Prevalence of methicillin-resistant Staphylococcus aureus in healthy Chinese population: A system review and meta-analysis

Autoři: Man Wu aff001;  Xiang Tong aff001;  Sitong Liu aff001;  Dongguang Wang aff001;  Lei Wang aff001;  Hong Fan aff001
Působiště autorů: Department of Respiratory and Critical Care Medicine, West China Hospital/West China School of Medicine, Sichuan University, Chengdu, China aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article



To comprehensively determine the prevalence of MRSA in healthy Chinese population, the influencing factors of MRSA colonization and its antibiotic resistance.


Articles that studied prevalence or influencing factors of MRSA carriage in healthy Chinese population were retrieved from PubMed, Ovid database, three Chinese electronic databases. The pooled prevalence of MRSA, its antibiotic resistance and influencing factors were analyzed by STATA12.0.


37 studies were included. The pooled prevalence of MRSA was 21.2% (95% CI: 18.5%-23.9%), and the prevalence of S.aureus was 15% (95% CI: 10%-19%), with a significant heterogeneity (MRSA: I2 = 97.6%, P<0.001; S.aureus: I2 = 98.4%, P < 0.001). In subgroup analysis, the pooled prevalence of MRSA was 28% (95%CI: 10%-51%) for Livestock-related workers, 18% (95%CI: 11%-26%) for children, 20% (95%CI: 12%-29%) for healthcare workers, 7% (95%CI: 3%-13%) for community residents. The prevalence of MRSA in studies with oxacillin disk diffusion method (28%, 95%CI: 21%-35%) seemed higher than that with the mecA gene method(12%, 95%CI: 7%-19%). MRSA in studies conducted in Taiwan was more common than in Mainland China and Hong Kong. Similar results were found in meta-regression. Influencing factors for MRSA colonization were noted in seven eligible studies, they included younger age (OR: 3.54, 95% CI: 2.38–5.26; OR: 2.24, 95% CI: 1.73–2.9), attending day care centers (DCCs) (OR: 1.95, 95% CI: 1.4–2.72; OR: 1.53, 95% CI: 1.2–1.95), flu vaccination (OR:1.73, 95% CI: 1.28–2.35), using antibiotics within the past year (OR: 2.05, 95% CI:1.35–3.11), residing in northern Taiwan (OR: 1.45, 95% CI: 1.19–1.77), regular visits to health care facility (OR: 23.83, 95% CI: 2.72–209.01), household member working in health care facility (OR: 8.98, 95% CI:1.4–55.63), and contact with livestock (OR: 6.31, 95% CI: 3.44–11.57). Moreover, MRSA was found to be highly resistant to penicillin, ampicillin, erythromycin, and clindamycin, with a pooled resistance ratio of 100, 93, 88, and 75%, respectively. However, no resistance were noted to vancomycin.


The pooled prevalence of MRSA was considerably high in health Chinese population. Additionally, these strains showed extreme resistance to penicillin, ampicillin, erythromycin and clindamycin. Public MRSA protection measures and the surveillance of MRSA should be strengthened to reduce the spread of MRSA among hospitals, communities, and livestock.

Klíčová slova:

Antibiotics – Bacterial disk diffusion – Hong Kong – Child health – Methicillin-resistant Staphylococcus aureus – Taiwan – Veterinary medicine


1. Hassoun A, Linden PK, Friedman B. Incidence, prevalence, and management of MRSA bacteremia across patient populations—a review of recent developments in MRSA management and treatment. Critical Care. 2017;21:211. doi: 10.1186/s13054-017-1801-3 28807042

2. Sahreena L, Zhang KY. Methicillin-Resistant Staphylococcus aureus: Molecular Characterization, Evolution, and Epidemiology. Clin Microbiol Rev, 2018,12;31(4).

3. Hurley JC. Risk of death from methicillin-resistant Staphylococcus aureus bacteraemia: a meta-analysis. Med J Aust. 2002;176:264–267.

4. Jokinen E, Laine J, Huttunen R, Rahikka P, Huhtala H, Vuento R, et al. Comparison of outcome and clinical characteristics of bacteremia caused by methicillin-resistant, penicillin-resistant and penicillin-susceptible Staphylococcus aureus strains. Infect Dis. 2017;49:493–500.

5. Stryjewski ME, Corey GR. Methicillin-resistant Staphylococcus aureus: an evolving pathogen. Clinical Infectious Diseases. 2014;58 Suppl 1:S10.

6. Abdulgader SMA, Shittu A, Nicol MP, Kaba M. Molecular epidemiology of methicillin-resistant Staphylococcus aureus in Africa: A systematic review of the published literature. International Journal of Infectious Diseases. 2014;21:107–107.

