Cholera in India: an analysis of reports, 1997–2006
S Kanungo a, BK Sah b, AL Lopez b, JS Sung b, AM Paisley b, D Sur a, JD Clemens b & G Balakrish Nair a
a. National Institute of Cholera and Enteric Diseases, P-33 – CIT Road Scheme XM, Beliaghata, Kolkata, 700 010, India.
b. International Vaccine Institute, Seoul, Republic of Korea.
Correspondence to G Balakrish Nair (e-mail: firstname.lastname@example.org).
(Submitted: 20 October 2009 – Revised version received: 13 January 2010 – Accepted: 18 January 2010.)
Bulletin of the World Health Organization 2010;88:185-191. doi: 10.2471/BLT.09.073460
Cholera is an acute diarrhoeal illness caused by toxigenic strains of Vibrio cholerae serogroups O1 and O139. Presently, V. cholerae O1 belonging to the El Tor biotype is the most common serogroup in India, while the frequency of serogroup O139 has declined considerably over the past few years. When analysed by 5-year periods, the incidence of cholera and the absolute number of deaths from the disease have increased steadily since the beginning of the millennium. Whereas a cumulative total of 838 315 cases had been notified to the World Health Organization (WHO) for the period 2004 to 2008, 676 651 cases were reported from 2000 to 2004. This represents a 24% increase in the number of cases reported with respect to the previous 5-year period (2000–2004).1 However, the estimated actual burden of cholera is in the vicinity of 3 to 5 million cases and 100 000 to 130 000 deaths per year.2
Cholera is also changing epidemiologically. Multiple antibiotic resistant strains of V. cholerae have emerged,3,4 along with the El Tor variants that produce the cholera toxin of the classical biotype that has spread into Asia and parts of Africa.5–7 The severity of the disease appears to be intensifying,8,9 and recent cholera outbreaks in various places, including Zimbabwe,10 have run a more protracted course.
During a meeting of the WHO Strategic Advisory Group of Experts on immunization that was held in October 2009 in Geneva, Switzerland, cholera control was identified as a priority in areas with endemic cholera, since outbreaks of the disease can disrupt health systems.11 While long-term intervention to improve water and sanitation should be the mainstay of cholera control measures, the group recommended the use of oral cholera vaccines (OCVs) to obtain a short-term effect for an immediate response. Given the availability of two OCVs (one prequalified and the other pending prequalification by WHO) and new data on their efficacy, field effectiveness, feasibility and acceptance in cholera-affected populations, these vaccines should be used in areas where cholera is endemic, particularly in those at risk of outbreaks, in conjunction with other prevention and control strategies.11
Of the two OCVs, the low-cost bivalent inactivated whole-cell OCV known as Shanchol® (Shantha Biotechnics Ltd., Hyderabad, AP, India) is now licensed in India following clinical trials in Viet Nam12 and in the city of Kolkata.13,14 A safe, inexpensive and efficacious cholera vaccine has thus become available in India after almost three decades of non-availability of any cholera vaccine in India. Shanchol® traces its lineage to the original bivalent ORC-Vax® (VaBiotech, Hanoi, Viet Nam) that was licensed in Viet Nam in 1997. In collaboration with the manufacturer, the International Vaccine Institute (IVI) modified the ORC-Vax® by altering the cocktail of immunizing strains, which resulted in an increase in the lypopolysaccharide content.15 Another live oral attenuated cholera vaccine known as VA1.4, created in India and manufactured by Shantha Biotechnics, Ltd., will shortly undergo phase III field trials in Kolkata.16
India, which comprises 28 states and 7 union territories, has a total population of 1.15 billion people. Nearly two-thirds of them live in rural areas, where only 28% of households use piped drinking water and 26% of households have access to good sanitation.17 It is not surprising that cholera continues to be an important public health problem in the country. However, cholera cases are hugely underreported mainly because disease surveillance is limited, laboratory capacity is inadequate, especially at peripheral health-care centres, and authorities are reluctant to acknowledge, for fear of societal repercussion, that there has been a breakdown in sanitation and in the supply of safe water. Yet the above-cited reasons for poor case reporting appear to apply to cholera exclusively. Acute diarrhoeal diseases overall are also underreported, but mainly on account of poor reporting by private health-care services. According to National health profile 2008, 11 231 039 cases of acute diarrhoea were recorded that year, but only 2 680 were cholera cases and only one death was due to cholera.18 These were the national figures conveyed to WHO.
