Dairy Cows Reproduction, Nutritional,, Manegment y Disease

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ANIMAL SCIENCE, ISSUES AND PROFESSIONS
DAIRY COWS
REPRODUCTION, NUTRITIONAL
MANAGEMENT AND DISEASES
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ANIMAL SCIENCE, ISSUES AND PROFESSIONS
DAIRY COWS
REPRODUCTION, NUTRITIONAL
MANAGEMENT AND DISEASES
CATHERINE T. HERNANDEZ
EDITOR
New York
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CONTENTS
Preface vii
Chapter 1 A Novel, Illustrated Classification System
to Define the Causes of Bovine Perinatal
Mortality Internationally 1
John F. Mee
Chapter 2 Resetting Priorities for Sustainable Dairy
Farming under Global Changing 53
I. Blanco-Penedo, J. Perea,
J. O. L. Cerqueira and R. Payan-Carreira
Chapter 3 Somatic Cell Count as the Factor Conditioning
Productivity of Various Breeds of Cows
and Technological Suitability of Milk 91
Joanna Barłowska, Zygmunt Litwińczuk,
Aneta Brodziak and Jolanta Król
Chapter 4 Strategies to Improve the Reproductive
Efficiency of Dairy Cattle 127
L. S. R. Marinho, F. Z. Machado
and M. M. Seneda
Index 149
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PREFACE
In this book, the authors discuss the reproduction, nutritional management

and diseases relating to dairy cows. Topics include strategies to improve the
reproductive efficiency of dairy cattle; an illustrated classification system to
define the causes of international bovine perinatal mortality; resetting the
priorities for sustainable dairy farming under global change; and somatic cell
count as a factor conditioning productivity of various breeds of cows and
technological suitability of milk.
Chapter 1 - Currently there is no published classification system for the
causes of death in cases of bovine perinatal mortality internationally. In
addition, the criteria used to define these causes of death are also not
standardised, nor published. This results in inconsistent reporting of many
different causes of death and often a high proportion of cases being
unexplained.
A system is required for codifying bovine perinatal mortality for
epidemiological surveillance and perinatal audit, as in human perinatology
where the World Health Organisation’s International Classification of
Diseases Manual is used internationally. Hence, the objective of this study was
to develop a novel classification system for both the criteria and the causes of
death in cases of bovine perinatal mortality internationally in order to improve
our understanding of the main causes of such reproductive loss. A foeto-
maternal, clinico-pathological classification system was developed over a
period of three years using three primary sources of information. A systematic
literature-based review, the findings of an international Delphi survey and
epidemiological and pathological data from an active surveillance, whole-herd
necropsy study were used to design the system. Ten major causal categories of
death were assigned with sub-classification as required; alphabetically –
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viii Catherine T. Hernandez
combination of contributory factors (more than one cause of death), congenital

defect (economically lethal and lethal), dystocia (bradytocia, traumotocia,
bradytocia and traumotocia, dystocia anamnesis, dystoxia and fetal
maldisposition), eutoxia, haemorrhage and anaemia (external omphalorrhagia,
internal omphalorrhagia, idiopathic hemoperitoneum, anaemia), infection,
iodine imbalance, premature placental expulsion, prematurity and other
specific disorders (e.g. accidental death, hypothermia, intra-uterine growth
retardation, etc..). Each cause of death was assigned a degree of confidence of
diagnosis from certain through probable to possible.
These causes of death were assigned using the written anamnesis from the
farmer or veterinary practitioner, gross necropsy observations (including
photo-documentation) and the associated laboratory tests, i.e. an algorithmic,
summary diagnosis. The cause of death indicated the pathological condition of
the fetus or calf which made the greatest contribution towards the death. Only
proximate (immediate) factors were listed in the cause of death, e.g. a genetic
mutation may be the ultimate cause of a lethal congenital defect but the defect
was the proximate cause of death. Some causes of death, e.g. dystocia, were
disaggregated in order to differentiate separate components (where a
portmanteau is used, e.g. dystoxia) which can be re-aggregated as necessary
for different reporting formats.
Differential diagnoses were reached through both processes of inclusion
and of exclusion. This ten-level classification system can be used to calculate
cause-specific mortality rates (CSMR) and the attributable fraction (AF) of
perinatal mortality due to each cause of death.
Chapter 2 – Global change increasingly affected agricultural production
and global community has begun to refocus in a change in livestock
production, defending the use of sustainable strategies. Considerations with
respect to changing environments should also address the dairy farm systems
and new goals have to be designed. Good farming practices should regard their
need for on-going adaptation to an ever-changing environment that should
offer solutions for buffering against climatic extremes, disease epidemics,
changing nutrient availability, seasonal availability of forage and other stresses
that will add to an already heterogeneous environmental condition. Sustainable
dairy systems should be adjusted to these new expectations, and be indeed
adapted to the new agricultural policies and the increasing demands of the
consumers for products free of drug residues (safety) and be more ecofriendly
produced. The key to success is to maximise farm efficiency finding the right
balance between the production system and the management techniques to
maximise the output for food production, involving a suitable dairy cow
Preface ix
biotype, which may trigger new strategies for feeding, breeding and health
control whilst minimising impact on the environment and ensuring animal
welfare and profitability for their business. This chapter book pretends to
present a holistic capture of main issues regarding management, feeding
regimes, breeding, reproductive efficiency with examples of current
sustainable production systems.
Chapter 3 – Early detection of mastitis with subclinical symptoms is
possible by determining somatic cell count (SCC). SCC is the most widely
accepted indicator of the mammary gland health as well as milk quality and its
technological suitability. The authors’ research has revealed that an increase of
SCC (independently of a breed of cows) mainly causes a rise in a total crude
protein content and a distinct reduction in lactose level (P≤0.01). Moreover,
SCC also lengthens the time of milk enzymatic coagulation (P≤0.01) but it
does not influence its thermal stability. Distinct negative relationship between
casein content and SCC is confirmed by relatively high value of correlation
coefficient (r=-0.59). In the authors’ studies the significant interactions (breed
of cows x SCC) for the daily yield of cows, content of protein, casein and
lactose, protein to fat ratio and rennet-induced milk coagulation time also have
been stated, which indicates a differentiated response of various breeds of
cows to udder inflammations. Holstein-Friesian cows are more sensitive to
decline of daily yield, that is reflected in higher negative value of correlation
coefficient between SCC and milk yield (-0.245). In Simmental and Jersey
cows the correlations were negative as well but their values were substantially
lower (r=-0.123 and r=-0.148) and statistically insignificant. With the age of
cows increase in SCC was noted and in the cows of local breeds (Polish Red,
Polish Black and White, Whitebacked) and Jersey that rise was much smaller
in comparison to Polish Holstein-Friesian cows. Significant interaction
(P≤0.05) for SCC between breed of cows and subsequent lactation was
indicated. However, the significant changes in milk constituents were recorded
only when the SCC exceeded 500 thous. ml-1, that is in milk that does not meet
the current regulatory quality standards.
Somatic cell count also affects the changes in whey protein content. Rise
of SCC decreased the content of major albumins, i.e. alpha-LA and beta-LG,
by small degree, and that was confirmed by very low statistically insignificant
correlation coefficients (r=-0.07 i r=-0.05). Negative value of both
correlations, though, indicates a direction of changes and may imply that in
more advanced stages of udder diseases the decrease of milk proteins is likely
to be higher. However, with rise of SCC, content of immunoactive proteins
(lactoferrin and lysozyme) as well as bovine albumin serum (BSA)
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x Catherine T. Hernandez
significantly increased. The significant impact of SCC on content of these

proteins in milk is confirmed by relatively high positive values of computed
correlation coefficients (lactoferrin r=0.65, lysozyme r=0.63 and BSA r=0.59).
In the case of BSA that correlations were clearly differentiated in particular
breeds of cows, i.e. r=0.711 for Holstein-Friesian, r=0.577 for Simmental and
r=0.472 for Jersey. Thus, it can be assumed that there is a differentiated degree
of permeability of mammary gland cell membranes in cows of various breeds.
Chapter 4 - The reproductive performance of a lactating herd is a major
component of the profitability of a dairy farm. Factors such as negative energy
balance, heat stress and failures in heat detection can severely compromise
reproductive parameters. To overcome these problems, a variety of strategies
can be used. For example, failures in estrus detection can be solved with the
use of fixed-time artificial insemination (FTAI). Progesterone implants
combined with estradiol administration are very effective in promoting the
onset of a new follicular wave. With the use of a luteolytic agent and an
inducer of ovulation, AI can be performed at the appropriate time without the
need for estrus observation. In countries where the use of such drugs is not
allowed, protocols based on GnRH and PGF2α may also offer optimal
synchronization of ovulation. In locations where pregnancy rates are
compromised by high temperatures, a viable alternative to FTAI may be the
fixed-time embryo transfer (FTET). Embryos at the morula and blastocyst
stage are more resistant to heat stress than gametes and embryos in early
stages of development. Thus, embryo transfer (ET) on day 7 of development
can ensure satisfactory pregnancy rates throughout the year, even in months
and/or regions with higher average temperatures. ET has also been effective in
preventing early embryonic mortality and increasing pregnancy rates in repeat
breeders. Another strategy that can enhance the reproductive efficiency of
dairy herds is the cryopreservation of embryos; embryos are stored and can be
used at strategic times, such as in the warmer months of the year. This chapter
will discuss technological strategies that can lead to higher breeding
efficiency, improved reproductive efficiency and increased profitability of
livestock on dairy farms.
In: Dairy Cows ISBN: 978-1-62618-574-6
Editor: Catherine T. Hernandez © 2013 Nova Science Publishers, Inc.
Chapter 1
A NOVEL, ILLUSTRATED CLASSIFICATION

SYSTEM TO DEFINE THE CAUSES OF BOVINE
PERINATAL MORTALITY INTERNATIONALLY
John F. Mee
Animal and Bioscience Research Department, Teagasc,
Moorepark Research Centre, Fermoy, Co. Cork, Ireland
ABSTRACT
Currently there is no published classification system for the causes of
death in cases of bovine perinatal mortality internationally. In addition,
the criteria used to define these causes of death are also not standardised,
nor published. This results in inconsistent reporting of many different
causes of death and often a high proportion of cases being unexplained.
A system is required for codifying bovine perinatal mortality for
epidemiological surveillance and perinatal audit, as in human
perinatology where the World Health Organisation’s International
Classification of Diseases Manual is used internationally. Hence, the
objective of this study was to develop a novel classification system for
both the criteria and the causes of death in cases of bovine perinatal
mortality internationally in order to improve our understanding of the
main causes of such reproductive loss. A foeto-maternal, clinico-
pathological classification system was developed over a period of three
years using three primary sources of information. A systematic literature-

E-mail: john.mee@teagasc.ie.
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2 John F. Mee
based review, the findings of an international Delphi survey and

epidemiological and pathological data from an active surveillance, whole-
herd necropsy study were used to design the system. Ten major causal
categories of death were assigned with sub-classification as required;
alphabetically – combination of contributory factors (more than one cause
of death), congenital defect (economically lethal and lethal), dystocia
(bradytocia, traumotocia, bradytocia and traumotocia, dystocia
anamnesis, dystoxia and fetal maldisposition), eutoxia, haemorrhage and
anaemia (external omphalorrhagia, internal omphalorrhagia, idiopathic
hemoperitoneum, anaemia), infection, iodine imbalance, premature
placental expulsion, prematurity and other specific disorders (e.g.
accidental death, hypothermia, intra-uterine growth retardation, etc..).
Each cause of death was assigned a degree of confidence of diagnosis
from certain through probable to possible.
These causes of death were assigned using the written anamnesis
from the farmer or veterinary practitioner, gross necropsy observations
(including photo-documentation) and the associated laboratory tests, i.e.
an algorithmic, summary diagnosis. The cause of death indicated the
pathological condition of the fetus or calf which made the greatest
contribution towards the death. Only proximate (immediate) factors were
listed in the cause of death, e.g. a genetic mutation may be the ultimate
cause of a lethal congenital defect but the defect was the proximate cause
of death. Some causes of death, e.g. dystocia, were disaggregated in order
to differentiate separate components (where a portmanteau is used, e.g.
dystoxia) which can be re-aggregated as necessary for different reporting
formats.
Differential diagnoses were reached through both processes of
inclusion and of exclusion. This ten-level classification system can be
used to calculate cause-specific mortality rates (CSMR) and the
attributable fraction (AF) of perinatal mortality due to each cause of
death.
INTRODUCTION
Classification may be described as a construct systematically arranging
similar entities with criteria or differing characteristics. Currently there is no
classification system for bovine perinatal mortality. This contrasts with human
perinatology where more than 35 classification systems have been published
since the first system was developed in 1954 (Lawn et al., 2011).
Such systems attempt to establish the cause of inevitable/unavoidable
death in an individual perinate, not the correlates of death in a population of
perinates, such as, for example, maternal parity (Mee et al., 2008).
A Novel, Illustrated Classification System … 3
Classification attempts to define whether a perinate died of or due to a disorder

(causal) or merely with a disorder (associative). The gradual evolution of these
systems over time has resulted in the percentage of unexplained human
stillbirths drop from 66% in the Wigglesworth system to only 15% in the
ReCause of death (relevant condition at death) system (Gardosi et al., 2005).
This demonstrates the potential for improved diagnosis rate in veterinary
perinatology were an evolved classification system to be adopted. An
improved diagnosis rate would in turn assist in encouraging higher carcass
submission and hence necropsy rates, a major problem currently in the
diagnosis of bovine perinatal mortality (Mee, 2008).
An ideal classification system for research and for routine diagnosis by
veterinary pathologists for veterinary practitioners would identify the
pathophysiologic entity initiating the chain of events that irreversibly led to
death based on clinical, pathologic and laboratory data.
The criteria to be used to categorize a particular condition as a cause of
perinatal mortality should consider the following principles: 1) there are
epidemiologic data demonstrating a significant excess of perinatal mortality
associated with the condition, 2) there is biologic plausibility that the condition
causes perinatal mortality, 3) the condition is either rarely seen in association
with live births or, when seen in live births, results in a significant increase in
perinatal death, 4) a dose–response relationship exists so that the greater the
“dose” of the disorder, the greater the likelihood of perinatal mortality, 5) the
condition is associated with evidence of fetal compromise, and 6) the perinatal
mortality likely would not have occurred if that condition had not been
present, i.e., lethality.
When attempting to classify causes of perinatal mortality it is often
difficult to determine the ‘definite’ cause of death. Risk factors may be
significantly associated with perinatal mortality but can also occur in liveborn
calves, multiple disorders can occur in the same calf and many cases cannot be
explained. All perinatal classification systems suffer from these uncertainties
(Reddy et al., 2009). One way of dealing with this inherent issue is to define
each condition as a certain, probable or possible cause of death. In addition,
the use of photographic images can assist in clarifying lesion assessment or
scoring (Mee and Szenci, 2012).
The paucity of information on the classification of bovine perinatal
mortality stems from the lack of any centralised coding of such deaths as
exists for human perinatology, e.g. International Classification of Diseases
(WHO, 2005). While national bovine laboratory data recording systems such
as VIDA and FarmFile in the UK (Gibbens et al., 2008) and veterinary
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4 John F. Mee
diagnostic support systems such as the Cornell Consultant in the USA

(www.vet.cornell.edu/consultant) exist they are not specialised perinatology
classification systems.
The absence of an internationally accepted bovine classification system is
a substantial barrier to any reliable audit of perinatal mortality causation and
data meta-analysis including analysis of secular and geographical trends.
Having a unified perinatal mortality causation mapping system would allow
researchers, veterinary diagnosticians and veterinary practitioners share
information in the same ‘language’ across laboratory, institutional and national
boundaries. This would lead to a better understanding of perinatal mortality
causation by farmers and veterinary practitioners, derive learning points for
best clinical practice for students and provide a firmer foundation for
prioritising interventions aimed at all-cause rate reduction by agri-
stakeholders.
Definition of Perinatal Mortality
Bovine perinatal mortality may be defined as the death of a fullterm

(>260d gestation) fetus before, during or within 48h after calving (Mee,
2008a). In this definition fetal death is death prior to complete expulsion in the
perinatal period. Stillbirth is birth after fetal death. Differentiation between the
continuum of abortion and stillbirth is based on arbitrary gestational thresholds
(e.g. <260 or 270 days) which are associated with the potential independent
viability of the fetus (lower limits of viability). These bovine thresholds have
been in use for over 150 years (Spencer, 1840). The data in Table 1 show the
variability internationally in the definition of the term bovine ‘stillbirth’. An
early attempt to standardise the nomenclature for bovine reproductive terms
defined stillbirth as a full-term dead fetus and perinatal mortality as death from
42 days of gestation up to 28 days after birth (Anon, 1972). In human
perinatology stillbirth is defined as death of a fetus weighing at least 500g or
following a gestation of at least 22 weeks, showing no signs of life.
The data in Table 2 show the variability internationally in the definition of
the term bovine ‘perinatal mortality’. In human medicine the term perinatal
mortality includes stillbirths and early neonatal deaths up to 7 days of age.
While these are the definitions recommended by the WHO (WHO, 2005),
other national definitions are also used.
Table 1. Examples of descriptors used to define the term

bovine ‘stillbirth’ in recent literature
Gestation Postnatal
Country Reference
threshold (days) threshold (hours)
>260 12 USA Linden et al., (2009)
>270 24 UK MAFF (1985)
265-295 48 USA Meyer et al., (2001)
NR 48 Iran Atashi (2011)
Ghavi Hossein-Zadeh, et al.,
>260 0 Iran
(2008)
NR 24 France Chassagne et al., (1999)
NR 24 Canada Luo et al., (1999)
>255 48 USA Olson et al., (2009)
NR 24 Poland Stefaniak et al., (2011)
>260 0 Ireland Mee, (2008a)
NR 48 USA Cole et al., (2007)
>260 24 Norway Gulliksen et al., (2009)
>240 1 Canada Waldner et al., (2010)
>260 24 Sweden Berglund et al., (2003)
NR - not reported.
Table 2. Examples of descriptors used to define the term bovine

‘perinatal mortality’ in recent literature
Gestation Postnatal
Country Reference
threshold (days) threshold (days)
NR <7 Mali Wymann et al., (2006)
>272 <1 England Brickell et al., (2009)
>260 <2 Ireland Mee (2008a)
NR <1 Finland Syrjala et al., (2007)
NR <1 Germany Gundelach et al., (2009)
>260 <2 Canada Khodakaram and Ikede (2005)
>275 <14 Japan Ogata et al., (1999)
>260 <2 hours Ireland Collery et al., (1996)
>260 <2 USA Johanson et al., (2011)
260-330 <1 Switzerland Bleul (2011)
>260 <1 Germany Hoedemaker et al., (2010)
NR - not reported.
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6 John F. Mee
Causes of Bovine Perinatal Mortality
There appears to be some agreement in the literature on the common

causes of bovine perinatal mortality (Table 3). The major causes of bovine
perinatal mortality, as described in recent necropsy studies internationally, are
anoxia (approximately 50%) and dystocic trauma (approximately 25%) and, to
a much lesser extent, other causes (approximately 15%), infections
(approximately 10%) and congenital defects (approximately 5%), (Table 3).
On average, some 20% of cases have no diagnosed cause but this varies
between 0 and 70% between studies (Table 3). The variation in the proportions
of necropsy-diagnosed causes of death reflects variations in the causative risk
factors but also variations in diagnostic definitions and the number and
selection criteria for calves and herds examined.
While the cause of death is usually determined from a necropsy
examination it is recognised that in some cases pathognomonic lesions may
not be visible at necropsy, e.g. accidental non-parturient trauma or premature
placental expulsion. Hence, a clinico-pathological diagnosis is often used to
assign weight to the clinical signs or anamnesis as well as the necropsy
findings.
This may explain why some cases of bovine perinatal mortality are
classified as unexplained where there is an inadequate history supplied with
the carcass.
Within studies on bovine perinatal mortality the number of calves or herds
investigated as well as any exclusion criteria, (e.g. heifers’ calves only, beef
calves only, singletons only), also affect the proportion of bovine perinatal
mortality caused by any particular cause of death. In addition to these
differences in diagnostic criteria and study design, the attributable fraction of
bovine perinatal mortality caused by any particular cause of death may be
predetermined by the surveillance system implemented. In passive
surveillance only extreme cases may be voluntarily submitted to the laboratory
unsolicited due to cost or inconvenience resulting in a non-random sample of
the population at risk. With risk-based, targeted or whole-herd active
surveillance a more representative sample of the population at risk may be
collected.
Thus there is wide variation in the number of causes of death diagnosed in
different calf studies internationally (Table 4) suggesting ad hoc recording of
the cause of death. It must be recognised that these studies differed in
diagnostic criteria and in design, both of which can contribute to differences in
the number of causes of death recorded. By comparison, 11 cause of death
categories, each with sub-classes, are listed by the WHO for perinatal
mortality in babies; maternal factors, disorders of fetal growth, birth trauma,
respiratory and cardiovascular disorders, infections, haemorrhagic and
haematological disorders, endocrine and metabolic disorders, digestive system
disorders, temperature regulation disorders, other disorders and congenital
malformations, (WHO, 2005). These categories are widely used
internationally often with some modifications. For example, in Ireland these
categories can be collapsed into 5 mega-categories (maternal factors,
immaturity, respiratory/cardiovascular disorders, congenital malformations
and all other specific causes) (ESRI, 2012). In addition, a standardised
protocol has been developed recently on how to conduct an autopsy in cases of
human stillbirth (Pinar et al., 2011).
These observations indicate the need for standardisation of assignable
causes of death in cases of bovine perinatal mortality as previously proposed
(Mee, 2009).
Table 3. Necropsy-diagnosed causes of death (%) for calves dying

in the perinatal period internationally (1990-2010)
Congenita
Reference
Unknown
Infection
Dystocia
l defects
Country
Anoxia
Calves
Other
(No.)
De Kruif and Benedictus

Belgium 1 100 7 55 6 18 4 10
(1993)
Canada 3 560 40.2 NR 2 4.3 2.9 31 21.6 Waldner et al., (2010)
Denmark 1 130 9 81 1.5 8 0.1 0 Agerholm et al., (1993)
Finland 148 43 4 10 10 8 29 Syrjala et al., (2007)
Iceland 129 34 37 NR 12 13 3.9 Siguroarson et al., (2007)
Ireland 1 119 4
34 1 14 9 42 Collery et al., (1996)
Japan 3 155 21 NR 3.9 NR 5.1 69.7 5 Ogata et al., (1999)
4
Netherlands 193 36.8 8.3 7.3 5.6 42 Muskens and Vos (2008)
Nr Ireland 1 365 23 46 NR 31 NR NR McCoy et al., (1997a)
Sweden 76 46.1 NR 5.3 2.6 10.5 35.5 Berglund et al., (2003)
USA 60 25 28.5 3.3 5 6.6 31.6 Schefers (2009)
1
dairy and beef calves, all others are dairy calves unless superscripted 3, 2 NR=not
recorded, 3 Beef calves; 4 Anoxic and dystocic lesions combined, 5 these calves
had shorter gestation and lower birth weights.
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8 John F. Mee
Table 4. Number of cause of death categories (excluding undetermined)

in necropsy studies of bovine perinatal mortality internationally
Causes of death Calves (No.) Reference

(No.)
16 560 Waldner et al., (2010)
10 43 Essmeyer (2006)
7 8,995 Kirkbride, (1992)
7 492 Bellows et al., (1987)
6 100 De Kruif and Benedictus (1993)
6 119 Collery et al., (1996)
5 130 Agerholm et al., (1993)
5 129 Siguroarson et al., (2008)
5 293 Smyth et al., (1992)
5 148 Syrjala et al., (2007)
4 60 Schefers (2009)
4 31 Khodakaram-Tafti and Ikede, (2005)
4 193 Muskens and Vos (2008)
4 76 Berglund et al., (2003)
3 155 Ogata et al., (1999)
Criteria Used to Define Causes of Perinatal Mortality
The foregoing indicates that there is limited consensus on the common

causes of bovine perinatal mortality. In addition, the criteria used to assign
causes of death vary considerably between published studies. For example,
while Khodakaram-Tafti and Ikede, (2005) used the history of dystocia and
detection of traumatic lesions, Collery et al., (1996) used the history of
dystocia or posterior presentation with or without the detection of traumatic
lesions to assign this cause of death. In other studies only the detection of
traumatic lesions was used (Agerholm et al., 1993, Smyth et al., 1992). Thus
while dystocia may be a commonly diagnosed cause of death, as the criteria
used to define ‘dystocia’ vary between studies, logically the proportion of
bovine perinatal mortality attributed to dystocia (the attributable fraction) will
vary also.
Similarly, while meconium staining of the hair coat and subserosal
haemorrhages has been induced experimentally by anoxia in the bovine foetus
(Dufty and Sloss, 1977), in some studies only meconium staining was used as
a criterion to diagnose anoxia (Collery et al., 1996) while in other studies
subserosal haemorrhages and tracheal congestion and mucus have been used,
but not meconium staining (Wilsmore, 1989).
For other causes of death, e.g. intrauterine growth retardation (IUGR)
there is no consensus on which criteria are diagnostic. Some authors have used
body weight (Murray, 1990, Orgeig, 2010) or organ weights (Steinhardt et al.,
1993), others crown rump length (Collery et al., 1996, Sharpe, 1998) and
others compact bone percentage (Dwyer, 1991), presence of radiodense
growth retardation lines in long bones (Smyth and Ellis, 1996) or bone lengths
(Richardson 1978).
These observations indicate that there are no minimal standards for bovine
perinatal necropsy and the need for standardisation of criteria used to assign
causes of bovine perinatal mortality. Hence, the objective of this study was to
develop a novel classification system for both the criteria and the causes of
death in cases of bovine perinatal mortality internationally in order to improve
our investigations of the understanding of the main causes of such
reproductive loss.
MATERIALS AND METHODS

A foeto-maternal, clinico-pathological classification system to define the
criteria for, and the causes of, bovine perinatal mortality was developed over a
period of three years (2010-2012) using three primary sources of information.
A systematic literature review (Mee, 2013), the findings of an international
Delphi survey (Mee et al., in press) and epidemiological and pathological data
from a whole-herd necropsy study (Mee, 2013) were sequentially used to
design the system.
1. Literature Review
Initially all publications where a necropsy-derived diagnosis of bovine

perinatal mortality was recorded, with or without diagnostic criteria, in the last
25 years (1987-2012) were retrieved from the author’s personal files and
electronic databases by cross-referencing sourced publications.
The information in these publications was extracted and tabulated, e.g.
Tables 3 and 4. In addition, publications from other species (e.g. humans,
primates, sheep, pigs, horses, dogs) with relevant information were included,
particularly where experimental models of causes of death produced
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10 John F. Mee
pathological lesions. A total of 173 publications are cited here from this
literature review. The findings from this literature review are reported in detail
by Mee (2013).
2. Delphi Survey
In order to elicit current consensus from veterinarians about both the

criteria and the causes of death in cases of bovine perinatal mortality
internationally two groups of veterinarians [subject matter experts (SME) and
non-SMEs] were contacted in a Delphi survey in 2012. The SMEs were
selected on the basis of their scientific publications or experience of working
in a veterinary diagnostic or research laboratory in the area of bovine perinatal
mortality.
The non-SMEs were self-selected as cattle veterinarians without particular
expertise in bovine perinatology. A total of 74 veterinarians (46 SMEs and 28
non-SMEs) from 23 countries responded. The study was conducted using
Delphi methodology over seven rounds. Respondents were asked to agree the
causes of bovine perinatal mortality and for each cause to agree the supporting
diagnostic criteria. The findings from this study are reported in detail by Mee
et al., (in press).
3. Necropsy Study
A prospective, longitudinal, active surveillance necropsy study was

carried out in 30 Irish dairy herds over three years (2010-2012) by the author.
Herd- and animal-level epidemiological data were collected and complete
necropsy examinations, including gross pathology, histopathology,
bacteriology, serology and virology, were carried out on 680 carcasses from
foetuses and calves which died before, during or within 48 hours after calving
following a gestation period of at least 260 days. For cases of indeterminate
gestational age (e.g. unrecorded natural services) parity and fetal plurality-
adjusted birth weight was used as a surrogate criterion using the third
percentile (mean-2SD) as the lower inclusion limit (depending on the dam and
sire breeds and whether the calf was a singleton or a twin); the same principle
used by the WHO to define human perinatal mortality cases (Lawn et al.,
2011).
Data from an independent dataset where gestation length and birth weight
were recorded were used to establish the variation in birth weight of full-term
calves (Table 5). For Jersey or Jersey x cows mated to Jersey or Jersey x bulls
an inclusion threshold of >15 kg was used for singletons or twins.
For Jersey or Jersey x dams or sires mated to non-Jersey or Jersey x dams
or sires, respectively, (i.e. only the dam or the sire was Jersey or Jersey x, not
both) an inclusion threshold of >20 kg was used for singletons or twins. For
other dairy breed dams (non-Jersey or Jersey x) mated to other dairy sires
(non-Jersey or Jersey x) or beef sires, inclusion thresholds of >25 and >20 kg
were used for singletons and multifetal pregnancies, respectively.
All necropsy information was recorded by the same prosector (the author)
on a dictaphone and photo-documentation of lesions was carried out as the
case indicated. The findings from this study are reported in detail by Mee
(2013).
When the results of the literature review and the Delphi survey responses
were applied to the necropsy database the causes of death were ranked in order
of individual cause incidence, i.e. where more than one cause of death was
recorded for a calf (combination cause of death category) both were included
in the individual cause of death incidence database.
Table 5. Birth weights (kg) (mean, mean+2SD, range), gestation length

(days) and number of records for fullterm (260-300 days), singleton
(n=10,422) and twin (n=615) calves from nine Teagasc research dairy
herds over a twenty year period (1991-2011)
Singletons Twins
Sire genotype
Mean+2S
Mean+2S
Gestation
Gestation
genotype
Mean
Mean
Min.-
Min.-
Max.
Max.
Dam
No.
No.
D
Jersey, Jersey, 16.54- 21.8 10.92- 284.6

26.21 200 14-45 281.15 6 15-30
JerseyX JerseyX 35.88 3 32.74 6
Jersey, Jersey,
20.31- 26.6 22.04- 277.8
JerseyX or JerseyX or 32.63 919 14-51 280.34 32 15-34
44.95 3 31.22 7
dairy dairy
Dairy (excl. Dairy (excl. 29.61- 11 to 34.1 23.18- 277.0
41.84 7,960 281.62 496 18-55
Je, JeX) * Je, JeX) 54.07 76 4 45.1 2
Dairy (excl. 30.86- 35.0 22.45- 278.8
Beef 42.82 1,343 18-63 283.6 81 21-51
Je, JeX) 54.78 7 47.69 6
* Dairy (excl. Je, Jex) = Holstein-Friesian, Friesian, Friesian x, Ayrshire, Norwegian
Red, Norwegian Red x, Swedish Red, Swedish Red x, Montbeliarde,
Montbeliarde x, Normande, Normande x; Beef = all recorded beef breeds.
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12 John F. Mee
The causes of death with an incidence >5% were assigned individual

categories and the other causes of death were aggregated into an ‘other
specific disorder’ category. Following completion of these iterations the
classification system was refined for each cause of death and its sub-
categories, with each criterion contributing to a certain, probable or possible
cause of death. Certain referred to a condition which unequivocally was the
cause of death, probable referred to a condition which with high likelihood
caused death and possible to a condition which with reasonable certainty was
involved in a pathophysiologic sequence that led to death.
RESULTS
Causes of Perinatal Mortality in 680 Dairy Calves
When the causes of death were originally classified following the

Necropsy Study (Mee, 2013) the three most common causes of death were: a
combination of causes of death, dystocia and eutoxia. When the combination
cause of death category was disaggregated the three most common causes of
death were dystocia, lethal congenital defects and eutoxia (Table 6).
Definitions of Cause of Death
The cause of death was assigned using the Literature Review, Delphi
survey and the Necropsy Study (written history from the farmer, the gross
necropsy observations and the laboratory tests), i.e. an algorithmic, summary
diagnosis.
This is a foeto-maternal clinicopathological classification system. The
main cause of death indicates the pathological condition of the fetus or calf
which made the greatest contribution towards the death (ESRI, 2012). Only
proximate (immediate) factors are listed in the cause of death, e.g. a genetic
mutation may be the ultimate cause of a lethal congenital defect but the defect
was the proximate cause of death. Some cause of death, e.g. dystocia, are
disaggregated in order to differentiate separate components (where a novel
portmanteau is used, e.g. dystoxia) which can be re-aggregated as necessary
for different reporting formats. The causes of death are assignable,
presumptive, mutually exclusive causes of death based on the evidence
available on the factors which contributed to death in each case. Differential
diagnoses of cause of death are reached through both processes of inclusion,

e.g. detection of a significant lesion, and of exclusion, e.g. absence of
diagnostic criteria – unexplained perinatal mortality. The causes of death can
be used to calculate cause-specific mortality rates (CSMR) and the attributable
fraction (AF) of PCM due to each cause of death.
Table 6. Prevalence of individual * causes of perinatal mortality

