Equine psittacosis: an emerging cause of equine abortion and neonatal illness in Australia

Charles El-Hage; Joanne Devlin; Kristopher Hughes; Cheryl Jenkins; Susan Anstey; Martina Jelocnik; James Gilkerson

doi:10.1071/MA25006

RESEARCH ARTICLE (Open Access)

Equine psittacosis: an emerging cause of equine abortion and neonatal illness in Australia

Charles El-Hage ^A ^B ^* , Joanne Devlin ^B , Kristopher Hughes ^C , Cheryl Jenkins ^D , Susan Anstey ^E , Martina Jelocnik ^F and James Gilkerson ^A ^B

+ Author Affiliations

- Author Affiliations

^A Centre for Equine infectious Disease, Melbourne Veterinary School, The University of Melbourne, Parkville, Vic. 3010, Australia.

^B Asia Pacific Centre for Animal Health, Melbourne Veterinary School, The University of Melbourne, Parkville, Vic. 3010, Australia.

^C School of Agricultural, Environmental and Veterinary Sciences, Faculty of Science and Health, Charles Sturt University, Wagga Wagga, NSW 2650, Australia.

^D Elizabeth Macarthur Agricultural Institute, NSW Department of Primary Industries, Menangle, NSW 2568, Australia.

^E Kenilworth Veterinary Surgery, 4 Elizabeth Street, Kenilworth, Qld 4574, Australia.

^F School of Science, Technology and Engineering, University of the Sunshine Coast, Sippy Downs, Qld 4556, Australia.

Dr Charlie El-Hage graduated from The University of Melbourne and worked locally and internationally in rural veterinary practices, Charlie returned to The University of Melbourne as an equine clinician and lecturer in 2001, subsequently completing a PhD in equine virology and immunology in 2016. Now an honorary fellow, he has maintained an active range of projects supervising students in equine interests including infectious diseases, welfare, immunology, toxicology and endocrinology. He has a range of publications include reviews and original articles.

Prof. Joanne Devlin is head of the Melbourne Veterinary School, having graduated from The University of Sydney and completed her PhD in veterinary virology at The University of Melbourne. Her research includes diseases of domestic animals and wildlife, including birds, horses and marsupials including vaccine development and testing. She was awarded an Australian Research Council (ARC) Postdoctoral Fellowship in 2008. She is a current member of the ARC College of Experts.

Kristopher Hughes is a Fellow of the Australian and New Zealand College of Veterinary Scientists in equine medicine and a diplomate of the European College of Equine Internal Medicine. Kris is currently professor of equine medicine at Charles Sturt University, Australia. Kris is active in referral equine veterinary practice, undergraduate and post-graduate teaching, research and veterinary hospital management. His research interests include infectious diseases of horses, equine parasitology, equine endocrinology and intensive care of horses.

Cheryl Jenkins is a principal research scientist leading a molecular biology laboratory within the Microbiology and Parasitology section at the Elizabeth Macarthur Agricultural Institute. She has 15 years’ experience in molecular biology with a focus on microbial pathogenesis, diagnostic test development, proteomics and genomics. She has over 80 published works in peer-reviewed journals.

Dr Susan Anstey is a distinguished veterinarian and researcher. She graduated from The University of Queensland in 1991, laying the foundation for a successful career in veterinary medicine. Since 2001, Dr Anstey has owned and operated Kenilworth Veterinary Surgery, a mixed animal practice. Dr Anstey completed her PhD at the University of the Sunshine Coast in 2023. Her doctoral research focused on the epidemiology of Chlamydia psittaci in pregnant thoroughbred mares, contributing valuable insights to equine reproductive health and disease prevention.

Dr Martina Jelocnik is a lecturer in microbiology at the University of the Sunshine Coast. She leads the ‘Molecular Chlamydia’ research team that investigates key questions in the molecular epidemiology, zoonotic potential, control and diagnosis of veterinary chlamydia. Martina’s research is focused on fine-detailed molecular epidemiology of chlamydial infections in Australian livestock as well as wildlife, employing novel molecular approaches. Martina has been at the forefront of the emerging chlamydia infections in horses and applying innovative ‘One Health approach’ to dissect these infections. She also works on the development of rapid isothermal assays that can be deployed at the point-of-care for detection of chlamydia.

