Author:
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Bisoffi Z et al. 2013. Strongyloides stercoralis: a plea for action. PLoS Negl Trop Dis 7: e2214.
-
2.
Nutman TB, 2017. Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology 144: 263–273.
-
3.
Buonfrate D, Requena-Mendez A, Angheben A, Munoz J, Gobbi F, Van Den Ende J, Bisoffi Z, 2013. Severe strongyloidiasis: a systematic review of case reports. BMC Infect Dis 13: 78.
-
4.
Buonfrate D, Requena-Mendez A, Angheben A, Cinquini M, Cruciani M, Fittipaldo A, Giorli G, Gobbi F, Piubelli C, Bisoffi Z, 2018. Accuracy of molecular biology techniques for the diagnosis of Strongyloides stercoralis infection—a systematic review and meta-analysis. PLoS Negl Trop Dis 12: e0006229.
-
5.
Requena-Mendez A, Chiodini P, Bisoffi Z, Buonfrate D, Gotuzzo E, Munoz J, 2013. The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Negl Trop Dis 7: e2002.
-
6.
Centre for Reviews and Dissemination, 2018. Prospero International Prospective Register of Systematic Reviews. York, UK: University of York. Available at: https://www.crd.york.ac.uk/prospero. Accessed June 12, 2018.
-
7.
Equator Network. Enhancing the Quality and Transparency Of Health Research. Available at: http://www.equator-network.org/?post_type=eq_guidelines&eq_guidelines_study_design=systematic-reviews-and-meta-analyses&eq_guidelines_clinical_specialty=0&eq_guidelines_report_section=0&s=+. Accessed May 21, 2018.
-
8.
R Core Team, 2017. R: A Language and Environment for Statistical Computing. Available at: https://www.R-project.org/. Accessed February 9, 2018.
-
9.
Aru RG, Chilcutt BM, Butt S, deShazo RD, 2017. Novel findings in HIV, immune reconstitution disease and Strongyloides stercoralis infection. Am J Med Sci 353: 593–596.
-
10.
Becker SL, Sieto B, Silue KD, Adjossan L, Kone S, Hatz C, Kern WV, N’Goran EK, Utzinger J, 2011. Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Negl Trop Dis 5: e1292.
-
11.
Forrer A, Khieu V, Schar F, Hattendorf J, Marti H, Neumayr A, Char MC, Hatz C, Muth S, Odermatt P, 2017. Strongyloides stercoralis is associated with significant morbidity in rural Cambodia, including stunting in children. PLoS Negl Trop Dis 11: e0005685.
-
12.
Herrera J, Marcos L, Terashima A, Alvarez H, Samalvides F, Gotuzzo E, 2006. Factors associated with Strongyloides stercoralis infection in an endemic area in Peru [in Spanish]. Rev Gastroenterol Peru 26: 357–362.
-
13.
Khieu V, Schar F, Marti H, Bless PJ, Char MC, Muth S, Odermatt P, 2014. Prevalence and risk factors of Strongyloides stercoralis in Takeo Province, Cambodia. Parasit Vectors 7: 221.
-
14.
Oliver NW, Rowbottom DJ, Sexton P, Goldsmid JM, Byard R, Tooth M, Thomson KS, 1989. Chronic strongyloidiasis in Tasmanian veterans–clinical diagnosis by the use of a screening index. Aust N Z J Med 19: 458–462.
-
15.
Rodriguez Calabuig D, Igual Adell R, Oltra Alcaraz C, Sanchez Sanchez P, Bustamante Balen M, Parra Godoy F, Nagore Enguidanos E, 2001. Agricultural occupation and strongyloidiasis. A case-control study [in Spanish]. Rev Clin Esp 201: 81–84.
-
16.
Tufanaru C, Munn Z, Stephenson M, Aromataris E, 2015. Fixed or random effects meta-analysis? Common methodological issues in systematic reviews of effectiveness. Int J Evid Based Healthc 13: 196–207.
