Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming

BMC Infectious Diseases

Annalisa Pantosti¹  Annamaria Indelicato²  Annalisa Bonomini²  Andrea Sanchini³  Palmino Pedroni²  Monica Monaco¹ 

[1] Department of Infectious, Parasitic and Immuno-mediated Diseases, Istituto Superiore di Sanità, viale Regina Elena, 299, Rome, Italy;Presidio Ospedaliero Manerbio-Leno, Azienda Ospedaliera Desenzano del Garda, Lungomella Valsecchi, Brescia, Italy;Present address: European Public Health Microbiology Training Programme (EUPHEM), European Centre for Disease Prevention and Control (ECDC), Tomtebodavägen 11a, 171 83, Stockholm, Sweden

关键词: ST398;    Pigs;    Colonization, Community-acquired infections;    Livestock-associated (LA)-MRSA;   

Others  :  1147960
DOI  :  10.1186/1471-2334-13-258

 received in 2013-03-26, accepted in 2013-05-23,  发布年份 2013

【 摘 要 】

Background

Livestock-Associated MRSA (LA-MRSA) belonging to ST398 lineage, common among pigs and other animals, emerged in Central and Northern Europe, becoming a new risk factor for MRSA among farm workers. Strains belonging to ST398 can be responsible for human colonization and infection, mainly in areas with high livestock-farming. The aim of this study was to investigate the occurrence of livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) human colonization and infections in an area of the Lombardy Region (Italy), the Italian region with the highest density of pig farming.

Methods

In the period March-April 2010, 879 nasal swabs were taken from subjects at admission to a local hospital serving an area of the Lombardy Region devoted to agriculture and farming. In the period March 2010-February 2011, all MRSA strains from community-acquired infection (CAI) observed in the same hospital, were collected. Molecular characterization of the isolates included SCCmec typing, spa typing and multilocus sequence typing (MLST).

Results

Out of 879 nasal swabs examined, 9 (1%) yielded MRSA. Five strains were assigned to sequence type (ST)398 (spa t899, 3 isolates; t108 and t2922, 1 isolate each) and were therefore categorized as LA-MRSA. The other 4 isolates were likely of hospital origin. No strains were positive for Panton-Valentine Leukocidin genes. Twenty MRSA isolates were detected from CAI, 17 were from skin and soft-tissue infections and 3 from other infections. An MRSA isolate from otitis externa was t899/ST398 and PVL-negative, hence categorized as LA-MRSA. Four isolates were assigned to t127/ST1. Eight strains were PVL-positive community acquired (CA)-MRSA and belonged to different clones, the most frequent being ST8.

Conclusions

In an area of Italy with high density of pig farming, LA-MRSA is able to colonize the population and rarely to produce infections. Typical CA-MRSA is more common than LA-MRSA among CAI.

