Health  Vol.9 No.4 , April 2017
Screening of Bacterial and Fungal Biota Associated with Oreochromis niloticus in Lake Manzala and Its Impact on Human Health
In this study fish samples were investigated for Bacteria and Fungi, in fish parts, such as intestine, gills and skin. Bacterial counts of Total viable bacteria (T.V.B) reached more than 9.5 × 105 cfu and faecal coliforms (F.C) reached 1.2 × 105 cfu. Different species were identified, Using API technology. Escherichia coli comes first by being recording thirty number case of isolation constituting 36%, it followed by Proteus mirabilis which is represented by twenty four number case of isolation accounting for 30%. Other taxa viz: Klebsiella pneumonia, Citrobacter freundii, Providencia stuartii and Erwinia sp. came next according to their case number of isolation, they represented only by 7%. They showed different antibiotics with different inhibitory concentrations, resistance pattern to gentamycin 10 μg, Penicillin G, tetracycline 30 μg, Ampicillin 10 μg, Ampicillin 30 μg, chloramphenicol (C) 30 μg, Rifampicin 25 μg, Streptomycin 5 μg, cefotaxime 15 μg. Mycological investigation revealed the presence of variety of fungal species, particularly, toxigenic species, such as, Aspergillus spp, Penicillium spp and Fusarium spp. These results are indication of the spoilage of fishes which caught from Lake Manzala and are risky for human consumption and hazardous to human health in this important area of Egypt, due to the high pollution condition of Lake Manzala.
Cite this paper: Zaky, M. and Ibrahim, M. (2017) Screening of Bacterial and Fungal Biota Associated with Oreochromis niloticus in Lake Manzala and Its Impact on Human Health. Health, 9, 697-714. doi: 10.4236/health.2017.94050.

[1]   WRI (World Resources Institute) (1994) World Resources 1994-5. Oxford University Press, New York, 400.

[2]   Håstein, T., Hjeltnes, B., Lillehaug, A., Utne Skåre, J., Berntssen, M. and Lundebye, A.K. (2006) Food Safety Hazards That Occur during the Production Stage: Challenges for Fish Farming and the Fishing Industry. Revue Scientifique et Technique, 25, 607-625.

[3]   Hassan, A.H.M., Noor-El Deen, A.E., Galal, H.M., Sohad, M., Dorgham, M.A., Bakry, M.A. and Hakim, A.S. (2012) Further Characterization of Enterobacteriaceae Isolated from Cultured Freshwater Fish in Kafr El Shiek Governorate: Clinical, Biochemical and Histopathological Study with Emphasis on Treatment Trials. Global Veterinaria, 9, 617-629.

[4]   Zaky, M.M.M. and Salem, M.A.M. (2015) Environmental Factors Influencing Antibiotic Resistant Bacterial Pathogens in Polluted Lake Manzala, Egypt. Journal of Bacteriology & Parasitology, 6, Article ID: 1000249.

[5]   Trewavas, E. (1983) Tilapine Fishes of the Genera Sarotherodon, Oreochromis and Danakilia. Cornell University Press, Ithaca, NY.

[6]   Mur, R. (2014) Development of the Aquaculture Value Chain in Egypt. Report of the National Innovation Platform Workshop, Cairo, 19-20 February 2014.

[7]   Tahoun, S.A. (2007) Environmental Perspectives of the Port Said Area. Final Report of Plan of Action for an Integrated Coastal Zone Management in the Area of Port Said (Egypt), 230.

[8]   Ahmed, M., El Leithy, B., Thompson, J., Flower, R., Ramdani, M., Ayache, F. and Hassan, S. (2009) Application of Remote Sensing to Site Characterization and Environmental Change Analysis of North Africa Coastal Lagoons. Hydrobiologia, 622, 147-171.

