Epidemiology, Genetics, and Ecology of ToxigenicVibrio cholerae

SUMMARY Cholera caused by toxigenic Vibrio cholerae is a major public health problem confronting developing countries, where outbreaks occur in a regular seasonal pattern and are particularly associated with poverty and poor sanitation. The disease is characterized by a devastating watery diarrhea which leads to rapid dehydration, and death occurs in 50 to 70% of untreated patients. Cholera is a waterborne disease, and the importance of water ecology is suggested by the close association of V. cholerae with surface water and the population interacting with the water. Cholera toxin (CT), which is responsible for the profuse diarrhea, is encoded by a lysogenic bacteriophage designated CTXΦ. Although the mechanism by which CT causes diarrhea is known, it is not clear why V. cholerae should infect and elaborate the lethal toxin in the host. Molecular epidemiological surveillance has revealed clonal diversity among toxigenic V. cholerae strains and a continual emergence of new epidemic clones. In view of lysogenic conversion by CTXΦ as a possible mechanism of origination of new toxigenic clones of V. cholerae, it appears that the continual emergence of new toxigenic strains and their selective enrichment during cholera outbreaks constitute an essential component of the natural ecosystem for the evolution of epidemic V. cholerae strains and genetic elements that mediate the transfer of virulence genes. The ecosystem comprising V. cholerae, CTXΦ, the aquatic environment, and the mammalian host offers an understanding of the complex relationship between pathogenesis and the natural selection of a pathogen.

[1]  J. Knop,et al.  Protection against cholera. A bactericidal mechanism on the mucosal surface of the small intestine of mice. , 1975, The Australian journal of experimental biology and medical science.

[2]  J. Holmgren,et al.  Identification of a mannose-binding pilus on Vibrio cholerae El Tor. , 1991, Microbial pathogenesis.

[3]  R. Hall,et al.  Origins of the mobile gene cassettes found in integrons. , 1997, Trends in microbiology.

[4]  A. C. Ghose,et al.  Major outer membrane proteins of Vibrio cholerae and their role in induction of protective immunity through inhibition of intestinal colonization , 1992, Infection and immunity.

[5]  F. K. Graaf,et al.  Molecular cloning of a gene coding for a Vibrio cholerae haemagglutinin , 1986 .

[6]  S. Faruque,et al.  Emergence of a new clone of toxigenic Vibrio cholerae O1 biotype El Tor displacing V. cholerae O139 Bengal in Bangladesh , 1997, Journal of clinical microbiology.

[7]  V. Baselski,et al.  Survival and multiplication of Vibrio cholerae in the upper bowel of infant mice , 1978, Infection and immunity.

[8]  J. Mekalanos,et al.  Expression of ToxR, the transcriptional activator of the virulence factors in Vibrio cholerae, is modulated by the heat shock response. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[9]  K. Zaman,et al.  SIMULTANEOUS OUTBREAKS OF CONTRASTING DRUG RESISTANT CLASSIC AND EL TOR VIBRIO CHOLERAE 01 IN BANGLADESH , 1989, The Lancet.

[10]  A. T. Shousha Cholera Epidemic in Egypt (1947): A Preliminary Report. , 1948, Bulletin of the World Health Organization.

[11]  Rita R. Colwell,et al.  The Ecology of Vibrio cholerae , 1992 .

[12]  J. Mekalanos,et al.  TcpP protein is a positive regulator of virulence gene expression in Vibrio cholerae. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Koch An Address on Cholera and its Bacillus , 1884, British medical journal.

[14]  Ø. Olsvik,et al.  Vibrio cholerae and cholera : molecular to global perspectives , 1994 .

[15]  N. Nakasone,et al.  Characterization of Vibrio cholerae 01 recently isolated in Bangladesh. , 1987, Transactions of the Royal Society of Tropical Medicine and Hygiene.

[16]  J. Wells,et al.  Cholera in Piura, Peru: a modern urban epidemic. , 1992, The Journal of infectious diseases.

[17]  J. Mekalanos,et al.  Cholera toxin transcriptional activator ToxR is a transmembrane DNA binding protein , 1987, Cell.

