Brucella suis in Australian dogs and pigs

Introduction

Brucellosis, caused by Brucella suis, is an emerging disease in Australia predominantly affecting pig hunters, hunting dogs and veterinary professionals. Primarily a disease of pigs (Sus scrofa), B. suis is a contagious, zoonotic species of bacteria, endemic in feral pig populations of eastern Australia. Hunting and butchering of feral pigs is the major risk factor for human infection.^1,2 Over the past decade, however, there has been a significant increase in the diagnosis of B. suis in dogs exposed to feral pigs, most commonly during hunting. This has driven research and subsequent management and policy review on the zoonotic risk posed by these working companion animals.

Brucellosis in Australia

Brucella are Gram-negative, facultative intracellular coccobacilli, of the class Alphaproteobacteria. The bacteria localise in lymphoreticular tissue and primarily cause reproductive pathology and chronic infection in the natural host.³ Infection is transmitted between hosts by contact with infected body fluids and tissue.⁴ Brucella has a worldwide distribution and there are currently 13 identified species, delineated by microbial characteristics, host preference, genome sequencing and pathogenicity. Most Brucella species have preferred reservoir hosts but can also infect a range of secondary host species, including humans, with five species known to be zoonotic.⁵

Owing to strict quarantine laws and relative geographical isolation, Australia has remained free of several major Brucella species, namely B. melitensis and B. canis. Although several articles have mistakenly stated that B. canis is endemic in Australia,^6–8 it remains exotic to this country.⁹ Australia is also one of a few countries to have successfully eradicated B. abortus, from both the domestic cattle population and wildlife reservoirs, being declared free of the disease in 1989 after an extensive test and slaughter program.⁹

Currently there are only three terrestrial species of Brucella present in Australia: the non-zoonotic pathogen Brucella ovis that affects sheep, an atypical species detected in rodents and amphibians,^10,11 and B. suis biovar 1.

The latter is the only zoonotic Brucella species endemic to Australia.^2,12 It primarily infects pigs, which are its natural host, but can also affect horses, cattle, dogs, and humans. In fact, B. suis is considered second only to B. melitensis in its pathogenicity to humans where it can cause serious and chronic disease.

Brucella suis biovar 1 was first diagnosed in Australian domestic pigs in Queensland (Qld) in 1936. It caused decreased fertility and production loss in commercial piggeries until being eradicated in this state in 1968.¹³ It was subsequently isolated in feral pigs (Sus scrofa) in Qld in 1976 and has remained endemic in this species, forming a reservoir for infection in other species.^13,14 Before 2011, B. suis had not been detected in feral pigs outside of Qld^15,16; however, it has since been detected in feral pigs in northern New South Wales (NSW) in 2012,¹⁷ in the Top End of the Northern Territory (2022)¹⁸ and in north eastern South Australia (2022).¹⁹

Recent research has estimated the prevalence of B. suis exposure in feral pigs to be 17% in Qld (one in six feral pigs seropositive) and 11% in NSW (one in nine).²⁰ Additionally, the geographic range has expanded, with detection 450 km further south than previously reported.²⁰ With an estimated 3.2 million feral pigs inhabiting 38–45% of Australia,²¹ increasing feral pig numbers and their dispersal across eastern Australia²² are considered major factors in the geographical spread of B. suis and the subsequent risk of transmission to humans and dogs. People considered most at risk of contracting brucellosis in Australia include pig hunters, abattoir workers handling feral pig carcasses, and laboratory staff and veterinarians exposed to infectious material from dogs.

Brucella suis in dogs

Before 2011, there was only a single confirmed case of B. suis in an Australian dog.²³ However, between 2011 and 2015 there was a 17-fold increase in the number of notified cases of brucellosis in NSW in dogs exposed to feral pigs, primarily through hunting or consuming uncooked feral pig meat.²⁴ This trend has continued in the ensuing years with increasing diagnosis of B. suis infection in dogs that hunt feral pigs not only in Australia but also in the United States of America.^25,26 A seroprevalence survey of Qld and NSW dogs with exposure to feral pigs found that nearly one in ten (9.3%) are seropositive for B. suis.²⁷ Furthermore, seropositive dogs were widespread, detected in 26 of 53 Qld local government areas (LGAs) and 37 of 95 NSW LGAs.²⁰ This is due not only to the high levels of participation in the activity, as there are an estimated 100,000–300,000 hunters in Australia, but also hunters often travel and hunt in multiple locations²⁷ making it difficult to identify where transmission occurs. Furthermore, dogs that travelled for hunting were found to be four times more likely to be seropositive than those that only hunted in their home region.²⁷