[9]   Rabeh, S.A., Sabae, S.Z. and Abou El-Gheit, E.N. (2013) Microbiological Water Quality and Bacterial Infections among Tilapia Fish of Lake Manzala, Egypt. International Journal of Environment & Water, 2, 75-85.

[10]   Zaky, M.M., Salem, M., Persson, K.M. and Eslamian, S. (2011) Incidence of Aeromonas Species Isolated from Water and Fish Sources from Lake Manzala in Egypt. International Journal of Hydrology Science and Technology, 1, 47-62.

[11]   Cabral, P.S. (2010) Water Microbiology. Bacterial Pathogens and Water. International Journal of Environmental Research and Public Health, 7, 3658-3703.

[12]   Alam, M., Hasan, N.A., Sadique, A., Bhuiyan, N.A., Ahmed, K.U., Nusrin, S., Nair, G.B., Siddique, A.K., Sack, R.B., Sack, D.A., Huq, A. and Colwell, R.R. (2006) Seasonal Cholera Caused by Vibrio cholerae Serogroups O1 and O139 in the Coastal Aquatic Environment of Bangladesh. Applied Environmental Microbiology, 72, 4096-4104.

[13]   Pitlik, S., Berger, S.A. and Huminer, D. (1987) Nonenteric Infections Acquired through Contact with Water. Reviews of Infectious Diseases, 9, 54-63.

[14]   Arvanitidou, M., Kanellou, K. and Vagiona, D.G. (2005) Diversity of Salmonella spp. and Fungi in Northern Greek Rivers and Their Correlation to Fecal Pollution Indicators. Environmental Research, 99, 278-284.

[15]   Fadaeifard, F.F., Raissy, M., Bahrami, H., Rahimi, E. and Najafipoor, A. (2011) Freshwater Fungi Isolated from Eggs and Broodstocks with an Emphasis on Saprolegnia in Rainbow Trout Farms in West Iran. African Journal of Microbiology Research, 4, 3647-3651.

[16]   O’Brien, T.F. (2002) Emergence, Spread and Environmental Effect of Antimicrobial Resistance: How Use of an Antimicrobial Anywhere Can Increase Resistance to Any Antimicrobial Anywhere Else. Clinical Infectious Diseases, 34, S78-S84.

[17]   Weese, J.S., Blondeau, J.M., Boothe, D., Breitschwerdt, E.B., Guardabassi, L., Hillier, A., Lloyd, D.H., Papich, M.G., Rankin, S.C., Turnidge, J.D. and Sykes, J.E. (2011) Antimicrobial Use Guidelines for Treatment of Urinary Tract Disease in Dogs and Cats: Antimicrobial Guidelines Working Group of the International Society for Companion Animal Infectious Diseases. Veterinary Medicine International, 2011, Article ID: 263768.

[18]   Maclaren, J.F., Stevenson, M. and Kellogg, R. (1980) Lake Manzala Study. Aquaculture Site Selection Report, Ministry of Development and New Communities and United Nations Development Programme, Office of Projects Execution.

[19]   Fayed, D.B. (2004) Aspects of Manzalah Lake Pollution on Mugil Species. M.Sc. Thesis, Girls’ College, Ain Shams University, Cairo.

[20]   Fawole, M.O. and Oso, B.A. (2001) Laboratory Manual of Microbiology. Revised Edition, Spectrum Books, Ibadan.

[21]   Esther, A., Oramadike, C.E., Abraham-Olukayode, A.O. and Adejonwo, O.A. (2010) Bacteriological Quality of Street Vended Smoked Blue Whiting (Micromesistus poutasou). International Journal of Food Safety, 12, 122-126.

[22]   Bergey, D.H. and Holt, J.G. (1994) Bergey’s Manual of Determinative Bacteriology. 9th Edition, Williams & Wilkins, Baltimore, Maryland.

[23]   Treagan, L. and Pulliam, L. (1982) Medical Microbiology Procedures. W. B. Saunders Company, Toronto, Canada, 234-236.

