Redalyc.Nonsuppurative Myocarditis Associated with Bovine Viral

Red de Revistas Científicas de América Latina, el Caribe, España y Portugal
Sistema de Información Científica
Pinto, Ana Paula; Silva Santos, Bethania; Lilge Kawski de Sá Ribas, Nickolly; Barbieri Bacha, Flávia; Marques
Carvalho, Nilton; Driemeier, David; Bobbi Antoniassi, Nadia Aline; Amaral Lemos, Ricardo Antonio
Nonsuppurative Myocarditis Associated with Bovine Viral Diarrhea Virus Infection in Calves in the State of Mato
Grosso do Sul, Brazil
Acta Scientiae Veterinariae, vol. 41, núm. 1, enero-diciembre, 2013, pp. 1-7
Universidade Federal do Rio Grande do Sul
Porto Alegre, Brasil
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Acta Scientiae Veterinariae, 2013. 41: 1113.
RESEARCH ARTICLE
ISSN 1679-9216
Pub. 1113
Nonsuppurative Myocarditis Associated with Bovine Viral Diarrhea Virus Infection
in Calves in the State of Mato Grosso do Sul, Brazil
Ana Paula Pinto1, Bethania Silva Santos1, Nickolly Lilge Kawski de Sá Ribas1,
Flávia Barbieri Bacha1, Nilton Marques Carvalho1, David Driemeier2,
Nadia Aline Bobbi Antoniassi2 & Ricardo Antonio Amaral Lemos3
ABSTRACT
Background: Bovine viral diarrhea virus (BVDV) refers to a heterogeneous group of viruses belonging to the family
Flaviviridae and genus Pestivirus. This family of viruses is one of the main pathogens of cattle and causes significant economic losses to the cattle industry worldwide. BVDV is an enveloped virus with a diameter of 45 nm and single-stranded
RNA genome of 12.5 kb. BVDV infection has been associated with a number of clinical manifestations ranging from unapparent infection and mild signs to acute illness and death. In general, calves are more susceptible to BVDV infection, but
adult cattle can develop the clinical disease if they are infected with highly virulent virus strains. This study describes clinical,
anatomopathological and epidemiological findings of a BVDV outbreak in calves in the state of Mato Grosso do Sul, Brazil.
Materials, Methods & Results: The outbreak occurred in the town of Agua Clara in the state of Mato Grosso do Sul. Epidemiological and clinical data were collected by the farm manager during a visit to the property. The outbreak involved
two Nelore heifer calves that died between 30 and 40 days of age. One calf was taken to the Laboratory of Pathological
Anatomy (LAP) of the Faculty of Veterinary and Animal Husbandry, Federal University of Mato Grosso do Sul (FAMEZ/
UFMS). The calf was necropsied, and white streaks were seen on the heart, indicating congestive failure with swelling of
body cavities and congestive hepatopathy (nutmeg liver). Fragments of different organs and tissues were collected during
necropsy, fixed in 10% formalin for 48 h, embedded in paraffin, cut in 5 µm sections and stained with hematoxylin-eosin
(HE) or analyzed by immunohistochemistry (IHC) in the Veterinary Pathology sector of the Federal University of Rio
Grande do Sul (UFRGS). Histologically, the heart lesion was characterized by fibrous coagulative necrosis associated with
marked infiltrate (predominantly lymphocytic) and some macrophages. The diagnosis was confirmed by immunohistochemical agent identification in Peyer’s patches within the intestine.
Discussion: The diagnosis of congestive heart failure due to myocarditis caused by BVDV infection was confirmed by
the IHC technique. While in other countries, myocarditis caused by natural infection in cattle and experimental infection
in goats and sheep due to BVDV has been described, there have been no reports of this clinical and pathological manifestation of the disease in Brazil. The heart lesions observed in the outbreak should be differentiated from similar injuries
caused by certain plants and from Neospora caninum infection. In the present study, while the virus was identified by
immunohistochemistry only in Peyer’s patches, BVDV was considered to be the cause of the cardiac lesions by a process
of elimination and because there is no correlation between the amount of viral antigen and the location of histological lesions. Other studies have used the IHC technique to detect BVDV antigen in other tissues of cattle and observed that the
antigen is not uniformly distributed among the organs, suggesting that no specific organ of aborted fetuses can be chosen
for BVDV diagnosis. Immunohistochemistry was shown to be an efficient method for detecting the antigen in the Peyer’s
patches of infected calves. This is the first report of nonsuppurative myocarditis associated with BVDV causing perinatal
cattle death with agent identification in Mato Grosso do Sul. However, these data are insufficient to determine the importance of BVDV infection in terms of reproductive losses in this state because the methodological approaches used were
different from those adopted in earlier studies.
