Active surveillance of Cryptococcus neoformans in Nakhon Ratchasima Zoo, Thailand
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Abstract
Cryptococcus neoformans is an important pathogenic fungus causes cryptococcosis in humans and animals. This pathogen is usually found in avian droppings. For active surveillance of C. neoformans in Nakhon Ratchasima Zoo in Thailand, we investigated the incidence of C. neoformans in droppings of various captive birds in this zoo in April 2021. Dropping samples were collected from 29 avian species in various bird groups which comprised cranes (5 species), pheasants (8 species), hornbills (4 species), parrots (4 species), storks (3 species), pelican (1 species), vulture (1 species), and flightless birds including emu, cassowary, and penguin (1 species each). A total of 67 fresh avian dropping samples were collected using 0.85 % NaCl with 4 mg/mL penicillin G. Fungal isolation was performed by Sabouraud dextrose agar (SDA) with 0.05 mg/mL chloramphenicol and sunflower seed extract, cultured at 37oC and daily observed for 5 days. No colony of C. neoformans was found in all samples. Our study indicates that incidence of C. neoformans in avian droppings of captive birds has not been occurred in Nakhon Ratchasima Zoo.
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Maziarz, E.K., & Perfect, J.R. (2016). Cryptococcosis. Infectious Disease Clinics of North America, 30(1), 179-206. 2016;30(1):179-206. https://doi.org/10.1016/j.idc.2015.10.006.
Rosario, I., Acosta, B., & Colom M.F. (2008). Pigeons and other birds as a reservoir for Cryptococcus spp. Revista Iberoamericana de Micología, 25(1), S13-18. https://doi.org/10.1016/s1130-1406(08)70020-2.
Maepa, H.M. (2019). Cryptic pulmonary cryptococcosis: An atypical presentation of pulmonary cryptococcosis in a HIV-infected patient. African Journal of Thoracic and Critical Care Medicine, 25(4), 145-147. https://doi.org/10.7196/AJTCCM.2019.v25i4.002.
Chariyalertsak, S., Sirisanthana, T., Saengwonloey, O., & Nelson, K. E. (2001). Clinical presentation and risk behaviors of patients with acquired immunodefciency syndrome in Thailand, 1994-1998: regional variation and temporal trends. Clinical Infectious Diseases,
-32(6), 955-62. https://doi:10.1086/319348.
Rajasingham, R., Smith, R. M., Park, B. J., Jarvis, J. N., Govender, N. P., Chiller, T. M., Denning, D.W., Loyse, A., & Boulware, D.R. (2017). Global burden of disease of HIV-associated cryptococcal meningitis: an updated analysis. The Lancet Infectious Diseases, 17(8), 873-881. https://doi:10.1016/S1473-3099(17)30243-8.
Tangwattanachuleeporn, M., Somparn, P., Poolpol, K., Gross, U., Weig, M., & Bader, O. (2013). Prevalence and antifungal susceptibility of Cryptococcus neoformans isolated from pigeon excreta in Chon Buri Province, Eastern Thailand, Journal of Medical Mycology, 54(3), 303-307. https://doi.org/10.3314/mmj.54.303 5.
González-Hein, G., González-Hein, J., & Jarabrán, M.C.D. (2010). Isolation of Cryptococcus neoformans in dry droppings of captive birds in Santiago, Chile. Journal of Avian Medicine and Surgery, 24(3), 227-236. https://doi.org/10.1647/2009-003.1.
Kobayashi, C.C.B.A., Souza, L.K.H., Fernandes, O.F.L., Brito, S.C.A., Silva, A.C., Sousa, E.D., & Silva, M.R.R. (2005). Characterization of Cryptococcus neoformans isolated from urban environmental sources in Goiânia, Goiás State, Brazil. Revista do Instituto de Medicina Tropical de São Paulo, 47(4), 203-207.
Levitz S.M. (1998). Cryptococcus neoformans by Casadevall, Arturo & Perfect, John R. ASM Press, Washington, DC: American Society for Microbiology Press. https://doi.org/10.1111/j.1365-280X.1999.00238.x.
Franzot, S.P., Salkin, I.F., & Casadevall, A. (1999). Cryptococcus neoformans var. grubii: separate varietal status for Cryptococcus neoformans serotype A isolates. Journal of Clinical Microbiology, 37, 838-840. https://doi.org/10.1128/JCM.37.3.838-840.1999.
Nelson, R.T., & Lodes J.K (2006). Cryptococcus neoformans pathogenicity. In: Brown, A.J.P. (Ed), The Mycota XIII. Heidelberg:Springer-Verlag, Berlin, 237-266. https://link.springer.com/book/10.1007/978-3-642-00286-1?noAccess=true.
Ito-Kuwa, S., Nakamura, K., Aoki, S., & Vidotto, V. (2007). Serotype identification of Cryptococcus neoformans by multiplex PCR. Mycoses, 50(4), 277-281. https://doi.org/10.1111/j.1439-0507.2007.01357.x.
