Reprod Dom Anim doi: 10.1111/rda.
12139
ISSN 0936–6768
An International Delphi Study of the Causes of Death and the Criteria Used to
Assign Cause of Death in Bovine Perinatal Mortality
JF Mee1, C Sanchez-Miguel2 and M Doherty3
1
Animal and Bioscience Research Department, Teagasc, Moorepark Research Centre, Fermoy, Co., Cork, Ireland; 2Regional Veterinary Laboratory,
Department of Agriculture, Food and the Marine, Cork, Ireland; 3Section of Herd Health & Animal Husbandry, School of Veterinary Medicine,
University College Dublin, Dublin, Ireland
Contents
The objective of the present study was to elicit opinion from
two groups of veterinarians [subject matter experts and non-
subject matter experts] about the causes of bovine perinatal
mortality and the criteria used to assign such causes. The
subject matter experts 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-subject matter experts were self-
selected as cattle veterinarians without particular expertise in
bovine perinatology. A total of 74 veterinarians (46 subject
matter experts and 28 non-subject matter experts) 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. There was a
close agreement between groups on 16 causes of death apart
from intra-uterine growth retardation (IUGR) and micronu-
trient imbalances which were accepted by fewer subject matter
experts. There was inter-group consensus on the criteria to
diagnose accidents, congenital defects, dystocia, hyperthermia,
infections, premature placental separation, prematurity and
prolonged calving. There was inter-group consensus on the
criteria to diagnose anoxia, apart from gingival cyanosis; on
haemorrhage, apart from haemorrhagic anaemia; on IUGR,
apart from organ weights; and on iodine imbalance, apart
from goitre and thyroid iodine content. The results from this
study highlighted the current lack of standardization of the
criteria used to define the cause of death for bovine perinatal
mortality and the need for such standardization.
Introduction
The Delphi technique is a tool for gathering information
and judgements from recognized sources of expertise
and non-expertise through an iterative process consist-
ing of ‘rounds’ of questions. Individual responses are
summarized in each successive round and returned to
respondents, allowing them to refine responses until a
consensus is met (Iqbal and Pipon-Young 2009). The
diagnosis of the cause of death in cases of bovine
perinatal mortality is subject to wide variation between
veterinarians and laboratories both in the accepted
causes of death and in the criteria used to assign these
causes of death. This leads to non-comparable data
when attempting to decide whether the proportion of
such calves dying from a particular cause is the same in
different laboratories, regions or countries or not. The
Delphi technique has not been used heretofore to
examine the cause of death in bovine perinatal mortal-
ity, to the authors’ knowledge.
The objective of this survey was to establish consensus
criteria to assign cause of death and the causes of death
© 2013 Blackwell Verlag GmbH
in bovine perinatal mortality to assist in a more
standardized classification of cause of death for bovine
perinatal mortality.
Materials and Methods
The survey was prospectively designed to elicit opinion
from subject and non-subject matter expert veterinari-
ans, as defined below. The survey was conducted over
7 months (February through August, 2012) in seven
rounds by blind carbon copy (bcc) emails. Two types of
respondents were targeted. First, a purposive sampling
design was used to invite a list of veterinarians with
expertise in bovine perinatology (subject matter experts)
drawn up based on their research work and publications
and/or diagnostic work in a veterinary laboratory and
dealing with bovine perinatal mortality. Second, a case
study sampling design was used to invite veterinarians
(confined to veterinarians who were members of an e-
discussion forum) without particular expertise in bovine
perinatology but working with cattle herds (non-subject
matter experts), through membership of a veterinary
e-discussion forum; Ireland: Veterinary Ireland
members (Vet.ie), Europe: European College of Bovine
Health Management members (ECBHM) and Interna-
tional but predominantly USA: American Association
of Bovine Practitioners (AABP).
An invitation email was sent to each list inviting
participation and requesting registration information
about the respondent’s work (diagnostic laboratory,
university or research institute, farm practice, or other-
specify). Of the 58 subject matter experts contacted, 42
(72%) registered and five other subject matter experts
and 35 non-subject matter experts self-registered, a total
of 82 registrants. Of these registrants, 74 (90%)
responded. Veterinarians worked in 23 countries around
the world. Respondents worked in universities or
research institutes (36), diagnostic laboratories (19),
farm practice (14) or as consultants (5).
In the initial round, general questions were asked
about the list of causes of death in bovine perinatal
mortality. In subsequent rounds more in-depth ques-
tions were posed on individual causes of death focussing
on the criteria used to assign a cause of death. In each
round, questions were asked about the topic and the
answers were collated, summarized and returned to the
respondents for further feedback by a deadline, with a
reminder email, in an iterative process. The data were
managed using Microsoft Excel 2007 (Microsoft Cor-
poration, Redmond, WA, USA). Differences between
the number of subject matter experts and non-subject
2 JF Mee, C Sanchez-Miguel and M Doherty

