Document Type : Research Paper
Authors
- Tesfaye Legesse Bedada 1
- Teshome Belachew Eshete 2
- Adey Feleke Desta 3
- Fitsum Tigu Yifat 3
- Dagim Jirata Birri 3
- Kassu Desta Tullu 4
- Samson Girma Gebre 1
- Firehiwot Abera Dera 1
- Kaleab Sebsibe Awoke 1
- Tatek Kasim Feto 1
- Waktole Gobena Sima 1
- Elias Seyoum Deribe 5
- Dejenie Teklu Teklu 5
- Getinet Fikresilasie Irena 1
- Geremew Tassew Weledesemayat 1
- Tigist Yohannis Negassi 1
- Asnake Desalegn Garedew Garedew 3
1 Public Health Microbiology Research Team, Ethiopian Public Health Institute, Addis Ababa, Ethiopia.
2 Gondar University, Gondar, School of Biomedical and Laboratory Sciences, Ethiopia.
3 Department of Microbial, Cellular and Molecular Biology, Addis Ababa University, Ethiopia.
4 Department of Medical Laboratory Science, College of Health Sciences, Addis Ababa. University, Ethiopia.
5 Clinical Bacteriology and Mycology Reference Laboratory, Ethiopian Public Health Institute, Ethiopia.
10.22126/arww.2024.9527.1305
Abstract
A total of 114 samples collected from hospital wastewaters and rivers in Addis Ababa, Ethiopia were tested for non-sorbitol fermenting bacteria and coliphages. Sorbitol MacConkey agar is mainly used in the detection of E. coli O157:H7. However, other emerging diarrhoeagenic enteropathogens such as Plesiomonas shigelloides, Edwardsiella tarda, Providencia alcalifaciens, Escherichia albertii, Escherichia vulneris and Escherichia fergusonii were detected in the samples using this medium. Information for most of the emerging enteropathogens is scarce in most countries including Ethiopia. A total of 20 different genera, 38 species of non-sorbitol fermenting bacteria were isolated. Escherichia coli O157 could not be detected from any of the samples. All these backgrounds may mask the detection of Escherichia coli O157. Even if sorbitol MacConkey agar has several background limitations, different emerging diarrhoeagenic non-sorbitol fermenting bacteria were detected in the majority of the rivers and hospitals` wastewaters samples. The correlation between coliphages and non-sorbitol fermenting bacteria were not significant. As several bacteria have been isolated on sorbitol MacConkey agar medium, it is essential that the most selective laboratory techniques will be desired for outbreak investigation of E. coli O157, but other non-sorbitol fermenting enteropathogens should also be detected using sorbitol MacConkey agar in low resources countries.
Keywords
Ammon, A., Petersen, L. R., and Karch, H. (1999) ‘A large outbreak of hemolytic uremic syndrome caused by an unusual sorbitol-fermenting strain of Escherichia coli O157: H’, The Journal of Infectious Diseases, 179, pp. 1274–1277. doi: https://doi.org/10.1086/314715
Baek, S. D., Chun, C., and Hong, K. S. (2019) ‘Hemolytic uremic syndrome caused by Escherichia fergusonii infection’, Kidney Research and Clinical Practice, 38(2), pp. 253–255. doi: https://doi.org/10.23876/j.krcp.19.012
Boisen, N. et al. (2015) ‘Shiga toxin 2a and enteroaggregative Escherichia coli – a deadly combination’, Gut Microbes, 6(4), pp. 272–278. doi: https://doi.org/ 10.1080/19490976.2015.1054591
Bonetta, S et al. (2016) ‘Detection of pathogenic Campylobacter, E. coli O15: H7 and Salmonella spp. in wastewater by PCR assay’, Environmental Science and Pollution Research, 23(15), pp. 15302–15309. doi: https://doi.org/10.1007/s11356-016-6682-5
Brenden, R. A., Miller, M. A., and Janda, J. M. (1988) ‘Clinical disease spectrum and pathogenic factors associated with Plesiomonas shigelloides infections in humans’, Reviews of Infectious Diseases, 10(2), pp. 303–316. doi: https://doi.org/10.1093/clinids/10.2.303
Campos, C. et al. (2019) ‘Aptness of Escherichia coli host strain CB390 to detect total coliphages in Colombia’, Scientific Reports, 9(40), pp. 9246. doi: https://doi.org/10.1038/s41598-019-45775-y
Canizalez-Roman, A. et al. (2013) ‘Prevalence and antibiotic resistance profiles of diarrheagenic Escherichia coli strains isolated from food items in northwestern Mexico’, International Journal of Food Microbiology, 164(1), pp. 36–45. doi: https://doi.org/ 10.1016/j.ijfoodmicro.2013.03.020
Canizalez-Roman, A. et al. (2019) ‘Detection of antimicrobial-resistance diarrheagenic Escherichia coli strains in surface water used to irrigate food products in the northwest of Mexico’, International Journal of Food Microbiology, 304, pp. 1–10. doi: https://doi.org/10.1016/j.ijfoodmicro.2019.05.017
Cao, Y. et al. (2019) ‘Molecular monitoring of disinfection efficacy of E . coli O157: H7 in bottled purified drinking water by quantitative PCR with a novel dye’, Journal of Food Processing and Preservation, 43(2), pp. 13875. doi: https://doi.org/10.1111/jfpp.13875
Chapman, P. A. et al. (1991) ‘An improved selective medium for the isolation of Escherichia coli 0 157’, Journal of Medical Microbiology, 35, pp. 107–110. doi: https://doi.org/ 10.1099/00222615-35-2-107