Prof. James Gilkerson is an equine veterinarian whose research interests are focused on the diagnosis, epidemiology and prevention of infectious diseases. James graduated from The University of Sydney awarded a BVSc, BSc (Vet) and a PhD and is currently a professor of veterinary microbiology and director of the Centre for Equine Infectious Disease at The University of Melbourne. James has written more than 130 peer-reviewed publications, numerous textbook chapters and has supervised 20 PhD students to completion.

^* Correspondence to: cmeh@unimelb.edu.au

Microbiology Australia https://doi.org/10.1071/MA25006

Submitted: 16 January 2025 Accepted: 10 February 2025 Published: 21 February 2025

© 2025 The Author(s) (or their employer(s)). Published by CSIRO Publishing on behalf of the ASM. This is an open access article distributed under the Creative Commons Attribution 4.0 International License (CC BY).

Abstract

Chlamydia psittaci is an obligate, intracellular, bacterial pathogen generally associated with clinical and subclinical infection of birds. It is a zoonotic pathogen in humans causing psittacosis a serious respiratory disease and reported to cause infection in animals including cattle, sheep and horses. Although there have been sporadic reports of disease due to C. psittaci in horses since the last century, reports from Australia over the last decade have highlighted the potential of disease in horses and zoonotic transfer. Epizootics of abortions and stillbirths in mares and serious neonatal disease, termed equine psittacosis (EP), have highlighted the potential of C. psittaci to both cause disease in horses and recognise them as major mammalian vectors for zoonotic transmission. Molecular characterisation techniques for these Australian isolates have demonstrated that the majority of equine associated C. psittaci strains have identified the globally disseminated pathogenic 6BC/ST24 type. Diagnosis is primarily through molecular techniques to identify C. psittaci genomically as seroconversion has not been reliably observed in horses. In tissues from abortion samples histopathological changes typically include lymphohistiocytic placentitis though this is neither a sensitive or specific finding in cases of EP. Neonatal foal illness is characterised by severe interstitial pneumonia and disease is generally fatal. Recognition of EP has heightened both awareness of C. psittaci as an equine abortigenic pathogen and the zoonotic threat that infected horses pose. Personal protective equipment should be donned by exposed personnel and strict biosecurity and control measures should be enforced following equine abortion or foetal loss cases and neonatal illness pending diagnostic evaluation.

Keywords: Chlamydia psittaci, equine psittacosis, mare abortion, neonatal illness, placentitis, psittacines.

Introduction

Although primarily associated with infection in birds, infection with Chlamydia psittaci is also seen in mammals.¹^–⁵ However, until recently, it was rarely considered among the causes of reproductive loss in horses. Although several European reports identified C. psittaci as an infrequent cause of foetal loss,⁶^,⁷ in a recent epizootic of reproductive loss in Australian thoroughbred horses, 21% of the abortions and 24% of neonatal foal deaths could be attributed to C. psittaci.⁸ A subsequent retrospective study of equine abortion cases in Australia detected C. psittaci in 6.5% of over 500 abortion cases from 1994 to 2019,⁹ suggesting that this organism may be an under-diagnosed cause of equine reproductive loss. Infection with C. psittaci can also be subclinical, with studies detecting it in newborn foals, stallions and mares,¹⁰^,¹¹ Increased awareness about equine psittacosis (EP) in Australia is partially attributable to the potential for zoonotic transmission of C. psittaci from horses to humans, as demonstrated by the infection of several veterinary staff and students who attended a case in 2014.¹²

Birds are considered the most common source of infections of humans and other mammals,¹³^–¹⁶ and transmission from mammals to humans has only rarely been reported,¹⁷ but cases reported over the last decade have implicated infected horses as a significant zoonotic threat.¹⁷^,¹⁸

Equine psittacosis has been adopted as an appropriate term to describe disease in horses caused by infection with C.psittaci,¹⁹ as infection appears to result from spillover from native birds sharing pasture spaces.⁸^,¹⁸ Although other Chlamydia species have been detected in cases of equine abortion in Europe and Western Canada,²⁰^,²¹ the vast majority of cases have been associated with C. psittaci.

