Users Online: 298 Home Print this page Email this page Small font sizeDefault font sizeIncrease font size
 

 

Home About us Editorial board Search Ahead of print Current issue Archives Submit article Instructions Subscribe Contacts Login 
     

 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 65  |  Issue : 5  |  Page : 18-22  

Acute gastroenteritis outbreak in a school associated with religious ceremony in Mirzapur District, Uttar Pradesh, India


1 India Epidemic Intelligence Services Officer, National Centre for Disease Control, New Delhi, India
2 Assistant Director, Division of Epidemiology, National Centre for Disease Control, New Delhi, India
3 Associate Professor, Department of Community Medicine, Armed Forces Medical College, Pune, Maharashtra, India
4 Professor and Head, Department of Community Medicine, Armed Forces Medical College, Pune, Maharashtra, India

Date of Submission22-Aug-2020
Date of Decision31-Oct-2020
Date of Acceptance08-Dec-2020
Date of Web Publication29-Jan-2021

Correspondence Address:
Rajesh Sahu
Department of Community Medicine, Armed Forces Medical College, Pune - 411 040, Maharashtra
India
Login to access the Email id

Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijph.IJPH_1045_20

Rights and Permissions
   Abstract 


Background: A suspected food-poisoning outbreak occurred in a residential school in Mirzapur, India, in February, 2017. Objective: We investigated the outbreak to find out the epidemiology and to identify the risk factors. Methods: A descriptive study followed by retrospective-cohort study was done to investigate the outbreak. Cases (defined as ≥3 or more loose stools in 24 h, abdominal pain, or vomiting with onset between February 1 and 4, 2017) were searched by reviewing sick/patient registers from school and nearby health facilities. Cases were also searched through active surveillance by visiting school hostels. Stool samples were sent for microbiological testing. Food sources and food handlers were also assessed. Results: Among 468 students, 204 cases were identified (44% attack rate) without any mortality. The median age was found to be 14 years (range: 10–18 years) and 59% were male. Relative risk with consumption of curd, apple, and panjiri (sweetened wheat flour) was found to be 15.4, 2.5, and 3.7, respectively. All these three food items were served as prasad, a religious offering. Only consumption of sweetened curd (adjusted odds ratio = 36.1, 95% confidence interval = 12.1–107.8) was significantly associated with gastroenteritis. No microorganism was isolated from two tested stool samples. Curd from the vendor was prepared from nonpasteurized milk. There were no illnesses among food-handlers. Conclusions: This outbreak of acute gastroenteritis in a residential school was associated with consumption of curd, likely contaminated with preformed toxins. We recommend implementation of the food safety and standards authority of India regulations.

Keywords: Food poisoning, Foodborne diseases, gastroenteritis, outbreak investigation, retrospective cohort study


How to cite this article:
Sahu R, Ray A L, Yadav A K, Kunte R, Faujdar D S, Working Group*. Acute gastroenteritis outbreak in a school associated with religious ceremony in Mirzapur District, Uttar Pradesh, India. Indian J Public Health 2021;65, Suppl S1:18-22

How to cite this URL:
Sahu R, Ray A L, Yadav A K, Kunte R, Faujdar D S, Working Group*. Acute gastroenteritis outbreak in a school associated with religious ceremony in Mirzapur District, Uttar Pradesh, India. Indian J Public Health [serial online] 2021 [cited 2021 Feb 28];65, Suppl S1:18-22. Available from: https://www.ijph.in/text.asp?2021/65/5/18/308315

Working Group: Samir V. Sodha, CDC Resident Advisor, US Centers for Disease Control and Prevention (CDC), Atlanta, Georgia, USA; Sushma Choudhary, India Epidemic Intelligence Services Officer, National Centre for Disease Control, New Delhi; R. Singh, State Epidemiologist; V. Kumar, State Entomologist, State Surveillance Office, Integrated Disease Surveillance Program, Swasthya Bhawan, Lucknow, Uttar Pradesh, India





   Introduction Top


Foodborne diseases, commonly manifesting as acute diarrheal diseases, caused an estimated 600 million illnesses with 420,000 deaths in 2010 worldwide.[1] There are no estimates of foodborne disease burden in India, but acute diarrheal diseases and food-poisoning accounted for 40% (778/1935) of all reported outbreaks in 2015.[2] In many parts of India, acute diarrheal disease outbreaks are assumed to be waterborne without an in-depth epidemiological investigation. There is likely a higher burden of foodborne outbreaks in India than currently reported.[3]

