Laboratory diagnosis of ruminant abortion in Europe

doi:10.1016/j.tvjl.2014.03.015

The Veterinary Journal

Volume 200, Issue 2, May 2014, Pages 218-229

https://doi.org/10.1016/j.tvjl.2014.03.015 Get rights and content

Abstract

Abortion in ruminants is a major cause of economic loss worldwide, and the management and control of outbreaks is important in limiting their spread, and in preventing zoonotic infections. Given that rapid and accurate laboratory diagnosis is central to controlling abortion outbreaks, the submission of tissue samples to laboratories offering the most appropriate tests is essential. Direct antigen and/or DNA detection methods are the currently preferred methods of reaching an aetiological diagnosis, and ideally these results are confirmed by the demonstration of corresponding macroscopic and/or histopathological lesions in the fetus and/or the placenta. However, the costs of laboratory examinations may be considerable and, even under optimal conditions, the percentage of aetiological diagnoses reached can be relatively low. This review focuses on the most commonly occurring and important abortifacient pathogens of ruminant species in Europe highlighting their epizootic and zoonotic potential. The performance characteristics of the various diagnostic methods used, including their specific advantages and limitations, are discussed.

Introduction

An increase in the number of spontaneous abortions in a herd or flock is a dramatic event for the farmer involved, and a range of epizootic and/or zoonotic diseases, or even emerging diseases, may be the cause. Farmers, their veterinary practitioners and, where appropriate, State veterinarians require rapid and reliable results from diagnostic veterinary laboratories, a process that is not always easily achieved. While a plethora of pathogens can cause abortion in ruminants, there is no single diagnostic procedure that can be used to identify these, and in some circumstances the infectious event triggering an abortion may precede it by some weeks or even months and evidence of the presence of the pathogen may have become obliterated by autolysis. By this time it may no longer be possible to demonstrate a rise in maternal antibody indicative of recent infection. Since attempting to rule out all the possible causes of abortion can prove costly, diagnostic laboratories primarily focus on the most likely aetiologies and those with zoonotic potential.

This review assesses the most important viral, bacterial, fungal and protozoal causes of abortion in cattle, sheep and goats in Switzerland, focusing on the methods used to reach a diagnosis and highlighting protocols that optimise pathogen detection. The information presented will be of interest to laboratory diagnosticians, as well as veterinary practitioners and State veterinarians. An overview of the infectious abortifacients discussed is given in Table 1.

Section snippets

Bovine herpesvirus type I

Bovine herpesvirus 1 (BoHV-1) infections remain a major cause of abortion, venereal and respiratory disease in ruminants in countries where the pathogen has not been eradicated (Kirkbride, 1992). Latency with recurrent infection is typical of infection with these viruses: during latency the virus survives within cells without causing clinical signs, and upon reactivation, repeated abortion may occur (Nandi et al., 2009). Given that virus is shed during reactivation, an infected animal remains a

Brucella spp

Brucellosis causes significant losses due to abortion and infertility in ruminants, but is also zoonotic resulting in persistent or ‘undulant’ fever with influenza-like symptoms and can be fatal when endocarditis and encephalitis ensues (OIE, 2012). The genus Brucella contains highly infectious species that infect a wide variety of mammals. Brucella spp. are small, non-motile gram-negative rods, and infection in humans arises from direct or indirect contact with infected animals or through the

Neospora caninum

Neospora caninum is one of the most important causes of infectious abortion in dairy cattle in industrialised countries, with a prevalence rate of up to 40% (Dubey and Schares, 2011). Abortions due to N. caninum have also been reported for small ruminants (Hässig et al., 2003). This protozoan parasite is taxonomically located within the family Toxoplasmatidae and the order Eimeriina. It is closely related to Toxoplasma gondii, and dogs, wolves, coyotes and dingoes have been identified as final