Chapman, P. A. (2000) ‘Methods available for the detection of Escherichia coli O157 in clinical, food and environmental samples’, World Journal of Microbiology and Biotechnology, 16, pp. 733-740. doi: https://doi.org/ 10.1023/A:1008985008240
Chen, X. et al. (2013) ‘Plesiomonas shigelloides infection in Southeast China’, Plos One, 8(11), pp. e77877. doi: https://doi.org/10.1371/journal.pone.0077877
Croxen, M. A. et al. (2013) ‘Recent advances in understanding enteric pathogenic Escherichia coli’, Clinical Microbiology Reviews, 26(4), pp. 822–880. doi: https://doi.org/10.1128/CMR.00022-13
Durso, L. et al. (2013) `Primary isolation of shiga toxigenic Escherichia coli from environmental sources quality`, Journal of Environmental Quality, 42(5), pp. 1295-307. doi: https://doi.org/10.2134/jeq2013.02.0035
Ewuoso, L. M. et al. (2019) ‘Virulence factors and antibiotic resistance of Escherichia coli O157:H7 isolated from Ogun river, Abeokuta metropolis, Nigeria’, Applied Environmental Research, 41(1), pp. 22–30. doi: https://doi.org/10.35762/AER.2019.41.1.3
Garci, C., and Blanch, A. R. (2006) ‘Occurrence of Escherichia coli O157: H7 and other enterohemorrhagic Escherichia coli in the environment’, Environmental Science Technology, 40, pp. 7141–7149. doi: https://doi.org/ 10.1021/es060927k
Gould, L. H. et al. (2012) ‘Update: recommendations for diagnosis of shiga toxin-producing Escherichia coli infections by clinical laboratories’, Clinical Microbiology Newsletter, 34(10), pp. 75–83. doi: https://doi.org/10.1016/j.clinmicnews.2012.04.004
Guzman-Herrador B. et al. (2012) ‘Waterborne outbreaks in the Nordic countries, 1998 to 2012’, Eurosurveillance, 20(24), pp. 1–10. doi: https://doi.org/10.2807/1560-7917.ES2015.20.24.21160
Hirai, Y., Asahata-tago, S., and Ainoda, Y. (2015) ‘Edwardsiella tarda bacteremia. A rare but fatal water and foodborne infection: review of the literature and clinical cases from a single centre’, Canadian Journal of Infectious Diseases and Medical Microbiology, 26(6), pp. 313–318. doi: https://doi.org/ 10.1155/2015/702615
Humphries, R. M., and Linscott, J. (2015) ‘Laboratory diagnosis of bacterial gastroenteritis’, Clinical Microbiology Review, 28(1), pp. 3–31. doi: https://doi.org/10.1128/CMR.00073-14
Hussein, A. et al. (2019) ‘Validity of a single antibody-based lateral flow immunoassay depending on graphene oxide for highly sensitive determination of E. coli O157: H7 in minced beef and river water’, Food Chemistry, 297, pp. 124965. doi: https://doi.org/10.1016/j.foodchem.2019.124965
Hyma, K. E. et al. (2005) ‘Evolutionary genetics of a new pathogenic Escherichia species: Escherichia albertii and related Shigella boydii strains’, Journal of Bacteriology, 187(2), pp. 619–628. doi: https://doi.org/10.1128/JB.187.2.619
Iijima, Y. et al. (2017) ‘High prevalence of diarrheagenic Escherichia coli among children with diarrhea in Kenya’, Japanese Journal of Infectious Diseases, 70, pp. 80–83. doi: https://doi.org/ 10.7883/yoken.JJID.2016.064 Islam, M. M., Sokolova, E., and Hofstra, N. (2018) ‘Modelling of river faecal indicator bacteria dynamics as a basis for faecal contamination reduction’, Journal of Hydrology, 563, pp. 1000–1008. doi: https://doi.org/ 10.1016/j.jhydrol.2018.06.077
Jain, S. et al. (2016) ‘Escherichia vulneris: an unusual cause of complicated diarrhoea and sepsis in an infant. A case report and review of literature’, New Microbes and New Infections, 13, pp. 83–86. doi: https://doi.org/10.1016/j.nmni.2016.07.002
Janda, J., and Abbott, S. (2011) ‘Revisiting bacterial gastroenteritis, part I: issues, possible approaches, and an ever-expanding list of etiologic agents’, Clinical Microbiology Newsletter, 33(10), pp. 71–76. doi: https://doi.org/10.1016/j.clinmicnews.2011.04.002
Janda, J. M., Abbott, S. L., and Mciver, J. (2016) ‘Plesiomonas shigelloides revisited’, Clinical Microbiology Reviews, 29(2), pp. 349–374. doi: https://doi.org/10.1128/CMR.00103-15
Jofre, J. et al. (2016) ‘Coliphages as model organisms in the characterization and management of water resources’, Water, 8(5), pp. 199. doi: https://doi.org/10.3390/w8050199
Karch, H. et al. (1993) ‘Clonal structure and pathogenicity of shiga-like toxin-producing, sorbitol-fermenting Escherichia coli O157:H, Journal of Clinical Microbiology, 31(5), pp. 1200–1205. doi: https://doi.org/10.1128/jcm.31.5.1200-1205.1993
Kelly, P. (2011) ‘Diarrhoeal disease’, Clinical Medicine, 11(5), pp. 488–491. doi: https://doi.org/ 10.7861/clinmedicine.11-5-488
Kristiani, M. et al. (2019) ‘Detection of Escherichia coli O157: H7 and shiga toxin 2a gene in pork, pig feces, and clean water at Jagalan slaughterhouse in Surakarta, Central Java Province, Indonesia’, Veterinary World, 12(10), pp. 1584–1590. doi: https://doi.org/10.14202/vetworld.2019.1584-1590
