CASE NOTES


An investigation into the serological evidence of Coxiella burnetii infection in beef cattle in the Lachlan Livestock Health and Pest Authority in NSW

Nik Cronin, District Veterinarian Central West Local Land Services, Forbes

Posted Flock & Herd September 2015

INTRODUCTION

Q fever is an important zoonotic infectious disease in Australia.  It is caused by the organism Coxiella burnetii and is more frequently diagnosed in humans than some of the more commonly known zoonotic diseases.  In Australia in 2013 there were 487 human notifications of Q fever compared to 88 notifications of leptospirosis reported by the National Notifiable Diseases Surveillance System.  

Although approximately 60% of human infections are asymptomatic, in the remaining 40% there can be serious acute and chronic disease with potentially significant and prolonged effects on health and well being.  The classic presentation of acute disease is a severe influenza-like illness lasting from 2-6 weeks, often with significant weight loss (Marmion B. 2009).  Hepatic involvement is common and there may also be pneumonitis and neurological signs.  Chronic manifestations include the post-infection Q fever Fatigue Syndrome (QFS), endocarditis and other ongoing/recrudescent granulomatous infections.  QFS is the most common chronic complication and affects 10-15% of acutely affected patients and frequently for more than 5-10 years (Marmion B. 2009).  

Both wildlife and domestic reservoirs of C. burnetii exist, although traditionally cattle, sheep and goats are thought to be the most significant sources of human disease (NCIRS. 2010).  C. burnetii is shed in the urine, milk, faeces and birth products of infected animals and is transmitted from animals to humans most commonly by inhalation of contaminated aerosols (NCIRS. 2010).  The organism is particularly concentrated in birth products – it is said that 1 gram of uterine tissue may contain as many as one billion C. burnetii organisms (Australian Q Fever Register. 2015).  Inhalation of aerosols generated during parturition or during the slaughtering process is the most common route of infection (Marmion B. 2009).  This poses a significant occupational risk to people working in the livestock and meat processing industries.  

Preventative vaccination is currently the most effective tool available to protect people who are at an increased risk of exposure to C. burnetii.  Q-Vax® (CSL) is an efficacious vaccine using a purified, formalin-inactivated suspension of C. burnetii which has been commercially available in Australia since 1989.  Early vaccine uptake was initially poor until CSL helped establish vaccination programs in a number of larger abattoirs in 1994 (Hendry S. 2012).  This likely influenced the fall in the number of notifications from approaching 900 (868) in 1993 to below 500 (449) cases in 1995 (NNDSS. 2015).  Then from 2001-2006 the Federal Government established the National Q Fever Management Program (NQFMP) which provided free vaccination to people in high risk occupations.  Phase I initially targeted abattoir workers, contractors and sheep shearers and Phase II expanded to involve sheep, dairy and beef cattle farmers, employees and unpaid family members working on farms (NCIRS. 2010).  Uptake in the meat industry was strong –the industry is now seen as ‘engaged’ in Q fever prevention with vaccination programs being continued beyond the national program (Hendry S. 2012).  This has seen a reduction in meat industry representation in Q fever statistics with notifications in meat industry workers falling from 51% in 1991-2000, to only 10% between 2001 and 2010 (Lowbridge CP, Tobin S, Seale H et al. 2012).  This is in direct contrast to the very broad agricultural industries which had a much lower uptake during the NQFMP and currently do not have a vaccination or well-organised awareness program in place.  People working in agriculture-related occupations comprised 29% of notifications in 1999-2000, a statistic that increased to 52% in 2001-2010 (Lowbridge CP, Tobin S, Seale H et al. 2012). 

AIM

The aim of this study was to estimate the herd level seroprevalence of C. burnetii infection in beef cattle in the Lachlan Livestock Health and Pest Authority (LHPA).  