7. Chih-Jung C, Kuang-Hung H, Tzou-Yien L, Kao-Pin H, Po-Yen C, Yhu-Chering H. Factors associated with nasal colonization of methicillin-resistant Staphylococcus aureus among healthy children in Taiwan. Journal of Clinical Microbiology. 2011;49:131. doi: 10.1128/JCM.01774-10 21084507

8. Philippe C, Hélène M, Olivier J, Josiane C, Anne-Laure BU. Molecular evidence that nasal carriage of Staphylococcus aureus plays a role in respiratory tract infections of critically ill patients. Journal of Clinical Microbiology. 2005;43:3491–3. doi: 10.1128/JCM.43.7.3491-3493.2005 16000487

9. Yhu-Chering H, Chen-Fang H, Chih-Jung C, Lin-Hui S, Tzou-Yien L. Nasal carriage of methicillin-resistant Staphylococcus aureus in household contacts of children with community-acquired diseases in Taiwan. Pediatric Infectious Disease Journal. 2007;26:1066–1068. doi: 10.1097/INF.0b013e31813429e8 17984820

10. Liu W, Liu Z, Yao Z, Fan Y, Ye X, Chen S. The prevalence and influencing factors of methicillin-resistant Staphylococcus aureus carriage in people in contact with livestock: A systematic review. Ajic American Journal of Infection Control. 2015;43:469–475.

11. Boyle MH. Guidelines for evaluating prevalence studies. Evidence-Based Mental Health. 1998;1:37–39.

12. Dersimonian R, Nan L. Meta-analysis in clinical trials revisited. Contemporary Clinical Trials. 2015;45:139–145. doi: 10.1016/j.cct.2015.09.002 26343745

13. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Statistics in Medicine. 2002.

14. Barendregt JJ, Doi SA, Yong YL, Norman RE, Vos T. Meta-analysis of prevalence. J Epidemiol Community Health. 2013;67:974–978. doi: 10.1136/jech-2013-203104 23963506

15. Ye X, Liu W, Fan Y, Wang X, Zhou J, Yao Z, et al. Frequency-risk and duration-risk relations between occupational livestock contact and methicillin-resistant Staphylococcus aureus carriage among workers in Guangdong, China. Ajic American Journal of Infection Control. 2015;43:676–681.

16. Fan J, Zhou W, Shu M, Deng JJ, Zhu Y, Deng S Y, et al. Nasal carriage of community-acquired methicillin-resistant Staphylococcus aureus in healthy children from Chengdu. Chinese Journal of Contemporary Pediatrics. 2011;13:16–19. 21251379

17. Zhang W, Hao Z, Wang Y, Cao X, Logue CM, Wang B, et al. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and veterinary staff in China. Veterinary Journal. 2011;190:e125–e129.

18. Xiao XM, Sun DD, Wang S, Wang ML, Li M, Shang H, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus among preclinical medical students: epidemiologic and molecular characteristics of methicillin-resistant S. aureus clones. Diagn Microbiol Infect Dis. 2011;70:22–30. doi: 10.1016/j.diagmicrobio.2010.12.004 21513841

19. Ma XX, Luo EJ. Distribution of Staphylococcus aureus strains colonized in healthy community population and molecular epidemiological characteristics for MRSA strains. Chin J Epidemiol. 2011;32:804–807.

20. Chen B, Dai X, He B, Pan K, Li H, Liu X, et al. Differences in Staphylococcus aureus nasal carriage and molecular characteristics among community residents and healthcare workers at Sun Yat-Sen University, Guangzhou, Southern China. Bmc Infectious Diseases. 2015;15:303. doi: 10.1186/s12879-015-1032-7 26223250

21. Jimei D, Chun C, Baixing D, Jinjing T, Zhiqiang Q, Chris P, et al. Molecular characterization and antimicrobial susceptibility of nasal Staphylococcus aureus isolates from a Chinese medical college campus. Plos One. 2011;6:e27328. doi: 10.1371/journal.pone.0027328 22114670

22. O'Donoghue MM, Boost MV. The prevalence and source of methicillin-resistant Staphylococcus aureus (MRSA) in the community in Hong Kong. Epidemiology & Infection. 2004;132:1091–1097.

