Warm-region parasites invasion in temperate climate countries
DOI:
https://doi.org/10.17420/ap71.555Keywords:
Balamuthia mandrillaris, Naegleria fowleri, Trypanosoma cruzi, Strongyloides stercoralis, opportunistic amoebaAbstract
Long-term changes in weather conditions on Earth have a significant impact on the world around us. These include not only increasingly extreme weather events such as droughts and heatwaves. These effects can be felt throughout the natural environment, influencing the spread of parasites and the diseases they transmit. Climate change can alter the range and life cycles of parasites, and accelerate and lengthen the activity period of vectors. Four species are described in this manuscript: Balamuthia mandrillaris, Naegleria fowleri, Trypanosoma cruzi and Strongyloides stercoralis. Balamuthia mandrillaris is a species of an opportunistic cyst-forming free-living amoeba. The main habitat is moist soil and freshwater reservoirs. It could be pathogenic to humans. The amoeba consumes cutaneous tissue and excretes enzymes leading to an immune response of the host. Naegleria fowleri is a free-living amoeba that might cause primary amoebic meningoencephalitis (PAM) whose mortality rate reaches as much as 98%. Trophozoites enter the body through the nasal cavity while underwater. Most often cases of PAM include immunocompetent children and young adults. Trypanosoma cruzi is a flagellate protozoan with life cycle between hematophagous insects of the Triatominae subfamily and various mammal species including human. Trypanosoma cruzi causes the Chagas disease (American trypanosomiasis). Strongyloidiasis, caused by the parasite Strongyloides stercoralis, is a neglected tropical disease (NTD). Infection starts when the host walks barefoot on soil contaminated with filariform larvae that penetrate the skin. Immunosuppression in infected patients can lead to hiperinfection and death.
References
[1] Phan I.Q., Rice C.A., Craig J., Noorai R.E., McDonald J.R., Subramanian S., Tillery L., Barrett L.K., Shankar V., Morris J.C., Van Voorhis W.C., Kyle D.E., Myler P. J. 2021. The transcriptome of Balamuthia mandrillaris trophozoites for structure-guided drug design. Scientific Reports 11(1): 21664. https://doi.org/10.1038/s41598-021-99903-8
[2] Bronstein A.M., Lukashev A.N., Maximova M.S., Sacharova T.V. 2021. The autochthonous cases of acute strongyloidiasis in the Moscow region. Germs 11(1): 116–119. https://doi.org/10.18683/germs.2021.1248
[3] Forsyth C., Agudelo Higuita N.I., Hamer S.A., Ibarra-Cerdeñ C.N., Valdez-Tah A., Stigler Granados P., Hamer G.L., Vingiello M., Beatty N.L. 2024. Climate change and Trypanosoma cruzi transmission in North and central America. The Lancet. Microbe 5(10): 100946. https://doi.org/10.1016/j.lanmic.2024.07.009
[4] Schuster F.L, Visvesvara G.S. 2004. Free-living amoebae as opportunistic and non-opportunistic pathogens of humans and animals. International Journal for Parasitology 34: 1001–1027.
[5] Lorenzo-Morales J., Cabello-Vílchez A.M., Martín-Navarro C.M., Martínez-Carretero E., Piñero J.E., Valladares B. 2013. Is Balamuthia mandrillaris a public health concern worldwide? Trends in Parasitology 29(10): 483–488. https://doi.org/10.1016/j.pt.2013.07.009
[6] Wang L., Cheng W., Li B., Jian Z., Qi X., Sun D., Gao J., Lu X., Yang Y., Lin K., Lu C., Chen J., Li C., Wang G., Gao T. 2020. Balamuthia mandrillaris infection in China: A retrospective report of 28 cases. Emerging Microbes and Infections 9(1): 2348–2357. https://doi.org/10.1080/22221751.2020.1835447
