Abstract
As Cryptosporidium parvum and Giardia lamblia can be disseminated in the environment by avian hosts, a total of 499 fecal dropping from 308 free-ranging, 90 captive, and 101 domestic birds were tested by conventional, immunological, and molecular techniques for these human enteropathogens. Twenty-six (5.2%) tested positive for G. lamblia cysts and 19 (3.8%) for C. parvum oocysts. A bird total of 23 (7.5%) free-ranging, two (2.2%) captive, and one (0.1%) domestic tested positive for cysts, whereas 18 (5.8%) free-ranging, one (1.1%) captive, and zero livestock birds tested positive for oocysts. G. lamblia cysts and C. parvum oocysts were found significantly more frequently in fecal droppings of free-ranging aquatic birds than in birds not normally associated with water. No specimen tested positive for both pathogens simultaneously. Aquatic birds represent an important epidemiologic link in water-associated transmission cycles of Cryptosporidium and Giardia and play a significant role in environmental contamination of aquatic habitats with these anthropozoonotic pathogens.
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Ash LR, Orihel TC (1987) Parasites: a guide to laboratory procedures and identification. ASCP, Chicago, p 327
Buck JD (1990) Isolation of Candida albicans and Halophilia Vibrio spp. from aquatic birds in Connecticut and Florida. Am Soc Microbiol 56:826–828
Graczyk TK, Cranfield MR, Fayer R, Anderson MS (1996) Viability and infectivity of Cryptosporidium parvum oocysts are retained upon intestinal passage through a refractory avian host. Appl Environ Microbiol 62:3234–3237
Graczyk TK, Cranfield MK, Fayer R, Trout J, Goodale HJ (1997) Infectivity of Cryptosporidium parvum oocysts is retained upon intestinal passage through a migratory waterfowl species (Canada goose, Branta canadensis). Trop Med Intl Hlth 2:341–347
Graczyk TK, Fayer R, Trout JM, Lewis EJ, Farley CA, Sulaiman I, Lal AA (1998) Giardia sp. and infectious Cryptosporidium parvum oocysts in the feces of migratory Canada geese (Branta canadensis). Appl Environ Microbiol 64:2736–2738
Graczyk TK, Lucy FE, Tamang L, Miraflor A (2007a) Human enteropathogen load in activated sewage sludge and corresponding sewage sludge-end products. Appl Environ Microbiol 73:2013–2015
Graczyk TK, Sunderland D, Rule AM, da Silva AJ, Moura INS, Tamang L, Girouard AS, Schwab KJ, Breysse PN (2007b) Urban feral pigeons (Columbia livia) as a source for air-and-waterborne contamination with Enterocytozoon bieneusi spores. Appl Environ Microbiol 73:4357–4358
Graczyk TK, Majewska AC, Schwab KJ (2008) The role of birds in dissemination of human waterborne enteropathogens. Trends Parasitol 24:55–59
Haro M, Izquierdo F, Henriques-Gil N, Andres I, Alonso F, Fenoy S, del Aguila C (2005) First detection and genotyping of human-associated microsporidia in pigeons from urban parks. Appl Environ Microbiol 71:3153–3157
Haro M, Henriques-Gil N, Fenoy S, Izquierdo F, Alonso F, del Aguila C (2006) Detection and genotyping of Enterocytozoon bieneusi in pigeons. J Eukaryot Microbiol 53:58–60
Heuvelink AE, Zwartkruis JT, van Heerwaarden C, Arends B, Stortelder V, de Boer E (2008) Pathogenic bacteria and parasites in wildlife and surface water. Tjdschr Diergeneeskd 133:330–335
Jellinson KL, Distel DL, Hemond HF, Schauer DB (2004) Phylogenetic analysis of the hyperviariable region of the 18S rRNA gene of Cryptosporidium oocysts in feces of Canada geese (Branta canadensis): evidence for five novel genotypes. Appl Environ Microbiol 70:452–458
Jellinson KL, Distel DL, Hemond HF, Schauer DB (2007) Phylogenetic analysis implicates birds as a source of Cryptosporidium spp. oocysts in agricultural watersheds. Environ Sci Technol 15:3620–3625
Jenkins MC, Trout J, Abrahamsen MS, Higgins J, Fayer R (2000) Estimating viability of Cryptosporidium parvum oocysts using reverse transcriptase–polymerase chain reaction (RT-PCR) directed at mRNA encoding amyloglucosidase. J Microbiol Methods 34:97–106
Karanis P, Kourenti C, Smith H (2007) Waterborne transmission of protozoan parasites: A worldwide review of outbreaks and lessons learnt. J Water Hlth 5:1–38
