Retrospective study of bovine neonatal mortality: cases reported from INTA Balcarce, Argentina
E. L. Morrell1, D. P. Moore1, 2, A. C. Odeón1, M. A. Poso1, E. Odriozola1, G. Cantón1, F. Paolicchi1, R. Malena1, M. R. Leunda1, C. Morsella1, C. M. Campero1*
1 Animal Health Group, Instituto Nacional de Tecnología Agropecuaria (INTA), Balcarce;
2 Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina;
*Correspondence. E-mail: ccampero@balcarce.inta.gov.ar
ABSTRACT
A retrospective study was performed on 169 beef and dairy calves aged from 1 to 7 days old submitted to the Diagnostic Laboratories at INTA Balcarce, Argentina. Bacterial culture was performed for aerobic and microaerophilic organisms. Samples from spleen and lymph nodes, and peripheral blood mononuclear cells were also cultured for viral isolation on cell culture. Bovine rotavirus was detected by direct-ELISA. Multiple tissue samples were fixed in 10% formalin, routinely processed and stained with hematoxylin and eosin for microscopic examination. Etiological diagnosis was made in 70 of the 169 calves. Infectious agents were identified in 49 cases, the most common being Escherichia coli. When the histopathological examination was performed in cases with undetermined diagnosis, it was noted that 44 specimens had histological lesions, which suggested the presence of an infectious agent. In order to characterize the causes of bovine neonatal mortality, the protocols and methodology should be improved in further works.
Key words: Bovine; Neonatal mortality; Diagnosis; Beef; Dairy
RESUMEN
Estudio retrospectivo de mortalidad neonatal bovina. Casos hallados en INTA-Balcarce, Argentina. Se realizó un estudio restrospectivo en 169 terneros muertos 1 a 7 días después del nacimiento pertenecientes a rodeos para carne y leche, remitidos a los Laboratorios de Diagnóstico del INTA Balcarce, Argentina. Para detectar organismos aeróbicos y microaerófilos se realizó el cultivo bacteriano. Para el aislamiento viral sobre cultivo celular, se recolectaron muestras de bazo, ganglios linfáticos y sangre periférica. El rotavirus bovino fue identificado por ELISA directo. Se efectuó el examen microscópico de diferentes tejidos, los cuales fueron fijados en formol al 10%, procesados y teñidos con hematoxilina y eosina. Se obtuvo un diagnóstico etiológico en 70 de los 169 terneros. Se identificaron agentes infecciosos en 49 casos, siendo el más común Escherichia coli. En los casos con diagnóstico indeterminado, el examen histopatológico realizado determinó que 44 especímenes poseían lesiones compatibles con la presencia de agentes infecciosos. Es necesario mejorar los protocolos y las metodologías de trabajo a los fines de caracterizar las causas de mortalidad neonatal en bovinos.
Palabras clave: Bovino; Mortalidad neonatal; Diagnóstico; Carne; Leche
INTRODUCTION
Bovine neonatal mortality has generated several studies
worldwide (1, 4, 8, 27). Environment, management,
and presence of pathogenic agents are critical factors involved
in bovine neonatal mortality (8, 19, 26). Characterization
of its causes is an important step in controlling
and preventing productive and economic losses in the
bovine industry (1, 4, 5).
In Argentina, beef cattle are usually raised in extensive
grazing systems. In contrast, intensive farming methods
are used for dairy herds (11, 15). Reproductive and
productive losses resulting from infectious, metabolic, toxic
and genetic diseases have a considerable economic impact
on both beef and dairy herds (7). Although, several
causes have been associated with bovine neonatal mortality
worldwide (1, 4, 5, 8), regional data is scant. The
aim of this retrospective study was to characterize the
most relevant findings of bovine neonatal mortality in beef
and dairy herds according to the INTA Balcarce records.
MATERIALS AND METHODS
Background and origin of the specimens
Calves and various specimens (tissue samples, sera, feces
and intestinal content) were submitted to the Diagnostic Laboratories
at INTA, Balcarce, from 1994 to 2005 for diagnostic
purposes. The referred cases came from 61 commercial beef
herds (Aberdeen Angus, Hereford breeds and their crossbreeds)
and 15 dairy premises (Holstein and Jersey breeds) located in
37 counties from the pampas in Buenos Aires province.
The period of neonatal mortality (hebdomadal period) was
defined as calf loss occurring between 1 and 7 days of life (24).
