Advanced Search

Preplanned Studies: DiarrheagenicEscherichia coliOutbreak Reporting to Foodborne Disease Outbreaks Surveillance System — China, 2011–2022

View author affiliations
  • Summary

    What is already known about this topic?

    Foodborne diarrheagenicEscherichia coli(DEC) outbreaks constitute a significant global public health concern, yet comprehensive data on outbreak incidence and epidemiological characteristics in China remain limited.

    What is added by this report?

    Between 2011 and 2022, there were 413 foodborne DEC outbreaks reported to foodborne disease outbreak surveillance system, resulting in 8,127 illnesses, 2,565 hospitalizations, and one fatality. EnteroaggregativeEscherichia coli(EAEC) emerged as the predominant causative pathogen (48.82% of outbreaks), with school canteens being the most frequent outbreak setting (21.79%).

    What are the implications for public health practice?

    This systematic analysis of foodborne DEC outbreak trends and epidemiological characteristics in China over the past decade provides crucial insights for enhancing outbreak investigation capabilities and identifying specific etiologies, food vehicles, and high-risk settings associated with these outbreaks.

  • loading...
  • Conflicts of interest:No conflicts of interest.
  • Funding:Supported by the National Key Research and Development Program of China (No. 2022YFC2303905)
  • [1] Croxen MA, Finlay BB. Molecular mechanisms ofEscherichia colipathogenicity. Nat Rev Microbiol 2010;8(1):26 − 38. https://doi.org/10.1038/nrmicro2265.
    [2] Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. Recent advances in understanding enteric pathogenicEscherichia coli. Clin Microbiol Rev 2013;26(4):822 − 80. https://doi.org/10.1128/CMR.00022-13.
    [3] World Health Organization. Diarrhoeal disease fact sheet [Internet]. Geneva: WHO; 2022. https://www.who.int/en/news-room/fact-sheets/detail/diarrhoeal-disease. [2023-4-23].
    [4] Zhou SX, Wang LP, Liu MY, Zhang HY, Lu QB, Shi LS, et al. Characteristics of diarrheagenicEscherichia coliamong patients with acute diarrhea in China, 2009‒2018. J Infect 2021;83(4):424 − 32. https://doi.org/10.1016/j.jinf.2021.08.001.
    [5] Kampmeier S, Berger M, Mellmann A, Karch H, Berger P. The 2011 German enterohemorrhagicEscherichia coliO104:H4 outbreak—the danger is still out there. In: Frankel G, Ron EZ, editors. Escherichia coli, a versatile pathogen. Cham: Springer. 2018; p. 117-48. http://dx.doi.org/10.1007/82_2018_107.
    [6] European Food Safety Authority, European Centre for Disease Prevention and Control. The European Union one health 2021 zoonoses report. EFSA J 2022;20(12):e07666. https://doi.org/10.2903/j.efsa.2022.7666.
    [7] Painter JA, Hoekstra RM, Ayers T, Tauxe RV, Braden CR, Angulo FJ, et al. Attribution of foodborne illnesses, hospitalizations, and deaths to food commodities by using outbreak data, United States, 1998-2008. Emerg Infect Dis 2013;19(3):407 − 15. https://doi.org/10.3201/eid1903.111866.
    [8] National Bureau of Statistics. Demographic figures by year [Internet]. Beijing: NBSC; 2021. https://data.stats.gov.cn/easyquery.htm?cn=C01. [2023]. (In Chinese).
    [9] Jian YN, Zhu D, Zhou DN, Li NN, Du H, Dong X, et al. ARIMA model for predicting chronic kidney disease and estimating its economic burden in China. BMC Public Health 2022;22(1):2456. https://doi.org/10.1186/s12889-022-14959-z.
    [10] Wu YN, Liu XM, Chen Q, Liu H, Dai Y, Zhou YJ, et al. Surveillance for foodborne disease outbreaks in China, 2003 to 2008. Food Control 2018;84:382 − 8. https://doi.org/10.1016/j.foodcont.2017.08.010.
    [11] Li WW, Pires SM, Liu ZT, Ma XC, Liang JJ, Jiang YY, et al. Surveillance of foodborne disease outbreaks in China, 2003–2017. Food Control 2020;118:107359. https://doi.org/10.1016/j.foodcont.2020.107359.
    [12] Wang LP, Han JY, Zhou SX, Yu LJ, Lu QB, Zhang XA, et al. The changing pattern of enteric pathogen infections in China during the COVID-19 pandemic: a nation-wide observational study. Lancet Reg Health West Pac 2021;16:100268. https://doi.org/10.1016/j.lanwpc.2021.100268.
    [13] Chen G. Research on family food safety in Yunnan minority areas. Soc Sci Yunnan 2016;(6):95-101. https://kns.cnki.net/kcms2/article/abstract?v=NK8hpUzgeRXhjIGRRijxzH3ypvleof3ohFc8nvg9Ibo6gMu8fwfaL8xkaMI8heQtX_DVBrfrtnfvBLL_4__NsbsIyfwpX99dNE_zF8g-t4Va719Cg_WkVZDRSOM7OonBbSKDRabbyN9OQS89r_EeFgVGDlrqtTsTR1j4RhgDBPoz4rbqH-Ei85rri1_9VlVU&uniplatform=NZKPT&language=CHS. (In Chinese).
  • FIGURE 1.Annual incidence and rate of foodborne DEC outbreaks in China, 2011–2022.