History of EP in Australia

Prior to 2016, there was only sporadic retrospective evidence of disease and or reproductive loss in horses associated with C. psittaci.³^,⁵^,⁹^,²² In addition, it had been detected in both diseased and healthy horses, raising questions about the pathogenicity of C. psittaci in horses.³^,⁵^,⁶^,¹¹^,²² In an epizootic of reproductive loss in 2016 in New South Wales (NSW), C. psittaci was detected by polymerase chain reaction (PCR) in 21% of 161 cases of abortion and 24% of 38 ill foals. Clinical and laboratory findings of detection was considered consistent with EP in the vast majority of positive detections.⁸ This outbreak resulted in a major shift in our awareness and understanding of the significance of C. psittaci in horses and was also linked with a number of zoonotic cases, revealing a previously unidentified zoonotic source of C. psittaci.¹²^,²³ Between 2016 and 2018, additional cases of respiratory disease in neonatal foals attributed to C. psittaci were seen in NSW²⁴ and abortion associated with C. psittaci was seen on a horse stud in South East Queensland.⁸^,¹²^,²⁵^,²⁶ A longitudinal study of 14 horse studs in NSW detected C. psittaci in 13% of healthy newborn foals, although no cases of reproductive loss were reported.¹¹ A 25-year retrospective study of over 500 equine abortion cases across multiple Australian states detected C. psittaci in 6.5% of cases, suggesting that this pathogen could have been an important contributor to equine reproductive loss for a number of decades.⁹

Disease in horses due to Chlamydia psittaci

Historically, C. psittaci in horses had been sporadically associated with a range of disease presentations, including acute respiratory disease), recurrent airway obstruction, and polyarthritis.³^,²²^,²⁷^,²⁸ In mares, the only clinical signs associated with psittacosis are late-term abortion or stillbirths, with no other indications of systemic disease. Premature lactation can also occur as a sign of impending abortion.²⁹ While mares appear otherwise healthy, C. psittaci can occasionally be detected in vaginal swabs for up to a week after abortion by PCR,⁸ However, C. psittaci has also been detected in vaginal or uterine swabs from mares with no prior or subsequent disease history.¹⁰^,¹¹ No difference has been detected in the incidence of abortion or foetal loss in the first pregnancy or later pregnancies, and mares have been reported to abort in successive pregnancies,¹⁹ suggesting the lack of a robust immune response, which may be reflected by the variable serological responses seen after infection of horses.²⁵

Neonatal foals with systemic psittacosis are often acutely ill, with respiratory dysfunction and decreased awareness and responsiveness.²⁴ Foals usually develop clinical signs of disease within 24 h of birth. Increased respiratory effort and distress is a consistent feature, reflecting the development of acute interstitial pneumonia, acute lung injury and acute respiratory distress syndrome. Affected foals are usually recumbent, hypothermic (occasionally pyrexic) and have evidence of cardiovascular dysfunction, including bradycardia or tachycardia, hypotension and hyperlactataemia. Foals with this condition have a poor prognosis for survival and most die or are euthanased within 1–2 days, despite intensive veterinary management, due to progressive cardiorespiratory dysfunction.²⁴

Temporal and spatial aspects of EP in Australia

Cases of EP and subclinical infections have a strong seasonal pattern of occurrence, with infection often detected in the cooler months of the year, coinciding with the latter stages of pregnancy in mares in Australia.¹⁹^,³⁰^,³¹ Although cooler, wetter climates have been suggested as a risk factor,¹⁹^,³⁰ host factors, such as hormonal and tissue changes in late pregnancy, and ecological aspects, including the proximity of avian reservoirs and exposure to fomites could also play a role. NSW cases have been concentrated in the eastern regions of the state and cases in Victoria and Queensland have occurred within several hundred kilometres of the NSW borders.¹⁹^,³¹

Molecular analysis of Chlamydia psittaci strains asssociated with EP

Molecular characterisation by whole genome sequencing (WGS) and other molecular strain typing methods have consistently detected the globally disseminated pathogenic clonal 6BC/ST24 type strains of C. psittaci associated with EP in Australia.⁹^,³¹^–³⁴ The majority of positive samples were from horses on properties on which psittacine birds reside and these birds are also common hosts for ST24 strains in Australia.⁸^,³⁵

