Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-23T04:22:58.389Z Has data issue: false hasContentIssue false
  • English
  • Français

Occurrence of Giardia and Cryptosporidium in wild birds in Galicia (Northwest Spain)

Published online by Cambridge University Press:  11 February 2015

AURORA REBOREDO-FERNÁNDEZ ,
ELVIRA ARES-MAZÁS ,
SIMONE M. CACCIÒ  and
HIPÓLITO GÓMEZ-COUSO
AURORA REBOREDO-FERNÁNDEZ
Affiliation:
Laboratory of Parasitology, Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Santiago de Compostela, Campus Vida, 15782 Santiago de Compostela, A Coruña, Spain
ELVIRA ARES-MAZÁS
Affiliation:
Laboratory of Parasitology, Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Santiago de Compostela, Campus Vida, 15782 Santiago de Compostela, A Coruña, Spain
SIMONE M. CACCIÒ
Affiliation:
Department of Infectious, Parasitic and Immunomediated Diseases, Istituto Superiore di Sanità, Viale Regina Elena 299, 00161, Rome, Italy
HIPÓLITO GÓMEZ-COUSO*
Affiliation:
Laboratory of Parasitology, Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Santiago de Compostela, Campus Vida, 15782 Santiago de Compostela, A Coruña, Spain Department of Infectious, Parasitic and Immunomediated Diseases, Istituto Superiore di Sanità, Viale Regina Elena 299, 00161, Rome, Italy
*
*Corresponding author. Laboratory of Parasitology, Department of Microbiology and Parasitology, Faculty of Pharmacy, University of Santiago de Compostela, Campus Vida, 15782 Santiago de Compostela, A Coruña, Spain. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Faecal samples were obtained from 433 wild birds being treated in wildlife recovery centres in Galicia (Northwest Spain), between February 2007 and September 2009. The birds belonged to 64 species representing 17 different orders. Giardia cysts and Cryptosporidium oocysts were detected by an immunofluorescence antibody test and identified at the molecular level by established PCR-sequencing methods. The overall prevalence of Giardia was 2·1% and that of Cryptosporidium, 8·3%. To our knowledge, this is the first description of Giardia sp. in Tyto alba and Caprimulgus europaeus; and of Cryptosporidium sp. in Apus apus, Athene noctua, C. europaeus, Falco tinnunculus, Morus bassanus, Parabuteo unicinctus and Strix aluco. Furthermore, the first PCR-sequence confirmed detection of Giardia duodenalis assemblage B in, Buteo buteo, Coturnix coturnix and Pica pica; G. duodenalis assemblage D in Garrulus glandarius; and G. duodenalis assemblage F in Anas platyrhynchos; Cryptosporidium parvum in Accipiter nisus, B. buteo, Milvus migrans, Pernis apivorus and P. pica; and Cryptosporidium meleagridis in Streptopelia turtur. The study findings demonstrate the wide spread of Giardia and Cryptosporidium between wild birds.

Keywords

wild birdsGiardiaCryptosporidiumimmunofluorescence microscopymolecular characterizationGalicia (Northwest Spain)
Type
Research Article
Information
Parasitology , Volume 142 , Issue 7 , June 2015 , pp. 917 - 925
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Abreu-Acosta, N., Foronda-Rodríguez, P., López, M. and Valladares, B. (2009). Occurrence of Cryptosporidium hominis in pigeons (Columba livia). Acta Parasitologica 54, 1–5.Google Scholar
Anonymous (2014). Factores que determinan a biodiversidade en Galicia. Xunta de Galicia. Retrieved 17 December 2014 from http://www.cmati.xunta.es/seccion-organizacion/c/DX_Conservacion_Natureza?content=Direccion_Xeral_Conservacion_Natureza/Biodiversidade/seccion.html&std=Factores_que_determinan_a_biodiversidade_en_Galicia.html Google Scholar
Appelbee, A. J., Thompson, R. C. and Olson, M. E. (2005). Giardia and Cryptosporidium in mammalian wildlife – current status and future needs. Trends in Parasitology 21, 370–376.Google Scholar
Baroudi, D., Khelef, D., Goucem, R., Adjou, K. T., Adamu, H., Zhang, H. and Xiao, L. (2013). Common occurrence of zoonotic pathogen Cryptosporidium meleagridis in broiler chickens and turkeys in Algeria. Veterinary Parasitology 196, 334–340.Google Scholar
