Am. J. Trop. Med. Hyg., 71(6), 2004, pp. 822-827
Copyright © 2004 by The American Society of Tropical Medicine and Hygiene
A CHOLERA EPIDEMIC AMONG THE NICOBARESE TRIBE OF NANCOWRY, ANDAMAN, AND NICOBAR, INDIA
ATTAYOOR P. SUGUNAN,
ASIT R. GHOSH,
SUBARNA ROY,
MOHAN D. GUPTE, AND
SUBHASH C. SEHGAL
Regional Medical Research Centre (Indian Council of Medical Research), Port Blair, Andaman and Nicobar Islands, India; National Institute of Epidemiology (Indian Council of Medical Research), Chetput, Chennai, India
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ABSTRACT
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Cholera has not been reported from the Andaman and Nicobar Islands in India. In October 2002, an outbreak of diarrhea occurred among the Nicobarese tribe of the Nancowry group of islands. The outbreak affected 16 of the 45 inhabited villages of three islands with an attack rate of 12.8% and a case fatality ratio of 1.3%. Vibrio cholerae O1 El Tor was isolated from 18 of the 67 patients tested. A study conducted in one of the villages indicated that the outbreak was started there by a person who traveled to a nearby village where an outbreak was occurring. No specific water source could be identified as the source of infection because persons consuming water from all wells were affected. Water samples from 55 sources were tested and 38 of them were contaminated with Escherichia coli. The possible sources of V. cholerae are effluents from ships or poachers from neighboring countries where cholera is endemic.
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INTRODUCTION
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Cholera is one of the few bacterial diseases capable of pandemic spread.1 It is caused by Vibrio cholerae O1, and since 1992, by V. cholerae O139. Seven distinct pandemics of cholera have been recorded since 1817.2 An eighth pandemic was suspected when epidemic cholera, which spread in Chennai and other parts of India and Bangladesh, was found to be due to a new serotype, O139.2,3 The first six pandemics originated from the Ganges Delta of India. The sixth and probably the fifth were caused by the classic V. cholerae O1.2 The seventh pandemic caused by V. cholerae O1 El Tor biotype originated on the island of Sulawesi in Indonesia and moved to affect the Indian subcontinent and later other countries, including Latin America. The pandemic potential of cholera is exemplified by the rapid spread of it in Latin America once reintroduced there in 1991 after a century of absence.4 Between 1991 and 1994, more than one million cases were recorded in Latin American countries.5 The explosive outbreak among Rwandan refugees in Zaire in July 1994, which affected 70,000 people and killed 12,000, is another example of its potential for rapid spread,6,7 particularly among marginalized or internally displaced populations.
The seventh cholera pandemic spread from Sulawesi to other Indonesian islands and by the end of 1962 it had spread to the entire Southeast Asian archipelago. From 1963 to 1969 the pandemic spread to the Asian mainland and affected Malaysia, Thailand, Burma, Cambodia, Vietnam, India, Bangladesh, and Pakistan.2 The Andaman and Nicobar Islands, which lie close to the route of this spread, were not affected. In 1992, V. cholerae serotype O139 caused large epidemics in India and Bangladesh.3 Although this epidemic spread to most parts of India, the Andaman and Nicobar Islands remained unaffected. Vibrio parahaemolyticus is frequently isolated from seawater and seafood samples in the islands.8 However, no case of diarrheal disease due to V. cholerae has been detected in a hospital-based surveillance started in 1994 in South Andaman.9
In October–November 2002, an outbreak of severe watery diarrhea appeared on three islands in the Nancowry group of islands, which are part of the Nicobar District of the Andaman and Nicobar Islands in India. The outbreak spread to many villages on these three islands and affected a large number of tribal people. In this report, we present the epidemiologic features of this first recorded outbreak of cholera in the Andaman and Nicobar Islands.
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MATERIALS AND METHODS
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Study area.