Morbidity and mortality rates were not recorded in the present work.
Necropsy procedures
Standard necropsy procedures were performed, and breed,
sex and age were recorded (25). Data regarding the age of death,
when available, was provided by the private practitioner. In
addition, the postmortem findings such as thrombus in umbilical
artery, aerated lungs, presence of colostrum and/or milk in
digestive tract, and body fat metabolism were used to determine
the cause of neonatal death as was mentioned by Wikse et al.
(1994). One hundred and forty seven of the 169 (86.9%) calves
had died spontaneously, the remainders were euthanized due
to agonic stage and/or severe hypothermia. All animal experiments
were conducted in accordance with the guidelines of the
National Service of Animal Health.
Samples and laboratory procedures
Cultural isolation and characterization of bacteria were
performed by standard methods. Briefly, samples from several
tissues (lungs, liver, intestine, spleen, mesenteric lymph node
gall bladder and synovial fluid) were cultured aerobically on 5%
horse blood agar and MacConkey agar. Lung was also cultured
microaerophilically both on 5% horse blood agar for Brucella spp.
(3) and Skirrow agar and incubated for 7 days at 37 °C for Campylobacter
spp. (13, 16). Selection of the samples for specific culture
was based on previous herd antecedents and gross necropsy
findings. No attempt was made to identify Clostridium perfringens,
mycoplasmas and chlamydias.
Spleen and lymph node samples and peripheral blood
mononuclear cells were also subjected to viral isolation. Briefly,
a 10% tissue homogenate was prepared and inoculated onto
cultures of Madin Darbin Bovine Kidney (MDBK) cells. After four
blind passages, inoculated cultures were tested for bovine viral
diarrhea virus (BVDV) and bovine herpes-virus (BHV) antigens
by indirect fluorescent antibody tests (IFAT) with commercially
available polyclonal antibodies (American Bio-Research, Sevierville,
TN, USA). In addition, a direct-ELISA was performed in
feces for bovine rotavirus identification (17). Diagnosis of bovine
coronavirus was disregarded in this study due to its low incidence
in Argentina and because this virus affects clinically mostly 2-3
week old calves (34).
Tissue samples were taken from brain (cortex, midbrain,
medulla and cerebellum), adrenal glands, heart, kidney, liver,
lung, lymph nodes, skeletal muscle, spleen and thymus for histological
examination. Samples of all tissues with macroscopic
pathological changes were also taken for histopathological
analysis. Tissues were fixed in neutral-buffered 10% formalin,
routinely processed and stained with hematoxylin and eosin.
Kidney and liver smears were only taken from specimens having
macroscopic lesions compatible with Leptospira spp. (i.e., the
presence of jaundice and/or macroscopic lesions on liver and
kidney) and processed by a direct fluorescent antibody test
(DFAT) using a commercial conjugated antibody (rabbit antiserum
NVLS, Ca, USA) as described (20). Samples were selected for
laboratory analysis according to herd antecedents or based on
observations during macroscopic examination.
Diagnosis criteria
The diagnostic findings were categorized in groups according
to the necropsy, histopathological and microbiological findings
as previously described by the authors (14). After that, all the
specimens submitted were classified as determined (infectious
and non-infectious conditions) and undetermined cases (with and
without histological lesion).
Data Analysis
Data analysis regarding age of death were carried out by
comparison of mean pairs using the Student's t test. Causes of
death (determined or undetermined), death day, sex, and herd
origin were assessed by the Chi square test. The number of
cases for each etiological agent was analyzed by tests of
proportions. Statistical analyses were performed using SAS Software
v.6.0 (SAS Institute Inc.) (35). All statistical analyses were
considered significant when p < 0.05.
RESULTS
All calves were Bos taurus, being beef genotype (Aberdeen
Angus, Hereford and crossbreed) in 122 (72.2%)
cases, and dairy genotype (Holstein and Jersey) in 38
(22.5%) cases. The genotype was not recorded in 9 (5.3%)
cases.
Eighty five (50.3%) of calves were males whereas 67
(39.6%) were females. Sex was not recorded in 17 (10%)
cases. There were significant statistical differences between
the number of females and males according to their
origin p < 0.05, being 62 males and 47 females from the
beef herds, and 19 males and 18 females from the dairy
herds. Data regarding sex and/or origin were not available
in 23 cases.
Average age at time of death was 3.2 ± 2.3 days in
beef calves and 4.9 ± 2.4 days in dairy calves p < 0.05.
