Volume 97, Issue 1
  • ISSN: 0002-9637
  • E-ISSN: 1476-1645



Northwestern Argentina is endemic for soil-transmitted helminths, and annual deworming programs are carried out in prioritized areas. High prevalence of was reported in this area; therefore, control programs including ivermectin are being evaluated. The NIE-enzyme linked immunosorbent assay (ELISA) was used for this purpose. In this community trial, two groups of patients, classified according to housing and living conditions were evaluated. Simultaneous with baseline survey, Group 1 was moved to new households with access to improved water and sanitation facilities (W and S), where deworming (MDA, massive drug administration) took place within 1 month; whereas Group 2 received MDA but remained living with unimproved W and S. The mean time interval between baseline and the follow-up was 331 days for Group 1 and 508 for Group 2. Anti-NIE levels were measured for each individual before and after interventions and follow-up optical density (OD) ratios were calculated to quantify the variation. A significant decrease of the anti-NIE levels between baseline and follow-up was observed in both groups. Nonetheless, the number of patients that achieved the cure criteria (OD ratio < 0.6) was higher in Group 1 than Group 2 with values of 72.7% (24/33) and 45.0% (18/40), respectively ( = 0.0197). Our results support the conclusion that a combined intervention including deworming and improvements in life conditions is more effective, in terms of the proportion of subjects cured than deworming alone. Furthermore, we found that NIE-ELISA is a useful test for assessing the response to treatment and to evaluate the outcome of control intervention programs.


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  1. Socias E, Fernandez A, Gil JF, Krolewiecki AJ, , 2014. Geohelmintiasis en la Argentina una Revisión Sistemática. Med(Buenos Aires) 74: 2936.
  2. World Health Organization, 2011. The Soil Transmitted Helminth Infections. Geneva, Switzerland: World Health Organization, 366.
  3. Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, Stothard R, Thybo SS, Verweij JJ, Magnussen P, , 2009. Strongyloidiasis: the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg 103: 967972.[Crossref]
  4. Bisoffi Z, Buonfrate D, Montresor A, Requena-Méndez A, Muñoz J, Krolewiecki AJ, Gotuzzo E, Mena MA, Chiodini PL, Anselmi M, Moreira J, Albonico M, , 2013. Strongyloides stercoralis: a plea for action. PLoS Negl Trop Dis 7: e2214.[Crossref]
  5. Albonico M, Becker S, Odermatt P, Angheben A, Anselmi M, Amor A, Barda B, Buonfrate D, Cooper P, Gétaz L, Keiser J, Khieu V, Monster A, Muñoz J, Requena-Méndez A, Savioli L, Speare R, Steinmann P, van Lieshout L, Utzinger J, Bisoffi Z, StrongNet Working Group, 2016. StrongNet: an International network to improve diagnostics and access to treatment for strongyloidiasis control. PLoS Negl Trop Dis 10: e0004898.[Crossref]
  6. Echazú A, Bonanno D, Juarez M, Cajal SP, Heredia V, Caropresi S, Cimino RO, Caro N, Vargas PA, Paredes G, Krolewiecki AJ, , 2015. Effect of poor access to water and sanitation as risk factors for soil-transmitted helminth infection: selectiveness by the infective route. PLoS Negl Trop Dis 9: e0004111.[Crossref]
  7. Taranto NJ, Cajal SP, De Marzi MC, Fernández MM, Frank FM, Brú AM, Minvielle MC, Basualdo JA, Malchiodi EL, , 2003. Clinical status and parasitic infection in a Wichí Aboriginal community in Salta, Argentina. Trans R Soc Trop Med Hyg 97: 554558.[Crossref]
  8. Krolewiecki AJ, Ramanathan R, Fink V, McAuliffe I, Cajal SP, Won K, Juarez M, Di Paolo A, Tapia L, Acosta N, Lee R, Lammie P, Abraham D, Nutman TB, , 2010. Improved diagnosis of Strongyloides stercoralis using recombinant antigen-based serologies in a community-wide study in northern Argentina. Clin Vaccine Immunol 17: 16241630.[Crossref]
  9. Altcheh J, Fernandez G, Guarnera E, Gutierrez N, Pizzi H, Taranto N, , 2007. Geohelmintiasis en la Republica de Argentina. Buenos Aires, Argentina: REMEDIAR-Minist Salud la Nación, 1116.
