Serology-Based Screening and Prevalence of Schistosomiasis, Strongyloidiasis, and Chagas Disease in Migrants Living with HIV: Results from a 10-Year Retrospective Cohort in an Italian Tertiary Healthcare Center
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Setting, Design, Aims, and Population
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- Age ≥ 18 years;
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- HIV infection confirmed with serological and molecular methods in our laboratory;
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- Individuals born in countries outside Italy but living in Italy for at least six months.
2.2. Migration Policies in Italy
2.3. Definitions
2.4. Serological Screening Assays
2.5. Statistical Analysis
3. Results
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- IOM UN Migration. Migration and Migrants: Regional Dimensions and Developments-Europe. Available online: https://worldmigrationreport.iom.int/what-we-do/world-migration-report-2024-chapter-3/europe (accessed on 22 August 2025).
- European Commission; Eurostat. Migration and Asylum in Europe. 2024. Available online: https://data.europa.eu/doi/10.2785/43971 (accessed on 22 August 2025).
- Migration Data Portal. International Migrant Population (Stocks). Available online: https://www.migrationdataportal.org/themes/international-migrant-stocks-overview?utm_source=chatgpt.com (accessed on 22 August 2025).
- Terminski, B. Realizing the right to health of undocumented immigrants in Europe: Legal and social challenges. In Proceedings of the 13th World Congress on Public Health, Bologna, Italy, 21 April 2013; Monduzzi, Ed.; 2013; p. 12. [Google Scholar]
- Torres-Cantero, A.M.; Miguel, A.G.; Gallardo, C.; Ippolito, S. Health care provision for illegal migrants: May health policy make a difference? Eur. J. Public Health 2007, 17, 483–485. [Google Scholar] [CrossRef]
- HIV/AIDS Surveillance in Europe 2023 (2022 Data). Available online: https://www.ecdc.europa.eu/en/publications-data/hivaids-surveillance-europe-2023-2022-data (accessed on 20 October 2024).
- HIV/AIDS Infection in Italy Up to 31 December 2022. Volume 36, no. 11, November 2023. Available online: https://www.iss.it/-/volume-36-no-11-november-2023-hiv/aids-infection-in-italy-up-to-december-31-2022 (accessed on 20 October 2024).
- Salvador, F.; Molina, I.; Sulleiro, E.; Burgos, J.; Curran, A.; den Eynde, E.V.; Villar del Saz, S.; Navarro, J.; Crespo, M.; Ocaña, I.; et al. Tropical Diseases Screening in Immigrant Patients with Human Immunodeficiency Virus Infection in Spain. Am. J. Trop. Med. Hyg. 2013, 88, 1196–1202. [Google Scholar] [CrossRef]
- Chagas Disease. Available online: https://www.who.int/news-room/fact-sheets/detail/chagas-disease-(american-trypanosomiasis) (accessed on 10 September 2024).
- Basile, L.; Jansá, J.M.; Carlier, Y.; Salamanca, D.D.; Angheben, A.; Bartoloni, A.; Seixas, J.; Gool, T.V.; Cañavate, C.; Flores-Chávez, M.; et al. Chagas disease in European countries: The challenge of a surveillance system. Eurosurveillance 2011, 16, 19968. [Google Scholar] [CrossRef]
- SciELO Brazil-Co-Infection Trypanosoma Cruzi/HIV: Systematic Review (1980–2010) Co-Infection Trypanosoma Cruzi/HIV: Systematic Review (1980–2010). Available online: https://www.scielo.br/j/rsbmt/a/cN85tTnkzFGyXpr6ffYsJCp/?lang=en (accessed on 24 March 2025).
