Skip to main content
SpringerLink
Log in

Trends of foodborne diseases in China: lessons from laboratory-based surveillance since 2011

  • Review
  • Published:
Frontiers of Medicine Aims and scope Submit manuscript

Abstract

Foodborne disease is one of the most important public health issues worldwide. China faces various and unprecedented challenges in all aspects of the food chain. Data from laboratory-based foodborne disease surveillance systems from 2013 to 2016, as well as different regions and ages, can be found along with differences in the patterns of pathogens detected with diverse characteristics. Vibrio parahaemolyticus has been the leading cause of infectious diarrhea in China, especially among adults in coastal regions. Salmonella has been a serious and widely distributed pathogen responsible for substantial socioeconomic burden. Shigella was mostly identified in Northwest China and the inland province (Henan) with less-developed regions among children under 5 years. Data from foodborne disease outbreak reporting system from 2011 to 2016 showed that poisonous animals and plant factors responsible for most deaths were poisonous mushrooms (54.7%) in remote districts in southwest regions. The biological hazard that caused most cases reported (42.3%) was attributed to V. parahaemolyticus, the leading cause of foodborne outbreaks. In this review, we summarize the recent monitoring approach to foodborne diseases in China and compare the results with those in developed countries.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, Praet N, Bellinger DC, de Silva NR, Gargouri N, Speybroeck N, Cawthorne A, Mathers C, Stein C, Angulo FJ, Devleesschauwer B; World Health Organization Foodborne Disease Burden Epidemiology Reference Group. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med 2015; 12(12): e1001923

    Article  PubMed  PubMed Central  Google Scholar 

  2. Halliday ML, Kang LY, Zhou TK, Hu MD, Pan QC, Fu TY, Huang YS, Hu SL. An epidemic of hepatitis A attributable to the ingestion of raw clams in Shanghai, China. J Infect Dis 1991; 164(5): 852–859

    Article  CAS  PubMed  Google Scholar 

  3. Xiong Y, Wang P, Lan R, Ye C, Wang H, Ren J, Jing H, Wang Y, Zhou Z, Bai X, Cui Z, Luo X, Zhao A, Wang Y, Zhang S, Sun H, Wang L, Xu J. A novel Escherichia coli O157:H7 clone causing a major hemolytic uremic syndrome outbreak in China. PLoS One 2012; 7(4): e36144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chen JS. A worldwide food safety concern in 2008 — melaminecontaminated infant formula in China caused urinary tract stone in 290,000 children in China. Chin Med J (Engl) 2009; 122(3): 243–244

    Article  Google Scholar 

  5. Chen JS. Food safety: an important public health problem in China. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2003; 24 (8): 649–650 (in Chinese)

    CAS  Google Scholar 

  6. Liu X. International perspectives on food safety and regulations—a need for harmonized regulations: perspectives in China. J Sci Food Agric 2014; 94(10): 1928–1931

    Article  CAS  PubMed  Google Scholar 

  7. [No authors listed]. Food safety in China: a long way to go. Lancet 2012; 380(9837): 75

  8. Buchholz U, Bernard H, Werber D, Böhmer MM, Remschmidt C, Wilking H, Deleré Y, an der Heiden M, Adlhoch C, Dreesman J, Ehlers J, Ethelberg S, Faber M, Frank C, Fricke G, Greiner M, Höhle M, Ivarsson S, Jark U, Kirchner M, Koch J, Krause G, Luber P, Rosner B, Stark K, Kühne M. German outbreak of Escherichia coli O104:H4 associated with sprouts. N Engl J Med 2011; 365(19): 1763–1770

    Article  CAS  PubMed  Google Scholar 

  9. Li D, Yap KS. Climate change and its impact on food and nutrition security and food safety in China. World Rev Nutr Diet 2011; 102: 175–182