23. Xie X, Dai X, Ni L, Chen B, Luo Z, Yao Y, et al. Molecular epidemiology and virulence characteristics of Staphylococcus aureus nasal colonization in medical laboratory staff: comparison between microbiological and non-microbiological laboratories. Bmc Infectious Diseases. 2018;18:122. doi: 10.1186/s12879-018-3024-x 29529992

24. Yan X, Song Y, Yu X, Tao X, Yan J, Luo F, et al. Factors associated with Staphylococcus aureus nasal carriage among healthy people in Northern China. Clinical Microbiology & Infection the Official Publication of the European Society of Clinical Microbiology & Infectious Diseases. 2015;21:157–162.

25. Chen BJ, Xie XY, Ni LJ, Dai XL, Lu Y, Wu XQ, et al. Factors associated with Staphylococcus aureus nasal carriage and molecular characteristics among the general population at a Medical College Campus in Guangzhou, South China. Annals of Clinical Microbiology & Antimicrobials. 2017;16:28.

26. Chen CH, Kuo KC, Hwang KP, Lin TY, Huang YC. Risk factors for and molecular characteristics of methicillin-resistant Staphylococcus aureus nasal colonization among healthy children in southern Taiwan, 2005–2010. Journal of Microbiology, Immunology and Infection.

27. Deng JJ, Wan CM, Mu D Z, Zhou w, Xu AL, Fan J, et al. Nasal Carriage of Community-acquired Staphylococcu saureus and Drug Sensitivity Testsin Healthy Children in Chengdu. J Sichuan Univ (MedSciEdi). 2012;43:391–394.

28. Zhang M, O’Donoghue MM, Ito T, Hiramatsu K, Boost MV. Prevalence of antiseptic-resistance genes in Staphylococcus aureus and coagulase-negative staphylococci colonising nurses and the general population in Hong Kong. Journal of Hospital Infection. 2011;78:113–117. doi: 10.1016/j.jhin.2011.02.018 21507521

29. Ho PL, Chiu SS, Chan MY, Gan Y, Chow KH, Lai EL, et al. Molecular epidemiology and nasal carriage of Staphylococcus aureus and methicillin-resistant S. aureus among young children attending day care centers and kindergartens in Hong Kong. Journal of Infection. 2012;64:500–506. doi: 10.1016/j.jinf.2012.02.018 22406412

30. Gong Z, Shu M, Xia Q, Tan S, Zhou W, Zhu Y, et al. Staphylococcus aureus nasal carriage and its antibiotic resistance profiles in children in high altitude areas of Southwestern China. Archivos Argentinos De Pediatria. 2017;115:274. doi: 10.5546/aap.2017.eng.274 28504494

31. Boost MV, So SYC, Perreten V. Low rate of methicillin-resistant coagulase-positive staphylococcal colonization of veterinary personnel in Hong Kong. Zoonoses & Public Health. 2011;58:36–40.

32. Jin-Jian FU, Xiao-Hua YE, Yao ZJ, Fan YP, Chen SD. Antibiotic resistance of Staphylococcus aureus from the nasal carriage in healthy school children. Modern Preventive Medicine. 2015.

33. Ge YL, Chen YH, Zhu SY, Shen W. Study on Methicllin—Resistant Staplococccus aureus Carrying and Drug—Resistance Related Genes In Medical Staff. Chin J Disinfection. 2012;29:565–568.

34. Liu H, Fei CN, Dong J, Shen P, Liu J, Ji XY, et al. Study of bacterium drug—resistance in nasal vestibular of medical staff. Chin J Disinfection. 2016;33:983–985.

35. Zhong J, Zhang C, Lai L, Yu X, Wang X, Ye X. Carriage and antibiotic resistance of methicillin resistant Staphylococcus aureus isolates among meat processing and sales workers. Chin J Nosocomio. 2016;26:5315–5317.

36. Yhu-Chering H, Kao-Pin H, Po-Yen C, Chih-Jung C, Tzou-Yien L. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among Taiwanese children in 2005 and 2006. Journal of Clinical Microbiology. 2007;45:3992–5. doi: 10.1128/JCM.01202-07 17942647

37. Po-Liang L, Lien-Chun C, Chien-Fang P, Yi-Hsiung C, Tyen-Po C, Ling M, et al. Risk factors and molecular analysis of community methicillin-resistant Staphylococcus aureus carriage. Journal of Clinical Microbiology. 2005;43:132. doi: 10.1128/JCM.43.1.132-139.2005 15634961

38. Wen-Tsung L, Wei-Jen L, Min-Hua T, Sheng-Ru W, Mong-Ling C, Chih-Chien W. Methicillin-resistant Staphylococcus aureus in children, Taiwan. Emerging Infectious Diseases. 2006;12:1267–1270. doi: 10.3201/eid1208.051570 16965712

