|Year : 2021 | Volume
| Issue : 5 | Page : 29-33
Shellfish poisoning outbreaks in Cuddalore District, Tamil Nadu, India
Anoop Velayudhan1, Janardhan Nayak1, Manoj V Murhekar2, Tanzin Dikid3, Samir V Sodha4, Working Group*5
1 EIS Officer, Epidemic Intelligence Service India Programme, National Centre for Disease Control, New Delhi, India
2 Director, National Institute of Epidemiology, Chennai, India
3 Deputy Director, National Centers for Disease Control, Ministry of Health and Family Welfare, Government of India, New Delhi, India
4 Resident Advisor, EIS CDC India, Centers for Disease Control and Prevention, Atlanta, Georgia, USA
|Date of Submission||19-Aug-2020|
|Date of Decision||08-Oct-2020|
|Date of Acceptance||08-Dec-2020|
|Date of Web Publication||29-Jan-2021|
EIS Officer, National Centres for Disease Control, New Delhi
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Background: Two suspected shellfish poisoning events were reported in Cuddalore District in Tamil Nadu, India, between January and April 2015. Objectives: The study was conducted to confirm the outbreaks and to identify the source and risk factors. Methods: For both outbreaks, a case was defined as a person with nausea, vomiting, or dizziness. Sociodemographic details and symptoms were noted down. Data were also collected in a standard 3-day food frequency questionnaire, along with a collection of clam samples. A case–control study was initiated in the April outbreak. Stool samples were collected from cases, and clam vendors were interviewed. Results: In an outbreak that happened in January, all the twenty people reported to be consumed clams were diagnosed as cases (100% attack rate, 100% exposure rate). In the April outbreak, we identified 199 cases (95% attack rate). In both outbreaks, the clams were identified as genus Meretrix meretrix. The most common reported symptoms were dizziness and vomiting. The clams heated and consumed within 30–60 min. No heavy metals or chemicals were detected in the clams, but assays for testing shellfish toxins were unavailable. All 64 selected cases reported clam consumption (100% exposure rate) as did 11 controls (17% exposure rate). Illness was associated with a history of eating of clams (odds ratio = 314, 95% confidence interval = 39–512). Of the six stool samples tested, all were culture negative for Salmonella, Shigella, and Vibrio cholerae. The water at both sites was contaminated with garbage and sewage. Conclusion: Coordinated and timely efforts by a multidisciplinary team of epidemiologists, marine biologists, and food safety officers led to the outbreaks' containment.
Keywords: Case–control study, India, outbreak investigation, Meretrix meretrix, Shellfish poisoning
|How to cite this article:|
Velayudhan A, Nayak J, Murhekar MV, Dikid T, Sodha SV, Working Group*. Shellfish poisoning outbreaks in Cuddalore District, Tamil Nadu, India. Indian J Public Health 2021;65, Suppl S1:29-33
|How to cite this URL:|
Velayudhan A, Nayak J, Murhekar MV, Dikid T, Sodha SV, Working Group*. Shellfish poisoning outbreaks in Cuddalore District, Tamil Nadu, India. Indian J Public Health [serial online] 2021 [cited 2022 Jan 27];65, Suppl S1:29-33. Available from: https://www.ijph.in/text.asp?2021/65/5/29/308318
V. Kumar, MPH Scholar, National Institute of Epidemiology,
Chennai, India; G. K. Durairaj, State Epidemiologist, Department of Public Health
and Preventive Medicine, Government of Tamil Nadu, India; P. Manoharan,
District Epidemiologist, Department of Public Health and Preventive Medicine,
Government of Tamil Nadu, India; R. Sivadoss, Deputy Director, Department of
Public Health and Preventive Medicine, Government of Tamil Nadu, India; S.