[18]  J. Mekalanos,et al.  Regulatory cascade controls virulence in Vibrio cholerae. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[19]  M. Kovach,et al.  Identification of a ToxR-activated gene, tagE, that lies within the accessory colonization factor gene cluster of Vibrio cholerae O395. , 1994, Gene.

[20]  J. Kaper,et al.  Vibrio cholerae produces a second enterotoxin, which affects intestinal tight junctions. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[21]  S. L. Chiang,et al.  CTX genetic element encodes a site-specific recombination system and an intestinal colonization factor. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[22]  D. Chitnis,et al.  Role of somatic antigen of Vibrio cholerae in adhesion to intestinal mucosa. , 1982, Journal of medical microbiology.

[23]  K. Wachsmuth,et al.  Genetic diversity among toxigenic and nontoxigenic Vibrio cholerae O1 isolated from the Western Hemisphere , 1991, Epidemiology and Infection.

[24]  J. Kaper,et al.  Accessory cholera enterotoxin (Ace), the third toxin of a Vibrio cholerae virulence cassette. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[25]  A. Barker,et al.  Identification of VCR, a repeated sequence associated with a locus encoding a hemagglutinin in Vibrio cholerae O1 , 1994, Journal of bacteriology.

[26]  V. DiRita Co‐ordinate expression of virulence genes by ToxR in Vibrio cholerae , 1992, Molecular microbiology.

[27]  Swerdlow Dl,et al.  Vibrio cholerae non-O1--the eighth pandemic? , 1993 .

[28]  A. Baqui,et al.  Surveillance of patients attending a rural diarrhoea treatment centre in Bangladesh. , 1991, Tropical and geographical medicine.

[29]  A. M. Dawson The Conquest of Cholera: , 1938, Nature.

[30]  K. Peterson,et al.  The Vibrio cholerae toxin-coregulated-pilus gene tcpI encodes a homolog of methyl-accepting chemotaxis proteins , 1994, Infection and immunity.

[31]  T. Shimada,et al.  Vibrio cholerae O139 Bengal in Bangkok. , 1993, Lancet.

[32]  P. Fontelo Protection against cholera , 1995, Science.

[33]  J. Holmgren,et al.  Protection against Vibrio cholerae El Tor infection by specific antibodies against mannose-binding hemagglutinin pili , 1992, Infection and immunity.

[34]  R. Y. Morita,et al.  Survival of a Psychrophilic Marine Vibrio Under Long-Term Nutrient Starvation , 1977, Applied and environmental microbiology.

[35]  B. Cvjetanović,et al.  The Seventh Pandemic of Cholera , 1972, Nature.

[36]  M. Ogierman,et al.  Genetic organization and sequence of the promoter-distal region of the tcp gene cluster of Vibrio cholerae. , 1993, Gene.

[37]  D. Mazel,et al.  A distinctive class of integron in the Vibrio cholerae genome. , 1998, Science.

[38]  Imported Cholera Imported cholera associated with a newly described toxigenic Vibrio cholerae O139 strain--California, 1993. , 1993, MMWR. Morbidity and mortality weekly report.

[39]  M. S. Islam,et al.  The aquatic environment as a reservoir of Vibrio cholerae: a review. , 1993, Journal of diarrhoeal diseases research.

[40]  J. Holmgren,et al.  Role of antibodies against biotype-specific Vibrio cholerae pili in protection against experimental classical and El Tor cholera , 1994, Infection and immunity.

[41]  J. Holmgren,et al.  Vibrio cholerae expresses cell surface antigens during intestinal infection which are not expressed during in vitro culture , 1989, Infection and immunity.

[42]  S. Faruque,et al.  Molecular analysis of rRNA and cholera toxin genes carried by the new epidemic strain of toxigenic Vibrio cholerae O139 synonym Bengal , 1994, Journal of clinical microbiology.

[43]  Matthew K. Waldor,et al.  Lysogenic Conversion by a Filamentous Phage Encoding Cholera Toxin , 1996, Science.

[44]  I. Huq,et al.  Epidemiologic analysis of endemic cholera in urban East Pakistan, 1964-1966. , 1969, American journal of epidemiology.