As policymakers have pointed out, to decide the scope of control strategies, including vaccination, it is essential to know the age-specific incidence of cholera.19 Now that a cholera vaccine has been introduced in India, it is important to assess its impact in the country, and that is not possible unless the disease burden can be estimated. With this goal in mind, we searched the biomedical literature to investigate the burden of cholera in India, compare the findings to the “official” figures reported to WHO, and determine how much the burden of cholera is underestimated.
We searched in PubMed with the key words “India” and “cholera” and identified 1134 publications, 500 of which were included in this review. We also searched with the key words “acute gastroenteritis”, “acute watery diarrhoea” (or “diarrhea”) and “India” but found no additional papers. Using the same keywords, we also searched the following databases: Freemedicaljournals, Medexplorer, Medscape and Medhunt. No additional publications were identified. We included publications in which cases were detected from 1997 to 2006, the specific regions in India where the cases occurred were indicated, and the dates of occurrence were specified. To identify the state or union territory where the cholera cases occurred, we included reports of routine surveillance activities as well as outbreaks. A routine surveillance system was defined as any mechanism existing in a hospital or institute for the purpose of using microbiological techniques to identify the pathogens responsible for cases of diarrhoea. Thus, all cholera cases identified during routine surveillance were confirmed by bacterial culture. However, during outbreaks not all cases of diarrhoea were confirmed in the laboratory, and the authors used the WHO case definition: any patient with diarrhoea in an area where culture-confirmed cases of infection with V. cholerae O1 or O139 were identified during the outbreak.20 An outbreak was defined as the occurrence of more cholera cases than expected during a specific period. Since information on “expected” cases was unavailable in most instances, we relied on the authors’ discretion when reporting these outbreaks.
Since outbreaks may occur during routine surveillance, to avoid duplication of cases we tabulated and counted outbreak cases with special attention to the point in time and geographical location of the cases. When we came upon multiple reports of the same outbreak, we drew on data from the source with more detailed information.
By definition, cholera is endemic when the causative organisms reside in the local environment and the occurrence of the disease in humans is not dependent on the importation of cholera from outside. The mechanism by which cholera becomes endemic depends on the environmental reservoir of cholera. Major outbreaks of cholera usually result from an interplay of factors, such as favourable climate conditions and poor sanitation.1
We excluded papers in languages other than English or that dealt with laboratory or environmental issues and focused on molecular mechanisms or other aspects of V. cholerae. We also excluded studies encompassing several years but without a yearly breakdown of the number of cholera cases.
We supplemented our literature search by looking up reports from the Field Epidemiology Training Program of the National Institute of Epidemiology (Chennai, India)21–28 and annual reports published by the National Institute of Cholera and Enteric Diseases (NICED) (Kolkata, India).29 Cholera cases in India are not systematically reported to the NICED. Thus, NICED contains no information on cholera outbreaks that are not reported to the institute. However, NICED is a WHO collaborating centre for research and training on diarrhoeal diseases and is also the National Phage Typing Centre for Cholera in India. It receives, on average, more than 900 strains of V. cholerae O1, O139 and non-O1, non-O139 annually from all parts of the country for phage typing, biotyping and serotyping. Additionally, the NICED is periodically called upon by the Indian Council of Medical Research and the Ministry of Health and Family Welfare of the Government of India to investigate outbreaks of cholera occurring in different parts of the country. The results of phage typing and outbreak investigations are described in the NICED’s annual reports, which are available on the NICED web site beginning in 2005.29 Annual summaries of cholera cases in India reported to WHO are provided by the Central Bureau of Health Intelligence through National health profile, a yearly publication initiated in 2005. The Central Bureau acknowledges that the database is incomplete, the reason being that private medical and health-care institutions do not always report to their respective government health units. Thus, the data come primarily from the directorates of health and family welfare services of the 35 states and union territories.18 The WHO’s annual summaries of cholera case reports30–39 as well as National health profile 2006 data were compared with the results of the literature search.
