Indian Journal of Animal Research

  • Chief EditorK.M.L. Pathak

  • Print ISSN 0367-6722

  • Online ISSN 0976-0555

  • NAAS Rating 6.50

  • SJR 0.263

  • Impact Factor 0.5 (2023)

Frequency :
Monthly (January, February, March, April, May, June, July, August, September, October, November and December)
Indexing Services :
Science Citation Index Expanded, BIOSIS Preview, ISI Citation Index, Biological Abstracts, Scopus, AGRICOLA, Google Scholar, CrossRef, CAB Abstracting Journals, Chemical Abstracts, Indian Science Abstracts, EBSCO Indexing Services, Index Copernicus
Indian Journal of Animal Research, volume 54 issue 2 (february 2020) : 228-233

Antifungal resistance in cnlac1 possessing Cryptococcus neoformans isolated from domestic and feral pigeons in West Bengal, India

A. Banerjee, K. Batabyal, C. Debnath, S.N. Joardar, D.P. Isore, S. Dey, S. Taraphder, A.D. Singh, S. Pal, I. Samanta
1Department of Veterinary Microbiology, Faculty of Veterinary and Animal Sciences, West Bengal University of Animal and Fishery Sciences, Belgachia, Kolkata-700 037, West Bengal, India.
Cite article:- Banerjee A., Batabyal K., Debnath C., Joardar S.N., Isore D.P., Dey S., Taraphder S., Singh A.D., Pal S., Samanta I. (2019). Antifungal resistance in cnlac1 possessing Cryptococcus neoformans isolated from domestic and feral pigeons in West Bengal, India. Indian Journal of Animal Research. 54(2): 228-233. doi: 10.18805/ijar.B-3739.
Cryptococcus neoformans acts as a major etiology of human infections in immunocompromised, cancer and transplant patients. The present study was conducted to detect the occurrence and antifungal resistance of C. neoformans in domestic and feral pigeons in and around Kolkata, a metropolitan city in India with considerable size of pigeon population. Weathered droppings of domestic and feral pigeons (n=917) were collected from different pet bird shelters, different buildings and other places. Isolation and identification of C. neoformans was performed based on cultural, biochemical properties. Antifungal sensitivity of the confirmed isolates were performed according to standard CLSI protocols with seven antifungals and caspofungin. A total of 153(16.68%) samples were found positive for Cryptococcus neoformans var. neoformans. All the isolates possessed CNLAC1 outer gene in PCR. Antifungal sensitivity revealed marked resistance to amphotericin-B (33.33%), fluconazole (20.91%), flucytosine (11.11%), and ketoconazole (8.49%). This is of great concern as the study area (Kolkata) is a densely populated city and the birds are in close proximity to the people.
  1. Abulreesh, H.H., Organji, S.R., Elbanna, K., Osman, G.E.H., Almalki, M.H.K. and Abdel-Mallek, A.Y. (2015). First report of environmental isolation of Cryptococcus neoformans and other fungi from pigeon droppings in Makkah, Saudi Arabia and in vitro susceptibility testing. Asian Pacific J. Trop. Dis., 5: 622-626.
  2. Archibald, L.K., Tuohy, M.J., Wilson, D.A., Nwanyanwu, O., Kazembe, P.N., Tansuphasawadikul, S., Eampokalap, B., Chaovavanich, A., Reller, L.B., Jarvis, W.R. and Hall, G.S. (2004). Antifungal susceptibilities of Cryptococcus neoformans. Emerg. Infect. Dis.,10: 143-145.
  3. Bii, C.C., Makimura, K., Abe, S., Taguchi, H., Mugasia, O.M., Revathi, G., Wamae, N.C. and Kamiya, S. (2007). Antifungal drug susceptibility of Cryptococcus neoformans from clinical sources in Nairobi, Kenya. Mycoses, 50:25-30.
  4. Bose, I., Reese, A.J., Ory, J.J., Janbon, G. and Doering, T.L. (2003). A yeast under cover: the capsule of Cryptococcus neoformans.    Eukaryotic Cell, 2: 655-663.
  5. Cafarchia,C., Romito, D., Iatta, R., Camarda, A., Montagna, M.T. and Otranto, D. (2006). Role of birds of prey as carriers and spreaders of Cryptococcus neoformans and other zoonotic yeasts. Medi. Mycol., 44: 485-492. 
  6. Capoor, M.R., Mandal, P., Deb, M., Aggarwal, P. and Banerjee, U. (2008). Current scenario of cryptococcosis and antifungal susceptibility pattern in India: a cause for reappraisal. Mycoses, 51: 258-265.
