Identification, Antifungal Susceptibility and Phylogenetic Comparison of Fungi in Poultry Environment in Nigeria
DOI:
https://doi.org/10.3923/ijps.2020.548.556Keywords:
Antifungal agents, fungal contamination, fungi, layers farm, poultryAbstract
Objective: This study was conducted to investigate the fungal community structure in Nigerian poultry environments. Materials and Methods: In ten (layer and broiler) farms, samples were collected from drinkers, doors, feeders, floors, poles, roofs, walls and window nets. Fungal isolation was done on Sabouraud dextrose agar (SDA) followed by identification using morphological and microscopic features. The fungal identities were confirmed by sequencing the internal transcribed spacer region, followed by phylogenetic analysis. Antifungal susceptibility testing was done using nystatin (100 μg mL–1), fluconazole (25 μg mL–1) and voriconazole (1 μg mL–1). Results: A total of 244 fungi were identified in all the locations. In the layers farm, 112 fungal isolates were identified, while 132 isolates were identified in the broiler farm. In all the poultry farms, Aspergillus and Candida species had the highest occurrence of 32.4 and 24.6%, respectively while other fungi (Dematiaceous, Rhizopus, Penicillium, Mucor and Rhodotorula) had 43% occurrence. For the locations, poles and window nets had the highest isolation frequency of 15.2% each. The roofs, feeders and floors had 14.3 and 13.1%, while other locations had 27% isolation rate. Phylogenetic comparison of the isolates showed that closely related fungi from different countries formed separate clades. Candida species were sensitive to the three antifungal agents with the zone of inhibition diameter ranging from 19.08-25.36 mm. All the Aspergillus species were resistant to fluconazole but were sensitive to nystatin and voriconazole. Conclusion: Different fungi were identified in this study and they were all susceptible to nystatin antifungal agent.
References
Ekwue, E.I., M. Gray and A. Brown, 2003. Poultry farm buildings in Trinidad: present and future prospects. West Indian J. Eng., 25: 1-17.
Heise, H., A. Crisan and L. Theuvsen, 2015. The poultry market in Nigeria: Market structures and potential for investment in the market. Int. Food Agribus. Manage. Rev., 18: 197-222.
Ola-Fadunsin, S.D., 2017. Investigations on the occurrence and associated risk factors of avian coccidiosis in Osun state, Southwestern Nigeria. J. Parasitol. Res., 2017: 1-6.
Adeyemo, A.A. and M.P. Onikoyi, 2013. Prospects and challenges of large scale commercial poultry production in Nigeria. Agric. J., 7: 388-393.
Fulleringer, S.L., D. Seguin, S. Warin, A. Bezille and C. Desterque et al., 2006. Evolution of the environmental contamination by Thermophilic fungi in a Turkey confinement house in France. Poult. Sci., 85: 1875-1880.
Shin, S.H., J.U. Ponikau, D.A. Sherris, D. Congdon and E. Frigas et al., 2004. Chronic rhinosinusitis: An enhanced immune response to ubiquitous airborne fungi. J. Allergy Clin. Immunol., 114: 1369-1375.
Sajid, M.A., I.A. Khan and U. Rauf, 2006. Aspergillus fumigates in commercial poultry flocks, a serious threat to poultry industry in Pakistan. J. Anim. Plant Sci., 16: 79-81.
Viegas, C., E. Carolino, J. Malta-Vacas, R. Sabino, S. Viegas and C. Verissimo, 2012. Fungal contamination of poultry litter: A public health problem. J. Toxicol. Environ. Health A, 75: 1341-1350.
Kwanashie, C.N., H.M. Kazeem, P.A. Abdu and J.U. Umoh, 2013. Fungal contamination of some poultry houses in Kaduna State, Nigeria. J. Adv. Vet. Res., 3: 98-101.
Dhama, K., S. Chakraborty, A.K. Verma, R. Tiwari and R. Barathidasan et al., 2013. Fungal/mycotic diseases of poultry-diagnosis, treatment and control: A review. Pak. J. Biol. Sci., 16: 1626-1640.
Ghaemmaghami, S.S., M. Modirsaneii, A. Khosravi and M. Razzaghi-Abyaneh, 2016. Study on mycoflora of poultry feed ingredients and finished feed in Iran. Iran J. Microbiol., 8: 47-54.
Zafra, R., J. Perez, R.A. Perez-Ecija, C. Borge, R. Bustamante and A. Carbonero, 2008. Concurrent aspergillosis and ascites with high mortality in a farm of growing broiler chickens. Avian Dis., 52: 711-713.
