Skip to main content
×
Home

Identification of a novel assemblage G subgenotype and a zoonotic assemblage B in rodent isolates of Giardia duodenalis in the Canary Islands, Spain

  • ÁNGELA FERNÁNDEZ-ÁLVAREZ (a1), AARÓN MARTÍN-ALONSO (a1), NÉSTOR ABREU-ACOSTA (a2), CARLOS FELIU (a3), JEAN-PIERRE HUGOT (a4), BASILIO VALLADARES (a1) and PILAR FORONDA (a1)...
Summary
SUMMARY

The flagellated parasite Giardia duodenalis is known as one of the most common causes of protozoal diarrhoea in both humans and animals worldwide. The aim of the present work was to perform the first study of G. duodenalis in rodents in the Canary Islands (Spain) and analyse the level of genetic variation and the potential zoonotic role of the isolates. Stool samples were collected from 284 wild rodents and Giardia cysts were detected by light microscopy. The overall prevalence of giardiasis was 25·4% and ranged from 19·4% in El Hierro to 34% in Gran Canaria. Positive samples were further characterized by PCR and nucleotide sequencing of the triose phosphate isomerase (TPI), β-giardin (BG) and glutamate dehydrogenase (GDH) genes. Our study revealed assemblage G as the most frequent genotype and identified two rodent-infecting G. duodenalis haplotypes of this assemblage, HI and HII. Phylogenetic analysis supported the monophyly of haplotype HI, which we suggest to be considered as a novel G. duodenalis sub-assemblage GII, due to the high genetic distances among this sub-genotype and assemblage G. Furthermore, G. duodenalis assemblage B was detected in an inhabited area in La Palma, a fact that may pose a potential risk of G. duodenalis transmission from rodents to humans.

