A Survey of Chinese Pig Farms and Human Healthcare Isolates Reveals Separate Human and Animal Methicillin-Resistant Staphylococcus aureus Populations.

Geng Zou, Marta Matuszewska, Ming Jia, Jianwei Zhou, Xiaoliang Ba, Juan Duan, Caishi Zhang, Jian Zhao, Meng Tao, Jingyan Fan, Xiangming Zhang, Wenping Jin, Tianpen Cui, Xianyu Zeng, Min Jia, Xiaojuan Qian, Chao Huang, Wenxiao Zhuo, Zhiming Yao, Lijun Zhang, Shaowen Li, Lu Li, Qi Huang, Bin Wu, Huanchun Chen, Alexander W Tucker, Andrew J Grant, Mark A Holmes, Rui Zhou
Author Information
  1. Geng Zou: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  2. Marta Matuszewska: Department of Veterinary Medicine, University of Cambridge, Cambridge, CB3 0ES, UK.
  3. Ming Jia: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  4. Jianwei Zhou: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  5. Xiaoliang Ba: Department of Veterinary Medicine, University of Cambridge, Cambridge, CB3 0ES, UK.
  6. Juan Duan: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  7. Caishi Zhang: Jianli People's Hospital, Jianli, 433300, China.
  8. Jian Zhao: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  9. Meng Tao: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  10. Jingyan Fan: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  11. Xiangming Zhang: Wuhan Third Hospital, Wuhan, 430060, China.
  12. Wenping Jin: Wuhan Third Hospital, Wuhan, 430060, China.
  13. Tianpen Cui: Wuhan First Hospital, Wuhan, 430014, China.
  14. Xianyu Zeng: Wuhan First Hospital, Wuhan, 430014, China.
  15. Min Jia: Wuhan First Hospital, Wuhan, 430014, China.
  16. Xiaojuan Qian: Huangmei People's Hospital, Huangmei, 435500, China.
  17. Chao Huang: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  18. Wenxiao Zhuo: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  19. Zhiming Yao: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  20. Lijun Zhang: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  21. Shaowen Li: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  22. Lu Li: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  23. Qi Huang: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  24. Bin Wu: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  25. Huanchun Chen: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China.
  26. Alexander W Tucker: Department of Veterinary Medicine, University of Cambridge, Cambridge, CB3 0ES, UK.
  27. Andrew J Grant: Department of Veterinary Medicine, University of Cambridge, Cambridge, CB3 0ES, UK.
  28. Mark A Holmes: Department of Veterinary Medicine, University of Cambridge, Cambridge, CB3 0ES, UK.
  29. Rui Zhou: State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University College of Veterinary Medicine, Wuhan, 430070, China. ORCID

Abstract

There has been increasing concern that the overuse of antibiotics in livestock farming is contributing to the burden of antimicrobial resistance in people. Farmed animals in Europe and North America, particularly pigs, provide a reservoir for livestock-associated methicillin-resistant Staphylococcus aureus (LA-MRSA ST398 lineage) found in people. This study is designed to investigate the contribution of MRSA from Chinese pig farms to human infection. A collection of 483 MRSA are isolated from 55 farms and 4 hospitals in central China, a high pig farming density area. CC9 MRSA accounts for 97.2% of all farm isolates, but is not present in hospital isolates. ST398 isolates are found on farms and hospitals, but none of them formed part of the "LA-MRSA ST398 lineage" present in Europe and North America. The hospital ST398 MRSA isolate form a clade that is clearly separate from the farm ST398 isolates. Despite the presence of high levels of MRSA found on Chinese pig farms, the authors find no evidence of them spilling over to the human population. Nevertheless, the ST398 MRSA obtained from hospitals appear to be part of a widely distributed lineage in China. The new animal-adapted ST398 lineage that has emerged in China is of concern.