India reported cholera cases and deaths to WHO regularly from 1997 to 2006 (Table 1). Over the 10-year period, the average number of cases reported annually was 3 631. The case fatality rate showed a somewhat decreasing trend (range: 0.57–0.07). The numbers of cholera cases and deaths in National health profile 2006 were found to be similar to the numbers reported to the WHO.
Table 1. Cholera cases and deaths reported by India to the World Health Organization, 1997–200630–39
Of the 35 states or union territories we identified in our search, 21 reported cholera cases in at least one year from 1997 to 2006. However, the 14 states or union territories that reported no cholera cases were not necessarily free of cholera. They may simply have lacked proper surveillance or the laboratory capacity to identify V. cholerae O1 or O139.
The state of West Bengal reported cholera cases during all of the 10 years reviewed, while the state of Maharashtra and the union territory of Delhi reported cases during nine of those years, Orissa during seven, and Gujarat, Kerala, Tamil Nadu and Punjab during five.
Fig. 1 shows the distribution of cholera cases from routine surveillance and during cholera outbreaks from 1997 to 2006. Routine surveillance was in place in six institutes located in Kolkata, Nagpur, Chandigarh, Kerala, Vellore and Orissa. The states of Assam, Chhattisgarh, Himachal Pradesh, Madhya Pradesh, Tripura and the union territory of Andaman and Nicobar Islands did not report cholera cases on a regular basis but did report outbreaks over the 10-year period. Some states, however, such as West Bengal, Maharashtra and Orissa and in the union territory of Delhi, reported epidemics during multiple years over 1997–2006. Although the causative agent of the outbreaks before 2004 was not identified, Orissa had four outbreaks from 1999–2003. The number of states affected by cholera outbreaks has varied considerably. Only two states reported outbreaks in 1997, while eight reported them in 2004. On average, seven outbreaks occurred annually throughout the country. Since cholera incidence follows a seasonal pattern, cholera outbreaks did not recur in the same geographical area during the same year.
Fig. 1. Distribution of cholera cases and outbreaks in India, 1997–2006
Several states reported outbreaks during multiple years in 1997–2006. Table 2 shows the actual figures obtained through our literature search. The states of Andhra Pradesh, Assam, Haryana, Karnataka, Kerala, Madhya Pradesh, Maharashtra, Orissa and West Bengal and the union territories of Andaman and Nicobar Islands, Delhi and Chandigarh had cholera outbreaks during more than 1 year. During the 10-year period studied, the states having the highest number of reported outbreaks were West Bengal, Orissa, Maharashtra and Kerala, which together accounted for 60% of all reported outbreaks. Of the cholera cases that occurred during outbreaks, 91% were identified in the states or union territories of Orissa, West Bengal, Andaman and Nicobar Islands, Assam and Chhattisgarh. The number of affected individuals ranged from a low of 4 in Himachal Pradesh to a high of 102 778 in Orissa. In the 10-year period, 823 deaths were reported, and the overall case fatality rate was 0.37%.
Table 2. Distribution of identified cholera outbreaks in India in 1997–2006 and population of the states affected by cholera in 2006
Our analysis shows that cholera occurs over a wider geographic area in India than was previously recognized. The annual number of cholera cases reported to WHO by the government was several times lower than the numbers we obtained. The reporting of cholera in India is therefore incomplete and the methods used to keep cholera statistics are inadequate. Although the data are sparse and heterogeneous, notification of cholera cases in India is extremely deficient. When we compared the numbers of cases that occurred during outbreaks alone, according to our search, to the number officially reported to WHO, we found that only one-sixth of the cases were reported. This does not necessarily mean, however, that cholera is not present in those areas. Reporting bias or poor laboratory facilities for diagnosis could well account for the lack of reported cases. Furthermore, the reporting of cholera cases is not standardized at either the national or the international level.