Aspergillus spp

Mycotic abortions in ruminants are usually sporadic events. Knudtson and Kirkbride (1992) evaluated the results of the laboratory diagnoses of 6858 cases of bovine abortion and stillbirth in the northern plains region of the USA: they identified fungi as the cause of abortion in 6.8% of cases with Aspergillus fumigatus most frequently incriminated (5%). This fungal species was also determined to be the most common mycotic cause of abortion in Denmark (Jensen et al., 1991) and Ireland (Sheridan

Discussion

The objective of this review article is to provide essential information about the most commonly occurring causes of ruminant abortion in Europe. Veterinary laboratory diagnosticians need to provide expert advice to veterinary practitioners and state veterinarians on the taking of the most appropriate samples in cases of ruminant abortion as well as on the interpretation of test results. Sourcing the relevant information can prove challenging as such material is often dispersed over a wide

Conclusions

The accurate diagnosis of abortion in ruminants (or indeed other species) needs to be based on obtaining a concise clinical history, careful gross and histopathological examination of any placental/fetal lesions, and the selection and submission to the laboratory of appropriate samples. The results of the tests carried out should be correlated back to the particular circumstances of the abortion problem in order to validate their plausibility. While such stepwise, methodical procedures may not

Conflict of interest statement

None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper.

Acknowledgement

The authors wish to thank Professor M.M. Wittenbrink of the Institute for Veterinary Bacteriology, Vetsuisse Faculty, at the University of Zurich for his helpful input und discussion.