The Andaman and Nicobar Islands are an archipelago of 527 islands, islets, reefs, and rocks in the Bay of Bengal. The total population, as per the 2001 census, is approximately 350,000. About 9% of the population is constituted by tribes. The largest tribal group is the Nicobarese, who inhabit the islands in the Nicobar District. The major inhabited islands in the Nicobar District include Car Nicobar, the Nancowry group of islands, and Great Nicobar. Except for Great Nicobar, all the other islands in the Nicobar District are inhabited almost exclusively by Nicobarese. The Nancowry group, lying in between Car Nicobar in the north and Great Nicobar in south, comprises several small islands. The main town in the Nancowry group of islands is Kamorta, which is in the Kamorta Islands. The community health center (CHC) at Kamorta, the primary health center on Katchal Island, and several sub-centers provide primary health care to the tribal population.
Case definition.
A person reporting with watery diarrhea on or after October 5, 2002 was considered a suspected case of cholera. A suspected case whose stool samples/rectal swab yielded cultures of V. cholerae was considered a confirmed case of cholera.
Data sources.
Patient records kept at the CHC in Kamorta were used as source of information about patients. A list of residents of the Nancowry Islands maintained by the Andaman and Nicobar Administration was used as the source of information about the population at risk. Patients admitted to the CHC after the beginning of the investigations and their relatives were interviewed. A house-to-house survey was conducted in one village, where the outbreak was continuing. Information about illness and water sources were collected from the residents of the village.
Clinical specimens and laboratory tests.
Stool sample were collected from all the patients admitted to the CHC in Kamorta after the beginning of the investigations. When whole stool samples could not be obtained, rectal swabs were collected. Samples were collected from different water sources in the villages visited. Samples of seawater near the shore were also collected.
Stool samples/rectal swabs were processed for bacterial enteric pathogens following standard procedures at the temporary laboratory set up at the CHC in Kamorta. Isolated bacteria were serotyped using commercially available antisera. Samples were also sent to National Institute of Cholera and Enteric Diseases in Kolkata for confirmation.
Initial control measures.
All drinking water sources in all villages in Kamorta, Nancowry, and the Trinket Islands were super-chlorinated. Public awareness campaigns were initiated based at sub-centers located in various villages. The sub-center staffs were instructed to refer all cases of diarrhea to the Kamorta CHC. Intravenous fluids, oral rehydration solution, and essential drugs were stocked in the sub-centers. Pharmacists and auxiliary nurse midwives at the sub-centers were instructed to start early rehydration in all cases of diarrheal diseases. They were also instructed to provide intravenous fluids while referring cases to the CHC.
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RESULTS
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The first case and death occurred on October 5, 2002. The Directorate of Health Services of the Andaman and Nicobar Administration in Port Blair was notified about the possibility of an outbreak by October 10. Investigations were initiated in first week of November. Until October 2002, the usual number of cases of severe watery diarrhea reporting to the Kamorta CHC was approximately 10 per month. In October 2002, this increased to more than 250, which is clearly in excess of the number of cases expected.
The outbreak started at Tapong village on Nancowry Island on October 5, 2002. The index case was an 18-year-old woman. During the next few days, several persons in Tapong village were affected. By this time, awareness about early hospitalization was spread among the people and patients were reporting early. Thus, there were no additional fatalities in Tapong village. Eight cases occurred during the period October 5–7. After a lull of three days, an additional four cases occurred on October 11 and 12. This probably indicates secondary cases.
Figure 1
shows the dates of onset of outbreak in different villages in the three islands (Nancowry, Kamorta, and Trinket) The outbreak started at Tapong on October 5. Within the next few days, it spread to the villages on the northern part of Nancowry Island and then to Kamorta and other villages on the southern edge of Kamorta Island. The outbreak then spread northward on both the eastern and western costs of Kamorta Island. During this spread, villages in Trinket Island lying east of Kamorta were also affected. There were a few exceptions to the general pattern of spread. For example, Bunder Khadi village, which lies further north than the villages of Ramzo, Payuha, Munak, and Changuwa, was affected earlier. Apparently Kamorta was affected soon after the outbreak appeared in Tapong on October 5. All patients from Tapong were treated at Kamorta and it is possible that these patients were the source of infection in Kamorta. None of the villages south of Tapong, where the outbreak started, was affected.