matter experts who agreed on a topic were compared
using chi-square analysis; the differences were consid-
ered significant if p < 0.05.
Results
The response rate to each round (77–98%) is shown in
Table 1.
Round 1: Causes of death
In this round, an alphabetical list of 16 possible causes
of death was sent to the participants (Table 2), and they
were asked whether they agreed with these diagnoses as
causes of deaths and whether not to explain why and
what other causes of death they would suggest.
The causes of death about which most respondents
(3–9%) disagreed, in order of frequency, were IUGR,
micronutrient imbalances, accident, prematurity, haem-
orrhage, infection after calving and premature placental
separation. Subject matter experts were less likely to
accept IUGR and micronutrient imbalances than
non-subject matter experts (p < 0.05). In total, 31
additional causes of death were suggested the most
frequent (4–10% of respondents) of which were, in
order of frequency, hypothermia, unexplained stillbirth,
trauma alone, body condition too low or too high and
intoxications. Approximately half of all respondents
suggested extra causes of death (49% of experts, 42% of
non-experts and 48% overall).
Round 2: Accidents and anoxia
Accidents
While the majority of respondents agreed with the
criteria listed to diagnose post-parturient trauma as an
accidental cause of death, more (15%) disagreed with
the criteria for aspiration pneumonia (Table 3). Addi-
tional causes of accidents suggested were accidental
trauma during assisted calving caused by inappropriate
use of a calf puller leading to calf death or euthanasia, a
blow to calf from a cow, stress of mustering pregnant
cows for tuberculin testing, cow slipping in the yard pre-
calving, excess umbilical haemorrhage if the umbilical
cord is severed too quickly and calf drowning in a water-
filled ditch.

Table 1. Number of registrants to each round and the number of Anoxia

subject and non-subject matter experts (SME and non-SME, respec-
tively) who responded to each round Haemorrhage, meconium staining, organ congestion and
cyanosis were accepted by the majority of respondents, in
SME Non-SME Total that order of frequency, as criteria to diagnose anoxia
Registrants respondents respondents respondents Response (Table 3). Subject matter experts were less likely to
Round (no.) (no.) (no.) (no.) rate (%) accept gingival cyanosis than non-subject matter experts
1 82 46 28 74 90
(p < 0.05). Additional criteria to diagnose anoxia sug-
2 63 37 23 60 95 gested were immaturity of the surfactant system, poor
3 68 35 23 58 85 colostral immunoglobulin absorption, umbilical haem-
4 62 30 18 48 77 orrhages, pooling of blood in the thorax and abdomen,
5 60 30 18 48 80 mid-laminar cerebrocortical necrosis, squames and
6 49 30 18 48 90
7 50 31 18 49 98
debris in alveoli, mild interstitial pneumonia without
accompanying bacteria, fractured vertebrae, atelectasis,

Table 2. Causes of death in alphabetical order (n = 16) and percentage of subject matter experts (SME) and non-SME respondents who agreed
with the listed causes of death

Cause of death SME (n = 46) Non-SME (n = 28) All (n = 74)

Accident 93 96 95
Anoxia (without difficult calving) 100 100 100
Anoxia (with difficult calving) 100 100 100
Combinations of causes of death 100 96 99
Difficult calving (history only of prolonged or 100 100 100
maldisposition calving and/or moderate–
severe traction – C-section)
Difficult calving (calving trauma lesions +/- 100 100 100
Dystocia history)
Difficult calving (prolonged calving lesions +/- 100 100 100
Dystocia history)
Difficult calving (trauma and prolonged calving 100 100 100
lesions +/ Dystocia history)
Haemorrhage in calf 96 100 97
Infection in utero 100 100 100
Infection after calving 96 100 97
Intra-uterine growth retardation 87 100 92
Lethal congenital defect 100 100 100
Micronutrient imbalance 89 100 93
Premature placental separation 96 100 100
Prematurity 93 96 95