  10. Krolewiecki AJ, Lammie P, Jacobson J, Gabrielli A-F, Levecke B, Socias E, Arias LM, Sosa N, Abraham D, Cimino R, Echazú A, Crudo F, Vercruysse J, Albonico M, , 2013. A public health response against Strongyloides stercoralis: time to look at soil-transmitted helminthiasis in full. PLoS Negl Trop Dis 7: e2165.[Crossref]
  11. Mejia R, Nutman TB, , 2012. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis . Curr Opin Infect Dis 25: 458463.[Crossref]
  12. Requena-Méndez A, Chiodini P, Bisoffi Z, Buonfrate D, Gotuzzo E, Muñoz J, , 2013. The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Negl Trop Dis 7: e2002.[Crossref]
  13. Henriquez-Camacho C, Gotuzzo E, Echevarria J, Clinton White A, Terashima A, Samalvides F, Pérez-Molina JA, Plana MN, , 2016. Ivermectin versus albendazole or thiabendazole for Strongyloides stercoralis infection. Cochrane Database Syst Rev, doi: 10.1002/14651858.CD007745.pub3.
  14. Levenhagen M a, , 2014. Costa-Cruz JM. Update on immunologic and molecular diagnosis of human strongyloidiasis. Acta Trop 135: 3343.[Crossref]
  15. Siddiqui AA, Berk SL, , 2001. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 33: 10401047.[Crossref]
  16. Conway DJ, Lindo JF, Robinson RD, Bundy DAP, , 1995. Towards effective control of Strongyloides stercoralis . Parasitol Today 11: 420423.[Crossref]
  17. Puthiyakunnon S, Boddu S, Li Y, Zhou X, Wang C, Li J, Chen X, , 2014 Strongyloidiasis: an insight into its global prevalence and management. PLoS Negl Trop Dis 8 (8): e3018 .
  18. Sato Y, Kobayashi J, Shiroma Y, , 1995. Serodiagnosis of strongyloidiasis. The application and significance. Rev Inst Med Trop Sao Paulo 37: 3541.[Crossref]
  19. Loutfy MR, Wilson M, Keystone JS, Kain KC, , 2002. Serology and eosinophil count in the diagnosis and management of strongyloidiasis in a non-endemic area. Am J Trop Med Hyg 66: 749752.[Crossref]
  20. Wehner J, Kirsch C, Kagawa F, Jensen W, Campagna A, Wilson M, , 1994. The prevalence and response to therapy of Strongyloides stercoralis in patients with asthma from endemic areas. Chest 106: 762766.[Crossref]
  21. Page WA, Dempsey K, McCarthy JS, , 2006. Utility of serological follow-up of chronic strongyloidiasis after anthelminthic chemotherapy. Trans R Soc Trop Med Hyg 100: 10561062.[Crossref]
  22. Karunajeewa H, Kelly H, Leslie D, Leydon J, Saykao P, Biggs B, , 2006. Parasite-specifi c IgG response and peripheral blood eosinophil count following albendazole treatment for presumed chronic strongyloidiasis. J Travel Med 13: 8491.[Crossref]
  23. Biggs B, Caruana S, Mihrshahi S, Jolley D, Leydon J, Chea L, Nuon S, , 2009. Short report: management of chronic strongyloidiasis in immigrants and refugees: is serologic testing useful? Am J Trop Med Hygeine 80: 788791.
