IGF-I treatment increases protein synthesis in neonatal pigs consuming milk
replacer in a variety of tissues, but this response is markedly lower in 26-d-old as
compared to 7-d-old pigs (Davis et al. 2002). Schoknecht et al. (1997) found that
chronic IGF-I infusion (4 µg/h) for 7 d increased growth rate of suckling normal
and intra-uterine growth retarded (IUGR) piglets. However, similar doses (2, 4
and 8 µg/h for 8 d) of IGF-I or the potent analogue LR3IGF-I had little effect upon
growth rate in artificially-reared pigs that were restrictively-fed to grow at similar
rates to those observed in pigs suckling the sow (ca. 200 g/d) (Dunshea et al.
2002a). In a study in the same series, IGF-I or LR3IGF-1 were infused into neonatal
pigs (from ca. 4 d of age) that were consuming cow’s milk ad libitum. While neither
IGF-I nor LR3IGF-1 infusion (8 µg/h) had any effect upon feed intake or growth
rate over the first 9 d of Experiment 2, when the infusion rates were doubled (16
µg/h), there was an increase in feed intake and growth rate over the second 9 d,
particularly in pigs infused with LR3IGF-I (Dunshea et al. 2002a). Although there
were few significant effects of IGFs on visceral organs, the liver and small
intestinal weights tended to be greater in pigs infused with LR3IGF-I. In a
subsequent experiment, the interactions between nutrient intake (manipulated
through establishing litter sizes of 6 and 12 piglets) and LR3IGF-I infusion in
suckling piglets were investigated (Table 5.1). Again, although there was an increase
in growth during LR3IGF-I treatment, this did not become manifest until the latter
stages of the experiment. Also, growth responses to LR3IGF-I were greater in the
piglets from litters of 12. LR3IGF-I infusion increased visceral organ size and, as
for growth rate, the responses were greatest in the piglets under the greater
nutritional stress. Therefore, it could be hypothesised that neonatal treatment with
IGF-I or analogues either before and/or after weaning may help piglets withstand
the weaning check. However, subsequent studies directed at ameliorating the post-
Table 5.1. Effect of LR3IGF-I infusion on growth performance and organ size in suckling
piglets from litters of 6 or 12 piglets (Dunshea and Walton, 1995).
Growth factor (GF) Control LR3IGF-I P value
Litter size (L) 6 12 6 12 sed L GF
ADG (0-27 d), g/d 299 187 304 199 19.0 0.001 0.43
ADG (18-27d), g/d 294 114 325 167 32.0 0.001 0.036
Small intestine, g 359 247 373 311 34.0 0.011 0.047
Liver, g 263 168 312 221 23.0 0.001 0.003
Spleen, g 29 16 53 40 6.3 0.033 0.001

Dunshea
weaning check in pigs infused with LR3IGF-I both before and after weaning and
in piglets that did or didn’t receive supplemental milk failed to show any
benefits of LR3IGF-I on growth performance although increases in the mass of
some visceral organs were observed (Tomas, 1996).
5.4.2 Insulin
Insulin plays a key role in the regulation of growth and tissue deposition in the
young pig. Insulin stimulates the partitioning of amino acids to protein deposition
and away from oxidation and gluconeogenesis while also stimulating glucose
incorporation into fat (Dunshea et al. 1992b; Wray-Cahen et al. 1998; Davis et al.
2001). In the sucking pig, insulin increases skeletal muscle protein synthesis although
this response declines between 7 and 26 d of age (Davis et al. 2001;2002). However,
insulin has no effect upon protein synthesis in visceral and intestinal tissues nor
is there a decline in protein synthesis over this age range (Davis et al. 2001;2002).
Insulin decreases during fasting in neonatal pigs (Davis et al. 1996), and although
there are little supporting data, it is reasonable to assume that insulin decreases
immediately post-weaning. For example, plasma insulin decreases precipitiously
on the day following weaning (Rantzer et al. 1997) but returns to pre-weaning values
within 2-3 days. Similarly, plasma insulin was comparable 5-7 days after weaning
as in pigs that had been maintained on liquid cow’s milk (Pluske, 1995, Zijsltra
et al. 1996). Also, plasma insulin was higher in pigs weaned onto a liquid milk
replacer diet than in those weaned onto a cereal diet on d2 after weaning but not
subsequently (McCracken et al. 1995). Thus, a decrease in insulin immediately after
weaning would result in a mobilisation of fat and glycogen to meet the energy
demands of the young pig. A decrease in insulin would also favour an increase in
gluconeogenesis since elevated insulin inhibits gluconeogenesis (Dunshea et al.
1992b). Presumably, weaning would cause a decrease in protein synthesis in skeletal
muscle but not necessarily in visceral and intestinal tissues. This may partially explain
how total and relative intestinal masses are maintained, or even increased, during
the immediate post-weaning period (see Figure 5.2). In addition, refeeding
stimulates protein synthesis in visceral and intestinal tissues via a mechanism
independent of insulin and post-hepatic amino acid supply (Davis et al. 2002).
The inference is that once pigs do commence feeding after weaning then visceral
mass will be stimulated, in part because of first-pass utilization of nutrients from
the gut lumen (Stoll et al. 1999). On the other hand, the increase in skeletal muscle
protein synthesis is due to the post-prandial increase in insulin rather than directly
to an increase in nutrients (Davis et al. 2002).
5.4.3 Hypothalamic-pituitary axis
The stress associated with weaning generally results in a rapid, but transient, increase
in plasma and urinary cortisol concentrations that lasts for 1-2 d (Carroll et al. 1998;
72 Weaning the pig

Kanitz et al. 1998; 2002; Hay et al. 2001). By 5 d post-weaning, plasma and urinary
cortisol concentrations have decreased to pre-weaning or suckled control values
(Pluske, 1995; Hay et al. 2001). Funderburke and Seerley (1990) attempted to
partition the immediate post-weaning plasma cortisol responses into psychological,
climatic and nutritional effects. While they found none of the treatments resulted
in average plasma cortisol concentrations over the 48 h post-weaning that were
significantly different from those of pigs that remained nursing, plasma cortisol
were highest in pigs that faced the nutritional stress. Also, in samples that were
obtained via venipuncture (as compared to bleeding via a catheter), plasma cortisol
was significantly higher in pigs that were subject to a nutritional as compared to
psychological or cold stress (Funderburke and Seerley, 1990). Cortisol stimulates
gluconeogenesis and has been implicated in the development of gluconeogenic
capacity in the fetal pig (Martin et al. 1980; Fowden et al. 1995). Indeed, the latter
authors speculated that the prepartum rise in endogenous cortisol may be
responsible for the increase in fetal gluconeogenic capacity observed towards term.
It is possible that the post-weaning surge in cortisol may be involved in the next
developmental increment in gluconeogenic capacity. Although there may be a
transient decrease in circulating glucose concentrations immediately post-weaning,
plasma glucose quickly returns to pre-weaning levels before pigs really commence
to consume feed (Stanton and Mueller, 1976; Rantzer et al. 1997; Funderburke and
Seerley, 1990) suggesting an increase in gluconeogenesis.
Plasma catecholamine concentrations in the pig are very sensitive to acute stress.
For example, the concentrations of both epinephrine and norepinephrine can
increase many-fold (>25-fold) within a minute of the application of stressor such
as restraint (Neubert et al. 1996). Exogenous catecholamine injection increases fat
and glycogen mobilisation (Dunshea and King, 1995; Dunshea et al. 1998) and
so it may be anticipated that weaning would increase circulating catecholamines
to favour the mobilisation of energy stores during the early post-weaning period.
However, the effects of weaning on the catecholamine system are equivocal. Stanton
and Mueller (1973) found that the adrenal glands of weaned pigs were larger and
tended to contain more norepinephrine than those of pigs that remained with the
sow. Likewise the activities of some of the adrenal gland enzymes involved in
catecholamine synthesis, including tyrosine hydroxylase, were higher in weaned
pigs. Adrenal epinephrine was not altered by weaning. Mann and Sharman
(1983) found that that while there was a decrease in the amount of tyrosine
hydroxylase in the adrenal gland of early weaned pigs there was an increase in the
activity of the enzyme, and suggested that this indicates a mechanism compensating
for the decreased amount of enzyme. In contrast, Hay et al. (2001) found that urinary
norepinephrine was lower on d 7, 11 and 14 of age in pigs that were weaned at 6
d of age compared to their suckled contemporaries. Urinary epinephrine
concentrations were lower at 14 and 19 d of age in the early-weaned pigs. Therefore,
given these contrasting observations the actual role of the catecholamine system

Dunshea
in adrenergic system in the regulation of metabolism of the weaned pig is still

unclear.
5.5 Conclusions
One of the major stressors for the weaning pig is the rapid change from a liquid
milk based diet to a solid pelleted cereal-based diet. All this occurs at the same
time as the pigs are introduced into a new environment, mixed with other pigs
and removed from the sow. The combined effect of this transition and these stressors
is that newly weaned pigs do not eat for up to 2 d and often lose considerable
weight which may not be regained until up to 7 d post-weaning. Most of the tissue
loss is fat that is mobilised to meet the energy deficit that occurs as a result of the
low feed intake. On the other hand, carcass and particularly visceral protein is not
as labile, although there are certainly morphological changes in the gut. These
metabolic adaptations are favoured by the hormonal milieu that exists immediately
post-weaning and beyond.
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80 Weaning the pig

6 Factors affecting the voluntary feed intake
of the weaned pig
P.H. Brooks and C.A. Tsourgiannis
6.1 Introduction
For the wild pig, or the domestic pig kept under natural conditions, weaning
represents a slow transition from reliance totally on sows milk to a situation where
the pig has become an independent forager no longer reliant on nutrients
supplied by its mother. For the domesticated piglet, weaning is an event, an abrupt
separation from the sow and a sudden denial of maternal support. The response
of the piglet to this separation depends upon the experience that it has gained before
this event, and the age at which the event takes place. Typically, domestic piglets
are removed from the sow, between 12 and 28 days of age; much earlier than they
would be denied maternal support in natural conditions. Consequently, they have
to develop new feeding strategies in hours rather than weeks. Their inability to make
this transition quickly frequently results in a reduction in growth rate immediately
following weaning. Pigs that may have been growing at around 200-300 grams per
day before weaning, experience a period of very low or even negative growth
immediately following weaning. This has usually been treated as a nutritional
problem. Nutritionists have attempted to compensate for the low feed intake of
weaned piglets by increasing the nutrient density of the diets and have responded
to the enteric problems that ensue by the addition of antimicrobial products to
the diet. However, this chapter will propose that the problems facing the newly
weaned domestic pig are behavioural rather than nutritional. By attempting to
understand the evolutionary advantages that the pig would gain from certain natural
patterns of behaviour, we may be able to appreciate the extent to which commercial
weaning practices for domestic pigs have subverted these behaviour patterns. By
understanding the changes that the pig has to make to its behaviour following
weaning, we can explain why some management practices may adversely affect feed
intake. Conversely, an improved understanding of behaviour may allow us to develop
management practices that will enable the young pig to maintain its pre-weaning
growth in the post-weaning period.
6.2 Feeding behaviour of piglets kept under

‘natural’ or ‘semi-natural’ conditions
In order to understand the problems that the domestic piglet faces in confinement
housing systems, it is important to refer to our knowledge of behavioural
development in wild pigs and domestic pigs kept under conditions that are more
natural. In nature, weaning is not an event, but a process that takes place over a

Brooks and Tsourgiannis
several weeks. This process has three different but interrelated developmental strands,
namely, behavioural, nutritional and immunological. The appropriate development
of each strand influences the health of the pig and its ability to function
independently from of its mother and from its littermates.
The piglet has to adapt from a situation in which it obtains all its food by suckling
the sow, which is an instinctive behaviour, to foraging / independent feeding, which
has significant learned components. Initially, the piglet relies totally on its
mother’s milk. Sows milk provides not only nutrients, but also immunoglobulins,
bioactive proteins and peptides, which stimulate and modulate the development
of the gut (Zabielski, 1998). The sow is the most important factor influencing the
microbial environment into which the piglet is born (Conway, 1966). The first
bacteria that the piglet encounters are organisms colonising the sow’s vagina and
teats and emanating from her faeces. These organisms are ingested during the birth
process, and from the sow’s teats when the piglet subsequent suckles, and have a
profound influence on the structure and biochemistry of the gut, the gut ecosystem,
and on immunological development (Kelly and King, 2001).
Under natural conditions, the pre-weaning lactation period can be divided into
four phases (Table 6.1). For the first 10 days of lactation (range 3-16d), the piglets
remain in, or in very close proximity to, a nest prepared by their mother (hiding
phase) (Jensen and Redbo, 1987). When the piglets leave the nest their mother
takes them to rejoin the matriarchal group. From this point on the piglets will
accompany the sow on her foraging trips (following phase) (Jensen, 1986). The
piglets do not necessarily forage, but will rest close by the sow as she forages. As
the piglets grow, their fat reserves increase; they gain strength, and will spend
increasing amounts of time in the close proximity of the sow and will watch her
foraging. They will sample the feed that the sow eats. This sampling of food and
non-food substrates (e.g. soil) exposes the gut to novel food sources, antigens and
microorganisms. In turn, this exposure to novel substrates stimulates the
development of the piglet’s gut enzyme system (Kidder and Manners, 1978) and
contributes to the development of active immunity. The period around three weeks
of lactation can be considered an immunological low point. Passive (colostrum
derived) immunity has declined to a low level and active immunity is only just
starting to develop.
The sow initially determines the pattern of food acquisition by the piglet. Sows initiate
nursing on a cyclical basis (Lewis and Hurnik, 1986). Pigs are drawn to the sow by
her vocalisations regardless of how hungry they may be (Lewis and Hurnik, 1985).
This response maintains the contiguity of the litter and synchronises behaviour
(Castren et al., 1989). Although piglets generally suckle from the same teat
throughout lactation (de Passille and Rushen, 1989; Fraser and Morley-Jones, 1975;
McBride, 1963), the pattern is not constant (Puppe et al., 1993). There is considerable
82 Weaning the pig

Factors affecting the voluntary feed intake of the weaned pig
Table 6.1. Schematic outline of the development of piglets under natural conditions.
Week Phase Behavioural features Influence on piglet development
1 Hiding Piglets initially isolated in nest Nutrients provided entirely by mother.

built by mother. Development of GI tract determined
Limited excursions beyond the by nutrients and bioactive molecules
nest. in sow’s milk.
Initial microbial colonisation of GIT
dominated by flora from sow.
Passive immunity provided by
immunoglobulins in sow’s milk.
2-3 Following Piglets leave nest and follow Milk still dominates nutrition.
(Familiarizing) sow. Bioactive molecules in milk continue
Sow and litter rejoin to influence GIT development.
matriarchal group. Limited sampling of environment
Piglets remain in litter group exposes GIT to other microbes.
with little or no integration Active immunity develops in response
with other piglets. to sampling of environment.
Piglets start rooting.
4-7 Integration Piglets increase foraging Nutritional demand of piglets starts to
(Learning?) (grazing) behaviour. outstrip supply by sow stimulating
Piglets start to integrate with pigs to forage for themselves, usually
others. in proximity of sow.
Sow leaves piglets for increasing Reduced suckling opportunities and
periods. limitations of nutrient supply by
Interval between nursing events sow encourage piglets to forage
increases. independently.
Sows increasingly terminate New food sources stimulate develop-
nursing events. ment of GIT and immune system.
Piglet become fully integrated Milk still contributes to gut health and
with other members of the development.
social group. Passive immunity is no longer effective.
Piglets engage in agonistic behaviour,
resolve conflicts and develop new
social structure.
8-17 Independent Nursing by the sow becomes Piglets become increasingly
less frequent and at some independent of both the sow and
point ceases (pigs weaned). their litter group.
Piglets function independently as Piglets develop independent feeding
part of extended social group. strategies (meal size/ meal interval).
Piglets may still sleep in family Removal of milk represents the final
group with sow. stage in GIT development.

variation in milk production from different teats (Algers and Jensen, 1991; Fraser,
1980; Fraser and Thompson, 1986). It is generally presumed that the anterior teats
are the most productive and are claimed by the stronger more vigorous piglets. Recent
studies on domestic pigs would suggest that this is correct and that teat order becomes
more rigid as the lactation progresses (Puppe and Tuchscherer, 1999). The formation
of a teat order may promote orderly feeding and eliminate competition between
piglets when feeding (Fraser, 1980; McBride, 1963). This may be important for the
piglet’s survival, as milk is only available for 10-20 seconds at each nursing event
(Barber et al., 1955; Fraser, 1980; Whittemore and Fraser, 1974).
There is considerable variation in the interval between nursing events (Table 6.2),
but it averages approximately 50 minutes in the first week of lactation. The intra-
suckling interval increases to around 90 minutes after 2-4 weeks (Horrell, 1997)
and over 300 minutes by ten weeks of lactation (Bøe, 1991). It also becomes
increasingly variable (30->200 minutes) between 6 and 10 weeks of lactation
(Newberry and Wood-Gush, 1985). Similar intra-suckling intervals occur in wild-
type and domestic sows in the first week post farrowing (Gustafsson et al., 1999).
However, in the second week of lactation the intra-suckling interval tended to be
longer in domestic sows.
Table 6.2. Estimates of intra-suckling intervals.
Interval (minutes) Day of lactation Reference
40 to 45 1 to 13 (Arey and Sancha, 1996)

40 to 60 1 to 14 (Gustafsson et al., 1999)
29 to 78 1 to 42 (Newberry and Wood-Gush, 1984)
76 3 (Spinka et al., 1997)
51and 63 (range 26-96) 6 to 51 (Barber et al., 1955)
44 range (21 to 92) 7 to 28 (Ellendorff et al., 1982)
48 to 52 10 to 24 (Auldist and King, 1995)
52 (range 42 to 68) 14 to 5 (Wechsler and Brodmann, 1996)
53± 9.7 First 48 h (Horrell, 1997)
42± 2.4 6 to 8
91± 6.7 14-28
86± 21.3 42-49
64 14 (Bøe, 1991)
72 28
102 42
182 56
334 70
84 Weaning the pig

The extension of the interval between nursing events coincides with the increasing
nutrient demand of the piglets and the reduction in nutrient supply by the sow,
which occurs from 3-4 weeks onwards (Mackenzie and Revell, 1998). The sow
increasingly terminates suckling bouts and by the fourth week of lactation sows
terminate them all (Jensen and Recen, 1989). Sows have been observed to nurse
their pigs while standing from 4 weeks of lactation (Bøe, 1991). This encourages
the piglets to find alternative sources of nutrients. Despite this, some sows
continue to suckle their piglets intermittently for up to 20 weeks. Bøe (1991)
observed that although the number of sucklings per day gradually decreased there
was no drop in daily weight gain as the piglets increased their intake of solid food
to compensate for the reduced intake of sow’s milk.
The period from around four to around eight weeks of age can be regarded as an
integration and learning phase in the piglet’s behavioural development. Despite being
part of the group, there is little mixing or interaction with other pigs before four
weeks of age (Jensen, 1986). The family affiliations loosen between six and eight
weeks, with piglets increasingly associating with pigs in the group that are not
littermates (Jensen, 1995). There is considerable variation in the relationship between
sows and individual pigs in their litter. The proportion of sucklings at which one
or more of the litter was missing increased up to 12 weeks post-partum. The pigs
that missed sucklings were within the lighter half of litters and, although near the
sow, did not seem to take any interest in suckling. The average age for complete
weaning of litters appears to be around 17 weeks of age (Jensen and Recen, 1989;
Petersen, 1994). However, there were large variations between pigs within litters (range
15.6 to 19.5 weeks). This implies that piglets suckling less productive teats invest
less time and effort in trying to obtain nutrients from their dam and increasingly
adopt an independent foraging strategy. From around four weeks onwards, piglets
become members of a larger matriarchal group and will forage alongside the adults
within that group (integration/learning phase). The piglets learn foraging behaviour
by following their mother and by copying her behaviour patterns. It is likely that
they learn from her example which sources are suitable food materials and which
are not. Although piglets have been observed to root from the first week of life
onwards, grazing behaviour appears to commence at around three weeks of age and,
between 4 and 11 weeks of age, piglets increased the proportion of time spent grazing
from 7 to 56% (Petersen, 1994). The pig is an opportunistic feeder and is primarily
herbivorous (Baber and Coblenz, 1987). Ninety percent of the diet of the wild pig
is vegetable matter, of which 50% comprises seeds and fruits (Spitz, 1986). The
remaining 10% of the diet comprises ground-dwelling insects, molluscs and
earthworms. Consequently, when the wild piglet starts taking solid food, that food
will have a dry matter content of between 15 and 30%.
In nature, this gradual transition from a milk diet, through a mixed diet, to a diet
devoid of milk, provides the stimulus, and allows time for, the enzyme and immune

systems of the immature gastrointestinal tract (GIT) to develop and for adaptation
of the microbial population in the gastrointestinal tract.
We can summarise the key features of the weaning process under natural or semi-
natural conditions as follows: -
• Weaning is not a single event, but an extended process of gradual adjustment

that occurs over a period of three or more months.
• Sow milk continues to be available to the piglet while it samples novel foods
and while its gut adapts microbiologically and immunologically to these new
food sources.
• The slow changeover from total dependence on sow’s milk to total dependence
on solid food maintains continuity of nutrient input and prevents transient
starvation.
• The piglet integrates into the larger social group over a period of time and with
a minimum of aggression.
• Initially, the sow determines the feeding strategy of the piglet and sow
vocalisations and the behaviour of littermates reinforces group-feeding
behaviour.
• Independent foraging starts at different ages for different pigs, prompted by an
inadequate supply of sow milk to the individual. However, for the majority of
pigs within a litter, group-feeding (suckling) behaviour is still a significant
component through to 8-10 weeks of age.
6.3 Commercial weaning practice - an event rather

than a process
For practical reasons weaning on commercial pig units has little in common with
weaning in natural conditions. Some of the key differences between natural and
commercial weaning are summarised in Table 6.3. Sows and their litters are normally
housed individually prior to weaning, so there is no opportunity for the pigs to
socialise with non-littermates. In order to maximize sow reproductive output piglets
are removed from their dams before they have achieved behavioural independence.
In recent years, there has been a trend towards very early weaning in North America
(12-18 days) while in the EU weaning below 21 days is not permitted. The EU plans
to increase the minimum age at weaning to 28 days and in some European countries,
such as Sweden, where the use of antibiotic growth promoters has been banned,
weaning age is often increased to 35 or even 42 days. At weaning pigs are moved
to a new environment and frequently new and larger social groups are formed by
mixing unfamiliar pigs. Solid feed and water is provided for them from unfamiliar
dispensers. The age at which weaning takes place, and the amount of experience
that the piglet has had of alternative feed sources, influence its ability to cope with
these changes. In addition, the environment into which the pig is weaned and the
86 Weaning the pig

Table 6.3. Key differences between natural and commercial weaning.
Natural weaning Commercial weaning
Piglets integrate with other members of an Piglets generally have no opportunity to

extended group before and during the integrate with non-littermates before
weaning process. weaning.
Weaning is an extended process occurring Weaning is a single event, taking place on a
over a period of around three months. specific day (generally varies between 14
and 35 days).
Sow milk continues to be available to the Sow milk (and its bioactive constituents) is
piglet while it samples novel foods and not available to support the transition to
while its gut adapts microbiologically and dry feed.
immunologically to these new food
sources.
The slow changeover from total dependence Sudden removal of sow milk results in
on sow’s milk to total dependence on transient starvation, adverse effects on the
solid food maintains continuity of nutrient gut architecture and limited, zero, or
input and prevents transient starvation. negative growth for a period immediately
post weaning
Solid food contains around 200 g DM per kg Solid food contains around 800-850 g DM
per kg.
No change of environment at weaning Piglets usually moved to a new environment
and have to adapt to different feeding and
drinking equipment.
Piglets continue to sleep with sow(s) in the Piglets removed from the sow.
matriarchal group even after weaning.
The piglet integrates into the larger social Piglets frequently regrouped and mixed
group over a period of time and with a unfamiliar pigs at weaning, resulting in
minimum of aggression. considerable aggression and potential
physical damage.
way the pig is managed following weaning contribute to the success or failure of
the transition. The following sections consider the ways in which pre- and post-
weaning management influence feed intake and contribute to the success or failure
of the weaning process.
6.4 Pre-weaning feed and water intake

The young pig has little control over its food intake. While the young of any species
are being suckled, there is no evolutionary value in them having their intake limited.
It is beneficial for them to consume all the nutrients that the dam can provide.

Consequently, the mother is the factor determining feed intake, not the physiology
of the animal being suckled. Despite selection to produce large quantities of milk,
modern sows are still unable to satisfy the demands of their growing litter from a
relatively early stage of lactation. Over the years a number of authors have shown
that piglets can achieve greater growth on milk based diets than they can if left to
suckle the sow (Benevenga et al., 1990; Braude et al., 1970; Harrell et al., 1993;
Zijlstra et al., 1996). Harrell et al. (1993) have calculated that the milk production
of modern sow genotypes becomes limiting to the growth of their litters at around
8-10 days of lactation. They also calculate that by 21 days of age the sow would
need to produce in excess of 18 kg milk per day (approximately twice the milk
yield of modern sows) in order to support growth rates equivalent to those achieved
by artificially reared pigs. As the sow’s milk output is inadequate to meet the piglet’s
demands, and in order to prepare pigs for weaning, piglets may be offered solid
(creep) feed before weaning. However, as discussed earlier, in natural conditions
piglets take little in the way of solid food in the first three weeks after birth. Domestic
pigs in confinement housing show the same pattern. Consequently, piglets weaned
at 21 days or less will have consumed little or no solid food. For example, Metz
and Gonyou (1990), reported that piglets weaned at two weeks of age consumed
only 7 g food per day in the two days before weaning, whereas piglets weaned at
four weeks of age consumed 127 g. Pajor et al. (1991) found that although confined
piglets began sampling feed at around day 12 (ranging between day 10 and 28),
intake was generally less than 5 g per pig per day up until day 20 of lactation. Between
day 20 and 28 piglets consumed an average of 63 g/d, but there was great variation
between individual piglets (2-205 g/d). The total intake before weaning varied from
13-1911 g/pig. Similarly, Delumeau and Meunier-Salaün (1995) found that
feeding activity started around 21 days and, in weeks 3 and 4, creep feed intake
was very variable between litters (range 0-2382 g). It would appear that while the
sow is available as a provider of nutrients, the piglet concentrates its efforts on
stimulating the sow to suckle more frequently and provide more milk, rather than
utilising other available sources of nutrients to maximise its feed intake. This is
demonstrated by the data of Bøe and Jensen (1995) (Figure 6.1). In their study,
piglets continued to suckle sows for eight weeks. The intake of creep feed by
individual pigs ranged between 0-437 g/d at four weeks of age and 0-1571 g/d at
eight weeks of age. The range in weight of piglets at eight weeks of age (range 6.3-
26.6; mean 17.7) reflected the wide difference in nutrient intake.
It would seem reasonable to expect that the pigs suckling less productive teats would
compensate for their limited nutrient supply by taking more creep feed, and this
has been confirmed in some studies (Algers et al., 1990). Fraser et al.(1994) reported
that, in piglets weaned at 28 days, creep feed consumption varied greatly between
littermates, but that pigs consuming more creep feed than their littermates tended
to be those that had the lowest weight gains up to three weeks of age. However,
other authors have reported that larger piglets, occupying the more productive teats,
88 Weaning the pig

2000 20
Creep feed intake (g/d)
Mean piglet weight (kg)

1600 16
1200 12
800 8
400 4
0 0
4 5 6 7 8
Week of lactation
Creep feed intake (mean and range) Piglet weight
Figure 6.1. Variation in the creep feed intake of individual pigs during weeks 4-8 of
lactation. (After Bøe and Jensen, 1995). N.B. the bars represent the range of individual
pig intake at each sampling point.
also consumed more creep feed (Bøe, 1991; Bøe and Jensen, 1995). The variability
in feeding behaviour and feed intake by individuals before weaning has important
implications for weight at weaning and for the development of the gastrointestinal
tract (Nabuurs et al., 1996). Therefore, it is important to try to understand the reasons
for these wide variations in pre-weaning feed intake.
In recent years, researchers have attempted to classify piglets based on individual

behaviour traits. Hessing et al. (1993) classified piglets as ‘aggressive’ and ‘non-
aggressive’ based on them displaying an active or passive coping strategy. However,
other researchers have robustly refuted this classification (Forkman et al., 1995;
Jensen et al., 1995a). Forkman et al. (1995) identified three personality traits that
explained 60% of the total variation, namely, aggression (25%), sociability (20%)
and exploration (15%), whereas Jensen et al.(1995b) found no evidence of
consistent individual behaviour strategies similar to those displayed by rodents.
However, individual ‘personality’ was not related to performance in any of these
studies. To date the only evidence for a link between individual behaviour traits
and growth performance comes from studies undertaken using 17-day-old, weaned
pigs (Giroux et al., 2000). In their study, they found a relationship between rank
order and growth in piglets. However, the social rank of the piglets accounted for
only 9% of the variation among individuals. It is our contention, that the strongly
reinforced group feeding behaviour of suckling pigs provides the explanation for
the observed differences. We have noted that piglets with a less productive teat will
often take creep feed while littermates with productive teats suckle the sow. This
is consistent with the findings of Appleby et al. (1991; 1992), who compared creep
feed intake of piglets provided with 2 or 8 creep feeding spaces (Figure 6.2).

140
Creep food intake per piglet (g)
120
100
Gain 21-28d=261g
80
60
40 Gain 21-28d=248g
20
2 feeding spaces 8 feeding spaces
0
21 22 23 24 25 26 27
Day of lactation
Figure 6.2. Consumption of creep feed by piglets provided with 2 or 8 creep feeding
places (After Appleby et al., 1992).
On average, 4.1 piglets per litter consumed very little on the day before weaning
when only two feeding spaces were provided. These tended to be piglets that had
a high birth weight, and high growth rates on days 0 to 21, but low growth rates
from day 28 (weaning) to day 42. Conversely, piglets that ate the most creep feed
were often those that had gained least on days 0-21. Providing eight feeding spaces
increased the average intake on the three days before weaning and reduced the
number of pigs eating very little on the day before weaning to 0.6 pigs per litter.
Usually, creep feed is supplied as a meal or a pellet; however, there have been some
notable improvements in performance when piglets have been offered
supplementary nutrients in liquid form. In a very large study, Azain et al. (1996),
offered piglets a liquid milk replacer from birth to weaning at 21 days and found
that they consumed 0.375 and 1.49 kg DM during the cool and warm season
respectively, resulting in a significant increase in weaning weight. However, as with
solid feed intake there was great variation in consumption between and within litters.
Significant increases in weaning weight resulting from feeding liquid diets have
been reported in other studies (Kavanagh et al., 1995).
Not only food intake but also water intake varies considerably in the pre-weaning
period. The type of drinker provided also affects water intake (Gill, 1989). In the
humid tropics, piglets began to drink water between 3 and 5 hr after birth (Kabuga
and Annor, 1992; Nagai et al., 1994). Nagai et al. (1994) found that water
consumption per pig increased from 36 ml/day at day 1 of lactation to 403 ml/day
90 Weaning the pig

at day 28. Interestingly, water consumption per kg body weight remained constant
at 51 to 62 ml, regardless of age. Over a 7-week lactation, piglets provided with
water ate more creep food (3215 g/pig) than control piglets that had no water
provided (2166 g/pig) (Friend and Cunningham, 1966). However, up to 3 weeks
of age, there were no treatment differences and the piglets consumed only 62 g
creep food per pig. Gill et al. (1991) found that up to 3 weeks of age piglets consumed
only 34.7 ± 3.4 g creep feed per pig, and that the provision of water did not increase
creep feed consumption.
6.5 Relationship between pre-weaning food

consumption and post-weaning growth
It might be anticipated that familiarity with food and water before weaning would
be an advantage to the pig and would result in improved feed intake and live weight
gain thereafter. However, there is no compelling evidence that this is the case when
pigs are weaned at 21 days or less as they will have had little experience of feed.
Piglets that ate more solid food before weaning gained more weight in the two
weeks following weaning (Appleby et al., 1991). However, the pigs with the higher
creep feed intakes also had higher birth weights so the apparent response may merely
reflect greater developmental maturity in these pigs. Subsequently, Appelby et al.
(1992) characterised pigs based on their individual creep feeding behaviour (Table
6.4). They found an inverse relationship between birth weight and creep feeding
behaviour, and that increasing creep feed intake did not result in any increase in
growth rate in the post-weaning period. By 42 day of age, there was no significant
difference between the pigs classified in the different groups.
Table 6.4. Weights and performance of piglets according to their creep feeding category
(based on the proportion of time they were seen at the creep feeder) (After Appleby
et al., 1992).
Creep feeding category
Body weight (g) Very low Low Medium High
Birth 1572 1509 1471 1280

42 days 10939 11308 10774 10601
Gain (g/d)
Day 0-21 218 198 170 177
Days 21-28 240 267 244 254
Days 28-42 224 271 284 257

In the case of pigs weaned at 28 days or later, there is some evidence of beneficial
effects of creep feeding. Pajor et al.(1991) found that litters with the greatest average
feed intake had the highest post-weaning gains. However, there was little evidence
of a similar relationship within litters. Post-weaning feed intake tended to be higher
in piglets with an estimated creep feed intake above 100g between days 14 and 27
(Delumeau and Meunier-Salaün, 1995). Friend et al. (1966) found that pigs that
consumed more creep feed than their littermates tended to be those with low gains
in the first three weeks after birth. They found that creep feed intake accounted
for only 4% of individual variation in post-weaning gain.
In another study, pigs weaned at 27 days were fed creep feed either as dry pelleted
feed or as fermented liquid feed (Brooks and van Zuylen, 1998). Piglets were divided
into two weight groups at weaning, 5.5-7.5 kg (Low) and 7.5-9.5 kg (High) and
were all fed fermented liquid feed for three weeks post weaning. Dry feed was offered
in addition from 14 days post weaning. There were no significant differences in
post weaning growth rate, although pigs that had low weaning weights, and pigs
that had received fermented liquid creep feed, tended to have higher growth rates
(Table 6.5).
Examination of the growth rate data on a weekly basis revealed a significant

difference in growth rate between the two weaning weight groups during the first
week post weaning (Table 6.6). Pigs with a low weaning weight had a growth rate
more than double that of their heavier littermates. However, the higher growth rate
was not sufficient for them to catch up with the initially heavier pigs by three weeks
post weaning.
In practical situations, producers often attempt to encourage intake by providing

continuity of feed pre- and post-weaning. However, this is of little assistance if the
pre-weaning pig has not sampled the feed. A different approach was attempted by
Campbell (1976) who fed a flavouring agent to sows that would expressed in their
Table 6.5. Post-weaning performance of pigs with low or high weights at weaning offered
fermented liquid feed (FLF) or dry pelleted feed (DPF) during the suckling period
(After Brooks and van Zuylen, 1998).
Weaning weight (kg) Pre-weaning feed regime
5.5-7.5 7.5-9.5 FLF DPF
Dry matter feed intake (g/d) 427 402 422 406

Daily gain (g) 372 353 373 351
Dry matter FCR 1.15 1.13 1.14 1.14
92 Weaning the pig

Table 6.6. Post-weaning growth rate (g/d) of pigs with low or high weights at weaning
offered fermented liquid feed (FLF) or dry pelleted feed (DPF) during the suckling
period (After Brooks and van Zuylen, 1998).
Weaning weight (kg) Pre-weaning feed regime SED
5.5-7.5 7.5-9.5 FLF DPF
Week 1 204a 97a 156 144 37

Week 2 333 411 378 366 41
Week 3 577 552 585 544 37
Overall 427 402 422 406 82
a means with the same superscript differ significantly P<0.05.
milk and then added the same flavour to the post-weaning diet of the piglets, which
were weaned at 30 days of age. The aim was to encourage consumption feed intake
by association with a familiar flavour. In this study, the provision of flavour in both
the sow feed and the weaner diet the pigs significantly increased feed intake and
daily gain. These studies do not appear to have been repeated in pigs, although a
similar approach has been investigated in human infants (Mennella and Beauchamp,
1991; 1993; Mennella et al., 2001).
In summary:
• Piglets weaned at 21 days or less, and previously offered creep feed, are unlikely
to have consumed more than a few grams. Therefore, they will be unfamiliar
with the concept of consuming solid food.
• In litters weaned at 28 or more days piglets will have a very variable experience
of solid food consumption. Some will have become familiar with solid food;
others will have little or no experience of solid food.
• The balance of evidence would suggest that in pigs weaned at 28-35 days the
larger pigs in the litter, which have suckled the most productive teats, would
have least experience of eating solid food.
• Providing more feeding spaces is likely to improve creep food consumption.
• Liquid feed supplements may be consumed more readily than dry feed.
• Irrespective of the form in which creep feed is presented the differences in intake
between litters and between pigs within litter are extremely large.
• Experience of obtaining water and water intake will be very variable within and
between litters.

6.6 Feeding behaviour of the post-weaned pig

Following abrupt weaning the piglet has to adapt its feeding and drinking
behaviour very rapidly to take account of its new environment. Generally, it fails
to do this and as a result, there is a dramatic reduction in its dry matter intake
(Figure 6.3) following weaning. Dry matter intake does not recover to the pre-
weaning level until the second week post weaning.
As described earlier, in natural conditions, weaning is a gradual transition from

sow’s milk (circa 20% dry matter), to a solid diet containing 15-30% dry matter,
over a number of weeks. This is in marked contrast to the situation on commercial
units. The confinement-reared piglet is weaned abruptly and expected to make an
instant transition from a liquid diet, of around 20% dry matter, to a compound
diet containing 80-90% dry matter, usually presented in pelleted form. Before
weaning the stimulus provided by the sow has two important effects on feeding
behaviour. First, the sow calling her piglets to feed conditions them to suckle at
regular intervals and, second, it programmes the litter to feed as a group (Brooks
and Burke, 1998). Abrupt weaning removes the stimulus to eat at regular intervals
that was previously provided by the sow. If litter groups are separated, the
stimulus of group (litter) behaviour is also disrupted.
700
Average dry matter intake (g/pig)
600
500
400
Weaning
300
200
100
0
1 2 3 Day Day Day Day Day Day Day 5 6 7 8
1 2 3 4 5 6 7
Week of Day following weaning Week of

Lactation* (Week 4 of age) age
Figure 6.3. Typical (mean) feed intake pattern of pigs weaned at 21 days.
* Dry matter intake in lactation is the sum of sow milk and creep feed.
94 Weaning the pig

Attempts have been made to stimulate feeding behaviour in pigs by playing recorded
sow feeding calls. Playing recorded sow nursing chants in a farrowing house at regular
intervals improved piglet growth by around 8% in one study (Cronin et al., 2001)
but had not noticeable effect on performance in another (Kasanen and Algers, 2002).
Similarly, playing recorded nursing chants to weaned piglets had some effect on
feeding behaviour (Csermely and Woodgush, 1981; Petrie and Gonyou, 1988). The
latter authors found that playing nursing chants to pigs increased feeding time from
104 to 127 minutes on the second day after weaning, with inconclusive effects on
growth performance.
Keeling and Hurnik (1996) hypothesized that familiar individuals would spend
more time at the feeder and be more synchronized than unfamiliar individuals.
They found that this was correct in the case of females but not males. Familiar males
were more synchronized in their feeding but unfamiliar males spent more time at
the feeder and ate most feed. We might expect that piglets that were unfamiliar
with food would learn to eat from watching their experienced pen mates. However,
this is not necessarily the case. Nicol and Pope (1994) allowed piglets to observe
either untrained-sibling, or trained-sibling, demonstrator pigs press one of two panels
for food reward during 10 daily sessions. In subsequent tests there were no significant
effects of observation experience on rewarded panel pressing. However, pigs that
had observed demonstrators spent significantly more time facing the operant panels
and directed more non-rewarded presses at the operant panels than did controls.
A recent study (Morgan et al., 2001) attempted to investigate the extent to which
experienced weaners transferred information about solid food to inexperienced
weaners. There was some indication that the presence of an experienced piglet
stimulated earlier feeding behaviour by inexperienced piglets. However, variation
among the experimental animals was such that none of the differences reached
statistical significance. Our observations on commercial units would be consistent
with these findings. We have observed pigs that have suckled together approaching
a feeder together, but this did not ensure that they all ate. If not all the pigs were
able to eat at the same time the dominant pigs fed and the subservient pigs stood
behind and observed. When the dominant pigs were satisfied, they left the feeder
and returned to the resting area. Subservient pigs either took very small meals and
then rejoined the group or did not feed and returned to the resting area with siblings
that had eaten (Brooks, unpublished data). The observed phenomena could indicate
a deficiency in the learning mechanism of some pigs, i.e. they are slow learners or
lack the confidence to act independently. Alternatively, it could indicate an
overriding influence of social behaviour (group synchrony). In nature, synchronous,
group behaviour would benefit the population even if it did not necessarily work
in the best interest of the individual. However, in commercial production, such
group behaviour could (and apparently does) disadvantage some individuals.

6.7 Feed and water intake of weaned pigs

When weaning occurs as a gradual process, piglets have the opportunity to learn
by experience about food and water, without interruption of nutrient intake from
the sow. In contrast, domestic pigs weaned at 21 days or less will have been used
to having both their hunger and their thirst satisfied by the sow’s milk. When weaned,
these piglets have to learn to distinguish between the physiological drives of hunger
and thirst. They also have to learn how to satisfy these drives by consuming water
and solid food. Lack of familiarity with food and water means that it may take
some time for the pig to learn how to satisfy its requirements and maintain its
homeostatic balance. Some years ago we reported a study demonstrating that in
the immediate post-weaning period, piglets consumed water rather than eating food
(Figure 6.4). Only when they learned to recognise food did they develop a more
normal water to feed ratio (Table 6.7).
Recent studies have demonstrated that not only is there great variation in the feeding
behaviour of pigs pre-weaning, but also there is great variation immediately post-
weaning. Using a computerized weighing station, Bruininx et al.(2001b) measured
the intake of individual pigs in a group-housing situation immediately post-weaning.
Their data (Figure 6.5) illustrated two important points. First, there was considerable
variation in the interval from weaning to the first feed, with around 10% of pigs
taking more than 40 hours to take their first feed and some taking almost 100 h.
2.2
2.0
1.8
1.6
Water intake (I)
1.4
1.2
1.0
0.8
0.6
0.4
0.2
0.0
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24
Day post weaning
Figure 6.4. Water intake (litres per pig per day) of piglets weaned at 21 days of age
(After Brooks et al., 1984).
96 Weaning the pig

Table 6.7. Ratio of water consumed (g) to food consumed (g) by pigs weaned at 21(1
days of age and fed on two commercial diets (After Brooks et al., 1984).
Week post weaning Water:Feed ratio
Commercial diet A Commercial diet B
1 4.3:1 4.0:1
2 3.2:1 3.5:1
3 2.9:1 3.6:1
4 2.8:1 3.7:1
Second, the number of pigs that had started to eat increased very little during the
dark phase. As the performance of the pigs fed using a computerised station was
similar to that of pigs fed using single space feeders (Bruininx et al., 2001a), it may
be assumed that the pattern of feed intake was similar to that pertaining in this
type of feeding system. However, such systems prevent social facilitation and prevent
the type of synchronous feeding behaviour that would be more normal in pigs of
this age.
100
90
Fasting pigs, % of total
80
70
60
50
40
30
20
10
0
0 10 20 30 40 50 60 70 80 90 100
Post-weaning interval, h
Figure 6.5. Percentage of pigs not having fed at different intervals post-weaning. Lines
represent pigs in different weaning weight categories. Shaded bands correspond with
dark periods (After Bruininx et al., 2001a).

We have recently studied the latency to first feed in pigs offered liquid feed in a
situation where 50% of the pigs could eat simultaneously (Brooks and Brice,
unpublished data). The results (Figure 6.6) show a similar pattern to the data of
Bruininx et al. (2001b). While a majority of pigs had taken their first meal within
3 minutes of weaning, some pigs were took a very long time (up to 54 h) before
eating their first meal, even though their pen mates had already found and were
consuming feed. We have been unable to find any data on the feeding behaviour
of pigs in situations where the entire litter group have the opportunity to eat together.
In recent years, there has been a trend to house weaners in larger and larger groups
(from 100 to 1000 pigs in a group). However, there has been little attempt to
determine the effect that this has on the individual or the extent to which large
group size affects variability. One advantage of large groups is that littermates are
generally kept together. Subjective observations of pigs in very large groups (100+
pigs) suggest that litters tend to retain an identity and continue to show
synchronised feeding behaviour. In such settings, generally there are insufficient
feeding places for the entire pen group to indulge in synchronous feeding.
However, there may be less disturbance of feeding behaviour than in small groups,
as litter groups can still feed together and independently of other litter groups in
the pen.
23
21
19
17
15
Pig number
13
11
9
7
5
3
1
0 10 20 30 40 50 60
Interval from weaning to first feed (h)
Figure 6.6. Interval from weaning to first feed for group housed piglets weaned at 21
days and offered liquid fermented feed (Brooks and Brice, unpublished data).
98 Weaning the pig

These observations have important implications both for practical management

and for experimental design. Stockpersons need to recognise that even if some pigs
are observed to use the feed and water provided in the pen this does not mean
that all the pigs are. Thus, management strategies must have the aim of ensuring
that feed and water acquisition by all pigs in the group takes place as soon after
weaning as possible. Because experiments usually consider the mean performance
of groups of pigs, treatment differences may result either from a change in the
behaviour of some pigs in the group or from a change in the biological response
of the whole population.
The period for which the pig does not eat post-weaning is particularly important
but so is the pattern of feeding that the pig adopts once it has started to eat. Bark
et al. (1986) allowed pigs weaned at 21 days to feed ad libitum or, for 15 minutes
at 2-, 4-, or 6-hourly intervals. Even the pigs fed ad libitum failed to consume enough
feed during the 3 days post-weaning to satisfy their maintenance requirements, and
feed intake was less in the pigs fed at increasing intervals (Figure 6.7). Consequently,
pigs fed at 4-, or 6-hourly intervals had not regained their weaning weight seven
days post weaning (Figure 6.8).
6.8 The significance of maintaining continuity of

food intake after weaning
It is easy to forget that the epithelial lining of the gut is the most rapidly growing
tissue in the body and that many of the nutrients required for gut growth are
absorbed direct from the gut lumen. The work of Pluske and his co-workers (Pluske
250
Average daily feed intake (g/pig)
200
150
100
50
0
1 2 3 4 5 6 7
Day post weaning
ad lib 2-hourly 4-hourly 6-hourly
Figure 6.7. Feed intake of pigs weaned at 21 days of age and fed ad lib. or for 15 minutes
at 2-, 4-, or 6-hourly intervals (After Bark et al., 1986).

7000
6800
Liveweight (g)
Weaning weight
6600
6400
6200
1 2 3 4 5 6 7
Day post weaning
ad lib 2-hourly 4-hourly 6-hourly
Figure 6.8. Live weight change in pigs weaned at 21 days of age and fed ad lib. or for
15 minutes at 2-, 4-, or 6-hourly intervals (After Bark et al., 1986).
et al., 1996a; 1996b; Pluske et al., 1997), showed that a continuous supply of
nutrients is essential in order to maintain the villous architecture of the gut post-
weaning.
Previous studies suggested that villus height was greater when pigs were fed a liquid
diet rather than a dry diet (Deprez et al., 1987). It was assumed that the physical
form of the food was responsible for this effect. However, the studies undertaken
by Pluske and his co-workers demonstrated that the change in villus height was
not a function of diet form, but of nutrient intake. In their study, feeding liquid
diets at a maintenance energy level still resulted in a reduction in villus height five
days post weaning. However, when pigs were fed an allowance equivalent to three
times the requirement for maintenance, villus height was actually greater than that
immediately pre-weaning. A recent study, using a larger data set (Ward and Moran
unpublished data), has again demonstrated the positive relationship between dry
matter intake and villus height (Figure 6.9).
Conversely, there is good evidence, from rats, that transient starvation can result
in atrophy of the villi (Rudo et al., 1976; Steiner et al., 1968). A reduction in villus
height reduces absorption and leaves more nutrients escaping digestion and entering
the lower gut. This promotes the development of an inappropriate gut microflora
that in turn can result in enteric disease. The practical implication of these findings
is that every effort must be made to maintain continuity of food and water intake
following weaning.
100 Weaning the pig

800
700
Mean villous height (µm)
600
500
400
300
200
100
0
0 500 1000 1500 2000 2500 3000 3500 4000 4500
Total dry matter intake (g)
Figure 6.9. Relationship between total dry matter feed intake (days 5-13 post weaning)
and villus height in piglets fed liquid diets for 14 days post weaning (Ward and Moran
unpublished data).
It appears that the short inter-meal intervals entrained by the suckling pattern of
the sow are important in maintaining the integrity and effectiveness of the piglet’s
gut. The behavioural imposition by the sow of short inter-meal intervals may be
necessary because of the relative immaturity of the piglet at birth. As discussed
previously, when the interval between feeds was increased piglets were unable to
consume sufficient nutrients to satisfy their maintenance requirements (Bark et al.,
1986). More recently, Thorpe et al.(1998) found that the digestibility of nutrients
was dramatically reduced as the interval between feeds increases. Nitrogen
digestibility in pigs fed at hourly intervals was double that of pigs fed 2-hourly
and five times greater than that of pigs fed 3- or 4-hourly. They also noted that a
steady state flow of digesta occurred only when pigs were fed on an hourly basis.
In a recent study, Miller (2002 personal communication) recorded the individual

feeding patterns of group-housed pigs following weaning at 21 days of age. Analysis
of the data demonstrates how misleading conventional statistical treatment of the
data can be. The combined data from 48 pigs indicated a smooth transition to solid
food following weaning albeit with a large standard deviation (Figure 6.10). The
temptation is to assume that the standard deviation represents a range in
performance and that individuals within the population behave in a consistent
manner. However, a more detailed analysis reveals a very different picture. The post-
weaning behaviour of one pen of pigs is presented in Figure 6.11. The results are
separated into two parts for clarity. These data demonstrate that the apparent smooth
transition in Figure 6.10 is actually a statistical artefact, and that there were very
large variations in the feeding patterns of individual pigs. Half the pigs in the group
(Figure 6.11A) had a peak of intake on Day 2 and then a fall, which had not recovered

700
600
Feed intake (g/d) 500
400
300
200
100
0
1 3 5 7 9 11 13 15 17 19 21
Days post weaning
Figure 6.10. Feed intake of pigs housed in groups but individually fed using a
computerised feeding system (After B Miller 2002, personal communication; with
acknowledgement to Parnutt Feeds).
by the end of the first week. Almost half had erratic feed intakes (Figure 6.11B)
with peak intakes occurring on days 4, 5 or 6. In this pen of pigs only one pig (broken
line) showed the steady increase in feed intake over the first week following weaning
that the data in Figure 6.10 might suggest.
Given the results of Thorpe et al.(1998), we hypothesize that such large differences
in feed intake pattern will have profound effects on the villous architecture, the
ecophysiology of the gut and the development of the immune system.
A retrospective analysis of data collected in a number of studies at our centre

demonstrated a highly significant (P<0.001) effect of dry matter feed intake in the
first week post-weaning on the weight of pigs 28 days post-weaning (Geary and
Brooks, 1998). The results of this analysis suggest that each 50g per day increase
in DM feed intake in the week following weaning increased 28-day post-weaning
weight by 870g. Dry matter feed intake in the week post weaning accounted for
as much variation in the 28 day post weaning weight as any combination of weaning
weight, weaning age, sex and dietary treatment.
6.9 The interaction between water and feed intake

post weaning
Voluntary or involuntary deprivation of water post-weaning has serious consequences
for the piglet. Gill (1989) showed that it could take more than a week for the weaned
piglet to restore its daily fluid intake to the equivalent of that on the day before
weaning. Piglets experiencing such reduced fluid intakes can become seriously
dehydrated. The resulting disturbance of the pig’s homeostatic balance has
102 Weaning the pig

500
A
450
400
Feed intake (g/d)
350
300
250
200
150
100
50
0
1 2 3 4 5 6 7
500
B
450
400
Feed intake (g/d)
350
300
250
200
150
100
50
0
1 2 3 4 5 6 7
Days post weaning
Figure 6.11. The pattern of feed intake in individual pigs, weaned at 21 days of age,
housed in a group and fed using a computerised feeding system (After B Miller 2002,
personal communication; with acknowledgement to Parnutt Feeds).
important repercussions on its physiology, as does any subsequent, rapid, re-

hydration that occurs when the pig finally starts drinking. Therefore, it is important
to encourage pigs to maintain fluid intake following weaning. Water consumption
levels in the five days post-weaning appear to have little relationship with
presumed physiological need (Brooks et al., 1984; McLeese et al., 1992). Both over-
and under-consumption of water will reduce feed intake in the weaned pig; over-
consumption by producing physical feelings of satiety, and under-consumption
through disruption of the homeostatic balance.
There are important behavioural components to post-weaning water intake that

must not be underestimated. Pigs that have learned to eat and drink will minimise

their intake of water per unit of feed (water to feed ratio) when fed ad libitum and,
when they are restrict fed, will take additional water to produce feelings of satiety
(Yang et al., 1981; Yang et al., 1984). Suckling pigs have been conditioned to consume
milk to satisfy their needs for total volumetric fill, and in the early post-weaning
period may fail to discriminate between the separate drives of hunger and thirst.
Consequently, they consume water to provide gut fill. Having been used to a liquid
diet they may mistakenly believe that water is also a source of nutrients.
The weaned pig also has to learn to locate water. Piglets may find some difficulty
identifying nipple drinkers as a supply of water. However, there is little evidence that
providing water drinkers that drip encourages water consumption (Ogunbameru et
al., 1991). Providing readily available water in a bowl has been shown to encourage
water consumption and increase feed intake (English et al., 1981). If bowls are used,
their management is critical, as fouling may reduce the palatability and consumption
of water (Brooks and Carpenter, 1990; Phillips and Phillips, 1999; Sorensen et al.,
1994). Some UK producers are now using bell-shaped turkey drinkers to water newly
weaned pigs. They claim that these drinkers encourage water consumption because
the suspended drinker attracts the attention of the piglet and the free water surface
encourages exploration and subsequent consumption. Although there appears to be
no research data to support these claims, performance on commercial units has been
improved by the use of this type of drinker in the immediate post-weaning period.
Drinker design and positioning can influence the acquisition of water post-weaning
and can affect both piglet performance and water use (Table 6.8). It is most important
to position nipple drinkers correctly. Drinkers placed at the incorrect height and
angle or in an appropriate part of the pen will inhibit intake. Building designs that
provide a warm kennelled area for sleeping and a cooler (cold) area where the pigs
feed, drink and eliminate are particularly problematic. The necessity to leave a warm
Table 6.8. Water use by weaned piglets from 3 to 6 weeks of age, provided with water
from five different drinker types (After Gill, 1989).
Drinker type Daily gain Water to feed ratio Water to weight ratio
(g) (l/kg) (l/kg LW)
Mono-flo nipple 199b 5.32 0.23

Arato 76 nipple 260a 3.23 0.13
Lubing bite type I 213b 3.68 0.12
Lubing bite type II 221b 2.90 0.13
Alvin bowl 224ab 3.49 0.14
a, b Means with the same superscript are not significantly different (P>0.05)
104 Weaning the pig

environment and go to a colder area to feed or drink will inhibit these behaviours.
The limited data available on the effects of water temperature on consumption
indicates that, as might be expected, warm water encourages consumption in cold
environmental conditions and cold water encourages consumption at high ambient
temperatures (Standing Committee on Agriculture; Pig Subcommittee).
In the weaned pig, the rate and velocity of the water delivered by the drinker affects
feed intake and performance (Table 6.9). Nipple drinkers with a restricted flow
rate significantly affected both water and food intake with consequent effects on
the performance of pigs weaned at 21 days of age (Barber et al., 1989). The interesting
observation in this study was that pigs given drinkers with low flow rates would
not increase the amount of time that they spent drinking in order to optimise their
intake. In a study involving somewhat older pigs, drinking times were extended,
but they still did not increase the time spent drinking sufficiently to compensate
for the restricted intake (Nienaber and Hahn, 1984).
In another study, increasing water flow rate from 70 to 700 ml/min did not increase
the performance of pigs weaned at 28 days of age (Celis, 1996). In the study of
Barber et al. (1989), pigs provided with water at the lowest flow rate spent only
268 seconds per day drinking. This is similar to the 290 seconds1 per day that they
would have spent actively drinking milk when suckled by the sow. These results
suggest a degree of activity scheduling by the pig, once again conditioned by the
behavioural patterns imposed by the sow during suckling. This becomes less stringent
as the pig increases in age and becomes more familiar with food and water.
1 Calculated on the basis that at in the third week of lactation sows would nurse their piglets 25-29
times per day and the milk ejection per suckling event lasts for 10-20 seconds.
Table 6.9. The effects of water delivery rate on the voluntary food intake and water
use of weaned pigs (After Barber et al., 1989).
Water delivery rate (ml/ minute)
175 350 450 700 SEd
Daily feed intake (g) 303c 323b 341a 347a 3.68

Daily gain (g) 210c 235b 250a 247a 5.57
FCR 1.48 1.39 1.37 1.42 0.03
Daily water used (l) 0.78d 1.04c 1.32b 1.63a 0.01
Time spent drinking (sec./d) 268b 176a 175a 139a 14.4
a, b, c, d Means with the same superscript are not significantly different (P>0.05)

It is clear from the above that the amount of food that the piglet will eat is
determined by the amount of water that it consumes and not the reverse.
Therefore, strategies that increase water consumption may have a positive effect
on feed intake. Responses may be variable. For example, Maenz et al. (1993) found
no improvement in water intake when a commercial sweetener was added to water.
However, if water has a poor taste, the addition of flavourings or sweeteners may
encourage greater water consumption and hence food intake. Perversely, if the water
has good taste characteristics, the addition of a flavour or sweetener may encourage
over-consumption of water to the detriment of feed intake (Table 6.10). Barber
(1992) offered weaned pigs water containing two sweetener/flavour products from
nipple drinkers for the first three days post-weaning and found that it increased
the average number of visits to the drinker in the first hour post weaning from 4
to 10 but did not significantly affect the number of visits made subsequently. Where
facilities exist to make additions to the water it may be desirable to use a product
of this type on the day of weaning to help the pigs locate and start using the water
supply. Because water flavour is so variable, it will be necessary to experiment on
the individual farm to determine whether promoting water intake increases feed
intake or results in the pig over-consuming water at the expense of feed intake.
Table 6.10. Effect on water and feed intake of including a sweetener in the drinking
water of 21 day old weaners for the first three days after weaning (After Barber, 1992).
Control Palasweet™ Palasweet Plus™ SEM
Water intake (L/pig)

Days 1-3 1.23a 1.63b 1.65b 0.09
Days 4-7 1.99a 2.25ab 2.62b 0.12
Days 8-16 6.99 7.30 7.51 0.39
Feed intake (g/pig)

Days 1-3 414a 314b 283b 21
Days 4-7 721 728 691 34
Days 8-16 2580 2214 2434 112
a, b Means with the same superscript are not significantly different (P>0.05)
6.10 Liquid feeding post-weaning

The case for liquid feeding young pigs has been reviewed recently (Brooks et al.,
2001) so only a brief summary is included here, focussing on the behavioural aspects
of this method of feeding.
106 Weaning the pig

In view of the problems that the piglet has in discriminating hunger and thirst it
might be anticipated that post-weaning performance would be improved by offering
a liquid diet. Liquid feeding has potential advantages because: -
• It provides a diet with a dry matter concentration more like that of sow milk
and more like the solid food that the pig would encounter in the wild. This
might encourage intake and maintain continuity of nutrient supply.
• It provides a diet that more closely meets the piglet’s need for both nutrients
and water.
• It overcomes some of the problems posed by the piglets having to learn to satisfy
their drives of hunger and thirst separately.
Until relatively recently, liquid feeding was confined to the use of milk replacer
for the artificial rearing of pigs or for pigs weaned at very young ages. In this context,
and with good hygiene, it has been demonstrated that pigs will grow faster on liquid
diets than they will on the sow (Odle and Harrell, 1998) Liquid feeding has been
limited in application because of the problems in maintaining the feed in a
wholesome and palatable form. However, developments in delivery systems had
resulted in renewed interest in the approach. If feed hygiene can be maintained,
feed intake and growth of weaners is increased by feeding liquid diets and further
improved by feeding fermented liquid diets (Table 6.11).
The greatest benefits were obtained in the week immediately following weaning
where dry matter intake and growth rate are improved by 20-30% (Kim et al., 2001;
Russell et al., 1996). Importantly, the acceleration of early growth is maintained
to market weight (Kim et al., 2001).
Pig producers have been encouraged to offer pigs a liquid ‘porridge’ or ‘gruel’ in
addition to dry feed in the immediate post weaning period. Experimental data on
this is sparse and contradictory. In one study (Beattie et al., 1999), feed intake in
Table 6.11. Improvement (%) in growth rate and food conversion ratio in experiments
in which the performance of pigs fed dry feed (DF), liquid feed (LF) or fermented
liquid feed (FLF) was compared (From the review of Jensen and Mikkelsen, 1998).
No. of trials Improved daily weight gain Improved food conversion ratio
Mean ± SD Range Mean ± SD Range
LF v. DF 10 12.3 ± 9.4 -7.5 - 34.2 -4.1 ± 11.8 -32.6 - 10.1

FLF v. DF 4 22.3 ± 13.2 9.2 - 43.8 -10.9 ± 19.7 -44.3 - 5.8
FLF v. LF 3 13.4 ± 7.1 5.7 - 22.9 -1.4 ± 2.4 -4.8 - 0.6

the 2 days following weaning was improved by offering additional wet feed in an
easily accessible trough increased, but growth performance was not improved over
the 3 week post-weaning period. In another study, Dunshea et al. (2000) provided
weaned pigs with supplemental fermented milk for 8 days after weaning and
reported significantly increased growth rates and pigs that were 20% heavier at 42
days of age. In our own studies, the growth rate of pigs offered fermented liquid
feed in addition to dry feed was intermediate between that of pigs offered either
a dry or a liquid diets (Brooks et al., 2001). An important observation in this study
was that, compared with the pigs offered liquid or dry diets, more of the pigs offered
a choice of diets engaged in antisocial behaviours such as belly-nosing.
Given the previous discussion it is clear that it may not be a sensible approach to
offer both dry and liquid diets. The weaned pig already has the challenge of learning
to differentiate between hunger and thirst and recognising that food and water will
satisfy these needs. Providing it with water, food and a third option of wet feed is
likely to hamper this learning process not accelerate it.
6.11 Conclusions
From the discussion above, it is clear that a wide range of different factors affect
the behaviour of the newly weaned pig and many of these impact directly or
indirectly on its ability to find feed and water (see summary Table 6.12). In addition,
either through lack of experience, or because its homeostatic control mechanisms
have not matured, the piglet can fail to satisfy its physiological requirements for
water and/or nutrients. Thus, the theoretical models of voluntary food intake that
we would employ to describe the control of intake of food and water in pigs with
mature homeostatic mechanisms have no value when trying to explain the
phenomena observed in the period immediately post-weaning when pigs are
weaning at 5 weeks of age or less.
Our attempts to improve performance of the newly weaned pig need to focus on
the development of management strategies that will increase the independence of
the weaned pig from its dam and increase its exploratory behaviour. In this context
we may need to concentrate on the effects that pre-weaning environment can have
on equipping the pig to cope with the changes it faces at weaning. Recent reports
have shown that the housing experienced by sows may affect the behaviour of their
piglets (Beattie et al., 1996), that enriched environments increase piglet activity
(Beattie et al., 1994), and that piglets from outdoor farrowing systems feed more
frequently than pigs from confinement systems (Cox and Cooper, 2001; Webster
and Dawkins, 2000). These findings may point the way forward, suggesting as they
do that more diverse and stimulating environments encourage the development
of exploratory skills that may assist the piglet in making the transition to
independence.
108 Weaning the pig

Table 6.12. Summary of factors affecting feed and water intake in weaned pigs (21-
28 days of age).
Factors adversely affecting feed intake Factors adversely affecting water intake in
in the newly-weaned pig the newly-weaned pig
Lack of previous experience of eating solid food and/or drinking.

(Underdeveloped feeding, drinking and exploratory behaviour).
Inability to discriminate between hunger and thirst.
Inability to find food or water (unfamiliar feed and water presentation).
Cold conditions (pigs huddle rather than actively seeking food or water).
Hot conditions (pigs rest rather than actively seeking food or water).
Agonistic behaviour (fighting in mixed pigs displaces other behaviours).

Lack of feeding stimulus . Water quality (flavour, mineral content,
(no sow vocalisations) microbiology).
Palatability (taste, smell, texture, Water temperature (cold water reduces

freshness, nutrient balance). intake in cold conditions, hot water reduces
intake in hot conditions).
Feed availability (accessibility of Water availability (accessibility of drinkers,

feeding places). flow rate).
Inadequate or excessive water intake
What is not clear from the literature is whether we should be encouraging the weaned
pig to develop individual foraging behaviour, or reinforcing synchronous group
feeding as a way of ensuring that all piglets in a cohort make a successful
transition to solid food. The answer to this question may differ according to the
weaning age and hence the ease with which modifications can be made to entrained
behaviour. This fundamental question needs answering. Without a satisfactory
answer, it is not possible to specify feeding and watering equipment or to devise
management systems that will optimise the performance of all the individuals within
a group.
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Spinka, M., G. Illmann, B. Algers and Z. Stetkova, 1997. The role of nursing frequency in milk
production in domestic pigs. Journal of Animal Science 75, 197-212.
Spitz, F., 1986. Current state of knowledge of wild boar biology. Pig News and Information 7, 171-
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Standing Committee on Agriculture; Pig Subcommittee, 1987. Feeding standards for Australian
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Steiner, M., H.R. Bourges, L.S. Freedman and S.J. Gray, 1968. Effect of starvation on the tissue
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116 Weaning the pig

7 Digestive physiology of the weaned pig
H.M. Miller and R.D. Slade
Summary
Descriptions of the changes in piglet digestive physiology following weaning abound
in the literature to such an extent that review of the subject is suited more to a
dedicated book than just this one chapter. Accordingly we have attempted to draw
the literature together into a brief yet cohesive analysis of intestinal events pre and
post-weaning. In doing so we have encapsulated conventional opinion whilst
endeavouring to introduce novel or poorly documented perspectives. We hope that
this review will help to provoke thought and stimulate continuing innovative
research in this fascinating area.
7.1 Introduction
Profound changes in piglet digestive physiology occur following weaning as the
piglet gut adapts to the change in feed type. In wild pigs these changes would occur
progressively over time as the piglet made a gradual transition from a wholly milk
diet to a wholly non-milk diet, the piglets finally achieving nutritional independence
from the sow at about 8 to 12 weeks of age. However in the commercial situation
piglets are weaned suddenly and uncompromisingly by removal from the sow and
her milk supply at 14 to 28 days of age. Although highly digestible diets are supplied
to the newly weaned piglet, such weaning practice is invariably associated with a
dramatic reduction in feed intake, which in turn is associated with rapid changes
in gut structure and function and reduced overall growth rate. Whilst traditionally
the effects of sudden early weaning have been compared with delayed weaning (35
to 42 days) or gradual weaning in the continuing presence of the sow, such a
dramatic change in piglet diet is not without precedent. At birth the piglet must
face a symphony of changes in which the successful switch from placental to enteral
nutrition plays a key role. Although the gut has had the whole of gestation to develop
a structure suitable for enteral nutrition, extensive functional changes have to occur
within hours of birth to enable adequate digestion and absorption. This adaptation
to enteral nutrition at birth is accomplished with an alacrity that is markedly absent
in the commercial weaning situation.
In this review we will discuss the changes in gut structure and function that occur
with current commercial weaning practice. In addition to describing how these
changes may be affected by age at weaning we have also compared them with the
developmental strategies of the neonatal pig. We hope that this may help us to
understand regulation of postweaning events and thereby improve our ability to
counteract the characteristic post-weaning check in piglet growth. Where appropriate

Miller and Slade
we have also made comparisons with digestive development in other species,

however distinctive differences in gestational, post-natal and post-weaning
development between the pig (precocial) and altrical species (eg. rat, mouse and
rabbit) prohibit generalised comparisons of their digestive physiology. In addition,
the pig has frequently been used as a model for human research because of the
homogeneity of anatomy, physiology, nutrition and metabolism across the two
species (Moughan et al., 1992; Wykes et al., 1993; Ball et al., 1995). Just as the pig
is regarded as a good model for the human we likewise consider the human to be
a good model for the pig and therefore, where research progress in human infant
digestive physiology exceeds that made in the pig, a cautious paralleling of
developmental aspects of the two species has been made.
7.2 Strategies for adaptation to enteral nutrition in

the neonatal pig
The rapid changes in the structure and function of the digestive tract that are triggered
by weaning undoubtedly result in a transient period of sub optimal digestive
competence. Let us first consider how similar problems are resolved in the
neonate.
7.2.1 Preparation
During gestation the complex multicellular systems required for postnatal nutrition
develop progressively (Zabielski et al., 1999) so that by the time of birth the
architecture and mechanisms required for extra-uterine life are already established.
Differentiation of the gut into individual recognisable organs is complete early in
gestation. Thereafter refinement of the structure and development of digestive and
absorptive systems must take place.
Fetal and neonatal gastric development in pigs are described in recent reviews by
Sangild et al. (2000) and Xu et al. (2000). Prenatal growth of the stomach is similar
to whole body growth. Gastric fluid pH (important for bacterial suppression and
activation of gastric zymogens) gradually reduces during gestation to reach 2-4 at
birth. These reductions are paralleled by increases in both intrinsic factor in the
gastric fundus, and gastrin. Development of proteolytic capability coincides with
birth and is evidenced initially by activity of milk clotting chymosins and, with
increasing age, by the general proteolytic activity of pepsins.
Immediately post-partum, growth of the stomach exceeds that of the whole body,
its mass increasing approximately two-fold from birth to 7 days of age (doa). Gastric
acid secretory capacity doubles during the 24 hours following birth (presumably
secretagogue stimulated) and again between 1 and 3 doa. This reflects augmentation
of the gastric tissue and increased gastric gland oxyntic cell volume density and
118 Weaning the pig

Digestive physiology of the weaned pig
HCl secretory capacity per unit of tissue mass. Gastric proteolytic competence also
develops rapidly after birth with protease secretory capacity enhanced 9-fold by 7
doa.
Structural development and cytodifferentiation of the fetal intestinal mucosa follow

a highly organised temporal pattern. Briefly, villi forming from the presumptive
small intestine mucosa are separated one from another by distinct regions of
proliferating cells termed primordial crypts. Subsequently, primordial crypt cells
invade the underlying mesenchyme to form crypt cell regions. Cells produced in
the crypt regions differentiate and mature as they migrate along the crypt to villus
axis. Thus, villus form and function emerge during fetal development. For example,
mechanisms for amino acid transport have been detected in porcine fetal villus
enterocytes as early as 40% gestation (Buddington and Malo, 1996). Rate of amino
acid absorption increases as gestation progresses and rapidly immediately prior
to birth (Buddington et al., 2001), suggesting that the transport mechanisms continue
to be upregulated as gestation proceeds. Similarly, capacities for carbohydrate
digestion and absorption are already established at birth (Manners and Stevens,
1972; Puchal and Buddington, 1992). Following resolution of villus structure and
enterocyte differentiation, ingestion of amniotic fluid is thought to contribute
significantly toward gastro intestinal growth (Buddington, 1993; Buddington et al.,
2001) and may have positive priming effects on post-partum enterocyte competence.
Thus fundamental mucosal characteristics associated with enteral nutrition are fully
developed prior to birth.
Prenatal development of enzyme activities is not limited to intestinal tissues alone.