[7] Rodríguez-Expósito R.L., Carbonell L., Recuero-Gil J., Martinez J., Martinez-Valverde R., Martinez-Fernandez C., Ortega-Porcel J., Hernández A.B., Corpa J.M., Cortijo E.M., Sánchez-Nicolás J., Moya S., Pérez-Pérez P., Reyes-Batlle M., Domíngez-de-Barros A., García-Pérez O., Magnet A., Izquierdo F., Fenoy S., Del Águila C., Lorenzo-Morales J. 2025. Fatal amoebic meningoencephalitis caused by Balamuthia mandrillaris in Pongo pygmaeus and first case report in Pan troglodytes verus. Frontiers in Veterinary Science 12: 1534378. https://doi.org/10.3389/fvets.2025.1534378
[8] Matin A., Siddiqui R., Jayasekera S., Khan N.A. 2008. Increasing importance of Balamuthia mandrillaris. Clinical Microbiology Reviews 21(3): 435–448. https://doi.org/10.1128/CMR.00056-07
[9] Javed Z., Hussain M.M., Ghanchi N., Gilani A., Enam S.A. 2024. Non-granulomatous meningoencephalitis with Balamuthia mandrillaris mimicking a tumor: first confirmed case from Pakistan. Surgical Neurology International: 15: 238. https://doi.org/10.25259/SNI_181_2024
[10] Bhosale N.K., Parija S.C. 2021. Balamuthia mandrillaris: An opportunistic, free-living amoeba – an updated review. Tropical Parasitology 11(2): 78–88. https://doi.org/10.4103/tp.tp_36_21
[11] Balczun C., Scheid P.L. 2016. Detection of Balamuthia mandrillaris DNA in the storage case of contact lenses in Germany. Parasitology Research 115(5): 2111–2114. https://doi.org/10.1007/s00436-016-4979-4
[12] Mbaeyi C. 2010. Transplant-transmitted Balamuthia mandrillaris – Arizona, 2010. Morbidity and Mortality Weekly Report 59(36): 1182. https://www.cdc.gov/mmwr/preview/mmwrhtml/mm 5936a4.htm
[13] Schlessinger S., Kokko K., Fratkin J., Butt F,. Hawxby A., Todaro M. 2010. Balamuthia mandrillaris transmitted through organ transplantation – Mississippi, 2009. Morbidity and Mortality Weekly Report 59(36): 1165–1170. CDC. https://www.amjtransplant.org/article/S1600-6135 (22)27793-4/pdf
[14] Basavaraju S.V., Kuehnert M.J., Zaki S.R., Sejvar J.J. 2014. Encephalitis caused by pathogens transmitted through organ transplants, United States, 2002–2013. Emerging Infectious Diseases 20(9): 1443–1451. https://doi.org/10.3201/eid2009.131332
[15] Cope J.R., Landa J., Nethercut H., Collier S.A., Glaser C., Moser M., Puttagunta R., Yoder J.S., Ali I.K., Roy S.I. 2019. The epidemiology and clinical features of Balamuthia mandrillaris disease in the United States, 1974–2016. Clinical Infectious Diseases 68(11): 1815–1822. https://doi.org/10.1093/cid/ciy813
[16] Visvesvara G.S., Martinez A.J., Schuster F.L., Leitch G.J., Wallace S.V,. Sawyer T.K., Anderson M. 1990. Leptomyxid ameba, a new agent of amebic meningoencephalitis in humans and animals. Journal of Clinical Microbiology 28(12): 2750–2756. https://doi.org/10.1128/jcm.28.12.2750-2756.1990
[17] Kodet R., Nohýnková E., Tichý M., Soukup J., Visvesvara G.S. 1998. Amebic encephalitis caused by Balamuthia mandrillaris in a Czech child: description of the first case from Europe. Pathology, Research and Practice 194(6): 423–429. https://doi.org/10.1016/S0344-0338(98)80033-2
[18] Rowen J.L., Doerr C.A., Vogel H., Baker C.J. 1995. Balamuthia mandrillaris: a newly recognized agent for amebic meningoencephalitis. The Pediatric infectious Disease Journal 14(8): 705–710.