    Note: Z andPvalues indicate trend analysis results for the entire period 2011–2022; Z* andP* values indicate trend analysis results for the pre-pandemic period 2011–2019.

    Abbreviation: DEC=diarrheagenicEscherichia coli;CI=confidence interval.

    FIGURE 2.Geographic distribution of foodborne DEC outbreaks, illnesses, and hospitalizations by PLAD in China, 2011–2022.

    Abbreviation: DEC=diarrheagenic Escherichia coli; PLAD=provincial-level administrative division.

    TABLE 1.Number and percentage of foodborne diarrheagenicEscherichia colioutbreaks, illnesses, and hospitalizations by setting and food vehicle in China, 2011–2022.

    Settings Outbreaks,n(%) Illnesses,n(%) Hospitalizations,n(%)
    Canteens
    School canteens 90 (21.79) 3,206 (39.45) 1,002 (39.06)
    Workplace cafeteria 43 (10.41) 737 (9.07) 87 (3.39)
    Catering services
    Restaurant 89 (21.55) 1,609 (19.80) 593 (23.12)
    Street stall 19 (4.60) 127 (1.56) 28 (1.09)
    Takeaway 6 (1.45) 91 (1.12) 4 (0.16)
    Fast food service 5 (1.21) 27 (0.33) 10 (0.39)
    Homes
    Household 63 (15.25) 297 (3.65) 152 (5.93)
    Rural banquet 34 (8.23) 745 (9.17) 483 (18.83)
    Markets
    Food supermarket 6 (1.45) 80 (0.98) 63 (2.46)
    Other locations 8 (1.94) 66 (0.81) 7 (0.27)
    Unknown locations 50 (12.11) 1,142 (14.05) 136 (5.30)
    Food vehicles
    Animal-based food
    Meat 91 (22.03) 1,735 (21.35) 609 (23.74)
    Aquatic animals 15 (3.63) 124 (1.53) 53 (2.07)
    Egg 6 (1.45) 91 (1.12) 2 (0.08)
    Dairy 1 (0.24) 23 (0.28) 23 (0.90)
    Plant-based food
    Vegetable 22 (5.33) 296 (3.64) 133 (5.19)
    Grains 21 (5.08) 248 (3.05) 56 (2.18)
    Bean 8 (1.94) 112 (1.38) 63 (2.46)
    Fruit 4 (0.97) 13 (0.16) 0 (0)
    Pastry 3 (0.73) 68 (0.84) 59 (2.30)
    Multiple/complex food
    Multiple food 46 (11.14) 873 (10.74) 59 (2.30)
    Complex food 84 (20.34) 1,869 (23.00) 964 (37.58)
    Drinks
    Drinking water 13 (3.15) 431 (5.30) 199 (7.76)
    Beverages 3 (0.73) 117 (1.44) 0 (0)
    Unknown food 96 (23.24) 2,127 (26.17) 345 (13.45)
    Total 413 (100) 8,127 (100) 2,565 (100)
    Download: CSV

Citation:

通讯作者:陈斌, bchen63@163.com
  • 1.

    沈阳化工大学材料科学与工程学院 沈阳 110142

  1. 本站搜索
  2. 百度学术搜索
  3. 万方数据库搜索
  4. CNKI搜索
Turn off MathJax
Article Contents

Article Metrics

Article views(1736) PDF downloads(9)Cited by()

Share

Related

DiarrheagenicEscherichia coliOutbreak Reporting to Foodborne Disease Outbreaks Surveillance System — China, 2011–2022

View author affiliations

Summary

What is already known about this topic?

Foodborne diarrheagenicEscherichia coli(DEC) outbreaks constitute a significant global public health concern, yet comprehensive data on outbreak incidence and epidemiological characteristics in China remain limited.

What is added by this report?