Cacciò, S. M., Thompson, R. C., McLauchlin, J. and Smith, H. V. (2005). Unravelling Cryptosporidium and Giardia epidemiology. Trends in Parasitology 21, 430–437.CrossRefGoogle ScholarPubMed
Cacciò, S. M., Beck, R., Almeida, A., Bajer, A. and Pozio, E. (2010). Identification of Giardia species and Giardia duodenalis assemblages by sequence analysis of the 5·8S rDNA gene and internal transcribed spacers. Parasitology 137, 919–925.Google Scholar
Cama, V. A., Bern, C., Roberts, J., Cabrera, L., Sterling, C. R., Ortega, Y., Gilman, R. H. and Xiao, L. (2008). Cryptosporidium species and subtypes and clinical manifestations in children, Peru. Emerging Infectious Diseases 14, 1567–1574.Google Scholar
Carignan, V. and Villard, M.-A. (2002). Selecting indicator species to monitor ecological integrity: a review. Environmental Monitoring and Assessment 78, 45–61.Google Scholar
Castro-Hermida, J. A., García-Presedo, I., Almeida, A., González-Warleta, M., Correia Da Costa, J. M. and Mezo, M. (2009). Detection of Cryptosporidium spp. and Giardia duodenalis in surface water: a health risk for humans and animals. Water Research 43, 4133–4142.Google Scholar
Castro-Hermida, J. A., García-Presedo, I., González-Warleta, M. and Mezo, M. (2010). Cryptosporidium and Giardia detection in water bodies of Galicia, Spain. Water Research 44, 5887–5896.Google Scholar
Clavel, A., Doiz, O., Morales, S., Varea, M., Seral, C., Castillo, F. J., Fleta, J., Rubio, C. and Gómez-Lus, R. (2002). House fly (Musca domestica) as a transport vector of Cryptosporidium parvum . Folia Parasitologica 49, 163–164.CrossRefGoogle ScholarPubMed
Conn, D. B., Weaver, J., Tamang, L. and Graczyk, T. K. (2007). Synanthropic flies as vectors of Cryptosporidium and Giardia among livestock and wildlife in a multispecies agricultural complex. Vector Borne and Zoonotic Diseases 7, 643–651.Google Scholar
Daszak, P., Cunningham, A. A. and Hyatt, A. D. (2001). Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Tropica 78, 103–116.Google Scholar
Feng, Y. and Xiao, L. (2011). Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clinical Microbiology Reviews 24, 110–140.Google Scholar
Fernández, A., Quezada, M., Gómez, M. A., Navarro, J. A., Rodríguez, J. and Sierra, M. A. (1990). Cryptosporidiosis in chickens from southern Spain. Avian Diseases 34, 224–227.Google Scholar
Gomes, R. S., Huber, F., da Silva, S. and do Bomfim, T. C. B. (2012). Cryptosporidium spp. parasitize exotic birds that are commercialized in markets, commercial aviaries, and pet shops. Parasitology Research 110, 1363–1370.Google Scholar
Gómez-Couso, H., Méndez-Hermida, F., Castro-Hermida, J. A. and Ares-Mazás, E. (2005). Giardia in shellfish-farming areas: detection in mussels, river water and waste waters. Veterinary Parasitology 133, 13–18.Google Scholar
Gómez-Couso, H., Méndez-Hermida, F., Castro-Hermida, J. A. and Ares-Mazás, E. (2006). Cryptosporidium contamination in harvesting areas of bivalve molluscs. Journal of Food Protection 69, 185–190.CrossRefGoogle ScholarPubMed
Gracenea, M., Gómez, M. S. and Ramírez, C. M. (2011). Occurrence of Cryptosporidium oocysts and Giardia cysts in water from irrigation channels in Catalonia (NE Spain). Revista Ibero-Latinoamericana de Parasitología 70, 172–177.Google Scholar
Graczyk, T. K., Majewska, A. C. and Schwab, K. J. (2008). The role of birds in dissemination of human waterborne enteropathogens. Trends in Parasitology 24, 55–59.Google Scholar
Gregory, R. D. and Strien, A. V. (2010). Wild bird indicators: using composite population trends of birds as measures of environmental health. Ornithological Science 9, 3–22.Google Scholar
Kuhn, R. C., Rock, C. M. and Oshima, K. H. (2002). Occurrence of Cryptosporidium and Giardia in wild ducks along the Rio Grande River valley in southern New Mexico. Applied and Environmental Microbiology 68, 161–165.Google Scholar