Keywords

References

  1. Emerg Microbes Infect. 2020 Dec;9(1):2526-2535 [PMID: 33174510]
  2. J Infect Dis. 2020 Mar 16;221(Suppl 2):S220-S228 [PMID: 32176793]
  3. Trends Microbiol. 2020 Jun;28(6):465-477 [PMID: 31948727]
  4. PLoS Pathog. 2010 Jun 03;6(6):e1000927 [PMID: 20532214]
  5. mSystems. 2021 Jun 29;6(3):e0049221 [PMID: 34156294]
  6. Antibiotics (Basel). 2015 Nov 06;4(4):521-43 [PMID: 27025639]
  7. Nucleic Acids Res. 2016 Jul 8;44(W1):W16-21 [PMID: 27141966]
  8. J Antimicrob Chemother. 2009 Oct;64(4):680-3 [PMID: 19684078]
  9. F1000Res. 2018 Aug 24;7:1338 [PMID: 30254741]
  10. Clin Microbiol Rev. 2018 Sep 12;31(4): [PMID: 30209034]
  11. Vet Microbiol. 2013 Mar 23;162(2-4):779-784 [PMID: 23116588]
  12. Emerg Infect Dis. 2005 Dec;11(12):1965-6 [PMID: 16485492]
  13. mSphere. 2018 Feb 14;3(1): [PMID: 29468193]
  14. Antimicrob Agents Chemother. 2014;58(1):212-20 [PMID: 24145532]
  15. Clin Infect Dis. 2017 Oct 1;65(7):1072-1076 [PMID: 28575216]
  16. Methods Ecol Evol. 2016 Jan;7(1):80-89 [PMID: 27110344]
  17. mBio. 2018 Nov 13;9(6): [PMID: 30425152]
  18. EFSA J. 2019 Feb 27;17(2):e05598 [PMID: 32626224]
  19. PLoS One. 2015 Nov 24;10(11):e0143670 [PMID: 26599635]
  20. Genome Med. 2018 Jan 29;10(1):5 [PMID: 29378646]
  21. Nucleic Acids Res. 2017 Jul 3;45(W1):W30-W35 [PMID: 28472413]
  22. Clin Microbiol Infect. 2017 Jun;23(6):373-380 [PMID: 27851997]
  23. mBio. 2012 Feb 21;3(1): [PMID: 22354957]
  24. Antimicrob Agents Chemother. 2005 Feb;49(2):813-5 [PMID: 15673776]
  25. Food Microbiol. 2019 Sep;82:287-293 [PMID: 31027785]
  26. J Antimicrob Chemother. 2018 Oct 1;73(10):2652-2661 [PMID: 29986036]
  27. Euro Surveill. 2015;20(37): [PMID: 26535590]
  28. Mol Biol Evol. 2012 Aug;29(8):1969-73 [PMID: 22367748]
  29. PLoS Comput Biol. 2017 Jun 8;13(6):e1005595 [PMID: 28594827]
  30. Environ Pollut. 2016 Dec;219:993-997 [PMID: 27180067]
  31. mSphere. 2021 Aug 25;6(4):e0054321 [PMID: 34319128]
  32. Vet Microbiol. 2017 Mar;201:183-187 [PMID: 28284608]
  33. Antimicrob Agents Chemother. 1987 Oct;31(10):1648-50 [PMID: 3324958]
  34. Antimicrob Agents Chemother. 2005 Sep;49(9):3948-51 [PMID: 16127079]
  35. Bioinformatics. 2019 Nov 1;35(21):4453-4455 [PMID: 31070718]
  36. PLoS One. 2014 Jul 07;9(7):e101988 [PMID: 25000530]
  37. EFSA J. 2017 Feb 23;15(2):e04694 [PMID: 32625402]
  38. Environ Sci Process Impacts. 2013 Apr;15(4):802-13 [PMID: 23411720]
  39. Sci Rep. 2019 Dec 9;9(1):18655 [PMID: 31819134]
  40. PLoS One. 2013 Nov 14;8(11):e79645 [PMID: 24244535]
  41. Antimicrob Agents Chemother. 2008 Nov;52(11):3875-82 [PMID: 18710917]
  42. Int J Antimicrob Agents. 2019 Jul;54(1):8-15 [PMID: 30959181]
  43. Lancet Infect Dis. 2011 Aug;11(8):595-603 [PMID: 21641281]
  44. J Comput Biol. 2012 May;19(5):455-77 [PMID: 22506599]
  45. Emerg Infect Dis. 2011 Mar;17(3):502-5 [PMID: 21392444]
  46. Genome Res. 2015 Jul;25(7):1043-55 [PMID: 25977477]
  47. Adv Sci (Weinh). 2022 Feb;9(4):e2103388 [PMID: 34894204]
  48. Appl Environ Microbiol. 2014 Dec;80(23):7275-82 [PMID: 25239891]
  49. Vet Microbiol. 2007 May 16;122(1-2):190-5 [PMID: 17300883]
  50. Mol Biol Evol. 2007 Feb;24(2):513-21 [PMID: 17119011]
  51. Bioinformatics. 2014 Jul 15;30(14):2068-9 [PMID: 24642063]
  52. BMC Bioinformatics. 2009 Dec 15;10:421 [PMID: 20003500]
  53. PLoS One. 2009;4(1):e4258 [PMID: 19145257]
  54. Nucleic Acids Res. 2015 Feb 18;43(3):e15 [PMID: 25414349]
  55. J Clin Microbiol. 2013 Dec;51(12):4259-61 [PMID: 24048528]

Grants

  1. 81661138003/National Natural Science Foundation of China
  2. MR/P007201/1/UK Medical Research Council

MeSH Term

Animal Population Groups
Animals
China
Farms
Humans
Livestock
Methicillin-Resistant Staphylococcus aureus
Staphylococcal Infections
Swine
Swine Diseases

Word Cloud

Created with Highcharts 10.0.0ST398MRSAfarmspighospitalsisolatesStaphylococcusaureuslineagefoundChineseChinaconcernfarmingpeopleEuropeNorthAmericamethicillin-resistanthumanhighfarmpresenthospitalpartpopulationHumanincreasingoveruseantibioticslivestockcontributingburdenantimicrobialresistanceFarmedanimalsparticularlypigsprovidereservoirlivestock-associatedLA-MRSAstudydesignedinvestigatecontributioninfectioncollection483isolated554centraldensityareaCC9accounts972%noneformed"LA-MRSAlineage"isolateformcladeclearlyseparateDespitepresencelevelsauthorsfindevidencespillingNeverthelessobtainedappearwidelydistributednewanimal-adaptedemergedSurveyPigFarmsHealthcareIsolatesRevealsSeparateAnimalMethicillin-ResistantPopulationsstructures

Similar Articles

Cited By