- Buonfrate, D.; Requena-Mendez, A.; Angheben, A.; Muñoz, J.; Gobbi, F.; Van Den Ende, J.; Bisoffi, Z. Severe strongyloidiasis: A systematic review of case reports. BMC Infect. Dis. 2013, 13, 78. [Google Scholar] [CrossRef] [PubMed]
- Buonfrate, D.; Angheben, A.; Gobbi, F.; Muñoz, J.; Requena-Mendez, A.; Gotuzzo, E.; Mena, M.A.; Bisoffi, Z. Imported strongyloidiasis: Epidemiology, presentations, and treatment. Curr. Infect. Dis. Rep. 2012, 14, 256–262. [Google Scholar] [CrossRef]
- Forrer, A.; Khieu, V.; Schär, F.; Hattendorf, J.; Marti, H.; Neumayr, A.; Char, M.C.; Hatz, C.; Muth, S.; Odermatt, P. Strongyloides stercoralis is associated with significant morbidity in rural Cambodia, including stunting in children. PLoS Neglected Trop. Dis. 2017, 11, e0005685. [Google Scholar] [CrossRef]
- Patel, P.; Rose, C.E.; Kjetland, E.F.; Downs, J.A.; Mbabazi, P.S.; Sabin, K.; Chege, W.; Watts, D.H.; Secor, W.E. Association of schistosomiasis and HIV infections: A systematic review and meta-analysis. Int. J. Infect. Dis. 2021, 102, 544–553. [Google Scholar] [CrossRef] [PubMed]
- Kallestrup, P.; Zinyama, R.; Gomo, E.; Butterworth, A.E.; Mudenge, B.; van Dam, G.J.; Gerstoft, J.; Erikstrup, C.; Ullum, H. Schistosomiasis and HIV-1 infection in rural Zimbabwe: Effect of treatment of schistosomiasis on CD4 cell count and plasma HIV-1 RNA load. J. Infect. Dis. 2005, 192, 1956–1961. [Google Scholar] [CrossRef] [PubMed]
- Mulu, A.; Maier, M.; Liebert, U.G. Deworming of intestinal helminths reduces HIV-1 subtype C viremia in chronically co-infected individuals. Int. J. Infect. Dis. 2013, 17, e897–e901. [Google Scholar] [CrossRef]
- Martelli, G.; Girolamo, C.D.; Zammarchi, L.; Angheben, A.; Morandi, M.; Tais, S.; Degani, M.; Hamad, I.E.; Caligaris, S.; Ciannameo, A.; et al. Seroprevalence of five neglected parasitic diseases among immigrants accessing five infectious and tropical diseases units in Italy: A cross-sectional study. Clin. Microbiol. Infect. 2017, 23, 335.e1–335.e5. [Google Scholar] [CrossRef]
- Mascarello, M.; Gobbi, F.; Angheben, A.; Gobbo, M.; Gaiera, G.; Pegoraro, M.; Lanzafame, M.; Buonfrate, D.; Concia, E.; Bisoffi, Z. Prevalence of Strongyloides stercoralis infection among HIV-positive immigrants attending two Italian hospitals, from 2000 to 2009. Ann. Trop. Med. Parasitol. 2011, 105, 617–623. [Google Scholar] [CrossRef]
- Sadlier, C.M.; Brown, A.; Lambert, J.S.; Sheehan, G.; Mallon, P.W.G. Seroprevalence of Schistosomiasis and Strongyloides infection in HIV-infected patients from endemic areas attending a European infectious diseases clinic. AIDS Res. Ther. 2013, 10, 23. [Google Scholar] [CrossRef] [PubMed]
- Tilli, M.; Botta, A.; Bartoloni, A.; Corti, G.; Zammarchi, L. Hospitalization for Chagas disease, dengue, filariasis, leishmaniasis, schistosomiasis, strongyloidiasis, and Taenia solium taeniasis/cysticercosis, Italy, 2011–2016. Infection 2020, 48, 695–713. [Google Scholar] [CrossRef] [PubMed]
- Zammarchi, L.; Gobbi, F.; Angheben, A.; Spinicci, M.; Buonfrate, D.; Calleri, G.; De Paola, M.; Bevilacqua, N.; Carrara, S.; Attard, L.; et al. Schistosomiasis, strongyloidiasis and Chagas disease: The leading imported neglected tropical diseases in Italy. J. Travel Med. 2020, 27, taz100. [Google Scholar] [CrossRef]
- Ministero del Lavoro e delle Politiche Sociali La Presenza dei Migranti Nella Città Metropolitana di Firenze. Available online: https://integrazionemigranti.gov.it/it-it/Dettaglio-ricerca/id/1258 (accessed on 24 August 2025).