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FIGURE 1. Map of the Nancowry group of islands of India showing the dates on which the outbreak started in each village during the cholera outbreak in October–November 2002.
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The distribution of cases that occurred on Nancowry, Kamorta, and Trinket islands by date of reporting is shown in Figure 2. It shows multiple peaks indicating the occurrence of secondary cases. The overall trend showed an increase in the number of cases reaching a peak by first week of November and then a decrease. The epidemic curve shown in Figure 2 is a combination of multiple epidemic curves in different villages on the three islands. Each of these epidemic curves showed multiple peaks. Figure 3 shows the distribution of the cases in some of the villages. In some villages, the outbreak reappeared after being absent for many days. In Tapong, the initial outbreak ended on October 12, but reappeared on November 2 after a gap of 20 days. In Dering village, the outbreak started on October 14 and continued up to October 27. After a lull of five days, it started again on November 3. Four cases occurred between November 3 and 5. Another case occurred on November 8. After a lull of four days, another six cases occurred on November 13 and 14.
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FIGURE 2. Distribution of cases based on date of reporting at the communty health center (CHC) in Kamorta during the cholera outbreak in the Nancowry group of islands of India, October–November 2002.
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FIGURE 3. Distribution diarrhea cases in different villages and dates of reporting during the cholera outbreak in the Nancowry group of islands of India, October–November 2002.
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There are 45 inhabited villages on the three islands and 16 of them were affected. As per the residents list maintained by the Andaman and Nicobar Administration, there were 3,806 persons residing on the three islands. From October 5 to November 20, 468 cases were reported to the CHC in Kamorta, giving an attack rate of 12.3%. Attack rates ranged between 0.9% and 82.2% (Table 1). All age groups were affected. The attack rate was highest among infants and those 20–24 years old. Figure 4 shows the age-specific attack rates. The attack rate was 11.8% among males and 13.7% among females. This difference was not statistically significant (
2 = 2.56, P = 0.109). There were three deaths in the hospital. An additional three persons, including the index cases, died in their homes. Thus, the case fatality ratio (CFR) was 1.3%. All deaths occurred among adults.
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TABLE 1 Attack rate in different villages during the cholera outbreak in the Nancowry group of islands, October–November 2002
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FIGURE 4. Age group-specific attack rates during the cholera outbreak in the Nancowry group of islands of India, October– November 2002.
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Stool samples/rectal swabs were collected from 67 patients. Vibrio cholerae was isolated from 21 cases, 18 of which were O1 Ogawa El Tor biotype and three were non-O1 non-O139. V. cholerae was isolated from patients from 11 of the 16 affected villages and from all the three islands. Isolates of V. cholerae were recovered from stool samples of patients in all age groups except in those 1–4 and 10–14 years old. Age group samples processed, isolates. and positivity rates are shown in Table 2. Water samples from 53 drinking water sources were tested for contamination with Escherichia coli and 38 (69.1%) were found to be contaminated. Vibrio cholerae was not isolated from any of the water samples.
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TABLE 2 Age group samples, isolates, and positivity rate during the cholera outbreak in the Nancowry group of islands, October–November 2002
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An investigation regarding use of different water sources as the source of infection was conducted in Dering village. This village has 17 households located on the beach. There are 11 wells out of which seven are used for drinking water purposes. The remaining four wells are used exclusively for washing and bathing. Each well is used by certain families. There are seven groups of households with different well usage patterns. The first case occurred on October 20 in household no. 1. The patient had traveled to another village where the outbreak was ongoing. During his return journey, he had abdominal discomfort and vomiting. The day he arrived in Dering he had diarrhea. During the next eight days, nine households using different wells were affected. Three other households were affected on November 11, 12, and 17, respectively. Attack rates among these groups and households are shown in Table 3. Households in all the groups were affected. The attack rates among the groups of households ranged from 14.3% to 37.5%. Attack rates in individual households ranged from 14.3% to 60%.
