Abstract
Cholera is a diarrheal disease caused by the gram-negative bacterium Vibrio cholerae, and an estimated 120,000 deaths from cholera occur globally every year. The natural reservoir of the bacterium is environmental. A recent report indicated an association between V. cholerae and chironomid egg masses. Chironomids, the “non-biting midges” (Diptera; Chironomidae), are the most widely distributed and frequently the most abundant insects in freshwater. Females attach egg masses, each containing hundreds of eggs encased in a layer of gelatin, to the water’s edge where bacteria are abundant and may encounter the nutrient-rich substrate. Here we report the isolation of non-O1 and non-O139 V. cholerae from chironomid egg masses from different freshwater bodies in Israel, India, and Africa. In a yearly survey in Israel, chironomid populations were found to peak biannually, and it seemed that those peaks were followed by subsequent bacterial growth and disappearance during the winter in the Mediterranean region. The bacterial population rose as water temperature surpassed 25°C. Thirty-five different serogroups of V. cholerae were identified among the bacteria isolated from chironomids, demonstrating population heterogeneity. Two strains of V. cholerae O37 and O201 that were isolated from chironomid egg masses in Zanzibar Island were NAG-ST positive. Our findings support the hypothesis that the association found between chironomids and the cholera bacteria is not a rare coincidence, indicating that chironomid egg masses may serve as yet another potential reservoir for V. cholerae.




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References
InstitutionalAuthorNameAPHA, AWWA, WPCF (1992) Standard methods for the examination of water and wastewater, 18th ed. American Public Health Association Washington, DC
P Armitage PS Cranston LCV Pinder (1995) . P Armitage PS Cranston LCV Pinder (Eds) The Chironomidae: The Biology and Ecology of Non-biting Midges. Chapman and Hall London
M Broza M Halpern M Inbar (2000) ArticleTitleNon-biting midges (Diptera; Chironomidae) in waste stabilization ponds: an intensifying nuisance in Israel. Wat Sci Technol 42 71–74
M Broza M Halpern L Gahanma M Inbar (2003) ArticleTitleNuisance chironomids in waste stabilization ponds: monitoring and action threshold assessment, based on public complaints. J Vector Ecol 28 31–36 Occurrence Handle1:STN:280:DC%2BD3szgtlSjuw%3D%3D Occurrence Handle12831126
M Broza M Halpern (2001) ArticleTitleChironomid egg masses and Vibrio cholerae. Nature 412 40 Occurrence Handle10.1038/35083691 Occurrence Handle1:CAS:528:DC%2BD3MXlt1Crsrc%3D
K Bagchi P Echeverria JD Arthur O Sethabutr O Serichantalergs CW Hoge (1993) ArticleTitleEpidemic of diarrhea caused by Vibrio cholerae non-O1 that produced heat-stable toxin among Khmers in a camp in Thailand. J Clin Microbiol 31 1315–1317 Occurrence Handle1:STN:280:ByyB2szpsV0%3D Occurrence Handle8501234
S Chakraborty AK Mukhopadhyay RK Bhadra AN Ghosh R Mitra T Shimada S Yamasaki SM Faruque Y Takeda RR Colwell GB Nair (2000) ArticleTitleVirulence genes in environmental strains of Vibrio cholerae. Appl Environ Microbiol 66 4022–4028 Occurrence Handle10.1128/AEM.66.9.4022-4028.2000 Occurrence Handle1:CAS:528:DC%2BD3cXmsVajsLY%3D Occurrence Handle10966424
CT Codeco (2001) ArticleTitleEndemic and epidemic dynamics of cholera: the role of the aquatic reservoir. BMC Infect Dis 1 1 Occurrence Handle10.1186/1471-2334-1-1 Occurrence Handle1:STN:280:DC%2BD38votF2htQ%3D%3D Occurrence Handle11208258
RR Colwell (1996) ArticleTitleGlobal climate and infectious disease: the cholera paradigm. Science 274 2025–2031 Occurrence Handle10.1126/science.274.5295.2025 Occurrence Handle1:CAS:528:DyaK2sXivVCm Occurrence Handle8953025
RR Colwell A Huq (1999) ArticleTitleGlobal microbial ecology: biogeography and diversity of Vibrios as a model. J Appl Microbiol Symp Supp 85 134S–137S
RR Colwell A Huq (2001) ArticleTitleMarine ecosystems and cholera. Hydrobiologia 460 141–145 Occurrence Handle10.1023/A:1013111016642
JH Epler (2001) Identification manual for the larval Chironomidae (Diptera) of North and South Carolina. JH Epler (Eds) . North Carolina Department of Environment and Natural Resources Division of Water Quality .
