Epidemiology of methicillin resistant Staphylococcus pseudintermedius in guide dogs in Finland

Acta Veterinaria Scandinavica

Thomas Grönthal³  Matti Ollilainen³  Marjut Eklund³  Heli Piiparinen³  Veera Gindonis³  Jouni Junnila²  Leena Saijonmaa-Koulumies³  Riitta Liimatainen¹  Merja Rantala³ 

[1] Guide Dog School of the Finnish Federation of the Visually Impaired, Siltaniitynkuja 1, Vantaa, 01260, Finland

[2] 4Pharma Ltd., Ahventie 4, Espoo, 02170, Finland

[3] Department of Equine and Small Animal Medicine, Faculty of Veterinary Medicine, University of Helsinki, Helsinki, 00014, Finland

关键词: Risk factor;    Prevalence;    Epidemiology;    MRSP;    MRSA;    Staphylococcus;   

Others  :  1219977
DOI  :  10.1186/s13028-015-0129-8

 received in 2015-04-09, accepted in 2015-06-30,  发布年份 2015

【 摘 要 】

Background

Methicillin resistant Staphylococcus pseudintermedius (MRSP) and Staphylococcus aureus (MRSA) are common multi-drug resistant (MDR) bacteria in dogs. In 2012–2013 three dogs of the Guide Dog School of the Finnish Federation of the Visually Impaired were found to be MRSP positive. Guide dogs have regular contact with each other during their first year of life and prolonged contact when in training. Since dogs are placed in different parts of Finland after training, there is a risk for national spread of MDR bacteria. In this study the prevalence of MRSP and MRSA, as well as the risk factors for MRSP were determined in the Finnish guide dog population. MRSP isolates were investigated using molecular methods and compared to the earlier isolates.

Results

Out of 132 tested dogs 4 were MRSP positive thus giving the prevalence estimate of 3% (95% CI: 1–8%) for MRSP in the target population. MRSA was not detected (prevalence estimate 0%, 95% CI: 0–3%). Risk factors associated with MRSP were being a breeding bitch (OR = 8.4; 95% CI: 1.1–64.1, P = 0.012), the number of veterinary visits (OR = 1.23; 95% CI: 1.0–1.5, P = 0.025) and number of antimicrobial courses (OR = 1.63; 95% CI: 1.0–2.55; P = 0.035). Identified MRSP isolates belonged to five different sequence types (ST45, 71, 402, 403 and 404). All ST71 isolates carried SCCmec II-III, while the SCCmec type of the ST45 and ST402 (a single locus variant of ST45) isolates were non-typeable with the method used.

Conclusions

MRSP and MRSA had low prevalence in the studied dog population despite the close contact between dogs, and the MRSP population was heterogenic. Antimicrobial therapy and veterinary visits are risk factors for MRSP even among a small case group.

【 授权许可】

   
2015 Grönthal et al.

【 图 表 】

Figure1.

Figure2.