Keywords: bovine viral diarrhea virus, myocarditis, immunohistochemistry, diagnosis.
Received: 14 April 2012
Accepted: 2 October 2012
1
Published: 23 January 2013
Programa de Pós-graduação em Ciência Animal, Faculdade de Medicina Veterinária e Zootecnia (FAMEZ), Universidade Federal de Mato Grosso do Sul
(UFMS), Campo Grande, MS, Brazil. 2Setor de Patologia Veterinária, Faculdade de Veterinária, Universidade Federal do Rio Grande do Sul (UFRGS),
Porto Alegre, RS, Brazil. 3Departamento de Medicina Veterinária, FAMEZ, UFMS. CORRESPONDENCE: R.A.A. Lemos [[email protected] - Tel.:
+55 (67) 3345-3615]. Departamento de Medicina Veterinária, Faculdade de Medicina Veterinária e Zootecnia (FAMEZ), UFMS. Av. Senador Filinto
Müller n. 2443, Bairro Cidade Universitária. CEP 79070-900 Campo Grande, MS, Brazil.
1
A.P. Pinto, B.S. Santos, N.L.K.S. Ribas, et al. 2013. Nonsuppurative Myocarditis Associated with Bovine Viral Diarrhea Virus Infection
in Calves in the State of Mato Grosso do Sul, Brazil.
Acta Scientiae Veterinariae. 41: 1113.
INTRODUCTION
were collected during necropsy and fixed in 10% formalin for 48 h. Following routine procedures, the fragments
were embedded in paraffin and cut into five-micrometer
sections. These sections were stained with hematoxylineosin (HE) or analyzed by immunohistochemistry
(IHC) in the Veterinary Pathology sector of the Federal
University of Rio Grande do Sul (UFRGS).
IHC was performed using the commercial DAKO
1
kit according to the technique described by Haines et al.
[23]. The kit contains a secondary antibody and avidin
complex conjugated to peroxidase in addition to the commercial monoclonal anti-BVDV 15C5 antibody2, which
was diluted at 1:1500 in phosphate buffer solution.
Bovine viral diarrhea virus (BVDV) is an enveloped virus that can be classified into two biotypes,
cytopathic (CP) and non-cytopathic (NCP), depending on their effect in cell culture. Because of its high
antigenic variability, the virus can also be sub-divided
into two major antigenic groups: type 1 and type 2 [37].
The clinical manifestations of BVDV infection
include respiratory disease, acute or chronic gastrointestinal syndrome, hemorrhagic syndrome with thrombocytopenia, mucosal disease, skin diseases and immunodepression [10,16,19,22]. The infection of pregnant
females produces a series of reproductive failures such
as embryo resorption, abortion, mummification, fetal
malformations, stillbirth, and the birth of weak and
unviable calves [18]. Hypomyelination is less frequent
[33], but immunotolerant and persistently infected (PI)
calves are commonly born when the infection occurs
between 60 and 90 days of pregnancy [2]. Congenital
defects seen in fetuses include cerebellar hypoplasia,
microencephaly, hydrocephalus, hydranencephaly,
porencephaly, hypomyelination, osteochondrosis,
growth delay, optic neuritis, retinal degeneration, thymic hypoplasia, hypotrichosis, alopecia, osteosclerosis
microphthalmia, cataracts and overbite [7]. Necrotizing
inflammatory lesions in the fetal myocardium, lung
and eyelid, which are associated with abortion, may
also occur [34]. In sheep and goats, BVDV infection
also causes lymphocytic myocarditis associated with
disseminated multifocal necrosis [7,26].
