{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T10:57:28Z","timestamp":1791975448023,"version":"4.4.0"},"reference-count":57,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2021,2,10]],"date-time":"2021-02-10T00:00:00Z","timestamp":1612915200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Cholera is a negative public health event caused by Vibrio cholerae. Although V. cholerae is abundant in natural environments, its pattern and transmission between different niches remain puzzling and interrelated. Our study aimed to investigate the occurrence of nonpathogenic V. cholerae in the natural environment during endemicity periods. It also aimed to highlight the role of molecular ecoepidemiology in mapping the routes of spread, transmission, and prevention of possible future cholera outbreaks. V. cholerae was detected in different aquatic environments, waterfowl, and poultry farms located along the length of the Nile River in Giza, Cairo, and Delta provinces, Egypt. After polymerase chain reaction amplification of the specific target outer membrane gene (Omp W) of suspected isolates, we performed sequence analysis, eventually using phylogenetic tree analysis to illustrate the possible epidemiological relationships between different sequences. Data revealed a significant variation in the physicochemical conditions of the examined Nile districts related to temporal, spatial, and anthropogenic activities. Moreover, data showed an evident association between V. cholerae and the clinically diseased Synodontis schall fish. We found that the environmental distress triggered by the salinity shift and elevated temperature in the Middle Delta of the Nile River affects the pathogenesis of V. cholerae, in addition to the characteristics of fish host inhabiting the Rosetta Branch at Kafr El-Zayat, El-Gharbia province, Egypt. In addition, we noted a significant relationship between V. cholerae and poultry sources that feed on the Nile dikes close to the examined districts. Sequence analysis revealed clustering of the waterfowl and broiler chicken isolates with human and aquatic isolated sequences retrieved from the GenBank databases. From the obtained data, we hypothesized that waterfowl act as a potential vector for the intermediate transmission of cholera. Therefore, continuous monitoring of Nile water quality and mitigation of Nile River pollution, in addition to following good managemental practices (GMPs), general hygienic guidelines, and biosecurity in the field of animal production and industry, might be the way to break this cyclic transmission between human, aquatic, and animal sectors.<\/jats:p>","DOI":"10.3390\/pathogens10020190","type":"journal-article","created":{"date-parts":[[2021,2,12]],"date-time":"2021-02-12T16:12:10Z","timestamp":1613146330000},"page":"190","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":11,"title":["Ecoepidemiology and Potential Transmission of Vibrio cholerae among Different Environmental Niches: An Upcoming Threat in Egypt"],"prefix":"10.3390","volume":"10","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-6191-6950","authenticated-orcid":false,"given":"Eman M.","family":"Ismail","sequence":"first","affiliation":[{"name":"Department of Veterinary Hygiene and Management, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mona","family":"Kadry","sequence":"additional","affiliation":[{"name":"Department of Zoonoses, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6127-5716","authenticated-orcid":false,"given":"Esraa A.","family":"Elshafiee","sequence":"additional","affiliation":[{"name":"Department of Zoonoses, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7363-2496","authenticated-orcid":false,"given":"Eman","family":"Ragab","sequence":"additional","affiliation":[{"name":"Department of Microbiology, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eman A.","family":"Morsy","sequence":"additional","affiliation":[{"name":"Department of Poultry Diseases, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Omar","family":"Rizk","sequence":"additional","affiliation":[{"name":"Faculty of Biotechnology\u2014MSA University, 6th October City 12573, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Manal M.","family":"Zaki","sequence":"additional","affiliation":[{"name":"Department of Veterinary Hygiene and Management, Faculty of Veterinary Medicine, Cairo University, Giza 12211, Egypt"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2021,2,10]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1441","DOI":"10.1016\/j.watres.2008.12.025","article-title":"A molecular survey on virulence associated genotypes of non-O1 non-O139 Vibrio cholerae in aquatic environment of Tehran, Iran","volume":"43","author":"Bakhshi","year":"2009","journal-title":"Water Res."