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In the past decade, cases of Q fever have been reported in Brazil. Although the previous report of Coxiella burnetii in humans and animals, the knowledge about the occurrence of this pathogen in livestock in Brazil is scarce. This study aimed to search C. burnetii and possible coinfections in tissues of aborted bovine fetuses from Brazil. Tissue samples from seventy-six aborted bovine fetuses sent to the laboratory of molecular diagnosis of infectious diseases from 2013 to 2019 were evaluated by real-time PCR for C. burnetii. Overall, 9.2% (7/76) of the samples were positive for C. burnetii. Moreover, the molecular diagnostic history of our lab revealed the coinfection with Neospora spp. in three fetuses and the presence of histopathological features suggestive with fetal neosporosis in another one. The previous report of C. burnetii in humans and animals in the country, with the detection of C. burnetii from tissues of aborted bovine fetuses reported here, reinforces the neglected state of the disease in Brazil and raises the question of the role of the pathogen in reproductive disorders in national livestock.
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In Europe, it is considered the most frequent cause of abortion due to an infectious agent both in sheep and goats (Borel et al., 2014). OEA is characterized by the occurrence of abortion at the end of the gestation, weak or lifeless animals born at the end of the gestational time, with release of a large number of potentially infectious organisms (Borel et al., 2014). Placental membranes have great value for Chlamydia infection diagnose, however, vaginal swabs can also be collected at the time of abortion (Borel et al., 2014).
Sheep and goat farming are still a traditional practice in Portugal. These animals are produced for raw material production and consumption, such as wool and milk. Abortion occurrence is an economic issue for the producer and a health and food safety concern. Chlamydia abortus and Coxiella burnetii are amongst the infectious agents with greater abortive potential. Samples from animals that suffered abortion and suspected to be carriers of Chlamydia spp. or Coxiella burnetii were screened for the presence of these agents by the polymerase chain reaction (PCR) technique. The main objective was to assess coinfection occurrence in these samples, but also evaluate their presence individually. A total of 73 tissue samples from sheep (n = 29) and goats (n = 44) were collected between 2015 and the first trimester of 2020. There were detected 25 cases of Chlamydia spp. (34.2 %), 11 cases of Coxiella burnetii (15.1 %) and 12 cases of coinfection (16.4 %). At the best of our knowledge, this is the first Portuguese study regarding Coxiella and Chlamydia coinfection in ruminants. Our data revealed a relevant presence of coinfection in small ruminants in Portugal, drawing attention for the importance of taking into account both agents in abortion diagnostic. Further investigation is warranted in order to better support veterinary diagnostic practice.
Bacterial, protozoal and viral abortions in sheep and goats in South America: A review
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Abortion rates up to 5% are often considered normal (Edmondson et al., 2012). Bacterial, parasitic (protozoal), viral, nutritional, genetic, metabolic and toxic causes of abortion have been identified (Borel et al., 2014). Among them, bacterial, protozoal and viral diseases are the most frequently recognized causes of abortion in sheep and goats worldwide (Kirkbride, 1993; Moeller, 2001).
Bacterial, protozoal and viral diseases are major causes of abortion in sheep and goats. These agents cause significant economic losses, and many are considered of concern for public health (zoonotic pathogens) and/or the international trade of livestock, such as those causing diseases notifiable to the World Organization of Animal Health (OIE). In South America, information about their occurrence, prevalence and economic impact is scarce. We review the available literature on bacterial, protozoal and viral abortifacients identified through laboratory testing in sheep and goats in South America and discuss whether the diagnostic investigations are conclusive in demonstrating abortion causality. We also compile information on diagnostic methods recommended by the OIE for the laboratory diagnosis of these abortifacients and on salient fetoplacental lesions induced by them. Campylobacteriosis (Campylobacter fetus subsp. fetus), listeriosis (Listeria ivanovii), chlamydiosis (Chlamydia abortus), toxoplasmosis, neosporosis and sarcocystiosis have been confirmed as small ruminant abortifacients in this region. Brucella ovis, Brucella melitensis, Campylobacter jejuni, Chlamydia pecorum, Coxiella burnetii, Leptospira spp., Bacillus licheniformis and bluetongue virus, are probable causes of abortion in the region since they have been detected in aborted fetuses and/or associated with abortions through seroepidemiologic studies. Listeria monocytogenes, Histophilus ovis, Actinobacillus seminis, Trueperella pyogenes, Yersinia spp., Trypanosoma vivax, caprine herpesvirus 1 and pestiviruses also infect small ruminants in the region and could thus be considered possible causes of abortion, although they have not been associated with abortion in South America (i.e., not detected in aborted fetuses nor associated with abortion through seroepidemiologic studies). Other agents such as Flexispira rappini, Francisella tularensis, Anaplasma phagocytophilum, Rift Valley fever virus, Wesselbron disease virus and bunyaviruses, known to be abortifacients for sheep and goats in other regions of the world, have not been documented in South America. While some of these agents could be exotic in this subcontinent, others may have been undiagnosed considering the limitations of active animal disease surveillance systems, which hamper the eventual detection of emerging, re-emerging, and communicable diseases in South America.
Retrospective study of factors associated with bovine infectious abortion and perinatal mortality
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Thus, calculating the prevalence of APM caused by BVDv, based only on fetal BVDv antigen detection, may lead to an underestimation of the true prevalence. However, Borel et al. (2014) mentioned that the use of ELISA Ag tests on fetal tissue might result in false-positive results, perhaps because of the effect of autolysis. As the fetus is able to produce BVDv specific antibodies when an infection is acquired after 150–180 days of gestation (Hansen et al., 2010), demonstrating antibodies in fetal/calf fluids may confirm intrauterine infection (Lanyon et al., 2014b).