Between 2011 and 2022, there were 413 foodborne DEC outbreaks reported to foodborne disease outbreak surveillance system, resulting in 8,127 illnesses, 2,565 hospitalizations, and one fatality. EnteroaggregativeEscherichia coli(EAEC) emerged as the predominant causative pathogen (48.82% of outbreaks), with school canteens being the most frequent outbreak setting (21.79%).

What are the implications for public health practice?

This systematic analysis of foodborne DEC outbreak trends and epidemiological characteristics in China over the past decade provides crucial insights for enhancing outbreak investigation capabilities and identifying specific etiologies, food vehicles, and high-risk settings associated with these outbreaks.

  • 1. Institute for Nutrition and Food Hygiene, Beijing Center for Disease Prevention and Control, Beijing, China
  • 2. Division of Foodborne Disease Surveillance, China National Center for Food Safety Risk Assessment, Beijing, China
  • 3. Jiangsu Provincial Center for Disease Prevention and Control, Nanjing City, Jiangsu Province, China
  • 4. Guangdong Provincial Center for Disease Prevention and Control, Guangzhou City, Guangdong Province, China
  • Corresponding authors:

    Yunchang Guo,gych@cfsa.net.cn ;

    Xiaochen Ma,maxch@bjcdc.org

  • Funding:Supported by the National Key Research and Development Program of China (No. 2022YFC2303905)
  • Online Date:December 20 2024
    Issue Date:December 20 2024
    doi:10.46234/ccdcw2024.272
  • Escherichia colitypically exists as a commensal organism in the gastrointestinal tract of humans and animals, remaining harmless under normal conditions (1). However, certain pathogenic strains can cause severe clinical manifestations, including acute diarrhea, hemolytic uremic syndrome (HUS), and thrombocytopenic purpura (2). Foodborne diarrheagenicEscherichia coli(DEC) represents one of the predominant etiological agents of acute diarrhea in low- and middle-income countries (3), and has emerged as a significant pathogen in diarrheal cases throughout China (4).

    DEC outbreaks persist globally, affecting both developed and developing nations, with potential fatal outcomes and substantial public health and economic implications (5). Many countries have implemented comprehensive national surveillance systems specifically designed to monitor and track DEC outbreaks, such as the Foodborne Disease Outbreak Surveillance System (FDOSS) in the USA and the Rapid Outbreak Assessment system for multi-country foodborne outbreaks in the European Union (6-7). This study analyzes DEC outbreaks reported to the FDOSS in China during 2011–2022 to inform evidence-based food safety policies and interventions for the Chinese population.

    The FDOSS, established in 2011, serves as a centralized system for managing and mitigating foodborne disease outbreaks. For each outbreak, the system collects comprehensive data including reporting unit, temporal and geographic information, food preparation setting, case counts (illnesses, hospitalizations, and deaths), confirmed etiology, and implicated food vehicles. All outbreak investigation reports undergwent systematic review by dedicated personnel. A foodborne DEC outbreak is defined as two or more cases presenting with similar illness and/or one or more deaths resulting from consumption of a common food source, with laboratory confirmation ofE. colias the causative pathogen. Outbreaks involving multiple etiologic agents were excluded from this analysis.

    Food source attribution was determined based on epidemiological evidence. Food vehicles were categorized using a two-tiered classification system. The first tier comprises five broad categories (including animal-based foods), while the second tier subdivides foods into 14 mutually exclusive categories. Single-ingredient foods or foods containing ingredients from the same category were classified accordingly. Foods containing ingredients from multiple categories were designated as complex or multiple foods.

    Statistical analyses were conducted using R software (version 4.1.2, R Foundation for Statistical Computing, Vienna, Austria). Exact binomial tests were employed to calculate 95% confidence intervals (CI) for outbreak rates, illness rates, and hospitalization rates. Temporal trends were assessed using the Mann-Kendall trend test (M-K test). Population-based rates were computed using demographic data from the National Bureau of Statistics of China (8).

    Given the seasonal nature of foodborne DEC infections, we employed a Seasonal Autoregressive Integrated Moving Average (SARIMA) model to generate short-term forecasts (2020–2022) based on historical time series data. The SARIMA model, widely applied across various fields, has demonstrated utility in time series analysis and prediction. For example, it was successfully used to model USA oil consumption patterns during the COVID-19 pandemic, enabling assessment of pandemic-related impacts on consumption from January 2020 to March 2021 (9).

