Ovine Observer

Coxiella burnetii (Q-fever) in Australian breeding ewes

Thomas Clune, Amy Lockwood, Serina Hancock, Andrew N. Thompson, Sue Beetson, Caroline Jacobson, Murdoch University, WA; Angus J. D. Campbell, Elsa Glanville, Daniel Brookes, University of Melbourne, VIC; Colin Trengove and Ryan O’Handley,University of Adelaide, SA

Introduction

The reproductive performance of maiden ewes is often lower than for mature ewes due to greater losses of the fetus or lamb between pregnancy diagnosis and lamb marking. The causes of these are not well defined, however a number of diseases may cause abortion and poor lamb viability in Australian sheep.

Coxiella burnetii is a bacteria that has been detected in Australian livestock (sheep, cattle, goats) and wildlife (e.g. kangaroos), as well as a wide variety of domestic and feral animals. People can become infected with C. burnetii through infected fluids or by inhaling bacteria in dust or air, resulting in the disease Q-fever. In sheep, C. burnetii infections may cause abortion, stillbirth and the birth of weak lambs that are less likely to survive. Infection is more likely to cause abortion if sheep are infected for the first time during pregnancy, with no lasting impacts on subsequent pregnancies. The risk of exposure to infection increases with time and previous infection confers some level of immunity. This means that younger ewes are particularly at risk of disease outbreak if infection occurs during pregnancy. The prevalence (frequency) of C. burnetii infections in Australian sheep is not well studied, nor whether infection is an important cause of abortion and perinatal lamb mortality in maiden ewes.

Therefore, the aim of this study is to determine if natural exposure to C. burnetii is widespread in breeding ewes and whether seropositivity is associated with poor reproductive performance of maiden ewes.

Key findings

• There was no evidence of widespread exposure to C. burnetii in breeding ewes with seropositivity (detection of antibodies) in less than 0.1% in primiparous ewes and 0.4% in mature ewes
• Exposure to C. burnetii was detected in at least one sheep on 3 farms (11% farms) in this study. These farms were located in Western Australia, South Australia, and Victoria
• Coxiella burnetii was not detected by qPCR in tissue samples from aborted or stillborn lambs recovered from primiparous ewes

Materials and methods

Study location and sheep flock characteristics

This study was conducted at 28 farms using 30 total flocks located in Western Australia, South Australia, and Victoria between 2018 and 2020, with approximately 200 maiden ewes from each farm randomly selected at mating.

Maiden ewes were mated as either ewe lambs or maiden hogget ewes and monitored between mating and lamb marking.

Reproductive data

Foetal mortality was determined via repeated pregnancy ultrasounds at 62–101 days (scan 1) and 108–136 days (scan 2). Lamb mortality between birth and marking was determined for each ewe based on birth type (single, twin or triplet), birth status (lambs dead or alive at lambing rounds) and survival status at marking. Aborted and stillborn lambs were collected for necropsy on a subset of 7 flocks in Western Australia.

For the ewe lamb flocks, foetal/lamb mortality between scan 1 and lamb marking was 36% with mid-pregnancy abortion detected in 5% ewe lambs (range 0–50% ewes). For the maiden hogget flocks, foetal/lamb mortality between scan 1 and lamb marking was 29% with mid-pregnancy abortion detected in 1% ewe hoggets (range 0–4%).

Coxiella burnetii serology and qPCR

Blood samples were collected from maiden ewes at marking, and from randomly selected mature ewes aged 3 years and older (20 mature ewes per farm). A subset at least 40 maiden ewes from each flock were selected for C. burnetii serology (detection of antibodies) with ewes that aborted or failed to successfully rear a lamb selected where possible. Ewes that had reared single or twin lambs were included for flocks with less than 40 ewes that failed to rear a lamb.

Serology for anti-C. burnetii IgG antibodies was conducted Vetpath Laboratories (Perth, Western Australia) using a commercial indirect ELISA kit (ID Screen Q-Fever Indirect Multispecies, ID Vet, France) according to the manufacturer’s instructions.

Tissue samples from aborted or stillborn lambs were screened using qPCR.

