Companion Animal Zoonoses Guidelines

Australian Companion Animal Zoonoses Advisory Panel (ACAZAP)

Proudly supported by Boehringer Ingelheim Animal Health

HOW DO I NAVIGATE THESE GUIDELINES?

• You can jump directly to any section by clicking the section title in the Table of Contents.

Antimicrobial Resistance

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CONTENTS

- infection control practices (inclusive of PPE and isolation requirements) to be implemented. The AVA Guidelines for Veterinary Industry Personal Biosecurity are a useful resource in this regard.

• Hyperlinks within the text are indicated in blue text and will take you to additional resources.

• The icons opposite are used as a quick guide to the modes of transmission of the pathogens listed in the guidelines.

TRANSMISSION IN ANIMALS

Direct contact

Indirect contact

Foodborne

Waterborne

Vector-borne

IN HUMANS

Cover image: Medical illustration of nontyphoidal Salmonella spp. bacteria. (Public Health Image Library, CDC)

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2 Companion Animal Zoonoses Guidelines

Contents

Introduction

Australian Companion Animal Zoonoses Advisory Panel Members

Antimicrobial Resistance

Bordetella bronchiseptica

Brucellosis ( Brucella suis )

Campylobacteriosis ( Campylobacter spp.)

Cat Scratch Disease ( Bartonella spp.)

Cryptosporidiosis ( Cryptosporidium spp.)

Dog and Cat Bite Wounds

Flea-Borne Spotted Fever ( Rickettsia felis )

Giardiasis ( Giardia spp.)

Hookworm ( Ancylostoma spp., Uncinaria stenocephala )

Hydatid Disease ( Echinococcus granulosus )

Leptospirosis ( Leptospira spp.)

Q Fever ( Coxiella burnetii )

Ringworm

Salmonellosis ( Salmonella spp.)

Sarcoptic Mange ( Sarcoptes scabiei var. canis )

Strongyloidiasis ( Strongyloides stercoralis )

Toxocariasis ( Toxocara canis, T. cati )

Toxoplasmosis ( Toxoplasma gondii )

Animals In Care Facilities

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Companion Animal Zoonoses Guidelines 3

COMPANION ANIMAL ZOONOTIC DISEASES

The agreeable nature of many domestic animals has seen them become indispensable companions to many around the world. In Australia, 60% of households are reported to have a pet, with an estimated 5.1 million pet dogs and 3.7 million pet cats. 1 The reasons for pet ownership, like the pets themselves, are many and varied. In addition to companionship, pet ownership has a range of positive emotional, physical, and psychological benefits including improved mental wellbeing, increased independence, and increased physical activity. 2,3 Dogs and cats, both healthy and sick, may carry a range of different zoonotic organisms. Given the close relationship between pets and people and their shared living environment, it is not surprising that interspecies transfer may occur occasionally, either directly or indirectly. Whilst transmission of zoonotic pathogens has always been a risk, increasing anthropomorphism of companion animals and the associated high-intensity human-animal interactions make such infections more likely as opportunities for transmission increase. Coupled with this is an increase in the population of those at greatest risk for severe consequences of these infections, including people with compromised immune systems (e.g. HIV, organ transplants, cancer), pregnant women, the very young and the elderly. “Animals are such agreeable friends – they ask no questions, they pass no criticisms” Mary Ann Evans (aka George Eliot)

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4 Companion Animal Zoonoses Guidelines

With zoonotic diseases, there is no such thing as a “no-risk” pet, or a “no-risk” owner. It is important however to consider the risks in a rational and evidence-based manner. By implementing appropriate risk mitigation strategies, the benefits of pet ownership can be enjoyed safely in the vast majority of circumstances. AUSTRALIAN COMPANION ANIMAL ZOONOSES ADVISORY PANEL (ACAZAP) In February 2020, Boehringer Ingelheim brought together an expert panel of veterinary and human infectious disease experts to review and discuss the latest research and make evidence-based recommendations around the control of zoonotic diseases in dogs and cats. The pathogens included in these guidelines were chosen by the panel based on consideration of their significance in the Australian context. In this regard, significance is a broad term encompassing factors such as the probability and/or consequences of infection. In reviewing each pathogen, the panel considered animal factors, environmental factors,

THE AIMS OF THE PANEL WERE TO:

• P rovide recommendations and strategies to minimise the risk of zoonotic disease transfer from dogs and cats in the veterinary clinic and community setting • Facilitate discussion and collaboration between human and veterinary medical professionals to optimise health outcomes, both for pets and people • Promote awareness of zoonotic diseases and strategies to control them to pet owners

and human factors that contribute to zoonotic disease. Inclusion of a pathogen in these guidelines does not imply that companion animals are the sole or even primary source of infection for people. In some cases, the contribution of dogs and cats to the disease burden in humans may be small and overshadowed by other potential routes of transmission. In such instances, an understanding of the minor role companion animals play remains important as it allows veterinarians and pet owners to fully evaluate the risk and implement a proportional management response. Whilst it is not necessary for veterinarians to treat or manage human zoonotic infections, a knowledge of risk factors and the consequences of infection in humans allows for a more considered analysis of risk for themselves, their staff, and their clients. From a medicolegal perspective, veterinarians have a duty of care for their staff and clients and are obligated to provide advice and protective strategies to protect people under their guidance. However, veterinarians must use caution not to exceed the scope of their veterinary registration while fulfilling their public health responsibilities. Information concerning veterinary or public health aspects of zoonoses should be provided to clients as indicated and requested, with all recommendations clearly documented in clinical records. Veterinarians should not diagnose or treat diseases in humans or make recommendations about those issues. On the other side of the zoonoses coin, for human medical professionals, an understanding of the epidemiology of these pathogens in animals, and the associated risk factors in animals, will assist in assessing and managing potential cases, and providing advice to patients about minimising the risk of zoonoses from companion animals. In this regard there is much to be gained by facilitating greater interaction between the medical and veterinary professions to help prevent, diagnose, and treat zoonotic diseases. 4

References: 1. Animal Medicines Australia, Pets in Australia: A national survey of pets and their people. 2019. 2. Smith, B., (2012) The ‘pet effect’: Health related aspects of companion animal ownership. Aust Fam Physician , 41(6), 439. 3. McConnell, A.R., et al (2011) Friends with benefits: on the positive consequences of pet ownership. J Pers Soc Psychol , 101(6), 1239. 4. Steele, S.G., et al (2019) What makes an effective One Health clinical practitioner? Opinions of Australian One Health experts. One Health , 8, 100108.