    During 2011–2022, 413 foodborne DEC outbreaks were documented in China, resulting in 8,127 illnesses, 2,565 hospitalizations, and one death (Figure 1). The annual averages (rates) were 34.4 outbreaks [0.024 (95%CI: 0.024, 0.025) per 100,000], 677.2 illnesses [0.487 (95%CI: 0.484, 0.490) per 100,000], and 213.8 hospitalizations [0.154 (95%CI: 0.152, 0.156) per 100,000]. The annual rate of reported foodborne DEC outbreaks showed a significant increasing trend from 2011 to 2019 (0.013–0.032 per 100,000) (Pfor trend =0.021), followed by a declining trend from 2020 to 2022 (0.038 to 0.012 per 100,000,Pfor trend =0.085).

    Figure 1.

    Annual incidence and rate of foodborne DEC outbreaks in China, 2011–2022.

    Note: Z andPvalues indicate trend analysis results for the entire period 2011–2022; Z* andP* values indicate trend analysis results for the pre-pandemic period 2011–2019.

    Abbreviation: DEC=diarrheagenicEscherichia coli;CI=confidence interval.

    School canteens were the predominant outbreak setting, accounting for 21.79% of all outbreaks and the highest proportions of outbreak-related illnesses (3,206, 39.45%) and hospitalizations (1,002, 39.06%). In contrast, fast food establishments were associated with the lowest numbers of illnesses (27, 0.33%) and hospitalizations (10, 0.39%). The single reported death occurred in a workplace cafeteria. Food vehicles were identified in 76.76% (317) of outbreaks, with 187 (58.99%) attributed to a single food category, resulting in 6,000 illnesses and 2,220 hospitalizations. Animal-based foods were the most frequently implicated single commodity (113 outbreaks, 27.36%). The sole outbreak-associated death was linked to multiple foods (fried lesser croaker, quail eggs, lamb liver) served in a workplace cafeteria (Table 1).

    Settings Outbreaks,n(%) Illnesses,n(%) Hospitalizations,n(%)
    Canteens
    School canteens 90 (21.79) 3,206 (39.45) 1,002 (39.06)
    Workplace cafeteria 43 (10.41) 737 (9.07) 87 (3.39)
    Catering services
    Restaurant 89 (21.55) 1,609 (19.80) 593 (23.12)
    Street stall 19 (4.60) 127 (1.56) 28 (1.09)
    Takeaway 6 (1.45) 91 (1.12) 4 (0.16)
    Fast food service 5 (1.21) 27 (0.33) 10 (0.39)
    Homes
    Household 63 (15.25) 297 (3.65) 152 (5.93)
    Rural banquet 34 (8.23) 745 (9.17) 483 (18.83)
    Markets
    Food supermarket 6 (1.45) 80 (0.98) 63 (2.46)
    Other locations 8 (1.94) 66 (0.81) 7 (0.27)
    Unknown locations 50 (12.11) 1,142 (14.05) 136 (5.30)
    Food vehicles
    Animal-based food
    Meat 91 (22.03) 1,735 (21.35) 609 (23.74)
    Aquatic animals 15 (3.63) 124 (1.53) 53 (2.07)
    Egg 6 (1.45) 91 (1.12) 2 (0.08)
    Dairy 1 (0.24) 23 (0.28) 23 (0.90)
    Plant-based food
    Vegetable 22 (5.33) 296 (3.64) 133 (5.19)
    Grains 21 (5.08) 248 (3.05) 56 (2.18)
    Bean 8 (1.94) 112 (1.38) 63 (2.46)
    Fruit 4 (0.97) 13 (0.16) 0 (0)
    Pastry 3 (0.73) 68 (0.84) 59 (2.30)
    Multiple/complex food
    Multiple food 46 (11.14) 873 (10.74) 59 (2.30)
    Complex food 84 (20.34) 1,869 (23.00) 964 (37.58)
    Drinks
    Drinking water 13 (3.15) 431 (5.30) 199 (7.76)
    Beverages 3 (0.73) 117 (1.44) 0 (0)
    Unknown food 96 (23.24) 2,127 (26.17) 345 (13.45)
    Total 413 (100) 8,127 (100) 2,565 (100)

    Table 1.Number and percentage of foodborne diarrheagenicEscherichia colioutbreaks, illnesses, and hospitalizations by setting and food vehicle in China, 2011–2022.

    Using the SARIMA model, we analyzed and predicted DEC outbreak patterns in China. The model forecasted 51, 57, and 57 outbreaks for 2020–2022, while actual reported numbers were 54, 51, and 17, respectively. Similarly, predicted illness counts for 2021 (1,137) and 2022 (1,389) exceeded actual reported cases (1,125 and 189). Hospitalization predictions (252,240,240) also surpassed actual numbers (181,158,8) during 2020–2022 ( Supplementary Table S1 ).

