Archives of Clinical Infectious Diseases

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Strongyloides stercoralis in Immunosuppressed Patients

Marcelo Corti 1 , *
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1 Medicine Department, School of Medicine, Infectious Diseases F. J. Muniz Hospital, Infectious Diseases Orientation, University of Buenos Aires, Buenos Aires, Argentina
Article information
  • Archives of Clinical Infectious Diseases: January 1, 2016, 11 (1); e27510
  • Published Online: January 23, 2016
  • Article Type: Review Article
  • Received: March 15, 2015
  • Revised: September 30, 2015
  • Accepted: October 6, 2015
  • DOI: 10.5812/archcid.27510

To Cite: Corti M. Strongyloides stercoralis in Immunosuppressed Patients, Arch Clin Infect Dis. 2016 ; 11(1):e27510. doi: 10.5812/archcid.27510.

Abstract
Copyright © 2016, Infectious Diseases and Tropical Medicine Research Center. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.
1. Context
2. Evidence Acquisition
3. Results
4. Conclusions
Acknowledgements
References
  • 1. Marcos LA, Terashima A, Dupont HL, Gotuzzo E. Strongyloides hyperinfection syndrome: an emerging global infectious disease. Trans R Soc Trop Med Hyg. 2008; 102(4): 314-8[DOI][PubMed]
  • 2. Bollela VR, Feliciano C, Teixeira AC, Junqueira AC, Rossi MA. Fulminant gastrointestinal hemorrhage due to Strongyloides stercoralis hyperinfection in an AIDS patient. Rev Soc Bras Med Trop. 2013; 46(1): 111-3[PubMed]
  • 3. Olsen A, van Lieshout L, Marti H, Polderman T, Polman K, Steinmann P, et al. Strongyloidiasis--the most neglected of the neglected tropical diseases? Trans R Soc Trop Med Hyg. 2009; 103(10): 967-72[DOI][PubMed]
  • 4. Keiser PB, Nutman TB. Strongyloides stercoralis in the Immunocompromised Population. Clin Microbiol Rev. 2004; 17(1): 208-17[PubMed]
  • 5. Wang C, Xu J, Zhou X, Li J, Yan G, James AA, et al. Strongyloidiasis: an emerging infectious disease in China. Am J Trop Med Hyg. 2013; 88(3): 420-5[DOI][PubMed]
  • 6. Liu LX, Weller PF. Strongyloidiasis and other intestinal nematode infections. Infect Dis Clin North Am. 1993; 7(3): 655-82[PubMed]
  • 7. Scowden EB, Schaffner W, Stone WJ. Overwhelming Strongyloidiasis. Medicine. 1978; 57(6): 527???544[DOI]
  • 8. Paula FM, Costa-Cruz JM. Epidemiological aspects of strongyloidiasis in Brazil. Parasitology. 2011; 138(11): 1331-40[DOI][PubMed]
  • 9. Grove DI. Human Strongyloidiasis. Adv Parasitol. 1996; 38: 251-309[DOI]
  • 10. Evering T, Weiss LM. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006; : 60607032511001[DOI]
  • 11. Manatsathit S, Tansupasawasdikul S, Wanachiwanawin D, Setawarin S, Suwanagool P, Prakasvejakit S, et al. Causes of chronic diarrhea in patients with AIDS in Thailand: a prospective clinical and microbiological study. J Gastroenterol. 1996; 31(4): 533-7[PubMed]
  • 12. Silva CV, Ferreira MS, Borges AS, Costa-Cruz JM. Intestinal parasitic infections in HIV/AIDS patients: experience at a teaching hospital in central Brazil. Scand J Infect Dis. 2005; 37(3): 211-5[DOI][PubMed]
  • 13. Garcia C, Rodriguez E, Do N, Lopez de Castilla D, Terashima A, Gotuzzo E. [Intestinal parasitosis in patients with HIV-AIDS]. Rev Gastroenterol Peru. 2006; 26(1): 21-4[PubMed]
  • 14. Woodring JH, Halfhill 2nd H, Berger R, Reed JC, Moser N. Clinical and imaging features of pulmonary strongyloidiasis. South Med J. 1996; 89(1): 10-9[PubMed]