Pancreatic enzyme activities increase as gestation progresses (Westrom et al., 1987)
and appear to be maximal by the end of gestation, as demonstrated for elastase II
(Gestin et al., 1997a) and chymotrypsin (Gestin et al., 1997b).
There is little discussion of prenatal development of the porcine colon in the

literature. The colon functions to absorb water and electrolytes, and this function
appears developed in the neonate. Conservation of dietary carbohydrate (CHO)
through the action of colonic bacteria relies on inoculation with the appropriate
microbial population since the intestinal tract will be sterile at birth. In early life,
bacteria whose substrate is lactose would be necessary for this function, although
efficient digestion and absorption in the upper gastrointestinal tract (GIT) may
significantly limit the necessity for such bacterial activity. Measurements in the
human neonate indicate the small intestine (SI) is incapable of hydrolyzing and
absorbing all dietary lactose, thus the colon may play a role in CHO conservation.
Murray et al. (1991) studied conceivable routes of colonic energy retrieval from
bypass dietary lactose, including mucosal metabolism and absorption as well as
bacterial degradation to SCFA and subsequent absorption. Their studies indicate
that in the neonatal pig lactose may be directly absorbed by colonocytes in the

Miller and Slade
disaccharide form. The peri-natal colon is able to absorb electrolytes and amino
acids (see for example Henin and Smith, 1976; Sepulveda and Smith, 1979).
However we were unable to find any information describing prenatal development
or activity of these functions.
It is apparent that at birth the young piglet potentially has all the digestive equipment
to start extra-uterine life but the system now requires activation and fine-tuning.
Colostrum intake provides the activation signal required.
7.2.2 Implementation I
Colostrum stimulates intensive growth of the neonatal pig’s stomach, pancreas and
small intestine within 24 hours of intake (Zabielski et al., 1999). Mucosal growth
is characterised by increased DNA synthesis, an increase in protein content (Zhang
et al., 1997), and a decrease in cell turnover (Moon and Joel, 1975). This is
accompanied by marked expansion of villi and microvilli surface areas (Xu et al.,
1992). These changes are thought to be initiated and regulated by intrinsic growth
factors and hormones in the colostrum (Kelly et al., 1992; Buddington, 1993; Pacha,
2000). Cells produced by the crypts during the perinatal period rapidly replace the
fetal villus enterocyte population and this coincides with the onset of changes in
villus structural configuration. The finger-like villi gradually shorten and thicken
throughout the suckled period (Cera et al., 1988), a process paralleled by
reshuffling of hydrolase and nutrient transport activities.
After birth there is a decline in amino acid absorption and monosaccharide uptake
relative to tissue protein content of the enterocytes. However this is compensated
for by rapid mucosal growth (Puchal and Buddington, 1992; Zhang et al., 1998;
Buddington et al., 2001), such that overall capacity for nutrient uptake is unaffected
or increased slightly (Zhang et al., 1997).
Colostrum mediates rapid changes in intestinal hydrolase activity. Zhang et al. (1997,
1998) demonstrated colostrum-induced regional (proximal, mid and distal small
intestine) and compartmental (brush border membrane vesicles and mucosal
homogenate) modification of the specific activities of hydrolases within 24 hours
of birth (Table 7.1). Total intestinal activities of lactase, sucrase, maltase and
aminooligopeptidase are higher 24 hours post-partum than at birth, although their
activities per unit of intestinal protein decrease (Zhang et al., 1997). Pre-partum
endogenous secretion of cortisol is positively implicated in stimulation of these
brush-border hydrolases (Sangild et al., 1995; Sangild et al., 2000). Amplification
of absolute maltase and sucrase activities within 24 hours of birth is paralleled by
increases in fructose transport capacity relative to glucose (Puchal and Buddington,
1992). This may seem surprising for an animal which is receiving an entirely milk
120 Weaning the pig

Table 7.1. Changes from birth in specific (µmol/[min/g protein]) and total hydrolase
activities in small intestine mucosa homogenate and brush-border membrane vesicles
(BBMV) during the initial 24 hours post-partum.
(Adapted from Zhang et al. 1997)
Small intestine homogenate Small intestine BBMV
Region Proximal Mid Distal Proximal Mid Distal
Specific activity
Lactase = = = ↓ 6hrs* = =
Sucrase = ↓ 6hrs = = = =
Maltase ↓ 6hrs ↓ 6hrs ↓ 6hrs = = =
Aminoligopeptidase (AOP) ↓ 6hrs ↓ 6hrs = = = =
Hours post-partum 6 12 24 6 12 24
Total activity
Lactase ↑ ↑ ↑ = ↑ ↑
Sucrase = ↑ ↑ = = =
Maltase ↑ ↑ ↑ = ↑ ↑
Aminoligopeptidase (AOP) = = ↑ = ↑ ↑
= no significant change in activity

↓↑ significant decrease or increase in activity
* decreased at 6 hours, = at 12 hours, decreased at 24 hours
diet, but indicates that the piglet is evolutionally equipped to digest and absorb
non-milk as well as milk foods almost immediately after birth.
The nascent capacity to digest sucrose and maltose apparently develops

independently of luminal exposure to these compounds, but is influenced by feed
intake and composition. Zhang et al. (1998) examined intestinal structure and
function in piglets 6 hours after birth in response to feed deprivation (FD) or gastric
intubation with similar volumes of colostrum (C), milk replacer (MR) or an oral
electrolyte solution (OES). In this study, total intestinal maltase activity in mucosal
homogenate was elevated in C compared to FD pigs; MR and OES were intermediate
but tended to be lower than in C contemporaries. Brush-border membrane vesicle
(BBMV) total maltase and aminooligopeptidase activities were greater for C than
OES with MR measurements falling between the two: FD values were comparable
with MR and OES treatments. Treatment effects on gut morphology were not
reported, however intestinal length and nominal surface area (intestinal

Miller and Slade
circumference x length) declined in the order C/MR >OES/FD and C > MR/OES
> FD respectively. Therefore it appears that intestinal hydrolase activities and
intestinal enlargement are stimulated by the physical presence of material in the
intestine and that such stimulation is differentially enhanced by the material’s
nutritional and/or bioactive composition. Furthermore, the compositional qualities
of colostrum appear to initiate development of intestinal characteristics associated
with weaned pig digestive physiology.
In addition to their role in promoting structural and functional development of

the GIT, colostrum and milk provide the piglet with an arsenal of specific and non-
specific biologically active proteins and peptides. These factors mediate interaction
between the contents of the intestinal tract and it’s epithelial surface and,
subsequent to transmission across the gut wall, provide initial systemic immune
protection. Comment on the immunological benefits this confers to the piglet is
beyond the scope of this chapter but is addressed elsewhere in this publication.
7.2.3 Perspective 1
The transition from placental to enteral nutrition is immediate and abrupt. For it
to be achieved successfully the neonate requires a competent digestive physiology
within hours of birth. Three major factors ensure success. First, preliminary
morphological adaptation of the tissues necessary for enteral nutrition occurs before
birth. Second, development of enzyme and transport systems is pre-emptively
targeted toward arrival of a known substrate package (colostrum/milk) within a
given timeframe. Third, arrival of the substrate package activates up-regulation of
the system and induces changes that fine-tune digestive physiology to the enteral
diet. In addition, the substrate package has evolved to meet the nutritional
requirement of the neonate completely.
The neonate rapidly and effectively resolves the problems of adaptation to the extra-
uterine diet. However, commercial weaning enforces a second immediate and abrupt
change to piglet diet. What are the consequences of this change, and does the piglet
contend with this second transition as successfully?
7.3 The weaned pig

Natural weaning is a gradual process rather than the single episode we impose on
the piglet commercially. The development of adult digestive physiology initiated
by colostrum intake continues progressively during suckling and is more advanced
when weaning is delayed (Hampson,1986; Miller et al., 1986; Cera et al., 1988;
Kelly et al., 1991). Buddington (1993) suggested that normal progression of
postweaning intestinal maturation was regulated by intrinsic timing mechanisms
but was also dependent upon transition to the adult diet. This agreed with the
122 Weaning the pig

comment by Kelly et al. (1992) that luminal nutrition has a profound influence
on intestinal morphology at all developmental ages but is unlikely to be the ultimate
cue for intestinal differentiation.
7.3.1 Commercial weaning
Intestinal maturation of the commercial piglet, weaned at 3 to 4 weeks of age, is

compromised on two counts. First, the transition from lactation to adult diets is
abrupt rather than progressive. The sudden and vastly different functional
requirement this imposes on the intestine often results in profound reduction in
nutrient intake (Rantzer et al., 1997; Le Dividich and Seve, 2000) and a transitory
(5 d) failure of the piglet to meet its maintenance energy requirement (Pluske et
al., 1997). Second, at commercial weaning age the developmental demands
placed on the intestine by the change in dietary input generally precede the
temporally induced adaptations observed in unweaned piglets by between 2 and
4 weeks. Thus, commercial weaning superimposes our own timetable of events over
the natural maturation of the piglet’s digestive physiology instigating severe
acceleration of the weaning process and launching the developmental program into
a frantic ‘catch-up’ state. To confound this problem further, the piglet simultaneously
elects not to eat and therefore becomes severely energy deficient.
7.3.2 Gastrointestinal, pancreatic and hepatic response
Differential growth of the various compartments of the gastrointestinal tract occurs

following weaning. Makkink et al. (1994) reported a gradual increase in relative
stomach mass (g/kg liveweight) over the 10 days after weaning but a decrease in
that of the small intestine during the first three days that was not recovered until
day 10. Similar small intestinal responses have been demonstrated by other workers
(Cera et al., 1988; Kelly et al., 1991; Jiang et al., 2000) and appear positively related
to feed intake (Makkink et al., 1994). In contrast, the relative mass of the large intestine
increases rapidly during the early post-weaning period (van Beers-Schreurs et al.,
1998), an effect that is independent of age of weaning (Kelly et al., 1991).
The growth rates of organs associated with the GIT also change differentially relative
to overall body mass following weaning. For example, relative liver mass increases
significantly during the second week post-weaning, indicating increased hepatic
metabolic activity (Slade and Miller, 2000).
Following a period of accelerated growth during the perinatal period, pancreatic

weight relative to whole bodyweight stabilises from about 13 doa (Gestin et al.,
1997b). However, following weaning, and independent of age, pancreatic growth
and protein accretion again become positively allometric (Peng et al., 1996). This
second hypertrophic phase of pancreatic development is paralleled by enzyme

Miller and Slade
specific changes in biosynthetic function of the organ. Briefly, the activities of

chymotrypsin and elastase II relative to body weight decline dramatically, lipase
increases slightly and trypsin, amylase and elastase I increase to dominate
pancreatic contribution to the digestive process (Gestin et al., 1997a; Gestin et al.,
1997b). Pancreatic response to weaning is inconsistent. For example, Rantzer et
al. (1997) reported that adult exocrine volume, and protein and trypsin levels, were
achieved within 5 days of weaning pigs at 30 doa. Conversely Cranwell (1995)
reported that pancreatic enzymes were significantly depressed during the first week
after weaning. Biosynthesis of specific enzymes appears to be an adaptive response
to age at weaning (Gestin et al., 1997a), fat and dry matter intake (Gestin et al.,
1997b), and dietary protein content (Zebrowska et al., 1983; Makkink et al., 1994).
The source of protein in the diet also influences expression of pancreatic enzymes.
For example, Makkink et al. (1994) found that pancreatic tissue enzyme activity
was enhanced in pigs fed milk protein as opposed to soya. However, this result
contrasts directly with the earlier findings of Newport and Keal (1982) comparing
response to the same two proteins, but with different diets and methods of analysis.
Further clarification of dietary effects on pancreatic development and enzyme
expression is required.
7.3.3 Small intestine morphological response
The effects of weaning on intestinal morphology are acute. Over the last 30 years
there have been numerous observations of post weaning villus atrophy and crypt
hyperplasia. To summarise, reductions in the ratio of villus height to crypt depth
ratio (V:C) are evident within 24 hours of weaning and are most pronounced by
3 to 5 days (Hampson, 1986; Miller et al., 1986; Cera et al., 1988). Significant
increases in crypt depth may not be observed until 5 days post-weaning (Hampson,
1986) after which time V:C ratio stabilises between 1.5 and 2.0 (Hampson, 1983).
The decline in V:C ratio immediately following weaning is thus primarily the result
of villus shortening, an effect that is less pronounced proximal to distal along the
small intestine.
Figure 7.1 presents plots of least squares mean values for proximal jejunum crypt
depth, villus height and V:C ratio data extracted from seven different trials
reported during a period of 15 years (Hampson, 1986; Miller et al., 1986; Kelly et
al., 1991; Pluske et al., 1991; Makkink et al., 1994; Pluske et al., 1996b; Jiang et al.,
2000). Weaning ages, diets and days post-weaning of sampling are detailed for each
reference in Table 7.2. Analysis of the data used to generate Figure 7.1 indicates
the decline in villus height from d 0 (suckled) becomes significant on d 4 (P<0.05)
at which point villus height is reduced by approximately 50%. Hampson (1986)
reported that such villus atrophy is due to a reduction in enterocyte number rather
than a contraction of the villus structure. Villus height gradually recovers to d 8
and thereafter stabilises at approximately 70% of suckled height.
124 Weaning the pig

1000 7
Villous height to crypt depth ratio

Crypt depth Villous height V:C ratio
800 6
Crypt villous axis 600 5
*
400 ** ** 4
200 3
Villous crypt interface
0 2
- 200 ** * * 1
**
- 400 0
0 2 4 6 8 10 12 14 16 18
Days post weaning
Figure 7.1. Changes in villus and crypt morphology following weaning.
Table 7.2. Sources of data used for analysis of post-weaning gut morphology.
Reference Weaning age Diet type Sampling age
Hampson 1986 21 days Commercial creep feed 21, 22, 23, 24, 25, 26, 29,
32 days
Miller et al. 1986 21 days Soya flour 21, 28 days
35 days Soya flour 35, 42 days
Kelly et al. 1991 14 days Skim milk powder 14, 17, 19, 22 days
Pluske et al.1996a 28 days Whole milk 28, 33 days
Makkink et al. 1994 28 days Skim milk powder 34 days
Pluske et al.1996b 29 days Whole milk 34 days
Jiang et al. 2000 14 days Soyprotein 14, 16, 18, 22, 30 days
Crypt depth varies little to d 6 post-weaning and then rapidly and significantly
increases (P<0.01) to a stable depth in the region of twice the d 0 level. Elongation
of the crypts is initiated by the weaning event and is not influenced by age at weaning
(14, 21, 28 or 35 doa). The enterocyte migration distance (EMD: the distance from
crypt basin to villus apex along which the enterocyte migrates), does not alter with
age and is reduced significantly only on day 5 following weaning (P<0.1). Similar
EMD to that of the data presented here for day 16 is still in evidence 28 days
following weaning (calculated from Salgado et al., 2001). It appears from this data,
that the mechanisms that regulate post-weaning structural change are targeted toward
re-establishment of the suckled EMD.
Pre-weaning EMD is re-established in the weaned pig primarily through elongation

of the crypts. It is generally accepted that this phenomena is indicative of increased

Miller and Slade
crypt cell production of enterocytes and this appears confirmed by concomitant

increases in villus height. In light of the frequent associations made between
enterocyte migration, differentiation and post-weaning functional competence there
are startlingly few studies in which crypt cell proliferation rate (CCPR) has been
measured before and after weaning. Combination of EMD and CCPR data enable
calculation of proportional estimates of enterocyte migration rate:
Suckled (EMD / CCPR %)

Weaned (EMD / CCPR %
For example, substituting the data means of Jiang et al. (2000) into this equation
indicates that enterocyte migration from crypt basin to villus apex was proportionately
1.86, 3.42, 2.60 and 2.13 faster on d 2, 4, 8 and 16 postweaning than on d 0 (suckled).
Villus height, crypt depth and epithelial cell numbers reported by Hampson
(1986a) for creep fed pigs weaned at 21 doa indicate enterocyte size is unaffected
by weaning. Thus, relative to EMD, accelerated migration of cells from crypt basin
to villus apex following weaning would seem likely to result in a reciprocal reduction
in enterocyte lifespan. Reduced functionality of individual enterocytes will occur
only if there is insufficient time for complete differentiation as they migrate up the
villus. There is evidence that this does occur (see section 7.4).
The increase in villus diameter observed in parallel with villus shortening during
suckling (Cera et al., 1988) continues post-weaning and ultimately results in
acquisition of the leaf-shape, thickened development characteristic of the adult
intestine (Cera et al., 1988; Kelly et al., 1992). The maturing crypt-villus structure
is essentially a geometric tube of height EMD and increasing diameter. The negative
effect of post-weaning villus atrophy on enterocyte migration is thus to some degree
compensated for by a temporal program of crypt extension (maintenance of EMD)
and increasing villus diameter. However, restructuring of the villus after weaning
results in a marked loss of the apical surface and is consequently associated with
a reduction in enterocyte maturity and functionality.
Strikingly obvious from the data presented in Figure 7.1 is the inadequacy of V:C
ratio as a satisfactory indicator of the individual dynamics of villus and crypt
restructuring or their additive effects on EMD and enterocyte maturation. We propose
the expression of villus height, crypt depth and crypt basin to villus apex
measurements as a proportion of their absolute values in control animals to be
more worthwhile. This would facilitate rapid and informative comparison of data
between studies.
126 Weaning the pig

7.3.4 Small intestine carbohydrase and transporter response
At birth, nutrient uptake occurs along the entire crypt to villus axis but during the
suckling period this capability gradually becomes concentrated in the apical
enterocytes. Miller et al. (1986) elegantly demonstrated the negative that effect apical
enterocyte loss has on lactase and β-glucosidase activities, and on Na-dependent
uptake of alanine in pigs 5 d post-weaning. In this study, functional capacity of
the post-weaning villi remnant was greatly reduced, indicating immaturity of the
apical enterocytes. In contrast, Kelly et al. (1991) reported significant increases in
maltase and glucoamylase activities (absolute and per unit of protein) in 21-day
old pigs (weaned 14 doa) that were greater than age-related increases observed in
unweaned siblings at 22 d of age. In fact, significant increases in both enzymes
were apparent 3 days following the switch from milk to the gastric-intubated weaner
ration. Rapid carbohydrase induction post-weaning is therefore possible in
response to luminal substrate presence. Interestingly however, in this study,
weaning at 14 doa significantly compromised the chronological increase in total
sucrase activity evident at 22 doa in suckled pigs despite 5% inclusion of sucrose
in the diet of the weaned piglets.
Regional differences in carbohydrase activities (Figure 7.2) and rates of

monosaccharide transport (Figure 7.3) are evident following weaning and
consumption of solid food. During suckling, lactose is the predominant dietary
carbohydrate (CHO), and lactase the most active of the disaccharidases. Unlike
the complex CHO fed post-weaning, lactose is readily hydrolysed in the proximal
small intestine and its component monosaccharides, glucose and galactose,
rapidly taken up by enterocyte aldohexose transporters. In contrast, digestion of
the more complex CHO in weaner diets is protracted, requiring the breakdown of
macromolecules to their component disaccharides before these can be hydrolysed
by brush-border enzymes and absorbed. Consequently, post-weaning intestinal
Activity per unit mucosa
Lactase
Sucrase
Maltase
10% 30% 50% 70% 90%
Figure 7.2. Mucosa normalised proximal to distal disaccharidase activity profiles in

21 day old pigs weaned at 7 days (Adapted from Kelly et al. (1991)).

Miller and Slade
Day 10
(suckled) Proximal Medial Distal
Day 30
(weaned d 21) Proximal Medial Distal
Galactose transport Glucose transport Fructose transport
Figure 7.3. Mucosa normalised proximal to distal monosaccharide absorption profiles

in pigs 10 days post-partum and 9 days after weaning at 21 days (Adapted from Puchal
and Buddington (1992)).
carbohydrase activities extend further along the small intestine (Manners and Stevens,
1972; Kelly et al., 1991), and are supported by appropriate regional distribution
of monosaccharide transporters (Puchal and Buddington, 1992).
7.3.5 Amino acid transport
Developmental aspects of amino acid absorption in the pig appear to have received
little attention to date apart from a recent contribution from Buddington and
colleagues (Buddington et al., 2001). These workers investigated apical amino acid
absorption in intact tissues excised from the small intestine of pigs at developmental
stages ranging from late gestation (11 days prior to birth) through to 42 doa (12
days post-weaning). Sample tissues were collected at proximal, medial and distal
sites along the intestine. Rates of absorption per unit tissue mass (‘rate’) declined
sharply during the first 3 hours post-partum for all 5 free amino acids studied:
aspartate, leucine, lysine, methionine and proline (Asp, Leu, Lys, Met and Pro).
Pro rate then increased significantly to 7 doa. From day 7 to 28 specific rates declined
and thereafter remained stable. Relative to bodyweight, intestinal absorptive
capacity for Leu doubled to 7 doa and then stabilised. Absorption of the other amino
acids studied increased gradually to 28 doa after which uptake increased markedly
for Asp and Met and to a lesser extent for Lys. Absorption rates for Pro and Asp
were significantly and permanently reduced in the distal intestine 24 hours after
birth. No other age-related regional differences in rate or capacity were reported.
Affinity constants and carrier mediated maximum rates of absorption reduced for
128 Weaning the pig

all amino acids except Lys from 28 to 42 doa (12 days post-weaning), and were
paralleled by a universal increase (average 49%) in their apparent rates of
diffusion. Buddington et al. (2001) concluded that as a consequence of rapid
intestinal growth, increasing from 15 g wet mass at birth to 862 g at 42 doa, overall
capacities for amino acid absorption increased faster than did metabolic liveweight.
Weaning therefore does not compromise intestinal capacity for uptake of amino
acids, however, there may be a transient decline in amino acid uptake capability
corresponding with the period of villus shortening immediately after weaning. This
has yet to be investigated.
The majority of amino acids in the weaner diet comprise complex proteins. These
must be broken down enzymatically before amino acid absorption can occur, thus
the simultaneous development of appropriate gastric, pancreatic and mucosal
enzyme systems is necessary. Di- and tri-peptides are also generated during
protein breakdown and many of these can be absorbed directly from the intestinal
lumen. In older pigs peptide absorption can be of equal importance to amino acid
uptake, however, we have been unable to find any literature describing the
development of peptide absorption in the weaned pig.
7.3.6 Perspective 2
The digestive infrastructure necessary for neonatal enteral nutrition is established

during fetal development and includes nascent ability to digest non-milk dietary
components. Commencement of enteral nutrition amplifies the intestinal capacity
to process solid food whilst simultaneously instigating progressive changes in villus
structure. Thus gradual intestinal preparation for post-weaning nutritional input
continues throughout the suckling period. Just as fetal digestive development may
be primed/stimulated by ingestion of amniotic fluids, so the gradual luminal
introduction of novel nutrients in the natural situation generates appropriate changes
in gut growth and functionality. Parallels therefore exist between neonatal and
natural weaning digestive development; however, commercial early weaning
practices introduce fundamental differences between the two processes.
We previously identified three principal factors influencing digestive physiology

and the successful transition from placental to enteral nutrition in the neonate.
How do these factors differ between the neonate and the commercially weaned
pig? First, the neonate has been evolutionally pre-equipped with the digestive
apparatus requisite for the switch in nutrient intake. In contrast, intestinal
development in preparation for the transition from milk to solid diets is far from
complete in the commercially weaned piglet. Second, the neonate is provided with
a highly digestible, high fat, low fibre, tailor-made nutritional package temporally
matched to its stage of digestive development. Despite our best efforts, the weaner
is not. Third, the neonate receives dietary agents that direct appropriate changes

Miller and Slade
in intestinal physiology to fine-tune the digestive and absorptive processes.

Although intestinal adaptation in the commercially weaned piglet is primarily
substrate driven, the components of the weaner diet demand, rather than direct,
digestive development, and result in coarse adjustment rather than fine-tuning of
the digestive apparatus. We have described how these deficiencies are characterised
in the commercially weaned pig by rapid and severe alteration of intestinal form
and function, but how are such responses mediated by the piglet?
7.4 Regulation of post-weaning adaptation

Delayed or natural weaning extends the opportunity for piglet adaptation to the
adult intestinal format thereby reducing, or eliminating entirely, the digestive traumas
associated with transition to the adult diet (Hampson, 1986; Miller et al., 1986;
Kelly et al., 1991). The rapid intestinal modification which occurs in commercially
weaned pigs is therefore a consequence of differences between weaning scenarios,
ie. weaning stress and abrupt substitution of the milk diet with a weaner ration
resulting in a pronounced reduction in feed intake.
7.4.1 Milk withdrawal
It has been argued that the whole weaning process - removal of dam, change of
housing, mixing with other pigs, change of feed type and source etc. - is incredibly
stressful to the piglet. However the importance of milk removal per se and its
replacement by an alternative food cannot be overstated. The digestive physiology
of the suckled pig is focussed on digestion and absorption of milk components
and, in consequence, is transiently compromised by the sudden substitution of a
more complex diet at weaning. Nutritionally, milk is a source of protein, fat and
carbohydrate that can be further described in terms of essential amino acids,
carbohydrate moieties and different chain-length fatty acids. However, concealed
within this nutritional profile are a vast array of physiological, immunological,
biochemical and bacteriological mediators of gut health, efficiency and growth (Fox
and Flynn, 1993). Removal from the sow thus simultaneously deprives the piglet
of a readily digestible food source and potent regulators of intestinal structure and
function. The importance of milk is demonstrated by studies in which weaning
onto milk diets prevented the typical post-weaning change in crypt and villus
architecture (Pluske et al., 1996a and b).
An increasing awareness of the primary (non-nutritional) functions of lactation

products and their capacities to regulate intestinal health and adaptation is
apparent from the literature (see Xu et al., 2000). At least 16 distinct growth factors
have been detected in mammary secretions (Fox and Flynn, 1993). In addition, a
number of bioactive peptides are released by the hydrolysis of casein and whey
proteins (Meisel et al., 1989, Maubois and Lenoil, 1989: cited by Fox and Flynn,
130 Weaning the pig

1993). Intestinal receptors and modes of action have yet to be characterised for
many of these substances. In addition, the majority of studies in swine have
concentrated on neonatal response to factors in colostrum; considerably less
information is available regarding the effects of factors in milk on pig digestive
physiology (see Pluske et al., 1997). The consequences of individual bioactive milk
component withdrawal on intestinal stability are not well understood, and require
comprehensive investigation in order to further our comprehension of weaning
associated events.
7.4.2 Weaning stress
We have considered the physical and functional consequences of commercial early

weaning on piglet digestive physiology. However, separation from the sow,
handling, mixing and adaptation to new behavioural and nutritional situations
subjects the piglet to considerable physiological stress. Weaning is therefore
associated with significant increases in plasma cortisol concentration (Carroll et
al., 1998; Wu et al., 2000). Intestinal sensitivity to cortisol is generally thought to
be lost by the time of natural weaning, however, commercial early weaning practices
may well precede development of cortisol insensitivity.
A recent review of factors influencing small intestinal structure and function in the
weaned pig (Pluske et al., 1997), exposed the lack of evidence linking cortisol levels
at weaning with the subsequent growth check and intestinal ‘maladaptation’.
However, there is considerable support in the literature for a more benevolent role
of cortisol in intestinal adaptation. For example, pre-term pigs (82 - 96 days of
gestation) administered cortisol in utero exhibited significantly increased lactase,
maltase and aminopeptidase A and N activities six days later (Sangild et al., 1995).
Similar benefits on carbohydrase activities have been reported in suckled pigs at
26 doa (Chappel et al., 1989: cited by Flynn and Wu, 1997). Furthermore, intra-
muscular injection of glucocorticoid given to weaned pigs infected with transmissible
gastroenteritis virus prevented villus atrophy and increased electrolyte retention
through improved glucose-facilitated Na absorption (Rhoads et al., 1988).
More relevant to weaning physiology is the role of endogenous cortisol in

regulation of mucosal amino acid metabolism. Post-weaning redevelopment of
intestinal structure and function involves considerable increase in mucosal protein
synthesis with consequent high enterocyte demand for amino acids, both as energy
substrates (e.g. glutamine, glutamate, aspartate) and as building blocks for protein
synthesis (e.g. arginine). In theory, cells of the intestinal mucosal can obtain these
substrates from either the intestinal lumen or the mesenteric arterial circulation.
However in practice, with the notable exception of glutamine, uptake of circulatory
substrates/precursors is negligible. This is apparent from the mucosal atrophy which
occurs with total parenteral nutrition (TPN) (eg. Remillard et al., 1998a; Bertolo

Miller and Slade
et al., 2000). Enterocyte metabolism of dietary amino acids is always necessary for
intestinal homeostasis but becomes critical during post-weaning maturation of the
small intestine. Increased circulating cortisol concentrations appear to facilitate
appropriate amino acid metabolism by the small intestine post weaning. For
example, Flynn and Wu (1997) reported that blocking glucocorticoid receptors
abolished weaning-enhanced enterocyte production of ornithine, citrulline and CO2
from glutamine, and proline and CO2 from arginine. Similarly, Wu et al. (2000)
reported that enterocyte synthesis of citrulline from glutamine in pigs 8 days after
weaning was 10-fold greater than in unweaned contemporaries. Inhibition of adrenal
cortisol production during the immediate post-weaning period completely
eliminated this increase. In both studies the authors offered evidence of cortisol
involvement in the enhanced expression or activity of enterocyte enzymes
catalysing specific stages of glutamine and arginine metabolism. Therefore it appears
that cortisol release in response to the stress of weaning actually enhances the piglet’s
ability to react appropriately, at least in terms of its digestive physiology.
7.4.3 Direct dietary effects
The punitive effects of low feed intake on gut morphology are well documented
(Goldstein et al., 1985; Remillard et al., 1998a; Remillard et al., 1998b; Lopez-Pedrosa
et al., 1999). However, the weaned piglet undergoes a relatively short period of
sub-maintenance feed intake, with maintenance energy intake re-established
within 5 days of weaning (Le Dividich and Herpin, 1994, cited by Pluske et al.,
1997). In the interim, the significant mobilisation of lipid reserves post-weaning
(Whittemore et al., 1978) is likely to fund deficits in energy intake. Transient
depression in energy intake would therefore seem unlikely to reduce whole body
energy availability. However, we have already noted that the contribution of
circulatory energy substrates to metabolism and structural maintenance of the
mucosa is negligible, thus enteral nutrition would seem pivotal to gut maintenance.
Pluske et al. (1996b) clearly demonstrated that in piglets fed cows’ milk after
weaning, energy intake strongly influenced villus height. Similar effects of energy
intake on gut morphology were reported by van Beers-Schreurs et al. (1998).
Interestingly, data from Pluske et al. (1996b) also indicated that, independent of
dry matter and energy intake, mean villus height was maintained and crypt depths
less increased when pigs were weaned onto cows’ milk rather than a starter ration.
This response might reflect physical differences in the form of the diet or,
alternatively, the complementary effects of milk nutritional composition and
availability on enterocyte metabolism and hence intestinal homeostasis.
It is apparent from consideration of enterocyte metabolism that the amino acid

profile of the weaning diet is a key factor in the success of rapid post-weaning
intestinal development. However, as a consequence of mucosal metabolism, the
pattern of amino acids available for peripheral tissue metabolism will differ markedly
132 Weaning the pig

from that provided in the diet (Stoll et al., 1998). This effect is comprehensively
detailed for glutamate (eg Windmueller and Spaeth, 1980; Reeds et al., 1996; Reeds
et al., 2000), but with a few notable exceptions (Yu et al., 1990; Stoll et al., 1998;
Wu, 1998) is less well characterised for the essential amino acids (EAA). This
questions the ability of weaner diets to adequately support the nutritional
requirements for intestinal development or, following mucosal metabolism, to
effectively promote whole animal growth. The extent of EAA intestinal catabolism
is of obvious importance to both perspectives and as such requires further
elucidation.
Physical qualities of the post-weaning diet may contribute to villus atrophy. Pelleting
(see Pluske et al., 1997) and increased fibre content of the diet (Tasman-Jones et
al., 1982) may lead to mechanical erosion of apical enterocytes during digesta flow
along the small intestine. There is little direct evidence in the literature to support
this theory, indeed scanning electron microscopy failed to detect villus damage in
intestinal sections prepared from pigs fed pelleted cereal diets (Hampson, 1986).
However, villus atrophy to day 5 post-weaning followed by emergence of the more
compact, lower profile, leaf-shaped villus configuration may indicate an abrasion-
induced response. Similarly, the changes in digesta mucin noted after weaning
(Pestova et al., 2000) may be in response to the increased abrasive qualities of digesta.
Studies in our laboratory indicate goblet cell numbers per villi reduced post-weaning
(d 5) but increased per unit of villus height (unpublished data). Thus the capacity
for epithelial protection by mucin secretion increases after weaning.
Miller et al. (1986) speculated that the post-weaning changes in enterocyte

carbohydrase expression could not be completely reconciled with aetiological
theories implicating changes in diet, hormone levels and CCPR. These authors
hypothesised that enterocyte ontogenic development might instead be influenced
by interactions with the immune system following epithelial exposure to food
antigens. Hypersensitive responses to dietary antigens and their immunological
implications have been discussed extensively in the literature (see for example Miller
et al., 1991; Newby et al., 1994; Dreau and Lalles, 1999) and lie beyond the scope
of this chapter. However, in view of the implicit connection between immune-
mediated intestinal hypersensitivity and modification of weaned pig digestive
physiology, brief comment is justified.
Hypersensitivity (Types I and IV) requires previous exposure or ‘sensitisation’ of

the immune system to the antigen. Induction of hypersensitivity depends on the
extent of initial antigenic exposure. Very low or high exposure promotes ‘oral
tolerance’ of the antigen, whereas an intermediate antigen dose sensitises (primes)
the immune system. The dilemma is that division between priming and tolerising
antigen doses is not readily quantifiable. Furthermore, sensitisation varies
depending on individual antigenic, environmental and genetic determinants.

Miller and Slade
Sensitisation results in the production of antigen specific IgE and B memory cells
(Type I) or T memory cells (Type IV) that, on subsequent exposure to the antigen,
elicit particular immune responses. Simply, Type I responses (termed ‘immediate’)
are mediated primarily by antigen specific IgE attached to mast cell surface receptors;
cross-linking of IgE by the antigen results in rapid degranulation of mast cells. Type
IV responses (termed ‘delayed’) involve T cell activation and macrophage recruitment
to the site of antigen presence, mast cell degranulation and cytokine release. Both
responses elicit acute inflammatory effects and damage to antigen-associated tissues,
in this case the gut epithelium. Thereafter their Type I and IV responses are
suppressed by T helper 1 cells (Th1), and keratinocyte and macrophage-produced
prostaglandin E (PGE) respectively.
What is clear is that piglets weaned at between 21 and 28 doa which have had access
to creep feed during the nursing period are unlikely to have consumed the correct
antigen dose to elicit immune tolerance on subsequent exposure (Newby et al.,
1994). In humans Type I and IV responses peak approximately 12 and 72 hours
following re-exposure to the antigen (Roitt et al., 1998). Therefore it is likely that
in piglets, diet-induced immunological enteropathy contributes to the adverse
changes in villus architecture observed in the first 5 days post-weaning. In the
commercial situation the piglet’s first significant exposure to dietary antigens often
occurs at weaning. However, unless access to the sow’s diet is prevented, exposure
to sensitising doses of antigenic material may occur during the nursing period. In
a recent study, McCracken et al. (1999) determined jejunal expression of
proinflammatory immune system components in villus and crypt tissue of pigs
weaned onto milk or soy-based diets. These authors reported significant reductions
in villus height from 2 days post-weaning that were paralleled by marked increases
in villus CD4+ T cell numbers and preceded by significant depression in MHC class
I RNA expression. However, these effects were similar in both treatment groups.
Likewise, crypt and villus CD8+ T cell numbers and MHC class II determinations
were unaffected by dietary protein source whilst PGE concentrations, maximal at
48 hours plus in Type IV scenarios, were highest on day 1 for both treatments.
McCracken et al. (1999) reasoned that the temporal pattern of immune events
elicited in this experiment did not completely satisfy the hypersensitivity hypothesis.
Feed intake of piglets over the 2 days following weaning was typically low, less than
100 g per pig in total. This prompted the authors to suggest that weaning anorexia
itself might compromise epithelial integrity, thus initiating inflammatory response
through direct interaction of the antigen with the lamina propria.
7.4.4 Indirect dietary effects
Inadequate nutrient intake is a consistent feature of piglet response to weaning

and has clear effects on gut morphology. The expression or secretion of a variety
of somatotropic hormones is also strongly influenced by nutritional status
134 Weaning the pig

(Buonomo and Baile, 1991) and therefore is significantly altered at weaning (Carroll
et al., 1998; Le Dividich and Seve, 2000). Insulin-like growth factor I (IGF-I) and
growth hormone (GH) have been implicated in intestinotrophic events (see Burrin,
1997; Baksheev and Fuller, 2000), and are affected by nutrient intake. In fact, White
et al. (1991) reported similar significant reductions in circulating IGF-I in pigs that
were weaned to those that were fasted for 36 hours! However, it is the nutrient
responsive gut peptides that appear most strongly influenced by, and regulatory
of, weaning digestive events. The effects of several of these peptides on
gastrointestinal motility, adaptation and growth are summarised in Table 7.3. The
list of enteroendocrine factors already identified is extensive, and our understanding
of their actions and interactions is far from definitive. Changes in the endocrine
and metabolic status of the pig at weaning are discussed elsewhere in this book.
Comment here will therefore be restricted to a brief consideration of weaning-elicited
gut hormone secretion. Using the example of the proglucagon derived peptides
(PGDPs), particularly glucagon-like peptide 1 and 2 (GLP-1 and GLP-2), we will
discuss the enteroendocrine regulation of post-weaning digestive development.
Nutrient responsive secretion of gut peptides is suppressed by a reduction in feed

intake (van Goudoever et al., 2001) and may also be influenced by diet composition
(eg. fibre, complex carbohydrates, short-chain fatty acids: Burrin et al., 2001).
Endocrine response to re-feeding is equally pronounced. Van Goudoever et al. (2001)
reported that piglet arterial concentrations of glucose dependent insulinotropic
polypeptide (GIP) and GLP-2 increased 4 to 8-fold within 1 hour of feeding after
a fast of 13 hours.
GLP-2 is a member of a group of 5 peptides derived from post-translational

processing of intestinal proglucagon in the L cells of the colon and distal small
intestine. The other members of the group are GLP-1, glicentin, glicentin-related
pancreatic peptide (GRPP) and oxyntomodulin. Direct contact with luminal
nutrients stimulates L cell secretion of these peptides into the villus capillary system.
Glicentin promotes intestinal cell growth in vitro but immunoneutralisation
demonstrated that it has little effect on bowel growth in vivo (Bloom and Polak,
1982: cited by Drucker, 1997). Oxyntomodulin has no detectable intestinotrophic
effect but does stimulate intestinal glucose uptake, particularly in the ileum (Collie
et al., 1997). Nutrient intake also stimulates secretion of GIP from duodenal K cells.
Both GIP and GLP-1 function as incretin hormones, ie. their secretion in response
to nutrient intake stimulates insulin secretion that is disproportionately larger than
would otherwise be elicited by ingested nutrients. As such, both hormones play a
major role in extra-intestinal metabolism and growth. GIP stimulation of GLP
secretion in vivo was first demonstrated in rats by Roberge and Brubaker (1993)
for GLP-1 and has since been implicated in GLP-2 expression in pigs (van
Goudoever et al., 2001).

Miller and Slade
Table 7.3. Nutrient responsive enteroendocrine mediators of intestinal response to

weaning.
Peptide Site of secretion ‘Ileal brake’ Enterotropic References
EGF 1 Submandibular glands Yes Yes Peng et al. 1996

Brunner’s glands Cuber 1997
Paneth cells Drucker 1997
Baksheev and Fuller 2000
GIP 2 K cells Yes Insulinotropic Roberge and Brubaker 1993

Knapper et al. 1995
van Goudoever et al. 2001
GLP-1 3 L cells Yes Insulinotropic Roberge and Brubaker 1993

Knapper et al. 1995
Hansen et al. 1999
Holst 2000
GLP-2 4 L cells Yes Yes Drucker 1997

Drucker et al. 1997
Holst 2000
PYY 5 L cells Yes Yes Drucker 1997

CCK 6 I cells Yes Pancreatropic Cuber 1997
NT 7 N cells Yes Drucker 1997
1Epidermal growth factor

2Glucose dependent insulinotropic polypeptide
3Glucagon-like peptide 1
4Glucagon-like peptide 2
5Peptide YY
6Cholecystokinin
7Neurotensin
GLP-1 is one of the gut peptides involved in the ‘ileal brake’ phenomenon (Read
et al., 1994). This is the mechanism by which ileal presence of unabsorbed nutrients
inhibits upper gastrointestinal activity. Thus nutrient responsive GLP-1 release
136 Weaning the pig

inhibits gastric acid secretion and stomach emptying, depresses pancreatic exocrine
activity and reduces intestinal motility. Deactivation of GLP-1 is extraordinarily rapid.
Hansen et al. (1999) reported that 50 to 75% of GLP-1 is metabolised to an inactive
form before leaving the villus capillaries. More recently, one of the co-authors of
this study reasoned that GLP-1 intestinal effects might be mediated through
interaction with sensory afferent neurones terminating in the lamina propria (see
Holst, 2000). In summary, in response to unabsorbed lipid and carbohydrate in
the distal ileum and colon, GLP-1 prolongs nutrient exposure to upper GIT digestive
and absorptive processes. It is clearly possible that the nutrient complexity of post-
weaning diets in combination with reduced villus functionality might result in
physiological malabsorption with resulting GLP-1 secretion. This in turn would
down-regulate intestinal dynamics and consequently reduce feed intake. Intravenous
infusion of GLP-1 has been shown to depress appetite and food intake in man
(Flint et al., 1998; cited by Holst, 2000).
GLP-2 secretion parallels that of GLP-1 in that both are stimulated by direct exposure
of the L cell to intraluminal nutrients. Although to a lesser extent, gastrointestinal
motility is also inhibited by GLP-2, however the primary action of this peptide
appears to be stimulation of intestinal growth. Infusion of GLP-2 has been shown
to increase intestinal tissue mass, mucosal thickness, villus height and crypt depth
and has also been reported to increase hydrolase expression and hexose and amino
acid transport in several species (see reviews by Baksheev and Fuller, 2000;
Drucker, 1997; Holst, 2000; Burrin et al., 2001). In addition, in pigs receiving total
parenteral nutrition, GLP-2 infusion maintained intestinal growth by suppressing
proteolysis and apoptosis (Burrin et al., 2000). These responses were generated
following administration of supraphysiological levels of GLP-2. However, Fischer
et al. (1997) reported that an increase of approximately 50% in endogenous GLP-
2 secretion was sufficient to promote significant intestinal growth and villus and
crypt extension in rats. Arterial concentration of GLP-2 increased 4-fold in weaning
age pigs following re-alimentation after a 13 hour fast (van Goudoever et al., 2001).
The voluntary feed intake of the just-weaned pig is typically very low (see for example
Bark et al., 1986), and the duration of ‘non-eating’ invariably in excess of 24 hours.
We are unaware of any investigations in which the effects of weaning on GLP-2
concentrations in pigs have been reported. However, it would appear from the studies
presented here that a GLP-2 surge following significant ingestion of the weaning
diet is likely and, if so, would undoubtedly contribute to intestinal adaptation.
The combined action of GLPs thus presents a coherent response to villus atrophy
and subsequent physiological malabsorption that is supported by the actions of
other gut hormones, the mechanism effectively retarding nutrient transit whilst
adaptive growth of the intestine is instigated. Outwardly such events would be
characterised by a feed intake plateau or reduction as observed in our own studies
(Figure 7.4) and those of other workers (see for example Bark et al., 1986;

Miller and Slade
1000
Feed intake (g/pig/day) 800
600
400
200
0
0 2 4 6 8 10 12 14 16 18 20
Day post-weaning
Figure 7.4. Post-weaning feed intake of piglets weaned at 26 days of age and offered
diets containing skim milk.
McCracken, 1989). Inwardly, reduced nutrient intake would be paralleled by an

increase in intestinotrophic events as demonstrated in Figure 7.1.
7.4.5 Perspective 3
The changes in digestive physiology after weaning can be separated into 2 phases:
the decline of infant intestinal structure and function (phase I) and the development
of mature intestinal parameters (phase II). The transition from one phase to the
other is initiated by enteral nutrition and is subject to inherent developmental drives.
Ingestion of colostrum and subsequently milk stimulates elemental changes in gut
morphology and growth that are paralleled by reshuffling of intestinal secretory
and absorptive capacities. In the natural situation the developmental phases merge
seamlessly: the piglet continues to receive nutritional and immunological support
from the sow whilst luminal exposure to new dietary components increases;
improved intestinal capacity to process non-milk products is both developmentally
and adaptively generated; and tolerance of novel nutrients is mediated by lactation
components. The process continues until between 9 and 12 weeks after birth when
the milk component of the diet diminishes to nothing and the pig is weaned.
Commercial weaning effectively condenses the latter two thirds of the natural
weaning process into a period of days rather than weeks. As a consequence the
development phases become quite distinct. Phase I culminates 3 to 5 days
following weaning and is characterised by marked reductions in villus surface area,
enterocyte population, enterocyte maturity and secretory and absorptive function.
Initiation of phase II precedes or coincides with conclusion of phase I.
Developmental progression of intestinal maturation evident pre-weaning is
dominated and overtaken by adaptive responses to nutrient luminal presence. Crypt
cell proliferation is induced and villus height partially restored with consequent
138 Weaning the pig

re-establishment of the crypt-villus axis dimension. Intense growth of the digestive

tract maintains or increases total digestive and absorptive function whilst gastric
motility is transiently reduced and exposure of ingested nutrients to digestive
secretions increased. Pancreatic and intestinal hydrolase activities adapt responsively
to dietary input and are complemented by regionalised increases in nutrient
transporter capacities. Ultimately, equilibrium between cell production and cell
loss is achieved, enzyme expression and activities are optimised to diet intake and
composition, and nutrients are absorbed with maximum efficiency. The digestive
physiology of the weaned pig is thus established.
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144 Weaning the pig

8 Diet-mediated modulation of small
intestinal integrity in weaned piglets
M.A.M. Vente-Spreeuwenberg and A.C. Beynen
Summary
Piglets are faced with multiple changes around the weaning transition. This generally
results in low voluntary feed intake, sub-optimal growth rate and diarrhoea may
occur frequently. The small intestine not only digests and absorbs nutrients, but
also excludes pathogens, toxins and allergic compounds. Small intestinal function
depends on its integrity, which can be assessed on the basis of indicators such as
villous length, crypt depth, number of goblet cells, transepithelial permeability,
brush border enzyme activity and growth performance. Weaning of piglets
negatively affects small intestinal integrity as indicated by a decrease in villous length,
an increase in paracellular permeability and a decrease in total brush border enzyme
activities. This review focuses on dietary modulation of the weaning-induced
impairment of small intestinal integrity. It is concluded that the level of feed intake
is the most important determinant of mucosal function and integrity. Thus, the
temporal low feed intake immediately after weaning is the main cause of the decrease
in small intestinal integrity. Furthermore, the actual amount of feed consumed is
positively correlated with the development of the small intestine. Studies reviewed
are those dealing with potential functional feed ingredients, including protein source,
specific amino acids, fatty acids, fibres, non-digestible oligosaccharides, growth
factors, polyamines and nucleotides. It is concluded that the individual feed
constituents have only marginal effects on small intestinal integrity of the weaned
pig. Possibly, combinations of functional feed ingredients will be more successful.
Further research should involve identification of determinants of feed intake
immediately after weaning and functional feed ingredients to stimulate epithelial
cell proliferation and differentiation, enhance immune function and promote growth
of beneficial bacteria.
8.1 Introduction
At weaning, piglets are faced with changes of various nature. Under commercial
conditions, weaning at 24-28 days of age usually involves complex social changes
for the piglets, including their separation from the mother, separation from litter-
mates and exposure to unfamiliar counterparts (Fraser et al., 1998). The composition
of the piglets’ diet changes drastically at weaning; the liquid milk from the sow is
replaced by pelleted dry feed with starch instead of fat as the main energy source.
The transition from suckling to eating solid food is associated with a critical period
of underfeeding during which the pig is adapting itself to the dry food (Le Dividich

Vente-Spreeuwenberg and Beynen
and Herpin, 1994). The low feed intake during the first two days after weaning,
which essentially is independent of diet composition (McCracken et al., 1995),
causes growth stasis (Leibrandt et al.,1975; McCracken et al., 1995; 1999).
Diarrhoea frequently occurs after the weaning transition (Nabuurs, 1991). The
gastrointestinal tract not only allows for the digestion and absorption of nutrients,
but also acts as a barrier for bacteria, toxins and allergic compounds that otherwise
may reach the systemic organs and tissues. For the small intestine, the level of feed
intake is a critical determinant of its digestive and absorptive capacity (Pekas, 1991)
and also of its barrier function (Bishop et al., 1992). The low feed intake caused
by weaning often leads to maldigestion and malabsorption and also to reduced
small intestinal barrier function. When feed intake increases, diarrhoea may occur.
Enterotoxemic bacteria proliferate and release their toxins. An integrated concept
of the response to weaning is given in Figure 8.1.
The problems associated with weaning are mainly a consequence of the commercial
conditions. Weaning of piglets at an age as young as possible increases the number
of piglets per sow per year. Under natural conditions, piglets gradually develop the
capability to digest solid food and voluntary reduce their intake of milk. Thus, the
piglets themselves control the weaning process. Some nursing may still continue
until the piglets are 12-16 weeks of age, this being considered the natural age of
weaning (Jensen and Recén, 1989; Fraser et al., 1998).
Based on general knowledge of the influence of nutrition on gut function and health,
diets may be formulated that alleviate or prevent the adverse effects of weaning at
4 weeks of age. The objective of this chapter is to highlight the nutritional
Pathogenesis of the post-weaning syndrome
Social and diet changes
Low feed intake
Lack of enteral nutrition
Impairment of mucosal function
Uptake of antigens, toxins Maldigestion,

and translocation of bacteria Malabsorption
Inflammation Poor performance

Diarrhoea
Infections
Figure 8.1. An integrated concept of the effect of weaning on mucosal barrier

function, performance and health in piglets.
146 Weaning the pig

Diet-mediated modulation of small intestinal integrity in weaned piglets
opportunities to modulate the intestinal barrier function after weaning, thus resulting
in increased piglet performance. It is beyond the scope of this chapter to review
the effect of hormones on small intestinal integrity. Prior to describing the effects
of diet composition, the indicators of small intestinal integrity will be discussed
briefly.
8.2 Small intestinal integrity

One important function of the gastrointestinal tract is to transform ingested food
so that absorbable nutrients become available for the body. Morphologically, the
small intestine represents a maximum absorptive surface. The presence of
Kerckring’s folds, villi and microvilli in the small intestine produces a large surface
area compared with that of a cylindrical tube (Junqueira and Cerneiro, 1980;
Caspary, 1987, 1992; Dyce et al., 1987). The small intestinal villi of healthy piglets
are predominantly finger-shaped with few tongue-shaped villi (Mouwen, 1972).
A 10-day old, 3-kg piglet has a relatively small intestine with a total absorptive surface
area of 114 m2 (Buddle and Bolton, 1992). The epithelial cells lining of the
gastrointestinal tract renew rapidly. The small intestinal villus epithelium in 1-day-
old pigs is replaced in 7-10 days, whereas this process in 3-week-old pigs takes 2-
4 days (Moon, 1971). The epithelial cells have apical 0.5-2 µm intercellular
attachment zones or junctional complexes, which join them together. These tight
junctions regulate epithelial permeability by influencing para-cellular flow of fluid
and constituents. In general, the complexity, strand number and depth of the tight
junction correlate inversely with the permeability of epithelia (Trier and Madara,
1981).
The gastrointestinal tract provides an extensive surface area with intimate contact
between the host organism and dietary substances, microorganisms, parasites and
exogenous toxins. The intestine permits the uptake of dietary substances into the
systemic circulation, but at the same time excludes pathogenic compounds
(Gaskins, 1997). The gastrointestinal tract has multiple non-specific and
immunological defence mechanisms. The non-specific defence includes gastric acid
production, peristaltis, mucus layer, tight junctions, epithelial desquamation,
proteolysis, resistance against colonisation of pathogenic bacteria and the gut-liver
axis. The immunological defence of the small intestine includes the production
of secretory immunoglobulins, M-cells and lymphocytes (Madara et al. 1990; Walker
and Owen, 1990; Deitch, 1993; Wang, 1995). Components of the intestinal barrier
are shown in Figure 8.2.
Concurrent absorption of nutrients and exclusion of pathogenic compounds is

achieved through concerted actions of the small intestine. For example, tight
junctions are crucial for baseline intestinal barrier function, but regulation adapts
them to the uptake of nutrients (Madara, 1989). That the small intestine has two

Epithelial barrier function

Luminal transcellular paracellular
factors
Phospholipid layer
Epithelial Mucus layer
factors Tight junction
M-cell
Enterocyte
Goblet cell
Macrophage
Mast cell
Lymphocyte
Submucosal
factors Leukocyte
Capillary Lymph tube
Lymph node
Reticuloendothelial
system Spleen
Liver
Other organs
Figure 8.2. Schematic presentation of the gastrointestinal defence barrier and effector
factors (After Wang, 1995).
functions is reflected in the difficulty to interpretate numerical values as to small

intestinal integrity. Commonly used indicators of small intestinal integrity are villus
length, crypt depth, number of goblet cells, mucus production, transepithelial
permeability, inflammation, brush border enzyme activity and animal performance.
These indicators and their relation to the process of weaning are discussed briefly
below.
8.2.1 Small intestinal morphology
The depth and shape of the crypts of Lieberkühn, the shape and height of the villi
and the number of goblet cells are indicators of intestinal integrity. The villus
orientation and shape has been classified by Mouwen (1972), with classes
including tongue-shaped, finger shaped, leaf-shaped, ridged-shaped and convoluted
villi. Small intestinal integrity is most commonly assessed by histologic
measurements of villus height and crypt dept. Weaning causes a reduction in villus
height and an increase in crypt depth (Hampson, 1986; Miller et al., 1986; Cera
et al., 1988; Dunsfort et al., 1989; Hall and Byrne, 1989; Kelly et al., 1991a; Nabuurs
et al., 1993; Pluske et al., 1996a; 1996b). Villous atrophy after weaning is caused
by a combination of increased rate of cell loss and reduced rate of cell renewal
(Pluske et al., 1997a). The histological changes are smaller with higher post-weaning
feed intakes (Kelly et al., 1991b; McCracken et al., 1995; Van Beers-Schreurs, 1996;
148 Weaning the pig

Pluske 1996b). Ideally, specific diet formulations for weanling piglets should
ameliorate the weaning-induced decrease in villus height.
8.2.2 Mucus production
The mucus protects the mucosa against digestive secretions, pathogens and
physico-chemical damage (Mantle and Allen, 1989; Stokes and Bourne, 1989;
Forstner and Forstner, 1994). Binding of pathogens to mucins rather than to
epithelial cells is generally regarded as an important host defence mechanism
(Forstner and Forstner, 1994). Mucus gel is stored in the intestinal goblet cells and
secreted by baseline or accelerated secretion (Lamont, 1992). Baseline secretion
is continuous and provides renewal of the mucus coat that is lost due to erosion,
digestion and luminal digesta flow. Accelerated secretion is characterised by rapid,
massive goblet discharge in response to physiological or pathological stimuli
(Lamont, 1992, Epple et al., 1997), including inflammatory mediators (Specian
and Neutra, 1982; Cohen et al., 1991; Plaisancié et al., 1998) and bacterial toxins
(Roomi et al., 1984; Cohen et al., 1991, Epple et al., 1997). The actual amount of
mucus secreted cannot be measured. An increase in the number of goblet cells might
point to increased mucus production. Weaning of piglets has been shown to result
in either unchanged (Dunsford et al., 1991; McCracken et al., 1999) or decreased
(McCracken et al., 1995) numbers of goblet cells in the villi, and unchanged
(McCracken et al., 1995; Spreeuwenberg et al. 2001) or decreased (Dunsford et al.,
1991) numbers of goblet cells in the crypts. The importance of the number of goblet
cells as an indicator of intestinal integrity seems limited due to the inconsistent
response to weaning.
8.2.3 Transepithelial permeability
Small intestinal integrity can be estimated on the basis of intestinal permeability

for macromolecules, which can be measured as passive diffusion of a marker
compound. Ideal markers cross the intestinal epithelium by non-mediated
diffusion, are recovered quantitatively after oral administration, and can be
reliably measured in blood or urine by a convenient technique (Uil et al., 1997).
Various probe molecules have been used to measure intestinal permeability,
including the sugars lactulose and mannitol (Uil et al., 1997), horseradish
peroxidase, ova-albumin and chromium-labeled ethylene diamine tetra-acetate (51Cr-
EDTA) (Vellenga, 1989; Bjarnason et al., 1995). Transepithelial transport can also
be measured with the use of Ussing chambers. An intestinal biopsy is placed in
an Ussing chamber separating the mucosal and serosal site of the tissue. The marker
is added at the mucosal site. At given time points the serosal fluid is sampled to
measure the amount of marker that has crossed the epithelium. The trans-
epithelial electrical resistance (TEER) and short circuit current (Isc) may also be
measured. The TEER has been suggested to reflect tight junction function (Wirén

et al., 1999), whereas the Isc reflects ion pump activity (Wirén et al., 1999). With
increased paracellular transport of markers it is anticipated that mucosal integrity
is diminished and that pathogens and toxins may cross the epithelial barrier.
Weaning results in increased paracellular transport for mannitol in transport
chambers (Verdonk et al., 2001). Plasma xylose concentration after oral
administration was similar in weaned and unweaned piglets (Pluske et al., 1996b).
Thus, the formulation of diets for weanling piglets may aim at reducing the
paracellular transport of an appropriate marker in an intestinal biopsy placed in
a transport chamber.
8.2.4 Inflammation
If and when bacteria or other deleterious agents cross the first line of defence and
reach the connective tissue of the lamina propria, their metabolites or mediators
liberated from epithelial cells may evoke an inflammatory response (Gaskins, 1997).
The different T-cell subsets or major histocompatibility complex (MHC) classes
indicate the status of small intestinal immunity. Class I MHC molecules interact
with CD8-positive T cells which usually have a cytotoxic function. Class II MHC
molecules interact with CD4-positive T cells which provide help to the antigenic
peptide recognition (Shanahan, 1994). The measurement of pro-inflammatory
cytokines provides information as to local inflammation. The production of
interleukin-1 (Il-1), Il-6 and tumor necrosis factor (TNF) occurs rapidly following
infection, tissue injury and trauma. The cytokines activate receptors on different
target cells, leading to a wide range of effects, including anorexia, fever and acute
phase protein production (Gruys et al., 1999), and also inhibition of growth
(Johnson, 1997). Weaning results in an inflammatory response as measured by
an increased production of Il-1 at day 1 and 2 post weaning (McCracken et al.,
1995). However, the production of TNF is unchanged when compared to the
production rates at the day of weaning (McCracken et al., 1995). With an average
digestible energy intake of 1575 kJ during the first four days after weaning, the ratio
of CD4 to CD8 positive T cell subsets decreased compared to the ratio at the day
of weaning, which might point to an inflammatory response (Spreeuwenberg et
al., 2001). Thus, the formulation of diets for weanling piglets may aim at reducing
inflammation. Interleukins are indicators, which measure an inflammatory
response directly. Decreased ratios of CD4 to CD8 positive T cells or MHC II to
MHC I classes are indirect indicators of an inflammatory response.
8.2.5 Brush border enzyme activity
The enzyme activity of the brush border and pancreas may also serve as indicators
of small intestinal function. The maturing enterocytes embedded in the apical
membrane of the small intestine synthesise enzymes to hydrolyse disaccharides
and small peptides (Caspary, 1992). Enzyme production of enterocytes during the
150 Weaning the pig

weaning transition of piglets is determined by villus height and maturity of the

enterocytes (Smith et al., 1985; Miller et al., 1986). In general, the brush border
enzyme activity increases markedly when going from the bottom of the crypt to
the tip of the villus (Miller et al., 1986; Fan et al., 2001). The increased enzyme
activity at the villus tip is consistent with enterocyte differentiation (Fan et al., 2001).
Enzyme activity may be expressed in units produced per time interval (total enzyme
activity), in units per gram of brush border membrane protein (specific activity)
or units per cm of small intestine. Weaned piglets have low specific activity of sucrase,
lactase (Hampson, 1986; Miller et al., 1986; Kelly et al., 1991a) and isomaltase (Miller
et al., 1986) when compared to unweaned piglets of the same age. The effect of
weaning on disaccharidase activity is less pronounced when the pigs are weaned
at an older age (Miller et al., 1986). Activities of maltase II and maltase III increase
in response to weaning at six weeks of age when compared to unweaned piglets
of the same age, but show no change in four-week-old pigs (Miller et al., 1986).
Pluske and colleagues (1997b) showed that maltase and glucoamylase activities
increased with age (2 versus 4 weeks of age) and with day postweaning. Kelly and
co-workers (1991a) reported increases in specific activities of maltase and gluco-
amylase at 7 days post weaning when compared to sow-reared piglets of the same
age. The discrepancy in response of various disaccharidases specific activities
compared to weaning might be explained by substrate induction through the weaner
diet. Efird and colleagues (1982) found an increased amount of trypsin and
chymotrypsin in the intestinal contents (g / kg body weight) and a decreased amount
of pancreatic trypsin and chymotrypsin (g / kg body weight). The sum of trypsin
and chymotrypsin activities tended to be lower in weaned piglets compared to sow-
reared piglets (Efird et al., 1982). Thus, the formulation of diets for weanling piglets
may aim at stimulating the production of disaccharidase and pancreatic enzyme
activity in order to maintain the digestive capacity.
8.2.6 Animal performance
The length and weight of the small intestine, the weight of the digestive organs,
the average daily gain (ADG) and the health status are indicators of digestive
development and capacity, and thus of intestinal integrity. These indicators are
positively influenced by feed intake, which is the most important determinant. As
mentioned above, high feed intakes after weaning counteract the weaning-induced
negative changes in indicators of gut integrity. A major goal of formulating diets
for weanling piglets is to stimulate feed intake.
8.3 Modulation of small intestinal integrity by

luminal nutrition
During periods of stress, such as weaning, the nutrients that are required for cell
turnover and maintenance of barrier function are critically important. These nutrients

can be supplied via the intestinal lumen or via the splanchnic blood flow. Factors
in response to ingestion and digestion of food acting on mucosal growth include
cell loss, local nutrients, bulk properties and pH. Additionally, gastrointestinal
hormones and nerves also act on mucosal growth (Johnson and McCormack, 1994),
but are outside the scope of this review. The effect on intestinal integrity of route
of nutrient supplementation, energy intake level and specific dietary components
will be discussed below.
8.3.1 Modulation by route of administration
Exposure of the gastrointestinal tract to nutrients is essential for maintaining its

integrity (Goldstein et al., 1985; Bishop et al., 1992; Park et al., 1998; Bertolo et
al., 1999; Ganessunker et al., 1999; Burrin et al., 2000). The importance of the
presence of food in the lumen of the gastrointestinal tract (luminal nutrition) on
mucosal integrity can be assessed by intravenous (parenteral) feeding as the sole
source of nutrition. Table 8.1 summarises studies comparing the effects of total
parenteral nutrition (TPN) versus enteral nutrition (EN).
Despite similar body-weight gain in all studies, total intestinal mass, mucosal mass,
villus height and villus surface area were all markedly reduced in piglets receiving
TPN compared to their conterparts receiving EN (Goldstein et al., 1985; Park et
al., 1998; Bertolo et al., 1999; Ganessunker et al., 1999; Burrin et al., 2000). This
observation indicates that TPN can supply adequate nutrients to sustain somatic
growth, but for intestinal integrity nutrients have to be provided from the luminal
site. Interestingly, the intestinal length was not affected by TPN, pointing at selective
inhibition of mucosal growth (Park et al., 1998). The lack of enteral stimulation
associated with the administration of TPN may alter the intestinal immune cells
as shown by an increased number of CD4+ and CD8+ T lymphocytes (Ganessunker
et al., 1999). Total mucosal dissacharidase activity was also decreased by TPN (Park
et al., 1998). Park and co-workers (1998) showed that provision of enteral
nutrition at 1% of normal intake was not sufficient for improvement of intestinal
integrity compared to non-supplemented piglets. Total parenteral nutrition with
enteral IGF-I (1000 µg/l) had no effect on intestinal development relative to TPN
alone, but the dosage of IGF-I could have been too low (Park et al., 1998).
Burrin and colleagues (2000) showed, in an elegant study, that the minimal enteral
nutrient intake necessary for efficacy depends on the measure chosen. Piglets were
fed by both intravenous and enteral nutrition, the contribution of the two routes
to total feed intake being variable. Irrespective of the intestinal region studied, the
amount of enteral nutrition required to increase mass and protein content was less
than that required to stimulate proliferative activity as based on measurements of
DNA content, crypt depth and BrdU (5-bromodeoxyuridine) incorporation. The
protein mass of the proximal region of the intestine was more responsive to a
152 Weaning the pig

Table 8.1. Effect of route of feed administration on small intestinal integrity of weanling piglets.
Ref. a Treatments b Design Observations c Remarks
I • EN (TPN solution) • weaned piglets, 6 weeks of age, Comparing TPN-IV vs. EN (TPN solution): • ↑ lactase, maltase and
• EN (starter diet) 10 kg • 0 ADG sucrase specific activity for
• TPN-IV • duration experiment: 0, 21 d • ↓ intestinal weight EN (starter diet) when
• similar energy intake for all • ↓ villus height, 0 crypt depth, ↓ number of compared to EN (TPN
treatments: ± 711 kJ/kg/d epithelial cells solution)
• n=3 / treatment • similar lactase, maltase and sucrase specific

activity
II • EN (MR) • piglets, 1 d postpartum Comparing mean of TPN-IP across treatments • no effect of TPN-IP+EN
• TPN-IP + water • duration experiment: 0, 7 d vs. EN: (MR) or TPN-IP+EN
• TPN-IP + EN (MR) post weaning • 0 ADG (MR+IGF-I) vs. TPN-IP
• TPN-IP + EN (MR + IGF-I) • similar energy and protein • ↓ in intestinal weight (47%), ↓ mucosal
intake for all treatments weight (49%), ↓ mucosal protein content
• n=4, 5 or 6 / treatment (17%)
• 0 intestinal length
• ↓ villus height (24%), ↓ crypt depth (16%)
• ↓ lactase and sucrase total activity
III • EN (TPN solution) • piglets, 2-4 d postpartum Comparing TPN (IV and IP) vs. EN
• TPN-IV • duration experiment: 8 d • 0 ADG
• TPN- IP postweaning • ↓ intestinal weight (60%), ↓ mucosal weight
• similar intake (41%)
• n=5 / treatment • 0 intestinal length
• ↓ villus height, ↓ crypt depth for TPN-IV, 0
crypt depth TPN-IP
153
154
Table 8.1. Continued.
IV • EN (MR) • piglets, 1 d postpartum Comparing TPN-IP vs. EN • ↑ energy and protein intake
• TPN-IP • duration experiment: 0, 7 d • 0 ADG for EN
post weaning • ↓ in intestinal weight (50%)
• n=6 • 0 intestinal length
• 0 villus height, ↓ in crypt depth (30%)
• ↑ # goblet cells in villi (147%), 0 in crypts
• ↑ # CD4+ and CD8+ T lymphocytes
• ↓ in MHC-I (57%), 0 MHC-II in jejunum, ↑
in MHC-II in ileum (455%)
V Of diet supplied: • piglets 7 d postpartum, 3.1 kg Comparing increasing percentages of EN

• 100% TPN-IV • duration experiment: 0, 7 d • proximal small intestine more sensitive to
• 10% EN + 90% TPN-IV post weaning amount of EN then distal segment
• 20% EN + 80% TPN-IV • n=5 / treatment • 0 ADG
• 40% EN + 60% TPN-IV • TPN solution either fed via • ↑ in wet weight and protein content in
• 60% EN + 40% TPN-IV TPN-IV or via EN jejunum with from 40% EN onwards, in
• 80% EN + 20% TPN-IV • balanced for nutrient intake, ileum from 60% EN onwards, ↑ in DNA
• 100% EN energy intake for all treatments: content from 60% EN onwards
900 kJ/kg/dag • ↑ in villus height from 40% EN onwards, ↑
in crypt depth from 60% EN onwards
• ↑ in lactase activity from 80% EN onwards
a reference: I: Goldstein et al., 1985; II: Park et al., 1998; III: Bertolo et al., 1999; IV: Ganessunker et al., 1999; V: Burrin et al., 2000
b Abbreviations: ADG: average daily gain; d: day; CD: cell differentiation molecutes, surface markers of leukocyte subsets; EN: enteral nutrition; IGF-I:
insulin like growth factor; MHC: major histocompatibility complex; MR: milk replacer; TPN-IP: total parenteral nutrition fed intraportally; TPN-IV: total
parenteral nutrition fed intravenously
c 0: similar, ↑: increased, ↓: decreased, #: number
Weaning the pig

decrease in enteral nutrition than that of the distal region. In contrast, the
proportion of enteral nutrition needed to increase cell proliferation showed much
less regional variation along the gastrointestinal tract. The daily feed intake in the
study was approximately 900 kJ⋅kg-1⋅d-1, corresponding with 2800 kJ for piglets
of 3.1 kg (Burrin et al., 2000). Maintenance requirement for these piglets is
approximately 1040 kJ ME⋅d-1 (NRC, 1998) so that they were fed at ≈ 2.7 ×
maintenance. Sixty percent of total feed intake in the form of enteral nutrition was
necessary to sustain normal mucosal proliferation and growth, which corresponds
to 1.6 × maintenance requirement.
The piglets used in the experiments comparing the effects of TPN and EN were
generally weaned at a very young age, i.e. 1 to 7 days postpartum. The young age
relates to the fact that the piglets were used as a model for low birth-weight infants
with low nutrient stores, high metabolic rate and immature gastrointestinal
development. In piglets weaned at an older age (Goldstein et al., 1985) the results
were comparable to those weaned at a younger age. Total parenteral nutrition is
also used for critically injured patients (McCauley et al., 1996). The effect of early
EN, in addition to TPN, on post-surgery infectious complications or bacterial
translocation is not consistent. Some experiments show a reduction in infectious
complications (Kudsk, 1994), but others show no effect on bacterial translocation
(McCauley et al., 1996). A decreased mucosal integrity through lack of nutrients
in the small intestine might reduce its immunological defence mechanisms. So,
although TPN is generally used as a model for low birth weight infants or critically
ill patients, it can very well be used to study the effect of enteral nutrition on small
intestinal integrity.
The effect of short-term starvation immediately after hatching in chickens has been
investigated. Under commercial conditions, newly hatched pullets are usually
refrained from feed up to a maximum of 48 hours. The delay in access to feed results
in decreased body weight when compared to immediate access (Pinchasov and Noy,
1993; Uni et al., 1998; Noy and Sklan 1999), and also leads to decreased villus
height and shallower crypts (Uni et al., 1998). Access to a non-nutritious bulk
material in the form of sawdust to provide gut fill overcame the loss of body weight
during short-term starvation to a similar extent as did access to dry or liquid feed
(Noy and Sklan, 1999). This outcome indicates that mechanical stimulation by
non-nutritious gut fill is important in the early feeding process. It is not known
whether mechanical stimulation per se has positive effects on intestinal integrity
in weanling piglets.
8.3.2 Modulation by level of energy intake
Table 8.2 summarises studies comparing the effect of level of feed intake on small
intestinal integrity in early-weaned piglets. Underfed piglets show decreased daily

156
Table 8.2. Effect of level of feed intake on small intestinal integrity of weanling piglets.
I • continuous PD (± 200 • newly weaned piglets, 14 d Comparing restricted vs. continuous PD piglets were gavaged fed
g/pig/d) postpartum • ↓ in ADG
• 75% restricted PD (± 50 • duration experiment: 5 d post • ↓ in small intestinal weight (51%), 0
g/piglet/d) weaning mucosal protein content
• n=18 / treatment • ↓ villus height (10%), ↓ crypt depth (15%)
• 0 plasma xylose concentration
II • ad lib MR • newly weaned piglets, 5 d Comparing restricted vs. ad lib • energy intake not given
• 60% restriction of ad lib postpartum • ↓ in ADG (42%)
• duration experiment: 0, 30 d • ↓in small intestinal weight (51%), ↓ mucosal

post weaning weight (56%), ↓ mucosal protein content
• n= 6 or 7 / treatment 72%)
• ↓ villus height (47%), ↑ crypt depth (7%)
• ↓ # goblet cells in villi (34%)
• ↑ # infiltrated cells in lamina propria (51%)
III • PD • newly weaned piglets, 29 d Comparing MR fed at Ma vs. 2.5×Ma and ad

• MR at Ma pospartum lib
• MR at 2.5 × Ma • duration experiment: 0, 5 d • ↓ in ADG
• MR ad lib post weanig • ↓ mucosal protein content (21%)
• n=8 /treatment • ↓ villus height (29%), ↑ crypt depth (18%)
• 0 plasma xylose concentration
IV • sow milk semi ad lib d • newly weaned piglets, 28 d Comparing PD and sow milk pair fed with PD • ↑ crypt depth for PD when
• PD postpartum vs. sow milk semi ad lib compared to sow milk pair
• sow milk pair fed with PD • duration experiment 0, 4, 7 d • ↓ in ADG fed with PD at d 4
post weaning • ↓ in villus height, 0 crypt depth
• n=6 / treatment
Weaning the pig

Table 8.2 Continued.
V • ad lib MR • weaned piglets, 7 d postpartum Comparing restricted vs. ad lib

• 80% restriction of ad lib • duration experiment: 30 d post • ↓ weight /cm of the intestine, ↓ DNA,
weaning protein, triglyceride, cholesterol and
• n=6 / treatment phospholipid content in mucosa
• ↓ villus height, ↑ in enterocyte losses
• ↓ mucin levels in goblet cells

VI • semi ad lib MR • newly weaned piglets, 26 d Comparing restricted vs. semi ad lib • symposium paper
• 67% restriction of semi ad postpartum • ↓ in villus height in proximal small intestine
lib d • duration experiment 0, 1, 2, or (19%), 0 crypt depth
4 d post weaning • ↑ in paracellular transport (48%), 0
• n=6 / treatment transcellular transport
a reference: I: Kelly et al., 1991b; II: Núñez et al., 1996; III: Pluske et al., 1996b; IV: Van Beers- Schreurs, 1996; V: Lopez-Pedrosa et al., 1998; VI: Verdonk et
al. 2001
b Abbreviations: ADG: average daily gain; d: day; Ma: maintenance; MR: milk replacer; PD: pelleted starter diet;
d semi ad lib: according to formula describing voluntary feed intake of piglets (NRC, 1998)
157
gain, decreased intestinal and mucosal mass and decreased villus height (Kelly et
al., 1991b; Núñez et al., 1996; Pluske et al., 1996b; Van Beers-Schreurs, 1996; Lopez-
Pedrosa et al., 1998; Verdonk et al., 2001). These piglets also have lower numbers
of goblet cells in the villi (Núñez et al., 1996) with low levels of mucin (Lopez-
Pedrosa et al., 1998). The effect of low feed intake on crypt depth is inconsistent.
Crypt depth was either increased (Núñez et al., 1996, Pluske et al., 1996b), similar
(Van Beers-Schreurs, 1996; Verdonk et al., 2001), or decreased (Kelly et al., 1991b)
for low versus high feed intake. Shallower crypts are thought to be associated with
decreased cell renewal in the crypt and deeper crypts with increased cell proliferation
(Pluske et al., 1997a). The reason for the differences between studies as to the
response of crypt cells to underfeeding is not known.
In general (Table 8.3), total enzyme activities were decreased and specific activities
were increased in malnourished piglets. The increase in enzyme activity when
expressed per gram of mucosal protein implies that the relative effect of malnutrition
on total protein content of the small intestine is larger than that on enzyme activity.
Alternatively, underfeeding leads to an increase in enzyme capacity per enterocyte.
Table 8.3. Comparing restricted versus unrestricted feed intake on small intestinal brush
border dissacharidase activity.
Reference a I II III IV
unit µmol/min/ mol/d µmol/min/ µmol/ µmol/min/ µmol/min/ µmol/

g protein g protein min/cm g protein g protein min/cm
Lactase 0b 0 ↑ 83% ↓ 51% 0 ↑ 22% ↓ 123%

Sucrase ↑ 25% 0 ↑ 46% ↓ 56% 0 ↑ 37% ↓ 46%
Maltase 0 ↓ 55% ↑ 22% ↓ 60% ↑ 39% ↓ 38%
Isomaltase nd nd ↑ 182% ↓ 22% nd nd nd
Glucoamylase 0 ↓ 47% nd nd nd nd nd
Aminopeptidase nd nd ↑ 31% ↓ 60% nd nd nd
protein content 0 ↓ 72% ↓ 21% ↓ 113%
(mg/g) (mg/cm) (mg/g) (mg/cm)
a I: Kelly et al., 1991; II: Núñez et al., 1991; III: Pluske et al., 1996; IV: Lopez-Pedrosa et al.,
1998
b 0: similar enzyme activity;
↑: increased enzyme activity in restricted versus unrestricted-fed piglets;
↑: decreased enzyme activity in restricted versus unrestricted-fed piglets;
nd: not determined
158 Weaning the pig