[24]   Ólafsdóttir, G., Martinsdóttir, E., Oehlenschläger, J., Dalgaard, P., Jensen, B., Undeland, I., Mackie, I.M., Henehan, G., Nielsen, J. and Nielsen, H. (1997) Methods to Evaluate Fish Freshness in Research and Industry. Trends in Food Science and Technology, 8, 258-265.

[25]   American Public Health Association (APHA) (1995) Standard Methods for the Examination for Water and Wastewater. 19th Edition, Byrd Prepess Springfield, Washington DC.

[26]   Garrett, S.D. (1981) Soil Fungi and Soil Fertility. 2nd Edition, The Macmillan Company, Oxford, New York.

[27]   Smith, N.R. and Dawson, V.T. (1944) The Bacteriostatic Action of Rose Bengal in Media Used for the Plate Counts of Soil Fungi. Soil Science, 58, 467-471.

[28]   Pitt, J.I. (1980) The Genus Penicillium and Its Teleomorphic States Eupenicillium and Talaromyces. Academic Press, London, 634 p.

[29]   Raper, K.B. and Fennell, D.I. (1965) The Genus Aspergillus. Williams & Wilkins, Baltimore.

[30]   Ellis, M.B. (1971) Dematiaceous Hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey, England, 608.

[31]   Ellis, M.B. (1976) More dematiaceous hyphomycetes. Commonwealth Mycological Institute, Kew, Surrey, England, 507.

[32]   Booth, C. (1971) Fusarium, Laboratory Guide to the Identification of the Major Species. Commonwealth Mycological Institute, Kew, Surrey, England.

[33]   Domsch, K.H., Gams, W. and Anderson, T.H. (2007) Compendium of Soil Fungi. IHW-Verl, Eching, 672 p.

[34]   Guarro, J., Gene, J., Stchigel, A.M. and Figueras, M.J. (2012) Atlas of Soil Ascomycetes. Issue 10 of CBS Biodiversity Series, Holland.

[35]   CLSI, Ed. (2010) Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing: Twentieth Informational Supplement M100-S20. CLSI, Wayne, PA, USA.

[36]   Oteo, J.E., Lazaro, F.J., de Abajo, F.B. and Campos, J. (2005) Antimicrobial-Resistant Invasive Escherichia coli, Spain. Emerging Infectious Diseases, 11, 546-553.

[37]   Kumolu-Johnson, C.A. and Ndimele, P.E. (2011) A Review on Post-Harvest Losses in Artisanal Fisheries of Some African Countries. Journal of Fisheries and Aquatic Science, 6, 365-378.

[38]   Udeze, A.O., Talatu, M., Ezediokpu, M.N., Nmwanze, J.C., Onoh, C. and Ononko, I.O. (2012) The Effect of Klebsiella pneumoniae on Catfish (Clarias gariepinus). Researcher, 4, 51-59.

[39]   Saleh, A., Shawky, R., Sabae, Z. and Abou El-Gheit, E.N. (2013) Microbiological Water Quality and Bacterial Infections among Tilapia Fish of Lake Manzala, Egypt. International Journal of Environment & Water, 2, 75-85.

[40]   Elmossalami, M.K. (1997) Safety and Quality of Freshwater Crayfish (Procambarus clarkia)in the Nile River. Journal of Tropical Microbiology, 43, 126-128.

[41]   Gonzalez-Rodriguez, M.N., Sanz, J.J., Santos, J.A., Otero, A. and Garcia-Lopez, M.I. (2002) Numbers and Types of Microorganisms in Vacuum-Packed Cold-Smoked Freshwater Fish at the Retail Level. International Journal of Food Microbiology, 77, 161-168.

[42]   Tsai, Y.H., Kung, H.F., Lee, T.M., Lin, G.T. and Hwang, D.F. (2004) Histamine Related Hygienic Qualities and Bacteria Found in Popular Commercial Scombroid Fish Fillets in Taiwan. Journal of Food Protection, 67, 407-412.