Kwon-Chung, K.J., Boekhout, T., Fell, J.W., & Diaz, M. (2002). Proposal to conserve the name Cryptococcus gattii against C. hondurianus and C. bacillisporus (Basidiomycota, Hymenomycetes, Tremellomycetidae). Taxon, 51:804-806. https://doi.org/10.2307/1555045.
Kwon-Chung, K.J., Fraser, J.A., Doering, T.L., Wang, Z., Janbon, G., Idnurm, A., & Bahn, Y.S. (2014). Cryptococcus neoformans and Cryptococcus gattii, the etiologic agents of cryptococcosis. Cold Spring Harbor Perspectives in Medicine, 4(7), a019760. https://doi.org/10.1101/cshperspect.a019760
Faganello, J., Dutra, V., Schrank, A., Meyer, W., Schrank, I.S., & Vainstein, M.H. (2009). Identification of genomic differences between Cryptococcus neoformans and Cryptococcus gattii by Representational Difference Analysis (RDA), Journal of Medical Mycology, 47(6), 584-591. https://doi.org/10.1080/13693780802272148
Ahasan, S. A. & Rahaman, A. Z. (2008). Mortality in Dhaka zoo due to microbial agents. Bangladesh Journal of Microbiology, 24(2), 154-156. https://doi.org/10.3329/bjm.v24i2.1263.
Bauwens, L., Vercammen, F., Wuytack, C., Van Looveren, K., & Swinne, D. (2004). Isolation of Cryptococcus neoformans in Antwerp Zoo’s nocturnal house. Mycoses, 47(7), 292-296. https://doi.org/10.1111/j.1439-0507.2004.00991.x.
Ahasan, S., Chowdhury, E., Khan, M., Parvin, R., Azam, S., Mohiuddin, G., Uddin, J., Rahman, M., Akter, L. & Khair, A. (2014). Histopathological investigation of cryptococcosis in Animals at Dhaka Zoo. Progressive Agriculture, 24(1-2), 123-129. https://doi.org/10.3329/pa.v24i1-2.19114.
Caicedo, L. D., Alvarez, M. I., Delgado, M., & Cárdenas, A. (1999). Cryptococcus neoformans in bird excreta in the City Zoo of Cali, Colombia. Mycopathologia, 147(3), 121-124. https://doi.org/10.1023/a:1007146700339.
Keerativasee, S., Takarn, P., Sanwong, K., Tharavichitkul, P., & Sriburee, P. (2008). Isolation of Cryptococcus neoformans from avian droppings in Chiang Mai from December 2005 to May 2006. Chiang Mai Medical Journal, 47(4), 149-154. https://www.thaiscience.info/
Journals/Article/CMMJ/10886724.pdf.
Griner, L. A., & Walch, H. A. (1978). Cryptococcosis in columbiformes at the San Diego Zoo. Journal of Wildlife Diseases, 14(3), 389-394. https://doi.org/10.7589/0090-3558-14.3.389.
Prariyachatigul, C., Chaiprasert, A., Meevootisom, V., & Pattanakitsakul, S. (1996). Assessment of a PCR technique for the detection and identifcation of Cryptococcus neoformans. Journal of medical and veterinary mycology: bi-monthly publication of the International Society for Human and Animal Mycology, 34(4), 251-258. https://doi.org/10.1080/02681219680000431.
Kwon-Chung, K.J., & Bennett, J.E. (1992). Medical mycology. Philadelphia.
Pal, M., Onda, C., & Hasegawa, A. (1990). Isolation of saprophytic Cryptococcus neoformans. Nihon Juigaku Zasshi, 52(6), 1171-1174. https://doi.org/10.1292/jvms1939.52.1171.
Krema, Z. A., Mokthar, E. S., El Magrabi, H.S., Eshwika, A., Ellabib, M., & Cogliati, M. (2018). Evaluation of novel culture media prepared from plant substrates for isolation and identifcation of Cryptococcus neoformans species complex. International Journal of
Microbiology Biochemistry and Technology, 1, 9-13. https://doi.org/10.29328/journal.ijcmbt.1001002.
McTaggart, L. R., Lei, E., Richardson, S. E., Hoang, L., Fothergill, A., & Zhang, S. X. (2011). Rapid identifcation of Cryptococcus neoformans and Cryptococcus gattii by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Journal of Clinical Microbiology, 49(8), 3050-3053. https://doi.org/10.1128/JCM.00651-11.
Thunyaharn, S., Sungsirin, N., Sukhapridasap, P., Kunyaboon, R., Saichanma, S., Kesakomol, P., & Boonsiri, T. (2021). Isolation of Cryptococcus neoformans from pigeon excreta in Nakhon Ratchasima College, Nakhon Ratchasima Province. Progress in Applied
Science and Technology, 11(2), 6-9. https://doi.org/10.14456/past.2021.
Canteros, C. E., Rodero, L., Rivas, M. C., & Davel, G. (1996). A rapid urease test for presumptive identifcation of Cryptococcus neoformans, Mycopathologia, 136(1), 21-23. https://doi.org/10.1007/BF00436656.
