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Strongyloides stercoralis hyperinfection syndrome: a case series and a review of the literature

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Abstract

Background

Strongyloides stercoralis may lead to overwhelming infestation [Strongyloides hyperinfection syndrome (SHS)]. We aimed at describing a case series of patients admitted in intensive care unit (ICU) with SHS and report a literature review of such cases.

Patients and methods

Retrospective multicenter study of 11 patients admitted to the ICU of tertiary hospitals with SHS between 2000 and 2013. Literature review with Pubmed retrieved 122 cases. Logistic regression analysis was performed to identify predictive factors of ICU mortality and shock occurrence.

Results

133 patients [median age 53 (39, 64), 72.2 % males] were included. Underlying immunosuppression was present in 127 patients, mostly long-term corticosteroid treatment in 111 (83.5 %) patients. Fever (80.8 %), respiratory (88.6 %), and gastrointestinal (71.2 %) symptoms were common clinical manifestations. Shock occurred in 75 (57.3 %) patients and mechanical ventilation was required in 89 (67.9 %) patients. Hypereosinophilia and a concomitant bacterial infection were observed in 34 (34.3 %) and 51 (38.4 %) patients, respectively. The in-ICU mortality rate was 60.3 %. Predictive factors of ICU mortality were shock occurrence [Odds ratio (OR) 18.1, 95 % confidence interval (95 % CI) 3.03–107.6, p < 0.01] and mechanical ventilation (OR 28.1, 95 % CI 3.6–217, p < 0.01). Hypereosinophilia (OR 0.21, 95 % CI 0.06–0.7, p = 0.01) and a concomitant bacterial infection (OR 4.68, 95 % CI 1.3–16.8, p = 0.02) were independent predictors of shock occurrence.

Conclusion

SHS remains associated with a poor outcome, especially when associated with shock and mechanical ventilation. Deterioration to shock is often related to concomitant bacterial infection. The poor outcome of established SHS pleads for a large application of antiparasitic primary prophylaxis in at-risk patients.

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References

  1. Siddiqui AA, Berk SL. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis Off Publ Infect Dis Soc Am. 2001;33:1040–7.

    Article  CAS  Google Scholar 

  2. Vadlamudi RS, Chi DS, Krishnaswamy G. Intestinal strongyloidiasis and hyperinfection syndrome. Clin Mol Allergy CMA. 2006;4:8.

    Article  PubMed  Google Scholar 

  3. Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, et al. Strongyloides stercoralis: global Distribution and Risk Factors. Plos Negl Trop Dis. 2013;7:e2288.

    Article  PubMed Central  PubMed  Google Scholar 

  4. Ramanathan R, Nutman T. Strongyloides stercoralis infection in the immunocompromised host. Curr Infect Dis Rep. 2008;10:105–10.

    Article  PubMed Central  PubMed  Google Scholar 

  5. Keiser PB, Nutman TB. Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev. 2004;17:208–17.

    Article  PubMed Central  PubMed  Google Scholar 

  6. Concha R, Harrington W Jr, Rogers AI. Intestinal strongyloidiasis: recognition, management, and determinants of outcome. J Clin Gastroenterol. 2005;39:203–11.

    Article  PubMed  Google Scholar 

  7. Debussche X, Toublanc M, Camillieri JP, Assan R. Overwhelming strongyloidiasis in a diabetic patient following ACTH treatment and keto-acidosis. Diabète Métabolisme. 1988;14:294–8.

    CAS  PubMed  Google Scholar 

  8. Rivera E, Maldonado N, Vélez-García E, Grillo AJ, Malaret G. Hyperinfection syndrome with Strongyloides stercoralis. Ann Intern Med. 1970;72:199–204.

    Article  CAS  PubMed  Google Scholar 

  9. Milder JE, Walzer PD, Kilgore G, Rutherford I, Klein M. Clinical features of Strongyloides stercoralis infection in an endemic area of the United States. Gastroenterology. 1981;80:1481–8.

    CAS  PubMed  Google Scholar 

  10. Montes M, Sanchez C, Verdonck K, Lake JE, Gonzalez E, Lopez G, et al. Regulatory T cell expansion in HTLV-1 and strongyloidiasis co-infection is associated with reduced IL-5 responses to Strongyloides stercoralis antigen. Plos Negl Trop Dis. 2009;3:e456.

    Article  PubMed Central  PubMed  Google Scholar 

  11. Porto AF, Neva FA, Bittencourt H, Lisboa W, Thompson R, Alcântara L, et al. HTLV-1 decreases Th2 type of immune response in patients with strongyloidiasis. Parasite Immunol. 2001;23:503–7.

    Article  CAS  PubMed  Google Scholar 

  12. Blankenhaus B, Klemm U, Eschbach M-L, Sparwasser T, Huehn J, Kühl AA, et al. Strongyloides ratti infection induces expansion of Foxp3+ regulatory T cells that interfere with immune response and parasite clearance in BALB/c mice. J Immunol Baltim Md. 1950;2011(186):4295–305.

