Human Strongyloidiasis: a forgotten disease, an ongoing problema

Main Article Content

Humberto Zapata Lopera
Ana María Rincón González
Luz Elena Botero Palacio
Mauricio Hernández Sarmiento
Lina A. Gutiérrez Builes

Abstract

Strongyloidiasis is an infection in the upper small intestine that, in most immunocompetent hosts, occurs asymptomatically. It is estimated that this parasite affects 100 million people living in 70 countries around the world, with highest prevalence in tropical and sub-tropical regions. One characteristic of the Strongyloides stercoralis parasite is its ability to develop cycles of auto-infection, with the possibility of evolving to chronic infection in immunocompetent hosts. However, in immunocompromised hosts (mainly transplanted patients and those infected by human T-cell lymphotropic virus type 1), it can lead to a potentially fatal hyperinfection syndrome. Taking into account the increasing number of solid organ transplants in Colombia and the lack of diagnostic validity offered by the parasitological analysis tools available in this setting, which are used in the routine search for intestinal parasites in pre-transplant protocols or those prior to immunosuppressor therapy, a quick and precise diagnosis in these high-risk patients is necessary. This topic review calls for medical personnel to be informed in the regional and national sanitary conditions regarding strongyloidiasis as an opportunistic parasitosis that should be taken into account in clinical diagnosis and which is associated to mortality in the cases of hyperinfection by S. stercoralis in immunocompromised patients, particularly when not diagnosed and treated in a timely manner.

Keywords:
Strongyloides stercoralis, intestinal diseases, parasitic, opportunistic infections, immunosuppression, diagnosis

Article Details

Author Biographies

Humberto Zapata Lopera, Pontifical Bolivarian University

Medical student. Research Seedbed School of Medicine (Sifam). Pontifical Bolivarian University. Medellin Colombia.

Ana María Rincón González, Pontifical Bolivarian University

Medical student. Research Seedbed School of Medicine (Sifam). Pontifical Bolivarian University. Medellin Colombia.

Luz Elena Botero Palacio, Pontifical Bolivarian University

Systems Biology Group, Faculty of Medicine, School of Health Sciences, Universidad Pontificia Bolivariana. Medellin Colombia.

Mauricio Hernández Sarmiento, Pontifical Bolivarian University

Bacteriology and Mycobacteria Unit, Corporation for Biological Research - Universidad Pontificia Bolivariana. Medellin Colombia.

Lina A. Gutiérrez Builes, Pontifical Bolivarian University

Systems Biology Group, Faculty of Medicine, School of Health Sciences, Universidad Pontificia Bolivariana. Medellin Colombia.

References

Concha R, Harrington W Jr, Rogers AI. Intestinal strongyloidiasis: recognition, management, and determinants of outcome. J Clin Gastroenterol. 2005; 39(3):203-211.

Lim S, Katz K, Krajden S, Fuksa M, Keystone JS, Kain KC. Complicated and fatal Strongyloides infection in Canadians: risk factors, diagnosis and management. CMAJ. 2004; 171(5):479-484.

Nolan TJ, Megyeri Z, Bhopale VM, Schad GA. Strongyloides stercoralis: the first rodent model for uncomplicated and hyperinfective strongyloidiasis, the Mongolian gerbil (Meriones unguiculatus). J Infect Dis. 1993; 168(6):1479-1484.

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):967-972.

Bedoya AM, de Castro Andrade A, Robledo J, Restrepo PA. El caso de Infecciosas: Hiperinfección por Strongyloides stercoralis. Medicina UPB. 2002; 21(2):145-153.

Pérez-Rodríguez MT, Ocampo A, Longueira R, Martínez-Vázquez C. Síndrome de hiperinfección por Strongyloides stercoralis en un paciente colombiano con tratamiento inmunosupresor. Enferm Infecc Microbiol Clin. 2009; 27(7):425-434.

Viney ME, Lok JB. Strongyloides spp. Worm Book. 2007; 23:1-15.

Barnish G, Ashford RW. Strongyloides cf. fuelleborni and hookworm in Papua New Guinea: patterns of infection within the community. Trans R Soc Trop Med Hyg. 1989; 83(5):684-688.