39. Huang YC, Su LH, Chen CJ, Lin TY. Nasal carriage of methicillin-resistant Staphylococcus aureus in school children without identifiable risk factors in northern taiwan. Pediatric Infectious Disease Journal. 2005;24:276–278. doi: 10.1097/01.inf.0000154333.46032.0f 15750471

40. Chen CS, Chen CY, Huang YC. Nasal carriage rate and molecular epidemiology of methicillin-resistant Staphylococcus aureus among medical students at a Taiwanese university. International Journal of Infectious Diseases Ijid Official Publication of the International Society for Infectious Diseases. 2012;16:e799–e803. doi: 10.1016/j.ijid.2012.07.004 22878173

41. Wang JT, Liao CH, Fang CT, Chie WC, Lai MS, Lauderdale TL, et al. Prevalence of and risk factors for colonization by methicillin-resistant Staphylococcus aureus among adults in community settings in Taiwan. Journal of Clinical Microbiology. 2009;47:2957. doi: 10.1128/JCM.00853-09 19625471

42. Pan HH, Huang YC, Chen CJ, Huang FL, Ting PJ, Huang JY, et al. Prevalence of and risk factors for nasal methicillin-resistant Staphylococcus aureus colonization among children in central Taiwan. Journal of Microbiology Immunology & Infection. 2017S1684118217300634.

43. Wang HK, Huang CY, Chen CJ, Huang YC. Nasal Staphylococcus aureus and methicillin-resistant Staphylococcus aureus carriage among college student athletes in northern Taiwan. Journal of microbiology, immunology, and infection = Wei mian yu gan ran za zhi. 2017;50:S1684118217300749.

44. Wu TH, Lee CY, Yang HJ, Fang YP, Chang YF, Tzeng SL, et al. Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus among nasal carriage strains isolated from emergency department patients and healthcare workers in central Taiwan. Journal of Microbiology, Immunology and Infection.

45. Wen-Tsung L, Chih-Chien W, Wei-Jen L, Sheng-Ru W, Ching-Shen T, Ching-Feng H, et al. Changes in the nasal colonization with methicillin-resistant Staphylococcus aureus in children: 2004–2009. Plos One. 2010;5:e15791–e15791. doi: 10.1371/journal.pone.0015791 21209954

46. Huang Y-C, Chen C-J. Nasal Carriage of Methicillin-resistant Staphylococcus aureus During the First 2 Years of Life in Children in Northern Taiwan. Pediatric Infectious Disease Journal. 2015;34:131–5. doi: 10.1097/INF.0000000000000517 25144800

47. Lu PL, Tsai J-C, Chiu Y-W, Chang F-Y, Chen Y-W, Hsiao C-F, et al. Methicillin-resistant Staphylococcus aureus carriage, infection and transmission in dialysis patients, healthcare workers and their family members. Nephrology, dialysis, transplantation: official publication of the European Dialysis and Transplant Association—European Renal Association. 2008;23:1659.

48. Qu F, Cui E, Guo T, Li H, Chen S, Liu L, et al. Nasal Colonization of and Clonal Transmission of Methicillin-Susceptible Staphylococcus aureus among Chinese Military Volunteers. Journal of Clinical Microbiology. 2010;48:64–9. doi: 10.1128/JCM.01572-09 19889899

49. Chen CJ, Wang S-C, Chang H-Y, Huang Y-C. Longitudinal Analysis of Methicillin-Resistant and Methicillin-Susceptible Staphylococcus aureus Carriage in Healthy Adolescents. Journal of Clinical Microbiology. 2013;51:2508–2514. doi: 10.1128/JCM.00572-13 23678067

50. Chun-Jui C, Ning-Chun C, Chong-Kei L, Yhu-Chering H, Srinand S. Nasal Staphylococcus aureus and Methicillin-Resistant S. aureus Carriage among Janitors Working in Hospitals in Northern Taiwan. Plos One. 2015;10:e0138971. doi: 10.1371/journal.pone.0138971 26407070

51. Prevalence, Influencing Factors, Antibiotic Resistance, Toxin and Molecular Characteristics of Staphylococcus aureus and MRSA Nasal Carriage among Diabetic Population in the United States, 2001–2004

52. Hu FP, Guo Y, Zhu DM, Wang F, Jiang XF, Xu YC, et al. CHINET surveillance of bacterial resistance across China: report of the results in 2016. Chin J of Infect Chemother. 2017;17:7–17.

53. Heijer CDJ, Den, Bijnen EME, Van W John P, Mike P, Herman G, Bruggeman CA, et al. Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infectious Diseases. 2013;13:409–415. doi: 10.1016/S1473-3099(13)70036-7 23473661

54. Wang XL, Li L, Li SM, Huang JY, Fan YP, Yao ZJ, et al. Phenotypic and molecular characteristics of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus in slaughterhouse pig-related workers and control workers in Guangdong Province, China. Epidemiology and Infection.