  • 15. Woodring JH, Halfhill 2nd H, Reed JC. Pulmonary strongyloidiasis: clinical and imaging features. AJR Am J Roentgenol. 1994; 162(3): 537-42[DOI][PubMed]
  • 16. Muniswamappa K, Rao SD, Venkatramana K. Prevalence of Strongyloides stercoralis contaminating Coriandrum obtained from vendors in Karimnagar. Ann Trop Med Public Health. 2012; 5(4): 298[DOI]
  • 17. Davidson RA, Fletcher RH, Chapman LE. Risk factors for strongyloidiasis. A case-control study. Arch Intern Med. 1984; 144(2): 321-4[PubMed]
  • 18. Davidson RA. Infection due to Strongyloides stercoralis in patients with pulmonary disease. South Med J. 1992; 85(1): 28-31[PubMed]
  • 19. Igra-Siegman Y, Kapila R, Sen P, Kaminski ZC, Louria DB. Syndrome of Hyperinfection with Strongyloides stercoralis. Clin Infect Dis. 1981; 3(3): 397-407[DOI]
  • 20. Goyal SB. Intestinal strongyloidiasis manifesting as eosinophilic pleural effusion. South Med J. 1998; 91(8): 768-9[PubMed]
  • 21. Daugherty LE, Chhangani SV. The Syndrome of Hyperacute Strongyloidiasis Infection and Gram Negative Sepsis in an Immunocompromised Patient. Crit Care Shock. 2003; 6: 118-20
  • 22. Smith B, Verghese A, Guiterrez C, Dralle W, Berk SL. Pulmonary strongyloidiasis. Diagnosis by Sputum Gram stain. Am J Med. 1985; 79(5): 663-6[DOI]
  • 23. Wurtz R, Mirot M, Fronda G, Peters C, Kocka F. Short report: gastric infection by Strongyloides stercoralis. Am J Trop Med Hyg. 1994; 51(3): 339-40[PubMed]
  • 24. Roxby AC, Gottlieb GS, Limaye AP. Strongyloidiasis in transplant patients. Clin Infect Dis. 2009; 49(9): 1411-23[DOI][PubMed]
  • 25. Al Maslamani MA, Al Soub HA, Al Khal AL, Al Bozom IA, Abu Khattab MJ, Chacko KC. Strongyloides stercoralis hyperinfection after corticosteroid therapy: a report of two cases. Ann Saudi Med. 2009; 29(5): 397-401[PubMed]
  • 26. Siddiqui AA, Berk SL. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis. 2001; 33(7): 1040-7[DOI][PubMed]
  • 27. Fardet L, Genereau T, Cabane J, Kettaneh A. Severe strongyloidiasis in corticosteroid-treated patients. Clin Microbiol Infect. 2006; 12(10): 945-7[DOI][PubMed]
  • 28. Genta RM. Dysregulation of strongyloidiasis: a new hypothesis. Clin Microbiol Rev. 1992; 5(4): 345-55[PubMed]
  • 29. Schaffel R, Nucci M, Carvalho E, Braga M, Almeida L, Portugal R, et al. The value of an immunoenzymatic test (enzyme-linked immunosorbent assay) for the diagnosis of strongyloidiasis in patients immunosuppressed by hematologic malignancies. Am J Trop Med Hyg. 2001; 65(4): 346-50[PubMed]
  • 30. Cline MJ. A new white cell test which measures individual phagocyte function in a mixed leukocyte population. I. A neutrophil defect in acute myelocytic leukemia. J Lab Clin Med. 1973; 81(2): 311-6[PubMed]
  • 31. Twomey JJ, Laughter AH, Farrow S, Douglass CC. Hodgkin's disease. An immunodepleting and immunosuppressive disorder. J Clin Invest. 1975; 56(2): 467-75[DOI][PubMed]
  • 32. Pickering LK, Ericsson CD, Kohl S. Effect of chemotherapeutic agents on metabolic and bactericidal activity of polymorphonuclear leukocytes. Cancer. 1978; 42(4): 1741-6[PubMed]
  • 33. Incani RN, Hernandez M, Cortez J, Gonzalez ME, Salazar YD. Staphylococcus warneri meningitis in a patient with Strongyloides stercoralis hyperinfection and lymphoma: first report of a case. Rev Inst Med Trop Sao Paulo. 2010; 52(3): 169-70[PubMed]
  • 34. Wirk B, Wingard JR. Strongyloides stercoralis hyperinfection in hematopoietic stem cell transplantation. Transpl Infect Dis. 2009; 11(2): 143-8[DOI][PubMed]