【 参考文献 】

• [1]Paul NC, Bargman SC, Moodley A, Nielsen SS, Guardabassi L. Staphylococcus pseudintermedius colonization patterns and strain diversity in healthy dogs: a cross-sectional and longitudinal study. Vet Microbiol. 2012; 160:420-427.
• [2]van Duijkeren E, Catry B, Greko C, Moreno MA, Pomba MC, Pyorala S et al.. Review on methicillin-resistant Staphylococcus pseudintermedius. J Antimicrob Chemother. 2011; 66:2705-2714.
• [3]Loeffler A, Linek M, Moodley A, Guardabassi L, Sung JM, Winkler M et al.. First report of multiresistant, mecA-positive Staphylococcus intermedius in Europe: 12 cases from a veterinary dermatology referral clinic in Germany. Vet Dermatol. 2007; 18:412-421.
• [4]Jones RD, Kania SA, Rohrbach BW, Frank LA, Bemis DA. Prevalence of oxacillin- and multidrug-resistant staphylococci in clinical samples from dogs: 1,772 samples (2001-2005). J Am Vet Med Assoc. 2007; 230:221-227.
• [5]Perreten V, Kadlec K, Schwarz S, Gronlund Andersson U, Finn M, Greko C et al.. Clonal spread of methicillin-resistant Staphylococcus pseudintermedius in Europe and North America: an international multicentre study. J Antimicrob Chemother. 2010; 65:1145-1154.
• [6]Borjesson S, Landen A, Bergstrom M, Andersson UG. Methicillin-resistant Staphylococcus pseudintermedius in Sweden. Microb Drug Resist. 2012; 18:597-603.
• [7]Grönthal T, Moodley A, Nykäsenoja S, Junnila J, Guardabassi L, Thomson K et al.. Large Outbreak Caused by Methicillin Resistant Staphylococcus pseudintermedius ST71 in a Finnish Veterinary Teaching Hospital—from outbreak control to outbreak prevention. PLoS One. 2014; 9:e110084.
• [8]Boost MV, O’Donoghue MM, James A. Prevalence of Staphylococcus aureus carriage among dogs and their owners. Epidemiol Infect. 2008; 136:953-964.
• [9]Rich M, Roberts L. MRSA in companion animals. Vet Rec. 2006; 159:535-536.
• [10]van Duijkeren E, Kamphuis M, van der Mije IC, Laarhoven LM, Duim B, Wagenaar JA et al.. 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. 2011; 150:338-343.
• [11]Gomez-Sanz E, Torres C, Ceballos S, Lozano C, Zarazaga M. Clonal dynamics of nasal Staphylococcus aureus and Staphylococcus pseudintermedius in dog-owning household members. Detection of MSSA ST(398). PLoS One. 2013; 8:e69337.
• [12]Opaskoirakoulu Näkövammaisten keskusliitto ry [http://www.opaskoirakoulu.fi/?lang=en]. Accessed 20 February 2015
• [13]Epi Tools—Sample size to estimate a proportion with specified precision. [http://epitools.ausvet.com.au/content.php?page=1Proportion]. Accessed 16 May 2015
• [14]Feng Y, Tian W, Lin D, Luo Q, Zhou Y, Yang T et al.. Prevalence and characterization of methicillin-resistant Staphylococcus pseudintermedius in pets from South China. Vet Microbiol. 2012; 160:517-524.
• [15]Gingrich EN, Kurt T, Hyatt DR, Lappin MR, Ruch-Gallie R. Prevalence of methicillin-resistant staphylococci in northern Colorado shelter animals. J Vet Diagn Invest. 2011; 23:947-950.
• [16]Griffeth GC, Morris DO, Abraham JL, Shofer FS, Rankin SC. Screening for skin carriage of methicillin-resistant coagulase-positive staphylococci and Staphylococcus schleiferi in dogs with healthy and inflamed skin. Vet Dermatol. 2008; 19:142-149.
• [17]Hanselman BA, Kruth SA, Rousseau J, Weese JS. Coagulase positive staphylococcal colonization of humans and their household pets. Can Vet J. 2009; 50:954-958.
• [18]Murphy C, Reid-Smith RJ, Prescott JF, Bonnett BN, Poppe C, Boerlin P et al.. Occurrence of antimicrobial resistant bacteria in healthy dogs and cats presented to private veterinary hospitals in southern Ontario: A preliminary study. Can Vet J. 2009; 50:1047-1053.
• [19]Sasaki T, Kikuchi K, Tanaka Y, Takahashi N, Kamata S, Hiramatsu K. Methicillin-resistant Staphylococcus pseudintermedius in a veterinary teaching hospital. J Clin Microbiol. 2007; 45:1118-1125.
• [20]Vengust M, Anderson ME, Rousseau J, Weese JS. Methicillin-resistant staphylococcal colonization in clinically normal dogs and horses in the community. Lett Appl Microbiol. 2006; 43:602-606.
• [21]Hanselman BA, Kruth S, Weese JS. Methicillin-resistant staphylococcal colonization in dogs entering a veterinary teaching hospital. Vet Microbiol. 2008; 126:277-281.
• [22]Epi Tools—Calculate confidence limits for a sample proportion. [http://www.epitools.ausvet.com.au/content.php?page=CIProportion]. Accessed 15 March 2015
• [23]Brown LD, Cai TT, DasGupta A, Agresti A, Coull BA, Casella G et al.. Interval estimation for a binomial proportion—comment—rejoinder. Stat Sci. 2001; 16:101-133.
• [24]Firth D. Bias reduction of maximum likelihood estimates. Biometrika. 1993; 80:27-38.