    Google Scholar 

  13. Galioto AM, Hess JA, Nolan TJ, Schad GA, Lee JJ, Abraham D. Role of eosinophils and neutrophils in innate and adaptive protective immunity to larval strongyloides stercoralis in mice. Infect Immun. 2006;74:5730–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  14. Herbert DR, Lee JJ, Lee NA, Nolan TJ, Schad GA, Abraham D. Role of IL-5 in innate and adaptive immunity to larval Strongyloides stercoralis in mice. J Immunol Baltim Md. 1950;2000(165):4544–51.

    Google Scholar 

  15. Kerepesi LA, Hess JA, Nolan TJ, Schad GA, Abraham D. Complement component C3 is required for protective innate and adaptive immunity to larval strongyloides stercoralis in mice. J Immunol Baltim Md. 1950;2006(176):4315–22.

    Google Scholar 

  16. Rotman HL, Yutanawiboonchai W, Brigandi RA, Leon O, Gleich GJ, Nolan TJ, et al. Strongyloides stercoralis: eosinophil-dependent immune-mediated killing of third stage larvae in BALB/cByJ mice. Exp Parasitol. 1996;82:267–78.

    Article  CAS  PubMed  Google Scholar 

  17. Padigel UM, Hess JA, Lee JJ, Lok JB, Nolan TJ, Schad GA, et al. Eosinophils act as antigen-presenting cells to induce immunity to Strongyloides stercoralis in mice. J Infect Dis. 2007;196:1844–51.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  18. Padigel UM, Lee JJ, Nolan TJ, Schad GA, Abraham D. Eosinophils can function as antigen-presenting cells to induce primary and secondary immune responses to Strongyloides stercoralis. Infect Immun. 2006;74:3232–8.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Coffman RL, Seymour BW, Hudak S, Jackson J, Rennick D. Antibody to interleukin-5 inhibits helminth-induced eosinophilia in mice. Science. 1989;245:308–10.

    Article  CAS  PubMed  Google Scholar 

  20. Grimaldi JC, Yu NX, Grunig G, Seymour BW, Cottrez F, Robinson DS, et al. Depletion of eosinophils in mice through the use of antibodies specific for C-C chemokine receptor 3 (CCR3). J Leukoc Biol. 1999;65:846–53.

    CAS  PubMed  Google Scholar 

  21. Gurish MF, Humbles A, Tao H, Finkelstein S, Boyce JA, Gerard C, et al. CCR3 is required for tissue eosinophilia and larval cytotoxicity after infection with Trichinella spiralis. J Immunol Baltim Md. 1950;2002(168):5730–6.

    Google Scholar 

  22. Liu H-C, Hsu J-Y, Chang K-M. Strongyloides stercoralis hyperinfection presenting with symptoms mimicking acute exacerbation of chronic obstructive pulmonary disease. J Chin Med Assoc. 2009;72:442–5.

    Article  PubMed  Google Scholar 

  23. Lagacé-Wiens PRS, Harding GKM. A Canadian immigrant with coinfection of Strongyloides stercoralis and human T-lymphotropic virus 1. Can Med Assoc J . 2007;177:451–3.

  24. Igra-Siegman Y, Kapila R, Sen P, Kaminski ZC, Louria DB. Syndrome of hyperinfection with Strongyloides stercoralis. Rev Infect Dis. 1981;3:397–407.

    Article  CAS  PubMed  Google Scholar 

  25. Adedayo O, Grell G, Bellot P. Hyperinfective strongyloidiasis in the medical ward: review of 27 cases in 5 years. South Med J. 2002;95:711–6.

    Article  PubMed  Google Scholar 

  26. Fardet L, Généreau T, Poirot J-L, Guidet B, Kettaneh A, Cabane J. Severe strongyloidiasis in corticosteroid-treated patients: case series and literature review. J Infect. 2007;54:18–27.

    Article  PubMed  Google Scholar 

  27. Coulter C, Walker DG, Günsberg M, Brown IG, Bligh JF, Prociv P. Successful treatment of disseminated strongyloidiasis. Med J Aust. 1992;157:331–2.

    CAS  PubMed  Google Scholar 

  28. 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;17:1331–3.

    Article  PubMed  Google Scholar 

  29. Kakati B, Dang S, Heif M, Caradine K, McKnight W, Aduli F. Strongyloides duodenitis: case report and review of literature. J Natl Med Assoc. 2011;103:60–3.

    PubMed  Google Scholar 

  30. Gutierrez Y, Bhatia P, Garbadawala ST, Dobson JR, Wallace TM, Carey TE. Strongyloides stercoralis eosinophilic granulomatous enterocolitis. Am J Surg Pathol. 1996;20:603–12.

    Article  CAS  PubMed  Google Scholar 

  31. Sipahi AM, Damião AO, Simionato CS, Bonini N, Santos MA, de Moraes-Filho JP, et al. Small bowel bacterial overgrowth in strongyloidiasis. Digestion. 1991;49:120–4.