    Article  PubMed  Google Scholar 

  10. Pei X, Li N, Guo Y, Liu X, Yan L, Li Y, Yang S, Hu J, Zhu J, Yang D. Microbiological food safety surveillance in China. Int J Environ Res Public Health 2015; 12(9): 10662–10670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Wu Y, Chen Y. Food safety in China. J Epidemiol Community Health 2013; 67(6): 478–479

    Article  PubMed  Google Scholar 

  12. [No authors listed]. Foodborne Diseases Active Surveillance Network, 1996. JAMA 1997; 277(17): 1344–1345

  13. Marder EP, Cieslak PR, Cronquist AB, Dunn J, Lathrop S, Rabatsky-Ehr T, Ryan P, Smith K, Tobin-D’Angelo M, Vugia DJ, Zansky S, Holt KG, Wolpert BJ, Lynch M, Tauxe R, Geissler AL. Incidence and trends of infections with pathogens transmitted commonly through food and the effect of increasing use of cultureindependent diagnostic tests on surveillance—Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2013–2016. MMWR Morb Mortal Wkly Rep 2017; 66(15): 397–403

    Article  PubMed  Google Scholar 

  14. Huang JY, Henao OL, Griffin PM, Vugia DJ, Cronquist AB, Hurd S, Tobin-D’Angelo M, Ryan P, Smith K, Lathrop S, Zansky S, Cieslak PR, Dunn J, Holt KG, Wolpert BJ, Patrick ME. Infection with pathogens transmitted commonly through food and the effect of increasing use of culture-independent diagnostic tests on surveillance—Foodborne Diseases Active Surveillance Network, 10 U.S. Sites, 2012–2015. MMWR Morb Mortal Wkly Rep 2016; 65(14): 368–371

    Article  PubMed  Google Scholar 

  15. Zhang Y, Zhao Y, Ding K, Wang X, Chen X, Liu Y, Chen Y. Analysis of bacterial pathogens causing acute diarrhea on the basis of sentinel surveillance in Shanghai, China, 2006–2011. Jpn J Infect Dis 2014; 67(4): 264–268

    Article  PubMed  Google Scholar 

  16. Li Y, Xie X, Shi X, Lin Y, Qiu Y, Mou J, Chen Q, Lu Y, Zhou L, Jiang M, Sun H, Ma H, Cheng J, Hu Q. Vibrio parahaemolyticus, Southern Coastal Region of China, 2007–2012. Emerg Infect Dis 2014; 20(4): 685–688

    Article  PubMed  PubMed Central  Google Scholar 

  17. Henao OL, Jones TF, Vugia DJ, Griffin PM; Foodborne Diseases Active Surveillance Network (FoodNet) Workgroup. Foodborne Diseases Active Surveillance Network-2 Decades of Achievements, 1996–2015. Emerg Infect Dis 2015; 21(9): 1529–1536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Li J, Hu J, Wu H, Pan H, Zhang X, Xue Y, Wu F. Etiological surveillance for diarrhea in Shanghai from August 2013 to July 2014. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2015; 36(10): 1099 (in Chinese)

    Google Scholar 

  19. Liao Y, Li Y, Wu S, Mou J, Xu Z, Cui R, Klena JD, Shi X, Lu Y, Qiu Y, Lin Y, Xie X, Ma H, Li Z, Yu H, Varma JK, Ran L, Hu Q, Cheng J. Risk factors for Vibrio parahaemolyticus infection in a southern coastal region of China. Foodborne Pathog Dis 2015; 12 (11): 881–886

    Article  PubMed  PubMed Central  Google Scholar 

  20. Ke B, Sun J, He D, Li X, Liang Z, Ke CW. Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007–2012 in Guangdong, China. BMC Infect Dis 2014; 14(1): 338

    Article  PubMed  PubMed Central  Google Scholar 

  21. Dong B, Liang D, Lin M, Wang M, Zeng J, Liao H, Zhou L, Huang J,Wei X, Zou G, Jing H. Bacterial etiologies of five core syndromes: laboratory-based syndromic surveillance conducted in Guangxi, China. PLoS One 2014; 9(10): e110876