55. Chen CJ, Lauderdale TY, Lu CT, Chuang YY, Yang CC, Wu TS, et al. Clinical and molecular features of MDR livestock-associated MRSA ST9 with staphylococcal cassette chromosome mecXII in humans. J Antimicrob Chemother. 2017;73:33–40.

56. Dulon M, Peters C, Schablon A, Nienhaus A. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. Bmc Infectious Diseases. 2014;14:1–14. doi: 10.1186/1471-2334-14-1

57. Ken H, Kyoko KA, Munetaka Y, Teruyo I, Yasuo N, Longzhu C, et al. Dissemination of methicillin-resistant staphylococci among healthy Japanese children. Journal of Clinical Microbiology. 2005;43:3364–3372. doi: 10.1128/JCM.43.7.3364-3372.2005 16000461

58. Brown J. DF. Guidelines for the laboratory diagnosis and susceptibility testing of methicillin-resistant Staphylococcus aureus (MRSA). Journal of Antimicrobial Chemotherapy. 2005;56:1000. doi: 10.1093/jac/dki372 16293678

59. Kali A, Stephen S, Umadevi S. Laboratory Evaluation of Phenotypic Detection Methods of Methicillin-Resistant Staphylococcus Aureus. Biomedical Journal. 2014;37:411–414. doi: 10.4103/2319-4170.132907 25179712

60. Quinn GA, Cole AM. Suppression of innate immunity by a nasal carriage strain of Staphylococcus aureus increases its colonization on nasal epithelium. Immunology. 2010;122:80–89.

61. Gili RY, Krzysztof T, Thompson CM, Richard M, Marc L. Interference between Streptococcus pneumoniae and Staphylococcus aureus: In vitro hydrogen peroxide-mediated killing by Streptococcus pneumoniae. Journal of Bacteriology. 2006;188:4996. doi: 10.1128/JB.00317-06 16788209

62. Soltani B, Ardakani AT, Moravveji A, Erami M, Rezaei MH, Moniri R, et al. Risk Factors for Methicillin Resistant Staphylococcus aureus Nasal Colonization of Healthy Children. Jundishapur Journal of Microbiology. 2014;7:e20025. doi: 10.5812/jjm.20025 25485071

63. Waters EM, Rudkin JK, Coughlan S, Clair GC, Adkins JN, Gore S, et al. Redeploying β-Lactam Antibiotics as a Novel Antivirulence Strategy for the Treatment of Methicillin-Resistant Staphylococcus aureus Infections. Journal of Infectious Diseases. 2017;215:80. doi: 10.1093/infdis/jiw461 28077586

64. Jarajreh D, Aqel A, Alzoubi H, Al-Zereini W. Prevalence of inducible clindamycin resistance in methicillin-resistant Staphylococcus aureus: the first study in Jordan. Journal of Infection in Developing Countries. 2017;11:350. doi: 10.3855/jidc.8316 28459227

65. Lall M, Sahni AK. Prevalence of inducible clindamycin resistance in Staphylococcus aureus isolated from clinical samples. Medical Journal Armed Forces India. 2014;70:43–47.

66. Sievert DM, Rudrik JT, Patel JB, Mcdonald LC, Wilkins MJ, Hageman JC. Vancomycin-resistant Staphylococcus aureus in the United States, 2002–2006. Clinical Infectious Diseases. 2008;46:668–674. doi: 10.1086/527392 18257700

67. Susana G, Alexander T. Mechanisms of vancomycin resistance in Staphylococcus aureus. Journal of Clinical Investigation. 2014;124:2836. doi: 10.1172/JCI68834 24983424

68. Rodvold KA, Mcconeghy KW. Methicillin-resistant Staphylococcus aureus therapy: past, present, and future. Clinical Infectious Diseases. 2014;58 Suppl 1:S20.

69. Bitterman Y, Laor A, Itzhaki S, Weber G. Characterization of the best anatomical sites in screening for methicillin-resistant Staphylococcus aureus colonization. European Journal of Clinical Microbiology & Infectious Diseases. 2010;29:391–397.

70. Wertheim HF, Melles DC, Vos MC, Leeuwen WV, Belkum AV, Verbrugh HA, et al. The role of nasal carriage in Staphylococcus aureus infections. Lancet Infectious Diseases. 2005;5:751–762. doi: 10.1016/S1473-3099(05)70295-4 16310147

Článek vyšel v časopise


2019 Číslo 10
Nejčtenější tento týden