(in alphabetical order) in 680 dairy calves over three years (2010-2012)
Cause of death % of calves Rank

Congenital defect 20.3 2
Dystocia 51.6 1
Eutoxia 14.0 3
Haemorrhage or Anaemia 8.1 7
Infection 12.2 4
Iodine imbalance 6.5 9
Other specific disorder 7.5 8
Premature placental expulsion 12.1 5
Prematurity 9.4 6
Unexplained 12.2 -
* combination of causes of death category is disaggregated so % figures do not add up
to 100%.
Following sequential aggregation of these three primary sources of

information (literature review followed by Delphi survey followed by
necropsy results) ten major causal categories of death were assigned with sub-
classification as required; alphabetically –combination of contributory factors
(more than one cause of death), congenital defect (economically lethal and
lethal), dystocia (bradytocia, traumotocia, bradytocia and traumotocia,
dystocia anamnesis, dystoxia and fetal maldisposition) eutoxia, haemorrhage
and anaemia (external omphalorrhagia, internal omphalorrhagia, idiopathic
hemoperitoneum, anaemia), infection, iodine imbalance, premature placental
expulsion, prematurity and other specific disorders (e.g. accidental death,
hypothermia, intra-uterine growth retardation, etc.). These 10 causes of death
are defined hereunder in alphabetical order along with their sub-classifications
and brief commentaries.
1. Combination of Contributory Factors

Multiple causes of death are diagnosed in the same calf. Hence, if a lethal
congenital defect was diagnosed along with an infectious cause of death both
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14 John F. Mee
were combined into the combination cause of death category as it is not

always possible to assign which is the actual cause of death. This category
includes certain, probable and possible causes of death depending on the
combination involved.
2. Congenital Defect (Lethal and Economically-Lethal)

Grossly visible structural defects including lethal congenital defects
recorded by body system such as hydrocephalus, hydranencephaly, and
economically-lethal congenital defects (necessitating euthanasia) such as anal
atresia, intestinal atresia (Figure 1), (Mee and Kennelly, 2010), enterocoele,
omphalocoele (Mee, 1994), vestigial limbs, severe arthrogryposis (Leipold et
al., 1993), anasarca, severe cardiac defects, central nervous system defects
(Cornillie et al., 2004), palatoschisis, chondrodysplasia (Mee, 1995), or
combinations of these lethal defects, but not exclusively this list. Where
diagnostic facilities exist, this category also includes non-visible/occult lethal
congenital defects such as metabolic storage disorders, e.g. citrullinaemia.
This category includes certain and probable causes of death depending on the
defect.
3. Dystocia
The term dystocia is used to mean a difficult or abnormal calving (Hafez,
1980) encompassing traumotocia, bradytocia, traumotocia and bradytocia
combined, dystocia anamnesis, dystoxia and maldisposition in calves which
died during or after birth; each of these sub-classifications is defined below.
Traumotocia: severe antemortem lesions (haemorrhage at the lesion site)
consistent with iatrogenic (resulting from the action of the farmer or veterinary
practitioner) parturient trauma. For example, fractured spine/vertebral luxation
(Figure 2) (Agerholm et al., 1993), fractured ribs (costal and costo-chondral
junctions) (Schuijt, 1990), fractured mandible (Trent and Ferguson, 1985),
limb fractures (Ferguson et al, 1990), moderate and severe subcutaneous
thoracic and limb haemorrhages/bruising, haemoarthrosis, hepatic or renal
rupture, moderate and severe haemoperitoneum (Waldner et al., 2010),
diaphragmatic hernia (excluding hiatus hernia), (SAC, 2012a) or polytrauma.
These lesions were detected in calves born at assisted calvings (iatrogenic
trauma) with (traumotoxia – trauma and anoxia combined in the same calf) or
without anoxic lesions or subcutaneous bruising at site of calving ropes
placement on legs, and without bradytocia. This is a certain or probable cause
of death.
Figure 1. Atresi jejuni (type 1) showing marked distension of the proximal jejunum
with meconium (economically-lethal congenital defect).
Figure 2. Fractured spine at the thoraco-lumbar junction with extensive haemorrhage

(traumotocia).
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16 John F. Mee
Figure 3. Marked capital and lingual swelling due to subcutaneous oedema

(bradytocia).
Bradytocia: moderate or severe subcutaneous antemortem oedema (e.g.

legs, tongue, capital, cervical; Figure 3); prolonged stage two of calving;
Everett-Hincks et al., 2007, Khodakaram-Tafti and Ikede, 2005, Gee et al.,
1989), (excluding serosanguinous subcutaneous oedema following death and
retention in utero) with or without a written anamnesis of prolonged stage one
of calving (e.g. uterine inertia, milk fever/clinical hypocalcaemia, ‘slow
calving syndrome’, disturbance during calving, incomplete cervical dilatation,
uterine torsion; Collery et al., 1996), calving assistance score >3 (0-5 scale) or
anoxic lesions (bradytoxia) and without traumotocia. This is a probable cause
of death.
Traumotocia and bradytocia: combination of traumatic and bradytocic
lesions with calving assistance score >2 (0-5 scale), with or without anoxic
lesions. This is a certain or probable cause of death.
Dystocia anamnesis: history of a difficult calving [assistance score >3 (0-
5 scale)], (Collery et al., 1996), (without maldisposition, traumotocia,
bradytocia or dystoxia) or other abnormal calving history, e.g. uterine torsion,
uterine rupture. This is a probable or possible cause of death depending on the
anamnesis.
Dystoxia (dystocia with anoxia): calving assistance score >3 (0-5 scale),
with at least two locations of moderate or severe anoxic lesions. For example,
meconium stained hair coat or in lungs (Collery et al., 1996, Schefers, 2009,
Alonso-Spilsbury et al., 2005), ecchymotic (3-10 mm) or suffusive subserosal
haemorrhages on internal organs, e.g. tracheal mucosa, heart (epicardium,

endocardium), pleura, thymus, adrenal glands, sclera (Gavin and Zackery,
2011, Hey et al., 1986) or meningeal congestion (Dufty and Sloss, 1977,
Haughey, 1991). These lesions were detected in the presence or absence of
gingival cyanosis (Collery et al., 1996) and without traumotocic or bradytocic
lesions (Salihagic-Kadic, et al., 2006). This is a certain or probable cause of
death depending on the extent of the calving difficulty and lesions.
Maldisposition: Fetal mis-alignment (malpresentation, malposition or
malposture, entwined/co-presented twins) with a calving assistance score of >2
(0-5 scale), in the absence of traumotocia, bradytocia or anoxia (Collery et al.,
1996). This is a certain, probable or possible cause of death depending on the
maldisposition and degree of calving difficulty.
4. Eutoxia (Eutocia with Anoxia)

Calving assistance score <2 (0-5 scale), with at least two locations of
moderate or severe anoxic lesions [meconium stained hair coat or in lungs,
ecchymotic subserosal haemorrhages on internal organs, e.g. tracheal mucosa
(Figure 4), heart (epicardium, endocardium), pleura, thymus, sclera, adrenal
glands or meningeal congestion (Figure 5)] in the presence or absence of
gingival cyanosis and in the absence of dystocia (e.g. traumotocia, bradytocia,
maldisposition). Synonyms for this category of mortality include anoxia of
unknown origin, non-visible dystocia (e.g. non-visible delayed stage one of
calving) and idiopathic anoxia. This is a probable or possible cause of death
depending on the extent of lesions.
5. Haemorrhagic and Haematological Disorders

This category refers to haemorrhage and anaemia in or from the foetus or
perinate with the following sub-classifications.
Internal omphalorrhagia: moderate or severe haemoperitoneum or severe
peri-umbilical arterial haematoma (Figure 6) with at least one unsealed
umbilical artery in the absence of trauma or other source of haemorrhage
(Vanholder et al., 2001, Rademacher, 2006). This is a certain cause of death.
External omphalorrhagia: moderate or severe blood staining of the hair
coat from the umbilicus with anaemia and at least one unsealed umbilical
artery in the absence of hemoperitoneum, severe peri-umbilical arterial
haematoma and trauma with or without blood-staining of the calving site
(Meydan et al., 2009, Kamimura et al., 2001, Bentinck-Smith et al., 1960).
This is a probable or possible cause of death depending on the extent of
haemorrhage.
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18 John F. Mee
Figure 4. Extensive haemorrhage in the tracheal submucosa (anoxia).
Figure 5. Severe meningeal congestion (anoxia).

Figure 6. Severe bilateral peri-umbilical artery haematomata (internal omphalorrhagia).
Figure 7. Marked pallor of the entire carcass (anaemia).
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20 John F. Mee
Hepatic rupture associated-haemoperitoneum: moderate or severe

haemoperitoneum with subcapsular hepatic rupture in the absence of
omphalorrhagia and trauma (idiopathic hepatic rupture, e.g. hypovitaminosis
E; Green et al., 1995). This is a certain cause of death.
Idiopathic haemoperitoneum: moderate or severe haemoperitoneum in the
absence of omphalorrhagia, hepatic rupture or trauma (e.g. rupture of the aorta
or gastrointestinal vessel mesentery complex or severed vessels in enterocoele
or kidney; DAFM, 2011a, possible bacterial infection: VLA, 2010 or melaena,
SAC, 2012b). This is a probable or possible cause of death depending on the
extent of haemorrhage.
Anaemia only: severe anaemia [pallor of conjunctiva and at least three
other organs, e.g. skeletal muscles, thymus, tracheal mucosa, brain, liver,
heart, lungs or kidneys, (Figure 7)] with or without gingival pallor in the
absence of haemoperitoneum, omphalorrhagia, hepatic rupture or other source
of haemorrhage or trauma (e.g. BVDv infection; Bell, 2011, twin-to-twin
transfusion; WHO, 2005, neonatal isoerythrolysis; Dowsett et al., 1978,
anaemia of unknown origin; SAC, 2011a, Ogata et al., 1999). This is a
probable or possible cause of death depending on the extent of anaemia.
6. Infection
Examples of prenatal (congenital) and postnatal infections are detailed
hereunder though other foetopathogens may also be listed depending on their
relevance nationally, e.g. Coxiella burnetii, Mycoplasma/Ureaplasma,
Parachlamydia, Bluetongue virus, Schmallenberg virus, etc...
Bovine herpes virus-1: demonstration of viral antigen (e.g. isolation, PCR;
DAFM, 2011b), presumptive histopathological lesions (e.g. nonsuppurative
focal hepatic necrosis; Kirkbride, 1992) or antibodies (eg. ELISA positive
titre, excluding weak positive/ inconclusive titres) in fetal blood where the calf
had not consumed colostrum. This is a probable or possible cause of death
depending on the detection of lesions/antigen or antibodies, respectively.
Bovine viral diarrhoea virus: antigen detected in fetal tissues (e.g. ear,
spleen, lungs, thymus) or blood (e.g. by PCR, AG-ELISA or virus isolation;
Graham et al., 2009, Muskens and Vos, 2008) preferably with gross or
histopathological lesions. This is a certain, probable or possible cause of death
depending on the supporting evidence from lesions.
Leptospira serovar Hardjo: detection of the bacterium (e.g. PCR or
immunofluorescence; Smyth et al., 1999, Collery et al., 1996) or antibodies
detected in fetal blood (e.g. ELISA, MAT, Immunocomb) where the calf had
not consumed colostrum. This is a probable or possible cause of death

depending on the detection of antigen or antibodies, respectively.
Neospora caninum: demonstration of antigen (e.g. IHC), detection of
presumptive histopathological lesions (e.g. encephalitis, myocarditis) or
detection of antibodies (positive titre, excluding weak positive/inconclusive
titres) in fetal blood (e.g. ELISA, indirect fluorescent antibody test; Graham et
al., 1996) where the calf had not consumed colostrum, with or without
neurological clinical signs. This is a probable or possible cause of death
depending on the detection of lesions/antigen or antibodies, respectively.
Primary foetopathogen: Examples include Bacillus licheniformis,
Trueperella pyogenes, Listeria monocytogenes, Histophilus somni, Mann-
heimia haemolyticia, Salmonella Dublin cultured (or detected by PCR) in pure
or nearly pure growth from the abomasal contents/fetal tissues/placenta
(AFBI/DAFM, 2011, AHVLA, 2011a, SAC, 2012c, VLA, 2011), or diagnosed
by microscopy (fungi, e.g. Aspergillus spp.; Kirkbride, 1992) or by
demonstration of toxin (e.g. Clostridium perfringens ELISA; Watson and
Scholes, 2009). For other possible pathogens, e.g. E coli, in addition to
culture-positive results, lesions (gross or histopathological) should be present
(DAFM, 2012a).
Figure 8. Fibrinous pericarditis (infection).
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22 John F. Mee
Because the placenta is frequently contaminated, isolation from the

placenta should be supported by gross or histopathological lesions. This is a
certain or probable cause of death depending on the supporting evidence from
lesions.
Gross or histological lesions: indicative of infection, e.g. pericarditis
(Figure 8), multi-focal necrotising meningoencephalitis, haemorrhagic
emphysematous abomasitis, omphalo-peritonitis, chorio-amnionitis, omphalo-
sepsis, peritonitis, pleuropneumonia, pneumonia, systemic sepsis, pyothorax,
pneumonoenteritis or enteritis, (Waldner et al., 2010, DAFM, 2012b, 2011c,
AHVLA, 2011b). There may or may not be low serum immunoglobulin status
(e.g. Zinc Sulphate Turbidity test value <15 units). This is a certain, probable
or possible cause of death depending on the extent of the lesions.
7. Iodine Imbalance
Histopathologically abnormal thyroid morphology [moderate or severe
microfollicular hyperplasia (Figure 9) or macrofollicular hypoplasia; (‘colloid
goitre’) is the ‘gold standard’ for diagnosis of iodine imbalance in a perinate
(La Perle, 2012). Other findings consistent with iodine imbalance include
absolute goitre (thyroid gland weight >30g; Mee, 1993, Smyth et al., 1996),
(Figure 10) or relative goitre (thyroid gland weight/body weight ratio >0.70;
Knowles and Grace, 2007) usually found with abnormal thyroid morphology,
significant thyroid biochemistry (low iodine content) and associated
pulmonary pathology, e.g. atelectasis (Smyth et al., 1996). This is a probable
or possible cause of death depending on the detection of
histological/biochemical or thyroid weight abnormalities, respectively.
Figure 9. Severe microfollicular thyroid hyperplasia (iodine imbalance).

Figure 10. Absolute goitre (58.3g thyroid with comparator 6.9g thyroid), (iodine
imbalance).
8. Premature Placental Expulsion (PPE)

Calf born with entire placenta attached (Figure 11) based on written
anamnesis (placenta emerged before or with the fetus) or necropsy
observation, with or without visible anoxic lesions (as some foetuses are dead
in utero for some time prior to calving), (Mee, 1991a, Sluijter et al., 1990).
This is a certain cause of death.
Figure 11. Calf with entire placenta attached (premature placental expulsion).
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24 John F. Mee
9. Prematurity
Where gestation length is known, calf is born before physiological
maturity (singletons <270 days and twins <265 days gestation) (Roberts,
1986). Where gestation length is unknown, birth weight is below the breed and
plurality-adjusted range for term calves (Table 5).
Figure 12. Small (24.7kg) 267 day gestation fetus with light hair coat (prematurity).
Where gestation length and birth weight is unknown, at least two of these
findings: small calf, short light hair coat (Figure 12), partially erupted incisor
teeth (Figure 13), domed skull (in the absence of brain abnormalities) with or
without anamnestic information [respiratory distress syndrome (RDS), muscle
weakness, floppy ears, or delayed reflexes in the calf and/or lack of maternal
udder swelling or pelvic ligament relaxation precalving and/or sudden
unexpected calving preterm].
Though the underlying cause of the premature birth may or may not be
diagnosable, this is a probable or possible cause of death depending on the
degree of prematurity.
Figure 13. Partially erupted incisor teeth in a 267 day gestation fetus (prematurity).
10. Other Specific Disorders

It is not possible to be exhaustive in including all possible causes of death
in separate categories so a heterogeneous category was created to record other
uncommonly assigned causes of death (<5% individual cause of death
incidence). Examples include placentitis (Waldner et al., 2010), hyper-
thermia/heat stress (Yates et al., 2012), neoplasia (Kirkbride, 1992),
hyposelenosis/myocardial myopathy (Waldner et al., 2010, Murray et al.,
2008, Siguroarson et al., 2008), intoxications, for example nitrate toxicity
(‘blue baby syndrome’), (Ozmen et al., 2005, Johnson et al., 1994), uterine
haemorrhage, hormonal imbalances (Sorge et al., 2008), maternal endotox-
aemia (Kirkbride, 1992) and maternal euthanasia/death (Waldner et al., 2010),
accidents (DAFM, 2011d), hypothermia (Olson et al., 1980, 1981), IUGR
(Ogata et al., 1999) and iatrogenic causes. This is a certain, probable or
possible cause of death depending on the specific disorder.
In the necropsy database analysed here the following three causes of death
occurred individually in approximately 4% (accident), 1% (hypothermia) and
3% (IUGR) of cases.
Accidents
Two sub-classifications are included in this category.
Non-parturient trauma: death caused by being stood on or attacked by
cow (assault injury) or injured in the calving environment, e.g. by automatic
passage scraper in cubicle/freestall house. Diagnosis based on written
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26 John F. Mee
anamnesis and traumatic lesions, e.g. fractured ribs and haemothorax (Figure
14), (DAFM, 2011d), exsanguinations arising from hepatic rupture (DAFM,
2012c), usually in the absence of subcutaneous bruising (Munro and Munro,
2011) and in the absence of iatrogenic traumotocia. This is a certain, probable
or possible cause of death depending on the history and lesions detected.
Colostrum aspiration: death due to administration of colostrum by oro-
oesophageal tube. Diagnosis based on written anamnesis (history of failure to
suck, ‘stomach-tubing’, dyspnoea, weakness, depression, and recumbence) and
presence of colostrum in the trachea and bronchial tree, pulmonary oedema
and congestion and focal pulmonary consolidation. Note some calves die
before pneumonia develops. If they survive long enough a diffuse
suppurative/necrotising bronchopneumonia, particularly of the apical lobes,
develops with foreign basophilic material and bacterial colonies in the airways
(DAFM, 2012d). This is a certain or probable cause of death depending on the
history and lesions detected.
Hypothermia
History of extreme cold weather (ambient temperature close to 0oC, high
wind speed, rain/sleet/snow, i.e. wind chill factors), unobserved calving, and
calf not born into a straw bed (e.g. born in the cubicle/freestall house
passageway + pushed out by automatic scrapers, un-bedded tie-stall or
outdoors) and not dried off (wet or faeces-covered coat; abandoned by dam),
combined usually with distal limb subcutaneous haemorrhages and oedema,
particularly of the hind limbs (Olson et al., 1980, 1981, Haughey, 1973) and
no voluntary colostrum intake (abomasum containing mucus only). This is a
probable or possible cause of death depending on the history and lesions
detected.
Intrauterine Growth Retardation (IUGR)

Abnormally low breed and plurality-adjusted body weight in the third
percentile (<mean-2SD kg), (Table 5) in a full-term (>95% of gestation length,
i.e. not premature) calf (Richardson, 1978), (Figure 15). For example, a body
weight of 20kg or less and a gestation period of 275 days or more was used by
Ogata et al., (1999) to diagnose IUGR in Japanese Black stillborn calves.
Synonyms for IUGR include small for gestational age (SGA) and dysmature.
Possible causes include acute (e.g. summer mastitis; Richardson and Terlicki,
1980) or chronic maternal systemic infection or debilitating disease with or
without placentitis (e.g. Bacillus licheniformis, paratuberculosis; Scott, 2011,
Bluetongue virus; Richardson et al., 1985) and maternal undernutrition (Wu et
al., 2009). As these underlying causes are often difficult to differentially

diagnose in the fetus, IUGR is a possible cause of death.
Figure 14. Severe haemothorax after the dam kneeled on her calf (accidental non-
parturient trauma).
Figure 15. Abnormally small (12.2kg) for date full-term (289day) fetus (intrauterine
growth retardation).
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28 John F. Mee
Table 7. Causes of death, listed alphabetically, categorised by potential

lethality (certain, probable and possible)
Cause of death Levels Certain Probable Possible

Combination Multiple   
Congenital defect Multiple   
Dystocia Traumotocia  
Bradytocia 
Traumotocia and bradytocia  
Dystocia anamnesis  
Dystoxia  
Maldisposition   
Eutoxia  
Haemorrhage and
Internal omphalorrhagia 
anaemia
External omphalorrhagia  
Hepatic-rupture-haemoperitoneum 
Idiopathic-haemoperitoneum  
Anaemia  
Infection Antigen detected 
Lesions diagnosed   
Antigen and lesions  
Antibodies detected 
Antibodies and lesions 
Iodine imbalance Histopathology 
Goitre (absolute/relative)  
Histopathology and goitre 
Low thyroid iodine 
Premature placental

expulsion
Prematurity  
Other disorders Non-parturient trauma   
Colostrum aspiration  
Hypothermia  
IUGR 
Certain, Probable and Possible Causes of Death
The classification of causes of death into certain, probable and possible

causes of death is illustrated in Table 7. Given the complexity of bovine
perinatal mortality, it is not possible to be prescriptive in each and every case
of death so these severity bands are merely categorical guidelines indicating
the potential lethality of each cause of death. In the final analysis, the ten
causes of death may be grouped into certain (PPE), certain or probable

(congenital defect), probable or possible (eutoxia, iodine imbalance,
prematurity) and certain, probable or possible (combination cause of death,
dystocia, haemorrhage or anaemia, infection, other specific disorder)
depending on the circumstances and findings in each individual case.
Unexplained Perinatal Mortality
If none of the criteria above are met following thorough epidemiological,

clinical and necropsy investigations the cause of death is undetermined. This is
a diagnosis of exclusion in the absence of assignable cause of mortality;
‘idiopathic perinatal mortality or unexplained stillbirth’. Examples of findings
include death in utero of unknown origin (autolysed foetus), an anamnesis of
eutocia only with normal fetal alignment, multifetal pregnancy only, nonlethal
congenital defects, minor pathogens isolated from abomasal contents (e.g.
Streptococcus spp., Staphylococcus spp., Bacillus spp., Gardanellera spp. or
mixed bacterial growth), sparse anamnesis (e.g. calf found dead) or grossly no
visible lesions (NVL) at necropsy. In some cases it may not be possible with
routine diagnostics in veterinary laboratories to detect the cause of death, e.g.
karyotypic abnormalities and inborn errors of metabolism. In other cases the
absence of the placenta may hinder diagnosis, e.g. placentitis.
DISCUSSION
The classification system developed here seeks to establish what went
wrong, not necessarily why. It does not necessarily identify the underlying risk
factors associated with the cause of death (Mee et al., 2008). It is novel in
accepting more than one cause of death in the same calf as multiple causes of
death are common in bovine perinatal mortality. While it attempts to establish
the cause of death in an individual perinate these findings, unlike in human
perinatology, need to be interpreted also at the herd-level in order to effect
change in loss rates.
Central to the classification system is a thorough necropsy examination.
While the level of agreement between non-necropsy and necropsy-based
diagnosis can be high for some other conditions, e.g. bloat and respiratory
disease (Anspaugh et al., 2010), this is not necessarily the case in perinatal
mortality. For example, in one study verbal autopsy under-diagnosed IUGR
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30 John F. Mee
and prematurity in human perinates (Marsh et al., 2003) and, in another,

autopsy led to a change in diagnosis in 13% and additional findings in 26% of
human perinatal deaths (Cartlidge et al., 1995). Infection and congenital
defects were most commonly under-diagnosed in the latter study. In an earlier
study autopsy was the only means of establishing a cause of death in 26% of
human perinatal deaths when compared with clinical assessment (Meier et al.,
1986). Similar studies have not been published for calves. However, adoption
of routine all-carcass necropsy examinations has been proposed as an essential
procedure to encourage preventive medicine amongst farming clients (Lester,
1987). In addition to the findings from a gross necropsy examination, for some
disorders additional laboratory tests are essential for diagnosis, e.g. infections.
While a necropsy is essential to this classification system so also is the
clinical history of the circumstances surrounding the calf’s death, usually the
calving details. Collection of these details can be difficult in routine
submissions to veterinary diagnostic laboratories as the person submitting the
carcass may not know these details. While for some causes of death this is not
important, e.g. isolation of a foetopathogen with gross lesions, for others, e.g.
hypothermia, this information is critical. Thus this is a clinico-pathological
classification system relying on both strands of information to assist in
diagnosis.
The depth of diagnostic investigation employed for each case of perinatal
mortality often depends on the reported incidence of the problem at a herd-
level. Thus if only a single case is submitted and only a single case has
occurred some diagnostic tests may not be applied without supporting
evidence, e.g. testing of body fluids and organs for multiple infections. But
where such evidence exists, further analyses are conducted. Where a herd
problem is presented more extensive investigation will be carried out.
In drawing up this list of causes of death and the criteria used to assign
same there were many alternative causes and criteria considered both from the
literature review and in particular the Delphi survey. Hereunder some of the
discussion around these topics is presented for each cause of death
alphabetically.
Congenital Defect
Some congenital defects may not be lethal per se but are ‘economically-
lethal’. For example, a calf born with a cleft palate or a vestigial limb or
arthrogryposis can live but will not survive in an intensive dairy herd and will
be euthanized. These sub-lethal cases were included in this category. While

some congenital defects are easy to define as lethal, e.g. holoacardius
amorphous (Mee, 1990), others are less clear-cut, e.g. intestinal atresia,
because some affected calves can survive following reconstructive surgery
(Azizi et al., 2010). However, they are not independently viable. It is also
accepted that while some calves may be diagnosed with a congenital defect
and die in the perinatal period, e.g. ventricular septal defect, other calves with
this defect may survive longer. These may be described as defects which
significantly compromise viability and a normal productive life. As many
congenital defects are occult, e.g. anencephaly, a necropsy examination is
essential for this diagnosis. No attempt was made to differentiate hereditary
from non-hereditary defects as the ultimate aetiology of many defects is
unclear, particularly multiple defects.
Dystocia
This category is much broader than the traditional definition of dystocia

often used in epidemiological studies, e.g. by Mee et al., (2011), as only a
difficult assisted calving. Here it encompasses traumotocia, bradytocia,
traumotocia and bradytocia combined, dystocia anamnesis, dystoxia and
maldisposition. In this way two of the most common diagnoses in perinatal
mortality, anoxia and dystocia can be combined (dystoxia) whereas anoxia
associated with eutocia is categorised separately (eutoxia). Similarly, different
types of dystocia, e.g. bradytocia and traumotocia, which commonly occur
together do not need to be differentiated but can be coded as a separate sub-
class. Calves presented with a history of difficult or prolonged calving but
without traumatic lesions are included here also as these are not uncommon
findings. This can occur where a mechanical calving aid has not been used or
where calving has been unduly prolonged and the fetus dies in utero. In such
cases dystocia (abnormal calving) is present but traumatic lesions may not be
present in the calf. Many such cases have supporting clinical information such
as an oversized calf, vaginal lacerations or a downer cow. It was not possible
to be prescriptive about the duration of a prolonged calving as the frequency of
observations is so variable and the observable signs of the onset of calving are
also highly variable between animals.
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32 John F. Mee
Eutoxia
Eutoxia may be caused by utero-placental circulatory disturbances (e.g.

prolonged period of uterine contractions), placental insufficiency (e.g. partial
separation, placentitis, and dysfunction), umbilical cord disorders (e.g. torsion,
compression, entanglement, stretching or premature rupture) or maternal
conditions (e.g. anaemia, incomplete cervical dilatation). Pathological lesions
associated with anoxia have been recorded in experimental animal models
(e.g. Raju, 1992, Haughey, 1980, Dufty and Sloss, 1977, Glastonbury, 1977)
and in numerous observational studies (e.g. Muskens and Vos, 2008, Alonso-
Spilsbury et al., 2005, Gill, 2001, Collery et al., 1996, Smyth et al., 1992).
These lesions include meconium staining, ecchymotic subserosal haemor-
rhages, visceral or meningeal congestion and gingival cyanosis. These lesions
do not in themselves cause death but are patho-markers for hypoxic-ischaemia
/respiratory and metabolic acidosis and terminal encephalopathy (Buckmann
and Pattinson, 2009). In human perinatology ‘asphyxia’ is diagnosed clinically
from the Apgar score, cord pH and at autopsy from the lesions outlined above
(Becher et al., 2004, Wigglesworth, 1998). Autopsy lesions include cerebral
congestion, congested viscera, visceral haemorrhages and meconium
aspiration (Jezowa and Feit, 2011, Pinar, 2004, Wigglesworth, 1998). In the
case of meconium aspiration syndrome (meconium, squames and keratin
debris in alveoli possibly with mild interstitial pneumonia; Schoon and
Kikovic, 1987) and severe skin meconium staining, this may reflect the onset
of the fetal distress syndrome prior to the onset of stage two of parturition
(Motas-Rojas et al., 2006, Mee, 1991b, Miller, 1988). Although these lesions
occur in cases of perinatal mortality, individually they may have a low
diagnostic sensitivity, e.g. 20% (specificity 85%) for meconium staining (any
degree of) in caesarean-delivered calves (Schuijt, 1992), whether acidotic or
not (Szenci et al., 1989). This indicates that the presence of any degree of
meconium staining alone cannot predict perinatal viability. Similarly, low
sensitivities have been reported for individual anoxia lesions in human
perinates (Becher et al., 2004).
Haemorrhage or Anaemia
Perinatal mortality due to haemorrhage or anaemia is uncommon, and

without necropsy, can be difficult to diagnose clinically, and so is not listed in
some textbooks (e.g. Jubb and Kennedy, 1963). However, numerous examples
of different types of bovine perinate haemorrhage and anaemia have been

reported in the literature, e.g. DAFM, 2011a, Rademacher, 2006, Kamimura et
al., 2001, Vanholder et al., 2001, Ogata et al., 1999. Haemorrhage and
haematological disorders are also listed as a cause of death in other species,
e.g. babies (ESRI, 2012) and lambs (Dwyer, 1991).
Infection
As it is not always possible to be sure when infection occurred, pre-, intra-

and postnatal infections were combined in this category. Additionally, it is not
possible to be definitive about whether the presence of infection caused death,
e.g. BVDv-positive feti can survive to be PI calves, the presence of lesions can
be obscured by autolysis or missed by sub-sampling for histopathology and the
presence of lesions, antibodies or detection of a fetopathogen does not
automatically mean causality. In some cases, e.g. infection with Bacillus
licheniformis, the lesions/organism may be present in the placenta and not in
the fetus and so a negative fetal culture result cannot rule out infection as a
cause of death. For some infections, e.g. Salmonella Dublin, maternal serology
can be useful to predict fetal infection from a single sample with a moderate
degree of certainty (Sanchez, et al., 2011). All infections are not equally
pathogenic and some may interact. There is no consensus on a definitive list of
primary (cause disease as a result of their intrinsic virulence within the healthy
pregnant animal) and secondary opportunistic (cause disease in pregnant cattle
with depressed resistance) fetopathogenic infections. Hence, the need for more
than one piece of evidence of infection when assigning causality. Despite these
limitations, infection is a commonly listed cause of perinatal mortality in all
species, e.g. calves (Muskens and Vos, 2008), babies (ESRI, 2012), lambs,
(Sharpe, 1998) and foals (Smith et al., 2003).
Iodine Imbalance
If dietary iodine imbalance persists for long enough or is severe enough it

will cause hypothyroidism which in turn will lead to thyroid malfunction. This
may cause perinatal mortality via retarded fetal development (pulmonary,
cerebral, and skeletal), reduced surfactant production or impaired
thermogenesis (Grace and Knowles, 2010). For example, in calves hypo-
thyroidism has been associated with goitre, pulmonary atelectasis and fetal
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34 John F. Mee
pneumonia (Smyth et al., 1996), hyaline membrane formation (Grunert et al.,

