Prevalence of methicillin-resistant staphylococcus aureus in healthy population in China: a meta-analysis_Chinese Journal of Evidence-Based Medicine

Authors：

YANG Xue ¹ , LI Xiaobo ² , HAN Jing ² , XU Li ¹ , ZOU Linlin ¹ , WANG Jin ¹ , HU Zhong ¹ ,  ZHENG Juan ¹

1. Department of Respiratory Medicine, The First People’s Hospital of Chongqing Liang Jiang New Area, Chongqing, 401121, P.R.China;
2. Department of Respiratory Medicine, Chengdu Seventh People’s Hospital, Chengdu, 610000, P.R.China;
3. Department of Respiratory and Critical Care Medicine, Gui Zhou Provincial People’s Hospital, Guiyang, 550002, P.R.China;

Corresponding author：

ZHENG Juan, Email: zhengjuanlx@163.com

Keywords：

China; Healthy population; MRSA; Prevalence; Meta-analysis; Cross-sectional study

DOI：

10.7507/1672-2531.201904042

Video：

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Objectives To systematically review the prevalence of methicillin-resistant staphylococcus aureus (MRSA) in healthy Chinese population.Methods PubMed, EMbase, WanFang Data and CNKI databases were electronically searched to collect cross-sectional studies of the prevalence of MRSA in China from inception to December 16^th, 2018. Two reviewers independently screened literature, extracted data and assessed the risk of bias of included studies, and then, meta-analysis was performed by using Stata 12.0 software.Results A total of 25 cross-sectional studies were included. The results of meta-analysis showed that: the pooled prevalence of MRSA in healthy population was 13.9% (95%CI 9.6% to 18.2%). The results of subgroup analysis showed that: the prevalence of MRSA in children was 16% (95%CI 8% to 24%), and that in adults (non-children) was 13% (95%CI 9% to 16%). The prevalence of MRSA in individuals with occupational livestock exposure was 28% (95%CI 5% to 51%), in medical staff it was 16% (95%CI 8% to 25%), in medical students it was 12% (95%CI 3% to 20%) and in community residents it was 5% (95%CI 2% to 8%).Conclusions The overall prevalence of MRSA in healthy Chinese population is approximately 13.9%. Effective prevention and control measures are required to reduce the spread of MRSA.

Citation： YANG Xue, LI Xiaobo, HAN Jing, XU Li, ZOU Linlin, WANG Jin, HU Zhong, ZHENG Juan. Prevalence of methicillin-resistant staphylococcus aureus in healthy population in China: a meta-analysis. Chinese Journal of Evidence-Based Medicine, 2019, 19(9): 1037-1043. doi: 10.7507/1672-2531.201904042 Copy