Balasubramanian, State Surveillance Officer, Department of Public Health and
Preventive Medicine, Government of Tamil Nadu, India; K. R. Jawaharlal, Deputy
Director, Department of Public Health and Preventive Medicine, Government of
Tamil Nadu, India; V. Kesavan, Municipal Health Officer, Urban Health Center,
Government of Tamil Nadu, India; P. Srikantiah, Senior Medical Epidemiologist,
CDC India Centers for Disease Control and Prevention, Atlanta, Georgia, USA;
K. F. Laserson, Country Director, CDC India, Centers for Disease Control and
Prevention, Atlanta, Georgia, USA; M. Dwivedi, Senior Lab Advisor, CDC India,
Centers for Disease Control and Prevention, Atlanta, Georgia, USA; A. Desai,
MPH Scholar, Columbia University, Mailman School of Public Health, MPH
Program, New York, USA; S. Bragadeeswaran, Professor, Centre for Advanced
Study, Marine Biology, Annamalai University, Parangipettai, Tamil Nadu, India;
S. Venkatesh, Director, National Centers for Disease Control, Ministry of Health
and Family Welfare, Government of India, New Delhi, India
| Introduction|| |
According to the World Health Organization (WHO), one out of every ten people worldwide suffers from foodborne diseases annually. It has been estimated that 600 million foodborne illnesses and 420,000 deaths occurred in 2010. Although foodborne diseases are an important cause of morbidity and mortality worldwide, information on the extent and burden arising from chemical and parasitic contaminants in food is limited. There are over 2000 cases of paralytic shellfish poisoning reported globally every year with 15% mortality rate, but the burden is likely underestimated in developing countries.,
Clams, a type of shellfish or bivalve mollusc, are filter feeders that accumulate toxins in their digestive organs and soft tissues without lethality to themselves. Toxins produced in large quantities during episodic harmful algal blooms (HABs), known as “red tides,” affect a wide range of marine organisms that ingest these toxins and bioaccumulate them over time. Bivalve organisms, such as mussels, clams, and oysters, are the primary transvector for shellfish poisoning when contaminated with a bacteria, virus, or toxin.
India has a long coastline with easy access to seafood. Clams are widely eaten by poor and middle-class coastal populations in these areas, and seafood poisoning from contaminated shellfish is a dietary risk in these populations. Paralytic shellfish poisoning was first reported in Tamil Nadu State in 1981 when 82 serious cases, including three deaths, were reported after a history of oyster consumption. Although similar outbreaks have been subsequently reported in South India, many are likely missed and may not be well described.
In 2015, Cuddalore district in Tamil Nadu State reported two events of shellfish poisoning among impoverished and marginalized communities, the first in January 2015 and the second in April 2015. In this background, the epidemic investigation was carried out to confirm the outbreak and to identify the source and risk factors of this outbreak.
| Materials and Methods|| |
January 2015 outbreak
On January 29, 2015, the Integrated Disease Surveillance Program (IDSP), Cuddalore District, reported 14 people admitted to the district hospital with complaints of vomiting and dizziness after consuming clams. All 14 were from Cuddalore Ward I, an urban area with a population of 222 people.
We defined a case as a person with nausea, vomiting, or dizziness in a resident of Ward I of Cuddalore District from January 28, 2015, to January 30, 2015. We searched for cases by house-to-house survey and administered a questionnaire to collect sociodemographic details and symptoms and a standard 3-day food frequency questionnaire. Because preliminary food histories of hospitalized cases reported clam consumption, we also specifically asked about consuming clams. Ten uneaten clam samples were collected and sent to the Institute of Marine Biology, Annamalai University, for identification and microbiological analysis. In-depth interviews were conducted with housewives to ascertain the method of food preparation. Vendors were not traceable to help identify environmental sources.
April 2015 outbreak
On April 4, 2015, 64 people from Kondur Village, a rural area of Cuddalore District, reported to the emergency department of Cuddalore District Hospital with complaints of vomiting and dizziness after consuming clams that day. Kondur Village has a population of 1410 people and is located 14 km from Ward I, the location of the January 2015 outbreak.
We defined a case as a person with nausea, vomiting, or dizziness in a resident of Kondur Village on April 4, 2015. We searched for cases by reviewing medical records and by a house-to-house survey. We used a questionnaire to obtain sociodemographic details and symptoms and a standard 3-day food frequency questionnaire.
