Occurrence of methicillin-resistant Staphylococcus aureus in farm workers and the livestock environment in Mecklenburg-Western Pomerania, Germany

Acta Veterinaria Scandinavica

Carmen Dahms¹  Nils-Olaf Hübner²  Christiane Cuny³  Axel Kramer¹ 

[1] University Medicine Greifswald, Institute of Hygiene and Environmental Medicine, Walther-Rathenau-Straße 49a, Greifswald, 17487, Germany

[2] Institute of Medical Diagnostic (IMD), Pappelallee 1, Greifswald, 17489, Germany

[3] Robert Koch-Institute, National Reference Center for Staphylococci and Enterococci, Burgstraße 37, Wernigerode, 38855, Germany

关键词: Germany;    Zoonoses;    Cattle;    Pig;    Poultry;    Chickens;    Livestock;    Humans;    Animals;    MRSA;    Methicillin-resistant Staphylococcus aureus;   

Others  :  1082565
DOI  :  10.1186/s13028-014-0053-3

 received in 2014-03-25, accepted in 2014-08-13,  发布年份 2014

【 摘 要 】

Background

Livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA) has a wide host range and is transmissible to humans, especially to those with close contact to colonized animals. This study presents the first data on the occurrence of MRSA in farm workers and livestock farms (pig, cattle and poultry) in the federal state of Mecklenburg-Western Pomerania in northeast Germany. 78 farm workers at pig farms, cattle farms and poultry farms were tested for MRSA via pooled nasal and pharyngeal swabs. Additionally, from each of the 34 participating farms (17 pig farms, 11 cattle farms, 6 poultry farms) five dust samples were taken from the direct surroundings of the animals. Furthermore, oropharyngeal swabs were additionally taken from 10 animals per poultry farm. Isolated MRSA strains were characterized and confirmed using PCR and spa typing. Resistance patterns were obtained using the broth microdilution assay.

Results

In total, 20 of 78 (25.6%; 95% CI:17.3-36.3) farm workers were positive for MRSA. All MRSA-positive workers were employed at pig farms. Six of 17 (35.3%; 95% CI:17.3-58.7) pooled dust samples from pig farms were also positive. Overall, six spa types were identified, of which t034 predominated. All strains belonged to LA-MRSA CC398 and were resistant to tetracycline. Resistance to lincosamides, macrolides, fluoroquinolones and aminoglycosides was present in some strains. Three farm workers harbored the identical spa type and antimicrobial resistance pattern found in the corresponding dust sample. Neither workers, dust samples from cattle and poultry farms, nor oropharyngeal poultry swabs tested positive for MRSA.

Conclusions

The present study emphasizes the importance of MRSA on pig farms and pig-farm workers in the rural region of Mecklenburg-Western Pomerania, whereas LA-MRSA could not be isolated from cattle and poultry farms.