[19] Yu X., Xu W. 2025. A case report of Balamuthia mandrillaris encephalitis: experience from Central China. Neurosurgical Subspecialties 1(1): 44–47. https://doi.org/10.14218/NSSS.2025.00001
[20] Gianinazzi C., Schild M., Zumkehr B., Wüthrich F., Nüesch I., Ryter R., Schürch N., Gottstein B., Müller N. 2010. Screening of Swiss hot spring resorts for potentially pathogenic free-living amoebae. Experimental Parasitology 126(1): 45–53. https://doi.org/10.1016/j.exppara.2009.12.008
[21] van der Beek N.A., van Tienen C., de Haan J.E., Roelfsema J., Wismans P.J., van Genderen P.J., Tanghe H.L., Verdijk R.M., Titulaer M.J., van Hellemond J.J. 2015. Fatal Balamuthia mandrillaris Meningoencephalitis in the Netherlands after travel to the Gambia. Emerging Infectious Diseases 21(5): 896–898. https://doi.org/10.3201/eid2105.141325
[22] Visvesvara G.S., Moura H., Schuster F.L. 2007. Pathogenic and opportunistic free-living amoebae: Acanthamoeba spp., Balamuthia mandrillaris, Naegleria fowleri, and Sappinia diploidea. FEMS Immunology and Medical Microbiology 50(1): 1–26. https://doi.org/10.1111/j.1574-695x.2007.00232.x
[23] Krasaelap A., Prechawit S., Chansaenroj J., Punyahotra P., Puthanakit T., Chomtho K., Shuangshoti S., Amornfa J., Poovorawan Y. 2013. Fatal Balamuthia amebic encephalitis in a healthy child: a case report with review of survival cases. Korean Journal of Parasitology 51(3): 335–341. https://doi.org/10.3347/kjp.2013.51.3.335
[24] Li Z., Li W., Li Y., Ma F., Li G. 2024. A case report of Balamuthia mandrillaris encephalitis. Heliyon 10(5): e26905. https://doi.org/10.1016/j.heliyon.2024.e26905
[25] Huang Z.H., Ferrante A., Carter R.F. 1999. Serum antibodies to Balamuthia mandrillaris, a free-living amoeba recently demonstrated to cause granulomatous amoebic encephalitis. Journal of Infectious Diseases 179(5): 1305–1308. https://doi.org/10.1086/314731
[26] Schuster F.L., Yagi S., Wilkins P.P., Gavali S., Visvesvara G.S., Glaser C.A. 2008. Balamuthia mandrillaris, agent of amoebic encephalitis: detection of serum antibodies and antigenic similarity of isolates by enzyme immunoassay. Journal of Eukaryotic Microbiology 55(4): 313–320. https://doi.org/10.1111/j.1550-7408.2008.00333.x
[27] Kiderlen A.F., Radam E., Tata P.S. 2009. Assessment of Balamuthia mandrillaris-specific serum antibody concentrations by flow cytometry. Parasitology Research 104(3): 663–670. https://doi.org/10.1007/s00436-008-1243-6
[28] Combs F.J. Jr., Erly W.K., Valentino C.M., Rance N.E. 2011. Best cases from the AFIP: Balamuthia mandrillaris amebic meningoencephalitis. Radiographics: a review publication of the Radiological Society of North America, Inc 31(1): 31–35. https://doi.org/10.1148/rg.311105067
[29] Bravo F.G., Alvarez P.J., Gotuzzo E. 2011. Balamuthia mandrillaris infection of the skin and central nervous system: an emerging disease of concern to many specialties in medicine. Current Opinion in Infectious Diseases 24(2): 112–117. https://doi.org/10.1097/QCO.0b013e3283428d1e
[30] Mungroo M.R., Shahbaz M.S., Anwar A., Saad S.M., Khan K.M., Khan N.A., Siddiqui R. 2020. Aryl quinazolinone derivatives as novel therapeutic agents against brain-eating amoebae. ACS Chemical Neuroscience 11(16): 2438–2449. https://doi.org/10.1021/acschemneuro.9b00596
[31] Schuster F.L., Visvesvara G.S. 1996. Axenic growth and drug sensitivity studies of Balamuthia mandrillaris, an agent of amebic meningoencephalitis in humans and other animals. Journal of Clinical Microbiology 34(2): 385–388. https://doi.org/10.1128/jcm.34.2.385-388.1996
[32] Siddiqui R., Ali I.K.M., Cope J.R., Khan N.A. 2016. Biology and pathogenesis of Naegleria fowleri. Acta Tropica 164: 375–394. https://doi.org/10.1016/j.actatropica.2016.09.009
[33] Heilmann A., Rueda Z., Alexander D., Laupland K.B., Keynan Y. 2024. Impact of climate change on amoeba and the bacteria they host. Journal of the Association of Medical Microbiology and Infectious Disease Canada 9(1): 1–5. https://doi.org/10.3138/jammi-2023-09-08
[34] Kemble S.K., Lynfield R., DeVries A.S., Drehner D.M., Pomputius W.F.,3rd, Beach M.J., Visvesvara G.S., da Silva A.J., Hill V.R., Yoder J.S., Xiao L., Smith K.E., Danila R. 2012. Fatal Naegleria fowleri infection acquired in Minnesota: possible expanded range of a deadly thermophilic organism. Clinical Infectious Diseases 54(6): 805–809. https://doi.org/10.1093/cid/cir961
[35] Maciver S.K., Piñero J.E., Lorenzo-Morales J. 2020. Is Naegleria fowleri an emerging parasite? Trends in Parasitology 36(1): 19–28. https://doi.org/10.1016/j.pt.2019.10.008
[36] Dzikowiec M., Góralska K., Błaszkowska J. 2017. Neuroinvasions caused by parasites. Annals of Parasitology 63(4): 243–253. https://doi.org/10.17420/ap6304.111
[37] Güémez A., García E. 2021. