Food animals are a well-established source of antibiotic-resistant bacteria that can transfer to humans via the food chain. However, bacteria may also transfer from animals to humans via direct contact and indirect contact via contaminated fomites. This may be particularly relevant for companion animals, as they often share a close environment with human family household members. The aim of this talk is to highlight the current knowledge on transmission of antimicrobial-resistant bacteria between pets (dogs and cats) and humans within family households. Furthermore, examples of the occupational risk faced by small animal practitioners will be given. The focus of the talk will be methicillin-resistant staphylococci as typical skin colonizers, and extended­spectrum beta-lactamase (ESBL)-producing Escherichia coli that occur in the gastrointestinal tract.

Staphylococcus aureus is an opportunistic pathogen colonizing different hosts including humans, and less commonly pets. Methicillin-resistant isolates (MRSA) have the mecA gene conferring resistance to all beta­lactams, and in addition they are frequently resistant to other drug classes. MRSA isolates in pets mostly belong to genetic lineages adapted to humans, for example sequence type (ST)22, which is a well-established human healthcare-associated clone. The presence of the same clones suggests that transmission may occur, and case­based studies^2,3 have indeed proved transmission between pets and humans living in the same household. A recent phylogenetic study⁴ showed that human MRSA ST22 isolates from the UK are more ancient than pet isolates, thus indicating humans as the original source. Nevertheless, transmission may occur in both directions, and pets may serve as a source of infection or (re)colonization of human patients with MRSA.

Staphylococcus pseudintermedius is adapted to pets, in particular dogs, and rarely colonizes humans. Accordingly, occurrence of this bacterium in humans indicates direct or indirect transmission from a pet. Over the recent decade, methicillin-resistant isolates (MRSP) have emerged globally in dogs. MRSP is similar to MRSA in certain ways, as the resistance gene (mecA) is the same, and the bacterium spreads by clonal dissemination. Various case-based studies have shown transmission of MRSP from pets to humans in close contact.^5,6 One study⁷ showed frequent dissemination of MRSP to the near environment of infected pets and their animal contacts, whereas transmission to human contacts was a relatively rare phenomenon.

Escherichia coli is a ubiquitous bacterium colonizing the intestinal tract of both humans and animals. The bacterium can become resistant to most beta-lactams upon acquisition of an ESBL gene. There are hundreds of different ESBL genes. These are often located on plasmids that can transfer readily to other E. coli strains and to other bacterial species. Accordingly, transmission of ESBL-producing E. coli is a complex phenomenon that is difficult to investigate as it can occur both at the plasmid and clonal level. Several studies have shown sharing of (non-ESBL) E. coli clones between pets and humans living in same households.^8,9 Furthermore, it is well established that (i) some of the most common ESBL genes in humans (e.g., blaCTX-M-15) also predominate in pets, (ii) indistinguishable plasmids harbouring ESBL genes occur in pets and humans, and (iii) certain ESBL-producing clones such as ST131 occur in both hosts. Nevertheless, so far only one study¹⁰ has provided evidence of transmission of ESBL­producing E. coli clones between dogs and humans within family households.

Apart from the phenotypes listed above, several other antimicrobial-resistant bacteria with zoonotic potential occur in pets. Examples of these will be mentioned at the talk including colistin-resistant E. coli. This bacterium is particularly "hot news" as colistin represents a last-choice treatment for some of the most resistant Gram-negative bacteria in human medicine, and a recently discovered plasmid-borne colistin resistance gene favors its rapid dissemination.

In conclusion, pets are potential sources of important resistant bacteria occurring in human medicine, and several case-based studies have proven direct or indirect transmission between the two hosts. However, very little is known about the extent of transmission from pets to humans in close contact. There is therefore a need for other types of studies to clarify this, for example (i) case­control studies assessing if contact to, or ownership of pets, is a risk factor for colonization or infection with antibiotic-resistant bacteria, and (ii) longitudinal studies assessing the dynamics of bacterial shedding and transmission over time.

References

1.  Damborg P, Broens EM, Chomel BB, Guenther S, Pasmans F, Wagenaar JA, Weese JS, Wieler LH, Windahl U, Vanrompay D, Guardabassi L. Bacterial zoonoses transmitted by household pets: state-of-the-art and future perspectives for targeted research and policy actions. Journal of Comparative Pathology. 2016;155(1Suppl 1):S27–40.

2.  van Duijkeren E, Wolfhagen MJ, Box AT, Heck ME, Wannet WJ, Fluit AC. Human-to-dog transmission of methicillin-resistant Staphylococcus aureus. Emerging Infectious Diseases. 2004;10(12):2235–7.

3.  Weese JS, Dick H, Willey BM, McGeer A, Kreiswirth BN, Innis B, Low DE. Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Veterinary Microbiology. 2006;115(1–3):148–55.

4.  Harrison EM, Weinert LA, Holden MT, Welch JJ, Wilson K, Morgan FJ, Harris SR, Loeffler A, Boag AK, Peacock SJ, Paterson GK, Waler AS, Parkhill J, Holmes MA. A shared population of epidemic methicillin-resistant Staphylococcus aureus 15 circulates in humans and companion animals. MBio. 2014;5(3):e00985-13.

5.  Soedarmanto I, Kanbar T, Ülbegi-Mohyla H, Hijazin M, Alber J, Lämmler, C, Akineden O, Weiss R, Moritz A, Zschöck M. Genetic relatedness of methicillin-resistant Staphylococcus pseudintermedius (MRSP) isolated from a dog and the dog owner. Research in Veterinary Science. 2011;91(3):e25-7.

6.  van Duijkeren E, Houwers DJ, Schoormans A, Broekhuizen-Stins MJ, lkawaty R, Fluit AC, Wagenaar JA. Transmission of methicillin-resistant Staphylococcus intermedius between humans and animals. Veterinary Microbiology. 2008;128(1–2):213–5.

7.  van Duijkeren E, Kamphuis M, van der Mije IC, Laarhoven LM, Duim B, Wagenaar JA, Houwers DJ. Transmission of methicillin-resistant Staphylococcus pseudintermedius between infected dogs and cats and contact pets, humans and the environment in households and veterinary clinics. Veterinary Microbiology. 2011;150(3–4):338–43.

8.  Damborg P, Nielsen SS, Guardabassi L. Escherichia coli shedding patterns in humans and dogs: insights into within-household transmission of phylotypes associated with urinary tract infections. Epidemiology and Infection. 2009;137(10):1457–64.

9.  Stenske KA, Bemis DA, Gillespie BE, D’Souza DH, Oliver SP, Draughon FA, Matteson KJ, Bartges JW. Comparison of clonal relatedness and antimicrobial susceptibility o f fecal Escherichia coli from healthy dogs and their owners. American Journal of Veterinary Research. 2009;70(9):1108–16 .

10.  Ljungquist O, Ljungquist D, Myrenås M, Rydén C, Finn M, Bengtsson B. Evidence of household transfer of ESBL-/pAmpC-producing Enterobacteriaceae between humans and dogs - a pilot study. Infection Ecology & Epidemiology. 2016;6:31514.