-
17.
Cremades Romero MJ, Igual Adell R, Ricart Olmos C, Estelles Piera F, Pastor-Guzman A, Menendez Villanueva R, 1997. Infection by Strongyloides stercoralis in the county of Safor, Spain [in Spanish]. Med Clin (Barc) 109: 212–215.
-
18.
Grove DI, 1982. Treatment of strongyloidiasis with thiabendazole: an analysis of toxicity and effectiveness. Trans R Soc Trop Med Hyg 76: 114–118.
-
19.
Marcos L, Terashima A, Samalvides F, Alvarez H, Lindo F, Tello R, Canales M, Demarini J, Gotuzzo E, 2005. Thiabendazole for the control of Strongyloides stercoralis infection in a hyperendemic area in Peru [in Spanish]. Rev Gastroenterol Peru 25: 341–348.
-
20.
Marti H, Haji HJ, Savioli L, Chwaya HM, Mgeni AF, Ameir JS, Hatz C, 1996. 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 55: 477–481.
-
21.
Oyakawa T et al. 1991. New trial with thiabendazole for treatment of human strongyloidiasis [in Japanese]. Kansenshogaku Zasshi 65: 304–310.
-
22.
Shikiya K, Kinjo N, Uehara T, Uechi H, Ohshiro J, Arakaki T, Kinjo F, Saito A, Iju M, Kobari K, 1992. Efficacy of ivermectin against Strongyloides stercoralis in humans. Intern Med 31: 310–312.
-
23.
Shikiya K, Kuniyoshi T, Higashionna A, Arakkaki T, Oyakawa T, Kadena K, Kinjo F, Saito A, Asato R, 1990. Treatment of strongyloidiasis with mebendazole and its combination with thiabendazole [in Japanese]. Kansenshogaku Zasshi 64: 1408–1415.
-
24.
Shikiya K, Uehara T, Uechi H, Ohshiro J, Arakaki T, Oyakawa T, Sakugawa H, Kinjo F, Saito A, Asato R, 1991. Clinical study on ivermectin against Strongyloides stercoralis [in Japanese]. Kansenshogaku Zasshi 65: 1085–1090.
-
25.
Suputtamongkol Y, Premasathian N, Bhumimuang K, Waywa D, Nilganuwong S, Karuphong E, Anekthananon T, Wanachiwanawin D, Silpasakorn S, 2011. Efficacy and safety of single and double doses of ivermectin versus 7-day high dose albendazole for chronic strongyloidiasis. PLoS Negl Trop Dis 5: e1044.
-
26.
Zaha O, Hirata T, Kinjo F, Saito A, Fukuhara H, 2002. Efficacy of ivermectin for chronic strongyloidiasis: two single doses given 2 weeks apart. J Infect Chemother 8: 94–98.
-
27.
Zaha O et al. 1992. Clinical study on symptoms in patients with strongyloidiasis [in Japanese]. Kansenshogaku Zasshi 66: 1378–1382.
-
28.
