A Re-Look at Cholera Pandemics from Early Times to Now in the Current Era of Epidemiology
Thandavarayan Ramamurthy and Amit Ghosh
ICMR-National Institute of Cholera and Enteric Diseases
P-33 C.I.T. Road, Scheme-XM, Beliaghata Kolkata 700010, West Bengal, India
Cholera affects about three million people annually and kills several thousands. Since 1817 seven cholera pandemics have been described. While the nature of the strains responsible for the first four pandemics are not known, the fifth and sixth pandemics are associated with Vibrio cholerae O1 classical biotype. In the 1960s, V. cholerae El Tor replaced classical strains worldwide, ushering in the seventh pandemic. El Tor cholera is typified with less severe diarrhea, a lower case fatality rate and a higher percentage of asymptomatic cases. Historically, the Indian subcontinent was thought to be the homeland where cholera originated and has been implicated in spreading of the disease. Cholera broke out in Africa and now seems to be continuous and recurrent, leading to high morbidity and mortality in some countries. Current conflicts in the Middle East have been associated with the breakdown of healthcare systems and the emergence of cholera there in a big way. Several discoveries in the past two centuries helped us to understand and manage the disease. Some of the greatest inventions such as rehydration therapy have saved the lives of countless people afflicted with cholera. Whole genome sequencing of V. cholerae and the modern molecular epidemiology of cholera have led to advancements in understanding of the disease and also how the organism has persisted and re-emerged in new areas during the seventh pandemic. Currently, water, sanitation, and hygiene along with the new generation oral cholera vaccines are considered as important interventions and beneficial public health tools in cholera endemic countries and in areas at risk for outbreaks. This review highlights the pandemics that lead to important discoveries and also the new molecular approach in understanding the epidemiology of cholera.
-  J. B. Kaper, J. G. Morris Jr., and M. M. Levine, “Cholera,” Clinical Microbiology Reviews, Vol.8, No.1, pp. 48-86, doi: 10.1128/CMR.8.1.48-86.1995, 1995.
-  S. Yamasaki, S. Garg, G. B. Nair, and Y. Takeda, “Distribution of Vibrio cholerae O1 antigen biosynthesis genes among O139 and other Non-O1 serogroups of Vibrio cholerae,” FEMS Microbiology Letters, Vol.179, No.1, pp. 115-121, doi: 10.1111/j.1574-6968.1999.tb08716.x, 1999.
-  R. Pollitzer, “History of the Disease,” R. Pollitzer (Ed.), “Cholera,” World Health Organization, pp. 11-50. 1959.
-  D. Barua, “History of Cholera,” D. Barua and W. B. Greenoug III (Eds.), “Cholera,” pp. 1-36, Plenum Medical Co., 1992.
-  P. A. Blake, “Historical Perspectives on Pandemic Cholera,” I. K. Wachsmuth, P. A. Blake, and O. Olsvik (Eds.), “Vibrio cholerae and Cholera, Molecular to Global Perspectives,” ASM Press, pp. 357-370, 1994.
-  D. A. Sack, R. B. Sack, G. B. Nair, and A. K. Siddique, “Cholera,” The Lancet, Vol.363, No.9404, pp. 223-233, doi: 10.1016/s0140-6736(03)15328-7, 2004.
-  J. Sepúlveda, J. L. Valdespino, and L. García-García, “Cholera in Mexico: The Paradoxical Benefits of the Last Pandemic,” Int. J. of Infectious Diseases, Vol.10, No.1, pp. 4-13, doi: 10.1016/j.ijid.2005.05.005, 2006.
-  S. Y. Choi et al., “Phylogenetic diversity of Vibrio cholerae associated with endemic cholera in Mexico from 1991 to 2008,” mBio, Vol.7, No.2, e02160, doi: 10.1128/mBio.02160-15, 2016.
-  A. R. Samadi et al., “Classical Vibrio cholerae Biotype Displaces El Tor in Bangladesh,” The Lancet, Vol.321, No.8328, pp. 805-807, doi: 10.1016/s0140-6736(83)91860-3, 1983.
-  S. M. Faruque, “Clonal Relationships Among Classical Vibrio cholerae O1 Strains Isolated between 1961 and 1992 in Bangladesh,” J. of Clinical Microbiology, Vol.31, No.9, pp. 2513-2516, doi: 10.1128/JCM.31.9.2513-2516, 1993.
-  M. Alam et al., “Cholera between 1991 and 1997 in Mexico was associated with infection by classical, El Tor, and El Tor variants of Vibrio cholerae,” J. of Clinical Microbiology, Vol.48, No.10, pp. 3666-3674, doi: 10.1128/JCM.00866-10, 2010.