  24. Salvador F, Sulleiro E, Sánchez-Montalvá A, Saugar JM, Rodríguez E, Pahissa A, Molina I, , 2014. Usefulness of Strongyloides stercoralis serology in the management of patients with eosinophilia. Am J Trop Med Hyg 90: 830834.[Crossref]
  25. Bisoffi Z, Buonfrate D, Angheben A, Boscolo M, Anselmi M, Marocco S, Monteiro G, Gobbo M, Bisoffi G, Gobbi F, , 2011. Randomized clinical trial on ivermectin versus thiabendazole for the treatment of strongyloidiasis. PLoS Negl Trop Dis 5: e1254.[Crossref]
  26. Lindo JF, Atkins NS, Lee MG, Robinson RD, Bundy DAP, , 1996. Short report: Long-term serum antibody isotype responses to Strongyloides stercoralis filariform antigens in eight patients treated with ivermectin. Am J Trop Med Hyg 55: 474476.[Crossref]
  27. Ravi V, King TP, Andersen JF, Nutman TB, Neva FA, , 2005. Strongyloides stercoralis recombinant NIE antigen shares epitope with recombinant Ves v 5 and Pol a 5 allergens of insects. Am J Trop Med Hyg 72: 549553.
  28. Ramanathan R, Burbelo PD, Groot S, Iadarola MJ, Neva FA, Nutman TB, , 2008. A luciferase immunoprecipitation systems assay enhances the sensitivity and specificity of diagnosis of Strongyloides stercoralis infection. J Infect Dis 198: 444451.[Crossref]
  29. Buonfrate D, Sequi M, Mejia R, Cimino RO, Krolewiecki AJ, Albonico M, Gobbo M, Bonafini S, Angheben A, Requena-Mendez A, Muñoz J, Nutman TB, , 2015. Accuracy of five serologic tests for Strongyloides stercoralis infection. PLoS Negl Trop Dis 8: 12.
  30. Bisoffi Z, Buonfrate D, Sequi M, Mejia R, Cimino RO, Krolewiecki AJ, Albonico M, Gobbo M, Bonafini S, Angheben A, Requena-Mendez A, Muñoz J, Nutman TB, , 2014. Diagnostic accuracy of five serologic tests for Strongyloides stercoralis infection. PLoS Negl Trop Dis 8: 38.[Crossref]
  31. Garcia LS, , 2007. Diagnostic Medical Parasitology FAQ’s. Spinboro, OH: Hardy Diagnostics.
  32. Ravi V, Ramachandran S, Thompson RW, Andersen JF, Neva FA, , 2002. Characterization of a recombinant immunodiagnostic antigen (NIE) from Strongyloides stercoralis L3-stage larvae. Mol Biochem Parasitol 125: 7381.[Crossref]
  33. Swets JA, , 1988. Measuring the accuracy of diagnostic systems. Science 240: 12851293.[Crossref]
  34. Kobayashi J, Sato Y, Toma H, Takara M, Shiroma Y, , 1994. Application of enzyme immunoassay for post chemotherapy of human strongyloidiasis. Diagn Microbiol Infect Dis 18: 1923.[Crossref]
  35. Grove DI, , 1982. Treatment of strongyloidiasis with thiabendazole: an analysis of toxicity and effectiveness. Trans R Soc Trop Med Hyg 76: 114118.[Crossref]
  36. Satoh M, Toma H, Sato Y, Kikuchi M, Takara M, Shiroma Y, Kiyuna S, Hirayama K, , 1999. Production of a high level of specific IgG4 antibody associated with resistance to albendazole treatment in HLA-DRB1*0901-positive patients with strongyloidiasis. Am J Trop Med Hyg 61: 668671.[Crossref]
  37. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, Utzinger J, , 2012. Effect of sanitation on soil-transmitted helminth infection: systematic review and meta-analysis. PLoS Med 9: e1001162.[Crossref]
  38. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC, , 2014. Water, sanitation, hygiene, and soil-transmitted helminth infection: a systematic review and meta-analysis. PLoS Med 11: e1001620.[Crossref]
  39. Rascoe LN, Price C, Shin SH, McAuliffe I, Priest JW, Handali S, , 2015. Development of Ss-NIE-1 recombinant antigen based assays for immunodiagnosis of strongyloidiasis. PLoS Negl Trop Dis 9: 110.[Crossref]

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  • Received : 30 Oct 2016
  • Accepted : 13 Feb 2017

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