1992) and increased susceptibility to hypothermia (Vermorel and Vernet,
1985). However, as most of these are non-specific disorders, iodine imbalance
can only be diagnosed in dead calves where thyroid abnormalities are found
(e.g. AHVLA, 2011c, 2012, SAC, 2011b, van Wuijckhuise et al., 2003).
Abnormal thyroid histopathology is considered the gold standard when
diagnosing iodine imbalance in perinates, however, congenital dyshormono-
genetic goitre, though rare, displays similar lesions (La Perle, 2012). Histology
allows differentiation between current and historical dietary iodine imbalance
as goitre persists when iodine deficiency has been corrected (Livesey and
Payne, 2007). There are numerous ancillary tests to diagnose iodine imbalance
(thyroid, plasma, milk or urine iodine content) and hypothyroidism
(thyroxine). Goitre and relative goitre have traditionally been used to diagnose
thyroid malfunction in regions with a high incidence of bovine perinatal
mortality (Jamieson et al., 1945), but, the diagnostic thresholds for both can
vary (e.g. Suttle, 2004, Synge, 1982, Hernandez et al., 1972). In order to
prioritise which glands to sample for histology or iodine content, goitre is
often used as a criterion for further testing (e.g. VIDA, DAFM). However,
goitrous thyroid glands do not always have histological lesions indicative of
iodine imbalance (e.g. due to oedema, haemorrhage or autolysis) and non-
goitrous glands are not always euplastic (Mee, 1993, Smyth et al., 1996).
Given these limitations, abnormal thyroid weight (goitre or relative goitre)
cannot be used alone to diagnose iodine imbalance as a cause of bovine
perinatal mortality. In addition, experimental reproduction of simple iodine
deficiency alone while producing abnormalities in thyroid histology and mass
did not induce stillbirths in selenium-adequate heifers (McCoy et al., 1997b).
But, it is known that the effects of simple iodine deficiency may be compen-
sated by adequate selenium status (Zagrodzki et al., 1998, Mee, 1996). This
suggests that while iodine deficiency alone causes hypothyroidism, other
contributory factors, including possibly the duration and severity of iodine and
selenium deficiency, may be needed to cause iodine deficiency disorders
(Livesey and Payne, 2010). Given these caveats, in clinical veterinary practice
abnormal thyroid histopathology in conjunction with the response to
micronutrient supplementation is often used as diagnostic criteria (e.g. Wither,
1997, Mee et al., 1995, Seimiya et al., 1991, Rogers, 1992). Iodine imbalance
is considered an uncommon cause of death in calves and in other species also,
e.g. in lambs (Dwyer, 1991) and in babies (ESRI, 2012).
Premature Placental Expulsion (PPE)
In many cases the premature expulsion of the placenta may be because of

a delay in expulsion of the fetus and so the placental detachment and expulsion
may not be premature per se but it does precede or accompany fetal expulsion.
This may be induced by factors which do not stop the onset of calving but do
prevent the delivery of the fetus, e.g. uterine inertia or fetal maldisposition
(Mee, 1991a).
However, cases may occur where parturition is not delayed but the
placenta is prematurely separated (abruption) and expelled, e.g. placentitis or
premature/induced calving (MacDiarmid, 1983). This condition is an example
where an anamnesis is critical to diagnosis as although lesions of anoxia may
be found in the fetus they are not always visible and may be obscured by
autolysis where the fetus is retained in utero.
Prematurity
Given the continuum from immaturity through prematurity to maturity

and postmaturity all viability thresholds are arbitrary whether in bovine
(Roberts et al., 1986) or in human perinatology (WHO, 2005) or in other
species.
However, while in humans single ‘genotype’ criteria are used, in cattle
breed-specific gestational thresholds may be needed, though these do not
currently exist across breeds nor would they account for individual fetal
maturity-for-age trajectories.
In cases of indeterminate gestational age, surrogate indices have been
proposed, e.g. birth weight or crown-rump length (CRL). The latter metric is
susceptible to differing measurement techniques which can affect its external
validity and its correlation at term with gestational age is only moderate
(Richardson, et al., 1990).
In addition to these limitations, some premature calves can survive despite
neurological (reduced suck reflex, in-coordination, dullness, dysphagia) and
pulmonary immaturity (RDS) with good nursing care and therapy (Bleul,
2010) but have a higher neonatal mortality rate. Possible causes of prematurity
include pharmaceutically induced parturition, pre-term elective Caesarean
section, pre-natal calf cropping, twinning and infections causing pre-term
calving.
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36 John F. Mee
Other Specific Disorders
While there is a multitude of possible causes of perinatal mortality, many

of these conditions occur at a very low incidence and so they were included in
this heterogeneous category. Some are reliant on a good anamnesis (e.g.
accidents, hypothermia, hyperthermia, maternal toxaemia or euthanasia/death),
recording of fetal body weight and gestation length (IUGR), require
submission of the placenta (placentitis) or have indefinite diagnostic criteria
(e.g. nitrate toxicity, heat stress, hyposelenosis and hormonal imbalances).
While alternative diagnostic criteria can be used, e.g. in calves of indeter-
minate gestational age IUGR can be diagnosed from growth arrest lines in
long bones by radiography; these may have a low yield in stillborn calves
(Smyth and Ellis, 1996).
Classification System Critique
Comparison of the results from this system with those previously

published (Table 3) reveals some interesting findings. Firstly, this system
identified a combination of causes of death as the most common cause of
death category. This is a novel finding and contrasts with the data in the
literature where anoxia is generally the most common cause of death and the
‘other’ category ranks approximately third (Table 3). This difference occurs
because in the present system where another cause of death in addition to
anoxia is diagnosed, e.g. a lethal congenital defect, this is recorded as a
combination cause of death. Another major difference is the increase in the
diagnostic sensitivity in the current system. More causes of death are recorded
here than in most recent published reports where this varies between 3 and 16,
with an average of 6 cause of death categories (Table 4). This allows relatively
uncommon causes of death, such as haemorrhage and premature placental
expulsion to be more ‘visible’ amongst the data whilst not having too many
categories which may render their use confusing or complex.
The higher ranking of lethal congenital defects in this system than in many
previous studies (Table 3) probably reflects the study design (active whole-
herd surveillance) and higher incidence of individual defects (e.g. intestinal
atresia; Mee and Kenneally, 2010) in this dairy cattle population. Hence the
relative ranking of the causes of death reported here may not be valid in other
study designs (e.g. passive surveillance) or cattle populations. This is true for
other reports also where local risk factors affect the causes of death, e.g. a high
incidence of skeletal degenerative myopathy in a Canadian study (Waldner et

al., 2010), a high incidence of IUGR in a Japanese study (Ogata et al., 1999), a
high incidence of micronutrient disorders in an Icelandic study (Hardarson,
2012) and a high incidence of premature calves in heat stress zones
internationally (Yates et al., 2012).
In order to be of greatest use to the end users, i.e. veterinary pathologists,
practitioners and farmers, ideally a classification system will have a minimal
number of cases unexplained (Chan et al., 2004). In the current system less
than 15% of cases were unclassifiable and so were categorised as unexplained.
A comparison with recent studies (Table 3) shows that this figure varies
widely from 0 to 70% with an average of approximately 20%. This indicates
that the present system is slightly better than average, and markedly better in
comparison to some studies, in assigning a cause of death. These figures are
comparable with those in human perinatology (Gardosi et al., 2005). However,
the real value and limitations of this novel system will not be realised until it is
used by veterinarians.
There are many limitations in this novel system. Perhaps one of the
biggest obstacles to its benefits is the current ambivalence of many farmers,
veterinary practitioners and veterinary diagnosticians towards the value of
perinatal necropsy. This results in low carcass submission rates for cases of
fullterm bovine perinatal mortality (Mee, 2008b). In addition, the system does
not include information on placental pathology. Although submission of the
placenta with the dead fetus is best practice this rarely occurs with fullterm
calves, as opposed to aborted feti, and so was not included as a routine
diagnostic specimen. This is a clinico-pathological system which relies
partially on anamnestic information from the farmer or veterinary practitioner
which may be incomplete, unreliable or absent. It does not encompass
advanced diagnostic methodologies for some conditions, e.g. congenital
defects. While such techniques are available for some malformations in some
research or diagnostic laboratories, they are not widely available inter-
nationally. But where they are they will add value to the diagnosis rate.
Similarly, calf carcasses or organs are rarely weighed in veterinary diagnostic
laboratories currently so information on reference body weights or organ: body
weight ratios are not used. This system may encourage targeted weighing of
carcasses or organs where this is integral to better diagnostics.
The ease of use of the system will vary between veterinary diagnosticians
depending on the focus of their work, e.g. a research audit versus a busy
diagnostic laboratory workflow.
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38 John F. Mee
Similarly, inter-observer variability will inevitably exist in criterion

recording, hence the inclusion of exemplar photographic images here to
improve this level of concordance. Taxonomic issues may arise when a
classification system is transposed across language barriers. All of these
limitations will result in some degree of inaccurate assignment of a
classification.
This system will need to be revised, refined and updated based on the
requirements of individual users, possible changes in population risk factors
and the development of new diagnostic techniques. Thus it would be expected
to evolve, similar to the human perinatology classification systems, over the
years.
CONCLUSION
It is concluded from the literature review that currently there is no
published classification system for the causes of death in cases of bovine
perinatal mortality internationally. It is concluded from the international
Delphi survey that the criteria used to define these causes of death are also not
standardised. It is concluded from the necropsy study that the causes of death
in cases of bovine perinatal mortality can be aggregated into ten major causal
categories with sub-classification as required; combination of contributory
factors (more than one cause of death), congenital defect (economically lethal
and lethal), dystocia (bradytocia, traumotocia, bradytocia and traumotocia,
dystocia anamnesis, dystoxia and fetal maldisposition) eutoxia, haemorrhage
and anaemia (external omphalorrhagia, internal omphalorrhagia, idiopathic
hemoperitoneum, anaemia), infection, iodine imbalance, premature placental
expulsion, prematurity and other specific disorders (e.g. accidental death,
hypothermia, intra-uterine growth retardation, etc..). Each cause of death could
be assigned a degree of confidence of diagnosis from certain through probable
to possible. This ten-level classification system can be used to calculate cause-
specific bovine perinatal mortality rates.
ACKNOWLEDGMENTS
The author thanks the veterinarians internationally who contributed
generously of their time to respond to the Delphi survey. In particular, thanks
to Andy Holliman, AHVLA, UK whose enquiries stimulated the preparation
of this manuscript.
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Reviewed by: Andrew Holliman, BVMS, MRCVS.

Animal Health and Veterinary Laboratories Agency, Merrythought,
Calthwaite, Penrith, Cumbria, CA11 9RR, UK.
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Chapter 2
RESETTING PRIORITIES FOR SUSTAINABLE

DAIRY FARMING UNDER
GLOBAL CHANGING
I. Blanco-Penedo1*, J. Perea2, J. O. L. Cerqueira3

and R. Payan-Carreira4
1
Animal Welfare Subprogram, IRTA, Finca Camps i Armet,
(Girona), Spain
2
Departamento de Producción Animal, Facultad de Veterinaria,
Universidad de Córdoba, Campus de Rabanales, Córdoba, Spain.
3
Escola Superior Agrária do Instituto Politécnico
de Viana do Castelo, Portugal
4
Animal and Veterinary Research Center (CECAV),
University of Trás-os-Montes and Alto Douro, Vila Real, Portugal
ABSTRACT
Global change increasingly affected agricultural production and
global community has begun to refocus in a change in livestock
production, defending the use of sustainable strategies. Considerations
with respect to changing environments should also address the dairy farm
systems and new goals have to be designed. Good farming practices
should regard their need for on-going adaptation to an ever-changing
*
Corresponding author e-mail: isabel.blanco@irta.cat.
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54 I. Blanco-Penedo, J. Perea, J. O. L. Cerqueira et al.
environment that should offer solutions for buffering against climatic

extremes, disease epidemics, changing nutrient availability, seasonal
availability of forage and other stresses that will add to an already
heterogeneous environmental condition. Sustainable dairy systems should
be adjusted to these new expectations, and be indeed adapted to the new
agricultural policies and the increasing demands of the consumers for
products free of drug residues (safety) and be more ecofriendly produced.
The key to success is to maximise farm efficiency finding the right
balance between the production system and the management techniques
to maximise the output for food production, involving a suitable dairy
cow biotype, which may trigger new strategies for feeding, breeding and
health control whilst minimising impact on the environment and ensuring
animal welfare and profitability for their business. This chapter book
pretends to present a holistic capture of main issues regarding
management, feeding regimes, breeding, reproductive efficiency with
examples of current sustainable production systems.
1. SUSTAINABILITY IN THE AGROECOSYSTEM

DAIRY FARMING
Today, the dairy sector is among the most industrialised livestock sectors
worldwide. However, marked differences are found between countries and
production areas (IFCN Dairy Report, 2010). In the West, dairy farms are run
in accordance with industrial production models. Competitiveness depends on
increased output and enhanced economic efficiency. This has prompted an
ongoing search for economies of scale, intensification of production,
mechanisation, labour specialisation and rapid technological change (Wilson,
2001).
Developments over the last 100 years have also served to highlight the
real and potential damage to the environment caused by dairy farming (Styles
and Jones, 2007; Sevenster and De Jong, 2008). There is a growing awareness
that the resources on which progress is based are by no means infinite.
Therefore, many difficult decisions have been taken regarding the most
appropriate use of resources in the light of environmental degradation.
Long-term development requires dairy systems to be both economically
competitive and environmentally sustainable. A reductionist view of the issue
would lead to the adoption of “weak” sustainability, which seeks to ensure the
viability of the system by maintaining the total capital stock from generation to
generation. In this approach, economic growth is fully compatible with
Resetting Priorities for a Sustainable Dairy Farming … 55
environmental conservation, since natural capital and man-made capital can

substitute each other through technological progress (Perman et al., 2003).
However, the relationships between the various elements of dairy systems
are considerably more complex. If we agree that uncertainty regarding the
functioning of environmental processes and the risk of irreversibility of
ecosystems outweigh economic efficiency criteria, then we are accepting the
“strong” sustainability approach (Constanza and Patten, 1995), highlighting
the complementarity rather than the replaceability of man-made capital and
natural capital.
The viability is thus based on a complex interaction of two dynamic
systems: the socioeconomic system and the ecosystem. That interaction
involves an ongoing process of coadaptation in which the resilience of the
system as a whole plays a crucial role (Fiksel, 2006). The overall resilience of
a system is the degree to which disturbances can be absorbed or assimilated
into the dynamics of that system. In dairy systems, resilience is associated with
the natural services offered by the ecosystem to the agrosystem, such as the
circulation of nutrients and the supply of water (Grimm and Wissel, 1997).
Any imbalance in these services with respect to the agrosystem requires
external changes to be made in order to ensure that resilience of the system is
maintained.
If a dairy system aim to persist over time, it must also be socially
convenient, i.e. it must provide societal added values apart from the products
themselves (Shreck et al., 2006). The achievement of social sustainability
(Vallance et al., 2011) should passthrough the three main aspects of “what
people need”, “what is good for the environment”, and “what people want”.
The concept of social sustainability was also introduced as a further goal of
intergenerational solidarity, as explicitly demanded by the World Commission
on Environment and Development (WCED, 1988). The concept of
intragenerational equity is concerned with the fair distribution of the costs and
benefits of dairy farming among social actors, whereas intergenerational
solidarity implies the protection – and even the enhancement – of the rights
and opportunities of future generations to benefit from the resources in use
today.
The basic goals of sustainability in agriculture are environmental health,
economic profitability and social equity. Sustainable livestock-farming
practices should therefore be implemented at local scale, through a clear
understanding of the way that agroecosystems work. But at the same time they
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must take into account global issues and future considerations: global
problems require global and local solutions; local problems should be solved
at local level (Van Passel and Meul, 2012).
2. GLOBAL CHANGING AND FARM RESILIENCE

Global change is increasingly affecting agricultural production and
threatening food security. Agriculture is highly exposed to climate change,
which may have an impact on yields, location of production or costs of
production, with potential risks for food supply, agricultural product prices and
farm income (EUROSTAT, 2011). Furthermore, the extent to which the
agriculture is developed is continuously affecting the environment through its
direct impacts on land cover and ecosystems, global and regional cycles of
carbon, nutrients and water (EEA, 2006).
The future sustainable dairy farming systems should pass for a long
running transition to use innovative production methods and emission
reduction measures (Foley et al., 2011). But intervention programs are difficult
to set since links between the natural environment and farming practices are
complex (EUROSTAT, 2011). Pressures and benefits from different types of
agriculture confront the potentiability of intervention programs towards more
sustainable agriculture systems. The dilemma is based on the fulfillment of
different aspects of sustainability by different agricultural scenarios. In one
side, extensification would benefit semi-natural habitats and reduce local
pressures on soil, water and air but increase the area needed for agricultural
production. In contrast, intensification would achieve the opposite but
increases yields and input efficiency and would help to avoid further
deforestation. It can nevertheless harm the environment if it is not properly
managed and lead towards the homogenization of environmental conditions
and further increasing pollution and disturbance of the nutrient cycle. Thus,
the overall situation might still deteriorate (EAA, 2006).
The balance between intensive and extensive farming practices of
grasslands can be roughly assessed by studying livestock densities. High
stocking densities generally involve a risk of nutrient pollution and
overgrazing, and a need to import animal feedstuffs. They are likely to
contribute with more greenhouse gas emissions, as a result of manure
production and enteric fermentation, and may also result in nutrient leaching
into the water and air. At the other end of the range, a low level of livestock
densities may increase the need for industrial fertilisers to be used on
agricultural land or lead to the risk of land abandonment resulting in the loss of
environmental diversity (EUROSTAT, 2011).
In the context of the increasing demand for environmental considerations
and climate change mitigation, the scenario expected to be the mainstream
strategy of future organic dairy production should be accounted. Precision
farming and organic practices, combining crop rotation and non-chemical crop
protection, could increase overall efficiency in terms of land take, water use
and nutrient management. Transforming the major food production areas in
the world into low‑input systems, however, would be a major operation,
affecting productivity and food prices and potentially impacting global food
security.
Down in the scale, fast changing environments should also consider the
farm system. In fact, good farming practices in agricultural systems should
regard their need for on-going adaptation to an ever-changing environment.
Every farm is a complex system, characterized not only by the production
method but also by a large number of farm and management specific aspects.
The aims of a farm system under the resilience concept were to design a site-
specific farm system such that, at all its levels (plant, field, and animals),
would minimize the impact of sources of variation or disturbances, rather than
ruling out the sources of variation (Napel et al., 2006). In this sense, they
should offer solutions for buffering against climatic extremes, disease
epidemics, changing nutrient availability, seasonal availability of forage and
other stresses that will add to an already heterogeneous environmental
condition (Goldringer et al., 2010). Under an adaptation model, these specific
actions could be concretised in herd environment improvement (management,
hygiene, feeding and husbandry) as the precondition to find an acceptable
balance in limiting use of remedies but ensuring the necessary treatments in
the real challenging of farmers and their practicing veterinarians.
3. ORGANIC AND LOW-INPUT FARMING SYSTEMS

Organic and low-input farming systems emerge as a future more resilient
agriculture and a way to treat problems of food production and biodiversity as
one. Organic food and farming systems address, both holistically and
practically, many of the European policies on the sustainable management of
natural resources, the safeguarding of biodiversity and landscapes,
environmental concerns and improved integration of welfare friendly livestock
systems in crop rotations and agroecosystems (Niggli et al., 2008).
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Organic farming is a value-based method of agricultural production. The

values are held in four principles that were articulated by the International
Federation of Organic Movements (IFOAM). Through a worldwide
participatory stakeholder process the values from the pioneers in organic
agriculture were moved to the present time of globalization and extended
growth of the organic sector (Luttikholt, 2007).
Success of organic farming is highly depending on the biodiversity used in
its complex management system and adaptation to this fast changing world.
Dairy farming under the rules of organic farming will always be land-based
due to the requirement that manure production should not exceed 170 kg of
nitrogen per year/ hectare of agricultural area. It implies a maximum stocking
density of two dairy cows per hectare. With the existing standards, organic
dairy farming can be applied in a structure of mixed as well as of specialised
farming. However, various directions of intensification as seen in regular
animal production are not possible because of the four principle standards. But
a trend for a better economy is emerging regarding specialization and increase
of scale (within given standards). De Wit and Verhoog (2007) pointed to the
risk of conventionalization of organic agriculture with such trend, especially
on the Principles of Ecology and Health. The use of off-farm inputs is an
important factor in conventionalization itself and has negative effects of the
core organic values.
4. GREENHOUSE GASES EMISSIONS AND DAIRYING

The main atmospheric gases associated with the ‘greenhouse effect’ are
carbon dioxide (CO2), chlorofluorocarbons (CFC’s), methane (CH4) and
nitrous oxide (N2O). Greenhouse gases (GHG) arise from Agriculture, directly
produced by livestock populations as well as forage together with feed
production processes. Emissions of CO2, CH4 and N2O are all influenced in an
indirect way by intensive production systems (CEAS, 2000). Emissions of
CH4 result from human activities, such as agriculture, and the production and
distribution of oil and gas.
In general, dairying in the EU is becoming more intensive and more
specialised (CEAS, 2000). The dairy sector is aware of its hight impact on the
atmosphere, which arises from de-nitrification, the production of CH4,
ammonia (NH3) volatilisation and CO2. Furthermore, it also involves
emissions to the wider environment of nutrients, heavy metals, and drug
residues such as antibiotics or hormones (Steinfeld et al., 2010; Lesschen et

al., 2011).
For GHG emissions, the dairy farm itself (excluding the non-farming
practices like dairy processing and packaging production) contributes to more
than 80% of the impact for milk, from which about 50% is CH4 from enteric
fermentation, followed by N2O from manure management and nitrous
fertilizers. The third component, CO2 is associated to the use of motors and
electricity production.
Proportion between the different components in GHG emissions at farm
level vary with the system. If methane generation per animal tends to be higher
in low input systems than in those using feed supplements, ammonia emissions
are highest in conventional, intensively managed systems (these occur during
manure storage and application to arable and grassland). In terms of CO2 and
N2O emissions, dairy production has only an indirect impact (mainly the use
of energy to manufacture feed concentrates and to assist forage production as
well as housing systems).
Organic farming may offer environmental protection and benefits through
the less intensive use of land and by providing a changed balance in the use of
inputs. Despite composting, there are no evidences suggesting losses of
methane and ammonia are different from conventional farms (IDF, 2009).
Thus, it remains the need to adopt management practices and technologies that
improve productive efficiency to meet increasing product demand while
minimizing the environmental impact of dairy production. In general, there are
three possible strategies to follow: decrease of energy input; increase of energy
efficiency; and, recycle the energy through biogas production (see de Haan et
al., 1997).
Reducing the relatively high energy input in dairy systems would
contribute to the global goal of reducing the concentration of CO2 in the
atmosphere (Capper et al., 2009). Garnsworthy (2004) found that a high-milk-
producing system with high health and fertility status offers scope with
minimizing CH4 emissions per kilogram of milk, and that this can be achived
by reducing the number of milking herd replacements and the calving interval
length, while increasing the average daily milk yield of the herd. Better
management of slurry and manure involve high capital input to make
structural improvements that will reduce impacts on soil, water and air (CEAS,
2000).
It is not easy to conclude which system has less impact on the
environment. Organic farming does not seem to be better regarding Global
Warming Potential due to the nature of the fodder and the lower productivity
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of cows compared to conventional systems. The type of diets used for

production of organic milk emits a little bit more of methane but there is a
wide variation among studies (IDF, 2009). Regarding the energy use, since
fodder is largely produced on-farm and the use of concentrated feed is limited,
the non-renewable energy used is thus mainly located on-farm. Therefore,
organic dairying generally consumes less energy than conventional farming.
This is mainly due to differences in diet of the cows and the origin of fodder,
as well of the lower use of energy consuming from mineral fertilizer.
The acidification is another damage indicator to take into account. The
emission of acidifying substances per hectare are higher for conventional than
for organic farming, although the acidification potential for 1 kg of organic
milk is higher than for the conventional milk. This is mainly due to the higher
milk yield (kg milk/hectare) in conventional farms. Large quantities of
acidifying substances is small areas occurs at the intensive farming, leading
into high concentrations in the environment that consequently damage the
ecosystem.
There is no clear overall recommendation to be made regarding organic
farming. Research is being conducted on whether to alter cow’s diet to
decrease methane. Life-cycle assessment (LCA) methodology reflects present
research priorities and is related to future legislation and labelling. For that,
newly development impact assessment (water use, land occupation,
ecotoxicology, pressure on biodiversity) are needed to constitute the base of
initiatives to reduce the environment impact of the dairy industry that urge to
be adopted by the necessary stakeholders (IDF, 2009). The farmers would
ensure higher prices by becoming actively involved in other operations
forming part of the value chain, such as distribution and/or small-scale
processing.
5. MANAGEMENT AND FEEDING REGIMES

In organic and low-input systems, it is widely assumed that forage should
be the primary source of nutrients for ruminants (Lund, 2006). Under the new
legislation, the entire organic diet complies with the husbandry conditions that
are expected to improve animal health and welfare (Sundrum, 2001). Which,
however, are not ensured by the standards associated with organic farming per
se (Vaarst et al., 2006). They have to be tested and if a problem is identified, it
has to be solved both for reasons of health and welfare (Link, 2006).
In grazing systems, reducing stocking density may have a positive impact

on dairy cow welfare (Kondo et al., 1989). High stocking densities affect the
cow’s ability to access feeders and lying areas, although housing design also
affects aggression and access to these resources (Niggli et al., 2008).
Under extensive grazing systems, cattle will often synchronize their
behavior; that is, many animals in the group will feed, ruminate, and rest at the
same time (Rook and Huckle, 1995). However the synchronization of
behaviors may be reduced when cattle are housed intensively indoors perhaps
because of competition for space or resources.Thus a trend exists now for
housing dairy cows in freestall barns instead of tiestall barns. Consequently,
cows are no longer fed individually; instead, they are fed as a group with a
total mixed ration (TMR), where forages and concentrates are mixed together,
allowing the producers to incorporate all the required ingredients into a single
ration to meet cows’ nutritional requirements and optimize herd milk
production. However, feeding cows as groups is more challenging because
they can potentially sort feed and individual preferences can lead to cows
eating different diets. In addition, social interactions among cows at the feed
bunk can affect individual cowsteractions s is more challenging becaCurrent
industry recommendations typically advise that each cow have approximately
0.6 m of linear feed bunk space to ensure that all cows can feed simul-
taneously (Grant and Albright, 2001). In addition, type and design of the feed
barrier was shown to influence aggressive behavior between cows while they
were eating (Huzzey et al., 2006). Several management and environmental
factors affect feeding behavior of dairy cows. Increasing feed bunk space per
cow may result in a reduction in displacements of subordinate cows by
dominant cows while eating, in a reduced aggressive behavior among cows
and improved feeding time (DeVries et al., 2004). In contrast, an increase in
feeding competition may reduce intake and increase feeding rate, possibly
increasing the risk for metabolic problems such as left displaced abomasums
and subacute ruminal acidosis.
Meeting Increased Demands of Dairy Cattle under Extensive

Systems
In the EU, dairy production with pasture or rangeland as the primary feed
resource is mostly restricted to specific locations and linked with values like
landscape conservation or rangeland management. All year grazing does occur
in the EU. For example, in the Azores Islands more than 100.000 dairy cows
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pass the day in pasture, year-round, with some concentrate supplementation

when indoors or at milking. On the other hand, there are locations where
pasture does not provide sufficient feed resource for dairy cows.
In organic and low-input dairy systems, the cow must graze grassland
(outdoors) for a considerable period of time during the year. Such production
system is associated with pasture rotations and different agronomic practices,
which need to be coupled with strategies for pasture conservation and
supplementation, as well as stocking rates.
Pasturing of dairy cows during summer is very common in most of the EU
countries, even in the circumstances of intensive farming. But several factors
limit the time that the cows are outside and can graze. Firstly, cows may need
supplementary feeding indoors, to balance their N-rich grass diet and to
provide them with extra energy. Secondly, the growing herd size at a farm
may exceed the required area of grassland available for grazing of all cows,
and supplementary feeding indoors is necessary anyway. Thirdly, mineral
legislation may prohibit the farmer to put as many cows in the field as the
farmer otherwise would do. Fourthly, farmers who apply automatic milking
may prefer keeping their cows inside due to management reasons: for optimal
timing of the individual coweir cows inside due to management(Ketelaar-de
Lauwere et al., 1999).
In contrast to intensive systems, in extensive production systems the
return per unit of input is relatively low. In dairy farming production is linked
to the genetic disposition of the cows deployed for milk production and the
amount and quality of feed that is fed. Grazing systems are typically based on
maximal grazing of the animals during the year, as long as climate and
growing conditions permit. For the remainder period, conserved feed needs to
be available. During grazing periods in summer cows should have access to
sufficient water supply and adequate shelter from sun, wind and rain.
Open discussion may deal with the issue that cows can also benefit from
conditions provided indoors, most notably access to a high-quality diet and
protection from environmental extremes (e.g., heat, cold, and wetness). If both
pasture and indoor housing were provided freely, dairy cows would spend
more time outdoors (summer) and preferred to lie down outdoors in summer
nights and indoors in winter nights, at least under Danish conditions (Krohn et
al., 1992). Unfortunately, the analysis of daily variation in weather has not
been studied so far. Seasonal, pasture based systems of milk production will be
of crucial importance in the future of sustainable dairy farming. If managed
adequately, these systems guarantee a highly efficient and environmentally
friendly conversion of forage into milk, low use of concentrate supple-

mentation, high standards of animal welfare and elevated consumers’
acceptance.
6. ANIMAL HEALTH AND WELFARE CONCEPTS

