Japanese Journal of Ophthalmology

, Volume 62, Issue 1, pp 77–83 | Cite as

Toxocariasis: critical analysis of serology in patients attending a public referral center for ophthalmology in Brazil

  • Guita Rubinsky-Elefant
  • Joyce H. Yamamoto
  • Carlos E. Hirata
  • Luiz E. Prestes-Carneiro
Laboratory Investigation
  • 126 Downloads

Abstract

Purpose

To analyze the contribution of IgG anti-Toxocara antibodies in the diagnosis of ocular toxocariasis (OT) in serum samples of patients attending a public referral center for ophthalmology in Brazil and to determine the most frequent ocular signs and symptoms.

Study design

This was a retrospective descriptive study of a cohort of outpatients followed from December 1989 to May 2006.

Methods

IgG anti-Toxocara antibody titers were determined by enzyme-linked immunosorbent assay. The results were correlated with the clinical and funduscopic findings.

Results

Of the diagnoses for the 126 patients, 42 were considered as probable OT, 48 as negative, and 36 as inconclusive. The median IgG anti-Toxocara antibody titers of the patients with probable OT were significantly higher than those of the patients in the negative or inconclusive groups (P = 0.0001). Higher titers were observed more frequently in patients in the probable OT group (P = 0.01) than in the negative group, in which titers were absent or lower in most patients (P < 0.0001). The right eye was affected more in the OT group than in the negative group (P = 0.01), and inflammation was located mostly in the intermediate and posterior poles. The mean age of the patients diagnosed with probable OT was significantly lower (mean, 8 years) than that of the negative patients (mean, 14.5 years) (P = 0.006).

Conclusions

Higher levels of antibodies could help with the diagnosis of OT in patients with symptoms and clinical signs; however, negative results cannot exclude possible OT. Conversely, patients with negative serology or low titers make the diagnosis of OT less likely.

Keywords

Toxocara species Ocular toxocariasis IgG anti-Toxocara antibodies 

Notes

Acknowledgements

This work was supported by Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP Project Number 1234).

Conflicts of interest

G R. -Elefant, None; J. H. Yamamoto, None; C. E. Hirata, None; L. E. P. -Carneiro None.

