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Ultrasonography for early diagnosis of Toxocara canis infection in puppies

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Abstract

Toxocara canis is one of the most common intestinal parasites in dogs and represents a highly infectious zoonotic parasite worldwide. Adult worms live in the bowel of dogs, and infections in puppies are commonly acquired transplacentally. The biology of the parasite and the commonly used diagnostic method, based on faecal examination, often prevent an early diagnosis of toxocariasis in puppies. Ultrasonographic diagnosis of intestinal ascariasis could be a feasible alternative method to diagnose T. canis infection in puppies during the prepatent period. The present study evaluated the diagnostic accuracy of ultrasonography for the diagnosis of intestinal toxocariasis in new-born puppies during the prepatent period. Fifty-four new-born puppies were prospectively recruited in the study. Each dog underwent intestinal ultrasonography and copro-microscopic examination every 5 days, starting from the 10th day post-birth. Intestinal ultrasonography visualized adult T. canis nematodes in the puppies’ small intestine from the 10th day post-birth. On the 15th day after birth, ultrasonography showed 100% specificity and 85.4% sensitivity in diagnosing T. canis infection, despite negative results deriving from the copro-microscopic examination performed at the same time point. Our results showed that ultrasonography can be used as test for early diagnosis of T. canis infection in new-born puppies during the prepatent period. Early ultrasonographic diagnosis of T. canis infection in puppies could help control the disease in dogs and reduce the zoonotic risk for the human population.

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References

  • Barutzki D, Sohaper R (2003) Endoparasites in dogs and cats in Germany 1999-2002. Parasitol Res 90:S148–S150

    Article  PubMed  Google Scholar 

  • Burke TM, Roberson EL (1985) Prenatal and lactational transmission of Toxocara canis and Ancylostoma caninum: experimental infection of the bitch at midpregnancy and at parturition. Int J Parasitol 15:485–490

    Article  PubMed  CAS  Google Scholar 

  • Companion Animal Parasite Council (2014) Guidelines CAPC Vet. In: Guidelines. https://www.capcvet.org/guidelines/

  • Deshayes S, Bonhomme J, de La Blanchardière A (2016) Neurotoxocariasis: a systematic literature review. Infection 44:565–574

    Article  PubMed  CAS  Google Scholar 

  • Dore F, Varcasia A, Pipia AP, Sanna G, Pinna Parpaglia ML, Corda A, Romig T, Scala A (2014) Ultrasound as a monitoring tool for cystic echinococcosis in sheep. Vet Parasitol 203:59–64

    Article  PubMed  CAS  Google Scholar 

  • Elsemore DA, Geng J, Cote J, Hanna R, Lucio-Forster A, Bowman DD (2017) Enzyme-linked immunosorbent assays for coproantigen detection of Ancylostoma caninum and Toxocara canis in dogs and Toxocara cati in cats. J Vet Diagnostic Investig 29:645–653

    Article  CAS  Google Scholar 

  • Epe C (2009) Intestinal nematodes: biology and control. Vet Clin North Am - Small Anim Pract 39:1091–1107

    Article  PubMed  Google Scholar 

  • European Medicines Agency (2017) European Medicines Agency. http://www.ema.europa.eu/ema/index.jsp

  • European Scientific Counsel Companion Animal Parasites (2017) Guidelines | ESCCAP. https://www.esccap.org/guidelines/

  • Fan CK, Holland CV, Loxton K, Barghouth U (2015) Cerebral toxocariasis: silent progression to neurodegenerative disorders? Clin Microbiol Rev 28:663–686

    Article  PubMed  PubMed Central  Google Scholar 

  • Gabrielli S, Tasić-Otašević S, Ignjatović A, Fraulo M, Trenkić-Božinović M, Momčilović S, Cancrini G (2017) Seroprevalence and risk factors for Toxocara canis infection in Serbia during 2015. Foodborne Pathog Dis 14:43–49

    Article  PubMed  CAS  Google Scholar 

  • Genchi C, Di Sacco B, Gatti S et al (1990) Epidemiology of human toxocariasis in northern Italy. Parassitologia 32:313–319

    PubMed  CAS  Google Scholar 

  • Gillespie SH, Pereira M, Ramsay A (1991) The prevalence of Toxocara canis ova in soil samples from parks and gardens in the London area. Public Health 105:335–339

    Article  PubMed  CAS  Google Scholar 

  • Hakim SL, Mak JW, Lam PL (1993) ELISA seropositivity for Toxocara canis antibodies in Malaysia, 1989-1991. Med J Malaysia 48:303–307

    PubMed  CAS  Google Scholar 

  • Hoffmann H, Kawooya M, Esterre P, Ravaoalimalala VE, Roth J, Thomas AK, Roux J, Seitz HM, Doehring E (1997) In vivo and in vitro studies on the sonographical detection of Ascaris lumbricoides. Pediatr Radiol 27:226–229

