Parasitology Research

, Volume 114, Issue 5, pp 1963–1970 | Cite as

Copromicroscopic and molecular investigations on intestinal parasites in kenneled dogs

  • Giulia Simonato
  • Antonio Frangipane di Regalbono
  • Rudi Cassini
  • Donato Traversa
  • Paola Beraldo
  • Cinzia Tessarin
  • Mario Pietrobelli
Original Paper

Abstract

Intestinal parasites are common in dogs worldwide, and their importance has recently increased for a renewed awareness on the public health relevance that some of them have. In this study, the prevalence of helminths and protozoa was evaluated by microscopy in 318 canine faecal samples collected from eight rescue shelters in the North-eastern Italy; 285 of them were also submitted to the molecular characterization of Giardia duodenalis and Cryptosporidium spp. isolates. An analysis was performed to evaluate the prevalence rates in relation to canine individual data, shelter provenance and anthelmintic treatments. Overall, 52.5 % (167/318) of faecal samples were positive for at least one parasite. Trichuris vulpis showed the highest overall prevalence rate (29.2 %), followed by G. duodenalis (15.1 %), Toxocara canis (9.7 %), ancylostomatids (8.2 %) and Cystoisospora (5.7 %). The prevalence of G. duodenalis, evaluated by real-time PCR, was 57.9 % (165/285), and 79 isolates were characterized by nested PCR on the β-giardin gene. The assemblages found were mainly the host-specific genotypes C and D, while only one assemblage was identified as the human-specific genotype B1. Isolates of Cryptosporidium spp., recorded in 3/285 (1.1 %) stool samples, were Cryptosporidium parvum based on the characterization of the Cryptosporidium oocyst wall protein (COWP) gene. Although the results describe a relatively limited risk of dog-originating zoonoses, there is the need to improve the quality of shelter practices towards better health managements for safe pet-adoption campaigns and a minimization of the environmental faecal pollution with canine intestinal parasites.