Because underfeeding is associated with a negative nitrogen balance it is likely that

the increase in specific activity of digestive enzymes is caused by protein depletion
of the intestine.
Verdonk et al. (2001) showed increased paracellular transport of mannitol across

the small intestinal epithelium in underfed piglets. Wirén and colleagues (1999)
investigated the influence of starvation, anesthesia and surgical trauma in rats.
Starvation only caused a decrease in villous height in the jejunum and an increase
in paracellular permeability in the ileum and jejunum (Wirén et al., 1999). Yang
and coworkers (1999) found an inverse relation between the ATP levels in jejunal
mucosa and permeability in rats, indicating that low ATP levels are associated with
increased permeability. Starvation lowers the TEER, which also points at impaired
tight junction function being associated with increased permeability. Starvation also
produced a decrease in short-circuit current, indicating a decrease in the ion pump
activity (Wirén et al., 1999). So, underfeeding leads to increased paracellular
permeability, which is associated with diminished mucosal integrity, so that
pathogens and toxins may cross the epithelial barrier.
It is possible to improve feed intake at weaning by the use of liquid feeding. In

general, improvements in postweaning growth rates have been reported in most
of the studies with piglets fed liquid feed versus dry feed. However, the efficiency
of the feed utilisation is in general lower in piglets receiving liquid feed compared
to those receiving dry feed, as reviewed by Jensen and Mikkelsen (1998). Water
consumption also increased by supplying liquid feed (Russell et al., 1996;
Schellingerhout et al., 2002b). Water and feed intake are positively correlated (Barber
et al., 1989; Schellingerhout et al., 2002b ). Deprez and colleagues (1987) observed
smaller morphological change in the distal jejunum and in the ileum when a liquid
diet (water: feed = 2: 1; w/w) instead of a dry feed was offered to weaned piglets.
Blanchard and colleagues (2000) studied in a 2 × 2 factorial design the effect of
liquid or dry feed fed before and/or after weaning on villus architecture at 25, 50
or 75% along the small intestinal tract. Piglets fed liquid feed before and after
weaning showed increased villus height at 25% of the small intestine when
compared to the other treatments. Crypt depth and number of goblet cells were
not affected by dietary treatment. However, in both studies investigating the effect
of liquid versus dry feed on gut morphology, no information was given on actual
dry matter intakes of the experimental groups. Therefore it is not clear whether
the observed increased villus height is due to the liquid feed itself or due to the
increased feed intake.
8.3.3 Modulation by dietary components
It is clear that luminal nutrition and level of feed intake per se affect gut structure
and function. Functional feed ingredients may indirectly, through enhanced feed

intake, and / or directly, through specific effects, improve small intestinal integrity.
In the following sections, the effects of specific nutrients on gut integrity are discussed
with special attention given to actual feed intake as a possible confounder.
8.3.3.1 Protein
As to the effect of dietary protein on small intestinal integrity, there is ample work
on comparing the effect of soy proteins with that of treated soy proteins or milk
proteins. Table 8.4 summarises the reported effects of protein source on small
intestinal integrity in early-weaned piglets. The inclusion in the diet of soybean meal
instead of milk protein results in similar (Makkink, 1993; Makinde et al.,1996) or
decreased ADG (Efird et al., 1982; Owsley et al., 1986; Dunsford et al., 1989; Li et
al., 1991). Villus height after feeding soybean meal was either similar (Makkink,
1993; McCracken et al., 1999) or decreased (Dunsford et al., 1989; Li et al., 1991;
Makinde et al., 1996). Zarkadas and Wiseman (2000a; 2000b) showed that the intake
level of trypsin inhibitor as a component of soybean meal was negatively correlated
to body-weight gain and villus height in weaned piglets. Feed conversion ratio (feed
intake : weight gain) was positively correlated to the level of trypsin inhibitor intake
(Zarkadas and Wiseman, 2000a). Crypt depth responded inconsistently and is either
increased (Dunsford et al., 1989; Li et al., 1991), similar (McCracken et al., 1998;
1999; Makkink, 1993) or decreased (Makinde et al., 1996) by inclusion of soybean
meal. The number of goblet cells was not affected by dietary soybean meal
(Dunsford et al., 1991; McCracken et al., 1999).
Makkink (1993) compared, skimmed milk powder, soy protein concentrate,

soybean meal and fish meal with regard to small intestinal morphology. In the
proximal and distal jejunum, the type of protein source in the diet did not affect
villus length, crypt dept and intestinal weight. Within the experimental treatments,
the level of feed intake affected villus architecture. To assess the effect of protein
source per se, feed intake should be comparable as may be achieved by a pair-feeding
or restricted-feeding regimen. Newport and Keal (1983) reported a decrease in ADG
when milk protein was replaced by fish protein in the diet. However, the piglets
were weaned as young as 2 d of age and were fed a liquid milk replacer. The piglets
might have been too young to tolerate high levels of fish meal and the practical
relevance of this trial can be questioned. We have compared the effect of protein
from feather meal and skimmed milk powder, which both are low in anti-nutritional
factors (ANFs). The piglets fed the two protein sources and used for measurements
were selected on the basis of comparable feed intake. Villus architecture and growth
were measured at 4, 7 and 14 days post weaning. ADG was increased by 72% during
first two weeks post weaning when comparing piglets receiving the skimmed milk
powder diet to those fed the feather meal diet. Across days, skimmed milk powder
increased villus height (14%) and crypt depth (10%) compared to feather meal
(Spreeuwenberg, 2002).
160 Weaning the pig

Table 8.4. Effect of protein source in the diet on small intestinal integrity of weanling piglets.
Ref. a Dietary variables b Design Observations b, c Remarks
I Experiment 1 (dry feed) • newly weaned piglets, 21 d Experiment 1: Comparing SBM vs. MP • no data on feed intake
• MP postpartum • ↓ ADG (50%)
• SBM • duration experiment 1: 7, 14 d • 0 intestinal weight / cm, ↑ pancreas weight
Experiment 2 post weaning (n=6 / treatment) (19%), ↑ intestinal length (28%)
• MP (dry feed ) • duration experiment 2: 7, 14, 21 • ↑ trypsin in intestine (63%), 0 trypsin in
• MP (liquid feed) d post weaning (n=5 / pancreas, 0 chymotrypsin in intestine,

• CSBM (dry feed) treatment) ↓ chymotrypsin in pancreas (29%)
• balanced diets for protein Experiment 2 Comparing CSBM vs. MP (dry
delivered by test component (re feed)
= 24%) • ↓ ADG (49%)
• ↑ intestinal weight (15%) and length (20%),
0 intestinal weight / length, ↑ pancreas
weight (31%)
• ↑ total trypsin in intestine (341%), 0 total
trypsin in pancreas, ↑ total chymotrypsin in
intestine (95%), ↓ total chymotrypsin in
pancreas (61%)
II • CSBM • newly weaned piglets, 28 d Comparing CSBM vs. CSBM + DW • diets not balanced on
• CSBM + 20 % DW pospartum • ↓ ADG (6%) protein content (re = 23.82
• CSBM + 5% lard • duration experiment: 1, 3, 14, • ↓ total trypsin units in intestine (32%), 0 vs. 21.45 vs. 22.64) or
16, 28d post weaning total trypsin units in pancreas, ↑ lysine (1.21 vs. 1.09 vs.
• n=6 /treatment chymotrypsin in intestine (31%), 0 total 1.22)
chymotrypsin in pancreas • no data on feed intake
161
162
III • casein • newly weaned piglets, 21 d Comparing SBM and CSBM vs. casein
• SBM postpartum • ↓ ADG for SBM (30%) and CSBM (70%), ↓
• CSBM • duration experiment: 0, 3, 6, 9, FI for SBM (8%) and CSBM (51%)
12, 15 post weaning • ↓ in villus height for SBM (14%) and CSBM
• n=5 / treatment (9%), ↑ crypt dept for SBM (16%) and 0 for
• balanced diets for protein casein
delivered by test component (re • 0 areas of Peyer’s patches, 0 # goblet cells in
= 20%) villi and crypts
IV • MP • duration experiment: 7 d • ↓ ADG at week 1 and 2 for SBM and SPC

• SBM postweaning compared to MP, ↓ FI for SBM vs. SPC in
• SPC • newly weaned piglets, 21 d week 1, ↓ FI for MP vs. extruded SPC
• extruded SPC postpartum • ↓ villus height of all diets compared to MP,
• SPI • pigs were sensitised with the ↑ crypt dept for SBM compared to other
respective protein source from d diets
7 to 12 of age • ↑ lymphocyte density for SBM compared to
• n=8 / treatment other diets
• balanced diets for protein and • ↑ IgG titers to soy proteins for SBM
energy compared to other diets
• ↓ xylose concentration in plasma for SBM
and extruded SPC compared to SPI or MP
V • MP • newly weaned piglets, 28 d • ↓ ADG Cowpea compared to other diets. • diets not balanced for raw
• 15.5% SBM pospartum • ↓ villus height, ↓ crypt depth for SBM diets materials
• 31.5% SBM • duration experiment: 0, 7, 14, and cowpea diet compared to control at d 7. • cowpea was fed as a single
• Cowpea meal 21 d post weaning ↑ villus height and similar crypt depth for raw material
• before weaning, half of piglets SBM diets at d 21. ↓ villus height for cowpea • no data on feed intake
received creep feed diet at d 21
• n=5 / treatment
Weaning the pig

VI • MP • newly weaned piglets, 21 d Comparing SBM + SPC vs. MP • weaning itself resulted in
• SBM + SPC postpartum • 0 FI d 0-4, ↑ FI d 4-7 villus atrophy and
• duration experiment: 0, 0.5, 1, • 0 villus height and crypt depth intestinal inflammation
2, 4, 7 d • 0 # goblet cells
• n=10 / treatment • 0 # CD8+ and CD4+ T cells, 0 concentration
• balanced diets for protein deliver- of prostaglandin 2

ed by test component (re=20%)
VII • SMP • newly weaned piglets, 28 d • 0 ADG, ↑ FI for FM and SBM compared to • villus height and crypt
• SPC postpartum SMP from d 0-3, 0 FI from d 3-10. depth were affected by level
• SBM • duration experiment: 0, 3, 6, or • ↑ pancreatic weights for SMP and SPC of feed intake
• FM 10 days post weaning • 0 villus length, 0 crypt depth at d 6
• n=5 / treatment
• balanced diets for protein
VIII of protein in diet: • newly weaned piglets, 2 d Comparing different ratios of FM and MP in diets • diets fed as milk replacer
• 0% FM + 100% MP postpartum • ↓ ADG and ↑ feed : gain with increasing FM
• 35% FM + 65% MP • duration experiment: 0, 5, 26 content
• 52.5% FM + 47.5% MP • n=7 / treatment • ↓ pH, DM and total N in the stomach with
• 70% FM + 30% MP • balanced diets for protein increasing FM content, 0 total N in small
intestine
• 0 chymotrypsin and trypsin activity
IX • SMP • newly weaned piglets, 27 d Comparing feather meal with SMP • piglets were selected for
• feather meal postpartum • ↓ ADG (46%), ↓ feed efficiency (50%) comparable feed intake to
• duration experiment: 0, 4, 7, or • ↓ in villus height (12%), ↓ in crypt depth avoid entanglement
14 d post weaning (9%) between protein source and
• n=6 / treatment feed intake
• balanced diet for protein and
lactose
163
164
X • DW + SBM • newly weaned piglets, 14 d Comparing SDAP and pair fed SDAP to • diets not balanced for
• SDAP postpartum DW+SBM vs. DW+SBM: protein (re=24 vs. 22)
• SDAP pair fed to DW + • duration experiment: 0, 2, 4, 8, • ↑ ADG d 0-16 for SDAP, ↑ FI d 0-16 SDP, 0 • feed intake of pair fed
SBM 16 d post weaning ADG and FI for d 0-4 and 0-8 animals is lower than feed
• n=8 / treatment • ↓ small intestine weight / kg of body weight intake of control
at day 16, ↓ DNA and protein content at day
16
• 0 villus height, crypt depth, mucosal
thickness
• 0 5-bromo-2’-deoxyuridine labeling
• ↓ intravillus lamina propria cell density in
the proximal jejeunum at d 4, 8 and 16
XI • control • weaned piglets Comparing SDAP vs. control: • review combining 15

• SDAP • ↑ ADG (26.8%), ↑ FI (24.5%), ↓ feed published studies with
efficiency (3.2%) SDAP
XII • MP • newly weaned piglets, 4 d • ↓ ADG with SPI, 0 with hydrolysis, 0 feed • diets fed as milk replacer
• hydrolysed MP pospartum intake
• SPI • adaptation in groups for 3 d • ↑ small intestinal weight per kg of body
• hydrolysed SPI • duration experiment: 21 d after weight for piglets receiving SPI
adaptation • ↓ specific activities of trypsin and
• n=8 / treatment chymotrypsin in the duodenum and
• balanced diets for protein and pancreas by hydrolysis
lactose
Weaning the pig

XIII • casein • newly weaned piglets, 2 d. • tendency for ↑ ADG for hydrolysed
• SPI pospartum compared to normal SPI, 0 FI
• hydrolysed SPI • duration experiment: 0, 2, 5 • ↓ diarrhoea with hydrolysed SPI at d 2
and 10 d after adaptation for 5 • ↓ villus height at proximal jejunum at d 2
d for hydrolysed and normal SPI. 0 villus
• n=4 / treatment height at day 5 and 10 at proximal jejunum,

• balanced diets for protein 0 villus height at all days at mid and distal
jejunum, ↑ crypt depth at mid small
intesinte at d 2 for hydrolysed and normal
SPI, 0 crypt depth other days and segments
• 0 # CD8+ T cells and prostaglandin
concentration
XIV • untreated SBM • newly weaned piglets, 29 d Comparing vs. untreated SBM
• acid treated SBM postpartum • ↑ ADG (0-7d) for hydrolysed SBM (63%) and
• acid hydrolysed SBM • duration experiment 8-11 d post MP (48%), 0 ADG 0-14, 0-21d., ↑ FI (0-21d) for
• MP weaning hydrolysed (12%) and acid treated (13%) SBM
• SPC • n=24 / treatment, growth • 0 villus height, crypt depth, villus area
performance • 0 aminopeptidase, lactase, maltase, ↑ sucrase
• n=4 / treatment, intestinal for hydrolysed SBM (100%) and SPI (92%)
integrity (specific activity)
• 0 antibody titres
• 0 plasma xylose
a reference: I: Efird et al., 1982; II: Owsley et al., 1986; III: Dunsford et al., 1989; 1991; IV: Li et al., 1991; V: Makinde et al., 1996; VI: McCracken et al., 1999;
VII: Makkink, 1993; VIII: Newport and Keal, 1983; IX: Spreeuwenberg, 2002; X: Jiang et al., 2000; XI: Van Dijk et al., 2001; XII: Leibholz, 1981; XIII:
McCracken et al., 1998; XIV: Rooke et al., 1998
b Abbreviations: ADG: average daily gain; CD: cell differentiation molecutes, surface markers of leukocyte subsets; CSBM: corn + soybean meal, DW: dried
whey, FI: feed intake; FM: fish meal, MP: milk protein, SBM: soybean meal, SDAP: spray dried plasma protein, SMP: skimmed milk powder, SPC: soya
protein concentrate, SPI: soya protein isolate
165
Van Dijk and colleagues (2001) conducted a multiple regression analysis and
concluded that dietary sprayed dried animal plasma (SDAP) levels up to 6% in
the diet increase both average daily gain and feed intake in the first 2 weeks after
weaning in a dose-dependent fashion. The positive effect of SDAP was more
pronounced in the first than in the second week after weaning. It is suggested that
the positive effect of SDAP can be explained by increased feed intake, and possibly
also by specific bioactive components preventing attachment of pathogenic E. coli
to the intestine (Van Dijk et al., 2002). Villus height, crypt depth and cell
proliferation were unaffected by SDAP (Jiang et al., 2000; Van Dijk et al., 2001).
Due to health risks associated with the use of non-sterilised products of animal
origin as feed ingredients, SDAP may be banned as an ingredient for animal feed.
Unravelling the mechanism underlying the positive effect of SDAP would be
important for further developing functional feeds. However, the positive effect of
SDAP seems mainly to occur via stimulation of feed intake.
The early-weaned piglet has limited capacity to digest dietary proteins. By

enzymatic hydrolysis of feed proteins, protein digestibility and availability for early-
weaned piglets might be improved. It is difficult to draw general conclusions about
the efficacy of hydrolysed proteins because the conditions of processing and enzymes
used are variable, leading to different hydrolysis products. Treatment of soy proteins
has been shown to ameliorate effects of ANFs and to decrease the serum antibody
immunoglobulin G titers (Li et al., 1991). Rooke and co-workers (1998) showed
lower antigenic protein contents in hydrolysed soybean meal, but no effect on
antibody titers. When comparing soybean meal with hydrolysed soybean meal, ADG
was either similar (Leibholz, 1981) or increased (McCracken et al., 1998; Rooke
et al., 1998), and gut wall architecture was not different (McCracken et al., 1998;
Rooke et al., 1998). McCracken and colleagues (1998) showed less postweaning
diarrhoea after feeding diets with hydrolysed soy protein isolate instead of either
soy protein isolate or milk protein. However, there was no diet effect on intestinal
numbers of goblet cells, mast cells, T cells, local production of prostaglandins and
local expression of MHC genes, demonstrating that the type of protein did not
influence inflammation when fed to piglets weaned 2 d post partum (McCracken
et al., 1998). Poullain and colleagues (1989) compared the effects of alimentary
whole whey protein, whey protein oligopeptides and an amino acid mixture in
rats. Growth and nitrogen retention after starvation followed by realimentation was
highest for rats receiving the oligopeptides. Weanling rats recovering from severe
starvation by feeding either a casein hydrolysate or the native protein had similar
weight gain. However, intestinal permeability for ovalbumin remained increased
only in the group refed with the casein diet (Boza et al., 1995). Possibly, the feeding
of hydrolysed protein more effectively counteracts the weaning-induced impairment
of gut integrity than does feeding of the intact protein.
166 Weaning the pig

8.3.3.2 Amino Acids
Amino acids taken up by the intestinal mucosa are derived from the blood and
from the intestinal lumen. Stoll and colleagues (1998) conducted tracer balance
studies with radioactive amino acids and measured amino acid incorporation into
mucosal protein in piglets. The authors concluded that 60% of the essential amino
acids taken up from the intestinal lumen were catabolised by the intestine. The
amount of catabolised amino acid was equivalent to at least 20% of the essential
amino acids consumed and was directly related to the mucosal mass (Stoll et al.,
1998). This not only implies intestinal mass determines the efficiency of dietary
protein utilization, but also that the availability of luminal amino acids is
important for maintaining the mucosal mass and thus mucosal integrity.
Individual amino acids may have a specific role in regulating intestinal integrity
and function (Wu, 1998). Glutamine, glutamate and aspartate are major fuels for
small intestinal mucosa and support ATP-dependent metabolic processes such as
active nutrient transport and high rates of intracellular protein turnover. Ornithine,
which is derived from arginine, glutamine and proline, is the immediate precursor
for polyamine synthesis, which is essential for proliferation, differentiation and
repair of intestinal epithelial cells. Arginine is the physiological precursor of nitric
oxide (NO), which plays an important role in processes such as vasodilation,
immune responses, neurotransmission and adhesion of platelets and leucocytes
(Wu and Morris, 1998). Glutamate, glycine and cysteine are precursors for the
synthesis of glutathione, a tripeptide critical for defending the intestinal mucosa
against toxic and peroxidative damage (Wu, 1998). Thus dietary glutamine is
involved in the energy supply of the intestine, while the other amino acids through
conversion have regulatory properties.
We are not aware of studies on the effect of dietary supplementation of aspartate,

glycine, cysteine or proline on small intestinal integrity of the weaned pig as
measured by histology, specific enzyme activity and permeability. Supplementation
to the diet of either 0.6% or 0.93% arginine did not affect growth performance
and villus height (Touchette et al., 2000; Ewtushik et al., 2000). The effects of
glutamine have been repeatedly studied. Whilst not considered to be an essential
amino acid, L-glutamine is an abundant free amino acid in the plasma of animals
(Wu et al., 1996) and in sow’s milk (Wu and Knabe, 1994). As mentioned above,
glutamine is a major energy source for the gut and supports nucleotide biosynthesis,
but it also serves as an ammonia scavenger and preserves the immunological function
during total parenteral nutrition (Windmueller, 1982; Alverdy, 1990; Souba 1993;
Salway, 1995). Glutamine can be taken up with feed, but it can also be formed
from glutamate and NH4+ in an ATP-requiring reaction catalysed by glutamate
synthetase. Hydrolysis of the terminal amide group of glutamine by glutaminase
results in formation of glutamate and ammonia. As an energy source, glutamate

readily enters the Krebs cycle following oxidative deamination by glutamate

dehydrogenase into α-ketoglutarate. Complete oxidation of 1 molecule of glutamate
generates 12 molecules of ATP. A study by Houdijk and colleagues (1994) showed
that feeding a glutamine-enriched diet increased the splanchnic blood flow in the
rat. Thus extra glutamine provides energy in itself and indirectly by increasing the
blood flow to the intestine. Glutamine, but not glutamate, plays a role in
nucleotide metabolism as it donates the nitrogen atoms which form N-9 and N-
3 of the purine ring (Salway, 1995). Depending on the activity of glutamine
synthetase, glutamate can substitute for glutamine in purine metabolism.
A disadvantage of glutamine for dietary supplementation is its instability.

Degradation of glutamine can be minimised by the addition of L-glutamine shortly
before administration or by the use of a more stable form, e.g. L-alanyl-L glutamine
or L-glycyl-L-glutamine. Dipeptides are rapidly hydrolyzed to their respective amino
acids (Lacey and Wilmore, 1990), but are relatively expensive.
Table 8.5 summarises the reported effects of glutamine on the small intestine. In
newly-weaned piglets plasma concentrations of glutamine are reduced when
compared to unweaned, suckling piglets (Ayonrinde et al., 1995a). Some experiments
with weaned piglets showed no effect on villus height with either 1% (Kitt et al.,
2001) or 1.2% glutamine in the diet (Touchette et al., 2000). Some showed that
1% glutamine (Wu et al., 1996) or 6.5% glutamate (Ewtushik et al., 2000) had an
effect on one site of the proximal small intestine but not further along the intestine.
One study showed that 4% glutamine increased villus height in both the duodenum
and ileum (Ayonrinde et al., 1995b). Wu and colleagues (1996) showed improved
feed efficiency but similar growth during the second week postweaning when 1%
glutamine was fed. In other studies, growth was either similar (Ewtushik et al., 2000)
or increased by the addition of glutamine to the diet (Kitt et al., 2001). Lackeyram
and colleagues (2001) noted increased growth with 0.8% glutamine, but no effect
with either 1.6% or 2.4%. It may be concluded that the effects of glutamine
supplementation on villus architecture and growth performance are equivocal.
Perfusion of the epithelium of the ileum of weaned piglets with L-glutamine

increased tissue viability as indicated by an increase in transmembrane potential
difference (Smith et al., 1992). However, glutamine administration had no effect
on tissue integrity as based on the TEER (Smith et al., 1992). Bacterial translocation
of orally administered E. coli did not occur in either control or glutamine
supplemented weanling piglets (Smith et al., 1992). Dugan and McBurney (1995)
indicated that luminal glutamine is beneficial for the maintenance of normal
mucosal permeability during endotoxicosis. Ileal perfusion with a glutamine-
containing solution effectively abolished endotoxin-induced increases in mucosal
permeability in intestinal loops. In endotoxemic rats, glutamine-supplemented
parenteral nutrition improved the morphology of the jejunal mucosa as based on
168 Weaning the pig

Table 8.5. Effect of glutamine on small intestinal integrity of early weaned piglets.
I Enteral nutrition • newly weaned piglets, 21 d Comparing addition of gln vs. gly symposium paper
• 4% gln postpartum • 0 ADG, 0 FI
• 4% gly • duration experiment: 5 days • 0 protein content (mg/cm gut),↑ DNA
• n=10 / treatment content (µg/cm gut)
• ↑ villus height and crypt depth in ileum and
jejunum.

• ↑ jejunal glutaminase (µmol/h/cm)
II Enteral nutrition • newly weaned piglets, 21 d Comparing 1.0% vs. 0 % gln • no information on feed
• 0% gln postpartum • 0 ADG and FI during week 1 and 2, ↑ ADG intake for piglets with
• 0.2% gln • duration experiment: 0, 7, 14 and feed efficiency during week 2 morphology measurements
• 0.6% gln post weaning • ↑ villus height at 7 d post weaning at • In growth trial piglets
• 1.0% gln • n=5 / treatment jejunum, 0 villus height at 7 d post weaning receiving 1% gln had
in duodenum and at 14 d post weaning in numeric lower feed intake
duodenum and jejunum, ↓ crypt dept at 14
d post weaning at jejunum, 0 crypt depth at
14 d post weaning in duodenum and at 7 d
post weaning in duodenum and jejunum
III • 0% glu, arg • newly weaned piglets, 12 d Comparing the addition of 0 vs. 6.51% glu • Piglets receiving arginine
• 6.51% glu postpartum • 0 ADG and FI did not differ from control
• 0.93% arg • duration experiment: 0, 10 post • 0 organ weights group
weaning • 0 sucrase, lactase, maltase specific and total
• n=7 / treatment activity
• ↑ villus height duodenum, 0 villus height
proximal and mid jejunum and ileum. 0
crypt depth
169
170
IV • 0% gln • newly weaned piglets, 18 d • 0 ADG and FI from 0-14, ↑ ADG and FI • Piglets used to measure
• 1.0% gln postpartum from 14-21 growth performance or
• duration experiment • 0 villus height villus height were not the
(postweaning): same
0, 4 for histologic sampling.
0, 4, 7, 14, 21 for growth
performance
• n=4 / treatment
V • 0% gln, arg • newly weaned piglets, 17 d Comparing the addition of 0 vs. 1.2% gln: • arg vs. gln showed ↓ ADG
• 1.2% gln postpartum • 0 ADG and FI from 0-7 and 14-28
• 0.6% arg • duration experiment • 0 villus height, ↑ crypt depth at d 14 • arg vs. control and gln
(postweaning): showed either 0 and ↓ crypt
0, 7, 14 for histologic sampling. depth
0, 7, 14, 28 for growth
performance
• n=6 / treatment
VI TPN: • newly weaned miniature piglets, • 0 ADG

• 0% gln + 0% glu 2 d postpartum • 0 plasma and jejunal mucosa concentration
• 0.35% gln + 0% glu • adaptation period: 5 d of gln and glu
• 0% gln + 0.35% glu • duration experiment: 7 d post • 0 intestinal weight, protein , DNA content or
adaptation protein / DNA ratios
• similar lactase, sucrase or maltase specific
activities
Weaning the pig

VII Using chambers perfused • newborn piglets, 1 to 4 d Comparing weanling with gln vs. without
with: postpartum • ↑ potential difference (=tissue viability)
• newborn + HBBS (A) • weanling piglets, 21 d • 0 resistance (= tissue integrity)
• weanling + HBBS (B) postpartum • no bacterial translocation
• A + 0.29% gln (C) • permeability measured with
• B + 0.29% gln (D) Using chamber

• C + E. coli • n=4-8 / treatment
• D + E. coli
VIII perfused intestinal loops: • piglets 21 d postpartum • 0 permeability after endotoxin

• Ringer’s lactate solution • permeability estimated by ratio administration for gln perfused loops, ↑
• Ringer’s lactate solution + of clearance of 51Cr-EDTA and permeability for loops perfused with only
2% gln urea Ringer’s lactate solution
• oxygen-purged Ringer’s • administration of bacterial
lactate solution + 2% gln endotoxin
• n=4 / treatment
a reference: I: Ayonrinde et al., 1995b; II: Wu et al., 1996; III: Ewtushik et al., 2000; IV: Kitt et al., 2001; V: Touchette et al., 2000; VI Burrin et al., 1991; VII:
Smith et al., 1992; VIII: Dugan and McBurney, 1995
b abbreviations: ADG: average daily gain; FI: average daily feed; glutamic acid: glu; glutamine: gln; glycine: gly; HBBS: Hanks Balanced Salt Solution; TPN:
total parenteral nutrition
c 0: similar, ↑: increased, ↓: decreased
171
increased villus height, crypt depth and wall thickness. In the glutamine group,
the arterio - portal venous endotoxin difference after intravenous infusion of a
lipopolysaccharide of E. coli was less negative, suggesting that the absorption of
endotoxin across the gut was diminished through improved mucosal barrier function
(Chen et al., 1994). Yoo and colleagues (1997) studied the proliferative response
of lymphocytes to concanavalin A, which specifically activates T cells via binding
to specific membrane receptors (CD3). The proliferative response in lymphocytes
from pigs infected with E. coli and fed a diet without glutamine was depressed,
whereas lymphocytes from infected pigs fed a diet with 4% glutamine responded
similarly to those isolated from non-infected pigs. Both the control diet and the
diet with extra glutamine contained 4.4% glutamate. It may be concluded that
glutamine supplementation supports immune function during critical states, but
has no clear effect in non-challanged weanling piglets.
8.3.3.3 Fat and poly-unsaturated fatty acids
The addition of fat at the expense of corn to pig starter diets does not consistently
enhance growth rates and feed / energy conversion during the initial weeks post
weaning (Li et al., 1990; Cera et al., 1990b, Mahan, 1991). However, during the
second phase of the nursery period, the addition of extra fat improves daily gain
and feed efficiency (Li et al., 1990; Cera et al., 1990b; Mahan, 1991), but energy
conversion is not or slightly improved. The most pronounced effects of added fat
on daily gain during the second period are seen with coconut, soybean and corn
oil (Li et al., 1990; Cera et al., 1990b; Mahan, 1991). Cera and co-workers (1990a)
showed that luminal lipase activity is low during the initial post-weaning period,
but subsequently increases again. This observation confirms the increase in
growth and feed efficiency with post-weaning age.
Table 8.6 summarises the outcome of two studies on the influence of the fat source
in the weaner diet on small intestinal morphology. Cera and colleagues (1988)
showed that supplementation of the diet with 6% corn oil at the expense of corn
reduced villus height in the small intestine of weaned piglets. However, feed intake
data were not shown. However, body weight was similar in the low and high fat
diet. Li and colleagues (1990) compared diets supplemented with either soy oil,
coconut fat or a 50/50 mixture of these two fat sources. The piglets that received
either coconut or soybean oil had shorter villi than did the piglets that received
the fat mixture, but when compared to the control diet, fat supplementation did
not affect villus height. Fat supplementation at the expense of corn resulted in deeper
crypts, irrespective of the type of fat (Li et al., 1990). Likewise, in rats, the addition
of 8% instead of 4% corn oil to the diet increased crypt cell proliferation resulting
in deeper crypts (Pell et al., 1992). It may be concluded that the addition of extra
fat to the diet increases crypt depth and may lower villus height in weanling piglets
without affecting growth performance.
172 Weaning the pig

Table 8.6. Effect of fat source in the diet on small intestinal integrity of weanling piglets.
I • CSBM • newly weaned piglets, 28 d Comparing CSBM+ 5% lard vs. CSBM • diets not balanced on fat
• CSBM + DW pospartum • ↓ ADG (10%) content (ether extract (%) =
• CSBM + 5% lard • duration experiment: 0, 14, 27, • 0 trypsin in intestine and in pancreas, ↑ 1.34 vs. 2.38 vs. 8.68)
29, 31, 42, 44, 56 postpartum trypsin per kg of pancreas (77%), 0 • no data on feed intake
• n=6 / treatment chymotrypsin in the intestinal contents and
pancreas

II • 0% DW + 0% corn oil • newly weaned piglets, 21 d • ↓ lipase activity after weaning • no data on feed intake
• 25% DW + 0% corn oil postpartum Comparing 6% vs. 0% corn oil
• 0% DW + 6% corn oil • duration experiment 3, 7, 14, • 0 ADG and intestinal weight, ↑ pancreas
• 25% DW + 6% corn oil 21, and 28 d weight at d 28
• n=6 / treatment • ↓ villus height
• diets balanced on kcal ME / g • ↑ total lipase in pancreas, 0 lipase / g
lysine, increased ME content for pancreas, 0 lipase in intestine
diets with oil
III 4 trials with: • newly weaned piglets, between • 0 ADG, FE and ↓ FI with addition of 10% fat
• control 18 and 21 d during first 2 weeks, ↑ ADG with addition of
• white grease • diets balanced for lysine / fat from week 3-5 post weaning, especially
• soybean oil energy ratio with combination of soybean and coconut
• coconut oil oil
• soybean oil + coconut oil • ↓ ileal DM digestibility with addition of fat
• ↑ villus height with combination of soybean
and coconut oil compared to soybean or
coconut oil alone, 0 villus height with
addition of fat compared to control, ↑ crypt
depth with addition of fat compared to
control
173
174
IV • control • suckling piglets, 4 d post Comparing oil vs. control • no data on feed intake and
• oil: ω3:ω6 = 10:1 partum • 0 # leukocytes and lymphocyts, 0 migration growth
• n= 5 or 6 / treatment index of lymphocytes,.
• 0 CD4+, ↑ CD8+, 0 CD2+ lympocytes
• ↓ level of archidonic acid (ω6),↑
docosahexaenoic acid (ω6), ↑gamma-
linolenic acid (ω3), eicosapentaenoic acid
(ω3) and docosahexaenoic acid (ω3)
• ↑ growth factors
• ↑ IgM (43%)
V • Control • weaned piglets, 7 d post partum Comparing PUFA vs. no PUFA diet was supplemented with a
• Control + PUFA • malnutrition (20% of control) • ↑ weight per length ratio of the intestine for phospholipid concentrate
• Malnourished during 30 days followed by 10 d malnourished piglets of ω-6 and ω-3 long chain
• Malnourished + PUFA refeeding with or without fatty • ↑ recovery in the morphology in fatty acids also containing
acids malnourished piglets cholesterol.
• 0 disachharidase and alkaline phosphatase
activities
• ↑ DNA, protein, cholesterol, phospholipid
and triglyceride content in jujunal but 0 in
ileal mucosa of malnourished piglets
a reference: I: Owsley et al., 1986; II: Cera et al., 1988; 1990; III: Li et al., 1990; IV: Kastel et al., 1999; V: Lopez-Pedrosa et al. 1999
b abbreviations: ADG: average daily gain; DM: dry matter; DW: dried whey; FE: feed efficiency; IgM: immunoglobulin M; PUFA: poly unsatturated fatty
acids
Weaning the pig

Polyunsaturated fatty acids can belong to either the omega-3 (ω-3) or omega-6
(ω-6) family of fatty acids. Soybean, corn and sunflower oil are fat sources rich in
the ω-6 fatty acids. Linseed and fish oil are rich in the ω-3 fatty acids α-linolenic
and eicosapentanoeic acid, respectively. The ω-3 polyunsaturated fatty acids have
been investigated for use in the treatment of inflammatory diseases (Blok et al.,
1996; Calder, 1998). Calder (1998) reviewed the effect of dietary fatty acids on
the immune system and indicated that high-fat diets generally lower T-lymphocyte
proliferation and natural killer cell activation when compared with low-fat diets.
Among the fat sources in high-fat diets the order of potency was found to be:
saturated fat (e.g. palm oil, coconut fat) < n-6 polyunsaturated rich oils (e.g. corn
oil, soybean oil, sunflower seed oil) < olive oil < linseed oil < fish oil. Studies with
experimental animals indicate that diets rich in ω-3 polyunsaturated fatty acids
are anti-inflammatory and immunosuppressive in vivo (Calder, 1998).
The effect of ω-3 and ω-6 polyunsaturated fatty acids has not been extensively
investigated in piglets (Table 8.6). Kastel and colleagues (1999) found that oral
administration of ω-3 polyunsaturated fatty acids to piglets affected the immune
response. The production of ω-3 derived docosahexanoeic acid was significantly
increased in the blood at the expense of ω-6 derived arachidonic acid. The production
of IgM by B lymphocytes and growth factor (somatomedin C) was increased after
ω-3 supplementation, but so was the production of cytotoxic T lymphocytes (Kastel
et al., 1999). Lopez-Pedrosa and co-workers (1999) investigated the effect of feed
restriction and combined ω-6 and ω-3 polyunsaturated fatty acid supplementation
in a 2×2 factorial design. Extra fatty acids enhanced small intestinal recovery after
feed restriction, but had only limited effect in well-nourished piglets.
In weanling piglets, offering a diet containing linseed oil, which is rich in α-linolenic
acid, visually improved assessed body condition but not growth performance when
compared with a diet containing corn oil, which is rich in linoleic acid
(Schellingerhout et al., 2002a). It may be concluded that the addition of ω-3 fatty
acids to the diet of weanling piglets might have beneficial effects, especially when
feed intake is low and hygiene status is suboptimal.
8.3.3.4 Fibres and non-digestible oligosaccharides
The term dietary fibre refers to plant carbohydrates, including pectins that resist
hydrolysis by alimentary enzymes but can be fermented by the gastrointestinal flora.
Dietary fibres cover a wide variety of substances with different physical properties
and physiological effects. Some components are soluble, whereas others are
insoluble; some have a high water-holding capacity, whereas others have a low or
no water-holding capacity (Roberfroid, 1993). Soluble fibers may delay, whereas
insoluble fibers may accelerate, small intestinal transit time, influencing contact
time between digesta, enzymes and microbes. The major effect of soluble fibre is

a reduction in starch hydrolysis and carbohydrate absorption, leading to a reduced

and flattened glycemic response as well as reduced insulinemia (Bueno et al., 1981;
Silk, 1989; Scheppach et al., 1990; Roberfroid, 1993; Mosenthin and Hambrecht,
1998). Soluble fibers may increase the thickness of the unstirred water layer covering
the epithelial cells in the small intestine and thereby create a diffusion barrier that
limits contact between intestinal enzymes and their substrates, and consequently
reduces apparent enzyme activity. The increased unstirred layer may protect the
mucosa against damage from particles.
The reported effects of dietary fibres on small intestinal integrity in weaned piglets
are shown in Table 8.7. In general, inclusion of fiber in the diet did not affect growth
(Moore et al., 1988; Jin et al., 1994; Longland et al., 1994; Lizardo et al., 1997;
Hambrecht, 1998; Gill et al., 2000). Small intestinal weight was either unchanged
(Jin et al., 1994, Lizardo et al., 1997) or increased after fibre consumption
(Hambrecht, 1998). Hambrecht (1998) reported an increased incidence of
diarrhoea during the first 2 weeks after weaning with the inclusion of wheat bran
in the diet, however over a 5-week period, there was no effect on the incidence of
diarrhoea. Extra intake of fibre by weaned piglets increased total tract apparent
digestibility of non-starch polysaccharides, but had no effect on total tract apparent
digestibility of protein, dry matter and energy (Longland et al., 1994; Lizardo et
al., 1997; Gill et al., 2000). Lizardo and colleagues (1997) showed in weanling
piglets that faecal nutrient digestibility was similar for fibrous diets versus fibre-
free diets, but apparent ileal nutrient digestibility was decreased.
Jin and colleagues (1994) investigated the effect of 10% wheat straw in the diet on
small intestinal architecture in weaned piglets. Villus height was not affected by dietary
fibre, but the width of the villi and crypt depth were increased. Because the crypts
are the principal site of cell proliferation in the intestinal mucosa, these data, in
conjunction with the observed increase in cell proliferation and cell death, support
the hypothesis that high fibre intake increases the rate of turnover of intestinal
mucosal cells (Jin et al., 1994). Moore and coworkers (1988) showed no effect of
dietary fibre on microscopic morphology. The effects seen in weaned piglets agree
with those found in rats. In rats, supplementation of the diet with 10% guar gum
also increased crypt cell proliferation, resulting in deeper crypts. However insoluble
wood cellulose had no effect on crypt cell proliferation, which may be due to its
poor fermentability (Pell et al., 1992). In rats, dietary supplementation with either
guar gum or pectin increased crypt depth, crypt cell proliferation and the migration
rate of cells along the crypt villus axis when compared to either a fibre free diet or
diets supplemented with either cellulose or retrograded starch. The effects of the
soluble fibres were more pronounced in the proximal and mid small intestine than
in the distal small intestine. Villus height was not affected by the type and amount
of dietary fibre (Brunsgaard and Eggum, 1995).
176 Weaning the pig

Table 8.7. Effect of fibers in the diet on small intestinal integrity of piglets.
I • CWR • newly weaned piglets, 24 d post Comparing W and B vs CWR during 2 weeks:
• W and B partum • 0 ADG, FI and FE
• CWR, W and B • duration experiment: 14 or 35 d • ↑ incidence of diarrhoea
post weaning • ↑ weight of proximal and distal small
intestine
• 0 total VFA production in distal small

intestine, caecum and colon
Comparing all three diets during 5 weeks:
• ↓ FI in week 3, 4/5 for CWR. ↑ FE for CWR
in week 4/5
• 0 in diarrhoea
• ↑ weight of distal and similar weight of
proximal small intestine for W / B
• ↑ total VFA production in distal small
intestine for W / B and CWR/WB and similar
total VFA production in caecum and colon
II • CSBM • piglets, 9.7 kg • ADG and FE tended to be lower for AM diet

• OH • duration growth trial 34 d post compared to others, 0 FI
• SBH start of trial • 0 morphology (shape of villi)
• AM • n=3 / treatment
• diets balanced for protein and
energy
177
178
III • 0% WS • barrows, 14.3 kg Comparing 10 vs. 0 % WS

• 10% WS • n=4 / treatment • 0 ADG, FI and FE
• duration experiment: 14 d • 0 weight of small intestine
• diets balanced for protein and • 0 villus height, ↑ width of intestinal villi,
energy ↑ crypt depth
• ↑ rates of cell proliferation (5-bromo-2-
deoxy-uridine) in jejunum and colon
• ↑ rate of programmed cell death in jejunum
and ileum
IV • 0% SBP • weaned boars, 21 d post partum Comparing 15% with 0% SBP

• 15% SBP • n=6 / treatment • 0 ADG, ADFI and FE
• diets balanced for protein and • ↑ TTAD of NSP (39%), 0 TTAD of N and
energy energy
V Diet composition • weaned piglets, 28 d post • 0 ADG, FI, FE

• W partum • 0 TTAD of N, DM, GE, ↑ TTAD of NSP
• B • growth trial (n=6 / treatment),
• SBP duration experiment 4 weeks
Diet with or without enzymes post weaning
• digestibility trial (n=4 /
treatment), duration experiment
11 days post weaning
Weaning the pig

VI • SBM • weaned piglets, 25 d post Comparing 12% with 0% SBP: • for enzyme activities,
• SBM + SBP (12%) partum • 0 ADG and FI piglets were 56 days of age
• SFPC • duration experiment 31 days • 0 small intestinal weight and protein • ileal digestibilty measured
• SFPC + SBP (12%) • n=7 / treatment content.- by ileo-rectal anastomosis
• diets are balanced for energy, • ↑ TTAD of fibrous components, similar for
protein and total lysin other nutrients

• ↓ ileal nutrient apparent digestibility
• ↓ ileal N retention, ↑ faecal N retention,
• ↑ dipeptidyl peptidase, N-aminopeptidase,
alkaline phosphatase and similar maltase
and γ-glutamyl transferase in the ileum, 0
enzyme activities in jejunum, 0 α-amylase,
trypsin, chymotrypsin activity, ↑ lipase
activity
a reference: I: Hambrecht, 1998; II: Moore et al., 1988; III: Jin et al., 1994; IV: Longland et al., 1994; V: Gill et al., 2000; VI: Lizardo et al., 1997
b abbreviations: ADG: average daily gain, AM: Alfalfa meal; B: barley; CSBM: corn soybean meal; CWR: cooked white rice; FE: feed efficiency; FI: feed intake;
NSP: non starch polysaccharides; OH: oat hulls; SBH: soya bean hulls; SBM: soybean meal; SBP: sugar beet pulp; SFPC: soluble fish protein concentrate;
TTAD: total tract apperent digestibility; W: wheat, WB: wheat bran; WS: wheat straw
c 0: similar, ↑: increased, ↓: decreased
179
Short chain fatty acids (SCFA) may be involved in increased proliferation of crypt
cells caused by soluble fiber. In fistulated rats, SCFA infusion at a physiological
dose increased the crypt cell production rate in the small and large intestine in a
dose-dependent manner, the effectiveness being in the order n-butyric > propionic
> acetic acid (Sakata, 1987). Fermentation of dietary soluble fibres by microbes
leads to the generation of SCFA. The number of bacteria and SCFA production in
the different segments of the small intestine are indicators of fermentative capacity.
The stomach and proximal small intestine of the pig contain relatively low numbers
of microbes (103-105 bacteria per ml of digesta). The distal small intestine
(ileum), however, maintains a more diverse microbiota and higher bacterial numbers
(108 per ml of digesta) than the upper intestine. The large intestine is a major site
of microbial colonization and is characterised by large numbers of bacteria (1010-
1011per ml of digesta) (Gaskins, 2000). In piglets weaned at 5 1/2 weeks of age, SCFA
production (µmol/ g dry matter of digesta) in the distal small intestine was only
2 and 3% of SCFA production in the caecum and proximal large intestine,
respectively (Hambrecht, 1998). Although the number of bacteria and SCFA
production indicate that only limited fermentation occurs in the small intestine,
Houdijk (1998) showed that of the fructooligosaccharides (FOS) added to a weaner
diet at a level of 40 g / kg feed more than 90% was degraded pre-caecally. This
observation indicates that fermentation takes place in the small intestine. Thus, it
is feasible that the observed effects of soluble fibres on small intestinal integrity
are mediated by SCFA.
Non-digestible oligosaccharides (NDO) resist the hydrolysis by the alimentary

enzymes. The pH of the ileal digesta decreased after addition to the diet of 4%
FOS when compared to a negative control. An effect on pH was not detected with
1% FOS or either 1 or 4% transgalacto oligosaccharide in the diet. Short chain fatty
acid production and number of bacteria in the ileal digesta did not differ between
piglets fed diets with or without dietary oligosaccharides (Houdijk, 1998). The
inclusion in the diet of 0.2% transgalactosylated oligosaccharide, 0.2%
glucooligosaccharide, 0.2% lactitol (Gabert et al., 1995), 0.5% galactosyl lactose
(Mathew et al., 1997), either 1 or 2% sucrose thermal oligosaccharide caramel
(Orban et al., 1996) and 0.1% mannooligosaccharide (Kim et al., 2000) had no
effect on the composition and activity of the microflora, the pH and the
concentrations of SCFA and NH3 in the small intestinal digesta of weaned piglets.
The incidence of diarrhoea was not affected either. It follows that NDO’s have no
effect on small intestinal integrity in contrast to soluble fibres. The lack of effect
of NDO consumption on SCFA concentration in the digesta may be explained by
rapid absorption of SCFA. It could be suggested that soluble fibres not only act
through generation of SCFA.
Fibres and SCFA have accessory effects in relation to the small intestine. The inclusion
of fibre in orally or intravenously supplied TPN prevented bacterial translocation
180 Weaning the pig

to the mesenteric lymph nodes even in the absence of oral nutrients (Spaeth et al.,
1990). Dietary soluble fibre may enhance the faecal excretion of bile acids and render
them unavailable for the formation of intra-luminal micelles so that fat and
cholesterol absorption be reduced (Roberfroid, 1993). SCFAs are avidly absorbed
and at the same time stimulate colonic sodium and water absorption, thereby acting
as anti-diarrhoeal agents (Silk, 1989; Scheppach et al., 1990). SCFAs, especially
butyric acid, are preferred energy sources for colonocytes (Roediger, 1982).
8.3.3.5 Probiotics and lactic acid
It is reasonable to suggest that dietary measures which enhance colonisation

resistance and / or translocation resistance against enteropathogenic E. coli will have
a positive effect on the performance of weanling piglets. Colonisation and
translocation resitance may be influenced by the feeding of antibiotics, probiotics,
prebiotics and / or other ingredients that affect microbial ecology of the small
intestine. In weanling piglets, antibiotics may be used therapeutically, but in the
European Union most antibiotics have been banned for preventive use. In the
weanling pig, the effect of feeding probiotics, i.e. live microorganisms with
beneficial activity on the host, has been studied. The feeding of either 106 or 107
viable spores of B. licheniformis or 106 viable spores of B. toyoi when compared to
a negative control improved growth performance in piglets with 31, 99, or 28 %
respectively from 0 to 28 days postweaning (Kyriakis et al., 1999). However, the
extremely high morbidity and mortality in the negative control group may caused
the lower growth performance in the negative control group. Mortality was 44%
in the negative control and on average 20% in the probiotic treated groups. The
administration of commercial preparations of probiotics to weanling piglets
either showed no effect (Jost and Bracher-Jakob, 1998), or increased growth
performance by 4% when compared to a negative control (Inamoto and Waltanabe,
1998).
Prebiotics such as fructooligosaccharides have been shown to specifically stimulate

the growth of lactobacilli and bifidobacteria in the intestine, but as mentioned
previously there is no evidence that these probiotics influence gut integrity in
weanling piglets. Lactobacilli produce lactic acid, which is known to have
antibacterial activity. In weanling piglets dietary lactic acid concentrations of 0.8-
2.4% have been shown to stimulate feed intake and growth (Roth et al., 1993;
Smolders et al., 2000). Likewise, the feeding of fermented feed, which is rich in
lactic acid, also stimulated growth in weanling piglets (Jensen and Mikkeelsen, 1998;
Scholten, 2001) and increased villus height (Scholten, 2001). Thus probiotics, lactic
acid and fermented feed might be beneficial to weanling piglets, but it is not known
whether there is a direct effect on gut integrity or that these compounds act through
enhanced feed intake.

8.3.3.6 Growth factors
Growth factors, especially epidermal growth factor (EGF) and insulin-like growth
factors I and II (IGF-I and IGF-II), are present in the colostrum and milk of the
sow. The concentration of EGF per ml colostrum or milk is 1.5 µ and 0.15 - 0.25
µg, respectively (Xu, 1996). The concentration of IGF-I per ml colostrum or milk
is 0.07 - 0.35 µg and 0.004 - 0.014 µg, respectively (Xu, 1996). The growth factors
stimulate growth, maturation and / or functional development of the intestinal
tract (Kelly, 1994; Xu, 1996; Odle et al., 1996). Epidermal growth factor is a trophic
peptide for the gastrointestinal mucosa and acts both from the lumen and the blood.
Playford and colleagues (1993) showed that luminally-supplied EGF is rapidly
hydrolysed by proteases in the small intestine of human subjects while in the fasting
state. Hydrolysis was blocked by the presence of casein or a soybean trypsin inhibitor.
It was hypothesised that EGF is digested by pancreatic enzymes in the fasting state,
but is preserved when food proteins act as competitive substrates and / or block
the active sites of these enzymes (Playford et al., 1993). Oral supplementation of
372 µg/day EGF, but not 124 µg/day, to weanling piglets partly counteracted the
weaning-induce decrease in lactase specific activity. Small intestinal sucrase specific
activity was increased at day 3 after weaning by a supplementation with the high
dose of EGF. However, supplementation of EGF did not affect on the mucosal protein
content and the villus : crypt ratio in the small intestine (Jaeger et al., 1990). Zijlstra
and colleagues (1994) examined the effects of EGF given with a milk replacer (0,
500, or 1000 µg/l) on the recovery of piglets that were infected at 4 days of age
with rotavirus enteritis. EGF increased villus length and lactase specific activity in
a dose-dependent fashion. At the dose of 500 µg/l, effects were seen only in the
proximal portion of the small intestine, whereas with the higher EGF level there
also were effects further down the tract (Zijlstra et al., 1994). Houle and colleagues
(1997) looked at the effect of oral IGF-I administration (500 µg/l milk replacer)
in neonatal piglets until 7 and 14 days postpartum. Circulating concentrations of
IGF-I did not change and growth, organ weights, mucosal RNA, mucosal DNA and
mucosal protein content were not affected. Mean villus height in the proximal ileum
tended to be higher and that in the terminal ileum was significantly higher in IGF-
I-treated piglets. In other regions of the intestine, no effect of IGF-I on villus
architecture was detected. By day 14 after birth, sucrase and lactase specific activities
were increased throughout the jejunum and ileum in IGF-I-treated piglets. On day
7, enzyme specific activity was not affected by IGF-I administration (Houle et al.,
1997). The addition of IGF-I to sow’s milk so as to double the concentration of
that present in sows’ colostrum was found to increase the length of the tight junctions
by 23% in 36-hour old piglets. However, sows’ milk with a IGF-I concentration
similar to that in sows’ colostrum did not affect tight junction structure. Thus at
high intake levels IGF-I can modulate the tight junction structure and thereby
influence intestinal permeability (Zarrinkalam et al., 1999). In rabbits intestinal
transport of electrolytes and nutrients was measured with Ussing chambres. EGF
182 Weaning the pig

supplementation to the perfusate up-regulated intestinal transport (Opleta-Madsen

et al., 1991).
In may be concluded that dietary supplementation of IGF-I and EGF has only limited
effects on body or organ weight. Within the intestine, IGF-I and EGF increased
sucrase and lactase activities without significantly increasing intestinal weight, length,
villus architecture, protein or DNA content. Thus, IGF-I and EGF may regulate
disaccharidase activities through modifying the function or differentiation of
individual enterocytes. The action of orally administered IGF-I and EGF seems to
be limited to the intestine without exerting systemic effects. So far the role of growth
factors on intestinal development has been studied in neonatal and not in
weanling piglets. Applications might be restricted to prophylactic administration
of growth factors to enhance recovery from gastrointestinal trauma.
8.3.3.7 Polyamines
Polyamines are characterised by multiple NH2 groups in the molecule,

representatives being putrescine, spermidine and spermine (Halász and Baráth,
1998). Polyamines have been shown to play a role in regulating growth of the
gastrointestinal mucosa and also post-natal maturation, turnover of intestinal
mucosa, binding of the vitamin D receptor to DNA, postprandial intestinal
motility, transport of D-glucose and mucosal hyperplasia during lactation (Johnson
and McCormack, 1994; Blachier, 1997; Halász and Baráth, 1998). Polyamines are
present in sow milk (Kelly et al., 1991c). For the biosynthesis of the polyamines
in animal tissue the precursors ornithine, which is not found in proteins but is
synthesised from arginine, or L-methionine, are required (McCormack and
Johnson, 1991). Polyamines are synthesised from L-arginine in absorptive cells,
secreted by exocrine pancreas and provided by extruded enterocytes at the top of
villi (Blachier, 1997). Polyamines are also produced by intestinal flora (Blachier,
1997). Wu and colleagues (2000a) showed that intestinal polyamine synthesis is
enhanced after weaning of piglets at 21 days of age. Grant and colleagues (1990)
studied the effect of polyamine supplementation to a liquid milk replacer fed to
piglets weaned at 2 d of age. An all-milk-protein milk replacer was compared with
the same milk replacer in which 20% of the protein was replaced with soy protein
isolate without or with 25 g/l of either putriscine dihydrochloride or ethylamine
hydrochloride. Daily gain, villus height and the kinetics of xylose absorption did
not differ between dietary treatments. Crypt depth tended to be lowest in the milk-
soy diet without polyamines, but mitotic index was altered. Specific and total
activities of sucrase in the brush border were highest for the piglets fed the all-milk
diet. Specific activity of cytosolic dipeptidase was lowest for piglets fed the milk
replacer with putrescine. Total dipeptidase activity was lower in piglets fed the diets
with putrescine or ethulamine when compared to the milk diet. Grant and colleagues
(1989) applied the same dietary treatments to 3-day old preruminant calves as well.

The plasma xylose concentration was highest in calves receiving the milk diet.
Enterocyte proliferation was decreased in calves fed the soy-milk diet without added
polyamines when compared to the other diets. Thus supplementation of the milk-
soy protein diet with either putrescine or ethylamine enhanced enterocyte
proliferation. Villus architecture was not affected by any dietary treatment (Grant
et al., 1989). Oral daily supplementation of rats with 6 µmol spermine or 10 µ
mol spermidine in rats increased sucrase and maltase specific activity and decreased
lactase specific activity. Ileal villus enterocytes were maturer in either spermine or
spermidine treated rats, when compared to control animals, as based on changes
in enterocytes structure and dissacharase activities (Dufour et al., 1988). Osman
and colleagues (1998) investigated the effect of spermine on intestinal permeability
in rats by Ussing diffusion chambers. High spermine concentrations (10-50 mM)
enhanced transcellular permeability, whereas low concentrations (0.5-1 mM) either
had no effect or produced a decrease. Thus, spermine concentration has no
straightforward action on epithelial barrier function. It is clear that administration
of polyamines to rats induces intestinal maturation and increases proliferation. We
are not aware of any studies on polyamine supplementation in piglets weaned at
3 weeks of age. However, polyamines added to a liquid milk replacer for either
neonatal piglets or calves, did neither affect performance nor intestinal integrity.
8.3.3.8 Nucleotides
Nucleotides are building blocks of RNA and DNA, which can be either purine or
pyrimidine nucleosides. Nucleotides may also function as energy source in cellular
metabolism, influence lipid metabolism and serve as intermediates in biosynthetic
and oxidative pathways. Nucleotides are important for immunity and gut
development and repair (Boza et al., 1992; Carver and Walker, 1995; LeLeiko and
Walsh, 1996; Nagafuchi et al., 1997). Cellular proliferation requires nucleotides
derived either from glutamine, glycine and ribosylphosphates or from reuse of
digested desquamated mucosal cells (LeLeiko et al., 1996). Bueno and colleagues
(1994) fed weanling rats diets containing either corn starch or lactose for two weeks,
followed by a 4-week period during which the corn starch diet with or without a
nucleotide mixture was given. The lactose diet was used to induce diarrhoea. Rats
that recovered from diarrhoea and received the diet with nucleotides showed
increased villus height when compared to the rats not supplemented with
nucleotides. However, rats that received the corn starch diet throughout did not
benefit from nucleotide supplementation. This observation suggests that dietary
nucleotides may improve intestinal healing after injury as induced by chronic
diarrhoea. Adjei and colleagues (1996) fed mice either a casein diet, a protein-free
diet, the protein-free diet with individual components of nucleotides / nucleosides
or the protein-free diet with a nucleotide / nucleosides mixture to investigate the
effect of diet on endotoxin-induced (E. coli O26:B6) bacterial translocation and
small intestinal injury. Compared to the protein-deficient mice, dietary
184 Weaning the pig

supplementation of a mixture of nucleotides and nucleosides or the individual

component cytidine increased villus height and reduced the incidence of bacterial
translocation. However, preventing protein malnutrition by feeding the casein diet
resulted in higher villi and less bacterial translocation than did protein-free diet
with a mixture of nucleotides and nucleosides (Adjei et al., 1996). The authors do
not know published studies on dietary supplementation with nucleotides of weaner
diets for piglets. However, in specific rodent models nucleotide supplementation
may improve intestinal recovery after chronic diarrhoea or malnutrition.
8.4 Concluding remarks

Weaning is a stressful event as indicated by an increase of plasma cortisol
concentration and behavioral changes (Worsaae and Schmidt, 1980). Plasma cortisol
concentrations were more than 2.5 times higher in weanling pigs on day 2
postweaning when compared to unweaned pigs (Wu et al., 2000a; 2000b).
Inappetance and low feed intake, lethargy, reduced activity and fever are prevalent
during many types of stress (Elsasser et al., 2000). The transition from suckling to
eating solid food is typically associated with a critical period of underfeeding
(Leibrandt et al., 1975, Okai et al., 1976, Le Dividich and Herpin, 1994). Le Dividich
and Herpin (1994) and Pluske and colleagues (1995) used various data sets and
concluded that the daily metabolisable energy (ME) intake necessary for
maintenance was not met until the fifth day after weaning. The level of preweaning
ME intake was not attained until the end of the second week following weaning.
Clearly, the weaning transition of piglets causes underfeeding.
The low feed intake after weaning and the associated decreased mucosal integrity
both negatively affect growth performance and health of the early-weaned pig. There
generally is a high incidence of diarrhoea after weaning (Nabuurs, 1991). With early
weaning being fundamental, nutritional interventions to counteract the weaning-
induced decrease in mucosal barrier function should aim at increasing feed intake
and / or the formulation of specific diet compositions. Experiments indeed
confirm that feed intake level is critically important. Low feed intake is associated
with decreased absorptive and digestive capacity as indicated by the decreased
mucosal surface area and often low total brush border enzyme activities.
Permeability of macromolecues, an indicator of small intestinal integrity, is
increased by low feed intake. In contrast to feed intake level, dietary constituents
studied thus far only have marginal effects on small intestinal integrity in the weaned
piglet. The effect of dietary constituents generally is more pronounced in
malnourished / diseased piglets when compared to apparently healthy weanling
piglets. There are potential functional ingredients to improve the mucosal integrity,
but data for weanling pigs are relatively scarce, even though the weaned piglet is
a good model for human infants (Reeds et al., 1997). Most studies on potential
functional dietary ingredients have been conducted with rodents or neonatal piglets

instead of piglets weaned at 3 weeks of age. In the nutrition of monogastric farm

animals, emphasis has been on anti-nutritional factors (Van Weerden and
Huisman, 1989) and only recently researchers have started to explore the functional
properties of certain feed contituents.
Regarding the diet of weanling piglets, research should focus on critical determinants
of feed intake immediately after weaning and functional feed ingredients to
stimulate epithelial cell proliferation and differentiation, enhance immune
function, and promote growth of beneficial bacteria. Combinations of functional
feed ingredients may be more successful than the use of single ingredients. The
cost-efficiency of the ingredients will determine their application in practice.
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198 Weaning the pig

9 Interactions between the intestinal
microflora, diet and diarrhoea, and their
influences on piglet health in the
immediate post-weaning period
D.E. Hopwood and D.J. Hampson
Summary
The piglet is subjected to many environmental, behavioural and dietary stresses
immediately after weaning, and the intestinal microenvironment of the newly
weaned pig is particularly precarious. With weaning comes a major change in diet
that requires and induces significant changes in the types and numbers of micro-
organisms residing in the gastrointestinal tract, as well as in the physiology and
functionality of the tract. Given these circumstances, it is not surprising that the
newly weaned pig is highly susceptible to enteric disease. The balance between
development of a “healthy” intestinal microflora or the establishment of bacterial
intestinal disease can be easily tipped toward disease expression (Aumaitre et al.,
1995; Nabuurs, 1995). This chapter briefly describes the basic intestinal microflora
present during the post-weaning period, specific enteric diseases that can occur at
this time, and some potential precipitating dietary factors. Particular emphasis is
placed on Escherichia coli and its involvement in the condition known as post-
weaning colibacillosis (PWC), since this is the most common cause of intestinal
disease in the newly-weaned pig. The role of dietary fibre in altering susceptibility
to PWC receives special attention.
9.1 Changes in intestinal microflora at weaning

During and shortly after birth, piglets are exposed to micro-organisms within their
immediate environment. Ingestion of the sow’s faeces at this time introduces bacteria
that colonise the gastrointestinal tract. These bacteria then localise to suitable niches
where they compete and interact, and ultimately form a relatively stable and complex
population that represents the normal intestinal microflora. Following initial
establishment, the intestinal microbiota remains relatively stable except for times
of major dietary and environmental change, such as occurs following weaning
(Radecki and Yokoyama, 1991; Conway, 1994; Jensen, 1998). Pigs generally have
a relatively large number of bacteria both in the stomach and the distal small
intestine compared to other species. Consistent with this, considerable microbial
fermentation occurs in the stomach and the small intestine, particularly in the ileum
where the rate of passage of digesta slows and bacterial numbers are high (Jensen,

Hopwood and Hampson
1998). Whilst the piglet is suckling, the dominant bacteria within the stomach and
small intestine tend to be lactobacilli and streptococci, both of which are well-
adapted to utilise substrate from the milk diet. The large intestinal microbiota that
develops shortly after birth comes to contain a large and diverse selection of mainly
obligate anaerobic bacteria, including Bacteroides, Eubacterium, Bifidobacterium,
Propionibacterium, Fusobacterium, and Clostridium species (Radecki and Yokoyama,
1991). The metabolic activity and physical presence of this complex and stable
microflora provides a “colonisation resistance”, preventing or reducing colonisation
by other more transient bacteria, including potentially pathogenic species (Nurmi
and Rantala, 1973).
Following weaning, particularly if this occurs abruptly, a brief period of starvation

and then consumption of the new solid diet results in altered availability of specific
microbial substrate at sites all along the tract. The amount and type of substrate
available at the different sites is influenced by the type and amount of food
consumed after weaning, as well as by the relative functional capacity of the pig’s
gastrointestinal tract after weaning. The process of abrupt weaning induces quite
profound changes in intestinal structure, with associated disrupted functional
capacity, and it can take several weeks for full, efficient and appropriate functionality
to be restored (Hampson, 1986; van Beers-Schreurs, 1996; Pluske et al., 1997).
Concurrently, these intestinal changes result in changes to the mass, composition
and complexity of the intestinal microflora.
Jensen (1998) quantified changes in bacterial populations that occur in the small
and large intestine of pigs following weaning at 28 days of age. In the small intestine
the previously predominant lactobacilli decreased in number during the first week
after weaning, whilst the total number of bacteria and the proportion of coliforms,
Escherichia coli in particular, increased. Immediately after weaning, most of the
cultivable bacteria from the lumen of the large intestine are Gram-negative. In the
study by Jensen (1998), microbial activity in the large intestine was not significantly
increased until 20 days after weaning, whilst in the small intestine it took only a
week for the bacterial population to establish and undergo maximum fermentation.
Following this period of perturbation to the intestinal microflora, it subsequently
re-stabilises.
For more detailed review of the porcine intestinal microflora, and traditional culture-
based and modern molecular methodology for their detection and enumeration,
the reader is referred to articles by Conway (1994), Stewart (1997), Mackie et al
(1999), Jensen (2001), Gaskins (2001), Leser et al. (2002), and Pluske et al., (2002).
Few of these studies have specifically focused on changes in the microflora of healthy
pigs immediately after weaning, because this represents a dynamic and variable
process which is difficult to monitor without using large numbers of pigs killed
sequentially to obtain intestinal samples. For example, different microflora effects
200 Weaning the pig

Interactions between intestinal microflora, diet and diarrhoea, and their influences on piglet health
may be seen in pigs weaned at different ages (Franklin et al., 2002). The main
message from this section of the chapter is that both the composition and stability
of this microflora undergo disruption in the period immediately following
weaning, thus leaving the piglet more susceptible to overgrowth with potentially
disease-causing pathogenic bacteria.
9.2 Major enteric diseases at weaning

Diseases of the gastrointestinal tract in weaner piglets generally result in diarrhoea
of one form or another. Such diseases may be associated with the colonisation and
overgrowth of bacteria, viruses or intestinal parasites, or a nutritional imbalance
causing irritation and/or increased luminal osmotic forces. Diarrhoea occurs as a
result of inflammation of the intestinal tract, or from a disruption to the absorptive
or secretory processes of cells lining the epithelium of the intestinal tract (Liebler-
Tenorio et al., 1999), as well as from disorders of intestinal motility. Diarrhoea is
manifest as an increase in the water content of the faeces, and (or) as an increased
daily passage of faeces. Diarrhoea becomes visually apparent once the faecal water
content exceeds about 80%. Diarrhoea that is caused by the activity of bacterial
enterotoxins in the small intestine is alkaline and watery (eg E. coli “secretory”
diarrhoea), whilst that associated with damage and/or loss of function of the
epithelium and its brush border tends to be acidic and bulky (eg rotavirus or
enteropathogenic E. coli “osmotic” diarrhoea). Where the seat of infection is in
the large intestine, mucus is often present in the faeces, and if there is tissue damage
then fresh blood may be present (eg swine dysentery). Bleeding from further up
the tract usually results in dark tar-like faeces (eg following gastric ulceration).
Viruses are not a major cause of diarrhoea immediately after weaning. Rotaviruses
(rotavirus diarrhoea) and Coronaviruses (transmissible gastroenteritis, porcine
epidemic diarrhoea) may proliferate in the small intestine after weaning, but are
more usually a problem in younger suckling pigs (Fu and Hampson, 1987; Will
et al., 1994). Where they do occur after weaning, they may predispose to or
exacerbate problems rather than being the initial cause of the diarrhoea (Hampson
et al., 1985; Cox et al., 1988). Swine fever can cause severe intestinal lesions and
diarrhoea, but there are also systemic manifestations, and the disease is not just
focused on newly weaned pigs. Infestation with the large intestinal parasite
Trichuris suis can result in mucoid diarrhoea, and typically results when piglets are
weaned onto a dirt floor, but this disease is not usually seen until later in the post-
weaning period. On the other hand, infection with coccidia usually occurs in the
sucking period, where it causes a white diarrhoea.
Bacteria that have been associated with diarrhoeal diseases after weaning include
Escherichia coli (post-weaning colibacillosis/post-weaning diarrhoea, oedema
disease) and Salmonella species, particularly S. enterica Serovar Typhimurium, and

Hopwood and Hampson
similar serovars (salmonellosis). Pigs usually become infected with salmonella after
consumption of contaminated protein sources, or exposure to infected faeces from
rodents or wild birds. Salmonellosis is most commonly seen in older weaner pigs,
as is infection with the intestinal spirochaetes Brachyspira hyodysenteriae (swine
dysentery: SD), and Brachyspira pilosicoli (porcine intestinal spirochaetosis: PIS),
and with the intracellular bacterium Lawsonia intracellularis (porcine proliferative
enteropathy: PPE). PPE and PIS are particularly common causes of generally mild
but chronic diarrhoea, whilst salmonellosis and SD can cause severe illness, with
dysentery (blood in the faeces), systemic signs, and sometimes death. Of all these
bacterial diseases, post-weaning colibacillosis, caused by enterotoxigenic E. coli, is
the one that is the most common and widespread in the immediate post-weaning
period, and is the main focus of this chapter.
9.3 Post-weaning colibacillosis (PWC)

Post-weaning colibacillosis (PWC) is a major cause of post-weaning morbidity and
mortality worldwide, resulting in large economic losses (Cutler, 1981; Cutler and
Gardner, 1988). The anterior small intestine is the main focus of the infection, and
is the site of the underlying fluid and electrolyte loss into the intestinal lumen,
although the bacterium is present throughout the small and large intestine. It is
common for Escherichia coli (a coliform bacteria) to appear in the faeces of pigs
in increased numbers in the first week after weaning (Mathew et al., 1993). This
can happen in both healthy and diarrhoeic pigs, although the number and
proportion of potentially pathogenic strains of E. coli in the faeces of diarrhoeic
pigs is higher (Kenworthy and Crabb, 1963; Svendsen et al 1977; Hampson et al.,
1985; Hinton et al., 1985; Gyles, 1993). Most strains of E. coli are harmless, but
those that cause diarrhoea after weaning are often distinguished by their capacity
to lyse red blood cells, and are known as beta-haemolytic E. coli. This haemolytic
activity is not considered to be a virulence factor in itself. Pigs displaying post-
weaning diarrhoea harbour massive numbers (up to 109 colony forming units [CFU]
and higher) of such haemolytic E. coli in the small intestine, whilst there is minimal
change in the populations of other bacteria in the tract (Smith and Jones, 1963).
Although digesta flows relatively quickly through the small intestine, pathogenic
E. coli possess surface structures called fimbriae, or pili, that attach to the
enterocytes lining the small intestinal villi, or to the mucus covering the villi.
Attachment prevents the bacteria from being flushed through to the large intestine,
where there would be far greater competition for survival. The most common
adhesins present in the E. coli strains causing PWC are known as K88 (or F4), and
F18 (formerly F107), both of which display several antigenic variants (Francis, 2002).
After attaching to and colonising the small intestine, haemolytic enterotoxigenic

E. coli (ETEC) provoke hypersecretory diarrhoea through the release of specific
enterotoxins. Secretion of chloride ions, sodium ions, bicarbonate ions, and water
202 Weaning the pig

into the lumen is induced by the actions of a heat labile toxin (LT) binding
irreversibly to the mucosal cells and activating the adenyl cyclase-cyclic AMP system
(Argenzio, 1992). A second heat stable toxin (ST; variants STa and STb) inhibits
the absorption of sodium and chloride ions from the lumen into the epithelial
cell via the guanyl cyclase-cyclic GMP system (Gyles, 1993). The resultant excess
volume of fluid and electrolyte in the gut lumen can be reabsorbed in the large
intestine only if it is free from disease, has a well-developed microflora, and its
physical capacity is not overloaded (Argenzio, 1992). Other less common virulence
determinants possessed by certain strains of E. coli involved in some cases of PWC
include production of the enteroaggregative E. coli heat-stable enterotoxin 1, whose
function remains uncertain (Choi et al., 2001), and the presence of the attaching
and effacing genes (Eae) encoding intimins in enteropathogenic E. coli (Higgins
et al., 1997). These outer membrane proteins are involved in attachment of the
bacteria to colonic enterocytes, preceding effacement of their microvilli and
rearrangement of the enterocyte cytoskeleton (Nataro and Kaper, 1998). Other E.
coli strains which proliferate in the intestinal tract of weaned pigs produce a
verotoxin, which is involved in the production of oedema disease, a predominantly
neurological condition sometimes accompanied by diarrhoea (Osek, 1999).
The association between excessive proliferation of haemolytic ETEC in the

intestines of weaned pigs and the development of diarrhoea was first noticed in
the 1960s, and was subsequently confirmed in many studies (Richards and Fraser,
1961; Palmer and Hulland, 1965; Hill and Kenworthy, 1970; Armstrong and Cline,
1976; Okai et al., 1976; Bertschinger and Eggenberger, 1978; Thomlinson and
Lawrence, 1981; Ball and Aherne, 1982; Hampson, 1983; Cooke, 1985). The disease
was called post-weaning colibacillosis (PWC) and is characterised by diarrhoea,
dehydration, weight loss, metabolic acidosis, changes in the hair coat and shivering
(Hampson, 1994; MacKinnon, 1998; Bertschinger, 1999). In severe cases, and in
the absence of specific treatment with antibiotics and/or electrolyte solutions, death
results.
Immunity to one strain of pathogenic E. coli does not protect from others, and
successive infections can pass through herds. No effective vaccines are currently
available to control the disease, and many strains show resistance to multiple
antibiotics (Amezcua et al., 2002). Infections usually last between 4 and 14 days,
and are spread between animals primarily by the faecal-oral route, but also by
aerosols and probably fomites (Bertschinger, 1999). Research over the years has
shown that most E. coli associated with post-weaning diarrhoea are enterotoxin
producing, haemolytic strains. Disease-inducing haemolytic E. coli are usually
restricted to a small number of serotypes, in particular O8, O9, O71, O115, O138,
O139, O141, O147, O149, O157 and NT (Hampson, 1994; MacKinnon, 1998).