1.	Sahreena L, Zhang KY. Methicillin-resistant staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev, 2018, 31(4): 12.
2.	Hurley JC. Risk of death from methicillin-resistant Staphylococcus aureus bacteraemia: a meta-analysis. Med J Aust, 2002, 176(4): 188-189.
3.	赵旺旺. 耐甲氧西林金黄色葡萄球菌的研究进展. 社区医学杂志, 2006, 11(5): 78-80.
4.	Chen CJ, Hsu KH, Lin TY, et al. Factors associated with nasal colonization of methicillin-resistant Staphylococcus aureus among healthy children in Taiwan. J Clin Microbiol, 2011, 49(1): 131-137.
5.	Huang YC, Ho CF, Chen CJ, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus in household contacts of children with community-acquired diseases in Taiwan. Pediatr Infect Dis J, 2007, 26(11): 1066-1068.
6.	Boyle MH. Guidelines for evaluating prevalence studies. Evid Based Ment Heal, 1998, 1(2): 37-39.
7.	Laird N. Meta-analysis in clinical trials. Control Clin Trials, 1986, 7(3): 177.
8.	Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med, 2002, 21(11): 1539-1558.
9.	Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics, 1994, 50(4): 1088-1101.
10.	Seagroatt V, Stratton I. Bias in meta-analysis detected by a simple, graphical test. Test had 10% false positive rate. BMJ, 1998, 316(7219): 470-470.
11.	Ye X, Liu W, Fan Y, et al. Frequency-risk and duration-risk relations between occupational livestock contact and methicillin-resistant Staphylococcus aureus carriage among workers in Guangdong, China. Am J Infect Control, 2015, 43(7): 676-681.
12.	范娟, 周伟, 舒敏, 等. 成都地区健康儿童鼻腔社区获得性耐甲氧西林金黄色葡萄球菌的携带研究. 中国当代儿科杂志, 2011, 13(1): 16-19.
13.	Zhang W, Hao Z, Wang Y, et al. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and veterinary staff in China. Vet J, 2011, 190(2): e125-e129.
14.	Ma XX, Sun DD, Wang S, 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(1): 22-30.
15.	马笑雪, 罗恩杰. 社区分离金黄色葡萄球菌在健康人群中的分布及其分子生物学特点. 中华流行病学杂志, 2011, 32(8): 804-807.
16.	Chen B, Dai X, He B, 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 Infect Dis, 2015, 15(1): 303.
17.	Du J, Chen C, Ding B, et al. Molecular characterization and antimicrobial susceptibility of nasal Staphylococcus aureus isolates from a Chinese medical college campus. PLoS One, 2011, 6(11): e27328.
18.	O'Donoghue MM, Boost MV. The prevalence and source of methicillin-resistant Staphylococcus aureus (MRSA) in the community in HongKong. Epidemiol Infect, 2004, 132(6): 1091-1097.
19.	Xie X, Dai X, Ni L, et al. Molecular epidemiology and virulence characteristics of Staphylococcus aureus nasal colonization in medical laboratory staff: comparison between microbiological and non-microbiological laboratories. BMC Infect Dis, 2018, 18(1): 122.
20.	Yan X, Song Y, Yu X, et al. Factors associated with Staphylococcus aureus nasal carriage among healthy people in Northern China. Clin Microbiol Infect, 2015, 21(2): 157-162.
21.	Chen BJ, Xie XY, Ni LJ, 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. Ann Clin Microbiol Antimicrob, 2017, 16(1): 28.
22.	Chen CH, Kuo KC, Hwang KP, et al. Risk factors for and molecular characteristics of methicillin-resistant Staphylococcus aureus nasal colonization among healthy children in southern Taiwan, 2005-2010. DOI: 10.1016/j.jmii.2018.09.003.
23.	邓建军, 万朝敏, 母得志, 等. 在校健康儿童鼻前庭携带金黄色葡萄球菌检测及药物敏感分析. 四川大学学报(医学版), 2012, 43(3): 391-394.
24.	Zhang M, O'Donoghue MM, Ito T, et al. Prevalence of antiseptic-resistance genes in Staphylococcus aureus and coagulase-negative staphylococci colonising nurses and the general population in Hong Kong. J Hosp Infect, 2011, 78(2): 113-117.
25.	Ho PL, Chiu SS, Chan MY, 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. J Infect, 2012, 64(5): 500-506.
26.	Gong Z, Shu M, Xia Q, et al. Staphylococcus aureus nasal carriage and its antibiotic resistance profiles in children in high altitude areas of Southwestern China. Arch Argent Pediatr, 2017, 115(3): 274-277.
27.	Boost MV, So SY, Perreten V. Low rate of methicillin-resistant coagulase-positive staphylococcal colonization of veterinary personnel in Hong Kong. Zoonoses Public Health, 2011, 58(1): 36-40.
28.	傅锦坚, 叶小华, 姚振江, 等. 健康儿童鼻携带金黄色葡萄球菌耐药性研究. 现代预防医学, 2015, 42(12): 2175-2177.
29.	葛忆琳, 陈越火, 朱仁义, 等. 医护人员携带MRSA及其耐药基因的研究. 中国消毒学杂志, 2012, 29(7): 565-568.
30.	刘贺, 费春楠, 董杰, 等. 医护人员鼻前庭带菌情况及其耐药性研究. 中国消毒学杂志, 2016, 33(10): 983-985, 988.
31.	钟嘉冀, 张川, 赖莉莉, 等. 乳肉加工销售人员中耐甲氧西林金黄色葡萄球菌的携带与耐药情况分析. 中华医院感染学杂志, 2016, 26(23): 5315-5317.
32.	陈百计, 姚泽宇, 代鑫露, 等. 广州社区人群金黄色葡萄球菌鼻腔携带调查和分子流行特征. 热带医学杂志, 2017, 17(12): 1583-1588.
33.	Huang YC, Hwang KP, Chen PY, et al. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among Taiwanese children in 2005 and 2006. J Clin Microbiol, 2007, 45(12): 3992-3995.
34.	Lu PL, Chin LC, Peng CF, et al. Risk factors and molecular analysis of community methicillin-resistant Staphylococcus aureus carriage. J Clin Microbiol, 2005, 43(1): 132-139.
35.	胡付品, 朱德妹, 汪复, 等. 2014年CHINET中国细菌耐药性监测. 中国感染与化疗杂志, 2015, (5): 401-410.
36.	den Heijer CD, van Bijnen EM, Paget WJ, et al. Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis, 2013, 13(5): 409-415.
37.	Ma E, Wong S, Wong C, et al. Effects of public health interventions in reducing transmission of hand, foot, and mouth disease. Pediatr Infect Dis J, 2011, 30(5): 432-435.
38.	Dulon M, Peters C, Schablon A, et al. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infect Dis, 2014, 14: 363.
39.	Bitterman Y, Laor A, Itzhaki S, et al. Characterization of the best anatomical sites in screening for methicillin-resistant Staphylococcus aureus colonization. Eur J Clin Microbiol Infect Dis, 2010, 29(4): 391-397.