Keywords

Helminths Protozoa Giardia Cryptosporidium Shelter dog Italy 

References

  1. Ballweber LR, Xiao L, Bowman DD, Kahn G, Cama VA (2010) Giardiasis in dogs and cats: update on epidemiology and public health significance. Trends Parasitol 26:180–189. doi:10.1016/j.pt.2010.02.005 CrossRefPubMedGoogle Scholar
  2. Berrilli F, Di Cave D, De Liberato C, Franco A, Scaramozzino P, Orecchia P (2004) Genotype characterisation of Giardia duodenalis isolates from domestic and farm animals by SSU-rRNA gene sequencing. Vet Parasitol 122:193–199. doi:10.1016/j.vetpar.2004.04.008 CrossRefPubMedGoogle Scholar
  3. Blagburn B, Schenke R, Gagne F, Drake J (2008) Prevalence of intestinal parasites in companion animals in Ontario and Quebec, Canada, during the winter months. Vet Ther 9:169–175PubMedGoogle Scholar
  4. Bowman DD, Lucio-Forster A (2010) Cryptosporidiosis and giardiasis in dogs and cats: veterinary and public health importance. Exp Parasitol 124:121–127. doi:10.1016/j.exppara.2009.01.003 CrossRefPubMedGoogle Scholar
  5. Cama VA, Bern C, Sulaiman IM, Gilman RH, Ticona E, Vivar A, Kawai V, Vargas D, Zhou L, Xiao L (2003) Cryptosporidium species and genotypes in HIV-positive patients in Lima, Peru. J Eukaryot Microbiol 50(Suppl):531–533CrossRefPubMedGoogle Scholar
  6. Capelli G, Paoletti B, Iorio R, Frangipane di Regalbon A, Pietrobelli M, Bianciardi P, Giangaspero A (2003) Prevalence of Giardia spp. in dogs and humans in Northern and Central Italy. Parasitol Res 90:S154–S155. doi:10.1007/s00436-003-0924-4 CrossRefPubMedGoogle Scholar
  7. Capelli G, Frangipane di Regalbono A, Iorio R, Pietrobelli M, Paoletti B, Giangaspero A (2006) Giardia species and other intestinal parasites in dogs in North-east and Central Italy. Vet Rec 159:422–424. doi:10.1002/0471684228.egp05102 CrossRefPubMedGoogle Scholar
  8. Claerebout E, Casaert S, Dalemans AC, 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 CrossRefPubMedGoogle Scholar
  9. Covacin C, Aucoin DP, Elliot A, Thompson RCA (2011) Genotypic characterisation of Giardia from domestic dogs in the USA. Vet Parasitol 177:28–32. doi:10.1016/j.vetpar.2010.11.029 CrossRefPubMedGoogle Scholar
  10. Deplazes P, van Knapen F, Schweiger A, Overgaauw PAM (2011) Role of pet dogs and cats in the transmission of helminthic zoonoses in Europe, with a focus on echinococcosis and toxocarosis. Vet Parasitol 182:41–53. doi:10.1016/j.vetpar.2011.07.014 CrossRefPubMedGoogle Scholar
  11. 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 CrossRefPubMedGoogle Scholar
  12. Epe C, Rehkter G, Schnieder T, Lorentzen L, Kreienbrock L (2010) Giardia in symptomatic dogs and cats in Europe—results of a European study. Vet Parasitol 173:32–38. doi:10.1016/j.vetpar.2010.06.015 CrossRefPubMedGoogle Scholar
  13. ESCAAP (2011) ESCAAP Guideline 06 first edition - control of intestinal protozoa in dogs and cats. http://www.esccap.org/uploads/docs/09t40rlc_esccapgl6_lowres.pdf. Accessed 02 Feb 2015
  14. Fontanarrosa MF, Vezzani D, Basabe J, Eiras DF (2006) An epidemiological study of gastrointestinal parasites of dogs from Southern Greater Buenos Aires (Argentina): age, gender, breed, mixed infections, and seasonal and spatial patterns. Vet Parasitol 136:283–295. doi:10.1016/j.vetpar.2005.11.012 CrossRefPubMedGoogle Scholar
  15. Gates MC, Nolan TJ (2009) Endoparasite prevalence and recurrence across different age groups of dogs and cats. Vet Parasitol 166:153–158. doi:10.1016/j.vetpar.2009.07.041 CrossRefPubMedCentralPubMedGoogle Scholar