References

  1. 1.
    Magnaval JF, Glickman LT, Dorchies P, Morassin B. Highlights of human toxocariasis. Korean J Parasitol. 2001;39:1–11.CrossRefPubMedPubMedCentralGoogle Scholar
  2. 2.
    Hotez PJ, Wilkins PP. Toxocariasis: America’s most common neglected infection of poverty and a helminthiasis of global importance? PLoS Negl Trop Dis. 2009;3:e400.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Fillaux J, Magnaval JF. Laboratory diagnosis of human toxocariasis. Vet Parasitol. 2013;193:327–36.CrossRefPubMedGoogle Scholar
  4. 4.
    Despommier D. Toxocariasis: clinical aspects, epidemiology, medical ecology, and molecular aspects. Clin Microbiol Rev. 2003;16:265–72.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    de Visser L, Rothova A, de Boer JH, van Loon AM, Kerkhoff FT, Canninga-van Dijk MR, et al. Diagnosis of ocular toxocariasis by establishing intraocular antibody production. Am J Ophthalmol. 2008;145:369–74.CrossRefPubMedGoogle Scholar
  6. 6.
    Wilkins PP. Immunodiagnosis of human toxocariasis and prospects for improved diagnostics. Curr Trop Med Rep. 2014;1:44–51.CrossRefGoogle Scholar
  7. 7.
    Taylor MR. The epidemiology of ocular toxocariasis. J Helminthol. 2001;75:109–18.PubMedGoogle Scholar
  8. 8.
    Rubinsky-Elefant G, Hirata CE, Yamamoto JH, Ferreira MU. Human toxocariasis: diagnosis, worldwide seroprevalences and clinical expression of the systemic and ocular forms. Ann Trop Med Parasitol. 2010;104:3–23.CrossRefPubMedGoogle Scholar
  9. 9.
    Ahn SJ, Ryoo NK, Woo SJ. Ocular toxocariasis: clinical features, diagnosis, treatment, and prevention. Asia Pac Allergy. 2014;4:134–41.CrossRefPubMedPubMedCentralGoogle Scholar
  10. 10.
    Logar J, Soba B, Kraut A, Stirn-Kranjc B. Seroprevalence of Toxocara antibodies among patients suspected of ocular toxocariasis in Slovenia. Korean J Parasitol. 2004;42:137–40.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Stewart JM, Cubillan LDP, Cunningham ET Jr. Prevalence, clinical features, and causes of vision loss among patients with ocular toxocariasis. Retina. 2005;25:1005–13.CrossRefPubMedGoogle Scholar
  12. 12.
    Sánchez JE, López JP, González M, Villaseca E, Manieu D, Roizen A, et al. Prevalence of ocular lesions in children seropositive to Toxocara canis. Rev Chilena Infect. 2011;28:431–4.CrossRefGoogle Scholar
  13. 13.
    Elefant GR, Shimizu SH, Sanchez MC, Jacob CM, Ferreira AW. A serological follow-up of toxocariasis patients after chemotherapy based on the detection of IgG, IgA, and IgE antibodies by enzyme-linked immunosorbent assay. J Clin Lab Anal. 2006;20:164–72.CrossRefPubMedGoogle Scholar
  14. 14.
    de Savigny DH, Voller A, Woodruff AW. Toxocariasis: serological diagnosis by enzyme immunoassay. J Clin Pathol. 1979;32:284–8.CrossRefPubMedPubMedCentralGoogle Scholar
  15. 15.
    Smith H, Holland C, Taylor M, Magnaval JF, Schantz P, Maizels R. How common is human toxocariasis? Towards standardizing our knowledge. Trends Parasitol. 2009;25:182–8.CrossRefPubMedGoogle Scholar
  16. 16.
    Woodhall D, Starr MC, Montgomery SP, Jones JL, Lum F, Read RW, et al. Ocular toxocariasis: epidemiologic, anatomic, and therapeutic variations based on a survey of ophthalmic subspecialists. Ophthalmology. 2012;119:1211–7.CrossRefPubMedGoogle Scholar
  17. 17.
    Savigny DH. In vitro maintenance of Toxocara canis larvae and a simple method for the production of Toxocara ES antigen for use in serodiagnostic tests for visceral larva migrans. J Parasitol. 1975;61:781–2.CrossRefPubMedGoogle Scholar
  18. 18.
    Kanamura HY, Hoshino-Shimizu S, da Silva LC. Solubilization of antigens of S. mansoni adult worms for the passive hemagglutination test. Preliminary reports. Rev Inst Med Trop Sao Paulo. 1981;23:92–5.PubMedGoogle Scholar
  19. 19.
    Prestes-Carneiro LE, Souza DH, Moreno GC, Troiani C, Santarém V, Zago SC, et al. Toxocariasis/cysticercosis seroprevalence in a long-term rural settlement, São Paulo, Brazil. Parasitology. 2009;136:681–9.CrossRefPubMedGoogle Scholar
  20. 20.