    Article  PubMed  CAS  Google Scholar 

  • Jacobs DE, Pegg EJ, Stevenson P (1977) Helminths of British dogs: Toxocara canis—a veterinary perspective. J Small Anim Pract 18:79–92

    Article  PubMed  CAS  Google Scholar 

  • Joffe D, Van Niekerk D, Gagné F et al (2011) The prevalence of intestinal parasites in dogs and cats in Calgary, Alberta. Can Vet J 52:1323–1328

    PubMed  PubMed Central  Google Scholar 

  • Kara T (2013) Ultrasonographic appearance of intestinal Ascaris. J Med Ultrason 40:177–178

    Article  Google Scholar 

  • Kroten A, Toczylowski K, Kiziewicz B, Oldak E, Sulik A (2016) Environmental contamination with Toxocara eggs and seroprevalence of toxocariasis in children of northeastern Poland. Parasitol Res 115:205–209

    Article  PubMed  Google Scholar 

  • Lassen B, Janson M, Viltrop A, Neare K, Hütt P, Golovljova I, Tummeleht L, Jokelainen P (2016) Serological evidence of exposure to globally relevant zoonotic parasites in the Estonian population. PLoS One 11:e0164142

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lassen B, Jokelainen P (2016) Survey of the presence of Toxocara spp. eggs in dog feces in Tartu, Estonia. Vector-Borne Zoonotic Dis 16:212–214

    Article  PubMed  Google Scholar 

  • Li L, Gao W, Yang X, Wu D, Bi H, Zhang S, Huang M, Yao X (2014) Asthma and toxocariasis. Ann Allergy Asthma Immunol 113:187–192

    Article  PubMed  Google Scholar 

  • Liu EW, Chastain HM, Shin SH, Wiegand RE, Kruszon-Moran D, Handali S, Jones JL (2018) Seroprevalence of antibodies to Toxocara species in the United States and associated risk factors, 2011-2014. Clin Infect Dis 66:206–212

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ljungström I, van Knapen F (1989) An epidemiological and serological study of Toxocara infection in Sweden. Scand J Infect Dis 21:87–93

    Article  PubMed  Google Scholar 

  • Lloyd S, Amerasinghe PH, Soulsby EJL (1983) Periparturient immunosuppression in the bitch and its influence on infection with Toxocara canis. J Small Anim Pract 24:237–247

    Article  Google Scholar 

  • Ma G, Holland CV, Wang T, Hofmann A, Fan CK, Maizels RM, Hotez PJ, Gasser RB (2018) Human toxocariasis. Lancet Infect Dis 18:e14–e24

    Article  PubMed  Google Scholar 

  • Macpherson CNL (2013) The epidemiology and public health importance of toxocariasis: a zoonosis of global importance. Int J Parasitol 43:999–1008

    Article  PubMed  Google Scholar 

  • Mahmood T, Mansoor N, Quraishy S, Ilyas M, Hussain S (2001) Ultrasonographic appearance of Ascaris lumbricoides in small bowel. J Ultrasound Med 20:269–274

    Article  PubMed  CAS  Google Scholar 

  • Mughini-Gras L, Harms M, van Pelt W, Pinelli E, Kortbeek T (2016) Seroepidemiology of human Toxocara and Ascaris infections in the Netherlands. Parasitol Res 115:3779–3794

    Article  PubMed  Google Scholar 

  • Nielsen MK, Donoghue EM, Stephens ML, Stowe CJ, Donecker JM, Fenger CK (2016) An ultrasonographic scoring method for transabdominal monitoring of ascarid burdens in foals. Equine Vet J 48:380–386

    Article  PubMed  CAS  Google Scholar 

  • Overgaauw PAM (1997a) Aspects of Toxocara epidemiology: toxocarosis in dogs and cats. Crit Rev Microbiol 23:233–251

    Article  PubMed  CAS  Google Scholar 

  • Overgaauw PAM (1997b) Prevalence of intestinal nematodes of dogs and cats in the Netherlands. Vet Q 19:14–17

    Article  PubMed  CAS  Google Scholar 

  • Page AP, Johnstone IL (2007) The cuticle, WormBook, ed. The C. elegans research community, WormBook, https://doi.org/10.1895/wormbook.1.138.1, http://www.wormbook.org.Parsons

  • Parsons JC (1987) Ascarid infections of cats and dogs. Vet Clin North Am - Small Anim Pract 17:1307–1339

    Article  PubMed  CAS  Google Scholar 

  • Peck RJ (1990) Ultrasonography of intestinal ascaris. J Clin Ultrasound 18:741–743

    Article  PubMed  CAS  Google Scholar 

  • Pinelli E, Aranzamendi C (2012) Toxocara infection and its association with allergic manifestations. Endocrine, Metab Immune Disord - Drug Targets 12:33–44