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TABLE 3 Well usage and attack rates of all households at Dering during the cholera outbreak, October–November 2002
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DISCUSSION
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The epidemic of severe watery diarrhea that occurred in the Nancowry group of islands of India was due to V. cholerae O1 Ogawa El Tor biotype, the strain of V. cholerae responsible for the seventh pandemic. The seventh pandemic began 40 years ago in the Indonesian archipelago, which is located close to the Nicobar group of islands. During the past 40 years when the pandemic spread to all of the southeast Asian archipelago and then to the Asian mainland,2 the scarcely populated Andaman and Nicobar Islands remained free of the disease.
The present epidemic affected one of every eight persons in the tribal community inhabiting the three islands. The number of individuals with unapparent infection for every clinical case of cholera gravis was more for the El Tor biotype cholera than for the classic biotype cholera.10 Therefore, a significant proportion of the tribal population might have become infected during the outbreak. The attack rate was as high as 82% in some villages.
Age group-specific attack rates showed two peaks. The peak corresponding to the 0–1-year-old age group was perhaps due to the practice of early weaning among the Nicobarese since person-to-person contact spread virtually never occurs for cholera.1 The rest of the age group-specific attack rate trend with a peak attack rate among young adults is typical of an infectious disease that is newly introduced into a community. In spite of the aberrant peak corresponding to 0–1-year-old age group, the age group-specific attack pattern can be considered as an indication that the infection was new to the community. It has been reported that women of childbearing age exhibit a high incidence of cholera during these outbreaks.11 Although the attack rate among women 15–45 years old was slightly higher than in the remaining population (13.7% versus 11.8%), the difference was not statistically significant.
The epidemic curve showed multiple peaks. The height of these peaks increased until the early part of the second week of November and then decreased rapidly. The repeated peaks represent spread of the outbreak to new areas. Even in individual villages, the outbreak showed multiple peaks, perhaps due to secondary cases. In some of the villages, the outbreak apparently reappeared after a gap greater than the incubation period. This could be either because of asymptomatic carriers in the hamlet contaminated water/food sources or because of the epidemic spreading to the hamlet a second time from other hamlets where the epidemic was continuing. The spread of the outbreak had a general northerly direction and none of the villages south of Tapong was affected. There is a possibility of seawater acting as a vehicle of transmission and the changes in water currents playing a role in the spread of the epidemic. It has been shown that V. cholerae El Tor can survive in untreated seawater for up to a week.12
Although the attack rate was high, the CFR was only 1.3%, which is similar to the average CFR reported for the entire world in 1993.13 Early rehydration at the sub-centers and use of intravenous fluids while transferring patients from the sub-centers to the CHC could have helped in reducing deaths. When use of health care by people is poor and rehydration at primary health care facilities is inadequate, case fatality a during cholera outbreak could be very high.14 Access of the population of most of the affected hamlets in the Nancowry Islands to the CHC in Kamorta, which is the only hospital in the areas with a doctor and facilities for inpatient treatment, was poor. In such situations, peripheral health units manned by paramedics can play an important role in reducing morbidity and mortality. During an outbreak of cholera in rural Bangladesh, intervention by a paramedical staff at a makeshift hospital reduced the mortality substantially.15
The tribal community in the Nancowry Islands lives in small hamlets along the shoreline. These hamlets are not connected to one another by roads, and in many of these the only access to transportation is by sea. However, the epidemic spread rapidly from Tapong, where it first appeared, to many hamlets in the three islands. The ability of the El Tor biotype of V. cholerae to spread widely in a short period has been documented in mainland India.16 The experience at Dering village, where the index case was a person who traveled to another village where the outbreak was continuing, indicates that the movement of people between villages had played a role in the spread of the outbreak. No single water source could be identified as the source of infection. Although the wells used for drinking water have concrete walls, parapet, and platforms around them, these were very shallow and there is a possibility of seepage from the surrounding stagnant water. A few latrines have been constructed at the hamlets, but most of the people defecate in the open.