Kutz, S., Thompson, R. and Polley, L. (2009). Wildlife with Giardia: villain or victim and vector? In Giardia and Cryptosporidium: From Molecules to Disease. (eds. Ortega-Pierres, G., Cacciò, S. M., Fayer, R., Mank, T. G., Smith, H. V. and Thompson, R. C. A.), pp. 94–106. Oxford University Press, Oxford.Google Scholar
Lim, Y., Rohela, M. and Shukri, M. M. (2007). Cryptosporidiosis among birds and bird handlers at Zoo Negara, Malaysia. Southeast Asian Journal of Tropical Medicine and Public Health 38, 19–26.Google Scholar
Majewska, A. C., Graczyk, T. K., Slodkowicz-Kowalsk, A., Tamang, L., Jȩdrzejewski, S., Zduniak, P., Solarczyk, P., Nowosad, A. and Nowosad, P. (2009). The role of free-ranging, captive, and domestic birds of Western Poland in environmental contamination with Cryptosporidium parvum oocysts and Giardia lamblia cysts. Parasitology Research 104, 1093–1099.Google Scholar
Matos, O., Alves, M., Xiao, L., Cama, V. and Antunes, F. (2004). Cryptosporidium felis and C. meleagridis in persons with HIV, Portugal. Emerging Infectious Diseases 10, 2256–2257.Google Scholar
McLauchlin, J., Amar, C., Pedraza-Díaz, S. and Nichols, G. L. (2000). Molecular epidemiological analysis of Cryptosporidium spp. in the United Kingdom: results of genotyping Cryptosporidium spp. in 1,705 fecal samples from humans and 105 fecal samples from livestock animals. Journal of Clinical Microbiology 38, 3984–3990.Google Scholar
Méndez-Hermida, F., Gómez-Couso, H., Romero-Suances, R. and Ares-Mazás, E. (2007). Cryptosporidium and Giardia in wild otters (Lutra lutra). Veterinary Parasitology 144, 153–156.Google Scholar
Molina-López, R. A., Ramis, A., Martín-Vázquez, S., Gómez-Couso, H., Ares-Mazás, E., Cacciò, S. M., Leiva, M. and Darwich, L. (2010). Cryptosporidium baileyi infection associated with an outbreak of ocular and respiratory disease in otus owls (Otus scops) in a rehabilitation centre. Avian Pathology 39, 171–176.Google Scholar
Morgan, U. M., Monis, P. T., Xiao, L. H., Limor, J., Sulaiman, I., Raidal, S., O'Donoghue, P., Gasser, R., Murray, A., Fayer, R., Blagburn, B. L., Lal, A. A. and Thompson, R. C. A. (2001). Molecular and phylogenetic characterisation of Cryptosporidium from birds. International Journal for Parasitology 31, 289–296.Google Scholar
Nakamura, A. A., Simões, D. C., Antunes, R. G., da Silva, D. C. and Meireles, M. V. (2009). Molecular characterization of Cryptosporidium spp. from fecal samples of birds kept in captivity in Brazil. Veterinary Parasitology 166, 47–51.Google Scholar
Neira, O., Muñoz, S., Stanley, V., Gosh, C. and Rosales, L. M. (2010). Cryptosporidium parvum in wild gastropods as bioindicators of fecal contamination in terrestrial ecosystems. Revista Chilena de Infectología 27, 211–218.Google Scholar
Ng, J., Pavlasek, I. and Ryan, U. (2006). Identification of novel Cryptosporidium genotypes from avian hosts. Applied and Environmental Microbiology 72, 7548–7553.Google Scholar
Nguyen, S. T., Fukuda, Y., Tada, C., Huynh, V. V., Nguyen, D. T. and Nakai, Y. (2013). Prevalence and molecular characterization of Cryptosporidium in ostriches (Struthio camelus) on a farm in central Vietnam. Experimental Parasitology 133, 8–11.CrossRefGoogle ScholarPubMed
Pagès-Manté, A., Pagès-Bosch, M., Majó-Masferrer, N., Gómez-Couso, H. and Ares-Mazás, E. (2007). An outbreak of disease associated with cryptosporidia on a red-legged partridge (Alectoris rufa) game farm. Avian Pathology 36, 275–278.Google Scholar
Papazahariadou, M., Diakou, A., Papadopoulos, E., Georgopoulou, I., Komnenou, A. and Antoniadou-Sotiriadou, K. (2008). Parasites of the digestive tract in free-ranging birds in Greece. Journal of Natural History 42, 381–398.Google Scholar
Papini, R., Girivetto, M., Marangi, M., Mancianti, F. and Giangaspero, A. (2012). Endoparasite infections in pet and zoo birds in Italy. The Scientific World Journal Article ID 253127, 1–9.Google Scholar
