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Coxiella burnetii associated reproductive disorders in small ruminants

Lucienne Downs, Central Tablelands Local Land Services, Orange

This paper was presented at the 2017 Australian Veterinary Association Conference, Melbourne
Posted Flock & Herd August 2018

Summary

Coxiella burnetii has been found in the foetal fluids, vaginal mucous, semen, milk, urine and faeces of many domestic and wild animals (Maurin & Raoult, 1999; Arricau-Bouvery & Radolakis, 2005, Van der Brom, 2015). C. burnetii may be detected during normal parturition or in association with abortion events, making determination of the abortifacient potential of this organism complicated. A review by Algerholm in 2013 found that there was solid evidence for the association between C. burnetii and sporadic cases of abortion, premature delivery, the birth of weak offspring and stillbirth (APWS complex) in cattle, sheep and goats. Coxiellosis remains an infrequent diagnosis in domestic ruminants. Diagnosis of C. burnetii associated abortion events should be supported by demonstrating appropriate pathology in addition to finding the organism or the animal’s exposure to the organism. Investigation of other causes of abortion should be undertaken. 

Introduction

C. burnetii is the causal agent of Query (Q) fever, a zoonosis that occurs worldwide except for New Zealand. It is a Gram-negative, obligate intracellular bacterium that is capable of long-term environmental persistence (Maurin & Raoult, 1999, Arricau-Bouvery & Rodalakis, 2005). The organism survives well in air, soil, water and dust and may be disseminated on fomites such as wool, hides, clothes, straw and packing material but is inactivated at pasteurisation temperatures. 

Domestic ruminants are considered the primary animal reservoir of C. burnetii but a wide range of species including cats, dogs, rabbits, alpacas, birds and arthropods can be infected (Van der Brom, 2015).  Kangaroos (Benazis et al, 2010) and Bandicoots (Derrick & Smith, 1940) have been identified as reservoirs of C. burnetii in Australia. There is clear epidemiological and experimental evidence that the infection is principally transmitted by inhalation of desiccated aerosolised particles and through contact with infected animals, their reproductive tissues or other animal products, like wool (Arricau-Bouvary & Rodolakis, 2005, Maurin & Raoult, 1999). 

In Australia, the notification of Q fever cases in humans is mandatory, the identification of the source and route of infection by C. burnetii and its importance in public health is evaluated by epidemiological investigation. Demonstration of C. burnetii exposure by serological methods, shedding using PCR and genotyping from in-contact animals implicated in the epidemiological assessment is not routinely performed except in large outbreaks or in a research context. 

In humans the disease can manifest as an acute, chronic or subclinical form (Maurin & Raoult, 1999). Diagnosis is often delayed due to the non-specific manifestations of the disease and thus the disease is underreported. The chronic form may be complicated by endocarditis (especially in case of preexisting valvulopathies), vascular infections, hepatitis or chronic fatigue syndrome. The acute form usually resolves with appropriate antibiotic treatment but may still require hospitalisation. Prolonged antibiotic therapy may be required in the chronic condition and even so it may be fatal. C. burnetii infection in pregnant women may provoke placentitis resulting in obstetrical complications and fetal death.

Due to the non-specific symptoms and sometimes transient nature of the symptoms, Q fever is underdiagnosed and therefore underreported. Despite this, Q fever is the most frequently reported zoonotic disease in Australia with 469 cases (2.0 per 100,000) of 651 zoonotic diseases reported from October 2013 - October 2014 (National Communicable Diseases Surveillance Report October 2014). This was a 26% increase compared with the 5-year mean (2009 to 2013) (n=373). According to the NSW Zoonoses Annual Report, there were 262 confirmed cases of Q fever notified in 2015. www.health.nsw.gov.au report

Q Fever continues to be one of the major concerns of workers within meat and livestock industries. It has been claimed that Q Fever costs the Australian meat industry around $1M annually due to WorkCover claims. The Australian Government funded the National Q Fever Management Program (NQFMP) between 2001 and 2006 for states and territories to provide free vaccine to at-risk occupational groups (such as abattoir workers). Prior to the commencement of vaccination programs in Australia, approximately half of all cases were among abattoir workers. Between 1991 and 2001, and prior to the introduction of the NQFMP, Q fever notification rates ranged between 2.5 and 4.9 cases per 100,000. In Australia the notification rate is approaching these levels once again. People working in the agricultural sector are now more likely to be diagnosed. They comprised 29% of notifications in 1999-2000. This increased to 52% in 2001-2010.