Kwon-Chung, K. J., Polacheck, I., & Bennett, J. E. (1982). Improved diagnostic medium for separation of Cryptococcus neoformans var. neoformans (serotypes A and D) and Cryptococcus neoformans var. gattii (serotypes B and C). Journal of Clinical Microbiology, 15(3), 535-537. https://doi.org/10.1128/jcm.15.3.535-537.1982.
Chae, H. S., Jang, G. E., Kim, N. H., Son, H. R., Lee, J. H., Kim, S. H., Park, G. N., Jo, H. J., Kim, J. T., & Chang, K. S. (2012). Classifcation of Cryptococcus neoformans and yeast-like fungus isolates from pigeon droppings by colony phenotyping and ITS genotyping and their seasonal variations in Korea. Avian Diseases, 56(1), 58-64. https://doi.org/10.1637/9703-030711-Reg.1.
Kuroki, M., Phichaichumpon, C., Yasuoka, A., Chiranairadul, P., Chosa, T., Sirinirund, P., Miyazaki, T., Kakeya, H., Higashiyama, Y., Miyazaki, Y., Ishida, Y., Kohno, S. (2004). Environmental isolation of Cryptococcus neoformans from an endemic region of HIVassociated cryptococcosis in Thailand. Yeast, 21, 809-812.https://doi.org/10.1002/yea.1112.
Lugarini, C., Goebel, C. S., Condas, L. A., Muro, M. D., de Farias, M. R., Ferreira, F. M., & Vainstein, M. H. (2008). Cryptococcus neoformans isolated from passerine and psittacine bird excreta in the state of Paraná, Brazil. Mycopathologia, 166(2), 61-69.
https://doi.org/10.1007/s11046-008-9122-3.
Mirpourian, S. S., Sharif, N., Talazadeh, F., Jafari, R. A., & Ghorbanpoor, M. (2021). Isolation, molecular identification, and phylogenetic evaluation of Cryptococcus neoformans isolated from pigeon lofts, Psittaciformes, and Passeriformes in Ahvaz, Iran. Comparative Immunology, Microbiology & Infectious Diseases, 76, 101618. https://doi.org/10.1016/j.cimid.2021.101618.
Bertout, S., Gouveia, T., Krasteva, D., Pierru, J., Pottier, C., Bellet, V., Arianiello, E., Salipante, F., Roger, F., & Drakulovski, P. (2022). Search for Cryptococcus neoformans/gattii complexes and related genera (Filobasidium, Holtermanniella, Naganishia, Papiliotrema, Solicoccozyma, Vishniacozyma) spp. biotope: Two years surveillance of wild avian fauna in Southern France. Journal of Fungi, 8(3), 227.
https://doi.org/10.3390/jof8030227.
Khayhan, K. (2018). Prevalence of Cryptococcus neoformans in avian droppings and tree debris in the North and Northeast, Thailand. 20th Congress of the International Society for Human and Animal Mycology. P414. https://doi.org/10.26226/morressier.5ac39996d462b8028d89a07a.
Sriburee, P., Khayhan, S., Khamwan, C., Panjaisee, S., & Tharavichitkul, P. (2004). Serotype and PCRfngerprints of clinical and environmental isolates of Cryptococcus neoformans in Chiang Mai, Thailand. Mycopathologia, 158(1), 25-31. https://doi.
org/10.1023/b:myco.0000038435.14281.f4.
Krangvichain, P., Niyomtham, W., & Prapasarakul, N. (2016). Occurrence and susceptibilities to disinfectants of Cryptococcus neoformans in fecal droppings from pigeons in Bangkok, Thailand. The Journal of Veterinary Medical Science, 78(3), 391-396. https://doi.org/10.1292/jvms.15-0594.
Weber, A., & Schäfer, R. (1991). The occurrence of Cryptococcus neoformans in fecal samples from birds kept in human living areas. Berliner und Münchener tierärztliche Wochenschrift, 104(12), 419-421. https://pubmed.ncbi.nlm.nih.gov/1786044/
Nielsen, K., de Obaldia, A.L., & Heitman, J. (2007). Cryptococcus neoformans Mates on Pigeon Guano: Implications for the Realized Ecological Niche and Globalization. Eukaryotic Cell, 6(6), 949-959. https://doi.org/10.1128/EC.00097-07.
Oh, K.S., & Hwang, S.M. (2005). Isolation and characterization of Cryptococcus neoformans from environmental sources in Busan. Mycobiology, 33(4), 188-193. https://doi.org/10.4489/MYCO.2005.33.4.188.
Gilad, A., Bakal-Weiss, M., Blum, S. E., Polacheck, I., & Elad, D. (2015). Environmental survey for Cryptococcus gattii in an Israeli Zoo populated with animals originating from Australia. Israel Journal of Veterinary Medicine, 70(3), 47-51.
Kaocharoen, S., Ngamskulrungroj, P., Firacative, C., Trilles, L., Piyabongkarn, D. Banlunara, W., Poonwan, N., Chaiprasert, A., Meyer, W., Chindamporn A. (2013). Molecular epidemiology reveals genetic diversity amongst isolates of the Cryptococcus neoformans/C. gattii species complex in Thailand. PLOS neglected Tropical Diseases, 7(7), e2297. https://doi.org/10.1371/journal.pntd.0002297.
