The Prevalence and Assemblages of Giardia Duodenalis in Dogs: A Systematic Review in Europe

Mravcová, K.; Štrkolcová, G.; Goldová, M.

doi:10.2478/fv-2019-0036

Abstract

Giardiasis is one of the most frequent causes of diarrhoeic diseases in the world. Giardia cysts are most commonly transferred via ingestion of contaminated water or food. On the basis of genetic characteristics Giardia duodenalis is classified in eight assemblages A—H. Zoonotic assemblages A and B are increasingly found in isolates from dogs which may constitute the reservoir of human giardiasis. This article presents a brief review of G. duodenalis assemblages detected in dogs that were documented in European countries.

References

1. Adam, R. D., 2001: Biology of Giardia lamblia. Clin. Microbiol. Rev., 14, 447—475. DOI: 10.1128/CMR.14.3.447–475.2001.10.1128/CMR.14.3.447475.2001
Open DOI Search in Google Scholar Back to article
2. Bajer, A., 2008: Cryptosporidium and Giardia spp. infections in humans, animals and the environment in Poland. Parasitol. Res., 104, 1, 1—17. DOI:10.1007/s00436-008-1179-x.10.1007/s00436-008-1179-x18791739
Open DOI Search in Google Scholar Back to article
3. Ballweber, L. R., Xiao, L., Bowman, D. D., Kahn, G., Cama, V. A., 2010: Giardiasis in dogs and cats: update on epidemiology and public health significance. Trends in Parasitology, 26, 180—189. DOI: 10.1016/j.pt.2010.02.005.10.1016/j.pt.2010.02.00520202906
Open DOI Search in Google Scholar Back to article
4. Barutzki, D., Schaper, R., 2011: Results of parasitological examinations of faecal samples from cats and dogs in Germany between 2003 and 2010. Parasitol. Res., 1, 45—60. DOI: 10.1007/s00436-011-2402-8.10.1007/s00436-011-2402-821739375
Search in Google Scholar Back to article
5. Beck, R., Sprong, H., Pozio, E., Caccio, S. M., 2012: Geno-typing Giardia duodenalis isolates from dogs: Lessons from a multilocus sequence typing study. Vector-Borne and Zoonotic Diseases, 12, 1—5. DOI: 10.1089/vbz.2011.0751.10.1089/vbz.2011.075122022810
Open DOI Search in Google Scholar Back to article
6. Cacciò, S. M., Beck, R., Lalle, M., Marinculic, A., Pozio, E., 2008: Multilocus genotyping of Giardia duodenalis reveals striking differences between assemblages A and B. Int. J. Parasitol., 38, 1523—1531. DOI: 10.1186/s12866-016-0706-7.10.1186/s12866-016-0706-7487573927209324
Open DOI Search in Google Scholar Back to article
7. Cacciò, S. M., Lalle, M., Svärd, S. G., 2018: Host specificity in the Giardia duodenalis species complex. Infect. Genet. Evol., 66, 335—345. DOI: 10.1016/j.meegid.2017.12.001.10.1016/j.meegid.2017.12.00129225147
Open DOI Search in Google Scholar Back to article
8. Cirak, V. Y., Bauer, C., 2004: Comparison of conventional coproscopical methods and commercial coproantigen ELISA kits for the detection of Giardia and Cryptosporidium infections in dogs and cats. Berl. Munch Tierarztl. Wochenschr., 11, 410—413.