The present study aimed to describe the
epidemiology, clinical signs, pathology and laboratory
diagnosis of an outbreak of BVDV with calf mortality
in Mato Grosso do Sul (MS), Brazil.
RESULTS
The outbreak involved two Nellore heifer
calves that died between 30 and 40 days of age. They
belonged to a herd of 4300 animals, including 900
calves divided into lots of 100 animals. The morbidity and mortality rates were 0.0005% and 100%, respectively. The cattle were vaccinated against FMD,
brucellosis, leptospirosis, blackleg and botulism.
Tetrapterys multiglandulosa or other plants responsible
for cardiomyopathies were not found on the premises.
According to the owner, no cattle had been introduced
on the property in the three years preceding the onset
of the outbreak.
The analyzed calf died 10 min after experiencing ataxia, falling and paddling. She had exhibited
good body condition. At necropsy, a reddish liquid
was found in the thoracic (100 mL) and abdominal
(200 mL) cavities and in the pericardial sac (20 mL).
In the heart, whitish streaks were diffusely distributed
throughout the myocardium (Figure 1). The omentum
was thickened, yellowish and gelatinous (edema).
The liver was enlarged, displaying rounded edges and
interspersed with dark and light areas (nutmeg liver).
The histological examination showed extensive
areas of coagulative necrosis of myocardial fibers associated with a marked, predominantly lymphocytic
infiltrate and incipient fibrosis around the Purkinje fibers
and blood vessels. Diffuse congestion was observed in
the liver, especially in the centrilobular area. Hepatocytes
adjacent to the centrilobular vein had pyknotic nuclei
and condensed eosinophilic cytoplasm (necrosis).
IHC was positive for BVDV in lymphoid follicles of the small intestine. The test was negative in
the fragments of the other tissues.
MATERIALS AND METHODS
Epidemiological and clinical data on the outbreak were collected. Information on the outbreak was
provided by the farm manager during a visit to the
property when the pasture was inspected to search for
cardiotoxic plants such as Tetrapterys multiglandulosa.
One affected calf was taken to the Laboratory of Pathological Anatomy (LAP) of the Faculty of Veterinary and
Animal Husbandry, Federal University of Mato Grosso
do Sul (FAMEZ/UFMS). The calf was necropsied, and
tissues were collected for laboratory diagnosis.
Fragments of different organs and tissues (brain,
tongue, lung, heart, liver, spleen, intestine and kidneys)
2
A.P. Pinto, B.S. Santos, N.L.K.S. Ribas, et al. 2013. Nonsuppurative Myocarditis Associated with Bovine Viral Diarrhea Virus Infection
in Calves in the State of Mato Grosso do Sul, Brazil.
Acta Scientiae Veterinariae. 41: 1113.
Figure 1. Spontaneous BVDV infection in calves. Staining reveals diffusely
distributed whitish streaks in the myocardium.
DISCUSSION
died a few hours after birth, showing no macroscopic
changes in the heart; however, histological lesions
showed lymphohistiocytic multifocal infiltrates with
scattered small areas of myocardial necrosis [7]. These
lesions differ from those found in this report, as the
necropsied calf was born healthy, died 40 days after
birth and presented with more severe macroscopic and
histological lesions. In previous reports of myocarditis
in cattle associated with BVDV infection, there have
been no descriptions of the detection of the antigen by
IHC in myocardial lesions. This fact may also explain
the lack of detection of the agent in the myocardium, as
the injury may have been caused several months before
death, allowing time for the subsequent clearing of the
agent. Moreover, the absence of correlation between the
amount of viral antigen and the location of histological
lesions has been described by other authors [29,39].
It is noteworthy that the antigen must be identified in sequential samples collected at intervals of 30
days for an animal to be confirmed PI [8]. It is also noteworthy that the histological findings of heart lesions
and the absence of proliferative vascular lesions, which,
in cattle, are presumably attributed to persistent BVDV
infection, allow the differential diagnosis between
BVDV and systemic reactive angioendotheliomatosislike syndrome [6].
Myocarditis resulting from BVDV infection
should be differentiated from injuries to calves born
to cows that consumed non-lethal doses of the plant
Tetrapterys multiglandulosa during pregnancy [13].