METHOD

Funding was sourced from NSW Department of Primary Industries and Lachlan Livestock Health and Pest Authority through a targeted surveillance project to survey a total of 440 cattle on 22 properties in the Lachlan LHPA.  Support in experimental design was sought from NSW Department of Primary Industries Biometrics.  Producers within each of the three regions of the Lachlan Authority (Forbes, Condobolin and Young), were selected for contact using a randomised list of beef herds.

Map 1 – The Lachlan LHPA area and Forbes, Young and Condobolin within NSW

Properties were visited from January to October 2013.  Cattle within 6 months of the start and 1 month of the finish of the calving period were eligible, although on some properties calving was year round.  This was based on the assumption that calving would be an increased risk period for shedding of the organism from infected animals and therefore new infections.  During each property visit a single blood sample was collected from 20 animals via convenience sampling, and the producer answered a questionnaire relating to on-farm husbandry and knowledge about Q fever and the preventative vaccine, Q-Vax® (CSL).  Blood samples were submitted to Elizabeth Macarthur Agricultural Institute laboratory for testing using the Idexx Q Fever Ab Test, previously called the CHEKIT Q fever Antibody ELISA Test Kit.  The test is an indirect ELISA assay using inactivated Phase 1 and 2 antigens from the Nine Mile strain of C. burnetii (Rousset E, Durand B, Berri M et al. 2007).    

RESULTS

Cattle with antibody titres positive for Q fever were found on only two out of the 22 properties tested in the survey - one in the Forbes area, and the other in Condobolin.  One animal on the Forbes property was positive (S/P% greater than or equal to 40) and one animal was considered suspect (S/P% greater than or equal to 30 but less than 40).  Two animals on the Condobolin property were positive.  At an individual animal level this gives a seroprevalence of 0.7% (Table 1), and at the herd level, a seroprevalence of 9.1% (Table 2) of previous exposure to C. burnetii on Lachlan LHPA beef properties.

Table 1 – Results of the Idexx Q Fever Ab Test, Individual Animals 

+ve animals Suspect -ve animals Total animals Total Individual animals +ve
Forbes 1 1 158 160 0.6%
Condobolin 2 0 138 140 1.4%
Young 0 0 140 140 0%
Total 3 1 436 440 0.7%
Table 2 – Results of the Idexx Q Fever Ab Test, Herd Level
Properties with positive animals Properties with no positive animals Total properties tested Total properties positive
Forbes 1 7 8 12.5%
Condobolin 1 6 7 14.3%
Young 0 7 7 0%
Total 2 20 22 9.1%
Information captured by the questionnaire found the following variations between the 22 participants from the three regions

DISCUSSION

The results of this study demonstrate a very low seroprevalence of Q fever in beef cattle in the Lachlan LHPA as measured using a commercially available ELISA that detects Phase 1 and 2 antibodies against C. burnetii.  At the individual animal level our survey found a seroprevalence of 0.7%, which was low compared to the survey conducted in Queensland in 2007 (Cooper A, Hedlefs R, McGowan M et al.) which used a different ELISA, developed and validated in house, where the overall seroprevalence was 16.8%.  The herd level seroprevalence of 9.1% found in the current study was also lower than in the Queensland survey where positive samples were returned from 40% of properties at abattoir, and 78.2% of properties on farm in samples obtained from breeders and heifers.  

Seroprevalence studies tell us the number of positive animals that have either been recently infected with, or exposed to, C. burnetii and have detectable defensive antibodies at the time of sampling.  Our findings cannot be used to confer a direct degree of risk of Q fever infection to the local human population as they do not determine if animals are actively shedding C. burnetii, they merely confirm the animal’s response to its presence.  Berri et al (2001) showed that there is not necessarily a correlation between seropositivity and shedding of infection.  Their study compared serological findings (ELISA and IFA) in a flock of sheep with PCR detection of C. burnetii and showed that seropositive animals may not be shedding the organism (through vaginal fluid, milk or faeces), and conversely shedding animals may be negative on serology.   Berri et al suggested that seronegativity despite PCR antigen detection could be due to the choice of antigen used in the serological test, early infection in the individual animal pre-development of the humoral immune response, or localisation of the bacteria within the uterus and a lack of stimulation of systemic antibodies.  Any of these, along with no previous exposure, could apply to the seronegative animals within our study.              