    Cassenote AJ, Lima AR, Pinto Neto JM, Rubinsky-Elefant G. Seroprevalence and modifiable risk factors for Toxocara spp. in Brazilian schoolchildren. PLoS Negl Trop Dis. 2014;8:e2830.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Gillespie SH, Dinning WJ, Voller A, Crowcroft NS. The spectrum of ocular toxocariasis. Eye (Lond). 1993;7:415–8.CrossRefPubMedGoogle Scholar
  22. 22.
    Bae KW, Ahn SJ, Park KH, Woo SJ. Diagnostic value of the serum anti-Toxocara IgG titer for ocular toxocariasis in patients with uveitis at a tertiary Hospital in Korea. Korean J Ophthalmol. 2016;30:258–64.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Jacob CM, Pastorino AC, Peres BA, Mello EO, Okay Y, Oselka GW. Clinical and laboratorial features of visceral toxocariasis in infancy. Rev Inst Med Trop Sao Paulo. 1994;36:19–26.CrossRefPubMedGoogle Scholar
  24. 24.
    Sharkey JA, McKay PS. Ocular toxocariasis in a patient with repeatedly negative ELISA titre to Toxocara canis. Br J Ophthalmol. 1993;77:253–4.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Schantz PM. Toxocara larva migrans now. Am J Trop Med Hyg. 1989;41:21–34.CrossRefPubMedGoogle Scholar
  26. 26.
    Speiser F, Gottstein B. A collaborative study on larval excretory/secretory antigens of Toxocara canis for the immunodiagnosis of human toxocariasis with ELISA. Acta Trop. 1984;41:361–72.PubMedGoogle Scholar
  27. 27.
    Dubinsky P, Akao N, Reiterová K, Konáková G. Comparison of the sensitive screening kit with two ELISA sets for detection of anti-Toxocara antibodies. Southeast Asian J Trop Med Public Health. 2000;31:394–8.PubMedGoogle Scholar
  28. 28.
    Glickman L, Schantz P, Dombroske R, Cypess R. Evaluation of serodiagnostic tests for visceral larva migrans. Am J Trop Med Hyg. 1978;27:492–8.CrossRefPubMedGoogle Scholar
  29. 29.
    Roldán WH, Espinoza YA. Evaluation of an enzyme-linked immunoelectrotransfer blot test for the confirmatory serodiagnosis of human toxocariasis. Mem Inst Oswaldo Cruz. 2009;104:411–8.CrossRefPubMedGoogle Scholar
  30. 30.
    Jacquier P, Gottstein B, Stingelin Y, Eckert J. Immunodiagnosis of toxocarosis in humans: evaluation of a new enzyme-linked immunosorbent assay kit. J Clin Microbiol. 1991;29:1831–5.PubMedPubMedCentralGoogle Scholar
  31. 31.
    Dinning WJ, Gillespie SH, Cooling RJ, Maizels RM. Toxocariasis: a practical approach to management of ocular disease. Eye (Lond). 1988;2:580–2.CrossRefPubMedGoogle Scholar
  32. 32.
    Urban B, Bakunowicz-Łazarczyk A, Michał S. Clinical features, the effectiveness of treatment and function of vision organ in children and adolescents with ocular toxocariasis. Klin Oczna. 2008;110:364–6.PubMedGoogle Scholar
  33. 33.
    Yoshida M, Shirao Y, Asai H, Nagase H, Nakamura H, Okazawa T, et al. A retrospective study of ocular toxocariasis in Japan: correlation with antibody prevalence and ophthalmological findings of patients with uveitis. J Helminthol. 1999;73:357–61.CrossRefPubMedGoogle Scholar
  34. 34.
    Kwon SI, Lee JP, Park SP, Lee EK, Huh S, Park IW. Ocular toxocariasis in Korea. Jpn J Ophthalmol. 2011;55:143–7.CrossRefPubMedGoogle Scholar
  35. 35.
    Seong S, Moon D, Lee DK, Kim HE, Oh HS, Kim SH, et al. A case of ocular toxocariasis successfully treated with albendazole and triamcinolon. Korean J Parasitol. 2014;52:537–40.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 36.
    Centers for Disease Control and Prevention (CDC). Ocular toxocariasis-United States, 2009-2010. MMWR Morb Mortal Wkly Rep. 2011;60:734–6.Google Scholar
  37. 37.
    Yokoi K, Goto H, Sakai J, Usui M. Clinical features of ocular toxocariasis in Japan. Ocul Immunol Inflamm. 2003;11:269–75.CrossRefPubMedGoogle Scholar

Copyright information

© Japanese Ophthalmological Society 2017

Authors and Affiliations

  • Guita Rubinsky-Elefant
    • 1
  • Joyce H. Yamamoto
    • 2
  • Carlos E. Hirata
    • 2
  • Luiz E. Prestes-Carneiro
    • 3
  1. 1.Laboratory of Seroepidemiology and ImmunobiologyInstitute of Tropical Medicine of São PauloSão PauloBrazil
  2. 2.Department of Ophthalmology, Clinics Hospital of the Faculty of MedicineUniversity of São PauloSão PauloBrazil
  3. 3.Infectious Diseases and Immunology DepartmentUniversity of Oeste PaulistaPresidente PrudenteBrazil

Personalised recommendations