Search in Google Scholar Back to article
9. Claerebout, E., Casaert, S., Dalemans, A. C., De Wilde, N., Levecke, B., Vercruysse, J., Geurden, T., 2009:Giardia and other intestinal parasites in different dog populations in Northern Belgium. Vet. Parasitol., 161, 41—46. DOI: 10.1016/j.vetpar.2008.11.024.10.1016/j.vetpar.2008.11.02419155136
Open DOI Search in Google Scholar Back to article
10. deLucio, A., Bailo, B., Aguilera, M., Cardona, G. A., Fernández-Crespo, J. C., Carmena, D., 2017: No molecular epidemiological evidence supporting household transmission of zoonotic Giardia duodenalis and Cryptosporidium spp. from pet dogs and cats in the province of Álava, Northern Spain. Acta Trop., 170, 48—56. DOI: 10.1016/j.actatropica.2017.02.024.10.1016/j.actatropica.2017.02.02428235458
Search in Google Scholar Back to article
11. Dormond, M., Gutierrez, R. L., Porter, C. K., 2016:Giardia lamblia infection increases risk of chronic gastrointestinal disorders. Trop. Dis. Travel Med. Vaccines, 2, 17. DOI: 10.1186/s40794-016-0030-0.10.1186/s40794-016-0030-0553092528883961
Open DOI Search in Google Scholar Back to article
12. Dubná, S., Langrová, I., Nápravník, J., Jankovská, I., Vadlejch, J., Pekár, S., Fechtner, J., 2007: The prevalence of intestinal parasites in dogs from Prague, rural areas, and shelters of the Czech Republic. Vet. Parasitol., 145, 120—128. DOI: 10.1016/j.vetpar.2006.11.006.10.1016/j.vetpar.2006.11.00617169492
Open DOI Search in Google Scholar Back to article
13. Epe, C., 2009: Intestinal nematodes: biology and control. Vet. Clin. North Am. Small Anim. Pract., 39, 1091—1107. DOI: 10.1016/j.cvsm.2009.07.002.10.1016/j.cvsm.2009.07.00219932365
Open DOI Search in Google Scholar Back to article
14. Escobedo, A. A., Lalle, M., Hrastnik, N. I., Rodríguez-Morales, A. J., Castro-Sánchez, E., Cimerman, S., et al., 2016: Combination therapy in the management of giardiasis: What laboratory and clinical studies tell us, so far. Acta Trop., 162, 196—205. DOI: 10.1016/j.actatropica.2016.06.026.10.1016/j.actatropica.2016.06.02627349189
Open DOI Search in Google Scholar Back to article
15. Feng, Y., Xiao, L., 2011: Zoonotic potential and molecular epidemiology of Giardia species and giardiasis. Clin. Microbiol. Rev., 24, 110—140. DOI: 10.1128/CMR.00033-10.10.1128/CMR.00033-10302120221233509
Open DOI Search in Google Scholar Back to article
16. Fink, M. Y., Singer, S. M., 2017: The Intersection of Immune Responses, Microbiota, and Pathogenesis in Giardiasis. Trends Parasitol., 33, 901—913. DOI: 10.1016/j.pt.2017.08.001.10.1016/j.pt.2017.08.001566094228830665
Open DOI Search in Google Scholar Back to article
17. Geurden, T., Berkvens, D., Casaert, S., Vercruysse, J., Claerebout, E., 2008: A Bayesian evaluation of three diagnostic assays for the detection of Giardia duodenalis in symptomatic and asymptomatic dogs. Vet. Parasitol., 157, 14—20. DOI: 10.1016/j.vetpar.2008.07.002.10.1016/j.vetpar.2008.07.00218723290
Open DOI Search in Google Scholar Back to article
18. Gill, H., Cano, L., deLucio, A., Bailo, B., deMingo, M. H., Cardona, G. A., et al., 2017: Detection and molecular diversity of Giardia duodenalis and Cryptosporidium spp. in sheltered dogs and cats in Northern Spain. Infect. Genet. Evol., 50, 62—69. DOI: 10.1016/j.meegid.2017.02.013.10.1016/j.meegid.2017.02.01328219812
Open DOI Search in Google Scholar Back to article
19. Goldová, M., Valenčáková, A., Mojžišová, J., Halanová, M., Letková, V., Ravaszová, P., 2011: Occurrence of Giardia and Cryptosporidium in dogs. In Southern European Veterinary Conference, Barcelona, Spain, 7—11.
Search in Google Scholar Back to article
20. Györke, A., Kalmár, Z., Dumitrache, M. O., German, C. M., Mircean, V., 2016:Giardia duodenalis genotypes in domestic and wild animals from Romania identified by PCR-RFLP targeting the gdh gene. Vet. Parasitol., 2017, 71—75. DOI: 10.1016/j.vetpar.2015.10.017.10.1016/j.vetpar.2015.10.01726827864
Open DOI Search in Google Scholar Back to article
21. Hinney, B., Gottwald, M., Moser, J., Reicher, B., Schäfer, B. J., Schaper, R., et al., 2017: Examination of anonymous canine faecal samples provides data on endoparasite prevalence rates in dogs for comparative studies. Vet. Parasitol., 245, 106—115. DOI: 10.1016/j.vetpar.2017.08.016.10.1016/j.vetpar.2017.08.01628969828
Open DOI Search in Google Scholar Back to article
22. Hooshyar, H., Rostamkhani, P., Arbabi, M., Delavari, M., 2019:Giardia lamblia infection: review of current diagnostic strategies. Gastroenterol. Hepatol. Bed Bench., 12, 1, 3—12.