[45]  Dawson Am The conquest of cholera. , 1988 .

[46]  M. Lebens,et al.  Cloning and sequencing of Vibrio cholerae mannose‐sensitive haemagglutinin pilin gene: localization of mshA within a cluster of type 4 pilin genes , 1994, Molecular microbiology.

[47]  J. Kaper,et al.  CVD110, an attenuated Vibrio cholerae O1 El Tor live oral vaccine strain , 1993, Infection and immunity.

[48]  R. Taylor,et al.  Control of the ToxR virulence regulon in Vibrio cholerae by environmental stimuli , 1997, Molecular microbiology.

[49]  G. Jonson Expression of virulence factors by classical and El Tor Vibrio cholerae , 1990 .

[50]  Michael E. Kovach,et al.  The Vibrio cholerae acfB colonization determinant encodes an inner membrane protein that is related to a family of signal-transducing proteins , 1994, Infection and immunity.

[51]  M U Khan,et al.  Endemic cholera in rural Bangladesh, 1966-1980. , 1982, American journal of epidemiology.

[52]  M. Waldor,et al.  Regulation, replication, and integration functions of the Vibrio cholerae CTXφ are encoded by region RS2 , 1997, Molecular microbiology.

[53]  P. Fields,et al.  Difference between toxigenic Vibrio cholerae 01 from South America and US gulf coast , 1991, The Lancet.

[54]  B. Stoll,et al.  Surveillance of patients attending a diarrhoeal disease hospital in Bangladesh , 1982, British medical journal.

[55]  S. Payne,et al.  Effect of iron limitation on growth, siderophore production, and expression of outer membrane proteins of Vibrio cholerae , 1982, Journal of bacteriology.

[56]  J. Mekalanos,et al.  Periplasmic interaction between two membrane regulatory proteins, ToxR and ToxS, results in signal transduction and transcriptional activation , 1991, Cell.

[57]  R. Bryant,et al.  Current perspectives on the epidemiology and pathogenesis of clinically significant Vibrio spp , 1988, Clinical Microbiology Reviews.

[58]  M. Sherman,et al.  A Preliminary Report , 1953 .

[59]  Cholera and other vibrio-associated diarrhoeas. , 1980, Bulletin of the World Health Organization.

[60]  R. Glass,et al.  Emergence of multiply antibiotic-resistant Vibrio cholerae in Bangladesh. , 1980, The Journal of infectious diseases.

[61]  S. Faruque,et al.  Molecular analysis of toxigenic Vibrio cholerae O139 Bengal strains isolated in Bangladesh between 1993 and 1996: evidence for emergence of a new clone of the Bengal vibrios , 1997, Journal of clinical microbiology.

[62]  M. Waldor,et al.  ToxR-Independent Expression of Cholera Toxin from the Replicative Form of CTXφ , 1998, Infection and Immunity.

[63]  S. Faruque,et al.  Genetic relation between Vibrio cholerae 01 strains in Ecuador and Bangladesh , 1992, The Lancet.

[64]  C. Sciortino,et al.  Vitek system antimicrobial susceptibility testing of O1, O139, and non-O1 Vibrio cholerae , 1996, Journal of clinical microbiology.

[65]  K. Wachsmuth,et al.  THE QUESTION OF CLASSICAL CHOLERA , 1983, The Lancet.

[66]  A. Barker,et al.  Nucleotide sequence encoding the mannose-fucose-resistant hemagglutinin of Vibrio cholerae O1 and construction of a mutant , 1993, Infection and immunity.

[67]  P. West The human pathogenic vibrios – A public health update with environmental perspectives , 1989, Epidemiology and Infection.

[68]  R. Freter,et al.  Role of chemotaxis in the association of motile bacteria with intestinal mucosa: fitness and virulence of nonchemotactic Vibrio cholerae mutants in infant mice , 1981, Infection and immunity.

[69]  M. Vasil,et al.  Studies on toxinogenesis in Vibrio cholerae. I. Isolation of mutants with altered toxinogenicity. , 1974, The Journal of infectious diseases.

