carriage in UK veterinary staff and owners of infected pets: new risk groups

Journal of Hospital Infection (2009) -, 1e7 Available online at www.sciencedirect.com www.elsevierhealth.com/journals/jhin Meticillin-resistant Staphylococcus aureus carriage in UK veterinary staff and owners of infected pets: new risk groups A. Loeffler a, *, D.U. Pfeiffer a, D.H. Lloyd a, H. Smith a, R. Soares-Magalhaes a, J.A. Lindsay b a Department of Veterinary Clinical Sciences, Royal Veterinary College, Hatfield, North Mymms, Hertfordshire, UK b Centre for Infection, Department of Cellular and Molecular Medicine, St George s, University of London, London, UK Received 5 June 2009; accepted 25 September 2009 KEYWORDS Meticillin-resistant Staphylococcus aureus; Nasal carriage; Pet owners; Risk groups; Veterinary staff Summary Meticillin-resistant Staphylococcus aureus (MRSA) nasal carriage on admission to hospital remains one of the most important risk factors for subsequent infection. Identification of high risk groups for MRSA carriage is vital for the success of infection control programmes. Veterinary staff may be one such risk group but little is known about pet owners and the role of contact with infected pets. As part of a UK-wide caseecontrol study investigating risk factors for MRSA infection in dogs and cats between 2005 and 2008, 608 veterinary staff and pet owners in contact with 106 MRSA and 91 meticillin-susceptible S. aureus (MSSA)-infected pets were screened for S. aureus nasal carriage. Laboratory isolation and characterisation included salt broth enrichment, standard and automated microbiological tests, demonstration of the S. aureus-specific thermonuclease gene (nuc) and of meca, and polymerase chain reaction-based lineage characterisation. MRSA carriage was 12.3% in veterinarians attending MRSA-infected animals and 7.5% in their owners. In the MSSA control group, MRSA carriage was 4.8% in veterinary staff and 0% in owners. Veterinary staff carried MRSA more frequently than owners (odds ratio: 2.33; 95% confidence interval: 1.10e4.93). All MRSA from humans and all but one animal MRSA were CC22 or CC30, typical for hospital MRSA in the UK. This study indicates for the first time an occupational risk for MRSA * Corresponding author. Address: Department of Veterinary Clinical Sciences, Royal Veterinary College, Hawkshead Lane, Hatfield, North Mymms, Hertfordshire AL9 7TA, UK. Tel.: þ44 1707 666246; fax: þ44 1707 666298. E-mail address: aloeffler@rvc.ac.uk 0195-6701/$ - see front matter ª 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.jhin.2009.09.020

2 A. Loeffler et al. carriage in small animal general practitioners. Veterinary staff and owners of MRSA-infected pets are high risk groups for MRSA carriage despite not having direct hospital links. Strategies to break the cycle of MRSA infection must take these potential new reservoirs into account. ª 2009 The Hospital Infection Society. Published by Elsevier Ltd. All rights reserved. Introduction Meticillin-resistant Staphylococcus aureus (MRSA) remains a common cause of hospital-acquired infection even though the number of reported bloodstream infections for England has recently been falling. However, without knowing the reservoirs of MRSA, our ability to design effective control measures is compromised. The natural habitat of S. aureus, irrespective of its antimicrobial resistance pattern, is the human nares with 20% of the population permanently colonised and another 60% transiently colonised. 1 Nasal S. aureus carriers are up to ten times more likely to develop S. aureus infection than non-carriers and genetic analyses of S. aureus carriage and infection isolates have shown that more than 80% of hospitalacquired S. aureus infections were caused by endogenous strains carried nasally by the patient. 2,3 In addition, nasal carriage is highly relevant for successful transmission and survival of MRSA. It is regularly shed from nasal carriage sites and primarily spread by hand contact to patients, to other potential carriers, or into the environment. 4,5 The proportion of carriage isolates that are MRSA is largely unknown despite the high profile campaigns to reduce MRSA in many countries including the UK. In the UK, only three studies have investigated community prevalence. One identified 1.5% carriage among 274 people aged >16 years in 2001; two other studies both found 0.8% MRSA carriage among 258 and 962 people aged >65 years in 2002 and 2004. 6e8 In other countries with a high burden of hospital-associated MRSA infections such as the USA, Portugal and Italy, MRSA carriage in the healthy population is usually <1.5%. 9e11 Certain risk groups have higher carriage rates, typically those exposed to healthcare-related risk factors. In the UK and Ireland, several small studies found that 5e15% of hospitalised patients and that 9e22% of nursing or care home residents carried MRSA. 12e17 Healthcare workers have long been recognised as potential vectors and a recent meta-analysis found that 5% of healthcare workers worldwide were MRSA positive with UK/Ireland rates slightly higher at 7e8%. 14,18,19 Over the past 10 years, MRSA has emerged as an important pathogen in small animal veterinary practice worldwide. 