- EpiCentro I Controlli alla Frontiera. La Frontiera dei Controlli. Available online: https://www.epicentro.iss.it/migranti/LGFrontiere (accessed on 28 August 2025).
- CDC Yellow Book 2024|Travelers’ Health|CDC. Available online: https://wwwnc.cdc.gov/travel/page/yellowbook-home (accessed on 10 September 2024).
- WHO. World Health Organization. Available online: https://apps.who.int/neglected_diseases/ntddata/sch/sch.html (accessed on 10 September 2024).
- Buonfrate, D.; Bisanzio, D.; Giorli, G.; Odermatt, P.; Fürst, T.; Greenaway, C.; French, M.; Reithinger, R.; Gobbi, F.; Montresor, A.; et al. The Global Prevalence of Strongyloides stercoralis Infection. Pathogens 2020, 9, 468. [Google Scholar] [CrossRef]
- Pubblicazioni SIMET. Available online: https://www.simetweb.eu/attivita/pubblicazioni-simet/ (accessed on 10 September 2024).
- Rodríguez-Guardado, A.; Alvarez, V.A.; Perez, M.R.; Alvarez, P.M.; Flores-Chavez, M.; González, P.A.; Sánchez, J.A.C. Screening for Chagas’ disease in HIV-positive immigrants from endemic areas. Epidemiol. Infect. 2011, 139, 539–543. [Google Scholar] [CrossRef]
- Llenas-García, J.; Fiorante, S.; Salto, E.; Maseda, D.; Rodríguez, V.; Matarranz, M.; Hernando, A.; Rubio, R.; Pulido, F. Should We Look for Strongyloides Stercoralis in Foreign-Born HIV-Infected Persons? J. Immigr. Minor. Health 2013, 15, 796–802. [Google Scholar] [CrossRef]
- McLellan, J.; Gill, M.J.; Vaughan, S.; Meatherall, B. Schistosoma and Strongyloides screening in migrants initiating HIV Care in Canada: A cross sectional study. BMC Infect. Dis. 2020, 20, 76. [Google Scholar] [CrossRef] [PubMed]
- Hochberg, N.S.; Moro, R.N.; Sheth, A.N.; Montgomery, S.P.; Steurer, F.; McAuliffe, I.T.; Wang, Y.F.; Armstrong, W.; Rivera, H.N.; Lennox, J.L.; et al. High prevalence of persistent parasitic infections in foreign-born, HIV-infected persons in the United States. PLoS Neglected Trop. Dis. 2011, 5, e1034. [Google Scholar] [CrossRef]
- Smith, C.; Smith, H.; Seaton, R.A.; Fox, R. Seroprevalence of schistosomiasis in African patients infected with HIV. HIV Med. 2008, 9, 436–439. [Google Scholar] [CrossRef]
- Lillie, P.J.; Bazaz, R.; Greig, J.M. Screening African HIV positive patients for imported parasitic infections. J. Infect. 2008, 57, 481–484. [Google Scholar] [CrossRef] [PubMed]
- Lowther, S.A.; Johnson, G.; Hendel-Paterson, B.; Nelson, K.; Mamo, B.; Krohn, K.; Pessoa-Brandão, L.; O’Fallon, A.; Stauffer, W. HIV/AIDS and associated conditions among HIV-infected refugees in Minnesota, 2000–2007. Int. J. Environ. Res. Public Health 2012, 9, 4197–4209. [Google Scholar] [CrossRef]
- Rodari, P.; Tamarozzi, F.; Tais, S.; Degani, M.; Perandin, F.; Buonfrate, D.; Nicastri, E.; Lepore, L.; Giancola, M.L.; Carrara, S.; et al. Prevalence of Chagas disease and strongyloidiasis among HIV-infected Latin American immigrants in Italy-The CHILI study. Travel Med. Infect. Dis. 2022, 48, 102324. [Google Scholar] [CrossRef] [PubMed]