Foodborne outbreaks draw media and political attention especially when a well-known school is affected. Such outbreaks in residential schools have far-reaching consequences beyond health-care emergencies. These incidents lead to disruption in academics and development of hostile environment causing fear among students and parents.[4]

A suspected foodborne outbreak was reported in a residential school with students from grade 6–12 in Mirzapur district, Uttar Pradesh, India, on February 1, 2017. There was a large media and political attention, but no cause of the outbreak was identified leading to rumors and speculations. An outbreak investigation team, including officers from Uttar Pradesh's Integrated Disease Surveillance Programme, and an Epidemic Intelligence Service (EIS) officer from the National Centre for Disease Control (NCDC), New Delhi, were deployed to the campus of the residential school, located 37 km from district headquarters of Mirzapur, Uttar Pradesh. We investigated the outbreak to find out the epidemiology and to identify the risk factors.


   Materials and Methods Top


Case finding

We defined a case as three or more loose stools in 24 h, abdominal pain, or vomiting with onset between February 1 and 4, 2017, in a resident of the school campus. We conducted passive surveillance by reviewing the register of sick students and staff at the school and patient registers of hospitals where cases were treated. We carried out active case finding by conducting a comprehensive case search in hostels and staff quarters on the school campus.

Retrospective cohort study

Retrospective cohort study was conducted by including all the students who were present on the school campus on February 1, 2017. We excluded students suffering from abdominal pain, vomiting, or loose stools before February 1, 2017. We interviewed students using a pretested semi-structured questionnaire. Details regarding sociodemographics, food, and drink items consumed on January 31, 2017, and February 01, 2017, symptoms, course of illness, and treatment sought were included in the questionnaire. Details of symptoms (including fever) were recorded based on the interview findings. Students who were present in the school on February 01, 2017, but were on leave as on date of interview were interviewed by phone. We calculated food-specific attack rates, relative risks for each food items, and did a multivariate logistic regression analysis of food items with P < 0.2 on univariate analysis using Epi Info version 7.2.0.1, Centers for Disease Control, Atlanta, Georgia, USA. In this model, three food items, including sweetened curd, panjiri (sweetened flour), and apple were included. We checked for the presence of any confounding and interaction among the factors with P < 0.2.

Laboratory investigations

We collected two stool samples on February 03, 2017, from symptomatic cases to isolate Salmonella sp., Shigella sp., Vibrio cholerae, Escherichia coli, and Campylobacter sp. by culture at the microbiology laboratory of King George's Medical University, Lucknow. However, no toxin testing was available.

Environmental investigations

We assessed hygiene and sanitation of the school's kitchen, food storage facilities, and area where all students consumed food. We evaluated the supply chain of epidemiologically implicated food items. We also clinically examined all food handlers to rule out any obvious infection. No food samples were available for testing.

Ethical considerations

The investigation was a public health response to an outbreak as part of the India EIS Program, undertaken with the purpose to identify the source of spread for immediate control of outbreak and intended for benefit of the community at large. Ethical approval is not applicable as a part of public health response. The investigation did not involve any human laboratory sample collection for research purpose and there were no invasive investigations or medical interventions/experiments. Ethical principles and guidelines as laid down by ICMR were maintained during the outbreak response: the investigation was aimed at achieving public good (beneficence) and collective welfare (solidarity); no harm was done to any individual (non-maleficence); fair, honest, and transparent (accountability and transparency); and participants' data were de-identified prior to analysis (confidentiality).


   Results Top


Descriptive epidemiology

We identified 204 cases (59% males) with a median age of 14 years (range: 10–18 years). Onset of symptoms in the index case occurred at 6 pm on February 1, 2017 [Figure 1]. Of all cases, 123 (60%) occurred between 9 pm on February 1 and 12 am on February 2, 2017 and the last case occurred at 6 pm on February 2, 2017. Among the 204 cases, 193 (95%) cases were residing in the hostel and 11 (5%) cases were in the staff quarters. Cases were reported from all hostel blocks without any clustering.
Figure 1: Distribution of cases of acute gastroenteritis by time of onset at residential school A, Mirzapur, Uttar Pradesh, February 2017 (n = 204).

Click here to view


All 204 (100%) cases had at least one gastrointestinal symptom of abdominal pain, nausea, vomiting, or diarrhea. Of these, 162 (79%) had abdominal pain, 89 (44%) nausea or vomiting, 77 (38%) diarrhea, 72 (36%) giddiness, 45 (22%) headache, 38 (19%) fever, and 22 (11%) unconsciousness. Of all cases, 67 (33%) were hospitalized. There were no deaths. The median duration of illness was 18 h (range: 1–34 h). The cases were treated with oral fluids (100%), hyoscine butylbromide (78%) as antispasmodic, ciprofloxacin (45%) as an antibiotic, and intravenous fluids (33%).