Pérez Cordón, G., Hitos Prados, A., Romero, D., Sánchez Moreno, M., Pontes, A., Osuna, A. and Rosales, M. (2008). Intestinal parasitism in the animals of the zoological garden “Peña Escrita“(Almuñecar, Spain). Veterinary Parasitology 156, 302–309.Google Scholar
Plutzer, J. and Tomor, B. (2009). The role of aquatic birds in the environmental dissemination of human pathogenic Giardia duodenalis cysts and Cryptosporidium oocysts in Hungary. Parasitology International 58, 227–231.Google Scholar
Ponce Gordo, F., Herrera, S., Castro, A. T., García Durán, B. and Martínez Díaz, R. A. (2002). Parasites from farmed ostriches (Struthio camelus) and rheas (Rhea americana) in Europe. Veterinary Parasitology 107, 137–160.Google Scholar
Qi, M., Wang, R., Ning, C., Li, X., Zhang, L., Jian, F., Sun, Y. and Xiao, L. (2011). Cryptosporidium spp. in pet birds: genetic diversity and potential public health significance. Experimental Parasitology 128, 336–340.Google Scholar
Quah, J. X., Ambu, S., Lim, Y. A. L., Mahdy, M. A. K. and Mak, J. W. (2011). Molecular identification of Cryptosporidium parvum from avian hosts. Parasitology 138, 573–577.Google Scholar
Read, C., Walters, J., Robertson, I. D. and Thompson, R. C. (2002). Correlation between genotype of Giardia duodenalis and diarrhoea. International Journal for Parasitology 32, 229–231.CrossRefGoogle ScholarPubMed
Reboredo-Fernández, A., Prado-Merini, O., García-Bernadal, T., Gómez-Couso, H. and Ares-Mazás, E. (2014). Benthic macroinvertebrate communities as aquatic bioindicators of contamination by Giardia and Cryptosporidium . Parasitology Research 113, 1625–1628.Google Scholar
Ryan, U. (2010). Cryptosporidium in birds, fish and amphibians. Experimental Parasitology 124, 113–120.Google Scholar
Ryan, U. and Cacciò, S. M. (2013). Zoonotic potential of Giardia . International Journal for Parasitology 43, 943–956.Google Scholar
Ryan, U. and Xiao, L. (2008). Birds. In Cryptosporidium and Cryptosporidiosis (eds. Fayer, R. and Xiao, L.), pp. 395–418. CRC press, Boca Ratón, Florida.Google Scholar
Ryan, U., Xiao, L., Read, C., Zhou, L., Lal, A. A. and Pavlasek, I. (2003). Identification of novel Cryptosporidium genotypes from the Czech Republic. Applied and Environmental Microbiology 69, 4302–4307.Google Scholar
Ryan, U., Fayer, R. and Xiao, L. (2014). Cryptosporidium species in humans and animals: current understanding and research needs. Parasitology 141, 1667–1685.Google Scholar
Sevá, A. D. P., Funada, M. R., Richtzenhain, L., Guimarães, M. B., Souza, S. D. O., Allegretti, L., Sinhorini, J. A., Duarte, V. V. and Soares, R. M. (2011). Genotyping of Cryptosporidium spp. from free-living wild birds from Brazil. Veterinary Parasitology 175, 27–32.Google Scholar
Thompson, R. C. A. (2013). Parasite zoonoses and wildlife: one health, spillover and human activity. International Journal for Parasitology 43, 1079–1088.CrossRefGoogle ScholarPubMed
Wang, R., Wang, F., Zhao, J., Qi, M., Ning, C., Zhang, L. and Xiao, L. (2012). Cryptosporidium spp. in quails (Coturnix coturnix japonica) in Henan, China: molecular characterization and public health significance. Veterinary Parasitology 187, 534–537.Google Scholar
Wang, Y., Yang, W., Cama, V., Wang, L., Cabrera, L., Ortega, Y., Bern, C., Feng, Y., Gilman, R. and Xiao, L. (2014). Population genetics of Cryptosporidium meleagridis in humans and birds: evidence for cross-species transmission. International Journal for Parasitology 44, 515–521.Google Scholar
Xiao, L. (2010). Molecular epidemiology of cryptosporidiosis: an update. Experimental Parasitology 124, 80–89.Google Scholar
Yong, L. H., Ambu, S., Devi, S. and Maung, M. (2008). Detection of protozoan and bacterial pathogens of public health importance in faeces of Corvus spp. (large-billed crow). Tropical Biomedicine 25, 134–139.Google Scholar
Ziegler, P. E., Wade, S. E., Schaaf, S. L., Stern, D. A., Nadareski, C. A. and Mohammed, H. O. (2007). Prevalence of Cryptosporidium species in wildlife populations within a watershed landscape in southeastern New York State. Veterinary Parasitology 147, 176–184.Google Scholar