Our study has several limitations. Because we used the NICED’s annual reports to broaden our search, the cholera surveillance performed by the institute resulted in our having a more detailed picture of the epidemiologic distribution of cholera cases in the state of West Bengal, where the NICED is located. Other Indian states may also have experienced outbreaks every year but may have lacked investigators interested in studying and reporting them because they are not novel and therefore unlikely to result in a publication. Clearly, laboratory capacity to isolate the bacterial pathogen was not uniform throughout the country, and this may have influenced the case distribution. Many of the states and union territories did not detect any outbreaks, despite having the same risk factors as those states that did detect outbreaks. For example, in Assam, large numbers of diarrhoeal episodes occurred in 2000 and 2001 but no laboratory investigation was performed, despite the fact that the clinical profile strongly resembled the profile observed during the laboratory-confirmed cholera outbreak of 2002.40
A second limitation is that for some outbreaks,41–43 information was available only for the confirmed cases and not for all clinical cases, which means that even if the outbreak was identified, the number of individuals affected was often underestimated.44,45 Lastly, there were significant delays in the publication and reporting of outbreaks and cholera cases. While most reports were published after two years, some were published three to four years after the initial reporting.46–49 We ended our review in 2006 to increase the chances of capturing all the reports published during the 10-year study period.
The annual numbers of cholera cases and deaths reported to WHO were very conservative, yet they illustrate temporal trends in cholera incidence in India and provide at least some insights. The decreasing trend in the case fatality rates may be the result of the widespread use and effectiveness of oral rehydrating solutions and of improved cholera case management. However, the fact that the number of cholera cases reported to WHO was about the same in 2006 as in 1997 suggests that large segments of the population continue to have little or no access to clean water and sanitation.
A total of 68 outbreaks occurred in 18 states and union territories and the overall number of cases was 222 038, a figure several times higher than the one reported to WHO (37 783) over the same time period. Furthermore, the numbers reported to WHO include both cases from endemic areas as well as from outbreaks, while the non-outbreak-related cases of cholera occurring repeatedly in endemic areas were not among the cases belonging to the 68 outbreaks included in this review. According to data from population-based diarrhoea surveillance in an endemic area of Kolkata, the incidence of cholera was 2.2 cases per 1000 person–years.50 If this data were extrapolated to all endemic areas in the country, the total number of cases would far exceed the numbers quoted above. Our findings confirm that cholera is an under-recognized problem in India.
Our 10-year period analysis indicates that cholera affects areas outside the traditional Gangetic and Brahmaputra deltaic regions of India. An increasing trend was noted in the number of outbreaks, particularly from 2002 to 2005, as well as in the number of individuals affected during each outbreak. That the new El Tor variant strain that produces classical cholera toxin may have caused these increases cannot be ruled out.
As is true for other diseases spread by the faecal-oral route, an adequate supply of potable water, improved sanitation and the promotion of good hygienic practices, especially in developing countries like India, remain the mainstay for preventing both endemic and epidemic cholera. Improved surveillance of the disease will be useful in assessing the cholera burden in the country and in planning interventions appropriately. Acknowledging that cholera is a significant public health threat in south-eastern Asia will allow policy-makers to target control interventions in high-risk areas. Vaccines, as discussed earlier, may be another preventive strategy that is more feasible in cholera-endemic countries. They may be used in addition to other traditional cholera control strategies, along with improved access to safe water and adequate sanitation. ■
We thank Dr Shannon Grahek for her assistance in data compilation.
Competing interests: None declared.
- World Health Organization. Cholera: global surveillance summary, 2008. Wkly Epidemiol Rec 2009; 84: 309-24 pmid: 19645127.
- Zuckerman JN, Rombo L, Fisch A. The true burden and risk of cholera: implications for prevention and control. Lancet 2007; 7: 521-30 doi: 10.1016/S1473-3099(07)70138-X.
- Roychowdhury A, Pan A, Dutta D, Mukhopadhyay AK, Ramamurthy T, Nandy RK, et al., et al. Emergence of tetracycline-resistant Vibrio cholerae O1 serotype Inaba, in Kolkata, India. Jpn J Infect Dis 2008; 61: 128-9 pmid: 18362401.