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Mendes-Marques, C.L., Silveira Filho, V.D.M., da Costa, A.P.R., Nunes, M.D.L., Silva Filho, S.V.D., Figueir\u00f4a, \u00c2.C.T.D.A., Hofer, E., de Almeida, A.M.P., and Leal, N.C. (2013). The aquatic environment as a reservoir of Vibrio cholerae O1 in hydrographic basins of the state of Pernambuco, Brazil. Sci. World J.","DOI":"10.1155\/2013\/746254"},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"Racault, M.F., Abdulaziz, A., George, G., Menon, N., Punathil, M., McConville, K., Loveday, B., Platt, T., Sathyendranath, S., and Vijayan, V. (2019). Environmental reservoirs of Vibrio cholerae: Challenges and opportunities for ocean-color remote sensing. Remote Sens., 11.","DOI":"10.3390\/rs11232763"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Almagro-Moreno, S., and Taylor, R.K. (2013). Cholera: Environmental reservoirs and impact on disease transmission. Microbiol. Spectrum, 1.","DOI":"10.1128\/microbiolspec.OH-0003-2012"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"146","DOI":"10.22159\/ajpcr.2017.v10i6.17883","article-title":"Antibiogram and molecular characterization of Vibrio cholerae isolated from marine fish","volume":"10","author":"Angelo","year":"2017","journal-title":"Asian J. Pharm Clin. Res."},{"key":"ref_6","first-page":"363","article-title":"Detection of Vibrio cholerae biotype El Tor by purging","volume":"34","author":"Gangarosa","year":"1966","journal-title":"Bull. World Health Organ."},{"key":"ref_7","first-page":"12","article-title":"Cholera and estuarine salinity in Calcutta and London","volume":"1","author":"Miller","year":"1982","journal-title":"Lancet"},{"key":"ref_8","first-page":"3","article-title":"Cholera epidemiology in developed and developing countries: New thoughts on transmission, seasonality, and control","volume":"261","author":"Miller","year":"1985","journal-title":"Lancet"},{"key":"ref_9","first-page":"197","article-title":"The aquatic environment as a reservoir of Vibrio cholerae: A review","volume":"11","author":"Islam","year":"1993","journal-title":"J. Diarrhoeal Dis. Res."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"2025","DOI":"10.1126\/science.274.5295.2025","article-title":"Global climate and infectious disease: The cholera paradigm","volume":"274","author":"Colwell","year":"1996","journal-title":"Science"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"A52","DOI":"10.1016\/j.vaccine.2019.06.033","article-title":"Environmental reservoirs of Vibrio cholerae","volume":"38","author":"Islam","year":"2020","journal-title":"Vaccine"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"767","DOI":"10.1016\/S0160-4120(98)00058-0","article-title":"Lead and cadmium in Nile River water and finished drinking water in Greater Cairo, Egypt","volume":"24","author":"Mohamed","year":"1998","journal-title":"Environ. Int."},{"key":"ref_13","first-page":"200","article-title":"Water quality assessment of river Nile from Idfo to Cairo","volume":"31","year":"2005","journal-title":"Egypt. J. Aquat. Res."},{"key":"ref_14","first-page":"219","article-title":"Investigations on Mass Mortalities among Oreochromis niloticus at Mariotteya Stream, Egypt: Parasitic Infestation and Environmental Pollution Impacts","volume":"5","author":"Mahmoud","year":"2014","journal-title":"J. Aquac Res. Dev."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"40","DOI":"10.1038\/35083691","article-title":"Chironomid egg masses and Vibrio cholerae","volume":"412","author":"Broza","year":"2001","journal-title":"Nature"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"4200","DOI":"10.1128\/AEM.69.7.4200-4204.2003","article-title":"Vibrio cholerae hemagglutinin\/protease degrades chironomid egg masses","volume":"69","author":"Halpern","year":"2003","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_17","first-page":"1","article-title":"Food as a vehicle of transmission of Cholera","volume":"1","author":"Rabbani","year":"1999","journal-title":"J. Diarrhoeal Dis. Res."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"583","DOI":"10.3201\/eid0707.017741","article-title":"Cholera outbreak in southern Tanzania: Risk factors and patterns of transmission","volume":"7","author":"Acosta","year":"2001","journal-title":"Emerg. Infect. Dis."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"345","DOI":"10.5694\/j.1326-5377.2007.tb01278.x","article-title":"Vibrio cholerae O1 El Tor cluster in Sydney linked to imported whitebait","volume":"187","author":"Forssman","year":"2007","journal-title":"Med. J. Aust."},{"key":"ref_20","first-page":"60","article-title":"Antibiotic resistance of Vibrio cholerae from poultry sources of Dhaka, Bangladesh","volume":"2","author":"Akond","year":"2008","journal-title":"Adv. Biol. Res."