LeJeune, J. et al. (2001) ‘Methods for the isolation of water-borne Escherichia coli O157’, Letters in Applied Microbiology, 32(5), pp. 316–320. doi: https://doi.org/10.1046/j.1472-765X.2001.00905.x
Limaheluw, J., Medema, G., and Hofstra, N. (2019) ‘An exploration of the disease burden due to Cryptosporidium in consumed surface water for sub-Saharan Africa’, International Journal of Hygiene and Environmental Health, 222(5), pp. 856–863. doi: https://doi.org/10.1016/j.ijheh.2019.04.004
Liu, J. et al. (2016) ‘Viable but non-culturable state and toxin gene expression of enterohemorrhagic Escherichia coli O157 under cryopreservation’, Research in Microbiology, 168(3), pp. 188–193. doi: https://doi.org/10.1016/j.resmic.2016.11.002
Lupindu, A. et al. (2016) ‘Occurrence and characterization of shiga toxin-producing Escherichia coli O157:H7 and other non-sorbitol–fermenting E. coli in cattle and humans in urban areas of Morogoro, Tanzani’, Foodborne Pathogens and Disease, 11, pp. 6. doi: https://doi.org/10.1089/vbz.2013.1502
Lupindu, A. M. (2018) ‘Epidemiology of shiga toxin-producing Escherichia coli O157: H7 in Africa in review’, Southern African Journal of Infectious Diseases, 33(1), pp. 24–30. doi: https://doi.org/10.1080/23120053.2017.1376558
Luther, A. et al. (2016) ‘Quantitative microbial risk assessment (QMRA) shows increased public health risk associated with exposure to river water under conditions of riverbed sediment resuspension’, Science of the Total Environment, 566–567, pp. 1143–1151. doi: https://doi.org/ 10.1016/j.scitotenv.2016.05.155
Mahapatra, A., and Mahapatra, S. (2005) ‘Escherichia fergusonii: an emerging pathogen in South Orissa’, Indian Journal of Medical Microbiology, 23(3), pp. 204–208. doi: https://doi.org/10.4103/0255-0857.16598
Maheux, A. F. et al. (2014) ‘Characterization of Escherichia fergusonii and Escherichia albertii isolated from water’, Journal of Applied Microbiology, 117, pp. 597–609. doi: https://doi.org/10.1111/jam.12551
March, S. B., and Ratnam, S. (1986) ‘Sorbitol-MacConkey medium for detection of Escherichia coli 0157: H7 associated with hemorrhagic colitis’, Journal of clinical microbiology, 23(5), pp. 869–872. doi: https://doi.org/10.1128/jcm.23.5.869-872.1986
Mcminn, B. R. et al. (2017) ‘Bacteriophages as indicators of fecal pollution and enteric virus removal’, Letter of Applied Microbiology, 65(1), pp. 11–26. doi: https://doi.org/10.1111/lam.12736
Michael, J. et al (2021) `The changing face of the family Enterobacteriaceae (order: “Enterobacterales”): new members, taxonomic issues, geographic expansion, and new diseases and disease syndromes, Clinical Microbiology Review, 34, pp. e00174-20. doi: https://doi.org/ 10.1128/CMR.00174-20
Marejková M. (2013) `enterohemorrhagic Escherichia coli as causes of hemolytic uremic syndrome in the Czech Republic`, PLOS ONE, 8, pp. e73927. doi: https://doi.org/ 10.1371/journal.pone.0073927
Mullan, G. D., Dueker, M. E., and Juhl, A. R. (2017) ‘Challenges to managing microbial fecal pollution in Coastal environments: extra-enteric ecology and microbial exchange among water, aediment, and air’, Current Pollution Report, 3, pp. 1–16. doi: https://doi.org/10.1007/s40726-016-0047-z
Müller, E., and Ehlers, M. (2005) ‘Biolog identification of non-sorbitol fermenting bacteria isolated on E. coli O157 selective CT-SMAC agar’, Water, 31(2), pp. 247–252. doi: https://doi.org/ 10.4314/wsa.v31i2.5191 Murray, R. P. et al. (eds.) (2007) Post mortem: Solving history’s great medical mysteries. 9th edn. Washington: ASM.
Myataza, A. et al. (2017) ‘Incidence and antimicrobial susceptibility of Escherichia coli O157: H7 isolates recovered from dairy farms in Amathole district municipality, Eastern Cape, South Africa’, Asian Pacific Journal of Tropical Disease, 7(12), pp. 765–770. doi: https://doi.org/10.12980/apjtd.7.2017D7-198
Namdari, A. (1985) ‘Detection of Escherichia albertii in urinary and gastrointestinal infections in Kermanshah, Iran’, International Journal of Enteric Pathogens, pp. 1–14. doi: https://doi.org/ 10.34172/ijep.2021.08
Ngwa, G. A. et al. (2013) ‘Detection and enumeration of E. coli O157: H7 in water samples by culture and molecular methods’, Journal of Microbiological Methods, 92(2), pp. 164–172. doi: https://doi.org/10.1016/j.mimet.2012.11.018
Nimmervoll, H. et al. (2014) ‘Septicaemia caused by Edwardsiella tarda and Plesiomonas shigelloides in captive penguin chicks’, SAT Schweizer Archiv für Tierheilkunde, 153(3), pp. 117–121. doi: https://doi.org/10.1024/0036-7281/
Noveir, M. R. and Halkman, A. K. (2000) ‘A Study on selective broths and agar media for the Isolation of Escherichia coli O157: H7 serotype’, Turkish Journal of Veterinary and Animal Sciences, 24, pp. 459–464. Available at: https://journals.tubitak.gov.tr/veterinary/vol24/iss5/7/ (Accessed: 8 April 2024).
Nezami, S. et al. (2023) `Assessing the suitability of river water quality using water quality indices: a case study on Balikhlou river in northwest of Iran, Iran', Journal of Applied Research in Water and Wastewater, 10 (1), pp. 1-6. doi: https://doi.org/ 10.22126/ARWW.2022.7574.1239
Odero, J. et al. (2023) `Changes in water quality parameters along Thika river sub-catchment, upper Tana, Kenya`, Journal of Applied Research in Water and Wastewater, 10, PP. 48-55. doi: https://doi.org/ 10.22126/arww.2023.9078.1288
Onyemelukwe, N. (2014) ‘Plesiomonas shigelloides diarrhea in Enugu area of south eastern Nigeria: incidence, clinical and epidemiological features’, Journal of Dental and Medical Sciences, 13(4), pp. 68–73. doi: https://doi.org/10.9790/0853-13426873
Osuolale, O. et al. (2018) `Investigating the occurrence of E. coli O157:H7 in the final effluents of two wastewater treatment plants`, BioRxiv, pp.1-15. doi: https://doi.org/ 10.1101/161737
Yinur, D, et al ((2023) `Loop mediated isothermal amplification as a molecular diagnostic assay: application and evaluation for detection of enterohaemorrhagic Escherichia coli (O157:H7)’, Practical Laboratory Medicine, 37, pp. e00333. doi: https://doi.org/10.1016/j.plabm.2023.e00333
Ooka, T. (2013) ‘Human gastroenteritis outbreak associated with Escherichia albertii, Japan’, Emerging Infectious Diseases, 19(1), pp. 1–3. doi: https://doi.org/ 10.3201/eid1901.120646
Ori, E. L. et al. (2019) ‘Diarrhoeagenic Escherichia coli and Escherichia albertii in Brazil: pathotypes and serotypes over a 6-year period of surveillance’, Epidemiology and Infection, 147, pp.1–9. doi: https://doi.org/10.1017/S0950268818002595
Pan, D. et al. (2020) 'Efficiency evaluation of urban wastewater treatment: evidence from 113 cities in the Yangtze river economic belt of China` Journal of Environmental Management, 270, pp. 110940. doi: https://doi.10.1016/j.jenvman.2020.110940
Pence, M. A. (2016) ‘Wound infection with Plesiomonas shigelloides following a freshwater injury’, Journal of Clinical Microbiology, 54(5), pp. 1180–1182. doi: https://doi.org/10.1128/JCM.02652
Rice, E. W. et al. (1995) ‘Detection of Escherichia coli in water using a colorimetric gene probe assay’, Journal of Environmental Science and Health, 30(5), pp. 1059–1067. doi: https://doi.org/10.1080/10934529509376249
Schlenker, C., Fellow, S., and Surawicz, C. M. (2009) ‘Best practice & research clinical gastroenterology emerging infections of the gastrointestinal tract’, Best Practice and Research Clinical Gastroenterology, 23(1), pp. 89–99. doi: https://doi.org/10.1016/j.bpg.2008.11.014
Seng, P. et al. (2016) ‘Emerging role of Raoultella ornithinolytica in human infections: a series of cases and review of the literature’, International Journal of Infectious, Diseases, 45, pp. 65–71. doi: https://doi.org/10.1016/j.ijid.2016.02.014
Shah, M. M. et al. (2015) ‘First report of a foodborne Providencia alcalifaciens outbreak in Kenya’, American Journal of Tropical Medicine and Hygen, 93(3), pp. 497–500. doi: https://doi.org/10.4269/ajtmh.15-0126
Smith, H. R. et al. (1987) ‘Haemorrhagic colitis and verocytotoxin-producing Escherichia coli in England and Wales’, The Lancet, 329(8541), pp. 1062–1065. doi: https://doi.org/10.1016/S0140-6736(87)90485-5
Sobsey, M. D. (2014) Comparison of single-agar layer and two-step enrichment spot plate methods in the detection of somatic and male specific coliphages in NC type II reclaimed water samples. MSc thesis. University of North Carolina. Available at: https://cdr.lib.unc.edu/concern/masters_papers/vd66w184v (Accessed: 8 April 2024).
Tânia, T. et al. (2020) `Escherichia albertii pathogenesis`, EcoSal Plus, 25, pp. 1296-1307. doi: https://doi.org/10.2134/jeq2013.02.0035
Tseng, H. et al. (2020) ‘Characteristics of Plesiomonas shigelloides infection in Taiwan’, Journal of Microbiology, Immunology and Infection, 34(1), pp. 47–52. doi: https://doi.org/10.17615/ffb6-7b96
Tsiraki, M. I. et al. (2018) ‘Viability of and Escherichia coli O157: H7 and Listeria monocytogenes in a delicatessen appetizer (yogurt-based ) salad as affected by citrus extract (Citrox ©) and storage temperature’, Food Microbiology, 69, pp. 11–17. doi: 1. doi: https://doi.org/ 10.1016/j.fm.2017.07.014
U.S. Environmental Protection Agency. (2001) Method 1602: Male-specific (F_) and somatic coliphage in water by single agar layer (SAL) procedure. Washington: U.S. Environmental Protection Agency.