1. Sahreena L, Zhang KY. Methicillin-resistant staphylococcus aureus: molecular characterization, evolution, and epidemiology. Clin Microbiol Rev, 2018, 31(4): 12.
2. Hurley JC. Risk of death from methicillin-resistant Staphylococcus aureus bacteraemia: a meta-analysis. Med J Aust, 2002, 176(4): 188-189.
3. 赵旺旺. 耐甲氧西林金黄色葡萄球菌的研究进展. 社区医学杂志, 2006, 11(5): 78-80.
4. Chen CJ, Hsu KH, Lin TY, et al. Factors associated with nasal colonization of methicillin-resistant Staphylococcus aureus among healthy children in Taiwan. J Clin Microbiol, 2011, 49(1): 131-137.
5. Huang YC, Ho CF, Chen CJ, et al. Nasal carriage of methicillin-resistant Staphylococcus aureus in household contacts of children with community-acquired diseases in Taiwan. Pediatr Infect Dis J, 2007, 26(11): 1066-1068.
6. Boyle MH. Guidelines for evaluating prevalence studies. Evid Based Ment Heal, 1998, 1(2): 37-39.
7. Laird N. Meta-analysis in clinical trials. Control Clin Trials, 1986, 7(3): 177.
8. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med, 2002, 21(11): 1539-1558.
9. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics, 1994, 50(4): 1088-1101.
10. Seagroatt V, Stratton I. Bias in meta-analysis detected by a simple, graphical test. Test had 10% false positive rate. BMJ, 1998, 316(7219): 470-470.
11. Ye X, Liu W, Fan Y, et al. Frequency-risk and duration-risk relations between occupational livestock contact and methicillin-resistant Staphylococcus aureus carriage among workers in Guangdong, China. Am J Infect Control, 2015, 43(7): 676-681.
12. 范娟, 周伟, 舒敏, 等. 成都地区健康儿童鼻腔社区获得性耐甲氧西林金黄色葡萄球菌的携带研究. 中国当代儿科杂志, 2011, 13(1): 16-19.
13. Zhang W, Hao Z, Wang Y, et al. Molecular characterization of methicillin-resistant Staphylococcus aureus strains from pet animals and veterinary staff in China. Vet J, 2011, 190(2): e125-e129.
14. Ma XX, Sun DD, Wang S, 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(1): 22-30.
15. 马笑雪, 罗恩杰. 社区分离金黄色葡萄球菌在健康人群中的分布及其分子生物学特点. 中华流行病学杂志, 2011, 32(8): 804-807.
16. Chen B, Dai X, He B, 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 Infect Dis, 2015, 15(1): 303.
17. Du J, Chen C, Ding B, et al. Molecular characterization and antimicrobial susceptibility of nasal Staphylococcus aureus isolates from a Chinese medical college campus. PLoS One, 2011, 6(11): e27328.
18. O'Donoghue MM, Boost MV. The prevalence and source of methicillin-resistant Staphylococcus aureus (MRSA) in the community in HongKong. Epidemiol Infect, 2004, 132(6): 1091-1097.
19. Xie X, Dai X, Ni L, et al. Molecular epidemiology and virulence characteristics of Staphylococcus aureus nasal colonization in medical laboratory staff: comparison between microbiological and non-microbiological laboratories. BMC Infect Dis, 2018, 18(1): 122.
20. Yan X, Song Y, Yu X, et al. Factors associated with Staphylococcus aureus nasal carriage among healthy people in Northern China. Clin Microbiol Infect, 2015, 21(2): 157-162.
21. Chen BJ, Xie XY, Ni LJ, 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. Ann Clin Microbiol Antimicrob, 2017, 16(1): 28.
22. Chen CH, Kuo KC, Hwang KP, et al. Risk factors for and molecular characteristics of methicillin-resistant Staphylococcus aureus nasal colonization among healthy children in southern Taiwan, 2005-2010. DOI: 10.1016/j.jmii.2018.09.003.
23. 邓建军, 万朝敏, 母得志, 等. 在校健康儿童鼻前庭携带金黄色葡萄球菌检测及药物敏感分析. 四川大学学报(医学版), 2012, 43(3): 391-394.
24. Zhang M, O'Donoghue MM, Ito T, et al. Prevalence of antiseptic-resistance genes in Staphylococcus aureus and coagulase-negative staphylococci colonising nurses and the general population in Hong Kong. J Hosp Infect, 2011, 78(2): 113-117.
25. Ho PL, Chiu SS, Chan MY, 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. J Infect, 2012, 64(5): 500-506.
26. Gong Z, Shu M, Xia Q, et al. Staphylococcus aureus nasal carriage and its antibiotic resistance profiles in children in high altitude areas of Southwestern China. Arch Argent Pediatr, 2017, 115(3): 274-277.
27. Boost MV, So SY, Perreten V. Low rate of methicillin-resistant coagulase-positive staphylococcal colonization of veterinary personnel in Hong Kong. Zoonoses Public Health, 2011, 58(1): 36-40.
28. 傅锦坚, 叶小华, 姚振江, 等. 健康儿童鼻携带金黄色葡萄球菌耐药性研究. 现代预防医学, 2015, 42(12): 2175-2177.
29. 葛忆琳, 陈越火, 朱仁义, 等. 医护人员携带MRSA及其耐药基因的研究. 中国消毒学杂志, 2012, 29(7): 565-568.
30. 刘贺, 费春楠, 董杰, 等. 医护人员鼻前庭带菌情况及其耐药性研究. 中国消毒学杂志, 2016, 33(10): 983-985, 988.
31. 钟嘉冀, 张川, 赖莉莉, 等. 乳肉加工销售人员中耐甲氧西林金黄色葡萄球菌的携带与耐药情况分析. 中华医院感染学杂志, 2016, 26(23): 5315-5317.
32. 陈百计, 姚泽宇, 代鑫露, 等. 广州社区人群金黄色葡萄球菌鼻腔携带调查和分子流行特征. 热带医学杂志, 2017, 17(12): 1583-1588.
33. Huang YC, Hwang KP, Chen PY, et al. Prevalence of methicillin-resistant Staphylococcus aureus nasal colonization among Taiwanese children in 2005 and 2006. J Clin Microbiol, 2007, 45(12): 3992-3995.
34. Lu PL, Chin LC, Peng CF, et al. Risk factors and molecular analysis of community methicillin-resistant Staphylococcus aureus carriage. J Clin Microbiol, 2005, 43(1): 132-139.
35. 胡付品, 朱德妹, 汪复, 等. 2014年CHINET中国细菌耐药性监测. 中国感染与化疗杂志, 2015, (5): 401-410.
36. den Heijer CD, van Bijnen EM, Paget WJ, et al. Prevalence and resistance of commensal Staphylococcus aureus, including meticillin-resistant S aureus, in nine European countries: a cross-sectional study. Lancet Infect Dis, 2013, 13(5): 409-415.
37. Ma E, Wong S, Wong C, et al. Effects of public health interventions in reducing transmission of hand, foot, and mouth disease. Pediatr Infect Dis J, 2011, 30(5): 432-435.
38. Dulon M, Peters C, Schablon A, et al. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infect Dis, 2014, 14: 363.
39. Bitterman Y, Laor A, Itzhaki S, et al. Characterization of the best anatomical sites in screening for methicillin-resistant Staphylococcus aureus colonization. Eur J Clin Microbiol Infect Dis, 2010, 29(4): 391-397.

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Prevalence of methicillin-resistant staphylococcus aureus in healthy population in China: a meta-analysis

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