IMPACT OF TRANSPORT AND RELATED STRESSES ON

THE INCIDENCE AND EXTENT OF HUMAN PATHOGENS

IN PIGMEAT AND POULTRY
R.W.A.W. MULDER

DLO-Institute for Animal Science and Health

Information Services)
Agricultural Research Department @LO-NL)
P.O. Box 59, 6700 AB Wageningen, The Netherlands

(The former Spelderholt Centre for Poultry Research and

Accepted for Publication June 27, 1995

ABSTRACT

Meat products are very important sources of protein in the human diet. The
contamination of these products with pathogenic microorganism, such as
Salmonella and Campylobacter, make both production and consumption of them
a precarious proposition. Several methods can decrease the level of contamination with these pathogenic microorganisms. However, there are still situations
of high microbial load which cannot be explained and are ofen attributed to
stress. This paper describes the effect of transport, husbandry and nutrition
practices on contamination of slaughtered products. Examples of the stress
occurring duringfattening, catching and loading, transport and conditioning at
the processing plant, are given.
INTRODUCTION
Meat forms an important component in the Western diet. Over the years,
there have been increasing requirements from consumers for foods that are safe,
do not need the addition of preservatives and need little or no preparation or
cooking by the consumer. Thus there is a real pressure to produce meat and
meat products that contain minimal numbers of both spoilage and human
pathogenic organisms.
Human foodborne diseases are considered to be one of the major problems
in the modem world, and they are an important cause of economic losses due
to hospitalization and absenteeism. Salmonella and Campylobacter infections
account for the majority of acute cases of human gastroenteritis. The results of
sentinel and population studies (Table l), carried out in The Netherlands since
1987, demonstrate that Campylobacter bacteria are the most prominent cause of
acute gastroenteritis in humans. This seems in contrast to traditional reports,
Journal of Food Safety 15 (1995) 239-246. A f f Rights Reserved.
OCopyright 1995 by Food & Nutrition Press, Inc., Trumbull, Connecticut.

239

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where Salmonella is the top-seeded organism. This difference is probably caused

by the past (and in some cases continued use) use of investigating and reporting
systems, that do not include Campylobacter.
Salmonella spp., Campylobacter spp., Listeria monocytogenes and
Staphylococcus aureus are the potentially pathogenic microorganisms which are
most frequently isolated from live animals and pig and poultry meat.

TABLE 1 .
CAUSES AND INCIDENCES OF ACUTE GASTROENTERITIS IN MAN
IN THE NETHERLANDS 1987-1992

Frequency

Incidence
(#/lo00 individuals
per year)

Microorganisms

(X)

Campylobacter
Salmonella
Shigella
Escherichia coli
Clostridium perfringens
Rotaviruses

12-15

18-23

4-5
0-3
3
3

6-11

Adapted from Notermans and van de Giessen (1993).

Although the reports of isolations are not consistent for all organisms from
all commodities, some trends can be observed. Salmonella isolations are most
frequently reported; the most important Salmonella serotypes in isolates from
humans, poultry and pigs are shown in Table 2. Unfortunately, comparable data
are not available for Campylobacter and other pathogenic microorganisms. From
these results, it is evident that even in a two year period the top-five Salmonella
serotypes have changed. In 1985, S. enteritidis accounted for approx 2.4% of
the human isolates in The Netherlands. In 1989 this figure was 20.1 % and rose
to 34.4% of the isolates in 1991. The data in Table 2 also suggest that S.
typhimuriuminfections in humans are caused by pigs, and S. enteritidis infection
by poultry.
In a recent survey, Jacobs-Reitsma et al. (1994), estimated the Cumpylobacter and Salmonella incidence in broiler flocks over a one year period from
early 1992 to early 1993. Campylobacter spp. were isolated from 153 out of 187
broiler flocks (82 %). Campylobacterjejuni was the dominant species, although
due to novel serotyping systems the difference with C. coli isolates is not very

HUMAN PATHOGENS IN PIG AND POULTRY

24 1

clear. There was a seasonal variation with maximum isolation rates in JuneSeptember and minimum isolations in March. In the same flocks the Salmonella
contamination was not influenced by the season and Salmonella was isolated
from 49 out of 181 flocks (27%). Consumer-ready poultry products were
Campylobacter-positive in 62.6 % of the samples and Salmonella-positive in
44.2% of the total number of samples (Bolder 1993).