[43]   Thampuran, N., Surendraraj, A. and Surendran, P.K. (2005) Prevalence and Characterization of Typical and Atypical Escherichia coli from Fish Sold at Retail in Cochin, India. Journal of Food Protection, 68, 2208-2211.

[44]   Arannilewa, S.T., Salawu, S.O., Sorungbe, A.A. and Ola-Salawu, B.B. (2006) Effect of Frozen Period on the Chemical, Microbiological and Sensory Quality of Frozen Tilapia fish (Sarotherodun galiaenus). Nutrition and Health, 18, 185-192.

[45]   Yagoub, S.O. (2009) Isolation of Enterobacteriaceae and Pseudomonas spp. from Raw Fish Sold in Fish Market in Khartoum State. Journal of Bacteriology Research, 1, 85-88.

[46]   Wogu, M.D. and Maduakol, M. (2010) Evaluation of Microbial Spoilage of Some Aqua Cultured Fresh Fish in Benin City Nigeria. Ethiopian Journal of Environmental Studies and Management, 3, 18-22.

[47]   Geldreich, E.E. and Clarke, N.A. (1966) Bacterial Pollution Indicators in the Intestinal Tract of Freshwater Fish. Applied Environmental Microbiology, 14, 429-437.

[48]   Mhango, M., Mpuchane, S.F. and Gashe, B.A. (2010) Incidence of Indicator Organisms, Opportunistic and Pathogenic Bacteria in Fish. African Journal of Food Agriculture Nutrition and Development, 10, 4202-4218.

[49]   Paleologos, E.K., Savvaidis, I.N. and Komtominas, M.G. (2004) Biogenic Amine Formation and Its Relation to Microbiological Sensory Attributes in Ice-Stored Whole Gutted and Filleted Mediterranean Sea Bass (Dicentrarchus labrax). International Journal of Food Microbiology, 21, 549-557.

[50]   Institute of Food Technologists (2004) Bacteria Associated with Foodborne Diseases. 1-25.

[51]   Green, H.C., Dick, L.K., Gilpin, B., Samadpour, M. and Field, K.G. (2012) Genetic Markers for Rapid PCR Based Identification of Gull, Canada Goose, Duck and Chicken Fecal Contamination in Water. Applied and Environmental Microbiology, 78, 503-510.

[52]   Mauffret, A., Caprais, M. and Gourmelon, M. (2012) Relevance of Bacteroidales and F-Specific RNA Bacteriophages for Efficient Fecal Contamination Tracking at the Level of a Catchment in France. Applied and Environmental Microbiology, 78, 5143-5152.

[53]   Da Costa, P.M., Loureiro, L., Augusto, J. and Matos, F. (2013) Transfer of Multidrug-Resistant Bacteria between Intermingled Ecological Niches: The Interface between Humans, Animals and the Environment. International Journal of Environmental Research and Public Health, 10, 278-294.

[54]   El-Sayed, Y.S.A. (1995) Mycological Studies on Locally Produced Smoked Fish with Special Reference to Toxigenic Strains. PhD Thesis, Zagazig University, Egypt.

[55]   Edris, A.M. (1996) Microbial Evaluation of Some Marketed Smoked Fish. Zagazig Zagazig Veterinary Journal, 24, 76-81.

[56]   Hashem, M. (2011) Isolation of Mycotoxin-Producing Fungi from Fishes Growing in Aquacultures. Research Journal of Microbiology, 6, 862-872.

[57]   Refai, M.K., Laila, A.M., Amany, K.M. and Shimaa, El-S.M.A. (2010) The Assessment of Mycotic Settlement of Freshwater Fishes in Egypt. Journal of American Science, 6, 595-602.