© 2013 Blackwell Verlag GmbH

Delphi Survey of Bovine Perinatal Mortality
Table 3. Criteria suggested defining two causes of death, accident and anoxia and percentage of subject matter experts (SME) and non-SME
respondents who agreed with the listed criteria
Cause of death Criteria
Accident Post-parturient trauma – lesions indicative of trauma,
(e.g. fractured ribs, liver tear), with no history of
dystocia but with history of post-parturient trauma,
for example, cow stood on calf, automatic scrapers
on, and other
Aspiration pneumonia – colostrum in trachea and in
lungs +/- history of stomach tubing of colostrum
Other accident criteria?
Anoxia Haemorrhages on internal organs (trachea, epicardium,
endocardium, pleura, thymus, adrenals, sclera,
and other).
Congestion of meninges, internal organs (liver, kidneys,
adrenals), and other
Meconium staining of hair coat, abomasal contents,
tracheal contents, other
Cyanosis of gums
Other anoxia criteria?
peripheral oedema, meningeal haemorrhages and
endophthalmos.
Round 3: Dystocia and prolonged calving
This round raised the issue of nomenclature regarding
the term dystocia. While some respondents felt it should
be reserved for the cases of moderate or severe traction
only, with or without foetal lesions, others felt that
prolonged calvings should be incorporated under the
umbrella-term dystocia. Using the Greek basis for the
term, ‘dys’ means abnormal, bad or difficult, indicates
that dystocia does encompass all abnormal calvings
including prolonged calvings; thus, the terms traumot-
ocia (dystocia as a result of parturient trauma) and
bradytocia (dystocia as a result of prolonged calving)
are suggested as subcategories of dystocia.
Dystocia
There was almost unanimous agreement on the
criteria proposed to diagnose dystocia as a result of
parturient trauma as a cause of death (Table 4). Other
criteria suggested to diagnose dystocia as a cause of
death included supportive gross or microscopic foetal
lesions such as anoxia (CNS haemorrhages), fractured
spine, femoral nerve damage, dehydration, bruising of
the head, uterine torsion, incomplete cervical dilata-
tion, uterine inertia, small pelvic diameter, maternal
trauma (torn, ecchymoses, and/or swelling of the
vulva/vagina, difficulty in standing/unable to rise)
where the calving is unobserved and an oversized calf
is delivered.
Prolonged calving
There was almost complete agreement on the criteria
proposed to diagnose prolonged calving as a cause of
death (Table 4). Additional criteria suggested to diag-
nose prolonged calving as a cause of death included
gross and histological anoxic/foetal distress lesions
(meconium staining, CNS haemorrhages, tracheal,
© 2013 Blackwell Verlag GmbH
3
SME (n = 37) Non-SME (n = 23) All (n = 60)
95 100 97
86 87 87
14 22 17
92 87 90
78 83 80
89 83 87
65 91 75
32 9 23
pericardial, and other organ petechiae, slow rise of the
calf to sternal recumbence), premature placental expul-
sion, foetal skeletal trauma (owing to excessive breath-
ing movements), uterine torsion, incomplete cervical
dilatation, uterine inertia caused by low dietary magne-
sium, olfactory aberrant amniotic fluid, loss of foetal
hair or hoof capsules and foetal maceration.
Round 4: Haemorrhage and hypothermia
Haemorrhage
While the majority of respondents agreed with the
criteria listed to diagnose haemorrhage as a cause of
death, this varied with the different categories of
haemorrhage (Table 5). Additional comments included
a higher prevalence in fat cow calvings (disturbed
coagulation as a result of hepatic steatosis) and the
presence of excess blood on the floor of the calving site.
Hypothermia
Two-thirds of respondents agreed with the criteria listed
to diagnose hypothermia as a cause of death, a low
proportion relative to other causes of death (Table 5).
Additional comments included other factors may com-
promise the calf, for example, no colostrum intake, (the
‘starvation/mismothering/exposure’ complex in lambs
was cited as an analogous condition), lesions are not
striking as some calves die quickly, more likely to occur
in hypoxic calves after dystocia which are unable/slow
to stand and often seen in calves born unobserved in
unbedded tie-stalls or in cubicle houses pushed out by
the automatic passage scrapers, that is, born onto a wet
surface. Additional criteria suggested to diagnose hypo-
thermia as a cause of death included no evidence of
colostrum intake, history of severe weather conditions,
no suck reflex, low rectal temperature (<36.5°C),
inability to stand, depleted internal adipose reserves,
change in body fat colour to red hue, low muscle
glycogen and blood glucose concentrations, frozen legs
and ear tips, wet hair coat and absence of other
diagnostic signs.
4 JF Mee, C Sanchez-Miguel and M Doherty

Table 4. Criteria suggested defining two causes of death, dystocia and prolonged calving and percentage of subject matter experts (SME) and
non-SME respondents who agreed with the listed criteria

Cause of death Criteria SME (n = 35) Non-SME (n = 23) All (n = 58)

Dystocia Parturient trauma lesions (e.g. fractured ribs, spine, 100 96 98

mandible, legs, diaphragmatic tear and liver tear)
+/ dystocia history (e.g. unobserved calving)
History of dystocia without traumatic lesions 91 96 93
(e.g. maldisposition…)
Other criteria you suggest? 43 35 40
Prolonged calving Oedema of peripheries (e.g. tongue, head, neck, 97 96 97
legs..) +/ prolonged calving history
(e.g. unobserved calving)
History of prolonged/slow calving without oedema 91 91 88
lesions (e.g. uterine inertia, hypocalcaemia, maldisposition)
Other criteria you suggest? 43 9 29

Table 5. Criteria suggested defining two causes of death, haemorrhage and hypothermia and percentage of subject matter experts (SME) and
non-SME respondents who agreed with the listed criteria

SME Non-SME All

Cause of death Criteria (n = 30) (n = 18) (n = 48)