Copyright
Corresponding author
* Corresponding author: University Institute of Tropical Diseases and Public Health of the Canary Islands, University of La Laguna. Avda. Astrofísico Fco. Sánchez, s/n 38203 La Laguna, Canary Islands, Spain. E-mail: pforonda@ull.es
References
Hide All
Amar C. F. L., Dear P. H., Pedraza-Diaz S., Looker N., Linnane E. and McLauchlin J. (2002). Sensitive PCR-restriction fragment length polymorphism assay for detection and genotyping of Giardia duodenalis in human feces. Journal of Clinical Microbiology 40, 446452. doi: 10.1128/JCM.40.2.446-452.2002.
Armson A., Yang R., Thompson J., Johnson J., Reid S. and Ryan U. M. (2009). Giardia genotypes in pigs in Western Australia: prevalence and association with diarrhea. Experimental Parasitology 121, 381383. doi: 10.1016/j.exppara.2009.01.008.
Bajer A. (2008). Between-year variation and spatial dynamics of Cryptosporidium spp. and Giardia spp. infections in naturally infected rodent populations. Parasitology 135, 16291649. doi: 10.1017/S0031182008004952.
Bajer A., Bednarska M., Pawelczyk A., Behnke J. M., Gilbert F. S. and Sinski E. (2002). Prevalence and abundance of Cryptosporidium parvum and Giardia spp. in wild rural rodents from the Mazury Lake District region of Poland. Parasitology 125, 2134. doi: 10.1017/S0031182002001865.
Bajer A., Bednarska M., Paziewska A., Romanowski J. and Siński E. (2008). Semi-aquatic animals as a source of water contamination with Cryptosporidium and Giardia . Wiadomości parazytologiczne 54, 315318.
Bednarska M., Bajer A., Sinski E., Girouard A. S., Tamang L. and Graczyk T. K. (2007). Fluorescent in situ hybridization as a tool to retrospectively identify Cryptosporidium parvum and Giardia lamblia in samples from terrestrial mammalian wildlife. Parasitology Research 100, 455460. doi: 10.1007/s00436-006-0276-y.
Bitto A. and Aldras A. (2009). Prevalence of Giardia and Cryptosporidium in muskrats in northeastern Pennsylvania and New Jersey. Journal of Environmental Health 71, 2026.
Cacciò S. M. and Ryan U. (2008). Molecular epidemiology of giardiasis. Molecular and Biochemical Parasitology 160, 7580. doi: 10.1016/j.molbiopara.2008.04.006.
Cacciò S. M., De Giacomo M. and Pozio E. (2002). Sequence analysis of the beta-giardin gene and development of a polymerase chain reaction-restriction fragment length polymorphism assay to genotype Giardia duodenalis cysts from human faecal samples. International Journal for Parasitology 32, 10231030. doi: 10.1016/S0020-7519(02)00068-1.
Castro-Hermida J. A., Almeida A., Gonzalez-Warleta M., Correia da Costa J. M., Rumbo-Lorenzo C. and Mezo M. (2007). Occurrence of Cryptosporidium parvum and Giardia duodenalis in healthy adult domestic ruminants. Parasitology Research 101, 14431448. doi: 10.1007/s00436-007-0624-6.
Coklin T., Farber J., Parrington L. and Dixon B. (2007). Prevalence and molecular characterization of Giardia duodenalis and Cryptosporidium spp. in dairy cattle in Ontario, Canada. Veterinary Parasitology 150, 297305. doi: 10.1016/j.vetpar.2007.09.014.
Covacin C., Aucoin D. P., Elliot A. and Thompson R. C. (2011). Genotypic characterization of Giardia from domestic dogs in the USA. Veterinary Parasitology 177, 2832. doi: 10.1016/j.vetpar.2010.11.029.
De Souza P. N. B., Bomfim T. C. B., Huber F., Abboud L. C. S. and Gomes R. S. (2009). Natural infection by Cryptosporidium sp., Giardia sp. and Eimeria leuckarti in three groups of equines with different handlings in Rio de Janeiro, Brazil. Veterinary Parasitology 160, 327333. doi: 10.1016/j.vetpar.2008.10.103.
Dunlap B. G. and Thies M. L. (2002). Giardia in beaver (Castor canadensis) and nutria (Myocastor coypus) from east Texas. Journal of Parasitology 88, 12541258. doi: 10.1645/0022-3395(2002)088[1254:GIBCCA]2.0.CO;2.
Fayer R., Santín M., Trout J. M., DeStefano S., Koenen K. and Kaur T. (2006). Prevalence of Microsporidia, Cryptosporidium spp., and Giardia spp. in beavers (Castor canadensis) in Massachusetts. Journal of Zoo and Wildlife Medicine 37, 492497. doi: 10.1638/06-013.1.
Felsenstein J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791. doi: 10.2307/2408678.
Foronda P., Del Castillo A., Abreu N., Figueruelo E., Piñero J. and Casanova J. C. (2003). Parasitic helminths of the wild rabbit, Oryctolagus cuniculus, in different bioclimatic zones in Tenerife, Canary Islands. Journal of Helminthology 77, 305309. doi: 10.1079/JOH2003182.
Foronda P., López-González M., Hernández M., Haukisalmi V. and Feliu C. (2011). Distribution and genetic variation of hymenolepidid cestodes in murid rodents on the Canary Islands (Spain). Parasites and Vectors 4, 185. doi: 10.1186/1756-3305-4-185.
Gelanew T., Lalle M., Hailu A., Pozio E. and Cacciò S. M. (2007). Molecular characterization of human isolates of Giardia duodenalis from Ethiopia. Acta Tropica 102, 9299. doi: 10.1016/j.actatropica.2007.04.003.
Hasegawa M., Kishino H. and Yano T. (1985). Dating of the human–ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22, 160174. doi: 10.1007/BF02101694.