Uddin, M. et al. (2019) ‘Identification of pathogenic Escherichia coli strain from river and sewage water in Bangladesh’, Archives of Agriculture and Environmental Scienc, 4(1), pp. 39–44. doi: https://doi.org/ 10.26832/24566632.2019.040106
Urška-Rozman, U. et al. (2020) `Hospital wastewater effluent: hot spot for antibiotic resistant bacteria`, Journal of Water, Sanitation and Hygiene for Development, 10(2), pp. 171-178. doi: https://doi.org/10.2166/washdev.2020.086
Walker, C. W., Upson, R., and Warren, R. E. (1988) ‘Haemorrhagic colitis: detection of verotoxin producinrg Escherichia coli 0157 in a clinical microbiology laboratory’, Journal of Clinical Pathology, 41, pp. 80–84. doi: https://doi.org/ 10.1136/jcp.41.1.80
Wanjugi, P. et al. (2016) ‘Differential decomposition of bacterial and viral fecal indicators in common human pollution types’, Water Research, 105, pp. 591–601. doi: https://doi.org/ 10.1016/j.watres.2016.09.041
World Health Organization. (2011) Guidelines for drinking-water quality. 4th edn. Switzerland: Switzerland: WHO.
Yakubu, Y. et al. (2018) ‘Risk of shiga toxigenic Escherichia coli O157: H7 infection from raw and fermented milk in Sokoto metropolis, Nigeria’, Journal of Pathogens, 2018, pp. 1–5. doi: https://doi.org/ 10.1155/2018/8938597
Yu, D. et al. (2021) `A review of the taxonomy, genetics, and biology of the genus Escherichia and the type species Escherichia coli`, Canadia Journal of Microbiology, 67, pp. 553–571. doi: https://doi.org/ 10.1139/cjm-2020-0508
Zhang, X. H. et al. (2020) ‘Viable but non-culturable bacteria and their resuscitation: implications for cultivating uncultured marine microorganisms’, Marine Life Science and Technology, 5, pp. 13. doi: https://doi.org/10.1007/s42995-020-00041-3
Baek, S. D., Chun, C., and Hong, K. S. (2019) ‘Hemolytic uremic syndrome caused by Escherichia fergusonii infection’, Kidney Research and Clinical Practice, 38(2), pp. 253–255. doi: https://doi.org/10.23876/j.krcp.19.012
Boisen, N. et al. (2015) ‘Shiga toxin 2a and enteroaggregative Escherichia coli – a deadly combination’, Gut Microbes, 6(4), pp. 272–278. doi: https://doi.org/ 10.1080/19490976.2015.1054591
Bonetta, S et al. (2016) ‘Detection of pathogenic Campylobacter, E. coli O15: H7 and Salmonella spp. in wastewater by PCR assay’, Environmental Science and Pollution Research, 23(15), pp. 15302–15309. doi: https://doi.org/10.1007/s11356-016-6682-5
Brenden, R. A., Miller, M. A., and Janda, J. M. (1988) ‘Clinical disease spectrum and pathogenic factors associated with Plesiomonas shigelloides infections in humans’, Reviews of Infectious Diseases, 10(2), pp. 303–316. doi: https://doi.org/10.1093/clinids/10.2.303
Campos, C. et al. (2019) ‘Aptness of Escherichia coli host strain CB390 to detect total coliphages in Colombia’, Scientific Reports, 9(40), pp. 9246. doi: https://doi.org/10.1038/s41598-019-45775-y
Canizalez-Roman, A. et al. (2013) ‘Prevalence and antibiotic resistance profiles of diarrheagenic Escherichia coli strains isolated from food items in northwestern Mexico’, International Journal of Food Microbiology, 164(1), pp. 36–45. doi: https://doi.org/ 10.1016/j.ijfoodmicro.2013.03.020
Canizalez-Roman, A. et al. (2019) ‘Detection of antimicrobial-resistance diarrheagenic Escherichia coli strains in surface water used to irrigate food products in the northwest of Mexico’, International Journal of Food Microbiology, 304, pp. 1–10. doi: https://doi.org/10.1016/j.ijfoodmicro.2019.05.017
Cao, Y. et al. (2019) ‘Molecular monitoring of disinfection efficacy of E . coli O157: H7 in bottled purified drinking water by quantitative PCR with a novel dye’, Journal of Food Processing and Preservation, 43(2), pp. 13875. doi: https://doi.org/10.1111/jfpp.13875
Chapman, P. A. et al. (1991) ‘An improved selective medium for the isolation of Escherichia coli 0 157’, Journal of Medical Microbiology, 35, pp. 107–110. doi: https://doi.org/ 10.1099/00222615-35-2-107
Chapman, P. A. (2000) ‘Methods available for the detection of Escherichia coli O157 in clinical, food and environmental samples’, World Journal of Microbiology and Biotechnology, 16, pp. 733-740. doi: https://doi.org/ 10.1023/A:1008985008240
Chen, X. et al. (2013) ‘Plesiomonas shigelloides infection in Southeast China’, Plos One, 8(11), pp. e77877. doi: https://doi.org/10.1371/journal.pone.0077877
Croxen, M. A. et al. (2013) ‘Recent advances in understanding enteric pathogenic Escherichia coli’, Clinical Microbiology Reviews, 26(4), pp. 822–880. doi: https://doi.org/10.1128/CMR.00022-13