20,21 Of particular concern are potential zoonotic implications as there is often a very close relationship between owners and their pets. Healthy animal carriers have been associated with transfer of MRSA to humans, and infected pets may present an even greater risk to susceptible humans. Whereas Staphylococcus pseudintermedius (formerly Staphylococcus intermedius) remains the predominant staphylococcal pathogen in dogs and cats, S. aureus is not an uncommon commensal and pathogen of small animals. 22e24 Pets frequently carry staphylococci on skin and mucosae (30e70%) and more than 14% have been S. aureus. 25,26 In addition, most small animal veterinarians will encounter staphylococcal infections on a daily basis and up to 10% of those are reported to be S. aureus. 27 Furthermore, typing studies from various countries have shown MRSA isolated from dogs and cats are typically indistinguishable from hospital-associated MRSA lineages dominant in each particular country. 21,28,29 The genetic relatedness of these human and animal MRSA supports transfer between hosts and highlights the need for integrated epidemiological research of this primarily human-hospital-associated pathogen. The presented study describes the screening of veterinary staff and owners of infected pets for MRSA nasal carriage as part of an investigation into risk factors for MRSA infection in dogs and cats. As in medical staff, frequent MRSA carriage at 18e27% has been reported among veterinarians working in UK animal referral hospitals but the prevalence in small animal general practitioners remains largely unquantified. 28,29 Methods Study design and identification of participants UK veterinary staff and owners (excluding Northern Ireland) closely handling dogs and cats infected with either MRSA or meticillin-susceptible

MRSA in vets and owners of infected pets 3 S. aureus (MSSA) were invited to submit nasal swabs for MRSA carriage screening. Recruitment was based on identification and enrolment of dogs and cats with S. aureus infection from clinical material submitted to a veterinary diagnostic laboratory (IDEXX Laboratories, Wetherby, UK) for bacterial culture and antimicrobial susceptibility testing. Submitting veterinary surgeons were telephoned by the authors and participation was invited from up to two members of veterinary staff and up to two owners who had had close contact with the infected pet during the time of sampling or disease. Owners were recruited via their veterinary surgeon. Supportive study material including consent forms, participant information sheets summarising background and purpose of the study, swabs and a sampling protocol were posted to the practices. Another two reminder phone calls per practice were scheduled at fortnightly intervals to improve compliance. Full details of the enrolment protocol for animals, the risk factor analysis and the remaining results will be published in the veterinary literature. Ethics Enrolment of veterinary practices and dogs and cats had been agreed by the Royal Veterinary College Ethics and Welfare Committee. Practice and animal details were only disclosed to the investigators after written or verbal consent by the case veterinary surgeon had been given to the laboratory. Recruitment and sampling of humans, and supportive study material had been approved by the NHS Central Office for Research Ethics Committees (COREC, now NRES, UK NHS National Research Ethics Service) via the local Research and Ethics Committee, Bedford. S. aureus isolates and records were coded. Owners could withhold or disclose their details on the signed questionnaires and consent forms. Participants were informed of their nasal swab results individually in writing if they had provided their address. MRSA carriers were referred to the participant information sheet and advised to inform their medical practitioner of the swab result. Human nasal sampling Each participant sampled their own nose on veterinary practice premises at a convenient time; pet owners were supervised by practice staff. Briefly, dry sterile cotton swabs were rolled for 5 s in both nostrils against the median septum (same swab for each side), followed by immediate transfer to charcoal transport medium (Technical Service Consultants, Heywood, UK) and submission by post. Human swabs were initially processed by the same veterinary laboratory using methods applied for animal submissions. Laboratory methods For all nasal swabs, isolation and identification were preceded by enrichment in tryptone soya broth (Oxoid, Basingstoke, UK) with a total salt concentration of 6.5%. 30 S. aureus was identified and characterised by a combination of an automated bacterial identification and antimicrobial susceptibility testing system (Vitek2, biomérieux, Basingstoke, UK), standard microbiological tests and by latex agglutination tests for PBP2a 0 for suspected MRSA (Oxoid). S. aureus isolates from nasal swabs and from related animal infections were subsequently confirmed and epidemiologically typed at the Royal Veterinary College research laboratory. Phenotypic confirmation included assessment of colony morphology, haemolysis, positivity of Gram s staining, DNase and coagulase testing using dog plasma on slides for clumping factor and rabbit plasma (SigmaeAldrich, Gillingham, UK) in tube coagulase tests, the VogueseProskauer reaction and fermentation of trehalose and lactose. 31 Resistance to meticillin was examined from colonies grown on mannitol salt agar (Oxoid) supplemented with 6 mg/l of oxacillin (SigmaeAldrich) by disc diffusion according to Clinical and Laboratory Standards Institute guidelines. 