  7. Carter, G.R. and Wise, D.J. (2004). Infections caused by yeast and yeast like fungi. In: Essentials of Veterinary Bacteriology and Mycology. 6th edn. Iowa State Press, Iowa. pp. 258-259.
  8. Chae, H.S., Park, G.N., Kim, S.H., Jo, H.J., Kim, J.T., Jeoung, H.Y. and Chang, K.S. (2012). Rapid direct identification of Cryptococcus neoformans from pigeon droppings by nested PCR using CNLAC1 gene. Poult. Sci., 91: 1983-1989.
  9. Chowdhary, A., Randhawa, H.S., Sundar, G., Kathuria, S., Prakash, A., Khan, Z., Sun, S. and Xu, J. (2011). In vitro antifungal susceptibility profiles and genotypes of 308 clinical and environmental isolates of Cryptococcus neoformans var. grubii and Cryptococcus gattii serotype B from north-western India. J. Medi. Microbiol., 60: 961-967.
  10. Clinical and Laboratory Standards Institute (CLSI) (2008). Reference method for broth dilution antifungal susceptibility testing of yeasts; approved standard-Third Edition. CLSI document M27-A3 (ISBN 1-56238-666-2), Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite2500, Wayne, Pennsylvania 19087, USA.
  11. Costa, A.K., Sidrim, J.J., Cordeiro, R.A., Brilhante, R.S., Monteiro, A.J., Rocha, M.F. (2010). Urban pigeons (Columba livia) as a potential source of pathogenic yeasts: a focus on antifungal susceptibility of Cryptococcus strains in Northeast Brazil. Mycopathol.,169: 207-213.
  12. Datta, K., Jain, N., Sethi, S., Rattan, A., Casadevall, A. and Banerjee, U. (2003). Fluconazole and itraconazole susceptibility of clinical isolates of Cryptococcus neoformans at a tertiary care centre in India: a need for care. J. Antimicro. Chemother., 52: 683-686.
  13. Dongmo, W., Kechia, F., Tchuenguem, R., Nangwat, C., Yves, I., Kuiate, J.R. and Dzoyem, J.P. (2016). In vitro antifungal susceptibility of environmental isolates of Cryptococcus spp. from the West Region of Cameroon. Ethiopian J. Hlth. Sci., 26: 555-560.
  14. Eastman, A.J., He, X., Qiu, Y., Davis, M.J., Vedula, P., Lyons, D.M. and Wormley, F.L. (2015). Cryptococcal heat shock protein 70 homolog Ssa1 contributes to pulmonary expansion of Cryptococcus neoformans during the afferent phase of the immune response by promoting macrophage M2 polarization. J. Immunol., 194: 5999-6010.
  15. Emmons, C.W. (1951). Isolation of Cryptococcus neoformans from soil. J. Bacteriol., 62: 685.
  16. Garcia-Hermoso, D., Mathoulin-Pelissier, S., Couprie, B., Ronin, O., Dupont, B. and Dromer, F. (1997). DNA typing suggests pigeon droppings as a source of pathogenic Cryptococcus neoformans serotype D. J. Clin. Microbiol., 35: 2683-2685.
  17. Granados, D.P. and Castaneda, E. (2005). Isolation and characterization of Cryptococcus neoformans varieties recovered from natural sources in Bogotá, Colombia, and study of ecological conditions in the area. Micro. Ecol., 49: 282-290.
  18. Gugnani, H.C., Sandhu, R.S. and Shome, S.K. (1976). Prevalence of Cryptococcus neoformans in avian excreta in India. Mycoses, 19: 183-187.
  19. Jain, N., Wickes, B.L., Keller, S.M., Fu, J., Casadevall, A., Jain, P., Ragan, M.A., Banerjee, U. and Fries, B.C. (2005). Molecular epidemiology of clinical Cryptococcus neoformans strains from India. J. Clin. Microbiol., 43: 5733-5742.
  20. Khan, Z.U., Pal, M., Randhawa, H.S. and Sandhu, R.S. (1978).Carriage of Cryptococcus neoformans in the crops of pigeons. J. Medi. Microbiol.,11: 215-218.
  21. Kumar, G.C.P., Prabu, D., Mitani, H., Mikami, Y. and Menon, T. (2010).Environmental isolation of Cryptococcus neoformans and Cryptococcus gattii from living trees in Guindy National Park, Chennai, South India. Mycoses, 53: 262-264.
  22. Kumarasamy, N., Solomon, S., Flanigan, T.P., Hemalatha, R., Thyagarajan, S.P. and Mayer, K. H. (2003). Natural history of human immunodeficiency virus disease in southern India.Clin. Infect. Dis.,36: 79-85.
  23. Kumlin, U., Olsen, B., Granlund, M., Elmqvist, L.G. and Tarnvik, A. (1998).Cryptococcosis and starling nests. The Lancet, 351: 1181.