- Theunissen, C.; Bottieau, E.; Van Esbroeck, M.; Tsoumanis, A.; Florence, E. Should We Screen HIV-Positive Migrants for Strongyloidiasis? Pathogens 2020, 9, 388. [Google Scholar] [CrossRef]
- Llenas-García, J.; Hernando, A.; Fiorante, S.; Maseda, D.; Matarranz, M.; Salto, E.; Rubio, R.; Pulido, F. Chagas disease screening among HIV-positive Latin American immigrants: An emerging problem. Eur. J. Clin. Microbiol. Infect. Dis. 2012, 31, 1991–1997. [Google Scholar] [CrossRef]
- Simon, G.G. Impacts of neglected tropical disease on incidence and progression of HIV/AIDS, tuberculosis, and malaria: Scientific links. Int. J. Infect. Dis. 2016, 42, 54–57. [Google Scholar] [CrossRef]
- Asundi, A.; Beliavsky, A.; Liu, X.J.; Akaberi, A.; Schwarzer, G.; Bisoffi, Z.; Requena-Méndez, A.; Shrier, I.; Greenaway, C. Prevalence of strongyloidiasis and schistosomiasis among migrants: A systematic review and meta-analysis. Lancet Glob. Health 2019, 7, e236–e248. [Google Scholar] [CrossRef]
- BHIVA Guidelines for the Routine Investigation and Monitoring of Adult HIV-1-Positive Individuals 2016 (2019 Interim Update). Available online: https://www.bhiva.org/monitoring-guidelines (accessed on 21 October 2024).
- Requena-Méndez, A.; Buonfrate, D.; Gomez-Junyent, J.; Zammarchi, L.; Bisoffi, Z.; Muñoz, J. Evidence-Based Guidelines for Screening and Management of Strongyloidiasis in Non-Endemic Countries. Am. J. Trop. Med. Hyg. 2017, 97, 645–652. [Google Scholar] [CrossRef]
- EACS Guidelines. Available online: https://www.eacsociety.org/guidelines/eacs-guidelines/ (accessed on 20 October 2024).
- Agbata, E.N.; Morton, R.L.; Bisoffi, Z.; Bottieau, E.; Greenaway, C.; Biggs, B.-A.; Montero, N.; Tran, A.; Rowbotham, N.; Arevalo-Rodriguez, I.; et al. Effectiveness of Screening and Treatment Approaches for Schistosomiasis and Strongyloidiasis in Newly-Arrived Migrants from Endemic Countries in the EU/EEA: A Systematic Review. Int. J. Environ. Res. Public Health 2018, 16, 11. [Google Scholar] [CrossRef]
- Public Health Guidance on Screening and Vaccination for Infectious Diseases in Newly Arrived Migrants Within the EU/EEA. Available online: https://www.ecdc.europa.eu/en/publications-data/public-health-guidance-screening-and-vaccination-infectious-diseases-newly (accessed on 4 April 2025).
- CDC Guidance for Overseas Presumptive Treatment of Strongyloidiasis, Schistosomiasis, and Soil-Transmitted Helminth Infections for Refugees Resettling to the United States. Available online: https://www.cdc.gov/immigrant-refugee-health/hcp/overseas-guidance/intestinal-parasite-guidelines.html (accessed on 4 April 2025).