Abortion and perinatal mortality, leading causes of economic loss in cattle industry, are the consequence of both non-infectious and a wide range of infectious causes. However, the relative contribution of pathogens to bovine abortion and perinatal mortality is poorly documented, since available studies involved only a limited number of pathogens. Therefore, the objectives of the present monitoring study were to determine the prevalence of infectious agents associated with bovine abortion and perinatal mortality, and to identify differences in production type, gestation length, parity and seasonality by using mixed effect models (logistic regression). A pre-established sampling protocol based on the collection of the aborted fetus/calf and a corresponding maternal blood sample, involving diagnostic testing for 10 pathogens, was performed. At least one potential causal agent of the abortion or perinatal mortality was detected in 39 % of cases. In these diagnosed cases, Neospora caninum was the most detected pathogen, followed by Trueperella pyogenes, BVDv, Escherichia coli, and Aspergillus fumigatus. Neospora caninum [odds ratio (OR): 0.4; 95 % confidence interval (CI): 0.3–0.7] and Aspergillus fumigatus (OR: 0.1; 95 % CI: 0.1–0.3) were detected less in late versus early gestation. Aspergillus fumigatus was less common in dairy in comparison to beef abortion cases (OR: 0.2; 95 % CI: 0.1–0.6). Winter was associated with a lower positivity for Neospora caninum and BVDv in comparison to warmer seasons. Despite extensive diagnostic testing, an etiological diagnosis was not reached in 61 % of cases, highlighting the need for even more extensive (non-)infectious disease testing or more accurate tests.
Knowledge, attitude, and practices to zoonotic disease risks from livestock birth products among smallholder communities in Ethiopia
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Animal to human transmission mainly results from direct contact with infected materials such as uterine discharge, aborted foetus, and placenta infected while assisting with animal delivery and while caring for the new-born, or through dealing with abortion cases or exposure to a contaminated environment with abortion products [28,40]. Animal birth products from an infected dam carry a large number of these pathogens, which can be a source of infection for an entire household because of their close contact with livestock in unsanitary conditions [13,22]. There is increasing evidence that zoonotic causes of animal abortion are prevalent and widely spread in all livestock production systems in Ethiopia [17,19,20,25,54,56,57].
Many causes of abortion in livestock are due to zoonotic pathogens that pose serious infection risks for humans. Carefully designed, empirical One Health research allows to untangle the complexity around these risks and guides the development of practical health education guidelines and best prevention practices for veterinary public health interventions. To support this, the study presented here aimed at understanding knowledge, attitudes, and practices (KAP) on zoonotic risks from livestock birth products among rural communities in Ethiopia. From July 2018 to February 2019, a cross-sectional study design was conducted with 327 randomly selected farmers and pastoralists in five districts in three regions in Ethiopia. The structured questionnaire consisted of 48 items to evaluate knowledge (24), attitude (9), and prevention practices (15) related to zoonotic diseases risks from livestock birth products. A unidimensional two-parameter logistic (2-PL) Item Response Theory (IRT) model was used for zoonotic disease risk KAP scale construction and evaluation. The 2-PL IRT model was fitted to determine the probability of a person to appropriately respond to an item with a provided zoonotic disease KAP level. We then examined differential item functioning (DIF) concerning to five important covariates. The attitude subscale had the highest total mean score (37.3, ± 28.92%) and the knowledge subscale had the lowest mean score (22.4, ± 33.6%) among the three subscales. The mixed model regression analysis indicated that region was the only apparent factor explaining differences in zoonotic diseases knowledge, attitude, and practice total mean scores. The knowledge and attitude subscales had good internal consistency with a Cronbach's α at 0.83 and 0.81, respectively, whereas the practice subscale had lower internal consistency with 0.51. There was a positive association between responding to knowledge questions correctly and a positive attitude (r2 = 0.44, p < 0.0001) and self-reported good practice (r² = 0.307, p < 0.0001). The differential item functioning test showed that 19 of 37 (51.35%) and 12 of 37 (32.43%) items of the retained KAPs survey items had non-uniform and uniform DIF linked to at least one covariate respectively and all the covariates were related with DIF in at least one item. This study found substantial knowledge gaps, a low level of the desired attitude, and high-risk behavioural practices regarding zoonotic disease from livestock birth products. Consequently, livestock keepers are likely exposed to pathogens and thus these practices are an important contributing factor for zoonotic disease infection in people.
Improvement of Leptospira spp. diagnosis in aborted bovine fetuses by qPCR
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Leptospirosis is a disease with major economic impact on livestock industry. The objective of this work was to determine the presence of Leptospira spp. DNA by qPCR in bovine fetuses with presumptive diagnosis of leptospirosis as the cause of abortion. Leptospira spp. DNA was detected by qPCR in 11 out of 34 fetuses. These specimens (10/11) had histopathological findings in hepatic and/or renal tissues compatible with leptospirosis. qPCR detection rate (32.4 %) was higher compared with direct immuno-fluorescence antibody test (DFAT) (11.8 %). The concordance coefficient between both techniques was 0.44. qPCR is a rapid and sensitive technique for the diagnosis of leptospirosis and improved the detection rate in fetal tissues compared with DFAT. Implementation of molecular techniques may increase the accurate detection of leptospirosis as a cause of bovine abortion allowing the application of rapid therapeutic and prophylactics measures in order to reduce the impact of this zoonotic disease.

