Parasitology Research

, Volume 101, Issue 3, pp 703–708 | Cite as

Evaluation of human IgG class and subclass antibodies to a 24 kDa antigenic component of Gnathostoma spinigerum for the serodiagnosis of gnathostomiasis

  • Porntip Laummaunwai
  • Kittisak Sawanyawisuth
  • Pewpan M. Intapan
  • Verajit Chotmongkol
  • Chaisiri Wongkham
  • Wanchai Maleewong
Original Paper

Abstract

The immunoglobulin G class (total IgG) and subclass (IgG1, IgG2, IgG3, and IgG4) antibody responses to the spirurid worm Gnathostoma spinigerum were analyzed by immunoblotting technique for the antibodies’ potential use in the serodiagnosis of human gnathostomiasis. Serum samples from patients with proven gnathostomiasis and from clinically suspected cases of gnathostomiasis with migratory swelling were tested. Sera from patients with other parasitic illnesses and from healthy volunteers were also analyzed. The total IgG antibody to an antigenic band of approximately 24 kDa from a somatic extract of G. spinigerum advanced third-stage larvae (GS24) gave the highest sensitivity (91.6%) and 87.8% specificity. Individual IgG subclass detection had a lower sensitivity than the detection of specific total IgG antibody, but IgG4 had a slightly higher specificity (93.9%). However, for cost effectiveness, we suggest that anti GS24 total IgG is sufficient for the routine serodiagnosis of human gnathostomiasis as well as for seroepidemiological studies in developing countries.

Notes

Acknowledgement

This investigation was supported by grants from Khon Kaen University and Research and Diagnostic Center for Emerging Infectious Diseases, Khon Kaen University. We thank Dr. Mark Roselieb for improving the English-language presentation of the paper. The use of experimental animals complied with the current laws of Thailand wherein the experiment was performed.