Khan, A.A.H., 2010. Studies on indoor fungi and their control. Thesis of Doctor of Philosophy in Biotechnology, School of Life Sciences, Swami Ramanand Teerth Marathwada University, Nanded, Maharashtra, India.
Gros, R.V., I. Nichita, M. Seres, M.S. Ilie, A. Marcu, A. Cucerzan and E. Tirziu, 2015. Study of the fungi dynamics in a poultry house with permanent litter. Lucrari Stiintifice Med. Veterinară, 48: 257-262.
Kataria, J.M., C.M. Mohan, S. Dey, B.B. Dash and K. Dhama, 2005. Diagnosis and immunoprophylaxis of economically important poultry diseases: A review. Indian J. Anim. Sci., 75: 555-567.
Shivachandra, S.B., R.L. Sah, S.D. Singh, J.M. Kataria and K. Manimaran, 2004. Comparative pathological changes in aflatoxin fed broilers infected with hydropericardium syndrome. Indian J. Anim. Sci., 74: 600-604.
Amit-Romach, E., D. Sklan and Z. Uni, 2004. Microflora ecology of the chicken intestine using 16s ribosomal DNA primers. Poult. Sci., 83: 1093-1098.
Yudiarti, T., V.D. Yunianto, R. Murwani and E. Kusdiyantini, 2012. Isolation of fungi from the gastrointestinal tract of indigenous chicken. J. Trop. Anim. Agric., 37: 115-120.
Samantha, I., 2015. Veterinary Mycology. 1st Edn., Springer India India Pages: 179.
Bankole, S.S. and A.A. Adebanjo, 2003. Mycotoxins in food in West Africa: Current situation and possibilities of controlling it. Afr. J. Biotechnol., 2: 254-263.
NPC, 2007. Report of Nigeria's national population commission on the 2006 census. Popul. Dev. Rev., 33: 206-210.
Abbas, M.S., S.N. Yassein and J.M. Khalaf, 2017. Isolation and identification of some important mycological isolates from dropping of birds in Baghdad. J. Entomol. Zool. Stud., 5: 671-673.
El-Diasty, E.M., M.A.E.H. Ibrahim and G.K. El-Khalafawy, 2017. Isolation and molecular characterization of medically important yeasts isolated from poultry slaughterhouses and workers. Pak. J. Zool., 49: 425-759.
Guinea, J., T. Peláez, L. Alcalá and E. Bouza, 2006. Outdoor environmental levels of Aspergillus spp. conidia over a wide geographical area. Med. Mycol., 44: 349-356.
Winn, W., S. Allen, W. Janda, E. Koneman, G. Procop, P. Schreckenberger and G. Woods, 2006. Koneman's Color Atlas and Textbook of Diagnostic Microbiology. 6th Edn., Lippincott Williams and Wilkins, Philadelphia, USA.
Allimuthu, V., L.R. Gopinath, S. Archaya and R. Bhuvaneswari, 2014. Fungal species dynamics in decomposing poultry manure. Int. J. Adv. Interdis. Res., 1: 18-20.
De la Maza, L.M., M.T. Pezzlo and E.J. Baron, 1997. Color Atlas of Diagnostic Microbiology. Mosby Maryland Heights, Missouri, United States. Pages: 216.
Nygren, C.M.R., U. Eberhardt, M. Karlsson, J.L. Parrent, B.D. Lindahl and A.F.S. Taylor, 2008. Growth on nitrate and occurrence of nitrate reductase‐encoding genes in a phylogenetically diverse range of ectomycorrhizal fungi. New Phytol., 180: 875-889.
Gardes, M. and T.D. Bruns, 1993. ITS primers with enhanced specificity for basidiomycetes-application to the identification of mycorrhizae and rusts. Mol. Ecol., 2: 113-118.
White, T.J., T. Bruns, S. Lee and J. Taylor, 1990. Amplification and Direct Sequencing of Fungal Ribosomal RNA Genes for Phylogenetics. In: PCR Protocols: A Guide to Methods and Applications, Innis, M.A., D.H. Gelfand, J.J. Sninsky and T.J. White (Eds.), Academic Press, Cambridge, Massachusetts, ISBN: 9780123721808, pp: 315-322.
Rosling, A., R. Landeweert, B.D. Lindahl, K.H. Larsson, T.W. Kuyper, A.F.S. Taylor and R.D. Finlay, 2003. Vertical distribution of ectomycorrhizal fungal taxa in a podzol soil profile. New Phytol., 159: 775-783.
Edgar, R.C., 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res., 32: 1792-1797.