Hopwood and Hampson
9.4 Factors predisposing to post-weaning

colibacillosis at weaning
9.4.1 The role of the small intestine
Although haemolytic ETEC have been identified as the primary infectious agent
in PWC, there is abundant evidence to suggest that other factors are necessary for
this disease to take hold (Madec et al., 2000). The act of weaning is an essential
precipitating factor for the development of post-weaning colibacillosis, regardless
of the age at weaning. Factors involved with the weaning process create an
environment suitable for the proliferation of ETEC and other pathogens in the small
intestine. Slower intestinal transit time and relative intestinal stasis immediately
after weaning allow bacteria the opportunity to attach to the intestinal epithelium
and time to multiply. Undigested food particles in the lumen of the small
intestine supply substrate for bacterial growth, and there is no longer any protective
passive immunity provided by sows’ milk. An inability to thermoregulate adequately
often results in cold stress, which alters intestinal motility and is thought to be an
important predisposing factor in the pathogenesis of PWC (Wathes et al., 1989).
Social stresses from mixing, fighting and crowding trigger blood cortisol release,
depressing the immune response to bacterial infection. Moving to a new pen
environment causes increased antigenic exposure to microbes residing in fresh or
dried faecal matter. The presence of other organisms such as rotavirus in the
environment increases the likelihood and severity of disease occurring (Lecce, 1983;
Tzipori et al., 1983), whilst poorer pen hygiene will also result in a greater antigenic
load, as a result of faecal-oral cycling (Madec et al., 1998).
Morphological changes and reduced functional capacity within the small intestine
associated with weaning may contribute to the development of PWC. Small
intestinal villous atrophy and a reduced ability of the small intestine to absorb water
and electrolytes at weaning are magnified when the small intestine is infected with
haemolytic E. coli, thereby contributing to more severe diarrhoea (Nabuurs, 1998).
The role of villus atrophy as a predisposing factor for PWC remains unclear, however,
a reduced ability of enterotoxigenic E. coli to colonise has been found in pigs with
experimentally-induced villus atrophy (Cox et al., 1988). Lack of familiarity with
the new food source at weaning frequently results in anorexia followed by
overeating, which starves the enterocytes lining the small intestine, and then overloads
the digestive process. Overeating by individual pigs has been linked to an increased
occurrence of PWC in these animals (Hampson and Smith, 1986).
In the small intestine, E. coli fimbriae attach to glycoprotein receptors expressed

in the brush border cells lining the intestinal villi. Receptors for F4 and F18 are
not expressed in neonatal animals, but develop subsequently. Although receptors
204 Weaning the pig

for F4 and F18 are still present in adult pigs, susceptibility to ETEC infection decreases
with age (Erickson et al., 1992). Some pigs are resistant to PWC because they do
not express the receptors at all, and some have receptors that are only weakly adhesive
(Chandler et al., 1994). The presence of receptors varies between pig breeds (Baker
et al., 1997), as well between individuals within a litter. Overall, this distribution
has a strong influence on whether or not PWC will eventuate (Madec et al., 2000).
9.4.2 The role of the large intestine
There is growing evidence that the weaner pig’s immature large intestine influences
the pathogenesis of nutritional and infectious diarrhoea (Bolduan et al., 1988; van
Beers-Schreurs et al., 1992; Aumaitre et al., 1995; Hambrecht, 1998; Nabuurs, 1998;
van Beers-Schreurs et al., 1998a; van Beers-Schreurs et al., 1998b). The large intestine
is often viewed as a “salvage” organ. The populations of microbes residing there
degrade and utilise undigested food and sloughed cells, whilst the epithelial cells
reabsorb significant amounts of water and electrolytes along with volatile fatty acids
(VFA) produced from microbial fermentation.
The three-week old pig can absorb considerable water and electrolyte from its large
intestine (Hamilton and Roe, 1977), even in the face of small intestinal villous
atrophy (Argenzio et al., 1984). The capacity for intestinal resorption of water and
VFA is similar in weaned or unweaned piglets, however, the pig’s absorptive capacity
becomes greater within approximately two weeks after weaning. In the few days
after weaning, the absorption of VFA does not augment the absorption of water
(van Beers-Schreurs et al.,1998a), as it does in adult pigs (Argenzio, 1992), and
these few days are a vulnerable time for the piglet. There is evidence that the reduced
large intestinal absorption during this period may exacerbate the effects of
enterotoxins in the small intestine (Nabuurs, 1998). Some authors recommend
providing a weaning diet that results in higher VFA concentrations, especially
butyrate, in the large intestine to maximise the absorptive function of the epithelial
cells (van Beers-Schreurs et al., 1998b). This can be achieved by inclusion of fibrous
ingredients in the diet. Dietary fibre is not digested in the small intestine, but
subsequently is fermented in the large intestine to produce VFA.
9.4.3 The specific role of diet
The composition of the weaning diet has a central role in the pathogenesis of enteric
disease, as it influences intestinal morphology, digestive and absorptive ability,
intestinal motility and transit time, and selective growth of the microflora and their
resultant fermentation patterns. Whether changes in the microflora at weaning will
culminate in disease depends on the nature, number and activity of the specific
bacteria present. Expression of PWC in particular depends on the existence of a

Hopwood and Hampson
range of dietary and other predisposing factors, with a greater number of risk factors
acting in concert carrying a greater risk of disease occurring (Madec et al., 1998).
It has been known for a long time that it is possible to influence the development
of PWC by changing the composition of the weaner diet (see review by Hampson,
1987). Some highly digestible and milk-based diets have been associated with
reduced clinical evidence of post-weaning diarrhoea, although the presence of E.
coli has not always been monitored (English, 1981). Conversely, there is evidence
that diets high in dietary fibre provide some protection from this disease
(Bertschinger and Eggenberger, 1978; Bolduan et al., 1988; Aumaitre et al., 1995).
In addition, components of some feed, such as soybean, are considered harmful
in weaner pigs as they have been implicated in invoking intestinal mucosal damage
(Li et al., 1990; Li et al., 1991), and intestinal fluid accumulation (Nabuurs et al.,
1996). High levels of dietary protein have been suggested to predispose to PWC
due to their high acid-binding capacity in the stomach, which then allows ETEC
to escape the less-acidic environment of the stomach and colonise the small intestine
(Prohaszka and Baron, 1980). The source of dietary protein used in feed
formulation also has received some attention with regard to PWC. Diets containing
complex or large number of protein sources may increase severity of diarrhoea
compared to diets with few sources of protein (Okai et al., 1976; Ball and Aherne,
1982; Etheridge et al., 1984). Excess protein within the intestines is degraded by
microbes, and may contribute to a proteolytic diarrhoea irrespective of E. coli
presence, producing harmful amine by-products which irritate the mucosa and
induce diarrhoea (Nollet et al., 1999). Plasma protein, however, is popular in some
countries, particularly the US, as a spray-on additive for weaner feeds, and has shown
to markedly improve the growth performance and robustness of pigs after weaning
(Ermer et al., 1994).
9.4.4 The specific role of dietary non-starch polysaccharides in PWC
As previously mentioned, dietary fibre has been shown to influence intestinal

physiology and the microflora in weaner pigs. Recently we have been investigating
the influence of the type and level of dietary fibre on the expression of PWC
(McDonald et al., 2000; McDonald, 2001; McDonald et al., 2001; Hopwood et al.,
2002), and some concepts arising from this work are presented here.
In this work, newly-weaned pigs were offered diets containing different levels of
dietary fibre in the form of non-starch polysaccharide (NSP). Pigs fed these diets
were either monitored for the development of natural infection with PWC, or
experimentally infected with a pathogenic haemolytic ETEC strain. In these
experiments a highly digestible diet, the main ingredient of which was cooked white
rice, was used as a control diet because it is very low in dietary NSP (less than 1%
of the diet). In the other test diets, sources of NSP replaced the cooked rice
206 Weaning the pig

component so that the chosen NSP source comprised the major carbohydrate source
in these diets (greater than 50% inclusion). The protein and energy contents of
the different test diets remained essentially unchanged. The foods providing the
sources of NSP were selected according to the type of NSP they contained. They
were comprised of the following: mixed, approximately equal amounts of low
viscosity soluble (easily fermented) and insoluble (slow to ferment) NSP (hammer-
milled wheat and extruded wheat diets), primarily soluble NSP of a moderate
viscosity (pearl barley diets), and a highly viscous soluble synthetic NSP that resists
large intestinal fermentation (carboxymethylcellulose diet: CMC). As added
variables, a diet based on a hydrolysed form of rice was also offered to pigs as a
comparison with the control cooked white rice diet, and exogenous digestive
enzymes were added to the pearl barley diet to determine whether they could reverse
any effects induced by the presence of soluble NSP.
For all experiments, Large White x Landrace pigs from a specific pathogen free piggery
were weaned at 21 days of age and transported to a research facility, where they
were allocated to an experimental diet in a manner that ensured the average pig
weight was the same for all experimental groups. From the day of weaning until
the end of each experiment, faecal swabs were collected and cultured daily for the
presence of haemolytic ETEC. An estimate of the proportion of faecal ETEC that
grew from these swabs was recorded. Pigs that became naturally infected with PWC
harboured ETEC of serotype O149;K91;K88 (enterotoxins LT, STa, STb). Where
experimental infection was carried out, pigs were orally inoculated 48-72 hours
post-weaning with 5-50mls of a broth containing an average of 108.5 haemolytic
ETEC/ml of serotype O8;K88;K87 (enterotoxins LT, STb, STab) or O149;K91;K88
(enterotoxins LT, STa, STb), the latter being the same serotype cultured from the
natural infection which occurred in pigs from this source.
Pigs experimentally infected with ETEC began excreting the bacteria in their faeces
within 24 hours of inoculation, and the severe watery diarrhoea that followed soon
after was associated with a heavy, almost pure growth of haemolytic ETEC in their
faeces. Pigs that naturally developed PWC began excreting heavy growths of
haemolytic ETEC within a day of developing diarrhoea, usually 4-5 days after
weaning.
As the numbers of haemolytic ETEC cultured from faecal swabs can reflect the growth
of E. coli within the large intestine, rather than in the small intestine where they
stimulate diarrhoea (Armstrong and Cline, 1977; Sarmiento, 1988), growth from
faecal swabs was not taken as the only indication of colonisation and proliferation
of haemolytic E. coli. A more accurate method of determining the site of
proliferation was by making viable counts of the bacteria from the intestinal contents.
Counts from the small intestine of experimentally infected pigs have been reported
to range from 2.7 to 9.7 CFU/g (log 10) (Smith and Halls, 1968), and similar counts

Hopwood and Hampson
were obtained in the current series of experiments. Scrapings from the small intestinal
wall were collected from pigs killed 7-8 days post-weaning, 3-4 days after the
commencement of diarrhoea. The viable counts obtained in these experiments
allowed quantitative comparison between pigs fed different sources of NSP, and
allowed an insight into the effect of infection on intestinal development. A summary
of the viable counts of haemolytic ETEC from the mid-small intestine of all dietary
groups with PWC is shown in Figure 9.1.
The number of ETEC in the mid-small intestine and the expression of PWC increased
as the amount of soluble NSP in the feed increased. In addition, all the natural
sources of NSP that exacerbated PWC were soluble, readily fermented by intestinal
bacteria, and tended to be viscous in nature, with greater viscosity being associated
with higher ETEC numbers (Figure 9.2). The greatest proliferation of ETEC
occurred as part of a natural infection, and was precipitated by the presence in the
diet and in the intestinal digesta of the synthetic soluble viscous compound CMC.
The distinguishing features of the diet containing CMC were its high water-holding
capacity, highly viscous nature, high solubility and resistance to intestinal
8 8
Haemolytic E. coli per gram digesta (log10)
7 7
c
6 6
% sNSP in diet
5 bc 5
b b
4 4
b ab
3 3
a
2 2
1 1
0 0
Rice HR Wheat EW Barley+E Barley CMC
Figure 9.1. Viable counts of enterotoxigenic E. coli in the small intestine of pigs fed
different diets.
Effect of diet (vertical bars, P= 0.0001) on enterotoxigenic haemolytic E. coli numbers
in the mid-small intestine of pigs with experimental or naturally-occurring PWC, and
the corresponding % soluble NSP in the diet (line). Bars without the same letters
represent diets that differ significantly.
Rice = cooked rice/animal protein diet, HR = hydrolysed rice, Wheat = raw wheat diet,
EW = extruded wheat, Barley +E = pearl barley with enzyme added, Barley = pearl barley
diet, CMC cooked rice +4% carboxymethylcellulose (medium viscosity).
208 Weaning the pig

8 8
Haemolytic E. coli per gram jejunal digesta (log10)
7 7
6 6
Ileal viscosity (mPa.s)

5 5
4 4
3 3
2 2
1 1
0 0
Rice Barley+E Barley CMC
Figure 9.2. Comparison of intestinal enterotoxigenic E. coli numbers with intestinal

viscosity of weaner pigs fed diets differing in soluble NSP content.
Mean (±sem) enterotoxigenic haemolytic E. coli numbers in the mid-small intestine
(vertical bars) and the corresponding mean viscosity of small intestinal contents (line)
in groups of pigs with experimental or naturally-occurring PWC that were fed
different diets.
All diets contained cooked rice. The Barley and Barley+E (included enzyme) diets
contained 50% of the diet as barley, and CMC was added to the cooked rice diet at
4% of the diet.
fermentation. The increased intestinal proliferation of haemolytic ETEC in pigs fed

the non-fermentable, viscous CMC infers that low fermentability (which is also a
feature of consuming the cooked white rice diet) is not a protective feature per se.
Viscosity can in itself have a significant influence on the complex interaction between
intestinal microflora, diet and enteric disease. This is a concept which is well accepted
in poultry science (Choct and Annison, 1992; Langhout, 1998).
The most significant and consistent result in all PWC infection experiments was
the low level of intestinal proliferation of haemolytic ETEC in pigs fed the cooked
rice diet. Although an occasional pig had moderate numbers of the bacteria in its
intestinal tract, many of the pigs fed the cooked rice diet had minimal ETEC
colonisation. Although not fully protective, the diet seemed to reduce the impact
of the disease, and inhibit the ability of the bacteria to establish within the small
intestine. The prominent features of the cooked rice diet were its highly digestible
nature, low bulking properties, low viscosity and lack of fermentable substrates
(i.e. dietary fibre). Highly digestible diets such as this provide energy to the

Hopwood and Hampson
individual, generally reducing both the impact of disease on the body and the
duration of diarrhoea. This is the principle behind many oral rehydration solutions
used to treat diarrhoea in humans.
The cooked rice diet left little residue within the intestinal tract, and this is likely
to have inhibited the growth of small intestinal pathogens by reducing the
amount of available substrate. The piglet is unable to fully digest solid food
immediately after weaning, resulting in food residues entering the large intestine
(regardless of diet), where they undergo fermentation. This presence increases the
osmolality of intestinal contents (Etheridge et al., 1984) and contributes to an influx
of water into the lumen, potentially predisposing to diarrhoea (Etheridge et al.,
1984). The presence of NSP, or any substance with strong water-holding capacity,
is most likely to exacerbate this problem. Consistent with this principle, the cooked
rice diet would have minimised this occurrence.
The ability to significantly minimise the establishment of haemolytic ETEC was

confined to the low-fibre cooked rice diet. In the last few years, research using guinea
pigs has identified a substance in boiled rice that inhibits one of the mechanisms
by which enterotoxins induce secretory diarrhoea (Mathews et al., 1999). It is
possible that this substance contributed to the protective effect of cooked white
rice seen in the experiments described here. Unexpectedly, consumption of the
hydrolysed rice diet, which was of flour-like consistency, did not prevent the
proliferation of ETEC. This lack of a protective effect may have been the result of
the presence of an excess of easily-available starch in the small intestine, which
acted as a substrate for bacterial growth. Addition of exogenous enzymes to the
pearl barley diet also was not protective, perhaps because it increased the
digestibility of the diet, so providing excess substrate for the bacteria in a similar
way to the hydrolysed rice-based diet. Consistent with this idea of substrate in the
small intestine being important in regulating E. coli numbers, diets that are high
in insoluble NSP previously have been shown to reduce colonisation by haemolytic
E. coli (Bertschinger and Eggenberger, 1978). In this case the insoluble fibre may
physically trap substrate, preventing ETEC from gaining access to it in the small
intestine.
In addition to the abovementioned aspects of the experiments, all pigs with

experimental or natural PWC had reduced whole body growth, and had less
microbial fermentation within their large intestines than their healthy counterparts.
All infected pigs fed any of the diets containing more than 1% dietary NSP lost
weight post-inoculation. Subjectively, infected pigs eating the cooked rice diet
(containing less than 1% NSP) were more alert and had a better appetite than pigs
fed other diets, although this simply may have been a result of them remaining
healthy whilst their littermates developed diarrhoea.
210 Weaning the pig

Whether an invading pathogen will establish and proliferate in the intestinal tract
depends upon the rate of its adhesion to the intestinal wall and the ability of normal
regulatory factors to suppress the pathogen. These regulatory mechanisms include
competitive exclusion (competition for nutrients or attachment sites) and the
production of toxic metabolites that directly suppress pathogens or create adverse
environmental conditions (Hentges, 1992). There are four habitats in which the
bacteria can proliferate: the epithelial cell surface, within the mucus layer of the
intestinal crypts, in the mucus lining the epithelium, and in the lumen of the
intestines (Freter, 1974). Mucus can be beneficial or detrimental to the health of
the animal, depending on whether it is used as an attachment site or whether it
inhibits bacteria accessing the epithelial sites. The mucus layer lining the tract is
thickened by the presence of viscous substances in the digesta (such as CMC), and
increasing the amount of fibre in the diet also increases production of mucus. Not
only does this increased thickness increase the distance for nutrients to move across
prior to absorption (Blackburn and Johnson, 1981; Blackburn et al., 1984), but
also it provides an attachment site for the haemolytic E. coli that is full of degraded
nutrients required for bacterial growth. Escherichia coli have the ability to attach to
mucins, which would reduce their initial establishment time by decreasing the
distance required to access attachment sites. In fact, thicker mucus or more volume
may allow more rapid establishment because there are, in effect, more attachment
sites available. The primary bacteriostatic mechanism in the lumen of the intestines
is that of mechanical forces. Slowing of mixing will allow bacterial proliferation,
and it is feasible that both the presence of viscous and non-viscous fibre may interfere
with mixing patterns and transit times.
Interestingly, in older weaned pigs, the presence of fermentable and non-

fermentable soluble, viscous NSP also can increase and hasten the onset of shedding
of intestinal spirochaetes from the large intestine (Siba et al., 1996; Pluske et al.,
1998; Hampson et al., 2000; Hopwood et al., 2002). Similarly, the highly digestible
cooked white rice diet used in the PWC experiments described here has been the
most successful diet for reducing or preventing the expression of experimental
intestinal spirochaetal diseases (SD and PIS). These observations emphasise the
need for further study on the underlying effects of viscous NSP on facilitating
colonisation and proliferation of pathogenic enteric bacterial species in pigs.
9.5 Conclusions
Given that enteric diseases after weaning have a multifactorial origin, prevention
should be aimed at reducing the number of predisposing risk factors present
(Hampson, 1994; Madec et al., 1998; Bertschinger and Fairbrother, 1999). Three
main means of manipulating the development of enteric disease stand out as being
options that are easily implementable:

Hopwood and Hampson
1. Optimising the weaning environment (socially, thermally and hygienically),

2. Reducing the impact of weaning on the gut environment by optimising diet
(composition, form, intake or additives), and
3. Manipulating the development and stability of the intestinal microflora
through the judicial use of medication or diet (composition and specific
antibacterial additives).
In particular, diets that are easily digestible, and contain low concentrations of
soluble NSP, are recommended for use in the control PWC.
Acknowledgements
Parts of the work described in this chapter were undertaken with the financial support
of Australian Pork Limited (the former Australian Pig Research and Development
Corporation). At the time of conducting the work described, Dr Hopwood (née
McDonald) was in receipt of a postgraduate scholarship from the former
Corporation.
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Role of the large intestine in the pathogenesis of diarrhoea in weaned pigs. American Journal
of Veterinary Research 59, 696-703.
Wathes, C.M., B.G. Miller and F.J. Bourne, 1989. Cold stress and post-weaning diarrhoea in piglets
inoculated orally or by aerosol. Animal Production 49, 483-496.
Will, L.A., P.S. Paul, T.A. Proescholdt, S.N. Aktar, K.P. Flaming, B.H. Janke, J. Sacks, Y.S. Lyoo, H.T.
Hill and L.J. Hoffman, 1994. Evaluation of rotavirus infection and diarrhea in Iowa commercial
pigs based on an epidemiologic study of a population represented by diagnostic laboratory
cases. Journal of Veterinary Diagnostic Investigation 6, 416-422.
218 Weaning the pig

10 Aspects of intestinal immunity in the pig
around weaning
M.R. King, D. Kelly, P.C.H. Morel and J.R. Pluske
10.1 Introduction
Two equally important functions performed by the small intestine are the digestion
and absorption of dietary nutrients, and the defence of the body from infection
via the gastrointestinal mucosa. Some antagonism exists between these tasks, since
any increase in the digestive and absorptive area of the intestine also enlarges the
area that must be protected by the intestinal immune system. From a teleological
perspective, the intestine has sought to perform its functions by providing a physical
barrier to most luminal antigens while areas which specialise in sampling of antigen
enable controlled induction of immune responses, and by providing a vast area
for nutrient absorption which necessitates an equally vast immune system to
effectively protect it from infection. The intestinal immune system is constantly
exposed to a barrage of antigenic material, ranging from dangerous antigens
associated with pathogenic bacteria and viruses to harmless antigens present in a
normal diet. This has led to the development of a sophisticated system enabling
the induction of active immune responses against harmful antigens and tolerance
towards those that are innocuous.
Because the pig is born with an immature gastrointestinal immune system, the early
postnatal period is of particular developmental significance. The modern practice
of abrupt weaning at an early age is highly unnatural for the piglet, which would,
under normal circumstances, be gradually weaned at a much greater age and level
of developmental maturity. Modern weaning practices abruptly remove the passive
protection of maternal milk-derived immunoglobulins and other protective
immune factors exposing the piglet to a plethora of novel dietary and environmental
antigens. Along with these changes, the piglet is required to rapidly adapt to
differences in diet presentation and composition, and social environment, while
maintaining a high level of growth and productive efficiency. Given theses
psychological and physiological hurdles, the weaning period is, unsurprisingly, often
accompanied by poor performance. Weaning is also accompanied by significant
alterations in intestinal immunity (Vega-López et al., 1995; McCracken et al., 1999;
Pluske et al., 1999; Solano-Aguilar et al., 2001) and intestinal immune responses,
in particular inflammatory responses directed against dietary and bacterial antigens,
which have been implicated in the pathogenesis of the post-weaning ‘growth check’
(Li et al., 1990; Pluske et al., 1997).

King, Kelly, Morel and Pluske
10.2 Overview of immune systems

10.2.1 Active immunity
10.2.1.1 Innate immunity
During their evolutionary development, vertebrates and invertebrates were subjected

to selection pressure conveyed by infectious pathogens, which resulted in the early
development of the non-specific, or innate immune system (Mushegian and
Medzhitov, 2001). Functioning independent to prior exposure to bacterial
pathogens, innate immunity can respond to bacterial invasion extremely quickly,
and may be considered the ‘first line of defence’ against bacterial infection. The
predominant leukocytes that mediate the actions of the innate immune system are
natural killer cells, mast cells, macrophages and neutrophils, which are derived from
the myeloid descendants of the hematopoietic stem cells that reside in bone marrow.
Constituting approximately 50% of the leukocytes found in blood, neutrophils are
considered the most active of the cells involved in innate responses, and circulate
constantly in the blood.
In the gut, epithelial cells provide the first point of contact for both bacterial and
dietary antigens. These cells play a pivotal role in initiating inflammatory immune
responses by secreting chemokines and cytokines that promote the activation and
recruitment of myelolymphoid effector cells to sites of infection or damage. An
important feature of the epithelial cell is its ability to discriminate between harmful
and innocuous antigens; with respect to antigens associated with gut bacteria, various
receptor recognition systems expressed on apical and basolateral surfaces fulfil this
function. An important receptor class in bacterial recognition is the toll-like receptor
(TLR) (Cario et al. 2000); these receptors recognise pathogen-associated molecule
patterns (PAMPS) such as gram negative lipopolysaccharide and gram positive
peptidoglycan and trigger downstream signalling cascades that activate epithelial
transcription factors which drive inflammatory gene expression. Gene products
including IL-8 and MIP-2α are chemotactic for neutrophils and macrophages
(McCormick et al. 1993; Hang et al. 1999). Epithelial cells also produce anti-
microbial peptides referred to as beta-defensins, an important constituent of the
innate immune system, that kill bacteria thus limiting their translocation across
the epithelial barrier during infection and invasion (O’Neil et al. 1999).
Intestinal inflammation leads to expression of adhesion molecules on endothelial

cells lining the tissue capillaries, to which blood-borne neutrophils bind by virtue
of complimentary cell-surface receptors that they express (Osborne, 1990; Butcher,
1991). Bound neutrophils infiltrate the tissue via the capillary wall by a process
known as diapedesis, which allows the cell to fit through a pore much smaller than
its size. After entering the infected tissue, neutrophils also recognise PAMPs via
220 Weaning the pig

Aspects of intestinal immunity in the pig around weaning
specific cell-surface pattern recognition receptors including TLRs (Kelly and King,
2001). Neutrophils migrate towards the source of these antigens by a process known
as ‘chemotaxis’ and non-specifically engulf the invading bacteria. Recognition of
bacterial antigens activates the neutrophil, resulting in an ‘effector’ phase
characterised by activation of the complement system, and secretion of inflammatory
agents such as such as chemokines and cytokines including interleukin (IL) -1, IL-
6, interferon (IFN) -γ, tumor necrosis factor (TNF) -α and reactive oxygen
metabolites, all of which have direct or indirect anti-bacterial actions (Sandborg
and Smolen, 1998; Zhang et al., 2000; Morein and Hu, 2001). However although
present in low numbers at birth, blood-borne neutrophils do not reach adult levels
until 21 days after weaning (McCauley and Hartmann, 1984), also the chemotactic
mechanism of neutrophils (and macrophages) is reported to be impaired in young
pigs, and the complement system may not reach adult concentrations until 4 weeks
of age (Stokes et al., 1992).
Another component of the innate immune system is the mast cell. Mast cells are
present in the lamina propria of the intestine and respond to antigen and non-
antigen-dependent stimulation, releasing a broad range of bioactive mediators which
serve to recruit further leukocytes such as neutrophils, and promote the development
of the intestinal inflammatory response (Befus et al., 1988; Malaviya and Abraham,
2001; Yu and Perdue, 2001). Mast cells are of particular importance in the
pathogenesis of allergic reactions, in which they play a central role (Befus et al.,
1988; Malaviya and Abraham, 2001; Yu and Perdue, 2001).
In addition to the innate immune system, which provides a generic response to

repeated bacterial invasion, there exists the adaptive immune system, providing
what is known as ‘acquired’ immunity. This comprises two arms of the immune
system, which are primed by initial exposure to antigens, allowing an antigen-specific
immune response that provides long-term immunity. These immune systems are
functionally distinct, and their activation is dependent on the nature of the antigen
involved. In the case of viral infection, in which a mammalian ‘host cell’ and its
machinery is exploited to enable viral replication, the infected cell must be destroyed
in order to eliminate the viral pathogen. These actions are performed by the cellular
arm of the immune system. In the case of bacteria, which replicate independently
in most environments, such cytotoxic responses alone are largely ineffectual and
the antibody-mediated response of the ‘humoral’ arm of the immune system is
engendered. These systems will now be discussed.
10.2.1.2 Adaptive immunity
Humoral immunity
Activation of the adaptive immune response begins with the processing and
presentation of intracellular antigens to either the humoral or cellular arm of the

immune system. In the case of humoral immunity, bacterial or other soluble antigens
are taken up by specialised antigen-presenting cells (APCs) such as tissue
macrophages and dendritic cells (Kagnoff, 1987), which use proteolytic enzymes
to degrade (process) the antigen into immunogenic peptides. These peptides are
presented on the surface of the APC, associated with specialised antigen-receptor
molecules referred to as major histocompatibility complex (MHC) class II
molecules. The MHC class II-antigen complex is subsequently recognised by antigen-
specific helper T cells. T cells are commonly identified by specific ‘cluster of
differentiation’ (CD) molecules which are expressed on their cell surfaces - in the
case of helper T cells this is CD4, and on this basis helper T cells are often referred
to as CD4+ T cells. Antigen recognition by helper T cells causes them to secrete
specific lymphokines. These lymphokines stimulate antigen-specific B cells to
undergo clonal expansion (multiplication) and differentiation, producing large
numbers of antibody-secreting plasma cells (Gaskins and Kelley, 1995). The
immunoglobulins (antibodies) secreted by plasma cells recognise and bind
specific antigens associated with the pathogenic agent that initiated the immune
response, and effect removal of the agent through such processes as opsonisation
and complement-mediated direct cytotoxicity (Gaskins and Kelley, 1995). The
humoral immune system therefore provides a potent, antigen-specific response to
extracellular infection.
Cellular immunity
Viral infection, which subverts the cellular machinery of host cells to enable viral
replication, necessitates the destruction of the infected cell, using the cytotoxic actions
of the so-called ‘cellular’ immune response. Most somatic cells are susceptible to
viral infection, and most are therefore also able to process and present viral antigen
to the cellular arm of the immune system. The process of antigen presentation begins
with the intracellular processing of a subset of viral antigens into immunogenic
peptides, which are then presented on the cell surface as MHC class I-antigen
complexes (Jackson and Peterson, 1993). In contrast to the humoral immune system,
the cellular immune system employs MHC class I molecules in antigen presentation,
which mediate recognition of antigen by antigen-specific cytotoxic T lymphocytes.
Cytotoxic T lymphocytes express the CD8 surface molecule, and are therefore often
referred to as CD8+ T cells. Recognition of the antigen-MHC class I complex ‘activates’
the cytotoxic T lymphocyte, causing it to multiply by clonal expansion, and to
synthesise and secrete bioactive factors that destroy the infected cell (Gaskins and
Kelley, 1995). As in the case of humoral B lymphocytes, once activated, the cytotoxic
action of the T cell is antigen-specific, meaning it will only kill cells expressing the
stimulating antigen in conjunction with the same MHC class I molecules involved
in induction of the immune response (Kagnoff, 1987). The cell-mediated immune
response therefore specifically targets and destroys only the infected cells that are
the source of viral replication, effectively removing the intracellular pathogenic threat
while leaving healthy cells unperturbed.
222 Weaning the pig

10.2.2 Passive immunity
The use of preformed antibodies derived from an individual to provide temporary

protection against infection in another individual, is termed ‘passive’ immunity.
The acquisition of passive immunity is crucial to the survival of the neonatal pig
for several reasons. First, the epitheliochorial placentation of the pig foetus
prevents the transfer of maternal antibodies during gestation (Sterzl and Silverstein,
1967) resulting in a pig that is agammaglobulinemic at birth (Salmon, 1984).
Second, although the cellular components of the immune system are qualitatively
represented at birth (Binns, 1973), they are quantitatively and functionally
immature (Stokes and Bourne, 1989; Stokes et al., 1992). The acquisition of passive
immunity therefore provides crucial protection from pathogens while the cellular
components of the immune system mature.
Passive immunity is provided by maternal immunoglobulins, which are selectively

concentrated in the mammary gland towards the end of gestation and absorbed
intact across the ‘open’ small intestine of the neonatal pig upon the initiation of
suckling (Holland, 1990). The open gut of the piglet can endocytose macromolecules
such as immunoglobulins in massive quantities within the first forty-eight hours
after birth, resulting in serum antibody titres similar to those of sow (Holland, 1990),
and a spectrum of antibodies indistinguishable from that of the sow (Bourne, 1977).
The absorbed antibodies circulate in the serum, providing short-term passive systemic
protection from infectious agents. However, the passively acquired antibody
repertoire of the neonate is necessarily restricted to those antigens to which the
sow has been exposed, and developed memory B cells (Porter, 1986). The
predominant immunoglobulin isotype in colostrum reflects that of the serum from
which it is derived - immunoglobulin-G (IgG) (Jensen and Pedersen, 1979; Butler
and Brown, 1994). Immunoglobulins A (IgA) and M (IgM) are present in
colostrum in much smaller concentrations than IgG (Jensen and Pedersen, 1979;
Butler and Brown, 1994), and are derived from both serum and local synthesis
within the mammary gland (Bourne and Curtis, 1973).
The macromolecular endocytosis of the open gut is non-selective, and its gradual
cessation (referred to as ‘gut closure’) is complete by 48 hours after birth (Murata
and Namioka, 1977; Weström et al., 1984). This prevents further large-scale
absorption of immunoglobulins, but has the benefit of also preventing further
absorption of macromolecules that might be antigenic or pathogenic in nature.
After colostrum formation, established lactation proceeds and the character of
immunoglobulins present in mammary secretions changes, reflecting a change in
the site of their synthesis with most immunoglobulins in milk derived from local
synthesis within the mammary gland (Stokes et al. 1992; Salmon, 1999). This is
associated with a decrease in total immunoglobulin concentration in milk, and
an alteration in the relative concentration of milk immunoglobulins, with IgA

predominating (Jensen and Pedersen, 1979; Stokes et al., 1992; Butler and Brown,
1994; Salmon, 1999). These changes coincide with gut closure, and mark a change
in the major function of maternally-derived immunoglobulin for the piglet.
Prior to gut closure, a secondary function of unabsorbed maternal immunoglobulin

is the provision of local passive protection against the many pathogenic agents
encountered at the intestinal mucosa; after gut closure this becomes the predominant
function of maternal immunoglobulins. However, IgG antibodies are relatively
ineffective at mucosal surfaces (Gaskins and Kelley, 1995; Gaskins, 1998), whereas
IgA is largely resistant to the action of digestive and bacterial proteolytic enzymes
and binds to mucous components (Kerr, 1990) where it functions largely to bind
antigens, prevent bacterial and viral colonisation and invasion at mucosal surfaces,
and neutralise bacterial enterotoxins (Porter, 1986; Kagnoff, 1993; Salmon, 1999).
Although a minor component of the immunoglobulins present in colostrum and
milk, maternal IgM antibodies nonetheless bolster local passive protection by virtue
of a lower adherence to the mucous lining of epithelial surfaces, making IgM
particularly suitable for opsonizing pathogens in the gut lumen (Salmon, 1999).
As with passive systemic immunity, the protection afforded by passive local

immunity only extends to antigens to which the sow has been exposed and
developed active immunity. Other protective factors present in milk and colostrum,
such as lactoferrin and lactoperoxidase, perform non-specific antimicrobial
functions, however a discussion of these factors falls outside of the scope of this
review, and the reader is directed to recent reviews of the topic (Chierici, 2001; van
der Strate et al., 2001; van Hooijdonk et al., 2000; Wagstrom et al., 2000). Both
forms of passive immune protection extend for the entirety of the lactation period,
and their removal at weaning marks a significant breach in the immune protection
of the piglet, which will be discussed later in this review.
10.3 The intestinal immune system

The intestinal epithelium provides an extensive and complex interface between the
piglet’s immune system and its environment, which must function simultaneously
to absorb digested nutrients and provide a barrier against a vast array of ingested
antigens. The barrier is composed of the basement membrane underlying epithelial
cells, the epithelial cells themselves, the tight junctions that join adjacent cells, and
the cell glycocalyx (Kagnoff, 1987; Perdue 1999; Podolsky, 1999). In addition to
its barrier function the epithelium also functions in surveillence, communicating
information regarding the contents of the intestinal lumen to the underlying mucosal
immune system through the production of cytokines (Gaskins 1998; Perdue 1999;
Lu and Walker, 2001; Sanderson, 2001). Innate defense is provided by epithelial
goblet cells, which secrete mucin and trefoil peptides that form a visoelastic gel
which covers the mucosal surface, providing a barrier which protects the mucosa
224 Weaning the pig

from luminal bacteria and antigens (Kindon et al., 1995; Podolsky, 1999; Deplanke
and Gaskins, 2001). Trefoil peptides have also been implicated in mucosal repair
as well as prevention of injury (Babyatsky et al., 1996; Playford, 1997; Podolsky,
1999). A further innate defense mechanism is performed by epithelial Paneth cells,
which secrete antimicrobial peptides into the gut lumen, contributing to a
biochemical barrier against colonisation (Ouellette, 1999; Zhang et al., 2000). The
continual and rapid migration of epithelial cells from the crypts of Lieberkühn,
culminating in their extrusion from the villous tip into the gut lumen, removes
damaged or infected cells and also provides a mechanism for rapid epithelial
restitution after mucosal injury (Podolsky, 1999). Further protection is provided
by the intestinal immune system, which is the largest immune organ in vertebrate
species (Gaskins, 1998; Kraehenbuhl and Neutra, 1992). Approximately 25% of
the intestinal mucosa consists of lymphoid tissue (Kagnoff, 1987), which in turn
constitutes approximately 50% of the total body lymphoid tissue (James, 1993).
The gut-associated lymphoid tissue, commonly abbreviated as GALT, contains three

major lymphoid compartments consisting of (1) dispersed or non-organised cells
residing in the lamina propria and epithelium (lamina propria leukocytes and
intraepithelial T lymphocytes); (2) collections of highly organised lymphoid follicles,
such as Peyer’s patches and lymph nodes; and (3) scattered individual or small
aggregates of lymphoid follicles (Kagnoff, 1987; Gaskins, 1998). Approximately
20-30 discrete Peyer’s patches exist in the jejunum and upper ileum of the pig, which
increase only slightly in number but significantly in size and cellularity, during the
post-natal period (Pabst et al., 1988; Stokes et al., 1994). One continuous patch,
which can extend for 2.5 metres, exists in the distal ileum, but this involutes at
approximately 1 year of age (Pabst et al., 1988; Stokes et al., 1994).
Antigen transport function is performed by specialised antigen-transporting cells

known as M-cells, which are expressed in the epithelium overlying organised
lymphoid follicles such as Peyer’s patches (Neutra et al., 1980; Neutra, 1999;
Kraehenbuhl and Neutra, 2000). M-cells efficiently endocytose and transcytose
luminal antigens, bacteria and viruses, which then interact with APCs in the
underlying lymphoid follicle, which acts as an antigen ‘sampling site’ (Neutra et
al. 1980; Neutra, 1999; Kraehenbuhl and Neutra, 2000). APCs process the antigen
into immunogenic peptides, which are then presented in association with class II
MHC molecules to helper T lymphocytes. Antigen presentation causes T lymphocytes
to secrete lymphokines that induce B lymphocytes to undergo immunoglobulin
class-specific switching within the lymphoid follicle, dedicating themselves to
production of a single class of antibody. Class-switching of B-cells in Peyer’s patches
favours the IgA+ phenotype, due to unknown factors within the follicular
microenvironment (Kagnoff, 1987, 1993).

A proportion of the activated T and B lymphocytes then migrate from the Peyer’s
patch through the lymphatic system before entering the systemic circulation,
thereupon ‘homing’ to the lamina propria and intraepithelial region of the small
intestine (Kagnoff, 1987; Thiele, 1991; Gaskins and Kelley, 1995; Corthesy and
Kraehenbuhl, 1999). Upon reaching the lamina propria, activated B lymphocytes
differentiate into plasma cells, capable of secreting large quantities of IgA antibody,
a process controlled by cytokines (such as TGF-β, IL4, IL-5 and IL-6) which are
produced by helper T lymphocytes in response to reintroduction of antigen
(Corthesy and Kraehenbuhl, 1999).
The dimeric IgA produced by plasma cells in the lamina propria interacts with a
specialised receptor on the basal surface of intestinal epithelial cells, and the bound
IgA is then endocytosed and trancytosed across the cell to be released into the lumen,
retaining a cleaved portion of the receptor known as the secretory component (Solari
and Kraehenbuhl, 1985; Kerr, 1990; James, 1993). The presence of the secretory
component stabilises the structure of the antibody, known as secretory IgA, and
increases its resistance to proteolysis (Lindh, 1975; James, 1993), making it
particularly suitable for activity in the gut lumen. The main action of secretory IgA
is at the mucosal surface, where it binds antigens and prevents viral and bacterial
invasion of epithelial surfaces (Williams and Gibbons, 1972; Kagnoff, 1987, 1993;
Kraehenbuhl and Neutra, 1992). There is also evidence that secretory IgA can act
on antigens within the lamina propria, causing them to be expelled into the gut
lumen via the IgA secretory pathway described previously (Kaetzel et al., 1991;
Mazanec et al., 1993). A further feature of dimeric IgA is that it is relatively
nonphlogistic compared to other immunoglobulins, participating in neither
complement activation nor antibody-directed cytotoxic responses (Kagnoff, 1987,
1993). Since a vast number of the antigens commonly present in the gut lumen
are likely to be harmless and non-pathogenic, from a teleological perspective it is
sensible that the predominant immunoglobulin at mucosal surfaces functions
through antigen binding and exclusion rather than induction of mucosal
inflammation (Kagnoff, 1987, 1993).
In addition to professional APCs, processing and presentation of luminal antigens

to the immune system has been postulated to occur via small intestine epithelial
cells expressing class II MHC (Bland and Warren, 1986a, b; Hoyne, et al. 1993;
Kaiserlian, 1999). Although epithelial cells have been shown to display class I and
II MHC antigens (Olivier et al., 1994), their role in antigen presentation remains
contentious (Dvorak et al., 1987; Vega-López et al. 1993, 1995; Chianini et al., 2001).
226 Weaning the pig

10.3.1 Intestinal inflammation
Despite the protection afforded by the aforementioned mechanical barriers and

secretory IgA, enterocytes can transport a small proportion of luminal antigenic
material to the underlying tissues by transcytosis (Wheeler et al. 1993; Heyman,
2001). Similarly, enteric pathogens and antigenic material can invade the intestinal
epithelium and the underlying lamina propria via paracellular routes, particularly
during times of compromised mucosal integrity such as intestinal infection and
inflammation (Heyman, 2001).
The epithelial monolayer is interspersed with a heterogenous population of

intraepithelial T lymphocytes, which are predominantly cytotoxic, although so-called
double-negative T cells (which express neither the CD4+ nor CD8+ surface
antigen) are also present, particularly in the neonate (Vega-López et al., 1993, 2001).
Intraepithelial T cells, which represent around 50% of all intestinal lymphocytes
in the mature pig (Vega-López et al., 2001), are capable of mediating antibody
dependent and direct cytotoxic activity (see Stokes et al., 1994; MacDonald, 1999)
and, because of their proximity to the intestinal lumen, are ideally positioned to
potentially effect and regulate immune responses (Vega-López et al., 2001). The
function of intraepithelial T cells is not well established, although it is hypothesised
that they may maintain epithelial integrity by destroying damaged, virally infected
or parasitised epithelial cells (Kraehenbuhl and Neutra, 1992; MacDonald, 1999),
or promote epithelial growth and renewal through the production of cytokines
during active immune responses (Mowat and Viney, 1997).
The lamina propria is populated by a wide range of diffuse immune cells, such as
T lymphocytes, antibody-forming B lymphocytes and plasma cells, macrophages,
dendritic cells, mast cells, eosinophils, neutrophils, and biologically active
fibroblasts (Kagnoff, 1987; Gaskins and Kelley, 1995; Gaskins 1997). The
distribution of T cells in lamina propria of the pig appears to be distinctly
compartmentalised by 6 months of age (Vega-López et al., 1993; Olivier et al., 1994),
with cytotoxic (CD8+) T cells generally positioned in and around the epithelium,
and helper (CD4+) T cells generally situated deeper in the lamina propria. The
ontogenesis and functional significance of this distribution is yet to be established.
Antigenic material that is present in the lamina propria as a result of disruption

of the epithelial barrier is processed by lamina propria APCs such as dendritic cells
and macrophages (Stokes et al., 1992, 1996; Iwasaki and Kelsall, 1999; Haverson
et al., 2000). Antigen is then presented as immunogenic peptides in the context
of class II MHC and co-stimulatory molecules to helper T lymphocytes either in
the lamina propria or, in the case of mature dendritic cells, after the APC has migrated
to the mesenteric lymph nodes, (Haverson et al., 2000; Guermonprez et al., 2001).
Antigen recognition by helper T lymphocytes causes activation and secretion of a

range of cytokines (Murtaugh, 1994; Wood and Seow, 1996). Activated T

lymphocytes in the mesenteric lymph nodes proliferate in response to inflammatory
signals and migrate to the mucosa to interact with antigen-specific B-cells (Jenkins
et al., 2001). The cytokines released by activated T lymphocytes recruit and
activate further lymphocytes and the cellular components of the innate immune
system, such as eosinophils, neutrophils and lamina propria mast cells, which in
turn produce pro-inflammatory cytokines (such as IL-1, IL-4, IL-8, IFN-γ, TNF-α,
and granulocyte-monocyte colony stimulating factor), neurotransmitters, and other
inflammatory mediators such as complement, nitric oxide and granulocyte
proteins which perform or aid antimicrobial functions (Murtaugh, 1994; Elwood
and Garden, 1999; Miller and Sandoval, 1999; Zhang et al., 2000).
Proinflammatory cytokines and other mediators produce an array of enteropathic

effects in the mucosa: induction of matrix metalloproteinase expression in
macrophages, which destroys supporting elements in the mucosa; induction of MHC
class II expression in APCs; increased ion secretion into the gut lumen; increased
epithelial permeability; and induction of goblet cell differentiation and crypt cell
mitosis (MacDonald and Spencer, 1988; Goetzl et al., 1996; Elwood and Garden,
1999; Ferreira et al., 1990, Pender et al., 1997; MacDondald et al., 1999; Monteleone
et al., 1999). A detailed discussion of the nature of the inflammatory process in
intestinal mucosa is outside the scope of this review, and the previous explanation
represents an extreme simplification. Physiological and immunological processes
in the intestine represent a complex interaction between immune and non-immune
cells and the extracellular matrix, and pathological inflammation may result from
dysfunction of one or more of these components, resulting in a homeorhetic
response involving all constituents (see Fiocchi, 1997). Evidence of intestinal
inflammation has been observed in pigs after weaning (McCracken et al., 1999),
and this will be explored later in this review.
10.3.2 Oral tolerance
The gastrointestinal immune system is constantly sampling antigenic material from

the intestinal lumen, a large proportion of which is dietary protein. It is essential
for the gastrointestinal immune system to be able to discriminate between
antigens of dietary origin, to which immunological tolerance must be induced, and
those derived from pathogenic bacteria, against which an active immune response
must be mounted. Failure of this discriminatory system results in inappropriate
immune responses to innocuous antigens, which can take the form of allergic
reactions to dietary components. There is also evidence that a similar state of
tolerance exists with regard to harmless commensal gut bacteria (Duchmann et al.,
1995, 1996), and perturbations of this state may be crucial for the development
and maintenance of chronic intestinal inflammation (Duchmann et al., 1997).
228 Weaning the pig

The most common example of the induction of oral tolerance is the feeding of a
novel protein antigen to an animal, which results in systemic immunological
hyporesponsiveness when the animals are subsequently challenged with the same
antigen (Challacombe and Tomasi, 1980). The mechanisms by which oral
tolerance is induced are the subject of active research, and are not yet fully
understood; in particular, the specific cellular and molecular interactions which
generate mucosal tolerance, and their localisation, have yet to be fully identified,
and the mechanisms which allow the mucosal immune system to accurately
discriminate between innocuous and hazardous antigen are unclear (Bailey et al.,
2001a). For detailed discussions of current concepts of oral tolerance, the reader
is directed to recent reviews of the topic (Strobel and Mowat, 1998; Weiner, 2000;
Garside and Mowat, 2001).
Mucosal exposure to antigen from living and multiplying pathogens generally leads
to priming of the local or systemic immune system, whereas exposure to soluble
antigen most commonly results in the development of oral tolerance (Kagnoff, 1993;
Strobel and Mowat, 1998; Strobel, 2001). The current understanding of the
development of oral tolerance implicates several possible mechanisms of induction:
clonal anergy, clonal suppression or regulation, and clonal deletion (Strobel and
Mowat, 1998; Czerkinsky et al., 1999; Strobel, 2001; Bailey et al., 2001a). Apoptosis
of T lymphocytes has also been suggested as a mechanism by which mucosal
unresponsiveness may be maintained (Bu et al., 2001). It is thought that multiple
mechanisms are likely to be involved in induction and maintenance of oral tolerance,
many of which may not necessarily be mutually exclusive (Strobel and Mowat, 1998;
Weiner, 2000; Garside and Mowat, 2001; Strobel, 2001).
Antigen processing and presentation may be a central determinant of whether active

immunity or tolerance to an antigen is induced. Soluble antigens may be processed
and presented to helper T lymphocytes by APCs which express class II MHC, but
not the full range of co-stimulatory molecules (such as B7-1 (CD80) or B7-2
(CD86)) which are normally required for induction of an active immune response,
resulting in clonal anergy and oral tolerance (Strobel, 2001; Strobel and Mowat,
1998). Alternatively, the MHC class II+ APC may express a specialised inhibitory
receptor (such as cytotoxic T lymphocyte-associated antigen-4), which may be
required to induce tolerance (Bluestone, 1997; Frauwirth and Thomson, 2002),
possibly through interaction with regulatory T cells (Toms and Powrie, 2001). At
low doses of antigen, tolerance may also be induced through non-professional APCs
that express class I MHC or possibly non-classical class I restriction elements, which
present immunogenic peptides to suppressor T lymphocytes, producing a dose-
dependent induction of T lymphocyte-mediated clonal suppression (Strobel and
Mowat, 1998; Strobel, 2001).

T lymphocyte-mediated regulation or suppression of immune responses is likely

to be effected by production of transforming growth factor (TGF) -β, and other
immunosuppressive cytokines such as IL-4 and IL-10 (Khoury et al. 1992; Chen
et al., 1994; Friedman and Weiner, 1994). Interestingly, these cytokines are also
implicated in the class switching of B lymphocytes to the IgA+ phenotype (Murray
et al., 1987; Defrance et al., 1992; van Vlasselaer et al., 1992), which is compatible
with the observation that systemic tolerance and humoral secretory immune
responses can develop concurrently (Challacombe and Tomasi, 1980).
There is significant evidence that the intestinal immune system of the pig is highly
regulated, and perhaps biased in favour of the induction of mucosal tolerance rather
than active immune responses to antigen. Activation of porcine T cells in vitro has
been shown to induce secretion of the immunosuppressive lymphokines IL-4 and
IL-10, and only low levels of IL-2, which implies preferential induction of tolerance
and secretory immune responses rather than cellular immunity (Bailey et al., 1994,
1998; Whary et al., 1995). There is also some evidence that isolated pig lamina
propria lymphocytes undergo increased apoptosis in response to activation
compared to similarly isolated splenic lymphocytes (Stokes et al., 2001). Increased
susceptibility to apoptosis is consistent with the observation that lamina propria
T cells are generally in an advanced state of differentiation indicating memory or
recent activation status (Haverson et al., 1999), which may predispose T cells to
apoptosis after activation (Salmon et al., 1994). Furthermore, many of the MHC
class II+ cells in the pig lamina propria are non-professional APCs, such as
endothelial cells and eosinophils, which may induce anergy by presenting antigen
in the absence of appropriate co-stimulatory molecules (Haverson et al., 1994; Stokes
et al., 1996; Wilson et al., 1996; Haverson et al., 2000).
The induction of oral tolerance is likely to result from a complex interaction of

many immunological factors, many of which are only partially understood at
present. Failure of the mucosal immune system to develop oral tolerance towards
innocuous antigen leads to induction of an active immune response in the lamina
propria, resulting in pathological inflammation of the intestine, as described
previously. An example of this condition is gluten intolerance resulting in coeliac
disease in humans (Ferguson et al., 1984). In the pig, it has been suggested that
the induction of oral tolerance is perturbed by the process of early-weaning, resulting
in hypersensitivity reactions to dietary proteins including soy protein (Miller and
Stokes, 1994; Bailey et al., 2001a, b), which will be discussed later. Supporting this
hypothesis, weaning has been reported to be associated with reduced ease of oral
tolerance induction in mice (see Strobel, 1996).
230 Weaning the pig

10.3.3 Development of intestinal immunity
The neonatal pig may be considered essentially immunoincompetent at birth, due

to low numbers of intestinal MHC class II+ cells that are required for the
presentation of antigen, and CD4+ and CD8+ T cells, which are necessary for the
induction of active immune responses (Bianchi et al., 1992; Vega-López et al., 1995,
2001; Pabst and Rothkötter, 1999; Rothkötter et al., 1999). However T cells (which
express the characteristic CD2 surface antigen and are therefore classified as CD2+
cells) are present in the intestine, but these cells express neither the CD4 or CD8
surface antigen, and are therefore predominantly of the double-negative phenotype
CD2+CD4-CD8- (Rothkötter et al. 1991, Vega-López et al., 1995, 2001; Whary et
al., 1995). The presence of this double-negative population of T cells in pigs has
been reported elsewhere (Pescovitz et al., 1985; Saalmuller et al., 1989; Binns et
al., 1992, Vega-López et al., 1993), as has a double-positive (CD2+CD4+CD8+)
population of T cells (Whary et al. 1995; Zuckermann and Gaskins, 1996;
Zuckermann, 1999; Solano-Aguilar et al., 2001), however currently their function
is unclear. Intraepithelial T cells are present at birth, accounting for around 40%
of all intestinal T cells, and are also predominantly of the double-negative
phenotype (Chu et al. 1979; Vega-López et al., 2001). A small number of IgM+ and
IgA+ cells are present in the intestine at birth (Bianchi et al. 1992). Components
of the innate immune system are present at birth, with low numbers of macrophage
and granulocyte cells present in an even distribution throughout the villous and
crypt regions (Vega-López et al., 1995), however they may not yet be functionally
mature (Stokes et al., 1992). As previously described, jejunal and upper ileal Peyer’s
patches are present at birth in approximately the same number and positions as
adult animals, although the single continuous Peyer’s patch present in the distal
ileum involutes at around 1 year of age.
During the postnatal period the intestinal immune system undergoes extensive
change, as the pig is exposed to a plethora of environmental antigens, both injurious
and innocuous in nature. The presence of macrophages and polymorphonuclear
cells increases after birth, becoming more concentrated in the crypt rather than
villous region of the lamina propria and reaches adult levels at five weeks of age
(Vega-López et al., 1995). The number of dendritic cells likewise increases after birth
although, in contrast to macrophages, dendritic cells become prevalent in the villous
lamina propria rather than the crypt (Stokes et al., 1992). This is confirmed by the
development of MHC class II+ cells, which are about twice as abundant in the villus
compared to the crypt area of lamina propria by one week of age (although
significant numbers are still present in crypt area), and reach adult levels at 5 weeks
after birth (Vega-López et al., 1995). At present it is unclear what may be the
functional significance this apparent compartmentalisation of APCs in the lamina
propria.

The lymphocyte profile of the intestinal mucosa alters dramatically after birth, with
the number of lamina propria T lymphocytes doubling in the first four weeks after
birth (Rothkötter et al., 1991; Stokes et al., 1992). This process is driven largely by
exposure to microbial antigens, with gnotobiotic pigs displaying only minor
increases in intestinal lymphocytes despite being exposed to nutritional antigens
(Rothkötter et al., 1991, 1994, 1999; Pabst and Rothkötter, 1999). Immature lamina
propria T lymphocytes begin to differentiate into CD4+ and CD8+ subsets by the
fifth day of age, with their collective number equalling that of CD2+ T cells by 12
days of age (Rothkötter et al., 1994). However the CD4+ and CD8+ T cell subsets
display different developmental patterns, with the presence of CD4+ T cells
rapidly increasing immediately after birth, while CD8+ T cell numbers increase in
a comparatively sedate fashion in the first 5-7 weeks after birth (Rothkötter et al.,
1991; Bianchi et al., 1992; Stokes et al., 1992; Vega-López et al., 1995, 2001). By
6 months of age, lamina propria CD4+ and CD8+ T cells display distinct patterns
of localisation within the lamina propria, as previously described, and are four times
more concentrated in the villous area of the lamina propria than the crypt area
(Vega-López et al., 1993).
The number of intraepithelial T lymphocytes increases significantly with age and

exposure to microbial antigen, and intraepithelial lymphocytes represent around
50% of all intestinal lymphocytes by 5 weeks of age (Rothkötter et al., 1999; Whary
et al., 1999; Vega-López et al., 2001). Lymphocytes accumulating in the epithelium
in early life are predominantly CD2+, with significant numbers of CD8+ T cells
only detectable later in life (Vega-López et al., 1995, 2001). The number of
intraepithelial T cells remains comparatively low during the first 5 weeks of life
which, combined with the paucity of CD8+ T cells, may predispose the young pig
to enteric infection (Vega-López et al., 2001). Adult numbers of intraepithelial T
cells are not reached until around 24 weeks of age, at which time approximately
half are CD8+ T cells and half double-negative T cells, with some granular
lymphocytes also present (Vega-López et al., 2001).
B lymphocytes in the lamina propria respond to antigenic stimulation during the

post-natal period, with IgA+ plasma cells increasing rapidly in number from 6 to
28 days of age, around which time adult levels are reached (Brown and Bourne,
1976). The presence of IgM+ plasma cells is also significant, outnumbering IgA+
cells until around 4 weeks of age, after which time IgA+ cells predominate (Brown
and Bourne, 1976; Allen and Porter, 1977; Butler et al., 1981; Rothkötter et al., 1991;
Bianchi and van der Heijden, 1994; Pabst and Rothkötter, 1999). In contrast to T
cells, plasma cells are more concentrated in the crypt rather than villus area of the
lamina propria (Brown and Bourne, 1976; Rothkötter et al., 1991; Pabst and
Rothkötter, 1999).
232 Weaning the pig

Peyer’s patches undergo enlargement during the postnatal period, with their length
increasing around three times in the first 38 days after birth (Pabst et al., 1988).
The enlargement and lymphocyte composition of Peyer’s patches is at least
partially determined by environmental conditions such as disease load. Germ-free
pigs display a smaller increase in size of the ileal Peyer’s patch in the first 38 days
after birth, whereas jejunal patches showed no change (Pabst et al., 1988).
Similarly at 6 weeks of age the vast majority of lymphocytes present in Peyer’s patches
of conventional pigs are B cells, whereas in germ-free pigs, T cells predominate
(Rothkötter and Pabst, 1989; Pabst and Rothkötter, 1999).
The swift and extensive accumulation of MHC class II+ APCs and both the CD4+
and CD8+ subsets of T lymphocytes in the postnatal period indicates that the piglet
rapidly develops the potential for direct antigen recognition and subsequent
induction of active immune responses in the lamina propria of the small intestine.
However, the components of the intestinal immune system do not resemble that
of the adult pig by three weeks of age, the time when weaning usually occurs. In
particular, the ratio of CD4+ to CD8+ T cells at this time is the reverse of that which
is observed in the adult pig. In adult pigs this ratio is less than 1, whereas in younger
pigs the disparity in the relative proliferation of these T cell subsets produces a ratio
greater than 1, which could potentially influence the capacity of the piglet to regulate
normal intestinal immune responses (Miller and Stokes, 1994). Furthermore,
absolute levels of lymphocytes in the lamina propria and intraepithelial
compartments are far below adult levels at weaning, which may compromise
immunological defence against enteric infections in the intestine (Vega-López et
al., 1995, 2001). Withdrawal of the maternal supply of immunoglobulins at this
time at this time eliminates their passive immunological function in the intestinal
lumen, leaving the mucosa vulnerable to opportunistic infections such as
haemolytic E. coli and rotavirus (see van Beers-Scheurs et al., 1992; Pluske et al.,
1997). Weaning is associated with numerous other sources of stress for the young
pig, throughout which the animal must attempt to maintain homeostasis. It is
therefore unsurprising that weaning has a significant effect on intestinal immunity,
which will now be explored.
10.4 The effect of weaning on the intestinal immune

system
10.4.1 Overview of the weaning process
In modern pig production systems weaning generally occurs at 2 to 4 weeks of age.

Common characteristics of the weaning process are: separation of the sow and
piglets, ensuring immediate and complete cessation of piglet access to sow’s milk;
relocation of the piglets to a nursery facility, which is recommended to be
thoroughly cleaned and disinfected prior to piglet entry and maintained at

thermoneutral temperature; mixing of different litters of piglets in nursery pens,

which may be random or based on common liveweight or sex within a pen;
provision of a high nutrient density compound diet, which may be offered in dry
(pelleted or meal) or liquid form from easily accessed feeders; water is provided
ad libitum from specialised drinkers or water-nipples, and an electrolyte solution
may also be provided. This weaning system provides a stark contrast to that which
occurs under ‘natural’ conditions, where piglets, after a gradual decline in intake,
generally cease consumption of sow’s milk between 15 and 22 weeks of age (Jensen
and Stangel, 1992), during which time they have learned foraging behaviour to
provide nutrition to supplement and eventually replace the declining maternal
supply of nutrition.
Weaning under the majority of commercial conditions currently practiced

worldwide generally results in a ‘growth check’, which is characterised by low
voluntary feed intake, poor weight gain or weight loss and occasionally diarrhoea,
morbidity and death (see Pluske et al. 1995). The impaired growth performance
may persist for up to 14 days after weaning, with growth during this time reduced
by 25-40% compared to that observed in unweaned piglets of the same age
(Musgrave et al. 1991; Pajor et al., 1991). This phenomenon is variously attributed
to nutritional stress, due to removal of sow’s milk and provision of a novel
replacement diet; psychological stress, caused by removal of the sow, relocation
and mixing, and unfamiliarity with the nature of the weaning diet; and
environmental stress, caused by fluctuations in ambient temperature, air-borne dust,
and the presence of environmental antigens.
A further cause of the post-weaning growth check may be postulated to be that of

immunological ‘stress’. Since the immunological state of the animal is affected by
alterations in nutritional, psychological, and environmental factors (Kelley, 1980),
immunological stress may be considered to interpenetrate the effects of all of these
variables, forming a potential secondary cause of growth stasis at weaning. The
notion that immunological stress can inhibit animal growth is well established,
with pro-inflammatory cytokines such as IL-1, IL-6 and TNF-α implicated as primary
mediators of this effect, through their modulation of intermediary metabolism of
fat, protein and carbohydrate, inhibition of voluntary feed intake, stimulation of
hepatic acute-phase protein synthesis, and other physiological and behavioural
effects (Kelley et al., 1994; Johnson, 1997).
10.4.2 Alteration of intestinal morphology
The post-weaning period is usually characterised by villous atrophy and crypt

hyperplasia in the small intestine (see Kelly et al., 1992; Pluske et al., 1997). Villous
height has been shown to decrease rapidly to around 75% of pre-weaning values
within 24 hours of weaning in pigs weaned at 21 days, and this villous atrophy
234 Weaning the pig

was observed to continue, albeit at a slower rate, until 5 days after weaning (Figure
10.1; Hampson, 1986). Crypt elongation was observed to occur at a slower rate
over the first 11 days of the weaning period, indicating an increase in epithelial
cell mitosis (Hampson, 1986). Similarly, reductions in the length of microvilli have
been reported after weaning (Cera et al., 1988). After the small intestine has recovered
from the weaning process, the long thin villi that are typical of the neonate have
been remodelled into the shorter tongue or leaf-shaped villi characteristic of the
adult intestine. In more natural conditions, this transition is likely to have
occurred slowly over the course of a gradual weaning process, however the abrupt
weaning system employed in modern pig farming induces more precipitous
morphological restructuring.
a
800
700
600
500
U n w eaned
um
400
W eaned*
300
200
100
0
21 22 23 24 25 26 29 32
Age (days)
b
350
300
250
200 U n w eaned
um
150 W eaned*
100
50
0
21 22 23 24 25 26 29 32
Age (days)
Figure 10.1. Comparison of villous height (a) and crypt depth (b) at 2% along the
small intestine, between unweaned pigs and pigs weaned at 21 days of age.
* Significant difference between values for weaned vs. unweaned pigs (P<0.001) (from
Hampson, 1986).

The deleterious effects of weaning on gut architecture have been associated with
a reduction in the specific activities of brush-border enzymes such as lactase
isomaltase and sucrase, within 4 to 5 days after weaning (Hampson and Kidder,
1986; Miller et al., 1986). The combined effect of reductions in brush-border enzyme
activity and small intestinal absorptive area are likely to impair the absorptive
function of the intestine after weaning. This has been confirmed in several studies,
measuring absorption of a standard dose of D-xylose (Miller et al., 1984a, b;
Hampson and Smith 1986), alanine (Smith, 1984; Miller et al., 1986), and a solution
containing glucose and electrolytes (Nabuurs et al., 1994). However, contrary to
these results, Kelly et al. (1990, 1991a) and Pluske et al. (1996c) observed no
reduction in the ability of villi to absorb xylose after weaning. Nevertheless, decreases
in the absorptive capacity of the intestine may be a central determinant of the severity
of post-weaning growth stasis. Supporting this notion, several authors have
reported a high correlation between post-weaning growth rate and small intestine
villous height (Li et al., 1991b; Pluske et al., 1995, 1996b).
10.4.3 Activation of the intestinal immune system
Activation of the gastrointestinal immune system during weaning has been

described in various animal species, including the rat (Cummins et al., 1988a, b,
1991; Thompson et al., 1996; Masjedi et al., 1999) human (Machado et al. 1994;
Cummins and Thompson, 1997), and pig (Vega-López et al., 1995; McCracken et
al., 1999; Pluske et al., 1999; Solano-Aguilar et al., 2001).
Using values derived at weaning (day 0) as a comparison, McCracken et al. (1999)

observed that weaning in the pig at 21 days of age is associated with an increase
in jejunal lamina propria CD4+ and CD8+ T lymphocytes within 2 and 7 days after
weaning, respectively. These authors also reported increased expression of the active
form of the matrix metalloproteinase stromelysin in jejunal explants during the
initial 7 days after weaning, and a decrease in jejunal expression of MHC class I
and II mRNA (McCracken et al., 1999). Similarly, Pluske et al. (1999) observed an
increase in jejunal lamina propria CD4+ T cells within 24 hours of weaning at 21
days of age, but no change in CD8+ T cells, compared to values obtained at weaning.
In contrast to these results, Vega-López et al. (1995) reported that by 4 days after
weaning, piglets weaned at 21 days of age displayed an increase in lamina propria
T cells (CD2+) compared to unweaned control piglets, but no increase in CD4+
or CD8+ T cells, indicating that the infiltrating cells were of the CD2+CD4-CD8-
phenotype. Vega-López et al. (1995) also observed an increase in
granulocyte/macrophage cells in the crypt and villous regions of proximal small
intestine lamina propria, and an increase in MHC class II+ APCs, after weaning.
Somewhat paradoxically, despite the observed influx of immunocytes into the
236 Weaning the pig

mucosa of piglets in this study, there was no evidence of increased activation of T

cells or macrophages after weaning, as determined by IL-2 receptor expression.
Similar results to Vega-López et al. (1995) were reported by Solano-Aguilar et al.

(2001), who observed gradual changes in CD4+ and CD8+ T cells, monocytes
granulocytes and macrophages (cells expressing the SWC3 surface antigen), and
expression of the SLA-DQ surface antigen in the month after weaning at 17 days
of age. However the study of Solano-Aguilar et al. (2001) did not provide an
unweaned control for comparison, and sampling occurred somewhat erratically
due to animal and/or lymphocyte yield limitations, making discrimination
between age and weaning related changes problematic. Similarly determination
of the time-course of immunological activity in the immediate post-weaning period
(i.e. 1-7 days after weaning) is difficult due to long intervals between sampling and,
in many cases, the absence data taken at the point of weaning. In this study the
final pre-weaning sample was taken 6 days prior to weaning, and the first post-
weaning sample was taken 1 day after weaning. Since significant changes in
immunological variables, such as T lymphocytes and MHC mRNA expression, have
been observed in the first 24 hours after weaning (McCracken et al., 1999; Pluske
et al., 1999), rigorous temporal sampling is required to illustrate the dynamic
alterations in intestinal immunity in the immediate post-weaning period. However
the study of Solano-Aguilar et al. (2001) provides useful and extensive data
characterising relatively long-term alterations in mucosal lymphocyte subsets in
the first month after weaning.
Linking activation of the intestinal immune system at weaning with metabolic

inflammatory responses on a systemic level, McCracken et al. (1995) observed that
the decreasing ratio of villous height to crypt depth immediately after weaning is
accompanied by an increase in plasma concentrations of the proinflammatory
cytokine IL-1, the acute-phase protein fibrinogen, and glucagon, as well as
increased liver weight, which is associated with acute-phase responses.
Determining the causes of immune system activation at weaning has become a major
focus in the pursuit of methods to ameliorate the physiological responses of piglets
to the weaning process. In this context, two main hypotheses have emerged: (1)
that anorexia of the piglet during the weaning period compromises the integrity
of the intestine, allowing luminal antigens to penetrate the epithelial barrier initiating
an active immune response in the underlying lamina propria; and (2) that the
intestinal immune system is in an immature state at weaning, which impairs its
ability to discriminate between harmful and innocuous antigen, and to generate
appropriate active immune responses These hypotheses will now be discussed.

