Summary of studies included in the meta-analysis (n=37)
Country | Study type | Period | Sex* | Age | Exposed population | Control population | Samples | Main Spa types of LA-MRSA | Non-LA-MRSA colonisation | Infection | |
Angen et al 21 | Denmark | One-week longitudinal study. | 2016 | 27/7 | – | 48 volunteers visiting a swine farm. | 46 passive observers. | Nasal and throat swabs. | LA-MRSA CC398 (t011). | ||
Bisdorff et al 18 | Germany | Cross-sectional study. | 2009–2010 | Non-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 Netherlands | Longitudinal study | – | 291/371 | 30.7 (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 | Germany | Cross-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 | Belgium | Cross-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 | Taiwan | Cross-sectional study. | June–October 2012 | 16/84 | 52 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 Netherlands | Cross-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 26† | Belgium, Denmark and The Netherlands | 6 months longitudinal study. | 2009–2010 | – | – | 15 pig farmers. | 45 household members. | Nasal swabs. | ST398 (t011, t034, t0108 and t1451). | ||
Gracia-Graells et al 25 | Belgium | Cross-sectional study, Belgium. | February–April 2010 | 50/96 | 45.1 | 105 veterinarians working with livestock. | 41 veterinarians not working with livestock. | Nasal swabs. | ST398 (t011, t034, t1451 and so on). | – | |
Gracia-Graells et al 25 | Denmark | Cross-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 Netherlands | Cross-sectional study. | October 2007–March 2008 | 177/213 | 0–85 | 97 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 | USA | Cross-sectional study. | 2014 | Adult: 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 | Switzerland | Conference participants. | March–September 2009 | – | – | 148 pig farmers and 133 veterinarians. | 179 slaughterhouse employees. | Nasal swabs. | All CC398 (ST8 t064, ST398 t011 and t034). | ||
Köck et al 31 | Germany | Case–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 | Denmark | Case–control study. | 2004–2007 | Case-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 | Denmark | Conference participants. | August 2006–February 2007 | – | – | 231 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 | Germany | Cross-sectional study. | June–October 2012 | – | – | 63 occupationally exposed individuals. | 126 patients. | Nasal and rectal swabs. | Farmers CC398; 4/126 control inpatients CC398. | ||
Nadimpalli et al 35 | USA | Cross-sectional study. | October 2013–February 2014 | 94/89 | Mean: 30. | 103 IHO workers. | 80 family members. | Nasal swabs. | CC398 | 6 IHO and 6 of 80 household members had SSTI. | |
Neyra et al‡36 | USA | Cross-sectional study. | September–November 2011 | 196/140 | 15–82 | 162 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 | Switzerland | Cross-sectional study. | June 2008–July 2009 | – | – | 75 pig farmers and veterinarians. | 128 persons without animal contact. | Nasal swabs. | CC398. | – | |
Pletinckx et al 38 | Belgium | Cross-sectional study. | July 2009–October 2010 | – | – | 10 farmers and 10 veterinarians. | 13 family members (living in farms). | Nasal swabs. | ST398 (t011 t034 t567). | ||
Richter et al 39 | Germany | Cross-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 | USA | Cross-sectional study. | May–December 2011 | ILO: 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 | Australia | Cross-sectional study. | 2015 | 12/40 | – | 37 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 | Germany | Cross-sectional study. | June–December 2012 | – | – | 79 pig farmers. | 7 family members. | Nasal swabs. | ST398 (t011 and t034). | ||
van Cleef et al 44 45† | The Netherlands | Prospective cohort study. | 2010–2011 | 103/68 | Median: 16 (0–70). | 110 pig farmers. | 171 household members. | Nasal swabs. | MLVA complex (MC) 398. | ||
van den Broek et al 46 | The Netherlands | Cross-sectional study. | January–October 2007 | 107/125 | 0–86 | 50 farmers. | 171 family members and 11 coworkers. | Anterior nasal swabs. | ST398 (t108, t011 and t567 and others). | – | |
Van Cleef et al 43 | The Netherlands | Cross-sectional study. | 2008 | 16/233 | Mean: 43. | 207 slaughterhouse workers, 13 veterinarians and auxiliaries. | 29 administrative and technical personnel. | Nasal swabs. | ST398 (t011 and t108). | ||
Vandendriessche et al 49 | Belgium | Cross-sectional study. | August 2009–May 2011 | – | – | 149 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 Netherlands | Cross-sectional study. | November 2013–September 2014 | – | – | 11 turkey farmers. | 32 family members and employees. | Nasal swabs. | ST398 (t011) | ||
van Loo et al 48 | The Netherlands | Case–control study. | 2003–2005 | 56/55 | Case: 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 Netherlands | A 1-year prospective cohort study. | 2009–2011 | – | 18–65. | 135 livestock veterinarians. | 386 non-exposed household members. | Anterior nares or oropharynx swabs. | MC398. | ||
Walter et al 51 52 | Germany | Prospective cohort study. | 2011–2014 | – | Median of 45 for LA-MRSA participants. | 1435 participants of veterinary congresses. | Nasal swabs. | CC398 (t011, t034 and t571). | |||
Wang et al 13 | China | Cross-sectional study. | November 2013–November 2014 | 597/593 | Workers: 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 Netherlands | Prospective surveillance study. | – | 726/127 | Mean: 36.9. | 222 healthcare worker. | 633 controls. | Throat and nasal swabs. | ST398 (t108). | ||
Ye et al 14 | China | Cross-sectional study. | November 2013–November 2014 | 669/1191 | 15–60 | 682 occupational livestock workers (224 farm workers, 20 veterinarians, 194 slaughterhouse workers and 244 butchers). | 1178 controls | Anterior 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.