Kumar, S., G. Stecher, M. Li, C. Knyaz and K. Tamura, 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol., 35: 1547-1549.
NCCLS., 2004. Method for Antifungal Disk Diffusion Susceptibility Testing of Yeasts: Approved Guideline. National Committee for Clinical Laboratory Standards (NCCLS), Wayne, PA., USA., ISBN-13: 9781562385323, Pages: 23.
Petrikkou, E., J.L. Rodrı́guez-Tudela, M. Cuenca-Estrella, A. Gómez, A. Molleja and E. Mellado, 2001. Inoculum standardization for antifungal susceptibility testing of filamentous fungi pathogenic for humans. J. Clin. Microbiol., 39: 1345-1347.
McFarland, J., 1907. The nephelometer: An instrument for estimating the number of bacteria in suspensions used for calculating the opsonic index and for vaccines. J. Am. Med. Assoc., 49: 1176-1178.
Chan, G.F., S. Sinniah, T.I.N.T. Idris, M.S.A. Puad and A.Z.A. Rahman, 2013. Multiple rare opportunistic and pathogenic fungi in persistent foot skin infection. Pak. J. Biol. Sci., 16: 208-218.
Schlecht, L.M., B.M. Peters, B.P. Krom, J.A. Freiberg and G.M. Hänsch et al., 2015. Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology, 161: 161-168.
Okemo, P.O., E.K. Kemoi and C.C. Bii, 2013. Isolation of candida species in domestic chicken (Gallus gallus) droppings in Kabigeriet Village, Nakuru County Kenya. Eur. Sci. J., 9: 309-318.
Beernaert, L.A., F. Pasmans, L. Van Waeyenberghe, F. Haesebrouck and A. Martel, 2010. Aspergillus infections in birds: A review. Avian Pathol., 39: 325-331.
Arne, P., S. Thierry, D. Wang, M. Deville and G. Le Loch et al., 2011. Aspergillus fumigatus in poultry. Int. J. Microbiol.
Van Waeyenberghe, L., F. Pasmans, L.A. Beernaert, F. Haesebrouck and A. Martel, 2009. Interaction of the avian macrophage with Aspergillus fumigatus: To let live or let die. Proceedings of the 10th European Conference of the Association of Avian Veterinarians, 8th ECAMS Scientific Meeting of the Association of the European College of Avian Medicine and Surgery, March 17-21, 2009, Antwerp, Belgium.
Yassein, S.N. and Z.R. Zghair, 2012. Study of toxicity and pathogenicity of aflatoxin B1 and G1 in mice. Al-Anbar J. Vet. Sci., 5: 23-31.
Mgbeahuruike, A.C., T.E. Ejioffor, O.C. Christian, V.C. Shoyinka, M. Karlsson and E. Nordkvist, 2018. Detoxification of aflatoxin-contaminated poultry feeds by 3 adsorbents, bentonite, activated charcoal, and fuller’s earth. J. Applied Poult. Res., 27: 461-471.
Seifi, S., H. Shokri and M.K. Madab, 2018. Isolation and characterization of mycoflora of chicken hatcheries in Mazandaran province, north of Iran. Vet. Res. Forum, 9: 373-378.
Burch, M. and E. Levetin, 2002. Effects of meteorological conditions on spore plumes. Int. J. Biometeorol., 46: 107-117.
Silvana, P., C. Borda and E. Diugan, 2013. Microbiological air contamination in different types of housing systems for laying hens. ProEnvironment, 6: 549-555.
Pianalto, K.M. and J.A. Alspaugh, 2016. New Horizons in Antifungal Therapy. Fungi, Vol. 2, No. 4.
Scorzoni, L., A.C.A.d.P. Silva, C.M. Marcos, P.A. Assato and W.C.M.A.d. Melo et al., 2017. Antifungal therapy: new advances in the understanding and treatment of mycosis. Front. Microbiol., Vol. 8.
Arendrup, M.C., 2014. Update on antifungal resistance in Aspergillus and Candida. Clin. Microbiol. Infect., 20: 42-48.
Espinel-Ingroff, A., M.A. Pfaller, B. Bustamante, E. Canton and A. Fothergill et al., 2014. Multilaboratory study of epidemiological cutoff values for detection of resistance in eight Candida species to fluconazole, posaconazole, and voriconazole. Antimicrob Agents Chemother, 58: 2006-2012.
Downloads
Published
Issue
Section
License
Copyright (c) 2020 The Author(s)

This work is licensed under a Creative Commons Attribution 4.0 International License.
This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution and reproduction in any medium, provided the original author and source are credited.