- Tamarozzi, F.; Martello, E.; Giorli, G.; Fittipaldo, A.; Staffolani, S.; Montresor, A.; Bisoffi, Z.; Buonfrate, D. Morbidity Associated with Chronic Strongyloides stercoralis Infection: A Systematic Review and Meta-Analysis. Am. J. Trop. Med. Hyg. 2019, 100, 1305–1311. [Google Scholar] [CrossRef] [PubMed]
- Nabha, L.; Krishnan, S.; Ramanathan, R.; Mejia, R.; Roby, G.; Sheikh, V.; McAuliffe, I.; Nutman, T.; Sereti, I. Prevalence of Strongyloides stercoralis in an urban US AIDS cohort. Pathog. Glob. Health 2012, 106, 238–244. [Google Scholar] [CrossRef] [PubMed]
- Marcos, L.A.; Terashima, A.; Canales, M.; Gotuzzo, E. Update on Strongyloidiasis in the Immunocompromised Host. Curr. Infect. Dis. Rep. 2011, 13, 35–46. [Google Scholar] [CrossRef]
- Sivaram, M.; White, A.; Radcliffe, K.W. Eosinophilia: Clinical significance in HIV-infected individuals. Int. J. STD AIDS 2012, 23, 635–638. [Google Scholar] [CrossRef] [PubMed]
- Forsyth, C.J.; Manne-Goehler, J.; Bern, C.; Whitman, J.; Hochberg, N.S.; Edwards, M.; Marcus, R.; Beatty, N.L.; Castro-Sesquen, Y.E.; Coyle, C.; et al. Recommendations for Screening and Diagnosis of Chagas Disease in the United States. J. Infect. Dis. 2022, 225, 1601–1610. [Google Scholar] [CrossRef]
- Barbiero, A.; Mazzi, M.; Mantella, A.; Trotta, M.; Rossolini, G.M.; Antonelli, A.; Bordonaro, P.; Colao, M.G.; Speciale, A.R.; Di Benedetto, T.; et al. A Questionnaire Integrated with the Digital Medical Record Improved the Coverage of a Control Program for Congenital Chagas Disease in Tuscany, Italy. Microorganisms 2023, 11, 154. [Google Scholar] [CrossRef] [PubMed]
- de Moraes, F.C.A.; Souza, M.E.C.; Dal Moro, L.; Donadon, I.B.; da Silva, E.R.; de Souza, D.D.S.M.; Burbano, R.M.R. Prevention of congenital chagas disease by trypanocide treatment in women of reproductive age: A meta-analysis of observational studies. PLoS Neglected Trop. Dis. 2024, 18, e0012407. [Google Scholar] [CrossRef]
- Lagi, F.; Kiros, S.T.; Di Giambenedetto, S.; Lombardi, F.; Pecorari, M.; Borghi, V.; Lepore, L.; Monno, L.; Setti, M.; Micheli, V.; et al. Long-term maintenance of virologic suppression in native and migrant HIV-1 naïve patients: An Italian cohort study. AIDS Care 2021, 33, 1159–1166. [Google Scholar] [CrossRef]
- Peng, B.; Ling, L. Health service behaviors of migrants: A conceptual framework. Front. Public Health 2023, 11, 1043135. [Google Scholar] [CrossRef]
- Gasparro, G.; Trevisan, S.; Kiros, S.T.; Malcontenti, C.; Trotta, M.; Barbiero, A.; Borchi, B.; Bartalesi, F.; Corsi, P.; Fiorelli, C.; et al. UNAIDS 90-90-90 Target and Retention in Care of a Cohort of Migrants Living with HIV in a Tertiary Referral Hospital in Florence, Italy. AIDS Behav. 2025, 29, 2554–2563. [Google Scholar] [CrossRef]
- Rade, D.A.; Crawford, G.; Lobo, R.; Gray, C.; Brown, G. Sexual Health Help-Seeking Behavior among Migrants from Sub-Saharan Africa and South East Asia living in High Income Countries: A Systematic Review. Int. J. Environ. Res. Public Health 2018, 15, 1311. [Google Scholar] [CrossRef]
General Population (n = 251) | At Risk for CD (n = 137) | At Risk for Sc (n = 85) | At Risk for St (n = 219) | |
---|---|---|---|---|
Cisgender men, n (%) | 116 (46.2) | 47 (34.3) | 43 (50.6) | 94 (43.0) |