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Companion Animal Zoonoses Guidelines 5

AUSTRALIAN COMPANION ANIMAL ZOONOSES ADVISORY PANEL MEMBERS

Associate Professor Gottlieb is an Infectious Diseases physician and microbiologist, Head of the Infectious Diseases and Microbiology Department at Concord Hospital, and Senior Lecturer at the University of Sydney. He is a past president and honorary member of the Australasian Society for Infectious Diseases (ASID) and a past president of the Australian Society for Antimicrobials (ASA). Thomas is an executive member of the Australian Group on Antimicrobial Resistance (AGAR) and ASA. He has represented ASA on the Australian Strategic and Technical Advisory Group on Antimicrobial Resistance (ASTAG), responsible for the development and implementation of Australia’s National Antimicrobial Resistance (AMR) Strategy. He has been chair of advisory committees supervising training in Infectious Diseases and Microbiology. He has participated in the writing groups for the Australian Infection Control Guidelines, the national Therapeutic Guidelines for Antibiotic Use, Australian recommendations for the control of carbapenemase-producing Enterobacteriaceae (CPE) in acute care health facilities and guidelines for Antimicrobial Stewardship in Australian Healthcare. He is a member of the NPS Antibiotic Resistance Reference Group and the National Antimicrobial Stewardship Advisory Committee for the Australian Commission on Safety and Quality in Health Care (ACSQHC). Following the completion of a BSc (Vet) in 1990 and BVSc in 1991 at the University of Sydney, Katrina worked in mixed and small animal veterinary practice. Katrina returned to the University of Sydney in 1995 to undertake a PhD in collaboration with CSIRO, Animal Production entitled “Eosinophils and Interleukin 5 in Sheep”. On completion of her PhD, Katrina commenced training in Clinical and Anatomical Veterinary Pathology and Microbiology at the University Veterinary Centre, Camden earning a Graduate Diploma in Veterinary Clinical Studies. Since 2002, Katrina has been an academic staff member at the Sydney School of Veterinary Science, University of Sydney where her current teaching within the Doctor of Veterinary Medicine degree is centred on the pathogenesis of infectious diseases (including those considered zoonotic) and the biosecurity practices associated with controlling and preventing those diseases. Her current research projects follow the same themes with a general interest in zoonotic diseases. Her true passion however is all things concerning Coxiella burnetii and she is involved in many projects investigating this intriguing pathogen in a wide variety of species including Q fever in humans. Dr Timothy Gilbey is a Fellow of the Royal Australasian College of Physicians in Infectious Diseases, a member of the Australasian Society for Infectious Diseases, and is currently Infectious Disease Visiting Medial Officer (VMO) for the Murrumbidgee Local Heath District (MLHD). In addition to clinical responsibilities, Tim has been heavily involved in education and training in medicine and infectious diseases; he holds a Conjoint Associate Lecturer position with the University of New South Wales where he is responsible for teaching clinical aspects of infectious disease to medical students; is involved in the Royal Australasian College of Physicians as a Regional Examiner; and was the founding chair of “Bug School”, a teaching program specifically designed to bridge experience gaps in the teaching of infectious diseases to registrars. Tim has a specific interest in antimicrobial stewardship, serving as co-chair of the Antimicrobial Stewardship Committee for MLHD. Tim’s research interests include antimicrobial resistance and the use of bacteriophages to treat severe bacterial infections, having presented and published in this area. Tim is also passionate about rural medicine and One Health.

Associate Professor Katrina Bosward BSc (Vet) Hons 1, BVSc, PhD, Grad Dipl Vet Clin Sci, Grad Cert (Higher Ed), MASM, MASID Associate Professor in Veterinary Microbiology, Sydney School of Veterinary Science, University of Sydney

Dr Timothy Gilbey MBBS, FRACP, BSc (phys)

Infectious Disease Visiting Medical Officer (VMO), Murrumbidgee Local Health District (MLHD). Conjoint Associate Lecturer, University of New South Wales

Associate Professor Thomas Gottlieb MBBS, FRACP, FRCPA Senior Staff Specialist Microbiology and Infectious Diseases, Concord Hospital. Clinical Associate Professor, University of Sydney

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6 Companion Animal Zoonoses Guidelines