ON ORGANIC DAIRYING
The regional intensification of animal production has led to more risks of

environmental damage and to increased risks for animal and human health. In
some extent, the regional agglomeration stimulated the development of
vaccines, antibiotics, new technologies and herd health programmes in
response (Steinfeld et al., 2010). In fact, diseases and outbreaks and zoonotic
threats are more present and environmentally affected. Simultaneously, the
risks for lower economic gains and lesser genetic diversity do exist.
To improve the sustainability of dairy production it is essential to establish
practices to reduce medicine use, whilst safeguarding or improving herd health
and productivity. Thus, the reduction in the use of chemical and the
improvement of animal welfare is a common wish to reduce medication in
organic animal husbandry (Vaarst et al., 2001). Under organic farming
regulations, many of the conventional medical prophylactic measures
associated with animal health control are either prohibited or restricted. The
EC Regulation (2092/91 or 505/2012) on organic production specifies that
disease prevention should be based on management systems that promote
resistance to disease and recovery from infection, adapting the requirements to
each species.
By consequence, animal health has been identified as a priority area for
organic research. Previous studies on the animal health status of organic dairy
cows have primarily focussed on areas where organic regulations may have
most impact (Rutherford et al., 2009). Difficulties in methodology appeared
when comparing organic and conventional farms. Comparative studies were
mostly based on official health records where good records are available only
for the most easily diagnosed diseases (Valle et al., 2007); and make
production system comparisons will be also dependent of the health indicators
in use. Furthermore, potential different treatment schemes by production
system might happen.
Over time, questions regarding health in organic farms have moved
beyond the focus under a systemic approach. There is a requirement to assess
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current organic methods of animal health care and to identify practical

constraints and critical points in their application.
Studies of health and health handling on organic dairy farms are scarce. It
seems that main problems in descending order are: mastitis, fertility disorders,
and hoof diseases whereas metabolic disorders such as acetonaemia and milk
fever are less frequent (Krutzinna et al., 1996). The role for the immune
system in the incidence of such diseases is not truly highlighted but it is
currently accepted that organic farming promotes the development of a more
competent immune function, particularly if selection for disease resistence is
implemented on animal selection.
There is only a limited amount of research in the area, but the reduction in
the use of chemically allopathic treatments is part of the leading ideas in
organic livestock production. Within organic dairy farming, there is a great
interest on preventive strategies, earlier detection of diseases and treatments of
diseased animals at an early stage. The implementation of these steps is
expected to result in more favourable clinical outcomes and less antibiotic
usage.
The majority of antimicrobial drugs are used for udder treatments (during
lactation and combined with drying off; Menéndez Gonzalez et al., 2010),
since mastitis is one of the most frequent health problems in dairy cattle,
causing heavy economic losses in conventional dairying (Aeberhardt et al.,
1997; Stärk et al., 1997). Advances made on this field are also of interest to
reduce mastitis incidence as it represents more than two-thirds of antibiotic use
in organic farms (Wagenaar et al., 2011), in particular if Holstein genetics
(which is higly predisposed to clinical mastitis) is used. Also, the negative
reflexes of udder diseases over the herd economy are relatively higher in
organic than in conventional systems.
Again, based on the organic principles the organic dairy production should
promote cow health and welfare. In this context, the use of robust cows well
adapted to the organic farm is pursuit. Cow robustness can be defined as the
cow´s ability to function well within a particular system, and this is reflected
by its longevity. So, the longevity is a reflection of the cow´s ability to avoid
being culled.
Resulting from its standards organic farming may have a positive impact
on animal welfare, as it includes a broad range of practices complying with
maintaince of healthy livestock under the high standards of welfare demands.
Recent interest in farm animal welfare focused more on pain or distress
experienced by animals under “unnatural” conditions, with limited space and
limitations on the full expression of natural behaviour, including social
interactions (Weary and von Keyserlingk, 2009), even if animal welfare goes
beyond such concept. Combating overpopulation and ensuring a minimum of
animal load per area, along with the imposition for grazing for a minimal
period over the year, organic dairy systems provide a number of welfare
benefits: cows have access to a more natural environment, they can perform
behaviors that may be important to them such as grazing (Krohn, 1994), and
cows on pasture sometimes experience a lower incidence of diseases such as
mastitis (Washburn et al., 2002) and lameness (Hernandez-Mendo et al.,
2007).
Nevertheless, cows in pasture-based systems can still suffer from poor
welfare. Furthermore, non-regulated aspects of organic farming, such as the
accepted ways of feeding and management, could restrict aspects of genetic
selection towards a more “sustainable” biotype. Assessments of welfare on
farm ought to include measures of the system and measures of how the system
affects the animals (Rushen and de Passillé, 1998).
The assumption that grass-based systems have an advantage over other
systems simply because cows are better adjusted to grazing needs to be
confirmed. In fact, they can still suffer from poor welfare. Furthermore, animal
biotype and genetics would solely generate a great variation under grazing
conditions. The majority of the existing research comparing the welfare of
dairy cow indoors and at pasture has focused on single indicators of animal
welfare (e.g. behaviour, O’Connell, 1991) or health (e.g. mastitis, Washburn et
al., 2002). It is mandatory to use a wide range of indicators simultaneously for
a comprehensive evaluation of a production system (e.g. Broom et al., 1995).
A wider and more complete evaluation of the cow´s welfare in organic
farming is needed, and should include the animal behaviour, health (including
mastitis and lameness), fertility/reproductive performance and measures of
immune function.
Conventional dairy cows have been genetically bred to maximise the
conversion of nutrients to milk. Prioritizing the nutrient for milk production
reduces its availability to other biological functions such as maintenance of
body weight, reproduction and health (Hoekstra et al., 1994; Pryce and
Veerkamp, 2001) and increase the predisposition to inferior hoof health and
lameness (Emanuelson, 1998). Maximizing DMI to overcome such deep
negative energy balance (NEB) is one of the key issues in dairy cow feeding
around calving and during early and mid lactation. NEB is specially
exacerbated during the ‘Transition Period’ (three weeks prior to and three
weeks after parturition; Grummer, 1995), coinciding to the period when most
infectious diseases (e.g. mastitis) and metabolic disorders (e.g. milk fever,
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ketosis, retained foetal membranes, metritis) occur (Goff and Horst, 1997;
Mallard et al., 1998). Thus conventional dairying systems require feeding
early lactating cows with balanced diets which offer excellent quality and
palatability and simultaneously meet energy requirements and provide
sufficient amounts of fiber in order to avoid subclinical metabolic diseases.
This is currently the greatest challenge in dairy cow management.
Compared to cows under conventional management, cows in organic
farms exhibit less negative energy balance or at least less body fat
mobilization at early lactation (Fall et al., 2008), as demonstrated through the
assessement of blood metabolites in cows under organic and conventional
management and of cow´ body condition score (BCS) (Roesch et al., 2005;
Fall et al., 2008). The resemblances in breeds and the overall management
used in both systems, apart from the nutritional and sanitary impositions, could
in part explain these findings. Such findings would indirectly influence the
incidence of metabolic disorders, which may be lower in organic farms than in
the conventional ones, if the cow genetics is taken into consideration (Fall,
2009). However, reports on this matter are controversial, and additional
clarification is needed for breed influences on the incidence of metabolic
disorders in organic dairy farms, by using new predictors for the occurrence of
such diseases.
Adequate provision of suitable feed is one of the primary requirements to
ensure the health of livestock (Lund, 2006; Manteca et al., 2008). Restrictions
on the use of concentrates diets, according to organic standards (EEC
505/2012) may lead to a situation where organic dairy cows have difficulty in
consuming enough energy. Recent studies on the levels of blood metabolites
(β-hydoxybutyrate, free fat acids and insulin) before and after the change of
legislation showed that blood changes were similar and that the incidence of
clinical ketosis was not associated with herd type or the change of legislation.
Thus the legislated changes in the nutritional management did not appear to
have had any detrimental effects on the metabolic profiles of organic cows in
early lactation and there was no evidence that organic cows were
metabolically more challenged or had a severe negative energy balance
(Blanco-Penedo et al., 2012).
Another source for the production stress includes the extreme
environmental conditions that negatively impact the animal production,
behavior, health and welfare. Climatic factors such as air temperature, solar
radiation, relative humidity, airflow and their interactions, often limit animal
performance in conventional dairying systems (Sharma et al., 1983). Dairy
cattle research has tended to concentrate on genetic improvements to increase
milk production and on nutrient supply to the cow during early lactation. Little
attention has been paid to the thermoregulatory ability of the modern cow as
her capacity to produce milk has increased (Kadzere et al., 2002). However,
most studies conducted in controlled environments focus on the effects of heat
(temperatures between 24d environmentsthe moder-based systems where the
animals are exposed to direct sunlight (Fuquay, 1981), rather than those of the
cold (Hemsworth et al., 1995). Extensive data on the effect of heat stress on
dairy production responses exists (Beede and Collier, 1986) and it has been
demonstrated that milk production is reduced 15%, accompanied by a 35%
decrease in the efficiency of energy utilization for productive purposes, when a
lactating Holstein cow is transferred from an air temperature of 18 to 30for
productivet al., 1976). At ambient temperatures above 26ºC, the cow reaches a
point where she can no longer cool herself adequately and enters heat stress
(Roenfeldt, 1998). High-producing cows are affected more than low-producing
cows, particularly in early lactation, because the zone of thermal neutrality
shifts to lower temperatures as milk production, feed intake, and metabolic
heat production increase (Coppock et al.; 1982), which may lead to rectal
temperatures exceeding 39tureured mperatures above 26ºC, the cow reaches
aHeat stress is characterized by elevated respiration rates and rectal temper-
atures, and has been implicated in impaired metabolism (Bandaranayaka and
Holmes, 1976) and in poor reproductive performance (Ingraham et al., 1974)
in dairy cattle under conventional systems, independently of feed intake
effects. Yet, Sharma et al. (1983) showed that different breeds have distinct
ability to deal with hight environmental temperatures, the called resistance to
heat stress, thus allowing the dairyman to select the most suitable animal for a
particular environment.
In organic and low-input systems, access to grassland should be
complemented with several management measures to reduce the detrimental
effects of heat stress and simultaneously improve animal welfare and milk
yield. Some easily implemented measures include: the existance of shadows,
either natural (trees) or artificial (portable shade-cloth blocking 50% of
radiation or permanent structures), in size and amount adequate to allow all the
cows to lie down, the availability of clean water and high quality forage within
the shadowed areas, to minimizing the permanence indoors during milking, the
use of sprinklers to cool housing facilities and to reduce insects infestation, as
well as changings on the feed schedules, if necessary.
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7. BREEDING FOR ORGANIC AND LOW-INPUT

FARMING SYSTEMS
Sustainability applied to dairy farming and organic dairy production has
received increased attention in Europe, where pasture based milk production
systems exists as alternative to conventional dairy farming, following the spirit
of “naturalness”, to produce according to the principals of healthy and animal-
friendly systems. Although organic and sustainable farming are not
overlapping concepts, despite their aspirations for a production system based
on good animal health and welfare, we can learn from experience from organic
dairy farms that are closer to the sustainability- concept than the intensive
farms do.
In sustainable and organic dairy systems the breed in use, the milk
production and the reproductive management (with or without calving season)
vary, hence inducing differences between dairy farms from different
geographic location. These, combined to the cow biotype and milk yield, may
determine the establishment of different goals for sustainable dairying
diverging from those of conventional systems. And for that dairy cow breeding
needs to be adapted towards an increased importance of fertility and other
fitness traits, resulting in animals more suitable for organic, low-input systems.
So, one important aspect in organic and low-input dairy farming is to define
the cow attributes (the topic will be addressed later on).
A parameter of major influence for the reproductive traits is the breeding
program and the strategies used in farms. Biological, ethical and economic
considerations must be pondered when discussing future challenges for
breeding in sustainable systems. On what concerns the reproductive
management, in low-input systems and particularly in organic farming natural
mating is preferred over artificial insemination (Nauta, 2010), while more
sophisticated reproductive technologies such as embryo transfer are forbidden
or discouraged. Also hormone treatments using GnRH agonist, progestagens
or prostaglandins are prohibited, unless for treatment of medical conditions
such as ovarian cysts or luteolysis. Thus most estrus synchronization programs
are not an available strategy to modulate the reproductive efficiency in those
farming systems (Garmo et al., 2010). Organic dairy herds using a bull in
natural mating services usually have better fertility performance than those
using the artificial insemination (Ahlman, 2010).
It is important to remember that by selecting the male line to be used for
breeding, and while establishing the specific traits that are important in their
particular herd, the farmer strongly influences the daughters´ performance.

Furthermore, the inappropriate use of sires may lead to a decline in the farm
reproduction success (Rodriguez-Martinez et al., 2008.) Yet, for most
countries, information concerning important traits for organic and low-input
systems is often absent from the bull core information from a semen catalogue,
limiting the identification of the conventional bulls best suited for organic
production (Ahlman, 2010). Despite that total merit indexes adjusted for
organic production developed in Switzerland, Germany and Canada (Bapst,
2001; Krogmeier, 2003; Rozzi et al., 2007), its use is somehow limited.
Which Is the Expectable Reproductive Performance

in Sustainable Dairying?
In sustainable and organic dairy farming scenarios, functional and

reproductive traits rather than milk yield are of key importance. The fertility of
the cow is a major factor on the economy of the system (Figure 1) and is
determined by multiple factors, including the management regime,
environment, genetics, nutrition, and biological and health status (Löf, 2012).
Figure 1. Major influences over cattle fertility in organic farming.
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Available information concerning reproductive efficiency and the

productive performance for such systems is still limited. Currently, established
reproductive management in sustainable dairying does not differ much from
the conventional one. This is particularly true if the organic or low-input farm
derived from a previously existent conventional farm (Nauta et al., 2006b).
Reproductive efficiency of the cows is essential when establishing sustainable
breeding programs and choosing the most suitable breed for a particular
environment or management system (Ahlman, 2010).
As for the more conventional dairy systems, reproductive performance
will be directed by the triangle energy balance/nutrition/milk yield in a breed-
related manner. The breed will determine the feed efficiency and the
equilibrium in the nutrient partition between the different organic
compartments, thus influencing also the potential milk production level. It is
the ability to mobilize body reserves at the onset of lactation, which was
highly developed in modern Holstein-Friesian cows, that ultimately defines the
cow's potential of milk production. One should remember, however, that
energy density tends to be lower in organic feed rations (Reksen et al., 1999)
and in grassland based systems, and low energy intake is known to influence
the fertility in Holstein cows (Pryce et al., 1999; Rodriguez-Martinez et al.,
2008).
Milk production as well as the ability to mobilize fat reserves and change
the body energy metabolism (which can be followed through blood
metabolites measurements) to assist milk production after calving differs with
the breed genetic merit for milk yield (Barth et al., 2011), and rearing animals
in low-input, grassland-based systems may highlight such differences. In
addition, within the Holstein genetics, animals with similar genetic merit for
milk production now show a wide range of genetic merit for fertility traits
(from good - Fert+, to poor - Fert−), which has been associated to different
priorities in the nutrition partition nutrients towards reproduction and milk
production (Cummins et al., 2012).
Organic or low-input systems must comply with this framework and try to
adjust the cow biotype in order to achieve the best profit from the system. The
first parameter that needs to be defined is the existence of seasonal calving
periods (block calving), like it happens in the New Zealand system (Kelly et
al., 2004), or if calvings are allowed to occur year-round. This managerial
decision may interfere with the breed selection and with forage and pastures
management, as well as with milk availability, and indirectly may influence
the reproductive parameters.
Figure 2. Determinant functional traits for sustainable dairy systems.
Animal selection for both functional and productive traits is complicated

unless main objectives are clearly established. Functional traits in sustainable
dairy farming may be grouped into three segments. One includes the
reproductive parameters that positively correlate with a profitable system, such
the interval from calving to conception, the calving intervals, the age at first
calving, the day open and the rate of stillbirth. Another important segment is
the animal health and its resistance to diseases, in particular mastitis and
parasitic infestations. The third element of the functional traits is constituted
by parameters related to cow longevity, such as the cow robustness, including
the leg and claws fitness, the weight gain and metabolism, the live weigh, and
the productive lifespan (Figure 2).
Organic and low-input farms in different regions or countries have
different basic conditions and different cow number and breeds, and may be
subjected to different regulations, which must be taken into consideration
when analyzing the available information on reproductive efficiency of the
system. In Nordic countries, the organic dairy production usually presents a
slightly higher herd size while the milk production level tends to be 10-30%
lower than in conventional system (Reksen, 2005; Fall, 2009; Ahlman, 2010).
However, the breeds used (mainly the Swedish Holstein and the Swedish or
Norwegian Reds and their crosses) are similar. For this scenario, the overall
fertility is slightly better for the organic farms, together with lower culling
rates and longer longevity, than for the conventional ones (Ahlman, 2010; Löf,
2012), similarly to the reported for other countries and different cows breeds
(Hovi et al., 2002).
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Yet, this will probably change according to cow´s milk yield and with the
cow´s breed. In fact, Reksen and colleagues (1999) working with Norwegian
Red cows reported no differences in the reproductive indices in organic
dairying in Norway, except for a reduction in the number of days open for
organic cows, and pointed out the existence of predictors of compromised
fertility, particularly when associated with external factors such as the calving
season (summer vs. winter), the age of the cow (first calving intervals being
longer in the organic than in conventional systems) and parity, which the
authors associate to different individual ability to correct the negative energy
metabolism balance with the forage between both systems. The breeding
regime (natural services vs. artificial insemination) was shown to interfere
with the calving interval in organic cows (Garmo et al., 2010), the interval to
first and last artificial inseminations, as well as a reduction in the total number
of inseminations (Löf et al., 2007; Ahlman, 2010) along with to increase in the
number of cows getting pregnant at first insemination, even if highly
influenced by the breed used in those farms (Ahlman et al., 2012).
When analysing the possible influence of individual and environmental
factors (highlighting the Genetic x Environmental interaction) over the
reproductive efficiency in organic farms, one can conclude that there is room
for improvement within this production system.
Moreover, it is generally accepted that lower intensity of production will
ease the stress pressure over the cow under organic systems thus improving its
ability to survive longer and have an increased productive lifespan (Reksen et
al., 1999; Fall, 2009; Ahlman, 2010).
Thus, on what concerns to the reproductive management, the sustainable
dairymen must ponder on the use of alternative breeding scenarios (Nauta,
2009), always taking into account the interaction GxE and the weighing of
different traits targeted in the managerial outcome proposed for the farm:
1. The use of adapted conventional breeding, where the reproduction

techniques used should also be addressed, e.g. by excluding direct use
of ET bulls.
2. The use of separate breeding programs within the organic production
system, where bulls are evaluated based on their daughters’
performance in organic farms. All modern reproduction techniques
except AI should be excluded.
3. Use local breeding programs based on natural mating within the farm
or region.
8. SELECTING THE BEST COW BIOTYPE

FOR LOW-INPUT SYSTEMS
The selection of the most suitable animal or breed to a particular farm

system, whatever the production involved, might represent one major factor of
success. Dairy producers need to understand that the final production does
reflect both the action of the animal genes and the environment (Nauta et al.,
2006a), although the later might be versatile. Thus, expectably not all the
cattle breeds behave as one, depending on the production environment.
It is frequently discussed that cow performance frequently differs between
organic and conventional herds (Pryce et al., 2004), hence raising the question
of whether the dairy cows have the ability to adapt to the organic production
environment. Several concerns were raised regarding the ability of high
producing breeds to adapt to organic environments, particularly to a reduction
in the energy and protein intake and the limited use of antimicrobial drugs.
The main issue relates to the Genotype vs. Environmental interactions, which
were found to be of major importance in the occurrence of production traits
(Nauta et al., 2006a). High-producing Holstein Frisian cows might not be the
most suitable animal for sustainable dairy farming as it requires high standards
of nutritional and management support. Those animals were mainly selected
for high production in a highly controlled environment that differs from that of
organic production, mainly regarding a more demanding feed quality, ration
composition, feed management and feed intake, animal health management,
and housing, although they are more efficient in the use of resources per unit
of milk produced (Dobson, 2009).
A specific organic or sustainable breed of dairy aptitude doesn’t exist.
Under controlled conditions for technology and drug usage, and the actual
limitations concerning the feed origin, as it happens in organic farming,
animals need to fit and cope with the environment. Selection of the animal
biotype is important to reach a good balance between the production level, the
animal physiology (welfare, behaviour, health, reproduction), and the societal
value about the production system.
Therefore different breeds are needed for different local conditions,
making the biodiversity of farm animals a necessity (Spengler Neff, 2007;
Spengler Neff, 2009).
On the basis of the current knowledge on dairy cow adaptation to different
environments it is suggested that organic farmers should use robust breeds
with broad breeding goals, including both production and functional traits
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(Pryce et al., 2004). In sustainable/organic systems, which encompass with

reduced intensity of production and moderate to low-input systems, the
functional traits (usually of low heritability and often unfavorably correlated
with milk production) such as health and longevity, and the milk quality,
would be more important than the productive traits itselves (with higher
heritability). Also, selection of the animals would follow these guidelines, and
increased value should be attributed to the functional traits, like the disease
resistance (in particular to mastitis), parasite resistance, strong legs and claws,
foraging ability, fertility traits, persistency of lactation and increased milk
yield from first to third lactation and longevity (Bapst, 2001; Pryce et al.,
2004; Ahlman et al., 2012; Spengler Neff, 2012a, b).
As a resume, the decision on what sort of animal that best suits a farm is a
main issue when deciding for sustainable dairying. The foreseen biotype for
sustainable dairy systems is a very balanced cow which is highly efficient at
producing milk using less feed, i.e. a better feed-converter animal. There is no
prescription ever for the best cow for a given region. An equilibrium have to
be established in sustainable dairy systems between the cow biotype, feeding
and land management, and a compromise with the milk yield must be reached
taking into consideration the economic profit of the system. So, it is important
to choose the breed most suited to a particular management system and to the
market where it is intend to sell the milk, since the existence of specific fed
requirements and the need to minimize the use of drugs to treat or prevent
diseases will have reflexes on the cow productivity. Cross breeding with dual-
purpose breeds may be another solution available to sustainable and organic
dairy farmers (Nauta, 2009; Spengler Neff et al., 2012b), since it may allow
improving milk yielding of local breeds, which are generally best adapted to
local environmental conditions.
9. SOCIO-ECONOMIC ISSUES IN SUSTAINABLE

DAIRY SYSTEMS
The most likely future scenarios suggest that the dairy sector will continue
to bear at least part of the cost of global warming. As a result, at present the
best bet might be to identify and quantify the consequences of climate change,
and then work on identifying the best options for the future (Easterling et al.,
2007; Thornton et al., 2007; Nardone et al., 2010).
In operational terms, it is essential that the end-users, their aims and

motivations will be actively involved (Bélanger et al., 2012). Obviously, the
farmers themselves are responsible for practical actions at farm level, and thus
play a key role in social equity. The current loss of purchasing power among
livestock producers has a direct impact on generational solidarity.
Other factors, such as the hard work involved and the lack of rural areas
facilities, favour the disappearance of farms (Bernués et al., 2011),
aggravatting the imbalance in regard to urban areas. Research into
intergenerational issues suggests that younger generations see no future for
themselves in dairy farming (Perea et al., 2010).
If the social equity of dairy farms is to be guaranteed, there has to be a full
understanding of the farmers’ view of sustainability, and priorities have to be
established with a view to making the rural world more attractive, and
providing it with improved facilities and amenities.
10. ON THE NEED FOR NEW POLITICAL CONTEXTS

There is a considerable lack of information regarding what scenarios are
desirable for the dairy farms of the future. Some authors regard the link of
sustainability evaluations and simulation models as a promising development
(Oudshoorn et al., 2011; Vayssières et al., 2011). One major constraint for this
approach is the limited availability of real-time data to base the design and
monitoring of forecast scenarios. Moreover, sustainability-evaluation tools
alone still do not generate the required quantitative information, so simulation
models may serve as a robust framework for qualitative assessment. In this
context, it is difficult to draw up general guidelines regarding which models
are most appropriate, but there is a general agreement regarding a number of
key criteria: sustainable dairy farm models should be diversified, robust, with
efficient links to the industry. They should be more self-sufficient, place
greater emphasis on direct marketing and have closer links to local lifestyles
and fewer links to business (Steinfeld et al., 2006; Thornton et al., 2007; Gill
et al., 2010; Hoffmann, 2010; Nardone et al. 2010; Bernués et al., 2011; ten
Napel et al., 2011; Augustin et al., 2012).
The dairy industry will also have to bear the cost of relocation, since some
current farm locations are very unlikely to be sustainable in future. Thus,
simulation models might provide a framework for predictions regarding global
warming, and can be used as a basic instrument for analysing the different
options (Turnpenny et al., 2001).
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The major critical issues in regards to climate change are those related to
water, soil and habitats (Gill et al., 2010). Other relevant aspects are those
linked to energy efficiency, both at farm level and in terms of more effective
relationships with the industry (Augustin et al., 2012).
The best-placed dairy farms in the race towards sustainability will
therefore be those most closely bound to the land, i.e. organic farms or
integrated agriculture/livestock systems, whose efficiency – and not just
productive efficiency – is today a priority.
Since sustainable production tends to be more expensive, due to lower
physical yields and higher production costs, it is clearly essential to devise and
implement a system of rewards for the efforts involved in sustainability at a
farm level (Gibbon, 2005; Jay, 2007; Roeder et al., 2010). Clearly, the farmer
is the first to benefit from sustainable livestock rearing, since it enables him to
obtain profits without jeopardising the future production capacity, i.e. without
lossing natural or man-made capital. But it also benefits the Society, while
having a positive impact on other related economic activities: it provides food
and non-productive services, both environmental and social. The question is
how much are those non-productive services worthwhile. If the market does
not reward them through higher prices, society will have to do so. Otherwise,
market inertia will rebalance the systems at a less sustainable, though
economically fair, level. Society therefore has to assume part of the cost of
sustainability, since it also profits of the benefits. This is crucial for the
implementation of sustainable dairy farming.
The EU has pioneered the development of reward systems aimed to a
greater degree of sustainability. However, a number of studies (e.g. Franco et
al., 2012) highlighted failures in certain agricultural and rural development
policies. A thorough review of this whole issue is both essential and
controversial. The need for balanced reward systems must be weighed against
the fact that they run counter to the current trend of global agreements on the
gradual elimination of production subsidies and tariffs.
11. ASSESSING SUSTAINABILITY IN DAIRY SYSTEMS

The suitability, advantages and drawbacks of the various currently used
methods to assess sustainability have been examined in a number of studies
(Pannell and Glenn, 2000; Payraudeau and van der Werf, 2005; Singh et al.,
2012). Presently, they are not sufficiently reliable to fully support decisions
regarding dairy system sustainability (Gasparatos et al., 2008; Gasparatos,

2010).
First difficulties for the assessment of sustainability are inherent to the
very nature of the issue: sustainability requires multidisciplinary conceptual
frameworks in which social, economic and ecological considerations form a
coherent whole. Failure to ensure adequate representation of all three
dimensions often leads to fairly speculative multidimensional approaches
using a range of tools. The social aspects of sustainability tend to be those
least represented tools (Van Passel and Meul, 2012).
Methods for measuring sustainability face three major constraints: (1)
sustainability cannot be directly measured; (2) there are no absolute scales for
sustainability; (3) no quantitative criteria are available, so that it is impossible
at present to predict with any certainty the extent to which changes made today
will ensure sustainability tomorrow.
The first constraint gave rise to the development of the so-called
sustainability indicators, which can be defined as the indirect measurements of
sustainability. At farm level, clearly, the best approaches are those based
directly on sets of indicators, whilst at higher levels a certain degree of
aggregation is required. Various sets of indicators have been applied to dairy
systems, including the IDEA method (Vilain, 2008), one of the first tools to be
designed in Europe, the RISE method (Häni et al., 2003) in Switzerland, the
FarmSmart in the UK (Tzilivakis and Lewins, 2004), and the MESMIS
framework (Masera et al., 1999).
Since priorities for evaluation are different for each setting, the ideal
approach is to develop a specific set of indicators (Hueting and Reijnders,
2004). In fact, when building the conceptual framework, two key questions
need to be considered: which indicators should be selected? And what is the
optimal value for each indicator in terms of sustainability? Since a cohort of
researchers, end-users and experts selects the indicators and optimal values
they inevitably reflect a certain degree of subjectivity, which also masks the
effects of premises and simplifications. These problems have been widely
examined by researchers (Table 1).
At political or industry level, arguments have been adduced in favour of
compound indices, on the grounds that they are easier to use (Van Passel and
Meul, 2012). Methods of aggregating indicators vary considerably, and also
depend on whether the approach is ecological or economic.
Arguments have been advanced in favour of adopting an economic
approach for evaluating dairy systems, based generally on the principles of
productive efficiency and utility theory.
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Table 1. Summary examples of sustainability indices
Number of
Name Scaling Weighting Aggregation
sub-indicators
Index of sustainable Monetary Arithmetic
20 Equal
and economic welfare terms average
Index of
Weighted
environmental 11 Normalization Subjective
sum
friendless
Ecological footprint 6 Area Equal Summation
Carbon footprint 4 Normalization Equal Summation
Environmental Arithmetic
68 Normalization Equal
sustainability index average
0 – 1, using
minimum and
Human development maximum Arithmetic
3 Equal
index value for each average
indicator as
goal post
Environmental Aim = 7,
50 Equal Average
vulnerability index worst = 7
Weighted
Well being index 87 0 - 100 Subjective
average
Linear and
Geometric
Live cycle index 21 non linear AHP
mean
functions
G score 5 Subjective Equal Summation
The value of resources and products are assumed to reflect expected

utilities derived from the consumption or existence of the product (Tyteca,
1998; van Calker et al., 2006). This concept of value is the most readily-
comprehensible and acceptable one for decision-makers with settings based on
economic values (Farrell and Hart, 1998).
Models are more viable if they are able to reflect that certain forms of
capital are irreplaceable, or that at least a minimum threshold level is required
to avoid irreversible loss (Perman et al. 2003; Kuosmanen and Kuosmanen,
2009). Classical economic approaches are based on measures of efficiency use
for the different forms of capital, or on cost-benefit analysis (Figge and Hahn,
2004a, 2005; Meul et al., 2005). In practical terms, these approaches are
limited by the method used to assign economic values, since the market can
only provide the direct utility of some elements of the model.
In general, these models have achieved a fair indication of whether or not

a production unit is sustainable. However, few models have focused on the
question of what is the most sustainable way of assigning resources. One such
model is the sustainable-value method (Figge and Hahn, 2004b).
Conceptually, it is based on the constant-capital rule, and is essentially a
relative measure of efficiency. A number of methodological issues have
recently been highlighted which need to be revised in order to ensure the
proper implementation of the sustainable-value method (Kuosmanen and
Kuosmanen, 2009). Even so, this remains a promising approach, which is
likely to receive considerable attention in the forthcoming years.
CONCLUSION
This chapter book aims to present a comprehensive and up-to-date
overview of the results of research and innovation in sustainable dairy farms.
The dairy sector supports a long-term vision in which a top performance in
sustainability is the goal. Based on this vision, ambitions have been
formulated, which in many cases go much further than the current standards.
Priority issues in sustainability are the following: animal welfare, a clean
environment, climate neutral production, on-farm nature and biodiversity,
close connection with society and consumers, healthy, and safe dairy products
and no depletion of resources. All are essential and the balance and integration
of these focus areas constructively contribute to the sustainability of this farm
system.
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Chapter 3
SOMATIC CELL COUNT AS THE FACTOR

CONDITIONING PRODUCTIVITY OF VARIOUS
BREEDS OF COWS AND TECHNOLOGICAL
SUITABILITY OF MILK
Joanna Barłowska1, Zygmunt Litwińczuk2,

Aneta Brodziak2 and Jolanta Król1
1
Department of Commodity Science and Processing
of Animal Raw Materials
2
Department of Breeding and Protection of Genetic Resources of Cattle
University of Life Sciences in Lublin, Faculty of Biology
and Animal Breeding, Poland
ABSTRACT
Early detection of mastitis with subclinical symptoms is possible by
determining somatic cell count (SCC). SCC is the most widely accepted
indicator of the mammary gland health as well as milk quality and its
technological suitability. The authors’ research has revealed that an
increase of SCC (independently of a breed of cows) mainly causes a rise
in a total crude protein content and a distinct reduction in lactose level
(P≤0.01). Moreover, SCC also lengthens the time of milk enzymatic
coagulation (P≤0.01) but it does not influence its thermal stability.
Distinct negative relationship between casein content and SCC is
confirmed by relatively high value of correlation coefficient (r=-0.59). In
www.ebook777.com
92 Joanna Barłowska, Zygmunt Litwińczuk, Aneta Brodziak et al.
the authors’ studies the significant interactions (breed of cows x SCC) for
the daily yield of cows, content of protein, casein and lactose, protein to
fat ratio and rennet-induced milk coagulation time also have been stated,
which indicates a differentiated response of various breeds of cows to
udder inflammations. Holstein-Friesian cows are more sensitive to
decline of daily yield, that is reflected in higher negative value of
correlation coefficient between SCC and milk yield (-0.245). In
Simmental and Jersey cows the correlations were negative as well but
their values were substantially lower (r=-0.123 and r=-0.148) and
statistically insignificant. With the age of cows increase in SCC was
noted and in the cows of local breeds (Polish Red, Polish Black and
White, Whitebacked) and Jersey that rise was much smaller in
comparison to Polish Holstein-Friesian cows. Significant interaction
(P≤0.05) for SCC between breed of cows and subsequent lactation was
indicated. However, the significant changes in milk constituents were
recorded only when the SCC exceeded 500 thous. ml -1, that is in milk that
does not meet the current regulatory quality standards.
Somatic cell count also affects the changes in whey protein content.
Rise of SCC decreased the content of major albumins, i.e. alpha-LA and
beta-LG, by small degree, and that was confirmed by very low
statistically insignificant correlation coefficients (r=-0.07 i r=-0.05).
Negative value of both correlations, though, indicates a direction of
changes and may imply that in more advanced stages of udder diseases
the decrease of milk proteins is likely to be higher. However, with rise of
SCC, content of immunoactive proteins (lactoferrin and lysozyme) as
well as bovine albumin serum (BSA) significantly increased. The
significant impact of SCC on content of these proteins in milk is
confirmed by relatively high positive values of computed correlation
coefficients (lactoferrin r=0.65, lysozyme r=0.63 and BSA r=0.59). In the
case of BSA that correlations were clearly differentiated in particular
breeds of cows, i.e. r=0.711 for Holstein-Friesian, r=0.577 for Simmental
and r=0.472 for Jersey. Thus, it can be assumed that there is a
differentiated degree of permeability of mammary gland cell membranes
in cows of various breeds.
1. INTRODUCTION
Mammary gland inflammations are induced by as many as even over 140
various types of microorganisms inhabiting both animal and its environment
[Malinowski and Kłossowska, 2000]. The cause of mastitis can be a variety of
microorganisms such as bacteria, mycoplasmas, yeast like fungi, algae and in
the rare cases viruses [Bradley, 2002; Khan and Khan, 2006]. The principal
Somatic Cell Count as the Factor Conditioning Productivity … 93
etiological factors inducing the inflammation of mammary gland of cows are

bacteria. The severity of clinical symptoms and course of mammary gland
inflammation is largely dependent on the type of bacteria causing the
infection. With regard to the etiological factor, a classic division of mastitis
into two categories, depending on a method of infection, was established, i.e.
mammary gland inflammation caused by “infectious” factors (e.g.
Staphylococcus aureus) and “environmental” (e.g. Escherichia coli). Micro-
organisms inducing the infectious mastitis exist on the skin of udder and they
are well adapted to a survival and proliferation in host organism, in particular
in the mammary gland. Nevertheless, they are not adjusted to life outside the
body of a host. These bacteria are primarily responsible for subclinical and
chronic inflammation of the mammary gland. The “environmental” factors, i.e.
bacteria living in an environment of cows (bedding, water, earth), are less
virulent pathogens and generally rapidly eradicated by the immune system of a
host [Blowey and Edmondson, 1995; Bradley, 2002]. However,
Staphylococcus aureus and Streptococcus agalactiae as well as the environ-
mental bacteria, mainly from the coli group: Escherichia coli (most
frequently) and Klebsiella pneumoniae perform a primary function in the
inflammation induction [Smulski et al., 2011].
According to Klastrup et al. [1987], the susceptibility to mastitis was in
25% a result of environmental factors, 20% – genetic factors and 50% – herd
management.
2. SOMATIC CELL COUNT AS THE INDICATOR