Transgender women, n (%) | 81 (32.3) | 80 (58.4) | 15 (17.7) | 81 (37.0) |
Median age [IQR] | 33.1 [26.7–43.0] | 31.9 [26.5–39.3] | 35.9 [26.8–45.1] | 32.7 [26.1–41.6] |
Regular migrants 1, n (%) | 150 (59.8) | 49 (35.8) | 66 (77.7) | 120 (54.8) |
Naïve, n (%) | 105 (41.8) | 49 (35.8) | 36 (42.4) | 92 (42.0) |
Sex workers, n (%) | 68 (29.6) | 65 (50.0) | 9 (12.5) | 68 (34.2) |
HIV diagnosed in Italy, n (%) | 135 (53.8) | 53 (38.7) | 59 (69.4) | 117 (53.4) |
Previous AIDS-defining condition, n (%) | 43 (17.1) | 19 (13.9) | 19 (22.35) | 36 (16.4) |
Median nadir CD4+ count (cell/mmc) [IQR] | 402 [157–595] | 402 [193–633] | 448.5 [210–619] | 410 [169–596] |
Europe | Asia | Latin America | Africa | Total | p-Value | |
---|---|---|---|---|---|---|
Screening ratio | ||||||
Strongyloidiasis | 1/16 (6.3) | 5/18 (27.8) | 70/139 (50.4) | 19/46 (41.3) | 95/219 (43.4) | 0.003 |
Schistosomiasis | - | 1/8 (12.5) | 4/28 (14.3) | 17/49 (34.7) | 22/85 (25.9) | 0.096 |
Chagas disease | - | - | 89/137 (65.0) | - | 89/137 (65.0) | - |
Seroprevalence | ||||||
Strongyloidiasis | 0/1 (0.0) | 0/5 (0.0) | 5/70 (7.1) | 0/19 (0.0) | 5/95 (5.3) | 0.597 |
Schistosomiasis | - | 0/1 (0.0) | 1/4 (25.0) | 2/17 (11.8) | 3/22 (13.6) | 0.724 |
Chagas disease | - | - | 0/89 (0.0) | - | 0/89 (0.0) | - |
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Barbiero, A.; Paggi, R.; Trevisan, S.; Gasparro, G.; Spinicci, M.; Malcontenti, C.; Pozzi, M.; Corsi, P.; Rossolini, G.M.; Colao, M.G.; et al. Serology-Based Screening and Prevalence of Schistosomiasis, Strongyloidiasis, and Chagas Disease in Migrants Living with HIV: Results from a 10-Year Retrospective Cohort in an Italian Tertiary Healthcare Center. Trop. Med. Infect. Dis. 2025, 10, 294. https://doi.org/10.3390/tropicalmed10100294
Barbiero A, Paggi R, Trevisan S, Gasparro G, Spinicci M, Malcontenti C, Pozzi M, Corsi P, Rossolini GM, Colao MG, et al. Serology-Based Screening and Prevalence of Schistosomiasis, Strongyloidiasis, and Chagas Disease in Migrants Living with HIV: Results from a 10-Year Retrospective Cohort in an Italian Tertiary Healthcare Center. Tropical Medicine and Infectious Disease. 2025; 10(10):294. https://doi.org/10.3390/tropicalmed10100294
Chicago/Turabian StyleBarbiero, Anna, Riccardo Paggi, Sasha Trevisan, Giuseppe Gasparro, Michele Spinicci, Costanza Malcontenti, Marco Pozzi, Paola Corsi, Gian Maria Rossolini, Maria Grazia Colao, and et al. 2025. "Serology-Based Screening and Prevalence of Schistosomiasis, Strongyloidiasis, and Chagas Disease in Migrants Living with HIV: Results from a 10-Year Retrospective Cohort in an Italian Tertiary Healthcare Center" Tropical Medicine and Infectious Disease 10, no. 10: 294. https://doi.org/10.3390/tropicalmed10100294
APA StyleBarbiero, A., Paggi, R., Trevisan, S., Gasparro, G., Spinicci, M., Malcontenti, C., Pozzi, M., Corsi, P., Rossolini, G. M., Colao, M. G., Bartoloni, A., Zammarchi, L., & Lagi, F. (2025). Serology-Based Screening and Prevalence of Schistosomiasis, Strongyloidiasis, and Chagas Disease in Migrants Living with HIV: Results from a 10-Year Retrospective Cohort in an Italian Tertiary Healthcare Center. Tropical Medicine and Infectious Disease, 10(10), 294. https://doi.org/10.3390/tropicalmed10100294