Table 1

Summary of studies included in the meta-analysis (n=37)

CountryStudy typePeriodSex*AgeExposed populationControl populationSamplesMain Spa types of LA-MRSANon-LA-MRSA colonisationInfection
Angen et al 21 DenmarkOne-week longitudinal study.201627/748 volunteers visiting a swine farm.46 passive observers.Nasal and throat swabs.LA-MRSA CC398 (t011).
Bisdorff et al 18 GermanyCross-sectional study.2009–2010Non-OLC: 913/742; OLC: 58/132.Non-OLC: 42.2; OLC 42.7.1655 OLC group.190 non-OLC group.Nasal swabs.ST398 (t034 and t011).7 out of 25 non-OLC carried HA-MRSA.
Bos et al 22 The NetherlandsLongitudinal study291/37130.7 (0–83)182 pig farmers and 67 cattle farmers.286 family members of pig farmers and 127 of cattle farmers.Nasal swabs.ST398
Cuny et al 23 GermanyCross-sectional study.September 2007–January 2009--113 pig farmers; 49 veterinarians.116 non-exposed family members of pig farmers; 44 non-exposed family members of veterinarians.Nasal swabs.ST398 (t011, t034, t2974 and t108).
Denis et al 24 BelgiumCross-sectional.April–July 2007--75 pig farmers.27 persons without pig contact.Nasal swabs and wound.ST398 (t011, t034 and t567).One LA-MRSA carrier had hand lesion infection.
Fang et al 12 TaiwanCross-sectional study.June–October 201216/8452 pig farm workers.32 auction market employers and 16 regular visitors.Nasal swabs.ST9 (t899 and t1939).Three farmers carried CA-MRSA.
Geenen et al 27 The NetherlandsCross-sectional study.July 2010–May 2011.Mean: 36.47 farmers.89 family members and 9 employees.Nasal swabs.ST398 (t011, t034 and t0108).
Gracia-Graells et al 26Belgium, Denmark and The Netherlands6 months longitudinal study.2009–201015 pig farmers.45 household members.Nasal swabs.ST398 (t011, t034, t0108 and t1451).
Gracia-Graells et al 25 BelgiumCross-sectional study, Belgium.February–April 201050/9645.1105 veterinarians working with livestock.41 veterinarians not working with livestock.Nasal swabs.ST398 (t011, t034, t1451 and so on).
Gracia-Graells et al 25 DenmarkCross-sectional study, Denmark.February–October 2010--97 veterinarians working with livestock.46 veterinarians not working with livestock.Nasal swabs.ST398 (t011, t034, t1451 and so on).
Graveland et al 28 The NetherlandsCross-sectional study.October 2007–March 2008177/2130–8597 calf farmers.259 family members and 34 employees.Nasal swabs.ST398 except four (t002, t015, t084 and t166).1 HA-MRSA and 3 CA-MRSA carriers.
Hatcher et al 29 USACross-sectional study.2014Adult: 252/148; children: 187/213.198 IHO worker–child household pairs.202 community referent adult–child household pairs.Nasal swabs.ST5 (t002), ST8 (t008 and t088).
Huber et al 30 SwitzerlandConference participants.March–September 2009148 pig farmers and 133 veterinarians.179 slaughterhouse employees.Nasal swabs.All CC398 (ST8 t064, ST398 t011 and t034).
Köck et al 31 GermanyCase–control study.January 2005–December 2008.Case group: 23/77; control: 38/62.Case group: 48; control: 54.100 patients with LA-MRSA.100 patients with other than LA-MRSA.Nasal swabs.ST398 (t011, t034, t108 and t1451).
Lewis et al 32 DenmarkCase–control study.2004–2007Case-patients: 13/8.Median of case-patients 29 (8 monnths–80 years).21 case patients with CC398 MRSA.42 controls.MRSA isolates from patients.ST398 (t034, t108 and t1793).10 case-patients had reported SSTI.
Moodley et al 33 DenmarkConference participants.August 2006–February 2007231 veterinarians, 72 veterinary students or nurses, 98 farmers.301 unexposed persons.Nasal swabs.CC8 (t008), CC22 (t020 and t022), CC59 (t216), CC88 (t186) CC398 (t011 and t034).Exposed: 6/9 were LA-MRSA carriers; unexposed: 1/2 was LA-MRSA carrier.
Mutters et al 34 GermanyCross-sectional study.June–October 201263 occupationally exposed individuals.126 patients.Nasal and rectal swabs.Farmers CC398; 4/126 control inpatients CC398.
Nadimpalli et al 35 USACross-sectional study.October 2013–February 201494/89Mean: 30.103 IHO workers.80 family members.Nasal swabs.CC3986 IHO and 6 of 80 household members had SSTI.
Neyra et al36 USACross-sectional study.September–November 2011196/14015–82162 hog slaughter workers.63 household members of plant workers and 111 community residents.Nasal swabs.ST1 (LA-MRSA), ST5 (HA-MRSA), ST8, 1 of ST72 (CA-MRSA) and ST398.