Ashford RW, Barnish G, Viney ME. Strongyloides fuelleborni kellyi: infection and disease in Papua New Guinea. Parasitol Today. 1992; 8(9):314-318.

Siddiqui AA, Berk SL. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis. 2001; 33(7):1040-1047.

Boscolo M, Bisoffi Z. Dissemination: the fatal risk for a missed diagnosis of Strongyloides stercoralis infection. J Infect. 2007; 55(3):284-285.

Scowden EB, Schaffner W, Stone WJ. Overwhelming strongyloidiasis: an unappreciated opportunistic infection. Medicine (Baltimore). 1978; 57(6):527-544.

Requena-Méndez A, Chiodini P, Bisoffi Z, Buonfrate D, Gotuzzo E, Muñoz J. The Laboratory Diagnosis and Follow Up of Strongyloidiasis: A Systematic Review. PLoS Negl Trop Dis. 2013; 7(1):e2002.

Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, et al. Strongyloides stercoralis: Global distribution and risk factors. PlosOne. 2013; 7(7):e2288.

Cimerman S, Cimerman B, Lewi DS. Prevalence of intestinal parasitic infections in patients with acquired immunodeficiency syndrome in Brazil. Int J Infect Dis. 1999; 3(4):203-206.

Machado ER, Costa-Cruz JM. Strongyloides stercoralis and other enteroparasites in children at Uberlandia city, state of Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 1998; 93(2):161-164.

Borda CE, Rea MJ, Rosa JR, Maidana C. Intestinal parasitism in San Cayetano, Corrientes, Argentina. Bull Pan Am Health Organ. 1996; 30(3):227-233.

Taranto NJ, Bonomi de Filippi H, Orione O. [Prevalence of Strongyloides stercoralis infection in childhood. Oran, Salta, Argentina]. Bol Chil Parasitol. 1993; 48(3-4):49-51.

Mahmoud AA. Strongyloidiasis. Clin Infect Dis. 1996; 23(5):949-952.

Botero D, Restrepo M. Parasitosis humanas, incluye animales venenosos y ponzoñosos. 5ªed. Medellín: CIB; 2012.

Botero J, Zuluaga N. Revisión de tema: Nemátodos intestinales de importancia médica en Colombia: ¿un problema resuelto? Iatreia. 2001; 14:47-56.

Panqueba C, Rodríguez G, Téllez N. Estrongiloidiasis diseminada. Biomédica 1986; 6(1):115-126.

Álvarez S, Salazar J, Salazar E, Vivar N. Estrongiloidiosis. A propósito de un caso clínico. Rev Mex Patol Clin. 2010; 57(4):209-211.

Mogollón L. Prevalencia de parasitosis intestinal en consultantes al hospital de Suaita-Santander. Salud UIS. 2003; 35:131-134.

Evering T, Weiss LM. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006; 28(11):549-565.

Rivero FD, Kremer LE, Allende L, Casero RD. [Strongyloides stercoralis and HIV: a case report of an indigenous disseminated infection from non-endemic area]. Rev Argent Microbiol. 2006; 38(3):137-139.

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):314-318.

Kitamura D, Roes J, Kühn R, Rajewsky K. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature. 1991; 350(6317):423-426.

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. 2000; 165(8):4544-4551.

Shi HZ. Eosinophils function as antigen-presenting cells. J Leukoc Biol. 2004; 76(3):520-527.

Hogarth PJ, Bianco AE. IL-5 dominates cytokine responses during expression of protective immunity to Onchocerca lienalis microfilariae in mice. Parasite Immunol. 1999; 21(2):81-88.

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

Beltran Catalan S, Crespo Albiach JF, Morales Garcia AI, Gavela Martinez E, Gorriz Teruel JL, Pallardo Mateu LM. [Strongyloides stercoralis infection in renal transplant recipients]. Nefrologia. 2009; 29(5):482-485.

Mokaddas EM, Shati S, Abdulla A, Nampoori NR, Iqbal J, Nair PM et al. Fatal strongyloidiasis in three kidney recipients in Kuwait. Med Princ Pract. 2009; 18(5):414-417.

Balagopal A, Mills L, Shah A, Subramanian A. Detection and treatment of Strongyloides hyperinfection syndrome following lung transplantation. Transpl Infect Dis. 2009; 11(2):149-154.