We conducted an unmatched 1:1 case–control study to test the hypothesis of shellfish poisoning. We calculated a sample size of 65 cases and 65 controls based on 95% confidence interval (CI), 80% power, estimated 20% control exposure rate to clams, and a desired odds ratio (OR) of at least 3. We systematically sampled every third case from the line list sorted by time of illness onset. Controls were selected randomly from houses at least two houses apart from a case.
Stool samples were collected from cases with a history of active diarrhea on April 6, 2015 and samples were sent to the Cuddalore District Public Health Laboratory and the Madras Medical College, Chennai, for culture of Salmonella, Shigella, and Vibrio cholerae. Environmental samples, such as clams, sand, and water, were also collected from the fishing site on April 7, 2015, and were sent to the Marine Biology Department of Annamalai University, Parangipettai, to detection and identification of toxins. Focus group discussion was carried out in Kondur Village with housewives to learn about cooking and cultural food practices. Clam vendors were interviewed to acquire information about clam fishing and vending.
The investigation was a public health response to an outbreak as a part of the India Epidemic Intelligence Service Program, undertaken with the purpose to identify the source of spread for immediate control of outbreak and intended for the 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 purposes, and there were no invasive investigations or medical interventions/experiments. All Government of India ethical principles and guidelines were adopted during the outbreak response: the investigation was aimed at achieving public good (beneficence) and collective welfare (solidarity); no harm was done to any individual (nonmaleficence); fair, honest, and transparent (accountability and transparency); and participants' data were de-identified before analysis (confidentiality).
| Results|| |
January 2015 outbreak
We surveyed 222 individuals in Ward 1 and identified twenty cases: 45% males from six households with a median age of 16.5 years (range: 3–62 years); most were agricultural laborers. The most common presenting symptoms were dizziness (95%), followed by vomiting (45%). All cases reported clam consumption for 100% exposure rate and 100% attack rate. The community attack rate was 9% (20/222).
The illness onset time period was within a 3-h window between 6 and 9 PM on January 29, 2015 [Figure 1]. The median incubation period from clam consumption to illness was 15 min (range: 0–60 min). Clams were identified as the genus Meretrix meretrix. Clams were purchased from local vendors on January 29, 2015. They were cooked within 30 min of purchase without any additional ingredients in three households by dry heating in a pan for 15–20 min until the clams burst open, exposing the edible flesh. The clams were distributed to other neighboring houses and eaten within 30 min from the time of preparation.
|Figure 1: Shellfish poisoning cases by time of illness onset, Ward I, Cuddalore District, Tamil Nadu, India, January 29, 2015 (n = 20).|
Click here to view
April 2015 outbreak
Among the 210 people in Kondur Village, we identified 199 cases: 47% males with median age of 22 years (range: 2–70 years). Symptoms reported were dizziness (95%), vomiting (94%), nausea (51%), headache (7%), abdominal cramps (6%), fever (4%), diarrhea (3%), perioral paresthesia (3%), and distal paresthesia (1%). The attack rate was 95%. The median incubation period from clam consumption to illness onset was 30 min (range: 5–140 min) [Figure 2].
|Figure 2: Shellfish poisoning cases by time of illness onset, Kondur Village, Cuddalore District, Tamil Nadu, India, April 4, 2015 (n = 199).|
Click here to view
Cases and controls were similar with respect to socioeconomic status and educational status [Table 1]. All 64 selected cases reported clam consumption for a 100% exposure rate, while only 11 controls reported eating the clams for a 17% exposure rate. Illness was associated with a history of eating of clams (OR = 314, 95% CI = 39–512).
|Table 1: Characteristics of cases and controls in Kondur Village, Cuddalore District, Tamil Nadu, India, April 4, 2015|
Click here to view
Of the six stool samples tested, all were culture negative for Salmonella, Shigella, and Vibrio cholerae. The clams were identified as genus M. meretrix. Housewives reported that they believed consuming clams helped prevent jaundice. They prepared the clams by washing them with water, heating them in a dry pan for 15–20 min until they opened, and then scooping out and eating the edible flesh without any condiments or spices within 1 h from the time of preparation.