These cases are characterized by abortions and the
development of weak calves that die soon after birth
or following physical exercise. Calves poisoned by
The diagnosis of BVDV infection in the outbreak was confirmed by detecting the agent in the small
intestine (Peyer’s patches). Clinical and pathological
findings are consistent with diagnosis of fetal BVDV
infection, in this case, resulting in chronic congestive
heart failure (CHF) due to myocarditis [25]. No other
symptoms described in lethal BVDV infections in
cattle [18,33] were observed in the affected calves.
Although cattle CHF associated with BVDV
infection has been described [25], detailed reports
on the epidemiology, clinical aspects and macroscopic and microscopic lesions caused by this form
of infection are not available. Lesions provoked by
myocarditis are described in detail for sheep and goat
fetuses experimentally infected with BVDV at different gestation stages (41 to 60 days) [7,26], but those
lesions were less severe than the ascites, hydrothorax,
hydropericardium, hydroperitoneum and nutmeg liver
observed in the calf of the present study. Although
it was not possible to determine whether the calves
were persistently infected (PI), the chronic nature of
the cardiac and hepatic lesions indicates that they had
been infected during intrauterine life.
A similar phenomenon occurs in poisoning by
Tetrapterys multiglandulosa in cattle, in which calves
born from cows that consumed the plant in early gestation are born apparently healthy but die in the first
weeks of life with chronic cardiac and hepatic lesions
[13]. In one study, BVDV antigen was detected by
IHC in the heart of three aborted or premature goat
fetuses with histological lesions and in a fetus without histological lesions [26]. These fetuses aborted or
3
A.P. Pinto, B.S. Santos, N.L.K.S. Ribas, et al. 2013. Nonsuppurative Myocarditis Associated with Bovine Viral Diarrhea Virus Infection
in Calves in the State of Mato Grosso do Sul, Brazil.
Acta Scientiae Veterinariae. 41: 1113.
T. multiglandulosa have macroscopical and histological
lesions similar to those observed in the present study;
however, lesions in poisoned calves are associated
with fibrosis, while BVDV-infected calves have lesions characterized by the predominance of infiltrates
of lymphocytes and macrophages. Another important
histological characteristic differentiating these diseases is the lack of spongy lesions formed by dilation of periaxonal spaces or axonal swelling (status
spongiosus) in brain white matter in infected animals.
This deformation is described in natural poisoning by
T. multiglandulosa in cattle and in experimental poisoning in cattle and sheep [12,13].
In areas where Tetrapterys multiglandulosa
does not grow, BVDV infections associated with heart
lesions should be differentiated from poisoning by
other plants, such as Ateleia glazioviana, that cause
similar injuries [1,20]. Heart lesions and sudden death
can also occur in calves infected with foot and mouth
disease virus (FMDV); however, this is a rare form
of infection that occurs primarily in outbreaks [28].
Moreover, the herd that was studied was vaccinated,
and no viral activity had been reported in the study area.
Differential diagnosis may consider other
causes of heart lesions in cattle, such as poisoning
by ionophore antibiotics or vitamin E and selenium
deficiency [3]. These diseases, however, have not been
described in calves several days old, and the symptoms
of these diseases include muscular lesions that were not
detected in the calves of the present study. Furthermore,
the cattle studied had not received ionophores.
Sudden death in cattle following exercise is
not rare in Mato Grosso do Sul because the animals
commonly consume Mascagnia pubiflora [35]. However, death usually does not occur in 30- to 40-day-old
cattle, and macroscopic or histological lesions in the
myocardium are not typically seen. Intoxication with
this plant causes histological lesions such as vacuolar
interface dermatitis of the distal convoluted kidney
tubules [42].
Differential diagnoses may also include Neospora caninum infection, which causes nonsuppurative
myocarditis, necrosis of certain areas and extensive
polymorphonuclear infiltrates in the subendocardial
region and around the Purkinje fibers [14]. In addition
to heart infection, N. caninum can also damage the
nervous system, causing multiple areas of necrosis in
both white and gray matter, with or without bleeding
and with mononuclear cell infiltrate. N. caninum also
causes vacuolization in areas surrounding brain lesions, the presence of eosinophilic spheroids, diffuse
gliosis, hypertrophy of the vascular endothelium, the
occurrence of perivascular cuffs in mononuclear cells
and small areas of mineralization [38]. Neither these
lesions nor the presence of intracellular tachyzoites
was observed in the case reported.