In a recently published paper, the majority of Q fever patients in NSW who completed a survey reported animal contact (89%). Of those 63% were with cattle, 11% with sheep, and 7% with kangaroos (Graves and Islam, 2016). These rates vary in different countries. The differences observed may be due to agricultural practices (intervention during parturition, proximity of animals, housed indoors or extensively managed, the biosecurity and hygiene practices adopted  and other husbandry practices), genotypic variability regionally or between species, number of a particular species kept, environmental and climactic conditions and other factors not yet determined. Georgiev et al, 2015 found that proximity to farm animals and contact with infected animals or their birth products have been identified as the most important risk factors for human disease in the four European countries they studied.

One of the largest outbreaks of Q fever associated with intensive dairy goat farming occurred between 2007 and 2010 in The Netherlands in which a total of 4,026 human cases were notified however it is likely that up to 44,000 individuals were infected (Van der Brom et al, 2015). In 2012-13, an outbreak of Q fever associated with a dairy goat farm occurred in Victoria, Australia in which 18 cases were reported (Bond, 2014).   

Guatteo et al, 2011 in a critical review of papers focused on C. burnetii prevalence in sheep, goats and cattle.  Major methodological issues were detected in many of the papers and the authors concluded there was a persistent need to conduct well-designed studies, aiming at estimating the true prevalence of C. burnetii infection in the three main domestic ruminant species. Prevalence of C. burnetii varied considerably worldwide, between regions and between species. Animal and herd level seroprevalence, regardless the species, were between 15–20% in many countries. In countries where the reported prevalence was lower, the information collected was considered insufficient to be considered reliable. The apparent prevalence of C. burnetii was higher in cattle (20.0% and 37.7% of mean apparent prevalence at animal and herd level respectively) than in small ruminants (around 15.0% and 25% respectively for animal and herd level in sheep and goats).

Published studies on prevalence of C. burnetii in sheep and goats in Australia are few, and additionally, many are older studies that utilised methodologies such as complement fixation testing (CFT). A 1981 study in feral goats at abattoirs in South Australia described a prevalence of 51.5% (method not specified) (McKenzie et al, 1979) and another study published in 1979 found two out of 20 feral goats (10%) were serologically positive on CFT (Hein and Cargill, 1971).  There are fewer studies of prevalence of C. burnetii in Australian sheep however one study of sheep (n=50) and beef cattle (n=329) in Western Australia found antibodies against C. burnetii with a commercially available ELISA in 2/379 (0.5%) of animals tested and 41/379 (~11%) animals were positive on faecal PCR (Benazis et al, 2009), none of the ELISA positives were sheep.

C. burnetii infection in the uterus can cause a spectrum of disorders including abortion, delivery of premature offspring, stillbirth and weak offspring (APSW complex) in addition to the birth or normal offspring that may be congenitally infected. The outcome of an infection depends on a number of factors including strain virulence, infective dose, immune response of dam and foetus, severity of the resulting lesions, gestational age, number of foetuses (Algerholm, 2013). Placentitis in goats attributed to C. burnetii results in a yellow, leathery thickening of the intercotyledonary chorioallantois with a surface exudate. Gross foetal lesions are non-specific. On microscopic examination the placental lesions are an acute inflammatory infiltration primarily affecting the intercotyledonary area. Coxiella organisms fill the hypertrophic trophoblasts. Foetal lesions may be present and may include peribronchiolar, renal medullary and hepatic portal lymphoid accumulations (McGarvin and Zachary, 2007). 

In the past the detection of infected animals has been difficult due to the lack of safe, relatively inexpensive, sensitive and specific laboratory tests. Enzyme linked immunosorbent assay (ELISA) is now commercially available and readily accessible. Indirect immunofluorescence assays are validated for some domestic species but are not currently commercially available. Polymerase chain reaction PCR assays for animals may be available through Universities or human laboratories but are not offered as standard tests through veterinary laboratories.  Culturing demands biosafety level 3 facilities and is difficult due to the inabiltity of the organism to grow on agar plates requiring to be grown intracellularly or in eggs. Immunohistochemistry can be performed on fixed tissue. Molecular studies have shown that different C. burnetii strains exist and that such strains may be more likely to be associated with different hosts. Investigation into strain variance between host species and regionally has not been undertaken in Australia to date. 

In association with pathological and epidemiological investigations PCR-based methods and genotyping should be applied in routine diagnostic investigations of abortion events and research, to clarify the role of C. burnetii and genotypic variation in reproductive disorders of livestock.

In this presentation, preliminary results of a collaborative study undertaken by the LLS, University of Sydney and NSW DPI to investigate the seroprevalence of previous exposure to Coxiella burnetii in goats in the Central Tablelands of NSW will be shown.

References

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