- Garg P, Chakraborty S, Basu I, Datta S, Rajendran K, Bhattacharya T, et al., et al. Expanding multiple antibiotic resistance among clinical strains of Vibrio cholerae isolated from 1992-7 in Calcutta, India. Epidemiol Infect 2000; 124: 393-9 doi: 10.1017/S0950268899003957 pmid: 10982062.
- Nair GB, Faruque SM, Bhuiyan NA, Kamruzzaman M, Siddique AK, Sack DA. New variants of Vibrio cholerae O1 biotype El Tor with attributes of the classical biotype from hospitalized patients with acute diarrhea in Bangladesh. J Clin Microbiol 2002; 40: 3296-9 doi: 10.1128/JCM.40.9.3296-3299.2002 pmid: 12202569.
- Safa A, Nair GB, Kong RYC. Evolution of new variants of Vibrio cholerae O1. Trends Microbiol 2010; 18: 46-54 doi: 10.1016/j.tim.2009.10.003 pmid: 19942436.
- Ansaruzzaman M, Bhuiyan NA, Nair GB, Sack DA, Lucas M, Deen JL, et al., Mozambique Cholera Vaccine Demonstration Project Coordination Group., et al. Cholera in Mozambique, variant of Vibrio cholerae. Emerg Infect Dis 2004; 10: 2057-9 pmid: 16010751.
- Faruque SM, Tam VC, Chowdhury N, Diraphat P, Dziejman M, Heidelberg JF, et al., et al. Genomic analysis of the Mozambique strain of Vibrio cholerae O1 reveals the origin of El Tor strains carrying classical CTX prophage. Proc Natl Acad Sci USA 2007; 104: 5151-6 doi: 10.1073/pnas.0700365104 pmid: 17360342.
- Siddique AK, Nair GB, Alam M, Sack DA, Huq A, Nizam A, et al., et al. El Tor cholera with severe disease: a new threat to Asia and beyond. Epidemiol Infect 2010; 138: 347-52 doi: 10.1017/S0950268809990550 pmid: 19678971.
- Mintz ED, Guerrant RL. A lion in our village — the unconscionable tragedy of cholera in Africa. N Engl J Med 2009; 360: 1060-3 doi: 10.1056/NEJMp0810559 pmid: 19279337.
- World Health Organization. Oral cholera vaccines. Wkly Epidemiol Rec 2001; 76: 117-24 pmid: 11338983.
- Trach DD, Clemens JD, Ke NT, Thuy HT, Son ND, Canh DG, et al., et al. Field trial of a locally produced, killed, oral cholera vaccine in Vietnam. Lancet 1997; 349: 231-5 doi: 10.1016/S0140-6736(96)06107-7 pmid: 9014909.
- Mahalanabis D, Lopez AL, Sur D, Deen JL, Manna B, Kanungo S, et al., et al. A randomized, placebo-controlled trial of the bivalent killed, whole-cell, oral cholera vaccine in adults and children in a cholera endemic area in Kolkata, India. PLoS One 2008; 3: e2323- doi: 10.1371/journal.pone.0002323 pmid: 18523643.
- Sur D, Lopez AL, Kanungo S, Paisley A, Manna B, Ali M, et al., et al. Efficacy and safety of a modified killed-whole-cell oral cholera vaccine in India: an interim analysis of a cluster-randomised, double-blind, placebo-controlled trial. Lancet 2009; 374: 1694-702 doi: 10.1016/S0140-6736(09)61297-6 pmid: 19819004.
- Anh DD, Canh DG, Lopez AL, Thiem VD, Long PT, Son NH, et al., et al. Safety and immunogenicity of a reformulated Vietnamese bivalent killed, whole-cell, oral cholera vaccine in adults. Vaccine 2007; 25: 1149-55 doi: 10.1016/j.vaccine.2006.09.049 pmid: 17055622.