Jacqui is a Professor of Veterinary Microbiology and Infectious Diseases, and Associate Head of Research at the Sydney School of Veterinary Science, at the University of Sydney. She is a registered practicing veterinarian and is passionate about practical research projects and education programs for veterinary professionals, animal breeders and animal owners. Her main research areas include: 1) Development of diagnostics and treatments for companion animal viral diseases; 2) Q fever; 3) Multidrug resistant (MDR) Staphylococcus species; 4) Infection prevention and control in veterinary practices; 5) Chronic renal disease in domestic and zoo felids and 6) Factors influencing antimicrobial prescribing behaviour of vets and health professionals. Peter graduated in veterinary science from the Royal Veterinary College, London University in 1982 and has a PhD from James Cook University (1991) for studies into canine babesiosis in Australia. He is a Fellow of the Australian and New Zealand College of Veterinary Scientists and is a registered specialist in canine medicine. He is currently Emeritus Professor at Murdoch University in Perth. Peter has worked in academia in Australia and overseas for 30 years as a teacher of companion animal medicine and as a researcher in the fields of veterinary parasitology and medical microbiology. He is an internationally recognised expert in vector-borne diseases and is a director of the Vector and Waterborne Pathogens Research Group (the Cryptick Laboratory) at Murdoch University. After completing a BSc with a major in psychology and mathematics, Jane graduated with a BVSc(Hons) from the University of Sydney. Following some years of clinical work in private practice and at the Universities of Sydney (where she also obtained two additional postgraduate qualifications, DipVetClinStud and MVetClinStud) and Glasgow, she completed her training in Veterinary Epidemiology and Public Health through a PhD and DiplECVPH residency at the University of Glasgow. In 2009 Jane took up a faculty position at Charles Sturt University and progressed to work as an Associate Professor in Veterinary Epidemiology and Public Health, currently still holding this position as a part time appointment. Jane also works as a consultant epidemiologist within her business ‘Heller Consulting’. Jane has been involved in numerous research projects, acting as principal investigator for many of these, has published over 70 journal articles and delivered over 100 scientific presentations at national and international conferences. Jane’s main research interest is in infectious disease epidemiology, with particular reference to antimicrobial resistance and the potential for zoonotic transfer of pathogens between animals and humans. Prof. Traub graduated as a veterinarian from Murdoch University, WA in 1997 and subsequently worked in small animal practice. In 2004, she completed her PhD on canine parasitic zoonoses for which she was awarded the John Adrian Sprent Prize by the Australian Society for Parasitology. Prof. Traub was subsequently awarded a fellowship to continue her research in this field by the Australian Research Council. In 2006, she gained employment as a lecturer in Veterinary Public Health at the University of Queensland and in 2014 moved to the Melbourne Veterinary School, where she currently works as a Professor of Veterinary Parasitology and Australian Research Council Future Fellow (2021-2025). Prof. Traub has published over 145 international peer-reviewed papers and book chapters covering the diagnosis, zoonotic potential, epidemiology and control of canine endoparasites and vector- borne diseases, with much of her research based in the Asia Pacific. Dr Traub’s research expertise has been formally recognized through consultations for the WHO, FAO, OIE, The Gates Foundation, the veterinary pharmaceutical industry, and not-for-profit organisations. In 2019, she was awarded the Bancroft Mackerras Medal of Excellence by the Australian Society for Parasitology. In 2015, Prof. Traub founded the Tropical Council for Companion Animal Parasites and currently serves as the President Elect of the Australian Society for Parasitology (President, 2021-2023).

Associate Professor Jane Heller BSc, BVSc(Hons), DipVetClinStud, MVetClinStud, PhD, MANZCVS Associate Head of School /Associate Professor in Veterinary Epidemiology and Public Health, School of Animal and Veterinary Sciences, Charles Sturt University

Professor Peter Irwin BVetMed, PhD, FANZCVS, MRCVS

Emeritus Professor, Murdoch University. Founding Director, Co-Chair and Hon. Treasurer, Tropical Council for Companion Animal Parasites (TroCCAP)

Professor Jacqueline Norris BVSc (Hons), MVS (Melb), PhD, FASM, MASID, Grad Cert Educ Stud (Higher), RCVS (Vet Micro) Professor of Veterinary Microbiology & Infectious Diseases, Associate Head of Research, Sydney School of Veterinary Science, University of Sydney

Professor Rebecca J. Traub BSc, BVMS (Hons), PhD

Professor of Veterinary Parasitology, Faculty of Veterinary and Agricultural Sciences, The University of Melbourne. Founding Director, Tropical Council for Companion Animal Parasites (TroCCAP)

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Companion Animal Zoonoses Guidelines 7

ANTIMICROBIAL RESISTANCE • Antimicrobial resistance (AMR) is a critical global health challenge in human medicine and an emerging problem in companion animal medicine. • In addition to rendering some animal infections more difficult, or even impossible to treat, the development of AMR in pets poses a risk to human health. The close relationship between companion animals and humans facilitates the transfer, directly or indirectly, of shared resistant organisms or genetic determinants. There is potential for bi-directional flow, with the transfer of resistant organisms/ genes from animal-to-human or vice versa, and thus a One Health approach to the problem is essential. • The role and contribution of companion animals to AMR in humans is complex and incompletely understood. It is clear however that antimicrobial use in animals, as in humans, is a risk factor for colonisation or infection with resistant pathogens. Prudent use of antimicrobials by the veterinary profession is an important component of addressing the threat of AMR in animals, and by extension in minimising the contribution animals may play in human AMR. Surveys of companion animal veterinarians and a review of veterinary antimicrobial prescribing practices report the regular use of broad-spectrum antibiotics of high importance to human health, highlighting a need for an increased focus on the principles of prudent use in the profession. 1,2 • The prevalence and impact of AMR varies globally, and not all resistant organisms have a potential zoonotic component. Specific organisms of concern which have a demonstrated or potential involvement of companion animals in their transmission include methicillin-resistant S. aureus (MRSA), methicillin-resistant S. pseudintermedius (MRSP), extended-spectrum beta- lactamase producing Enterobacterales (ESBL-E), carbapenemase-producing Enterobacterales (CPE), and Clostridioides difficile . Antimicrobial resistance in Campylobacter and Salmonella are also a potential zoonotic concern and are discussed in the relevant sections on pages 24 and 71 respectively.