No conclusive evidence on how the organism gained access to this hitherto unaffected population could be obtained. Several possibilities have been proposed. One possibility is that the organism was introduced to the marine environment as a result of discharge of effluents from ships that sail between Andaman and Nicobar and mainland India, as well as between the islands of the territory. Even ballast water carried by large ships may act as a vehicle of transmission of cholera across long distances.17 The large ships that sail often between Port Blair (the main town in the Andaman and Nicobar Islands) and Kolkata occasionally sail from Port Blair to the Nicobar group of islands. At Nancowry, these large ships cannot enter the port and thus stay anchored in the sea. This anchoring point is near Tapong village where the outbreak first appeared. The other possibilities include V. cholerae carriers among poachers from neighboring Southeast Asian countries, who often mingle with the local tribal population.
It appears that the seventh pandemic of cholera, more than 40 years after it originated on a nearby island, has now spread to the Nancowry group of islands. These islands have an estuarine environment and V. cholera are free-living bacterial flora in estuarine areas.2 Although environmental isolates of V. cholerae O1 outside the epidemic areas are almost always negative for cholera toxin (CT),2 it has been shown that CT-producing V. cholerae O1 can persist in the environment.18,19 The outbreak of cholera on the Nancowry Islands may have ended because the pool of susceptible people was depleted when a major proportion of the population got acquired subclinical or symptomatic infections. It is possible that the hardy V. cholera El Tor20 may persist in this estuarine environmental niche and may cause repeated outbreaks. Strengthened surveillance, preferably with an environmental surveillance component,21 is an immediate need to protect the tribal community from recurrent outbreaks.
Received February 19, 2004.
Accepted for publication May 29, 2004.
Acknowledgments: We gratefully acknowledge the help and cooperation of the Nicobarese tribal chiefs of the various villages of Nancowry, Dr. Sher Singh (Chief Medical Officer, Community Health Centre, Kamorta), Justin Pereira (Assistant Commissioner, Nancowry), and the paramedical staff of the CHC of Kamorta and sub-centres at Tapong and Derring villages. We are also grateful to the Director and scientists of National Institute of Cholera and Enteric Diseases in Kolkata for their help in laboratory confirmation of diagnosis, and Professor K. Ramachandran (Consultant to the Field Epidemiology Training Programme of the National Institute of Epidemiology [NIE]) and Dr. P. Manickam (Research Officer at the NIE) for useful suggestions in the preparation of this manuscript. The American Committee on Clinical Tropical Medicine and Travelers’ Health (ACCTMTH) assisted with publication expenses.
Authors’ addresses: Attayoor P. Sugunan, Asit R. Ghosh, and Subarna Roy, Regional Medical Research Centre (Indian Council of Medical Research), Post Bag No. 13, Port Blair 744 101, Andaman and Nicobar Islands, India, Telephone: 91-3192-251158, Fax: 91-3192-251163, E-mails: pblsugunan{at}sancharnet.in and pblicmr{at}sancharnet.in. Mohan D. Gupte, National Institute of Epidemiology (Indian Council of Medical Research), Mayor V. Ramanathan Road, Chetput, Chennai, India, Telephone: 91-44-2836-1980, E-mail: nieicmr{at}vsnl.com. Subhash C. Sehgal, Regional Medical Research Centre (Indian Council of Medical Research), Post Bag No. 13, Port Blair 744 101, Andaman and Nicobar Islands, India, Telephone: 91-3192-251043, Fax: 91-3192-251163, E-mail: pblicmr{at}sancharnet.in.
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TOP
ABSTRACT
INTRODUCTION