Six of the seven reported vendors were traceable, and each said that had moved from their usual place of catching clams, from Gedilam River to Pennai River, on April 4 to catch bigger clams. There were no heavy metals or chemicals detected from either the clams, sand, and water samples, but assays for testing shellfish toxins were not available in the laboratory. We observed that the water at both the Gedilam River and Pannai River was contaminated with garbage and sewage.
Intervention and follow-up
In January, based on our investigation, the Cuddalore District Health Team and the Food Safety Department collaborated to prohibit the sale of shellfish in the area for the next 3 months. No subsequent cases with similar exposures were reported in Cuddalore District until the second outbreak in April. Then, the Tamil Nadu State Health Department and the Cuddalore Food Safety Department prohibited the sale of shellfish for another 3 months. No outbreaks were subsequently reported from this area through 2017.
| Discussion|| |
These were two consecutive outbreaks of shellfish poisoning in Cuddalore District reported through IDSP. These outbreaks represented a potential public health problem in coastal areas of India. The investigations highlight the importance of rapid epidemiological response and intersectoral coordination between health authorities and food safety regulators to identify risk factors for foodborne outbreaks and to implement effective control and prevention measures.
There are four types of shellfish poisoning currently recognized: paralytic shellfish poisoning caused by saxitoxin; neurotoxic shellfish poisoning caused by brevetoxin; diarrheal shellfish poisoning caused by okadaic acid; and amnesic shellfish poisoning caused by domoic acid. The specific type of shellfish poisoning in this outbreak could not be ascertained due to a lack of a specific commercial assay to detect the exact toxin. However, clams were identified as M. meretrix in both outbreaks. Studies have shown that this species exhibits bioaccumulation of paralytic shellfish toxins, albeit usually in sublethal concentrations., The presenting symptoms of vomiting and dizziness, and the absence of diarrhea, loss of coordination, speech defects, and memory loss in both outbreaks were suggestive of paralytic shellfish poisoning from low concentrations of toxin consumption. In addition, the April 2015 outbreak included several patients with perioral and distal paresthesia. Ingestion of the toxin was likely lower than the threshold to produce severe neurological symptoms ranging from tightness of the throat to total muscular paralysis, respiratory arrest, and death., Paralytic shellfish poisoning is caused by saxitoxin, and the source of toxin is dinoflagellates. These toxins are heat stable and remain even after the food has been cooked., HABs, resulting from increased anthropogenic activities such as environmental pollution of oceans, accelerated by climate change, can facilitate the accumulation of toxin into bivalve molluscs, leading to shellfish poisonings. The presence of sewage and garbage, as seen at the fishing site during the April 2015 outbreak, could have contributed to water pollution and stagnation, bio-amplifying the nutrients available for dinoflagellates, leading to an increase of HABs. In addition, climate research suggests that an increase in ocean temperature may facilitate intensification of HABs. Outbreaks can be prevented by advising the vendors and public to avoid harvesting clams during HABs and from polluted waters.
Although shellfish poisoning has been documented in Tamil Nadu before, this was the first-time shellfish poisoning outbreaks were reported through the state's IDSP. The IDSP District Unit identified the outbreak cluster from reports of increased hospital emergency consultations and promptly alerted the Tamil Nadu IDSP State Team that decided to investigate. In recent years, the India National Centre for Disease Control (NCDC) in collaboration with the United States Centres for Disease Control and Prevention (CDC) have been working to increase public health capacity of districts and states to detect and respond to outbreaks such as these. To augment the availability of field epidemiologists at subdistrict, district, and state level, NCDC, in collaboration with CDC, initiated the India Epidemic Intelligence Service (EIS) program, an intensive 2-year training in field epidemiology. In addition, short-term district-level epidemiological and laboratory trainings were conducted in Cuddalore District in 2014. These trainings helped improve the capacity to detect and investigate this outbreak by the district with assistance from India EIS officers from NCDC.