    Article  PubMed  PubMed Central  Google Scholar 

  22. Qu M, Lv B, Zhang X, Yan H, Huang Y, Qian H, Pang B, Jia L, Kan B, Wang Q. Prevalence and antibiotic resistance of bacterial pathogens isolated from childhood diarrhea in Beijing, China (2010–2014). Gut Pathog 2016; 8(1): 31

    Article  PubMed  PubMed Central  Google Scholar 

  23. Zhang J, Jin H, Hu J, Yuan Z, Shi W, Ran L, Zhao S, Yang X, Meng J, Xu X. Serovars and antimicrobial resistance of non-typhoidal Salmonella from human patients in Shanghai, China, 2006–2010. Epidemiol Infect 2014; 142(4): 826–832

    Article  CAS  PubMed  Google Scholar 

  24. Shen H, Zhang J, Li Y, Xie S, Jiang Y,Wu Y, Ye Y, Yang H, Mo H, Situ C, Hu Q. The 12 gastrointestinal pathogens spectrum of acute infectious diarrhea in a sentinel hospital, Shenzhen, China. Front Microbiol 2016; 7: 1926

    PubMed  PubMed Central  Google Scholar 

  25. Ran L, Wu S, Gao Y, Zhang X, Feng Z, Wang Z, Kan B, Klena JD, Lo Fo Wong DM, Angulo FJ, Varma JK. Laboratory-based surveillance of nontyphoidal Salmonella infections in China. Foodborne Pathog Dis 2011; 8(8): 921–927

    Article  PubMed  Google Scholar 

  26. Xia S, Hendriksen RS, Xie Z, Huang L, Zhang J, Guo W, Xu B, Ran L, Aarestrup FM. Molecular characterization and antimicrobial susceptibility of Salmonella isolates from infections in humans in Henan Province, China. J Clin Microbiol 2009; 47(2): 401–409

    Article  CAS  PubMed  Google Scholar 

  27. Liang Z, Ke B, Deng X, Liang J, Ran L, Lu L, He D, Huang Q, Ke C, Li Z, Yu H, Klena JD, Wu S. Serotypes, seasonal trends, and antibiotic resistance of non-typhoidal Salmonella from human patients in Guangdong Province, China, 2009–2012. BMC Infect Dis 2015; 15(1): 53

    Article  PubMed  PubMed Central  Google Scholar 

  28. Soyer Y, Moreno Switt A, Davis MA, Maurer J, McDonough PL, Schoonmaker-Bopp DJ, Dumas NB, Root T, Warnick LD, Gröhn YT, Wiedmann M. Salmonella enterica serotype 4,5,12:i:-, an emerging Salmonella serotype that represents multiple distinct clones. J Clin Microbiol 2009; 47(11): 3546–3556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Jin Q, Yuan Z, Xu J,Wang Y, Shen Y, Lu W,Wang J, Liu H, Yang J, Yang F, Zhang X, Zhang J, Yang G, Wu H, Qu D, Dong J, Sun L, Xue Y, Zhao A, Gao Y, Zhu J, Kan B, Ding K, Chen S, Cheng H, Yao Z, He B, Chen R, Ma D, Qiang B, Wen Y, Hou Y, Yu J. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157. Nucleic Acids Res 2002; 30(20): 4432–4441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chang Z, Zhang J, Ran L, Sun J, Liu F, Luo L, Zeng L, Wang L, Li Z, Yu H, Liao Q. The changing epidemiology of bacillary dysentery and characteristics of antimicrobial resistance of Shigella isolated in China from 2004–2014. BMC Infect Dis 2016; 16(1): 685

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O’Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 2013; 382(9888): 209–222