Haemorrhage in/ Omphalorrhagia only: moderate or severe haemoperitoneum or severe periumbilical 97 100 98
from perinate arterial haematoma with at least one unsealed umbilical artery (in the presence
or absence of dystocia)
Presumptive omphalorrhagia: moderate or severe blood staining of the hair coat 87 94 90
around the umbilicus and anaemia with at least one unsealed umbilical artery
(in the absence of haemoperitoneum or umbilical artery haematoma in the
presence or absence of dystocia).
Hepatic rupture–associated haemoperitoneum: moderate or severe haemoperitoneum 80 72 77
with hepatic rupture (in the absence of dystocia trauma)
Haemorrhagic anaemia only: blood loss causing pallor of skeletal muscles, conjunctiva 70 89 77
and internal organs, for example, liver, kidneys, thymus and brain (in the absence
of haemoperitoneum, omphalorrhagia, hepatic rupture or dystocia)
Hypothermia History of <0°C ambient temperature, unobserved calving, and calf not born into a 60 78 66
straw bed (e.g. born in the cubicle house passageway or outdoors) combined with
distal limb subcutaneous haemorrhages and oedema, particularly of the hind limbs.
Other criteria for hypothermia you suggest? 40 22 33

Round 5: Hyperthermia and infection
Hyperthermia
Less than half of all respondents agreed with the criteria
listed to diagnose hyperthermia as a cause of death
(Table 6). Additional comments included that heat
stress may be caused by maternal hyperthermia inde-
pendent of the weather (e.g. pyrexia as a result of
mastitis, meningitis, pneumonia or tick-borne fever) and
that this is not an important cause of death in cases of
bovine perinatal mortality.
Infection in utero
While the majority of respondents agreed with the
criteria listed to diagnose infection in utero as a cause of
death, this varied with the different criteria (Table 6).
Additional comments included the need to include
placental pathology and microbiology; other foetal
tissues for detection of antigens, if a low pathogenic
organism is detected one needs to grow a pure culture
and find associated lesions; tests other than culture; and
other pathogens, and antibodies are only relevant in the
absence of colostrum ingestion or maternal vaccination
and have poor diagnostic specificity. Other criteria
suggested for infection in utero included antigen detec-
tion by microscopy of abomasal fluid, elevated immu-
noglobulins (Ig) in pre-colostral foetal fluids, IUGR,
placentitis, chorioamnionitis and a history of maternal
illness.
Post-natal infection
The majority of respondents agreed with the criteria
listed to diagnose post-natal infection as a cause of
death (Table 6). Other criteria suggested for post-natal
infections included detection of antigens, very low
serum Ig concentrations and increased serum acute-
phase protein concentrations.
Round 6: Intra-uterine growth retardation (IUGR) and
congenital defects
Intra-uterine growth retardation
While the majority of respondents agreed with the body
size criteria (weight and CRL) listed to diagnose IUGR
as a cause of death, the majority of respondents
disagreed with the organ weight criteria (absolute and
relative weights) (Table 7). Subject matter experts were

© 2013 Blackwell Verlag GmbH

Delphi Survey of Bovine Perinatal Mortality 5

Table 6. Criteria suggested defining two causes of death, hyperthermia and infection and percentage of subject matter experts (SME) and non-
SME respondents who agreed with the listed criteria

SME Non-SME All

Cause of death Criteria (n = 30) (n = 18) (n = 48)

Hyperthermia (heat stress) Lesions of anoxia (haemorrhages, congestion of organs) or of death 53 50 52

in utero (autolysis) in carcass, +/ foetal undersize, and a history
of high ambient temperature or temperature–humidity index (THI)
Infection in utero Gross/histological lesions of infection in foetus, for example, 100 100 100
pneumonia, pericarditis…
Culture of significant pathogen in pure or nearly pure culture 100 94 98
from the foetus (e.g. abomasum) (e.g. L monocytogenes,
T. pyogenes, S. Dublin…)
Detection of antibodies to significant pathogens in the foetus 80 78 79
(e.g. L.hardjo, N. caninum…)
Detection of BVDV antigen in the foetus 93 94 94
Other criteria for infection in utero you suggest? 43 22 35
Post-natal infection Gross/histological lesions of infection in the neonate (0–48 h 93 94 94
old), for example, pneumonia, peritonitis, meningitis, pericarditis
Other criteria for post-natal infection you suggest? 47 28 40

Table 7. Criteria suggested defining two causes of death, intra-uterine growth retardation (IUGR) and congenital defects and percentage of
subject matter experts (SME) and non-SME respondents who agreed with the listed criteria

SME Non-SME All

Cause of death Criteria (n = 30) (n = 18) (n = 48)