【 授权许可】

   
2013 Monaco et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Pantosti A, Venditti M: What is MRSA? Eur Respir 2009, 34:1190-1196.
• [2]Grundmann H, Aanensen DM, van den Wijngaard CC, Spratt BG, Harmsen D, Friedrich AW: Geographic distribution of Staphylococcus aureus causing invasive infections in Europe: a molecular-epidemiological analysis. PLoS Med 2010, 7:e1000215.
• [3]Deleo FR, Otto M, Kreiswirth BN, Chambers HF: Community-associated meticillin-resistant Staphylococcus aureus. Lancet 2010, 375:1557-1568.
• [4]Sanchini A, Spitoni MG, Monaco M, Raglio A, Grigis A, Petro W, et al.: Outbreak of skin and soft tissue infections in a hospital newborn nursery in Italy due to community-acquired meticillin-resistant Staphylococcus aureus USA300 clone. J Hosp Infect 2013, 83:36-40.
• [5]Boyle-Vavra S, Daum RS: Community-acquired methicillin-resistant Staphylococcus aureus: the role of Panton-Valentine leukocidin. Lab Invest 2007, 87:3-9.
• [6]Bubeck Wardenburg J, Bae T, Otto M, Deleo FR, Schneewind O: Poring over pores: alpha-hemolysin and Panton-Valentine leukocidin in Staphylococcus aureus pneumonia. Nat Med 2007, 13:1405-1406.
• [7]Labandeira-Rey M, Couzon F, Boisset S, Brown EL, Bes M, Benito Y, Barbu EM, et al.: Staphylococcus aureus Panton-Valentine leukocidin causes necrotizing pneumonia. Science 2007, 315:1130-1133.
• [8]Hasman H, Moodley A, Guardabassi L, Stegger M, Skov RL, Aarestrup FM: spa type distribution in Staphylococcus aureus originating from pigs, cattle and poultry. Vet Microbiol 2010, 141:326-331.
• [9]van Cleef BA, Monnet DL, Voss A, Krziwanek K, Allerberger F, Struelens M, et al.: Livestock-associated methicillin-resistant Staphylococcus aureus in humans, Europe. Emerg Infect Dis 2011, 17:502-505.
• [10]Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M: Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis 2005, 11:1965-1966.
• [11]Kock R, Harlizius J, Bressan N, Laerberg R, Wieler LH, Witte W, et al.: Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) among pigs on German farms and import of livestock-related MRSA into hospitals. Eur J Clin Microbiol Infect Dis 2009, 28:1375-1382.
• [12]van Cleef BA, Verkade EJ, Wulf MW, Buiting AG, Voss A, Huijsdens XW, et al.: Prevalence of livestock-associated MRSA in communities with high pig-densities in The Netherlands. PloS One 2010, 5:e9385.
• [13]Bisdorff B, Scholholter JL, Claussen K, Pulz M, Nowak D, Radon K: MRSA-ST398 in livestock farmers and neighbouring residents in a rural area in Germany. Epidemiol Infect 2012, 140:1800-1808.
• [14]Wulf MW, Sorum M, van Nes A, Skov R, Melchers WJ, Klaassen CH, et al.: Prevalence of methicillin-resistant Staphylococcus aureus among veterinarians: an international study. Clin Microbiol Infect 2008, 14:29-34.
• [15]Cuny C, Nathaus R, Layer F, Strommenger B, Altmann D, Witte W: Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PloS One 2009, 4:e6800.
• [16]European Food Safety Authority: Analysis of the baseline survey on the prevalence of methicillin-resistant Staphylococcus aureus (MRSA) in holdings with breeding pigs, in the EU, 2008. Part A: MRSA prevalence estimates. EFSA Journal 2009, 7:1376.
• [17]Pan A, Battisti A, Zoncada A, Bernieri F, Boldini M, Franco A, et al.: Community-acquired methicillin-resistant Staphylococcus aureus ST398 infection, Italy. Emerg Infect Dis 2009, 15:845-847.
• [18]Soavi L, Stellini R, Signorini L, Antonini B, Pedroni P, Zanetti L, et al.: Methicillin-resistant Staphylococcus aureus ST398, Italy. Emerg Infect Dis 2010, 16:346-348.
• [19]Battisti A, Franco A, Merialdi G, Hasman H, Iurescia M, Lorenzetti R, et al.: Heterogeneity among methicillin-resistant Staphylococcus aureus from Italian pig finishing holdings. Vet Microbiol 2010, 142:361-366.
• [20]Franco A, Hasman H, Iurescia M, Lorenzetti R, Stegger M, Pantosti A, et al.: Molecular characterization of spa type t127, sequence type 1 methicillin-resistant Staphylococcus aureus from pigs. J Antimicrob Chemother 2011, 66:1231-1235.