ACAZAP RECOMMENDATIONS

MINIMISING SELECTION FOR RESISTANCE IN ANIMALS • Prescribing veterinarians should follow established guidelines for the prudent use of antimicrobials. The Australian Antibacterial Importance Ratings, developed by the Australian Strategic Technical Advisory Group (ASTAG) on Antimicrobial Resistance, categorises antimicrobials as

of high, medium or low importance. Veterinarians should avoid the use of antimicrobials of high importance in human medicine, such as third generation cephalosporins and fluoroquinolones, where possible. Lower-importance, narrow-spectrum antimicrobials should be used as first line treatment options when antimicrobial agents are deemed clinically necessary.

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8 Companion Animal Zoonoses Guidelines

ACAZAP RECOMMENDATIONS continued

ASTAG ANTIBACTERIAL IMPORTANCE RATING

High Importance: These are essential antibacterials for the treatment or prevention of infections in humans where there are few or no treatment alternatives. These have also been termed “last resort” or “last line” antibacterials.

Medium Importance: There are some alternative antibacterials in different classes available to treat or prevent human infections, but less than for those rated as Low Importance.

Low Importance: There are a reasonable number of alternative antibacterials in different classes available to treat or prevent most human infections even if antibacterial resistance develops.

– Fluoroquinolones, e.g. enrofloxacin, marbofloxacin, pradofloxacin

– Amoxicillin with clavulanic acid

– Amoxicillin/Ampicillin

– Cephalexin/Cephazolin

– Chloramphenicol (topical)

– Fusidic acid (topical)

– Clindamycin

– Doxycycline

– Polymyxin B (topical)

– Gentamicin

– Neomycin

– Third generation cephalosporins, e.g. cefovecin, ceftiofur

– Metronidazole

– Procaine penicillin

Importance ratings for some antibacterials commonly used in dogs and cats

• Antimicrobial prescribing guidelines provide a useful framework to help inform treatment decisions. A range of prescribing guidelines and tools to support prudent antimicrobial use can be found through the AMR Vet Collective.

• Animals should be bathed after visiting hospitals or aged care facilities to minimise the risk of acting as mechanical vectors. Animals with known AMR infections should not be used in animal assisted therapy programs. For additional information see Animals in Care Facilities on page 93. • For animals with documented active AMR infections additional precautions are recommended: - Enhanced infection control should be practiced in the veterinary clinic setting including appropriate isolation and use of PPE (gowns and gloves). Consideration of the pathogen(s) involved and mode of transmission are important in determining the appropriate level of infection control practices (inclusive of PPE and isolation requirements) to be implemented. The AVA Guidelines for Veterinary Industry Personal Biosecurity are a useful resource in this regard. - Owners should be counselled to avoid contacting the infected area. Skin lesions or infections should be covered with impermeable dressings to avoid environmental contamination. - Thorough homecare instructions should be provided, specifically regarding wound management and environmental cleaning. - Contact should be minimised with other animals in the household. - Animal faeces should be promptly collected and disposed of.

• Culture and susceptibility (C&S) results should be used to guide antimicrobial choice whenever possible. If broad-spectrum higher-importance antimicrobial therapy is implemented in critical patients, de-escalation of antimicrobial therapy should occur if indicated when C&S results are available. Clinicians need to reconsider duration of therapy to match the clinical needs of the patient. • Veterinarians should discuss with owners the importance of antimicrobials to human and animal health and the need to preserve their efficacy through prudent use. Veterinarians should reinforce to pet owners the importance of following the directions for use of any prescribed antimicrobial. MINIMISING TRANSFER OF RESISTANT ORGANISMS BETWEEN PETS AND PEOPLE • Good infection control practices are essential to help prevent transmission of potentially zoonotic bacteria between pets and people, whether AMR or not. This encompasses not only hand hygiene but also regular cleaning of contaminated surfaces, as a failure to do either may contribute to transmission of resistant organisms.

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Companion Animal Zoonoses Guidelines 9

Staphylococcus spp.

Staphylococci are gram-positive cocci frequently found as commensals on the skin and mucous membranes of mammals and birds. They may also act as opportunistic pathogens, particularly in animals with predisposing conditions, resulting in localised and invasive disease. More than 40 species are described, which are broadly divided into coagulase-positive and coagulase- negative organisms, with the former more commonly associated with infection than the latter. 3 Staphylococci display different host specificities, although cross-species transmission is common. Staphylococcus pseudintermedius • Staphylococcus pseudintermedius is a common organism colonising cutaneous and mucocutaneous surfaces in dogs and cats. Like other coagulase-positive staphylococci, colonisation is more commonly seen at mucocutaneous surfaces rather than skin. Staphylococcus pseudintermedius is more frequently isolated from dogs than cats, where S. felis is more common. Staphylococcus pseudintermedius colonisation or infection is uncommon in humans. • Carriage rates of S. pseudintermedius in healthy dogs in Australia have been reported from 85.5% (rural Victoria) 4 to 46.2% (remote NSW) 5 , and are similar to those from other countries. Carriage rates are highest in the nose, mouth and perineum. 6 In cats, carriage rates of 8.8% (remote NSW) have been reported. 5 Carriage is not typically associated with clinical signs, however opportunistic infections may occur, particularly cutaneous infections where it is the predominant pathogen in over 90% of cases of pyoderma. 7 • Methicillin-resistance in S. pseudintermedius is a more recent phenomenon than in S. aureus, with the first reports in Australian dogs in 2014. 8 Methicillin-resistant S. pseudintermedius (MRSP) isolates have however been identified in archived samples in Australia dating back to 1999 (USYD archives, J. Norris, unpublished data). MRSP isolates are frequently resistant to a broad range of antimicrobials, including fluoroquinolones. As with S. aureus, resistance to beta-lactam antimicrobials in S. pseudintermedius is usually due to the presence of the mecA gene (which encodes penicillin-binding protein 2a [PBP2a]). • Prevalence of MRSP varies depending on study population and methods. MRSP carriage in dogs in Queensland is reported as 8.7% versus 0% in cats. 9 A study from Sydney reported a similar finding, with MRSP carriage in 7% of client owned dogs, 8% of dogs owned by veterinary personnel, and 0% of cats. 10 Studies in remote Indigenous communities failed to identify MRSP in sampled dogs and cats, likely associated with limited access to veterinary care and use of antimicrobials in these communities. 5,11 • Carriage of MRSP is not associated with clinical signs, however opportunistic infections may result in disease. In Australia, 11.8% of S. pseudintermedius submissions from clinical infections were MRSP, with resistant isolates most commonly associated