References

  1. Anantaphruti MT, Nuamtanong S, Dekumyoy P (2005) Diagnostic values of IgG4 in human gnathostomiasis. Trop Med Int Health 10:1013–1021PubMedCrossRefGoogle Scholar
  2. Beaver PC, Jung RC, Cupp EW (1984) Clinical parasitology, 9th edn. Lea and Febiger, PhiladelphiaGoogle Scholar
  3. Boongird P, Phuapradit P, Siridej N, Chirachariyavej T, Chuahirun S, Vejjajiva A (1977) Neurological manifestations of gnathostomiasis. J Neurol Sci 31:279–291PubMedCrossRefGoogle Scholar
  4. Chai JY, Han ET, Shin EH, Park JH, Chu JP, Hirota M, Nakamura-Uchiyama F, Nawa Y (2003) An outbreak of gnathostomiasis among Korean emigrants in Myanmar. Am J Trop Med Hyg 69:67–73PubMedGoogle Scholar
  5. Chanteau S, Plichart R, Spiegel A, Martin PM, Cartel JL (1991) Diagnostic values of ELISA-IgG4 as compared to ELISA-IgG and indirect immunofluorescence, for the routine diagnosis of bancroftian filariasis in the South Pacific. Application on capillary blood collected on filter paper. Trop Med Parasitol 42:339–342PubMedGoogle Scholar
  6. Daengsvang S (1981) Gnathostomiasis in Southeast Asia. Southeast Asian J Trop Med Public Health 12:319–332PubMedGoogle Scholar
  7. Dharmkrong-at A, Migasena S, Suntharasamai P, Bunnag D, Priwan R, Sirisinha S (1986) Enzyme-linked immunosorbent assay for detection of antibody to Gnathostoma antigen in patients with intermittent cutaneous migratory swelling. J Clin Microbiol 23:847–851PubMedGoogle Scholar
  8. Diaz Camacho SP, Zazueta Ramos M, Ponce Torrecillas E, Osuna Ramirez I, Castro Velazquez R, Flores Gaxiola A, Baquera Heredia J, Willms K, Akahane H, Ogata K, Nawa Y (1998) Clinical manifestations and immunodiagnosis of gnathostomiasis in Culiacan, Mexico. Am J Trop Med Hyg 59:908–915PubMedGoogle Scholar
  9. Egwang TG, Nguiri C, Kombila M, Duong TH, Richard-Lenoble D (1993) Elevated antifilarial IgG4 antibody levels in microfilaremic and microfilaridermic Gabonese adults and children. Am J Trop Med Hyg 49:135–142PubMedGoogle Scholar
  10. Elkins DB, Haswell-Elkins M, Anderson RM (1986) The epidemiology and control of intestinal helminths in the Pulicat Lake region of Southern India. I. Study design and pre- and post-treatment observations on Ascaris lumbricoides infection. Trans R Soc Trop Med Hyg 80:774–792PubMedCrossRefGoogle Scholar
  11. Feinstein RJ, Rodriguez-Valdes J (1984) Gnathostomiasis, or larva migrans profundus. J Am Acad Dermatol 11:738–740PubMedCrossRefGoogle Scholar
  12. Fleury A, Beltran C, Ferrer E, Garate T, Harrison LJ, Parkhouse RM, Garcia E, Fragoso G, Costa-Cruz J, Biondi G, Agapejev S, Sciutto E (2003) Application of synthetic peptides to the diagnosis of neurocysticercosis. Trop Med Int Health 8:1124–1130PubMedCrossRefGoogle Scholar
  13. Galen RS (1980) Predictive value and efficiency of laboratory testing. Pediatr Clin North Am 27:861–869PubMedGoogle Scholar
  14. Garraud O, Perraut R, Riveau G, Nutman TB (2003) Class and subclass selection in parasite-specific antibody responses. Trends Parasitol 19:300–304PubMedCrossRefGoogle Scholar
  15. Genta RM, Lillibridge JP (1989) Prominence of IgG4 antibodies in the human responses to Strongyloides stercoralis infection. J Infect Dis 160:692–699PubMedGoogle Scholar
  16. Gorgolas M, Santos-O’Connor F, Unzu AL, Fernandez-Guerrero ML, Garate T, Troyas Guarch RM, Grobusch MP (2003) Cutaneous and medullar gnathostomiasis in travelers to Mexico and Thailand. J Travel Med 10:358–361PubMedCrossRefGoogle Scholar
  17. Intapan PM, Maleewong W, Sawanyawisuth K, Chotmongkol V (2003) Evaluation of human IgG subclass antibodies in the serodiagnosis of angiostrongyliasis. Parasitol Res 89:425–429PubMedGoogle Scholar
  18. Iskander R, Das PK, Aalberse RC (1981) IgG4 antibodies in Egyptian patients with schistosomiasis. Int Arch Allergy Appl Immunol 66:200–207PubMedGoogle Scholar
  19. Jaroonvesama N (1988) Differential diagnosis of eosinophilic meningitis. Parasitol Today 4:262–266PubMedCrossRefGoogle Scholar
  20. Jassim A, Hassan K, Catty D (1987) Antibody isotypes in human schistosomiasis mansoni. Parasite Immunol 9:627–650PubMedCrossRefGoogle Scholar
  21. Kong Y, Ito A, Yang HJ, Chung YB, Kasuya S, Kobayashi M, Liu YH, Cho SY (1998) Immunoglobulin G (IgG) subclass and IgE responses in human paragonimiases caused by three different species. Clin Diagn Lab Immunol 5:474–478PubMedGoogle Scholar
  22. Laemmli UK (1970) Cleavage of structural protein during the assembly of the head of bacteriophage T4. Nature 227:680–685PubMedCrossRefGoogle Scholar