Oppliger et al 37 SwitzerlandCross-sectional study.June 2008–July 200975 pig farmers and veterinarians.128 persons without animal contact.Nasal swabs.CC398.
Pletinckx et al 38 BelgiumCross-sectional study.July 2009–October 201010 farmers and 10 veterinarians.13 family members (living in farms).Nasal swabs.ST398 (t011 t034 t567).
Richter et al 39 GermanyCross-sectional study.June–October 2009--39 people with frequent contact with turkeys.20 persons being rarely or never in turkey houses.Nasal swabs.ST398 (t011 and t034).
Rinsky et al 40 USACross-sectional study.May–December 2011ILO: 59/40; AFLO: 46/59.80 ILO workers.19 household members of ILO workers, 92 AFLO workers and their 13 household members.Nasal swabs.CC398
Sahibzada et al 41 AustraliaCross-sectional study.201512/4037 piggery staff working in pig contact.15 workers working in the agriculture or feedmill section.Nasal swabs.LA-MRSA ST398.29 piggery staff carried ST93; two workers working in the agriculture or feedmill carried ST93.
Schmithausen et al 42 GermanyCross-sectional study.June–December 201279 pig farmers.7 family members.Nasal swabs.ST398 (t011 and t034).
van Cleef et al 44 45The NetherlandsProspective cohort study.2010–2011103/68Median: 16 (0–70).110 pig farmers.171 household members.Nasal swabs.MLVA complex (MC) 398.
van den Broek et al 46 The NetherlandsCross-sectional study.January–October 2007107/1250–8650 farmers.171 family members and 11 coworkers.Anterior nasal swabs.ST398 (t108, t011 and t567 and others).
Van Cleef et al 43 The NetherlandsCross-sectional study.200816/233Mean: 43.207 slaughterhouse workers, 13 veterinarians and auxiliaries.29 administrative and technical personnel.Nasal swabs.ST398 (t011 and t108).
Vandendriessche et al 49 BelgiumCross-sectional study.August 2009–May 2011149 farmers: pig (25), veal (45), dairy (22), beef (21) and broiler (36).42 farmers and family members living on horticulture farms.Nasal swabs.CC398 (t011, t034 and t567).
van Duijkeren et al 47 The NetherlandsCross-sectional study.November 2013–September 201411 turkey farmers.32 family members and employees.Nasal swabs.ST398 (t011)
van Loo et al 48 The NetherlandsCase–control study.2003–200556/55Case: 42.7; control: 47.2.35 case patients with CC398.76 control patients with non-CC398 MRSA.NT-MRSA isolates from patients.ST398 (t108, t011, t034 and t571).
Verkade et al 50 The NetherlandsA 1-year prospective cohort study.2009–201118–65.135 livestock veterinarians.386 non-exposed household members.Anterior nares or oropharynx swabs.MC398.
Walter et al 51 52 GermanyProspective cohort study.2011–2014Median of 45 for LA-MRSA participants.1435 participants of veterinary congresses.Nasal swabs.CC398 (t011, t034 and t571).
Wang et al 13 ChinaCross-sectional study.November 2013–November 2014597/593Workers: 39.3 controls: 36.4.335 pig-related workers (including 178 slaughterhouse workers and 157 butchers).855 control workers.Nasal swabs.Only 4 MRSA in workers and 3 in controls were LA.
Wulf et al 53 The NetherlandsProspective surveillance study.726/127Mean: 36.9.222 healthcare worker.633 controls.Throat and nasal swabs.ST398 (t108).
Ye et al 14 ChinaCross-sectional study.November 2013–November 2014669/119115–60682 occupational livestock workers (224 farm workers, 20 veterinarians, 194 slaughterhouse workers and 244 butchers).1178 controlsAnterior nasal swabs.CC9 (ST9, ST63 and ST2359).Farmers: 18/48 were LA-MRSA; controls: 2/16 were LA-MRSA.
  • *The number of female and male participants.

  • †LA-MRSA carriers were those who were colonised by LA-MRSA persistently or intermittently.

  • ‡Tetracycline resistance was considered as the marker for livestock association among MRSA strains that showed resistance to cefoxitin.

  • AFLO, antibiotic free livestock operation; CA, community-associated; HA, healthcare associated; IHO, industrial hog operation; LA, livestock-associated; MLVA, multilocus variable-number-tandem-repeats analysis; OLC, occupational livestock contact; Spa, Staphylococcus aureus protein A; SSTI, skin and soft tissue infection.