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1128\/aem.43.5.1219-1220.1982","article-title":"Campylobacter jejuni: Incidence in processed broilers and biotype distribution in human and broiler isolates","volume":"43","author":"Shanker","year":"1982","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"827","DOI":"10.1007\/s10096-002-0832-z","article-title":"Domestic cholera in Germany associated with fresh fish imported from Nigeria","volume":"21","author":"Ebert","year":"2002","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1430","DOI":"10.3389\/fmicb.2020.01430","article-title":"A hopeful sea-monster: A very large homologous recombination event impacting the core genome of the marine pathogen Vibrio anguillarum","volume":"11","author":"Coyle","year":"2020","journal-title":"Front. Microbiol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"197","DOI":"10.1186\/s13756-019-0657-5","article-title":"Evidence of colistin resistance genes (mcr-1 and mcr-2) in wild birds and its public health implication in Egypt","volume":"8","author":"Ahmed","year":"2019","journal-title":"Antimicrob. Resistance Infect. Control"},{"key":"ref_25","first-page":"245","article-title":"Probable role of blue-green algae in maintaining endemicity and seasonality of cholera in Bangladesh: A hypothesis","volume":"12","author":"Islam","year":"1994","journal-title":"J. Diarrhoeal Dis Res."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1111\/j.1749-6632.1994.tb19852.x","article-title":"Environmental reservoir of Vibrio cholerae. The causative agent of cholera","volume":"740","author":"Colwell","year":"1994","journal-title":"Ann. NY Acad. Sci."},{"key":"ref_27","first-page":"119","article-title":"Cholera and climate: A demonstrated relationship","volume":"120","author":"Colwell","year":"2009","journal-title":"Trans. Am. Clin. Climatol Assoc."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"303","DOI":"10.4269\/ajtmh.2011.11-0181","article-title":"Warming oceans, phytoplankton, and river discharge: Implications for cholera outbreaks","volume":"85","author":"Jutla","year":"2011","journal-title":"Am. J. Trop Med. Hyg."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"38","DOI":"10.21608\/bvmj.2015.31788","article-title":"Incidence of Vibrio species in fish with special emphasis on the effect of heat treatments","volume":"29","author":"Saad","year":"2015","journal-title":"Benha Vet. Med. J."},{"key":"ref_30","unstructured":"Al-Agha, D.E., Closas, A., and Molle, E. (Report, 2015). Survey of groundwater use in the central part of the Nile Delta. Water and salt management in the Nile Delta, Report, report number 6."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"525","DOI":"10.3844\/ajessp.2011.525.530","article-title":"Impact of abattoir and saw-mill effluent on water quality of upper ogun river (Abeokuta)","volume":"7","author":"Adeogun","year":"2011","journal-title":"Am. J. Environ. Sci."},{"key":"ref_32","first-page":"299","article-title":"Macrophytic vegetation-environment relationship along rosetta branch of the River Nile in Egypt","volume":"45","year":"2016","journal-title":"J. Environ. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"69","DOI":"10.21608\/ejabf.2015.2277","article-title":"Ecological Studies of the Macrobenthic Fauna of Ashtoum El-Gamil Protectorate, Port Said Egypt","volume":"19","author":"Elshenawy","year":"2015","journal-title":"J. Aquat. Biol. Fish."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"133","DOI":"10.21608\/ejabf.2008.1998","article-title":"Assessment of some water quality characteristics and determination of some heavy metals in Lake Manzala, Egypt","volume":"12","author":"Ali","year":"2008","journal-title":"Egypt. J. Aquat. Biol. Fish."},{"key":"ref_35","doi-asserted-by":"crossref","unstructured":"Finlayson, C., Milton, G., Prentice, R., and Davidson, N. (2018). Nile Delta (Egypt). The Wetland Book, Springer.","DOI":"10.1007\/978-94-007-4001-3"},{"key":"ref_36","first-page":"12","article-title":"Water quality observations in the marine aquaculture complex of the Deeba Triangle, Lake Manzala, Egyptian Mediterranean coast","volume":"190","author":"Digna","year":"2018","journal-title":"Environ. Monit Assess."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Senderovich, Y., Izhaki, I., and Halpern, M. (2010). Fish as reservoirs and vectors of Vibrio cholerae. PLoS ONE, 5.","DOI":"10.1371\/journal.pone.0008607"},{"key":"ref_38","first-page":"141","article-title":"Environmental damage caused by wastewater discharge into the Lake Manzala in Egypt","volume":"5","author":"Ismail","year":"2017","journal-title":"Am. J. Biosci. Bioeng."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"139","DOI":"10.21608\/ejabf.2020.95750","article-title":"Environmental studies on water quality, plankton and bacterial community in Mariout Lake, Egypt","volume":"24","author":"Farouk","year":"2020","journal-title":"Egypt. J. Aquat. Biol. Fish."