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ReviewLaboratory diagnosis of ruminant abortion in Europe

Abstract

Introduction

Section snippets

Bovine herpesvirus type I

Brucella spp

Neospora caninum

Aspergillus spp

Discussion

Conclusions

Conflict of interest statement

Acknowledgement

Veterinary Microbiology

Vaccine

Veterinary Microbiology

Veterinary Parasitology

Veterinary Microbiology

Veterinary Microbiology

Research in Veterinary Science

Veterinary Microbiology

Molecular Cellular Probes

Clinical Microbiology Newsletter

Biologicals: Journal of the International Association of Biological Standardization

Veterinary Clinics of North America: Food Animal Practice

Journal of Comparative Pathology

The Veterinary Journal

International Journal of Parasitology

Veterinary Parasitology

Veterinary Parasitology

Veterinary Parasitology

Veterinary Parasitology

Antiviral Research

Veterinary Parasitology

Clinical Microbiology and Infection

Veterinary Clinics of North America: Food Animal Practice

Veterinary Parasitology

Veterinary Clinics of North America: Food Animal Practice

Vaccine

Journal of Comparative Pathology

Veterinary Journal

The Veterinary Journal

Preventive Veterinary Medicine

Animal Reproduction Science

Journal of Comparative Pathology

Veterinary Microbiology

British Veterinary Journal

Comparative Immunology, Microbiology and Infectious Diseases

Veterinary Microbiology

Preventive Veterinary Medicine

Chlamydial abortion

Is Q fever an emerging or re-emerging zoonosis?

Veterinary Research

Detection by PCR of Neospora caninum in fetal tissues from spontaneous bovine abortions

Journal of Clinical Microbiology

Emerging role of Chlamydia and Chlamydia-like organisms in adverse pregnancy outcomes

Current Opinion Infectious Diseases

Waddlia chondrophila: From bovine abortion to human miscarriage

Clinical Infectious Diseases

Coxiella burnetii infection is associated with placentitis in cases of bovine abortion

Journal of Veterinary Diagnostic Investigation

Detection of Tritrichomonas foetus by polymerase chain reaction in cultured isolates, cervicovaginal mucus, and formalin-fixed tissues from infected heifers and fetuses

Journal of Veterinary Diagnostic Investigation

Chlamydia-related abortions in cattle from Graubunden, Switzerland

Veterinary Pathology

Border Disease in einem Schafbetrieb

Schweizer Archiv für Tierheilkunde

Variation in Bluetongue virus real-time reverse transcription polymerase chain reaction assay results in blood samples of sheep, cattle, and alpaca

Journal of Veterinary Diagnostic Investigation

Pathogenesis and epidemiology of bovine virus diarrhoea virus infection of cattle

Annales de Recherches Vétérinaires

Genomic analysis of an attenuated Chlamydia abortus live vaccine strain reveals defects in central metabolism and surface proteins

Infection and Immunity

Review
Laboratory diagnosis of ruminant abortion in Europe