M Halpern H Gancz M Broza Y Kashi (2003) ArticleTitle Vibrio cholerae hemagglutinin/protease degrades chironomid egg masses. Appl Environ Microbiol 69 4200–4204 Occurrence Handle10.1128/AEM.69.7.4200-4204.2003 Occurrence Handle1:CAS:528:DC%2BD3sXlsFagu7g%3D Occurrence Handle12839800
A Huq EB Small PA West R Rahman RR Colwell (1983) ArticleTitleEcology of V. cholerae with special reference to planktonic crustacean copepods. Appl Environ Microbiol 45 275–283 Occurrence Handle1:STN:280:BiyC38rltl0%3D Occurrence Handle6337551
MS Islam BS Drasar RB Sack (1996) Ecology of Vibrio cholerae: role of aquatic flora and fauna. BS Drasar BD Forrest (Eds) Cholera and the Ecology of Vibrio cholerae. Chapman and Hall London 187–227
AM Kamal (1971) ArticleTitleOutbreak of gastro-enteritis by non-agglutinable (NAG) vibrios in the republic of the Sudan. J Egypt Public Health Assoc XLVI 125–159
SM Lewin (1996) Zoological microhabitats of Vibrio cholerae. BS Drasar BD Forrest (Eds) Cholera and the Ecology of Vibrio cholerae. Chapman and Hall London 228–254
M Li T Shimada G Morris Jr A Sulakvelidze S Sozhamannan (2002) ArticleTitleEvidence for the emergence of non-O1 and non-O139 Vibrio cholerae strains with pathogenic potential by exchange of O-antigen biosynthesis regions. Infec Immun 70 2441–2453 Occurrence Handle10.1128/IAI.70.5.2441-2453.2002 Occurrence Handle1:CAS:528:DC%2BD38XjtFKgu78%3D
AK Mukhopadhyay S Garg R Mitra A Basu K Rajendran D Dutta SK Bhattacharya T Shimada T Takeda Y Takeda GB Nair (1996) ArticleTitleTemporal shifts in traits of Vibrio cholerae strains isolated from hospitalized patients in Calcutta: a 3-year (1993 to 1995) analysis. J Clin Microbiol 34 2537–2543 Occurrence Handle1:CAS:528:DyaK28XmtVSmtL8%3D Occurrence Handle8880516
U Nolte (1993) ArticleTitleEgg masses of Chironomidae (Diptera). A review, including new observations and a preliminary key. Ent Scand Suppl 43 5–75
M Pascual MJ Bouma AP Dobson (2002) ArticleTitleCholera and climate: revisiting the quantitative evidence. review. Microb Infect 4 237–245 Occurrence Handle10.1016/S1286-4579(01)01533-7
IN Rivera J Chun A Huq RB Sack RR Colwell (2001) ArticleTitleGenotypes associated with virulence in environmental isolates of Vibrio cholerae. Appl Environ Microbiol 67 2421–2429 Occurrence Handle10.1128/AEM.67.6.2421-2429.2001 Occurrence Handle1:CAS:528:DC%2BD3MXkt1Cis7Y%3D Occurrence Handle11375146
T Shimada E Arakawa K Itoh T Okitsu A Matsushima Y Asai S Yamai T Nakazato GB Nair MJ Albert Y Takeda (1994) ArticleTitleExtended serotyping scheme for Vibrio cholerae. Curr Microbiol 28 175–178
R Tauxe L Seminario R Tapia M Libel (1994) The Latin America Epidemic. IK Wachsmuth PA Blake . Olsvik (Eds) Vibrio cholerae and Cholera: Molecular to Global Perspective. ASM Press Washington, DC 321–344
WJ De Van Bund D Groenendijk (1994) ArticleTitleSeasonal dynamics and burrowing of littoral chironomid larvae in relation to competition and predation. Arch Hydrobiol 132 213–225
WJ Van De Bund C Davids SJH Spaas (1995) ArticleTitleSeasonal dynamics and spatial distribution of chydorid cladocerans in relation to chironomid larvae in the sandy littoral zone of an oligo-mesotrophic lake. Hydrobiologia 299 125–138
G Wolfram K Donabaum M Schager VA Kowarc (1999) ArticleTitleThe zoobenthic community of shallow salt pans in Austria—preliminary results on phenology and the impact of salinity on benthic invertebrates. Hydrobiologia 408/409 193–202 Occurrence Handle10.1023/A:1017011414599
Acknowledgements
We thank Dr. Moshe Inbar for his fruitful advice and help in the statistical analysis, Dr. Ariel Kushmaro for his comments on an earlier draft of the manuscript, and Amikam Shoob for photographing Fig. 1a.
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Halpern, M., Broza, Y., Mittler, S. et al. Chironomid Egg Masses as a Natural Reservoir of Vibrio cholerae Non-O1 and Non-O139 in Freshwater Habitats . Microb Ecol 47, 341–349 (2004). https://doi.org/10.1007/s00248-003-2007-6
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DOI: https://doi.org/10.1007/s00248-003-2007-6