Patel G, Arvelakis A, Sauter BV, Gondolesi GE, Caplivski D, Huprikar S. Strongyloides hyperinfection syndrome after intestinal transplantation. Transpl Infect Dis. 2008; 10(2):137-141.

Rodriguez-Hernandez MJ, Ruiz-Perez-Pipaon M, Canas E, Bernal C, Gavilan F. Strongyloides stercoralis hyperinfection transmitted by liver allograft in a transplant recipient. Am J Transplant. 2009; 9(11):2637-2640.

Vilela EG, Clemente WT, Mira RR, Torres HO, Veloso LF, Fonseca LP, et al. Strongyloides stercoralis hyperinfection syndrome after liver transplantation: case report and literature review. Transpl Infect Dis. 2009; 11(2):132-136.

Grover IS, Davila R, Subramony C, Daram SR. Strongyloides infection in a cardiac transplant recipient: making a case for pretransplantation screening and treatment. Gastroenterol Hepatol (NY). 2011; 7(11):763-766.

Roxby AC, Gottlieb GS, Limaye AP. Strongyloidiasis in transplant patients. Clin Infect Dis. 2009; 49(9):1411-1423.

Orlent H, Crawley C, Cwynarski K, Dina R, Apperley J. Strongyloidiasis pre and post autologous peripheral blood stem cell transplantation. Bone Marrow Transplant. 2003; 32(1):115-117.

Weiser JA, Scully BE, Bulman WA, Husain S, Grossman ME. Periumbilical parasitic thumbprint purpura: strongyloides hyperinfection syndrome acquired from a cadaveric renal transplant. Transpl Infect Dis. 2011; 13(1):58-62.

Siegel MO, Simon GL. Is human immunodeficiency virus infection a risk factor for Strongyloides stercoralis hyperinfection and dissemination. PLoS Negl Trop Dis. 2012; 6(7):e1581.

Bava AJ, Troncoso AR. Strongyloides stercoralis hyperinfection in a patient with AIDS. J Int Assoc Physicians AIDS Care (Chic). 2009; 8(4):235-238.

Carvalho EM, da Fonseca Porto A. Epidemiological and clinical interaction between HTLV-1 and Strongyloides stercoralis. Parasite Immunol 2004; 26(11-12):487-497.

Genta RM. Global prevalence of strongyloidiasis: critical review with epidemiologic insights into the prevention of disseminated disease. Rev Infect Dis. 1989; 11(5):755-767.

Ben-Youssef R, Baron P, Edson F, Raghavan R, Okechukwu O. Stronglyoides stercoralis infection from pancreas allograft: case report Transplantation. 2005; 80(7):997-998.

Hamilton KW, Abt PL, Rosenbach MA, Bleicher MB, Levine MS, Mehta J, et al. Donor-derived Strongyloides stercoralis infections in renal transplant recipients. Transplantation. 2011; 91(9):1019-1024.

Herrera J, Marcos L, Terashima A, Alvarez H, Samalvides F, Gotuzzo E. [Factors associated with Strongyloides stercoralis infection in an endemic area in Peru]. Rev Gastroenterol Peru. 2006; 26(4):357-362.

Instituto Nacional de Salud. Red de donación y trasplante de órganos y tejidos. Informe de avance I trimestre de 2013. Bogotá, Colombia. Disponible en http://www.ins.gov.co. Fecha de consulta: agosto de 2013.

Bermeo S, Ostos H, Cubillos J. Trasplantes de órganos: perspectiva histórica y alternativas futuras. Revista Facultad de Salud – RFS. 2009; 1(2):63-71.

Agrawal V, Agarwal T, Ghoshal UC. Intestinal strongyloidiasis: a diagnosis frequently missed in the tropics. Trans R Soc Trop Med Hyg. 2009; 103(3):242-246.

Abrescia FF, Falda A, Caramaschi G, Scalzini A, Gobbi F, Angheben A, et al. Reemergence of strongyloidiasis, northern Italy. Emerg Infect Dis. 2009; 15(9):1531-1533.

Nielsen PB, Mojon M. Improved diagnosis of Strongyloides stercoralis by seven consecutive stool specimens. Zentralbl Bakteriol Mikrobiol Hyg A. 1987; 263(4):616-618.