TABLE 2.
TOP FIVE SALMOh'ELLA SEROTYPES IN ISOLATES FROM HUMANS,
POULTRY AND PIGS IN THE NETHERLANDS
Human (%)

S. typhimurium
S. enteritidis
S. virchow
S. hadar
S. infantis

Poultry (%)

Pig (%)

1989

1990

1989

1990

1989

1990

44.9
20.1
6.2
2.2
2.4

39.7
29.5
6.8
2.6
1.9

16.9
19.5
8.6
9.9
11.3

18.4
10.0
13.1
18.8
14.2

81.2
1.0

77.6
<1
0
<1
1.5

<I
0
1.9

Data: National Institute of Public Health and Environmental Protection, Bilthoven, The Netherlands

In contrast to poultry, where Campylobacter jejuni is the predominant

species, pigs are believed to be the most important source of Campylobacter
coli. Faecal carriage rates of Campylobacter spp. among pigs may be as, in
poultry, up to 100%. Contamination of slaughter pigs before chilling is up to
30 % , after overnight chilling this is below 3 % . The treatment of pigs before
slaughter influences contamination of pig products with these organisms. The
length of stay in lairage is an important factor in reducing Salmonella
contamination of pig products (Morgan er al. 1987).
The reduction of contamination of live animals with Salmonella and other
potentially pathogenic microorganisms has been the subject of study in many
countries over the last 25 years. Until now no single treatment or process able
to eradicate Salmonella and other pathogens could be identified. Even the
mechanism of infection with these organisms could not completely be elucidated
for all potentially pathogenic microorganisms. The use of competitive exclusion
has been somewhat successful. The treatment of day-old broiler chicks with a
microbiota which colonizes them and confers resistance to colonization by
pathogens, the so-called competitive exclusion treatment, reduces the contamination of flocks by Salmonella and Campylobacter under laboratory and farm

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conditions. In studies where flocks were also transported to the slaughterhouse

and examined again for these microorganisms, higher contamination rates were
found (Goren er al. 1988). Similar results were reported for pigs. The collection
of the animals on the farm, their transport to the processing plant and the
holding time and conditions before slaughtering seem to induce the spreading of
organisms, resulting in higher contamination and a continued carrier state of the
animals.
Salmonella and other pathogenic microorganisms may be transferred from
one animal to another when they are waiting slaughter, via faeces and drinking
troughs. The prevention of an excessively long period of holding in lairages and
prevention of overcrowding, specially in pigs, will considerably reduce the
proportion of animals found contaminated at slaughter. Clinically healthy animals carrying Salmonella and other pathogenic microorganisms may change their
excretion pattern of the organisms from intermittent to constant shedding if an
external factor upsets the equilibrium of their intestinal flora. A disturbance of
the intestinal functions will lower the resistance of the live animal and facilitates
the spreading of intestinal bacteria.
Stress is the word often used in those situations which are too complex
to be understood, and it is often used to explain why preventive measures to
control spreading of pathogens in live animals do not work. Stress factors
described in the literature were observed during fattening, catching and loading,
transport and conditioning. Stress can, among others, be accompanied by
symptoms such as damage to the intestinal tract and a lower capacity of the
immune system.
The influence of stress on the immune system is complex and depends on
a number of factors. Among these are: the stressor, genetics, nutrition, antigen
concentration. Some stressors are believed to influence positively the resistance
to infections with pathogens. Examples are some forms of so-called social stress
which seem to increase resistance against S. aureus and E. coli. On the other
hand, other social stressors, for example mixing pigs from different herds
together at transport, have resulted in higher rates of contamination in pigs.
(Williams and Newel1 1968; Gallwey and Tarrant 1979). Renwick et al. 1993,
recently, demonstrated, that products became more contaminated with microorganisms when the time between crating and holding before slaughter increased.
This indicates shedding of faecal material, which spreads over live birds. The
number of hours of feed withdrawal prior to crating also influences excretion of
pathogens. Normally chickens empty their caeca every 24 h, but because of the
change in environmental conditions the excretion pattern changes. In the
literature most data relate to spreadinghhedding of Salmonella bacteria.
Although Campylobacfer seem to cause more problems with regard to human
public health, this prominent position is not reflected yet in the literature.