  16. Giangaspero A, Iorio R, Paoletti B, Traversa D, Capelli G (2006) Molecular evidence for Cryptosporidium infection in dogs in Central Italy. Parasitol Res 99:297–299. doi:10.1007/s00436-006-0169-0 CrossRefPubMedGoogle Scholar
  17. Giangaspero A, Berrilli F, Brandonisio O (2007) Giardia and Cryptosporidium and public health: the epidemiological scenario from the Italian perspective. Parasitol Res 101:1169–1182. doi:10.1007/s00436-007-0598-4 CrossRefPubMedGoogle Scholar
  18. Guy RA, Payment P, Krull UJ, Horgen PA (2003) Real-time PCR for quantification of Giardia and Cryptosporidium in environmental water samples and sewage. Appl Environ Microbiol 69:5178–5185. doi:10.1128/AEM.69.9.5178 CrossRefPubMedCentralPubMedGoogle Scholar
  19. Hopkins RM, Meloni BP, Groth DM, Wetherall JD, Reynoldson JA, Thompson RCA (1997) Ribosomal RNA sequencing reveals differences between the genotypes of Giardia isolates recovered from humans and dogs living in the same locality. J Parasitol 83:44–51CrossRefPubMedGoogle Scholar
  20. Hunter PR, Thompson RCA (2005) The zoonotic transmission of Giardia and Cryptosporidium. Int J Parasitol 35:1181–1190. doi:10.1016/j.ijpara.2005.07.009 CrossRefPubMedGoogle Scholar
  21. Itoh N, Kanai K, Hori Y, Hoshi F, Higuchi S (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. doi:10.4142/jvs.2009.10.4.305 CrossRefPubMedCentralPubMedGoogle Scholar
  22. Joffe D, Van Niekerk D, Gagné F, Gilleard J, Kutz S, Lobingier R (2011) The prevalence of intestinal parasites in dogs and cats in Calgary, Alberta. Can Vet J 52:1323–1328PubMedCentralPubMedGoogle Scholar
  23. Lalle M, Pozio E, Capelli G, Bruschi F, Crotti D, Cacciò SM (2005) Genetic heterogeneity at the beta-giardin locus among human and animal isolates of Giardia duodenalis and identification of potentially zoonotic subgenotypes. Int J Parasitol 35:207–213. doi:10.1016/j.ijpara.2004.10.022 CrossRefPubMedGoogle Scholar
  24. Lee ACY, Shantz PM, Kazacos KR, Montgomery SP, Bowman DD (2010) Epidemiologic and zoonotic aspects of ascarid infection of dogs and cats. Trends Parasitol 26:155–161. doi:10.1016/j.pt.2010.01.002 CrossRefPubMedGoogle Scholar
  25. Leonhard S, Pfister K, Beelitz P, Wielinga C, Thompson RCA (2007) The molecular characterisation of Giardia from dogs in Southern Germany. Vet Parasitol 150:33–38. doi:10.1016/j.vetpar.2007.08.034 CrossRefPubMedGoogle Scholar
  26. Lucio-Forster A, Griffiths JK, Cama VA, Xiao L, Bowman DD (2010) Minimal zoonotic risk of cryptosporidiosis from pet dogs and cats. Trends Parasitol 26:174–179. doi:10.1016/j.pt.2010.01.004 CrossRefPubMedGoogle Scholar
  27. MAFF (1986) Manual of veterinary parasitological laboratory techniques. Her Majesty's Stationary Office, LondonGoogle Scholar
  28. Meireles P, Montiani-Ferreira F, Thomaz-Soccol V (2008) Survey of giardiosis in household and shelter dogs from metropolitan areas of Curitiba, Paraná state, Southern Brazil. Vet Parasitol 152:242–248. doi:10.1016/j.vetpar.2007.12.025 CrossRefPubMedGoogle Scholar
  29. Monis PT, Andrews RH, Mayrhofer G, Ey PL (2003) Genetic diversity within the morphological species Giardia intestinalis and its relationship to host origin. Infect Genet Evol 3:29–38. doi:10.1016/S1567-1348(02)00149-1 CrossRefPubMedGoogle Scholar
  30. Monis PT, Caccio SM, Thompson RCA (2009) Variation in Giardia: towards a taxonomic revision of the genus. Trends Parasitol 25:93–100. doi:10.1016/j.pt.2008.11.006 CrossRefPubMedGoogle Scholar
  31. Morgan U, Weber R, Xiao L, Sulaiman I, Thompson RCA, Ndiritu W, Lal A, Moore A, Deplazes P (2000) Molecular characterization of Cryptosporidium isolates obtained from human immunodeficiency virus-infected individuals living in Switzerland, Kenya, and the United States. J Clin Microbiol 38:1180–1183PubMedCentralPubMedGoogle Scholar