Calf's age was not recorded in 21 cases. Although arbitrarily
grouped, there were significant differences in the
number of calves dying between days 1 and 4 compared
with those between days 5 and 7 ( p < 0.05). Most calves
died between days 1 and 4 after birth (Figure 1). The
number of beef calves dying between days 1 and 4 was
higher than that recorded for dairy calves during the same
period ( p < 0.05) (Figure 1). In contrast, little variation
was recorded between beef and dairy calves dying between
days 5 and 7.
Figure 1. Number of deaths in beef and dairy calves arbitrary
grouped in days 1 to 4 and 5 to 7, * p < 0.05.
Moderate to severe autolysis was present in spontaneously
dying calves. Gross pathological findings including fibrinous pleuritis and/or pericarditis, peritonitis, pneumonia,
enteritis, meningitis, icterus and congenital defects
were seen at necropsy. In addition, starvation diagnosis
(4 calves) was performed by the appearance of the epicardial
and perirenal fat that changed from white and firm
to brown-red and gelatinous and presence of grass and/
or soil in the abomasum instead of milk or colostrum.
Hairballs were found in the abomasum of 2 beef calves
with seven-day death. Severe signs of dehydration,
diarrhea, dyspnea, anorexia, lethargy, stupor and coma
were also seen.
Based on the anamnesic data submitted by the practitioner
and changes observed during gross examination,
samples were obtained for diagnosis. According to that
criterion, bacterial cultures were requested in 97 (57.4%)
cases, viral isolation or identification was solicited in 90
(53.3%) cases, and histological studies were performed
on 121 (72.3%) cases.
Non-specific microscopic lesions possibly related to
an infectious cause were observed in several tissues.
Suppurative bronchopneumonia and/or enteritis were
seen. Large numbers of neutrophils and macrophages
were present in necrotic enteritis, fibrinous pericarditis,
and multifocal necrotizing hepatitis. Epithelial necrosis with
hemorrhagic lesions and cyst glands were also seen in
intestine. Leukocytes filled the airspace, and bronchi or
bronchioles were present in cases of pneumonia. Additionally,
suppurative meningitis was noted in cases with
septicemic form. Presence of leptospires on kidney
smears was associated with non-suppurative multifocal
nephritis. Frequency of histopathological lesions found
in several organs is shown in Figure 2.
Figure 2. Frequency of histopathological lesions according to
the affected organs.
Table 1 summarizes the diagnostic results. A specific cause of neonatal mortality was established in 70/169 (41.4%) cases; however, it was statistically lower than in undetermined cases 99/169 (58.6%) ( p < 0.05). This fact suggests limited diagnostic efficiency. Deaths caused by infectious agents were higher than those related to noninfectious agents 49/169 (29.0%)( p < 0.05). Although no statistical differences were found between the proportions of undetermined cases with and without histopathological lesions ( p < 0.05), 44/99 (44.4%) of those cases had microscopic findings suggestive of an infectious disease.
Table 1. Diagnostic of neonatal mortality in 169 calves.
No significant differences were observed when proportions
of determined and undetermined causes in beef
and dairy calves were considered ( p > 0.05). Similarly, no
significant differences were observed in the proportions
of determined and undetermined causes on days when
neonatal mortality was recorded ( p > 0.05).
Most common isolated agents were E. coli following
by Brucella abortus, Arcanobacterium pyogenes and Salmonella spp . ( Table 1). In all septicemic cases due to E.
coli, bacteria were isolated from several tissues. Similarly,
septicemic forms caused by other bacteria isolated
from multiple tissues included Nocardia spp. (lungs and
liver), Pseudomonas aeruginosa (spleen, lymph node and
gall), Salmonella spp. (intestine, spleen, mesenteric lymph
node, gall bladder and synovia), and Streptococcus spp. (synovia). Dual or multiple infections due to several agents
were recorded in 6 cases (Table 1). In addition, miscellaneous
agents were frequently isolated in omphalophlebitis
cases. BVDV was isolated in 2 (1.2%) cases and bovine
rotavirus was identified in 5 (2.9%) cases, 2 of which
E. coli.
Congenital abnormalities were the most common noninfectious
etiology. These included spastic syndrome and
paresis (1 case), cerebellar hypoplasia (2 cases), palatoschisis
(2 cases), palatoschisis associated with hydranencephaly
(1 case), hydrocephalus (2 cases), heart septal
defects (2 cases), segmental aplasia of intestine (1
case) and hypoplasia of kidney (1 case).