Durso, L. et al. (2013) `Primary isolation of shiga toxigenic Escherichia coli from environmental sources quality`, Journal of Environmental Quality, 42(5), pp. 1295-307. doi: https://doi.org/10.2134/jeq2013.02.0035
Ewuoso, L. M. et al. (2019) ‘Virulence factors and antibiotic resistance of Escherichia coli O157:H7 isolated from Ogun river, Abeokuta metropolis, Nigeria’, Applied Environmental Research, 41(1), pp. 22–30. doi: https://doi.org/10.35762/AER.2019.41.1.3
Garci, C., and Blanch, A. R. (2006) ‘Occurrence of Escherichia coli O157: H7 and other enterohemorrhagic Escherichia coli in the environment’, Environmental Science Technology, 40, pp. 7141–7149. doi: https://doi.org/ 10.1021/es060927k
Gould, L. H. et al. (2012) ‘Update: recommendations for diagnosis of shiga toxin-producing Escherichia coli infections by clinical laboratories’, Clinical Microbiology Newsletter, 34(10), pp. 75–83. doi: https://doi.org/10.1016/j.clinmicnews.2012.04.004
Guzman-Herrador B. et al. (2012) ‘Waterborne outbreaks in the Nordic countries, 1998 to 2012’, Eurosurveillance, 20(24), pp. 1–10. doi: https://doi.org/10.2807/1560-7917.ES2015.20.24.21160
Hirai, Y., Asahata-tago, S., and Ainoda, Y. (2015) ‘Edwardsiella tarda bacteremia. A rare but fatal water and foodborne infection: review of the literature and clinical cases from a single centre’, Canadian Journal of Infectious Diseases and Medical Microbiology, 26(6), pp. 313–318. doi: https://doi.org/ 10.1155/2015/702615
Humphries, R. M., and Linscott, J. (2015) ‘Laboratory diagnosis of bacterial gastroenteritis’, Clinical Microbiology Review, 28(1), pp. 3–31. doi: https://doi.org/10.1128/CMR.00073-14
Hussein, A. et al. (2019) ‘Validity of a single antibody-based lateral flow immunoassay depending on graphene oxide for highly sensitive determination of E. coli O157: H7 in minced beef and river water’, Food Chemistry, 297, pp. 124965. doi: https://doi.org/10.1016/j.foodchem.2019.124965
Hyma, K. E. et al. (2005) ‘Evolutionary genetics of a new pathogenic Escherichia species: Escherichia albertii and related Shigella boydii strains’, Journal of Bacteriology, 187(2), pp. 619–628. doi: https://doi.org/10.1128/JB.187.2.619
Iijima, Y. et al. (2017) ‘High prevalence of diarrheagenic Escherichia coli among children with diarrhea in Kenya’, Japanese Journal of Infectious Diseases, 70, pp. 80–83. doi: https://doi.org/ 10.7883/yoken.JJID.2016.064 Islam, M. M., Sokolova, E., and Hofstra, N. (2018) ‘Modelling of river faecal indicator bacteria dynamics as a basis for faecal contamination reduction’, Journal of Hydrology, 563, pp. 1000–1008. doi: https://doi.org/ 10.1016/j.jhydrol.2018.06.077
Jain, S. et al. (2016) ‘Escherichia vulneris: an unusual cause of complicated diarrhoea and sepsis in an infant. A case report and review of literature’, New Microbes and New Infections, 13, pp. 83–86. doi: https://doi.org/10.1016/j.nmni.2016.07.002
Janda, J., and Abbott, S. (2011) ‘Revisiting bacterial gastroenteritis, part I: issues, possible approaches, and an ever-expanding list of etiologic agents’, Clinical Microbiology Newsletter, 33(10), pp. 71–76. doi: https://doi.org/10.1016/j.clinmicnews.2011.04.002
Janda, J. M., Abbott, S. L., and Mciver, J. (2016) ‘Plesiomonas shigelloides revisited’, Clinical Microbiology Reviews, 29(2), pp. 349–374. doi: https://doi.org/10.1128/CMR.00103-15
Jofre, J. et al. (2016) ‘Coliphages as model organisms in the characterization and management of water resources’, Water, 8(5), pp. 199. doi: https://doi.org/10.3390/w8050199
Karch, H. et al. (1993) ‘Clonal structure and pathogenicity of shiga-like toxin-producing, sorbitol-fermenting Escherichia coli O157:H, Journal of Clinical Microbiology, 31(5), pp. 1200–1205. doi: https://doi.org/10.1128/jcm.31.5.1200-1205.1993
Kelly, P. (2011) ‘Diarrhoeal disease’, Clinical Medicine, 11(5), pp. 488–491. doi: https://doi.org/ 10.7861/clinmedicine.11-5-488
Kristiani, M. et al. (2019) ‘Detection of Escherichia coli O157: H7 and shiga toxin 2a gene in pork, pig feces, and clean water at Jagalan slaughterhouse in Surakarta, Central Java Province, Indonesia’, Veterinary World, 12(10), pp. 1584–1590. doi: https://doi.org/10.14202/vetworld.2019.1584-1590
LeJeune, J. et al. (2001) ‘Methods for the isolation of water-borne Escherichia coli O157’, Letters in Applied Microbiology, 32(5), pp. 316–320. doi: https://doi.org/10.1046/j.1472-765X.2001.00905.x