[70]  Cholera situation in the Americas. , 1994, Epidemiological bulletin.

[71]  E. Boedeker,et al.  A Vibrio cholerae pathogenicity island associated with epidemic and pandemic strains. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[72]  T. Takeda,et al.  The Gene Encoding the Heat‐Stable Enterotoxin of Vibrio cholerae Is Flanked by 123‐Base Pair Direct Repeats , 1993, Microbiology and immunology.

[73]  R. Bradley Sack,et al.  Large outbreak of clinical cholera due to Vibrio cholerae non-01 in Bangladesh , 1993, The Lancet.

[74]  J. Mekalanos,et al.  Safe, live Vibrio cholerae vaccines? , 1988, Vaccine.

[75]  K. Peterson,et al.  Identification of a Vibrio cholerae ToxR-activated gene (tagD) that is physically linked to the toxin-coregulated pilus (tcp) gene cluster. , 1994, Gene.

[76]  A. Faruque,et al.  CLASSICAL VIBRIO CHOLERAE BIOTYPE DISPLACES EL TOR IN BANGLADESH , 1983, The Lancet.

[77]  C Carrillo,et al.  The molecular epidemiology of cholera in Latin America. , 1993, The Journal of infectious diseases.

[78]  S. Attridge,et al.  The specificity of Vibrio cholerae adherence and the significance of the slime agglutinin as a second mediator of in vitro attachment. , 1983, Journal of Infectious Diseases.

[79]  The Cholera Epidemic of 1873 in the United States , 1875, The American Journal of Dental Science.

[80]  J. Kaper,et al.  Cloning of a gene (zot) encoding a new toxin produced by Vibrio cholerae , 1992, Infection and immunity.

[81]  M. Levine,et al.  Safety and immunogenicity of live oral cholera vaccine candidate CVD 110, a delta ctxA delta zot delta ace derivative of El Tor Ogawa Vibrio cholerae. , 1993, The Journal of infectious diseases.

[82]  V. DiRita,et al.  Genetic analysis of the interaction between Vibrio cholerae transcription activator ToxR and toxT promoter DNA , 1996, Journal of bacteriology.

[83]  V. Baselski,et al.  In vivo and in vitro characterization of virulence-deficient mutants of Vibrio cholerae , 1979, Infection and immunity.

[84]  Amit Ghosh,et al.  Molecular Epidemiology of Reemergent Vibrio cholerae O139 Bengal in India , 1998, Journal of Clinical Microbiology.

[85]  R. Sack,et al.  Vibrio cholerae O139: How great is the threat of a pandemic? , 1996, Tropical medicine & international health : TM & IH.

[86]  C. Proby,et al.  New broad-spectrum sunscreen for polymorphic light eruption , 1993, The Lancet.

[87]  V. L. Miller,et al.  Synthesis of cholera toxin is positively regulated at the transcriptional level by toxR. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[88]  E. Lebenthal,et al.  Textbook of Secretory Diarrhea , 1990 .

[89]  S. Boyko,et al.  Transcriptional regulation by iron of a Vibrio cholerae virulence gene and homology of the gene to the Escherichia coli fur system , 1990, Journal of bacteriology.

[90]  T. Popović,et al.  Molecular Epidemiology of Cholera , 1994 .

[91]  C. Sciortino,et al.  Vibrio cholerae expresses iron-regulated outer membrane proteins in vivo , 1983, Infection and immunity.

[92]  J. Mekalanos,et al.  Affinity filters, a new approach to the isolation of tox mutants of Vibrio cholerae. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[93]  T. Shimada,et al.  Additional serovars and inter-O antigenic relationships of Vibrio cholerae. , 1977, Japanese journal of medical science & biology.

[94]  J. Snow On the Mode of Communication of Cholera , 1856, Edinburgh medical journal.

[95]  D. Satcher,et al.  Emerging infections: getting ahead of the curve. , 1995, Emerging infectious diseases.

[96]  M. Kothary,et al.  Non-01 Vibrio cholerae , 1993, The Lancet.