- Thungapathra M, Sharma C, Gupta N, Ghosh RK, Mukhopadhyay A, Koley H, et al., et al. Construction of a recombinant live oral vaccine from a non-toxigenic strain of Vibrio cholerae O1 serotype Inaba biotype E1 Tor and assessment of its reactogenicity and immunogenicity in the rabbit model. Immunol Lett 1999; 68: 219-27 doi: 10.1016/S0165-2478(99)00076-0 pmid: 10424424.
- Ministry of Health and Family Welfare. States profile. New Delhi: MOHFW, Government of India. Available from: http://www.mohfw.nic.in/NRHM/State_Profile.htm [accessed 16 December 2009].
- Central Bureau of Health Intelligence. National health profile 2008. New Delhi: Ministry of Health and Family Welfare, Government of India. Available from: www.cbhidghs.nic.in [accessed 16 December 2009].
- DeRoeck D, Clemens JD, Nyamete A, Mahoney RT. Policymakers’ views regarding the introduction of new-generation vaccines against typhoid fever, shigellosis and cholera in Asia. Vaccine 2005; 23: 2762-74 doi: 10.1016/j.vaccine.2004.11.044 pmid: 15780724.
- Prevention and control of cholera outbreaks: WHO policy and recommendations. Geneva: World Health Organization, Global Task Force on Cholera Control; 2010. Available from: http://www.who.int/cholera/technical/prevention/control/en/index1.html [accessed 12 June 2009].
- Bhunia R, Ramakrishnan R, Gupte MD. Contaminated pipe-water was a probable cause for cholera outbreak in a semi-urban area in Garulia municipality, West Bengal, India. Presented at: the Fourth TEPHINET Global Conference, 3–7 November 2006, Brasilia, Brazil.
- Das A, Rao TV, Gupte MD. Investigation of an outbreak of cholera in a community – Parbatia, Dhenkanal, Orissa, India, 2003. Presented at: the Third TEPHINET Global Scientific Conference, 8–12 November 2004, Beijing, China.
- Das PK, Biswas A, Ramakrishnan R, Hutin Y, Gupte M. Unprotected wells continue to cause cholera outbreaks in West Bengal, India, 2006. Presented at: the Fourth South-East Asia and Western Pacific Bi-regional TEPHINET Scientific Conference, 26–30 November 2007, Taipei, Taiwan, China.
- Mohan A, Radhakrishnan R. Dhanapal, Manickam P, Gupte MD. Outbreaks of cholera in central Tamil Nadu, 2002. Presented at: the Third TEPHINET Global Scientific Conference, 8– 2 November 2004, Beijing, China.
- Pradhan MM, Pal BB, Narayan S, Rao TV. Outbreak of cholera in Pitazodi village of Orissa, 2002. Presented at: the Joint Annual Conference of the Indian Society for Malaria and other Communicable Diseases and the Indian Association of Epidemiologists, 9-11 November 2002, New Delhi, India.
- Rudra S, Ramakrishnan R, Hutin Y, Gupte M. A cholera outbreak in a village of West Bengal, India, 2006: the danger of using ponds for soiled clothes disposal. Presented at: the Fourth South-East Asia and Western Pacific Bi-regional TEPHINET Scientific Conference, 26–30 November 2007, Taipei, Taiwan, China.
- Saha S, Ramakrishnan R, Gupte MD. Cholera outbreak at Kachua village of Magrahat – I block, South 24 Parganas, West Bengal, India, 2005. Presented at: the Third South-East Asia and Western Pacific Bi-regional TEPHINET Scientific Conference, 9–12 January 2006, Chennai, India.
- Sisodiya R, Hutin Y, Murhekar M, Gupte M. Unsafe water source during an outbreak of cholera in Barwai village, Madhya Pradesh, India, 2006. Presented at: the Fourth South-East Asia and Western Pacific Bi-regional TEPHINET Scientific Conference, 26–30 November 2007, Taipei, Taiwan, China.
- National Institute of Cholera and Enteric Diseases. Annual reports. Beliaghata: Government of India. Available from: http://www.niced.org.in/annual_reports.htm [accessed 10 January 2009].
- World Health Organization. Cholera 2005. Wkly Epidemiol Rec 2006; 81: 297-307 pmid: 16888873.