},{"key":"ref_40","unstructured":"Steele, J.H. (2009). Fish: Demersal Fish (Life Histories, Behavior, Adaptations). Encyclopedia of Ocean Sciences, Academic Press. [2nd ed.]."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1400","DOI":"10.1111\/j.1462-2920.2007.01559.x","article-title":"Global impact of Vibrio cholerae interactions with chitin","volume":"10","author":"Pruzzo","year":"2008","journal-title":"Environ. Microbiol."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"4145","DOI":"10.1128\/JCM.38.11.4145-4151.2000","article-title":"Rapid method for species-specific identification of Vibrio cholerae using primers targeted to the gene of outer membrane protein OmpW","volume":"38","author":"Nandi","year":"2000","journal-title":"J. Clin. Microbiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1111\/j.1469-185X.2008.00076.x","article-title":"Bacterial pathogens in wild birds: A review of the frequency and effects of infection","volume":"84","author":"Benskin","year":"2009","journal-title":"Biol. Rev."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"328","DOI":"10.1111\/1462-2920.13612","article-title":"High genetic diversity of Vibrio cholerae in the European lake Neusiedler See is associated with intensive recombination in the reed habitat and the long-distance transfer of strains","volume":"19","author":"Pretzer","year":"2017","journal-title":"Environ. Microbiol."},{"key":"ref_45","doi-asserted-by":"crossref","unstructured":"Halpern, M., Senderovich, Y., and Izhaki, I. (2008). Waterfowl: The missing link in epidemic and pandemic cholera dissemination?. PLoS Pathog., 4.","DOI":"10.1371\/journal.ppat.1000173"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1688","DOI":"10.1128\/AEM.64.5.1688-1693.1998","article-title":"Isolation of an amoeba naturally harboring a distinctive Legionella species","volume":"64","author":"Newsome","year":"1998","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_47","unstructured":"Sakr, S.A., Attia, F.A., and Millette, J.A. (2004, January 3\u20134). Vulnerability of the Nile Delta aquifer of Egypt to seawater intrusion. Prodceedings of the International conference on water resources of arid and semi-arid regions of Africa, Issues and challenges, Gaborone, Botswana."},{"key":"ref_48","first-page":"3","article-title":"Water resources management: Alarming crisis for Egypt","volume":"4","year":"2014","journal-title":"J. Manag. Sustain."},{"key":"ref_49","unstructured":"Beattie, A. (2005). Cairo: A Cultural History, Oxford University Press."},{"key":"ref_50","unstructured":"Bird, K. (2010). Crossing Mandelbaum Gate: Coming of Age Between the Arabs and Israelis, Scribner."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"41","DOI":"10.2495\/WS130041","article-title":"Hydraulic analysis of El Mahmoudia canal","volume":"178","author":"Moghazy","year":"2013","journal-title":"Trans. Ecol. Environ."},{"key":"ref_52","unstructured":"American Public Health Association (APHA) (2005). Standard Methods for the Examination of Water and Wastewater, American Public Health Association (APHA)."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Amlacher, E. (1970). Textbook of Fish Diseases, TFH Publications Inc.","DOI":"10.2307\/1441637"},{"key":"ref_54","unstructured":"APHA (1970). Recommended Procedures for the Examination of Seawater and Shellfish, American Public Health Association. [4th ed.]."},{"key":"ref_55","unstructured":"Kaysner, C.A., and De Paola, A.J. (2004). Bacteriological Analytical Manual, Chapter 9."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"1242","DOI":"10.1128\/aem.62.4.1242-1247.1996","article-title":"PCR detection and quantitation of predominant anaerobic bacteria in human and animal fecal samples","volume":"62","author":"Wang","year":"1996","journal-title":"Appl. Environ. Microbiol."},{"key":"ref_57","first-page":"359","article-title":"Phylogenetic and evolutionary analysis of Vibrio parahaemolyticus and Vibrio alginolyticus isolates based on toxR gene sequence","volume":"33","author":"Montieri","year":"2010","journal-title":"New Microbiol."}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/2\/190\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T05:22:18Z","timestamp":1760160138000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/10\/2\/190"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,2,10]]},"references-count":57,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2021,2]]}},"alternative-id":["pathogens10020190"],"URL":"https:\/\/doi.org\/10.3390\/pathogens10020190","relation":{},"ISSN":["2076-0817"],"issn-type":[{"value":"2076-0817","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,2,10]]}}}