  • 35. Hayashi J, Kishihara Y, Yoshimura E, Furusyo N, Yamaji K, Kawakami Y, et al. Correlation between human T cell lymphotropic virus type-1 and Strongyloides stercoralis infections and serum immunoglobulin E responses in residents of Okinawa, Japan. Am J Trop Med Hyg. 1997; 56(1): 71-5[PubMed]
  • 36. Satoh M, Toma H, Sato Y, Takara M, Shiroma Y, Kiyuna S, et al. Reduced efficacy of treatment of strongyloidiasis in HTLV-I carriers related to enhanced expression of IFN-gamma and TGF-beta1. Clin Exp Immunol. 2002; 127(2): 354-9[PubMed]
  • 37. Liepman M. Disseminated Strongyloides stercoralis. A complication of immunosuppression. JAMA. 1975; 231(4): 387-8[PubMed]
  • 38. Brites C, Goyanna F, Franca LG, Pedroso C, Netto EM, Adriano S, et al. Coinfection by HTLV-I/II is associated with an increased risk of strongyloidiasis and delay in starting antiretroviral therapy for AIDS patients. Braz J Infect Dis. 2011; 15(1): 6-11[PubMed]
  • 39. Walzer PD, Milder JE, Banwell JG, Kilgore G, Klein M, Parker R. Epidemiologic features of Strongyloides stercoralis infection in an endemic area of the United States. Am J Trop Med Hyg. 1982; 31(2): 313-9[PubMed]
  • 40. Barrett-Connor E. Parasitic pulmonary disease. Am Rev Respir Dis. 1982; 126(3): 558-63
  • 41. Cirioni O, Giacometti A, Burzacchini F, Balducci M, Scalise G. Strongyloides stercoralis first-stage larvae in the lungs of a patient with AIDS: primary localization or a noninvasive form of dissemination? Clin Infect Dis. 1996; 22(4): 737[PubMed]
  • 42. Dutcher JP, Marcus SL, Tanowitz HB, Wittner M, Fuks JZ, Wiernik PH. Disseminated strongyloidiasis with central nervous system involvement diagnosed antemortem in a patient with acquired immunodeficiency syndrome and Burkitts lymphoma. Cancer. 1990; 66(11): 2417-20[DOI]
  • 43. Corti M, Villafañe MF, Trione N, Risso D, Abuín JC, Palmieri O. Infección por Strongyloides stercoralis: estudio epidemiológico, clínico, diagnóstico y terapéutico en 30 pacientes. Revista chilena de infectología. 2011; 28(3): 217-22[DOI]
  • 44. Sullivan TJ, Hembree SC. Enhancement of the density of circulating microfilariae with diethylcarbamazine. Trans R Soc Trop Med Hyg. 1970; 64(5): 787-8[PubMed]
  • 45. Bruno P, McAllister K, Matthews JI. Pulmonary strongyloidiasis. South Med J. 1982; 75(3): 363-5[PubMed]
  • 46. Lawn SD. Immune reconstitution disease associated with parasitic infections following initiation of antiretroviral therapy. Curr Opin Infect Dis. 2007; 20(5): 482-8[DOI][PubMed]
  • 47. Brown M, Cartledge JD, Miller RF. Dissemination of Strongyloides stercoralis as an immune restoration phenomenon in an HIV-1-infected man on antiretroviral therapy. Int J STD AIDS. 2006; 17(8): 560-1[DOI][PubMed]
  • 48. Tanaka M, Hirabayashi Y, Gatanaga H, Aizawa S, Hachiya A, Takahashi Y, et al. Reduction in interleukin-2-producing cells but not Th1 to Th2 shift in moderate and advanced stages of human immunodeficiency virus type-1-infection: direct analysis of intracellular cytokine concentrations in CD4+ CD8- T cells. Scand J Immunol. 1999; 50(5): 550-4[PubMed]
  • 49. Petithory JC, Derouin F. Aids and Strongyloidiasis in Africa. Lancet. 1987; 329(8538): 921[DOI]
  • 50. Rivera E, Maldonado N, Velez-Garcia E, Grillo AJ, Malaret G. Hyperinfection syndrome with Strongyloides stercoralis. Ann Intern Med. 1970; 72(2): 199-204[PubMed]