• [21]Bellini S, Alborali L, Massirio I, Cinotti S: Evoluzione del comparto suinicolo in Italia: criticità e fattori di rischio. L' Osservatorio 2010, 13:1-8.
• [22]Clinical and Laboratory Standards Institute: Performance Standards for Antimicrobial Susceptibility Testing: Eighteenth Informational Supplement M100-S18. Wayne, PA, USA: CLSI; 2008.
• [23]Brakstad OG, Aasbakk K, Maeland JA: Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J Clin Microbiol 1992, 30:1654-1660.
• [24]Murakami K, Minamide W, Wada K, Nakamura E, Teraoka H, Watanabe S: Identification of methicillin-resistant strains of staphylococci by polymerase chain reaction. J Clin Microbiol 1991, 29:2240-2244.
• [25]Sanchini A, Campanile F, Monaco M, Cafiso V, Rasigade JP, Laurent F, Etienne J, et al.: DNA microarray-based characterisation of Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus from Italy. Eur J Clin Microbiol Infect Dis 2011, 30:1399-1408.
• [26]van Wamel WJ, Rooijakkers SH, Ruyken M, van Kessel KP, van Strijp JA: The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J Bacteriol 2006, 188:1310-1315.
• [27]Milheirico C, Oliveira DC, de Lencastre H: Multiplex PCR strategy for subtyping the staphylococcal cassette chromosome mec type IV in methicillin-resistant Staphylococcus aureus: 'SCCmec IV multiplex'. J Antimicrobl Chemother 2007, 60:42-48.
• [28]Harmsen D, Claus H, Witte W, Rothganger J, Claus H, Turnwald D, et al.: Typing of methicillin-resistant Staphylococcus aureus in a university hospital setting by using novel software for spa repeat determination and database management. J Clin Microbiol 2003, 41:5442-5448.
• [29]Enright MC, Day NP, Davies CE, Peacock SJ, Spratt BG: Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol 2000, 38:1008-1015.
• [30]Kock R, Siam K, Al-Malat S, Christmann J, Schaumburg F, Becker K, et al.: Characteristics of hospital patients colonized with livestock-associated meticillin-resistant Staphylococcus aureus (MRSA) CC398 versus other MRSA clones. J Hosp Infect 2011, 79:292-296.
• [31]van der Mee-Marquet N, Francois P, Domelier-Valentin AS, Coulomb F, Decreux C, Hombrock-Allet C, et al.: Emergence of unusual bloodstream infections associated with pig-borne-like Staphylococcus aureus ST398 in France. Clin Infect Dis 2011, 52:152-153.
• [32]Wulf MW, Markestein A, van der Linden FT, Voss A, Klaassen C, Verduin CM: First outbreak of methicillin-resistant Staphylococcus aureus ST398 in a Dutch hospital, June 2007. Euro Surveill 2008., 13pii: 8051
• [33]Jamrozy DM, Fielder MD, Butaye P, Coldham NG: Comparative genotypic and phenotypic characterisation of methicillin-resistant Staphylococcus aureus ST398 isolated from animals and humans. PloS One 2012, 7:e40458.
• [34]Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, et al.: Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. mBio 2012., 3pii: e00305-11
• [35]McCarthy AJ, Witney AA, Gould KA, Moodley A, Guardabassi L, Voss A, et al.: The distribution of mobile genetic elements (MGEs) in MRSA CC398 is associated with both host and country. Genome Biol Evol 2011, 3:1164-1174.
• [36]Aschbacher R, Pichon B, Spoladore G, Pagani E, Innocenti P, Moroder L, et al.: High clonal heterogeneity of Panton-Valentine leukocidin-positive meticillin-resistant Staphylococcus aureus strains from skin and soft-tissue infections in the Province of Bolzano, Northern Italy. Int J Antimicrob Agents 2012, 39:522-525.
• [37]Monaco M, Sanchini A, Grundmann H, Pantosti A: Vancomycin-heteroresistant phenotype in invasive methicillin-resistant Staphylococcus aureus isolates belonging to spa type 041. Eur J Clin Microbiol Infect Dis 2010, 29:771-777.
• [38]Dauwalder O, Lina G, Durand G, Bes M, Meugnier H, Jarlier V, et al.: Epidemiology of invasive methicillin-resistant Staphylococcus aureus clones collected in France in 2006 and 2007. J Clin Microbiol 2008, 46:3454-3458.