[58]   Junaid, S.A., Olauboin, F. and Olabode, A.O. (2010) Mycotic Contamination of Stock Fish Sold in Jos, Nigeria. Journal of Yeast and Fungal Research, 1, 136-141.

[59]   Shahbazian, N., Ebrahimzadeh Mousavi, H.A., Soltani, M., Khosravi, A.R., Mirzargar, S. and Sharifpour, I. (2010) Fungal Contamination in Rainbow Trout Eggs in Kermanshah Province Propagations with Emphasis on Saprolegniaceae. Iranian Journal of Fisheries Sciences, 9, 151-160.

[60]   Fayioye, O.O., Fagbohun, T.R. and Olubanjo, O.O. (2008) Fungal Infestation and Nutrient Quality of Traditionally Smoke-Dried Freshwater Fish. Turkish Journal of Fisheries and Aquatic Sciences, 8, 7-13.

[61]   Olufemi, B.E. (1983) The Aspergilli as Pathogens of Cultured Fishes. In: Munir, J.F. and Roberts, R.J., Eds., Recent Advances of Aquaculture, Springer, US, 193-217.

[62]   Crow, G.L., Brock, J.A. and Kaiser, S. (1995) Fusarium solani Fungal Infection of the Lateral Line Canal System in Captive Scalloped Hammerhead Sharks (Sphyra lewini) in Hawaii. Journal of Wildlife Diseases, 31, 562-565.

[63]   Wolf, J.C. and Smith, S.A. (1999) Systemic Zygomycosis in Farmed Tilapia Fish. Journal of Comparative Pathology, 121, 301-306.

[64]   Hussein, M.M., Hatai, K. and Nomura, T. (2001) Saprolegniasis in Salmonid and Their Eggs in Japan. Journal of Wildlife Diseases, 37, 204-207.

[65]   Shabana, Y.M. (2002) The Use of the Host Specific Fungus, Alternaria eichhorniae, for Biological Control of Water Hyacinth. The 2nd Conference on Biological Control of Pests in Egypt, International Center of Agriculture, Cairo, 180-212.

[66]   Ali-Shtayeh, M.S., Khaleel, T.Kh.M. and Jamous, R.M. (2002) Ecology of Dermatophytes and Other Keratinophylic Fungi in Swimming Pools and Polluted and Unpolluted Streams. Mycopathologia, 156, 103-205.

[67]   Abubakar, M.I. and Tsadu, S.M. (2003) A Survey of Fungal Infestation of Some Commercially Important Fishes in Selected Ponds and Fresh Fish Market in Minna, Niger Sate. Proceedings of the 8th Annual Conference of Animal Science Association of Nigeria, Federal University of Technology, Minna, 15-18 September 2003.

[68]   Gamal El-Deen, M.R. and El-Shamery G.R. (2010) Studies on Contamination and Quality of Fresh Fish Meats during Storage. Egyptian Academic Journal of Biological Sciences, 2, 65-74.

[69]   Nofiani, R., Kalbar, M. and Ardiningsih, P. (2010) Chemical Characteristic and Microbiological Safety of Commercial Fermented Ale-Ale from West Kalimantan, Indonesia. Journal of Fisheries and Aquatic Science, 5, 483-493.

[70]   Salem-Bekhe, M.M., Abd Al-Azeem, M.W. and Hashim, E.S.Y. (2011) Mycological Aspect of Smoked Fish at Retail Outlet at the Delta Province of Egypt. Journal of Applied Environmental and Biological Sciences, 1, 26-31.

[71]   Iqbal, Z., Sheikh, U. and Mughal, R. (2012) Fungal Infections in Some Economically Important Freshwater Fishes. Pakistan Veterinary Journal, 32, 422-426.

[72]   Iqbal, Z. and Saleemi, S. (2013) Isolation of Pathogenic Fungi from a Freshwater Commercial Fish, Catla catla (Hamliton). Science International (Lahore), 25, 851-855.