  23. Lillywhite JE, Bundy DA, Didier JM, Cooper ES, Bianco AE (1991) Humoral immune responses in human infection with the whipworm Trichuris trichiura. Parasite Immunol 13:491–507PubMedCrossRefGoogle Scholar
  24. Loukas A, Opdebeeck J, Croese J, Prociv P (1996) Immunoglobulin G subclass antibodies against excretory/secretory antigens of Ancylostoma caninum in human enteric infections. Am J Trop Med Hyg 54:672–676PubMedGoogle Scholar
  25. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  26. Maleewong W, Morakote N, Thamasonthi W, Charuchinda K, Tesana S, Khamboonruang C (1988a) Serodiagnosis of human gnathostomiasis. Southeast Asian J Trop Med Public Health 19:201–205PubMedGoogle Scholar
  27. Maleewong W, Sithithaworn P, Tesana S, Morakote N (1988b) Scanning electron microscopy of the early third-stage larvae of Gnathostoma spinigerum. Southeast Asian J Trop Med Public Health 19:643–647PubMedGoogle Scholar
  28. Moore DA, McCroddan J, Dekumyoy P, Chiodini PL (2003) Gnathostomiasis: an emerging imported disease. Emerg Infect Dis 9:647–650PubMedGoogle Scholar
  29. Nawa Y, Maruyama H, Ogata K (1997) Current status of gnathostomiasis dorolesi in Miyazaki Prefecture, Japan. Southeast Asian J Trop Med Public Health 28(Suppl 1):11–13PubMedGoogle Scholar
  30. Nopparatana C, Setasuban P, Chaicumpa W, Tapchaisri P (1991) Purification of Gnathostoma spinigerum specific antigen and immunodiagnosis of human gnathostomiasis. Int J Parasitol 21:677–687PubMedCrossRefGoogle Scholar
  31. Nuchprayoon S, Sanprasert V, Suntravat M, Kraivichian K, Saksirisampant W, Nuchprayoon I (2003) Study of specific IgG subclass antibodies for diagnosis of Gnathostoma spinigerum. Parasitol Res 91:137–143PubMedCrossRefGoogle Scholar
  32. Ogata K, Nawa Y, Akahane H, Diaz Camacho SP, Lamothe-Argumedo R, Cruz-Reyes A (1998) Gnathostomiasis in Mexico. Am J Trop Med Hyg 58:316–318PubMedGoogle Scholar
  33. Ollague W, Ollague J, Guevara de Veliz A, Penaherrera S (1984) Human gnathostomiasis in Ecuador (nodular migratory eosinophilic panniculitis). First finding of the parasite in South America. Int J Dermatol 23:647–651PubMedCrossRefGoogle Scholar
  34. Ottesen EA, Skvaril F, Tripathy SP, Poindexter RW, Hussain R (1985) Prominence of IgG4 in the IgG antibody response to human filariasis. J Immunol 134:2707–2712PubMedGoogle Scholar
  35. Schmutzhard E, Boongird P, Vejjajiva A (1988) Eosinophilic meningitis and radiculomyelitis in Thailand, caused by CNS invasion of Gnathostoma spinigerum and Angiostrongylus cantonensis. J Neurol Neurosurg Psychiatry 51:80–87PubMedCrossRefGoogle Scholar
  36. Suntharasamai P, Desakorn V, Migasena S, Bunnag D, Harinasuta T (1985) ELISA for immunodiagnosis of human gnathostomiasis. Southeast Asian J Trop Med Public Health 16:274–279PubMedGoogle Scholar
  37. Tapchaisri P, Nopparatana C, Chaicumpa W, Setasuban P (1991) Specific antigen of Gnathostoma spinigerum for immunodiagnosis of human gnathostomiasis. Int J Parasitol 21:315–319PubMedCrossRefGoogle Scholar
  38. Towbin H, Staehelin T, Gordon J (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci USA 76:4350–4354PubMedCrossRefGoogle Scholar
  39. Wongkham C, Maleewong W, Ieamviteevanich K, Intapan PM, Morakote N (2000) Antigenic components of Gnathostoma spinigerum recognized by infected human sera by two-dimensional polyacrylamide gel electrophoresis and immunoblotting. Asian Pac J Allergy Immunol 18:47–52PubMedGoogle Scholar
  40. Wongkham C, Intapan PM, Maleewong W, Miwa M (2005) Evaluation of human IgG subclass antibodies in the serodiagnosis of Paragonimiasis heterotremus. Asian Pac J Allergy Immunol 23:205–211PubMedGoogle Scholar
  41. Xuan le T, Rojekittikhun W, Punpoowong B, Trang le N, Hien TV (2002) Case report: intraocular gnathostomiasis in Vietnam. Southeast Asian J Trop Med Public Health 33:485–489PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Porntip Laummaunwai
    • 1
  • Kittisak Sawanyawisuth
    • 2
  • Pewpan M. Intapan
    • 1
  • Verajit Chotmongkol
    • 2
  • Chaisiri Wongkham
    • 3
  • Wanchai Maleewong
    • 1
  1. 1.Department of Parasitology, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  2. 2.Department of Medicine, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand
  3. 3.Department of Biochemistry, Faculty of MedicineKhon Kaen UniversityKhon KaenThailand

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