Of the three serological tests available for C. burnetii in livestock - Complement Fixation Test (CFT), Immunofluorescence Assay (IFA) and ELISA, the Idexx Q Fever Ab Test (ELISA) was chosen as it was readily available for use in this survey, economical, and the validation report lists excellent sensitivity and specificity (both at 100%, although this testing was not conducted in Australia). CFT has traditionally been the standard test used in the past (Horigan MW, Bell MM, Pollard TR et al. 2011), however it is limited by relatively lower sensitivity and possibly also lower specificity as compared to IFA and ELISA.  The IFA was less accessible for our use in this study.  

Conclusions to be made from the questionnaire responses are limited as the number of people interviewed was not statistically significant when compared to the broader population.  However, Q fever was present within the survey population with participants having previously been diagnosed or knowing others that had been diagnosed (13/22).  It was also found that all who took part in the survey were currently conducting, or had in the past conducted, activities which would be perceived as high risk for infection with C. burnetii  and subsequent development of Q fever, ie. assisting calvings or home slaughtering of livestock.  This is despite almost three-quarters of the people within the survey (14/19) potentially being unprotected against new Q fever infection by not being vaccinated.  In 2009 Massey et al. found that difficulty in accessing the vaccine was a significant reason cited by at risk people included in a retrospective case series as to the reason why they were not vaccinated (24%), as well as poor awareness of the disease (37%).  Access to the vaccine is likely to be an issue in the Lachlan LHPA region, particularly in the western areas with local doctors not routinely providing Q-Vax® (CSL) vaccination.  Travel to larger centres where Q-Vax® (CSL) is more freely available is an option.  However vaccination requires two visits 7 days apart, with this time off work off farm likely to be a further disincentive.  The direct out of pocket cost of the vaccination may also be a factor, at $130/person vaccinated (May 2015 NSW Central West region).  

Despite a finding of only low seroprevalence of C. burnetii in local beef cattle in the current study we know that the disease is still affecting our communities with people affected among our survey participants, and more broadly, a reported 177 Q fever notifications in NSW residents in 2013 and 179 in 2014 (NSW Department of Health, 2015).  Further studies looking at other potential sources of Q fever infection for livestock producers in our local area may be considered in the future. 

ACKNOWLEDGEMENTS

Thanks to both NSW Department of Primary Industries Biosecurity and the Lachlan Livestock Health and Pest Authority for their financial support of this targeted surveillance funding project and to the survey participants in the Forbes, Condobolin and Young areas for donating their time.   Thanks to the Lachlan Livestock Health and Pest Authority District Veterinarians - Eliz Braddon, Belinda Edmonstone and Kasia Hunter for their efforts in liasing with producers to organise sample collection.  Thanks also to Barb Maloney for her support as Project Supervisor and production of the map included in this report, and to Lucienne Downes and Katrina Bosward for their much valued assistance in the production of this report.    

REFERENCES

  1. National Notifiable Diseases Surveillance System (NNDSS) Australian Government Department of Health. Number of notifications of all diseases received from State and Territory health authorities, www9.health.gov.au 2015
  2. Marmion B. (CSL Biotherapies) A Guide to Q fever and Q fever Vaccination, www.meatiesohs.org 2009
  3. National Centre for Immunisation Research and Surveillance of Vaccine Preventable Diseases (NCIRS). Vaccine Preventable Diseases in Australia, 2005 to 2007. Communicable Diseases Intelligence, www.health.gov.au  2010
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  8. Cooper A, Hedlefs R, McGowan M et al. Serological evidence of Coxiella burnetii infection in beef cattle in Queensland. Australian Veterinary Journal. 2011; 89: 260-264
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