[97]  J. Carter,et al.  Antibiotic resistance pattern of Vibrio cholerae and Shigella causing diarrhoea outbreaks in the eastern Africa region: 1994-1996. , 1997, East African medical journal.

[98]  V. L. Miller,et al.  Use of phoA gene fusions to identify a pilus colonization factor coordinately regulated with cholera toxin. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[99]  A. M. Davies,et al.  Epidemiological aspects of cholera El Tor outbreak in a non-endemic area. , 1971, Lancet.

[100]  Y. Takeda,et al.  Outbreak of Vibrio cholerae non-01 in India and Bangladesh , 1993, The Lancet.

[101]  W. Ewing,et al.  Studies on the Aeromonas Group. , 1961 .

[102]  A. Barker,et al.  VlpA of Vibrio cholerae O1: the first bacterial member of the alpha 2-microglobulin lipocalin superfamily. , 1997, Microbiology.

[103]  Rita R. Colwell,et al.  Vibrios in the environment: viable but nonculturable Vibrio cholerae , 1994 .

[104]  R. Y. Morita,et al.  Morphological characterization of small cells resulting from nutrient starvation of a psychrophilic marine vibrio , 1976, Applied and environmental microbiology.

[105]  S. Faruque,et al.  Molecular epidemiology of toxigenic Vibrio cholerae in Bangladesh studied by numerical analysis of rRNA gene restriction patterns , 1995, Journal of clinical microbiology.

[106]  MyronM. Levine South America: The return of cholera , 1991, The Lancet.

[107]  M. Waldor,et al.  A new type of conjugative transposon encodes resistance to sulfamethoxazole, trimethoprim, and streptomycin in Vibrio cholerae O139 , 1996, Journal of bacteriology.

[108]  S. Attridge,et al.  The role of toxin-coregulated pili in the pathogenesis of Vibrio cholerae O1 El Tor. , 1993, Microbial pathogenesis.

[109]  J. Marchand,et al.  The amino‐terminal part of ActA is critical for the actin‐based motility of Listeria monocytogenes; the central proline‐rich region acts as a stimulator , 1995, Molecular microbiology.

[110]  K. Peterson,et al.  The accessory colonization factor and toxin-coregulated pilus gene clusters are physically linked on the Vibrio cholerae 0395 chromosome. , 1994, DNA sequence : the journal of DNA sequencing and mapping.

[111]  J. Kaper,et al.  Molecular characterization of environmental and nontoxigenic strains of Vibrio cholerae , 1981, Infection and immunity.

[112]  A. Baqui,et al.  Cholera epidemics in Bangladesh: 1985-1991. , 1992, Journal of diarrhoeal diseases research.

[113]  J. Mekalanos Cholera toxin: genetic analysis, regulation, and role in pathogenesis. , 1985, Current topics in microbiology and immunology.

[114]  R. Taylor,et al.  Organization of tcp, acf, and toxT genes within a ToxT‐dependent operon , 1995, Molecular microbiology.

[115]  J. Morris,et al.  Cholera and other vibrioses in the United States. , 1985, The New England journal of medicine.

[116]  S. Faruque,et al.  Induction of the Lysogenic Phage Encoding Cholera Toxin in Naturally Occurring Strains of Toxigenic Vibrio cholerae O1 and O139 , 1998, Infection and Immunity.

[117]  J. Holmgren,et al.  Relative significance of mannose-sensitive hemagglutinin and toxin-coregulated pili in colonization of infant mice by Vibrio cholerae El Tor , 1996, Infection and immunity.

[118]  J. Mekalanos,et al.  ToxR regulates the production of lipoproteins and the expression of serum resistance in Vibrio cholerae. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[119]  R. Glass,et al.  Plasmid-borne multiple drug resistance in Vibrio cholerae serogroup O1, biotype El Tor: evidence for a point-source outbreak in Bangladesh. , 1983, The Journal of infectious diseases.

[120]  M. Vasil,et al.  Studies on toxinogenesis in Vibrio cholerae. III. Characterization of nontoxinogenic mutants in vitro and in experimental animals. , 1975, The Journal of clinical investigation.