OF MAMMARY GLAND HEALTH STATUS
In numerous research it was shown that somatic cell count (SCC) in cow
milk is a good indicator of mammary gland health status. Furthermore,
occurring subclinical and clinical inflammations are associated with the
significant increase in the count of somatic cells [Rainard and Riollet, 2006].
This fact was confirmed by generally high positive correlation coefficients
between SCC and inflammation status (r=0.30-0.97) [Carlen et al., 2004;
Bloemhof et al., 2009].
It should be emphasized that interbreed differences in the susceptibility of
cows to mastitis exist. Rupp and Boichard [2003] reported that cows of dairy
breeds originating from the eastern France (Montbéliarde and Abondance) and
central Europe (Simmental and Brown Swiss) are less frequent in clinical form
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of mastitis and their milk contains lower level of somatic cells compared to
Holstein breed. Gołębiowski and Brzozowski [2007], who claimed that
Montbéliarde breed characterizes a higher susceptibility to mastitis than
Holstein, due to the lower by 23-38% somatic cell count in milk, also
confirmed this fact.
The SCC of milk includes leucocytes derived from the blood (75%), i.e.
neutrophils, macrophages, lymphocytes and erythrocytes, and epithelium cells
of udder (25%). In milk obtained from a healthy udder leucocytes are
consisted in 5010% of neutrophils (polymorphonuclear granulocytes –
PMNs), in 369% of lymphocytes and in 142% of macrophages. It should be
noted that the percentage of particular types of cells varies depending on the
udder health, age and stage of lactation. Share of leukocytes increase in
response to bacterial infection, tissue injury, stress and final stadium of
lactation. Leucocytes are transported into the milk gland directly from the
blood as a response to the chemical substances, released by mammary glands
during inflammation [Aniulis et al., 2003; Sharma et al., 2011]. The increase
in somatic cell count in milk, primarily neutrophil granulocytes (neutrophils),
is the first signal informing about changes in the health status of mammary
gland. In uninfected quarters of mammary gland, i.e. without mastitis, SCC is
lower than 150 thous. ml-1, at simultaneously lower percentage of neutrophils
(5-25% of the total SCC). It is assumed that the somatic cell count in cow milk
exceeding 150 thous. ml-1 is one of the first signals of mammary gland
infection. During inflammation an elevation in milk SCC is mainly
conditioned by the increase of share of the polymorphonuclear cells by 99-
100% [Schukken et al., 2003; Tao and Mallard, 2007]. Scheppers et al. [1997]
established the so called “physiological threshold level”, i.e. the SCC limit of
200 thous. ml-1, to differentiate between a healthy and infected quarter.
Furthermore, they stated that each doubling of SCC above 50 thous. ml-1
results in losses in milk production. Griffin et al. [1987] established, however,
the SCC lower limit of subclinical stage of mastitis at 125 thous. cells ml-1,
whereas the upper limit at 250 thous. cells ml-1. Whereas Kherli and Shuster
[1994] as a limit value of SCC 100 thous. ml-1 and Harmon [1994] accepted
only 50 thous. ml-1.
For the dairy industry the most pernicious are subclinical (non-
symptomatic) inflammations since milk obtained often becomes the
commercial milk. In Europe, in accordance to the Commission Regulation
(EC) No 1662/2006 of 6 November 2006 (No L230/4) modifying the
Regulation (EC) No 853/2004 of the European Parliament and of the Council
of 29 April 2004, milk intended for human consumption should not contain
more than 400 thous. somatic cells ml-1. Furthermore, the identical limits apply
in Canada and New Zealand. In the U.S. the official standard was up to 750
thous. cells ml-1 until 2011, however, a gradual reduction of SCC limit to the
requirements of the European Union is planned, in order to allow the
American producers to export dairy products to European markets [National
Mastitis Council, 2011].
3. ECONOMIC EFFECTS OF UDDER INFLAMMATION

Mastitis remains the most expensive and hard to overcome by veterinary
methods the disease affecting dairy cattle. According to SABRE [2006], the
total losses due to mastitis in the dairy industry in the EU in 2005 amounted to
EUR 1.55 billion.
Bovine mammary gland inflammations result not only in reduction of milk
synthesis but also in alterations in milk constituents, leading to deterioration of
its nutritive value and technological suitability. Simultaneously, they belong to
the most common causes (except for infertility and lameness) of culling of
cows from herd. The udder inflammations constitutes approximately 70% of
all economic farm losses [Huijps et al., 2008]. Costs associated with the
mammary gland inflammation differentiate depending on the etiological
factor, course of clinical form, animal and milk prices, fodders, services and
drugs [Halasa et al., 2007; Malinowski et al., 2011]. In various countries these
costs are varied, however, each time they are a large financial burden in dairy
farms (Table 1). For instance, in the United States in the case of one clinical
mastitis the costs are estimated at USD 107 and in Sweden even the USD 735
[Malinowski et al., 2011]. The size of losses associated with an occurrence of
mammary gland inflammations also results in a number of cows in herd and a
form of mastitis. Huijps et al. [2008] reported that in smaller herds, consisting
of approximately 30 dairy cows, losses were definitely lower (EUR 17 /cow
per year) in relation to the herds comprising of approximately 160 heads (EUR
198 /cow per year). In the extreme cases, at the presence of inflammations in
clinical form, the average losses were estimated at EUR 210, varying from
EUR 164 to EUR 235 /cow/month, respectively, in the final and the initial
stage of lactation. In the case of subclinical affliction in the herd of cows with
productivity of 8,500 kg/cow/305 days of lactation, at SCC in bulk tank milk
amounted to approximately 200 thous. ml-1, losses were estimated at EUR 20
/cow per year. Chassagne et al. [2005] and Aniulis et al. [2003] stated that the
most susceptible to mastitis were animals in the initial period of lactation.
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Table 1. Costs bearing to treatment and prevention of mastitis according

to various authors
Additional
Cost Mastitis status Country References
information
Treatment
EUR 28 average cost USA, Kaneene and
/cow/year Michigan Hurd, 1990
EUR 31 average cost USA, Ohio Miller and
/cow/year Dorn, 1990
EUR 22 average cost USA, Sischo et al.,
/cow/year California 1991
EUR 279 average cost in England Hillerton et al.,
/cow/year summer 1992
EUR 102 subclinical average cost England McInerney et
/cow/year al., 1992
EUR 20 average cost Germany Reinsch and
/cow/year Dempfle, 1997
EUR 287 average cost England Kossaibati and
/average case Essleniant,
of cow/year 1997
EUR 26 (19- cost of control France Fourichon et
32) /cow/year of udder health al., 2001
status because
of mastitis
EUR 65-182 subclinical the Huijps et al.,
/cow/year and clinical Netherlands 2008
EUR 117 Spain Pérez-Cabal et
/cow/lactation al., 2008
EUR 71 USA, New Bar et al., 2008
/cow/year York
EUR 179 cost of USA, New Bar et al., 2008
/cow complete York
treatment
EUR 78 (17- in dependence the Huijps et al.,
198) on herd size, Netherlands 2008
/cow/year assessed by
farmers
EUR 210 clinical cost in () the Huijps et al.,
(164-235) respectively in Netherlands 2008
/cow/month the final and the
initial stage of
lactation
Additional
Cost Mastitis status Country References
information
EUR 275 Clinical Sweden Nielsen, 2009
/cow/year
EUR 60 subclinical Sweden Nielsen, 2009
/cow/year
USD 224-275 clinical average total the Steeneveld et
/cow cost of Netherlands al., 2011
treatment and Canada
USD 107 clinical USA Malinowski et
(161.8-344.2) al., 2011
USD 735 clinical cost of Sweden Malinowski et
treatment of al., 2011
one case
EGP* in dependence Egypt El-Awady and
15.80±5.25 – on SCC, Friesian Oudah, 2011
1734±281 respectively:
/cow/lactation ≤50 – >2000
thous. cells ml-1
Prevention
EUR 3.56 (0- USA, Kaneene and
22) /cow/year Michigan Hurd, 1990
EUR 4-12 USA, Ohio Miller and
/cow/year Dorn, 1990
EUR 4 USA, Sischo et al.,
/cow/year California 1991
EUR 3 Germany Reinsch and
/cow/year Dempfle, 1997
EUR 50 Sweden Nielsen, 2009
/cow/year
*EGP – Egyptian pounds.
According to the French data [Chassagne et al., 2005], it results that in the
first 30 days after calving, even in a well-managed herd, the percentage of
those animals amounts to approximately 30%. This is due to an attenuation of
immune defense reaction of cow in a perinatal period and more frequent
incidence of mammary gland inflammation associated with that. According to
the data provided by SABRE [2006], in the European Union 30% of cows
remains infected by mastitis in 2005. Furthermore, the analyses conducted in
the same period in Poland proved that the percentage of animals with
symptoms of mastitis is at a similar level but clinical forms of the disease are
recognized in 2-5% of cows [Głowacki, 2006]. The research conducted in
Lithuania by Aniulis et al. [2003] demonstrated that about 42-47% of cows in
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that country had symptoms of subclinical mastitis. It should be emphasized

that subclinical states are more serious problem in dairy herds. Averagely
approximately 40% of cows are constantly affected by changes specific to
subclinical mammary gland inflammations [Malinowski and Kłossowska,
2000]. The changes are usually long-term and often unrecognized by farmer
and ipso facto undiagnosed, especially in herds without SCC monitoring.
According to Östensson et al. [2012], the degree of spreading of subclinical
form of mastitis is very high, both on the level of quarter (63.2%) and cow
(88.6%). However, these results are much higher than those obtained by other
authors [Nam et al., 2010; Petrovski et al., 2011], i.e. 35% and 55%,
respectively.
4. EFFECT OF SCC ON PRODUCTIVITY OF COWS

AND BASIC COMPOSITION OF MILK
Susceptibility or resistance to mastitis of dairy cows is genetically

conditioned. The genetic antagonism between milk yield and udder health
status has been proved, resting on a deterioration of health status of mammary
gland as a result of selection for increase in milk yield [Rupp and Boichard,
2003].
The disease is therefore a problem in high productive herds, in which an
intensive husbandry conditions are used. However, direct selection for mastitis
resistance is not widely applied because of its low heritability. The results of
numerous research (Table 2 and 3) indicate that the values of heritability for
somatic cell count (SCC) or natural logarithm of SCC (SCS – somatic cell
score) are not exceeded 0.20. However, the results obtained by Dube et al.
[2008] point to lower value of heritability in primiparous Jersey cows
(h2=0.07) and slightly higher at multiparous cows (h2=0.11) (Table 3). The
heritability estimates for udder inflammations are even lower than for SCC
(Table 3). Low values of heritability for susceptibility of cows to mastitis do
not mean, however, the absence of genetic variation. Nevertheless, the
environmental factors strongly influence on phenotypic effect.
Inflammation primarily results in a reduction in milk production. Seegers
et al. [2003] reported that the total loss in milk production arising from clinical
mastitis was 375 kg, i.e. approximately 5% of lactation yield. However,
production losses were highly variable and mainly eventuate from a lactation
period in which cows suffering from mastitis.
Table 2. Heritability estimates (h2) and genetic correlations (r) among

lactational somatic cell score (SCS) [Dube et al., 2008]
Heritability estimates Genetic correlations

SCS1 SCS2 SCS3 SCS1 SCS2 SCS3
SCS1 0.07±0.01 0.82±0.09 0.85±0.05
SCS2 0.11±0.01 0.96±0.06
SCS3 0.11±0.02
SCS1 – SCS for first lactation; SCS2 – SCS for second lactation; SCS3 – SCS for third
lactation.
Table 3. Heritability estimates (h2) for somatic cell count and mastitis
h2 Parameter Additional information References

Welper and Freeman,
0.16 SCC Holstein
1992
0.18 SCC Danish Holstein Lund et al., 1994
Mrode and Swanson,
0.11±0.04 SCC
1996
0.10-0.14 SCC Mrode et al., 1998
0.136±0.028 during the first lactation
SCC Sender, 2001
0.096±0.016 for all lactations
0.06±0.02 SCS Finnish Ayrshire Ikonen et al., 2004
0.11-0.22 SCS Ptak et al., 2007
0.07 in primiparous cows Dube et al., 2008
0.11 SCC in multiparous cows
Jersey
0.14-0.15 Danish Holstein, Danish Norberg et al., 2009
SCC
Red and Danish Jersey
0.07-0.14 SCC Ptak et al., 2009
0.05 (0.01- Burlina Penasa et al., 2010
SCS
0.11)
0.15 lactations 1 and 2 National Research
0.20 lactation 3 Institute of Animal
SCS
Production, Poland,
2010
0.09-0.18 lactations 1-3 Rzewuska et al., 2011
0.11-0.14 daily average for
SCC
lactations 1-3
Holstein-Friesian
0.025 mastitis Lund et al., 1994
ca. 0.04 mastitis Mrode and Swanson,
1996
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Table 3. (Continued)
h2 Parameter Additional information References

0.02-0.04 clinical Rupp and Boichard,
mastitis 1999
0.01-0.17 mastitis Pösö and Mäntysaari,
1996; Rupp and
Boichard, 1999; Carlen
et al., 2004; Bloemhof
et al., 2009
SCC – somatic cell count; SCS – somatic cell score (natural logarithm of SCC).
Table 4. Genetic (rg) and phenotypic (rp) correlation coefficients

between milk yield and SCC
Correlation Type of Additional

References
coefficient (r) correlation information
-0.16 (for SCS) genetic primiparous cows Welper and

-0.02 (for SCS) phenotypic Holstein Freeman, 1992
Mrode and
0.14±0.04 (for SCS) genetic
Swanson, 1996
-0.07 (for SCS) genetic test-day milk yield
Ikonen et al., 2004
-0.13 (for SCS) phenotypic Finnish Ayrshire
beside genetic
-0.19 (for SCC) Sawa et al., 2007
(phenotypic)
0.12 (-0.48-0.91) test-day milk yield
genetic Penasa et al., 2010
(for SCS) Burlina
lactational milk
-0.55 (for SCC) genetic El-Awady and
yield
-0.47 (for SCC) phenotypic Oudah, 2011
Friesian
total for Polish
-0.157 (for SCC, see Holstein-Friesian, Litwińczuk et al.,
Table 5) Simmental and 2011
Jersey
-0.22 – -0.16 (for
Jakiel et al., 2011
SCC)
SCC – somatic cell count; SCS – somatic cell score (natural logarithm of SCC).
Thus, Hagnestam et al. [2007] noticed that the reduction in milk

production in the period of 305-day lactation ranged from 0 to 902 kg,
depending on the stage of lactation and subsequent lactation, in which the
Swedish Holstein and Swedish Red cows become ill. Hortet et al. [1999]
analyzed 32,148 control milkings from 4,968 cows of French Holstein breed,
in the milk samples in which SCC was lower than 600 thous. cells ml-1. Value
of 50 thous. cells ml-1 was accepted as a reference level of somatic cell. The
authors found that daily milk yield of primiparous cows decreased by 0.30 kg
at the SCC raise up to 100 thous. cells ml-1, by 0.61 kg at SCC to 200 thous.
cells ml-1 and by 1.09 kg at SCC to 600 thous. cells ml-1. Numerous studies
(Table 4) show that an increase in the somatic cell count affects the losses of
daily milk production to a lesser extent (rp from -0.02 to -0.19). Nevertheless,
in a case of lactational milk production, however, higher negative correlation
(r=-0.55) exists.
The study of Litwińczuk et al. [2011] indicate on sundry sensitivity of
cow breeds to an increase of SCC in milk, that is confirmed by differences in
correlation coefficients obtained between the SCC and daily yield. Out of three
breeds, i.e. Polish Holstein-Friesian, Simmental and Jersey, Polish Holstein-
Friesian cows were distinguished by the highest sensitivity to udder infections
(r=-0.245 at P≤0.01). At the other two cow breeds (characterized by lower
productivity), i.e. Simmental and Jersey, the values of r were substantially
lower (r=-0.123 and r=-0.148, respectively).
Increase in the somatic cell count in milk also affects the changes in the
basic composition. The most sensitive milk component to mammary gland
inflammation is lactose. It is responsible, along with some elements (primarily
Na and Cl), for regulating the osmotic pressure in udder, which must be in
balance with osmotic pressure of blood [Bleck et al., 2009; Litwińczuk, 2012].
Rise in SCC effects on decline in lactose content, as the result of synthetic
activity of mammary gland reduced [Ikonen et al., 2004; Bleck et al., 2009].
This leads to flow of higher quantity of Cl- and Na+ from blood to milk and K+
into the blood to compensate for the osmotic pressure in mammary gland
[Bansal et al., 2005; Litwińczuk, 2012]. Forsbäck et al. [2009] reported that at
the SCC level ≤100 thous. ml-1 (healthy udder) lactose content was 4.66 g 100
ml-1 and at the SCC>200 thous. ml-1 (threshold physiological limit) – 4.51 g
100 ml-1. The research of Barłowska et al. [2009], carried out on milk obtained
from four breeds of cows (Black-White and Red-White variety of Polish
Holstein-Friesian, Simmental and Whiteback), proves that a significant
decrease in lactose content also followed by the cellular element level ≥200
thous. ml-1. Nevertheless, the highest decline in this component percentage (by
0.24%) was recorded at the level of SCC ≥1 million ml-1 (P≤0.01), while in the
Black-White variety of Polish breed Holstein-Friesian cows it was the lowest
(by 0.13%) and the highest in Whiteback (0.35%). The similar tendencies were
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noticed by Król et al. [2010] and Litwińczuk et al. [2011] in milk of cows of
the greatest importance in global milk production (Holstein-Friesian,
Simmental and Jersey). Ogola et al. [2007] demonstrated also the reduction in
lactose content from 48.8 g l-1 at the SCC level <250 thous. ml-1 to 43.8 g l-1 at
SCC>750 thous. ml-1. Relatively high negative correlation coefficients
between somatic cell count in milk and lactose concentration (from r=-0.38 to
r=-0.59) determined by a number of authors are a confirmation of this
relationship [Zumbo et al., 2004; Bansal et al., 2005; Sawa et al., 2007; Bleck
et al., 2009; Pazzola et al., 2012]. Juozaitiene et al. [2004] indicated that a
correlation coefficient between SCC in milk and lactose concentration was
relatively high and oscillated between -0.38 in lactation I and -0.44 in lactation
III (P≤0.01), while this dependence for protein or fat content was very low and
found within -0.1 – -0.04 range. Lindmark-Månsson et al. [2000] reported (as
a few), though, a totally different relationships between log10SCC and lactose
percentage (0.073) and higher for fat, and protein level, respectively: r=0.277
and r=0.374 (in milk of Swedish Holstein cows).
With the increase in somatic cell count in milk protein percentage is
generally unchanged or could slightly rise. However, significant changes occur
in particular fractions. Accordingly to Lindmark-Månsson et al. [2006],
concentration of total protein usually remains unchanged at SCC to 1 million
ml-1. Whereas, the results of Litwińczuk et al. [2011], obtained on the basis of
research performed on milk of cows of four breeds, indicates that content of
this component decreased to SCC level in the range of 401-500 thous. ml-1,
and then slightly increased (at SCC: 501-1,000 thous. ml-1). El-Awady and
Oudah [2011], analyzing monthly and lactational losses in protein production
in the milk of Friesian cows, stated that they successively followed and
occurred at SCC level >100 thous. ml-1. At SCC>2 million ml-1 the losses
amounted to 2.12 kg monthly and 21.0 kg during lactation. The results of other
authors indicate that there is no clear correlation between somatic cell count
and protein content [Ikonen et al., 2004; Ogola et al., 2007; Barłowska et al.,
2009; Forsbäck et al., 2009]. Generally low correlation coefficients obtained
are (as already was mentioned) the confirmation of absence of an unequivocal
relationship between SCC and protein content.
There is also no unequivocal opinion among researchers in the case of the
relationship between somatic cell count and fat content in milk. Król et al.
[2010] pointed at a downward tendency of this component with an increase in
SCC, but the differences were generally statistically insignificant in almost all
breeds. However, Barłowska et al. [2009] indicated a reverse tendency. In the
opinion of Ogola et al. [2007] and Forsbäck et al. [2009], changes in protein
and fat content in milk at elevated somatic cell count aroused from an
increased risk of proteolysis and lipolysis. El-Awady and Oudah [2011],
analyzing monthly and lactational wastage in fat production in the milk of
Friesian cows, stated that the losses occurred at SCC level >100 thous. ml-1. At
SCC>2 million ml-1 the losses amounted to 3.01 kg monthly and 27.9 kg
during lactation. According to sundry authors [Lindmark-Månsson et al., 2000;
Ikonen et al., 2004; Zumbo et al., 2004; Sawa et al., 2007; Pazzola et al.,
2010], the correlation coefficients between SCC and fat content in milk are
generally low and oscillated from negative (r=-0.05) to positive (in a range of
r=0.07 to r=0.37). Whereas in the research of Sender et al. [2001], the genetic
correlations between somatic cell count and yield of fat and protein were
positive and higher in the first lactation (r=0.39) than those estimated for all
lactations (r=0.16).
Heuer et al. [1999] and Windig et al. [2005] postulated that a higher risk
of mastitis incidence appeared with an elevation in fat to protein ratio in milk.
According to Heuer et al. [1999], the acute inflammatory response is more
likely to occur when 1.5 value of this ratio has been exceeded.
5. SCC AND MILK WHEY PROTEINS

Somatic cell count also affects the changes in whey protein content. They
represent 20-25% of milk proteins, including approximately 75% of albumin,
i.e. α-lactalbumin (α-LA), β-lactoglobulin (β-LG) and bovine serum albumin
(BSA). The remainder constitutes immunoglobulins, protezo-peptones,
glycomacropeptides, lactoferrin, growth factors, hormones and various
enzymes – including lysozyme. These compounds are globular proteins with a
three-dimensional structure. It should be noted that the aforementioned
proteins, except BSA and immunoglobulins deriving from the blood, are
synthesized in mammary gland of cow [Farrell et al., 2004; Chatterton et al.,
2006; Michaelidou and Steijns, 2006; El-Loly and Farrag, 2007; Smithers,
2008].
Whey proteins demonstrate multidirectional pro-health effects on the
human body. They affect, among others, the digestive, immune, cardiovascular
and nervous systems and play a significant role in reducing a risk of
occurrence of various social diseases [Pan et al., 2006; Liu et al., 2007; Król et
al., 2008; Smithers, 2008].
The dominant whey protein presenting in the milk of cows and other
ruminants is β-lactoglobulin. It plays an important antioxidant role in milk. It
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also exhibits anticancerogenic, antiviral and antibacterial properties. With the

immunoglobulins G β-Lg is probably involved in forming the passive
immunity [Sutton and Alston-Mills, 2006; Hernández-Ledesma et al., 2008].
α-lactalbumin actively contributes in a control of lactation and milk secretion,
forming together with galactosyltransferase (GT) an indispensable component
of lactose synthetase. It also shows anticancerogenic, antibacterial (against
Gram-positive) and antiviral activity. Furthermore, α-La functions as an
immunological factor, inter alia, modulating (increasing) a neonatal immunity
[Séverin and Wenshui, 2005; Zimecki and Artym, 2005; Chatterton et al.,
2006; Riley et al., 2008; Kanwar et al., 2009]. Thus, bovine serum albumin in
milk is physically and immunologically identical to that of blood serum
albumin, as it is not synthesized in the mammary secretory cells but derives
from the so-called nonspecific “leakage” from the blood to milk. According to
Litwińczuk et al. [2011], BSA concentration in milk is an indicator of
permeability of the blood-milk barrier in the mammary gland. Mammary gland
inflammations are a major factor increasing the permeability of cell
membranes of the udder. Furthermore, lactoferrin is also involved in a natural
defense of body against bacterial infections. By binding and sequestrating of
iron, lactoferrin exhibits antibacterial properties against Gram-positive and
Gram-negative bacteria, non-capsular and capsular viruses as well as various
types of fungi and parasites. It functions both bacteriostatic and bactericidal
against Staphylococcus aureus, Esherichia coli, Pseudomonas aeruginosa and
Clebsiella pneumonia. An advantage of lactoferrin in a fight against bacterial
infections is possibility of increasing a bacteria sensitivity to certain antibiotics
(vancomycin, penicillin) and lowering their effective doses. The combination
of penicillin with lactoferrin doubles the inhibitory activity of antibiotic
against Staphylococcus aureus [Diarra et al., 2002]. Lactoferrin also
determines the innate immune.
The increase in concentration of this protein (cow milk contains an
average of 20-200 mg dm-3) is not only due to the secretion of colostrum and
development of the mammary glands but also it testifies of occurring
infections, inflammations or injuries. Lactoferrin is a component of the
secondary granules of neutrophils, where in the case of an injury, infection or
inflammation is released into the blood [Baker and Barker, 2005; Artym,
2010; Garcia-Mantoya, 2011]. Large variability of single-nucleotide
polymorphism – SNPs (more than 140) in the lactoferrin gene indicates that
there is a high probability of existing of a mastitis-resistance marker or
eventually also a marker of milk yield in this gene [Wojdak-Maksymiec et al.,
2006; Żukiewicz et al., 2012]. Furthermore, this protein determines the
maturation of immune cells. Besides lactoferrin, lysozyme also occurs to be

one of the most crucial component of the non-specific humoral immune
response, i.e. as a bactericidal component of various glandular secretions,
including mammary gland. Concentration of the protein varies according to an
udder health, i.e. is much higher in cow colostrum and mastitis milk than in
normal milk, what can be used in the mastitis diagnosis. Synergistic effect of
the enzyme with immunoglobulins and lactoferrin against Escherichia coli and
Micrococcus luteus was also noticed [Séverin and Wenshui, 2005; Moatsou,
2010]. Immunoglobulins are very important group of proteins exhibiting
antimicrobial activity. These compounds are globulins of high molecular
weight and occur in plasma and body fluids. Three major classes of
immunoglobulins are distinguished, i.e. IgG, IgM and IgA, depending on
physical-chemical structure and biological activity. IgG dominate in milk of
ruminants (approximately 80%), while IgA in other mammalian milk,
including human (approximately 90%). They determine the specific humoral
immunity of the body [El-Loly and Farrag, 2007]. During the process of
antigens binding as well as phagocytosis or complement activation these
proteins are involved in the destruction of pathogenic microorganisms, i.e.
Escherichia coli, Candida albicans, Clostridium difficile, Shigella flexneri,
Streptococcus mutans and Helicobacter pylori. Furthermore, immunoglobulins
block the action of toxins and viruses [Gapper et al., 2007].
The study of Litwińczuk et al. [2011], carried out on milk of cows of four
breeds, i.e. Black-White and Red-White variety of Polish Holstein-Friesian,
Simmental and Jersey, proved an effect of SCC on changes in whey protein
content (Table 6). It was found that the rise of somatic cell count decreased the
content of major albumins, i.e. α-LA and β-LG, to a small extent and that was
confirmed by very low, statistically insignificant correlation coefficient
obtained (r=-0.07 and r=-0.05, respectively). Negative value of the correlations
indicates, however, the direction of changes and may suggest that in more
advanced disease states a decline in these protein concentrations in milk can be
higher. Wickström et al. [2009], found a significant decrease in α-LA
concentration with an increase in somatic cell count in bulk tank milk obtained
in Sweden.
The authors also observed a reduction in β-LG concentration, along with
the decline in α-LA content. Similar tendencies were obtained in the study of
Bleck et al. [2009], including two herds maintained in U.S., i.e. the University
Illinois herd and the University Minnesota herd, wherein for the first herd
achieved a negative correlation between logSCC and α-LA (r=-0.059) and for
the second herd – positive (r=0.177).
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Table 5. Correlation coefficients (r) between SCC and milk yield as well
chosen milk components [Litwińczuk et al., 2011; Król et al., 2012]
Milk
Breed Casein BSA Lactoferrin Lysozyme IgG
yield
Polish
Holstein- -0.245** -0.573*** 0.711*** 0.687*** 0.694*** -
Friesian
Simmental -0.123 -0.691*** 0.577*** 0.710*** 0.603*** -
Jersey -0.148 -0.723*** 0.472*** 0.540*** 0.693*** -
Total -0.157 -0.591*** 0.591*** 0.652*** 0.632*** 0.790
**
– significant at P<0.01; *** – significant at P<0.001.
Table 6. Comparison of values (%) of normal milk with that of mastitis

milk having high somatic cell count [Jones and Bailey, 2009;
Litwińczuk et al., 2011]
Jones and Bailey, 2009 Litwińczuk et al., 2011 Direction

Normal Milk with Normal Milk with of
milk high SCC milk high SCC changes
Fat 3.5 3.2 - -
Lactose 4.9 4.4 - -
Total protein 3.61 3.56 3.75-4.08 3.56-4.06
Casein 2.80 2.30 2.81-3.14 2.44-2.82
Whey proteins 0.8 1.3 - -
Serum albumin 0.02 0.07 0.04-0.05 0.06-0.08
Lactoferrin 0.020 0.100 0.007- 0.010-0.012
0.009
Immunoglobulins 0.1 0.6 - -
α-LA - - 0.100- 0.092-0.098
0.120
β-LG - - 0.31-0.38 0.27-0.33
Content of immunoactive proteins (lactoferrin and lysozyme) and bovine

albumin serum increases, however, with a rise of somatic cell count. In the
research of Litwińczuk et al. [2011], milk with the highest SCC (501-1,000
thous. ml-1) included averagely more lactoferrin (by 34.8%), lysozyme (by
60.2%) and BSA (by 64.7%), in comparison to milk with SCC below 100
thous. ml-1. The authors confirmed a substantial effect of SCC on
immunoactive proteins and bovine albumin serum content by relatively high
positive values of the correlation coefficients calculated. For lactoferrin

content r was amounted to 0.65, for lysozyme – r=0.63 and BSA – r=0.59. In
the case of bovine albumin serum, these correlations were clearly
differentiated at certain breeds of cows (Table 5). The highest relationship, i.e.
at the level of r=0.711, was obtained for Holstein-Friesian cows, while a
noticeably lower dependence was found for Simmental (r=0.577) and Jersey
cows (r=0.472). Higher sensitivity of Holstein-Friesian cows to udder
infections was manifested by significantly greater drops in their daily yield of
milk. Therefore, it can be assumed that in Simmental and Jersey cows the SCC
growth is not followed by such intensive permeation of bovine serum albumin
from blood to milk, as it was observed in Holstein-Friesian cows. This would
indicate a higher resistance of Simmental and Jersey cows to mammary gland
infections. Furthermore, Urech et al. [1999], in the study of quarter milk,
noticed similar tendencies when 100 thous. cells ml-1 were recognized as the
threshold limit of somatic cell count. Quarter milk, obtained from clinically
healthy mammary glands, contained an average of 84 thous. somatic cells ml-1,
whereas the milk from infected glands included 293 thous. cells ml-1. The
authors showed the significant rise in the content of lactoferrin (by 0.45%),
BSA (by 0.10%) and immunoglobulins (by 0.39%) in milk from affected
udder. Hamann [2002] defined “the gold standard” for SCC at the level of 100
thous. ml-1. Higher somatic cell count testifies, in his opinion, to a
dysfunctional milk secretion, what leads to reduction in daily milk production,
changes in milk chemical composition and deterioration of technological
properties. However, similar tendencies and statements are also included in the
papers of other authors [Piccinini et al., 2006; Berlung et al., 2007; Barłowska
et al., 2009; Forsbäck et al., 2009]. Lindmark-Månsson et al. [2000 and 2006]
observed that a somatic cell count of over 5 thous. ml-1 increases lactoferrin
content in milk, and a close relationship between this component and udder
health status has been confirmed by very high correlation coefficients between
milk lactoferrin concentration and somatic cell count (r=0.962 and r=0.918)
obtained in two independent studies. Furthermore, Nudda et al. [2001], in the
research carried out on the milk obtained from Sarda sheep, also showed the
significant differences in whey protein content between SCC groups, and for
lactoferrin, BSA and IgG the significant positive correlations with somatic cell
count were noticed, amounting respectively: r=0.39, r=0.31 and r=0.35. Higher
correlation coefficient between SCC and BSA (r=0.53) was stated in the
research of Poutrel et al. [1983], conducted on milk of Holstein and Friesian-
Holstein breed. Król et al. [2012] received, however, high correlation
coefficient between SCC and IgG (r=0.790). A significant increase in
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lactoferrin, albumin and IgG content with deterioration of mammary gland

health status was also confirmed in the research of other authors [Leitner et al.,
2004; Piccinini et al., 2006; Liu et al., 2007].
6. SCC AND TECHNOLOGICAL PARAMETERS OF MILK