  • 51. Ribeiro LC, Rodrigues Junior EN, Silva MD, Takiuchi A, Fontes CJ. [Purpura in patient with disseminated strongiloidiasis]. Rev Soc Bras Med Trop. 2005; 38(3): 255-7[DOI][PubMed]
  • 52. Chan JFW, Choy BY, Lai KN. Nephrotic Syndrome Secondary to Strongyloidiasis: A Common Infection with an Uncommon Presentation. Hong Kong J Nephrol. 2008; 10(1): 37-41[DOI]
  • 53. Adedayo O, Grell G, Bellot P. Hyperinfective strongyloidiasis in the medical ward: review of 27 cases in 5 years. South Med J. 2002; 95(7): 711-6[PubMed]
  • 54. Ghoshal UC, Ghoshal U, Jain M, Kumar A, Aggarwal R, Misra A, et al. Strongyloides stercoralis infestation associated with septicemia due to intestinal transmural migration of bacteria. J Gastroenterol Hepatol. 2002; 17(12): 1331-3[PubMed]
  • 55. Fagundas LA, Busato O, Brentano L. Strongyloidiasis: fatal complication of renal transplantation. Lancet. 1971; 2(7721): 439-40[PubMed]
  • 56. Wilson S, Thompson AE. A Fatal Case of Strongyloidiasis. J Pathol Bacteriol. 1964; 87: 169-76[PubMed]
  • 57. Giannoulis E, Arvanitakis C, Zaphiropoulos A, Nakos V, Karkavelas G, Haralambidis S. Disseminated strongyloidiasis with uncommon manifestations in Greece. J Trop Med Hyg. 1986; 89(4): 171-8[PubMed]
  • 58. Lima JP, Delgado PG. Diagnosis of strongyloidiasis: importance of Baermann's method. Am J Dig Dis. 1961; 6: 899-904[PubMed]
  • 59. Koga K, Kasuya S, Khamboonruang C, Sukhavat K, Ieda M, Takatsuka N, et al. A modified agar plate method for detection of Strongyloides stercoralis. Am J Trop Med Hyg. 1991; 45(4): 518-21[PubMed]
  • 60. Wong B. Parasitic diseases in immunocompromised hosts. Am J Med. 1984; 76(3): 479-86[DOI]
  • 61. Joseph L, Gyorkos TW, Coupal L. Bayesian estimation of disease prevalence and the parameters of diagnostic tests in the absence of a gold standard. Am J Epidemiol. 1995; 141(3): 263-72[PubMed]
  • 62. Dreyer G, Fernandes-Silva E, Alves S, Rocha A, Albuquerque R, Addiss D. Patterns of detection of Strongyloides stercoralis in stool specimens: implications for diagnosis and clinical trials. J Clin Microbiol. 1996; 34(10): 2569-71[PubMed]
  • 63. Dafalla AA. The indirect fluorescent antibody test for the serodiagnosis of stongyloidiasis. J Trop Med Hyg. 1972; 75(6): 109-11[PubMed]
  • 64. Gam AA, Neva FA, Krotoski WA. Comparative sensitivity and specificity of ELISA and IHA for serodiagnosis of strongyloidiasis with larval antigens. Am J Trop Med Hyg. 1987; 37(1): 157-61[PubMed]
  • 65. Grove DI, Blair AJ. Diagnosis of human strongyloidiasis by immunofluorescence, using Strongyloides ratti and S. stercoralis larvae. Am J Trop Med Hyg. 1981; 30(2): 344-9[PubMed]
  • 66. van Doorn HR, Koelewijn R, Hofwegen H, Gilis H, Wetsteyn JC, Wismans PJ, et al. Use of enzyme-linked immunosorbent assay and dipstick assay for detection of Strongyloides stercoralis infection in humans. J Clin Microbiol. 2007; 45(2): 438-42[DOI][PubMed]
  • 67. Abdul-Fattah MM, Nasr ME, Yousef SM, Ibraheem MI, Abdul-Wahhab SE, Soliman HM. Efficacy of ELISA in diagnosis of strongyloidiasis among the immune-compromised patients. J Egypt Soc Parasitol. 1995; 25(2): 491-8[PubMed]
  • 68. Genta RM, Douce RW, Walzer PD. Diagnostic implications of parasite-specific immune responses in immunocompromised patients with strongyloidiasis. J Clin Microbiol. 1986; 23(6): 1099-103[PubMed]
  • 69. Page WA, Dempsey K, McCarthy JS. Utility of serological follow-up of chronic strongyloidiasis after anthelminthic chemotherapy. Trans R Soc Trop Med Hyg. 2006; 100(11): 1056-62[DOI][PubMed]