HUMAN PATHOGENS IN PIG AND POULTRY

243

EXAMPLES FROM PIGS AND POULTRY

Pigs
Preslaughter handling can affect the contamination rate of slaughtered
animals. Feeding, environmental conditions during transport and lairage, including the total time involved and mixing animals from several herds, are the main
factors. Slavkov ef al. (1974) demonstrated the effect of stress during loading,
transport and holding time before slaughter. Before pigs were delivered to the
abattoir, none were isolated; after delivering to the abattoir 0.1 % (2/1952) of the
samples were positive; after slaughter this percentage increased to 0.7%.The
authors conclude, that stress factors had been responsible for the increase in the
carrier state.
The most comprehensive work in this area is by Morgan el al. (1987).
These authors studied the effect of time spent in lairage on caecal and carcass
Salmonella contamination of groups of pigs originating from one producer and
slaughtered in two different abattoirs. The main differences between the abattoirs
were pen size and (visual) hygiene (abattoir 1: larger pens and less hygiene).
Table 3 presents some data from this study. Thus the time spent in lairage can
be used to minimize Salmonella contamination. The shorter the period, the
better. Pen size (smaller pens) and hygiene are the other important factors to
decrease (cross)contamination. In this study carcass contamination was caused
by intestinal Salmonella infections. This could be demonstrated by the Salmonella recovery rate and the Salmonella serotypes from caecal contents and the
carcass surface.

TABLE 3.
ISOLATION OF SALMOh'ELLA FROM CAECAL CONTENTS OF PIGS HELD IN
LAIRAGE FOR THREE DAYS (18,42 AND 66 H) IN TWO ABAnOIRS
Number of positivesltotal number sampled.
Caecal isolation rate
Abattoir

Day 1

Day 2

Day 3

20175
8/76

29/71
6/74

45/75
24/74

28/151
(18.5%)

351145
(24.1 %)

1
2
Total

Adapted from Morgan et nl. (1987).

711149
(47.7%)

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As carcass contamination was determined by the Salmonella entering the

abattoir in the intestine of the pigs, a very important strategy to reduce
contamination is preslaughter handling avoiding any form of multiplication of
Salmonella in the live animals (see also Huis int Veld et al. 1994). Another
reason for spending a short time in lairage, is the economic aspect of the carcass
weight loss with increasing time.

Poultry
Stress in poultry is accompanied by a series of symptoms. The increased
corticosteroid levels in blood plasma and the occurrence of damage to the
intestinal tract, heart and blood vessels are of major importance. Decreased
shear strength of the intestinal tract may result in gut breakage during
processing, which is responsible for further spreading of microorganisms over
carcasses and equipment (Bilgili 1988). Feed and water withdrawal prior to
transport, influences gut contents and the emptying of the digestive tract of
broilers. Papa and Dickens (1989)concluded that feed withdrawal 8-12 h before
slaughtering minimizes the faecal contamination of carcasses. Moran and Bilgili
(1990) demonstrated that stressing chicken broilers, under conditions simulating
the practice of feed withdrawal and live haul, results in a delayed caecal
retention for another 24 h.
Bolder and Mulder (1983) reported the increase of Salmonella contamination
of slaughtered broilers after transport. The similarity with findings in the pig
industry, as in other areas, is striking: Salmonella serotypes after transport
observed on slaughtered products originate from live birds, which indicates
intestinal origin. The question arises whether there is not a major discrepancy
between husbandry and nutrition factors aiming at the economical production of
poultry broilers and the contamination of consumer-ready products with
potentially pathogenic microorganisms. Preslaughter conditions influence the
contamination rate of slaughtered products. However, the real circumstances and
mechanisms are not known. To interrupt microbial cycles in animal production,
more attention should be paid to aspects of contamination in relation to
husbandry, nutrition and processing, including conditions of loading and transport.
CONCLUSIONS
The mechanism of spreadinghhedding of microorganisms from clinically
healthy carrier animals under stressing conditions is not clear. Nevertheless from
the literature and actual practice, it is known that preslaughter conditions in
handling live animals influence the contamination rate of the slaughtered
product. Therefore preloading activities in the shed, the loading procedure, the

HUMAN PATHOGENS IN PIG AND POULTRY

245

transport, the holding period and conditions at slaughter and the slaughter
process itself should be given more care.

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