with skin and soft-tissue infections and surgical site infections. 12 Overseas it is reported that up to 65% of S. pseudintermedius pyoderma cases are methicillin-resistant. 13 • Transmission of MRSP from colonised or infected companion animals to humans has been reported but it is thought to be uncommon, with carriage in humans relatively short lived. 14 • Staphylococcus pseudintermedius has been reported in up to 4% of owners of healthy dogs or cats based upon nasal swabbing, with carriage associated with rare or infrequent hand washing after handling pets. 15 • Infection with S. pseudintermedius in humans is rare, most commonly involving local infection of bite wounds. More severe manifestations including bacteraemia, endocarditis, pneumonia, brain abscesses, and otitis have been rarely reported. 16

Perineum-rectum 52% (28-72%)

Nose 31% (16-64%)

Mouth 57% (42-74%)

Groin 23% (16-38%)

Estimated carriage rates of Staphylococcus pseudintermedius at different body sites in dogs. Ranges are indicated in parentheses for each site Adapted from Bannoehr et al (2012). 6

Staphylococcus pseudintermedius is the most common pathogen associated with canine pyoderma

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10 Companion Animal Zoonoses Guidelines

Staphylococcus spp. continued

Staphylococcus aureus • Staphylococcus aureus is a cutaneous and mucocutaneous commensal in humans with approximately 30% of the human population thought to be asymptomatic carriers. 17 Three patterns of colonisation are recognised in humans: persistent colonisation, intermittent colonisation, and non-carriers. • Methicillin-resistant S. aureus (MRSA) is a significant and growing public health concern. Up to 3% of the general population may carry MRSA, predominantly in the nasal passages. Higher rates of carriage are reported in veterinarians, with a 5-fold higher prevalence in veterinarians working with dogs and cats than those with minimal animal contact. 18 • In humans, a range of presentations of MRSA infection may be seen. Localised infection is more common in people with underlying medical conditions – e.g. peripheral vascular disease or diabetes, and/or a history of hospitalisation. The strains causing this form of infection are usually hospital and long-term care facility associated strains (HA-MRSA). Sequence types ST22 and ST293 are the most prevalent in Australia. Invasive infection usually occurs when an MRSA colonised patient has an invasive procedure and sometimes follows cannulation and secondary line infection. Hence the focus of care is to reduce secondary complications of colonisation, using pre-operative decolonisation and prophylaxis and infection control management to prevent transmission in hospital. More recently, strains of MRSA causing recurrent localised and invasive infections in the community, have become more prevalent. These strains carry an associated virulence factor (PVL) which may enhance pyogenic potential. In Australia, ST93 is the most common. These strains may occur in patients without underlying diseases, including children, and are referred to as community-associated (CA-MRSA) strains. Decolonisation (e.g. using topical decolonisation with nasal mupirocin and chlorhexidine washes) is often used to prevent recurrent infection and intra-familial spread. • Isolation of S. aureus in healthy dogs is considerably less common than S. pseudintermedius . One study from rural

Victoria reported a prevalence of 14.5%, 4 with most of these animals having dual carriage with S. pseudintermedius. This study reported S. aureus isolation more commonly in female dogs. Another study in Australia reported a prevalence of 4.3% in dogs and 3.8% in cats in remote NSW. 5 Carriage of S. aureus in dogs may represent transient colonisation from cohabitating humans. In 50% of households where S. aureus was isolated from both dog and human, the strains were indistinguishable. 15 Interspecies transmission is evident, and although the direction of transfer is not certain, given the strains involved, this is likely to represent human-to- animal transmission. As with S. pseudintermedius, carriage of S. aureus is generally not associated with clinical signs, however opportunistic infections may occur. • MRSA carried by dogs are generally human adapted lineages. Several studies have failed to detect MRSA carriage in healthy urban pet dogs, while two studies in dogs from remote communities in NSW and WA have shown a carriage rate of 2.6%, with the sequence types isolated in dogs reflecting the prominent types present in the local human population. 9-11,19 The increased prevalence of MRSA carriage in these dogs likely reflects the comparatively high rate of carriage of MRSA among their owners. A study in healthy pet cats in Brisbane failed to detect MRSA. 9 • In other studies, being owned by human healthcare workers or being part of a hospital visitation program are risk factors for MRSA carriage in dogs, identifying that the carriage rate in pets reflects the prevalence in humans in their environment. • Most animals that carry MRSA have no clinical signs, however opportunistic infections may occur. MRSA infection is reported with increasing frequency in companion animals, and is associated with a range of different infections including skin and soft tissue infection, pneumonia, urinary tract infections, and surgical wound infections. Sequence types isolated often correspond to locally prevalent human strains. Nosocomial outbreaks are also reported. 20

ACAZAP RECOMMENDATIONS

dogs and cats may be a source of infection for humans. To reduce the risk of transmission, owners should minimise contact with areas most likely to harbour the organism, cover open wounds and practice good hand hygiene. • There are no validated methods for decolonisation of pets, and therefore this approach is not recommended. In most cases MRSA in dogs and cats will be a result of human-to-animal transmission and colonisation or carriage is likely to be transient. • Screening of dogs and cats for MRSA is generally not recommended, unless part of an overall strategy to manage recurrent MRSA in people. The clinical implications of carriage in pets may be low.