Diagnosis

Detection of C. psittaci requires specific pathogen testing as routine bacterial culture in cases of equine reproductive loss will lack sensitivity. Molecular detection of DNA is a useful screening tool, but, as C. psittaci can also be detected in clinically healthy horses,¹⁰^,¹¹ detection needs to be interpreted in the light of clinical and pathological findings. The chlamydial genomic load in placental tissues, or the lung tissue of aborted foals, as determined by quantitative PCR (qPCR), is correlated with disease, and high loads of C. psittaci are considered indicative of EP.⁸^,²⁹

Routine histological assessment is not considered specific for attributing causation to C. psittaci infection, although the presence of lymphohistiocytic placentitis is suggestive of psittacosis, and further ancillary testing should be used to support the diagnosis.²⁹ Intracellular chlamydia associated with pathological changes can be detected using Machiavello, Giemsa, Gimenez or modified Ziehl–Neelsen stains,²⁹^,³⁶ in situ hybridisation or immunohistochemistry. DNA probes or monoclonal antibodies targeting the chlamydial lipopolysaccharide (LPS) can be applied to histopathological sections to detected chlamydial DNA or antigens.²⁰^,³⁷ However, immunohistochemistry is not species specific, so speciation should be performed with a species-specific PCR or qPCR to confirm the presence of C. psittaci.

Culture of C. psittaci is not used for routine diagnosis because of the requirement for higher level microbiological containment and the extended turnaround times, which would delay the biosecurity and biosafety responses.

A pan-Chlamydiales (multiple Chlamydia species) qPCR assay can be used for initial screening, followed by, or alongside, a C. psittaci-specific assay.¹⁸^,²⁴^,³⁵^,³⁸ A benefit of using PCR-based methods is that the material used for detection can be subsequently used for strain typing or genomic sequencing, which can assist in identifying a possible origin of infection (see below). Recently, stall-side point-of-care isothermal (loop-mediated isothermal amplification, LAMP) assays have been validated, significantly decreasing the turnaround time for detection.¹¹^,³⁹

The chorioallantois, amnion and umbilical cord from the fetal membranes, and the lungs, liver, thymus and spleen from foetuses or deceased foals, should be submitted for gross and histological evaluation following equine abortion and neonatal illness.²⁹ The foetal membranes and foetal lung have the highest concentrations of C. psittaci, and the most marked histological changes.²⁹ Liver samples are also useful for histological examination, to determine if hepatitis is present.

In cases of neonatal illness, particularly in foals with respiratory disease, samples submitted should include the foetal membranes, if available, and nasal, oral and rectal mucosal swabs,²⁴ although concentrations of C. psittaci are usually much lower in nasal and rectal swabs than in foetal membranes. If the foetal membranes are not available, a swab sample can be obtained from the vestibule of the mare.

Serology

Although serological tests, including ELISAs or the complement fixation test are often used in other species, they are either unreliable or non-specific in cases of EP. The relationship between infection of the equine reproductive tract and seroconversion in mares is also not clear.²⁵ Assays for chlamydial DNA are considered more reliable diagnostic tests.²⁰^,²³^,³⁷

Treatment and prevention

No specific treatment of mares is considered necessary following C. psittaci abortion. Preventative measures include biosecurity to prevent exposure of other mares and personnel to aborted tissues and fluids, and limiting exposure of horses to bird fomites faeces and bodily fluids, where possible. Neonatal foals born to mares with a late-term C. psittaci infection have a poor prognosis.²⁴ A management plan to control the zoonotic risk is critical. This should include use of personal protective equipment (PPE), limiting proximity to infected material, appropriate and rapid diagnostic testing, and education.¹²^,³⁹

There are no data to indicate that prophylactic antibiotic treatment during an epizootic is effective in preventing infection or enhancing foal survival.³⁹

Consideration has been given to reducing the likelihood of contact between birds and horses, particularly during pregnancy, with emphasis on feeding strategies that reduce access or attractiveness to psittacines.³⁹ Such practices on at risk farms have included replacing cereal grains in with pelleted feed and feeding horses in areas not accessible to birds (P. Huntington, pers. comm., 2025).

Discussion

Although outbreaks of reproductive loss and neonatal disease due to C. psittaci have been reported across Australia since 2014, and retrospective studies have detected cases as early as 1997, there is much that remains unknown about this emerging pathogen in horses. The close relationship between psittacosis in horses and humans highlights the importance of a One Health approach to zoonotic disease and the need to examine the environmental factors that enable transmission between wildlife and domestic animal species.