  24. Kwon-Chung, K.J., Fraser, J.A., Doering, T.L., Wang, Z.A., Janbon, G., Idnurm, A. and Bahn, Y.S. (2014). Cryptococcus neoformans and Cryptococcus gattii, the etiologic agents of cryptococcosis. Cold Spring Harb.Perspect.Med.,4(7): 60-87.
  25. Kwon-Chung, K.J. and Bennett, J.E. (1992). Cryptococcosis. In Medical Mycology, Lea & Febiger. Philadelphia, pp 397-446.
  26. Lagrou, K., Van Eldere, J., Keuleers, S., Hagen, F., Merckx, R., Verhaegen, J., Peetermans, W.E. and Boekhout, T. (2005). Zoonotic transmission of Cryptococcus neoformans from a magpie to an immunocompetent patient. J. Inter. Medi., 257: 385-388.
  27. Matos, T., Meis, J.F. and Hagen, F. (2018). Molecular characterization and antifungal susceptibility testing of sequentially obtained clinical Cryptococcus deneoformans and Cryptococcus neoformans isolates from Ljubljana, Slovenia. Mycopathol.,183: 371-380.
  28. Mitchell, T.G. and Perfect, J.R. (1995). Cryptococcosis in the era of AIDS-100 years after the discovery of Cryptococcus neoformans. Clin. Microbiol. Reviews, 8: 515-548.
  29. NACO Annual Report 2016-17, Chapter 24. Available at: files/NACO%20ANNUAL% 20REPORT% 202016-17.pdf. Retrieved on 10th July, 2017.
  30. Ramirez, R., Robertstad, G.W., Hutchinson, L.R., Chavez, J. (1976). Mycotic flora in the lower digestive tract of feral pigeons (Columba livia) in the El Paso, Texas area. J. Wild.Dis., 12: 83-85.
  31. Salas, S.D., Bennett, J.E., Kwon-Chung, K.J, Perfect, J.R. and Williamson, P.R. (1996). Effect of the laccase gene CNLAC1, on virulence of Cryptococcus neoformans. J. Experi. Medi.,184: 377-386.
  32. Samanta, I, and Bandyopadhyay, S. (2017). Pet Bird Diseases and Care. pp13-166. Springer.
  33. Sar, B., Monchy, D., Vann, M., Keo, C., Sarthou, J.L. and Buisson, Y. (2004). Increasing in vitro resistance to fluconazole in Cryptococcus neoformans Cambodian isolates: April 2000 to March 2002. J. Antimicro. Chemother.,54: 563-565.
  34. Sethi, K.K., Randhawa, H.S., Abraham, S., Mishra, S.K. and Damodaran, V.N. (1966). Occurrence of Cryptococcus neoformans in Pigeon excreta in Delhi. Indian J. Chest Dis. Allied Sci.,8: 207-210.
  35. Souza, L.K.H., Fernandes, O.D.F.L., Kobayashi, C.C.B.A., Passos, X.S., Costa, C.R., Lemos, J. A., Souza-Júnior, A.H. and Silva, M.D.R.R. (2005).Antifungal susceptibilities of clinical and environmental isolates of Cryptococcus neoformans in goiânia city, Goiás, Brasil.Revista do Instituto de Medicina Trop de São Paulo,47: 253-256.
  36. Spina Tensini, T., Muro, M.D., Queiroz Telles, F., Strozzi, I., Moraes, S.T., Petterle, R.R., Vettorello, M., Staudacher, C., Miguez, L.A.L. and de Almeida S.M. (2017).Geographic distribution of patients affected by Cryptococcus neoformans/Cryptococcus gattii species complexes meningitis, pigeon and tree populations in Southern Brazil. Mycoses, 60: 51-58.
  37. Springer, D.J, Saini, D., Byrnes, E.J., Heitman, J. and Frothingham, R. (2013). Development of an aerosol model of Cryptococcus reveals humidity as an important factor affecting the viability of Cryptococcus during aerosolization. PLOS One, 8: 804.
  38. Tangwattanachuleeporn, M., Somparn, P., Poolpol, K., Gross, U., Weig, M. and Bader, O. (2013). Prevalence and antifungal susceptibility of Cryptococcus neoformans isolated from pigeon excreta in Chon Buri Province, Eastern Thailand. Medi. Mycol., 54: 303-307.
  39. Vajpayee, M., Kanswal, S., Seth, P. and Wig, N. (2003). Spectrum of opportunistic infections and profile of CD4+ counts among AIDS patients in North India. Infect.,31: 336-340.
  40. Wang, Y. and Casadevall, A. (1994). Susceptibility of melanized and nonmelanized Cryptococcus neoformans to nitrogen-and oxygen-    derived oxidants. Infect. Immun., 62: 3004-3007.
  41. Yildiran, S.T., SaracLi, M.A., Gönlüm, A., Gün, H. (1998). Isolation of Cryptococcus neoformans var. neoformans from pigeon droppings collected throughout Turkey. Medi. Mycol., 36: 391-394. 

Editorial Board

View all (0)