• [25]Venzon DJ, Moolgavkar SH. A method for computing profile-likelihood-based confidence intervals. Appl Stat J Roy St C. 1988; 37:87-94.
• [26]Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; approved standard. 4th ed. CLSI, Wayne; 2013.
• [27]Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals; second informational supplement. VET01-S2. CLSI, Wayne; 2013.
• [28]National Institute of Health and Welfare (2015) Vanha FiRe-standardi (the old FiRe-standard). https://www.thl.fi/fi/web/infektiotaudit/seuranta-ja-epidemiat/mikrobilaakeresistenssi/fire-suomalainen-mikrobilaakeresistenssin-tutkimusryhma/menetelmat/vanha-fire-standardi. Accessed 27 May 2015
• [29]Murchan S, Kaufmann ME, Deplano A, de Ryck R, Struelens M, Zinn CE et al.. Harmonization of pulsed-field gel electrophoresis protocols for epidemiological typing of strains of methicillin-resistant Staphylococcus aureus: a single approach developed by consensus in 10 European laboratories and its application for tracing the spread of related strains. J Clin Microbiol. 2003; 41:1574-1585.
• [30]DTU Food—National Food Institute (2012) Protocol for PCR-Amplification of mecA, mecC (mecA LGA251), spa and pvl Recommended by the EURL-AR, 2nd version. National Food Institute, Søborg
• [31]Stegger M, Andersen PS, Kearns A, Pichon B, Holmes MA, Edwards G et al.. Rapid detection, differentiation and typing of methicillin-resistant Staphylococcus aureus harbouring either mecA or the new mecA homologue mecA(LGA251). Clin Microbiol Infect. 2012; 18:395-400.
• [32]Kondo Y, Ito T, Ma XX, Watanabe S, Kreiswirth BN, Etienne J, Hiramatsu K. Combination of multiplex PCRs for staphylococcal cassette chromosome mec type assignment: rapid identification system for mec, ccr, and major differences in junkyard regions. Antimicrob Agents Chemother. 2007; 51:264-274.
• [33]Solyman SM, Black CC, Duim B, Perreten V, van Duijkeren E, Wagenaar JA et al.. Multilocus sequence typing for characterization of Staphylococcus pseudintermedius. J Clin Microbiol. 2013; 51:306-310.
• [34]Staphylococcus pseudintermedius MLST Databases. [http://www.pubmlst.org/spseudintermedius/]. Accessed 16 March 2015
• [35]Lehner G, Linek M, Bond R, Lloyd DH, Prenger-Berninghoff E, Thom N et al.. Case-control risk factor study of methicillin-resistant Staphylococcus pseudintermedius (MRSP) infection in dogs and cats in Germany. Vet Microbiol. 2014; 168:154-160.
• [36]Nienhoff U, Kadlec K, Chaberny IF, Verspohl J, Gerlach GF, Kreienbrock L et al.. Methicillin-resistant Staphylococcus pseudintermedius among dogs admitted to a small animal hospital. Vet Microbiol. 2011; 150:191-197.
• [37]Soares Magalhaes RJ, Loeffler A, Lindsay J, Rich M, Roberts L, Smith H et al.. Risk factors for methicillin-resistant Staphylococcus aureus (MRSA) infection in dogs and cats: a case-control study. Vet Res. 2010; 41:55.
• [38]Shaw SC, Wood JL, Freeman J, Littlewood JD, Hannant D. Estimation of heritability of atopic dermatitis in Labrador and Golden Retrievers. Am J Vet Res. 2004; 65:1014-1020.
• [39]Hellman JAO, Bengtsson B, Greko C. SWEDRES-SVARM 2013. Use of antimicrobials and occurrence of antimicrobial resistance in Sweden. Solna/Uppsala, Sweden; 2013.
• [40]Osland AM, Vestby LK, Fanuelsen H, Slettemeas JS, Sunde M. Clonal diversity and biofilm-forming ability of methicillin-resistant Staphylococcus pseudintermedius. J Antimicrob Chemother. 2012; 67:841-848.
• [41]Perreten V, Chanchaithong P, Prapasarakul N, Rossano A, Blum SE, Elad D et al.. Novel pseudo-staphylococcal cassette chromosome mec element (psiSCCmec57395) in methicillin-resistant Staphylococcus pseudintermedius CC45. Antimicrob Agents Chemother. 2013; 57:5509-5515.
• [42]Laarhoven LM, de Heus P, van Luijn J, Duim B, Wagenaar JA et al.. Longitudinal study on methicillin-resistant Staphylococcus pseudintermedius in households. PLoS ONE. 2011; 6:e27788.
• [43]Siak M, Burrows AK, Coombs GW, Khazandi M, Abraham S, Norris JM et al.. Characterization of meticillin-resistant and meticillin-susceptible isolates of Staphylococcus pseudintermedius from cases of canine pyoderma in Australia. J Med Microbiol. 2014; 63:1228-1233.
• [44]Windahl U, Reimegard E, Holst BS, Egenvall A, Fernstrom L, Fredriksson M et al.. Carriage of methicillin-resistant Staphylococcus pseudintermedius in dogs–a longitudinal study. BMC Vet Res. 2012; 8:34. BioMed Central Full Text
• [45]Saijonmaa-Koulumies L, Parsons E, Lloyd DH. Elimination of Staphylococcus intermedius in healthy dogs by topical treatment with fusidic acid. J Small Anim Pract. 1998; 39:341-347.
• [46]Miller L, Hurley K. Infectious disease management in animal shelters. 1st ed. Wiley-Blackwell, Iowa; 2009.