【 授权许可】

   
2014 Dahms et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

【 参考文献 】

• [1]Chambers HF, DeLeo FR: Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009, 7:629-641.
• [2]Enright MC: The evolution of a resistant pathogen–the case of MRSA. Curr Opin Pharmacol 2003, 3:474-479.
• [3]Köck R, Mellmann A, Schaumburg F, Friedrich AW, Kipp F, Becker K: The epidemiology of methicillin-resistant Staphylococcus aureus (MRSA) in Germany. Dtsch Arztebl Int 2011, 108:761-767.
• [4]Otto M: Staphylococcus aureus toxins. Curr Opin Microbiol 2014, 17:32-37.
• [5]Qu T, Feng Y, Jiang Y, Zhu P, Wei Z, Chen Y, Otto M, Yu Y: Whole genome analysis of a community-associated methicillin-resistant Staphylococcus aureus ST59 isolate from a case of human sepsis and severe pneumonia in China. PLoS ONE 2014, 9:e89235.
• [6]Cocchi P, Taccetti G, Montagnani C, Campana S, Galli L, Braggion C, de Martino M: Evidence of transmission of a Panton-Valentine leukocidin-positive community-acquired methicillin-resistant Staphylococcus aureus clone: a family affair. Clin Microbiol Infect 2013, 19:1158-1162.
• [7]Vandenesch F, Naimi T, Enright MC, Lina G, Nimmo GR, Heffernan H, Liassine N, Bes M, Greenland T, Reverdy ME, Etienne J: Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton-Valentine leukocidin genes: worldwide emergence. Emerg Infect Dis 2003, 9:978-984.
• [8]Voss A, Loeffen F, Bakker J, Klaassen C, Wulf M: Methicillin-resistant Staphylococcus aureus in pig farming. Emerg Infect Dis 2005, 11:1965-1966.
• [9]Graveland H, Wagenaar JA, Heesterbeek H, Mevius D, van Duijkeren E, Heederik D: Methicillin resistant Staphylococcus aureus ST398 in veal calf farming: human MRSA carriage related with animal antimicrobial usage and farm hygiene. PLoS ONE 2010, 5:e10990.
• [10]Fessler AT, Kadlec K, Hassel M, Hauschild T, Eidam C, Ehricht R, Monecke S, Schwarz S: Characterization of methicillin-resistant Staphylococcus aureus isolates from food and food products of poultry origin in Germany. Appl Environ Microbiol 2011, 77:7151-7157.
• [11]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.
• [12]Lowder BV, Guinane CM, Ben Zakour NL, Weinert LA, Conway-Morris A, Cartwright RA, Simpson AJ, Rambaut A, Nubel U, Fitzgerald JR: Recent human-to-poultry host jump, adaptation, and pandemic spread of Staphylococcus aureus. Proc Natl Acad Sci U S A 2009, 106:19545-19550.
• [13]van Duijkeren E, Jansen MD, Flemming SC, de Neeling H, Wagenaar JA, Schoormans AH, van Nes A, Fluit AC: Methicillin-resistant Staphylococcus aureus in pigs with exudative epidermitis. Emerg Infect Dis 2007, 13:1408-1410.
• [14]Fessler A, Scott C, Kadlec K, Ehricht R, Monecke S, Schwarz S: Characterization of methicillin-resistant Staphylococcus aureus ST398 from cases of bovine mastitis. J Antimicrob Chemother 2010, 65:619-625.
• [15]Price LB, Stegger M, Hasman H, Aziz M, Larsen J, Andersen PS, Pearson T, Waters AE, Foster JT, Schupp J, Gillece J, Driebe E, Liu CM, Springer B, Zdovc I, Battisti A, Franco A, Zmudzki J, Schwarz S, Butaye P, Jouy E, Pomba C, Porrero MC, Ruimy R, Smith TC, Robinson DA, Weese JS, Arriola CS, Yu F, Laurent F, et al.: Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio 2012, 3:6.
• [16]Krziwanek K, Metz-Gercek S, Mittermayer H: Methicillin-Resistant Staphylococcus aureus ST398 from human patients, upper Austria. Emerg Infect Dis 2009, 15:766-769.
• [17]Graveland H, Wagenaar JA, Bergs K, Heesterbeek H, Heederik D: Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS ONE 2011, 6:e16830.
• [18]Spohr M, Rau J, Friedrich A, Klittich G, Fetsch A, Guerra B, Hammerl JA, Tenhagen BA: Methicillin-resistant Staphylococcus aureus (MRSA) in three dairy herds in southwest Germany. Zoonoses Public Health 2011, 58:252-261.
• [19]Cuny C, Köck R, Witte W: Livestock associated MRSA (LA-MRSA) and its relevance for humans in Germany. Int J Med Microbiol 2013, 303:331-337.
• [20]Monecke S, Coombs G, Shore AC, Coleman DC, Akpaka P, Borg M, Chow H, Ip M, Jatzwauk L, Jonas D, Kadlec K, Kearns A, Laurent F, O’Brien FG, Pearson J, Ruppelt A, Schwarz S, Scicluna E, Slickers P, Tan HL, Weber S, Ehricht R: A field guide to pandemic, epidemic and sporadic clones of methicillin-resistant Staphylococcus aureus. PLoS One 2011, 6:e17936.
• [21]Argudin MA, Tenhagen BA, Fetsch A, Sachsenroder J, Kasbohrer A, Schroeter A, Hammerl JA, Hertwig S, Helmuth R, Braunig J, Mendoza MC, Appel B, Rodicio MR, Guerra B: Virulence and resistance determinants of German Staphylococcus aureus ST398 isolates from nonhuman sources. Appl Environ Microbiol 2011, 77:3052-3060.
• [22]van Cleef BA, Monnet DL, Voss A, Krziwanek K, Allerberger F, Struelens M, Zemlickova H, Skov RL, Vuopio-Varkila J, Cuny C, Friedrich AW, Spiliopoulou I, Paszti J, Hardardottir H, Rossney A, Pan A, Pantosti A, Borg M, Grundmann H, Mueller-Premru M, Olsson-Liljequist B, Widmer A, Harbarth S, Schweiger A, Unal S, Kluytmans JA: Livestock-associated methicillin-resistant Staphylococcus aureus in humans, Europe. Emerg Infect Dis 2011, 17:502-505.
• [23]Pantosti A: Methicillin-resistant Staphylococcus aureus associated with animals and its relevance to human health. Front Microbiol 2012, 3:127.