Kassa H, Harrington BJ, Bisesi MS (2004) Cryptosporidiosis: a brief literature review and update regarding Cryptosporidium in feces of Canada geese (Branta canadensis). J Environ Hlth 66:34–40
Kirschner AK, Zechmeister TC, Kavka GG, Beiwl C, Herzig A, Mach LR, Farnleither A (2004) Integral strategy for evaluation of fecal coliform indicator performance in bird-influenced saline inland waters. Appl Environ Microbiol 70:7396–7403
Kuhn RC, Rock CM, Oshima KH (2002) Occurrence of Cryptosporidium and Giardia in wild ducks along the Rio Grande river valley in Southern New Mexico. Appl Environ Microbiol 68:161–165
Lobo ML, Xiao L, Cama V, Magalha N, Antunes F, Matos O (2006) Identification of potentially human-pathogenic Enterocytozoon bieneusi genotypes in various birds. Appl Environ Microbiol 72:7380–7382
Majewska AC, Kasprzak W (1990) Axenic isolation of Giardia strains from primates and rodents. Vet Parasitol 35:169–174
Majewska AC, Kasprzak W (2000) New axenic isolates of Giardia from primates. Acta Parasitol 45:55–56
Majewska AC, Kasprzak W, Werner A (1997) Prevalence of Cryptosporidium in mammals housed in Poznań Zoological Garden, Poland. Acta Parasitol 42:195–198
Majewska AC, Kasprzak W, Werner A (1998) Prevalence of intestinal amoebae and flagellates in animals of the Zoological Garden in Poznań. Wiadomości Parazytologiczne 44:469
Méndez-Hermida F, Gómez-Couso H, Romero-Sounces R, Ares-Mazás E (2007) Cryptosporidium and Giardia in wild otters (Lutra lutra). Vet Parasitol 144:153–156
Messner MJ, Chappell CL, Okhuysen PC (2001) Risk assessment for Cryptosporidium: a hierarchical Bayesian analysis of human dose–response data. Water Res 35:3934–3940
Okhuysen PC, Chappell CL, Crabb JH, Sterling CR, Dupont HL (1999) Virulence of three distinct Cryptosporidium parvum isolates for healthy adults. J Infect Dis 180:1275–1281
Olson ME, O’Handley RM, Ralston BJ, McAllister TA, Thompson RC (2004) Update on Cryptosporidium and Giardia infections in cattle. Trends Parasitol 20:185–191
Rose JB, Huffman DE, Gennaccaro A (2002) Risk and control of waterborne cryptosporidiosis. FEMS Microbiol Rev 2:113–123
Slodkowicz-Kowalska A, Graczyk TK, Tamang L, Jędrzejewski S, Nowosad A, Zduniak P, Solarczyk P, Girouard AS, Majewska AC (2006) Microsporidia species known to infect humans are present in aquatic birds; implications for transmission via water? Appl Environ Microbiol 72:4540–4544
Solarczyk P, Majewska AC (2007) Identification of Giardia genotypes in artiodactyles. Wiadomości Parazytologiczne 53:109
Tamburrini A, Pozio E (1999) Long-term survival of Cryptosporidium parvum oocysts in seawater and in experimentally infected mussels (Mytilus galloprovincialis). Int J Parasitol 29:711–715
Upcroft JA, McDonnell PA, Gallagher AN, Chen N (1997) Lethal Giardia from a wild-caught sulphur-crested cockatoo (Cacatua galerita) established in vitro chronically infects mice. Parasitol 114:407–412
Upcroft JA, McDonnell PA, Upcroft P (1998) Virulent avian Giardia duodenalis pathogenic for mice. Parasitol Today 14:281–284
Wolfe MS (1992) Giardiasis. Clin Microbiol Rev 5:93–100
Zhou L, Kassa H, Tischler ML, Xiao L (2004) Host-adapted Cryptosporidium spp. in Canada geese (Branta canadensis). Appl Environ Microbiol 70:4211–4215
Acknowledgments
This study was supported by the Poznan University of Medical Sciences, Faculty of Medicine I, Poznan, Poland (grant no. 502-1-0003496), Environmental Protection Agency STRIVE Program (grant no. 2008-EH-MS-3-S3), and the Fulbright Senior Specialist Fellowship (grant no. 2225 to T.K. Graczyk). We thank Irena Robak for her technical assistance.
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Majewska, A.C., Graczyk, T.K., Słodkowicz-Kowalska, A. et al. The role of free-ranging, captive, and domestic birds of Western Poland in environmental contamination with Cryptosporidium parvum oocysts and Giardia lamblia cysts. Parasitol Res 104, 1093–1099 (2009). https://doi.org/10.1007/s00436-008-1293-9
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DOI: https://doi.org/10.1007/s00436-008-1293-9