Skip to main content

Advertisement

Log in

Evaluation of the initial and chronic phases of toxocariasis after consumption of liver treated by freezing or cooling

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Human toxocariasis is a neglected parasitic zoonosis of worldwide distribution. The consumption of raw or undercooked meat and offal from paratenic hosts of the Toxocara canis nematode can cause infection in humans, but there have been a lack of studies examining specific prophylactic measures to combat this mode of transmission. The aim of this study was to evaluate the establishment of infection by T. canis larvae at the initial and chronic phases of visceral toxocariasis after the consumption of mouse liver subjected to cold treatment. This study was divided into two stages using groups (G) of five donor mice inoculated with 2,000 eggs of T. canis. Two days post-inoculation, the livers of donor mice in G1 and G2 were kept at −20 °C and between 0 and 4 °C, respectively, for 10 days. In the first stage of the study, the livers of mice from G1, G2, and G3 (control) were subjected to a tissue digestion technique and found to be positive for infection. In the second stage, which evaluated infection in mice that had consumed livers from donor mice, receiver mice of G4 and G7 were fed with livers of donor mice from G1 (freezing), receiver mice of G5 and G8 were fed with livers of donor mice from G2 (cooling), and receiver mice of G6 and G9 with livers from G3 (control). Then, the tissue digestion technique was performed for recovering larvae from organs and carcasses of mice, at 2 days (G4, G5, and G6) and 60 days after liver consumption (G7, G8, and G9). It was observed that freezing inhibited the viability of 100 % of the larvae, while cooling promoted 87.7 and 95.7 % reductions in the intensity of infection at 2 and 60 days after liver consumption, respectively. Under the studied conditions, cold treatment shows great potential to help control this parasitosis, both in the initial and chronic phases of toxocariasis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Adang KL, Abdu PA, Ajanusi JO, Oniye SJ, Ezealor AU (2010) Histopathology of Ascaridia galli infection on the liver, lungs, intestines, heart and kidneys of experimentally infected domestic pigeons (C. l. domestica) in Zaria, Nigeria. Pac J Sci Technol 11:511–515

    Google Scholar 

  • Almeida LP, Reis DO, Moreira MD, Oliveira MEF (2003) Viabilidade do Cysticercus bovis em câmara frigorífica à temperatura de −30 °C. Rev Hig Alim 17:97–100

    Google Scholar 

  • Avila LFC, Conceição FR, Telmo PL, Dutra GF, Santos DG Dl, Martins LHR, Berne MEA, Silva PEA, Scaini CJ (2012a) Saccharomyces boulardii reduces infection intensity of mice with toxocariasis. Vet Parasitol 187:337–340

    Article  PubMed  Google Scholar 

  • Avila LFC, Fonseca JSV, Dutra GF, Telmo PL, Silva AMWA, Berne MEA, Silva PEA, Conceição FR, Scaini CJ (2012b) Evaluation of the immunosuppressive effect of cyclophosphamide and dexamethasone in mice with visceral toxocariasis. Parasitol Res 110:443–447

    Article  Google Scholar 

  • Azizi S, Oryan A, Sadjjadi SM, Zibael M (2007) Histopathologic changes and larval recovery of Toxocara cati in experimentally infected chickens. Parasitol Res 102:47–52

    Article  PubMed  CAS  Google Scholar 

  • Borji H, Razmyar J (2012) Aberrant migration of Ascaridia galli in a myna (Acridotheres tristis). Sci Parasitol 13:129–131

    Google Scholar 

  • Boziaris IS, Adams MR (2001) Temperature shock, injury and transient sensitivity to nisin in Gram negatives. J Appl Microbiol 91:715–724

    Article  PubMed  CAS  Google Scholar 

  • Brasil (1999) Portaria CVS 6, de 10/03/1999. Dispõe sobre o regulamento técnico, sobre os parâmetros e critérios para o controle higiênico-sanitário em estabelecimento de alimentos. Diário Oficial do Estado de São Paulo União. Disponível em <http://www.cvs.saude.sp.gov.br>. Acesso em: 05 de maio de 2012

  • Choi D, Lim JH, Choi DC, Paik SW, Kim SH, Huh S (2008) Toxocariasis and ingestion of raw cow liver in patients with eosinophilia. Korean J Parasitol 46:139–143

    Article  PubMed  Google Scholar 

  • Dangoudoubiyam S, Kazacos KR (2009) Differentiation of larva migrans caused by Baylisascaris procyonis and Toxocara species by Western blotting. Clin Vaccine Immunol 16:1563–1568

    Article  PubMed  CAS  Google Scholar 

  • Dubey JP (1988) Long-term persistence of Toxoplasma gondii in tissues of pigs inoculated with T. gondii oocysts and effect of freezing on viability of tissue cysts in pork. Am J Vet Res 49:910–913

    PubMed  CAS  Google Scholar 

  • Dunsmore JD, Thompson RC, Bates IA (1983) The accumulation of Toxocara canis larvae in the brains of mice. Int J Parasitol 13:517–521

    Article  PubMed  CAS  Google Scholar 

  • El-Nawawi FA, Tawfik MA, Shaapan RM (2008) Methods for inactivation of Toxoplasma gondii cysts in meat and tissues of experimentally infected sheep. Foodborne Pathog Dis 5:687–690