• [24]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.
• [25]Recommendations to prevent and control MRSA strains in hospitals and medical facilities [in German]. vol. 57. Robert Koch Institute,Bundesgesundhbl, Berlin-Heidelberg; 2014.
• [26]Federal Statistical Office: Annual Abstract of Statistics: Germany and International Statistics 2012 [in German]. Wiesbaden; 2012.
• [27]Federal Statistical Office: Annual Abstract of Statistics: Germany and International Statistics 2012 [in German]. Wiesbaden; 2012.
• [28]Tobi H, van den Berg PB, de Jong-van den Berg LT: Small proportions: what to report for confidence intervals? Pharmacoepidemiol Drug Saf 2005, 14:239-247.
• [29]Commission Decision of 20 December 2007 concerning a financial contribution from the Community towards a survey on the prevalence of Salmonella spp. and Methicillin-resistant Staphylococcus aureus in herds of breeding pigs to be carried out in the Member States (2008/55/EC) OJEU 2008, L 14:10-24.
• [30]Cuny C, Pasemann B, Witte W: Detection of oxacillin resistance in Staphylococcus aureus by screening tests. Eur J Clin Microbiol Infect Dis 1999, 18:834-836.
• [31]Harmsen D, Claus H, Witte W, Rothganger J, Turnwald D, Vogel U: 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.
• [32]Lina G, Piemont Y, Godail-Gamot F, Bes M, Peter MO, Gauduchon V, Vandenesch F, Etienne J: Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999, 29:1128-1132.
• [33]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.
• [34]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 J 2009, 7:82. Parma
• [35]Köck R, Harlizius J, Bressan N, Laerberg R, Wieler LH, Witte W, Deurenberg RH, Voss A, Becker K, Friedrich AW: 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.
• [36]Espinosa-Gongora C, Broens EM, Moodley A, Nielsen JP, Guardabassi L: Transmission of MRSA CC398 strains between pig farms related by trade of animals. Vet Rec 2012, 170:564.
• [37]Statistic 2012 Pigmeat. Danish Agricultre & Food Council, Copenhagen; 2013.
• [38]van de Vijver LP, Tulinski P, Bondt N, Mevius D, Verwer C: Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) in organic pig herds in The Netherlands. Zoonoses Public Health 2013, 61:338-345.
• [39]Cuny C, Friedrich AW, Witte W: Absence of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex CC398 as a nasal colonizer of pigs raised in an alternative system. Appl Environ Microbiol 2012, 78:1296-1297.
• [40]Köck R, Loth B, Koksal M, Schulte-Wulwer J, Harlizius J, Friedrich AW: Persistence of nasal colonization with livestock-associated methicillin-resistant Staphylococcus aureus in pig farmers after holidays from pig exposure. Appl Environ Microbiol 2012, 78:4046-4047.
• [41]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.
• [42]Commentary on the recommendations to prevent and control MRSA strains in hospitals and medical facilities [in German] Epidemiol Bulletin 2008, 42:363-364.
• [43]Vanderhaeghen W, Cerpentier T, Adriaensen C, Vicca J, Hermans K, Butaye P: Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Vet Microbiol 2010, 144:166-171.
• [44][http://www.lallf.de/fileadmin/media/PDF/lebensm/LHD/Zoon_Monitor_2009.pdf] webcite Monitoring of zoonoses in the food chain 2009 [in German]. []
• [45]Juhasz-Kaszanyitzky E, Janosi S, Somogyi P, Dan A, van der Graaf-van Bloois L, van Duijkeren E, Wagenaar JA: MRSA transmission between cows and humans. Emerg Infect Dis 2007, 13:630-632.
• [46]Richter A, Sting R, Popp C, Rau J, Tenhagen BA, Guerra B, Hafez HM, Fetsch A: Prevalence of types of methicillin-resistant Staphylococcus aureus in turkey flocks and personnel attending the animals. Epidemiol Infect 2012, 140:2223-2232.
• [47]Pletinckx LJ, Verhegghe M, Dewulf J, Crombe F, De Bleecker Y, Rasschaert G, Goddeeris BM, De Man I: Screening of poultry-pig farms for methicillin-resistant Staphylococcus aureus: sampling methodology and within herd prevalence in broiler flocks and pigs. Infect Genet Evol 2011, 11:2133-2137.
• [48][http://lallf.de/fileadmin/media/PDF/lebensm/LHD/JB12_Zoon_Monitor.pdf] webcite Monitoring of zoonoses in the food chain 2011 [in German]. []
• [49]Gazin M, Lee A, Derde L, Kazma M, Lammens C, Ieven M, Bonten M, Carmeli Y, Harbarth S, Brun-Buisson C, Goossens H, Malhotra-Kumar S: Culture-based detection of methicillin-resistant Staphylococcus aureus by a network of European laboratories: an external quality assessment study. Eur J Clin Microbiol Infect Dis 2012, 31:1765-1770.
• [50]Datta P, Vasdeva HR, Chander J: Optimization of multiple muco-cutaneous site sampling method for screening MRSA colonization in ICU. Indian J Crit Care Med 2013, 17:243-245.
• [51]Matheson A, Christie P, Stari T, Kavanagh K, Gould IM, Masterton R, Reilly JS: Nasal swab screening for methicillin-resistant Staphylococcus aureus–how well does it perform? A cross-sectional study. Infect Control Hosp Epidemiol 2012, 33:803-808.
• [52]Meurman O, Routamaa M, Peltonen R: Screening for methicillin-resistant Staphylococcus aureus: which anatomical sites to culture? J Hosp Infect 2005, 61:351-353.