Raw material intended for processing should be characterized by the
appropriate technological indicators, predisposing it to produce a dairy
product. It should be noticed that basic chemical composition, acidity, thermal
stability of milk and rennet clotting time are the most major indicators.
In the production of many dairy products, content of non-fat dry matter,
especially total protein, including casein, is considered to be of great
importance. Casein fraction determines the clotting time, curd firmness and
cheese yield from a milk volume specified. κ-casein is the sole casein fraction
sensitive to an addition of rennet (chymosin enzyme). However, it has no
sensitivity to calcium presence. κ-casein stabilizes other casein fraction toward
calcium, forming with them the micelles. It is precipitated at pH value 4.6 at
20°C. κ-casein specific feature is the ability to coagulate, both enzymatic and
acid, which is used in the production of rennet and curd cheese. Raw material
with high protein content is also needed in the production of fermented
beverages as it is responsible for binding an appropriate amount of water in
product. As a consequence, the product is stable and resistant to syneresis. The
whey protein with an importance in milk processing is β-lactoglobulin. During
the thermal treatment it is denatured, causing an exposure of -SH groups. -SH
groups bind the metal ions (especially copper and iron) and as a result they
inhibit the oxidation of milk fat in dairy products. The negative effect of β-
lactoglobulin denaturation is a binding of the molecules denatured with κ-
casein. Nevertheless, the binding hinders the process of enzymatic
coagulation. In the cheese production also a great importance has protein to fat
ratio. Furthermore, lactose presence in milk enables an acidification of milk,
owing to the fact that as a sugar lactose is a food for lactic acid bacteria
[Barłowska, 2007].
The preparation of stable dairy products such as UHT milk and cream,
sterilized drinking milk, unsweetened condensed milk and fermented
beverages requires a high temperature or a little lower but with a longer time
of duration. With regard to this, the raw material which is capable of physical
endurance of heat treatment used is needed, and thus of a high thermal
stability. This term is generally understood as the ability to retain the colloidal
properties of milk, in particular proteins, during high temperature operation. In

fact, low stability may cause sedimentation of proteins denatured in the final
product and occasionally even its gelification during the storage [Singh and
Creamer, 1992; Kruk, 2001; Faka et al., 2009]. Thermal stability of milk is not
constant and depends directly on its chemical composition and physical
characteristics. Milk as a raw material meets the quality criteria in this regard
if it withstands the time of heat treatment in temperature of 140°C≥8 min
[Kruk, 2001; Litwińczuk, 2012]. One of the direct factors that determine
thermal stability of milk is its acidity. The research of Barłowska et al. [2010]
indicates a significant negative correlation between active acidity (pH values)
and thermal stability of milk (r=-0.30). Thermal stability of milk increases in
the pH value range from 6.4 to 6.7 and at pH value above 6.7 it begins to
reduce significantly, reaching a minimum at pH value 6.9. The parameter
value begins to rise afresh at pH>6.9 [Singh and Fox, 1986, 1987; Rattay and
Jelena, 1996]. Singh and Fox [1985a, b, 1986, 1987] explained the reduction
in thermal stability of milk at pH value proximate to 6.9 as the result of
dissociation of -casein complex with whey proteins. This contributes to
higher sensitivity of micelles to high temperature and calcium ions operation
[Singh, 1995]. van Boekel et al. [1989a, b] stated that high thermal stability of
casein micelles at pH<6.7 (where whey proteins deposit and bind) was caused
by binding of calcium ions in the initial phase of the process, which reduced
the concentration of Ca2+ in milk. Furthermore, thermal stability of milk is
determined by the content of whey proteins and calcium ions. In milk with
normal concentration of whey proteins a protective activity of these proteins in
relation to casein and vice versa, i.e. casein with regard to whey proteins, is
observed.
On the one hand, whey proteins denatured undergo a microfloculation on
the casein micelle surface (in the order: serum albumin, β-lactoglobulin and α-
lactalbumin, according to the heat resistance), which prevents their stronger
aggregation and loss out of solution. On the other hand, they block calcium
access to the micelles (by interacting with casein) and as a result milk obtains
better stability. The micelle size also greatly influences on milk heat stability.
Small micelles contain relatively more -casein which stabilizes the remaining
casein fractions to calcium ions. Therefore they are more resistant to high
temperature (140C) [O’Connel and Fox, 2000]. Barłowska et al. [2010]
reported significant positive correlation between milk thermal stability and
rennet clotting time (r=0.32).
A crucial indicator determining the suitability of milk for rennet cheese
production is rennet clotting time. Defective milk, i.e. obtained from cows
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with udder inflammation, may clot after 20 minutes or does not coagulate at
all. The rate of clot formation and degree of firmness are largely dependent on
the casein content in milk [Ikonen et al., 2004], proportion of calcium to
nitrate compounds (0.2 – for slowly coagulating milk and 0.23 – for normal
and quickly coagulating milk) and casein micelle size [Litwińczuk, 2012]. It is
considered that rennet clotting time of milk is dependent on protein content, in
that casein primarily. Nevertheless, research results are quite divergent with
regard to these relationships. Analyzing milk of Finnish Ayrshire cows, Ikonen
et al. [2004] stated the relationship between coagulation time (or curd firming
time) and content of protein and casein. Similar analyses, which were
performed by Oloffs et al. [1992] on milk of Friesian cows and Ikonen et al.
[1999] on milk of Finnish cows, showed that shorter coagulation time was
associated with lower protein content. However, Oloffs et al. [1992],
evaluating milk of Angler cows, did not show any dependences. Results of
curd firmness assessment obtained by the various authors were also divergent.
In Oloffs et al. [1992], high values for curd firmness correlated with high
protein and casein content, whereas Ikonen et al. [1999, 2004] indicated a
reverse tendency, i.e. high values for curd firmness correlated with low protein
and casein content. Ability of milk to enzymatic coagulation depends greatly
on the size of casein micelles. Large micelles contain relatively less -casein,
which functions as a stabilizer for micelle particles, and thereupon milk
coagulates quickly [Ziajka, 2008]. Content of calcium in milk is considered of
great importance to enzymatic coagulation processes [Nájera et al., 2003;
Barłowska et al., 2010]. Milk coagulation time significantly affects the
firmness of curd formed. Ikonen et al. [2004] confirmed this strong
relationship by very high correlation coefficients (rg=-0.97 and rp=-0.92).
Breed of cows is crucial factor determinig milk suitability to cheese
production [Okigbo et al., 1985a, b; Malossini et al., 1996; Tyrisevä et al.,
2004]. Research of numerous authors indicate that cows of local breeds
produce milk which faster coagulates and curd obtained is more firm, in
comparison with highly productive breeds [Chiofalo et al., 2000; Barłowska
and Litwińczuk, 2006; De Marchi et al., 2007; Litwińczuk et al., 2012].
Furthermore, in the latter a large proportion of noncoagulating milk samples is
stated. Ikonen et al. [2004] found that in 4,700 milk samples collected from
Finnish Ayrshire cows approximately 13% of them (618 samples) had not
coagulated, i.e. they had not aggregated and formed any curd. Kübarsepp et al.
[2003] stated 8% of noncoagulating milk samples in dairy cattle breeds raised
in Estonia (Estonian Holstein, Estonian Red and Estonian native breeds) and
slightly more (11%) in Red and White Holsteins. Ikonen [2000], however, did
not noticed such problem in milk of Holstein-Friesian and Finnish cows.
Casein, as an essential milk component deciding about its suitability for
processing, particularly for cheese production, usually declines in
inflammations with accordance to mastitis status. This is due to the fact that
protein fraction is synthesized whole in the mammary gland. Mammary gland
infection results in the changes in milk component secretion, inter alia, the
noncasein fraction (NCN fraction) is found to be elevated, while the casein
content is decreased. It occurs partly due to increased proteolysis leading to a
reduction in the casein to total protein ratio in infected quarters. And this may
be linked to increased endogenous proteolysis which eventuates from the
elevation of plasmin or other proteases derived from somatic cells.
The result of increased permeability of mammary epithelium is the influx
of blood proteins (immunoglobulins, especially IgG, and bovine serum
albumin) into milk, which results in an elevated NCN content [Ogola et al.,
2007]. Forsbäck et al. [2009], analyzing milk of Swedish Red Breed and
Swedish Holstein, confirmed the fact of reduction in casein content in milk
with somatic cell count rise, i.e. from 2.61% at SCC<100 thous. ml-1 to 2.56%
at SCC>300 thous. ml-1 (P≤0.05). In the research of Litwińczuk et al. [2011],
carried out on milk of cows of four breeds, i.e. Black-White and Red-White
variety of Polish Holstein-Friesian, Simmental and Jersey, a downward
tendency for casein content was also showed. Its level declined in milk with
SCC rise, regardless of the breed of cows and production season. A distinct
negative relationship between milk casein and SCC was confirmed by a
relatively high value of correlation coefficient (r=-0.591 at P<0.001).
Nevertheless, it should be emphasized that the values of this coefficient were
various for particular breeds (Polish Holstein-Friesian – r=-0.573, Simmental –
r=-0.691 and Jersey – r=-0.723), which indicates the sundry sensitivity of
these cow breeds to udder inflammations.
As already mentioned, the milk acidity has significant effect on its
resistance during heat treatment. Normal (fresh) milk, derived from cows with
healthy udder, should have pH range from 6.5 to 6.8. Such pH guarantees the
colloidal stability of milk [Litwińczuk, 2012]. Many authors [Ikonen et al.,
2004; Bansal et al., 2005; Ogola et al., 2007] indicated the rise in values of
active acidity in milk taken from infected quarters. Higher levels of citrate and
bicarbonate found during udder inflammation may be responsible for elevated
pH levels. Ogola et al. [2007] showed the increase in pH value to 6.81 in milk
with elevated somatic cells count (SCC>750 thous. ml-1), while in milk
contained less than 250 thous. ml-1 this value was equal to 6.63. However, the
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differences were statistically insignificant. Results obtained by Ikonen et al.

[2004] confirmed these relationships by the positive correlation coefficients
between SCC and pH values (rg=0.16 and rp=0.26).
Udder inflammations also cause the changes in proportions of milk
proteins and mineral components, and consequently the reduction of milk
colloidal stability. In mastitis milk content of whey proteins increases, and as
the result a protective effect of casein in relation to them becomes insufficient.
This causes an imbalance between -casein and β-lactoglobulin, for which the
optimum molar ratio should be equal to 1 in normal milk [Żbikowska and
Szerszunowicz, 2002]. Furthermore, an increase in Ca and P content in milk
also lowers the thermal stability.
The balance between calcium and magnesium ions as well as phosphates
and citrates is greatly important for this parameter of milk technological
suitability [Ziajka, 2008].
Increase of SCC in milk causes an elongation of rennet clotting time or its
absence. Longer coagulation time of milk results in a decrease of curd
firmness, impairment of syneresis processes, raised cheese moisture and
reduced cheese yield efficiency (high losses of casein which passes to whey).
This is mainly due to the changes in content of milk components (the changes
in distribution of proteins, including casein, decline in lactose content, changes
in concentration of minerals, mainly calcium reduction).
The fact of clotting time lengthening due to milk SCC increase confirms
the results of many authors [Nudda et al., 2001; Ikonen et al., 2004; Zumbo et
al., 2004; Barłowska et al., 2009]. Ikonen et al. [1999, 2004] indicated strong
genetic correlations between milk coagulating properties (MCP), i.e. rennet
clotting time (RCT), curd firming time (k20) and curd firmness (a30), and SCS
estimated for cows of Finnish Ayrshire breed. They suggested that selection
for low SCC could improve MCP and reduce the occurrence of noncoagu-
lating milk samples. On the basis of the research of Barłowska et al. [2009],
conducted on cow milk of four breeds (Black-White and Red-White variety of
Polish Holstein-Friesian, Simmental and Whiteback), it should be also
emphasized that cows of Simmental and native Polish Whiteback breed
produced milk of noticeably better suitability to cheese production. It was
proved by evidently shorter milk enzymatic coagulation time (moment of the
first flakes of casein loss) for Simmental and Whiteback breed, which
amounted from 4:32 to 5:41 min at SCC<400 thous. ml-1, in comparison with
milk of Holstein-Friesian cows (from 7:05 to 8:32 min) – Table 7.
They also showed that milk with somatic cell count above 1,000 thous. ml-
1
had longer coagulation time by approximately 20-30% (depending on breed),
with regard to the milk samples at SCC from 201 to 400 thous. ml-1. Ikonen et
al. [2004] confirmed these strong relationships between SCC and milk
technological parameters to cheese production by genetic correlation
coefficients obtained, i.e. between SCC and RCT – rg=0.29 as well as SCC and
a30 – rg=-0.45. With regard to milk of Sarda sheep breed the similar
relationships between SCC and coagulation properties of milk were also noted
[Nudda et al., 2001]. Rennet clotting time significantly (P<0.01) lengthen from
16.05 min at SCC<300 thous. ml-1 to 23.64 min at SCC>2,000 thous. ml-1.
Furthermore, correlation coefficients obtained between SCC and RCT
(r=0.43), SCC and k20 (r=0.41) as well SCC and a30 (r=-0.43) were statistically
significant (P<0.01).
As mentioned above, a right behavior of milk during various technological
processes is determined by the content and proportions of individual minerals.
Udder inflammations cause a decline in Ca, P and K concentration but level of
Cl and Na significantly increases [Bruckmaier et al., 2004; Ogola et al., 2007;
Litwińczuk, 2012]. Ogola et al. [2007] analyzed effect of SCC on Ca, K, Na
and Cl content in 396 samples of quarter milk taken from cows of Holstein-
Friesian and Zebu crossbreed. They showed that Na content was 46.5 mg 100
g-1, K – 146.3 mg 100 g-1, Ca – 119.5 mg 100 g-1 and Cl – 100.5 mg 100 g-1 at
SCC<250 thous. ml-1. Rise in SCC over 750 thous. ml-1 elevated Na
concentration to 78.5 mg 100 g-1 (by over 68%) and Cl to 183.5 mg 100 g-1 (by
over 72%), however, reduced K content to 108.9 mg 100 g-1 (by over 34%)
and Ca to 97.8 mg 100 g-1 (by over 22%). Rise in chlorine concentration in
mastitis milk follows due to decline in lactose content which is an essential
component conditioning milk fermentation and acidification, and as a result
also the syneresis processes in cheese grains. This affects an increase in cheese
moisture and decrease in whey yield. A major mineral component of milk,
which appropriate concentration determines the rennet curd formation, is Ca. It
shields negative functional groups on the micelle surface and plays a crucial
role in formation of intermicelle calcium bridges [Ziajka, 2008]. Therefore, the
decrease in calcium content in mastitis milk is one the factors lengthening its
coagulation time or even contributing to the lack of coagulation. As most milk
Ca is associated with casein micelles, Ogola et al. [2007] reported that reduced
casein content could explain the lowered calcium levels in infected quarters.
Increasing of cellular component content in milk negatively affects not only
the raw material but also its products. During the ripening process of cheese
made from milk with high SCC undesired proteolytic processes occur, which
leads to the reduction in quality of cheeses or disqualification [Marino et al.,
2005; Wickström et al., 2009].
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Table 7. Productivity, basic chemical composition and technological suitability of milk obtained from different cow
breeds, with regard to somatic cell count [Barłowska et al., 2009]
Specification
SCC group
Breed Daily milk Dry matter Protein Lactos Clotting Thermal
(thous. ml-1) Fat (%) Protein/Fat
yield.(kg) (%) (%) e (%) time (min) stability (min)
Black-White I 26.1b 13.24a 3.40a 4.27a 0.81 4.91c 7:05A 4:40
variety of II 26.7b 13.17a 3.42a 4.26a 0.82 4.84b 7:52A 4:20
Polish III 23.8a 13.62b 3.66b 4.46b 0.84 4.84a 7:46A 4:51
Holstein-
Frisian IV 23.7a 13.38ab 3.59b 4.36ab 0.84 4.78a 9:46B 4:25
c b ab c
Red-White I 20.6 13.30 3.34 4.40 0.77 4.91 7:09a 4:32
variety of II 20.5bc 12.96a 3.26 4.23a 0.79 4.82b 8:32ab 4:53
Polish III 18.1ab 13.19ab 3.33 4.49b 0.76 4.73b 8:37b 4:48
Holstein-
Frisian IV 16.5a 13.08ab 3.40 4.43ab 0.78 4.60a 11:02c 4:45
b c a
I 19.5 13.32 3.50 4.29 0.83 4.89 5:41 3:57
II 17.6a 13.16 3.53 4.24 0.85 4.74b 5:16a 3:50
Simmental
III 18.0ab 13.19 3.50 4.38 0.82 4.66a 5:48a 3:54
IV 16.5a 13.29 3.56 4.45 0.82 4.63a 7:40b 3:42
I 12.7b 13.15 3.28a 4.36 0.77 4.85C 4:58ab 4:46
II 9.3a 13.12 3.51b 4.25 0.83 4.71B 4:32a 3:56
Whiteback
III 10.5a 13.08 3.54b 4.24 0.85 4.65B 4:56ab 4:04
IV 11.2ab 13.02 3.54b 4.33 0.83 4.50A 6:12b 4:25
I 21.7b 13.27b 3.42A 4.30ab 0.81a 4.90D 6:24A 4:24
II 20.5b 13.13a 3.44AB 4.25a 0.83b 4.78C 6:40AB 4:13
Average
III 18.9a 13.31b 3.51B 4.41c 0.81ab 4.74B 7:02BC 4:16
IV 18.6a 13.22ab 3.52B 4.40bc 0.82ab 4.66A 9:20C 4:32
I – to 200 thous. ml-1, II – 201-400 thous. ml-1, III – 401-1000 thous. ml-1, IV – above 1000 thous. ml-1;
A, B, C, a, b, c – differences between SCC within a breed; a, b, c – differences significant at P≤0.05; A,B, C – differences significant at
P≤0.01.
CONCLUSION
Udder inflammation remains the most frequent and expensive disease
affecting dairy cattle. For the dairy industry the most pernicious are subclinical
(non-symptomatic) inflammations, which are very often undiagnosed. As a
result, milk with lowered quality becomes a commercial milk. SCC in cow
milk is a good indicator of the mammary gland health status, that is why
clinical and subclinical inflammations occurred are associated with a
significant increase in their number in milk. Inflammations primarily affect a
reduction in the milk production. On the basis of the fact mentioned above, it
could be concluded that highly productive cow breeds are more susceptible to
inflammation, which in turn results in higher losses in milk production in such
herds. Decreased synthetic activity of infected mammary gland are also
revealed in the changes in individual milk component content and in the ratios
between them. As a consequence, milk nutritional value and suitability for
processing is reduced.
Reviewer
Prof. Anna Sawa
University of Technology and Life Sciences
Faculty of Animal Breeding and Biology, Department of Cattle Breeding
Mazowiecka 28, 85-084 Bydgoszcz, Poland
Phone number: +48 52 3749710, e-mail: sawa@utp.edu.pl
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Chapter 4
STRATEGIES TO IMPROVE
THE REPRODUCTIVE EFFICIENCY
OF DAIRY CATTLE
L. S. R. Marinho, F. Z. Machado and M. M. Seneda

Laboratório de Reprodução Animal, DCV-CCA-UEL, Londrina PR, Brazil
ABSTRACT
The reproductive performance of a lactating herd is a major
component of the profitability of a dairy farm. Factors such as negative
energy balance, heat stress and failures in heat detection can severely
compromise reproductive parameters. To overcome these problems, a
variety of strategies can be used. For example, failures in estrus detection
can be solved with the use of fixed-time artificial insemination (FTAI).
Progesterone implants combined with estradiol administration are very
effective in promoting the onset of a new follicular wave. With the use of
a luteolytic agent and an inducer of ovulation, AI can be performed at the
appropriate time without the need for estrus observation. In countries
where the use of such drugs is not allowed, protocols based on GnRH and
PGF2α may also offer optimal synchronization of ovulation. In locations
where pregnancy rates are compromised by high temperatures, a viable

Corresponding author: Marcelo Marcondes Seneda, Laboratório de Reprodução Animal, DCV,
CCA, Rodovia Celso Garcia Cid, Pr 445, Km 380, State University of Londrina (UEL),
Londrina, PR, Brazil, 86051-990, Phone: +55 43 3371-4064, Fax: +55 43 3371-4063,
Email: mseneda@uel.br.
www.ebook777.com
128 L. S. R. Marinho, F. Z. Machado and M. M. Seneda
alternative to FTAI may be the fixed-time embryo transfer (FTET).

Embryos at the morula and blastocyst stage are more resistant to heat
stress than gametes and embryos in early stages of development. Thus,
embryo transfer (ET) on day 7 of development can ensure satisfactory
pregnancy rates throughout the year, even in months and/or regions with
higher average temperatures. ET has also been effective in preventing
early embryonic mortality and increasing pregnancy rates in repeat
breeders. Another strategy that can enhance the reproductive efficiency of
dairy herds is the cryopreservation of embryos; embryos are stored and
can be used at strategic times, such as in the warmer months of the year.
This chapter will discuss technological strategies that can lead to higher
breeding efficiency, improved reproductive efficiency and increased
profitability of livestock on dairy farms.
1. INTRODUCTION
Over the last 50 years, reproductive efficiency has declined greatly in the
dairy industry. Currently, parameters such as conception at first service,
services per conception and calving interval have shown to be deteriorating.
The worsening of these features can be explained by modifications in the
management of dairy farms and by negative genetic correlations between milk
production and fertility. This decline in reproductive performance is of great
concern to milk producers, given the significance of good fertility to the dairy
industry. In addition to adequate nutritional management, which is of major
importance to achieving positive results, a variety of strategies can be used to
ensure better reproductive outcomes. Fortunately, there is currently enough
technology to at least partially reverse this setback. One of the most important
approaches developed to improve reproductive efficiency is artificial
insemination (AI). In the present context, AI is a hugely widespread
technology, and most milk producers use it at some level in their herds.
However, the failure to cycle and display estrus frequently leads to
unsatisfactory outcomes when only AI is used. Therefore, hormonal protocols
have been used to induce estrus and synchronize the moment of ovulation,
increasing the percentage of pregnant animals in the herd.
In addition to fixed-time artificial insemination (FTAI), embryo transfer
(ET) has provided fairly positive pregnancy rates. This strategy is especially
useful in regions with high temperatures because not even FTAI protocols can
offer acceptable rates in cattle with heat stress. The transfer of both in vivo and
in vitro-produced embryos has been widely used to ensure satisfactory
Strategies to Improve the Reproductive Efficiency of Dairy Cattle 129
pregnancy rates throughout the year, even in countries with high temperatures
in the summer. This chapter aims to present some of the most promising
technologies currently available to improve reproductive efficiency in dairy
cattle, as well as their pros and cons. Recent data will be reviewed, and the
most suitable situations to use each technique will be discussed.
2. FIXED-TIME ARTIFICIAL INSEMINATION

The detection of estrus is a determining factor for obtaining good
pregnancy rates. In dairy herds, over 50% of the cows in heat are not detected
due to a lack of mating behavior displayed by the animals (Van Eerdenburg,
2002). High milk production seems to seriously impact this reproductive
factor, as low estrus detection rates are even more pronounced among high-
producing animals (Jeong et al., 2012). The failure to detect estrus also
represents a significant challenge in programs that use cattle with some
proportion of Bos indicus blood, as these animals experience an estrus of
shorter duration and their estrus frequently begins and ends at night (Bó et al.,
2003). In recent years, the use of pharmacological methods to control the
estrus cycle (i.e., FTAI protocols) has done away with the need to monitor for
estrus. These protocols control the rise of follicular waves and regulate luteal
dynamics, promoting synchronization of the moment of ovulation (Nasser et
al., 2004). In addition to increasing the number of animals subjected to
insemination, FTAI also has brought dairymen great advantages in strategic
management of the reproduction of the herd. A wide range of synchronization
protocols for FTAI based on a variety of natural and synthetic drugs are
available on the market. Some of the most commonly used hormones are
prostaglandins, progestagens, estradiol, equine chorionic gonadotropin (eCG),
human chorionic gonadotropin (hCG) and gonadotropin-releasing hormone
(GnRH).
2.1. Drugs Most Frequently Used for Estrus Synchronization
2.1.1. Prostaglandin
Prostaglandin F2α (PGF2α) and its synthetic analogues interrupt luteal
activity and are widely used to regulate the estrus cycle of lactating dairy
cows. The action of this drug depends on how developed the dominant follicle
(DF) is at the time of the administration. If the DF is too mature to ovulate,
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only the DF of the next wave will be affected, resulting in a longer time span
until the next rut occurs.
However, if a DF able to ovulate is present, the manifestation of estrus
occurs approximately 48 h after the treatment with PGF2α. In general,
approximately 50-60% of cows treated with PGF2α rut within a period of 36 to
130 h after administration (Whittier et al., 1989). Some protocols have been
designed based on single or double doses of PGF2α to reduce treatment costs.
However, these protocols require estrus detection for a few days and/or the
detection of a corpus luteum (CL) that is likely to be responsive to the
treatment (CL of day 6 to 17 of the estrus cycle). One effective way to use the
luteolytic effect of PGF2α is to combine PGF2α with progesterone in cycling
cows. In general, females are treated with progesterone for 7 to 9 days and
PGF2α is administered 0 to 2 days before progesterone withdrawal.
2.1.2. Progesterone and Estradiol

The use of progesterone with estradiol controls the rise of follicular waves
by promoting atresia of the developing follicles and regulates CL function and
ovulation time. When combined with a luteolytic agent and an ovulation
inductor, this treatment allows the use of AI at a defined time without estrus
observation and with stable pregnancy rates. Estrus observation is not needed
and is actually not recommended because FTAI systems frequently induce
fertile ovulation without estrus expression (Thatcher et al., 2002). Such
hormonal protocols can also increase ovarian activity. Progesterone and its
synthetic analogues (progestagens) prevent the manifestation of heat because
they mimic the endocrine activity of a CL. Progesterone supplementation is
also an effective method for treating anestrus, which is a common problem in
dairy production systems.
The removal of the progesterone is followed by estrus, ovulation, and a
normal-length luteal phase in a large percentage of treated cows (Lucy et al.,
2004). Currently, synthetic progestagens are best supplied in the form of
subdermal ear implants; intravaginal implants are mostly used to release
progesterone itself. The releasing devices vary in shape, design and the
amount of hormone released. Estradiol suppresses the release of FSH, thus
inducing the atresia of minor follicles. Progesterone decreases the release of
LH, thus restricting the activity of larger follicles. It is therefore expected that
all follicles in the ovaries reach atresia. It is also likely that a new follicular
wave appears after 3 to 4 days of treatment with estradiol and progesterone
(starting from any day of the estrus cycle).
Figure 1. Example of a fixed-time artificial insemination (FTAI) hormonal protocol

used for lactating dairy cows. Estradiol benzoate is administered on a random day of
the estrus cycle with a progesterone-releasing device; on day 8, the device is removed,
together with a cloprostenol (a synthetic analogue of prostaglandin F2α) and eCG
(equine chorionic gonadotropin) administration; 24 h later, a new dose of estradiol
benzoate is administered; gonadorelin (synthetic analogue of GnRH - gonadotropin-
releasing hormone) is given 24 h later; following 8 to 10 h, timed-AI is performed.
Additionally, estrogen is essential for the expression of oxytocin receptors

in the endometrium which are critical to the release of PGF2α for CL
regression. Therefore, estrogen has been used for both the synchronization of
follicular waves and the promotion of luteolysis. Several drugs accomplish
these purposes. Esters of estradiol, estradiol benzoate (EB) or estradiol
cypionate (EC) have the lowest cost and are the most commonly used
inductors in traditional protocols. Intervals to wave emergence depend on the
dose and the half-life of the ester used. Hormones such as GnRH, LH and hCG
may also be used as ovulation inducers, but their use is less common due to
their higher costs. With the use of ovulation inductors, FTAI can be performed
52 h after the removal of progesterone, i.e., 8 to 12 h before the planned time
of ovulation (Hanlon et al., 1997). An example of a FTAI protocol with the
use of a progesterone-releasing device and estradiol is illustrated in Figure 1.
2.1.3. GnRH
GnRH is a hypothalamic hormone that acts by triggering the pituitary
release of FSH and LH, thereby inducing ovulation. Despite having a short
half-life in plasma (2 to 4 min), a single administration of GnRH results in an
enhanced and simultaneous release of both LH and FSH in a log-dose response
manner. In FTAI protocols, the ovulatory GnRH dose is typically given 48 h
after a luteolytic dose of PGF2α. In countries where the use of certain drugs
such as estrogen is not allowed, protocols with GnRH and PGF2α are highly
convenient for FTAI in dairy cattle. Both hormones were of great importance
for the consolidation of the FTAI protocol and the initiation of a series of other
protocols. In addition, GnRH can effectively be used to restore the cycling of a
female after calving because the ability of the pituitary to respond to GnRH is
restored approximately 20 days postpartum.
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2.1.4. eCG
Known as a mixed bioactive drug, eCG has been widely used in FTAI
protocols. It can be employed both at the end of the treatment and at the
emergence of the new wave because eCG is composed of 2/3 FSH and 1/3 LH.
Souza et al. (2009) reported improvement in the fertility of dairy cows with
low BCS treated with eCG on day 8 of the FTAI protocol. This effect was
most likely due to an increase in activity of the ovulatory follicle (and
consequently, of the CL) stimulated by this drug. High-producing milk cows
have high levels of hepatic metabolism of ovarian steroids; the decrease in
circulating progesterone during the luteal phase may therefore suppress early
embryonic development. Treatment with eCG prior to ovulation can increase
circulating progesterone levels and provide higher pregnancy rates in animals
with low BCS.
2.2. Association of GnRH and PGF2α: Ovsynch
Based on a GnRH and PGF2α combination, the Ovsynch program and its
variations are the most commonly used protocols for FTAI on North American
dairy farms. The first administration of GnRH occurs on a random day of the
estrus cycle and stimulates the ovulation of the current dominant follicle.
Ovulation is expected to happen within 2 or 3 days followed by the beginning
of a new follicular wave. In order for the luteolytic process to occur, a PGF2α
injection is required; such an injection takes place 7 days after the first supply
of GnRH. A second dose of GnRH is used 48 h after the PGF2α administration
to promote ovulation of the new DF. Ovulation then occurs in approximately
24 h, enabling the use of FTAI within 16 to 20 h (Pursley et al., 1995).
Figure 2. Ovsynch is a fixed-time artificial insemination (FTAI) program that

combines GnRH and PGF2α. GnRH is administered in a random day of the cycle; 7
days later, PGF2α; 48 h later, GnRH again; and AI 16 to 24 h after the last GnRH
administration.
The Ovsynch program is represented in Figure 2. It is possible that some

females may not respond to the initial application of GnRH, which can occur
in phases where there is no dominant follicle to ovulate, such as in the
beginning or middle of the estrus cycle, and can disrupt the entire sequence of
the protocol.
This is one of the critical problems associated with the Ovsynch program.
Another important factor to consider is the number of follicular waves. The
higher the number of waves, the less satisfactory the results will be. At the
beginning of every follicular wave, there is a range of 4 days during which
GnRH has no effect. When there are two follicular waves in the estrus cycle,
there are two intervals of 4 days (the beginning of the waves). These periods
where no response to GnRH can occur increase when the cycle has three
waves, or three 4-day intervals, corresponding to 12 days in which the first
application of the protocol will not be effective.
The number of waves is influenced by a number of factors, including the
age of the cow. Two-wave cycles are more common in older cows than in
heifers (Moreira et al., 2000). Diet can also influence the number of waves, as
the type of feed provided can greatly influence the hepatic metabolism of
steroid hormones. During digestion, a diet rich in grains requires greater
hepatic activity, consequently generating a low serum concentration of steroid
hormones such as progesterone. Lower levels of progesterone will lead to an
increase in LH levels because less of this gonadotropin will be inhibited by
progesterone. With higher levels of LH in the system, the DF present in the
first wave of the cycle may remain available for longer, extending its wave
duration and delaying the start of the next one. As a result, the third wave will
not have time to occur because the hormonal profile at the end of the second
wave will match that of the beginning of the third, thus culminating in
ovulation.
This type of highly concentrated diet is typically given to high-producing
cattle, explaining why these cows tend to have two follicular waves rather than
three. This high metabolic clearance rate, leading to a reduction in the levels of
circulating estradiol, can also result in a short duration of estrus, which
explains why it is difficult to detect signs of estrus in dairy herds (Wiltbank et
al., 2006). One approach for obtaining a better reproductive outcome in dairy
cattle is to use three consecutive FTAI protocols and later relocate the cow for
natural service by bulls. This allows the servicing of cows with several
inseminations before transfer and typically results in a 15% greater chance of
pregnancy. The resynchronization can be performed with either Ovsynch
program protocols or with progesterone implants.
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2.3. Important Considerations for FTAI In Dairy Herds
The use of FTAI protocols in dairy cattle is intended to decrease the

common flaws that occur when relying on estrus observation and to optimize
handling. However, the expected pregnancy rates with the use of hormonal
protocols are similar to the ones obtained without the use of any drug when
simply monitoring cows for signs of estrus. Therefore, the cost-benefit ratio
and the pros and cons of the implementation of FTAI must be clear and
rationally determined before using this tool. Most protocols of
pharmacological control of estrus provide benefits, and major additions to
reproductive efficiency can be expected when they are used in herds with
adequate conditions.
Some dairy breeds are particularly sensitive to climatic variations.
European breeds such as Holsteins and Jerseys suffer great thermal discomfort
under conditions of high temperatures and high humidity. Thermal stress is
very damaging to FTAI as gametes are sensitive to these conditions.
Nevertheless, it is important to remember that the male is responsible for half
of the process of fertilization; therefore, it is also necessary to rigorously
analyze the quality of the semen.
3. EMBRYO TRANSFER IN DAIRY COWS