    Article  PubMed  Google Scholar 

  • España A, Serna MJ, Rubio M, Redondo P, Quintanilla E (1993) Secondary urticaria due to toxocariasis: possibly caused by ingesting raw cattle meat? J Investig Allergol Clin Immunol 3:51–52

    PubMed  Google Scholar 

  • European Community (2004) Regulation (EC) No. 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2004:139:0055:0205:EN:PDF. Accessed 4 Nov 2010

  • Hill DE, Benedetto SM, Coss C, McCrary JL, Fournet VM, Dubey JP (2006) Effects of time and temperature on the viability of Toxoplasma gondii tissue cysts in enhanced pork loin. J Food Prot 69:1961–1965

    PubMed  CAS  Google Scholar 

  • Hoffmeister B, Glaeser S, Flick H, Pornschlegel S, Suttorp N, Bergmann F (2007) Cerebral toxocariasis after consumption of raw duck liver. AmJTrop Med Hyg 76:600–602

    Google Scholar 

  • Jones JL, Kruszon-Moran D, Won K, Wilson M, Schantz PM (2008) Toxoplasma gondii and Toxocara spp. co-infection. AmJTrop Med Hyg 78:35–39

    Google Scholar 

  • Magnaval JF, Dorchies P, Morassin B (2000) Actualités de la toxocarose humaine. Pyrexie 4:111–115

    Google Scholar 

  • Morimatsu Y, Akao N, Akiyoshi H, Kawazu T, Okabe Y, Aizawa H (2006) A familial case of visceral larva migrans after ingestion of raw chicken livers: appearance of specific antibody in bronchoalveolar lavage fluid of the patients. AmJTrop Med Hyg 75:303–306

    Google Scholar 

  • Pahari TK, Sasmal NK (1990) Experimental infection of mice with Toxocara canis larvae obtained from Japanese quails. Int J Parasitol 20:263–264

    Article  PubMed  CAS  Google Scholar 

  • Park SY, Glaser C, Murray WJ, Kazacos KR, Rowley HA, Fredrick DR, Bass N (2000) Raccoon roundworm (Baylisascaris procyonis) encephalitis: case report and field investigation. Pediatrics 106:E56

    Article  PubMed  CAS  Google Scholar 

  • Perlman JE, Kazacos KR, Imperato GH, Desai RU, Schulman SK, Edwards J, Pontrelli LR, Machado FS, Tanowitz HB, Saffra NA (2010) Baylisascaris procyonis neural larva migrans in an infant in New York City. J Neuroparasitology 1:1–5

    Article  Google Scholar 

  • Rubinsky-Elefant G, Hirata CE, Yamamoto JH, Ferreira MU (2010) Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms. Ann Trop Med Parasitol 104:3–23

    Article  PubMed  CAS  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 

  • Shafir SC, Sorvillo FJ, Sorvillo T, Eberhard ML (2011) Viability of Baylisascaris procyonis eggs. Emerg Infect Dis 17:1293–1295

    Article  PubMed  Google Scholar 

  • Smith H, Holland C, Taylor M, Magnaval JF, Schantz P, Maizels RM (2009) How common is human toxocariasis? Towards standardising our knowledge. Trends Parasitol 25:182–188

    Article  PubMed  Google Scholar 

  • Sotelo J, Rosas N, Palencia G (1986) Freezing of infested pork muscle kills cysticerci. J Am Med Assoc 256:893–894

    Article  CAS  Google Scholar 

  • Sprent JFA (1953) On the migratory behaviour of the larvae of various Ascaris species in white mice. II. Longevity of encapsulated larvae and their resistance to freezing and putrefaction. J Infect Dis 92:114–117

    Article  PubMed  CAS  Google Scholar 

  • Taira K, Permin A, Kapel CMO (2003) Establishment and migration pattern of Toxocara canis larvae in chickens. Parasitol Res 90:521–523

    Article  PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Theodoropoulos G, Kapel CM, Webster P, Saravanos L, Zaki J, Koutsotolis K (2000) Infectivity, predilection sites, and freeze tolerance of Trichinella spp. in experimentally infected sheep. Parasitol Res 86:401–405

    Article  PubMed  CAS  Google Scholar 

  • Tüzer E, Toparlak M, Gargili A, Gülanber A, Keles V, Efil I, Ulutas Esatgil M (2002) Visceral larva migrans in mice caused by eating Toxocara canis-infected chick livers. Turk J Vet Anim Sci 26:293–297

    Google Scholar 

  • Xi WG, Jin LZ (1998) A novel method for the recovery of Toxocara canis in mice. J Helminthol 72:183–184

    Article  PubMed  CAS  Google Scholar 

  • Yoshikawa M, Nishiofuku M, Moriya K, Ouji Y, Ishizaka S, Kasahara K, Mikasa K, 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 

Download references

Acknowledgments

Thanks to the Post-Graduate Program in Public Health for support and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for the scholarship grant for studies. The experiments were carried out following the Federal Government legislation on animal care.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gisele Ferreira Dutra.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dutra, G.F., Pinto, N.S.F., da Costa de Avila, L.F. et al. Evaluation of the initial and chronic phases of toxocariasis after consumption of liver treated by freezing or cooling. Parasitol Res 112, 2171–2175 (2013). https://doi.org/10.1007/s00436-013-3376-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3376-5

Keywords

Navigation