Intra-uterine growth Full-term calf (  95% gestational age; gestational age >280 days) 93 89 92
retardation (IUGR) but low body weight for gestational age (<mean-2SD) or
small size for gestational age [crown-rump length (CRL) <mean-2SD] or 87 89 92
 two low absolute organ weights for gestational age (<mean-2SD) or 40 66 50
 two low relative organ weights for gestational age (<mean-2SD). 27 66 42
Other criteria for IUGR you suggest? 43 5 29
Congenital defect (lethal and Grossly visible lethal structural defects such as (but not exclusively) 100 100 100
economically-lethal) hydranencephaly, schistosomus or….
Grossly visible structural defects which are economically-lethal such as 100 100 100
(but not exclusively) intestinal atresia, vestigial limbs, severe arthrogryposis,
severe cardiac defects, chondrodystrophy or…
Other criteria for congenital defects you suggest? 30 33 48

less likely to accept the absolute (p < 0.10) and relative
organ weight criteria (p < 0.01) than non-subject matter
experts. Other criteria suggested for IUGR included
full-term but clinical signs of immaturity (hair coat,
teeth, general development), radio-opaque growth arrest
lines in tibia, limb/bone length or circumference,
disproportionately large head size, birth weight/gesta-
tion length ratio, body mass index, abdominal circum-
ference, placental weight/dam weight ratio and low
blood IGF-I in live-born calves.
Congenital defects
There was unanimity of opinion amongst respondents
on the criteria listed to diagnose congenital defects as a
cause of death (Table 7). The term economically-lethal
was coined to cover defects which of themselves are not
immediately lethal but which when occurring in calves
on modern farms are likely to result in euthanasia, as
they are not independently viable, for example, arthro-
gryposis. Other criteria suggested for diagnosis of
congenital defects included non-visible functional
defects such as metabolic disorders and storage disor-
ders and histological or radiological abnormalities.
Euthanasia was considered the cause of death where
deformed calves survive but have to be killed on humane
or economical grounds. Differentiation of heritable
from non-heritable defects was considered important
also.
Round 7: Iodine imbalance, prematurity and premature
placental separation
Iodine imbalance
A small majority of respondents agreed with the absolute
thyroid weight (goitre) criterion to diagnose iodine
imbalance as a cause of death (Table 8). A minority of
respondents agreed with the relative thyroid weight
criterion to diagnose iodine imbalance as a cause of death
(Table 7). The majority of respondents agreed with the
histopathological abnormality criteria to diagnose iodine
imbalance as a cause of death (Table 8). A small majority
of respondents agreed with the low thyroid iodine content
criterion to diagnose iodine imbalance as a cause of death
(Table 8). Other criteria suggested for the diagnosis of
iodine imbalance included maternal plasma inorganic
iodine content (PII), urine iodine content, maternal blood
iodine content higher than pre-colostral calf iodine
content or abnormal maternal or foetal blood T3/T4
ratio or TSH concentrations, clinical signs of cretinism

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6 JF Mee, C Sanchez-Miguel and M Doherty

Table 8. Criteria suggested defining three causes of death, iodine imbalance, prematurity and premature placental separation and percentage of
subject matter experts (SME) and non-SME respondents who agreed with the listed criteria

SME Non-SME All

Cause of death Criteria (n = 31) (n = 18) (n = 49)

Iodine imbalance Goitre (weight of thyroid >30 g) or 55 61 57

Relative goitre (thyroid weight/birth 32 55 41
weight >0.70) or
Histopathologically abnormal thyroid (macrofollicular 77 72 76
hypoplasia or microfollicular hyperplasia) or
Low thyroid iodine content 48 66 55
Other criteria for iodine imbalance you suggest? 23 44 31
Prematurity Less than full-term gestational age (<95% of gestational 97 94 96
age or < mean-2SD) with proportionately small body size
(birth weight or CRL) and organ immaturity or
Where gestation length is unknown – clinical signs of immaturity 87 94 90
(small body size, short hair coat, partially erupted teeth,
rounded skull, perinatal respiratory distress)
Other criteria for prematurity you suggest? 19 11 16
Premature placental Emergence of the placenta during or immediately after calving 87 94 90
separation or where calving is unobserved, calf born with placenta attached.
Other criteria for premature placental separation you suggest? 26 16 22