Limaheluw, J., Medema, G., and Hofstra, N. (2019) ‘An exploration of the disease burden due to Cryptosporidium in consumed surface water for sub-Saharan Africa’, International Journal of Hygiene and Environmental Health, 222(5), pp. 856–863. doi: https://doi.org/10.1016/j.ijheh.2019.04.004
Liu, J. et al. (2016) ‘Viable but non-culturable state and toxin gene expression of enterohemorrhagic Escherichia coli O157 under cryopreservation’, Research in Microbiology, 168(3), pp. 188–193. doi: https://doi.org/10.1016/j.resmic.2016.11.002
Lupindu, A. et al. (2016) ‘Occurrence and characterization of shiga toxin-producing Escherichia coli O157:H7 and other non-sorbitol–fermenting E. coli in cattle and humans in urban areas of Morogoro, Tanzani’, Foodborne Pathogens and Disease, 11, pp. 6. doi: https://doi.org/10.1089/vbz.2013.1502
Lupindu, A. M. (2018) ‘Epidemiology of shiga toxin-producing Escherichia coli O157: H7 in Africa in review’, Southern African Journal of Infectious Diseases, 33(1), pp. 24–30. doi: https://doi.org/10.1080/23120053.2017.1376558
Luther, A. et al. (2016) ‘Quantitative microbial risk assessment (QMRA) shows increased public health risk associated with exposure to river water under conditions of riverbed sediment resuspension’, Science of the Total Environment, 566–567, pp. 1143–1151. doi: https://doi.org/ 10.1016/j.scitotenv.2016.05.155
Mahapatra, A., and Mahapatra, S. (2005) ‘Escherichia fergusonii: an emerging pathogen in South Orissa’, Indian Journal of Medical Microbiology, 23(3), pp. 204–208. doi: https://doi.org/10.4103/0255-0857.16598
Maheux, A. F. et al. (2014) ‘Characterization of Escherichia fergusonii and Escherichia albertii isolated from water’, Journal of Applied Microbiology, 117, pp. 597–609. doi: https://doi.org/10.1111/jam.12551
March, S. B., and Ratnam, S. (1986) ‘Sorbitol-MacConkey medium for detection of Escherichia coli 0157: H7 associated with hemorrhagic colitis’, Journal of clinical microbiology, 23(5), pp. 869–872. doi: https://doi.org/10.1128/jcm.23.5.869-872.1986
Mcminn, B. R. et al. (2017) ‘Bacteriophages as indicators of fecal pollution and enteric virus removal’, Letter of Applied Microbiology, 65(1), pp. 11–26. doi: https://doi.org/10.1111/lam.12736
Michael, J. et al (2021) `The changing face of the family Enterobacteriaceae (order: “Enterobacterales”): new members, taxonomic issues, geographic expansion, and new diseases and disease syndromes, Clinical Microbiology Review, 34, pp. e00174-20. doi: https://doi.org/ 10.1128/CMR.00174-20
Marejková M. (2013) `enterohemorrhagic Escherichia coli as causes of hemolytic uremic syndrome in the Czech Republic`, PLOS ONE, 8, pp. e73927. doi: https://doi.org/ 10.1371/journal.pone.0073927
Mullan, G. D., Dueker, M. E., and Juhl, A. R. (2017) ‘Challenges to managing microbial fecal pollution in Coastal environments: extra-enteric ecology and microbial exchange among water, aediment, and air’, Current Pollution Report, 3, pp. 1–16. doi: https://doi.org/10.1007/s40726-016-0047-z
Müller, E., and Ehlers, M. (2005) ‘Biolog identification of non-sorbitol fermenting bacteria isolated on E. coli O157 selective CT-SMAC agar’, Water, 31(2), pp. 247–252. doi: https://doi.org/ 10.4314/wsa.v31i2.5191 Murray, R. P. et al. (eds.) (2007) Post mortem: Solving history’s great medical mysteries. 9th edn. Washington: ASM.
Myataza, A. et al. (2017) ‘Incidence and antimicrobial susceptibility of Escherichia coli O157: H7 isolates recovered from dairy farms in Amathole district municipality, Eastern Cape, South Africa’, Asian Pacific Journal of Tropical Disease, 7(12), pp. 765–770. doi: https://doi.org/10.12980/apjtd.7.2017D7-198
Namdari, A. (1985) ‘Detection of Escherichia albertii in urinary and gastrointestinal infections in Kermanshah, Iran’, International Journal of Enteric Pathogens, pp. 1–14. doi: https://doi.org/ 10.34172/ijep.2021.08
Ngwa, G. A. et al. (2013) ‘Detection and enumeration of E. coli O157: H7 in water samples by culture and molecular methods’, Journal of Microbiological Methods, 92(2), pp. 164–172. doi: https://doi.org/10.1016/j.mimet.2012.11.018
Nimmervoll, H. et al. (2014) ‘Septicaemia caused by Edwardsiella tarda and Plesiomonas shigelloides in captive penguin chicks’, SAT Schweizer Archiv für Tierheilkunde, 153(3), pp. 117–121. doi: https://doi.org/10.1024/0036-7281/
Noveir, M. R. and Halkman, A. K. (2000) ‘A Study on selective broths and agar media for the Isolation of Escherichia coli O157: H7 serotype’, Turkish Journal of Veterinary and Animal Sciences, 24, pp. 459–464. Available at: https://journals.tubitak.gov.tr/veterinary/vol24/iss5/7/ (Accessed: 8 April 2024).