• Resistant skin infections in companion animals are more likely to be MRSP than MRSA, and while MRSP can be transmitted to humans (particularly if there are any predisposing risk factors such as breaks in the skin etc.) it is unlikely. To reduce risk of transmission, owners should minimise contact with areas most likely to harbour S. pseudintermedius (e.g. nose, mouth, or perineum), cover open wounds and practice good hand hygiene. • Dogs and cats are not primary reservoirs of S. aureus and colonisation is usually transient. The nose and perineum are high risk sites in pets. Colonisation will usually clear within a few weeks providing re-infection from a common source does not occur. Despite the generally transient nature of colonisation,

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Companion Animal Zoonoses Guidelines 11

Enterobacterales

animals is low and therefore transmission to, and carriage in dogs and cats is likely to be very uncommon. 26,27

Enterobacterales is an order of gram-negative bacterial rods comprising seven recognised families, including the family Enterobacteriaceae. 21 Enterobacteriaceae includes the genera Escherichia, Klebsiella, and Salmonella, with many species normal inhabitants of the gastrointestinal tract of mammals. These organisms may however cause opportunistic infections in susceptible patients or when spread to locations outside the gastrointestinal tract. Some Enterobacteriaceae (e.g. Salmonella sp., Shigella sp.) are primary enteric pathogens. Extended-spectrum beta-lactamase producing Enterobacterales (ESBL-E) • By virtue of their location, commensal gastrointestinal organisms are exposed to selection pressure from orally administered antimicrobials and are a potential source of resistance genes. A growing concern in veterinary and human medicine are organisms producing extended-spectrum beta- lactamases (ESBLs), enzymes which hydrolyse and render inactive third generation cephalosporins. As ESBL resistance is carried on a plasmid, this can be easily transferable to other species of Enterobacterales. Presence on plasmids allows for the accumulation of other resistance factors. Hence ESBL resistance is frequently associated with co-resistance to other classes of antimicrobials, including fluoroquinolones and aminoglycosides. • In humans the most common species carrying ESBL enzymes are E. coli, Klebsiella pneumoniae and Enterobacter cloacae. Presence of ESBL enzymes in Salmonella species is also a concern as this has considerable zoonotic potential. • ESBL-E are a very uncommon cause of disease in dogs and cats in Australia. 22 • Eating raw meat and recent antimicrobial treatment has been reported overseas as a risk factor for carriage of ESBL-E in dogs, 23,24 and a study of commercially available raw food diets for dogs in Sweden found E. coli in all tested samples (n=39), with ESBL isolated from 23%. 25 Owing to differences in antimicrobial prescribing and animal husbandry in Australia compared to other regions, the prevalence of ESBL-E in Australian production

Carbapenemase-producing Enterobacterales (CPE) • Carbapenems are beta-lactam antimicrobials frequently used as a last-line treatment for severe infections in human medicine. Consequently, they are classified as highly important antimicrobials. Carbapenemase-producing Enterobacterales (CPE) are of increasing concern worldwide as the presence of these enzymes may render the organism virtually untreatable with currently available antibiotics. Because of concern for spread, CPE incidence in human infection in Australia is reportable. • CPE have not been reported in dogs in Australia, and there is a single report of carbapenem resistant Salmonella enterica isolated from a systemically unwell cat and three cohabitating cats in the same facility. 28 The off-label use of carbapenems in dogs and cats is uncommon in Australia, with a review of over 4 million consultations, including almost 600,000 antimicrobial prescribing events failing to identify the use of this class of antimicrobial. 2 Despite this, CPE may develop in the absence of carbapenem use through co-selection of carbapenem-resistance associated with the use of other antimicrobials. • Human CPE infections are mostly associated with prolonged hospitalisation and underlying diseases. Infections with enzymes such as KPC can result in up to 50% mortality. Enzymes such as NDM and OXA-48 have become increasingly prevalent, especially in parts of South and East Asia. All patients who have been recently hospitalised overseas are screened on admission in Australia, in order to avoid transmission and potential outbreaks. • Occurrence in Australia is still relatively uncommon, with less than 1% prevalence in surveillance studies of blood-stream infections, 29 but some enzymes such as IMP-4 are locally endemic and have been found in environmental sources such as hospital drains and waste-water and in cats and wild birds in Australia. 28,30

ACAZAP RECOMMENDATIONS

• Good hand hygiene is essential following contact with animals, animal food or treats, food bowls, animal bedding and animal faeces. • Currently there is no known role of dogs and cats in transmission of CPE in Australia, however the possibility for human-to-animal transmission exists.

• Although the risk of ESBL-E in raw meat in Australia is very low, due to the risk of transmission of other potential pathogens (e.g. Campylobacter, Salmonella), it is recommended to avoid feeding raw meat diets to dogs and cats, or if fed, consider the potential for zoonotic infection through contact with the diet or the faeces of animals which have consumed the diet.