32 For genetic confirmation of S. aureus and MRSA, DNA was extracted using a commercial kit (Bacterial Genomic DNA Purification kit, Edge BioSystems, Gaithersburg, MD, USA) and the presence of the species-specific thermonuclease gene (S. aureus nuc) and of meca was determined respectively. 33,34 S. aureus lineages were determined by polymerase chain reaction-based characterisation of the specificity subunit (hsds )gene of the S. aureus restriction modification enzyme system. 35 Statistical analysis MRSA nasal carriage was compared between risk groups using Fisher s exact and c 2 -tests. The strength of association was expressed using odds ratios (ORs) and their 95% confidence intervals (CIs). P < 0.05 was considered significant. Results Between September 2005 and March 2008, 608 veterinary staff and pet owners were screened for S. aureus carriage and S. aureus was isolated from

4 A. Loeffler et al. 152/608 (25%) of nasal swabs. Participants had either been in contact with one of 106 MRSA case animals (N ¼ 340) or with one of 91 MSSA control pets (N ¼ 268). The 197 bacterial isolates from dogs and cats represented about 70% of all canine and feline S. aureus isolations during the study period. For the remaining 30%, consent for disclosure of practice details had been refused. The most common reasons for refusal were concerns about time commitment and stigma effect on private veterinary practice. Animals were enrolled from 149 different practices in urban and rural locations all over Britain. Based on the invited four participants per animal, the overall return rate was 76.5% (94.2% for veterinary staff, 54.6% for pet owners). The numbers of case and control animals enrolled per practice varied but the majority of practices (N ¼ 118, 79.2%) participated with only one animal during the study period; 18 practices contributed two each, nine contributed three each and four practices contributed four animals each. Three nasal swabs per animal were received on average. Noncompliance after three telephone calls accounted for the majority of non-returns. MRSA carriage among all participants was 7.2%, but percentages differed significantly between risk groups (Table I). The highest percentage (12.3%) was seen in veterinary staff attending to MRSA-infected pets. The risk of MRSA carriage in all veterinary staff, including both those attending MRSA-infected and MSSA-infected pets, was higher than in all pet owners (9% vs 4.1%; OR: 2.33; 95% CI: 1.10e4.93). Carriage was more frequent in participants, veterinary staff and owners, in contact with MRSA-infected animals than in people in the control group (10.6% vs 3%; OR: 3.85; 95% CI: 1.76e8.43). By contrast, MSSA carriage rates and negative swab results did not differ between groups (c 2 -test: P ¼ 0.62 and P ¼ 0.81, respectively) (Table I). Lineages were determined in 150 MRSA and 199 MSSA isolates from canine and feline infections and from human nasal carriage sites. All MRSA isolates except one from an animal were identified as CC22 and CC30. MSSA isolates were more widely distributed among the lineages with similar proportions of individual lineages seen in animal and human isolates (Table II). Discussion The high MRSA carriage prevalence identified in this large UK-wide screening study among general practice veterinary staff but also among owners of MRSA-infected dogs and cats should be highly relevant for hospital infection control teams. For the first time, the study highlighted an occupational risk for MRSA carriage in general practice veterinary staff, without a direct hospital link, as control-group veterinary staff who did not treat MRSA-infected pets, or at least not knowingly, were more frequent carriers than control-group owners. This is in support of previous smaller projects which investigated MRSA carriage in animal referral hospital staff in various countries and similar to the situation in medical staff. 18,28,29,36,37 However, a plausible explanation for this occupational hazard in veterinary staff is difficult to find. The role of animals as potential vectors needs further investigation, but, most importantly, exposure of veterinary staff to antimicrobial agents in the work place, either for use in animals or for disinfection of the environment, warrants future research. In addition, the overall MRSA carriage of 7.2% among all 608 participants from 169 practices remains substantially higher than the 1.5% estimated for the healthy UK community even though a certain degree of clustering per practice will Table I Frequency of Staphylococcus aureus nasal carriage in veterinary staff and pet owners Type of participant Nasal carriage in in-contact humans (%) MRSA MSSA No S. aureus Veterinary staff attending MRSA pet (N ¼ 220) 27 (12.3) 34 (15.5) 159 (72.3) Veterinary staff attending MSSA pet (N ¼ 168) 8 (4.8) 30 (17.9) 130 (77.4) Owners of MRSA pet (N ¼ 120) 9 (7.5) 25 (20.8) 86 (71.7) Owners of MSSA pet (N ¼ 100) 0 (0) 19 (19.0) 81 (81.0) Veterinary staff total (N ¼ 388) 35 (9.0) 64 (16.5) 289 (74.5) Owners total (N ¼ 220) 9 (4.1) * 44 (20.0) 167 (75.9) Participants in contact with MRSA pets (N ¼ 340) 36 (10.6) 59 (17.4) 245 (72.1) Participants in contact with MSSA pets (N ¼ 268) 8 (3.0) ** 49 (18.3) 211 (78.7) Total number of participants (N ¼ 608) 44 (7.2) 108 (17.8) 456 (75.0) MRSA, meticillin-resistant S. aureus; MSSA, meticillin-susceptible S. aureus. * P-value (c 2 -test) ¼ 0.02. ** P-value (c 2 -test) <0.001.