Retrospective cohort study

Among 534 resident students, 28 (5%) were not present on the campus on February 1, 2017. The remaining 506 qualified to be enrolled as participants in the cohort study, but 38 (8%) could not be contacted in person or by phone despite three attempts. Thus, we interviewed 468 students (92% participation rate). Among the 468 students, 297 (63%) were male; median age was 14 years (10–19 years). There were 204 cases (attack rate = 44%).

Food-specific attack rates were calculated for each specific food item served by the school [Table 1]. The consumption of charnamrit (sweetened curd), which was served as part of prasad (religious offering) after a vasantpanchmipooja (religious ceremony) had the strongest association with the illness (relative risk [RR] = 15.4, 95% confidence interval [CI] = 5.8–40.4). Apple(RR = 2.5, [95% CI = 1.5–3.8]) and panjiri (sweetened wheat flour mixed with oil, RR = 3.8, 95% CI = 2.1–6.7) were also served as prasad with the sweetened curd and were the only other items associated with illness.
Table 1: Food specific attack rates and risk ratios of acute gastroenteritis in a Cohort of Students of Residential School A, Mirzapur, Uttar Pradesh, February 2017 (n=468)

Click here to view


Using multiple logistic regression in a model including risk factors associated with illness at P < 0.20, we found that only consumption of sweetened curd (adjusted odds ratio of 36.1, 95% CI = 12.1–107.8) was significantly associated with illness. We did not observe significant confounding or effect modification by any exposure. Considering the time of consumption of curd as the exposure time (1:30 pm on February 1, 2017), we calculated the median incubation period of 9 h (range: 4–37 h).

Laboratory investigations

Two stool samples showed the absence of white blood cells or red blood cells and culture did not yield any growth.

Environmental investigation

Approximately 20 L of curd were procured from the dairy supplying milk to the school. This dairy was closed by the owner after the incident and we could not investigate. However, the dairy was neither registered nor licensed under the government regulatory body, Food Safety Standards Authority of India (FSSAI), which is mandated for all dairies. A dairy worker reported that the curd was prepared from raw milk that was not pasteurized before being curdled.

At the school, there was no evidence of sanitation infractions except for signs of rodent infestation in the ration store. No refrigeration facilities were available. The assessment of personal hygiene and clinical examination of all food handlers did not reveal any violations.


   Discussion Top


We evaluated a foodborne outbreak of acute gastroenteritis in a residential school strongly associated with consuming curd offered as prasad, a religious offering after a religious ceremony. Despite limited laboratory findings, evidence from the clinical, epidemiological, and environmental investigations strongly suggest this was a toxin-mediated outbreak.

There were limited laboratory investigations for this outbreak for multiple reasons. In many districts in India, including Mirzapur, there is limited laboratory capacity available. In addition, most patients had recovered by the time our investigation had begun. Nevertheless, our team was able to collect two stool samples from active cases, and the results were consistent with a noninflammatory diarrhea and showed no growth on culture.

Despite the inability to isolate an etiological agent, our investigation suggests that illness was consistent with a toxin-mediated illness, likely from Bacillus cereus toxin. Similar to the distribution of symptoms in this outbreak, B. cereus gastroenteritis commonly presents with abdominal pain, diarrhea, and vomiting.[5] The duration of illness in B. cereus gastroenteritis is usually <24 h, consistent with this outbreak (median duration = 18 h), and the incubation period for B. cereus is known to vary between 6 and 15 h, which was consistent with the median incubation period of 9 h in the present outbreak. Furthermore, commonly incriminated food items in B. cereus illness include rice and milk products, consistent with the association of illness in this outbreak with curd.[5] Toxin-mediated foodborne illness from Staphylococcus aureus and Clostridium perfringens may also present with similar clinical features, but were less likely as the incubation period of S. aureus is much shorter (30 min–6 h) and C. perfringens is usually not associated with milk products.[6],[7],[8]

Environmental investigations found the absence of pasteurization before curdling and serving to students. This potential hazard, combined with lack of cold chain, possibly caused the contaminated milk to turn into contaminated curd.[9] Curd and dairy products are a common and important part of the Indian diet. A large number of unorganized small dairies are operational in India especially at local levels, many of them are not registered under the FSSAI.[10],[11] Most of these dairies do not conform to these food safety standards and pose many potential public health hazards to consumers (e.g., Staphylococcus sp., B. cereus, Salmonella sp., E. coli, Streptococcus pyogenes, M. bovis, Brucella sp., pesticides, and chemical adulterants) and may lead to outbreaks such as this one.[12],[13]