(premature birth, fluffy, long hair coat, ‘baldy calf’,
visibly enlarged thyroid), neuropathological brain
changes, hypoplastic hair follicles, fibrous and nodular
goitre, at least two of three possible criteria (e.g. absolute
or relative goitre or abnormal histology) and response to
iodine supplementation.
Prematurity
The majority of respondents agreed with the gestational
and non-gestational criteria to diagnose prematurity as
a cause of death (Table 8). Other criteria suggested for
diagnosis of prematurity included low body weight for
date but good vitality, gestation less than 260 days,
other clinical signs (floppy ears, abnormally long and
soft hooves), incomplete ossification of carpus and
tarsus, neurological immaturity [reduced suck reflex,
uncoordination, respiratory distress syndrome (RDS),
dullness, dysphagia] and histological evidence of imma-
turity (histological evidence of acute RDS).
Premature placental separation
The majority of respondents agreed with the criteria to
diagnose premature placental separation as a cause of
death (Table 8). Other criteria suggested for diagnosis
of premature placental separation included uterine
inertia; normal calving duration but calf and placenta
expelled together; pre-parturient blood loss or bloody
mucous with an open cervix, part of placenta appears
before the calf is born; autolysis in the foetus, perhaps
placentitis if infection involved; hypoxia after a normal
calving, placenta previa and milk fever or uterine
torsion (i.e. factors which do not stop the onset of
calving but do prevent the delivery of the foetus).
Discussion
The results of this study provide unique insights into the
causes of bovine perinatal mortality as perceived by
subject matter experts and non-subject matter experts.
While equivalent results were obtained from the subject
matter experts and non-subject matter experts on the list
of causes of death of bovine perinatal mortality, the
subject matter experts tended to disagree more about
more causes of death than the non-subject matter
experts. The causes of death associated with the most
disagreement were those for which the diagnostic
criteria are unclear, for example, IUGR and micronu-
trient imbalances. Numerous ultimate and proximate
causes of death were suggested in addition to those
listed in round 1, but in only two cases, hypothermia
and unexplained stillbirth, was there more than a
sporadic suggestion for inclusion as a cause of death.
While the latter suggestion is technically not a cause of
death, it probably reflects the experience of the respon-
dents in assigning it as a diagnosis of exclusion and its
citation in the relevant literature (Berglund et al. 2003;
Muskens et al. 2004; Schefers 2009).
Post-parturient trauma was widely accepted as a cause
of death by both subject matter expert and non-subject
matter expert but with the caveat that the history was
critical to making the diagnosis. Studies on bovine
perinatal mortality have either not recorded this cause
of death (e.g. Muskens et al. 2004; Syrjala et al. 2007) or
shown this to be a very uncommon cause of death
(Waldner et al. 2010). While the majority of both
groups accepted aspiration of colostrum as a cause of
death, they emphasized that pneumonia may not always
be present at death; hence, the term should be changed
from aspiration pneumonia to colostrum aspiration.
The lesions commonly ascribed to anoxia (haemor-
rhages, congestion, meconium staining) were accepted
by the majority of both groups as criteria to diagnose
anoxia. Perhaps, it was noted that these lesions do not
cause death per se but do represent underlying anoxic-
ischaemic pathology. This was a recurring theme across
causes of death of visible lesions not causing death per
se. as while the pathology may be visible the patho-
physiology, in this case anoxia, hypercapnia and met-
abolic acidosis, may not. Gingival cyanosis was
accepted as a diagnostic criterion but by fewer of the
subject matter experts as it was felt this lesion is also
observed in calves which survive calving. Several addi-

© 2013 Blackwell Verlag GmbH

Delphi Survey of Bovine Perinatal Mortality
tional anoxic criteria were suggested, many of which are
accepted as lesions of anoxic pathology in the literature,
for example, squames and debris in the alveoli, atelec-
tasis and peripheral oedema (Dufty and Sloss 1977; Van
Dijk et al. 2008; Lopez 2012).
Round 1 highlighted the need for precision when
using nomenclature to describe clinicopathological con-
ditions. While some respondents reserved the term
dystocia for cases of moderate or severe traction at
calving with or without foetal lesions, others included
any abnormal calving. Thus, in round 3, the term was
clearly defined by subdividing it into trauma, dystocia
anamnesis and prolonged calving cases. The overwhelm-
ing majority of respondents from both groups agreed
with the criteria to assign traumatic and anamnesis-
based dystocia cases. This is not surprising as dystocic
trauma is considered one of the most important causes
of bovine perinatal mortality (Berglund et al. 2003;
Syrjala et al. 2007; Waldner et al. 2010).
The unanimity of agreement across groups on the
criteria to diagnose prolonged calving was tempered by
the need to more clearly define the term ‘prolonged
calving’. The subdivision between prolonged first and
second stage of calving was emphasized as the associ-
ated lesions are different. But the difficulty in clearly
defining prolonged stage one of calving in some cases
was noted, particularly in an unobserved calving. The
numerous additional criteria suggested associated with
prolonged calving demonstrated the breadth of clinico-
pathological experience in both groups of respondents
and the lesions commonly listed in the literature
(Everett-Hincks et al. 2007; Lopez 2012).
Unlike the foregoing causes of death, there was some
variation both between agreed causes of calf haemor-
rhages and in the criteria for these causes between groups.
Whereas omphalorrhagia is not commonly diagnosed as
a cause of death (Vanholder et al. 2001), internal
omphalorrhagia was almost unanimously accepted by
both groups as a cause of death of bovine perinatal
mortality. The subject matter experts were less likely to
accept presumptive omphalhorrhagia as a cause of death
than the non-subject matter experts unless extensive
blood–staining of the hair coat was evident along with the
other criteria. Even fewer of both groups accepted hepatic
rupture-associated haemoperitoneum as a cause of death
in the absence of dystocia trauma. A similarly lower
proportion of subject matter experts accepted haemor-
rhagic anaemia as a cause of death in the absence of visible
haemorrhage probably reflecting the very low prevalence
of this condition in cases of bovine perinatal mortality
(Kirkbride 1992; SAC 2011a).
Compared with these causes of death above, a
relatively modest majority of respondents, particularly
of subject matter experts, accepted hypothermia as a
cause of death. Pertinent points of disagreement
included the absence of pathognomonic pathological
lesions in such cases and the wide variability in the
inciting inclement weather conditions. However, exper-
imental studies in calves have demonstrated typical
lesions following exposure to low ambient temperature
(Olson et al. 1981) and this condition has been listed in
the literature as a cause of death in cases of bovine
perinatal mortality, albeit in a very small proportion of
© 2013 Blackwell Verlag GmbH
7
cases (Waldner et al. 2010). Hypothermia was more
accepted as a diagnosis of exclusion than of inclusion.
Hyperthermia was not accepted by the majority of
respondents, particularly the non-subject matter experts
as a cause of death. This disagreement centred on the
absence of pathognomonic lesions at necropsy and
the absence of any evidence that heat stress can affect
the full-term bovine foetus. However, there is a consid-
erable corpus of peer-review literature which clearly
demonstrates that heat stress can adversely affect the
bovine foetus (Yates et al. 2012). Infection in utero was
an accepted cause of death by the majority of both
groups of respondents particularly where gross or
histological lesions were observed. This is consistent
with the results of studies on bovine perinatal mortality
where such lesions are the most common criteria used to
diagnose infection as a cause of death (Syrjala et al.
2007; Waldner et al. 2010). However, a smaller majority
of respondents accepted detection of antibodies in the
foetus as evidence of infection as a cause of death citing
this as merely evidence of exposure after immune-
competence. For some infections, for example, Neospora
caninum, there is excellent agreement between foetal
seropositivity and confirmed diagnosis of Neospora
caninum (Barr et al. 1995). Although post-natal infec-
tions were accepted by the majority of both groups as a
cause of death, the difficulty in differentiating between
pre- and post-natal infections in some cases was
highlighted as well as the interaction with failure of
passive transfer of immunoglobulins.
In principle the majority of respondents from both
groups agreed with the gestational and body size criteria
to diagnose IUGR. However, caveats were suggested in
relation to the need for breed- and parity-specific
thresholds. Unfortunately these are not widely available
in the published literature for cattle except for certain
breeds, for example, Jersey (Richardson et al. 1990). In
contrast, the majority of respondents from both groups,
in particular the subject matter experts, disagreed with
the organ weight-based criteria for IUGR. This was a
surprising finding. However, the lack of clarity about
how many organs may be affected and whether organs
are differentially affected was noted. This lack of
confidence in organ weight-based criteria is supported
by the evidence in the literature of some calf organs
being lighter (e.g. thymus) while others are heavier (e.g.
brain) in cases of IUGR (Steinhardt et al. 1993). The
differential effects on organ weights in cases of IUGR
may depend on the acute (e.g. Bluetongue virus;
Richardson et al. 1985; summer mastitis; Richardson
et al. 1982) or chronic [e.g. maternal systemic infection
or debilitating disease with or without placentitis (e.g.
Bacillus licheniformis, paratuberculosis; Scott 2011) and
maternal undernutrition (Wu et al. 2009)] nature of the
insult. In contrast to bovine perinatology, IUGR is
considered a major antecedent of human stillbirth,
particularly ‘unexplained’cases (Gardosi et al. 2005).
Lethal congenital defects were accepted by almost all
respondents as a cause of death, although the nomen-
clature was debated with the term ‘defects that signif-
icantly compromise vitality’ suggested as an alternative.