Although much has been learned about EP over the last decade, there is still much to understand about its epidemiology and the susceptibility of horses to this disease. Of particular interest and concern is the detection of C. psittaci in horses with no signs of disease, as this not only poses a diagnostic challenge for clinicians, but also raises the concern that subclinically infected horses may be a zoonotic risk. It is clear that C. psittaci is a significant zoonotic risk, particularly for personnel exposed to breeding mares and foals. Although PPE and biosecurity measures should be in place, surveillance and rapid diagnostic testing are warranted for any mare abortion incident.

Equine veterinary practitioners and horse farm managers are increasingly facing challenges that require consideration of ecological factors and changes in wildlife behaviour associated with increased urbanisation, precipitating and spillover of pathogens like C. psittaci. Continued attention to surveillance, further studies and increased awareness are needed to limit the significant financial, animal welfare and public health burdens associated with these diseases.

Data availability

Data available upon request.

Conflicts of interest

The authors declare that they have no conflicts of interest.

Declaration of funding

This research did not receive any specific funding.

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Biographies

Dr Charlie El-Hage graduated from The University of Melbourne and worked locally and internationally in rural veterinary practices, Charlie returned to The University of Melbourne as an equine clinician and lecturer in 2001, subsequently completing a PhD in equine virology and immunology in 2016. Now an honorary fellow, he has maintained an active range of projects supervising students in equine interests including infectious diseases, welfare, immunology, toxicology and endocrinology. He has a range of publications include reviews and original articles.

Prof. Joanne Devlin is head of the Melbourne Veterinary School, having graduated from The University of Sydney and completed her PhD in veterinary virology at The University of Melbourne. Her research includes diseases of domestic animals and wildlife, including birds, horses and marsupials including vaccine development and testing. She was awarded an Australian Research Council (ARC) Postdoctoral Fellowship in 2008. She is a current member of the ARC College of Experts.

Kristopher Hughes is a Fellow of the Australian and New Zealand College of Veterinary Scientists in equine medicine and a diplomate of the European College of Equine Internal Medicine. Kris is currently professor of equine medicine at Charles Sturt University, Australia. Kris is active in referral equine veterinary practice, undergraduate and post-graduate teaching, research and veterinary hospital management. His research interests include infectious diseases of horses, equine parasitology, equine endocrinology and intensive care of horses.

Cheryl Jenkins is a principal research scientist leading a molecular biology laboratory within the Microbiology and Parasitology section at the Elizabeth Macarthur Agricultural Institute. She has 15 years’ experience in molecular biology with a focus on microbial pathogenesis, diagnostic test development, proteomics and genomics. She has over 80 published works in peer-reviewed journals.

Dr Susan Anstey is a distinguished veterinarian and researcher. She graduated from The University of Queensland in 1991, laying the foundation for a successful career in veterinary medicine. Since 2001, Dr Anstey has owned and operated Kenilworth Veterinary Surgery, a mixed animal practice. Dr Anstey completed her PhD at the University of the Sunshine Coast in 2023. Her doctoral research focused on the epidemiology of Chlamydia psittaci in pregnant thoroughbred mares, contributing valuable insights to equine reproductive health and disease prevention.

Dr Martina Jelocnik is a lecturer in microbiology at the University of the Sunshine Coast. She leads the ‘Molecular Chlamydia’ research team that investigates key questions in the molecular epidemiology, zoonotic potential, control and diagnosis of veterinary chlamydia. Martina’s research is focused on fine-detailed molecular epidemiology of chlamydial infections in Australian livestock as well as wildlife, employing novel molecular approaches. Martina has been at the forefront of the emerging chlamydia infections in horses and applying innovative ‘One Health approach’ to dissect these infections. She also works on the development of rapid isothermal assays that can be deployed at the point-of-care for detection of chlamydia.

Prof. James Gilkerson is an equine veterinarian whose research interests are focused on the diagnosis, epidemiology and prevention of infectious diseases. James graduated from The University of Sydney awarded a BVSc, BSc (Vet) and a PhD and is currently a professor of veterinary microbiology and director of the Centre for Equine Infectious Disease at The University of Melbourne. James has written more than 130 peer-reviewed publications, numerous textbook chapters and has supervised 20 PhD students to completion.