Search in Google Scholar Back to article
23. Hořejš, R., Koudela, B., 1994: Giardasis in dogs in a breeding centre (In Czech). Veterinární Medicína, 39, 39—101.
Search in Google Scholar Back to article
24. Itoh, N., Kanai, K., Hori, Y., Hoshi, F., Higuchi, F., 2009: Prevalence of Giardia intestinalis and other zoonotic intestinal parasites in private household dogs of the Hachinohe area in Aomori prefecture, Japan in 1997, 2002 and 2007. J. Vet. Sci., 10, 305—308. DOI: 10.4142/jvs.2009.10.4.305.10.4142/jvs.2009.10.4.305280726619934595
Search in Google Scholar Back to article
25. Joachim, A., Prosl, H., 2005: Giardiose ales oder neues problem ? Vet. J., 12, 18—20.
Search in Google Scholar Back to article
26. Kirkpatrick, C. E., 1988: Epizootology of endoparasitic infections in pet dogs and cats presented to a veterinary teaching hospital. Vet. Parasitol., 30, 113—124.10.1016/0304-4017(88)90158-6
Search in Google Scholar Back to article
27. Kostopoulou, D., Claerebout, E., Arvanitis, D., Ligda, P., Vout- zourakis, N., Casaert, S., Sotiraki, S., 2017: Abundance, zoonotic potential and risk factors of intestinal parasitism amongst dog and cat populations: The scenario of Crete, Greece. Parasit. Vectors, 10, 1—12. DOI: 10.1186/s13071-017-1989-8.10.1186/s13071-017-1989-8526433728122583
Open DOI Search in Google Scholar Back to article
28. Lassen, B., Janson, M., Viltrop, A., Neare, K., Hütt, P., Golovljova, I., et al., 2016: Serological evidence of exposure to globally relevant zoonotic parasites in the Estonian population. PLoS, 11, 1—13. DOI: 10.1371/journal.pone.0164142.10.1371/journal.pone.0164142505671627723790
Open DOI Search in Google Scholar Back to article
29. Lebbad, M., Mattsson, J. G., Christensson, B., Ljungstromd, B., Backhans, A., Andersson, J. O., Svärd, S. G., 2010: From mouse to moose: Multilocus genotyping of Giardia isolates from various animal species. Vet. Parasitol., 168, 231—239. DOI: 10.1016/j.vetpar.2009.11.003.10.1016/j.vetpar.2009.11.00319969422
Open DOI Search in Google Scholar Back to article
30. Lee, M. F., Auer, H., Lindo, J. F., Walochnik, J., 2017: Multilocus sequence analysis of Giardia spp. isolated from patients with diarrhea in Austria. Parasitol. Res., 116, 477—481. DOI: 10.1007/s00436-016-5306-9.10.1007/s00436-016-5306-927885465
Open DOI Search in Google Scholar Back to article
31. Leonhard, S., Pfister, S., Beelitz, P., Wielinga, C., Thompson, R. C. A., 2007: The molecular characterization of Giardia from dogs in southern Germany. Vet. Parasitol., 150, 33—38. DOI: 10.1016/j.vetpar.2007.08.034.10.1016/j.vetpar.2007.08.03417913365
Open DOI Search in Google Scholar Back to article
32. Letková, V., Czismárová, G., Goldová, M., 1999: Importance of carnivores in transmission of parasitoses (In Slovak). In Topical Issues of Parasitology, Košice. 56—59.