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12 Companion Animal Zoonoses Guidelines

Clostridioides difficile

• Clostridioides difficile is a gram-positive anaerobe and the most common cause of hospital-acquired antimicrobial diarrhoea in people. Clostridioides difficile infection (CDI) is related to toxin production, not the mere isolation of the organism in culture or by molecular testing. Different strains are identified that vary in virulence due to differential production of toxins. • Clostridioides difficile has been isolated from healthy dogs and cats, and those with diarrhoea. Globally, carriage of C. difficile in healthy adult dogs has been reported to be between 0-6%. 31 Carriage rates in healthy cats are thought to be similar to dogs. 31,32 • Higher rates of carriage are reported in dogs that visit human hospitals, have contact with children, or reside with immunocompromised owners. Recent hospitalisation or out- patient veterinary care, and treatment with antimicrobials is also associated with increased carriage. 31

• The role of C. difficile in infectious canine and feline gastrointestinal disease is unclear.

• There is low prevalence of C. difficile in healthy humans (except neonates, where C. difficile carriage is not uncommon), with increased risk of carriage of toxin positive strains and secondary C. difficile colitis associated with prolonged hospitalisation and prior antimicrobial therapy. • Disease in humans may range from mild to fulminant and potentially fatal pseudomembranous colitis or toxic megacolon. • Some strains are found in both humans and dogs suggesting interspecies transmission, however the direction of transmission is unclear (animal-to-human or vice versa).

ACAZAP RECOMMENDATIONS

• All diarrhoeic animals should be considered potential sources of transmission and appropriate infection control procedures implemented.

• The zoonotic potential of C. difficile is unclear, and infection in cohabitating companion animals and humans may represent zoonotic transmission or a

common source of exposure.

KEY CONSIDERATIONS 1. A One Health approach is essential in tackling the issue of AMR as bi-directional cross-species transmission of organisms/genes from animal-to-human or vice versa may occur. 2. Good hand hygiene practices following contact with animals, animal food or treats, food bowls, animal bedding and animal faeces can minimise the zoonotic transmission of AMR. Additional precautions should be taken, both

in the clinic and home environment, for animals with documented AMR infections. 3. The primary drivers of AMR are antimicrobial use and poor infection control practices. - Veterinarians should follow prudent use guidelines and avoid where possible the use of antimicrobials of high importance, such as fluroquinolones and third generation cephalosporins. - Clinics should have agreed and documented infection control practices that consider hand hygiene, environmental hygiene, and the appropriate use of PPE.

The primary drivers of AMR are antimicrobial use and poor infection control practices.

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Companion Animal Zoonoses Guidelines 13

References: 1. Norris, J.M., et al (2019) Factors influencing the behaviour and perceptions of Australian veterinarians towards antibiotic use and antimicrobial resistance. PLoS One, 14(10), e0223534. 2. Hur, B.A., et al (2020) Describing the antimicrobial usage patterns of companion animal veterinary practices; free text analysis of more than 4.4 million consultation records. PLoS One, 15(3), e0230049. 3. Gherardi, G., et al (2018), Staphylococcal taxonomy. In: Pet-To-Man Travelling Staphylococci. Elsevier. 1-10. 4. Bean, D.C., et al (2016) Carriage rate and antibiotic susceptibility of coagulase-positive staphylococci isolated from healthy dogs in Victoria, Australia. Aust Vet J, 94(12), 456-460. 5. Ma, G.C., et al (2020) Commensal staphylococci including methicillin-resistant Staphylococcus aureus from dogs and cats in remote New South Wales, Australia. Microb Ecol, 79(1), 164-174. 6. Bannoehr, J., et al (2012) Staphylococcus pseudintermedius in the dog: taxonomy, diagnostics, ecology, epidemiology and pathogenicity. Vet Dermatol, 23(4), 253-66, e51-2. 7. Lynch, S.A., et al (2021) The complex diseases of Staphylococcus pseudintermedius in canines: where to next? Vet Sci, 8(1). 8. Siak, M., et al (2014) Characterization of meticillin-resistant and meticillin-susceptible isolates of Staphylococcus pseudintermedius from cases of canine pyoderma in Australia. J Med Microbiol, 63(Pt 9), 1228-1233. 9. Rynhoud, H., et al (2021) Epidemiology of methicillin resistant Staphylococcus species carriage in companion animals in the Greater Brisbane Area, Australia. Res Vet Sci, 136, 138-142. 10. Worthing, K.A., et al (2018) Methicillin-resistant staphylococci amongst veterinary personnel, personnel-owned pets, patients and the hospital environment of two small animal veterinary hospitals. Vet Microbiol, 223, 79-85. 11. Ma, G.C., et al (2020) Molecular characterization of community-associated methicillin-resistant Staphylococcus aureus from pet dogs. Zoonoses Public Health, 67(3), 222-230. 12. Saputra, S., et al (2017) Antimicrobial resistance in coagulase-positive staphylococci isolated from companion animals in Australia: A one year study. PLoS One, 12(4), e0176379. 13. Kawakami, T., et al (2010) Antimicrobial susceptibility and methicillin resistance in Staphylococcus pseudintermedius and Staphylococcus schleiferi subsp. coagulans isolated from dogs with pyoderma in Japan. J Vet Med Sci, 72(12), 1615-9. 14. van Duijkeren, E., et al (2011) Transmission of methicillin-resistant Staphylococcus pseudintermedius between infected dogs and cats and contact pets, humans and the environment in households and veterinary clinics. Vet Microbiol, 150(3-4), 338-43. 15. Hanselman, B.A., et al (2009) Coagulase positive staphylococcal colonization of humans and their household pets. Can Vet J, 50(9), 954-8. 16. Starlander, G., et al (2014) Cluster of infections caused by methicillin-resistant Staphylococcus pseudintermedius in humans in a tertiary hospital. J Clin Microbiol, 52(8), 3118-20. 17. Verhoeven, P.O., et al (2014) Detection and clinical relevance of Staphylococcus aureus nasal carriage: an update. Expert Rev Anti Infect Ther, 12(1), 75-89.