[121]  A. Faruque,et al.  Large epidemic of cholera-like disease in Bangladesh caused by Vibrio cholerae 0139 synonym Bengal , 1993, The Lancet.

[122]  R M Hall,et al.  Gene cassettes: a new class of mobile element. , 1995, Microbiology.

[123]  Michael E. Kovach,et al.  A putative integrase gene defines the distal end of a large cluster of ToxR-regulated colonization genes in Vibrio cholerae. , 1996, Microbiology.

[124]  Amit Pal,et al.  Emergence of novel strain of Vibrio cholerae with epidemic potential in southern and eastern India , 1993, The Lancet.

[125]  Y. Takeda,et al.  Vibrio cholerae 0139 Bengal in Bangkok , 1993, The Lancet.

[126]  M. S. Islam,et al.  The aquatic flora and fauna as reservoirs of Vibrio cholerae: a review. , 1994, Journal of diarrhoeal diseases research.

[127]  W. Mosley,et al.  Endemic cholera in rural East Pakistan. , 1969, American journal of epidemiology.

[128]  Y. Takeda,et al.  Resurgence of Vibrio cholerae O139 Bengal with altered antibiogram in Calcutta, India , 1996, The Lancet.

[129]  H. Binder,et al.  Textbook of Secretory Diarrhea , 1991 .

[130]  W. Greenough,et al.  Cholera in Africa: a message for the West. , 1975, Annals of internal medicine.

[131]  B. Howard A Prototype Live Oral Cholera Vaccine , 1971, Nature.

[132]  J. Mekalanos Duplication and amplification of toxin genes in Vibrio cholerae , 1983, Cell.

[133]  J. Kaper,et al.  Molecular epidemiology of Vibrio cholerae in the U.S. Gulf Coast , 1982, Journal of clinical microbiology.

[134]  A. Baqui,et al.  Survival of classic cholera in Bangladesh , 1991, The Lancet.

[135]  M. S. Islam,et al.  Why treatment centres failed to prevent cholera deaths among Rwandan refugees in Goma, Zaire , 1995, The Lancet.

[136]  M. Levine,et al.  Toxin, toxin-coregulated pili, and the toxR regulon are essential for Vibrio cholerae pathogenesis in humans , 1988, The Journal of experimental medicine.

[137]  S. Calderwood,et al.  Positive transcriptional regulation of an iron-regulated virulence gene in Vibrio cholerae. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[138]  J. Mekalanos,et al.  A novel suicide vector and its use in construction of insertion mutations: osmoregulation of outer membrane proteins and virulence determinants in Vibrio cholerae requires toxR , 1988, Journal of bacteriology.

[139]  J. Mekalanos,et al.  Characterization of the Vibrio cholerae ToxR Regulon: Identification of Novel Genes Involved in Intestinal Colonization , 1989, Infection and immunity.

[140]  V. DiRita,et al.  A branch in the ToxR regulatory cascade of Vibrio cholerae revealed by characterization of toxT mutant strains , 1997, Molecular microbiology.

[141]  S. Faruque,et al.  Clonal relationships among classical Vibrio cholerae O1 strains isolated between 1961 and 1992 in Bangladesh , 1993, Journal of clinical microbiology.

[142]  R. Colwell Vibrios in the environment , 1984 .

[143]  R. Y. Morita,et al.  Possible strategy for the survival of marine bacteria under starvation conditions , 1978 .

[144]  R. Colwell,et al.  Vibrio mimicus with multiple toxin types isolated from human and environmental sources. , 1994, Journal of medical microbiology.

[145]  V. DiRita,et al.  Differential expression of the ToxR regulon in classical and E1 Tor biotypes of Vibrio cholerae is due to biotype-specific control over toxT expression. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[146]  A. Mukhopadhyay,et al.  Molecular characterization of Vibrio cholerae O1 biotype El Tor strains isolated between 1992 and 1995 in Calcutta, India: evidence for the emergence of a new clone of the El Tor biotype. , 1997, The Journal of infectious diseases.

[147]  V. DiRita,et al.  Identification of an iron-regulated virulence determinant in Vibrio cholerae, using TnphoA mutagenesis , 1990, Infection and immunity.