    Article  CAS  Google Scholar 

  • Poeppl W, Herkner H, Tobudic S, Faas A, Mooseder G, Burgmann H, Auer H (2013) Exposure to Echinococcus multilocularis, Toxocara canis, and Toxocara cati in Austria: a nationwide cross-sectional seroprevalence study. Vector-Borne Zoonotic Dis 13:798–803

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Roddie G, Stafford P, Holland C, Wolfe A (2008) Contamination of dog hair with eggs of Toxocara canis. Vet Parasitol 152:85–93

    Article  PubMed  Google Scholar 

  • Salem G, Schantz P (1992) Toxocaral visceral larva migrans after ingestion of raw lamb liver. Clin Infect Dis 15:743–744

    Article  PubMed  CAS  Google Scholar 

  • Scothorn MW, Koutz FR, Groves HF (1965) Prenatal Toxocara canis infection in pups. J Am Vet Med Assoc 146:45–48

    PubMed  CAS  Google Scholar 

  • Stensvold CR, Skov J, Møller LN et al (2009) Seroprevalence of human toxocariasis in Denmark. Clin Vaccine Immunol 16:1372–1373

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Stone WM, Girardeau MH (1967) Transmammary passage of infective-stage nematode larvae. Vet Med Small Anim Clin 62:252–253

    PubMed  CAS  Google Scholar 

  • Szwabe K, Błaszkowska J (2017) Stray dogs and cats as potential sources of soil contamination with zoonotic parasites. Ann Agric Environ Med 24:39–43

    Article  PubMed  Google Scholar 

  • Taira K, Saeed I, Permin A, Kapel CMO (2004) Zoonotic risk of Toxocara canis infection through consumption of pig or poultry viscera. Vet Parasitol 121:115–124

    Article  PubMed  CAS  Google Scholar 

  • Tamponi C, Varcasia A, Pinna S, Melis E, Melosu V, Zidda A, Sanna G, Pipia AP, Zedda MT, Pau S, Brianti E, Scala A (2017) Endoparasites detected in faecal samples from dogs and cats referred for routine clinical visit in Sardinia, Italy. Vet Parasitol Reg Stud Reports 10:13–17

    Article  CAS  PubMed  Google Scholar 

  • Traversa D (2012) Pet roundworms and hookworms: a continuing need for global worming. Parasites and Vectors 5(1):91–19

    Article  PubMed  Google Scholar 

  • Varcasia A, Tanda B, Giobbe M, Solinas C, Pipia AP, Malgor R, Carmona C, Garippa G, Scala A (2011) Cystic Echinococcosis in Sardinia: farmers’ knowledge and dog infection in sheep farms. Vet Parasitol 181:335–340

    Article  PubMed  CAS  Google Scholar 

  • Wigger A, Peppler C, Kramer M (2007) Ultrasonographic appearance of intestinal roundworms in a dog and a cat. Vet Rec 161:200–201

    Article  PubMed  CAS  Google Scholar 

  • Wright I, Stafford K, Coles G (2016) The prevalence of intestinal nematodes in cats and dogs from Lancashire, north-west England. J Small Anim Pract 57:393–395

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa M, Nishiofuku M, Moriya K, Ouji Y, Ishizaka S, Kasahara K, Mikasa KI, Hirai T, Mizuno Y, Ogawa S, Nakamura T, Maruyama H, Akao N (2008) A familial case of visceral toxocariasis due to consumption of raw bovine liver. Parasitol Int 57:525–529

    Article  PubMed  Google Scholar 

  • Yutuc LM (1954) The incidence and prepatent period of Aneyhstoma caninum and Toxocara canis in prenatally infected puppies. J Parasitol 40:18–19

    Google Scholar 

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Authors and Affiliations

  1. Department of Veterinary Medicine, University of Sassari, Via Vienna 2, 07100, Sassari, Italy

    Andrea Corda, Claudia Tamponi, Roberta Meloni, Antonio Varcasia, Maria Luisa Pinna Parpaglia & Antonio Scala

  2. Faculty of Veterinary Medicine, University of Zaragoza, Calle Miguel Servet, 177, 50013, Zaragoza, Spain

    Pablo Gomez-Ochoa

Authors
  1. Andrea Corda
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  2. Claudia Tamponi
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  3. Roberta Meloni
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  4. Antonio Varcasia
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  5. Maria Luisa Pinna Parpaglia
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  6. Pablo Gomez-Ochoa
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  7. Antonio Scala
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Corresponding author

Correspondence to Antonio Varcasia.

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The study protocol was approved by the Ethical Committee of the University of Sassari (Prot. N. 2218 of 15/01/2018), and all dog owners signed an informed consent form before the enrolment of their animals.

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Section Editor: Georg von Samson-Himmelstjerna

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Corda, A., Tamponi, C., Meloni, R. et al. Ultrasonography for early diagnosis of Toxocara canis infection in puppies. Parasitol Res 118, 873–880 (2019). https://doi.org/10.1007/s00436-019-06239-4

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  • DOI: https://doi.org/10.1007/s00436-019-06239-4

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