Viral antigen identification using IHC in
Peyer’s patches proved to be a sensitive and specific
tool for BVDV detection in cattle. These data confirm previous observations reported in the literature
[9,15,21,24]. Given that the antigen was found only in
Peyer’s patches, fragments of different organs must be
subjected to IHC tests in cases of suspected fetal infection with BVDV. Other studies used the IHC technique
to detect BVDV antigen in cattle brain, liver, lung,
placenta, spleen, thymus, adrenal glands [4], heart, intestine, kidney, lymphoid tissue, skin [41], esophagus,
omasum, thyroid and pancreas [40]. These studies also
observed that the antigen is not uniformly distributed
among the organs, suggesting that a specific organ of
aborted fetuses cannot be chosen for BVDV diagnosis.
On the other hand, in a study on the distribution and
quantification of IHC markings in different organs of
5 cows persistently infected with BVDV, viral antigens
were detected mainly in epidermal keratinocytes, epithelial hair follicles, dermal mononuclear cells of the
ears and skin, histiocytes and lymphocytes in the lymph
nodes, thyroid follicular cells, neuron cytoplasm and,
to a lesser extent, in microglial cells of the cerebral
cortex and hippocampus [39].
The marking of hair follicles, dendritic cells
and epidermal keratinocytes from ear skin fragments
are characteristic of PI animals [9,31,39,40]. Moreover,
in cattle with transient infection, the antigen is limited
to the epidermis and infundibulum of hair follicles.
However, IHC performed on ear skin fragments of
two PI calves confirmed by virus isolation was found
to be negative [16]. Although more laborious than the
sandwich ELISA, the IHC test has the advantage of
detecting the BVDV antigen in young cattle without interference from maternal antibodies [9,22]. Thus, skin
fragments must also be collected in cases of perinatal
and neonatal death.
Although cases of BVDV infection are well
documented in Brazil [5,11,17,27,30,32,36], few
reports have discussed the economic losses caused
4
A.P. Pinto, B.S. Santos, N.L.K.S. Ribas, et al. 2013. Nonsuppurative Myocarditis Associated with Bovine Viral Diarrhea Virus Infection
in Calves in the State of Mato Grosso do Sul, Brazil.
Acta Scientiae Veterinariae. 41: 1113.
by this infection [16,19], especially in terms of reproductive failure and mortality in neonatal and perinatal
periods. A study conducted in Rio Grande do Sul
found that only 3 (1.12%) of 161 fetuses examined
using the IHC technique were positive for BVDV
[40], while another investigation showed that this
virus accounts for 2 to 7% of cattle miscarriages in
other countries [34].
to systematically collect and analyze samples of all
tissues from suspected BVDV cases, especially using
IHC tests. Since the antigen is not distributed uniformly, evaluating all tissues increases the likelihood
of BVDV detection.
SOURCES AND MANUFACTURERS
1
DAKO kit - LSAB 2 kit, DAKO Corp., Carpinteria, CA. USA.
2
Antibody - primary monoclonal antibody 15C5 (Syracuse Bioanalyti-
cal), Syracuse, NY, USA.
CONCLUSIONS
Acknowledgements. To the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ, Process 480671/20095) and Fundação de Apoio ao Desenvolvimento do Ensino,
Ciência e Tecnologia do Estado de Mato Grosso do Sul (Fundect, Process 23/200.226/2010) for awarding a fellowship to
A.P. Pinto.
This is the first report of nonsuppurative myocarditis associated with BVDV causing perinatal cattle
death with agent identification in Mato Grosso do Sul.
However, these data are insufficient to determine the
importance of BVDV infection in terms of reproductive losses in this state because the methodological
approaches used were different from those adopted in
earlier studies. For diagnostic purposes, it is essential
Declaration of interest. The authors report no conflicts of
interest. The authors alone are responsible for the content and
writing of the paper.
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