Echazu A et al. 2017. Albendazole and ivermectin for the control of soil-transmitted helminths in an area with high prevalence of Strongyloides stercoralis and hookworm in northwestern Argentina: a community-based pragmatic study. PLoS Negl Trop Dis 11: e0006003.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 100 | 100 | 20 |
| Full Text Views | 987 | 233 | 3 |
| PDF Downloads | 470 | 100 | 3 |
Morbidity Associated with Chronic Strongyloides stercoralis Infection: A Systematic Review and Meta-Analysis
Francesca Tamarozzi
Francesca Tamarozzi
IRCCS Sacro Cuore Don Calabria Hospital, Verona, Italy;
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Elisa Martello
Elisa Martello
Department of Veterinary Sciences, University of Turin, Turin, Italy;
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Giovanni Giorli
Giovanni Giorli
IRCCS Sacro Cuore Don Calabria Hospital, Verona, Italy;
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Andrea Fittipaldo
Andrea Fittipaldo
IRCCS Istituto di Ricerche Farmacologiche Mario Negri, Milan, Italy;
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Silvia Staffolani
Silvia Staffolani
Ospedali Riuniti di Ancona, Ancona, Italy;
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Antonio Montresor
Antonio Montresor
WHO, Geneva, Switzerland;
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Zeno Bisoffi
Zeno Bisoffi
IRCCS Sacro Cuore Don Calabria Hospital, Verona, Italy;
Università degli Studi di Verona, Verona, Italy
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Università degli Studi di Verona, Verona, Italy
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Dora Buonfrate
Dora Buonfrate
IRCCS Sacro Cuore Don Calabria Hospital, Verona, Italy;
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Strongyloides stercoralis, a worldwide-distributed soil-transmitted helminth, causes chronic infection which may be life threatening. Limitations of diagnostic tests and nonspecificity of symptoms have hampered the estimation of the global morbidity due to strongyloidiasis. This work aimed at assessing S. stercoralis–associated morbidity through a systematic review and meta-analysis of the available literature. MEDLINE, Embase, CENTRAL, LILACS, and trial registries (WHO portal) were searched. The study quality was assessed using the Newcastle–Ottawa scale. Odds ratios (ORs) of the association between symptoms and infection status and frequency of infection-associated symptoms were calculated. Six articles from five countries, including 6,014 individuals, were included in the meta-analysis—three were of low quality, one of high quality, and two of very high quality. Abdominal pain (OR 1.74 [CI 1.07–2.94]), diarrhea (OR 1.66 [CI 1.09–2.55]), and urticaria (OR 1.73 [CI 1.22–2.44]) were associated with infection. In 17 eligible studies, these symptoms were reported by a large proportion of the individuals with strongyloidiasis—abdominal pain by 53.1% individuals, diarrhea by 41.6%, and urticaria by 27.8%. After removing the low-quality studies, urticaria remained the only symptom significantly associated with S. stercoralis infection (OR 1.42 [CI 1.24–1.61]). Limitations of evidence included the low number and quality of studies. Our findings especially highlight the appalling knowledge gap about clinical manifestations of this common yet neglected soil-transmitted helminthiasis. Further studies focusing on morbidity and risk factors for dissemination and mortality due to strongyloidiasis are absolutely needed to quantify the burden of S. stercoralis infection and inform public health policies.
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Author Notes
Financial support: This work was supported by the Italian Ministry of Health “Fondi Ricerca Corrente - Linea 2, progetto 4” to IRCCS Sacro Cuore Don Calabria Hospital.
Authors’ addresses: Francesca Tamarozzi, Giovanni Giorli, and Dora Buonfrate, Center for Tropical Diseases, IRCCS Sacro Cuore-Don Calabria Hospital, Verona, Italy, E-mails: francesca.tamarozzi@sacrocuore.it, giovanni.giorlisacrocuore.it, and dora.buonfrate@sacrocuore.it. Elisa Martello, Department of Veterinary Sciences, University of Turin, Turin, Italy, E-mail: martello.elisa@gmail.com. Andrea Fittipaldo, IRCCS Mario Negri Institute of Pharmacological Reserach, Milan, Italy, E-mail: vafittipaldo@hotmail.it. Silvia Staffolani, Unit of Emerging Infectious Diseases and of the Immunodepressed, Ospedali Riuniti di Ancona, Ancona, Italy, E-mail: silvia.staffolani@ospedaliriuniti.marche.it. Antonio Montresor, Department of Control of Neglected Tropical Diseases, WHO, Geneva, Switzerland, E-mail: montresora@who.int. Zeno Bisoffi, Center for Tropical Diseases, IRCCS Sacro Cuore-Don Calabria Hospital, Verona, Italy, and Diagnostic and Public Health Department, Infectious Diseases and Tropical Medicine Section, University of Verona, Verona, Italy, E-mail: zeno.bisoffi@sacrocuore.it.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Bisoffi Z et al. 2013. Strongyloides stercoralis: a plea for action. PLoS Negl Trop Dis 7: e2214.