10.4.3.1 Compromised epithelial barrier function
Transient anorexia during the immediate post-weaning period is common in modern

pig production. Voluntary feed intake after weaning is also extremely variable; group-
housed pigs weaned at 27 days of age have been reported to take an average of
around 15 hours to start eating, although the interval between weaning and eating
varied from close to zero to around four days after weaning (Bruininx et al., 2001).
In a summary of several data sets, Le Dividich and Herpin (1994) concluded that
the intake of piglets weaned at 21 days of age does not meet the daily metabolisable
energy requirement for maintenance until the fifth day after weaning, and that the
daily metabolisable energy intake achieved by the piglet during the pre-weaning
period is not reached until two weeks after weaning.
Increasing evidence supports the notion that luminal nutrition plays a pivotal role
in determining the structure and function of the small intestine. For example,
exclusion of luminal nutrients by total parenteral nutrition in piglets results in small
intestinal villous atrophy and reduced crypt depth (Park et al., 1998; Ganessunker
et al., 1999; Burrin et al., 2000); increased jejunal and ileal lamina propria CD4+
and CD8+ T cells, ileal MHC class II mRNA expression, and jejunal goblet cell
numbers (Ganessunker et al., 1999); reduced epithelial cell mitosis (Burrin et al.,
2000); reduced specific activity of mucosal sucrase and lactase (Park et al., 1998);
and a negative protein accretion rate in the intestine (Stoll et al., 2000), compared
to piglets offered luminal nutrition. Similar studies using rats have demonstrated
that total parenteral nutrition increases epithelial permeability and bacterial
translocation across the epithelial barrier, an effect that can be prevented through
provision of luminal nutrition (Omura et al., 2000; Mosenthal et al., 2002). Similar
symptoms are observed in piglets after weaning, from which it was inferred that
the level of luminal nutrition received over the post-weaning period may play a
key role in determining the structure and function of the piglet intestine during
this time, as initially proposed by Kelly et al. (1984) and McCracken and Kelly
(1984).
The effect of feed intake on the pig intestinal mucosa has been illustrated in
numerous studies (Kelly et al., 1984, 1991a, b; McCracken and Kelly, 1984; Pluske
and Williams, 1995; Núñez et al., 1996; Pluske et al., 1996a, b, c; McCracken et
al., 1999; Spreeuwenberg et al., 2001; Verdonk et al., 2001a, b). Taken together, these
studies show that a reduction in luminal nutrition produces atrophy of the intestinal
mucosa, and that mucosal atrophy over weaning can be ameliorated by maintaining
a continuous supply of luminal nutrition during this time. Furthermore, it is
hypothesised that transient anorexia over the weaning period compromises
intestinal barrier function, allowing luminal antigens to penetrate the lamina propria,
inducing intestinal inflammation which exacerbates the adverse morphology
(McCracken et al., 1999).
238 Weaning the pig

Supporting this hypothesis, Verdonk et al. (2001a) observed an increase in

paracellular, but not transcellular, transport within 2 days of weaning at
approximately 26 days of age, which continued until at least 4 days after weaning,
when measurement was ceased. This was accompanied by the characteristic post-
weaning reduction in villous height, and increase in crypt depth. Furthermore,
Verdonk et al. (2001a) showed that piglets maintained on a low level of nutrient
intake after weaning had significantly increased paracellular, but not transcellular,
transport, and reduced villous height in the proximal small intestine, compared
to piglets maintained on a high level of nutrient intake. Similar results were reported
by Spreeuwenburg et al. (2001), who concluded that diminished enteral stimulation
and stress at weaning compromise small intestinal barrier function in pigs within
2 days of weaning at 26 days of age. Commensurate with the increase in
paracellular transport observed in this study was a numerical increase in crypt lamina
propria CD8+ T cells, which was positively correlated to both paracellular and
transcellular transport (as measured by transport of GlySar and mannitol,
respectively), and a numerical decrease in CD4+ T cells, leading to a significantly
reduced ratio of CD4+:CD8+ T cells (Table 10.1). Spreeuwenburg et al. (2001)
observed that these changes were accompanied by atrophy of intestinal villi, with
villous height and ratio of villous height to crypt depth negatively correlated with
lamina propria CD8+ T cell numbers and tending to be negatively correlated with
lamina propria CD4+ T cell numbers. Collectively, these results suggest that low
nutrient intake after weaning impairs the integrity of the tight junctions between
epithelial cells lining the small intestine, increasing paracellular permeability, and
Table 10.1. Transepithelial transport and T lymphocyte subsets in the small intestine
of pigs fed a liquid milk replacer after weaning (from Spreeuwenburg et al., 2001).
Days Trans-epithelial transport T lymphocyte subsets

post-weaning
n GlySar Mannitol n CD4+ CD8+ CD4+:CD8+
10-6 cm/s n/106 mm2 crypt lamina propria
0 12 16.6 6.6b 12 216 117 2.2a

1 12 15.6 8.1b 18 125 116 1.1c
2 12 16.8 12.2a 18 195 168 1.4bc
4 12 19.8 11.9a 18 226 167 2.0ab
SEM 152 0.88 30.7 28.9 0.26
P-value of model NS 0.01 NS NS 0.05
a,b,c
Means within a column with different superscripts are significantly different at the P-
value designated by the model. NS, non-significant (P>0.05).

potentially allowing luminal antigens into the underlying lamina propria where
an active immune response may be initiated.
Similar results were reported by McCracken et al. (1999), who observed expansion
of lamina propria CD4+ and CD8+ T cells within 2 days of weaning at 21 days of
age (Figure 10.2), which coincided with a reduction in villous height of around
65% compared to that observed at the point of weaning. This was accompanied
A A
B B
Figure 10.2. Enumeration of CD4+ (i) and CD8+ (ii) T cells in jejunal villous (A) and
crypt (B) lamina propria of pigs offered either a milk (M)- or soy (S)-based diet after
weaning.
* Values differ significantly (P<0.05) from those at Day 0; Different letters (a,b) indicate
a significant difference (P<0.05) between groups M and S (from McCracken et al., 1999).
240 Weaning the pig

by increased expression of the matrix metalloproteinase stromelysin, which

peaked at 4 days after weaning, suggesting a link between expression of inflammatory
matrix metalloproteinases and intestinal atrophy in the weaner piglet. McCracken
et al. (1999) also observed reduced expression of MHC class I mRNA in the day
after weaning, which was attributed to an effect of increased plasma cortisol levels
caused by weaning stress, as observed by Wu et al. (2000). In the study by McCracken
et al. (1999), increased expression of MHC class I mRNA, which generally occurs
during inflammatory responses, did not occur in the first 7 days after weaning,
however they suggest this may also reflect cortisol-induced inhibition of the AP-
1 family of transcription factors which activate MHC class I gene expression, since
the post-weaning cortisol surge may not decline until between 2 and 8 days after
weaning (Wu et al., 2000).
Expansion of T cell subsets in the lamina propria after weaning reported by

Spreeuwenburg et al. (2001) and McCracken et al. (1999) was also reported by Pluske
et al. (1999), who observed an increase in lamina propria CD4+ T cells within 24
hours after weaning at 28 days of age, although CD8+ T cell numbers were
unchanged compared to that observed at the point of weaning. Expansion and
activation of CD8+ T cells can indicate induction of a cellular immune response,
which promotes secretion of various proinflammatory cytokines, such as INF-γ and
TNF-α, which bolster the inflammatory response and cause injury to the gut tissue
(MacDonald, 1999). T cell activation in this manner has been shown to induce
crypt hyperplasia, villous atrophy and matrix metalloproteinases that degrade
extracellular matrix proteins (MacDonald and Spencer, 1988; Ferreira et al., 1990,
Pender et al., 1997; MacDondald et al., 1999; Monteleone, 1999). The data of
Spreeuwenburg et al. (2001), in which CD8+ and to a lesser degree CD4+ T cell
numbers were negatively correlated to intestinal villous height, implicate anorexia-
induced expansion of T cell subsets in the pathology of mucosal atrophy at weaning.
Furthermore, the observation by McCracken et al. (1999) that weaning anorexia
is associated with increased expression of matrix metalloproteinases elucidates a
mechanism through which the observed tissue remodelling could be mediated in
pigs. The decreased expression of MHC class I mRNA observed by McCracken et
al. (1999) may also suggest a reduction in presentation of viral antigens and the
associated cytotoxic T lymphocyte recognition and destruction of host cells,
resulting in an increased susceptibility to viral disease during the post-weaning
period.
10.4.3.2 Hypersensitivity to dietary antigen
Villous atrophy and crypt hyperplasia similar to that observed at weaning has been
documented in cases of human dietary allergies, such as coeliac disease (Ferguson
et al., 1984), where inappropriate active mucosal immune responses are mounted
against dietary antigens. Immune responses to dietary proteins have often been

observed after weaning in the pig, where weaning onto a soy protein-based diet
has been shown to result in appearance of serum IgG antibodies specific for glycinin
and β-conglycinin, which are major storage proteins of the soybean (Wilson et al.,
1989; Li et al., 1990, 1991a, b; Dréau et al., 1994). Consumption of soy protein
containing glycinin and β-conglycinin after weaning has also been associated with
increased density of intestinal CD2+, CD4+ and CD8+ T cells (Figure 10.3) and
plasma cells (Dréau et al., 1995), as well as villous atrophy and crypt hyperplasia
(Dréau et al., 1994; Li et al., 1990, 1991a, b). This immune response has been linked
to depressed growth rate after weaning, with a significant amount of the variation
in weight gain after weaning explained by systemic immune responses to soybean
meal, as indicated by delayed-type skin hypersensitivity reactions and serum
antibodies (Li et al., 1990). In this study, weight gain after weaning was negatively
correlated with delayed-type hypersensitivity reactions to intradermal soybean
protein, which is consistent with the hypothesis that cellular immune responses
after weaning impair performance.
Immune response to dietary soybean protein appears to be most evident in younger

pigs, with antibody responses decreasing with age (Wilson et al., 1989). This suggests
that the immune system of the young pig is particularly prone to mounting
inappropriate immune responses to dietary antigen. Soy protein-induced primary
immune responses appear to be followed by immunological tolerance rather than
1400
**
1200
No. cells per mm 2
1000
800 ETSP
600 ** HTSP
*
400
200
0
CD2+ CD4+ CD8+
T lymphocyte subset
Figure 10.3. Lamina propria lymphocyte subsets of pig offered diets containing low
and high levels of conglycinin and (-conglycinin (ethanol-treated soy protein (ETSP)
and heat-treated soy protein (HTSP), respectively), for 7-9 days after weaning at 21
days of age.
*, ** Significantly different from ETSP group P<0.05 and P<0.01, respectively (from
Dréau et al., 1995).
242 Weaning the pig

priming, with pigs injected with soy protein after primary exposure displaying
minimal immune responses compared to those that are naïve to soy protein (Bailey
et al., 1993). This suggests that the primary immune mechanism controlling soybean
hypersensitivity is classical ‘oral tolerance’ (Bailey et al., 2001a), as previously
described. For more comprehensive reviews of this area of research the reader is
directed to the work of Stokes et al. (1987), Miller et al. (1994) and Bailey et al.
(2001a, b).
Exactly what immunological factors may predispose the weaner pig to development
of dietary hypersensitivity is currently unknown. However, it has been suggested
that weaning, which is associated with depression of humoral immune responses
(Blecha et al., 1983; Wattrang et al., 1998); mixing and housing changes, which
have been reported to alter parameters of immunity and immune response (Hicks
et al., 1998; Kelly et al., 2000); weaning stressors such as low temperatures or
draughts, which have been shown to influence T cell responses to non-specific
mitogens (Blecha and Kelley, 1981; Scheepens et al., 1994); and stress-induced
cortisol release, which has been observed to suppressive effect on immune
function (Westly and Kelley, 1984; Brown-Borg et al., 1993), may disturb the
development of the intestinal immune system, impairing its ability to discriminate
between harmful and innocuous antigen (Bailey et al., 2001).
Although the hypothesis that soybean hypersensitivity is a common cause of growth

stasis after weaning has generally gained acceptance in pig science, evidence of
mucosal mast cell involvement in its pathogenesis has yet to be shown (Gaskins,
1997). Mucosal mast cells are an integral component of classical hypersensitivity
reactions, producing a wide array of inflammatory mediators in response to antigenic
stimulation, resulting in increased ion secretion into the gut lumen and increased
epithelial and vascular permeability (Befus et al., 1988; Malaviya and Abraham,
2001; Yu and Perdue et al., 2001). Also, dietary and non-dietary factors have been
implicated in post-weaning growth stasis of pigs offered a soy-containing diet,
implying that, if present, hypersensitivity to soy protein may be one of several factors
involved in poor performance after weaning (McCracken et al., 1995). Indeed, the
observations of McCracken et al. (1999) led them to suggest that soy-hypersensitivity
reactions at weaning may occur subsequent to inflammation induced by post-
weaning anorexia, since expansion of T cell subsets occurred immediately after
weaning regardless of whether soy or milk-based diets were consumed at this time
(Figure 10.2). Given the apparently pivotal role of feed intake on intestinal
morphology and immunity, the absence of individual feed intake measurements
in many studies reporting immunological and morphological effects of soy
hypersensitivity (Dréau et al., 1994; Li et al., 1990, 1991a, b) suggests that these
two variables are often confounded.

To minimise or alleviate post-weaning inappetence through strategies that promote

food intake is obviously an important target in pig production, however
understanding the inputs required to stimulate functional maturity of the
developing pig immune system, in relation to handling both dietary and bacterial
antigens, is equally important. In this regard, factors that promote the regulatory
systems governing tolerance, inflammation and active immunity require further
investigation.
10.5 Conclusion
The modern practice of abrupt early weaning represents a formidable challenge
for the intestinal immune system, a fact that is exemplified by the alterations in
intestinal immunity that weaning causes. However, in a multi-factorial situation
such as weaning, determination of the relative importance of different factors is
inevitably difficult, and results are likely to vary due to subtle, and perhaps
unpredictable, factors. This renders problematic the goal of establishing, with a
high degree of certitude, the predominant cause of poor and variable post-
weaning performance. Significant evidence exists supporting both the luminal
nutrition and soybean hypersensitivity hypotheses, in some cases in the same
experiment (McCracken et al., 1995; McCracken et al., 1999). This serves to
emphasise that neither hypothesis precludes the other, and both problems are likely
to significantly affect post-weaning growth performance. In the absence of
irrefutable evidence contradicting either hypothesis, it is therefore prudent to make
every effort to maintain a constant level of luminal nutrition over the weaning period,
and to defer the inclusion of soybean protein in weaner diets until a greater level
of maturity has been reached. Weaning at a greater age, and hence level of
developmental maturity, can diminish weaning-induced immune responses
(Wilson et al., 1989; Bianchi et al., 1992). Given the extensive physiological and
behavioural effects of pro-inflammatory cytokines, which hinder growth during
active immune responses (Kelley et al., 1994; Johnson, 1997; Stahly, 2001), control
of the post-weaning immune response is a valuable objective in pig production.
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11 Nutritional requirements of the weaned pig
M.D. Tokach, S.S. Dritz, R.D. Goodband and J.L. Nelssen
Summary
The challenges for feeding early-weaned pigs extend beyond diet formulation and
nutrient requirements. Recognizing that many of these challenges are interrelated
and addressing areas will lead to successful early-weaned pig feeding programs.
11.1 Introduction
The basic rules for a successful nutritional program for the weaner pig can be
summarized as follows: 1) start with as heavy a pig as possible; 2) feed as simple
of diets (low cost) as possible, and 3) focus on nursery management. In this chapter,
we will discuss these three points and their importance in designing nutrition
programs for the weaner pig. Most of the chapter will focus on nutrient requirements
and diet formulation. However, we cannot overlook the importance of initial pig
weight and age and quality of husbandry, and their influence on pig performance
and the diet formulation strategy.
11.2 Importance of pig weight and age

The optimal feeding patterns for lactating sows continue to be debated. However,
the research results in this area are clear. Restricting feed, protein, or energy intake
during any period of lactation will reduce milk production, decrease litter-
weaning weight, and impair subsequent reproductive performance (King and Martin,
1989; Koketsu et al., 1997, Koketsu and Dial, 1998; Tokach et al., 1992). With the
implementation of early weaning strategies (< 21 days), the importance of litter
weaning weight has increased. Pigs weaned at heavier weights and older ages are
simply easier to manage in the nursery and have a lower risk of developing enteric
disease (Cranwell et al., 1995; Madec et al., 1998). Other data indicate that pigs
with lighter weights at weaning are at a higher risk of death (Deen et al., 1998).
Unfortunately, management-induced energy deficiency during lactation leading to
failure to achieve potential weaning weights is a major problem on many
commercial swine farms.
In a recent experiment, we characterized the importance of weaning age on growth

performance in the first 28 d after weaning. We grouped pigs by age (12 to 15 d,
16 to 18 d, and 19 to 21 d old) and weight (light or heavy) within each age category
(Table 11.1). We found a weaning age by growth performance interaction (P < .07).
Note that the difference in average weight between the heavy and lightweight
categories was approximately 1 kg (Figure 11.1). Thus, the heavy 12 to 15-d and

Tokach, Dritz, Goodband and Nelssen
Table 11.1. Influence of weaning age (d) and weaning weight (lb) on nursery
performance. (Dritz, 2002).
Age 12 to 15 16 to 18 19 to 21 P Value
Item Wt Light Heavy Light Heavy Light Heavy SEM Weight Age Wt x Age
d 0 to 28
ADG, g 213 241 286 286 309 295 5 0.05 0.01 0.07
ADFI, g 309 331 381 395 395 409 9 0.04 0.01 0.79
Feed/gain 1.46 1.38 1.35 1.39 1.37 1.39 0.02 0.83 0.10 0.04
*Each number is the mean of 12 pens (21 pigs/pen), and pigs averaged 5.3 kg at
weaning.
7
6 L1215
H1215
5
Weig ht , k g
L1618
4
H1618
3
L1921
2
H1921
1
0
0 7 14 21 28 35 42
Days after weaning
Figure 11.1. Influence of weaning weight and age on weight difference between groups
(Dritz, 2002).
the light 16 to 18-d old categories averaged similar weights at weaning. The heavy
16 to 18-d and light 19 to 21-d old categories also averaged similar weights at
weaning.
The youngest pigs at weaning gained the least from day 0 to 42 after weaning. The
data clearly show that weaning weight is important with all ages of pigs; however,
the impact of weaning weight was not as important as weaning age. When comparing
pigs that were 16 days or older at weaning, the weight differences at weaning were
only slightly increased by day 42 after weaning. Weaning weight was also important
for pigs weaned at less than 16 days; however, age also becomes a critical factor
as pigs with heavier weaning weights within the 12 to 15 d old category were not
able to compensate for their young age. The heavy 12 to 15 day old pigs had the
same weaning weight as the light 16 to 18 day old pigs; however, they were 2 kg
lighter at day 42 after weaning. Weaning weight differences also become magnified
260 Weaning the pig

Nutritional requirements of the weaned pig
with young pigs. Note that while the light 12 to 15 d old pigs were 1 kg lighter at
weaning than the light 16 to 18 d old pigs, the difference had magnified to 4 kg
by 42 d after weaning.
Average age at weaning or lactation length calculated at weaning is based on the

date of the last recorded wean event for the sow in most record keeping systems.
In many farms where pigs are weaned multiple times per week, the heaviest pigs
in a litter are weaned before the remainder of the litter. Thus, the actual average
weaning age of the pigs will be lower than that stated on the summary report. We
have observed actual weaning age as much as 1 day younger than that reported
from average lactation length calculated from the sow wean event. Another
common practice, even on farms that have strict policies about movement of pigs
among rooms, is to hold back older lightweight pigs to wean them at an older age.
This is another phenomena that will not be highlighted in records because the
average age at weaning will be calculated based on the wean event of the sow.
Actual data from an experiment by Donavan and Dritz (2000) indicated that, on
a farm with a 21 d maximum weaning age policy, 7.8% (83/1,062) of pigs were
actually greater than the desired 21 d maximum age (Figure 11.2) and 1.4%
(15/1,062) were weaned at greater than 26 d of age. Also, note that 12%
(128/1,062) of the pigs were weaned at 15 d of age or less. Examination of 1,800
pigs from another production system in which piglets are tattooed with date of
birth indicated that 17% were greater than 21 d of age at weaning when the policy
of maximum weaning age was 21 days.
Strict adherence to maximum weaning age has been advocated to minimize transfer
of infectious disease. Also, a narrow spread of weaning age has been indicated as
desirable for success of isowean programs with a maximum of 20 d of age suggested
200
180
160
140
Frequency
120
100
80
60
40
20
0
23
24
26
17
18
20
21
22
14
15
16
25
19
13
e
or
M
Age, d
Figure 11.2. Histogram of ages at weaning (Dritz, 2002).

for the elimination or control of most swine pathogens (Harris, 2000). Our
experience indicates that the actual weaning age of groups of pigs is highly variable
based on farrowing house management practices. Therefore, even though most
weaner pig nutritional programs are based on pig weight, we believe understanding
the mean and variation in age are important for successful nutrition programs.
11.3 Basis of nutrient specifications for weaner pigs

We adhere to three key concepts when formulating diets for the weaner pig. First,
the economics of today’s swine industry dictate that we must adjust pigs to the
simplest and relatively lowest cost diets (i.e., grain and soybean meal) as quickly
as possible after weaning. Second, we must remember that the newly weaned pig
is in an extremely energy dependent stage of growth and that maximizing feed
(energy) intake is essential. Third, we must remember the digestive physiology of
the weaner pig and formulate the initial diets with highly digestible ingredients
that complement the pattern of digestive enzymes secreted at weaning.
One example emphasizing all three of these concepts is the practice of using soybean
meal in diets fed immediately after weaning. Some nutritionists believe that weanling
pigs should be fed diets with no or very little soybean meal immediately after
weaning and that the level should be steadily increased over time. This slow and
very gradual introduction of soybean meal into the pig’s diet will minimize the
potential for delayed-type hypersensitivity to the soy proteins, conglycinin and beta-
conglycinin (Li et al., 1990a,b; 1991a,b) and, thus, generally results in excellent
growth performance initially after weaning. However, it also leads to very high
nursery feed cost. A second option is to feed a diet with a moderate level (10 to
15% of the diet for pigs weaned between 15 and 21 days of age) of soybean meal
as a partial replacement for more expensive specialty protein sources (Friesen et
al., 1993a). This approach is a compromise between feeding extremely expensive
all milk- and animal specialty protein-based diets and simple grain-soybean meal-
based diets. As a result, the pig’s feed intake is stimulated by the lactose and specialty
protein sources, which are highly digestible and palatable and, thus, increase energy
intake. At the same time, the pig becomes exposed to the moderate amount of
soybean meal protein, minimizing the negative effects of a delayed-type
hypersensitivity response. As a result the amount of soybean meal in the diet can
be quickly increased in a phase feeding program to decrease the need for the more
expensive specialty protein sources.
The net result of using soybean meal in this fashion is that we can still provide a
highly digestible complex diet that stimulates feed intake immediately after
weaning, and then quickly reduce diet complexity by increasing the amount of
soybean meal protein (Dritz et al., 1996a). This strategy takes advantage of the fact
that the impact of diet complexity on feed intake and pig performance decreases
262 Weaning the pig

rapidly after weaning, especially in high health pigs. Thus, a feeding program can
be developed that nutritionally allows for maximum growth performance and yet
will be economically competitive.
11.3.1 Ingredient selection based on digestive capacity
Selection of different types and amounts of other feed ingredients also should be
based on the three primary criteria of quickly reducing diet complexity to lower
feed cost, maximizing feed (energy) intake, and physiology of the digestive
system. Indeed, ingredient selection in addition to cost should be based on factors
including nutrient digestibility, amino acid density, lactose concentration, and
stimulatory affects on feed intake and(or) growth. Another consideration is how
an ingredient or combination of ingredients will react under various feed processing
methods. The use of added fat is an example of this latter consideration. Although
added fat is not well utilized by the pig as an energy source immediately after
weaning, its inclusion is essential if diets containing high levels of milk and other
specialty protein sources are to be pelleted.
The newly weaned pig’s digestive system is relatively immature but, at the age of
weaning, well adapted to digest the proteins, lactose, and lipids secreted in sow’s
milk. It has been well established that inclusion of lactose containing ingredients
assists in the transition at weaning from sow’s milk to a dry diet (Tokach et al.,
1989; Mahan, 1992; Nessmith et al., 1997). However, evidence may suggest that
despite our best attempts to mimic the nutrient composition of sow’s milk in a
dry diet, there are dramatic changes that take place in the size, shape, and
functioning of the villi in the small intestine (Cera et al., 1988a; Li et al., 1990a,
1991a,b; Jiang et al., 2000). The anatomical changes in the villi after weaning may
be a possible cause for poor utilization of some ingredients. For example, the
anatomical changes in the villi may cause the reduction in secretion of fatty acid
binding protein, which correlates with poor fat utilization by pigs for approximately
10 to 14 days after weaning (Reinhart et al., 1990). Ingredient selection also can
change the degree to which these changes in the structure and functioning of the
villi take place. An example is the shearing of villi caused by the delayed-type
hypersensitivity reaction to excessive soybean meal fed immediately after weaning
(Figure 11.3; Li et al. 1990a,b). Certain ingredients, such as spray-dried animal
plasma, also may have a positive effect on intestinal development (Jiang et al., 2000).
Although our understanding of the influence of ingredient selection on structure
and functioning of the villi has improved, the rapid change in function of the villi
at weaning still seems to be a primary challenge in weanling pig nutrition. Despite
the changes in digestive physiology at the time of weaning, protein source
solubility within the intestine appears to be the primary limitation to digestion
in the early-weaned pig (Asche et al., 1989a,b).

Figure 11.3. Villi of small intestine after being fed high levels of soybean meal (left
panel) or a milk-based diet for two weeks after weaning (right panel).
11.4 Nutrient requirements of the weaned pig

11.4.1 Energy
Weanling pigs simply do not eat enough feed to maximize their potential for protein
deposition. Thus, any increase in feed (energy) intake will result in a further increase
in growth rate provided proper nutrient to calorie ratios are maintained. In order
to maximize energy intake, ingredients must be highly palatable to stimulate feed
intake, highly digestible, and contain a high net energy concentration. When selecting
protein and energy sources, their impact on feed intake must be carefully
considered. Individual feed ingredients will be discussed later in this chapter, together
with the importance of management decisions to increase feed intake.
11.4.2 Amino acids
Because of dramatic improvements in our understanding of the environmental

requirements of weanling pigs as well as management and pig flow practices that
result in minimizing exposure to disease antigens, protein deposition and, thus,
amino acid requirements have increased over the past 10 years. Although the lysine
requirement estimate for the weanling pig has increased in recent publications (NRC,
1998), many would argue that these requirement estimates may still be too low for
the high-health, high lean growth potential pigs in commercial production systems.
264 Weaning the pig

Data from Owen et al. (1995d,e), Chung et al. (1996), and Williams et al. (1997b)
all estimate a similar lysine requirement of the weanling pig of approximately 1.60%
total lysine, or approximately 1.40% apparent digestible lysine for the first 14 days
after weaning at 14 to 22 days of age. Because weaner pigs are in an energy dependent
phase of growth, diets should be formulated on amino acid to calorie ratios, rather
than percentages of the diet. Using the energy content of the diets of Owen et al.
(1995d), Chung et al. (1996) and Williams et al. (1997b), a lysine to calorie ratio
of approximately 4.1 to 4.2 g apparent digestible lysine/Mcal ME is suggested. Because
of the limited utilization of added fat by the weanling pig immediately after weaning,
the actual lysine to calorie ratio may be underestimated in this age pig. As the pig
becomes older and heavier, the optimum lysine to calorie ratio decreases to
approximately 3.3 g apparent digestible lysine/Mcal ME for the 22 kg pig (Nam and
Aherne, 1994; Smith et al., 1999b). Information on the requirement estimates of
other amino acids, particularly on a ratio relative to lysine, is less abundant. However,
it would appear that the optimum minimum ratios of other amino acids relative
to lysine on a true digestible basis are: methionine, 30% of lysine (Chung and Baker,
1992; Owen et al., 1995a,b); methionine and cysteine, 55% of lysine; isoleucine,
55% of lysine (Kerr, 1999; James et al., 2001a); tryptophan 16% of lysine (Han et
al., 1993); valine 60% of lysine (James et al., 2001c). However, results of titration
studies evaluating threonine requirements are less definitive. Threonine estimates
range from approximately 60% to 68% relative to lysine (Johnston et al., 2000; James,
et al., 2001b). Because of the relatively low concentration of threonine in many
specialty protein sources fed to weanling pigs and the cost of crystalline threonine,
the variation in requirement estimates has a potentially large economic burden. Listed
in Table 11.2 are suggested lysine to calorie ratios and ratios of other amino acids
to lysine for pigs from 3 to 22 kg.
11.4.3 Other approaches to determining a requirement estimate
One reason for the disparity between requirement estimates derived from typical
titration studies and levels used in commercial production may be related to our
method of defining a requirement. In academia, we often titrate an increasing
concentration of an amino acid and record the response in daily gain and feed
efficiency. We then fit the data to a broken-line model, where we have an
increasing response up to a point (the requirement), after which there is a plateau
with no further improvement in performance. Full economic evaluation of a
requirement is not usually conducted in academia, but there might be an estimate
of feed cost per unit gain. Unfortunately, the fitting of most data to a “broken line”
is more the result of our inability to have as many treatments and replications as
what would be ideal because of the physical constraints of many research facilities.
From a biological standpoint, because there are frequently continued, albeit
diminishing, improvements in a response criterion beyond the estimated
requirement, fitting data to a broken line to establish a requirement will have its

Table 11.2. Amino acid recommendations for pigs from 3 to 22 kg.
Weight range, kg
Item 3 to 5 5 to 7 7 to 11 11 to 23
Total lysine:calorie ratio, g/Mcal ME 4.7 4.5 4.0 3.8

Apparent digestible lysine:calorie ratio 4.0 3.9 3.4 3.2
True digestible lysine:calorie ratio 4.2 4.1 3.5 3.3
Approximate total lysine, % 1.65 1.55 1.35 1.30
Approximate true digestible lysine, % 1.50 1.40 1.22 1.16
Ratios relative to lysine on true digestible basis

Isoleucine, % 55
Methionine, % 27.5
Total sulfur amino acids, % 55
Threonine, % 62
Tryptophan, % 16
Valine, % 60
limitations and almost in all cases derive a conservative (low) requirement

estimate.
For example, using the broken line method on the data in Table 11.3, we would
derive a requirement of approximately 1.10% lysine for ADG (James et al., 2000).
However, F/G continued to improve slightly through 1.40% lysine. The interesting
aspect of this case is trying to determine the optimal lysine level to feed in this
production system. To answer this question, we used a ten-year historical price series
for corn, soybean meal, choice white grease and market hogs. We then determined
which diet provided the lowest feed cost per pound of gain and the greatest margin
over feed cost in each month according to procedures of De La Llata et al. (2001).
The average value from the ten-year period (120 months) is shown in Table 11.3.
The diet containing 0.95% lysine provided the lowest feed cost per lb of gain in
100 of the 120 months, or 83% of the time. The diets containing 1.10% lysine or
1.40% lysine had the lowest feed cost per pound of gain in 5 (4%) and 15 (13%)
of the 120 months, respectively.
However, a slightly different answer results when a value is placed on the extra weight
gain of pigs fed the higher lysine diets. On average, diets formulated to 1.10, 1.25
or 1.40% lysine provide an extra $1.27 to $1.63 return over feed cost compared
to the diet formulated to 0.95% lysine. An additional $2.57 to $2.93 return over
feed cost was captured compared to the diet formulated to 0.80% lysine. In 118
266 Weaning the pig

Table 11.3. Economic value (in U.S. $) of increasing the dietary lysine level for pigs
from 40 to 80 lb. (James et al., 2000).
Total dietary lysine, %
Economic calculations 0.80 0.95 1.10 1.25 1.40
Diet cost, $/ton 147.52 154.53 161.55 168.82 176.05

Feed cost, $/pig 4.65 4.67 5.18 5.27 5.40
Wt gain in 28 d, lb 15.7 16.9 18.6 18.5 18.9

Feed cost, $/kg gain 0.295 0.276 0.280 0.287 0.284
Value of gain at $1.025/kg, $/pig 16.13 17.30 18.99 18.86 19.38
Return over feed cost, $/pig 13.58 14.88 16.28 16.05 16.51
Extra return over 0.8% lysine ($) 1.30 2.70 2.57 2.93
of the 120 months (98%), the diet containing 1.40% lysine provided the greatest
return over feed cost. The diet containing 1.10% lysine provided the greatest return
in the other 2 months.
The results of this analysis indicate that diets for pigs weighing 18 to 35 kg can be
formulated from 1.10 to 1.40% lysine with similar economic results. The slight
improvement in F/G at higher lysine levels offsets the increase in diet cost to result
in similar return over feed cost. It is important to note that the optimal lysine level
(1.10 to 1.40% lysine) would rarely have minimized feed cost per pound of gain,
but almost always maximized margin over feed costs. Clearly this type of analysis
can lead to different requirement estimate than more conventional procedures, thus
explaining a portion of the possible variation in nutrient concentrations used in
diets.
Another method to evaluate the same data set is shown with regression analysis.
Regression analysis was applied to the data from the growth trial to generate regression
equations. The regression equations allow us to predict the response in ADG and
F/G to each incremental increase in lysine in the diet. The regression equations also
allow us to predict which lysine level would provide the greatest margin over feed
cost for month in the 120-month price series (Figure 11.4). This analysis indicates
that, with the exception of late 1998 when the pig price dropped significantly, the
optimal lysine level for this period was always between 1.25 and 1.3%.

1.4
Lysine, % 1.3
1.2
1.1
1
1988
1989
1990
1991
1992
1993
1994
1995
1996
1997
1998
Figure 11.4. Dietery lysine level that would have provided the greatest return over feed
cost for each month (Adapted from James et al., 2000).
11.4.4 Vitamins
Conducting research evaluating vitamin requirements of weanling pigs is frustrating

because of the tremendous variation in response between trials. These often-
conflicting results appear to be somewhat characteristic of studies conducted on
vitamin requirement estimates. It is likely that factors such as age, health,
environment, lean growth potential, and diet may influence responses to added
vitamins. While it seems there is tremendous trial-to-trial variation in pigs’
responses to vitamin supplementation, one observation is certain: current NRC
(1998) vitamin requirement estimates are too low for pigs in commercial
production. Vitamins that should be routinely supplemented in weaner diets include
the fat soluble vitamins A, D, E, and K and the water soluble vitamins B12, niacin,
pantothenic acid, and riboflavin. Of the fat-soluble vitamins, the majority of research
has been conducted on vitamin E because it is generally one of the most expensive
vitamins to add to a diet. Data would indicate that if the sow has adequate
supplemental vitamin E and selenium in gestation and lactation diets (44 IU/kg
and 0.3 ppm, respectively; Mahan, 1994), supplementing nursery diets to 44 IU/kg
of added vitamin E should be adequate. However, if breeding herd diets contain
less than 44 IU/kg, greater than 44 IU/kg of feed added in nursery diets may be
needed in some herds to minimize the incidence of mulberry heart occurrence post
weaning.
Wilson et al. (1991, 1993), in a series of studies, observed that multiple B-vitamin
supplementation to concentrations 3 to 4 times NRC estimates resulted in
improved growth performance of weanling pigs. For the most part, the feed industry
typically fortifies diets for weanling pigs at a rate similar to this (BASF, 1997).
However, recently Stahly et al. (1996) observed increased growth performance of
high-health and high lean growth potential pigs when fed up to 6 times NRC
268 Weaning the pig

estimates for the major B-vitamins. Application of these results, however, is

limited because several vitamins were added at increasing concentrations. Therefore,
it is impossible to determine if the response is due to one specific vitamin or a
combination of several vitamins. Another factor that may be biasing the response
to vitamin supplementation is that pigs were fed a vitamin deficient diet before
the experiment began. However, a study recently conducted by a vitamin
manufacturer reported similar improvement in growth performance with vitamin
supplementation up to 16 times NRC (1998) requirement estimates (Coelho et
al., 2001). Additional research is needed in this area to confirm pig responses to
these “supra-nutritional” concentrations. Currently, there is justification for
vitamin supplementation at 3 to 4 times NRC (1998) requirements under field
conditions.
There is also data suggesting that some vitamins previously considered not
necessary to add to weanling pig diets, such as pyridoxine (Woodworth et al., 2000),
vitamin C (de Rodas et al., 1998) and carnitine (Real et al. 2001) may increase growth
performance of weanling pigs. The response to pyridoxine and vitamin C appears
to be greatest initially after weaning. The response to carnitine appears greatest from
2 to 4 weeks after weaning. Economics dictate that the decision to add pyridoxine
to diets immediately after weaning is easier than the decision to add either vitamin
C or carnitine. Further research is needed with vitamin C and carnitine before
definitive conclusions can be made.
11.4.5 Minerals
Weaner pig diets should be supplemented with the macro minerals calcium,
phosphorus, sodium and chloride and the trace minerals copper, iodine, iron,
manganese, selenium, and zinc. As for the macro minerals, because of their relative
abundance and availability in milk and other specialty protein sources, providing
a wide margin of safety above the pig’s actual requirements is neither difficult nor
costly. Because of the importance of bone growth early in the pig’s life, calcium
and available phosphorus concentrations should range from 0.90 to 0.75 and 0.48
to 0.40 from weaning to 20 kg, respectively. The other macro minerals that appear
to improve pig growth performance are sodium and chloride (Mahan et al., 1996).
Despite the relatively high concentrations of sodium and chloride in dried whey
and spray-dried animal plasma, studies show improved growth performance when
salt is supplemented to diets containing high levels of these ingredients (Mahan
et al., 1996). The sodium and chloride requirement of weaner pigs initially after
weaning is clearly higher than recommendations of NRC (1998).
Copper and zinc are the two trace minerals that have received the most attention
due to their potential as growth promoters. The basal requirement for copper and
zinc is approximately 10 and 100 ppm, respectively. Data on the addition of high

levels of copper (100 to 250 ppm) to starter diets as a growth promoter was
summarized well by NRC (1998). In recent years, numerous experiments have
demonstrated that adding high levels of zinc oxide (3,000 ppm) to nursery diets
improves pig performance (Hahn and Baker, 1993; Carlson et al., 1999; Woodworth
et al., 1999a,b,d) immediately after weaning and to a greater extent than copper
sulfate (Smith et al., 1997). In a series of experiments, Woodworth, et al. (1999a)
confirmed earlier work of Hahn and Baker (1993) and McCully et al. (1995) showing
that the oxide form of zinc was more effective in producing the growth-promotion
response than zinc sulfate or a zinc amino acid complex. Woodworth et al. (1999b)
also discovered that the source of zinc oxide, although important for bioavailability
(Edwards and Baker, 1999), did not influence the pharmacologic growth-promotion
response. Most commercial diets now use 2,000 to 3,000 ppm of zinc oxide as a
growth promoter immediately after weaning and 100 to 250 ppm of copper sulfate,
or no supplemental copper or zinc in the late nursery diets.
11.4.6 Post-weaning diarrhea and zinc oxide.
Post weaning diarrhea associated with hemolytic Escherichi-coli is a common problem

in early wean pigs. Supplementing nursery diets with 3000 ppm zinc from zinc
oxide (ZnO) post-weaning has also been observed to have beneficial effects in
helping control post-weaning E. coli associated challenges under field conditions
(Holm and Poulsen, 1996, Tokach et al., 2000).
A case study by Tokach et al. (2000) clearly illustrated the clinical and economic
impact ZnO can have in controlling post-weaning diarrhea. Piglets were being
weaned from a 1400-sow unit and sent to three different producers in loads of
600 pigs per week. Production records indicated poorer performance and a
greater problem with E. coli associated diarrhea in one herd compared to pigs from
the other two [394 g vs. 436 g of average daily gain (ADG) and 8.0% vs. 0.96%
mortality for the case herd and other two herds, respectively]. No environment and
management differences on the sow farm of origin were found to explain the
performance differences in these three groups of pigs. When diet formulations were
reviewed, it was discovered that the first two diets fed to the weaned pigs in the
case herd contained 612 ppm zinc from ZnO, instead of the specified 3,000 ppm.
Comparable diets for the pigs in the other two locations contained 3,000 ppm zinc.
The diet formulation error was corrected, and performance of the next groups of
pigs improved. This case study demonstrated the value of closeout records in
determining the economic impact of the diet formulation error, which was
calculated to be a loss of $3.13 to $5.88 per weaned pig.
In a challenge study, Jensen-Waern et al. (1998) found that adding 2500 ppm of
zinc from ZnO to the diet prevented postweaning diarrhea without affecting the
numbers of E. coli excreted in the feces. In another challenge study (Mores et al.,
270 Weaning the pig

1998), high concentrations of zinc from any of four ZnO sources reduced the
occurrence of E. coli diarrhea without affecting fecal shedding of the E. coli. In these
experiments, a high prevalence of diarrhea occurred in pigs that did not receive
high concentrations of ZnO when challenged.
Another recent study demonstrated that pigs supplemented with ZnO at 3,000 ppm
had a reduced translocation of bacteria to the ileal-mesenteric lymph node
(Huang et al., 1999). The potential mechanism for this finding, as well as the other
beneficial effects demonstrated above, is not clearly understood. Zinc has been
demonstrated to have an effect on cells undergoing rapid turnover, as it is needed
for DNA and protein synthesis. Zinc also seems to play a role in stabilizing cell
membranes and modifying membrane functions (Bray and Bettger, 1990). Zinc is
also a powerful anti-inflammatory agent and the gut often suffers an non-specific
inflammatory response after weaning. Therefore, zinc’s beneficial impact may be
in part due to a direct supportive or protective role of intestinal epithelial cells
(Huang et al., 1999).
Managing post-weaning E. coli challenges is increasingly becoming more complex.

These challenges need an ongoing effort for improved prevention or intervention
techniques. Utilizing excess supplemental zinc early in the nursery phase is one
option available to help minimize these challenges and promote growth. The
environmental concerns associated with feeding zinc are significant. This concern
reemphasizes the desire to restrict the 3,000 ppm ZnO inclusion in the first two
weeks after weaning when feed intake is the lowest and the benefit the greatest.
11.4.7 Organic trace minerals
The chemical form of trace minerals also has received considerable attention in
recent years. Organic sources of copper appear to provide growth promotion similar
to copper sulfate (Coffey et al., 1994; Apgar and Kornegay, 1996). Numerous organic
forms of zinc (zinc-lysine, zinc-methionine, zinc-amino acid complexes) also are
available for use in swine diets. However, supplementing diets with the organic
forms of zinc does not consistently improve pig performance to the same extent
as growth promoting levels of zinc oxide (Hahn and Baker, 1993; Woodworth et
al., 1999a,c). Environmental issues with trace mineral accumulation in swine waste
will force continued evaluation of different mineral sources for pigs in an attempt
to reduce zinc and copper excretion.

11.5 Selection of ingredients for the weaned pig

11.5.1 Energy sources
11.5.1.1 Lactose
Research with high quality lactose sources has demonstrated linear improvements
in pig performance as levels of lactose increase in the diet, even through levels as
high as 45% (Mahan, 1990). Most diets used in commercial application fed
immediately after weaning contain more modest and economical levels of 15 to
20% lactose. Lactose additions to the diet continue to improve growth performance
until approximately 21 to 28 days after weaning, or 10 to 13 kg (Crow et al., 1995).
After this time, lactose can be replaced with other, more economical carbohydrate
sources, such as cereal grains.
A high quality, edible-grade, dried whey is the predominant lactose source used
in starter diets. Recent research with lactose has focused on evaluating less
expensive lactose sources to replace dried whey in the diet. Several lactose sources
have emerged including L-lactose, deproteinized whey, and whey permeates. The
value of these sources was questionable in the past; however, processors have
improved their knowledge of the drying conditions required to maintain a high
quality product. Additionally, the quantity of these products has increased due to
the desire for whey proteins in human food products. Nutritionists’ understanding
of the use of whey replacements also has improved. Initial tests attempted to replace
dried whey on a lactose basis without substituting another high quality protein
source for the whey protein removed from the diet when substituting a lactose
product for dried whey. Recent trials have proven that other lactose sources can
replace whey in the diet (Nessmith et al., 1997; Touchette et al., 1995) with two
stipulations: 1) the spray drying must be well controlled, and 2) a high quality
protein source must be used to replace the whey protein fraction.
Recently, other non-lactose carbohydrates have been touted as replacements for

lactose or dried whey. These carbohydrates include dextrose, sucrose, or byproducts
of candy manufacturers. The research generally shows that these sources can replace
a portion of the whey in the diet, but they should not replace the entire lactose
fraction (Stephas and Miller, 1998).
Incremental replacements of whey or high quality proteins, such as animal

plasma, must be viewed with some skepticism. If the protein or carbohydrate source
cannot replace whey or plasma directly, care must be taken with an incremental
replacement approach. As an example, trials have shown that reducing the lactose
level from 15 to 10% will not reduce performance significantly (Owen et al., 1993).
Similarly, reducing the plasma level from 7 to 5% may not demonstrate a
272 Weaning the pig

significant response in a given experiment. However, if sufficient replication was

conducted or the plasma and lactose levels were reduced at the same time, significant
differences will often be found. Research results must be viewed with care when
evaluating ingredient replacements. These trials can be easily designed to find the
desired and potentially biased results.
11.5.1.2 Fat
The original high nutrient density diets for weanling pigs contained 8 to 10%
supplemental fat to provide levels similar to that of sows milk (Nelssen, 1986).
Since the introduction of these diets, numerous trials have been conducted to
examine the young pig’s ability to utilize fat. Nelssen (1990) explained that fat was
added to the diets for two reasons: 1) to increase dietary energy density, and 2) to
improve pellet quality and efficiency in the pellet mill. However, early research
examining the response to supplemental fat in diets containing high levels of milk
products failed to consider the importance of fat in maintaining pellet quality. Diets
containing high levels of milk products without supplemental fat are extremely
difficult to pellet with low passage rate through the pellet mill. The diet will, thus,
have a longer residence time in the die and may be scorched, lowering lysine
availability and milk product quality. Adding high levels of fat to the diet prevents
the scorching. Thus, a response that was attributed to added fat in early research
may have been due to an improvement in pellet quality rather than a response to
fat per se.
When carefully monitoring pellet quality, researchers (Li et al., 1989; Tokach et al.,
1995) have failed to show an improvement in performance when adding up to
10% fat to weaner diets fed immediately after weaning. However, the “pellet quality
factor” must be considered when adding fat to a diet containing high levels of milk
products. The ideal fat level for the pelleting process depends on the level of milk
products, thickness of the die, and skill of the pellet mill operator (Leaver, 1988).
Levels of 3 to 6% supplemental fat may be warranted in diets containing high levels
of milk products to improve pelleting efficiency; however, higher levels of fat addition
to the diet appear unjustified.
The reason that fat utilization is limited in the pig before 35 d of age is not well
understood. The lower digestibility of fat by weanling pigs during the initial period
after weaning may be part of the problem (Leibbrandt et al., 1975; Cera et al.,
1988a,b). The lower digestibility may be due to myriad of reasons. Dietary fat causes
the sloughing of intestinal villi cells impairing digestion immediately after weaning
(Cera et al., 1988a). The young pig also has decreased levels of fatty acid binding
protein during the first 2 wk after weaning (Reinhart et al., 1990). Furthermore,
enzyme secretion and(or) activity may be limited immediately after weaning at
an early age. Several researchers (Scherer et al., 1973; Corring et al., 1978;

Lindemann et al., 1986; Cera et al., 1990) have reported that lipase activity and
secretion in pancreatic tissue increased with increasing age postweaning. Quantities
of calcium and copper in the diet also have been implicated as influencing fat
digestibility. High levels of calcium in the small intestine may depress fat
absorption by increasing the formation of fatty acid soaps (Atteh and Leeson, 1983).
Conversely, Dove and Haydon (1992) and Dove (1993) demonstrated high levels
of copper sulfate in the diet improve fat utilization in the young pig.
The lower apparent digestibility may not fully explain the young pig’s poorer
utilization of energy from fat than that of older pigs. Part of the problem with fat
utilization also appears to occur at the tissue level. Cera et al. (1988c) found that
supplemental fat decreased nitrogen retention and increased serum urea
concentration during the initial 2 wk after weaning. Supplemental fat also
increased carcass fat (Endres et al., 1988) and decreased protein gain (Leibbrandt
et al., 1975) during this period. These results indicate that the young pig digests
and absorbs a large portion of the dietary fat and stores it as carcass fat. However,
during the initial weeks after weaning, the pig may not be able to efficiently
catabolize the fat for use as energy. Thus, an energy deficit may occur requiring
the pig to utilize dietary protein as an energy source. This would explain the decreased
nitrogen retention and increased serum urea concentration found by Cera et al.
(1988c). If a limitation in fat metabolism exists, further research is needed to
determine whether the limitation occurs in lipolysis, transport, or beta-oxidation.
Research in the human nutrition field suggests babies are born with limited ability
to synthesize the carnitine-acyl transferase enzyme needed to transport the fatty
acid into the mitochondria for beta-oxidation. Adding L-carnitine to diets
immediately after weaning has improved pig performance in some experiments
(Rincker et al., 2001); however, it does not appear to solve the entire problem
associated with fat utilization.
With increasing age after weaning, the ability of the pig to efficiently utilize fat
improves. Increasing the energy density of the diet by adding fat consistently
improves feed efficiency and growth rate for pigs greater than 42 days of age. After
this age, dietary fat decisions should be based on economics, as the ability of the
pigs to utilize the fat is not a concern.
Considerable research has been conducted in recent years to determine the

appropriate fat source for the early-weaned pig. Cera et al. (1988b) found corn oil
to be more digestible than lard or tallow, but differences among fat sources narrowed
from week 1 to 4 after weaning. Tokach et al. (1995) found no difference in
performance when comparing corn oil and soybean oil. Li et al. (1989) found that
a combination of soybean oil and coconut oil was superior to diets containing
soybean oil, choice white grease or a combination of coconut oil and choice white
grease. However, the high cost of refined coconut oil usually limits its use in swine
274 Weaning the pig

diets. Tallow and restaurant grease have consistently been found to be the least
desirable fat sources for nursery diets. Whenever fat is added to the starter diet, a
high quality, stabilized fat source must be used. Also, a constant ratio of nutrients
to energy must be maintained when adding fat to the diet. The importance of fat
in maintaining pellet quality in high milk, dry diet should not be underestimated.
11.5.1.3 Grain sources
Several grain sources have been used successfully in diets immediately after
weaning. In diets containing relatively high levels of specialty protein or lactose
sources, corn can be substituted as the main cereal source with tapioca, sorghum,
or rice (Rantanen et al., 1995a), oat groats (Mahan and Newton, 1993), whole oats,
oat groats or oat flour (Rantanen et al., 1995b), naked oats (Landblom and Poland,
1998), potato starch (Dritz et al., 1994a; Kerr et al., 1998b) or wheat. In none of
these trials, however, was performance improved by replacing corn with these
alternative grain sources. In the later nursery stages, pigs respond as expected with
grains containing higher energy concentrations providing improved pig performance.
11.5.2 Protein sources
11.5.2.1 Spray-dried animal plasma
Although animal plasma is expensive, it is necessary to encourage maximum feed

intake in the period immediately after weaning (Gatnau et al., 1991; Hansen et al.,
1993; Kats et al., 1994c) with very young pigs. Increasing the level of animal plasma
from 5 to 15% in the diet for SEW pigs results in a linear increase in pig performance
(Dritz et al., 1994b). However, the greatest portion of the response is evident with
the first 5% inclusion of plasma (Hansen et al. 1993). Thus, most nutritionists
include plasma in the SEW diet at 5 to 7%, depending on price and other
combinations of protein sources included in the diet.
Plasma contains high levels of cysteine, but low methionine levels, making it
necessary to formulate for methionine in addition to total sulfur amino acids. When
comparing various plasma sources, solubility and bacterial levels should be
considered. Higher solubility indicates less heat denaturing during the spray-drying
process. Lower bacterial levels are an indication of quality of the raw material.
Recently, DeRouchey et al. (2001a,b) found that lowering the bacterial levels in
plasma with irradiation or by applying a formaldehyde-based product improved
pig performance.
The main response to adding plasma to the diet is an increase in feed intake.
Numerous researchers have tried to find the mechanism for this feed intake response.
Owen et al. (1995c) and Peirce et al. (1995) demonstrated that the immunoglobulin

fraction of plasma appears to provide the greatest benefit in feed intake, as compared
to the albumin fraction or the remaining portions of plasma. Plasma normally
contains about 15 to 18% immunoglobulin.
Because of the feed intake response, plasma rapidly became the dominant protein
source in starter pig diets. Due to the high cost of plasma, research quickly shifted
to experiments to determine the optimal level of plasma in the diet and whether
other protein sources or combinations of protein and carbohydrate sources could
replace a portion of the plasma. Other protein sources, such as high quality fish
meal, spray-dried blood meal, and spray-dried whole egg, have been able to replace
a portion of the plasma in the starter diet; however, none of these protein sources
is a viable replacement for the entire plasma fraction of the diet.
One other peculiarity to plasma is the carryover effect after removing pigs from a
diet containing a high level of plasma. Many trials have fed high levels of plasma
(5 to 10%) for 1 to 2 weeks after weaning. After feeding these high levels, the pigs
were switched to diets without plasma. When this is done, most of the growth
advantage is lost within the next week or two. To overcome this problem, we advocate
a step-wise approach to removing plasma from the diet. If the first diet fed contains
5% plasma or greater, a second diet containing 1 to 2.5% plasma should be fed
before removing all the plasma from the diet (Dritz et al., 1996b; Bergstrom et al.,
1997). Because plasma is expensive, this strategy results in considerable cost savings
compared to maintaining the high level in the diet. Reducing the plasma level with
diet changes after weaning is an example of managing the inclusion rate of an
expensive ingredient to match the biology of the pig to derive maximum economic
benefit.
Because the response to plasma is due to an increase in feed intake, there also is
an interaction with the health level of the pigs on the response to plasma. If the
pigs are very high health and, thus, have a high level of feed intake without plasma,
plasma does not provide as much benefit as in a low health situation or more
challenging environment (Coffey and Cromwell, 1995).
In some European countries, animal proteins (other than milk products) can not
be fed to pigs due to concerns with Bovine Spongiform Encephalitis (BSE). Thus,
it is not legal to use spray-dried plasma in swine diets in these countries. Because
of this ban, diets must be formulated using many of the alternative protein sources
listed below.
11.5.2.2 Whey protein concentrate
Whey protein concentrate is a very high quality protein source. Recent research
(Grinstead et al., 2000) indicate that high protein (78%) whey protein concentrate
276 Weaning the pig

may be one of the few protein sources that consistently provides pig performance
similar to animal plasma. High protein, whey protein concentrate has a similar
amino acid profile to plasma. Grinstead et al. (2000) tested this product at levels
of 3 to 7% of the diet and found excellent similar ADG and feed efficiency in
comparison to plasma. Unfortunately, access to high protein, whey protein
concentrate is limited due to the high demand for use in non-fat foods by the human
food industry. Price may limit the application in the United States, but its
economic competitiveness should be watched closely around the world.
11.5.2.3 High quality fish meal
Several fish meal sources are available for starter diets. The highest quality fish meals
from various United States (Select Menhaden Fishmeal), European (Low temperature
Norwegian fish meals), and Chilean (low amine products) sources all have
proven to be excellent protein sources for young pigs. Researchers have found little
difference in feeding value between these high quality sources. However, none of
these sources can directly replace plasma in the starter diet. High quality fish meal
is used at 3 to 6% in most starter diets to increase the amino acid content and
increase feed intake without dramatically increasing cost. When a high quality fish
meal is available and economical, weaner diets can contain as much as 12% Select
Menhaden Fishmeal without compromising performance (Stoner et al., 1990).
Similar to other protein sources that rely on high quality raw materials and correct
drying, the quality of fish meal can deteriorate quickly when not handled properly.
11.5.2.4 Dried skim milk
In the past, most diets fed immediately after weaning routinely contained 10 to
25% dried skim milk. The use of animal plasma quickly eliminated skim milk as
a protein source in most diets. Skim milk has two problems: 1) expense, and 2)
the casein fraction decreases feed intake. Dritz et al. (1994c) found no benefit to
having skim milk in the diet, when the diet contains adequate plasma and lactose.
If fact, feed intake improved when skim milk was removed from the diet. Dried
skim milk still is being used in weaner diets in some instances because pigs look
cleaner and drier when fed a diet containing skim milk. The problem is that they
do not grow faster. However, when marketing to unsophisticated producers that
rely on their eyes instead of performance data to make decisions, ingredients like
skim milk and oat groat products increase in value. Because of the high biological
value, pigs fed diets containing dried skim milk often have better feed efficiency
than pigs fed diets containing plasma; however, feed intake and average daily gain
will be lower. Nevertheless, in addition to being more expensive than other protein
sources, our findings indicate that the skim milk can be replaced with lower cost
protein sources without sacrificing performance.

11.5.2.5 Spray-dried blood meal or red blood cells
Spray-dried blood cells are a byproduct of plasma manufacturing. Spray-dried blood

meal has the advantage of not having the plasma removed during processing. Spray-
dried blood meal and cells have high protein contents (85 to 95%) and, thus, can
be used in the weaner diets in small quantities as concentrated amino acid sources.
When fed to pigs weighing 5 to 15 kg, blood products increased feed intake and
growth rate (Hansen et al., 1993; Kats et al., 1994b). These products need to be
used with caution with pigs weighing less than 5 kg. Levels greater than 2% can
depress feed intake. Blood meal or blood cells should not be used at levels higher
than 3% in most diets due to the isoleucine deficiency that occurs in most practical
diets after this point. Spray-dried blood products also are deficient in methionine.
Methionine becomes the limiting amino acid when greater than approximately
5% spray-dried blood products (plasma and/or blood cells or meal) are included
in the diet (Kats et al., 1994b). It is critical that synthetic methionine is added to
the weaner diets containing plasma and other blood products for optimal
performance (Owen et al., 1995b). Processing method for the spray-dried blood
meal also appears to be critical to maintain the quality of protein sources. Kats et
al. (1994b) demonstrated that pigs fed spray-dried blood meal performed better
than pigs fed flash-dried blood meal.
11.5.2.6 Dried porcine solubles
Dried porcine solubles is a product that originates from the processing of porcine
mucosa and small intestines. Porcine solubles are available in various concentrations
with protein content ranging from 30 to 55%. These products have a high ash
content (approximately 32%). The fiber content varies whether soyhulls are added
to the product (18%) as a carrier in the drying process or not. The product is
extremely high in sodium (3.5%) and iron (500 ppm). The amino acid profile is
good, but the lysine level is relatively low (2.0 to 3.8% depending on the protein
content). The difficulty with using porcine solubles in research trials is determining
the method of substitution for other ingredients. The first research compared porcine
solubles to dried whey. Cost and nutrient profile led many researchers to question
whether this was a worthwhile comparison. Subsequent research attempting to
compare porcine solubles to plasma has had difficulty comparing them directly
as protein sources due to the large difference in protein and amino acid content.
Because porcine solubles has improved feed intake when being fed and has improved
subsequent intake after they have been removed from the diet, this protein source
may be a viable option for weaner pig diets (Zimmerman et al., 1997), however,
the database to determine optimum usage is still sparse.
278 Weaning the pig

11.5.2.7 Soybean meal
Soybean protein in the form of soybean meal has long been the predominant protein
source in swine diets. Unfortunately, soybeans contain many anti-nutritional factors
such as trypsin inhibitors, lectins, and complex carbohydrates and proteins that
impair the pigs’ ability to utilize them. Heat treatment of the soybeans in the process
of making soybean meal removes much of the trypsin inhibitor; however, complex
proteins and carbohydrates are not removed. Complex proteins in soybean meal
have been suggested as the cause of a transient hypersensitivity response in the early-
weaned pig. Before weaning, pigs can consume soybean proteins by eating small
quantities of sow feed or creep feed and become exposed or “sensitized” to the
soy proteins. Bourne (1984) explains that prior to building up a tolerance to an
antigen such as those in soybean proteins, the pig goes through a period of
heightened responsiveness. Feeding the soybean protein during this period can result
in damaging hypersensitivity responses, such as increased crypt cell division and
the appearance of immature enterocytes on the villus, resulting in reduced
digestive and absorptive capacity and an increased susceptibility to enterotoxins.
This response appeared to be caused by antigenic proteins present in soybeans,
such as glycinin and beta-conglycinin. The transient hypersensitivity is measured
experimentally as higher immunoglobulin G titers to soybean protein resulting from
the pig’s attempt to mount an immune response against the antigenic proteins.
However, the end result is that digestive abnormalities, including disorders in
digestive movement and inflammatory responses in the intestinal mucosa, can occur.
Villi are sloughed from the small intestinal mucosa and absorptive capabilities are
reduced.
The source and percentage of soy protein in diets for early-weaned pigs have been
controversial subjects among swine nutritionists because of the implication that
soybean protein causes an immune-mediated pathology leading to decreased growth
performance (Li et al., 1990). Engle (1994) reviewed the role of soybean meal in
causing immune-mediated delayed-type hypersensitivity (DTH) allergic reaction.
Some nutritionists believe soybean meal should not be included in the first diet
after weaning to prevent the DTH allergic reaction to the protein antigens it contains.
Most researchers agree that the ideal time to establish oral immune tolerance to
soy protein antigens is before weaning (Engle, 1994). However, with early weaning
ages, it is difficult for the pigs to consume enough soybean protein during the
lactation period to establish oral tolerance. Nutritionists that advocate not
including soybean meal in the first diet postweaning typically will replace it with
a further refined soy protein, such as soy protein concentrate, isolated soy protein,
or extruded soy protein concentrate. If a refined soy product is used in the diet,
several research trials have demonstrated an advantage to moist-extruded soy
products compared to those that have not been moist-extruded (Friesen et al.,
1993b).

Other researchers and nutritionists take a different approach. They believe that
exposing young pigs to increasing levels of soybean meal in each diet will allow
them to overcome the hypersensitivity to soy protein more quickly, without causing
a long-term reduction in performance. This approach also is substantially less
expensive than delaying acclimation to soybean meal. Friesen et al. (1993a) indicated
that delaying exposure to soybean meal until d 14 postweaning only delayed the
effects of DTH. In fact, overall growth performance from d 0 to 35 postweaning
was better for pigs exposed to soybean meal immediately postweaning than for
pigs whose diet did not contain soybean meal until d 14 postweaning. Thus,
formulations of diets for SEW pigs must consider the relationship with performance
in subsequent phases.
Pigs are born with an immature immune system. Over the first few weeks of life,
the immune system progressively develops a greater ability to distinguish between
native and foreign proteins. If exposed to foreign proteins, such as soy protein, at
a very young age, the immune system will be primed to recognize them as native.
The early exposure permits inclusion of soybean meal at higher levels in subsequent
diets without reducing growth performance. The appropriate level and source of
soy protein for the SEW pig are not well researched. We recommend a low level
(10 to 15%) of soybean meal in the initial diet after weaning as a means of
acclimating the young pig to soy protein (Dritz et al., 1994c, 1996b). Research of
Friesen et al. (1993a) and Dritz et al. (1994c) has indicated that early exposure to
soy protein may be beneficial.
11.5.2.8 Further processed soy products
Several experiments have been conducted to determine if further processing of

soybean products would improve the value of soy proteins for the young pig. Several
soy products are available including soybean meal (44 or 48% protein), soy flour
(50% protein), soy protein concentrate (70% protein) or isolated soy protein (90%
protein). Research indicates that these products are only superior to soybean meal
if they have been moist extruded (Li et al. 1990a,b). These experiments revealed
that further processing of soy proteins decreases transient hypersensitivity and
increases villus height, nutrient digestibility, and growth performance as compared
to pigs fed diets containing high levels of soybean meal. However, pigs fed milk-
based diets still had longer villi and higher nutrient digestibility than pigs fed the
further processed soy proteins. This research reveals that processing method
significantly affects the utilization of soy proteins by nursery pigs.
Further research (Friesen et al., 1993b) has suggested that moist extrusion of soybean
meal greatly improves its nutritive value for weanling pigs. In fact, pigs fed diets
containing moist extruded soybean meal performed as well as pigs fed diets
containing moist extruded soy protein concentrate. Moist extrusion appears to be
280 Weaning the pig

an effective means of improving the value of less expensive soy protein products.
Similar advantages of extrusion processing have been seen in a subsequent trial
comparing pigs fed an all-milk protein based diet to those fed either soybean meal,
moist extruded soybean meal, or dry extruded soybean meal. If further processed
soy products such as soy protein concentrate or isolated soy protein are used in
weaner diets, they should be extruded prior to use. Research consistently
demonstrates that the non-extruded products are similar to soybean meal in feeding
value at a much higher cost. However, once extruded, products like extruded soy
protein concentrate are excellent protein sources to use in combination with other
proteins in the starter pig diet. If a nutritionist has a goal of not using any soybean
meal in the diets immediately after weaning, extruded soy protein concentrate as
an excellent protein source.
11.5.2.9 Potato protein
Kerr et al. (1998a) conducted a series of trials with various potato proteins. These
refined products contain approximately 85% protein. The major problem with some
of these products is the level of alkaloids. Further processed potato proteins that
have the alkaloids removed appear to be excellent protein sources. Although potato
protein does not appear to be able to totally replace plasma in the diet, it may be
used in combination with other protein sources in the starter diet. Economics limit
their use in the United States; however, they are more appropriate in economic
situations presented in other parts of the world. Potato protein is a protein source
to watch for further improvement and utilization in the future. The greatest limitation
to use is the cost of removing alkaloids from the product.
11.5.2.10 Spray-dried egg protein
The high immunoglobulin content of whole eggs makes them a logical protein
source to use as a partial replacement to plasma. Egg products still hold promise
in starter diets, but there are still questions about their use. Trials to date
demonstrate inconsistent responses (Nessmith et al., 1995). There are several
potential reasons for the difference in responses in various trials, including: 1) the
purity of the raw material, 2) the level of egg whites and yolk in the product, 3)
the spray drying temperature, 4) post-processing handling of the product, or 5)
the avidin content all of which could limit performance. Similar to potato protein,
egg products hold promise as a protein source for starter pigs, but further work
must be done to determine the required quality parameters and changes in diet
formulation to fully utilize the eggs. The relatively low price of spray dried eggs
has led to renewed interest in egg products as a protein source for young pigs.

11.5.2.11 Spray-dried wheat gluten
Similar to egg protein, spray-dried wheat gluten is an interesting protein source.

Initial trials are quite variable in results (Richert et al., 1993). Spray-dried wheat
gluten is a high protein, extremely lysine-deficient protein source. When used in
the diet, high levels of synthetic lysine can be added before any other amino acids
will be limiting. Thus, wheat gluten can serve in combination with other high lysine
protein sources to improve the amino acid ratio of the diet. A unique result of the
wheat gluten trials appears to be an improvement in subsequent performance after
pigs have been fed a diet containing wheat gluten. Similar to most dried products,
processing conditions are extremely important in determining the quality of the
final product. Wheat gluten must be spray dried to maintain protein quality (Richert
et al., 1993). Wheat gluten is another protein source that has not been utilized to
the full extent of possibilities due to our lack of understanding of the reasons that
the responses have not been consistent in various experiments.
11.5.3 Non-nutritive Feed additives (eg., antibiotics, enzymes, organic

acids, etc.)
The NRC (1998) provided excellent background information on many of the non-
nutritive feed additives that have been used in weaner diets including antimicrobial
agents, microbial supplements, oligosaccharides, enzymes, acidifiers, flavors, and
pellet binders. Guidelines for selecting growth-promoting antimicrobials were
reviewed by Straw (1994), who also established guidelines for determining
growth-promoting antibiotic usage in swine herds. Growth promoting antimicrobials
have a greater response in young versus older pigs, in “dirty” versus “clean”
environments, and in low-health versus high-health animals (NRC, 1998). Recent
evidence indicates that the growth responses to including growth promoting
antimicrobials in swine diets are much lower in modern multi-site swine production
systems compared to previous summaries (Dritz et al., 2002). Also, there is increased
concern that agricultural use of antimicrobials can lead to transmission of resistant
pathogens to humans (Witte, 1998). Without a doubt, development of resistance
is reduced in the face of less selection pressure from lower usage of antimicrobials
(Levy, 1998; Dunlop et al., 1998). Therefore, we advocate implementation of
production practices that improve health status and decrease reliance on continuous
use of feed antimicrobials.
Although microbial supplements or probiotics have been reported to improve

performance under some field conditions, most controlled experiments have failed
to show consistent, beneficial responses (NRC, 1998). Oligosaccharides, such as
fructooligosaccharide and monooligosaccharide, also have been reported to
improve pig performance in some experiments. More research is needed to
determine the conditions (diet, environment, pathogen load, etc) necessary to
282 Weaning the pig

demonstrate a consistent benefit to including oligosaccharides in the diet. Other

additives include various plant extracts and spices (Turner et al., 2001). Many of
these additives are being advocated as replacements for antimicrobials. However,
the supporting data for their usage is limited and inconsistent. Therefore, we believe
implementation of sound production practices such as improved hygiene is a more
cost effective investment than many of these types of additives.
Phytase is an example of an effective enzyme that can be beneficial for the swine
industry. Adding phytase to the diet improves the utilization of phytate phosphorus
and decreases phosphorus excretion into the environment. Unfortunately, many
of the other enzymes on the market, including proteases, cellulases and
hemicellulases, have not shown the same consistency of response. As reviewed by
Gabert and Sauer (1994), supplementing weaner diets with organic acids has been
shown to improve pig performance. The response is greater with simple diet
formulations than with more complex diets (Giesting and Easter, 1985). Inorganic
acids, phosphoric or propionic acid, also have been shown to improve pig
performance during the first couple of weeks after weaning (Bergstrom et al., 1995).
The response to acidification of the diet declines rapidly as the pigs become older
after weaning. Flavors are often added to swine diets in an attempt to improve
palatability and increase feed intake. When given a choice, pigs will consume more
of a diet containing a flavor; however, when pigs are not given a choice, most research
shows little benefit to flavors (NRC, 1998). Pellet binders are often used to improve
pellet quality of nursery diets. Because high levels of milk products are often used
in the first couple of diets after weaning, pellet binders should not be required to
make a high quality pellet. Pellet binders may have more use in the later nursery
stages because diet formulas in this period make the diet more difficult to pellet.
Unless needed for improved pellet quality, non-nutritive binders should not be
routinely added to swine diets.
11.6 Example of phase feeding program for early

weaned pigs
11.6.1 SEW diet - weaning to 5 kg
Maximizing feed intake after weaning reduces stress and increases growth rate by
decreasing the mobilization of lipid stores to provide energy for protein deposition
(Whittemore et al., 1978). Consequently, the major objectives when formulating
an SEW diet, in order of importance are to: 1) select ingredients that stimulate feed
intake, 2) provide a substantial amount of highly-available amino acids in the proper
proportions, and 3) prepare pigs to utilize less expensive diets in subsequent phases.
The high amino acid fortification of the SEW diet necessitates multiple protein
sources to meet the young pig’s nutritional needs (Table 11.4). Several of the

Table 11.4. Recommended sequences and composition of SEW nutritional programs.
SEW Diet for pigs weighing less than 5 kg Transition Diet for pigs weighing 5 to 7 kg
Grain-based Grain-soybean meal-based
1.6 to 1.7% Lysine 1.5 to 1.6% Lysine
0.44 to 0.47% Methionine 0.38 to 0.43 Methionine
18 to 25% Lactose equivalent 15 to 20% Lactose equivalent
5 to 7% Spray-dried animal plasma 2 to 3% Spray-dried porcine plasma
10 to 15% Soybean meal 2 to 3% Spray-dried blood meal and (or)
3 to 6% Added fat Select menhaden fish meal
0 to 2% Spray-dried blood meal 3 to 5% Added fat
3 to 7.5% High quality fish meal 3,000 ppm Zinc oxide
3,000 ppm Zinc oxide Pellet or meal form
Pelleted
Phase 2 for pigs weighing 7 to 11 kg Phase 3 for pigs weighing 11 to 25 kg

Grain-soybean meal-based Grain-soybean meal-based
1.30 to 1.40% Lysine 1.15 to 1.30% Lysine
.36 to .38% Methionine .32 to .36% Methionine
6 to 8 % Lactose equivalent No added specialty ingredients
2 to 3% Spray-dried blood meal 0 to 6% Added fat
or 3 to 5% High quality fish meal 100 to 250 ppm Copper sulfate
0 to 3% Added fat Pellet or meal form
2,000 ppm Zinc oxide
Pellet or meal form
following protein sources often are used in combination in the SEW diet to meet
the amino acid requirements and to stimulate feed intake: spray-dried plasma
protein, fish meal, skim milk, whey-protein concentrate, spray-dried egg protein,
spray-dried blood meal, soybean meal, and further processed soy products. At the
present time, the only protein source considered somewhat essential in this diet
is spray-dried animal plasma because of its influence on feed intake. The SEW diet
often contains 5 to 7% plasma. Other protein sources used in the SEW diet will
depend on the availability and pricing in a particular location in relation to growth
performance benefits. The controversy surrounding the level of soybean protein
to include in this diet is discussed in the protein source section. We recommend
adding 10 to 15% soybean meal to the SEW diet in order to prepare the pig to
handle much higher levels of soybean meal in the next diets. The high cost of plasma
and detrimental effects of high levels of soybean meal limit their inclusion in the
SEW diet. Thus, other protein sources are required to increase the amino acid content
of the diet. Spray-dried blood meal (up to 2.5%) and/or a high quality fish meal
(up to 7.5%) are often the most economical protein sources other than soybean
284 Weaning the pig

meal that can increase feed intake immediately after weaning. Thus, they are often
used in SEW diets.
The SEW diet should contain 18 to 25% lactose. High levels of lactose are beneficial
for stimulating feed intake and increasing growth performance; however, care must
be taken during processing because high levels of milk products increase the difficulty
of pelleting the diet (Leaver, 1988). The appropriate added fat level in the SEW
diet depends on the level of milk products and the skill of the pellet mill operator
(Leaver, 1988). Typically, 3 to 6 % fat is added to the diet to lubricate the pellet
die. Diets containing plasma and high levels of milk products should be conditioned
at less than 77° C during pelleting (Steidinger et al., 2000).
Even though the SEW diet contains a high level of lactose, the grain source serves
as an important energy source. Further processed oat products (oat groats, oat flour)
improve diet appearance and can improve stool consistency and pig appearance.
However, research showed no differences in pig performance with diets containing
oat flour or corn ground to 600 microns (Dritz et al., 1994a). Additionally, refined
oat products are often 2 to 3 times the expense of other grain sources (corn, sorghum,
wheat, etc) and, thus, their inclusion in the diet must be carefully considered.
Growth-promoting levels of antibiotics normally are included in the SEW diet. As

discussed earlier in this chapter, research has demonstrated that ZnO at 3,000 ppm
is a better growth promotant for early-weaned pigs than copper sulfate. Addition
of high levels of ZnO is not legal in all countries; however, it provides an excellent
growth promotion response when available for commercial use. Other potential
additives in the SEW diet include dietary acids, such as propionic, fumaric, or other
acids at low levels. Research by Bergstrom et al. (1995) indicated that a buffered
propionic acid can improve growth performance and be a cost effective addition
to the SEW diet for pigs weaned at 14 d of age.
11.6.2 Transition diet - 5 to 7 kg
The transition diet is a natural extension of the SEW diet and contains many of
the same ingredients. However, feed intake increases rapidly in high-health-status
pigs that are free from immune challenge. Minimizing immune challenge limits
cytokine production, which leads to increased feed intake (Klasing, 1988; Williams
et al., 1997a). Consequently, the primary objectives when formulating a transition
diet are to provide a substantial amount of highly available amino acids in the
proper proportions and to prepare pigs to utilize less expensive diets in subsequent
phases. Selecting ingredients that stimulate feed intake is still an important but
secondary objective. The importance of maximizing growth performance and
optimizing economic performance by using a transition diet between the first diet
postweaning and the phase 2 diet was demonstrated by Dritz et al. (1996a).

The main difference between a conventional phase 1 diet and the transition diet
is the level of spray-dried animal plasma, which is added to the diet primarily to
increase feed intake. Because pigs receiving the transition diet are adjusted to feed,
the diet typically contains only 2 to 3% spray-dried plasma protein compared to
5 to 7% in the SEW diet. In addition, the response to adding spray-dried animal
plasma in the transition diet has not been as consistent as the response in the SEW
diet. In one experiment, pigs failed to exhibit increased growth performance when
plasma protein and (or) select menhaden fish meal were added to diets containing
2.5% spray-dried blood meal and 20% edible-grade dried whey (Bergstrom et al.,
1997). This experiment used pigs from a high-health-status herd and was conducted
in a facility operated all in-all out by site. In a subsequent experiment by the same
authors, growth performance of 5- to 7-kg pigs was improved by feeding a transition
diet containing 2.5% spray-dried plasma protein, 2.5% spray-dried blood meal,
and 20% edible-grade dried whey compared to a transition diet without spray-dried
plasma protein. The major difference was that the second trial was conducted on
a farm in which the nursery was operated on an all in-all out basis by room and
multiple rooms were in the same nursery complex. Until further research is
conducted, we support a standard recommendation of including 2.5% spray-dried
plasma protein in the transition diet, but recognize that the level may need to be
customized to a particular herd depending on health status.
Spray-dried blood meal and (or) a high quality fish meal also are used commonly
in the transition diet as major protein sources. However, as with the SEW diet,
inclusion level and source of proteins will depend up the balance between quality
and price. Because the pigs were acclimated to soybean meal while being fed the
SEW diet, the transition diet can contain higher levels of soybean meal (20 to 25%)
without risk of hypersensitivity. The addition of soybean meal also further
prepares the pig to efficiently utilize the less expensive diets in the successive phases.
The lactose level in the transition diet often is decreased compared to the SEW diet.
However, it is still critical that the transition diet contain at least 15% lactose for
optimal pig performance. A high quality fat source (3 to 6%) is added to the
transition diet for the same reason as the SEW diet (improved pellet quality). As
in the SEW diet, antibiotics, ZnO (3,000 ppm), and acidifiers should be maintained
in the transition diet as growth promoters.
11.6.3 Phase 2 - 7 to 11 kg
By the time the pigs in an SEW system weigh 11 kg, they already will have consumed
3 to 5 kg of feed. With feed intake rapidly increasing in these high-health-status
pigs, stimulating feed intake is less of a concern in this phase. Moreover, the major
concern when formulating this diet is to provide high levels of amino acids to
maximize protein deposition. The specialty products are needed only at minimal
286 Weaning the pig

levels to maximize growth performance, minimize cost, and efficiently shift pigs
to simple grain-protein source diets in the subsequent phases. Feeding behavior
is well adjusted and, thus, lower cost, less complex diets can be fed. Therefore, in
order to reduce total feed cost, that spray-dried plasma protein should not be
included in this diet.
The phase 2 diet is typically a grain-soybean meal-based diet with a high quality
source of lactose and a small amount of a specialty protein source; common choices
include spray-dried blood meal or high quality fish meal. Research has shown
consistently that these two protein sources result in similar performance for the
phase 2 diet (Kats et al., 1994b). Therefore, the choice of protein source will depend
on economics. Other specialty protein sources may be used in this diet depending
on economic considerations of a particular producer or location.
Research has shown an interaction between the inclusions of high quality fish meal,
such as select menhaden fish meal, and dried whey in the phase 2 diet (Stoner et
al., 1990). Those researchers found that when 4% select menhaden fish meal and
10% dried whey were added to the phase 2 diet, pig growth performance was similar
to that of pigs fed 20% dried whey and no fish meal. Other research indicated that,
when 2.5% spray-dried blood meal was used, approximately 10% dried whey in
the phase 2 diet resulted in the optimum balance between economics and pig growth
performance (Dritz et al., 1993). Additional research indicated that edible-grade
lactose is an acceptable substitute for dried whey in the phase 2 diet (Crow et al.,
1995). Therefore, we recommend supplementing the phase 2 diet with edible-grade
dried whey or another high quality lactose source.
If an economical fat source is available, the phase 2 diet should contain 3 to 5%

added fat. As with the SEW and transition diets, growth-promoting antibiotics and
ZnO are added to the phase 2 diet. However, research indicated that a lower level
(2,000 ppm) of ZnO results in optimum growth performance (Smith et al., 1999a).
Many producers make the phase 2 diet on their farms and feed it in a meal form.
Research has shown an approximately 14% improvement in feed efficiency by
feeding this phase in pellet form (Stark et al., 1994). The improvement in feed
efficiency will depend on diet formulation, pellet quality, and feeder adjustment.
However, the advantage of improvement in feed efficiency must offset the
disadvantage of the increased cost to obtain the diet in the pellet form.
11.6.4 Phase 3 - 11.5 to 23 kg
The strategic intent of the SEW, transition, and phase 2 diets using the various
combinations of specialty protein and carbohydrate sources is to efficiently
prepare the pig to use a low cost, simple phase 3 diet. Thus, the objective when

formulating the phase 3 diet for SEW pigs is to provide a simple grain-protein source
diet formulated to provide high levels of amino acids. The later are needed to
maximize lean tissue deposition. With proper dietary transition in the previous
phases, a simple grain, protein source diet can be fed by this stage.
The phase 3 diet is the lowest cost diet in the SEW nursery-feeding program. However,
because consumption of the phase 3 diet is the greatest (Table 11.5), it usually accounts
for 50% of the total feed cost from weaning to 23 kg. Thus, cost of this diet is critical
to minimize total feed cost while maximizing performance in the nursery. Specialty
ingredients, such as spray-dried blood meal, fish meal or dried whey are cost
prohibitive, because research has failed to indicate improved growth performance from
feeding such ingredients in phase 3 (Kats et al., 1994a). The fat level of the diet will
depend on the ability of the producer to economically purchase fat. Pigs will show
improved average daily gain and feed efficiency with increasing levels of fat in the phase
3 diet. Thus, 3 to 6% added fat is a common recommendation based on economics.
As with the SEW and transition diets, growth-promoting antibiotics are added to the
phase 3 diet. Because there is no advantage in growth performance and high levels
of excretion can occur, high levels of ZnO should not be fed during this phase. Many
nutritionists add copper sulfate (125 to 250 ppm) to this diet as a growth promoter.
11.7 Importance of management in the success of

the nutritional program
A successful nutritional program is not measured by projected cost of feed
delivered to the barn. Properly designed diets and feed budget are not enough to
ensure success. Several management factors are critical to the success of the feeding
program. The two biggest keys in management of the feed program in the barn
are a) proper management to encourage feed intake, and b) adjusting feeders to
minimize feed wastage.
Table 11.5. Example feed budget (amount, kg, of each diet that should be fed per pig;
Dritz et al., 1996b).
Weaning Age and Initial Weight
14 d 21 d 24 d
Diet Pig weight, kg 4 kg 5.9 kg 6.8 kg
SEW < 5 kg 0.9 0.4 ---

Transition 5 to 7 kg 2.3 0.9 0.9
Phase 2 7 to 11 kg 6 6 5
Phase 3 11 to 25 kg 23 23 23
288 Weaning the pig

11.7.1 Management to encourage feed intake
Numerous management procedures are critical to maximizing feed (energy)

intake and improving performance in the nursery. The factors necessary to
maximize feed intake include a warm draft-free environment and an overall herd
health program and pig flow that minimizes exposure to antigens. Providing easily
accessible drinking water fixtures and unlimited water supply is essential as there
is a linear relationship between water intake and feed intake in weaner pigs (Brooks
et al., 1984). An often overlooked but critical need, is a dedicated workforce that
can identify the signs of a “starve” out pig (Table 11.6) and then gently “teach”
the pig where and how to eat (Dritz et al., 1996b), with either mat or individual
feeding. Some pigs simply don’t start eating readily after weaning. Teaching these
“starve” out pigs to eat, rather than treating them with an antibiotic, will save more
pigs. Lastly, one of the most important factors in maximizing feed intake is allowing
ad libitum access to feed. Many times when pigs exhibit post-weaning diarrhea or
loose stools, producers will begin to limit-feed pigs thinking that this will
minimize the severity of the post weaning scours. However, failure to investigate
causative agents like improper air temperature or ventilation, poor sanitation, or
inappropriate ingredient selection or quality can lead to failure to solve the primary
problem. Limit feeding in the nursery results in reduced nursery exit weights. This
is demonstrated by the exit weight of nursery groups in a large production system
(Figure 11.5). Exit weights typically averaged 18 to 22 kg when nursery managers
limit fed pigs the initial week after weaning. However, when management switched
to ad libitum feeding by always having feed present in the trough throughout the
entire nursery phase (8 weeks), feed intake and exit weights increased dramatically.
Table 11.6. Conditions to Identify “Starve-out” Pigs.
• Mental status - alert or depressed

• Body condition - normal or thin
• Abdominal shape - round or gaunt
• Skin - sleek appearance vs fuzzy
• Appetite -feeding at the feeder or huddled
• Signs of dehydration - normal or sunken eyes
11.7.2 Adjust feeders frequently to minimize feed wastage
Proper and frequent feeder adjustment is the key to excellent feed efficiency and
low feed cost in the nursery. Proper feeder adjustment starts with the first additions
of feed to the feeder. Regardless of whether the first diet after weaning is in bags
or bulk, the feed gate in all feeders should be closed before the first pellets are placed

32 850
Feed intake
28 750
Exit wt, kg
ADFI, g
Exit wt
24 650
20 550
Management change
16 450
1 2 3 4 5 6 7 8
Grou p
Figure 11.5. Changes in nursery exit weight and feed intake as a result of switching
from limited- to ad libitum nursery feed intake (Dritz, 2002).
in them. The feed gate then should be opened so that a small amount of feed if
visible in the feed pan. Placing pelleted feed into an empty feeder with the agitation
gate open will result in large amounts of feed filling the trough leading to feed
wastage and difficulty in achieving the proper feeder adjustment.
Although adequate amounts of feed must be present in the feeder at all times after
weaning, too much feed present in the pan of the feeder also can decrease growth
rate. In an attempt to stimulate feeding behavior, some producers place large
amounts of the first diet in the feeding pan. Although the intention is correct, the
outcome is negative. Energy deficiency can result from pigs “sorting” the diet and
a buildup of fines in the feeding pan. These fines then lodge in the feed agitator
mechanism, making it difficult for new feed to flow from the feeder. This problem
can be corrected by managing the amount of feed flow in the pan to stimulate
development of feeding behavior. Approximately 50% of the feeding pan should
be visible in the first few days after weaning. As the pigs become more accustomed
to the location of the feed and adjust feeding behavior, the amount of the feed in
the feeding pan should be decreased rapidly to less than 25% coverage. Also, feed
agitators need to be tested frequently to ensure that the buildup of fines does not
prevent them from working freely.
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296 Weaning the pig

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12 Intestinal nutrient requirements in
weanling pigs
D. Burrin and B. Stoll
12.1 Introduction
In the postnatal life of the pig, the period of weaning is marked by significant changes
in nutrition and the environment. The extent to which the young pig can adapt
physiologically to these changes determines its survival, health and subsequent
growth rate. Of particular importance to this adaptation process is the functional
development of the gastrointestinal tract, particularly digestive, absorptive and
immune function. In the past few years, there has been considerable progress in
our understanding of intestinal nutrient metabolism, particularly in young pigs.
However, despite its overall importance to the pig’s health and adaptation the impact
of weaning on the rate and pattern of intestinal nutrient utilization remains a poorly
understood, yet critical, nutritional issue. The aim of this chapter is to first briefly
review the underlying changes in the gastrointestinal physiology of the weanling
pig and then to describe how these changes impact the nutrient needs of the
gastrointestinal tract and the animal as a whole. Although this chapter will focus
mainly on the small intestine, the nutrient requirements necessary to support
physiological functions in other components of the gastrointestinal tract during
weaning are also mentioned, including the stomach, large intestine and pancreas.
12.2 Changes in gut physiology during weaning

During the process of weaning, there are several key nutritional and environmental
factors that contribute to significant changes in structure and function of the
gastrointestinal tract; many of these factors are reviewed in detail in this book and
elsewhere (Maxwell and Stewart 1995; Pluske et al. 1995; Pluske et al. 1997; Fraser
et al. 1998; Gaskins 1998; Dreau and Lalles 1999; Le Dividich and Seve 2000; Stokes
et al. 2001). These factors are as follows, 1) the change in mode of nutrient ingestion,
namely from suckling milk from the dams udder to ingestion of feed from a feeder,
2) the change in the physical and chemical composition from a liquid to a dry
diet, 3) the psychological and behavioral stress associated with the change in mode
of nutrient ingestion, withdraw from the sow and mixing with unfamiliar pigs, and
4) the qualitative and quantitative changes in the gut microflora. During the process
of weaning, these factors simultaneously interact with each other to produce
temporal changes in gastrointestinal structure and function. For the purpose of this
discussion, these temporal changes are divided into the acute phase observed within
the first five to seven days after weaning and the adaptive phase that occurs
subsequently (Figure 12.1). The distinction between acute and adaptive phases is

Burrin and Stoll
1600 400
Pre-weani ng
0.75
1400 350
Energ y in take, MJ/kg
300
1200
Weight gain, g/d

250
1000
200
800
150
600
100
400 Energy int ake
50
Weight gain
200 0
Acut e phase Adapt ive phase
0 -50
1 5 10 15
Days post-weaning
Figure 12.1. Changes in energy intake and weight gain in young pigs before and after
weaning. Pigs were weaned from the sow at 14 days of age and fed a corn-based diet
containing soy or whey protein (24% crude protein and 14.8 MJ energy). Adapted from
Jiang et al. 2000.
based primarily on the changes in feed intake, since it takes about seven days for
weaned pigs to learn how to eat out of a feeder and resume an intake that is
comparable to that during the pre-weaning period (Pluske et al. 1997; Le Dividich
and Seve, 2000).
12.2.1 Acute phase
The dominant factor affecting gut structure and function during the acute phase
after weaning is the reduction in feed intake (Figure 12.1). Although the underlying
cause of the loss of appetite has not been clearly established, it is likely due to the
psychological and behavioral stress associated with the change in mode of nutrient
ingestion, withdraw from the sow and mixing with unfamiliar pigs. However, the
impact of reduced feed intake on the gut is clearly evident in the diminished overall
mass and mucosal structure of the small intestine (Figure 12.2). The reduced feed
intake appears to have a limited effect on stomach weight, however, the weight of
the colon is increased approximately threefold within seven days after weaning
(McCracken et al. 1995; Jiang et al. 2000). During the acute phase, there is a
significant reduction in protein and DNA mass, as well as villus height, in the small
intestine. In general, studies show that villus height is reduced approximately 50%
within the first three to five days after weaning (Pluske et al. 1997). Despite the
overall reduction in DNA content and villus height during the acute phase, the depth
and rate of proliferation in the crypt compartment increases substantially, indicative
of crypt hyperplasia. In addition, there is also an increased cell density in the lamina
302 Weaning the pig

Intestinal nutrient requirements in weanling pigs
300 200
250 Protei n mass

Percent of pre-weaning
Percent of pre-weaning
DNA mass
150
200
Vill us height
150
Crypt dept h 100
Cell pr oliferation
100
50
50
Acute phase Adaptive phase Acute phase Adaptive phase
1 5 10 15 1 5 10 15
Days pos t-weaning Days pos t-weaning
Figure 12.2. Changes in intestinal morphology, cell proliferation and mass in young
pigs before and after weaning. Pigs were weaned from the sow at 14 days of age and
fed a corn-based diet containing soy or whey protein (24% crude protein and 14.8
MJ energy). Adapted from Jiang et al. 2000.
propria of the villus region, indicative of increased infiltration and proliferation

of lymphoid cells (Jiang et al. 2000).
The reduction in gut mass and mucosal thickness in response to reduced feed intake
is a well known phenomenon (Bragg et al. 1991). In young pigs, the absence of
nutrients in the intestinal lumen, as a result of either reduced feed intake or
parenteral nutrition, leads to reduced cell proliferation, protein synthesis and villus
atrophy (Davis et al. 1996; Burrin et al. 2000; Stoll et al. 2000). The underlying
factors that mediate the loss of gut mass are multifactorial, but include deprivation
of lumen substrates for mucosal epithelial cell growth and reduced secretion and
expression of humoral gut growth factors, such as glucagon-like peptide 2 and IGF-
I (Carroll et al. 1998; Burrin, 2001; Stoll and Burrin, 2001). The crypt hyperplasia
that occurs despite the reduction in feed intake, however, is somewhat unexpected
and may be linked to several factors. One of the most important factors in
hyperplasia of both the crypt epithelium and lamina propria region is believed to
be gut hypersensitivity reactions in response to components in the weaning diet,
namely plant proteins, such as soy glycinins and lectins, and fiber (Jin et al. 1994;
Dreau and Lalle 1999; Jordinson et al. 1999). However, an additional factor that
contributes to increase in lymphoid cell density within the intestinal mucosa is
the normal development of adaptive immune function (Gaskins 1998; Kelly and
Coutts, 2000). During the acute phase of weaning, the pig is especially vulnerable
to pathogenic infection in part because of the abrupt withdraw of sow’s milk, which
contains numerous factors that bolster the intestinal immune defense. In addition,
however, the changes in the diet composition and the environment lead to a shift

Burrin and Stoll
in the colonization of commensal gut microorganisms, providing a situation for

growth of opportunistic pathogenic organisms. Pathogenic infection results in an
activation of the mucosal immune system and release of proinflammatory
cytokines (e.g. tumor necrosis factor α and interleukins) that have been shown to
increase crypt cell proliferation and villus enterocyte apoptosis (Rafferty et al. 1994;
Piguet et al. 1999). Infection, the presence of bacteria and proinflammatory cytokines
also have been shown to increase the synthesis of intestinal acute phase proteins
and mucins (Higashiguchi et al. 1994; Breuille et al. 1998; Wang et al. 1998; Mack
et al. 1999). Thus, there would appear to be a general increase in protein metabolic
activity associated with activation of the mucosal immune system, yet this is in
contrast to the observed loss of intestinal protein mass during the acute phase of
weaning (Figure 12.2). This loss of intestinal protein indicates a relative increase
in the balance of proteolysis versus protein synthesis. A plausible explanation for
the acute phase loss in intestinal protein mass is the apoptotic death and
proteolytic degradation of villus enterocytes. However, there is very little published
information about the temporal changes in gut protein metabolism during the acute
phase of weaning.
12.2.2 Adaptive phase
During the adaptive phase of weaning, the pig has regained its appetite and feed
intake is and comparable to, or in excess of, the preweaning intake (Figure 12.1).
The resumption of relatively normal feed intake is marked by significant increases
in the masses of the small intestinal, stomach and large intestine; however the levels
attained are in excess of those observed during preweaning (Figure 12.2) (Kelly et
al. 1991b; Jiang et al. 2000; McCracken et al. 1995). Within the small intestinal
mucosa the villus height increases to a small degree, but does not return to the
preweaning levels. The depth of the crypt compartment continues to increase, yet
the rates of proliferation appear to plateau.
Based on the few reported studies with weaned pigs, it would appear that the increase
in intestinal protein mass after weaning is accompanied by a significant increase
in the protein synthesis rate (Table 12.1) (Seve et al. 1986; Seve et al. 1993; Nyachoti
et al. 2000). This relative increase in small intestinal protein synthesis rate after
weaning may stem from the higher dry matter intake, but also could be linked to
presence of fiber and plant proteins, such as lectins (Southon et al. 1985; Palmer
et al. 1987). Moreover, there is evidence that the rates of protein synthesis are also
higher in the large intestine in young pigs fed a higher fiber (69%) cereal-based
diet than in those fed a low fiber (21%) diet containing casein and starch
(Nyachoti et al. 2000). These observations, coupled with the marked increase in
mass of the small and large intestines, suggest that the amino acid requirement
necessary to support gastrointestinal tissues are substantially higher during the
adaptive period of weaning.
304 Weaning the pig

Table 12.1. Fractional protein synthesis rates in tissues of young, milk-fed piglets and
weaned, growing pigs1.
Young-Milk-fed2 Weaned-growing3
Pancreas 60 -103 162

Stomach 32 nd
Jejunum 39 - 79 98 - 119
Ileum 53 104
Cecum nd 123
Colon nd 138
Liver 56 - 72 52 - 68
Muscle 6-8 3 - 33
Skin 13 nd
Kidney 25 nd
Spleen 14 nd
1 Values are expressed as %/d based on the bolus-dose phenylalanine method.

2 Values obtained from Davis et al. 2001; Burrin et al. 1999b; and Davis et al. 1996.
3 Values obtained from Nyachoti et al. 2000 and Seve et al. 1993.
The increased dry matter intake not only stimulates growth of the small and large
intestine, but the increase in fiber content and decreased digestibility of weaning
diets have further implications. First, there is an increase in the number of the colonic
microflora that translates into increased fermentation and production of short-chain
fatty acids (SCFA) (Risley et al. 1992; Maxwell and Stewart 1995). It is noteworthy
that the SCFA concentrations have been reported to increase not only in the lower
colon, but also increase several-fold in the stomach and jejunal fluid (Risley et al.
1992). Studies with colonocytes have demonstrated that SCFA may be used both
as oxidative substrates and as a stimulus of cell proliferation (Darcy-Vrillon et al.
1993; Darcy-Vrillon et al. 1996; Sakata and Inagaki, 2001), yet the capacity for SCFA
oxidation in enterocytes in the small intestine is lower than colonocytes (Fleming
et al.1991). A second potentially important consequence of increased SCFA
production in the lower intestine and colon is the stimulus of intestinal blood flow
(Kvietys and Granger, 1981). Furthermore, increased colonic SCFA stimulate gut
hormone secretion, in particular glucagon-like peptide 2 (GLP-2). GLP-2 is a potent
nutrient-dependent gut growth factor (Burrin et al. 2001). Studies in rats show that
feeding fiber and infusion of SCFA upregulates the expression of proglucagon in
the distal bowel and this is associated with increased circulating concentrations
of GLP-2 (Reimer and McBurney, 1996; Tappenden et al. 1998). The increased
circulating GLP-2 may serve as an indirect gut trophic signal that mediates the
increase in cell proliferation that is observed under these two conditions. These

Burrin and Stoll
observations suggest that, in the weaned pig, the increased production of SCFA
may trigger increased secretion of GLP-2 and explain the increase in crypt cell
proliferation.
The adaptive phase of weaning is also characterized by substantial increases in

digestive enzyme capacity, particularly gastric proteases and pancreatic proteases
and α-amylase activity (Lindemann et al. 1986; Kelly et al. 1991c;Cranwell, 1995;
Bach Knudsen and Jorgensen, 2001). In addition, there is a significant increase in
the activity and capacity of maltase and glucoamylase in the small intestine. The
increase in these carbohydrate digestive enzymes is diet-induced and a function
of the increased starch content found in most cereal-based weaning diets.
Furthermore, the increased pancreatic digestive enzyme production is associated
not only with increased specific activity, but also increased volume of pancreatic
enzyme output (Pierzynowski et al. 1990; Pierzynowski et al. 1993). The proteins
secreted from the pancreas, as well as the stomach, small and large intestine and
gallbladder, are collectively referred to as endogenous proteins. An important
nutritional consideration with respect to endogenous protein secretion is the extent
to which these endogenous proteins are digested and the amino acids reutilized
by the intestine. In particular, the mucin glycoproteins are a class of proteins present
in endogenous secretions that play an important role in the innate barrier function
throughout the gastrointestinal tract (Deplancke and Gaskins 2001). Given their
role in gut barrier function, one could predict that goblet cell density and mucin
secretion might increase after weaning, and there is some evidence to support this
in pigs (Brown et al. 1988). The production of mucins may be nutritionally
significant, in that, because they are relatively resistant to digestion within the small
intestine, the amino acids present in the mucin glycoproteins are not reabsorbed,
but instead are catabolized by microbial fermentation in the large intestine. There
is very little quantitative information as to the extent to which mucins and other
gastrointestinal secretions are digested, and their constituent amino acids and hexose
molecules are reabsorbed or fermented in the colon.
12.3 Intestinal nutrient utilization in young pigs

In the past five years, there have been significant advancements in the our
understanding of intestinal nutrient metabolism in young pigs. Quantitative
estimates of intestinal nutrient utilization and their impact on whole animal nutrient
requirements have been determined from in vivo studies in pigs using isotopic tracers
and measurements of trans-organ balance of substrates, such as glucose and amino
acids (Ebner et al. 1994; Reeds et al. 1996; Bertolo et al. 1998; Stoll et al. 1998;
Stoll et al. 1999; Van Goudoever et al. 2000; Van der Schoor et al. 2001). These
and other studies with cultured porcine intestinal enterocytes have revealed
important qualitative characteristics of the metabolic fate of key substrates and the
underlying cellular basis for intestinal nutrient utilization (Blachier et al. 1991;
306 Weaning the pig

Blachier et al. 1992; Blachier et al. 1993; Darcy-Vrillon et al. 1994; Blachier et al.
1995; Wu, 1998; Wu and Morris, 1998; Rhoads,1999). The recent advances in our
understanding of intestinal nutrient metabolism in young pigs fed milk-based diets
compliment the earlier pioneering studies with adult (50 to 70 kg body weight)
pigs published over the past twenty years (Rerat et al. 1984; Rerat et al. 1987; Rerat
and Simoes-Nunes, 1988; Rerat et al. 1988; Rerat and Simoes-Nunes 1988; Rerat
et al. 1992; Yen et al. 1997). However, despite the breadth in our current
knowledge, there is still a significant gap in our understanding of the intestinal
nutrient metabolism in young weanling pigs consuming conventional cereal-based
diets.
12.3.1 Physiological and cellular basis of gut metabolism
12.3.1.1 Relative metabolic rate
Much of what we know about intestinal nutrient utilization is derived from studies
that have measured the metabolic exchange of nutrients across the portal-drained
visceral (PDV) tissues. The PDV tissues are comprised largely of gastrointestinal
tissues, including the stomach, pancreas, small and large intestine, but also
includes the spleen. In pigs, the PDV tissues contribute approximately 5% of body
weight, yet they account for 20% to 35% of whole-body protein turnover and energy
expenditure (Yen et al., 1997; Stoll et al., 1999a; Van Goudoever et al. 2000). The
disproportionate impact of gastrointestinal tissues on whole-body metabolism is
a function of their relatively high fractional rates of protein synthesis and oxygen
consumption. Studies in pigs have demonstrated that the fractional protein
synthesis rates in the gastrointestinal tissues are substantially higher than that in
peripheral tissues, especially skeletal muscle (Table 12.1) (Simon et al. 1982; Seve
et al. 1986; Burrin et al. 1992; Davis et al. 1996). However, there are also
differences within the tissues of the gastrointestinal tract, where protein synthesis
rates are higher in the small intestine than in the stomach and large intestine (Attaix
and Arnal, 1987; Attaix et al., 1992; Burrin et al., 1999a; Burrin et al. 1999b; Stoll
et al. 2000).
The high rates of metabolism and nutrient utilization in the gut are directly linked
to the high rates of proliferation, protein secretion, cell death and desquamation
of various epithelial and lymphoid cells within the mucosa. In young pigs, epithelial
cells have a life span of about three to ten days (Fan et al., 2001). Within the small
intestinal epithelium, the proliferative crypt compartment contains pluripotent stem
cells which undergo mitosis and differentiation into four cell lineages: absorptive
enterocytes, mucin-producing goblet cells, antibacterial peptide-producing Paneth
cells, and enteroendocrine cells. In addition, present in the lamina propria region
beneath the epithelium are lymphoid and other cell types including, T and B
lymphocytes, macrophages, neutrophils, mast cells, dendritic cells and fibroblasts.

Burrin and Stoll
Studies in vitro show that these epithelial (Higashiguchi et al. 1993; Wu 1998) and
lymphoid (Szondy and Newsholme, 1990; Wu et al. 1991; Dugan et al., 1994) cell
types exhibit high rates of protein synthesis and glutamine metabolism. In the case
of goblet cells, there is a substantial utilization of nutrients for mucin secretion,
which make up a large component of endogenous secretions that are fermented
in the colon (Lien et al., 1997).
12.3.1.2 Luminal versus arterial nutrient utilization
Another critical anatomical consideration with respect to the metabolism of

intestinal epithelial cells is that they derive nutrients from two separate sources:
the luminal route via the diet and from the blood via the arterial circulation.
Estimates derived from studies in piglets fed a milk-based formula indicate that
the absolute rate of nutrient input to the PDV tissues from the arterial circulation
is significantly greater than from the diet (Figure 12.3) (Stoll et al. 1998). The diet
represents less than 30% of the total nutrient input to the PDV tissues, with the
exception of aspartate. However, there is a preferential utilization of some amino
acids from the luminal route, namely glutamate and glutamine (Table 12.2). When
expressed as a percentage of the inputs, the uptakes of glutamate and glutamine
are 96% and 67% from the lumen and 11% and 21% from the arterial circulation,
respectively. Interestingly, the uptake of luminal glucose, both on a relative and
absolute basis, is considerably less than that of amino acids. Instead the use of
glucose by the PDV tissues is preferentially derived from the arterial circulation.
Although the relative rate of extraction from the arterial input is nearly equal to
100
Tissu e Free Isotopic en richment
Prox ima l Jejunum

Distal Ileu m
% plasma enrichmen t
80
60
40
20
P < 0.05 vs 0%
0
0 20 40 60 80 100
Enteral intake, % total intake
Figure 12.3. Rates of amino acid input into the PDV tissues from the diet and arterial
circulation in young piglets. Dietary inputs were based on intake of sow’s milk replacer
fed at 12 g protein/kg per day. Arterial inputs were calculated from measurements of
arterial amino acid concentration and portal blood flow rate; this assumed arterial
and portal blood flow to be equal. Adapted from Stoll et al. 1998.
308 Weaning the pig

Table 12.2. Relative portal utilization of glucose, glutamate and glutamine from the
luminal and arterial sources in piglets fed a milk-based formula.1
Glucose Glutamate Glutamine
Luminal
Input 3,400 585 219
Uptake 217 562 147
% 6.4 96 67
Arterial
Input 18,874 731 934
Uptake 1227 80 191
% 6.5 11 21
1Data are expressed as µmol•kg-1•h-1 , unless otherwise indicated. Calculated from Stoll
et al. (1999a).
that from the diet, the absolute rate of arterial glucose utilization is substantially
greater than the combined uptake of both glutamate and glutamine. Thus, the
utilization of glucose by PDV tissues is derived largely from the arterial circulation
(85% total), with only a small contribution from the diet (15%).
The general preference for arterial nutrients is perhaps not surprising if one considers
how nutrients are normally presented to the PDV tissues. Under normal conditions,
when animals are fed diets with polymeric forms of carbohydrate and protein, the
level of free glucose and amino acids in the lumen is relatively low in the stomach
and large intestine. Because the digestive environment in the stomach and large
intestine limits the luminal availability of glucose and amino acids, the nutrient
needs of these tissues must be met by the arterial circulation. This idea should also
hold for the proximal versus distal small intestine, if one assumes that most of the
dietary carbohydrate and protein is digested and the resulting monosaccharides
and amino acids are absorbed efficiently in the proximal intestine. To demonstrate
this, we studied neonatal piglets infused intravenously with 3H-leucine and then
administered increasing amounts of their total nutrient intake intragastrically, while
maintaining a constant total nutrient intake via intravenous nutrient infusion (Stoll
et al. 2000). The results showed that in piglets receiving 100% of their nutrient
intake via the enteral route, the proportion of systemically-derived labeled leucine
in the mucosal free amino acid pool is significantly greater in the distal ileum than
the proximal jejunum (Figure 12.4). The results also show that as increasing amounts
of nutrients were infused via the enteral or luminal route, there was a marked
decrease in the isotopic enrichment in the proximal jejunum due to increased
absorption and dilution by unlabeled enteral leucine. Additional evidence

Burrin and Stoll
N
GL P U
100 A S GL
Net portal nutrient utilization
80
% of dietary intake
R
TH
60 T
ME Y
GL L YS U R
L E SE HE AL RO
P V P
40
IL E
E
OS
UC
20 GL
Figure 12.4. Changes in the tissue isotopic enrichment of 2H-leucine in the proximal
jejunum and distal ileum of neonatal pig fed varying proportions of their total nutrient
intake via the enteral versus parenteral route. Seven day-old piglets were fed an elemental
diet either intragastrically or intravenously for seven days, then infused intravenously
with 2H-leucine for six hours prior to sampling. Adapted from Stoll et al. 2000.
consistent with this idea can be found in pigs studied during acute-phase of weaning,
where atrophy occurs primarily in the small intestine, while the mass of the stomach
and large intestine is preserved (McCracken et al. 1995; Jiang et al. 2000).
12.3.1.3 Crypt versus villus enterocytes
Another important factor that affects the extent to which epithelial cells derive their
nutrients from the luminal or vascular input is their stage of differentiation and
physical location along the crypt-villus axis. Early studies (Alpers 1972) showed
that crypt cells are more highly labeled with isotopic tracers derived from the blood,
whereas villus cells are more highly labeled with tracers given luminally. These results
implied that crypt cells derive their nutrients predominantly from the arterial
circulation, whereas villus cells rely on nutrients absorbed luminally from the diet.
If this phenomenon is true, it may explain the reduced villus length seen during
the acute-phase of weaning, because luminal nutrient supply is significantly reduced.
However, studies with animals fed via total parenteral nutrition have shown that
intestinal mucosal growth and villus height can be maintained, even in the absence
of luminal nutrients, by providing intravenous gut growth factors, such as GLP-2,
IGF-I, EGF, or SCFA (Koruda et al. 1990; Goodlad et al. 1992; Peterson et al. 1996;
Burrin et al. 2001). These studies suggest that, if an appropriate intestinal growth
stimulus is provided, villus enterocytes are not strictly dependent on luminal
nutrients and have the capacity to extract sufficient nutrients from the arterial
310 Weaning the pig

circulation necessary for survival. Further studies using simultaneous systemic and
luminal isotope labeling coupled with isolation of crypt and villus enterocytes are
warranted to characterize how stage of differentiation and spatial localization affects
the source of nutrients for epithelial cells.
12.3.2 Major oxidative fuels
12.3.2.1 Glutamine, glutamate, aspartate
A significant proportion of the dietary nutrients are metabolized by gastrointestinal

tissues, due to their relatively high metabolic rate. However, the pattern of nutrient
utilization by the PDV tissues is not uniform and some nutrients are preferentially
metabolized. A number of studies in pigs have shown that there is substantial
utilization of dietary glutamine, glutamate and aspartate by PDV tissues (Reeds et
al. 1996; Rerat et al. 1992; Van der Muelen et al. 1997; Stoll et al. 1998; Reeds et
al. 2000). Results from young piglets fed a high protein, milk-based formula
indicated that more than 95% of the dietary glutamine, glutamate and aspartate
is utilized by the gut (Figure 12.5) (Stoll et al. 1998). These results are consistent
with the seminal studies of Windmueller and Spaeth (1974, 1975, 1976, 1978,
1980), which first showed evidence of extensive metabolism of these three
substrates in in situ intestinal perfusions in fasted, anaesthetized rats. These
studies have since spawned literally hundreds of studies that have tended to focus
on the role of glutamine as the major oxidative fuel in the gut. However, it is
important to note that both glutamate and aspartate are of perhaps equal
3500
L Y AL A
G
3000 Diet
R Arterial
PDV amino acid input
2500 TH
(µmol • kg-1 • h-1)
LN
G U
2000 LE
L O
VA PR S
LY LU
1500 G
E
IL
1000
P
AS E
500 PH G
ET
AR M
Figure 12.5. Rates of net portal nutrient utilization in young piglets. Dietary inputs
were based on intake of sow’s milk replacer fed at 12 g protein/kg per day. Adapted
from Stoll et al. 1998.

Burrin and Stoll
importance as intestinal oxidative fuels. Recent studies in young pigs and humans
confirm the extensive intestinal oxidation of dietary 13C-labeled glutamate and
glutamine (Battezati et al. 1995; Stoll et al. 1999a; Haisch et al. 2000).
The metabolism of glutamine is accomplished first by the catalysis via phosphate-

dependent glutaminase and subsequently by glutamate dehydrogenase (GDH)
enzymes, both of which are present in the stomach, small intestine and colon of the
young pig (Madej et al. 1999). Interestingly, the activity of GDH is increased
approximately threefold in the small intestine after weaning. The resulting keto-acid
product of GDH is α-ketoglutarate, which is then metabolized yielding CO2 via the
tricarboxylic acid cycle. It is important to note that, although there is extensive uptake
and metabolism of these three amino acids, their carbon skeletons are not completely
oxidized to CO2 and they do not account for all of the CO2 released by the gut. The
in situ studies with perfused rat intestine and those in vivo with piglets and humans
indicate that most of the glutamine (55% to 70%), glutamate (52% to 64%) and
aspartate (52%) are oxidized to CO2 (Windmueller and Spaeth 1976; Windmueller
and Spaeth 1978; Stoll et al. 1999a). The remaining carbon atoms from these three
substrates, that are not oxidized to CO2 , are converted to lactate, alanine, proline,
citrulline, ornithine and arginine and then released into the portal circulation
(Windmueller and Spaeth 1975; Stoll et al. 1999a). The metabolic fate of nitrogen
from these amino acids is not fully understood. However, evidence suggests that a
portion of the nitrogen derived from glutamine and glutamate metabolism is
transferred to ammonia and other amino acids, including citrulline, ornithine, proline
and arginine. Other potentially important biosynthetic products of glutamine
metabolism are nucleotides used for RNA and DNA synthesis (Gate et al. 1999).
12.3.2.2 Glucose
Glucose is another important oxidative fuel for the gut, although less significant
quantitatively than glutamate, glutamine, and aspartate. Glucose is often considered
as a “primal” oxidative fuel for most mammalian tissues, yet studies by Windmueller
and Spaeth (1978) showed that the uptake of arterial glutamine and glucose are
roughly equal in the postabsorptive rodent intestine. However, we are only
beginning to understand the quantitative significance of intestinal glucose
metabolism in growing pigs fed conventional diets. Early studies in finishing pigs
reported that only 57% to 70% of a dietary glucose load was absorbed into the
portal circulation, implying that 43% to 30% is metabolized by the intestine (Rerat
et al.1984). More recent studies in piglets fed a lactose-containing, milk-replacer
have reported higher rates of glucose absorption ranging from 85% to 92%,
suggesting that only 8% to 15% of the glucose is metabolized by the gut (Stoll et
al. 1999a; Van der Schoor et al. 2001). Thus, it appears that the proportion of
intestinal utilization of dietary glucose increases with age, yet its unclear whether
this is due to age, per se, or a variety of other factors.
312 Weaning the pig

Of the glucose utilized by the gut tissues, a relatively small fraction is completely
oxidized to CO2. In the perfused rat intestine, oxidation of arterial glucose was
about 10% to 15%, whereas 29% of luminal glucose is converted to CO2
(Windmueller and Spaeth, 1980). In contrast, in vivo measurements of PDV glucose
metabolism in piglets indicate a higher fractional oxidation of arterial (28%) than
of dietary glucose (3%) (Stoll et al. 1999a). Studies with isolated porcine
enterocytes confirm the relatively low oxidation rate of glucose (~10-15%) and also
demonstrated a significant decline in both the cellular uptake and oxidation of
glucose between birth and weaning (Darcy-Vrillon et al. 1994; Wu et al. 1995). The
ontogeny of intestinal glucose oxidation in the neonatal rat appears to differ from
the pig, and studies have shown that glucose oxidation increases markedly during
and shortly after weaning (Kimura, 1996). Interestingly, however, in porcine
intraepithelial lymphocytes isolated at 21, 29 and 56 days of age, glucose oxidation
was highest after weaning at 29 days (Dugan et al. 1994). Studies in enterocytes
also show that glucose oxidation is inhibited in the presence of glutamine, but
glutamine oxidation is not altered by addition of glucose (Wu et al. 1995). Taken
together, the results indicate that intestinal tissues preferentially derive much more
energy from glutamine and glutamate than glucose. However, given the evidence
in rodents, more studies are warranted to examine the impact of weaning on
intestinal substrate utilization and whether glucose perhaps becomes a quantitatively
more significant fuel source.
A majority of the glucose carbon utilized by gut tissues is either metabolized to

lactate and alanine or used for biosynthetic purposes. In the perfused rat intestine,
43% to 58% of arterial glucose is metabolized to lactate, 13% to 19% is converted
to alanine, and approximately 25% is incorporated into intestinal tissue and
mesenteric lipid (Windmueller and Spaeth 1978; Windmueller and Spaeth 1980).
Similarly, in vivo studies with pigs demonstrate that of the relatively small fraction
of dietary glucose utilized by the PDV tissues, 45% and 37% is metabolized to lactate
and alanine, respectively (Stoll et al. 1999a). However, considerably less of the arterial
glucose (approximately 10%) is metabolized to lactate and alanine. This implies
that a large proportion of the intestinal glucose requirement, which is derived largely
from the arterial circulation, may be used for biosynthesis of structural and functional
molecules, such as mucin glycoproteins, fatty acids and lipids.
12.3.2.3 Ketones and short-chain fatty acids
In the categories of ketones and short-chain fatty acids, there are several substrates
that have been shown to be metabolized by the gut, including acetoacetate, β-
hydroxybutyrate, acetate, propionate, and butyrate. The early studies by Windmueller
and Spaeth (1978) showed that in the perfused rat intestine approximately 50%
of CO2 production was derived from oxidation of β-hydroxybutyrate (26%) and
acetoacetate (24%). Although the total utilization of ketones was only 40% of that

Burrin and Stoll
observed with glutamine and glucose, the fractional oxidation of ketones to CO2
was high (64%). There is very limited information on intestinal ketone utilization
in pigs. In general, ketogenesis is relatively low in newborn piglets and increases
with age (Adams and Odle, 1993; Tetrick et al., 1995). However, studies in rats
indicate that β-hydroxybutyrate oxidation is relatively low in suckling rats and
increases significantly after weaning (Kimura, 1996). These studies indicate the
potentially significant metabolic role of ketones as an intestinal fuel, especially under
fasting conditions during the acute-phase of weaning, when ketones may be elevated
in the blood.
Short-chain fatty acids or volatile fatty acids are also potentially important
oxidative substrates. The total concentration of SCFA in luminal contents of
postweaned pigs are relatively high (~500-4000 mM) not only in the cecum, but
also in the stomach and jejunum (Risley et al. 1992). The most abundant SCFA
in the stomach and jejunum is acetate with negligible concentrations of propionate
and butyrate. In the cecum, acetate is also the most abundant SCFA, but there are
significant concentrations of propionate and butyrate; the molar proportion of
acetate, propionate and butyrate is 54%, 28% and 18%, respectively. In finishing
pigs fed a corn-fish meal diet, the rate of portal SCFA absorption is approximately
1000 µmol•kg-1•h-1 with the relative proportions of acetate, propionate and
butyrate being 52%, 38% and 10% (Rerat et al. 1987). In vivo studies in fasted dogs
indicate that the fractional extraction of circulating acetate by the PDV is high (~70%)
and represents approximately 5% of whole body acetate utilization (Pouteau et
al. 1998).
Studies in finishing pigs indicate that SCFA can represent up to 25% of whole body
energy expenditure (Yen et al. 1991), yet we know little about the extent of SCFA
metabolism specifically by gut tissues in pigs. Studies in rodents and ruminants
indicate that there is significant metabolism of all three of the major SCFA by
intestinal tissues (Bergman, 1990; Fitch and Fleming, 1999). The recent study using
the luminally-perfused rat colon indicates that approximately 10% to 20% of the
acetate and butyrate are oxidized to CO2 and substantial amounts of butyrate are
metabolized to β-hydroxybutyrate and lactate (Fitch and Fleming, 1999). Moreover,
when a complete mixture of substrates was perfused, as much as 40% of the butyrate
was preferentially metabolized relative to acetate (20%).
12.3.3 Essential amino acid utilization
12.3.3.1 Metabolic fate
The metabolic fate of dietary essential amino acids utilized by the intestinal tissues
has a critical influence on their availability for growth. Essential amino acids can
be used for three major metabolic purposes: (1) incorporation into protein; (2)
314 Weaning the pig

conversion via transamination into other amino acids, metabolic substrates and
biosynthetic intermediates; and (3) complete oxidation to CO2. Amino acids
incorporated into cellular protein can be degraded within the mucosal cells and
released into the portal circulation. In addition, amino acids incorporated into
cellular protein also can be secreted or sloughed into the gut lumen and then be
degraded and reabsorbed into the portal circulation. In either of the latter two
scenarios, the amino acids are “recycled” back into the body and are available for
lean tissue growth. However, when amino acids are metabolized irreversibly to either
non-amino acid intermediates or completely into CO2 , they become unavailable
for lean tissue growth. The following discussion will highlight the importance of
various essential amino acids for gut function and how this may impact their dietary
requirement in the weanling pig.
12.3.3.2 Intake level, chemical form, and digestibility
Studies of net portal amino acid balance in pigs suggest that the intestinal
utilization of essential amino acids is significant, ranging from 30% to 85% of the
dietary intake (Figure 12.6) (Rerat et al. 1988; Van Der Meulen et al. 1997; Stoll
et al. 1998; Van Goudoever et al. 2000; Van Der Schoor et al. 2001). Among the
studies with pigs using the portal A-V balance approach, a number of factors have
been shown to affect net absorption and utilization of dietary essential amino acids,
including the level of intake and chemical form. Recent studies in young pigs fed
cow’s milk-based liquid diets, demonstrated that the PDV utilization of essential
amino acids, expressed as a proportion of the dietary intake, is significantly higher
in pigs fed a low- (10%) versus high-protein (25%) diet (Van Goudoever et al. 2000;
125
High protein
Low protein
Portal amino acid utilization
100
75
% intake
50
25
0
THR LYS ILE PHE LEU
Figure 12.6. Net rates of portal essential amino acid utilization in young pigs fed either
a high (25%) or low (10%) protein diet for seven days. Adapted from Van Goudoever
et al. 2000.

Burrin and Stoll
Van Der Schoor et al. 2001). These and other previous (Ebner et al. 1994) studies
found that gut growth was preserved despite a reduced rate of whole body growth
when pigs are fed a low-protein diet. The critical implication from these studies
in that there is a preferential utilization of amino acids by the gut such that, when
the dietary intake is markedly reduced, it limits the net absorption and availability
of dietary amino acids for peripheral lean tissue growth.
Another factor that appears to affect the intestinal utilization of dietary essential
amino acids is the chemical form in which they are fed. Studies with finishing pigs,
found that the portal absorption of amino acids was significantly lower when fed
as free amino acids than as peptides (Rerat et al. 1988). These findings have
implications for feeding crystalline amino acids in weanling pig diets and suggest
that there is preferential intestinal utilization of supplemented free amino acids
compared to those fed as intact proteins. This preferential intestinal utilization of
crystalline amino acids may contribute to the reduced availability and increased
catabolism reported for free versus protein-bound lysine (Batterham and Bailey
1989; Daenzer et al. 2001). Although the intestinal absorption of crystalline free
amino acids is assumed to be 100%, further studies are warranted to establish their
“portal availability” in pig diets. Other studies in grower pigs (40 kg), demonstrated
that net portal uptake of essential amino acids was higher in pigs fed maize versus
pea starch (Van Der Meulen et al. 1997), implying an interaction between dietary
carbohydrate source and amino acid availability.
In pigs fed diets where the protein source is less than 95% to 100% digestible, the
ileal amino acid availability is a critically important consideration, when interpreting
the relative intestinal amino acid utilization rate. If the net portal utilization rate
of an amino acid is expressed relative to the dietary intake, and the digestibility
of the amino acid is not 100%, then the intestinal utilization rate will be
incorrectly overestimated. This concern is negligible in pigs fed diets containing
highly digestible, milk proteins, but is important with many other plant and animal
protein sources. On the other hand, however, if the intent is to determine the
availability of dietary amino acids for lean tissue growth, then it could be argued
that the net “portal availability” of an amino acid is perhaps a more valid,
biologically relevant estimate than the ileal availability. Moreover, because net portal
availability reflects the balance between the gut and the rest of the body, it avoids
the uncertainties of determining endogenous losses.
12.3.3.3 Threonine, methionine, and cysteine
Threonine utilization by the gut is higher than any other essential amino acid. Most
studies of net portal balance in pigs, indicate that approximately 40% to 60% of
the dietary threonine intake is utilized by the PDV tissues (Rerat et al. 1988; Van
der Meulen et al. 1997; Stoll et al. 1998). However, a recent report in young pigs
316 Weaning the pig

fed a high-protein, milk-based diet, indicated that as much as 85% of the dietary
threonine is used by the gut (Figure 12.6) (Van der Schoor et al. 2001). The utilization
of sulphur amino acids (methionine and cysteine) is also substantial, with various
estimates ranging from 30% to 58% of the dietary intake (Rerat et al. 1988; Van
der Meulen et al. 1997; Stoll et al. 1998). Estimates based on whole body amino
acids requirements demonstrated that the requirements for threonine and
methionine in parenterally fed neonatal piglets were 40% and 70%, respectively,
of that observed in enterally fed piglets (Bertolo et al. 1998; Shoveller et al. 2000).
These latter studies imply that intestinal uptake and metabolism account for 60%
and 30%, respectively, of the whole body threonine and methionine requirements
in neonatal pigs. Moreover, cysteine can be synthesized from methionine, and thus
represents a possible end-product of intestinal methionine utilization. Studies in
neonatal pigs also have shown that supplemental cysteine reduces the whole body
methionine requirement, when fed either enterally or parenterally (Shoveller et al.
2000). Thus, the extent to which the intestine can convert methionine to cysteine
warrants further study.
Two potentially important uses for threonine and cysteine in the gut are for the
synthesis of mucins and glutathione. The secretory mucins play a key role in the
innate immune defense of the mucosa, and the core protein of the major intestinal
mucins contains a large amount of threonine and cysteine (Fogg et al. 1996; van
Klinken et al. 1997). In addition, cysteine is a component of the tripeptide
antioxidant glutathione, which is critical for the maintenance of the structural
integrity and barrier function of the intestinal mucosa (Martensson et al. 1991).
The mucosal synthesis and secretion of mucins and glutathione are likely to be
quantitatively significant, and thus the needs for dietary threonine and cysteine
may be increased during the weaning process where there is gut hypersensitivity
or inflammation. A recent study demonstrated that feeding a threonine-deficient
diet to piglets significantly reduces intestinal mass and goblet cell numbers, and
this suppression of intestinal growth cannot be fully restored by providing
threonine parenterally (Ball et al. 1999). Besides incorporation into mucin and
other mucosal proteins, the extent to which threonine is further metabolized within
the intestine is poorly understood. There is some debate as to which metabolic
pathway is most important in the catabolism of threonine in mammals (House
et al. 2001). The two predominant pathways of threonine catabolism in the pig
are believed to be catalyzed by either threonine aldolase/dehydrogenase or
threonine dehydratase (Ballevre et al. 1990; Le Floc’h et al. 1996; Le Floc’h et al.
1997). Studies in pigs suggest that conversion to glycine via threonine
aldolase/dehydrogenase is the predominant pathway of irreversible threonine
catabolism. Moreover, threonine dehydrogenase activity was localized to both the
liver and pancreas, but not other gut tissues, implicating the PDV as a possible site
of threonine catabolism. Despite this evidence, there is negligible 13C-threonine
oxidation to CO2 by the PDV when given either enterally or systemically to young

Burrin and Stoll
piglets (Van Goudoever and Reeds unpublished results). However, this does not
preclude the possibility that metabolism of threonine to glycine is nutritionally
significant and warrants further study.
12.3.3.4 Lysine, phenylalanine and branched-chain amino acids
The intestinal utilization and net portal availability of dietary lysine are particularly
important, given that lysine is the first limiting amino acid in weanling pigs. Studies
in young piglets fed milk-replacer indicate that only about 55% of the dietary lysine
intake is absorbed, suggesting that the gut utilizes 45% (Figure 12.6) (Stoll et al.
1998; Van Goudoever et al. 2001). The net portal lysine utilization in grower-finishing
pigs fed cereal-based diets was similar (50% of intake) in one report (Rerat et al.
1988), but substantially lower (27.5% of intake) in another (Van Der Meulen et
al. 1997). Similar to lysine, the net portal utilization of phenylalanine and
branched-chain amino acids (BCAA) is also high, with the gut consuming on average
approximately 50% of the dietary intake (Stoll et al. 1998b; Stoll et al. 1999b; Van
Goudoever et al. 2001). In older pigs, estimates of net portal utilization rates of
BCAA are slightly greater (~60% of intake) (Rerat et al. 1988), whereas others found
much lower (~28%) rates (Van Der Meulen et al. 1997). The explanation for the
discrepancy between results of Rerat et al. (1988) and Van Der Meulen et al. (1997)
is probably due to the fact that the latter study expressed the portal fluxes relative
to the amount of the ileal digested amino acid rather than the intake, a point
mentioned previously.
In general, the catabolism of essential amino acids by the gut has been considered
to be negligible, based on the assumption that the liver is the main site of oxidation
(Wu, 1998). However, recent studies based on isotopic tracer kinetics in PDV tissues
suggest that dietary essential amino acids are oxidized within the gut, particularly
lysine and leucine. Studies in young pigs showed that intestinal oxidation of dietary
lysine accounted for about one-third of whole-body lysine oxidation and was
completely suppressed by feeding a low-protein diet (Van Goudoever et al. 2000).
Interestingly, although arterial lysine was taken up by the PDV, none of this was
oxidized, suggesting a preferential oxidation of dietary lysine (Van Goudoever et
al. 2000). As with lysine, there is significant leucine metabolism by the gut via both
transamination to α-ketoisocaproic acid (KIC) and complete oxidation to CO2.
Studies in young pigs and dogs have demonstrated that approximately 5-10 % of
whole-body leucine flux is oxidized by the PDV (Yu et al. 1995; Van Der Schoor
et al. 2001). Although approximately 40% of the leucine taken up by the gut was
converted to KIC, nearly all of this is transaminated back to leucine, thus, the net
KIC release is negligible (Yu et al. 1995). Studies in young, grower pigs (15-20 kg)
suggest that approximately 15% of the whole- body phenylalanine flux is oxidized
by the PDV tissues (Bush et al. 2001). The oxidation of phenylalanine implies that
phenylalanine hydroxylation occurs in the gut and is consistent with previous
318 Weaning the pig

observations suggesting net portal tyrosine production in excess of dietary intake.

Given that hydroxylation rather than complete oxidation to CO2 represents the
point of irreversible loss of phenylalanine, further studies are warranted to
quantify the proportion of whole body phenylalanine flux metabolize to tyrosine
by the gut. Additional studies are also needed to establish the localization of essential
amino acid catabolic enzymes within the different mucosal cell phenotypes, i.e.
enterocytes versus lymphoid cells.
12.3.3.5 Arginine and proline
In suckling pigs, arginine is considered to be essential in the diet. Studies have shown
that the small intestine is an important site of arginine and proline synthesis
(Murphy et al., 1996; Wu, 1998; Stoll et al. 1999a). In the healthy suckling pig,
the intestinal synthesis of arginine provides only about half of the animal’s needs
for growth and the arginine concentration in sow’s milk is also limiting (Davis et
al. 1994). Moreover, the net intestinal synthesis of arginine declines substantially
during the late suckling period (Wu and Morris 1998). These observations raise
the possibility that both the endogenous (via gut synthesis) and dietary arginine
supply may be limiting for maximal growth of suckling piglets. Studies with
enterocytes from newborn pigs (Blaicher et al. 1993; Wu and Knabe 1995) have
shown developmental changes in arginine-metabolizing enzymes. At birth, the
enterocytes are the major site of arginine synthesis, but gradually become the major
site of net citrulline production as intestinal arginase expression increases via a
glucocorticoid-dependent mechanism. In weanling pigs, intestinal citrulline
synthesis from glutamine, glutamate and proline is the main source for circulating
citrulline, which plays a critical role in whole body arginine homeostasis (Dugan
et al. 1995). This transition is compensated by the gradually increasing capacity
of the kidney to use citrulline for arginine synthesis. Thus, following the transition
from suckling to weanling, the intestine probably becomes a site of net arginine
degradation rather than synthesis (Wu and Morris 1998).
The limited arginine degradation by enterocytes from newborn pigs ensures a

maximum output of arginine (synthesized from glutamine or derived from milk)
into the portal circulation for utilization by extraintestinal tissues. The induction
of type II arginase in enterocytes after weaning possibly regulates the availability
of arginine for the synthesis of nitric oxide (NO), ornithine and thus, polyamines,
proline, and glutamate by the small intestinal mucosa. Major end-products of
arginine metabolism by intestinal enterocytes from weaned pigs are proline and
ornithine. Proline, required for collagen synthesis, is one of the most abundant
amino acids in human milk (Davis et al. 1994). Providing proline in the diet can
ameliorate the hyperammonemia associated with dietary arginine deficiency in
neonatal pigs (Brunton et al. 1999). Thus, while proline is not considered an absolute
dietary essential nutrient, it may be conditionally essential for maintaining

Burrin and Stoll
arginine synthesis in neonates. It is apparent from a number of studies that a

normally functioning gut is important for maintenance of whole-body arginine
and proline status, especially in neonates. Furthermore, these amino acids become
conditionally essential under conditions that markedly reduce gut mass or
compromise function, such as massive small bowel resection (Wakabayashi et al.
1995).
Recent studies in cultured intestinal cells have shown that ornithine derived from
arginine metabolism is converted to polyamines (Blaicher et al. 1995). Polyamines
(putrescine, spermidine, spermine, cadaverine) are ubiquitous cationic amines
involved in cell proliferation and differentiation in many tissues, including the
gastrointestinal tract. Ornithine decarboxylase (ODC) and S-adenosyl-methionine
decarboxylase (SAMDC), converting ornithine to putrescine and putrescine to
spermine, respectively, are the rate-limiting enzymes in polyamine synthesis. The
synthesis of polyamines from arginine is negligible in enterocytes of newborn and
suckling animals (Blaicher et al. 1991; Blaicher et al. 1992), but increases in
enterocytes of postweaning animals, concurrent with the induction of both
arginase and ODC (Wu and Morris 1998). Polyamines are present in porcine milk
and luminal administration of polyamines increases intestinal growth in adult rats
and enhances intestinal maturation and cell proliferation in developing rats (Dufour
et al. 1988; Grant et al. 1990; Kelly et al. 1991a). Thus, when the ingestion of
milkborne polyamines by the suckling pig ceases after weaning, the induction of
intestinal polyamine synthesis from ornithine, arginine and proline may become
physiologically significant for the maintenance of normal intestinal growth and
function (Wu et al. 2000a; Wu et al. 2000b). Furthermore, the weaning-induced
cortisol surge has been shown to be a key signal in the induction of intestinal
polyamine synthesis.
12.3.4 Interactions between nutrition and enteric health and function
12.3.4.1 Gut specific nutrients
In the past, weanling pig diets have been manipulated largely to overcome the
limitations or immaturity in digestive function in order to maximize growth of
the whole animal. However, given our increased understanding of intestinal nutrient
utilization, it is possible to now formulate weanling pig diets with the specific goal
of optimizing the growth, function and health of the gut. From the foregoing
discussion of intestinal nutrient utilization some of the most promising candidates
are glutamine, glutamate and threonine. A survey of the numerous literature reports
of dietary glutamine supplementation indicate that the effects on intestinal
growth are equivocal (Reeds and Burrin 2001). However, surprisingly few studies
have been done in weanling pigs, yet these studies suggest dietary glutamine
supplementation may be beneficial. Studies in weanling pigs by Ayonrinde et al.
320 Weaning the pig

(1995) and Wu et al. (1996) showed that supplementing the diet with crystalline
glutamine at either 4% or 1%, respectively, increased intestinal villus height. In
addition, Wu et al. (1996) and Kitt et al. (2001) found 1% dietary glutamine
supplementation to increase weight gain in weanling pigs. Another report found
that weanling pigs fed diets supplemented with 4% glutamine had increased muscle
glutamine concentrations and improved lymphocyte function (Yoo et al. 1997).
A more recent study with early-weaned pig diets showed that dietary
supplementation (% dry matter) with either glutamate (6.5%) or arginine (0.93%)
modestly increased intestinal mass and villus height, whereas neither citrulline
(0.94%), or ornithine (0.90%) had any effect and polyamines (0.39%) were
detrimental (Ewtushik et al. 2000). Interestingly, the latter study also showed that
glutamate supplementation markedly increased (200%) the plasma glutamine
concentration, implying that glutamate had a glutamine-sparing effect or perhaps
served as a precursor for glutamine synthesis. In the case of threonine, the studies
of Ball et al. (1999) suggest that dietary threonine is particularly essential for
intestinal growth and mucus production in young pigs. Another recent study showed
a dose-dependent increase in weight gain and feed efficiency in early-weaned pigs
fed a basal corn-soybean meal diets supplemented with crystalline threonine (0.25-
0.50 % diet dry matter), despite the fact that the basal diet was formulated to meet
the dietary threonine requirement (Lackeyram et al. 2001). Taken together, these
studies suggest that further studies are warranted to examine the dose efficacy of
dietary supplementation with these particular amino acids on enteric health and
post-weaning growth in pigs.
In addition to amino acids, there are other nutrients that have been shown to
improve intestinal growth and function in rodents, but have yet to be examined
in weanling pig diets. Among these are long-chain polyunsaturated fatty acids and
nucleotides. The interest in dietary long-chain fatty acids (LCFAs) stems from the
idea that n-3 long-chain, polyunsaturated fatty acids (LC-PUFAs) have been
shown to improve the health and development of infants. The concentrations of
several n-3 LC-PUFAs are higher in breast milk than in formulas and have
prompted the recent move to include the fatty acids in infant formulas. It is well
established that the n-3 LC-PUFAs or omega-3 fatty acids, particularly
docosahexanoic acid (DHA), eicosapentaenoic acid (EPA) and arachidonic acid
(AA), have pleiotropic biological effects on immune function, inflammation,
hemodynamics, and bone metabolism (Calder 1999). The interest in adding n-3
LC-PUFAs to infant formula has been heightened by recent studies showing that
supplementing these fatty acids can lower the incidence and inflammatory effects
of necrotizing enterocolitis in neonatal infants and rats (Akisu et al. 1998; Carlson
et al. 1998; Caplan et al. 2001). There is limited information regarding the intestinal
trophic effects of either n-3 LC-PUFA or other LCFA in developing animals. However,
a series of studies by Vanderhoof et al. (Vanderhoof et al. 1984; Vanderhoof et al.
1994; Kollman et al. 1999) have demonstrated that n-3 LC-PUFAs enhance

Burrin and Stoll
intestinal adaptation after small- bowel resection, and their effects were greater than
those of less saturated oils; they also found that medium-chain triglycerides are
less trophic than long-chain triglycerides. Another LC-PUFA of interest is the isomer
of n-6 linoleic acid, conjugated linoleic acid (CLA), which has been shown to
enhance lean tissue growth in pigs (Ostrowska et al. 1999; Bassanganya-Riera et
al. 2001a). The impact of CLA on the weanling pig intestine is unknown, but it
has been shown to increase colonocyte apoptosis (Park et al. 2001) and enhance
the cytotoxic function of lymphocytes (Bassanganya-Riera et al. 2001b).
Nucleotides are ubiquitous, low-molecular-weight, intracellular compounds that

are integral to numerous biochemical processes, and are especially important as
precursors for nucleic acid synthesis in rapidly dividing cells, such as epithelial and
lymphoid cells in the mucosa (Cosgrove, 1998). Nucleotides consist of a purine
or pyrimidine base, which can be synthesized within cells de novo from glutamine,
aspartic acid, glycine, formate, and carbon dioxide as precursors, or they can be
salvaged from the degradation of nucleic acids and nucleotides. The relative
significance of de novo synthesis versus the salvage pathway for intestinal
nucleotide requirements is not clear; however, the evidence suggests that dietary
sources of purine and pyrimidine bases are necessary (Uauy et al. 1994; Boza et
al. 1996). Numerous reports have demonstrated that dietary supplementation with
nucleosides, nucleotides, or nucleic acids supports small intestinal mucosal
immune function, growth and morphology in vivo and in vitro (Uauy et al. 1994;
Lopez-Navarro et al. 1996; Cosgrove 1998; Carver, 1999).
12.3.4.2 Impact of antimicrobials and infection
A critical factor influencing the growth of weanling pigs is the degree of infestation
with pathogenic microbes. Studies with growing animals indicate that exposure
to these organisms and their toxins can adversely affect intestinal structure and
function (Figure 12.7) (Von Allmen et al., 1992; Higashiguchi et al. 1994; Breuille
et al., 1998; Wang et al., 1998; Mack et al., 1999). The studies demonstrate that
the pro-inflammatory stimulus induced by bacteria, endotoxin and cytokines
significantly increases the intestinal protein synthesis rate. Recent work in sheep
demonstrated that parasitic infection increases the rate of leucine utilization and
oxidation by PDV tissues, thereby reducing the systemic availability of dietary amino
acids by 20-30% (Yu et al., 2000). In addition, most of the increased PDV leucine
utilization is either oxidized or lost as endogenous protein secretion; together, these
losses account for most of the reduced nitrogen retention associated with infection
(Yu et al., 2000). Thus, it is likely that enteric infection increases the intestinal nutrient
requirements, which in turn limits the availability of dietary nutrients for growth
of weanling pig. This raises two critical questions for future studies 1) how does
infection alter the pattern of intestinal nutrient utilization? and 2) what are the
key nutrients that may become limiting for either intestinal function or whole body
322 Weaning the pig

Dietary Amino Acids
An timicrobials
Bacteria
Villus Ce lls NH4
Toxins
Increased
Proinf lammator y
Increased Mucosal
Cytokines
Amino A cid
Proliferating
Util ization
Cry pt Cells
Blood Decrea sed Amino Acid

Ab sorption
Figure 12.7. Schematic illustration of the relationship between intestinal amino acid
metabolism and the luminal bacteria.
growth in infected pigs? It is likely that threonine will be a key nutrient under these
conditions, given its importance for intestinal metabolism and that it is one of the
first limiting amino acids for growth in swine.
Antimicrobial compounds are fed to weanling pigs in order to suppress the activity
of the gut microflora and enhance growth; although the exact mechanism for this
effect is unknown. However, it is generally held that by suppressing microbial activity,
antimicrobials reduce the luminal concentration and associated toxic insult of
ammonia, and thereby diminish the thickness and mass of the intestinal mucosa
and associated lymphoid tissue (Visek 1978). Studies in pigs and chickens show
that feeding antimicrobial compounds significantly reduces small intestinal mass,
cell proliferation and intestinal ammonia absorption (Yen et al. 1987; Yen and Pond
1990; Krinke and Jamroz 1996). Additional evidence indicates that the luminal
ammonia arises from bacterial hydrolysis of urea and deamination of dietary amino
acids. Thus, a critical mechanistic question regarding the site of dietary amino acid
utilization in the gastrointestinal tract is whether this activity is associated with
the luminal microbes or the cell populations of the mucosa.

Burrin and Stoll
12.4 Summary and perspectives

Three important themes of this chapter are 1) that the gut undergoes significant
morphological and functional adaptation during weaning, 2) that under normal
conditions, the gut consumes a substantial proportion of the dietary nutrients, and
3) that the gut preferentially uses specific nutrients. As young pigs transition from
suckling sow’s milk to consumption of cereal-based weaning diets there is an increase
in gastrointestinal growth, marked by increased proliferation of epithelial cells and
the synthesis and secretion of proteins within the stomach, intestine and pancreas.
Some of the important factors contributing to this increased growth are related to
increased voluntary dry matter intake and digestive enzyme production, as well
as, immune hypersensitive and inflammatory responses to noxious compounds
arising from the diet and microflora. This stimulation of gut growth likely
translates into increased intestinal nutrient requirements, yet further study is needed
to establish how the weaning processes alters the quantity and pattern of gut nutrient
utilization. Some of the key nutrients that are preferentially used by the gut include
glucose and nonessential amino acids, glutamate, glutamine and aspartate, but also
essential amino acids that are limiting for lean tissue growth, namely threonine.
It remains to be seen whether the increased intestinal utilization of these key
nutrients limits their availability for maximal growth of the weanling pig. If so,
then perhaps these “gut specific” nutrients should be supplemented or their dietary
requirements increased to improve growth. An alternate approach to enhancing
growth is to limit those factors which stimulate intestinal growth during weaning.
For example feeding antimicrobials or employing segregated weaning practices will
reduce the microbial pathogen load and the nutritional cost associated with immune
stimulation. A final point of consideration is that while the maintenance of enteric
health and intestinal function is key for supporting maximum growth of the weaned
pig, it’s clear that this imparts a nutritional cost. Thus, the aim of future research
should be to identify novel nutritional management approaches that optimize
intestinal function while minimizing the nutritional cost associated with increased
intestinal metabolism.
Acknowledgments
The authors would like to thank Jane Schoppe for her assistance in the preparation
of this manuscript. This work is a publication of the USDA/ARS Children’s
Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine
and Texas Children’s Hospital, Houston, TX. The work was supported in part by
federal funds from the U.S. Department of Agriculture Agricultural Research Service,
Cooperative Agreement No. 58-6258-6001, by the National Institutes of Health
R01 HD33920. The contents of this publication do not necessarily reflect the views
or policies of the U.S. Department of Agriculture, nor does mention of trade names,
commercial products, or organizations imply endorsement by the U.S. Government.
324 Weaning the pig

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13 Environmental requirements and housing
of the weaned pig
F. Madec, J. Le Dividich, J.R. Pluske and M.W.A. Verstegen
13.1 Introduction
In most pig producing countries, piglets are weaned between 17 and 30 days of
age in specialised nurseries (Hendriks et al., 1998) at an age when most of their
nutrient intake is still obtained from milk. Most of these nurseries are temperature-
controlled and have pens with perforated floors (Hendriks et al., 1998). Weaning
is commonly associated with mixing of piglets from different litters and sometimes
with transportation from breeding to nursery units and, with in an abrupt change
in both the pattern and the type of diet. The transition from nursery to consumption
of solid feed usually results in a critical period of underfeeding during which piglets
learn to eat and adapt to digest the solid feed (Le Dividich and Herpin, 1994). It
follows that weaning imposes simultaneous social, nutritional and environmental
stressors that affect the energy metabolism indeed the thermal requirements of
piglets.
The health of the weaned pig is very fragile. Weaning implies the withdrawal of
milk protection at an age when the immune system of the pig is not yet fully
developed (Dyrendhal, 1964). Diarrhoea leading to growth retardation and
sometimes to mortality is a major clinical problem encountered at weaning. Various
factors account for this complex disease. They include mainly nutrition (for details,
see chapters 9 and 12) and housing through its environmental and hygienic
conditions (van Beers-Schreurs et al., 1992; Madec et al., 1998). Because of the great
number of piglets kept together in the same unit, non-optimal indoor climate and
hygienic conditions and pen structure may lead to important economic losses.
The objective of this chapter is to consider the housing requirements of the pig
weaned between 3 and 4 weeks of age in the light of improving pig performance
and health. We first assess the environmental requirements and factors accounting
for changes associated with weaning. The second section focuses on the pen structure
including flooring material, feeders and waterers, stocking rate and group size, which
may influence piglet performance. Housing and management as causes of poor
health of the pig are considered in the last section. Unless specified, in this chapter,
piglets are weaned at 3-4 weeks of age and reared in groups on perforated flooring.

Madec, Le Dividich, Pluske and Verstegen
13.2 Environmental requirements of the weaned pig

Ambient temperature (Ta) is the predominant component of the climatic
environment. Requirement for temperature depends on several factors among which
the amount of feed consumed and body thermal insulation is the most important.
It is therefore relevant to assess the effects of weaning on feed consumption and
its ensuing consequences on fat accretion and body thermal insulation.
13.2.1 Events related to weaning that affect thermal requirements
13.2.1.1 Feed intake
At weaning between 3 and 4 weeks, most piglets have consumed very little solid
feed and hence they are unfamiliar with the weaning diet. It follows that feed intake
of piglets abruptly deprived of liquid milk provided by their dam pre-weaning and
offered a pelleted solid feed post-weaning is often very limited. Both the extent
and the duration of underfeeding vary enormously (Le Dividich and Sève, 2001).
However, the level of metabolizable energy (ME) intake attained at the end of the
1st post-weaning week approximates 70% of the pre-weaning milk ME intake. In
fact, the pre-weaning ME intake is only attained by about 2 weeks after weaning.
Attempts to reduce both the extent and duration of the underfeeding period can
be achieved by providing the piglets with liquid feed (for details, see Chapter 6).
Provision of liquid feed certainly attenuates the extent of underfeeding, but not
completely. However, this practice induces feed wastage, needs to be carefully
monitored for hygiene reasons, and requires sophisticated dispensers. Together, these
would suggest that a period of underfeeding following weaning is practically
unavoidable.
13.2.1.2 Fat metabolism and effects on body thermal insulation
Fat is a good insulating material. Its heat conductivity is three times lower than that
of water. Subcutaneous fat provides thermal insulation to the pig. At weaning, body
composition changes markedly towards a temporary decrease in fat content. At least
two factors account for this decrease in body fatness. First, mixing of unfamiliar pigs
at weaning results in vigorous fighting associated with the formation of a new social
order and, in a transient increase in heat production (Heetkamp et al., 1995). When
the effects of mixing and transportation are combined, a slight increase in heat
production is measurable for up to 5-7d post transportation (del Barrio et al., 1993).
Second, and most importantly, due to low feed intake, most of the newly-weaned
pigs are in negative energy balance during a period of 4-7 days following weaning.
However the nitrogen balance remains positive and is less dependent on the
environmental conditions (Le Dividich et al., 1980; Close and Stanier, 1984b;
Bruininx et al., 2002). It follows that the energy required for maintenance, physical
338 Weaning the pig

Environmental requirements and housing of the weaned pig
activity and for protein synthesis involves a mobilisation of body fat (Whittemore
et al., 1978). The rate of mobilisation depends on both level of feeding and
environmental temperature, it being more pronounced at low feed intake (Close
and Le Dividich, 1984) and at low environmental temperature (Le Dividich et al.,
1980). The extent to which this loss of body fat affects the decrease in body thermal
insulation is therefore variable, but depends on the available body fat stores at
weaning. In pigs of low weaning weight (4.55 kg at 21d of age), the rate of fat
mobilisation can be as high as 32% during the first week following weaning (Sloat
et al., 1985). According to Fenton et al. (1985), the decline in backfat thickness can
be as high as 33% in the 1st week following weaning at 2 weeks of age. These data
provide evidence that the body thermal insulation is reduced and leads to an increased
susceptibility of the weaned pig to cold. This is illustrated by the amount of extra
heat produced in the cold, i.e., 18kJ/kg 0.75 .°C-1, which is 50% higher than in a
60-kg pig (Le Dividich et al., 1998). With the low feed intake, this has major impacts
on the thermal requirement of the piglet at weaning.
13.2.2 Ambient temperature
Because of the transient effect of weaning of feed intake, two periods are examined
(Le Dividich and Herpin, 1994) (i) the critical period of 1 to 2 weeks following
weaning, representing the period of underfeeding and corresponding to the time
required to attain the pre-weaning level of ME intake, and (ii) the post-critical period,
i.e., when regular feed intake is established.
13.2.2.1 The critical period
The lower critical temperature (LCT) is defined as the ambient temperature at which,
for a given ME intake, energy retention is maximal. LCT corresponds to the optimum
temperature at weaning inasmuch as the main goal is to minimise heat loss to avoid
excessive loss of body fat and hence minimise the decrease in thermal insulation.
At weaning, the combination of a low feed intake and a reduced body thermal
insulation (Figure 13.1) results in a temporary increase in LCT from 22-23°C at
weaning to 26 to 28°C during the first post-weaning week (Le Dividich et al., 1980;
McCracken and Caldwell, 1980), decreasing thereafter to 23 to 24°C in the second
post-weaning week (Close and Stanier, 1984b; McCracken and Gray, 1984). In
addition, it should be noted that maintaining the ambient temperature at or above
the LCT during the critical period of weaning helps to prevent a possible over-
consumption occurring sometimes after piglets start to eat solid feed, thus limiting
the consequences of post-weaning digestive and (or) enteric disease disturbances.