South America currently leads the world in both in vitro and in vivo
bovine embryo production. Such a position is interesting when considering
that the predominant racial type in South America is Bos taurus indicus, also
known as Zebu, which is highly adapted to the tropics. Zebu cows naturally
produce more oocytes than taurine breeds, which leads to a higher number of
in vitro-produced (IVP) embryos and pregnancies. The larger number of
pregnancies justifies, in many occasions, replacing the in vivo-production of
embryos with the in vitro technique. This finding contributes to a large-scale
commercial application of in vitro fertilization (IVF). By promoting a prior
selection of donors and bulls, it is possible to achieve high levels of
productivity; this usually results in lower costs, thus enabling the use of IVF
on a commercial scale.
Despite the rapid development of the technique since its emergence in the
late 1980s, until a few years ago, IVEP was only used as a last resort when
traditional techniques failed. However, the high genetic gains provided by
IVEP to the herds and the constant pregnancy rates achieved with this system
have contributed to making this system a first-line option.
3.1. Embryo Transfer
Embryo transfer (ET) is a term generally used to define more than one
biotechnological technique. It involves the production and transfer of embryos
generated either in vivo by the technique of Multiple Ovulation and Embryo
Transfer (MOET) or in vitro. In both cases, the purpose is to obtain genetically
superior embryos and to generate pregnancies in female recipients. These
biotechnologies aim to produce a much larger number of offspring than would
be possible by natural methods of reproduction throughout the lifetime of a
female.
An additional advantage provided by these biotechnologies is a better
sanitary control of the reproductive process, especially with regard to diseases
of the reproductive tract. In addition to preventing sexually transmitted
diseases, the embryos can undergo sanitary procedures before the transfer,
further minimizing the chance of transmission of pathogens. Embryo transfer
can also be used to obtain descendants from donors that have acquired
reproductive disorders or any other non-congenital condition that could
prevent the female from producing and carrying healthy embryos. Thus, it is
possible to prevent the premature discarding of genetically superior females
that have acquired different types of reproductive disorders. Finally, these
biotechnologies allow the performance of basic research on the physiology of
reproduction and of surveys to assist the development of other biotechnologies
such as cloning and transgenesis.
3.2. Selection of Donors
To be selected as embryo donors, females must have high levels of milk

production. It is also very important to evaluate the reproductive performance
of the donors; if their reproductive efficiency is good, the chances of getting
the expected results with ET are higher. Donors must be free of infectious
diseases such as brucellosis, tuberculosis, leucosis, leptospirosis, IBR and
BVD.
Although some of these diseases can be controlled by treating the embryos
before the transfer, the efficiency of embryo production in these animals may
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be compromised by the infectious process. Donors with stressful conditions

such as hoof or udder disorders generate poor results and should therefore be
treated or allowed to recover from such situations before being included in ET
programs.
3.3. Multiple Ovulation and Embryo Transfer (MOET)
This technique is divided into five steps:
 Selection of donors and recipients;

 Superovulation and artificial insemination of the donor;
 Preparation of recipients;
 Embryo collection;
 Evaluation and transfer of embryos.
Superovulation aims to stimulate the growth and ovulation of the highest

possible number of follicles in a follicular wave. The administration of
hormones with gonadotrophic activity prevents the phenomenon of dominance
which would lead to atresia of many minor follicles. One of the biggest
drawbacks of the technique is the high individual variability in the response to
superovulation among the donors; an aggravating 20 to 30% of donors do not
produce any transferable embryo. The choice of the hormonal protocol should
be carefully evaluated, taking into consideration the breed, weight and
production of donors, the condition of the property and the skill of the
employees who will perform the work. An example of hormonal protocol used
for superovulation is described in Table 1. In general, the embryo collection is
performed seven days after the insemination of the donor. During this period,
the embryos are in the uterine lumen and at the morula or blastocyst stage, the
most suitable ones for transfer and cryopreservation. The collection method
mostly used currently is uterine flushing via the cervix. The viable embryos
that are found are categorized and transferred into the recipients via
transcervical or surgical implantation. In general, it is possible to perform
MOET in animals ranging in age from 10 months to 18 to 20 years. However,
very young heifers exhibit highly variable ovarian responses. Furthermore, the
size of the pelvis and the size and tortuosity of the cervix should be
considered, as they could potentially hinder the necessary procedures and
jeopardize the success of the collection. Senescent cows usually present with
lower production levels, and production rates tend to decrease as animals age.
Table 1. Example of hormonal protocol used for the superovulation

of bovine females
Day Time Treatment

D0 a.m. P4 Device Insertion + E2
a.m. FSH (20% dose)
D4
p.m. FSH (20% dose)
a.m. FSH (15% dose)
D5
p.m. FSH (15% dose)
a.m. FSH (10% dose) + PGF2α
D6
p.m. FSH (10% dose) + P4 Device Removal
a.m. FSH (5% dose)
D7
p.m. FSH (5% dose)
a.m. Estrus observation
D8
p.m. A.I. (12 h after estrus)
D9 a.m. A.I. (24 h after estrus)
a.m. Recipients evaluation
D 15
p.m. Embryo collection + embryo transfer
Doses: estradiol benzoate (E2): 2 mg IM; prostaglandin (PGF2α): 2 mL IM. FSH doses
vary according to breed, animal category and manufacturer.
3.4. In Vitro Embryo Production (IVEP)
IVEP aims to produce embryos in the laboratory using oocytes from

ovaries of slaughtered or living cows. Oocytes and sperm are prepared and
matured in vitro for the fertilization and subsequent embryo formation after a
period of in vitro culture. The embryos are then transferred to properly
prepared female recipients. In terms of genetic merit and sanitary aspects, the
same criteria previously mentioned in this chapter should be applied.
Specifically, the reproductive condition of females should be evaluated by
ultrasonography at the exact time of oocyte retrieval. As a strategy for
improving the cost/benefit ratio of IVEP, ideally only donors with a large
number of follicles would be subjected to OPU. Although all visible follicles
can be aspirated, there is a better retrieval of oocytes when the diameter of the
dominant follicles is <4 mm (Seneda et al., 2001). The animals that are
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subjected to follicular puncture should be evaluated periodically to control the

appearance and severity of the injuries caused by the aspiration procedure. In
general, there are few alterations in the vagina and cervix, and those that do
occur are mostly transient irritations. Sequelae such as fibrosis and adhesions
can occur in cows subjected to several sessions of follicular aspiration if the
procedures were not properly performed (Gibbons et al., 1994). It is important
to note that follicular aspiration is a technique that has pros and cons. The risk
of sequelae exists and should be considered. The procedure must be performed
with minimal damage so that the results outweigh the expected disadvantages.
3.4.1. Strategic Use of IVP Embryos in Dairy Farming

The large amount of oocytes and IVP embryos produced by Bos indicus
females has made IVEP commercially very attractive in recent years. When
the first commercial laboratories emerged, the demand was very limited. The
interest from breeders was small and the expense of the services almost
restricted their use to elite beef cattle producers. However, over the last six or
seven years, dairy farmers have begun to make greater use of the technique of
follicular aspiration and IVEP with the goal of rapidly multiplying the number
of animals with high genetic potential. During this period, IVEP became a
commercially viable alternative to improve pregnancy rates and speed up
genetic improvement. However, until a few years ago, large-scale IVEP was
limited by several drawbacks. One of them was the long distances between the
laboratories and the properties where the recipients were held. In Brazil, for
example, the large cattle herds are usually located in new areas of livestock
production, such as the northern region. Oocyte donors and the laboratories
which service them, on the other hand, are concentrated mainly in the south
and southeast regions of the country, thousands of miles away from the farms
with the recipient animals. The limited ability of IVP embryos to be
cryopreserved greatly restricted the contact between production and transfer
sites. Consequently, embryos that could not be transferred fresh were often
discarded.
Recently, some of these problems have been overcome. In a large-scale
IVEP program using exclusively sexed semen from bulls of Holstein and Gir
breeds, embryos were transported over distances ranging from 800 to 2000 km
to be transferred to the recipients (Pontes et al., 2010). Using portable
incubators, the embryos were transported during the early stages of
development. They began the development in the laboratory and were then
transported for 2 to 5 days at different stages of development (day 2 to day 5;
day 0 = day of IVF). At the end of transportation, embryos were re-evaluated
and loaded into straws to be transferred at morula or blastocyst stages. In this

outsized project, 20,000 Girolando (Gir-Holstein crossbred animals) embryos
were produced with female-sorted sperm. In just over a year, 8,000 Girolando
heifers were produced from Holstein, Gir or Girolando donors. The possibility
of transporting fresh IVP-embryos contributed to a satisfactory cost
effectiveness of the IVEP process, with pregnancy rates of 36 to 40% and an
overall average rate of 39%. In Holstein cows that typically show lower
production of oocytes, it is also possible to obtain good results with follicular
aspiration. The most effective strategy is to perform a pre-selection of females,
assessing follicular populations with the use of an ultrasound. By using only
the females with higher numbers of follicles, indices can be quite satisfactory.
It is interesting to note that non-lactating cows may have high numbers of
follicles and oocytes.
3.4.2. Sorted Sperm

In dairy cattle, the possibility of choosing the gender of the calf is
extremely advantageous because male calves are not of economic interest.
Some properties choose to produce embryos with unsorted sperm and
determine the gender of embryos by biopsy and DNA analysis. Although this
method is an accurate and sensitive technique, approximately 50% of the
embryos are found to be male and discarded. In addition, pregnancy rates are
considerably lower with biopsied embryos than with intact embryos (Hasler et
al., 2002). The use of sorted sperm makes it possible for almost all of the
embryos to be of the desired gender and of the same quality as embryos
produced with conventional semen. However, the process of sperm sorting
reduces sperm viability and pregnancy rates are not always satisfactory with
artificial insemination (AI). For IVEP, on the other hand, semen subjected to
this technique can successfully be used because this production system
requires fewer viable sperm cells. The rates obtained currently in IVEP with
sorted sperm are very encouraging. In the IVEP program described in the
previous section of this chapter, the use of sorted sperm allowed a more
rational use of embryo recipients. When unsorted sperm is used, twice as many
recipients are required to achieve the desired number of products of the
expected gender. Nevertheless, there were bull and ejaculate effects, showing
the need for a rigorous evaluation and previous selection of the best batches of
sperm to obtain more advantageous results (Pontes et al., 2010). Therefore,
transportation of embryos over long distances and the use of sorted sperm are
crucial ways to improve the efficiency of large-scale IVEP.
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3.5. Heat Stress
In dairy farms located in regions with humid and hot summers such as
Africa, India, South America, and the southern United States, pregnancy rates
can be very low during the months of heat stress. Some properties even opt for
extreme measures, and do not inseminate females in heat during the warmer
months of the year. Exposure of the oocytes to increased body temperatures
has been linked to the degeneration of thecal and granulosa cells and to low
quality oocytes with lower rates of fertilization and conception (Chebel et al.,
2008). Given the greater sensitivity of gametes and embryos to high
temperatures in early stages of development, ET on day 7 after fertilization
seems to be the most viable option. For this reason, ET has been used
efficiently to increase pregnancy rates in dairy cattle in months and/or regions
of higher average temperature (Hansen, 2007; Vasconcelos et al., 2011).
3.6. Recipients
Selection of recipients must be carefully conducted, as they represent a

step of fundamental importance to the success of MOET or IVEP programs.
Adequate recipients do not need to have superior genetic qualities, but they
must present with an appropriate size (suitable for the breed of the fetus) and
have good milk production and proven maternal ability to nurture the neonates
properly. The health criteria applied to the recipients should be the same as
those that are applied to the oocyte or embryo donors. To ensure the success of
IVEP programs and to achieve better pregnancy rates, a large number of
animals should be made available to allow a rigorous selection of the most
suitable recipients. However, the high cost of maintaining these animals may
be prohibitive and compromise the economic viability of the embryo industry.
The possibility of transporting fresh embryos in vitro solved the major
obstacle of large distances. It was originally cost-prohibitive to use recipients
located near the laboratories because the availability of these animals was low.
With the transport of IVP embryos over long distances, it became possible to
use animals from the largest recipients commercial herds situated far away
from the laboratories and establish IVEP on a commercial production scale.
Consequently, the use of large herds of embryo recipients resulted in
changes in the pattern of females used. Informally, the best recipients were
considered to be crossbred heifers, usually half-blood Nelore or European
breeds, such as Simmental and Braunvieh, with some production capacity.
However, due to a limited supply and high demand of these animals, this type
of recipient became costly and scarce. Particularly for large ET projects, it
became cost-prohibitive to use this type of heifer as embryo recipient. A
successful case in Brazil involved the use of recently calved beef cows (Nelore
- Bos indicus) as embryo recipients. This category of females is the most
numerous in South America, providing an adequate supply of recipients at a
fair price. Contradicting previously held ideas, these females have provided
acceptable pregnancy rates (approximately 40%), and more than 10,000 calves
have been born to these cows (In Vitro Brasil Ltda, Mogi Mirim, SP;
unpublished data). If animals have adequate nutritional and health statuses, the
use of cows may indeed present certain advantages over heifers. In general,
cows may have a higher recipient transferred-to-treated rate with FTET
because they usually show better response to hormonal protocols and heifers
often require a pre-synchronization. Cows usually have also been more
exposed to pathogens and thus may have greater disease resistance and better
quality colostrum. Finally, the frequency of dystocia tends to be higher in
heifers than in cows. Until a few years ago, the importance of recipients was
based mainly on their ability to respond to synchronization protocols and to
maintain pregnancy. However, with current advances in epigenetics, it became
evident that other factors, such as diet quality and maternal behavior, can
interfere with gene expression of the calf. Despite the fact that the genetic
sequence is established at the first cell division, the expression of genes may
be altered due to environmental factors. The follicular ovarian reserve of the
fetuses, for instance, can be hugely affected by the nutritional status of the
recipient during pregnancy. As a result, a future donor may have compromised
reproductive performance if the recipient underwent nutritional deprivation
during pregnancy (Ireland et al., 2011). Similarly, it was shown that females
with strongly maternal behavior influence DNA methylation and thus interfere
with the expression of important genes for environmental adaptation (Weaver
et al., 2004).
3.7. Fixed-Time Embryo Transfer (FTET)
Similarly to timed artificial insemination (TAI), FTET eliminates the need

for heat detection, resulting in great advantages for the strategic management
of the breeding of the herd. To solve problems related to heat detection and to
increase the proportion of suitable recipients to receive embryos, several
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hormonal protocols have been developed. An example of FTET protocol is

described in Figure 3.
3.8. Advantages of Using Embryos Instead of AI
Unlike AI, the use of embryos results in relatively constant pregnancy

rates throughout the year, including during periods of high temperatures. ET
allows the enhancement of genetic gain. With the use of AI, the number of
descendants of sires genetically evaluated for desirable characteristics can be
multiplied.
Embryo transfer, in turn, also increases the number of descendants of
females of high genetic merit, causing an even more significant impact on the
improvement of a herd. Therefore, greater genetic gain and a higher genetic
leap are achieved in each generation with ET than with the use of AI alone.
Embryo transfer can also increase the reproductive efficiency of repeat breeder
cows. These animals are defined as subfertile females that do not have any
anatomical or infectious abnormalities yet require three or more services to
become pregnant. ET increases conception rates of these animals to levels
close to those of normally fertile breeder cows, suggesting that reproductive
failures are associated with low oocyte quality and early embryonic
developmental defects. ET can therefore be an effective method of preventing
early embryonic mortality and increasing pregnancy rates.
Because of these advantages, some dairy farms have completely replaced
AI with ET, achieving better pregnancy rates and accelerating genetic gain
between generations. In these situations, recipients and donors are dairy cows
from the same herd; the cows with the best genetic potential are used as oocyte
or embryo donors and the remainders are used as recipients. Thus, efficient
genetic selection is achieved from animals from the same herd.
Figure 3. Example of a hormonal protocol for fixed-time embryo transfer (FTET).

3.9. Advantages of Using In Vitro- Instead

of In Vivo-Produced Embryos
When performing the in vivo production of embryos, it is necessary to

superovulate the donor with the administration of hormones. With OPU/IVEP,
oocytes can be obtained without the use of drugs and the sequential production
of embryos can be performed without exogenous hormone stimulation. The in
vitro technique also allows the use of a smaller interval between follicular
aspirations in the donor. In general, a minimum interval of 15 to 30 days is
used before the females are subjected to a new session of follicular aspiration.
There is no established limit for the number of aspirations, and reports of up to
20 procedures performed sequentially without harm to the donor exist.
Moreover, superovulation requires intervals of 40 to 60 days and can only be
used approximately 3 to 4 times before a gap of several months is recom-
mended. Perhaps one of the major advantages of IVEP is its efficient use of
sexed semen. The sorting process often compromises the fertilization
efficiency of a portion of the spermatozoa, making the process of in vivo
fertilization more challenging. In the in vitro process, the sperm are subject to
less demanding conditions, providing better results than AI and in vivo
embryo production. Production of embryos by MOET does not allow the use
of pregnant animals. In IVEP, it is possible to produce embryos by aspirating
the ovary of pregnant animals as long as the aspiration can be performed
without excessive pulling. Another advantage of IVEP is that it enables higher
use of a fixed dose of semen: a single dose can be used to fertilize oocytes of
10 or more females.
3.10. Critical Aspects of the Use Of IVP Embryos:
The OPU/IVEP technique has more steps than the in vivo production
technique. Thus, highly trained professionals are needed throughout the
process to obtain satisfactory results. The amount of embryos produced can be
decisive in the commercial viability of the technique. Because OPU and
laboratory staff are associated with fixed costs, higher numbers of attempted
pregnancies can result in lower overall costs. Both cryopreservation and
rewarming processes are more critical in IVEP than in other techniques.
Because they are structurally different from in vivo-generated embryos, IVP
embryos cannot be subjected to conventional freezing without suffering severe
damage. Currently, the most efficient method to cryopreserve IVP embryos is
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vitrification. In this technique, no method of direct transfer exists yet, and

vitrified embryos must go through a specific process of rewarming before
being loaded and transferred. The genetic impact on a herd is higher with IVF
than with other techniques. If the donors are selected properly, IVF can confer
a significant improvement on each generation. On the other hand, any mistake
in the selection of females can have a major negative impact on the herd.
Hence, rigorous and objective criteria must be used in the selection of oocyte
donors.
3.11. Cryopreservation and Strategic Use of the Embryo
To be cryopreserved, embryos generated in vivo are loaded into straws, in

a similar manner to fresh embryos, with an additional cryoprotectant added to
the medium. The most commonly used cryoprotectant is ethylene glycol, as it
protects the blastomeres from damage caused by the low temperatures. Once
they are filled, the straws are put in the freezing machine, which allows a
controlled decrease of the temperature. When the temperature reaches
approximately - 7 °C, a "seeding" procedure, which aims to induce homo-
geneous crystallization of the contents of the straw, should be performed.
After this procedure has been performed, the machine goes back to decreasing
the temperature at a rate of approximately 0.3 to 0.5 °C per minute. This speed
is calculated to prevent the formation of ice crystals within the embryo (if
freezing occurs too rapidly) or the induction of cell damage due to the rapid
dehydration of the embryo and hyper-saline concentration inside the cell (if
freezing occurs too slowly). When the final temperature is reached (-32 to -35
°C), the straws are immersed in liquid nitrogen and stored in nitrogen tanks.
Unlike in vivo-generated embryos, IVP embryos are more susceptible to
the damage caused by cryopreservation and rarely survive the freezing
process. The greater sensitivity of IVP embryos to cooling appears to be
directly related to higher lipid accumulation caused by the in vitro culture
(Abe et al., 2002). These lipids can undergo irreversible changes and severely
compromise embryonic development. A new method of increasing the
cryotolerance of these embryos that has proven effective is chemical
delipidation.
Forskolin, a substance derived from the Indian plant Coleus forskohlii, has
been successfully used to promote intracellular lipolysis in embryonic cells
(Men et al., 2006). When applied at strategic periods of the in vitro culture,
this substance is able to increase the embryonic cryotolerance to levels that
provide good pregnancy rates, enabling the commercial use of the technique.
The pregnancy rates obtained by the laboratory In Vitro Brasil with vitrified
embryos previously exposed to forskolin are described in Table 2 (unpublished
data). With the advances in cryopreservation techniques of IVP embryos, it is
possible to have a stock of female-sexed embryos for strategic use during the
months of greatest heat.
Table 2. Pregnancy rates of IVP Bos indicus embryos treated

with forskolin for 48 h in culture and submitted to vitrification
Transferred embryos Pregnancies Pregnancy rate

Breed (n) (n) (%)
taurus-indicus 87 37 42.5a
Gir 701 314 44.8a
Guzera 680 274 40.3a
Nelore 440 200 45.5a
Total 1,908 825 43.2
a
Within a column, rates with a common superscript are similar (P > 0.05).
In addition to enabling better pregnancy rates than AI, IVP embryos have
the added advantage of generating pregnancies of the desired gender. The use
of IVP embryos in dairy farming has been the most promising feature of recent
years, second only to the advances brought about by the pharmacological
control of the estrous cycle and ovulation. Highly efficient technologies are
already available, and large dairy farms have sought strategies to improve their
herds using technology from biotech companies.
CONCLUSION
The failure to detect estrus in an accurate manner is one of the most
common reasons for the failure of reproductive programs on dairy farms. Heat
stress also represents a significant challenge, causing low pregnancy rates and
therefore high economic losses. The technologies of FTAI and embryo transfer
have directly benefited dairy farms of all sizes (micro, small, medium and
large). However, the importance of factors such as nutrition and management
must be considered before implementing these strategies because these factors
directly influence reproductive efficiency. Any variation in these factors can
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affect the result of a FTAI protocol or rates of embryo production. Thus, a

proper analysis of the technique to be used combined with adequate conditions
for the herd can provide optimal results.
REFERENCES
Abe, H.; Yamashita, S.; Satoh, T.; Hoshi, H. (2002). Accumulation of
cytoplasmatic lipid droplets in bovine embryos and cryotolerance of
embryos developed in different culture systems using serum-free medium
or in serum-containing medium. Molecular Reproduction and
Development, 61, 57-66.
Bó, G. A.; Baruselli, P. S.; Martínez, M. F. (2003). Pattern and manipulation
of follicular development in Bos indicus cattle. Animal Reproduction
Science, 78, 307-326.
Chebel, R. C.; Demétrio, D. G. B.; Metzger, J. (2008). Factors affecting
success of embryo collection and transfer in large dairy herds.
Theriogenology, 69, 98-106.
Gibbons, J. R.; Beal, W. F.; Krisher, R. J.; Faber, F. G.; Pearson, R. F.;
Gwazdauskas, F. C. (1994). Effect of once versus twice-weekly
transvaginal follicular aspiration on bovine oocyte recovery and embryo
development. Theriogenology, 42, 405-419.
Hanlon, D.W.; Williamson, N.B.; Wichtel, J.J.; Steffert, I. J.; Craiqie, A. L.;
Pfeiffer, D. U. (1997). The effect of estradiol benzoate administration on
estrous response and synchronized pregnancy rate in dairy heifers after
treatment with exogenous progesterone. Theriogenology, 45, 775-785.
Hansen, P. J. (2007). Exploitation of genetic and physiological determinants of
embryonic resistance to elevated temperature to improve embryonic
survival in dairy cattle during heat stress. Theriogenology, 68, 242-249.
Hasler, J. F.; Cardey, E.; Stokes J. E.; Bredbacka, P. (2002). Nonelec-
trophoretic PCR-sexing of bovine embryos in a commercial environment.
Theriogenology, 58, 1457-1469.
Ireland, J. J.; Smith, G. W.; Scheetz, D.; Jimenez-Krassel, F.; Folger, J.K.;
Ireland, J. H. L.; Mossa, F.; Lonergan, P.; Evans, A. C. O. (2011). Does
size matter in females? An overview of the impact of the high variation in
the ovarian reserve on ovarian function and fertility, utility of anti-
Mullerian hormone as a diagnostic marker for fertility and causes of
variation in the ovarian reserve in cattle. Reproduction, Fertility and
Development, 23, 1-14.
Jeong J. K.; Kang H. G.; Hur T. Y.; Kim, I. H. (2012). Shynchronization

Using PGF and Estradiol with or whitout GnRH for timed AI in dairy
cows. Jornal of Reproduction and Development, online version.
Lucy M.C.; McDougall, S.; Nation. D.P. (2004) The use of hormonal
treatments to improve the reproductive performance of lactating dairy
cows in feedlot or pasture-based management systems. Animal
Reproduction Science, 82–83, 495–512.
Men, H.; Agca, Y.; Riley, L. K.; Critser, J. K. (2006). Improved survival of
vitrified porcine embryos after partial delipation through chemically
stimulated lipolysis and inhibition of apoptosis. Theriogenology, 66, 2008-
2016.
Moreira, F.; De La Sota, R.L.; Diaz, T. Thatcher, W. W. (2000). Effect of day
of the estrous cycle at the initiation of a timed artificial insemination
protocol on reproductive responses in dairy heifers. Journal of Animal
Science, 78, 1568-1576.
Nasser, L. F.; Reis, E. L.; Oliveira, M. A.; Bí, G. A.; Baruselli, P. S. (2004).
Comparison of four synchronization protocols for fixed-time bovine
embryo transfer in Bos indicus x Bos taurus recipients. Theriogenology,
62, 1577-1584.
Pontes, J. H. F.; Silva, K. C. F.; Basso, A. C.; Ferreira, C. R.; Santos, G. M.
G.; Sanches, B. V.; Porcionato, J. P. F.; Vieira, P. H. S.; Faifer, F. S.;
Sterza, F. A. M.; Schenk, J. L.; Seneda, M. M. (2010). Large-scale in vitro
embryo production and pregnancy rates from Bos taurus, Bos indicus,
and indicus-taurus dairy cows using sexed sperm. Theriogenology, 74,
1349-1355.
Pursley, J.R.; Mee, M.O.; Wiltbank, M.C. (1995). Synchronization of
ovulation in dairy cows using PGF2 and GnRH. Theriogenology, 44, 915-
923.
Rodrigues, C. A.; Teixeira, A. A.; Ferreira, R. M.; Ayres, H.; Mancilha, R. F.;
Souza, A. H.; Baruselli, P. S. (2010). Effect of fixed-time embryo transfer
on reproductive efficiency in high-producing repeat-breeder Holstein
cows. Animal Reproduction Science, 118, 110-117.
Seneda, M. M.; Esper, C. R.; Garcia, J. M.; Oliveira, J. A.; Vantini, R. (2001).
Relationship between follicle size and ultrasound-guided transvaginal
recovery. Animal Reproduction Science, 67, 37-43.
Souza, A. H.; Viechnieski, S.; Lima, F. A.; Silva, F. F.; Araújo, R.; Bó, G. A.;
Wiltbank, M. C.; Baruselli, P. S. (2009). Effects of equine chorionic
gonadotropin and type of ovulatory stimulus in a timed-AI protocol on
reproductive responses in dairy cows. Theriogenology, 72, 10-21.
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Thatcher,W. W.; Moreira, F.; Pancarci, S. M.; Bartolome, J. A.; Santos, J. E.

(2002). Strategies to optimize reproductive efficiency by regulation of
ovarian function. Domestic Animal Endocrinology, 23, 243–254.
Van Eerdenburg, F. J.; Karthaus, D.; Taverne, M. A.; Merics, I.; Szenci, O.
(2002). The relationship between estrous behavioral score and time of
ovulation in dairy cattle. Journal of Dairy Science, 85, 1150-1156.
Vasconcelos, J. L. M.; Jardina, D. T. G.; Sá Filho, O. G.; Aragon, F. L.; Veras,
M. B. (2011). Comparison of progesterone-based protocols with
gonadotropin releasing hormone or estradiol benzoate for timed artificial
insemination or embryo transfer in lactating dairy cows. Theriogenology,
75, 1153-1160.
Weaver, I. C. G.; Cervoni, N.; Champagne, F. A.; D`Alessio, A. C. D.;
Sharma, S.; Seckl, J. R.; Dymov, S.; Szyf, M.; Meaney, M. J. (2004).
Epigenetic programming by maternal behavior. Nature Neuroscience, 8,
847-854.
Whittier, W.D.; Gwazdauskas, F.C.; McGilliard, M. L. (1989). Prostaglandin
F2 usage in a dairy reproduction program for treatment of unobserved
estrus, pyometra and ovarian luteal cysts. Theriogenology, 32, 693-704.
Wiltbank, M.; Lopez, H.; Sartori, R.; Sangsritavong, S.; Gumen, A. (2006).
Changes in reproductive physiology of dairy cows due to elevated steroid
metabolism. Theriogenology, 65, 17-29.
INDEX
alternative causes, 30
alternative treatments, 89
A
alveoli, 32
ambivalence, 37
access, 61, 62, 65, 67, 109
ammonia, 58, 59, 83
acid, 49, 108
amniotic fluid, 48
acidity, 108, 109, 111
anal atresia, 14
acidosis, 32, 61
anamnesis, ii, 2, 6, 16, 23, 26, 28, 29, 35,
adaptation, ii, 53, 57, 58, 73, 141
36
adhesions, 138
anencephaly, 31
adrenal glands, 17
animal husbandry, 63
aetiology, 31
animal welfare, iii, 54, 63, 64, 65, 67, 79,
AFM, 20, 26
85, 86, 88, 90
Africa, 140
anoxia, 6, 8, 14, 16, 17, 18, 31, 32, 35, 36
age, iii, 4, 10, 26, 35, 36, 47, 71, 72, 92,
antagonism, 98
94, 133, 136
antibiotic, 64, 83, 104
agglutination, 48
antibiotic resistance, 83
agglutination test, 48
antibody, 21
aggregation, 13, 77, 109
antigen, 20, 21
aggression, 61, 81
antioxidant, 103
aggressive behavior, 61
aorta, 20
agonist, 68
apoptosis, 123, 147
agriculture, 55, 56, 57, 58, 76, 81, 82, 84,
aptitude, 73
85, 86, 88, 90
arrest, 36, 47, 49
agrosystem, 55
arteries, 47, 50
air temperature, 66
artery, 17, 19
airways, 26
arthrogryposis, 14, 30
albumin, iii, 92, 103, 104, 106, 109, 111,
artificial insemination, 68, 72, 127, 128,
123
131, 132, 136, 139, 141, 147, 148
algae, 92
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150 Index
asphyxia, 32, 39, 40, 42, 43, 47, 48 blood, 17, 20, 21, 49, 50, 66, 70, 94, 101,
aspiration, 26, 28, 32, 46, 48, 138, 139, 103, 104, 107, 111, 129, 140
143, 146 blue baby, 25
assault, 25 body fat, 66
assessment, 3, 30, 48, 60, 75, 77, 82, 83, body fluid, 30, 105
87, 88, 89, 90, 110, 117 body weight, 9, 22, 26, 36, 37, 40, 65
assessment tools, 83 bone, 9
atelectasis, 22, 33 bones, 9, 36
atmosphere, 58, 59 bradytocia, ii, 2, 13, 14, 16, 17, 28, 31, 38
attributable fraction, ii, 2, 6, 8, 13 brain, 20, 24, 48
audit, i, 1, 4, 37 brain abnormalities, 24
autolysis, 33, 34, 35 brain damage, 48
autopsy, 7, 29, 32, 44, 46 Brazil, 127, 138, 141
awareness, 54 breeding, iii, 54, 68, 70, 72, 73, 74, 80,
84, 86, 88, 123, 124, 128, 141
breeding goal, 73, 124
B
bronchial tree, 26
bronchopneumonia, 26
Baars, 86
brucellosis, 135
bacteria, 83, 92, 104, 108
buffalo, 123
bacterial colonies, 26
Butcher, 84
bacterial infection, 20, 94, 104
bacteriostatic, 104
bacterium, 20 C
barriers, 38
base, 45, 49, 60, 65, 67, 75, 80, 81, 147, Ca2+, 109, 117
148 calcium, 108, 109, 110, 112, 113, 122
basic research, 135 CAP, 82
bedding, 93 capital input, 59
beef, 6, 7, 11, 39, 40, 45, 46, 50, 138, 141 carbon, 56, 58
behaviors, 61, 65 carbon dioxide, 58
Belgium, 7, 118, 124 cardiovascular disorders, 7
benefits, 37, 55, 56, 59, 65, 76, 134 case study, 80
beverages, 108 casein, iii, 91, 108, 109, 110, 111, 112,
bicarbonate, 81, 111 113, 119, 122, 123, 124
biochemistry, 22 category a, 14, 137
biodiversity, 57, 58, 60, 73, 79 causality, 33
biogas, 59 causation, 4
biological activity, 105 CCA, 127
biopsy, 139 CEC, 50
birth weight, 7, 10, 11, 24, 35, 43, 44, 47 cell division, 141
births, 3, 42 cell membranes, 92, 104
birthweight, 44 Central Europe, 124
bleeding, 40, 43 central nervous system, 14
Index 151
certification, 84 conference, 86
cervix, 136, 138 confinement, 90
challenges, 68, 87, 89 congenital defect, ii, 2, 6, 12, 13, 14, 15,
changing environment, ii, 53, 57 29, 30, 36, 37, 38
cheese, 108, 109, 110, 111, 112, 113, 121 congenital malformations, 7
chemical, 57, 63, 94, 105, 107, 108, 109, Congress, 40, 45, 46, 86, 122
114, 144 conjunctiva, 20
chlorine, 113 consensus, 8, 9, 10, 33, 47
chondrodysplasia, 14 conservation, 55, 61, 62, 84, 120
chorionic gonadotropin, 129, 131, 147 consolidation, 26, 131
chronic hypoxia, 48 constituents, iii, 92, 95
circulation, 55 construction, 84
classes, 7, 105 consumers, ii, 54, 63, 79
classification, i, ii, 1, 2, 3, 4, 9, 12, 13, 28, consumption, 78, 94
29, 30, 37, 38, 47 controversial, 66, 76
cleft palate, 30 cooling, 144
clients, 30 coordination, 35
climate, 56, 57, 62, 74, 76, 79, 83, 84, 86, copper, 108
89 corpus luteum, 130
climate change, 56, 57, 74, 76, 83, 86, 89 correlation, iii, 35, 39, 91, 92, 93, 100,
clinical assessment, 30 101, 102, 103, 105, 107, 109, 110, 111,
clinical symptoms, 93 112, 113
cloning, 135 correlation coefficient, iii, 91, 92, 93,
CO2, 58, 59 100, 101, 102, 103, 105, 107, 110, 111,
coagulation process, 110 112, 113
coding, 3 correlations, iii, 92, 99, 103, 105, 107,
colostrum, 20, 21, 26, 104, 117, 126, 141 112, 118, 128
commercial, 39, 94, 115, 118, 134, 138, corticosteroids, 44
140, 143, 145, 146 cost, 6, 74, 75, 76, 78, 82, 88, 96, 97, 118,
community, ii, 53 131, 134, 137, 139, 140, 141
competition, 61 cost effectiveness, 139
complement, 105 cost-benefit analysis, 78
complementarity, 55 costs of production, 56, 119
complexity, 28 Croatia, 119
composition, 73, 80, 101, 107, 108, 109, crop, 57, 88
114, 115, 116, 117, 118, 119, 120, 121, crop rotations, 57
124 crops, 88
composting, 59 crown, 9, 35
compounds, 103, 105, 110, 120 crude protein, iii, 91
compression, 32 cryopreservation, 128, 136, 143, 144, 145
conception, 71, 84, 128, 140, 142 crystallization, 144
concordance, 38 crystals, 144
conditioning, i, 113 culture, 21, 33, 48, 137, 144, 145, 146
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152 Index
cure, 118 dietary iodine, 33

cyanosis, 17, 32 digestion, 133
cycles, 56, 133 discomfort, 134
cycling, 130, 131 disease epidemics, ii, 54, 57
diseases, i, iii, 39, 42, 63, 64, 65, 66, 71,
74, 82, 92, 103, 119, 121, 123, 135
D
disorder, 3, 12, 13, 25, 29
disposition, 62
dairy cattle, i, 36, 42, 43, 44, 46, 64, 67,
dissociation, 109, 124
83, 84, 86, 87, 88, 90, 95, 110, 115,
distress, 24, 32, 42, 64
117, 119, 120, 121, 123, 124, 126, 129,
distribution, 55, 58, 60, 112
131, 133, 134, 139, 140, 146, 148
diversity, 57, 63
dairy cows, i, 44, 58, 61, 62, 63, 65, 66,
DNA, 139, 141
73, 80, 81, 82, 83, 84, 85, 87, 88, 89,
dogs, 9
95, 98, 116, 118, 119, 121, 122, 125,
dominance, 136
129, 131, 132, 142, 147, 148
donors, 134, 135, 136, 137, 138, 139,
dairy farm, i, ii, 41, 53, 54, 55, 56, 58, 59,
140, 142, 144
62, 64, 66, 68, 69, 71, 73, 74, 75, 76,
drawing, 30
79, 80, 86, 88, 89, 95, 117, 121, 127,
drugs, 64, 73, 74, 89, 95, 127, 129, 131,
128, 132, 138, 140, 142, 145
143
dairy industry, 60, 75, 80, 94, 95, 115,
dry matter, 108
128
drying, 64
database, 11, 25
dwarfism, 45
deaths, 3, 4, 30, 39, 40, 44
dynamic systems, 55
defects, 6, 7, 12, 14, 29, 30, 36, 37, 44,
dysphagia, 35
142
dystocia, ii, 2, 8, 12, 13, 14, 16, 17, 29,
deficiencies, 45
31, 38, 43, 45, 141
deficiency, 34, 42, 44, 45, 46, 48, 50, 51
dystocia anamnesis, ii, 2, 13, 14, 31, 38
deforestation, 56
dystoxia, ii, 2, 12, 13, 14, 16, 31, 38
degradation, 54
dehydration, 144
denaturation, 108 E
Denmark, 7, 85, 86
depression, 26 economic efficiency, 54, 55
deprivation, 141 economic evaluation, 86
depth, 30 economic growth, 54
destruction, 105 economic losses, 64, 145
detachment, 35 economic values, 78
detection, iii, 8, 13, 20, 21, 22, 33, 64, 91, economic welfare, 78
116, 127, 129, 130, 141 economics, 82, 124
diagnostic criteria, 6, 9, 10, 13, 34, 36 economies of scale, 54
diaphragmatic hernia, 14 ecosystem, 55, 60
diarrhea, 42 editors, 81, 88
diet, 60, 62, 121, 133, 141 EEA, 56, 82
Index 153
efficiency criteria, 55 equity, 55, 75