18. Jordan, D., et al (2011) Carriage of methicillin-resistant Staphylococcus aureus by veterinarians in Australia. Aust Vet J, 89(5), 152-9. 19. Rusdi, B., et al (2018) Carriage of critically important antimicrobial resistant bacteria and zoonotic parasites amongst camp dogs in remote Western Australian indigenous communities. Sci Rep, 8(1), 8725. 20. Wieler, L.H., et al (2011) Methicillin-resistant staphylococci (MRS) and extended-spectrum beta-lactamases (ESBL)-producing Enterobacteriaceae in companion animals: nosocomial infections as one reason for the rising prevalence of these potential zoonotic pathogens in clinical samples. Int J Med Microbiol, 301(8), 635-41. 21. Adeolu, M., et al (2016) Genome-based phylogeny and taxonomy of the 'Enterobacteriales': proposal for Enterobacterales ord. nov. divided into the families Enterobacteriaceae, Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam. nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceae fam. nov. Int J Syst Evol Microbiol, 66(12), 5575-5599. 22. Salgado-Caxito, M., et al (2021) Global prevalence and molecular characterization of extended- spectrum beta-lactamase producing- Escherichia coli in dogs and cats - A scoping review and meta-analysis. One Health, 12, 100236. 23. Wedley, A.L., et al (2017) Carriage of antimicrobial resistant Escherichia coli in dogs: Prevalence, associated risk factors and molecular characteristics. Vet Microbiol, 199, 23-30. 24. van den Bunt, G., et al (2020) Faecal carriage, risk factors, acquisition and persistence of ESBL- producing Enterobacteriaceae in dogs and cats and co-carriage with humans belonging to the same household. J Antimicrob Chemother, 75(2), 342-350. 25. Nilsson, O., (2015) Hygiene quality and presence of ESBL-producing Escherichia coli in raw food diets for dogs. Infect Ecol Epidemiol, 5, 28758. 26. Abraham, S., et al (2015) First detection of extended-spectrum cephalosporin- and fluoroquinolone-resistant Escherichia coli in Australian food-producing animals. J Glob Antimicrob Resist, 3(4), 273-277. 27. van Breda, L.K., et al (2018) Antibiotic resistant Escherichia coli in southeastern Australian pig herds and implications for surveillance. Zoonoses Public Health, 65(1), e1-e7. 28. Abraham, S., et al (2016) Isolation and plasmid characterization of carbapenemase (IMP-4) producing Salmonella enterica Typhimurium from cats. Sci Rep, 6, 35527. 29. Australian Group on Antimicrobial Resistance (2019) Gram-negative sepsis outcome program: 2019 Report. https://agargroup.org.au/agar-surveys#Gram-Negative-Bacteria. 30. Dolejska, M., et al (2016) High prevalence of Salmonella and IMP-4-producing Enterobacteriaceae in the silver gull on Five Islands, Australia. J Antimicrob Chemother, 71(1), 63-70. 31. Weese, J.S., (2020) Clostridium (Clostridioides) difficile in animals. J Vet Diagn Invest, 32(2), 213-221. 32. Kachrimanidou, M., et al (2019) Clostridioides (Clostridium) difficile in food-producing animals, horses and household pets: A comprehensive review. Microorganisms, 7(12).

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14 Companion Animal Zoonoses Guidelines

Bordetella bronchiseptica • Bordetella bronchiseptica is a respiratory pathogen of a range of wild and domestic animals. It is a common primary pathogen of canine infectious respiratory disease complex (CIRDC) and a causative agent in feline upper respiratory tract disease. • Bordetella bronchiseptica is closely related to the host-specific human pathogens B. pertussis (the cause of whooping cough) and B. parapertussis.

ACAZAP RECOMMENDATIONS

• Good hand hygiene following animal contact or work in animal facilities is essential. • Advise owners on the potential zoonotic risk of kissing animals or allowing them to lick faces. • Acquisition of animals with a lower likelihood of B. bronchiseptica carriage (older, from low population density environments) should be considered for at risk individuals. • Good ventilation and air exchange are essential in animal care facilities (e.g. kennels and shelters) to minimise expose of staff

and animals in the facility to infectious aerosols produced by infected (clinical or asymptomatic) dogs. • Vaccination of dogs using mucosal (oral or intranasal) vaccines to reduce likelihood of shedding is recommended. • Although confirmed disease from modified live canine B. bronchiseptica vaccines has not been reported in humans, prudent practice would ensure immunocompromised individuals are not present at the time of vaccination. Oral vaccination is likely to result in reduced aerosolisation compared to intranasal administration.

IN ANIMALS

Bronchoalveolar lavage cytology (Diff-Quik stained) from a dog infected with B. bronchiseptica showing numerous coccobacilli adhered to the cilia of columnar epithelial cells (Courtesy of Prof. Michael Scott, Michigan State University)

AETIOLOGY AND EPIDEMIOLOGY • Bordetella bronchiseptica is a gram-negative aerobic coccobacillus found in a range of animals where it is associated primarily with upper respiratory tract infections. In severe cases B. bronchiseptica may be involved in lower respiratory tract infections, albeit rarely. • Although frequently isolated from healthy animals, B. bronchiseptica is not part of the normal flora. Prolonged

carrier status is common in dogs and cats following clinical or subclinical infection. The organism colonises the ciliated respiratory epithelium, inducing paralysis of the mucociliary apparatus (ciliostasis) rendering the respiratory tract susceptible to secondary bacterial colonisation and subsequent inflammation. 1 • Dogs and cats are infected through oronasal exposure (direct or indirect) to infectious respiratory secretions from shedding animals.

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15 Companion Animal Zoonoses Guidelines

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