-  T. Ramamurthy, S. Yamasaki, Y. Takeda, and G. B. Nair, “Vibrio cholerae O139 Bengal: Odyssey of a Fortuitous Variant,” Microbes Infection, Vol.5, No.4, pp. 329-344, doi: 10.1016/s1286-4579(03)00035-2, 2003.
-  S. Rebaudet et al., “Epidemiological and Molecular Forensics of Cholera Recurrence in Haiti,” Scientific Reports, Vol.9, No.1, pp. 1164. doi: 10.1038/s41598-018-37706-0, 2019.
-  H. M. Al-Mekhlafi, “Yemen in a Time of Cholera: Current Situation and Challenges,” The American J. of Tropical Medicine and Hygiene, Vol.98, No.6, pp. 1558-1562, doi: 10.4269/ajtmh.17-0811, 2018.
-  D. Lippi and E. Gotuzzo, “The Greatest Steps Towards the Discovery of Vibrio cholerae,” Clinical Microbiology and Infection, Vol.20, No.3, pp. 191-195, doi: 10.1111/1469-0691.12390, 2014.
-  J. Snow, “Cholera and the Water Supply in the South Districts of London in 1854,” J. of Public Health, and Sanitary Review, Vol.2, No.7, pp. 239-257, 1856.
-  N. Howard-Jones, “Robert Koch and the Cholera Vibrio: A Centenary,” British Medical J., Vol.288, No.6414, pp. 379-381, doi: 10.1136/bmj.288.6414.379, 1984.
-  J. B. Moon, “Sir William Brooke O’Shaughnessy – the Foundations of Fluid Therapy and the Indian Telegraph Service,” The New England J. of Medicine, Vol.276, No.5, pp. 283-284, doi: 10.1056/NEJM196702022760509, 1967.
-  W. B. O’Shaughnessy, “Proposal for a New Method of Treating the Blue Epidemic Cholera by the Injection of Highly-Oxygenised Salts into the Venous System,” The Lancet, Vol.17, No.432, pp. 366-371, 1831.
-  W. B. O’Shaughnessy, “Experiments on the Blood in Cholera,” The Lancet, Vol.17, No.435, pp. 490, 1831.
-  T. A. Latta, “Malignant Cholera,” The Lancet, Vol.18, No.457, pp. 274-280, 1832.
-  D. Mahalanabis, J. B. Brayton, A. Mondal, and N. F. Pierce, “The Use of Ringer’s Lactate in the Treatment of Children with Cholera and Acute Noncholera Diarrhoea,” Bulletin of the World Health Organization, Vol.46, No.3, pp. 311-319, 1972.
-  G. H. Bornside, “Jaime Ferran and Preventive Inoculation Against Cholera,” Bulletin of the History of Medicine, Vol.55, No.4, pp. 516-532, 1981.
-  B. J. Hawgood, “Waldemar Mordecai Haffkine, CIE (1860-1930): Prophylactic Vaccination Against Cholera and Bubonic Plague in British India,” J. of Medical Biography, Vol.15, No.1, pp. 9-19, doi: 10.1258/j.jmb.2007.05-59, 2007.
-  A. K. Siddique and R. Cash, “Cholera Outbreaks in the Classical Biotype Era,” Current Topics in Microbiology and Immunology, Vol.379, pp. 1-16, doi: 10.1007/82_2013_361, 2014.
-  K. Nobechi, “Contributions to the Knowledge of Vibrio cholerae. III. Immunological Studies Upon the Types of Vibrio cholerae,” Scientific Reports, Government Institute for Infectious Diseases, Vol.2, pp. 1-87, 1923.
-  A. D. Gardner and K. V. Venkatraman, “The antigens of the Cholera Group of Vibrios,” The J. of Hygiene, Vol.35, No.2, pp. 262-282, doi: 10.1017/s0022172400032265, 1935.
-  S. Mukerjee, “Bacteriophage Typing of Cholera,” Bulletin of the World Health Organization, Vol.28, No.3, pp. 337-345, 1963.
-  H. A. Reimann et al., “Asiatic Cholera; Clinical Study and Experimental Therapy with Streptomycin,” The American J. of Tropical Medicine and Hygiene, Vol.26, No.5, pp. 631-647, 1946.
-  L. W. Chu and C. H. Huang, “Effect of Sulfadiazine on Cholera,” The American J. of Tropical Medicine and Hygiene, Vols.a1-26, No.6, pp. 821-823, doi: 10.4269/ajtmh.1946.s1-26.821, 1946.
-  H. N. Chatterjee, “Control of Vomiting in Cholera and Oral Replacement of Fluid,” The Lancet. Vol.262, No.6795, p. 1063, doi: 10.1016/s0140-6736(53)90668-0, 1953.
-  S. J. Savarino, “A Legacy in 20th-Century Medicine: Robert Allan Phillips and the Taming of Cholera,” Clinical Infectious Diseases, Vol.35, No.6, pp. 713-720. doi: 10.1086/342195, 2002.