Nezami, S. et al. (2023) `Assessing the suitability of river water quality using water quality indices: a case study on Balikhlou river in northwest of Iran, Iran', Journal of Applied Research in Water and Wastewater, 10 (1), pp. 1-6. doi: https://doi.org/ 10.22126/ARWW.2022.7574.1239
Odero, J. et al. (2023) `Changes in water quality parameters along Thika river sub-catchment, upper Tana, Kenya`, Journal of Applied Research in Water and Wastewater, 10, PP. 48-55. doi: https://doi.org/ 10.22126/arww.2023.9078.1288
Onyemelukwe, N. (2014) ‘Plesiomonas shigelloides diarrhea in Enugu area of south eastern Nigeria: incidence, clinical and epidemiological features’, Journal of Dental and Medical Sciences, 13(4), pp. 68–73. doi: https://doi.org/10.9790/0853-13426873
Osuolale, O. et al. (2018) `Investigating the occurrence of E. coli O157:H7 in the final effluents of two wastewater treatment plants`, BioRxiv, pp.1-15. doi: https://doi.org/ 10.1101/161737
Yinur, D, et al ((2023) `Loop mediated isothermal amplification as a molecular diagnostic assay: application and evaluation for detection of enterohaemorrhagic Escherichia coli (O157:H7)’, Practical Laboratory Medicine, 37, pp. e00333. doi: https://doi.org/10.1016/j.plabm.2023.e00333
Ooka, T. (2013) ‘Human gastroenteritis outbreak associated with Escherichia albertii, Japan’, Emerging Infectious Diseases, 19(1), pp. 1–3. doi: https://doi.org/ 10.3201/eid1901.120646
Ori, E. L. et al. (2019) ‘Diarrhoeagenic Escherichia coli and Escherichia albertii in Brazil: pathotypes and serotypes over a 6-year period of surveillance’, Epidemiology and Infection, 147, pp.1–9. doi: https://doi.org/10.1017/S0950268818002595
Pan, D. et al. (2020) 'Efficiency evaluation of urban wastewater treatment: evidence from 113 cities in the Yangtze river economic belt of China` Journal of Environmental Management, 270, pp. 110940. doi: https://doi.10.1016/j.jenvman.2020.110940
Pence, M. A. (2016) ‘Wound infection with Plesiomonas shigelloides following a freshwater injury’, Journal of Clinical Microbiology, 54(5), pp. 1180–1182. doi: https://doi.org/10.1128/JCM.02652
Rice, E. W. et al. (1995) ‘Detection of Escherichia coli in water using a colorimetric gene probe assay’, Journal of Environmental Science and Health, 30(5), pp. 1059–1067. doi: https://doi.org/10.1080/10934529509376249
Schlenker, C., Fellow, S., and Surawicz, C. M. (2009) ‘Best practice & research clinical gastroenterology emerging infections of the gastrointestinal tract’, Best Practice and Research Clinical Gastroenterology, 23(1), pp. 89–99. doi: https://doi.org/10.1016/j.bpg.2008.11.014
Seng, P. et al. (2016) ‘Emerging role of Raoultella ornithinolytica in human infections: a series of cases and review of the literature’, International Journal of Infectious, Diseases, 45, pp. 65–71. doi: https://doi.org/10.1016/j.ijid.2016.02.014
Shah, M. M. et al. (2015) ‘First report of a foodborne Providencia alcalifaciens outbreak in Kenya’, American Journal of Tropical Medicine and Hygen, 93(3), pp. 497–500. doi: https://doi.org/10.4269/ajtmh.15-0126
Smith, H. R. et al. (1987) ‘Haemorrhagic colitis and verocytotoxin-producing Escherichia coli in England and Wales’, The Lancet, 329(8541), pp. 1062–1065. doi: https://doi.org/10.1016/S0140-6736(87)90485-5
Sobsey, M. D. (2014) Comparison of single-agar layer and two-step enrichment spot plate methods in the detection of somatic and male specific coliphages in NC type II reclaimed water samples. MSc thesis. University of North Carolina. Available at: https://cdr.lib.unc.edu/concern/masters_papers/vd66w184v (Accessed: 8 April 2024).
Tânia, T. et al. (2020) `Escherichia albertii pathogenesis`, EcoSal Plus, 25, pp. 1296-1307. doi: https://doi.org/10.2134/jeq2013.02.0035
Tseng, H. et al. (2020) ‘Characteristics of Plesiomonas shigelloides infection in Taiwan’, Journal of Microbiology, Immunology and Infection, 34(1), pp. 47–52. doi: https://doi.org/10.17615/ffb6-7b96
Tsiraki, M. I. et al. (2018) ‘Viability of and Escherichia coli O157: H7 and Listeria monocytogenes in a delicatessen appetizer (yogurt-based ) salad as affected by citrus extract (Citrox ©) and storage temperature’, Food Microbiology, 69, pp. 11–17. doi: 1. doi: https://doi.org/ 10.1016/j.fm.2017.07.014
U.S. Environmental Protection Agency. (2001) Method 1602: Male-specific (F_) and somatic coliphage in water by single agar layer (SAL) procedure. Washington: U.S. Environmental Protection Agency.
Uddin, M. et al. (2019) ‘Identification of pathogenic Escherichia coli strain from river and sewage water in Bangladesh’, Archives of Agriculture and Environmental Scienc, 4(1), pp. 39–44. doi: https://doi.org/ 10.26832/24566632.2019.040106
Urška-Rozman, U. et al. (2020) `Hospital wastewater effluent: hot spot for antibiotic resistant bacteria`, Journal of Water, Sanitation and Hygiene for Development, 10(2), pp. 171-178. doi: https://doi.org/10.2166/washdev.2020.086
Walker, C. W., Upson, R., and Warren, R. E. (1988) ‘Haemorrhagic colitis: detection of verotoxin producinrg Escherichia coli 0157 in a clinical microbiology laboratory’, Journal of Clinical Pathology, 41, pp. 80–84. doi: https://doi.org/ 10.1136/jcp.41.1.80
Wanjugi, P. et al. (2016) ‘Differential decomposition of bacterial and viral fecal indicators in common human pollution types’, Water Research, 105, pp. 591–601. doi: https://doi.org/ 10.1016/j.watres.2016.09.041
World Health Organization. (2011) Guidelines for drinking-water quality. 4th edn. Switzerland: Switzerland: WHO.
Yakubu, Y. et al. (2018) ‘Risk of shiga toxigenic Escherichia coli O157: H7 infection from raw and fermented milk in Sokoto metropolis, Nigeria’, Journal of Pathogens, 2018, pp. 1–5. doi: https://doi.org/ 10.1155/2018/8938597
Yu, D. et al. (2021) `A review of the taxonomy, genetics, and biology of the genus Escherichia and the type species Escherichia coli`, Canadia Journal of Microbiology, 67, pp. 553–571. doi: https://doi.org/ 10.1139/cjm-2020-0508
Zhang, X. H. et al. (2020) ‘Viable but non-culturable bacteria and their resuscitation: implications for cultivating uncultured marine microorganisms’, Marine Life Science and Technology, 5, pp. 13. doi: https://doi.org/10.1007/s42995-020-00041-3
)