    Article  PubMed  Google Scholar 

  32. Zhang ZK, Lai SJ, Yu JX, Yang WQ,Wang X, Jing HQ, Li ZJ, Yang WZ. Epidemiological characteristics of diarrheagenic Escherichia coli among diarrhea outpatients in China, 2012–2015. Chin J Epidemiol (Zhonghua Liu Xing Bing Xue Za Zhi) 2017; 38(4): 419 (in Chinese)

    CAS  Google Scholar 

  33. Panel on Biological Hazards. Public health risks associated with enteroaggregative Escherichia coli (EAEC) as a food-borne pathogen. Efsa J 2015; 13(12): 112–212

  34. King LA, Nogareda F,Weill FX, Mariani-Kurkdjian P, Loukiadis E, Gault G, Jourdan-DaSilva N, Bingen E, Macë M, Thevenot D, Ong N, Castor C, Noël H, Van Cauteren D, Charron M, Vaillant V, Aldabe B, Goulet V, Delmas G, Couturier E, Le Strat Y, Combe C, Delmas Y, Terrier F, Vendrely B, Rolland P, de Valk H. Outbreak of Shiga toxin-producing Escherichia coli O104:H4 associated with organic fenugreek sprouts, France, June 2011. Clin Infect Dis 2012; 54(11): 1588–1594

    Article  CAS  PubMed  Google Scholar 

  35. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E, Bhutta ZA, O’Brien KL, Campbell H, Black RE. Global burden of childhood pneumonia and diarrhoea. Lancet 2013; 381(9875): 1405–1416

    Article  PubMed  Google Scholar 

  36. Yu J, Jing H, Lai S, Xu W, Li M, Wu J, Liu W, Yuan Z, Chen Y, Zhao S, Wang X, Zhao Z, Ran L, Wu S, Klena JD, Feng L, Li F, Ye X, Qiu Y,Wang X, Yu H, Li Z, Yang W. Etiology of diarrhea among children under the age five in China: results from a five-year surveillance. J Infect 2015; 71(1): 19–27

    Article  PubMed  PubMed Central  Google Scholar 

  37. Chang Z, Zhang J, Ran L, Sun J, Liu F, Luo L, Zeng L, Wang L, Li Z, Yu H, Liao Q. The changing epidemiology of bacillary dysentery and characteristics of antimicrobial resistance of Shigella isolated in China from 2004–2014. BMC Infect Dis 2016; 16(1): 685

    Article  PubMed  PubMed Central  Google Scholar 

  38. Kotloff KL, Nataro JP, Blackwelder WC, Nasrin D, Farag TH, Panchalingam S, Wu Y, Sow SO, Sur D, Breiman RF, Faruque AS, Zaidi AK, Saha D, Alonso PL, Tamboura B, Sanogo D, Onwuchekwa U, Manna B, Ramamurthy T, Kanungo S, Ochieng JB, Omore R, Oundo JO, Hossain A, Das SK, Ahmed S, Qureshi S, Quadri F, Adegbola RA, Antonio M, Hossain MJ, Akinsola A, Mandomando I, Nhampossa T, Acácio S, Biswas K, O’Reilly CE, Mintz ED, Berkeley LY, Muhsen K, Sommerfelt H, Robins-Browne RM, Levine MM. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet 2013; 382(9888): 209–222

    Article  PubMed  Google Scholar 

  39. Zhang SX, Yang CL, Gu WP, Ai L, Serrano E, Yang P, Zhou X, Li SZ, Lv S, Dang ZS, Chen JH, Hu W, Tian LG, Chen JX, Zhou XN. Case-control study of diarrheal disease etiology in individuals over 5 years in southwest China. Gut Pathog 2016; 8(1): 58

    Article  PubMed  PubMed Central  Google Scholar 

  40. Qu M, Deng Y, Zhang X, Liu G, Huang Y, Lin C, Li J, Yan H, Li X, Jia L, Kan B, Huang F, Wang Q. Etiology of acute diarrhea due to enteropathogenic bacteria in Beijing, China. J Infect 2012; 65(3): 214–222