    Geographic distribution analysis revealed substantial regional variation in outbreak occurrence. Yunnan province reported the highest number of outbreaks (n=42), while Beijing, Xinjiang Autonomous Region, and Hebei province each reported the lowest (n=2) during the 12-year period. Provincial outbreak rates ranged from 0.027 per 1,000,000 population in Hebei to 0.899 per 1,000,000 in Yunnan. Illness rates showed similar variation, from 9 cases (0.372 per 1,000,000) in Xinjiang to 1,202 cases (25.74 per 1,000,000) in Yunnan (Figure 2). The single reported death occurred in Inner Mongolia Autonomous Region, with no cross-provincial outbreaks documented.

    Figure 2.

    Geographic distribution of foodborne DEC outbreaks, illnesses, and hospitalizations by PLAD in China, 2011–2022.

    Abbreviation: DEC=diarrheagenic Escherichia coli; PLAD=provincial-level administrative division.

    Laboratory confirmation of DEC pathotypes was available for 254 outbreaks (60.50%), accounting for 5,070 illnesses (62.38%) and 1,077 hospitalizations (41.99%). EnteroaggregativeE. coli(EAEC) emerged as the predominant etiologic agent, responsible for 124 outbreaks (48.82%), 2,124 illnesses (41.87%), and 235 hospitalizations (21.82%). EnteroinvasiveE. coli(EIEC) was the least common pathotype, associated with 21 outbreaks (8.27%), 217 illnesses (4.28%), and 150 hospitalizations (19.39%) ( Supplementary Table S2 ).

    • This comprehensive analysis characterizes the epidemiological patterns of foodborne DEC outbreaks across China from 2011 to 2022. The observed number of DEC outbreaks during this period showed a sixfold increase compared to 2003–2008 (10). This substantial rise can be attributed to enhanced surveillance measures implemented under the Food Safety Law of 2011, including the deployment of an advanced web-based reporting system, improved reporting compliance, and sophisticated trace-back technologies (11).

      The COVID-19 pandemic has profoundly impacted public health and socioeconomic systems globally over the past three years. In China, the implementation of comprehensive non-pharmacological interventions (NPIs) - including social distancing measures, mandatory face mask usage, stay-at-home orders, closure of public spaces (restaurants and educational institutions), and travel restrictions - has affected the transmission dynamics of various infectious diseases. These interventions have demonstrated measurable effects on gastrointestinal infections, including DEC, with our findings showing a consistent reduction in reported foodborne DEC outbreaks that aligns with previous research (12).

      Our analysis revealed significant provincial variations in foodborne DEC outbreak rates. These disparities likely reflect differences in lifestyle behaviors, including regional food consumption patterns (such as the consumption of raw meat in southwest China), dining habits, and hygiene awareness (10). For instance, the practice of consuming raw meat in Yunnan Province has been previously associated with increased risk of foodborne DEC illness (13). However, these regional differences should be interpreted cautiously, as they may partially reflect variations in FDOSS management capabilities and laboratory capacity across PLADs rather than true epidemiological differences.

      Among outbreaks with determined etiology, EAEC emerged as the predominant pathotype, consistent with its status as the most frequently isolated pathogen in acute diarrhea cases in China (4). EAEC has been implicated in significant outbreaks worldwide (2). Our findings indicate that EPEC and ETEC contributed to a smaller proportion of foodborne DEC outbreaks compared to EAEC, which aligns with PCR detection rates observed among outpatients with acute diarrhea in China (4).

      School canteens represented the most frequent outbreak setting, primarily due to inadequate cooking procedures or cross-contamination during food preparation. Given children's heightened susceptibility to DEC infections, there is an urgent need to enhance oversight of school food service operations and implement comprehensive professional training programs for food service workers.

      Several limitations warrant consideration when interpreting FDOSS data. The reported outbreaks likely represent only a fraction of actual occurrences due to constraints in outbreak investigation capacity. Furthermore, the dynamic nature of our web-based system means that data may vary at different time points, potentially leading to discrepancies with earlier or subsequent studies. Additionally, the absence of comprehensive surveillance for all DEC strains historically limits our ability to present a complete epidemiological picture. These limitations highlight areas for future research focus. Nevertheless, prompt investigation and reporting of foodborne DEC outbreaks remain crucial for developing effective prevention strategies.

    • The invaluable contributions of all personnel at participating hospitals and Centers for Disease Control and Prevention for their dedication to foodborne disease surveillance and outbreak investigation in China.

  • Conflicts of interest:No conflicts of interest.
  • Reference (13)

    Citation:

    Catalog

      /

      Return
      Return
        Baidu
        map