30
Critical temperature, °C
28
26
24
22
20
18
2000
14
ME intake, kJ/kg 0,75/d

12 1500
Body fat content, %
10
1000
8
6 500
4
Pre-weaning 0
week
2
Birth 1 2 1 3 5 7 14 21 28
Weaning Days post-weaning
at 21 d of age
Figure 13.1. Diagrammatic representation of the effects of the abrupt decline in feed
intake and of the reduction of body fat content occuring at weaning on the lower critical
temperature of piglets raised on perforated floor.
13.2.2.2 The post-critical period
Once regular feed intake is well established and inasmuch as there is no health
problem, the air temperature of the nursery can be rapidly reduced in relation to
the increase in feed intake (Figure 13.1). Most studies suggest a progressive decrease
in ambient temperature by 2 to 3°C/week until the temperature to be maintained
in the finishing house is reached (Le Dividich, 1981; Close and Stanier, 1984a;
Feenstra, 1985). In addition, the weaned pig is to some extent able to compensate
for a sub-optimal environment by increasing its voluntary feed intake. The
adjustment in feed intake is rapid since being stabilised within 6d after exposure
to “cold” (Verhagen et al. 1988). This is in agreement with the fact that within the
25 to 18-19°C temperature interval, growth rate remains practically constant, with
however an increase in feed to gain ratio (Fuller, 1965; Hata et al., 1986; Rinaldo
and Le Dividich, 1991). However, an abrupt reduction in the nursery temperature
after the critical period appears to be detrimental. For example, an abrupt 5°C
340 Weaning the pig

decrease of ambient temperature on d7 post-weaning is found to depress overall

growth rate by 21% and feed efficiency by 10% (McConnell et al., 1987).
13.2.2.3 Ways to reduce heating costs
Because of the relatively high ambient temperature considered essential for optimal
performance, the weaning house requires considerable heating. Consequently, several
ways of reducing the heating requirement while maintaining pig performance at
an acceptable level have been investigated. These include the provision of a
microenvironment, bedding and, reduction in nocturnal air temperature.
Provision of a microenvironment
A simple way to save energy is to create a microenvironment for the pig within
the weaning house. Use of covers is an alternative that offers the possibility to reduce
the heating cost. Pigs provided with hovers or covers at moderate air temperatures
(18 to 20°C) had performance similar to those maintained at recommended
temperatures (Shelton and Brumm, 1983). Similar results are recorded in Denmark
(Feenstra, 1985) where systems with a covered area and two-thirds solid floor have
become increasingly popular. The hovers reduce draughts and, to some extent, trap
the heat produced by the pigs.
Provision of bedding
Provision of bedding (straw, sawdust, wood shavings) lowers LCT. Verstegen and
van der Hel (1974) calculated the LCT of groups of 40-kg pigs to be 7-8°C lower
on straw than on concrete slats. From preference studies, Morrison et al. (1987)
calculated that, compared to perforated metal, weaned piglets on bedded solid floor
required 5.8 °C less Ta (Table 13.1). Similar performance is reported when
comparing weaned pigs on solid bedded floors (temperature initially 23°C
gradually decreasing to 16°C by the end of the weaner period) to those on metal
slatted floor with temperature initially 27°C decreasing gradually to 18°C) (Kelly
et al., 2000), while improving the welfare of piglets. In practise, pigs on solid bedded
Table 13.1. Difference in effective ambient temperature of various floors compared

to solid bedded floor.
Type of floor Difference in effective environmental temperature (°C)
Bare solid floor + 2.8

Perforated metal + 5.8
Raised rubber-coated floor + 3.0
(After Morrison et al., 1987)

floors require 4 to 6 °C less than those on perforated floor. However, the extra
cost associated with bedding (bedding, extra labour) must be compared to that
of extra heating.
Reduction of the nocturnal temperature

Another alternative is based on the fact that the pig displays a marked circadian
variation in metabolic rate, which is lower during the nighttime than during the
daytime. This variation in metabolic rate results in a variation of the LCT, being lower
during the night than during the day (van der Hel et al., 1985). Compared with a
constant temperature, a 4 to 9°C reduction in nocturnal temperature (RNT) does
not affect the pig’s performance (Table 13.2) while decreasing markedly heating cost
(Shelton and Brumm, 1988). No adverse consequence during the finishing phase
is reported. However, pigs on a RNT treatment tended to have a greater incidence
and severity of scouring (Swinkels et al., 1988). Similarly, data obtained by Rinaldo
et al. (1989) also indicated that within the 12 to 30 kg body weight interval, pigs
subjected to a 8°C reduction in nocturnal temperature (22 → 14°C) had similar
average daily gain (ADG) than those maintained at a constant temperature of 22°C.
However, the RNT treatment was associated with an overall increase in average daily
feed intake (ADFI) with a greater proportion (38 vs 32%) being consumed during
the nighttime. Also, pigs on the RNT treatment huddled more during the nighttime,
indicating an activation of the thermoregulatory behaviour. In practise, environmental
conditions are not constant. It is usually assumed that performance of pigs exposed
to daily air temperature fluctuation is equivalent to the average of that fluctuation.
Data of Kurihara et al. (1996) obtained in pigs aged 53 to 62d suggest that a diurnal
range of ±3°C around the mean is acceptable (Table 13.3). A higher range (± 7°C)
results in a significant decrease in performance.
Table 13.2. Effect of reduced nocturnal temperature (RNT) during the nursery phase
on the pig performance1.
Treatment Control (°C) RNT (°C)
ADG, g 340 360

ADFI, g 530 570
Feed:gain (kg/kg) 1.57 1.61
1There were 256 pigs per treatment, initial body weight = 6.7Kg. They were exposed to
either a constant regime (30°C for the first week and then decreased by 2°C per week for
four weeks) or a cycling daily temperature regime (the same temperature as the control
during the first week, but night temperature lowering to 22°C on week 2 and further by
2°C per subsequent week.
(After Shelton and Brumm, 1988)
342 Weaning the pig

Table 13.3. Effect of diurnal variation in ambient temperature on piglets performance

(initial age, 53-62 days).
Ambient temperature (°C) 21 21±31 21±62
ADG 682 660 602

Feed intake, g 1330 1300 1150
Feed: gain (kg/kg) 1.95 1.97 1.95
1 12h at 18°C and 12h at 24°C

2 12h at 15°C and 12h at 27°C
(After Kurihara et al, 1996)
13.2.3 Relative humidity and ventilation
Little attention has been paid to the effect of relative humidity (RH) and air velocity
on the performance of the weaned pig. However, relative humidity is expected to
have little influence on the performance of the weaned pig maintained within
thermal neutrality. For example, at 24°C, similar performance is obtained at 60
and 90% RH (Bresk and Stolpe, 1988). In contrast, in growing pigs, a 10% change
in RH, between 45 and 90% induced a 24 g/d reduction in feed intake with no
change in feed efficiency (Massabie et al., 1997).
Ventilation serves two major functions: (i) removal of air humidity and noxious
gases, and (2) assist with the control of the temperature of the animal house.
Ventilation determines air velocity at the pig level. As such, it plays an important
role in the rate of heat loss. Using the operant conditioning technique, Verstegen
et al. (1987) found that increasing the air velocity from 8 to 40cm/s resulted in a
3.8°C increase in the preferred temperature (Table 13.4). Results of Hacker et al.
(1979) indicate that below the LCT, an increase in air velocity from 0 (still air) to
50 cm/s resulted in a 15% decrease in ADG and a 23% decrease in gain to feed
Table 13.4. Effect of air velocity on preferred temperature by the 14-20kg pig.
Air velocity(cm s-1) Preferred temperature (°C)
8 17.9
25 20.5
40 21.7
(After Verstegen, et al., 1987)

ratio in pigs weaned at 21 to 25 d of age. Similarly, Riskowski and Bundy (1990)

calculated that during the second post-weaning week within the temperature range
of 24 to 35°C, each 10 cm/s increase in air velocity was associated with a 25 g/d
decrease in growth rate.
Because ventilation accounts for most (80 to 90%) of the heat loss of the weaning
house, the current recommendation during cold weather is “as low ventilation as
possible”. Studies conducted at the University of Minnesota (Boedicker et al. 1984;
Jacobson et al., 1985-86), indicated that ventilation rate lower that the recommended
minimum had no detrimental effect on performance and health despite 2-3 times
higher concentrations of ammonia and carbon dioxide. In practice (Ritz, 1971),
recommendations for ventilation rate during winter are 0.35-0.40 m3 h-1 kg-1 body
weight (BW). During summer, to remove heat and water vapour produced by the
pigs and hence to avoid excessive rise in temperature and humidity,
recommendations for ventilation are 1.60 - 2.10 m3 h-1 Kg-1 bodyweight. Effects
of noxious gases on performance have been the subject of an excellent review by
Wathes (2001) and will not be discussed here.
13.2.4 Lighting
Lighting as an environmental factor has received little attention. Bears et al. (1974)
suggested that complete darkness reduces the agonistic interactions at weaning.
However, constant illumination of 5 or 100lx has no effect on the behaviour
(included the feeding behaviour) of the newly weaned pig (Christison, 1996). In
contrast, photoperiod may have effects on performance. Bruininx et al. (2002)
reported that ADFI is 16 and 38% enhanced during the 1st and the 2nd postweaning
week, respectively, in pigs subjected to a 23:1h lighting schedule compared to 8:16
schedule. However, more data are necessary to substantiate these results. The EU
regulation mentions that pigs should be exposed to daily 8 h lighting of at least
40lx.
13.2.5 Effects of non-optimal climate on performance
The effects of cold and high ambient temperature on performance are shown in
Figure 13.2. Low ambient temperature during the critical period of weaning is the
most detrimental to performance mainly because feed intake is not increased. Pigs
maintained at 21°C during the first 10 post-weaning days are found to grow 33%
less on 53% more feed than those at 29°C (Maenz et al.,1994). Once regular feed
intake is established, the weaned pig is able, to some extent, to increase its feed
intake to compensate for a low temperature. However, maximum intake capacity
is reached at 18-19°C (Collin et al., 2001). It follows that at lower temperature,
ADG decreases by about 13g °C-1 coldness, and feed conversion ratio increases
by 0.04 unit °C-1 coldness (Le Dividich and Noblet, 1982; Close and Stanier, 1984a).
344 Weaning the pig

In addition, draughty conditions markedly affect performance. Draughts have

enormous effects on the behaviour of the piglets (Scheepens et al., 1991), resulting
mainly in an increased activity and therefore in an increase in the activity-related
heat production (Verhagen, 1987). Negative effects of draughts are the most
detrimental in the immediate post-weaning period. During this period, a 106 g/d
decrease in growth rate was found by Scheepens et al. (1991) due to draught, the
decrease amounting to 155 g/d when draughts were superimposed on fluctuating
temperature (25/15°C) (Verhagen, 1987).
700
ADG, g/d 600
500
400
2.5
2
FCR, kg/kg
1.5
0 1
0 10 20 30 40
Temperature, °C
Fuller, 1965
Rinaldo and Le Dividich, 1991
Hata et al, 1986
Figure 13.2. Effect of environmental temperature on the performance of weaned piglets.
At high ambient temperature, performance declines as a result of a decrease in feed

intake. During the overall post-weaning period, feed intake starts to decline markedly
at Ta higher than 25°C (Collin et al., 2001), the decline being dependent on the
pig body weight. For a 20-kg pig, ADFI decrease is in the range of 28-33 g. °C-1,
between 25 and 32-35°C, but may be as high as 42g.°C-1 (Sugahara et al., 1970).
This reduction in ADFI, leads to a decrease in ADG of 15-21% between 25 and 31-
33°C (Rinaldo and Le Dividich, 1991; Collin et al., 2001), with, however, no
detrimental effect on feed conversion ratio.

13.3 Pen structure

The major features of the pen structure that are likely to influence the environmental
and housing conditions of the weaner pig include flooring material, feeders and
waterers, stocking density and group size.
13.3.1 Flooring materials
There are many types of flooring materials available for nurseries, with fully or partly
slatted (or perforated) floors providing maximum manure throughput being the
most common types (Hendriks et al., 1998). Potential advantages are easiness of
clean, reduced labour and improved hygienic condition. Slatted or perforated floors
must be designed to minimise foot and claw injuries while facilitating cleaning.
Based on the morphology of the pig foot (Mitchell and Smith, 1978) and on the
occurrence of injuries (Vellenga et al., 1983), a slot width of 10-15 mm is
acceptable for pigs over 5-6 kg.
Similar performance is usually reported on bedded solid floors and slatted or

perforated floors (Schneider and Bronsch, 1974; Danielsen and Nielsen, 1978; Kelly
et al., 2000) when ambient conditions are appropriate. However, there is a trend
toward a reduced performance for pigs on aluminium floors (Wilson et al., 1977;
Orr et al., 1978). On the basis of preference studies (Farmer and Christison, 1982;
Pouteaux et al., 1983/84) and of the occurrence of foot lesions, plastic-coated
expanded metals are superior to other perforated flooring materials.
13.3.2 Feeders and waterers
Ideally, nursery pigs should be equipped with feeder space that allows at least half
of the pigs in the pen to eat at any one time, however this scenario is not always
attained and the issue of the ‘correct’ number of pigs per feeding space is always
a topic of discussion and contention. Feeding space is dictated by a number of factors,
one of which is the width of the pig; the relationship between feeding space per
pig and the pig’s physical conformation has led to the development of equations
to describe the minimum width needed in a feeder for a pig to eat. Baxter (1989)
described the equation: W = 61 x BW0.33, where W = width of the pig at the shoulder
(in mm) and BW is bodyweight (kg), that represents the minimum feeding space.
Practically, a margin of 10% to address individual pig variation should be used.
Using these calculations, therefore, a pig weighing 10 kg requires a minimum feeder
space of 130 mm.
Weanling pigs are commonly offered their feed from a partitioned linear (trough)
feeder that has a feeding pan in the front, and in which the rate of feed flow from
the hopper can be adjusted to prevent feed wastage. Single-space or wet/dry feeders
346 Weaning the pig

are generally not recommended for weanling pigs due to perceived problems of
access and excessive feed wastage, however Pluske and Williams (1996) reported
no difference in production indices in pigs fed from a linear (trough) feeder or a
single-space feeder between 28 and 56 days of age. However, pigs offered a single-
space feeder with a nipple waterer enclosed (‘wet/dry’ feeder) grew slower and wasted
more feed than pigs offered feed from the linear feeder or the ‘dry’ single-space
feeder.
Adequate water intake is essential in the immediate post-weaning period (see

Chapter 6 by Brooks and Tsourgiannis), so waterers (drinkers) need to be
accessible, working, kept clean and have the correct flow rates. Adjustable-height
nipple drinkers are generally preferred over cup waterers (bowls), at least in the
initial period after weaning. One nipple drinker should be provided for every 10-
15 pigs, however extensive pens (eg, straw-based shelters) can have 1 watering point
per 20-25 pigs seemingly without effects on production. The height of the waterer
should be adjusted to that of the pig’s back, and water pressure at the nipple (drinker)
should be limited to 20 pounds per square inch and 500-600 ml per minute.
13.3.3 Stocking densities
Floor space per pig is usually based on the space required for sternum and fully
recumbent resting positions. For a fully recumbent position, the relationship between
space allowance (A, m2) and BW (kg) is expressed as A = 0.047 x BW 2/3 (Petherick
and Baxter, 1982). According to these authors, adequate space allowance for a 6.8-
kg pig is 0.17m2 increasing to 0.44m2 for a 27-kg pig. From literature data, the
effects of space allowance (S, m2) on ADG and ADFI can be predicted from the
following equations (Kornegay and Notter, 1984):
ADG (kg) = 0.261 + 0.800 S - 1.051 S2 (R2 = 0.97)

ADFI (kg) = 0.533 + 1.125S - 1.383 S2 (R2 = 0.97)
In practise, within the body weight range of 5-6 to 25-30 kg, current
recommendations are 0.25 to 0.30 m2 per pig on perforated floors. A reduced space
area leads to a reduced feed intake and hence growth rate. During the overall post-
weaning period (from 21 to 63d of age), reducing the space allowance from 0.24
to 0.18 m2 results in a 13% reduction in both ADFI and ADG (Le Dividich, 1979).
However, feed conversion ratio is not usually affected. Less information exists on
the possible interaction between the type of flooring (bedded solid vs perforated
floors) and the space requirement. However, it is assumed that pigs on bedded solid
floors require some 20-25% more space.

13.3.4 Group size
There is a strong evidence that group penning of pigs may have a detrimental effect
on feed intake and performance. During the overall post-weaning period, increasing
the number of pigs from 8 to 24 per pen at constant space area of 0.21m2 reduced
ADFI and ADG by 13 and 12% respectively (McConnell, et al., 1987). Large group
sizes (100 or more per pen) are an increasingly feature in production, especially
in the USA and Australia. In Australia, pigs are sometimes weaned directly into
straw-based shelters (‘hoops’) in groups of up to 400. However, within the body
weight range of 5 to 15 kg, Wolter and Ellis (2002) consistently reported a small,
negative effect of increasing group size from 20 to 100 pigs per pen on growth rate
after weaning, with the extent of depression in ADG and ADFI ranging from 4.3
to 6.6% and from 5.1 to 6.6%, respectively. Using the prediction equations of
Kornegay and Notter (1984) obtained at constant floor area per pig, ADG and ADFI
decrease by 3.7 and 9.2 g, respectively, per each additional pig. However, in their
data set, only data from 4 studies were used and the range of group size (from 3
to 15) was rather narrow. In contrast, McConnell et al. (2001), in an experiment
using 1,280 pigs held in groups of 10, 20, 30, 40 and 60 from weaning at 28 days
of age to 10 weeks of age, reported no significant differences between treatments
in performance indices. Recently. Turner et al. (2003), using larger group sizes (3-
120), re-calculated Kornegay and Notter’s prediction equations. They are (N =
number of pigs per pen):
ADG (g) = 416 - 0.36N (R2 = 0.968)

ADFI (g) = 681 - 0.51N (R2 = 0.978),
indicating that the extent of decrease in both ADG and ADFI is much lower,
amounting to 0.36 and 0.51 g, respectively, per each additional pig. Of importance
is to notice that group size has no effect on both feed conversion ratio and on the
within-group variation in ADG (Giles et al., 2001; Turner, et al., 2003). Furthermore,
many other factors influence the relationships between group size and performance
post-weaning, of which feeder space, feeder design and water supply are influential.
Because mixing of litter is common at weaning, the question that arises is how
should pigs be grouped? Grouping by weight has been assumed to be beneficial
to the uniformity of the group. However, the effects of grouping pigs by weight
on performance are still unclear as illustrated by data of Francis et al. (1996) and
Bruininx et al. (2001), which failed to exhibit any difference in performance of
uniform and heterogeneous groups. From an economic standpoint, in deciding
the group size, the extra cost of housing must be compared to that of the
reduction of performance.
348 Weaning the pig

13.4 Housing as a cause of poor health of weaned

pigs
Enteric disease is the most common clinical problem encountered at weaning.
Usually, it peaks around 10d post-weaning, but its occurrence is closely dependent
on the herd. In some herds, piglets exhibit diarrhoea immediately post-weaning,
in others, on week 3 or 4 after weaning corresponding to a change in feed (Madec
and Leon, 1999). Feed additives including antibiotics, pro-or pre-biotics, and trace
elements (eg, Zn, Cu) to some extent, control it. In all cases, diarrhoea results in
a loss of ADG, as illustrated by the negative relationship between diarrhoea score
and ADG (r= -0.47 and -0.39 in the 1st and 2nd post-weaning week, respectively
(Madec et al., 1998)). Various factors account for this complex disease among which
both nutrition (for details, see Chapter 9) and housing conditions are the most
important.
13.4.1 Evidence that housing conditions predispose pigs to digestive

disorders
Evidence for the implication of the environment and housing in the development
of enteric disease is provided by experiments described by Madec and Leon (1999).
In brief, from 5 pig farms exhibiting high occurrence of diarrhoea, a sample of 28-
30 piglets from each herd was moved on the day of weaning to experimental facilities
at the Pig Veterinary Research Institute (Ploufragan). In these facilities, hygienic
and climatic conditions were of a very high standard (all-in / all out management,
no bacterial growth on Agar plates after cleaning operations, air filtration). In both
farms and experimental facilities, pigs were reared on perforated floors and fed ad
libitum the same diet. Enterotoxigenic E coli were found in pigs of both locations,
however, no mortality occurred in the experimental facilities whereas a rate of 2.1
to 4.5% was recorded in pigs weaned in farms (Table 13.5). Also, pigs weaned on
farms grew on average 30% less and exhibited a higher occurrence of diarrhoea.
In another study, using a similar protocol (Kerebel et al., 2000), feeding and drinking
behaviour of piglets were video-recorded during the first post-weaning week. Again,
the occurrence of diarrhoea was much higher in pigs weaned on farms. In
addition, both feeding and drinking frequencies were higher in pigs moved to the
experimental facilities. To some extent, similar results are also obtained when
comparing all-in/all-out nursery to a continuous flow nursery, in that overall
performance and health are markedly improved in the former facility (Schneider
and Bronsch, 1973) Together, these demonstrate the role of housing (in a broad
sense) on the occurrence of diarrhoea and suggest that (i) highly hygienic and
climatic conditions of the nursery and that (ii) early and high feed and water intake,
do not allow the expression of the most common pathogens.

Table 13.5. ADG, diarrhoea incidence and mortality of piglets selected at random on
farms severely affected with post-weaning diarrhoea and weaned either on farm or in
experimental facilities.
Number of pigs Diarrhoea ADG (g) Mortality (%)

(% of pigs)3
Farm Farm1 Exp. F2 Farm Exp. F Farm Exp. F Farm Exp. F
A 120 30 44.2 3.3 326 430 4.2 0

B 116 28 47.5 0 320 445 2.6 0
C 155 30 60.0 6.6 284 429 4.5 0
D 142 30 31.4 0 346 515 2.1 0
E 198 30 42.6 3.3 351 510 3.0 0
1Piglets weaned on farm

2Piglets from the corresponding farm that were transferred to experimental facilities
(Exp. F)
3Pigletswere daily examined for diarrhoea score ranging from 1 to 5. Faeces scored at 4
and 5 were considered diarrhoeic.
(After Madec and Leon 1999)
13.4.2 Impact of non-optimal indoor climate on the pig’s health status
Post-weaning gastrointestinal disturbances can be triggered or at least accentuated

by adverse climatic conditions. An increased incidence of diarrhoea at chronic
moderate cold temperatures (18-20 °C) has been observed by Le Dividich et al.
(1980), Close and Stanier (1984a) and Feenstra (1985). More importantly, acute
cold exposure (12 increasing to 18°C or 18 decreasing to 12°C) results in an
unacceptable 14-15% rate of mortality (Feenstra, 1984). Acute and continuous
changes in ambient temperature may also be detrimental to the health of piglets.
Le Dividich (1981) observed a greater incidence of post-weaning diarrhoea in piglets
kept in a continuous (hourly) fluctuating temperature (23.5±3°C) compared to
a constant temperature (23.5±0.5°C). In addition, the detrimental effect of a
continuous fluctuating temperature is particularly high during the 1st post-
weaning week. Also, reduced nighttime temperature appears to impose an
additional stress on sick pigs (Brumm et al., 1985). Intermittent exposure to draught
results in more coughing, sneezing and diarrhoea while decreasing growth rate
(Scheepens et al., 1991). Compared with constant temperature, fluctuating
temperatures have no effect on antibody level of 30-kg pigs challenged with
Haemophilus pleuropneumoniae. However, it is increased when draughts superimpose
fluctuating temperatures (Kreukniet et al., 1990).
350 Weaning the pig

Whereas it is clear that adverse climatic conditions are detrimental to the health
state of the weaned piglet, the accounting mechanisms are, however, less obvious.
For example, severe cold stress increases the susceptibility of the new-born
(Sarmiento, 1983) and the newly weaned piglet (Armstrong and Cline, 1977) to
enterotoxigenic E. coli diarrhoea. However, when piglets challenged with enterotoxigenic
E. coli are exposed to moderate cold stress, only those fed ad libitum suffer post-
weaning diarrhoea (Wathes et al., 1989). The literature review of Kelley (1980)
indicated that inadequate environment can affect the immune function of the pig.
Blecha and Kelley (1981) reported that exposure to severe cold (0 vs 25°C) for 4
days caused an increase in circulating γ globulin and in antibody titer in the weaned
pig. However, Crenshaw et al. (1986) and Bonnette et al. (1990) failed to
demonstrate any effect of moderate cold exposure (18-19 vs 25-30 °C) on the
systemic immunological state. Nevertheless, in field studies, air quality (temperature,
humidity, ventilation) at entry in the nursery is an important risk factor associated
with post-weaning digestive disorders (Madec et al., 1998), suggesting that it is
difficult to explain the post-weaning diarrhoea by a single environmental factor.
13.4.3 Multifactorial nature of post-weaning disorders: risk factors

associated with housing and management
From the above, it is clear that several factors interact in the onset of diarrhoea. In
an attempt to identify the risk factors associated with housing, Madec et al. (1998)
conducted a survey involving 106 commercial herds and more than 12,000 pigs.
At least 13 risk factors were identified, among which the most important (expressed
as Odds-Ratios) were: feed intake during the 1st post-weaning week, hygiene of
the nursery, air quality, age and body weight at weaning. In this survey,
environmental temperature does not appear to be a risk factor as recorded data
were close to recommended values. Other factors have been identified. For
example, a perforated floor in the dung area is less risky than a solid floor (Rantzer
and Svendsen, 2001). However, it is out of the scope of this single chapter to discuss
all risk factors. They are listed in Table 13.6 together with the corresponding
preventive measures. It is, however, relevant to notice that a high feed intake before
and immediately after weaning is a major factor that minimises the risk of diarrhoea.
As mentioned in Chapter 8, early post-weaning feed intake is considered to be an
important factor in the pathogenesis of the post-weaning diarrhoea that is
associated with villous atrophy (Pluske et al., 1997). A high creep feed intake before
weaning is, to some extent, consistent with both a higher weaning weight and a
higher feed intake post-weaning (Bruininx et al., 2002). Both weaning weight and
ADG (and hence feed intake) during the 1st week post-weaning are also the best
predictors of subsequent performance, accounting for about 80% of body weight
on day 20 after weaning (Miller et al., 1999). Conversely, post-weaning diarrhoea
is usually attenuated by feed restriction (Rantzer et al., 1995). Again, this
demonstrates how complex the aetiology of post-weaning enteric disease is.

Table 13.6. Risk factors to post-weaning digestive disorders and corresponding

preventive measures.
Risk factors Less risky value of the factor Relation with

the disorders1
• Hygiene status in the nursery at the All-in/all-out; cleaning; empty pit below ↓
arrival of the piglets. slatted floor; disinfection; dry floor;
warm (24°).
• Creep-feed intake/piglet last week > 470 g. ↓
prior to weaning (g).
• Air quality all along the post- NH3: < 10 ppm; CO2: < 0,15% + average ↓
weaning period air speed: < 0.10 m/sec; no draught; no
turbulence of the flow; no air flowing
out of the slatted floor; RH: < 85%.
• Temperature (2) • 1st wk PW 28°C (weaning at 4 weeks) Not determ.
• 2nd wk PW 27°C Not determ.
• Water supply (2) Waterers: easy access, to operate, to ↓
maintain clean, potable water.
• Feed intake/piglet during the 1st > 1700 g ↓
post weaning week.
• Age at weaning (days). ≥ 28 days ↓
• Live weight at weaning (kg). ≥ 9 kg ↓
• Number of litters origin per pen <4 ↑
(post-weaning room).
• Number of piglets/pen. < 13 ↑
• Space available at the feeder ≥ 8 cm per pig ↓
• Stocking density (pigs/m2) ≤3 ↓
• Level of concurrent respiratory absence of cough ↑
disorders. average sneezing counts: n < 2 (for 100
pigs, mean of 3 counts of 2 min.)
• Sow / person ≤ 80 ↓
• Overall farm health level Score calculated on the basis of annual ↓
(PW digestive disorders excluded) mortality rate in growing-finishing pigs
and in sows, occurrence of influenza-like
syndromes and PRRS infection in
growing-finishing pigs, diarrhoea prior to
weaning, and diarrhoea during growing-
finishing phase.
1Arrows indicate the relation between the factors and the risk of disease onset (e.g.; the risk of disease
onset increases with decreasing level of hygiene or decreases with the increase in stocking density etc...).
(After Madec et al., 1998).
352 Weaning the pig

13.4.4 Integrating the risk factors to improve health
It is evident that the occurrence of post-weaning diarrhoea is the result of the

cumulative effects of several risk factors. Therefore the approach first implies the
identification of these risk factors. The situation is then improved step-by-step in
an attempt to move towards a less risky profile and a subsequent reduction in
digestive disorders.
An example of a simulation conducted in a severely affected herd is provided in

Figure 13.3. An initial follow-up observation of the batch of piglets to ascertain
the situation regarding health provides the initial risk factors profile of the herd
(to be simple, only 8 categories of risk factors are considered). The initial profile
(left column of Figure 13.3) indicates several major failures (level 1) regarding
hygiene, air quality, etc. Multivariate analysis of the risk factors profile gives the
position (ie, in the ‘at risk’ or ‘secure’ zone) of the herd on the map of
correspondence analysis, as shown in the left part of Figure 13.3. Different
technical solutions can be proposed to attenuate the risks. For example, adoption
of a strict all-in/all out management system with other components of hygiene,
including cleaning and disinfection remaining unchanged, might be sufficient to
attain level 2 for the hygiene risk factor, which moves the herd in position 1 on
the map of correspondence. However, despite a great management effort, migration
towards the target secure area is not significant. Improving the overall category of
factors associated with hygiene moves the farm on position 2 on the map, still far
from the target area. Assuming now that two risk factors, ie, hygiene and air quality,
are simultaneously improved, this allows the producer to attain the secure level
of 4 for both. Because the weight of these two factors is high (as attested by their
Odd-Ratios), the herd position migrates to position 4 on the map and, a significant
improvement of health should be expected. In fact, any change in one risk factor
is dependent on values of other risk factors. When all risk factors are at their most
secure level, the herd is moved to the position 6 on the map. In practice, it is difficult
to attain this situation, however good results are obtained before attaining this ideal
stage. Together, these indicate that because of post-weaning diarrhoea is multifactorial
in nature, simultaneous reduction in risk factors associated with housing and
management is necessary to improve the pig health.
13.5 Conclusion
The period following weaning between 3 and 4 weeks of age is characterised by
rapid changes in environmental requirements of the piglets caused by changes in
feed intake, metabolism and tissue thermal insulation. During the first 10-14 days
after weaning climatic conditions are very important for a successful weaning and
a stable ambient temperature of 26-28°C is recommended for piglets penned on
perforated floors. Once regular feed intake is established the ambient temperature

“at risk” “secure”

area area
=Target area
6
4
2 5
3
1
The different farm profiles 1
Risk factors I : initial 1 2 3 4 5 62
Hygiene 1 2 4 1 4 4 4
Air quality 1 1 1 4 4 4 4
Creep feed intake 1 1 1 1 1 3 4
Feed intake 1st wk PW 1 1 1 1 1 3 4
Weaning age 2 2 2 2 2 2 3
Man power/sow 1 1 1 1 1 1 3
Respiratory. diseases 1 1 1 1 1 1 1
Overall farm health state 2 2 2 2 2 2 4
1 Categorial risk factors with levels ranging from 1 to 4 (i.e;, creep feed intake < 190g/pig
during the week preceding weaning corresponds to level 1; level 4 corresponds to creep
feed intake >490g/pig. Respiratory diseases is assumed to remain unchanged for the
six simulations
2 Profile 6 on the right side of the table corresponds to the less risky levels for all the risk
factors
Figure 13.3. Diagrammatic illustration of the multifactorial efforts needed to reduce

the post-weaning digestive disorders (simulation based on the map of correspondence
analysis described by Madec et al., 1998).
can be gradually decreased by 2-3°C per week until the temperature of the finishing
house is attained. Effects of the pen structure, including flooring materials, feeders
and waterers, stocking density and group size, on performance have been assessed.
Finally effects of climatic and hygienic conditions and management of the nursery
on the onset of digestive disorders are considered. It is suggested that disease
prevention should be directed towards provision of zootechnical profiles that reduce
risk factors. Attention to optimal hygiene, feed intake immediately post-weaning,
354 Weaning the pig

strategic animal movement, thermal environment and air quality all contribute to
reduce the risk of disease.
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360 Weaning the pig

14 Saving and rearing underprivileged and
supernumerary piglets, and improving their
health at weaning
J. Le Dividich, G.P. Martineau, F. Madec and P. Orgeur
14.1 Introduction
Variation in weight is a trait relevant to pig production. However, variations in weight
within groups of pigs under commercial conditions can have a high associated cost
to swine producers, particularly when the all-in, all-out concept of raising pigs is
followed. Within a litter, a two- to threefold difference in birthweights and in
weaning weights are very common in commercial herds. This variation in birth
weight is associated with a high level of mortality among the lightest piglets, termed
as underprivileged. When surviving, these piglets perform worse than their heavier
littermates causing high variation in days to market weight. Birth weight and growth
of the suckling piglets are dependent on several factors, among which, litter size
has the largest influence. During the past decade, pig production has been
characterised by a major improvement in litter size (see review by Legault , 1998).
However, this has resulted in a higher proportion of undersized piglets, whereas
the rearing capacity of- these more prolific sows has not been usually increased
proportionally so that, in a batch-farrowing system, the total pigs born alive can
exceed the rearing capacity of the batch.
Disease control both prior to and at weaning is another major problem encountered
in piglet rearing. Prior to weaning, piglets can be contaminated by the sow. In
addition, the weaned pig is highly susceptible to digestive disorders because of the
relatively immature defence mechanisms of its digestive tract to cope with the
proliferation of toxin-producing microorganisms (Mezoff et al., 1991). As a result,
diarrhoea is the most common clinical problem encountered in the first one or
two weeks after weaning, and this leads to a temporarily impaired growth rate and
sometimes to death.
Therefore, saving these supernumerary and light piglets while helping the latter to
catch up in growth their heavier littermates and improving the health status are
major concerns for the pig producer. Reviews on the nutrition of the weaned piglets
are available (see Chapter 11) and in Veum and Odle (2001).

Le Dividich, Martineau, Madec and Orgeur
14.2 What are underprivileged and supernumeraries?

The term underprivileged is applied to piglets weighing 65-70% of the mean birth
weight of the litter. Compared to their heavier littermates, these piglets have less
body energy stores, are more susceptible to cold, took longer to achieve their first
suckling, and are less competitive at the udder and hence consume less colostrum
(see review by Le Dividich et al., 1998). On the basis that they have a higher risk
of dying both during and/or soon after parturition and before weaning (Figure 14.1),
piglets from modern genotype weighing approximately 1.00 kg at birth can be
classified as underprivileged (Rydhmer, 1992; Léon and Madec, 1992; Herpin et
al., 1996). This body weight is close to the 1.10 kg below which the thermogenic
capacities of the newborn are also impaired (Herpin et al., 2001).
Within a litter, the term supernumerary is applied to piglets in excess of the number
of available functional teats. However, these piglets are usually saved by fostering.
More specifically, in batch - farrowing systems, the term supernumerary refers to
piglets in excess of the number of functional available teats of the batch. In this
chapter, the term supernumerary is referred to those piglets.
Occurrence of these underprivileged and supernumerary piglets is dependent on

several factors including litter size. Litter size is dependent on genotype, and within
a genotype, on the sow parity. However, during the last decades, selection of sows
for litter size at birth has been introduced successfully in many breeding
programmes (Bidanel et al., 1994; Estany and Sorensen, 1995; Legault et al., 1998).
In France, for example, total piglets born per litter has increased from 11.4 to 12.8
over the past decade, with the increase reaching 1 piglet over the last 5 years. This
1500
Stillborn piglets
1200
Birthweight (g)
900 Liveborn piglets dying

before weaning
600
Surviving piglets
300
0
Rydhmer Léon and Madec
(1992) (1992)
Figure 14.1. Birthweight of stillborn piglets, liveborn piglets dying before weaning
and piglets surviving to weaning.
362 Weaning the pig

Saving and rearing underprivileged and supernumerary piglets
increase in litter size has resulted in both a decrease in absolute mean birthweight
amounting to 35-40 g for every additional pig born, and an increased proportion
of low birthweight piglets. Surveys by Le Dividich (1999) and Quiniou et al. (2001)
showed that the increase in litter size from 12-13 to (16 increases the proportion
of weak piglets (< 1.0 kg) from 9 to 23%. In addition, the proportion of high litter
size (≥ 15 total born) has dramatically increased (Figure 14.2), while in most cases
the rearing capacity of these sows has not been increased proportionally unless
some components of the Chinese Meishan breed have been incorporated into these
more prolific sows (Tribout et al., 2002). It follows that selection for litter size has
resulted in an increased proportion of disadvantaged animals while creating
supernumerary piglets.
25 30
20 25
Percentage
20
15
15
10
10
5 5
0 0
< 11 12 - 13 14 - 15 > 16 1971 1981 1991 1995/96 2000
Litter size Year

Figure 14.2. Percentage of small piglets (< 1.0 kg) per litter in relation to litter size
(a) and percentage of high litter size (≥ 15 total born) throughout the three last decades
in France (b). (Adapted from Quiniou et al, 2002 (a) and J. Dagorn, 2002 (Personal
communication)(b).
14.3 Reasons accounting for variation in birthweight

and weaning weight
Piglets are not equal at birth at least with respect to body weight. In addition,
variations in growth rate can occur at any stage of pig life, but particularly during
the suckling phase due to nutritional / environmental influences.
14.3.1 Variation in birth weight
Foetal growth and hence birth weight is determined by the amount of nutrients
transferred from the mother to her foetuses and ultimately the genetic endowment
of the foetus. The transfer of nutrients from the mother to her foetuses depends

on both the size of placenta, uterine blood flow and, to a much lesser extent, on
sow nutrition. However, piglet birthweight is less dependent on level of feeding
of the pregnant sow because it increases by only 4 to 8 g for each additional
megajoule of daily digestible energy intake (Henry and Etienne, 1978). Small piglets
have a lower placental weight and a reduced placental blood flow when compared
with their larger littermates (DeRoth and Bisaillon, 1980; Wootton et al., 1977).
On the other hand, uterine blood flow per foetus decreases with the increase in
the number of foetuses present in the uterine horn (Père and Etienne, 2000), and
this explains why piglets from a large litter size are lighter at birth. These small
placentas are identified as early as 30 days of gestation (Wise et al., 1997), while
the within-litter variation in birthweight is established at 35 days of pregnancy (van
der Lende et al.,1990). Heritability of the within-litter standard deviation in
birthweight is low, ranging from 0.08 to 0.11 (Högberg and Rydhmer, 2000;
Damgaard et al., 2001), but significantly different from zero, thus offering some
premise for genetic selection of sows to give birth to more homogeneous litters.
14.3.2 Variation in weaning weight
During the suckling phase, growth rate of piglets is closely dependent on milk intake
(Noblet and Etienne, 1987) which, in turn, is dependent on both nursing position
of the piglet and its ability to extract milk from the teats. In addition, the mammary
glands are not equal in terms of functionality. The most anterior pairs have more
wet and dry weights, more protein and DNA contents, and, are more functional
than the most posterior pairs of glands (Kim et al., 2000). It follows that, even if
litters are uniform at birth, those piglets adopting the most posterior teats exhibit
a lower growth rate (Figure 14.3). However, heavier pigs at birth usually nurse
anterior mammary glands (Hartsock et al., 1977), which leaves the small pigs to
nurse the posterior glands. Further, there is a strong positive relationship between
piglet body weight, milk consumption and sow milk production (King et al., 1997)
indicating that piglet body weight itself contributes to differences in milk intake.
For example, through d17 to 24 of lactation, lighter piglets are reported to consume
25% less milk per sucking than do heavier ones (Pluske and Williams, 1996).
In summary, pigs are not equal at birth with respect to birthweight. Also the
functionality of the mammary glands is not uniform. These, combined with the
lower ability of the small pigs to compete at the udder and to extract milk from
the teats, may accentuate the disadvantage of the small pigs.
364 Weaning the pig

ADG
170
Birth weight 160
ADG
150
140
130
120
Birth weight, kg
110
1.6
1.4 100
1.2 90
1 80
1 2 3 4 5 6 7 8 Teat position
52 56 50 45 29 34 16 2 n piglets
Figure 14.3. Effect of teat position (1 = anterior) on the average daily gain of nursering
pigs in relation to birth weight (weaning age = 21 d) (Adapted from Kim et al., 2000).
14.4 Differences between underprivileged and

“normal” piglets
14.4.1 Body composition
Is the difference between an underprivileged and a “normal” piglet only a

difference in weight? Within a large range of birth weights (0.5-1.86 kg), Curtis et
al. (1967) and de Passillé and Hartsock (1979) did not observe any differences in
gross chemical composition in piglets. Liver and muscle glycogen concentrations
are only marginally affected (Ojamaa et al.., 1980). Because muscle fibre number
is a major determinant of muscle mass and hence of growth potential, it is important
to examine to what extent the number of muscle fibres is affected by birthweight.
A reduced number of muscle fibres is usually reported in small piglets when
comparing pairs of littermates differing extremely in body weight (Powell and Aberle,
1980; Wigmore and Stickland, 1983; Handel and Stickland, 1987), but not always
(Dwyer et al. 1993). Comparing small (0.80-1.00 kg) to large (1.90-2.10 kg)
littermates Gondret et al. (2003) found that total myofibre number was 13 and
20% reduced in semitendinosus (P < 0.09) and rhomboideus (P < 0.08) muscles,
respectively, in small piglets at slaughter. There is a strong, positive within-litter
correlation between circulating concentrations of insulin-like growth factor I (IGF-
1) and birthweight (Herpin et al., 1992; Wise et al., 1997). IGF-1 and analogues
are reported to stimulate growth in normal and intra-uterine growth-retarded piglets

(Schoknecht et al., 1997; Dunshea et al., 2002). In contrast, Ritacco et al. (1997)
failed to find any stimulatory effect of IGF-1 on the postnatal growth of low-birth
weight piglets. Body weight does influence body composition at weaning. Small
piglets at weaning are leaner (Sloat et al., 1985) and are suggested to have a less
functional digestive tract (de Passillé et al., 1989; Cranwell et al., 1997). Together,
these observations suggest a lower ability of light piglets to withstand the period
of underfeeding following weaning and to cope with the transition to the post-
weaning diet.
14.4.2 Performance of underprivileged pigs
Weight at a given age is important in terms of subsequent growth. This is

illustrated by the fact that 21 to 45% of the variation in weaning weight is explained
by the variation in birthweight (McBride et al., 1965; McConnell et al., 1987; Caugant
and Gueblez, 1993), and that 28 to 49 % of the variation in piglet bodyweight at
the end of the post-weaning phase is explained by the variation in weaning weight
(Miller et al., 1999; Lawlor et al., 2002). The relationships between birthweight and
weight at weaning and at the end of the post-weaning phase are shown in Figure
14.4. Based on these data, each 0.1 kg decrease in birth weight ranging from 0.7
Body weight, kg Body weight at the end of

35 the post-weaning phase
30
25
20
15
Body weight at weaning
10
0
0.7-0.8
0.8-0.9
0.9-1.0
1.0-1.1
1.1-1.2
1.2-1.3
1.3-1.4
1.4-1.5
1.5-1.6
1.6-1.7
1.7-1.8
1.8-1.9
1.9-2.0
2.0-2.1
2.1-2.2
2.2-2.3
2.3-2.4
Birthweight class, kg
Figure 14.4. Effects of piglets birthweight on the mean body weight at weaning and
at the end of the post-weaning phase (age at weaning = 27 d; duration of the post-
weaning phase = 36 d; total number of piglets = 4208). (Adapted from Quiniou et
al., 2001).
366 Weaning the pig

to 2.3 kg, translates into approximately 0.35 and 0.76 kg decrease in the weight
at weaning and at the end of the post-weaning phase, respectively. Overall (Table
14.1), every 0.1 kg decrease in birthweight increases days from birth to slaughter
by approximately 2.3 days. However, an important point is to notice that within
the range of 0.8 to 2.0 kg, birthweight has no marked effect on carcass lean meat
content and on feed efficiency.
From these observations and on the basis of the ability of the piglet to survive, it
is suggested that a birthweight of ≈ 0.9-0.95 kg represents a limit above which saving
of piglets from modern genotypes is not questionable.
Table 14.1. Effects of birth-weight on days to slaughter and carcass lean meat content.
Birthweight (kg) Days to slaughter kg feed : kg gain Lean meat References

content (%)
• 1.57 182 - - Hegarthy and

0.81 205 - - Allen (1978)
• 1.76 160 3.28 54.7 Powell and
1.06 174 3.34 55.6 Aberle (1980)
• 1.87 170 2.94 56.2 Caugant
1.18 179 3.06 56.5 and
1.5 - 2.0 173 - 55.6 Guéblez
< 1.0 184 - 55.2 (1993)
• > 1.35 167 - - Azain
< 0.9 182 - - (1993)
• 1.71 169 2.83 - Mahan
1.45 179 2.82 - (1993)
• 1.70 162 2.70 52.9 Wolter et al.,
1.40 170 2.70 51.7 (2001)
• 1.83 141 2.19 54.9 Wolter et al.,
1.32 148 2.23 55.1 (2002)
• 1.9 - 2.1 154 - 60.9 Gondret et al.
0.8 - 1.0 166 - 59.9 (2003, Pers.com.)
14.5 Management practices to improve survival and

growth of the underprivileged pigs
Management practices aimed at improving the survival and performance of the
disadvantaged pig are directed towards providing assistance to the neonatal pig,
reducing competition among littermates by grouping piglets of similar bodyweight

together within litters (cross-fostering), split weaning, that is, a permanent removal
of part (the heaviest piglets) of the litter a few days before complete weaning, and
appropriate feeding strategies.
14.5.1 Providing assistance to the underprivileged piglets at birth
This includes supervision of farrowing, provision of energy and immunoglobulins

to the pigs and cross-fostering.
14.5.1.1 Supervision of farrowing
Piglets of low birthweight have a high risk of dying during or soon after parturition
(see review in Le Dividich, 1999). These piglets are more susceptible to a higher
degree of asphyxia during parturition than their heavier littermates, and therefore
are less viable at the time of birth as they are less able to maintain their body
temperature, take longer to achieve the first sucking and are less competitive at the
udder (Herpin et al., 1996). Attending farrowing and providing assistance to the
piglets consist mainly in the removal of placenta envelopes around the pig to prevent
suffocation, providing the weak pigs with a source of energy, guiding them to nipples
and positioning them in the heated area. These practices improve survival as
illustrated by the reduction in the number of stillbirths from 0.6- 0.7 to 0.2- 0.3
per litter (Holyoake et al.,1995; White et al.,1996). Although the practices need to
be evaluated against the cost of the extra labour and the benefits derived from raising
extra pigs, it is clear that the economic benefits of the procedures would be
maximised when several litters are being born simultaneously as in the case in
operations which use batch farrowing.
14.5.1.2 Provision of energy and immunoglobulins
The requirement for energy is maximum at birth mainly because of the high rate
of heat loss associated with thermoregulation. Therefore, provision of an adequate
thermal environment and hence minimising heat loss from the piglet is a major
goal during the first postnatal days (see review in Le Dividich and Herpin, 1999).
Sow colostrum is certainly the best food for the newborn pig, providing passive
immunity, energy and growth factors for the developing digestive tract. Colostrum
consumption averages 315-340g/kg BW in the first day of life (Le Dividich et al.,1998)
but can be very variable as suggested by changes in body weight gain ranging from
-136 to + 233 g during the first postnatal day (Thompson and Fraser, 1988). In
addition, because of an increased competition at the udder or sometimes, an
insufficient number of teats or insufficient colostrum production by the sow, there
is a risk that consumption of colostrum will be insufficient with an increasing
number of piglets from a large litter size. Insufficient nutrient (colostrum) intake
368 Weaning the pig

is primarily implicated in deaths due to undernutrition and hypothermia. However,

a sub-optimal intake of colostrum may result in an inadequate transfer of maternal
immunoglobulins (Ig) to the new-born animal and therefore increase susceptibility
to infection, not only in the immediate post-natal period, but also during late
lactation as suggested by the positive relationship between the concentrations of
IgG in the plasma of piglets shortly after birth and survival rate (Blecha and Kelley,
1981; Hendrix et al., 1978).
In the case of litter size exceeding the number of available teats, if no alternative
exists, cross nursing (Donovan and Dritz, 2000) can be efficiently used. Similarly,
a number of pig producers collect colostrum during parturition, and then tube feed
colostrum (40-50g, twice daily). This is becoming a common practice to provide
supplemental energy and immunoglobulins (Ig) to the weak piglets. Freezing of
colostrum is a suitable means of creating a colostrum bank with intact nutritional
and immunological qualities (Klobasa et al., 1998). Several commercial colostrum
substitutes are available with most of them containing Ig derived from cow’s or
ewe’s colostrum. It is assumed that these Ig provide some local protection within
the digestive tract. However, IgG derived from these species is not specific for
pathogens affecting swine and are poorly absorbed by the neonatal pig intestine
(Gomez et al., 1998). More recently, purified porcine Ig has become commercially
available. However, porcine IgG is also poorly absorbed by the piglet (Gomez et
al. 1998; Jensen et al., 2001). Nonetheless, piglets deprived of sow colostrum and
fed artificial milk containing purified porcine IgG for two days are reported to survive
and perform similarly to those fed sow’s colostrum (Gomez et al., 1998).
14.5.2 Cross fostering
Fostering of piglets from one litter to another is used to avoid an excessive number
of piglets in a given litter while creating litters of light and heavy pigs to reduce
competition among littermates. Practised within a few hours after birth, cross-fostering
reduces mortality among the small pigs. English and Bampton (1982) found that
cross-fostered litters had a 40% improvement in piglet survival to weaning. Cross-
fostering is sometimes continuously practised up to weaning so that individuals that
fall back are transferred to a smaller litter. This practice reduces the variation of body
weight at weaning thus producing more uniform litters at weaning (Straw et al.,1998).
However, repeated mixings have detrimental effects on the behaviour of sows and
piglets, resulting in disruption of suckling patterns (Price et al., 1994), increased
non-productive milk letdowns and enhanced aggressive behaviour of sows towards
alien piglets. Compared with fostering limited to the first two days of life, repeated
fostering causes a 13 to 20% reduction in weight gain of the fostered piglets (Straw
et al., 1998; Robert and Martineau, 2001) and sometimes of the resident piglets. In
these conditions, it is doubtful that the reduced variation in weight at weaning is
desirable if it is associated with a reduction in growth rate.

An important point is to recognise that cross-fostering can have negative effects

on the health status of piglets. Extensive cross-fostering maintains a continuous
cycle of PRRSv (Porcine Reproductive and Respiratory Syndrome virus) transmission
(McCaw et al.. 1996). Similarly, Madec et al.. (1999) provide some evidence that
both the sow and contact between piglets are involved in the transmission of the
PCV2 (Porcine Circovirus type 2) which is involved in the Post-Weaning
Multisystemic Wasting Syndrome (PMWS). Reduced mixing of litters is therefore
strongly recommended to minimise the impact of these diseases in affected herds.
14.5.3 Split weaning
Selective weaning of the heaviest piglets of the litter some days before normal
weaning improves the growth of the lightest piglets left with the sow allowing, to
some extent, for these piglets to catch up in growth to their heavier littermates at
normal weaning. This practice reduces the competitive pressure at the udder at an
age when the supply of milk by the sow does not fulfil the energy needs of the
piglets, and results in an enhanced milk intake in the light piglets. Pluske and
Williams (1996) showed that when litters were reduced from 10 to 5 pigs per sow
for 7 days before weaning at 29 days, milk intake per pig increased by 49%. This
was related to multiple teat swapping and a longer duration of suckling during
milk let down. Most authors (Wu et al., 1985; Mahan, 1993; Pluske and Williams,
1996; Vesseur et al., 1997) reported an improved growth rate ranging from 27 to
61%. Kavanagh et al. (2002) showed that pig weaning weight improved by up to
0.23 kg for each 1 pig reduction in litter size. However, this weight advantage
disappears in the early post-weaning period (Pluske and Williams, 1996; Vesseur
et al., 1997). It is suggested (Pluske and Williams, 1996) that pigs that are left to
suckle after the reduction in litter size suffer a greater setback after weaning than
their counterparts in control litters. In summary, this practise temporarily promotes
the growth of small pigs but offers little in the way of improving their lifetime
performance.
14.5.4 Feeding strategy
14.5.4.1 Suckling phase
Providing litters with supplemental liquid milk replacer during lactation can increase
piglet weaning weights by 10 to 38% (Le Dividich and Sève, 2001). However, to
what extent this practice could promote the growth of litters of light piglets grouped
on a sow remains to be determined. Sometimes, piglets which do not keep up with
their littermates are weaned and reared with EMMA (Electronic Mother Milk
Application). However, to date there is only evidence from the popular farming
press in relation to this practise.
370 Weaning the pig

14.5.4.2 Weaning phase
Daily weight gain in the week after weaning is a significant predictor of subsequent
performance (Miller et al., 1999). However, provision of a complex diet high in
energy and dairy milk products to litters of small piglets (Himmelberg et al., 1985;
Mahan and Lepine, 1991; Mahan, 1993; Dritz et al., 1996a), or supplemental milk
replacer (Wolter and Ellis, 2001) or by increasing the duration of the phase 1 post-
weaning diet (Himmelberg, et al., 1985; Mahan et al., 1998), have only relatively
modest improvements in piglets performance in the overall post weaning phase.
Further, this advantage disappears gradually in the growing-finishing period
(Dritz et al., 1996a; Whang et al., 2000).
14.6 Growth potential of underprivileged piglets

From the above discussions, it is clear that most of the attempts failed to
substantially improve the life-long performance of underprivileged piglets. Now
the question is, to what extent can these piglets catch up in growth to the large
piglets? Neither intra-uterine growth retardation induced by protein restriction of
the sow (Davis et al., 1997) nor birthweight ranging from 0.85 to 1.40 kg
(Campbell and Dunkin, 1982) have effects on the potential for protein synthesis
and growth performance of the piglet. Milk intake (i.e., g milk/kg BW) is not affected
by birth weight (Campbell and Dunkin, 1982), however, absolute milk intake is
lower in light piglets. Similarly, in the growing-finishing period, absolute feed intake
is also consistently reported to be lower in lighter pigs, while feed efficiency is little
or not affected. Thompson and Fraser (1986) showed that piglets’ weight gain in
a given week tends to be a fixed percentage of the body weight at the beginning
of the week. Together, this suggests that the lower performance achieved by light
piglets is, to some extent, determined by their lower ingestive capacity and hence
by their body weight.
14.7 Supernumerary piglets

Because of the increased competition at the udder, a litter size higher than the
number of available functional teats results in delayed first colostrum ingestion
and formation of the nursing order, lower teat fidelity, higher rate of mortality, more
nursing failure and reduced growth of the litter (P. Orgeur, Personal
Communication). Ways to save and to rear the supernumeraries include (i) weaning
at d 1-3, or (ii) grouping on d 1 the piglets in excess of the available teats to form
a new litter. This new litter is fostered onto a dam of the previous batch whose
litter is weaned. In all cases, piglets are allowed to receive colostrum from their
dam.

14.7.1 Weaning at day 1-3
Piglets artificially fed a liquid diet high in dairy products can exhibit growth rates
as high as 400-550g / d (Hodge, 1974; Harrell et al., 1993). More usually, satisfactory
growth rates of ≈ 200 g/d are reported (Pettigrew and Harmon, 1977; Pettigrew et
al., 1977). Reduced performance was found by Huysman et al. (1994) in piglets
reared from d 3 to d 28 with EMMA compared with that obtained using foster-
sow nursing (122 vs 206g). In fact, this practice requires specialised nurseries,
sophisticated milk dispensers, and because of the high occurrence of diarrhoea, a
high level of sanitation.
14.7.2 Fostering onto a nurse sow
In a batch-farrowing system, the practice implies the choice of a nurse sow from
the previous batch so that, at the time of fostering, the older litter can be easily
weaned. The size of the new litter is similar to that of the nurse sow and, in practice,
is composed of large pigs which have more opportunity to ingest enough
colostrum from their dam. As mentioned above, fostering of piglets practised after
the nursing order has been established, i.e., after 2-3 days, has detrimental effects
on the behaviour of sows and piglets. However, supplying a nurse sow with a new
litter aged 24-36 hours has only minor effects on the nursing behaviour of the sow.
In a study involving 18 nurse sows (Orgeur et al., 2000), all piglets survived and
only one sow displayed aggressive behaviour towards the new litter and refused
to nurse. On average, sows nursed the new litter within 5h (range 1.35 to 8.15 h)
following the piglets introduction. The growth rate of the new litter during the first
postnatal week is acceptable, albeit lower (170 vs 205 g/pig/d) than that of the
control pigs. The new litter is then weaned at one week of age or sometimes at the
normal weaning age.
14.7.3 Weaning at one week of age
Weaning at 7-14 d of age is usually associated with a severe growth check caused
by the low dry food intake (Leibbrandt et al., 1975; Zijlstra et al., 1996; Heo et al.,
1999; Kim et al., 2001). In the study by Orgeur et al. (2000) involving weaning at
7 d of age, pigs at 21 days of age were 40% lighter than their counterparts (sow
reared). However, the difference decreased to 7.5% at d 74 and to 3.7% at slaughter
weight. Other studies (Hohenshell et al., 2000) reported similar performance in
early (8-13d) and late weaned pigs (27-34 d). However, the severity of the growth
check can be markedly overcame by providing the piglets with a liquid feed (Lecce
et al., 1979; Zijlstra et al., 1996; Heo et al., 1999; Kim et al., 2001). An important
point to recognise is that early weaning has little effect on body composition at
slaughter weight (Pluske et al., 1995; Dritz et al., 1996a; Kim et al., 2001; Le Dividich
et al., Pers. Communication).
372 Weaning the pig

In summary, advantages of the use of a foster sow associated with early weaning
are (i) no disturbance in the batch farrowing system, (ii) minimal mortality among
the fostered pigs while growing reasonably well, (iii) no marked digestive
disturbance at weaning and (iv) no effect on carcass composition. The weak point
of the practice is the low level of performance in the immediate period following
weaning, but this can be improved by feeding liquid diets.
14.8 Management to improve the health of piglets

One of the major problems in the pig industry is the postweaning syndrome (PWS),
which occurs mainly through diarrhoea mainly caused by E. coli, leading to poor
performance during a period of about 10 days following weaning (for details, see
Chapter 9 and the review of van Beers-Schreurs et al., 1992). Weaning at about 3
weeks of age, as practised in the major pig producing countries, implies the
withdrawal of milk resulting in the loss of milk immunoglobulins protection at
an age when maternal antibodies are at the lowest levels and active humoral and
mucosal immunity are still impaired. At weaning, the piglet is exposed to novel
antigens associated with food and to changes in microbial flora while the low feed
intake immediately postweaning induces marked morphological changes in the
intestine. Although the aetiology of diarrhoea is multifactorial, it is to some extent,
controlled by feed additives, including acidifiers, antibiotics and antimicrobial
growth promoters such as copper sulphate and zinc oxide and pre-and probiotics.
However, there is currently pressure to reduce the use of antibiotics, copper sulfate
and zinc oxide. In addition, dependent on the immune state of the piglet, the sow
also may be a source of contamination for her litter. Production systems such as
all-in / all-out (AIAO) production and weaning at an age when the immune
protection of the litter is still adequate have the potential to improve both the health
of the piglet and production efficiency.
14.8.1 All-in / All-out management system
The AIAO procedure has become an essential part of successful management of

the nursery. The procedure includes simultaneous weaning of pigs and simultaneous
emptying of the nursery, and involves cleaning and disinfection between batches,
and a delay of at least 3-4 days between two batches, thus limiting the disease
transmission between batches. The procedure is shown to improve the air quality
(Cargil and Banhazi, 1997). Advantages of the AIAO were first described by Schneider
and Bronsch (1973). Compared with continuous flow (CF), an AIAO system resulted
in a 26% and 8% improvement of ADG and feed efficiency, respectively (Table 14.2),
and this was due to reduced incidence of diarrhoea. More recently, Dewey et al.
(2002) assessed the health status for PRRS, Mycoplasma hyopneumoniae, Brachyspira
hyodysenteriae and Actinobacillus pleuropneumoniae of 3000 pigs from 8 commercial
herds in Ontario. Pigs were ear tagged and weighed at birth, weaning, 7, 14 and

Table 14.2. Continuous flow vs all-in, all-out management system on the performance
of piglets weaned at 3 weeks of age and on air quality.
Continuous All-in, References

flow all-out
Avg daily gain1 400 503 Schneider and Bronsch, (1973)

Feed/gain1 1.89 1.74
Total particles (mg/m3) 2 1.549 0.937 Cargill et al. (1997)
Airborne bacteria (103 cfu/m3) 2 124.6 94.2
1 From d 21 to d 63
2 Data obtained in growing-finishing houses
21 weeks, and managed in AIAO or CF. Farms using a CF management system were
more positive for disease-causing agents than those using the AIAO production
system. In addition, at 21 weeks of age, pigs on the AIAO system were 26 kg heavier
(100 vs 76 kg) than those on the CF system. Together, these highlighted that, when
applied correctly, the AIAO management system is effective in controlling a number
of diseases, while improving production. Yet, its efficiency is enhanced when it is
associated with segregation.
14.8.2 Segregation
Major progress in the control of the transmission of infectious agents from the sow
to her litter is associated with early weaning procedures. Early weaning is designed
to eliminate, or at least reduce, the effective risk of transfer of many diseases from
sows to piglets while the passive immunity that the piglet has derived from colostrum
intake is still at a high protective level. The original method (Medicated Early Weaning,
MEW) was first described in the UK by Alexander et al. (1980). The procedure includes
medication of the sow during late gestation and during lactation, farrowing in sites
physically isolated from the rest of the herd, weaning of piglets at 5 days of age and
moving them to off-site facilities (Off-site segregated early weaning, OFSSEW).
Subsequently the procedure has been modified towards weaning between 10-12 and
15-18 days of age and a reduced medication (non-medicated early weaning). These
include mainly ONSSEW (On Site Segregated Early Weaning, i.e., nursery physically
isolated from the breeding herd), ISOWEAN® (Isolated Weaning), or SEW (Segregated
Early Weaning) with nurseries strictly isolated from older groups of pigs (MSP, Multi-
Site Production). All these methods are largely related to the management of the
piglets’ passive immunity. The half life of IgG, IgA and IgM is approximately 10, 3
and 2 days, respectively, (Koblasa et al., 1981). However, both the level and duration
of passive immunity are quite variable (Figure 14.5) as they are dependent on the
374 Weaning the pig

amount of colostrum intake and on its quality which, in turn, is dependent on the
immune status of the sow, with all being variable.
Strategies aiming at eliminating pathogens are based on weaning age together with
a medicated protocol (Table 14.3). However, the practice fails to eliminate
Streptococcus suis and PRRSv. Vaginal secretions are assumed to be the source of
transmission of Streptococcus suis to piglets during parturition (Amass, et al., 1996).
Further, disease caused by Streptococcus suis is even suggested to be exacerbated in
some inappropriately managed SEW (Moore, 1995). However, the SEW / MSP system
does minimise the effects of disease outbreaks, as illustrated by the consistently
reported improvement in piglet performance (Coffey and Cromwell, 1995;
Patience et al., 1997; Fangman et al., 1996) (Table 14.4) but is not a panacea for
disease control.
However, early weaning may reduce sow productivity because short lactation lengths
are sometimes associated with an increased weaning-to-service interval, reduced
farrowing rate and subsequent litter size (for review, see Cosgrove et al., 1997).
Nonetheless, the SEW / MSP System has proven to be efficient to improve piglets
health and performance which, to some extent, can offset the extra cost associated
with the system and the possible reduced sow productivity.
50
45
40
Ig conc entration (mg/mL)
35
30
IgG
25 IgM
IgA
20
15
10
0
0 5 10 15 20 25 30 35
Post natal day
Figure 14.5. IgG, IgA and IgM levels in the sera of suckling piglets (Adapted from
Klobasa et al., 1981).

Table 14.3. Weaning age allowing to prevent spread of disease.
Disease Weaning age (days)
Mycoplasma hyponeumoniae < 10

Pasteurella multicoda < 10
PRRSv < 10
Salmonella choleraesuis < 12
Haemophilus parasuis < 14
Aujesky’s disease < 21
Actinobacillus pleuropneumoniae < 21
(After Harris, 1993)
Table 14.4. Effects of of site segregated early weaning on piglets performance1.
ADG Feed conversion ratio (kg feed / kg gain)
Period (d) Control ONSSEW OFSSEW Control ONSSEW OFSSEW
12-21 250 109 188 1.50 0.99

21-26 140 190 215 1.13 1.18 1.47
21 56 425 439 511 1.36 1.39 1.34
1 O SSEW, on site; OFSSEW, off site. Piglets were weaned at 21 ±3 days of age (Control)
N
or at 12 ± 2 days of age (ONSSEW, OFSSEW).
Adapted from Patience et al. (1997).
14.9 Conclusion: the need for research

In this chapter we attempted to provide information regarding the extent and the
occurrence of underprivileged and supernumerary piglets and ways of improving
their survival and performance. A major point to notice is that the occurrence of
small and supernumerary piglets is markedly increased in hyperprolific sows. As
a whole, saving small piglets (0.90 - 0.95 kg) at birth is not questionable, however
a long-term improvement of their performance is still questionable. The basic
question that arises is to what extent the growth potential of underprivileged piglets
is lower than that of their heavier littermates. However, because bodyweight at
weaning and growth rate during the week following weaning are major determinants
for subsequent performance, we suggest that more research should be focused on
specific strategies helping these piglets to realise their growth potential during the
376 Weaning the pig

suckling period and on feeding strategies making the suckling-weaning transition

smoother. Ultimately, in the light of reducing the extent of both supernumerary
and small piglets, it should be relevant to select sows having more available uniform
teats while giving birth to more uniform litters.
The all-in/all-out management system and, early weaning associated with off-site
nursery, have proven to be efficient in improving the health of the weaned piglet.
But weaning at an age lower than 21 days is not allowed in certain countries (i.e.,
in the EU), while segregation can be costly. However, adequate management of
the immune status of the sow and piglets appears promising in improving piglets
health.
References
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Amass, S.F., L.K. Clark, K. Knox, C.C. Wu and M.A. Hill, 1996. Streptococcus suis colonization of
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of Georgia, pp. 49-54.
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15 Productivity and longevity of weaned sows
A. Prunier, N. Soede, H. Quesnel and B. Kemp
15.1 Introduction
In modern pig producing systems, the reproductive life span of sows is close to 5
litters: 4.2 in the USA (Lucia et al., 1999), 4.7 in France (GTTT, 2000) and 5.4 in
Great Britain (MLC, 1999). This average of 4 to 5 litters is well below the
suggested optimum of about 7 to 8 litters (review: Gill, 2000). Interestingly enough,
this figure does not seem to have changed in the last decades: Dagorn and Aumaître
in 1979 reported an average sow life span of 4.2 litters in France and, Kroes and
Male, also in 1979, reported an average of 4.6 litters per sow in The Netherlands.
Therefore, the increase of on average 4.5 piglets weaned/sow/year over the last 20
years (GTTT, 1980 and 2000) does not seem to have resulted in a shorter
reproductive life span. A proportion part of the females in a pig herd is culled for
reproductive reasons, such as no estrus, failure to conceive, abortions, and small
litters. These culls are of great economic importance for pig producers for many
reasons. Females culled for reproductive reasons achieved a lower parity number,
have a higher proportion of non-productive days and produce fewer weaned pigs,
both per year of herd life and during their total herd life compared to females culled
for any other reason (Dijkhuizen et al., 1989; Lucia et al., 2000). First-litter sows
are well known for their reproductive problems. Field data show that these sows
have the highest risk of a prolonged weaning-to-estrus interval and of low
pregnancy rate after insemination (Vesseur et al., 1994a, b; Tummaruk et al., 2000),
resulting in a high culling rate (Dijkhuizen et al., 1989). In second-litter sows, a
relatively low litter size is frequent (the so-called ‘second-litter syndrome’; Morrow
et al., 1992), which is also attributed to the reduced reproductive functioning of
the sows after weaning their first litter. In this paper, an overview will be given of
the reproductive causes of culling. Thereafter, the physiological consequences of
lactation and weaning on the reproductive axis will be discussed. Subsequently,
the major reproductive parameters for reproductive performance will be discussed,
including the influence of internal and external factors on underlying reproductive
parameters, such as ovulation rate and embryo survival.
15.2 Reproductive causes of culling

Reasons of sow culling have been analysed in numerous retrospective studies based
on producer records in databases such as GTTT in France (Dagorn and Aumaître,
1979), VAMPP in the Netherlands (Dijkhuizen et al., 1989), NSRS in Norway
(Sehested and Schjerve, 1996) and PigCHAMP in the USA (Koketsu et al., 1997a;
Lucia et al., 2000). These studies have shown that a large proportion of culled sows
is removed from herds for reproductive reasons, such as anestrus, failure to farrow

Table 15.1. Reasons for culling sows in commercial herds from different countries (percentage of culled sows).
386
Reproductive Low Peripartum Low milk Other
Source failure2 litter size disorders3 production4 Locomotion Death Age reasons Country and year
Dagorn & Aumaître, 1979 39.2 4.6 6.3 6.1 8.8 6.5 27.2 1.3 France, 1975-1976
Zivkovic et al., 1986 36.4 15.9 ? 12.1 9.1 ? ? 26.5 Yugoslavia, 1984
Dijkhuizen et al., 1989 34.2 6.2 ? 13.9 10.5 ? 11.0 24.2 NL, 1985-1986
Bhatia, 1989 33.0 ? ? ? 8.7 8.0 8.4 41.9 India
Lucia et al., 20001 33.7 14.1 3.4 4.9 13.2 7.4 8.7 14.6 USA, 1992
Sehested & Schjerve, 1996 28.7 4.0 4.0 4.8 10.2 4.2 11.3 32.8 Norway, 1992-1994
Prunier, Soede, Quesnel and Kemp
Heinonen et al., 1998 31.2 7.9 4.3 3.4 12.6 3.9 15.5 21.2 Finland, 1992/1993
Mean 33.8 8.8 4.5 7.2 10.4 6.0 13.7 23.2
1Including gilts
2Including anestrus, failure to conceive and abortion
3Including farrowing difficulties such as matritis and mastitis...
4Including poor litter growth, abnormal teat
Weaning the pig

Productivity and longevity of weaned sows
and small litters. These reproductive reasons account for 33 to 52% of the total culls,
and even add up to 43-64% if mothering ability (peripartum disorders, agalactia
or low milk production) is added (Table 15.1). When looking more carefully at the
reproductive reasons of culling, data show that failure to conceive or to farrow are
the main causes accounting each for nearly one third of the culls (Table 15.2). Anestrus
(including silent ovulation) is another important reason which represents nearly
25% of the culls for reproductive failure. Besides culling for reproduction, other main
causes for culling are: old age (8-27% of total culls), locomotion disorders (8-13%
of total culls) and death (4-8% of total culls) (Table 15.1).
Table 15.2. Reasons for culling sows in commercial herds within the reproductive failure
category (percentage of sows).
Failure to Failure
Source Anestrus conceive2 to farrow3 Abortion Country and year
Koketsu et al., 1997a 25.2 37.1 30.4 7.4 USA, 1991

Sehested & Schjerve, 1996 23.4 31.7 36.8 8.0 Norway, 1992-1994
Lucia et al., 20001 27.0 39.7 33.34 USA, 1992
Heinonen et al., 1998 22.3 77.75 Finland, 1992/1993
1Including gilts
2Normal return to heat (18-25 days after service)
3Abnormal return to heat (>25 days after service)
4Including abortion
5Including failure to farrow and abortion
As could be expected, reasons for culling vary with parity of the females. “True”
reproductive disorders (anestrus + failure to conceive/farrow + low litter size at birth)
account for nearly 40% of total culls in young sows (parities 1 and 2) and only
for 17% in old ones (parity > 7); (Figure 15.1). However, when sows that are culled
because of their age are excluded from the analyses, the difference in the reasons
for culling between young and old sows is much smaller. For instance, it can be
calculated from Norwegian data that nearly 40% of first-parity sows are culled for
“true” reproductive disorders versus 34% of sows whose parity is higher than 7,
when the age reason is excluded (Sehested and Schjerve, 1996).
A potential limitation of studies from database analyses is the fact that definitions
of removal reasons are not standardised and, very often, sows are not culled for a
single reason but for several reasons. For instance, an old sow with low productivity
and lameness may be culled for low mothering ability, for lameness and for its

Figure 15.1. Influence of the parity on the reasons of culling in Landrace x Yorkshire
sows (based on Sehested and Schjerve, 1996).
age. However, the producer has to choose only one reason. This may underestimate
one parameter and overestimate the other. Moreover, producers may falsely
diagnose reproductive failures. Geudeke (1992), for example, examined genital tracts
of 5969 sows. Of the 13.7% sows that were culled for anestrus, almost 60% had
normal ovaries, 16.9% had inactive ovaries and 25.3% had cystic ovaries.
15.3 Consequences of lactation and weaning on the

reproductive axis
Lactation normally almost completely inhibits the activity of the reproductive axis.
Weaning removes this inhibition and thus results in estrus behaviour and ovulation
(reviews: Britt et al., 1985; Varley and Foxcroft, 1990; Quesnel and Prunier, 1995).
Under specific conditions, lactational estrus and ovulation may occur (see further).
15.3.1 Postpartum inhibition
15.3.1.1 Long-term effects of pregnancy and farrowing
Weaning piglets at birth, instead of at 3 to 5 weeks of age, results in a higher incidence

of anestrus and cystic ovaries, a longer weaning-to-estrus (weaning-to-service)
interval, or a reduced litter size (Peters et al., 1969; Elliot et al., 1980; Varley and
Atkinson, 1985). This suggests that physiological events associated with pregnancy
and farrowing have an inhibitory influence on the reproductive axis.
388 Weaning the pig