Search in Google Scholar Back to article
33. Litleskare, S., Wensaas, K.-A., Eide, G. E., Hanevik, K., Kahrs, G. E., Langeland, N., et al., 2015: Perceived food intolerance and irritable bowel syndrome in a population 3 years after a giardiasis-outbreak: a historical cohort study. BMC Gastroenterol., 15, 164. DOI: 10.1186/s12876-015-0393-0.10.1186/s12876-015-0393-0465384126585714
Open DOI Search in Google Scholar Back to article
34. Mircean, V., Györke, A., Cozma, V., 2012: Prevalence and risk factors of Giardia duodenalis in dogs from Romania. Vet. Parasitol., 184, 325—329. DOI: 10.1016/j.vetpar.2011.08.022.10.1016/j.vetpar.2011.08.02221899952
Open DOI Search in Google Scholar Back to article
35. Neves, D., Lobo L., Simões, L. B., Cardoso, L., 2014: Frequency of intestinal parasites in pet dogs from an urban area (Greater Oporto, northern Portugal). Vet. Parasitol., 200, 295—298. DOI: 10.1016/j.vetpar.2013.11.005.10.1016/j.vetpar.2013.11.00524433853
Open DOI Search in Google Scholar Back to article
36. Nikolić, A., Dimijević, S., Djurković-Djaković, O., Bobić, B., 2002: Giardiasis in dogs and cats in the Belgrade area. Acta Vet.-Beograd, 52, 1, 43—48 DOI: 10.2298/AVB0201043N.10.2298/AVB0201043
Open DOI Search in Google Scholar Back to article
37. Nikolić, A., Dimitrijević, S., Katic-Radivojević, S., Klun, I., Bobić, B., Djurković-Djaković, O., 2008: High prevalence of intestinal zoonotic parasites in dogs from Belgrade, Serbia—short communication. Acta Vet. Hung., 56, 335‒340. DOI:10.1556/AVet.56.2008.3.7.10.1556/AVet.56.2008.3.718828485
Open DOI Search in Google Scholar Back to article
38. Nikolić, A., Klun, I., Bobić, B., Ivović, V., Vujanić, M., Zivković, T., Djurković-Djaković, O., 2011: Human giardiasis in Serbia: asymptomatic vs symptomatic infection. Parasite, 18, 197—201. DOI: 10.1051/parasite/2011182197.10.1051//2011182197
Open DOI Search in Google Scholar Back to article
39. Nikolić, A., Kulišić, Z., Bojkovski, J., 1993: Giardiasis as a zoonosis—the prevalence of Giardia in dogs in Belgrade. Acta Vet.-Beograd, 43, 239—242.
Search in Google Scholar Back to article
40. Omeragič, J., Hrvat, H., Crnkič, Ć., 2015: Occurrence of protozoa in dogs in the area of Tuzla. In Proceedings of the International Congress ‘One World—One Health—One Vision’, Oct 14—16; Sarajevo, Bosnia and Herzegovina. Retrieved July 2019, from: https://www.researchgate.net/publication/322267 355.
Search in Google Scholar Back to article
41. Overgaauw, P. A. M., Zutphen, L., Hoek, D., Yaya, F., Roelfsema, J., Pinelli, E., et al., 2009: Zoonotic parasites in faecal samples and fur from dogs and cats in the Netherlands. Vet. Parasitol., 163, 115—122. DOI: 10.1016/j.vetpar.2009.03.044.10.1016/j.vetpar.2009.03.04419398275
Open DOI Search in Google Scholar Back to article
42. Pallant, L., Barutzki, D., Schaper, R., Thompson R. C. A., 2015: The epidemiology of infections with Giardia species and genotypes in well cared for dogs and cats in Germany. Parasit. Vectors, 2, 1—14. DOI: 10.1186/s13071-014-0615-2.10.1186/s13071-014-0615-2429899425558807
Open DOI Search in Google Scholar Back to article
43. Piekarska, J., Bajzert, J., Gorczykowski, M., Kantyka, M., Podkowik, M., 2016: Molecular identification of Giardia duodenalis isolates from domestic dogs and cats in Wroclaw, Poland. Ann. Agric. Environ. Med., 3, 410—415. DOI: 10.5604/12321966.1219178.10.5604/12321966.121917827660859
Open DOI Search in Google Scholar Back to article
44. Ryan, U., Cacciò, S. M., 2013: Zoonotic potential of Giardia. Int. J. Parasitol., 43, 943—956. DOI: 10.1016/j.ijpara.2013.06.001.10.1016/j.ijpara.2013.06.00123856595
Open DOI Search in Google Scholar Back to article
45. Savioli, L., Smith, H., Thompson, A., 2006:Giardia and Cryptosporidium join the ‘Neglected Diseases Initiative’. Trends Parasitol., 22, 203—208. DOI: 10.1016/j.pt.2006.02.015.10.1016/j.pt.2006.02.01516545611
Open DOI Search in Google Scholar Back to article
46. Scaramozzino, P., DiCave, D., Berrilli, F., D’Orazi, C., Spaziani, A., Mazzani, S., et al., 2009: A study of the prevalence and genotypes of Giardia duodenalis infecting kennelled dogs. Vet. J., 182, 231—234. DOI: 10.1016/j.tvjl.2008.07.003.10.1016/j.tvjl.2008.07.00318715807
Open DOI Search in Google Scholar Back to article
47. Sommer, M. F., 2015:Occurrence and Genetic Determination of Giardia in Dogs from South-Eastern Europe. Dissertation, LMU München, Faculty of Veterinary Medicine, 111 pp.