Pelletier LL Jr. Chronic strongyloidiasis in World War II Far East ex-prisoners of war. Am J Trop Med Hyg. 1984; 33(1):55-61.

Mejia R, Nutman TB. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis. Curr Opin Infect Dis. 2012; 25(4):458-463.

Anamnart W, Pattanawongsa A, Intapan PM, Maleewong W. Albendazole stimulates the excretion of Strongyloides stercoralis Larvae in stool specimens and enhances sensitivity for diagnosis of strongyloidiasis. J Clin Microbiol. 2010; 48(11):4216-4220.

De Kaminsky RG. Evaluation of three methods for laboratory diagnosis of Strongyloides stercoralis infection. J Parasitol 1993; 79(2):277-280.

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):1209-1214.

Silva LP, Barcelos IS, Passos-Lima AB, Espindola FS, Campos DM, Costa-Cruz JM. Western blotting using Strongyloides ratti antigen for the detection of IgG antibodies as confirmatory test in human strongyloidiasis. Mem Inst Oswaldo Cruz. 2003; 98(5):687-691.

Goka AK, Rolston DD, Mathan VI, Farthing MJ. Diagnosis of Strongyloides and hookworm infections: comparison of faecal and duodenal fluid microscopy. Trans R Soc Trop Med Hyg. 1990; 84(6):829-831.

Santos RB, Fonseca LE Jr, Santana AT, Silva CA, Guedes JC. Clinical, endoscopic and histopathological profiles of parasitic duodenitis cases diagnosed by upper digestive endoscopy. Arq Gastroenterol 2011; 48(4):225-230.

Boscolo M, Gobbo M, Mantovani W, Degani M, Anselmi M, Monteiro GB, et al. Evaluation of an indirect immunofluorescence assay for strongyloidiasis as a tool for diagnosis and follow-up. Clin Vaccine Immunol 2007; 14(2):129-133.

Biggs BA, Caruana S, Mihrshahi S, Jolley D, Leydon J, Chea L, et al. Management of chronic strongyloidiasis in immigrants and refugees: is serologic testing useful? Am J Trop Med Hyg. 2009; 80(5):788-791.

Montes M, Sawhney C, Barros N. Strongyloides stercoralis: there but not seen. Curr Opin Infect Dis 2010; 23(5):500-504.

Ramanathan R, Burbelo PD, Groot S, Iadarola MJ, Neva FA, Nutman TB. A luciferase immunoprecipitation systems assay enhances the sensitivity and specificity of diagnosis of Strongyloides stercoralis infection. J Infect Dis 2008; 198(3):444-451.

Basuni M, Muhi J, Othman N, Verweij JJ, Ahmad M, Miswan N, et al. A pentaplex real-time polymerase chain reaction assay for detection of four species of soil-transmitted helminths. Am J Trop Med Hyg. 2011; 84(2):338-343

Verweij JJ, Canales M, Polman K, Ziem J, Brienen EA, Polderman AM, et al. Molecular diagnosis of Strongyloides stercoralis in faecal samples using real-time PCR. Trans R Soc Trop Med Hyg. 2009; 103(4):342-346.

Naquira C, Jimenez G, Guerra JG, Bernal R, Nalin DR, Neu D, et al. Ivermectin for human strongyloidiasis and other intestinal helminths. Am J Trop Med Hyg. 1989; 40:304-309.

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(5):e1044.

Igual-Adell R, Oltra-Alcaraz C, Soler-Company E, Sánchez-Sánchez P, Matogo-Oyana J, Rodríguez-Calabuig D. Efficacy and safety of ivermectin and thiabendazole in the treatment of strongyloidiasis. Expert Opin Pharmacother. 2004; 5(12):2615-2619.

Suputtamongkol Y, Kungpanichkul N, Silpasakorn S, Beeching NJ. Efficacy and safety of a singledose veterinary preparation of ivermectin versus 7-day high-dose albendazole for chronic strongyloidiasis. Int J Antimicrob Agents. 2008; 31(1):46-49.

Bisoffi Z, Buonfrate D, Angheben A, Boscolo M, Anselmi M, Marocco S, et al. Randomized clinical trial on ivermectin versus thiabendazole for the treatment of strongyloidiasis. PLoS Negl Trop Dis. 2011; 5(7):e1254.