DISCUSSION
Data of this study revealed that beef calves had died
earlier than dairy calves. Although beef calves remain with
their dams after birth and dairy calves are fed with milk or
lacteal substitutes and concentrate nutriments, (11, 15)
differences in mortality age could possibly be attributed
to the differences in the management practices employed
by beef and dairy farms in Argentina (i.e. human care to
dairy calves prolonging their days of life). Similarly, in
another study performed on beef calves, 75% of 178
calves died by day 2 postpartum (8). Different diseases
or syndromes could be acting according to the type of
production system. For instance, in the present work, B.
abortus and congenital abnormalities (18 cases in total,
Table 1) were only detected in beef calves. These
etiologies caused death on the first days after birth. Nevertheless,
although a higher number of dead calves were
submitted during days 1 to 4, proportions of calves with
determined and undetermined causes on days 1 to 4 compared
with those on days 5 to 7, had similar distribution.
The high number of male beef calves (usually heavier
and larger than females) submitted for diagnosis could
be speculatively explained by dystocia problems as mentioned
before (22). However, no gross lesions related to
dystocia (edema in head, neck, tongue or forelimbs) were
observed in the present work.
Data obtained in this study, where diagnoses on 70
(29%) cases corresponded to infectious agents, contrast
with those reported by other authors (1). They considered
that the death of 78% of 47 calves had been due to
infections. However, the same authors attributed death
by infectious disease to those specimens with histopathological
changes compatible with presence of infectious
agent but without isolation (1). Had calves with microscopic
inflammatory lesions been considered in this work,
our percentage of dead calves due to infectious causes
would have reached 67.5% (Table 1). In the present study,
histopathological examinations of tissues from undetermined
cases showed that 26% of them had lesions which
suggested an infectious origin. Using conventional methods,
the final diagnosis rate in natural cases of bovine
neonatal mortality is usually low (12, 18). The low sensitivity
of all diagnostic tests used in this work plus a brief
clinical history and, probably the most important, an extensive
calf autolysis, could explain the poor final diagnosis
rate. Moreover, the time between the moment of calf death
and sampling is usually too long, which has a negative
effect on the identification of the microorganisms involved.
Another explanation for this high number of undetermined
causes is that samples were not systematically taken from
all specimens. This is due to several facts, namely, private
practitioners usually demand specific tests, the farmer's
interest in reducing the cost of the analysis or the previous
diagnosis of a specific disease in the herd. This sampling
methodology should be modified in future works.
As stated in other studies, our data also indicates that
neonatal mortality due to bacteria was the most prevalent
among the infectious agents (1, 2). Bacterial organisms
associated with environmental, nutritional factors or
poor husbandry can be causes of neonatal mortality (4,
5). Moreover, dystocia, stillbirth and hypothermia could
increase the calf's susceptibility to infection by a wide variety
of organisms during the first week of life (19, 41).
Since multiple infections due to several bacteria, alone
or associated with viruses, were recorded, any or all of
these factors could have contributed to calf mortality in
this study. Unfortunately, colostrum intake information was
not recorded in this work.
E. coli produces enterotoxic and septicemic colibacillosis
in young calves (27). In this study, septicemia was the
most prevalent form and histopathological lesions were
compatible with previous reports (1, 36). Although characterization
of E. coli strains was not attempted, the high
frequency of mortality and the presence of severe suppurative
microscopic lesions in multiple tissues suggest high
virulence in these isolated organisms. Although differences
in management practices are employed in beef and
dairy herds in Argentina (11, 15), this bacterium similarly
affects calves from both types of herds. (data not shown).
To date, bovine brucellosis remains present in Argentina,
and the disease is more frequent in beef herds (14).
In the present study, B. abortus isolations were only obtained
from beef newborn calves (data not shown), and
could have been the result of congenital infection or infected
colostrum intake. Unfortunately, this aspect was
not clarified in this study.
The isolation of Salmonella spp. in this work suggests
a role of this bacterium as etiological agent of bovine
neonatal mortality; however, its frequency is generally low
(7). This agent has been involved in bovine neonatal
mortality and its high prevalence has been reported in
other work (23). The fact that S. newport and S. enterica
were isolated from gall bladder, spleen, intestine and feces
(data not shown) in cases with presence of histopathological
lesions in several tissues demonstrates the high
virulence of this species (23).