Our investigations had several limitations. First, the toxin could not be identified from clinical or environmental samples because of nonavailability of the assay. However, we were still able to identify shellfish poisoning as the source of the outbreak based on our epidemiological investigations. Traceback investigations were limited in the January 2015 outbreak because of the major role of the informal sector in the food supply chain. However, with the April 2015 outbreak investigation, detailed investigation and interviews led to the identification of the likely source of clams.
Findings of the investigations were shared with the state health department and food safety department and led to the prohibition of sale of shellfish during the HABs. No outbreaks were subsequently reported from this area through 2017.
| Conclusion|| |
Coordinated and timely efforts by a multidisciplinary team of epidemiologists, marine biologists, and the food safety officers led to the containment of these shellfish poisonings and prevention of future outbreaks. These outbreaks were examples of the potential avenue to improve food safety through rapid outbreak detection and a closely coordinated response. We recommend such collaborations be further institutionalized across India.
We acknowledge the residents of the two affected areas for their willingness to share information and participate in this outbreak investigation. We thank the Cuddalore District Health Administration for their cooperation and assistance during field activities.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
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.
Hald T, Aspinall W, Devleesschauwer B, Cooke R, Corrigan T, Havelaar AH, et al.
World health organization estimates of the relative contributions of food to the burden of disease due to selected foodborne hazards: A Structured expert elicitation. PLoS One 2016;11:e0145839.
Hoffmann S, Devleesschauwer B, Aspinall W, Cooke R, Corrigan T, Havelaar A, et al.
Attribution of global foodborne disease to specific foods: Findings from a world health organization structured expert elicitation. PLoS One 2017;12:e0183641.
Havelaar AH, Kirk MD, Torgerson PR, Gibb HJ, Hald T, Lake RJ, et al
. Group on behalf of WHO FDBER. World Health Organization global estimates and regional comparisons of the burden of foodborne disease in 2010. PLoS Med 2015;12:e1001923.
Potasman I, Paz A, Odeh M. Infectious outbreaks associated with bivalve shellfish consumption: A worldwide perspective. Clin Infect Dis 2002;35:921-8.
Ciminiello P, Fattorusso E. Bivalve molluscs as vectors of marine biotoxins involved in seafood poisoning. Prog Mol Subcell Biol 2006;43:53-82.
Van Dolah FM. Marine algal toxins: Origins, health effects, and their increased occurrence. Environ Health Perspect 2000;108 Suppl 1:133-41.
Livingstone DR, Gallacher S. Shellfish Contamination and Spoilage of Molluscs and Crustaceans. In: Caballero B, editor. Encyclopedia of Food Sciences and Nutrition. 2nd
ed. Oxford: Academic Press; 2003. p. 5228-45.
James KJ, Carey B, O'Halloran J, van Pelt FN, Skrabáková Z. Shellfish toxicity: Human health implications of marine algal toxins. Epidemiol Infect 2010;138:927-40.
Sharma R, Venkateshvaran K, Purushothaman CS. Bioaccumulation and depuration of paralytic shellfish toxin in Perna viridis
and Meretrix meretrix
from Mumbai, India. Indian J Mar Sci 2011;40:8.
Karunasagar I, Gowda HS, Subburaj M, Venugopal MN, Karunasagar I. Outbreak of paralytic shellfish poisoning in Mangalore, west coast of India. Curr Sci 1984;53:247-9.
Watkins SM, Reich A, Fleming LE, Hammond R. Neurotoxic shellfish poisoning. Mar Drugs 2008;6:431-55.
Iwamoto M, Ayers T, Mahon BE, Swerdlow DL. Epidemiology of seafood-associated infections in the United States. Clin Microbiol Rev 2010;23:399-411.
Heisler J, Glibert P, Burkholder J, Anderson D, Cochlan W, Dennison W, et al.
Eutrophication and harmful algal blooms: A Scientific consensus. Harmful Algae 2008;8:3-13.
Gobler CJ, Doherty OM, Hattenrath-Lehmann TK, Griffith AW, Kang Y, Litaker RW, et al.
Ocean warming since 1982 has expanded the niche of toxic algal blooms in the north Atlantic and north pacific oceans. Proc Natl Acad Sci U S A 2017;114:4975-80.
[Figure 1], [Figure 2]