Dogs infected with B. suis most often present with reproductive (orchitis, abortion or dystocia) or osteoarticular disease (septic arthritis, discospondylitis) as well as variable, non-specific illness (lethargy, anorexia, soft tissue abscessation).^24,28 Owing to the cryptic intracellular nature of the bacteria, latent and subclinical infection is also a common feature, reported in up to 60% of cases.^24,28 Definitive diagnosis based on isolation of the organism is difficult to obtain and therefore serology remains the cornerstone for the diagnosis of brucellosis, not only in dogs but in all species.⁴ Brucellosis is a notifiable disease in Australia and all animal testing is performed at the state veterinary laboratories or the Australian Centre for Disease Preparedness (ACDP). Recent work has validated livestock serology tests, the Rose Bengal rapid plate agglutination test (RBRPT), the complement fixation test (CFT) and the competitive enzyme-linked immunosorbent assay (C-ELISA) for use in dogs.²⁹ Research has also shown that there is little correlation between B. suis antibody levels and health status in dogs, with high levels detected in both clinical and asymptomatic animals, as well as the persistence of seropositivity for long periods of time.²⁸

Transmission risks and management

Feral pigs are the primary source of B. suis infection with hunting, dressing carcases and consuming raw feral pig meat, the main transmission routes for both human and canine infections. Humans are considered incidental hosts for Brucella, and human-to-human transmission is described as rare and isolated.³⁰ Human-to-human transmission of B. suis has not been reported in the literature.

The transmission risk of B. suis from dogs to other species, specifically humans and other dogs is low, except at whelping and in the periparturient period²⁸ when bacteria are excreted in fluids and tissue. It has also been detected in milk, semen, joint fluid, infected testis, vertebrae and lymph nodes, and blood; however, as modes of transmission these are much less significant in the context of normal daily contact with dogs. Furthermore, systematic investigation of seropositive dogs, detected the organism only in dogs with clinical signs of disease.²⁸ Although sharing a household with a seropositive dog has been identified as a risk factor for canine infection,²⁷ distinguishing between clustering of cases due to shared exposure to feral pigs or feral pig meat versus actual dog-to-dog transmission is challenging, as both scenarios can produce similar patterns of infection within close-contact groups.

Transmission from dogs to humans through contact with infected reproductive material, although rare, has been reported³¹ and confirms that whelping and the post-parturient period, represents the highest transmission risk to humans, other dogs and potentially other species. Veterinarians performing invasive procedures and handling infected body fluids and tissues are at greater risk of infection.

Owing to concerns regarding the potential for zoonotic transmission of B. suis biovar 1, the initial government recommendation in NSW was that all test-positive dogs be euthanased. This policy was amended in 2017 to include a treatment option³²; however, euthanasia remains a primary government recommendation for dogs in Australia. Multi-antimicrobial treatment regimens, extrapolated from human medicine, combined with specific management protocols, have been formulated for use in dogs and have provided good clinical results.^28,33 Recommendations for the diagnosis and management of at-risk dogs, specifically the 4 ‘T’s (teach, test, treat and take precautions) have been published in the veterinary scientific literature.³³ However, a review of government policies and guidelines, incorporating evidence-based data, would be beneficial.

Conclusion

Brucella suis is endemic in the feral pig populations of eastern Australia, and eradication of this reservoir species is unlikely. Although humans and other animals remain at risk of infection, current evidence suggests that dogs pose a low transmission risk to humans and other dogs, outside of the breeding and whelping period. Additionally, infected dogs respond well to available treatment protocols. These findings indicate that euthanasia of all seropositive dogs appears unwarranted and although clinically affected dogs require careful handling and appropriate treatment, they can be managed without undue risk to humans. Formal updates to management guidelines and policies based on recent research, would improve both animal welfare and public health outcomes.