-  S. N. De, “Enterotoxicity of Bacteria-Free Culture-Filtrate of Vibrio cholerae,” Nature, Vol.183, No.4674, pp. 1533-1534, doi: 10.1038/1831533a0, 1959.
-  N. K. Dutta, M. V. Panse, and D. R. Kulkarni, “Role of Cholera a Toxin in Experimental Cholera,” J. of Bacteriology, Vol.78, No.4, pp. 594-595, doi: 10.1128/JB.78.4.594-595, 1959.
-  R. A. Finkelstein and J. J. LoSpalluto, “Pathogenesis of Experimental Cholera: Preparation and Isolation of Choleragen and Choleragenoid,” J. of Experimental Medicine, Vol.130, No.1, pp. 185-202, doi: 10.1084/jem.130.1.185, 1969.
-  R. A. Cash et al., “Response of Man to Infection with Vibrio cholerae. I. Clinical, Serologic, and Bacteriologic Responses to a Known Inoculum,” The J. of Infectious Disease, Vol.129, No.1, pp. 45-52, doi: 10.1093/infdis/129.1.45, 1974.
-  M. M. Levine, J. B. Kaper, R. E. Black, and M. L. Clements, “New knowledge on Pathogenesis of Bacterial Enteric Infections as Applied to Vaccine Development,” Microbiology Reviews, Vol.47, No.4, pp. 510-550, 1983.
-  H. S. Xu et al., “Survival and Viability of Nonculturable Escherichia coli and Vibrio cholerae in the Estuarine and Marine Environment,” Microbial Ecology, Vol.8, No.4, pp. 313-323, doi: 10.1007/BF02010671, 1982.
-  M. K. Waldor and J. J. Mekalanos, “Lysogenic Conversion by a Filamentous Phage Encoding Cholera Toxin,” Science, Vol.272, No.5270, pp. 1910-1904. doi: 10.1126/science.272.5270.1910, 1996.
-  M. Trucksis, J. Michalski, Y. K. Deng, and J. B. Kaper, “The Vibrio cholerae Genome Contains Two Unique Circular Chromosomes,” Proc. of the National Academy of Sciences of the United States of America, Vol.95, No.24, pp. 14464-14469, doi: 10.1073/pnas.95.24.14464, 1988.
-  J. F. Heidelberg et al., “DNA Sequence of both Chromosomes of the Cholera Pathogen Vibrio cholerae,” Nature, Vol.406, No.6795, pp. 477-483, doi: 10.1038/35020000, 2000.
-  A. M. Devault et al., “Second-pandemic strain of Vibrio cholerae from the Philadelphia Cholera Outbreak of 1849,” The New England J. of Medicine, Vol.370, No.4, pp. 334-340, doi: 10.1056/NEJMoa1308663, 2014.
-  J. Chun et al., “Comparative Genomics Reveals Mechanism for Short-Term and Long-Term Clonal Transitions in Pandemic Vibrio cholerae,” Proc. of the National Academy of Sciences of the United States of America, Vol.106, No.36, pp. 15442-15447, doi: 10.1073/pnas.0907787106, 2009.
-  A. Safa, G. B. Nair, and R. Y. C. Kong, “Evolution of New Variants of Vibrio cholerae O1,” Trends in Microbiology, Vol.18, No.1, pp. 46-54, doi: 10.1016/j.tim.2009.10.003, 2010.
-  O. C. Stine and J. G. Morris Jr., “Circulation and Transmission of Clones of Vibrio cholerae During Cholera Outbreaks,” Current Topics in Microbiology and Immunology, Vol.379, pp. 181-193, doi: 10.1007/82_2013_360, 2014.
-  G. B. Nair et al., “Cholera Due to Altered El Tor Strains of Vibrio cholerae O1 in Bangladesh,” J. of Clinical Microbiology, Vol.44, No.11, pp. 4211-4213, doi: 10.1128/JCM.01304-06, 2006.
-  A. Mutreja et al., “Evidence for Several Waves of Global Transmission in the Seventh Cholera Pandemic,” Nature, Vol.477, No.7365, pp. 462-465. doi: 10.1038/nature10392, 2011.
-  T. F. Wierzba, “Oral Cholera Vaccines and Their Impact on the Global Burden of Disease,” Human Vaccines & Immunotherapeutics, Vol.15, No.6, pp. 1294-1301, doi: 10.1080/21645515.2018.1504155, 2019.
-  H. Shaikh, J. Lynch, J. Kim, and J.L. Excler, “Current and Future Cholera Vaccines,” Vaccine, Vol.38, Supplement 1, pp. A118-A126, doi: 10.1016/j.vaccine.2019.12.011, 2020.
This article is published under a Creative Commons Attribution-NoDerivatives 4.0 International License.