Itagaki T., Kinoshita S., Aoki M., Itoh N., Saeki H., Sato N., Uetsuke J., Izumiyama S., Yagita K. and Endo T. (2005). Genotyping of Giardia intestinalis from domestic and wild animals in Japan using glutamate dehydrogenase gene sequencing. Veterinary Parasitology 133, 283287. doi: 10.1016/j.vetpar.2005.05.061.
Kimura M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120. doi: 10.1007/BF01731581.
Kosuwin R., Putaporntip C., Pattanawong U. and Jongwutiwes S. (2010). Clonal diversity in Giardia duodenalis isolates from Thailand: evidences for intragenic recombination and purifying selection at the beta giardin locus. Gene 449, 18. doi: 10.1016/j.gene.2009.09.010.
Lalle M., Pozio E., Capelli G., Bruschi F., Crotti D. and Cacciò S. M. (2005). Genetic heterogeneity at the β-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic sub-genotypes. International Journal for Parasitology 35, 207213. doi: 10.1016/j.ijpara.2004.10.022.
Levecke B., Geldhof P., Claerebout E., Dorny P., Vercammen F., Cacciò S. M., Vercruysse J. and Geurden T. (2009). Molecular characterisation of Giardia duodenalis in captive non-human primates reveals mixed assemblage A and B infections and novel polymorphisms. International Journal for Parasitology 39, 15951601. doi: 10.1016/j.ijpara.2009.05.013.
Levecke B., Meulemans L., Dalemans T., Casaert S., Claerebout E. and Geurden T. (2011). Mixed Giardia duodenalis assemblage A, B, C and E infections in pet chinchillas (Chinchilla lanigera) in Flanders (Belgium). Veterinary Parasitology 177, 166170.
Lv C. C., Feng C., Qi M., Yang H. Y., Jian F. C., Ning C. S. and Zhang L. X. (2009). Investigation on the prevalence of gastrointestinal parasites in pet hamsters. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 27, 279280.
Mendonça C., Almeida A., Castro A., de Lurdes Delgado M., Soares S., da Costa J. M. and Canada N. (2007). Molecular characterization of Cryptosporidium and Giardia isolates from cattle from Portugal. Veterinary Parasitology 147, 4750. doi: 10.1016/j.vetpar.2007.03.019.
Monis P. T., Andrews R. H., Mayrhofer G. and Ey P. L. (2003). Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infection, Genetics and Evolution 3, 2938. doi: 10.1016/S1567-1348(02)00149-1.
Page R. D. M. (1996). TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12, 357358. doi: 10.1093/bioinformatics/12.4.357.
Paziewska A., Bednarska M., Niewegłowski H., Karbowiak G. and Bajer A. (2007). Distribution of Cryptosporidium and Giardia spp. in selected species of protected and game mammals from North-Eastern Poland. Annals of Agricultural Environmental Medicine 14, 265270.
Read C. M., Monis P. T. and Thompson R. C. (2004). Discrimination of all genotypes of Giardia duodenalis at the glutamate dehydrogenase locus using PCR-RFLP. Infection, Genetics and Evolution 4, 125130. doi: 10.1016/j.meegid.2004.02.001.
Richie L. S. (1948). Another sedimentation technique for routine stool examination. US Army Medical Department Journal 8, 326.
Sprong H., Caccio S. M. and van der Giessen J. W. (2012). Identification of zoonotic genotypes of Giardia duodenalis . PLoS Neglected Tropical Diseases 3, e558. doi: 10.1371/journal.pntd.0000558.
Strimmer K. and Haeseler A. (1996). Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Molecular Biology and Evolution 13, 964969.
Sulaiman I. M., Fayer R., Bern C., Gilman R. H., Trout J. M., Schantz P. M., Das P., Lal A. A. and Xiao L. (2003). Triosephosphate isomerase gene characterization and potential zoonotic transmission of Giardia duodenalis . Emerging Infectious Diseases 9, 14441452. doi: 10.3201/eid0911.030084.
Tamura K., Dudley J., Nei M. and Kumar S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599. doi: 10.1093/molbev/msm092.
Thompson R. C. A., Hopkins R. M. and Homan W. L. (2000). Nomenclature and genetic groupings of Giardia infection in mammals. Parasitology Today 16, 210213. doi: 10.1016/S0169-4758(99)01624-5.
Traub R. J., Monis P., Robertson I., Irwin P., Mencke N. and Thompson R. C. (2004). Epidemiological and molecular evidence support the zoonotic transmission of Giardia among humans and dogs living in the same community. Parasitology 128, 5362. doi: 10.1017/S0031182003004505.
Traub R., Wade S., Read C., Thompson A. and Mohammed H. (2005). Molecular characterization of potentially zoonotic isolates of Giardia duodenalis in horses. Veterinary Parasitology 130, 317321. doi: 10.1016/j.vetpar.2005.02.011.
Valladares B., Lopez-Roman R., De Armas F. and Gijon H. (1983). Estudio epidemiológico del parasitismo intestinal humano en el archipiélago canario. Laboratorio 74, 5376.
Young K. H., Bullock S. L., Melvin D. M. and Sprnill C. L. (1979). Ethyl acetate as a substitute for the ethyl ether in the formalin-ether sedimentation technique. Journal of Clinical Microbiology 10, 852853.
Wielinga C. M. and Thompson R. C. A. (2007). Comparative evaluation of Giardia duodenalis sequence data. Parasitology 134, 17951821. doi: 10.1017/S0031182007003071.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 4
Total number of PDF views: 26 *
Loading metrics...

Abstract views

Total abstract views: 205 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 21st November 2017. This data will be updated every 24 hours.