The burden and risk due to nonadherence with food safety standards likely underestimated curd as the suspected vehicle. Despite limited laboratory support in this study, strong evidence generated through a well-designed epidemiological study helped in identifying the incriminated food item. This supports the continued need for field epidemiology training such as the India EIS, a 2-year advanced training program at NCDC in collaboration with the United States Centers for Disease Control and Prevention (CDC). As India EIS continues to grow and expand, epidemiological capacity in India will improve to investigate similar outbreaks and other public health problems in the country.[14]

During this outbreak, antibiotics were administered to all admitted cases without any laboratory confirmation. However, evidence suggests that most diarrhea cases do not require antibiotics as the duration of illness is not shortened by its use.[15] Antibiotic microbial resistance (AMR) is a growing global public health concern especially in India.[16] Unregulated overuse of antibiotics, high burden of infectious diseases, limited clinical and laboratory diagnostic capacity, and poor infection control and hygiene practices in health-care facilities all contribute to the high prevalence of AMR in India. Indiscriminate use of antibiotics, such as in this outbreak, remains an important challenge to address AMR.[17],[18],[19] Such practices are of concern and need to be curbed moving forward as a part of a multi-pronged strategy to tackle AMR.[19],[20],[21]

There were limitations to our investigation. First, there was limited laboratory capacity with only two stool samples available for culture. Second, there may have been recall bias in collecting information from students. However, this was likely minimal because the investigation started within 48 h and we were still able to find a strong association of illness with the curd. Third, our environmental investigation was unable to perform a detailed assessment of the dairy and farm from where curd and milk were supplied.

As a part of the public health action arising from this investigation, the school authorities were apprised of the investigations results. One of the findings was that the lack of a cold chain could have led to the contaminated curd. The school authorities initiated measures to ensure good hygiene in the school's kitchen, food storage facilities, and area where all students consumed food, which included creating a facility for cold storage.


   Conclusion Top


To improve food safety in India, there is a need to fully implement regulations under FSSAI in all parts of the country, including remote and rural areas to ensure pasteurization of milk, curdling under aseptic conditions, and health education for all food-handlers. There is also a need for the capacity building of laboratories and epidemiologists to detect outbreaks and identify etiologies and to be sensitized about the importance of collecting and testing clinical samples and judicious use of any antibiotics during outbreaks.

Acknowledgments

We would like to acknowledge contribution of all health workers, working at Community Health Centre, Manihar who helped us conduct this study.

This manuscript has been approved by the Director, NCDC, Ministry of Health and Family Welfare, New Delhi, India.

Financial support and sponsorship

This public health activity was conducted by India EIS program of National Centre for Disease Control at the request of the Government of Uttar Pradesh. The National Centre for Disease Control receives funding support for the India EIS Program through cooperative agreement No. NU2GGH001904GH10-1001 from the U.S. Centers for Disease Control and Prevention, Center for Global Health, Division of Global Health Protection. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Conflicts of interest

There are no conflicts of interest.



 
   References Top

1.
Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med 2015;12:e1001923.  Back to cited text no. 1
    
2.
Ministry of Health & Family Welfare, Government of India. About Integrated Disease Surveillance. Available from: http://idsp.nic.in/index4.php ?lang= 1&level=0&linkid=313&lid=1592. [Last accessed on 2017 May 26].  Back to cited text no. 2
    
3.
Vemula SR, NaveenKumar R, Polasa K. Foodborne diseases in India – A review. Br Food J2012;114:661-80.  Back to cited text no. 3
    
4.
Johler S, Weder D, Bridy C, Huguenin MC, Robert L, Jorg H, et al. Outbreak of staphylococcal food poisoning among children and staff at a Swiss boarding school due to soft cheese made from raw milk. J Dairy Sci 2015;98:2944-8.  Back to cited text no. 4
    
5.
Bennett SD, Walsh KA, Gould LH. Foodborne disease outbreaks caused by Bacillus cereus, Clostridium perfringens, and Staphylococcus aureus – United States, 1998-2008. Clin Infect Dis 2013;57:425-33.  Back to cited text no. 5
    
6.
Grass JE, Gould LH, Mahon BE. Epidemiology of foodborne disease outbreaks caused by Clostridium perfringens, United States, 1998–2010. Foodborne Pathog Dis 2013;10:131-6.  Back to cited text no. 6
    