-
2.
Nutman TB, 2017. Human infection with Strongyloides stercoralis and other related Strongyloides species. Parasitology 144: 263–273.
-
3.
Buonfrate D, Requena-Mendez A, Angheben A, Munoz J, Gobbi F, Van Den Ende J, Bisoffi Z, 2013. Severe strongyloidiasis: a systematic review of case reports. BMC Infect Dis 13: 78.
-
4.
Buonfrate D, Requena-Mendez A, Angheben A, Cinquini M, Cruciani M, Fittipaldo A, Giorli G, Gobbi F, Piubelli C, Bisoffi Z, 2018. Accuracy of molecular biology techniques for the diagnosis of Strongyloides stercoralis infection—a systematic review and meta-analysis. PLoS Negl Trop Dis 12: e0006229.
-
5.
Requena-Mendez A, Chiodini P, Bisoffi Z, Buonfrate D, Gotuzzo E, Munoz J, 2013. The laboratory diagnosis and follow up of strongyloidiasis: a systematic review. PLoS Negl Trop Dis 7: e2002.
-
6.
Centre for Reviews and Dissemination, 2018. Prospero International Prospective Register of Systematic Reviews. York, UK: University of York. Available at: https://www.crd.york.ac.uk/prospero. Accessed June 12, 2018.
-
7.
Equator Network. Enhancing the Quality and Transparency Of Health Research. Available at: http://www.equator-network.org/?post_type=eq_guidelines&eq_guidelines_study_design=systematic-reviews-and-meta-analyses&eq_guidelines_clinical_specialty=0&eq_guidelines_report_section=0&s=+. Accessed May 21, 2018.
-
8.
R Core Team, 2017. R: A Language and Environment for Statistical Computing. Available at: https://www.R-project.org/. Accessed February 9, 2018.
-
9.
Aru RG, Chilcutt BM, Butt S, deShazo RD, 2017. Novel findings in HIV, immune reconstitution disease and Strongyloides stercoralis infection. Am J Med Sci 353: 593–596.
-
10.
Becker SL, Sieto B, Silue KD, Adjossan L, Kone S, Hatz C, Kern WV, N’Goran EK, Utzinger J, 2011. Diagnosis, clinical features, and self-reported morbidity of Strongyloides stercoralis and hookworm infection in a co-endemic setting. PLoS Negl Trop Dis 5: e1292.
-
11.
Forrer A, Khieu V, Schar F, Hattendorf J, Marti H, Neumayr A, Char MC, Hatz C, Muth S, Odermatt P, 2017. Strongyloides stercoralis is associated with significant morbidity in rural Cambodia, including stunting in children. PLoS Negl Trop Dis 11: e0005685.
-
12.
Herrera J, Marcos L, Terashima A, Alvarez H, Samalvides F, Gotuzzo E, 2006. Factors associated with Strongyloides stercoralis infection in an endemic area in Peru [in Spanish]. Rev Gastroenterol Peru 26: 357–362.
-
13.
Khieu V, Schar F, Marti H, Bless PJ, Char MC, Muth S, Odermatt P, 2014. Prevalence and risk factors of Strongyloides stercoralis in Takeo Province, Cambodia. Parasit Vectors 7: 221.
-
14.
Oliver NW, Rowbottom DJ, Sexton P, Goldsmid JM, Byard R, Tooth M, Thomson KS, 1989. Chronic strongyloidiasis in Tasmanian veterans–clinical diagnosis by the use of a screening index. Aust N Z J Med 19: 458–462.
-
15.