Such unanimity is not surprising as congenital defects
are listed in nearly all studies on bovine perinatal
8 JF Mee, C Sanchez-Miguel and M Doherty
mortality as a minor, though easily diagnosed, cause of
death (Khodakaram-Tafti and Ikede 2005; Syrjala et al.
2007; Waldner et al. 2010). While the need to include
non-visible defects was suggested by many respondents,
in practice this is not possible in most routine veterinary
diagnostic laboratories or by veterinary practitioners
internationally, except for selected defects (Agerholm
2007).
Perhaps, surprisingly only a small majority of respon-
dents accepted goitre as a criterion for diagnosis of
iodine imbalance. This has long been a classical finding
in iodine deficiency across a wide range of species (e.g.
calves – Van Wuijckhuise et al. 2003; lambs – Knowles
and Grace 2007; babies – Hetzel and Mano 1989). For
some respondents, they were not familiar with micro-
nutrient imbalances as a cause of death for bovine
perinatal mortality in their experiences. For others they
had technical (e.g. they used a different goitre weight
threshold or felt calf body weight had to be taken into
account) or philosophical queries (e.g. goitre per se is
not a cause of death, merely a lesion).
Even fewer respondents accepted relative goitre as a
criterion to diagnose iodine imbalance as a cause of death
of bovine perinatal mortality. Again this is surprising as
this takes account of calf body weight and is accepted as a
criterion to assist diagnosis of iodine-responsive perina-
tal mortality (Synge 1982; Knowles and Grace 2007;
Judson and Barrell 2011). Disagreements with this
criterion were both technical (e.g. different thyroid/body
weight ratios used) and scientific (e.g. increased ratio may
be due to causes other than iodine imbalance). However,
many considered this a useful screening criterion to
decide whether to proceed with either biochemistry or
histology if the ratio was high.
In contrast to the above, the majority of respondents
agreed with abnormal thyroid histology as a criterion to
diagnose iodine imbalance. This is in agreement with the
literature on this subject (e.g. Durdevic et al. 1992;
Wither 1997).
A large minority of respondents disagreed with low
thyroid iodine content as a criterion to diagnose iodine
imbalance, mainly because of unfamiliarity with the
technique. While it is used in some veterinary labora-
tories (Smyth et al. 1996; AHVLA 2011; SAC 2011b), it
is not widely used internationally. Concern over the use
of a laboratory test in isolation to diagnose a clinical
condition was also expressed.
The other criteria suggested to diagnose iodine
imbalance included maternal blood or urine iodine
indicators, clinical signs in the calf and the response to
iodine supplementation. All of these have been used,
with variable success, in published studies (Mee et al.
1995; Guyot 2008; Judson and Barrell 2011).
While selenium deficiency was not specifically
addressed in the survey apart from the listing of
micronutrient imbalances as a cause of death in round
1, it may be involved in perinatal mortality by modu-
lating the severity of hypothyroidism-associated iodine
deficiency (Zagrodzki et al., 1998, Mee, 1996) or inde-
pendently via foetal cardiomyopathy (Yamini et al.
2005; Murray et al. 2008).
Gestational criteria were accepted by the majority of
respondents from both groups to diagnose prematurity
as a cause of death although caveats were offered, for
example, need breed-specific criteria, although the latter
are not widely available for cattle (Richardson et al.
1990). Despite the subjective nature of the non-gesta-
tional criteria the majority of respondents accepted
these to diagnose prematurity with some caveats, for
example, need more than one subjective feature of
prematurity. Unlike humans, where either a single
gestational or a foetal body weight threshold can be
used (Lawn et al. 2011), in cattle because of the
potential variation in both normal gestation length
and birth weight the definition of prematurity is less
clear cut. This is reflected in the absence of or variation
in the definitions used in standard texts (Roberts 1986;
Noakes et al. 2009) and original reference sources (e.g.
Schmidt et al. 2004; Karapinar and Dabak 2008).
While the majority of respondents from both groups
accepted the criteria to diagnose premature placental
separation, there was disagreement over the nomencla-
ture used. It was considered by some that technically the
placental does not separate prematurely merely that when
foetal expulsion is delayed the placenta is expelled at the
normal time but because of the delay in foetal expulsion it
now appears to be prematurely expelled. However, this
argument does not account for cases where the placenta
may separate before the foetus begins to be expelled
(placentitis, hormonal asynchrony) and in causing foetal
hypoxia may delay foetal expulsion, for example, through
induction of maldisposition, a frequent finding in the
cases of premature placental separation (Mee 1991).
Perhaps, the term premature placental expulsion should
replace premature placental separation?
Conclusion
The lack of standardization of the criteria used to define
cause of death internationally is the primary cause of the
lack of uniformity in the diagnosis of causes of death in
the cases of bovine perinatal mortality. This has been
one of the most important findings from this survey.
This study has generated some surprising findings on a
topic which rarely receives such international scrutiny.
These results indicate the need for both subject matter
experts and non-subject matter experts to engage more
regularly with peers to update their knowledge base on
conditions, such as bovine perinatal mortality, for which
they may assume conventional wisdom has been estab-
lished and does not require further debate. The results of
this survey suggest otherwise.
Acknowledgements
The authors thank the veterinarians who responded to the survey for
their cooperation and their time.
Conflict of interest
None of the authors have any conflict of interest to declare.
Authorship statement
Mee designed and conducted the survey and wrote the manuscript.
Sanchez-Miguel participated in the survey and assisted in redrafting
the manuscript. Doherty assisted in redrafting the manuscript.
© 2013 Blackwell Verlag GmbH
Delphi Survey of Bovine Perinatal Mortality
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Submitted: 24 Oct 2012; Accepted: 2 Dec
2012
Author’s address (for correspondence): John
F Mee, Animal and Bioscience Research
Department, Teagasc, Moorepark Research
Centre, Fermoy, Co. Cork, Ireland. E-mail:
john.mee@teagasc.ie