7.
Hennekinne JA, De Buyser ML, Dragacci S. Staphylococcus aureus and its food poisoning toxins: Characterization and outbreak investigation. FEMS Microbiol Rev 2012;36:815-36.  Back to cited text no. 7
    
8.
Nema V, Agrawal R, Kamboj DV, Goel AK, Singh L. Isolation and characterization of heat resistant enterotoxigenic staphylococcus aureus from a food poisoning outbreak in indian subcontinent. Int J Food Microbiol 2007;117:29-35.  Back to cited text no. 8
    
9.
Tewari A, Abdullah S. Bacillus cereus food poisoning: International and indian perspective. J Food Sci Technol 2015;52:2500-11.  Back to cited text no. 9
    
10.
Patel NK. Role of unorganized dairy sector in rural development. Int J Commer Bus Manag 2010;2:86-92.  Back to cited text no. 10
    
11.
Ministry of Health & Family Welfare. Government of India. Food Safety and Standards (Licensing and Registration of Food Businesses) Regulation; 2011. Available from: http://www.fssai.gov.in/home/fss-legislation/fss-regulations.html. [Last accessed on 2017 Nov 28].  Back to cited text no. 11
    
12.
Groot MJ, Van't Hooft KE. The hidden effects of dairy farming on public and environmental health in the netherlands, india, ethiopia, and uganda, considering the use of antibiotics and other agro-chemicals. Front Public Health 2016;4:12.  Back to cited text no. 12
    
13.
Government of India. Food Safety and Standards Authority of India. Expert Group on Milk and Milk Products Base Working Paper on Strategy and Action Plan for Ensuring Safety of Milk and Milk Products. Available from: http://old.fssai.gov.in/Portals/0/Baseworkingpaper_june2009.pdf. [Last accessed on 2017 Dec 15].  Back to cited text no. 13
    
14.
Lubogo M, Donewell B, Godbless L, Shabani S, Maeda J, Temba H, et al. Ebola virus disease outbreak; the role of field epidemiology training programme in the fight against the epidemic, Liberia, 2014. Pan Afr Med J 2015;22 Supp 1:5.  Back to cited text no. 14
    
15.
Riddle MS, DuPont HL, Connor BA. ACG clinical guideline: Diagnosis, treatment, and prevention of acute diarrheal infections in adults. Am J Gastroenterol 2016;111:602-22.  Back to cited text no. 15
    
16.
Ganguly NK, Arora NK, Chandy SJ, Fairoze MN, Gill JP, Gupta U, et al.; Global Antibiotic Resistance Partnership (GARP)-India Working Group. Rationalizing antibiotic use to limit antibiotic resistance in India. Indian J Med Res 2011;134:281-94.  Back to cited text no. 16
[PUBMED]  [Full text]  
17.
Chandy SJ, Michael JS, Veeraraghavan B, Abraham OC, Bachhav SS, Kshirsagar NA. ICMR programme on Antibiotic Stewardship, Prevention of Infection & Control (ASPIC). Indian J Med Res 2014;139:226-30.  Back to cited text no. 17
[PUBMED]  [Full text]  
18.
Laxminarayan R, Chaudhury RR. Antibiotic resistance in india: Drivers and opportunities for action. PLoS Med 2016;13:e1001974.  Back to cited text no. 18
    
19.
Swaminathan S, Prasad J, Dhariwal AC, Guleria R, Misra MC, Malhotra R, et al. Strengthening infection prevention and control and systematic surveillance of healthcare associated infections in india. BMJ 2017;358:j3768.  Back to cited text no. 19
    
20.
Ayukekbong JA, Ntemgwa M, Atabe AN. The threat of antimicrobial resistance in developing countries: Causes and control strategies. Antimicrob Resist Infect Control 2017;6:47.  Back to cited text no. 20
    
21.
Mahapatra T, Mahapatra S, Banerjee B, Mahapatra U, Samanta S, Pal D, et al. Predictors of rational management of diarrhea in an endemic setting: Observation from India. PLoS One 2015;10:e0123479.  Back to cited text no. 21
    


    Figures

  [Figure 1]
 
 
    Tables

  [Table 1]



 

Top
 
 
  Search
 
    Similar in PUBMED
   Search Pubmed for
   Search in Google Scholar for
 Related articles
    Access Statistics
    Email Alert *
    Add to My List *
* Registration required (free)  

 
  In this article
    Abstract
   Introduction
    Materials and Me...
   Results
   Discussion
   Conclusion
    References
    Article Figures
    Article Tables

 Article Access Statistics
    Viewed238    
    Printed2    
    Emailed0    
    PDF Downloaded28    
    Comments [Add]    

Recommend this journal