[73]   Fafioye, O. and Fafioye, O. (2013) Microbial Identification of Smoke-Dried Fish (Clarias gariepinus) from Some Local Markets in Ibadan Metropolis. Wudpecker Journal of Agricultural Research, 2, 294-298.

[74]   Rebecca I.E., Ayibawanaimi, O.L. and Chibueze, I.S. (2015) Assessment of Microbial Quality of Smoked Trachurus trachurus Sold in Some Markets of Three South-South States, Nigeria. International Journal of Food Microbiology, 2, 16-23.

[75]   Job, M.O., Agina, S.E. and Dapiya, H.S. (2016) Occurrence of Aflatoxigenic Fungi in Smoke-Dried Fish Sold in Jos Metropolis. British Microbiology Research Journal, 11, 1-7.

[76]   Galvano, F., Ritieni, A., Piva, G. and Pietri, A. (2005) Mycotoxin in the Human Food Chain. In: Diaz, D., Ed., The Mycotoxin Blue Book, Nottingham University Press, UK, 187-224.

[77]   Lass-Florl, C., Rief, A., Speth, C., Leitner, S., Wurzner, R. and Dierich, M.P. (2005) In Vitro Activities of Amphotericin B and Voriconazole against Aleurioconidia from Aspergillus terreus. Antimicrobial Agents and Chemotherapy, 49, 2539-2540.

[78]   Steinbach, W.J., Perfect, J.R., Schell, W.A., Walsh, J. and Benjamin, D.K. (2004) In Vitro Analyses, Animal Models, and 60 Clinical Cases of Invasive Aspergillus terreus Infection. Antimicrobial Agents and Chemotherapy, 48, 3217-3225.

[79]   Gibbs, S.G., Green, C.F., Tarwater, P.M., Mota, L.C. Mena, K.D. and Scarpino, P.V. (2006) Isolation of Antibiotic-Resistant Bacteria from the Air Plume Downwind of a Swine Confined or Concentrated Animal Feeding Operation. Environmental Health Perspectives, 114, 1032-1037.

[80]   Smith, S., Ganiyu, O., John, R., Fowora, M., Akinsinde, K. and Odeigah, P. (2012) Antimicrobial Resistance and Molecular Typing of Pseudomonas aeruginosa Isolated from Surgical Wounds in Lagos, Nigeria. Acta Medica Iranica, 50, 433-438.

[81]   Overdevest, I., Willemsen, I., Rijnsburger, M., Eustace, A., Xu, L., Hawkey, P., Heck, M., Savelkoul, P., Vandenbroucke-Grauls, C., van der Zwaluw, K., Huijsdens, X. and Kluytmans, J. (2011) Extended Spectrum β-Lactamase Gene of Escherichia coli in Chicken Meat and Humans, The Netherlands. Emerging Infectious Diseases, 17, 1216-12122.

[82]   Albuquerque, W.F., Macrae, A., Sousa, O.V., Vieira, G.H.F. and Vieira, R.H.S.F. (2007) Multiple Drug Resistant Staphylococcus aureus Strains Isolated from a Fish Market and From Fish Handlers. Brazilian Journal of Microbiology, 38, 131-134.

[83]   Miranda, C.D. and Zemelman, R. (2001) Antibiotic Resistant Bacteria in Fish from the Concepción Bay, Chile. Marine Pollution Bulletin, 42, 1096-1102.

[84]   Miranda, C.D. and Zemelman, R. (2002) Bacterial Resistance to Oxytetracycline in Chilean Salmon Farming. Aquaculture, 212, 31-47.

[85]   Rodgers, C.J. (2001) Resistance of Yersinia ruckeri to Antimicrobial Agents in Vitro. Aquaculture, 196, 325-345.

[86]   Nataro, J.P. and Kaper, J.B. (1998) Diarrheagenic Escherichia coli. Clinical Microbiology Reviews, 11, 142-201.