Statistical analyses

Apparent C. burnetii seropositivity (% sheep with C. burnetii IgG antibodies) was calculated using number of positive samples as a proportion of samples tested with 95% confidence interval determined using Jeffreys method. The true C. burnetii seropositivity proportion and 95% credible intervals (95% CrI) was estimated using Bayesian inference. Seropositivity (%) for the ewe age categories (ewe lamb, maiden hogget, mature ewes) were compared using a two-sample z-test, with P-value < 0.05 accepted as significant.

Results

Apparent C. burnetii seropositivity (detection of antibodies) was 0.08% in maiden ewes (ewe lambs and hoggets) and 0.4% in mature ewes (Table 1). There was no difference in detection between maiden ewes and mature multiparous ewes (P = 0.174), nor between maiden hoggets and ewe lambs (P = 0.165).

Table 1: Apparent and estimated true C. burnetii seropositivity using indirect ELISA for primiparous ewes mated as ewe lambs or yearlings) and mature multiparous ewes

CI95%: 95% confidence interval

CrI95%: 95% credible interval

At least one seropositive sheep was detected on 11% (3/28) of farms in this study. These 3 flocks were located in Western Australia, South Australia and Victoria.

Coxiella burnetii was not detected by qPCR in tissue samples from 35 aborted or stillborn lambs recovered from a subset of seven flocks in Western Australia.

Discussion

There was no evidence to implicate C. burnetii was an important contributor to abortions or perinatal lamb mortality in 30 maiden ewe flocks on farms across southern Australia. The low detection of C. burnetii seropositivity (detection of antibodies) was consistent with the absence of detection of C. burnetii in tissues from aborted or stillborn lambs from a subset of farms. Consequently, there was no evidence to support the implication of targeted preventative measures such as vaccination, which is utilised in some overseas countries, on these farms.

Our findings were consistent with a recent reviews of veterinary laboratory investigations that reported coxiellosis (Q-fever) to be an uncommon diagnosis in Australian sheep abortion investigations. Nonetheless, C. burnetii should be included as a differential diagnosis (potential cause) in sheep abortion and perinatal mortality investigation protocols due to the sporadic nature of coxiellosis and important zoonotic implications.

Despite the low level of C. burnetii seropositivity in these flocks, contact with sheep should still be considered a risk for Q-fever in humans. Sheep have been associated with human cases of Q-fever in in Australia and overseas, including from sheep with no symptoms of illness and without detectable seropositivity. People working with sheep (including farm, abattoir and veterinary staff) should take precautions to reduce the risk of zoonotic C. burnetii infection including appropriate personal protective clothing when handling birth material or lambing ewes (including gloves and mask where possible), good hygiene practices, controlling dust and vaccination.

Conclusion

There was no evidence of widespread exposure to C. burnetii in sheep from farms in southern Australia. Infection with C. burnetii was unlikely to be an important contributor to abortions or perinatal lamb mortality in maiden ewes on these farms.

Regardless, there is occupational risk of zoonotic infection with C. burnetii and people working with livestock (including sheep, goats and cattle) in Australia should take appropriate measures to avoid infection (Q-fever).

Further information

• Report on Reducing foetal and lamb losses in young ewes
• Scientific paper (free access)
• DPIRD ewe abortion and newborn lamb death surveillance program  

Acknowledgments

This project was funded by Meat and Livestock Australia. We thank the participating farmers who provided access to their animals and facilities. We thank Celia Smuts, Janine Simmonds and the staff at Vetpath for their assistance with the serological testing. We thank Shane Besier, Sam Hair, Cameron Loomes, Richmond Loh and Anna Erickson at DPIRD for their assistance with the laboratory diagnostic testing through the DPIRD ewe abortion and newborn lamb death surveillance scheme. We thank Tom La and Nyree Philip (Murdoch University), Louis Lignereux and Rob Paterson (University of Adelaide), Andrew Whale, Mary McQuillan and Patrick Hannemann (Livestock Logic, Hamilton, Victoria), Sean McGrath (Millicent Veterinary Hospital), Simon Edwards and Michelle Smart (Willunga Veterinary Hospital), and Lauryn Stewart and Deb Lehmann (Kangaroo Island Veterinary Hospital) for assistance with sample collection.

Adapted for Ovine Observer with assistance of Sofia Testa (Murdoch University Bachelor of Agricultural Science student).