Search in Google Scholar Back to article
48. Sommer, M. F., Pietschc, M., Kaspara, A., Beelitza, P., 2018: Giardia in a selected population of dogs and cats in Germany — diagnostics, coinfections and assemblages. Vet. Parasitol., 249, 49—56. DOI: 10.1016/j.vetpar.2017.11.006.10.1016/j.vetpar.2017.11.00629279086
Open DOI Search in Google Scholar Back to article
49. Stojecki, K., Sroka, J., Cacciò, S. M., Cencek, T., Dutkiewicz, J., Kusyk, D., 2015: Prevalence and molecular typing of Giardia duodenalis in wildlife from eastern Poland. Folia Parasitol., 62, 1—5. DOI: 10.14411/fp.2015.042.10.14411/fp.2015.04226278650
Search in Google Scholar Back to article
50. Štrkolcová, G., Goldová, M., Halanová, M., 2014: Circulation of giardiasis in selected groups of children and dogs in Košice surroundings (In Slovak). In IXth Seminar of PhD. Students Devoted to the Memory of Academicina Boďa, Košice, 101—104.
Search in Google Scholar Back to article
51. Štrkolcová, G., Maďar, M., Hinney, B., Goldová, M., Mojžišová, J., Halánová, M., 2015: Dog’s genotype of Giardia duodenalis in human: first evidence in Europe. Acta Parasitol., 60, 796—799. DOI: 10.1515/ap-2015-0113.10.1515/ap-2015-011326408607
Open DOI Search in Google Scholar Back to article
52. Svobodová, V., Doležil., Z., 2001: Diagnostic methods of giardiasis (In Czech). Veterinářství, 51, 29—30.
Search in Google Scholar Back to article
53. Svobodová, V., Svoboda, M., Vernerová, E., 2014:Clinical Parasitology of Dog and Cat (In Czech). Publ. House BVM, Prague, 256 pp.
Search in Google Scholar Back to article
54. Szabová, E., Juriš, P., Miterpáková, M., Antolová, D., Papajová, I., Šefčíková, H., 2007: Prevalence of important zoonotic parasites in dog populations from the Slovak Republic. Helminthologia, 44, 170—176.10.2478/s11687-007-0027-3
Search in Google Scholar Back to article
55. Szénási, Z., Marton, S., Kucsera, I., Tánczos, B., Horváth, K., Orosz, E., et al., 2007: Preliminary investigation of the prevalence and genotype distribution of Giardia intestinalis in dogs in Hungary. Parasitol. Res., 101, 145—152. DOI: 10.1007/s00436-007-0622-8.10.1007/s00436-007-0622-8
Open DOI Search in Google Scholar Back to article
56. Upjohn, M., Cobbb, Ch., Mongerb, J., Geurdenc, T., Claereboutc, E., Foxb, M., 2010: Prevalence, molecular typing and risk factor analysis for Giardia duodenalis infections in dogs in a central London rescue shelter. Vet. Parasitol., 172, 341— 346. DOI: 10.1016/j.vetpar.2010.05.010.10.1016/j.vetpar.2010.05.01020609523
Open DOI Search in Google Scholar Back to article
57. Zanzani, S. A., Gazzonis, A. L., Scarpa, P., Berrilli, F., Manfredi, M. A., 2014: Intestinal parasites of owned dogs and cats from metropolitan and micropolitan areas: Prevalence, zoonotic risks, and pet owner awareness in northern Italy. BioMed Res. Int., Apr. 28, Epub., 1—10. DOI: 10.1155/2014/696508.10.1155/2014/696508402219624883320
Open DOI Search in Google Scholar Back to article
58. Zylberberg, H. M., Green, P. H., Turner, K. O., Genta, R. M., Lebwohl, B., 2017: Prevalence and predictors of Giardia in the United States. Dig. Dis. Sci., 62, 432—440. DOI: 10.1007/s10620-016-4447-0.10.1007/s10620-016-4447-028070825
Open DOI Search in Google Scholar Back to article

The Prevalence and Assemblages of Giardia Duodenalis in Dogs: A Systematic Review in Europe

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