- World Health Organization. Cholera 2004. Wkly Epidemiol Rec 2005; 80: 261-8 pmid: 16106791.
- World Health Organization. Cholera 2003. Wkly Epidemiol Rec 2004; 79: 281-8 pmid: 15315149.
- World Health Organization. Cholera 2002. Wkly Epidemiol Rec 2003; 78: 269-76 pmid: 15581214.
- World Health Organization. Cholera 2001. Wkly Epidemiol Rec 2002; 77: 257-64 pmid: 12189690.
- World Health Organization. Cholera 2000. Wkly Epidemiol Rec 2001; 76: 233-40 pmid: 11505731.
- World Health Organization. Cholera 1999. Wkly Epidemiol Rec 2000; 75: 249-56 pmid: 10953668.
- World Health Organization. Cholera 1998. Wkly Epidemiol Rec 1999; 74: 257-9 pmid: 10453697.
- World Health Organization. Cholera 1997. Wkly Epidemiol Rec 1998; 73: 201-8 pmid: 9677852.
- World Health Organization. Cholera 1996. Wkly Epidemiol Rec 1997; 72: 227-35.
- Phukan AC, Borah PK, Biswas D, Mahanta J. A cholera epidemic in a rural area of northeast India. Trans R Soc Trop Med Hyg 2004; 98: 563-6 doi: 10.1016/j.trstmh.2004.01.002 pmid: 15251406.
- Batra P, Saha A, Vilhekar KY, Chaturvedi P, Mendiratta DK. Vibrio cholerae O1 Ogawa (Eltor) diarrhea at Sevagram. Indian J Pediatr 2006; 73: 543- doi: 10.1007/BF02759907 pmid: 16816524.
- Dutta B, Ghosh R, Sharma NC, Pazhani GP, Taneja N, Raychowdhuri A, et al., et al. Spread of cholera with newer clones of Vibrio cholerae O1 Eltor, serotype Inaba, in India. J Clin Microbiol 2006; 9: 3391-3 doi: 10.1128/JCM.00632-06.
- Sinha S, Chakraborty R, De K, Khan A, Datta S, Ramamurthy T, et al., et al. Escalating association of Vibrio cholerae O139 with cholera outbreaks in India. J Clin Microbiol 2002; 7: 2635-7 doi: 10.1128/JCM.40.7.2635-2637.2002.
- Geeta MG, Krishna Kumar P. Cholera in Kerala. Indian Pediatr 2005; 42: 89- pmid: 15695877.
- Gupta N, Dewan S, Saini S. Resurgence of Vibrio cholerae O139 in Rohtak. Indian J Med Res 2005; 121: 128-30 pmid: 15756047.
- Batra P, Saha A, Vilhekar KY, Chaturvedi P, Mendiratta DK. Vibrio cholerae O1 Ogawa (Eltor) diarrhea at Sevagram. Indian J Pediatr 2006; 73: 543- doi: 10.1007/BF02759907 pmid: 16816524.
- Das A, Manickam P, Hutin Y, Pattanaik B, Pal BB, Chhotray GP, et al., et al. Two sequential outbreaks in two villages illustrate the various modes of transmission of cholera. Epidemiol Infect 2009; 137: 906-12 doi: 10.1017/S0950268808001611 pmid: 19171080.
- Sharma NC, Mandal PK, Dhillon R, Jain M. Changing profile of Vibrio cholerae O1, O139 in Delhi and its periphery (2003-2005). Indian J Med Res 2007; 125: 633-40 pmid: 17642498.
- Sur D, Datta S, Sarkar BL, Manna B, Bhattacharya MK, Datta KK, et al., et al. Occurrence, significance and molecular epidemiology of cholera outbreaks in West Bengal. Indian J Med Res 2007; 125: 772-6 pmid: 17704555.
- Sur D, Deen J, Manna B, Niyogi SK, Deb A, Kanungo S, et al., et al. The burden of cholera in the slums of Kolkata, India: from a prospective, community-based study. Arch Dis Child 2005; 90: 1175-81 doi: 10.1136/adc.2004.071316 pmid: 15964861.