Leptospirosis is usually associated with abortions, but
premature weak and full-term calves may also be produced
(29,39). In the present study, leptospires were only
evidenced by DFAT in 1 case where non-suppurative
multifocal nephritis, interstitial pneumonia and thyroiditis
were also seen. Neonatal mortality associated with Leptospira infection may most frequently occur in the Humid
Pampa; however, not only is isolation of Leptospira spp.
difficult but also available diagnostic techniques have low
(29).
C. perfringens type C enterotoxemia produce severe
acute hemorrhagic enteritis in 1 to 10 day-calves (40). Unfortunately, this agent was not screened in this work.
Opportunistic bacteria can produce septicemia and
neonatal mortality in calves (37, 38). In the present study,
Actinomyces spp., Klebsiella spp., Streptococcus spp .,
Nocardia spp ., Pseudomonas spp. and other miscellaneous
bacteria were involved in neonatal mortality. Despite
the fact that Staphylococcus dysgalactiae and Moraxella
nonliquefaciens have not been commonly reported to be
the cause of calf death, they were always isolated in pure
culture and associated with the presence of histopathological
lesions (Table 1). Factors such as strain virulence
associated with poor hygiene and insufficient colostrum
intake had probably provided the opportunity for these
bacteria to reach several tissues by hematogenous route
from the point of infection (6). Unfortunately, these factors
were not established in the present work. It could be
probable that the histopathological lesions found had been
caused by other agent and the isolated bacteria had been
contaminants.
One of the major causes of neonatal calf mortality and
morbidity is diarrhea (8, 27). Although the causes of this
syndrome could have both infectious or non-infectious
origin (10), the presentation of diarrhea in the present
work (data not shown) was only associated with infectious
agents (diarrheagenic and septicemic forms of E.
coli infection, rotavirus, Salmonella and BVDV infections
(Table 1).
BVDV has high prevalence in Argentinean bovine
herds (32). However, neonatal mortality due to BVDV was
low (2 cases) in line with the results reported by others
(1). Viral isolation is difficult due to poor viability of BVDV
in autolyzed specimens submitted for diagnosis (30). Unfortunately,
the origin of infection with DVBV in these 2
cases could not be clarified in the present study. However,
infections causing death in calves are commonly
associated with congenital transmission rather than with
postnatal exposure (30).
Rotavirus is a common viral agent identified as the
cause of neonatal diarrhea in Argentinean calves (31).
However, studies indicate that mortality due to infection
with rotavirus alone is very low (9), which is coincident
with our records. Generally, rotavirus and bacteria act in
synergic form in cases of enteritis (21) as was found out
in this work (Table 1).
Other agents such as BHV and Cryptosporidium
parvum involved in neonatal bovine morbidity and mortality
(1, 12, 27) were not identified in the present work.
Nevertheless, both agents have been previously recorded
in this area (32, unpublished data).
In this work, congenital defects were found in non-viable
calves. Environmental, genetic factors, teratogenic
plants and infectious agents can be causes of abnormalities
during bovine gestation (28). Usually, the origin of
these congenital abnormalities is difficult to determine
(33). However, in this study some lesions (cerebellar hypoplasia,
palatoschisis, hydranencephaly) were suggestive
of BVDV infection. Antecedents of Conium maculatum
ingestion were recorded in 2 cases where congenital defects
(palatoschisis) were seen (data not shown).
The data given in this report provide useful information
to beef and dairy producers and veterinarians. Many
calf deaths could be prevented if producers and veterinarians
were more aware of the cause of calf mortality
and their relative importance.
Although standard culture and histopathological techniques
were successfully used for identifying some pathogens,
the protocols and methodology should be improved
in order to characterize the causes of bovine neonatal
mortality. A higher etiological diagnosis could be achieved
by the implementation of appropriate and modern techniques
such as molecular tests. Such improvement in the
diagnosis could help to establish strategic vaccination,
adequate husbandry methods, management and biosafety.
Acknowledgements: We thank technicians at Animal Health Group, INTA Balcarce and resident veterinarians for technical support. We are also grateful to participating farmers and bovine practitioners for submitting specimens for diagnosis. Part of this work and the fellowship for Eleonora Morrell were granted by INTA and Agencia Nacional de Promoción Científica y Tecnológica, PICT 08-11139, Argentina.
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Recibido: 23/10/07
Aceptado: 26/05/08