Egypt, 97 erythrocytes, 94
election, 73 ester, 30, 131
electricity, 59, 89 Estonia, 110, 120
ELISA, 20, 21 estrogen, 131
elongation, 112 ethylene, 144
e-mail, 53, 115 ethylene glycol, 144
embryo transfer, 68, 128, 137, 142, 145, EU, 58, 61, 62, 76, 80, 81, 82, 95
147, 148 Europe, 68, 77, 93, 94
emission, 56, 60 European market, 95
employees, 136 European Parliament, 94
encephalitis, 21 European Union, 95, 97
encephalopathy, 32 EUROSTAT, 56, 57, 82
endocardium, 17 euthanasia, 14, 25, 36
endocrine, 7, 130 eutoxia, ii, 2, 12, 13, 29, 31, 38
endurance, 108 evidence, 3, 12, 20, 22, 30, 33, 42, 66
end-users, 75, 77 evolution, 3
energy, 59, 60, 62, 65, 66, 67, 70, 72, 73, examinations, 10, 30, 40, 46
76, 88, 127 exclusion, ii, 2, 6, 13, 29
energy density, 70 expertise, 10
energy efficiency, 59, 76 exposure, 108
energy input, 59 expulsion, ii, 2, 4, 6, 13, 23, 28, 35, 36,
England, 5, 40, 89, 96, 119 38, 45
enteritis, 22 external validity, 35
enterocoele, 14, 20 extreme cold, 26
environment, ii, 25, 54, 55, 56, 57, 58, 59,
60, 65, 67, 69, 70, 73, 79, 81, 82, 86,
F
92, 126, 146
environmental conditions, 56, 66, 74
farm efficiency, ii, 54
environmental degradation, 54
farmers, 4, 37, 57, 60, 62, 73, 74, 75, 88,
environmental factors, 61, 72, 93, 98,
96, 138
124, 141
farms, 40, 54, 59, 60, 63, 64, 66, 68, 71,
environmental impact, 59, 80, 83
72, 75, 76, 79, 86, 87, 89, 95, 121, 128,
environmental protection, 59
132, 138, 140, 142, 145
environmental temperatures, 67
fat, iii, 66, 70, 92, 102, 103, 108
environments, ii, 53, 57, 67, 73, 85
feedstuffs, 56
enzyme, 105, 108, 121
femur, 41
enzymes, 103
fermentation, 56, 59, 113
epicardium, 17
fertility, 44, 59, 64, 65, 68, 69, 70, 71, 72,
epidemiologic, 3
74, 81, 83, 84, 87, 118, 121, 126, 128,
epigenetics, 141
132, 146
epithelium, 94, 111
fertilization, 134, 137, 140, 143
equilibrium, 70, 74
fertilizers, 59
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154 Index
fetal development, 33 gland, iii, 22, 91, 92, 93, 94, 95, 97, 98,
fetal distress, 32 101, 103, 104, 105, 107, 111, 115, 119,
fetal growth, 7, 50 123
fetal maldisposition, ii, 2, 13, 35, 38 global warming, 74, 75
fetus, ii, 2, 4, 12, 23, 24, 25, 27, 31, 33, globalization, 58
35, 37, 40, 41, 47, 140 glycol, 144
fever, 16, 64, 65 goat milk, 122
fiber, 66 goiter, 48, 50
fibrosis, 138 gonadotropin-releasing hormone (GnRH),
financial, 95 129
Finland, 5, 7, 49, 86, 120 granules, 104
fitness, 68, 71 grass, 62, 65
fixed costs, 143 grasslands, 56
flaws, 134 grazing, 61, 62, 65, 85, 87
fluid, 48 greenhouse, 56, 58, 88
foals, 33, 48 greenhouse gas, 56, 88
follicle, 129, 132, 133, 147 greenhouse gas emissions, 56
follicles, 130, 136, 137, 139 group size, 85
food, ii, 54, 56, 57, 76, 108 grouping, 83
food production, ii, 54, 57 growth, ii, 2, 7, 9, 13, 21, 27, 29, 36, 38,
food security, 56, 57 46, 47, 49, 50, 54, 58, 103, 107, 136
formaldehyde, 124 growth arrest, 36, 47, 49
formation, 34, 110, 113, 137, 144 growth factor, 103
fractures, 14, 39, 48 guidelines, 28, 74, 75, 118
France, 5, 40, 89, 93, 96, 117
freezing, 143, 144
H
fungi, 21, 92, 104
habitats, 56, 76
G haemorrhage, ii, 2, 13, 14, 15, 17, 18, 20,
25, 29, 32, 34, 36, 38, 43
gene expression, 141 hair, 8, 16, 17, 24
genes, 73, 125, 141 half-life, 131
genetic diversity, 63 health, iii, 54, 55, 59, 60, 63, 64, 65, 66,
genetic factors, 93 68, 69, 71, 73, 74, 83, 85, 87, 88, 89,
genetics, 64, 65, 66, 69, 70 91, 93, 94, 96, 98, 103, 105, 107, 115,
genomics, 123 117, 119, 121, 126, 140, 141
genotype, 11, 35, 79 health care, 64
Germany, 5, 41, 43, 69, 80, 85, 88, 96, 97 health effects, 103
gestation, 4, 7, 10, 11, 24, 25, 26, 36, 43, health problems, 64, 88
47, 49 health status, 63, 69, 93, 94, 96, 98, 107,
gestational age, 10, 26, 35, 36 115, 141
GHG, 58, 59 heavy metals, 58
gingival, 17, 20, 32 Helicobacter pylori, 105
Index 155
hematomas, 47 images, 3, 38, 45

hepatic necrosis, 20 imbalances, 25, 36
heritability, 74, 98 immune defense, 97
hernia, 14 immune function, 64, 65
herpes, 20 immune response, 105
herpes virus, 20 immune system, 64, 93
histology, 34 immunity, 104, 105, 123
history, 6, 8, 12, 16, 26, 30, 31 immunofluorescence, 20
hormone, 68, 129, 130, 131, 143, 146, immunoglobulin, 22, 117
148 immunoglobulins, 103, 104, 105, 107,
hormones, 59, 103, 129, 131, 133, 136, 111, 119
143 impact assessment, 60, 82, 87
horses, 9 implants, 127, 130, 133
host, 93 improvements, 59, 66, 82
housing, 59, 61, 62, 67, 73, 80, 83, 85 in utero, 16, 23, 29, 31, 35
human, i, 1, 2, 3, 4, 7, 10, 29, 30, 32, 35, in vitro, 128, 134, 135, 137, 140, 143,
37, 38, 39, 58, 63, 94, 103, 105, 119, 144, 147
129 in vivo, 128, 134, 135, 143, 144
human body, 103 incidence, 11, 12, 25, 30, 34, 36, 44, 46,
human chorionic gonadotropin, 129 64, 65, 66, 97, 103, 121, 122
human health, 63, 119 incisor, 24, 25
humidity, 66, 84, 134 income, 56
humoral immunity, 105 India, 140
Hungary, 40, 45 indirect measure, 77
husbandry, 57, 60, 63, 87, 98 inducer, 127
hyaline, 34 induction, 93, 144
hydrocephalus, 14 inductor, 130
hygiene, 57, 117 industry, 60, 61, 75, 76, 77, 80, 94, 95,
hyperplasia, 22 115, 128, 140
hyperthermia, 25, 36 inertia, 16, 35, 76
hypoplasia, 22 infection, ii, 2, 13, 20, 21, 22, 26, 29, 33,
hypothermia, ii, 2, 13, 25, 30, 34, 36, 38 38, 42, 48, 63, 93, 94, 104, 111
hypothyroidism, 33 infertility, 95
hypoxia, 40, 48 infestations, 71
inflammation, 93, 94, 95, 97, 101, 104,
110, 111, 115
I
ingredients, 61
inhibition, 147
iatrogenic, 14, 25, 26
initiation, 131, 147
Iceland, 7
injuries, 104, 138
ideal, 3, 77
injury, 25, 43, 50, 94, 104
identification, 69
insects, 67
idiopathic, ii, 2, 13, 17, 20, 29, 38
insulin, 66
idiopathic hemoperitoneum, ii, 2, 13, 38
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156 Index
integration, 57, 79 lactoferrin, iii, 92, 103, 104, 106, 115,

intensive farming, 60, 62 117, 119, 126
interface, 80 lactose, iii, 91, 101, 104, 108, 112, 113,
International Classification of Diseases, i, 125
1, 3 land abandonment, 57
interstitial pneumonia, 32 landscape, 61
Intervals, 131 landscapes, 57, 90
intervention, 56 language barrier, 38
intoxication, 50 leaching, 56
intrauterine growth retardation, 9, 27 lead, 4, 33, 54, 56, 57, 61, 66, 67, 69, 128,
iodine, ii, 2, 13, 22, 23, 28, 29, 34, 38, 44, 133, 136
45 leakage, 104
ions, 108, 109, 112 learning, 4
Iran, 5 legislation, 60, 62, 66
Ireland, 1, 5, 7, 40, 41, 45, 46, 48, 85, 87, legs, 14, 16, 74
88, 141, 146 lesions, 6, 7, 8, 10, 11, 14, 16, 17, 20, 21,
iron, 104, 108, 115 22, 23, 26, 28, 29, 30, 31, 32, 33, 34,
isolation, 20, 22, 30 35, 47
Israel, 126 leucocyte, 125
issues, iii, 38, 54, 55, 65, 75, 76, 79, 84 LEUKOCYTES, 94
Italy, 86, 122 life cycle, 88
lifetime, 135
ligament, 24
J
light, 24, 54
linear function, 78
Japan, 5, 7, 43
linear model, 43
jejunum, 15
lipids, 144
joints, 44
lipolysis, 103, 144, 147
Listeria monocytogenes, 21
K Lithuania, 97
liver, 20, 42
K+, 101 livestock, ii, 50, 53, 54, 55, 56, 57, 58, 64,
keratin, 32 66, 75, 76, 80, 82, 83, 86, 87, 89, 121,
kidney, 20 128, 138
kidneys, 20 local conditions, 73
longevity, 64, 71, 74, 79
L low temperatures, 144
lumen, 136
laboratory tests, ii, 2, 12, 30 Luo, 5, 44
lactation, iii, 39, 64, 65, 66, 67, 70, 74, lying, 61
82, 86, 92, 94, 95, 96, 97, 98, 99, 100, lymphocytes, 94
102, 103, 104, 116, 118, 121, 123 lysozyme, iii, 92, 103, 105, 106, 119
lactic acid, 108
Index 157
metals, 58
M
methodology, 10, 60, 63
methylation, 141
macrophages, 94
microorganisms, 92, 105
magnesium, 112
microscopy, 21
majority, 64, 65
milk coagulation, 118, 119, 125
man, 55, 76
milk quality, iii, 74, 91, 122
management, i, ii, 39, 43, 45, 50, 54, 57,
missions, 59, 83
58, 59, 61, 62, 63, 65, 66, 67, 68, 69,
modelling, 89
70, 72, 73, 74, 82, 84, 89, 93, 118, 128,
models, 9, 32, 47, 54, 75, 79, 89
129, 141, 145, 147
modifications, 7, 128
mandible, 14
moisture, 112, 113
manipulation, 146
molecular weight, 105
manure, 56, 58, 59
molecules, 108
mapping, 4
morphology, 22, 117, 125
marketing, 75
mortality, i, ii, 1, 2, 3, 4, 5, 6, 7, 8, 9, 10,
mass, 34
13, 17, 28, 29, 30, 31, 32, 33, 35, 36,
mastitis, iii, 26, 47, 64, 65, 71, 74, 83, 90,
37, 38, 39, 40, 41, 42, 43, 45, 46, 48,
91, 92, 93, 94, 95, 96, 97, 98, 99, 100,
50, 128, 142
103, 104, 106, 111, 112, 113, 115, 116,
mortality rate, ii, 2, 13, 35, 38, 50
117, 118, 119, 120, 121, 122, 123, 124,
morula, 128, 136, 139
125
mucosa, 17, 20
materials, 120
mucus, 9, 26
matter, 10, 66, 108, 114, 146
multidimensional, 77
MCP, 112
multiple factors, 69
measurement, 35
muscles, 20
measurements, 70, 77
musculoskeletal, 44
meconium, 8, 15, 16, 17, 32, 46
musculoskeletal system, 44
medical, 63, 68
mutation, ii, 2, 12
medication, 63
myocarditis, 21
medicine, 4, 30, 44, 46, 63
myopathy, 25, 37
Mediterranean, 80
membranes, 66, 92, 104
mesentery, 20 N
meta-analysis, 4
Metabolic, 80 Na+, 101
metabolic acidosis, 32 natural habitats, 56
metabolic disorder, 7, 48, 64, 65, 66, 83 natural resources, 57
metabolic disorders, 7, 48, 64, 65, 66, 83 NEB, 65
metabolism, 29, 45, 67, 70, 71, 72, 83, necropsy, i, ii, 2, 3, 6, 8, 9, 10, 11, 12, 13,
132, 133, 148 23, 25, 29, 30, 31, 32, 37, 38, 39
metabolites, 66, 70 necrosis, 20, 46
metal ion, 108 negative effects, 58
metal ions, 108 negative relation, iii, 91, 111
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158 Index
neonates, 47, 140

P
nervous system, 14, 103
Netherlands, 7, 48, 80, 81, 86, 96, 97
pain, 64
neutral, 79
Pakistan, 44, 119
neutrophils, 94, 104
palate, 30
New Zealand, 40, 41, 42, 44, 70, 84, 95,
pallor, 19, 20
123
parasite, 74
nitrification, 58
parasites, 104
nitrogen, 58, 144
parity, 2, 10, 72, 86
nitrous oxide, 58
Parliament, 94
North America, 44, 45, 132
partition, 70
Norway, 5, 72, 89
pasture, 45, 61, 62, 65, 67, 68, 80, 81, 83,
nucleotides, 121
85, 90, 147
nursing, 35
pastures, 70, 87
nursing care, 35
pathogenesis, 43, 46
nutrient, ii, 54, 56, 57, 65, 67, 70, 83
pathogens, 21, 29, 93, 122, 135, 141
nutrients, 55, 56, 58, 60, 65, 70
pathology, 10, 22, 37
nutrition, 69, 70, 145
pathophysiology, 39
nutritional status, 141
PCM, 13
PCR, 20, 21, 146
O pelvis, 136
penicillin, 104, 117
objective criteria, 144 peptides, 118, 122, 126
obstacles, 37 percentile, 10, 26
oedema, 16, 26, 34 pericarditis, 21, 22
oesophageal, 26 perinatal, i, ii, 1, 2, 3, 4, 5, 6, 7, 8, 9, 10,
oil, 58, 76 13, 28, 29, 30, 31, 32, 33, 36, 37, 38,
omphalorrhagia, ii, 2, 13, 17, 19, 20, 28, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48,
38 49, 50, 97
oocyte, 137, 140, 142, 144, 146 perinatal mortality, i, ii, 1, 2, 3, 4, 5, 6, 7,
operations, 60 8, 9, 10, 13, 28, 29, 30, 31, 32, 33, 36,
opportunities, 55, 89 37, 38, 42, 43, 45, 46
organ, 9, 37 peritonitis, 22
organism, 33, 93, 115 peri-urban, 50
organs, 17, 20, 30, 37 permeability, 92, 104, 111
osmotic pressure, 101 permeation, 107
ovarian cysts, 68 permit, 62
ovaries, 130, 137 pH, 32, 108, 109, 111, 119, 121, 122, 124
overgrazing, 56 phagocytosis, 105
overpopulation, 65 Philadelphia, 43
ovulation, 127, 128, 129, 130, 131, 132, phosphates, 112
133, 136, 145, 147, 148 physical characteristics, 109
oxidation, 108 Physiological, 83, 84, 123
Index 159
physiology, 73, 117, 135, 148 prostaglandins, 68, 129

pigs, 9 protection, 55, 57, 59, 62
placenta, 21, 22, 23, 29, 33, 35, 36, 37, 45 proteins, iii, 92, 103, 105, 106, 109, 111,
plausibility, 3 112, 117, 119, 122, 124, 125, 126
pleura, 17 proteolysis, 103, 111
pneumonia, 22, 26, 32, 34, 104 Pseudomonas aeruginosa, 104
Poland, 5, 91, 97, 99, 115, 116, 120, 125, purchasing power, 75
126 pyothorax, 22
policy, 82, 89
policy making, 89
Q
pollution, 56, 89
polymorphism, 104, 126
quality standards, iii, 92
population, 2, 6, 36, 38, 41
quantification, 86
Portugal, 53
positive correlation, 93, 107, 109, 112
poverty, 89 R
poverty alleviation, 89
pregnancy, 29, 127, 128, 129, 130, 132, race, 76
133, 134, 135, 138, 139, 140, 141, 142, radiation, 66, 67
145, 146, 147 radiography, 36
premature placental expulsion, ii, 2, 6, 13, rangeland, 61
23, 36, 38 raw materials, 120
prematurity, ii, 2, 13, 24, 25, 29, 30, 35, reactions, 47
38 receptors, 131
preparation, 39, 108 reciprocal cross, 47
prevention, 48, 63, 96 recommendations, 61
primary function, 93 recovery, 63, 146, 147
principles, 3, 58, 64, 77 rectal temperature, 67, 84
probability, 104 reflexes, 24, 64, 74
producers, 61, 73, 75, 80, 95, 121, 128, regression, 123, 131
138 regression model, 123
production costs, 76 regulations, 63, 71
productive efficiency, 59, 76, 77 relaxation, 24
professionals, 143 relevance, 20
profit, 70, 74 renewable energy, 60
profitability, iii, 54, 55, 127 rennet-induced milk coagulation, iii, 92
progesterone, 130, 131, 132, 133, 146, rent, 14
148 repair, 39
prognosis, 47 reproduction, i, 34, 45, 65, 69, 70, 72, 73,
programming, 148 81, 82, 129, 135, 148
project, 139 reproductive efficiency, i, iii, 54, 68, 70,
proliferation, 93 71, 72, 81, 85, 128, 129, 134, 135, 142,
prophylactic, 63 145, 147, 148
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160 Index
requirements, 38, 61, 63, 66, 74, 95 serology, 10, 33

researchers, 4, 77, 102 serum, iii, 22, 48, 92, 103, 104, 106, 109,
reserves, 70 111, 123, 133, 146
residues, ii, 54, 59 serum albumin, 103, 104, 107, 109, 111,
resilience, 55, 57, 82, 83 123
resistance, 33, 50, 63, 67, 71, 74, 83, 98, services, 10, 55, 68, 72, 76, 95, 128, 138,
104, 107, 109, 111, 123, 141, 146 142
resources, 54, 55, 57, 61, 73, 78, 79, 84, sex, 42
120 sex ratio, 42
respiration, 67 sexually transmitted diseases, 135
respiratory distress syndrome, 24, 42 shade, 67
response, iii, 3, 34, 48, 63, 92, 94, 103, shape, 130
105, 131, 133, 136, 141, 146 sheep, 9, 47, 48, 107, 113, 122
retardation, ii, 2, 9, 13, 27, 38, 46, 47, 50 shelter, 62
rewards, 76 showing, 4, 15, 139
rights, 55 signals, 94
risk, 6, 29, 36, 38, 45, 55, 56, 58, 61, 88, signs, 4, 6, 21, 31, 133, 134
103, 138 simulation, 75
risk factors, 6, 29, 36, 38, 45, 88 single-nucleotide polymorphism, 104
risks, 44, 56, 63 skeletal muscle, 20
rotations, 57, 62 skin, 32, 46, 93
rules, 58, 81 social behavior, 84
rural areas, 75 social interactions, 61, 65
rural development, 76 society, 76, 79
sodium, 81
solidarity, 55, 75
S
solution, 74, 109
somatic cell, i, iii, 86, 91, 93, 94, 95, 98,
safety, ii, 54
99, 100, 101, 102, 105, 106, 111, 113,
Salmonella, 21, 33, 48
114, 116, 117, 118, 119, 120, 121, 122,
science, 50
123, 124, 125, 126
scientific publications, 10
somatic cell count (SCC), iii, 91, 93, 98
sclera, 17
South Africa, 40, 43, 117, 126
scope, 59
South America, 134, 140, 141
secretion, 104, 107, 111
SP, 141
security, 56, 57
Spain, 53, 82, 87, 96
sedimentation, 109
specialisation, 54
seeding, 144
specialization, 58
selenium, 34, 45
species, 9, 33, 34, 35, 63
self-assessment, 48
sperm, 137, 139, 143, 147
semen, 69, 134, 138, 139, 143
spine, 14, 15
sensitivity, 32, 36, 101, 104, 107, 108,
spleen, 20
109, 111, 140, 144
sepsis, 22
Index 161
stability, iii, 83, 91, 108, 109, 111, 112, syndrome, 16, 24, 25, 32, 42, 44, 49
114, 117, 120, 123, 124 synthesis, 95
stabilization, 124 synthetic analogues, 129, 130
stakeholders, 4, 60
state, 120
T
states, 98, 105
statistics, 82
tanks, 144
steroids, 132
techniques, ii, 35, 37, 38, 42, 54, 72, 134,
stillbirth, 4, 5, 7, 29, 39, 40, 41, 42, 44,
143, 145
45, 46, 47, 49, 71
technological change, 54
stimulation, 143
technological progress, 55
stimulus, 147
technologies, 59, 63, 68, 129, 145
stock, 54, 145
technology, 73, 128, 145
stomach, 26
teeth, 24, 25
storage, 14, 59, 109
temperature, 7, 26, 67, 80, 84, 108, 109,
strategic management, 129, 141
121, 124, 140, 144, 146
stress, 25, 36, 37, 46, 47, 50, 66, 67, 72,
testing, 30, 34
80, 81, 83, 84, 87, 94, 127, 128, 134,
textbooks, 32
140, 145, 146
therapy, 35, 40, 125
stretching, 32
thermal stability, iii, 91, 108, 109, 112
structural defects, 14
thermal treatment, 108
structure, 58, 103, 105, 115
threats, 63
Styles, 54, 88
threshold level, 78, 94
subacute, 61
thymus, 17, 20
subjectivity, 77
thyroid, 22, 23, 28, 33, 44, 45
submucosa, 18
thyroid gland, 22, 34
Sun, 119
tissue, 94
supplementation, 34, 62, 63, 130
torsion, 16, 32
surfactant, 33, 47
toxicity, 25, 36
surveillance, i, 1, 6, 10, 36
toxin, 21
survival, 93, 146, 147
trace elements, 49
susceptibility, 34, 93, 98
trachea, 26
sustainability, 54, 55, 56, 63, 68, 75, 76,
trade, 80
77, 78, 79, 80, 81, 82, 83, 84, 86, 88,
trade-off, 80
89
traits, 68, 69, 70, 71, 72, 73, 80, 81, 84,
sustainable development, 86
86, 87, 88, 117, 119, 121, 122, 123,
Sweden, 5, 7, 79, 82, 85, 87, 95, 97, 105
125
swelling, 16, 24
transfusion, 20
Switzerland, 5, 40, 69, 77, 88
transmission, 135
symptoms, iii, 91, 93, 97
transport, 140
synchronization, 61, 68, 127, 129, 131,
transportation, 138, 139
141, 147
trauma, 6, 7, 14, 17, 20, 25, 27, 28
synchronize, 61, 128
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162 Index
traumotocia, ii, 2, 13, 14, 15, 16, 17, 26, vitamin E, 42

31, 38 vitamins, 121
treatment, 47, 63, 68, 96, 97, 108, 111, VLA, 20, 21, 50
115, 125, 130, 132, 146, 148 vulnerability, 78
tuberculosis, 135
Turkey, 46
W
twinning, 35
twins, 11, 17, 24, 45
Wales, 49
Washington, 88
U water, 55, 56, 57, 59, 60, 62, 67, 76, 93,
108
UK, 3, 5, 39, 48, 49, 51, 77, 80, 82, 84, weakness, 24, 26
87, 88 weight gain, 71
ultrasonography, 137 weight ratio, 22, 37
ultrasound, 139, 147 welfare, iii, 54, 57, 60, 61, 63, 64, 65, 66,
umbilical cord, 32 67, 68, 73, 78, 79, 80, 83, 85, 86, 88,
undernutrition, 26 90
United, 40, 46, 88, 95, 121, 140 well-being, 90
United Kingdom, 88, 121 WHO, 3, 4, 7, 10, 20, 35, 50
United Nations, 88 wind speed, 26
United States, 40, 46, 95, 140 withdrawal, 130
urban, 50, 75 workflow, 37
urban areas, 75 World Bank, 81
urine, 34 World Health Organisation, i, 1, 50
USA, 4, 5, 7, 43, 45, 48, 50, 96, 97, 119 worldwide, 54, 58
V Y
vagina, 138 yeast, 92

vancomycin, 104 yield, iii, 36, 59, 60, 62, 67, 68, 69, 70,
variations, 6, 132, 134 72, 74, 92, 98, 100, 101, 103, 104, 106,
ventricular septal defect, 31 107, 108, 112, 113, 114, 116, 118, 119,
vertebrae, 48 121, 122, 125, 126
vessels, 20
Vietnam, 122
Z
virology, 10
viruses, 92, 104, 105
zinc, 120
viscera, 32
vision, 79, 86

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ANIMAL SCIENCE, ISSUES AND PROFESSIONS

ANIMAL SCIENCE, ISSUES

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Additional e-books in this series can be found on Nova’s website

ANIMAL SCIENCE, ISSUES AND PROFESSIONS

Copyright © 2013 by Nova Science Publishers, Inc.

NOTICE TO THE READER

Independent verification should be sought for any data, advice or recommendations

Library of Congress Cataloging-in-Publication Data

ISBN:  (eBook)

Published by Nova Science Publishers, Inc. † New York

In this book, the authors discuss the reproduction, nutritional management

combination of contributory factors (more than one cause of death), congenital

significantly increased. The significant impact of SCC on content of these

A NOVEL, ILLUSTRATED CLASSIFICATION

based review, the findings of an international Delphi survey and

Classification attempts to define whether a perinate died of or due to a disorder

diagnostic support systems such as the Cornell Consultant in the USA

Definition of Perinatal Mortality

Bovine perinatal mortality may be defined as the death of a fullterm

Table 1. Examples of descriptors used to define the term

Table 2. Examples of descriptors used to define the term bovine

Causes of Bovine Perinatal Mortality

There appears to be some agreement in the literature on the common

Table 3. Necropsy-diagnosed causes of death (%) for calves dying

De Kruif and Benedictus

Table 4. Number of cause of death categories (excluding undetermined)

Causes of death Calves (No.) Reference

Criteria Used to Define Causes of Perinatal Mortality

The foregoing indicates that there is limited consensus on the common

MATERIALS AND METHODS

Initially all publications where a necropsy-derived diagnosis of bovine

In order to elicit current consensus from veterinarians about both the

A prospective, longitudinal, active surveillance necropsy study was

Table 5. Birth weights (kg) (mean, mean+2SD, range), gestation length

Jersey, Jersey, 16.54- 21.8 10.92- 284.6

The causes of death with an incidence >5% were assigned individual

When the causes of death were originally classified following the

Definitions of Cause of Death

diagnoses of cause of death are reached through both processes of inclusion,

Table 6. Prevalence of individual * causes of perinatal mortality

Cause of death % of calves Rank

Following sequential aggregation of these three primary sources of

1. Combination of Contributory Factors

were combined into the combination cause of death category as it is not

2. Congenital Defect (Lethal and Economically-Lethal)

Figure 2. Fractured spine at the thoraco-lumbar junction with extensive haemorrhage

Figure 3. Marked capital and lingual swelling due to subcutaneous oedema

Bradytocia: moderate or severe subcutaneous antemortem oedema (e.g.

haemorrhages on internal organs, e.g. tracheal mucosa, heart (epicardium,

4. Eutoxia (Eutocia with Anoxia)

5. Haemorrhagic and Haematological Disorders

Figure 4. Extensive haemorrhage in the tracheal submucosa (anoxia).

Figure 5. Severe meningeal congestion (anoxia).

Figure 6. Severe bilateral peri-umbilical artery haematomata (internal omphalorrhagia).

Figure 7. Marked pallor of the entire carcass (anaemia).

Hepatic rupture associated-haemoperitoneum: moderate or severe

not consumed colostrum. This is a probable or possible cause of death

Figure 8. Fibrinous pericarditis (infection).

Because the placenta is frequently contaminated, isolation from the

Figure 9. Severe microfollicular thyroid hyperplasia (iodine imbalance).

8. Premature Placental Expulsion (PPE)

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