  • 70. Rodrigues RM, de Oliveira MC, Sopelete MC, Silva DA, Campos DM, Taketomi EA, et al. IgG1, IgG4, and IgE antibody responses in human strongyloidiasis by ELISA using Strongyloides ratti saline extract as heterologous antigen. Parasitol Res. 2007; 101(5): 1209-14[DOI][PubMed]
  • 71. Agrawal V, Agarwal T, Ghoshal UC. Intestinal strongyloidiasis: a diagnosis frequently missed in the tropics. Trans R Soc Trop Med Hyg. 2009; 103(3): 242-6[DOI][PubMed]
  • 72. Silva LP, Barcelos ISDC, Passos-Lima AB, Espindola FS, Campos DMB, Costa-Cruz JM. Western blotting using Strongyloides ratti antigen for the detection of IgG antibodies as confirmatory test in human strongyloidiasis. Memórias do Instituto Oswaldo Cruz. 2003; 98(5): 687-91[DOI]
  • 73. Mokhlesi B, Shulzhenko O, Garimella PS, Kuma L, Monti C. Pulmonary Strongyloidiasis: The Varied Clinical Presentations. Clin Pulm Med. 2004; 11(1): 6-13[DOI][PubMed]
  • 74. Badparva E, Nayebzadeh H, Barkhordari MH, Ezatpour B. Epidemiological Study of Strongyloides stercoralis With a Comparative Diagnostic Approach, in Lorestan, West of Iran. Arch Clin Infect Dis. 2014; 9(2)[DOI]
  • 75. Boram LH, Keller KF, Justus DE, Collins JP. Strongyloidiasis in immunosuppressed patients. Am J Clin Pathol. 1981; 76(6): 778-81[PubMed]
  • 76. Rivasi F, Pampiglione S, Boldorini R, Cardinale L. Histopathology of gastric and duodenal Strongyloides stercoralis locations in fifteen immunocompromised subjects. Arch Pathol Lab Med. 2006; 130(12): 1792-8[DOI][PubMed]
  • 77. Nomura J, Rekrut K. Strongyloides stercoralis hyperinfection syndrome in a patient with AIDS: diagnosis by fluorescent microscopy. Clin Infect Dis. 1996; 22(4): 736[PubMed]
  • 78. Torres JR, Isturiz R, Murillo J, Guzman M, Contreras R. Efficacy of ivermectin in the treatment of strongyloidiasis complicating AIDS. Clin Infect Dis. 1993; 17(5): 900-2[PubMed]
  • 79. Zhang RY, Chen BJ, Lin JX. Ivermectin in intractable Strongyloides stercoralis infection. Strait J Prevent Med. 2002; 8: 79
  • 80. Gill GV, Bell DR. Strongyloides stercoralis infection in former Far East prisoners of war. bMJ. 1979; 2(6190): 572-4[DOI]
  • 81. Orem J, Mayanja B, Okongo M, Morgan D. Strongyloides stercoralis hyperinfection in a patient with AIDS in Uganda successfully treated with ivermectin. Clin Infect Dis. 2003; 37(1): 152-3[DOI][PubMed]
  • 82. Grove DI. Treatment of strongyloidiasis with thiabendazole: an analysis of toxicity and effectiveness. Tran Royal Soc Trop Med Hygiene. 1982; 76(1): 114-8[DOI]
  • 83. Nandy A, Addy M, Patra P, Bandyopashyay AK. Fulminating strongyloidiasis complicating Indian kala-azar. Trop Geogr Med. 1995; 47(3): 139-41[PubMed]
  • 84. Marti H, Haji HJ, Savioli L, Chwaya HM, Mgeni AF, Ameir JS, et al. A comparative trial of a single-dose ivermectin versus three days of albendazole for treatment of Strongyloides stercoralis and other soil-transmitted helminth infections in children. Am J Trop Med Hyg. 1996; 55(5): 477-81[PubMed]
  • 85. DeVault GA, King JW, Rohr MS, Landreneau MD, Brown ST, McDonald JC. Opportunistic infections with Strongyloides stercoralis in renal transplantation. Rev Infect Dis. 1990; 12(4): 653-71[PubMed]
  • 86. Fowler CG, Lindsay I, Levin J, Sweny P, Fernando ON, Moorhead JF. Recurrent hyperinfestation with Strongyloides stercoralis in a renal allograft recipient. BMJ. 1982; 285(6352): 1394[DOI]
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