    Article  PubMed  Google Scholar 

  41. McEntire J. Foodborne disease: the global movement of food and people. Infect Dis Clin North Am 2013; 27(3): 687–693

    Article  PubMed  Google Scholar 

  42. Johnson LR, Gould LH, Dunn JR, Berkelman R, Mahon BE; Foodnet Travel Working Group. Salmonella infections associated with international travel: a Foodborne Diseases Active Surveillance Network (FoodNet) study. Foodborne Pathog Dis 2011; 8(9): 1031–1037

    Article  PubMed  Google Scholar 

  43. McEntire J. Foodborne disease: the global movement of food and people. Infect Dis Clin North Am 2013; 27(3): 687–693

    Article  PubMed  Google Scholar 

  44. Centers for Disease Control and Prevention (CDC). Surveillance for Foodborne Disease Outbreaks, United States, 2015, Annual Report. Atlanta, Georgia: US Department of Health and Human Services, CDC, 2017

  45. Centers for Disease Control and Prevention (CDC). Surveillance for Foodborne Disease Outbreaks, United States, 2014, Annual Report. Atlanta, Georgia: US Department of Health and Human Services, CDC, 2016.

  46. Centers for Disease Control and Prevention (CDC). Surveillance for Foodborne Disease Outbreaks, United States, 2013, Annual Report. Atlanta, Georgia: US Department of Health and Human Services, CDC, 2015.

  47. Centers for Disease Control and Prevention (CDC). Surveillance for Foodborne Disease Outbreaks, United States, 2011, Annual Report. Atlanta, Georgia: US Department of Health and Human Services, CDC, 2013.

  48. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis 2011; 17(1): 7–15

    Article  PubMed  PubMed Central  Google Scholar 

  49. O’Brien SJ, Larose TL, Adak GK, Evans MR, Tam CC; Foodborne Disease Attribution Study Group. Modelling study to estimate the health burden of foodborne diseases: cases, general practice consultations and hospitalisations in the UK, 2009. BMJ Open 2016; 6(9): e011119

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by National Science and Technology Infrastructure Program (No. 2017YFC1601500), the National Natural Science Foundation of China (No. 81402685). We thank Professor Séamus Fanning and Dr. Juan Wang for the valuable suggestions for improving the manuscript.

Author information

Author notes

  1. These authors contributed equally to this work.

Authors and Affiliations

  1. Key Laboratory of Food Safety Risk Assessment, Ministry of Health and China National Center for Food Safety Risk Assessment, Beijing, 100022, China

    Jikai Liu, Li Bai, Weiwei Li, Haihong Han, Ping Fu, Xiumei Liu & Yunchang Guo

  2. Center for Disease Control and Prevention of Beijing, Beijing, 100013, China

    Xiaochen Ma

  3. Shandong Center for Disease Control and Prevention, Jinan, 250014, China

    Zhenwang Bi

  4. Center for Disease Control and Prevention of Sichuan Province, Chengdu, 610041, China

    Xiaorong Yang

  5. Center for Disease Control and Prevention of Henan Province, Zhengzhou, 450016, China

    Xiuli Zhang

  6. Center for Disease Control and Prevention of Jiangsu Province, Nanjing, 210009, China

    Shiqi Zhen

  7. Guangdong Provincial Center for Disease Control and Prevention, Guangzhou, 511430, China

    Xiaoling Deng

Authors
  1. Jikai Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Li Bai
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Weiwei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Haihong Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ping Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Xiaochen Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Zhenwang Bi
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiaorong Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Xiuli Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Shiqi Zhen
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Xiaoling Deng
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Xiumei Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Yunchang Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yunchang Guo.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, J., Bai, L., Li, W. et al. Trends of foodborne diseases in China: lessons from laboratory-based surveillance since 2011. Front. Med. 12, 48–57 (2018). https://doi.org/10.1007/s11684-017-0608-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11684-017-0608-6

Keywords

Search

Navigation