During the last month of pregnancy, LH secretion is inhibited by the high

concentrations of progesterone synthesized by corpora lutea and probably also by
the high levels of estrogens originating from the feto-placental units. Farrowing is
accompanied by a drop in progesterone and estrogen concentrations and is followed
by an immediate increase in gonadotropin secretion in suckled sows and in sows
weaned immediately after farrowing (zero-weaned sows; Smith et al., 1992; De Rensis
et al., 1993a). Therefore, postpartum anestrus in zero-weaned sows is not related
to an impaired secretion of gonadotropins just after farrowing, as observed in
domestic ruminants. Anestrus and cystic follicles can be due to the lack of a
preovulatory LH-surge resulting from either the high levels of corticosteroids
observed in early-weaned sows (Ryan and Raeside, 1991) or an impaired
responsiveness to positive feedback effects of estradiol-17β at the hypothalamic-
pituitary level (Elsaesser and Parvizi 1980; Cox et al. 1988; Sesti and Britt 1993).
This responsiveness is partially recovered between the third and the fourth weeks
of lactation. Decreased responsiveness of the pituitary in early lactation may be
partly related to LH stores in the pituitary gland, that are depleted just after farrowing
and progressively restored during lactation (Crighton and Lamming 1969; Bevers
et al. 1981). However, the pituitary answer to the positive feedback of estrogens
has not been investigated in zero-weaned sows.
Another long-term effect of gestation on the reproductive axis involves the uterus,
which was submitted to considerable changes during gestation. The uterine
involution is rapid during the first week postpartum (p.p.) but is completely achieved
only within 21 to 28 days p.p. in lactating sows (Palmer et al., 1965a, b; Smidt et
al., 1969). In early-weaned sows (4 days p.p.), the involution is still slower (Smidt
et al., 1969). Therefore, the morphology and physiology of the genital tract may
not be optimal for fertilization and blastocyst implantation in sows weaned at
farrowing or shortly after, resulting in a reduced rate of gestation (and a longer
weaning-to-service interval) or a reduced litter size.
15.3.1.2 Influence of suckling
Mean concentrations of circulating LH are high during the two or three days
following parturition and then decrease in lactating sows (Tokach et al., 1992; De
Rensis et al., 1993a, b). These concentrations and the number of LH pulses remain
low during early lactation, from about day 4 to 14, and gradually increase
thereafter (Stevenson et al., 1981; Shaw and Foxcroft, 1985; De Rensis et al., 1993b).
There is consistent evidence that suckling (stimulation of the teats by the piglets)
and piglet proximity provide physical and behavioural stimuli to the sow that induce
the release of neurotransmitters and opioid peptides, through neuroendocrine
reflexes (review: Kraeling and Barb 1990). These factors stimulate the secretion of
pituitary hormones involved in milk ejection and production (e.g. oxytocin,

prolactin, growth hormone, cortisol) and suppress LH secretion by inhibiting the

GnRH pulse generator. The suckling-induced inhibition of LH begins only within
two or three days p.p. (De Rensis et al., 1993a). It is mainly due to endogenous
opioids during established lactation, whereas its development during the early p.p.
period appears to be opioid-independent (De Rensis et al., 1993b, 1998a). In
addition to the opioidergic system, a dopaminergic regulation of LH secretion exists
during the fourth week of lactation as shown by De Rensis et al. (1998b).
However, these authors provided evidence that prolactin itself was not involved
in the control of the GnRH/LH secretion during lactation. This is in contradiction
with the prevailing hypothesis suggesting that prolactin may partly inhibit LH release
during lactation (reviews: Van de Wiel et al., 1985; Dusza and Tilton, 1990).
The progressive decrease in the inhibition of LH secretion could be related to a

decrease in suckling frequency and intensity over the four weeks of lactation
(Pederson et al., 1998; Jensen et Recén 1989) and could be related to the increase
in the pituitary LH response to GnRH as lactation progresses (Bevers et al., 1981;
Rojanasthien et al., 1987a).
Data on the variation in FSH secretion during lactation are less consistent. Within
the three days following parturition, FSH concentrations do not vary with time and
are similar in suckled and zero-weaned sows (De Rensis et al., 1993a). From the
second week of lactation onwards, a continuous increase in plasma FSH has been
observed by Stevenson et al. (1981) and De Rensis et al. (1993b). Ovariectomy during
lactation is accompanied by an increase in FSH concentrations without affecting
LH secretion (Stevenson et al., 1981), demonstrating that FSH secretion is more
controlled by the ovarian negative feedback (presumably by inhibin) than by
suckling.
In suckled sows, large follicles (> 5 mm) are present in the ovaries during the first
week p.p. and are replaced by small and medium-sized follicles (3-4 mm) during
the second week (Crighton and Lamming, 1969; Kunavongkrit et al., 1982;
Rojanasthien et al., 1987b). During the third and fourth weeks of lactation, follicular
growth resumes as a consequence of the progressive increase in LH pulse frequency
but most follicles are < 5 mm in diameter (review: Britt et al., 1985). Because of
the inhibition of follicular growth, circulating estrogens are generally low (Baldwin
and Stabenfeldt, 1975; Kirkwood et al., 1984; Prunier et al., 1993).
Beside this general pattern of follicular growth during lactation, Lucy et al. (2001)
reported differences in follicular development between sows before weaning
using ultrasonography. Sows can have relatively inactive ovaries (follicles less than
2 mm in diameter) or have large follicles present.
390 Weaning the pig

Ovulation can be induced during lactation by administration of exogenous

gonadotropins (review: Britt et al., 1985). Reduced follicular growth during
lactation is thus primarily due to low gonadotrophic signal. However, other factors
can act directly at the ovarian level for instance, by modulating the follicular
responsiveness to gonadotropins.
15.3.1.3 Influence of the metabolic status
During lactation, sows are usually fed ad libitum or close to ad libitum and their
voluntary feed intake increases during the first three weeks postpartum (review:
Dourmad, 1988). Energy requirements for milk production simultaneously
increase and peak during the third week of lactation (Noblet and Etienne 1986).
Voluntary feed intake depends on numerous endogenous and environmental factors
(review: Dourmad, 1988; Eissen et al., 2000) and is often not sufficient to meet
the high energy and nutrient requirements for milk production. This appears to
be particularly true in high-yielding multiparous sows and in most first-litter sows,
that have a lower feed intake than multiparous sows but a relatively high milk
production (> 7-8 kg/day). The energy balance of these sows is thus negative
throughout lactation. A slight catabolic state does not affect gonadotropin
secretion, even in first-litter sows, as evidenced in lactating sows that consume
between 80 and 90% of the metabolic energy requirements for maintenance and
milk production (review: Prunier and Quesnel, 2000). Moreover, making sows
anabolic during lactation, by superalimentation via a stomach cannula, did not
alleviate the negative impact of suckling on LH secretion around weaning and did
not improve reproductive performance after weaning, as shown by Zak et al. (1998).
In their experiment, however, the control sows already had a good reproductive
performance. In contrast, a strong catabolic condition during lactation has been
clearly demonstrated to inhibit the activity of the hypothalamo-pituitary complex
in primiparous sows. Indeed, restriction of feed (Reese et al., 1982; Zak et al., 1997a;
Quesnel et al., 1998a), energy (Armstrong et al., 1986a; Koketsu et al., 1996a) or
protein (King and Martin, 1989; Jones and Stahly, 1999a; Yang et al., 2000a)
generally inhibit the secretion of LH during lactation and delay estrus after weaning.
Lactation induces metabolic adaptations that favour the preferential drive of nutrients
towards mammary glands. Concentrations of prolactin, growth hormone (GH),
insulin-like growth factor-I (IGF-I) and insulin are relatively high during lactation
due to suckling and high feed consumption. During the course of lactation, prolactin,
GH and IGF-I decline slowly, possibly due to attenuated intensity of suckling stimuli
(Rojkittikhun et al., 1993; Schams et al., 1994). Plasma glucose, insulin, IGF-I and
leptin also decrease throughout lactation in those sows with increasing nutritional
deficit and body reserve mobilization (Prunier et al., 1993; Messias de Bragança
and Prunier, 1999; Van den Brand et al., 2001; Prunier et al., 2001). Metabolic
adaptations have been extensively described in primiparous sows submitted to a

severe level of nutritional restriction during lactation. Compared with well-fed sows,
feed-restricted sows have lower plasma insulin, IGF-I and leptin but higher plasma
NEFA and GH (Koketsu et al., 1996a; Zak et al., 1997a; Quesnel et al., 1998a; Mao
et al., 1999). Obviously, the GH-IGF-I axis becomes uncoupled. Together with low
insulin, this favors maternal catabolism. There is increasing evidence that these
changes in metabolites and metabolic hormones signal to the reproductive axis
the changes in metabolic state (reviews: Booth, 1990; Pettigrew and Tokach, 1993;
Prunier and Quesnel, 2000). Amongst these potential mediators, glucose, insulin
and IGF-I could play a preferential role. A strong reduction in glucose and/or insulin
has been associated with inhibited secretion of LH in prepuberal gilts submitted
to severe feed-restriction or to experimentally-induced glucose restriction (Booth,
1990; Barb, 1999) and in diabetic gilts (Angell et al., 1996). In lactating sows, LH
pulsatility around weaning has been positively related either to insulin (Quesnel
et al., 1998b) or IGF-I (Van den Brand et al., 2001). Feeding a carbohydrate-rich
diet increases LH pulsatility during early lactation (day 7) but not later in lactation
(days 14 or 21) despite higher post-feeding insulin levels at both stages (Kemp et
al., 1995; Van den Brand et al., 2000a). Evidence is still lacking that reduced insulin
alters LH pulses in catabolic lactating sows. At the ovarian level, consistent
evidence exists that insulin and IGF-I stimulate follicular responsiveness to
gonadotropins and folliculogenesis (Adashi et al., 1992). Therefore, reduced
concentrations of insulin and IGF-I in plasma and/or follicles observed in feed-
restricted lactating sows (Quesnel et al., 1998a, b) may reduce the ovarian
response to the gonadotropic stimulation at weaning and alter subsequent
follicular development. Indeed, Quesnel et al. (1998a, b) have observed that feed
restriction during lactation induces a reduction in insulin, IGF-I and LH
concentrations at day 27 of lactation. This results in a concomitant decrease in the
number of follicles measuring at least 4 mm in diameter and in the proportion of
healthy 1-3 mm follicles at weaning (day 28). Similarly, Clowes et al. (1999) have
shown that protein restriction of primiparous sows has a negative influence on the
number of large follicles (4 to 6 mm) on day 23 of lactation. Moreover, follicular
fluid from these sows has a lower potential to support in vitro nuclear maturation
of oocytes.
15.3.2 Removal of the inhibition of the hypothalamic-pituitary-ovarian

axis at weaning
Weaning piglets suppresses the inhibitions originating from the suckling stimuli
and from the potential catabolic status. This results in an immediate and transient
increase in mean concentrations of LH and LH pulse frequency ovulation (reviews:
Britt et al., 1985; Varley and Foxcroft, 1990; Quesnel and Prunier, 1995). Increased
secretion of FSH in response to weaning has been observed in some experiments
(Cox and Britt, 1982; Shaw and Foxcroft, 1985) but not in others (Stevenson et
al., 1981; Edwards and Foxcroft, 1983; Foxcroft et al., 1987). This divergence between
392 Weaning the pig

LH and FSH profiles around weaning supports the existence of different controls
of gonadotropin secretion: LH secretion mainly depends on suckling and lactation
influences, whereas FSH mainly depends on ovarian negative feedback.
The increase in gonadotropin secretion at weaning stimulates follicular growth and

maturation, as evidenced by the immediate increase in the number and size of large
follicles (diameter > 5 mm) after weaning (Palmer et al., 1965a; Cox and Britt, 1982;
Armstrong et al., 1986b). Relatively high concentrations of estradiol-17β and
testosterone are measured in follicles 24-48 hours after weaning (Foxcroft et al.,
1987; Killen et al., 1992). Plasma estradiol-17β rises significantly within 24-48 hours
after weaning in sows with a normal return to estrus (Rojanasthien, 1988; Tsuma
et al., 1995). Similarly, concentrations of inhibin in both plasma and follicular fluid
progressively rise during the first two days after weaning (Trout et al., 1992). As
during the follicular phase of the estrous cycle, high circulating concentrations of
estradiol-17β induce estrous behaviour, the preovulatory surge of gonadotropins
and then ovulation. However, a marked variability between sows is observed in
post-weaning follicular development (Foxcroft et al., 1987). It is likely that this is
related to the variation in the weaning-to-estrus interval and/or in the ovulation
rate.
Stimulation of LH secretion at weaning occurs in most sows, even when they were
strongly catabolic during lactation (Zak et al., 1997a; Quesnel et al., 1998a). The
amplitude of the increase is not necessarily related to the degree of inhibition of
LH during lactation (Zak et al., 1997a). The interval between weaning and estrus
was mainly related to mean or episodic secretion of LH during mid-lactation or just
before weaning in several experiments in which primiparous sows belonged to a
single population (Shaw and Foxcroft, 1985; Tokach et al., 1992) and in which LH
secretion during lactation was altered by nutritional treatments (Armstrong et al.,
1986a; Koketsu et al., 1996a; Zak et al., 1997a). This suggests that the degree of
inhibition of LH during lactation influences the resumption of ovarian activity after
weaning. However, several papers also describe a positive relationship between post-
weaning LH and subsequent WEI. For example, Van den Brand et al. (2000a) found
that this relation was linear for sows with a low number of LH pulses (< 8 pulses/12
h) whereas sows with a higher number of LH pulses had the same short WEI. Post-
weaning ovarian activity could also be modulated by the concentrations of
metabolic hormones during lactation (see 15.3.1) per se. Supporting that, alterations
in post-weaning ovulation rate and/or embryo survival were reported regardless of
variations in LH secretion around weaning (feed restriction: Zak et al., 1997a, b;
lysine/protein restriction: Mejia-Guadarrama et al., 2001). Based on the kinetic and
hormonal regulation of follicular growth, it is likely that FSH and LH induce follicle
recruitment immediately after piglet removal. These follicles that ovulate 4 to 7 days
later are healthy follicles measuring 2-3 mm at weaning. It is probable that their
number will influence the ovulation rate at first post-weaning estrus and that their

characteristics (‘quality’) could have consequences on the oocyte development and/or

on the luteinization process of the follicular cells, thus modulating fertilization rate
and embryo survival. In addition, the hormonal background existing after weaning
may influence the process of recruitment and maturation of the preovulatory follicles.
Therefore, both lactational and post-weaning events may act on the reproductive
performance of primiparous and multiparous sows. However, if the lactation period
does not have profound negative effects on LH secretion or follicle development,
no detrimental effects of lactation on post-weaning performance are expected and
effects of post-weaning events will be limited.
15.4 Variation in reproductive performance: extent

and sources of variation
15.4.1 Components of fertility and prolificacy
Fertility and prolificacy of sows can be influenced by many factors, including internal
(e.g. genetic factors, parity, body reserves, milk production) or environmental factors
(e.g. stress, light, ambient temperature, light, housing) as well as management
decisions (e.g. length of lactation, level of feeding). Field data give information
especially on the effects of parity, genotype, litter size, length of lactation and season
on the weaning-to-estrus interval, litter size and farrowing rate or longevity of sows
(e.g. Koketsu et al., 1997a, b; Le Cozler et al., 1997; Lucia et al., 2000). Information
on the influence of internal or environmental factors acting during lactation on
the underlying components of farrowing rate and litter size, that is ovulation rate,
fertilization rate, embryo survival and fetal survival comes from experimental herds.
In the following paragraphs, effects of factors acting either during lactation or after
weaning on the reproductive function will be summarised. However, it should be
noticed that most of field or experimental data concern factors acting during
lactation.
15.4.2 Influence of nutritional factors
15.4.2.1 Influence of nutrient supply
Feed supply during lactation has often been found to affect WEI, and also ovulation
rate and embryo survival, resulting in effects on pregnancy (farrowing) rate and
litter size but the effects can be very variable from study to study (Table 15.3). A
low feeding level during lactation increased WEI in most studies, but significantly
in only 4 out of 8. It significantly decreased ovulation rate in only one study, embryo
survival in three studies and pregnancy rate in two studies. Therefore, effects of low
feeding levels on WEI are more consistent than their effects on ovulation rate, embryo
survival and pregnancy rate. Even in modern crossbred primiparous sows (studies
394 Weaning the pig

in Table 15.3 from 1997 onwards) very different effects can be found: no effects
(Quesnel and Prunier, 1998); effects on WEI only (Zak et al., 1998); effects on
ovulation rate and embryo survival (Zak et al., 1997a), or effects on ovulation rate
only (Van den Brand et al., 2000a). It is not easy to verify the causes of this variability.
Table 15.3. Influence of feed supply during lactation or after weaning on liveweight
at weaning (LW, kg), subsequent weaning-to-estrus interval (WEI, days), ovulation rate,
embryo survival at day 25 to 35 of pregnancy (ES) or litter size (LS) in brackets and,
pregnancy rate (PR) or farrowing rate (FR) in brackets.
Feed sup.(%)a LW at weaning WEI Ovulation rate ESb (LS) PR (FR)
High Low High Low High Low High Low High Low High Low Sourcec
During lactation
85 40 135 108 7.6 19.9* 14.4 13.5 (9.7) (9.7) (79) (89) (1)
85 45 ~200 ~180 4.3 5.8* 18.1 18.6 83 68† 90 69* (2)
80 40 ~177 ~164 6.0 8.9* 17.6 17.7 83 72* 89 77† (3)
80 45 199 176 5.9 7.5 16.2 16.7 85 64* 82 62* (4)d
80 45d 179 162 3.7 5.6 19.9 15.4* 88 87 100 100 (5)
45 d 172 5.1 15.4* 64* 100 (5)
90 60 210 194 5.7 5.9 19.2 20.7 - - - - (6)
85 50 163 137 4.2 6.3* 14.4 15.6 83 72 100 100 (7)
79 67 152 145 5.1 5.7 18.1 16.2† 68 68 - - (8)
After weaning
- - 9.1 8.2 15.2 14.8 - - - (9)
285 115 122 121 13.4 14.1 14.6 13.2* (10.0) (9.5) (76) (92) (1)
245 155 199 199 6.0 5.9 16.6 16.2 78 85 87 82 (4)d
a For effects of feed supply during lactation, animals were restricted after lactation. For effects
of feed supply after lactation, animals were full fed during lactation. Feed supply (%) is the
estimated ratio between metabolic energy intake and requirements for maintenance in
weaned sows and for maintenance + milk production in lactating sows (see Prunier and
Quesnel, 2000).
b (1) King and Williams, 1984 (2) Kirkwood et al., 1987 (3) Kirkwood et al., 1990 (4) Baidoo
et al., 1992 (5) Zak et al., 1997a (6) Quesnel and Prunier, 1998 (7) Zak et al., 1998 (8) Van
den Brand et al., 2000a (9) Den Hartog and van der Steen, 1981.
c Percentage of viable embryos to number of corpora lutea.
d Low feed intake (5% of ME requirements) was imposed during the first three weeks of
lactation (first line of data) or last (4th) week of lactation (second line of data).
* P < 0.05, † P < 0.05.

It is dependent on the reproductive performance of the control group (which is

quite different from experiment to experiment), and may be related to factors such
as body condition at farrowing, litter size, litter gain, lactation length, degree of
feed restriction, weight loss during lactation etc. It seems reasonable to suggest that
a more severe energy deficit during lactation will have larger effects on WEI, ovulation
rate and embryo survival. Data from King and Dunkin (1986a) corroborate this
relationship between the degree of feed restriction and the effect on WEI. They
compared 6 levels of feed consumption during lactation of first-litter sows, and
observed that the proportion of sows exhibiting estrus within 8 days of weaning
was 83% at the highest feeding level and decreased linearly with daily feed intake
to only 8%. Contrarily, they did not find any influence of the feed intake on
ovulation rate. This may be due to the fact that the WEI was relatively long in all
their experimental groups. Data from Table 15.3 show that the decrease in the
ovulation rate in restricted sows was significant or close to significance only when
weaning-to-estrus interval was short (Zak et al., 1997a; Van den Brand et al., 2000a).
Therefore, factors imposed during lactation have decreasing effects on the post-
weaning ovulation rate when the WEI increases. Such a conclusion can not be drawn
regarding the effects of feed restriction on embryo survival and pregnancy rate.
The effects of lactational feed intake on ovulation rate seem to be associated with
altered follicular development at the time of weaning, which itself may depend
on the hormonal background at that time (see 15.3.2). Data obtained in gilts by
Soede et al. (2000) corroborate this hypothesis. These authors found that a feed
restriction of 60% of ad libitum feed intake during the last week of progesterone
dominance (Regumate®) resulted in fewer large follicles at the last day of treatment
(follicles larger than 4.5 mm/ovary: 4.2 vs. 9.5) and in lower subsequent ovulation
rate (14.8 vs. 17.2) without any influence on the interval between Regumate®
cessation and ovulation. Almeida et al. (2000) restricted feed intake during the
second week of the luteal phase and did not find effects on ovulation rate, but found
significant effects on progesterone rise during early pregnancy and subsequent
embryo survival rate (68% vs 83%). Similarly, the hormonal background existing
during lactation may influence quality of the oocytes and hence the subsequent
embryo survival and pregnancy rate.
Analyses of farm data have shown that the feed intake pattern during lactation is
another important factor influencing subsequent reproductive processes. Farm data
on feed intake patterns were analyzed by Koketsu et al. (1996b, c) who distinguished
6 feed intake patterns: Rapid (rapid increase in feed intake after farrowing, 23%
of lactating sows); Major (major drop in feed intake during lactation, 33% of sows);
Minor (minor drop, 28% of sows); LLL (low feed intake throughout lactation, 1%
of sows); LHH (low feed intake during the first week then increasing for the
remainder of lactation, (1% of sows); and Gradual (gradual increase in feed intake
throughout lactation, 15% of sows). Analyses of subsequent reproductive
396 Weaning the pig

performance revealed that sows showing either a rapid or gradual increase in feed
intake with no drop (or either a minor drop in feed intake) during the course of
lactation had the lowest weaning-to-conception interval and had a lower risk to
be culled due to anestrus. In sows that show a marked drop in feed intake at any
time during lactation, reproductive output was decreased. The authors concluded
that both the average daily feed intake and the feed intake pattern influenced
reproductive performance.
Experimental data also show that restricted feeding during different parts of lactation
differentially affect reproductive performance. In first-litter sows, Koketsu et al.
(1996a) restricted energy intake during the whole lactation or during either the
first, second or third week of lactation (diets were adjusted to ensure that energy
intake was restricted by 60%, but lysine intake was not restricted). The rather severe
restriction of energy intake during the second, third or whole lactation significantly
increased WEI (from on average 9 days to 18 to 23 days), whereas restriction in
the first week of lactation resulted in an intermediate WEI of on average 14 days.
No other parameters for reproductive performance were assessed. Zak et al.
(1997a) also varied the timing of feed restriction in primiparous sows weaned at
4 weeks of lactation. Sows were fed to appetite (= “control” group) or were submitted
to feed restriction (about 50% of ad libitum intake) either between parturition and
day 21 (= group “refed”) or between day 22 and day 28 (group “restricted”). In
this experiment, “refed” sows showed a significant increase in WEI (from 3.7 to
5.6 days) and a decrease in ovulation rate (from 19.9 to 15.4) but embryo survival
was not affected (from 88 to 86), whereas “restricted” sows showed an increase in
WEI (to 5.1 days), and decreases in ovulation rate (to 15.4) and embryo survival
(to 64 %). In a second experiment using a similar protocol, Zak et al. (1997b)
compared the ability of the oocytes of the 15 largest follicles to mature in vitro as
well as the ability of the follicles > 3 mm to support oocyte nuclear maturation.
Sows in the “restricted” group had fewer oocytes to mature in the Metaphase II
stage of meiosis than “refed” sows. Further, control oocytes matured less well in
the follicular fluid obtained from the ovarian follicles of the “restricted” sows than
of the “refed” sows. However, data showing that the ability of the ovocytes to mature
in vitro is closely linked to their ability to mature in vivo are still missing.
Data concerning the effects of feed supply after weaning on the subsequent
reproductive performance are scarce. The only significant effect observed was a lower
ovulation rate in restricted sows in one study (Table 15.3). This effect may be related
to an influence of the hormonal background existing after weaning on the
recruitment process (see 15.3.2). Indeed, ovulation rate can be increased by insulin
treatment after weaning which reduces the rate of atresia of selected follicles (for
review: Cox, 1997).

15.4.2.2 Influence of the composition of the diet
Proteins
Protein demand during lactation is high because of the protein demand for milk
production. The first limiting essential amino acid in most diets is lysine, and daily
lysine intake is therefore often taken as a primary determinant of lactation
performance. Low protein intake during lactation results in mobilization of
significant amounts of maternal body protein and in decreased milk production
(Jones and Stahly, 1999b). Numerous experiments have shown that a low protein
intake during first lactation (but with high energy intake) increases the subsequent
WEI (20 vs. 11 days in King and Williams, 1984; 13.9 vs. 8.4 in Jones and Stahly,
1999a) and decreases the percentage of sows expressing estrus within 8 days from
weaning (41 vs. 59% in King and Dunkin, 1986b; 33 vs. 83 % in King and Martin,
1989) or within 7 days from weaning (60 vs. 88 % in Brendemuhl et al., 1987)
without clear effect on ovulation rate or litter size. In contrast, in two more recent
experiments, protein/lysine restriction had no clear influence on the interval between
weaning and prestrus (Yang et al., 2000b) or estrus (Mejia-Guadarrama et al., 2001),
but affected follicular development and/or ovulation rate. Indeed, ovulation rate
was lower at the postweaning estrus in restricted compared to control sows (20.0
vs. 23.4, Mejia-Guadarrama et al., 2001). Moreover, protein/lysine restriction during
lactation retarded growth of preovulatory follicles collected at the postweaning
prestrus and reduced their ability to support oocyte maturation (Yang et al., 2000c).
Long term effects of protein/lysine deficiency during lactation have been tested by
Yang et al. (2000b). They compared five levels of lysine (0.60, 0.85, 1.10, 1.35 and
1.60%) over three successive parities. Increasing dietary lysine/protein linearly
decreased voluntary feed intake; e.g. in the first-litter sows from 5.4 to 4.6 kg. In
their study, dietary lysine did not affect WEI (which was on average 5.8, 4.7 and
4.1 days for parity 1, 2 and 3, respectively) or farrowing rate (75.2%, 74.8% and
84.4% for parity 1, 2 and 3, respectively). However, lysine levels during lactation
affected subsequent litter size, the effect depending on parity: second litter size
decreased linearly with the increase in dietary lysine during first lactation whereas,
third and fourth litter sizes were lowest in sows receiving 0.85 g of lysine/day.
Numerous authors have used two-factorial designs in order to test whether the effects
of protein and energy intakes during lactation on reproductive performance may
interact (King and Williams, 1984, King and Dunkin, 1986b; Brendemuhl et al.,
1987). Results show that the effects of protein intake on reproduction were rather
similar at the high and low level of energy intake suggesting that there was no
interaction between energy and proteins.
It has been suggested that increasing lysine/protein intake in lactating sows above
the nutritional requirements could improve the reproductive performance after
398 Weaning the pig

weaning. Some experiments support this hypothesis (reduced WEI: Wilson et al.,
1996; increased litter size: Tritton et al., 1996) but not others (littersize: Touchette
et al., 1998; Yang et al., 2000b; hormone profiles during lactation: Yang et al., 2000a;
follicular maturation at proestrus: Yang et al. 2000c; WEI: Yang et al., 2000b).
Therefore, no or only little improvement can be expected from high protein/lysine
regimen during lactation.
Starch/Fat
Increasing the energy content of sow lactational diets may reduce mobilization of
body stores during lactation even though a decrease in feed intake is often observed.
Indeed, high fat diets allowed total ME intake to increase by 3 to 32% (12% as a
mean) in high-parity sows (Drochner, 1989) and by on average 4.4 MJ (less than
10% fat added) to 6.5 MJ (more than 10% added fat) (Pettigrew and Moser, 1991).
Van den Brand et al. (2000c) measured energy and protein balances in primiparous,
isocalorically fed sows with diets containing 13.5% fat as compared to diets with
3.4% fat at two different feeding levels. At high feeding levels, the fat-rich diet resulted
in higher body fat loss without any clear effect on reproductive performance (Table
15.4). Therefore, fat-rich diets do not reduce mobilization of body stores, but in
fact increase the mobilization of body stores and thus are not expected to improve
reproductive performance in practice. However, it is conceivable that in circumstances
where the voluntary feed intake is very low (e.g. high ambient temperatures), the
extra uptake of energy when using fat-rich diets will be beneficial for the sows.
Table 15.4. Effect of feeding level and fat level of the diet on partitioning of energy
in first-litter sows during a 21 day lactation period (based on Van den Brand et al.,
2000a, b, c).
Energy intake/day 62.8 MJ ME 47.1 MJ ME
Diet Fat Starch Fat Starch
Sow losses during lactation

Protein (g/d) 50 31 69 75
Fat (g/d) 584a 401b 511a 521a
WEI (h) 123 122 152 130
Ovulation rate 17.9u 18.2u 15.5v 16.9v
Embryo survival (%) 75 66 65 70
ab P < 0.05
uv P < 0.10

In the experiment of Van den Brand et al. (2000c), a starch-rich diet was expected
to be beneficial for reproductive performance since one of the important mediators
between nutrition and reproduction could be insulin (see 15.3.1.3.). The starch-
rich diet was found to result in a higher and more prolonged insulin release (Van
den Brand et al., 1998). However, neither weaning-to-estrus interval, nor ovulation
rate, nor peri-estrus hormone profiles, nor embryo survival during subsequent
pregnancy were influenced by the diet (Table 15.4).
15.4.2.3 Influence of body stores
As has been discussed in 15.4.2.1., the level of feed intake during lactation has
important consequences for subsequent reproductive performance. An important
question is whether these effects are influenced by the levels of body stores, either
at the onset of lactation or at the end of lactation. Several studies have been
performed trying to reveal the relative importance of factors such as body stores
of protein and/or fat at farrowing, body stores of protein and/or fat at weaning,
protein losses during lactation and fat losses during lactation for post-weaning
Effects of body condition at farrowing have mostly been studied in relation to

weaning-to-estrus interval and in first-litter sows. Results are ambiguous: Mullan
and Williams (1989), Weldon et al. (1994), Le Cozler et al. (1998 and 1999) found
no effect of body condition on WEI; Prunier et al. (2001) did not observe
alteration in gonadotropin release and ovarian development at the end of lactation;
Yang et al. (1989) and Dourmad (1991) found a longer WEI in thin sows, whereas
Xue et al. (1997) found a longer WEI in fat sows. In fact, there is a negative
relationship between fatness at farrowing and appetite during lactation. Therefore,
it is likely that the influence of body stores at farrowing on the post-weaning
performance depends on their negative impact during lactation, being inhibitory
only when this effect is very marked as illustrated by the following experiments.
Firstly, Xue et al. (1997) compared two levels of feeding during gestation (46 vs.
27.2 MJ ME/day) which produced backfat depth at farrowing of 30.5 and 25.5 mm
in average. During lactation, spontaneous feed intake was highly reduced in fatter
sows (-29 %) and resulted in a similar body weight at weaning at day 21
(approximately 163 kg), but backfat was still higher in sows which were fatter at
farrowing (23 vs. 17.5 mm). At day 15 of lactation, basal and peak levels of insulin
after glucose infusion were lower in fatter sows. At days 7 and 14 of lactation, LH
release was impaired in the fatter sows and the WEI tended to be longer (8.0 vs.
6.4 days). The authors suggest that the increase in WEI in the sows with high
gestational energy intake was a result of the low feed intake during lactation through
an interaction of insulin with LH-secretion. Secondly, Le Cozler et al. (1998, 1999)
compared two levels of feeding during rearing which resulted in two levels of backfat
at farrowing (23.7 vs. 17.4 mm in 1998; 22.4 vs. 20.7 mm in 1999). They observed
400 Weaning the pig

that feed intake was only slightly reduced during lactation (- 8% in Le Cozler et
al., 1998; -3 % in Le Cozler et al., 1999) in fatter sows and did not show any influence
of fatness on the WEI and subsequent litter size.
Yang et al. (1989) tried to determine the respective effects of body stores at parturition
and at weaning on reproductive performance in sows over four parities. To
achieve this, two levels of feeding were used during gestation in order to reach 12
or 20 mm of backfat (P2) at farrowing. These levels were combined with two levels
of feeding (ad libitum or restricted at 3 kg/day) during lactation and two sizes of
sucking litters (6 vs. 10 piglets). All three factors significantly influenced backfat
at subsequent weaning, changes in backfat during lactation, sow live weight at
weaning and changes in sow live weight during lactation. Sows which were fatter
at farrowing had a lower ad libitum feed intake during lactation over the 4 parities
(-23%) but this difference was much lower in first-litter sows (-7%). In these latter
sows, WEI was influenced by fatness at parturition and by feed intake during lactation
but not by litter size. A significant relationship was also found between fatness at
weaning (P2 in mm) and WEI (WEI = 26.6 (s.e. 4.7) - 1.28 (s.e. 0.39) x P2 (r.s.d.
3.5)). No other relationships of body stores with WEI were presented. When looking
at the percentage of primiparous sows in estrus within 8 days after weaning, there
was a strong interaction between fatness at farrowing and feed intake during
lactation: this percentage was highly reduced only in sows which were thin at
farrowing and were restricted during lactation (30 vs. 83% in average for the three
other groups). In later parities, only litter size during lactation influenced WEI (6.0
vs. 8.0 days for 6 vs. 10 piglets).
In summary, reproductive performance of sows after weaning may be influenced

by fatness at farrowing in interaction with feed intake during lactation. Extremely
fat and extremely thin primiparous sows should both be avoided.
15.4.2.4 Conclusion
In most studies, return-to-estrus after weaning is delayed by low feed intake and
by low energy or protein intakes. For ovulation rate, the effects are less clear: in
older studies, no effects on ovulation rate were found and in recent studies, ovulation
rate was frequently decreased by both feed and protein restriction. For oocyte
maturation and embryonic survival, data are scarce and comes only from studies
published in the last five years. Both feed and protein deficiency during lactation
can have negative effects on these parameters.

15.4.3 Influence of lactational characteristics
15.4.3.1 Litter size
Reducing litter size decreases the suckling intensity and lowers the risk of
nutritional deficit and hence may improve the reproductive performance of sows
after weaning. Indeed, in their experimental farm, Vesseur et al. (1994b) observed
that sows with a larger litter size at weaning had a longer WEI (8.3 days vs. 7.5
days for sows weaning 11-12 vs. 7-8 pigs respectively). However, the percentage of
anestrous sows which were treated with gonadotropins to induce heat was not
influenced by the litter size at weaning. Similarly, in a retrospective study based
on farm data, Koketsu et al. (1997a) observed that neither the percentage of anestrous
sows nor the percentage of sows with return to heat after service were influenced
by litter size at weaning. On the overall, the effect of litter size during lactation on
reproductive performance after weaning seems to be weak. However, it should be
noted that sows with larger litter size at weaning have probably larger litter size at
farrowing and hence higher breeding values and a better potential for reproduction.
Suckling intensity during lactation can be manipulated by removal of the heaviest

piglets a few days before full weaning (= split-weaning) or by separating the whole
litter from the sow during a part of each day for the last days of lactation (=
interrupted suckling). It generally results in a shorter weaning-to-estrus interval
(review: Matte et al., 1992). The reduction is more marked with the interrupted
suckling but this latter method is more laborious and time-consuming. Moreover,
estrus may occur during lactation that will complicate management of the sows.
Therefore, in recent years, only the effect of split-weaning on reproductive
performance has been evaluated. Data from Vesseur et al. (1997) did not show any
clear effect of split-weaning (4-5 piglets out of 10-12 during the 4th week p.p.) on
the WEI, nor on the farrowing rate and subsequent litter size in parity-1 sows.
However, they observed a shorter WEI (4.6 vs. 5.4 days for sows returning to estrus
within 15 days) and a higher farrowing rate (97.2 vs. 86.3%) in parity-2 sows
submitted to split-weaning compared to control sows.
15.4.3.2 Length of lactation
Increasing the length of lactation from about 10 to 30 days results in a decrease

in the weaning-to-estrus interval and a raise in subsequent litter size and farrowing
rate in both primiparous and multiparous sows. The effect on litter size is more
marked in multiparous sows (Figures 15.2A and 2B). As a consequence, the weaning-
to-conception interval is reduced but this reduction is not sufficient to compensate
for the increase in the lactation length and the farrowing-to-conception interval
increases (Figure 15.3). The positive effect of the duration of lactation on fecundity
and prolificacy can be explained by several phenomena. Firstly, it may be assumed
402 Weaning the pig

Weaning-to-estrus interval (days)

Primiparous Primiparous
A
12 Multiparous Multiparous
10
4
10 15 20 25 30
13 B
Litter size (total born)
12
11
10
10 15 20 25 30
Duration of lactation (days)
Figure 15.2. Influence of the length of lactation on the weaning-to-estrus interval (A)
and on the farrowing-to-conception interval (B) in primiparous and in multiparous
sows (redrawn from Le Cozler et al., 1997: ; Koketsu and Dial, 1998: ).
45 Primiparous Multiparous
Farrowing-to-conception
40
interval (days)
35
30
25
10 15 20 25 30
Duration of lactation (days)
Figure 15.3. Influence of the length of lactation on the subsequent farrowing-to-

conception interval after weaning (adapted from Le Cozler et al., 1997).

that the recovery of the uterus from the previous gestation is more advanced at
the new conception which will allow a better fertilization rate and embryo
survival (see 15.3.1.1). Secondly, it seems that the percentage of sows that does
not ovulate at first estrus is abnormally high in case of short lactations (Table 15.5).
Thirdly, the reduction in the WEI associated with the increase in the length of
lactation itself has positive effects on litter size (see 15.4.5). Surprisingly, in sows
with very short lactation (7 to 10 days), litter size is higher than in sows with short
lactation (11 to 16 days) as shown by Marois et al. (2000). This can be explained
by a longer farrowing-to-conception interval and hence a better uterine recovery
at mating.
Table 15.5. Effect of the length of lactation on the percentage of sows ovulating within
8 days after weaning and on the percentage of these sows that ovulate (based on Knox
et al., 2001).
Length of lactation (days)
< 17 17-24 25-31 > 31
Sows in estrus (%) 35a 94b 98b 96b

Sows ovulating (%) 78a 92b 98b 96b
ab P < 0.05
15.4.4 Influence of the physical and social environment
15.4.4.1 Climatic environment
Even though the domestic pig is not a true seasonal breeder, it manifests variations
in reproductive performance throughout the year. Prolonged intervals between
weaning and subsequent estrus, ovulation and fertilization have been reported
during summer and early fall, the influence of season being more pronounced in
primiparous compared to multiparous sows (review: Prunier et al., 1996). The
highest remating rate and lowest farrowing rate are also observed for sows served
in summer whereas season has no clear effect on litter size (Koketsu et al., 1997a,
b; Hughes, 1998; Tummaruk et al., 2000). Lower feed intake during lactation in
summer is not sufficient to explain the delayed return to estrus after weaning: in
their retrospective analysis of farm data, Koketsu et al. (1997b) observed that the
weaning-to-mating interval was still prolonged during summer after adjusting data
for feed intake.
404 Weaning the pig

Long photoperiod and high ambient temperatures are the main environmental cues,
which may influence the reproductive activity. Results concerning the influence of
photoperiod variation using abrupt variations of light duration around farrowing
or weaning are controversial. In contrast, when progressive patterns of variation
are applied during gestation and lactation, it is clear that increasing light duration
has a detrimental influence on the return to estrus after weaning compared to
decreasing light duration (review: Prunier et al., 1996). Numerous experiments have
shown that high ambient temperatures increase the WEI and its variability
especially in first-parity sows (review: Prunier et al., 1996). Reduction in appetite
and subsequent increase in the nutritional deficit during lactation explains only
partly this negative effect of high ambient temperatures on the reproductive function
(Prunier et al., 1997; Messias de Bragança et al., 1998). Nutritionally-independent
variations in the secretion of hormones implied in the control of thermoregulation
(for example thyroid hormones and cortisol) and able to act on the hypothalamo-
pituitary-ovarian axis are probably involved.
15.4.4.2 Housing environment
Data related to the influence of the housing system during lactation or around
weaning on the subsequent reproductive performance of sows are scarce and
relatively old. Grouping sows during lactation induces fertile estrus during lactation
which is not desirable (Bryant et al., 1983). Penning sows in groups at weaning
has no or a positive effect on the weaning-to-estrus interval and on litter size
(Hemsworth et al., 1982; Lynch et al., 1984; Schmidt et al., 1985). It has no effect
(Hemsworth et al., 1982; Schmidt et al., 1985) or a negative effect (Lynch et al.,
1984) on the farrowing rate. However, more data are necessary to conclude
definitively whether grouping sows at weaning will improve or deteriorate
15.4.4.3 Boar effect
The boar is well known to have stimulatory effects on the reproductive function
of female pigs. Indeed, boar exposure of sows daily during the last 7/8 days of
lactation reduces the weaning-to-estrus interval (Walton, 1986; Newton et al., 1987),
but the effect seems to be more marked in multiparous than in primiparous sows
(Walton, 1986). Similarly it has been observed that in sows with daily boar contact
after weaning, estrus and ovulation occur earlier (Hemsworth et al., 1982; Walton,
1986; Pearce and Pearce, 1992) and in a higher proportion of sows (Langendijk
et al., 2000). However, some discrepancy exists. Hughes (1998), for example, did
not observe any effect of boar contact(s) but in his study the return to estrus after
weaning occurred very early even in sows without any boar contact (5.5 days). When
farrowing rate and litter size were measured, these parameters were not influenced
by boar exposure (Hemsworth et al., 1982; Hughes, 1998).

15.4.5 Relationships between WEI, litter size and farrowing rate
Several analyses of field data have related the WEI to subsequent litter size and
farrowing rate (Leman, 1990; Vesseur et al., 1994a; Le Cozler et al., 1997; Steverink
et al., 1999; Tummaruk et al., 2000; Figure 15.4). The analyses show that an increase
in WEI from 3 to about 8 days is associated with a decline in subsequent litter size
and farrowing rate. From about day 10 onwards, an increase in WEI is associated
with an increase in these reproductive parameters. This observation agrees well with
data from Clowes et al. (1994) and Vesseur (1997) who found that insemination
of sows during the second estrus after weaning compared to the first one resulted
in an increased pregnancy rate (+ 15 %) and subsequent litter size (+ 1.3 to 2.5
piglets). Therefore, it seems that some sows have a high genetic potential for
reproduction which includes rapid return-to-estrus after weaning, fertility and
prolificacy, whereas some other sows with delayed return-to-estrus after weaning
take advantage of this delay to recover from the negative effects of factors acting
during lactation, especially the nutritional deficit. An important question is to
determine whether the WEI related variations in fertility and prolificacy are due
to effects on ovulation rate, fertilization rate and/or embryo survival rate?
Ovulation rate Little is known about variation in ovulation rate in association with
variation in WEI. Data from three experiments with more than 350 multiparous
sows (Soede et al., 1995a, b; Steverink et al., 1997) show an average ovulation rate
of 21.6, 21.4, 20.5 and 19.5 at days 3 to 6 after weaning, respectively (significant
linear decrease). Recently, Patterson et al. (2001) also found a negative correlation
between WEI (varying between 3.0 and 5.3 days) and ovulation rate (varying between
13 and 31) in multiparous sows (r = -0.54). In contrast, in primiparous sows, Van
den Brand and Langendijk (unpublished results) did not find a relation between
Farrowing rate Total born
100 13
90 12,5
12
Farrowing rate
80
Total born
11,5
70
11
60
10,5
50 10
40 9,5
30 9
0 5 10 15 20 25
Weanin g to service interval in days (1-30)
Figure 15.4. Association of Weaning-to-estrus interval (WEI) with subsequent farrowing

rate and litter size (based on Leman, 1990).
406 Weaning the pig

the weaning-to-ovulation interval (varying between 4.6 and 8.9 days) and ovulation
rate (varying between 12 and 30), but they did find a relation with embryo survival
(Table 15.6). Although ovulation rate is normally quite high and not the first limiting
factor for litter size and farrowing rate, a role of the decrease in ovulation rate can
not be ruled out, especially if the decline in number of ovulations is associated
with a reduced quality of the corpora lutea, as has been suggested (Zak et al., 1997b;
Almeida et al., 2000). In these sows with a short WEI, ovulation rate is probably
closely related to the number of selectable follicles present at weaning.
Table 15.6. Reproductive characteristics of primiparous sows with variable weaning-

to-ovulation intervals (ovulation was assessed at 8-hour intervals) (Van den Brand and
Langendijk, unpublished results).
Weaning-to-ovulation interval (hours)
110 - 145 150 - 158 166 - 214
Pregnancy rate at day 35 (%) 91 96 86

Ovulation rate 19.7 ± 4.0 19.0 ± 4.5 19.9 ± 3.5
Normal of embryos at day 35 13.1 ± 3.1 11.7 ± 3.7 11.4 ± 3.2
Embryo survival at day 35 (%) 1 67 ± 12 62 ± 18 57 ± 14
Luteal weight (g) 7.0 ± 1.2 6.1 ± 1.1 6.5 ± 1.1
Number of sows 23 26 29
1 Correlation between weaning-to-ovulation interval and embryo survival rate: r = -0.26,

P < 0.05
For sows with a WEI of more than 10 days, it is not clear if the increase in
reproductive performance is associated with an increased ovulation rate. However,
an extended WEI which resulted from a three day treatment with altrenogest from
weaning onwards, also resulted in an increase in ovulation rate (Koutsotheodoros
et al., 1998).
Fertilization rate In sows, fertilization results are very much dependent on the interval
between insemination and ovulation (Waberski et al., 1994; Soede et al., 1995a),
subsequently affecting litter size and farrowing rate (Nissen et al., 1997; Terqui et
al., 2000). Kemp and Soede (1996) showed that, if sows with a WEI varying between
3 and 7 days were inseminated at an optimal time relative to ovulation (in the
period of 24 hours before ovulation), fertilization results were not affected by WEI.
In many experimental data, an increase in WEI (between 3 and 6 days) has found
to be associated with a decrease in the duration of estrus and, consequently, a shorter

interval between onset of estrus and ovulation (review: Soede and Kemp, 1997).
A similar relation between WEI and estrus duration was found on farms (Steverink
et al., 1999). If the insemination strategy on farms is not adjusted to WEI, the number
of sows in which the first insemination takes place after ovulation will be
increased in sows with a longer WEI and hence the risk of a low fertilization rate
(review: Kemp and Soede, 1997). It is not clear to what extent these phenomena
are responsible for the reduction in farrowing rate and litter size as found for sows
with a WEI from 3 up to 8-10 days.
For sows with a WEI of more than 10 days, the duration of estrus remains as short
as found for sows with a WEI of 6 days and beyond (Steverink et al., 1999). It
therefore does not seem likely that the increase in reproductive performance found
for these sows is associated with a better timing of insemination and therefore with
higher fertilization rates.
Embryonic mortality No clear information is available for the relationship between

the weaning-to-estrus interval and the subsequent embryo survival. However, Van
den Brand and Langendijk (unpublished results) found that, in primiparous sows,
an increase in the weaning-to-ovulation interval was indeed associated with a
decrease in subsequent embryo survival (Table 15.6). In these sows, ovulation rate
was not associated with the weaning-to-ovulation interval. There is some
circumstantial evidence suggesting that WEI is associated with subsequent embryo
survival, based on experiments in which feed restriction during lactation results
not only in an increase in WEI, but also in a decrease in embryo survival (Table
15.3). However, as discussed earlier (see 15.4.2.1.), this association does not seem
to be very strong and it is not clear which factors are of influence.
In summary, associations between WEI and subsequent reproductive performance

(both farrowing rate and litter size) seem to be a combined result of effects on
ovulation rate, fertilization rate and embryo survival. The relative importance of
these effects is not known.
15.5 Conclusion
During lactation, suckling-neuroendocrine reflexes are the main factors inhibiting
LH secretion and ovarian activity. Negative metabolic state due to high milk
production creates a hormonal milieu, which may have additional inhibitory effects.
In commercial farms, the timing of weaning is the decision of the producer. It
generally occurs when milk production is still very high and is not progressive as
in “natural” conditions. As a consequence, weaned sows are submitted to rapid
changes in the nutritional balance and the hormonal secretions that generally induce
estrus behavior and ovulation some days later. Internal (i.e. genetic factors, parity,
body reserves) and environmental factors (i.e. light, ambient temperature, housing)
408 Weaning the pig

may influence the nature and the amplitude of these changes as well as the ability
of the ovaries to respond to these changes. Therefore, both factors acting during
lactation and after weaning may influence reproductive performance of weaned
sows. Evidence from this review suggest that reproductive problems of sows,
especially primiparous sows, are related for a large part to lactational events and
less to post-weaning events. In order to improve reproductive performance and
longevity, lactational sources of inhibition should be decreased, especially in first
and-second litter sows. This can be done by reducing suckling stimulation and/or
nutritional deficit (e.g. split-weaning, interruped suckling). Moreover, short
lactations (< 21 days) should be avoided in order to allow the gonadotropic axis
and the uterus to recover from the previous gestation and farrowing.
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metabolites, hormones, and reproductive performance in primiparous sows. Journal of
Yang, H., J.E. Pettigrew, L.J. Johnston, , G.C. Shurson and R.D. Walker, 2000b. Lactational and
subsequent reproductive responses of lactating sows to dietary lysine (protein) concentration.
Yang, H., G.R. Foxcroft, J.E. Pettigrew, L.J. Johnston, G.C. Shurson, A.N. Costa and L.J. Zak, 2000c.
Impact of dietary lysine intake during lactation on follicular development and oocyte
maturation after weaning in primiparous sows. Journal of Animal Science 78, 993-1000.
Zak, L.J., J.R. Cosgrove, F.X. Aherne, G.R. Foxcroft, 1997a. Pattern of feed intake and associated
metabolic and endocrine changes differentially affect postweaning fertility in primiparous
lactating sows. Journal of Animal Science 75, 208-216.
418 Weaning the pig

Zak, L.J., X. Xu,. R.T. Hardinand and G.R. Foxcroft, 1997b. Impact of different patterns of feed
intake during lactation in the primiparous sow on follicular development and oocyte
maturation. Journal of Reproduction and Fertility 110, 99-106.
Zak, L.J., I.H. Williams, G.R. Foxcroft, J.R. Pluske, A.C. Cegielski, E.J. Clowes and F.X. Aherne, 1998.
Feeding lactating primiparous sows to establish three divergent metabolic states: I. Associated
endocrine changes and postweaning reproductive performance. Journal of Animal Science 76,
1145-1153.
Zivkovic, M., M. Teodorovic and S. Kovcin, 1986. Longevity of sows according to the management
in large units. World Review of Animal Production 22, 11-15.

Conclusions
The chapters in this book have presented the most up-to-date information, data
and background philosophy related to the various events associated with ‘weaning’.
Weaning is a stressful period for both the young pig and the sow, and the act of
‘weaning’ is an unusual event in the pig production cycle because of the many
changes that are simultaneously imposed on the system, eg, change of nutrition,
change of environment, change of social structure, and so on. Consequently, the
risks to the producer of decreased production, increased mortality and morbidity,
and deteriorated health status are high at weaning, and careful management is
required to ameliorate the weaning process so that any losses associated with
weaning are minimized. The large array of influences can cause enormous
variation in the response of piglets to the transition from the sow to the next phase.
This can cause big differences in development between animals, both within and
between litters. The chapters give insight how this occurs, and offer ways to avoid
the negative effects of weaning
A recent comment in the magazine ‘Pig International’ stated that pork remains the
most consumed meat in Europe, with an average of 43.7 kg per head eaten in 2002.
This compares to 23 kg for poultry and 19.4 kg for beef/veal. To maintain, and
increase, this level of consumption requires due diligence to all aspects of the pig
production and the supply chain, as well as improving practices and adopting new
technologies to achieve higher levels of production and consumption. Weaning is
an integral component of the overall pig production cycle, predominately because
of the impact weaning weight and post-weaning performance can have on finisher
pig performance and profitability. Fertility of the weaned sow is also an important
determinant of profitability in the system. However, new challenges are continually
being faced by the pig Industry, such as the increasing awareness of society with
respect to animal welfare, food safety, the environment, and the ‘quality’ of
production, especially with respect to antibiotics and some minerals as growth
promoters. Many of these challenges concern weaning and, on balance, the process
of ‘weaning’ and its effects has never been considered more important.
To this end, we believe that the material contained within “Weaning the Pig:
Concepts and Consequences”, is both timely and pertinent to many of the issues
being faced around the world today regarding weaning. We trust that you have
enjoyed the chapters in this book and believe that the diversity of topics covered,
including the fate of the weaned sow, will assist with your business or line of expertise
in the pig Industry.
John Pluske
Jean Le Dividich
Martin Verstegen

List of authors
A.C. Beynen, Department of Nutrition, Faculty of Veterinary Medicine, Utrecht

University, P.O. Box 80152, 3508 TD Utrecht, The Netherlands
P.H. Brooks, University of Plymouth, Faculty of Land, Food and Leisure, Seale-Hayne
Campus, Newton Abbot, Devon, TQ12 6NQ, United Kingdom
D. Burrin, USDA/ARS Children’s Nutrition Research Center, Department of

Pediatrics, Baylor College of Medicine, 1100 Bates Street, Houston, Texas 77030, USA
S.S. Dritz, Department of Animal Sciences and Industry, Kansas State University,
Manhattan KS 66506-0201, USA
F.R. Dunshea, Natural Resources and Environment, Sneydes Road, Werribee

Victoria 3030, Australia
R.D. Goodband, Department of Animal Sciences and Industry, Kansas State

University, Manhattan KS 66506-0201, USA
D.J. Hampson, School of Veterinary and Biomedical Sciences, Murdoch University,

Murdoch, Western Australia 6150, Australia.
M. Hay, Ecole Nationale Vétérinaire de Toulouse, 23 Chemin des Capelles, 31076

Toulouse, France
D.E. Hopwood, Animal Resources Centre, Murdoch Drive, Murdoch, WA 6150,

Australia
D. Kelly, Rowett Research Institute, Greenburn Road, Bucksburn, Aberdeen,

AB2 9SB, Scotland
B. Kemp, Animal Husbandry Group, Wageningen University, P.O. Box 338, 6700
AH Wageningen, The Netherlands
M.R. King, Institute of Food, Nutrition and Human Health, Massey University,
Private Bag 11-222, Palmerston North, New Zealand
R.H. King, Agriculture Victoria, Sneydes Road, Werribee Victoria 3030, Australia
J. Le Dividich, INRA-UMRVP, 35590 St-Gilles, France
F. Madec, Agence Française de Sécurité Sanitaire des Aliments, BP 53, Zoopôle Les
Croix, 22440 Ploufragan, France
G.P. Martineau, Ecole Nationale Vétérinaire de Toulouse, 31076 Toulouse, France
422 Weaning the pig

H.M. Miller, The , Centre for Animal Sciences, LIBA, School of
Biology, Leeds LS2 9JT, United Kingdom
P.C.H. Morel, Institute of Food, Nutrition and Human Health, Massey University,
Private Bag 11-222, Palmerston North, New Zealand
P. Mormède, Neurogénétique et Stress, INSERM U471, INRA, Université Victor

Segalen Bordeaux 2, Institut François Magendie, 33077 Bordeaux, France
J.L. Nelssen, Department of Animal Sciences and Industry, Kansas State University,
P. Orgeur, INRA- PRMD, 37380 Tours, France
J.R. Pluske, School of Veterinary and Biomedical Sciences, Murdoch University,

Murdoch WA 6150, Australia
A. Prunier, INRA, Unite Mixte de Recherches sur le Veau et le Porc, Saint-Gilles,

France
H. Quesnel, INRA, Unite Mixte de Recherches sur le Veau et le Porc, Saint-Gilles,

France
R.D. Slade, The , Centre for Animal Sciences, LIBA, School of

Biology, Leeds LS2 9JT, United Kingdom
N.M. Soede, Animal Husbandry Group, Wageningen University, P.O. Box 338, 6700
AH Wageningen, The Netherlands
B. Stoll, USDA/ARS Children’s Nutrition Research Center, Department of Pediatrics,

Baylor College of Medicine, 1100 Bates Street, Houston, Texas 77030, USA
M.D. Tokach, Department of Animal Sciences and Industry, Kansas State University,
C.A.Tsourgiannis, University of Plymouth, Faculty of Land, Food and Leisure, Seale-

Hayne Campus, Newton Abbot, Devon, TQ12 6NQ, United Kingdom
M.A.M. Vente-Spreeuwenberg, Nutreco Swine Research Centre, P.O. Box 240, 5830
AE Boxmeer, The Netherlands
M.W.A. Verstegen, Animal Nutrition Group, Wageningen University, P.O. Box 338,
6700 AH Wageningen, The Netherlands
I.H. Williams, School of Animal Biology, Faculty of Natural and Agricultural Sciences,
University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia

Index
A B
α-linolenic acid 175 bacterial translocation 180, 184
accumulate body fat 31 bedding 341-342
active immunity 220, 224 belly-nosing 57
active or passive coping strategy 89 biochemistry of the gut 82
acute IGF-I treatment 71 birth-weight 20, 25, 91, 363-364, 366-367,
acute phase protein production 150 371
ad libitum 25 blood plasma 56
adaptations to underfeeding 70 boar 405
adaptive immunity 221 body
adrenal reactivity to ACTH 54 – lipid 66
affinity constants 128 – protein 68
aggressive behaviours 57 – stores 399-401
AIAO see all-in / all out (AIAO) – thermal insulation 338-339
air velocity 343 butyric acid 181, 314
all-in / all out (AIAO) 349, 353, 373-374,
377 C
ambient temperature 338-340, 353 calcium 269, 274
amino acid transport 128 carbohydrase induction 127
amino acid utilization 314 carboxymethylcellulose (CMC) 207
ammonia 167 carnitine 269, 274
amylase 124 catecholamine excretion 54
amylolytic activity 40 CD4+ T cells 150
anestrus 385-388, 397 CD8+ T cells 134
anorexia 204, 237 cell proliferation 303, 305-306, 320
anterior teats 84 cellular immunity 230
antigen-presenting cell (APC) 222, 225-231, cereals, cooked 43
236 cereals, flaked 43
antigenic compounds 43 CF see continuous flow (CF)
antimicrobials 322-323 changing light patterns 63
APC see antigen-presenting cell (APC) chymotrypsin 124
apical 127 circulating cortisol 54
arginine 319, 320-321 circulating free fatty acid levels 54
aromatic compounds 45 citrulline 312
arterial nutrient utilization 308 climatic environment 404
aspartate 167, 311-312 CMC see carboxymethylcellulose (CMC)
ATP levels in jejunal mucosa 159 cold stress 73
colonocytes 181
colostrum 362, 368-369, 371
commercial

Index
– pellets 64 dominant pigs 95

– weaning 138 draughts 345, 350
– weaning age 123 dried porcine solubles 278
compensatory growth 25 dried skim milk 277
complex carbohydrates 40 dry pelleted feed 56
concanavalin A 172
confinement-reared piglet 94 E
conserve gut 68 early weaning 28, 372
conserve protein 67 easily digestible diet 56
continuity of food intake 99 ecophysiology 102
continuous flow (CF) 373-374 effects of gender 43
copper 269-271, 274, 288 EGF see epidermal growth factor (EGF)
corn starch 184 elastase I 124
cortisol insensitivity 131 elastase II 124
cortisol release 132 embryo survival 385, 393-397, 400, 404,
creep feed 21 408
creep feed consumption 42, 61, 88 endocrine changes 61
creep feeding 91 endotoxicosis 168
cross nursing 369 energy 264, 289, 368-369, 391
crypt depth 19, 124, 125 – deficit 65
crypt enterocytes 310 – sources 264, 272, 285
culling 385, 387 enteral nutrition 132
cysteine 265, 275, 316-317 enteric disease 199, 201, 211, 339, 349, 351
cytokines 220-221, 224, 226-228, 230, 234, enterocyte 127, 184, 310
237, 241, 244, 304, 322 – aldohexose transporters 127
cytosolic dipeptidase 183 – differentiation 151
– migration distance 125
D enteropathogenic E. coli 203
daily fluid intake 102 enterotoxigenic 202
diarrhoea 146, 199, 201, 203, 205-208, 210, enterotoxigenic E. coli 202, 204
337, 349, 351, 353, 372 enterotoxins 203, 205, 207, 210, 224
diet enzyme activities 119
– complexity 262-263 epidermal growth factor (EGF) 182
– formulation 259, 270, 287 epithelial barrier 99, 237, 238
– low-quality 56 epithelial integrity 134
dietary antigen 241 epithelial lining of the gut 99
dietary interventions 41 Escherichia coli 199-204, 206, 210-211
different chain-length fatty acids 130 essential amino acids 133
digestive estradiol-17β 389, 393
– enzymes 43 estrus 385, 388, 393-396, 398, 404-405, 408
– physiology 117, 301 ETEC 202, 204-205, 208-210
– problems 54 exogenous catecholamine 73
dipeptides 168
426 Weaning the pig

Index
F – tract 40
family affiliations 85 – trauma 183
farrowing rate 394, 398, 405-408 genotypes, modern 66
fasting heat 26 GLP-1 135, 137
fat 273-274, 286-288, 399, 400 GLP-2 135, 137, 305-306, 310
– reserves 65, 70 glucagon-like peptide 2 (GLP-2) 135, 137,
– supplementation 172 305-306, 310
fatness 400-401 glucoamylase 127, 151
feed glucocorticoid receptor levels 54
– flavour 45 glucocorticoid receptors 132
– intake pattern 396 gluconeogenesis 66, 72
– preferences 45 glucose 127, 312, 313
feeder 289, 337, 346, 354 glutamate 167, 308-309, 311-313, 319-320
feeding glutamine 167, 308-309, 31-313, 319-321
– activity 88 glutamine administration 168
– behaviour 47, 81 glutathione 167
– patterns 101 glycerol, mobilised 67
– spaces 47, 90 glycogen breakdown 66
– strategy 368, 370 goblet cells 133, 149
– systems 42 Gompertz function 18
fermentation 199, 200, 205, 207, 209 grain sources 275, 285
fermented liquid feed 56 group size 337, 348, 354
fertility 394, 406 growth
fertilization rate 394, 404, 407-408 – factors 130
fetal gluconeogenic capacity 73 – potential 17, 365, 371, 376
fetal villus enterocyte 120 – rates of organs 123
fibre 205-206, 210-211 – to slaughter 20
fish meal 56, 276-277, 284, 286-288 gruel 22
flooring material 337, 346, 354 gut
follicle 389-390, 392-397, 407 – development 39
foraging behaviour 85 – ecosystem 82
fostering 362, 368-369, 372 – metabolism 307
fresh liquid feed 56 – physiology 117, 301
FSH 390, 392-393
functional feed ingredients 145, 185 H
haemolytic E. coli 202, 207, 210-211
G haemolytic ETEC 203-204, 206-210
galactose 127 health 353, 361, 373
GALT 225 hepatic ST receptor mRNA 70
gastric development 118 high ambient temperature 344, 405
gastric motility 139 highly palatable 56
gastrointestinal homeorhesis 67
– hormones 152 homeostatsis 103

Index
housing system 337, 405 – absorptive capacity 128

HPA see hypothalamic-pituitary-adrenal (HPA) – barrier function 147
axis – enlargement 122
humoral immunity 221-222 – immune system 224, 230-231, 233,
hydrolase activities 122 236-237, 243
hygiene 351, 353-354 – immunity 219, 231, 233, 237, 243-244
hypersensitivity 133, 230, 241-244, 279-280, – inflammation 220, 228
286 – microflora 199
hypothalamic-pituitary axis 72 – morphology 124, 234
hypothalamic-pituitary-adrenal (HPA) axis – nutrient requirements 301
54 – nutrient utilization 301, 306
hypothalamic-pituitary-ovarian axis 392, – permeability 149
405 intestine
– large 200, 202, 205, 207, 211
I – small 199-210
IgA 223-224, 226 intestinotrophic events 138
– cells 232 intraluminal nutrients 137
IGF-I 69, 391, 392 intravenous infusion 68
IgG 223-224, 242 intravenously supplied TPN 180
IgM 223-224 inverse relationship 91
– cells 232 isoleucine 265
immediate post-weaning period 63
immune system 44, 102, 219-224, 226, 228, K
230, 233, 242, 244 ketones 313
immunoglobulin 29, 39, 219, 222-224, 226,
233, 368-369 L
immunological low point 82 L-arginine 183
inappropriate gut microflora 100 lack of
increased rate of cell loss 148 – enteral stimulation 152
incretin hormones 135 – familiarity 96
individual variation 57 – nutrients 155
infection 322 lactation length 394, 396, 402
inflammation 243-244 lactic acid 181
ingestion of amniotic fluid 119 – bacteria 63
ingredient selection 263 lactose 262-263, 272-273, 285-287
initial feed intake 56 lamina propria 221, 225-228, 230-233, 236,
innate immunity 220 238-241
insulin 69, 72, 391-392, 397, 400 larger matriarchal group 85
insulin-like growth factors 182 LC-PUFA see long-chain, polyunsaturated fatty
interleukin-1 (Il-1) 150 acid (LC-PUFA)
interleukin-6 Il-6 150 LCFA see long-chain fatty acid (LCFA)
interval between nursing events 84 LCT see lower critical temperature (LCT)
intestinal lean tissue 69
428 Weaning the pig

Index
learning phase 85 microbial environment 82

LH 389-393, 400 microenvironment 341
lighting 344 microflora 199-201, 203, 205-206, 209
lipase 124 microscopic morphology 176
lipase activity 172 milk energy intake 63
liquid diets 41, 90 milk products 273, 283, 285
liquid feeding 107 minerals 269
litter cohesion 57 minimising the growth check 27
litter size 37, 362-364, 388-389, 394, 398- mixing of animals 53-54
399, 401-402, 405-407 mobilisation of body lipid 65
long-chain fatty acid (LCFA) 321 monosaccharides 127
long-chain, polyunsaturated fatty acid (LC- morbidity 29
PUFA) 321-322 mortality 29
long-term benefits 23 mucin 211, 224, 306, 317
longevity 385, 394 mucosal function 145
lower critical temperature (LCT) 20, 339, mucosal integrity 167
341-343 mucus 202, 211
LR3IGF-I infusion in suckling piglets 71 muscle fibres 365
luminal nutrient utilization 308
lymphocyte 147, 222, 226-230, 232-233, N
236-237, 241 NDO see non-digestible oligosaccharides
lysine 264-267, 278, 282, 318, 398 (NDO)
NEFA concentrations 66
M negative protein balance 68
M-cells 147 neonatal enteral nutrition 129
macrophage 220, 227, 231, 236-237 neuroendocrine changes 53, 57
major histocompatibility complex (MHC) non-digestible oligosaccharides (NDO) 175,
222, 225-231, 236-238, 241 180
malnutrition 158 non-optimal indoor climate 350
maltase 127, 151 non-starch polysaccharide (NSP) 206-212
– activities 40 norepinephrine 73
maltose 121 novel environment 53
management options 38 noxious gases 344
management strategies 108 NSP see non-starch polysaccharide (NSP)
maternal catabolism 392 nucleosides 185
meal or a pellet 90 nucleotides 184, 322
mechanical stimulation 155 nutritional deficit 57
medicated early weaning (MEW) 374 nutritional management 37
metabolic status 391 nutritional program 259, 262, 288
methionine 265, 275, 278, 316-317 oedema 203
MEW see medicated early weaning (MEW)
MHC see major histocompatibility complex
(MHC)

Index
O portal-drained visceral (PDV) 307-309, 311,

oils 43 313-315, 318, 322
oligosaccharides 282-283 post-hepatic amino acid supply 72
ontogeny of somatotropin 69 post-weaning 92
operant panels 95 – colibacillosis (PWC) 199, 201-212
oral tolerance 228-229, 243 – diarrhoea 44
organic acids 283 – growth check 37
ornithine 312, 320 – growth rate 92
ovalbumin 166 – intestinal maturation 122
ovulation 385 – lean tissue deposition 70
ovulation rate 393-398, 400-401, 406-408 potato protein 281
oxidative fuels 311-312 pre-natal effects 39
pre-weaning creep food intake 39-40, 43
P prebiotics 181
pair-feeding 160 probiotics 181-282
pancreatic enzyme activities 119 production cycle 37
Paneth cells 225 proglucagon derived peptides 135
paracellular permeability 159 proinflammatory immune system
paracellular transport 150 components 134
passive immunity 223, 374 prolificacy 394, 402, 406
PDV see portal-drained visceral (PDV) proline 312, 319, 320
pen structure 337, 346, 354 protein intake 398, 401
pepsin 40 protein sources 30, 262-263, 275-278, 281-
peptide absorption 129 282, 284, 287-288
peri-natal colon 120 putriscine dihydrochloride 183
permeability 166 PWC see post-weaning colibacillosis (PWC)
Peyer’s patches 225-226, 233
phenylalanine 318-319 R
phosphorus 269 rapid intestinal growth 129
photoperiod 405 rate of lipogenesis 66
phytase 283 reduced functionality 126
pituitary hormones 389 reduced welfare 57
plant proteins 30 reduction in nocturnal temperature (RNT)
plasma 341-342
– catecholamine 73 relative humidity 343
– cortisol 73 reproductive axis 385, 388-389
– glucose 66 reproductive performance 385, 394, 396,
– glycerol concentrations 67 398, 400-401, 408
– IGF-I 69 restricted feeding 44, 160
– insulin 72 retrograded starch 176
– ST 69 ribosylphosphates 184
poly-unsaturated fatty acids 172 rice 206, 209-211
polyamines 183, 320-321 risk factors 351, 353-354
430 Weaning the pig

Index
RNT see reduction in nocturnal temperature – whole egg 276

(RNT) ST receptor gene 69
starch 399
S starter diets 27
salmonellosis 202 stimulation of food intake 28
satiety 103 stocking densities 347, 354
SCFA see short-chain fatty acids (SCFA) stocking rate 337
secretory IgA 226, 227 stomach mass 123
secretory immunoglobulins 147 stress hormones 53
segregation 374, 377 suckling 389, 402
serotype 203, 207 sucrose 121
SEW 53, 275, 280, 283-288, 375 supernumerary 361, 362-363, 371, 376-377
sexual dimorphism 43 supervision of farrowing 368
short-chain fatty acids (SCFA) 180, 305-306, supplemental water 47
310, 313-314 supplementary feeding 23
sigmoidal growth 18 supplementary milk 22
similar intra-suckling intervals 84 supplemented piglets 24
skeletal muscle protein synthesis 72 survival 367, 376
skim milk 63, 277, 284 sweetener 45, 106
small intestinal histology 64 synchronous feeding 97-98
small intestinal integrity 149
social facilitation 97 T
social rank 89 T cells 222
soluble fibre 175 taxation of the adaptive mechanisms 57
somatotrophic activity 70 temperature fluctuation 342, 344-345, 350
somatotrophic axis 54 thermal requirement 337-339
somatotropin 68 thermoregulation 39
sow threonine 265, 316-318, 320-321, 323
– genotypes 88 tight junctions 182, 224, 239
– milk 21, 86 tissue thermal insulation 353
– milk yield 56 TNF see tumor necrosis factor (TNF)
– vocalisations 86 total heat production 65
soybean meal 262, 279-281, 284, 286-287 trace minerals 269, 271
soybean, hydrolysed 166 transient starvation 100
spermine concentration 184 transportation 53
split weaning 22, 368, 370 true digestibilities 19
spray-dried trypsin 124
– animal plasma 263, 269, 275, 284, tryptophan 265
286 tumor necrosis factor (TNF) 150
– blood meal 276, 278, 284, 286-288 tyrosine 319
– bovine colostrum 28, 30
– egg protein 281, 284
– wheat gluten 282

Index
U whole-body fractional protein 67

underfed piglet 47 withholding soybean meal 44
underfeeding 185
undernutrition 67 Z
underprivileged 361-362, 365-367, 371, 376 zinc 269, 271
urinary excretion 53 – oxide 270-271, 285-288
urinary norepinephrine 73
V
valine 265
ventilation 343-344, 351
VFA see volatile fatty acids (VFA)
villous architecture 19, 100, 120, 126, 147
villus enterocytes 310
villus surface 138
viscosity 208-209
vitamins 268-269
volatile fatty acids (VFA) 205
volumetric fill 104
W
ω-3 polyunsaturated 175
ω-6 polyunsaturated 175
water
– availability 47
– intake 47, 87
– temperature 105
– holding capacity 208, 210
waterer 337, 346, 354
weaning
– age 28, 37, 259-261
– anorexia 54
– of piglets 149
– weight 260, 364, 366
– weight advantage 38
– elicited gut hormone secretion 135
– induced impairment 145
– to-estrus interval (WEI) 385, 393-395,
397-398, 400-402, 405-408
WEI see weaning-to-estrus interval (WEI)
weight of the small intestine 64
whey 272, 276-278, 284, 286-288
– protein 166
432 Weaning the pig

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Weaning the pig

Concepts and consequences

First published, 2003 The individual contributions in this

2 Growth of the weaned pig 17

3 Nutritional management of the pig in preparation for weaning 37

4 Behavioural changes and adaptations associated with weaning 53

Concepts and consequences 7

4.2 Neuroendocrine consequences of weaning 54

5 Metabolic and endocrine changes around weaning 61

6 Factors affecting the voluntary feed intake of the weaned pig 81

7 Digestive physiology of the weaned pig 117

8 Weaning the pig

7.2.1 Preparation 118

8 Diet-mediated modulation of small intestinal integrity in

9 Interactions between the intestinal microflora, diet and diarrhoea,

Concepts and consequences 9

9.2 Major enteric diseases at weaning 201

10 Aspects of intestinal immunity in the pig around weaning 219

11 Nutritional requirements of the weaned pig 259

10 Weaning the pig

11.5 Selection of ingredients for the weaned pig 272

12 Intestinal nutrient requirements in weanling pigs 301

13 Environmental requirements and housing of the weaned pig 337

Concepts and consequences 11

13.3.3 Stocking densities 347

14 Saving and rearing underprivileged and supernumerary piglets,

12 Weaning the pig

15 Productivity and longevity of weaned sows 385

List of authors 422

Concepts and consequences 13

Nevertheless, changes in the global business of pig production continue to occur

Concepts and consequences 15

16 Weaning the pig

2.2 The potential growth of weaned pigs

Concepts and consequences 17

experiments to those of Hodge (1974) were conducted with modern-day genotypes,

2.3 Description of growth

Daily gain = liveweight * B * ln(weight at maturity/liveweight),

where B is a growth coefficient.

The Gompertz function requires two parameters, an asymptote or description of

18 Weaning the pig

2.4 The growth check at weaning

Concepts and consequences 19

The third challenge at weaning is the psychological stress that accompanies

2.5 Bodyweight at weaning - its importance for

20 Weaning the pig

Because of the great importance of bodyweight at weaning, research has focused

2.6 Can weaning weight be increased by

Concepts and consequences 21

Growth of piglets during lactation can be stimulated if food is offered in a liquid

As suggested above, the success of stimulating growth by offering supplementary

22 Weaning the pig

The conclusion is that supplementary feeding during lactation can increase

2.7 Do pigs stimulated to reach higher weaning

Concepts and consequences 23

the milk available to each piglet by split weaning or offering it as a supplement

Heavy Light Milk No milk

24 Weaning the pig

2.8 Do pigs exhibit compensatory growth?

Whether animals exhibit compensatory gain after a period of restriction depends

Despite an exhaustive literature on compensatory growth (see reviews by

Concepts and consequences 25

intestinal tract. In a well-nourished animal these organs make up 10 to 15% of