    Article  CAS  PubMed  Google Scholar 

  32. Younis AE, Soblik H, Ajonina-Ekoti I, Erttmann KD, Luersen K, Liebau E, et al. Characterization of a secreted macrophage migration inhibitory factor homologue of the parasitic nematode Strongyloides acting at the parasite-host cell interface. Microbes Infect Inst Pasteur. 2012;14:279–89.

    Article  CAS  Google Scholar 

  33. Pastrana DV, Raghavan N, FitzGerald P, Eisinger SW, Metz C, Bucala R, et al. Filarial nematode parasites secrete a homologue of the human cytokine macrophage migration inhibitory factor. Infect Immun. 1998;66:5955–63.

    PubMed Central  CAS  PubMed  Google Scholar 

  34. Suputtamongkol Y, Premasathian N, Bhumimuang K, Waywa D, Nilganuwong S, Karuphong E, et al. Efficacy and safety of single and double doses of ivermectin versus 7-day high dose albendazole for chronic strongyloidiasis. Plos Negl Trop Dis. 2011;5:e1044.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Muennig P, Pallin D, Challah C, Khan K. The cost-effectiveness of ivermectin vs. albendazole in the presumptive treatment of strongyloidiasis in immigrants to the United States. Epidemiol Infect. 2004;132:1055–63.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  36. Hauber HP, Galle J, Chiodini PL, Rupp J, Birke R, Vollmer E, et al. Fatal outcome of a hyperinfection syndrome despite successful eradication of Strongyloides with subcutaneous ivermectin. Infection. 2005;33:383–6.

    Article  CAS  PubMed  Google Scholar 

  37. Leung V, Al-Rawahi GN, Grant J, Fleckenstein L, Bowie W. Case report: failure of subcutaneous ivermectin in treating Strongyloides hyperinfection. Am J Trop Med Hyg. 2008;79:853–5.

    PubMed  Google Scholar 

  38. Lichtenberger P, Rosa-Cunha I, Morris M, Nishida S, Akpinar E, Gaitan J, et al. Hyperinfection strongyloidiasis in a liver transplant recipient treated with parenteral ivermectin. Transpl Infect Dis Off J Transplant Soc. 2009;11:137–42.

    Article  CAS  Google Scholar 

  39. Pacanowski J, Santos MD, Roux A, Maignan CLE, Guillot J, Lavarde V, et al. Subcutaneous ivermectin as a safe salvage therapy in Strongyloides stercoralis hyperinfection syndrome: a case report. Am J Trop Med Hyg. 2005;73:122–4.

    PubMed  Google Scholar 

  40. Santiago M, Leitão B. Prevention of strongyloides hyperinfection syndrome: a rheumatological point of view. Eur J Intern Med. 2009;20:744–8.

    Article  CAS  PubMed  Google Scholar 

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Conflict of interest

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Author information

Authors and Affiliations

  1. Service de réanimation médicale, Hôpital Cochin, APHP, 27 rue du faubourg Saint-Jacques, 75014, Paris, France

    Guillaume Geri & Frédéric Pène

  2. Université Paris Descartes, Paris, France

    Guillaume Geri & Frédéric Pène

  3. Institut Cochin, INSERM U1016, CNRS UMR8104, Paris, France

    Frédéric Pène

  4. Unité de soins intensifs respiratoires, Hôpital Cochin, APHP, Paris, France

    Antoine Rabbat

  5. Service de réanimation médicale, Groupe Hospitalier Pitié-Salpêtrière, APHP, Paris, France

    Julien Mayaux

  6. Service de réanimation médicale, Hôpital Saint Louis, APHP, Paris, France

    Lara Zafrani & Elie Azoulay

  7. Université Paris Diderot, Paris, France

    Lara Zafrani & Elie Azoulay

  8. Service de réanimation polyvalente, Institut Gustave Roussy, Villejuif, France

    Ludivine Chalumeau-Lemoine

  9. Service de réanimation médicale, Hôpital Saint-Antoine, APHP, Paris, France

    Bertrand Guidet

  10. Université Pierre et Marie Curie, Paris, France

    Bertrand Guidet

Authors
  1. Guillaume Geri
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  2. Antoine Rabbat
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  3. Julien Mayaux
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  5. Ludivine Chalumeau-Lemoine
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  6. Bertrand Guidet
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  7. Elie Azoulay
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Corresponding author

Correspondence to Guillaume Geri.

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On behalf of the Groupe de Recherche sur la Réanimation Respiratoire en Onco-Hématologie (Grrr-OH).

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Geri, G., Rabbat, A., Mayaux, J. et al. Strongyloides stercoralis hyperinfection syndrome: a case series and a review of the literature. Infection 43, 691–698 (2015). https://doi.org/10.1007/s15010-015-0799-1

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  • DOI: https://doi.org/10.1007/s15010-015-0799-1

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