MRSA in vets and owners of infected pets 5 Table II Clonal clusters identified among human and animal S. aureus isolates Canine or feline infection (N ¼ 106) MRSA In-contact human carriage (N ¼ 44) Canine or feline infection (N ¼ 91) MSSA In-contact human carriage (N ¼ 108) CC22 103 43 69 65 CC30 2 1 11 31 CC45 0 0 1 0 CC1 0 0 2 1 CC8 1 0 3 2 CC5 0 0 4 2 NT a 0 0 1 7 a Not typeable by polymerase chain reaction-based characterisation of the restriction modification enzyme system. 35 have to be considered. 6 In particular, MRSA carriage in owners of MRSA-infected pets was substantially higher than that reported for the UK community. Although the nature of humaneanimal contact was not investigated and contact may only have been brief, this finding emphasises the role of pets as potential reservoirs or vectors. On the other hand, the lack of MRSA isolation from MSSA-infected animal owners confirms the validity of this control group because the <2% MRSA carriage rate in the UK community is very low and MSSA control pet owners are assumed to be closest to the average community setting. 6e8 In the UK, MRSA identified as belonging to CC22 and CC30 are currently consistent with one of the two dominant hospital-associated strains, EMRSA- 15 and EMRSA-16 respectively. Thus, the study finding that all MRSA except one animal isolate belonged to either CC22 or CC30 again suggested that canine and feline MRSA originated from human hospitals and have subsequently spread into the community and to pets. In addition, the predominance of hospital lineages in veterinarians and pet owners without direct hospital links raises concern over their role in the spread of MRSA. Although the mandatory MRSA screening scheme introduced in the UK by the Department of Health in 2009 aims to screen all hospital patients on or prior to admission for elective procedures, management of emergency admissions and infection control where isolation facilities are limited will remain problematic and carriers may continue to present reservoirs for MRSA. Previous guidelines and recommendations in other countries emphasised targeted screening of high risk groups, such as patients previously infected with MRSA or those admitted to intensive care unit, orthopaedic or vascular surgery wards. The recognition now of new high risk groups such as small animal veterinary staff and owners of ill pets may help to maximise the benefit from screening resources. Similarly, the identification of MRSA carriers and risk groups for carriage has been a cornerstone in the successful search-and-destroy policy in The Netherlands. In the Benelux and adjacent countries, there is currently increasing awareness of a new strain, MRSA ST398, originating in pigs and known to colonise pig and veal farmers, and attending vets, at high rates. 38 In The Netherlands, these groups are now considered high risk and, if admitted to hospital, targeted for isolation, MRSA screening and decolonisation. 39 For the UK in particular, where 22 000 veterinarians plus almost 10 000 veterinary nurses and trainee nurses are registered, awareness of veterinarians and owners of dogs and cats as risk populations is likely to have a positive impact on infection control strategies. 40 Although treatment of pet infections, typically with tetracyclines or co-trimoxazole, is mostly successful and the prognosis good if underlying causes can be resolved concurrently, veterinary medicine is dependent on fee-paying pet owners, and any association with the dirty hospital bug MRSA may be detrimental to business. The benefit of pet animals for human health, despite the existence of zoonotic pathogens, remains clear but awareness of an increased risk for MRSA carriage among veterinary staff and owners of infected pets, both among the medical and veterinary professions, will be beneficial for public health. 41 In order to break the cycle of infection, strategies to reduce MRSA infection must consider these new reservoirs e and fund the search for others. Acknowledgements We acknowledge the collaboration of M. Rich and L. Roberts from IDEXX Laboratories, Wetherby, UK. Conflict of interest statement None declared. Funding source The study was funded by the Department for Environment, Food & Rural Affairs (DEFRA), project number OD2019. References 1. Peacock SJ, de Silva I, Lowy FD. What determines nasal carriage of Staphylococcus aureus? Trends Microbiol 2001;9:605e610. 2. Davis KA, Stewart JJ, Crouch HK, Florez CE, Hospenthal DR. Methicillin-resistant Staphylococcus

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