  32. Neves D, Lobo L, Simões PB, 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 CrossRefPubMedGoogle Scholar
  33. Nikolic A, Dimitrijevic S, Katic-Radivojevic S, Klun I, Bobrc B, Djurkovic-Djakovic O (2008) High prevalence of intestinal zoonotic parasites in dogs from Belgrade, Serbia—short communication. Acta Vet Hung 56:335–340CrossRefPubMedGoogle Scholar
  34. Ortuño A, Castellà J (2011) Intestinal parasites in shelter dogs and risk factors associated with the facility and its management. Isr J Vet Med 66:103–107Google Scholar
  35. Ortuño A, Scorza V, Castellà J, Lappin M (2014) Prevalence of intestinal parasites in shelter and hunting dogs in Catalonia, Northeastern Spain. Vet J 199:465–467. doi:10.1016/j.tvjl.2013.11.022 CrossRefPubMedGoogle Scholar
  36. Palmer CS, Thompson RCA, Traub RJ, Rees R, Robertson ID (2008) National study of the gastrointestinal parasites of dogs and cats in Australia. Vet Parasitol 151:181–190. doi:10.1016/j.vetpar.2007.10.015 CrossRefPubMedGoogle Scholar
  37. Paoletti B, Iorio R, Capelli G, Sparagano OAE, Giangaspero A (2008) Epidemiological scenario of giardiosis in dogs from Central Italy. Ann N Y Acad Sci 1149:371–374. doi:10.1196/annals.1428.005 CrossRefPubMedGoogle Scholar
  38. Pedraza-Díaz S, Amar C, Iversen AM, Stanley PJ, McLauchlin J (2001) Unusual Cryptosporidium species recovered from human faeces: first description of Cryptosporidium felis and Cryptosporidium “dog type” from patients in England. J Med Microbiol 50:293–296PubMedGoogle Scholar
  39. Pieniazek NJ, Bornay-Llinares FJ, Slemenda SB, da Silva AJ, Moura INS, Arrowood MJ, Ditrich O, Addiss DG (1999) New Cryptosporidium genotypes in HIV-infected persons. Emerg Infect Dis 5:444–449. doi:10.3201/eid0503.990318 CrossRefPubMedCentralPubMedGoogle Scholar
  40. Ramírez-Barrios RA, Barboza-Mena G, Muñoz J, Angulo-Cubillán F, Hernández E, González F, Escalona F (2004) Prevalence of intestinal parasites in dogs under veterinary care in Maracaibo, Venezuela. Vet Parasitol 121:11–20. doi:10.1016/j.vetpar.2004.02.024 CrossRefPubMedGoogle Scholar
  41. Read C, Walters J, Robertson ID, Thompson RCA (2002) Correlation between genotype of Giardia duodenalis and diarrhoea. Int J Parasitol 32:229–231CrossRefPubMedGoogle Scholar
  42. Riggio F, Mannella R, Ariti G, Perrucci S (2013) Intestinal and lung parasites in owned dogs and cats from Central Italy. Vet Parasitol 193:78–84. doi:10.1016/j.vetpar.2012.11.026 CrossRefPubMedGoogle Scholar
  43. Rinaldi L, Biggeri A, Carbone S, Musella V, Catelan D, Veneziano V, Cringoli G (2006) Canine faecal contamination and parasitic risk in the city of Naples (Southern Italy). BMC Vet Res 2:29. doi:10.1186/1746-6148-2-29 CrossRefPubMedCentralPubMedGoogle Scholar
  44. Rinaldi L, Maurelli MP, Musella V, Veneziano V, Carbone S, Di Sarno A, Paone M, Cringoli G (2008) Giardia and Cryptosporidium in canine faecal samples contaminating an urban area. Res Vet Sci 84:413–415. doi:10.1016/j.rvsc.2007.05.006 CrossRefPubMedGoogle Scholar
  45. Robertson ID, Thompson RCA (2002) Enteric parasitic zoonoses of domesticated dogs and cats. Microbes Infect 4:867–873CrossRefPubMedGoogle Scholar
  46. Savilla TM, Joy JE, May JD, Somerville CC (2011) Prevalence of dog intestinal nematode parasites in South Central West Virginia, USA. Vet Parasitol 178:115–120. doi:10.1016/j.vetpar.2010.12.034 CrossRefPubMedGoogle Scholar
  47. Scaramozzino P, Di Cave D, Berrilli F, D’Orazi C, Spaziani A, Mazzanti S, Scholl F, De Liberato C (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 CrossRefPubMedGoogle Scholar