Rodriguez Calabuig D, Igual Adell R, Oltra Alcaraz C, Sanchez Sanchez P, Bustamante Balen M, Parra Godoy F, Nagore Enguidanos E, 2001. Agricultural occupation and strongyloidiasis. A case-control study [in Spanish]. Rev Clin Esp 201: 81–84.
-
16.
Tufanaru C, Munn Z, Stephenson M, Aromataris E, 2015. Fixed or random effects meta-analysis? Common methodological issues in systematic reviews of effectiveness. Int J Evid Based Healthc 13: 196–207.
-
17.
Cremades Romero MJ, Igual Adell R, Ricart Olmos C, Estelles Piera F, Pastor-Guzman A, Menendez Villanueva R, 1997. Infection by Strongyloides stercoralis in the county of Safor, Spain [in Spanish]. Med Clin (Barc) 109: 212–215.
-
18.
Grove DI, 1982. Treatment of strongyloidiasis with thiabendazole: an analysis of toxicity and effectiveness. Trans R Soc Trop Med Hyg 76: 114–118.
-
19.
Marcos L, Terashima A, Samalvides F, Alvarez H, Lindo F, Tello R, Canales M, Demarini J, Gotuzzo E, 2005. Thiabendazole for the control of Strongyloides stercoralis infection in a hyperendemic area in Peru [in Spanish]. Rev Gastroenterol Peru 25: 341–348.
-
20.
Marti H, Haji HJ, Savioli L, Chwaya HM, Mgeni AF, Ameir JS, Hatz C, 1996. 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 55: 477–481.
-
21.
Oyakawa T et al. 1991. New trial with thiabendazole for treatment of human strongyloidiasis [in Japanese]. Kansenshogaku Zasshi 65: 304–310.
-
22.
Shikiya K, Kinjo N, Uehara T, Uechi H, Ohshiro J, Arakaki T, Kinjo F, Saito A, Iju M, Kobari K, 1992. Efficacy of ivermectin against Strongyloides stercoralis in humans. Intern Med 31: 310–312.
-
23.
Shikiya K, Kuniyoshi T, Higashionna A, Arakkaki T, Oyakawa T, Kadena K, Kinjo F, Saito A, Asato R, 1990. Treatment of strongyloidiasis with mebendazole and its combination with thiabendazole [in Japanese]. Kansenshogaku Zasshi 64: 1408–1415.
-
24.
Shikiya K, Uehara T, Uechi H, Ohshiro J, Arakaki T, Oyakawa T, Sakugawa H, Kinjo F, Saito A, Asato R, 1991. Clinical study on ivermectin against Strongyloides stercoralis [in Japanese]. Kansenshogaku Zasshi 65: 1085–1090.
-
25.
Suputtamongkol Y, Premasathian N, Bhumimuang K, Waywa D, Nilganuwong S, Karuphong E, Anekthananon T, Wanachiwanawin D, Silpasakorn S, 2011. Efficacy and safety of single and double doses of ivermectin versus 7-day high dose albendazole for chronic strongyloidiasis. PLoS Negl Trop Dis 5: e1044.
-
26.
Zaha O, Hirata T, Kinjo F, Saito A, Fukuhara H, 2002. Efficacy of ivermectin for chronic strongyloidiasis: two single doses given 2 weeks apart. J Infect Chemother 8: 94–98.
-
27.
Zaha O et al. 1992. Clinical study on symptoms in patients with strongyloidiasis [in Japanese]. Kansenshogaku Zasshi 66: 1378–1382.
-
28.
Echazu A et al. 2017. Albendazole and ivermectin for the control of soil-transmitted helminths in an area with high prevalence of Strongyloides stercoralis and hookworm in northwestern Argentina: a community-based pragmatic study. PLoS Negl Trop Dis 11: e0006003.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 100 | 100 | 20 |
| Full Text Views | 987 | 233 | 3 |
| PDF Downloads | 470 | 100 | 3 |