  48. Soliman RH, Fuentes I, Rubio JM (2011) Identification of a novel Assemblage B subgenotype and a zoonotic Assemblage C in human isolates of Giardia intestinalis in Egypt. Parasitol Int 60:507–511. doi:10.1016/j.parint.2011.09.006 CrossRefPubMedGoogle Scholar
  49. Sotiriadou I, Pantchev N, Gassmann D, Karanis P (2013) Molecular identification of Giardia and Cryptosporidium from dogs and cats. Parasite 20:8. doi:10.1051/parasite/2013008 CrossRefPubMedCentralPubMedGoogle Scholar
  50. Thompson RCA (2004) The zoonotic significance and molecular epidemiology of Giardia and giardiasis. Vet Parasitol 126:15–35. doi:10.1016/j.vetpar.2004.09.008 CrossRefPubMedGoogle Scholar
  51. Traversa D (2011) Are we paying too much attention to cardio-pulmonary nematodes and neglecting old-fashioned worms like Trichuris vulpis? Parasit Vectors 4:32. doi:10.1186/1756-3305-4-32 CrossRefPubMedCentralPubMedGoogle Scholar
  52. Traversa D (2012) Pet roundworms and hookworms: a continuing need for global worming. Parasit Vectors 5:91. doi:10.1186/1756-3305-5-91 CrossRefPubMedCentralPubMedGoogle Scholar
  53. Traversa D, Frangipane di Regalbono A, Di Cesare A, La Torre F, Drake J, Pietrobelli M (2014) Environmental contamination by canine geohelminths. Parasit Vectors 7:67. doi:10.1186/1756-3305-7-67 CrossRefPubMedCentralPubMedGoogle Scholar
  54. Turkowicz M, Cielecka D (2002) Prevalence of intestinal nematodes in dogs from Warsaw region. Wiad Parazytol 48:407–411PubMedGoogle Scholar
  55. Uehlinger FD, Greenwood SJ, McClure JT, Conboy G, O’Handley R, Barkema HW (2013) Zoonotic potential of Giardia duodenalis and Cryptosporidium spp. and prevalence of intestinal parasites in young dogs from different populations on Prince Edward Island, Canada. Vet Parasitol 196:509–514. doi:10.1016/j.vetpar.2013.03.020 CrossRefPubMedGoogle Scholar
  56. Upjohn M, Cobb C, Monger J, Geurden T, Claerebout E, Fox 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 CrossRefPubMedGoogle Scholar
  57. Verweij JJ, Schinkel J, Laeijendecker D, van Rooyen MAA, van Lieshout L, Polderman AM (2003) Real-time PCR for the detection of Giardia lamblia. Mol Cell Probes 17:223–225. doi:10.1016/S0890-8508(03)00057-4 CrossRefPubMedGoogle Scholar
  58. Wang A, Ruch-Gallie R, Scorza V, Lin P, Lappin MR (2012) Prevalence of Giardia and Cryptosporidium species in dog park attending dogs compared to non-dog park attending dogs in one region of Colorado. Vet Parasitol 184:335–340. doi:10.1016/j.vetpar.2011.08.019 CrossRefPubMedGoogle Scholar
  59. Xiao L, Bern C, Limor J, Sulaiman I, Roberts J, Checkley W, Cabrera L, Gilman RH, Lal AA (2001) Identification of 5 types of Cryptosporidium parasites in children in Lima, Peru. J Infect Dis 183:492–497. doi:10.1086/318090 CrossRefPubMedGoogle Scholar
  60. Yoshiuchi R, Matsubayashi M, Kimata I, Furuya M, Tani H, Sasai K (2010) Survey and molecular characterization of Cryptosporidium and Giardia spp. in owned companion animal, dogs and cats, in Japan. Vet Parasitol 174:313–316. doi:10.1016/j.vetpar.2010.09.004 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Giulia Simonato
    • 1
  • Antonio Frangipane di Regalbono
    • 1
  • Rudi Cassini
    • 1
  • Donato Traversa
    • 2
  • Paola Beraldo
    • 3
  • Cinzia Tessarin
    • 1
  • Mario Pietrobelli
    • 1
  1. 1.Department of Animal Medicine, Production and HealthUniversity of PaduaPaduaItaly
  2. 2.Faculty of Veterinary MedicineUniversity of TeramoTeramoItaly
  3. 3.Department of Food ScienceUniversity of UdineUdineItaly

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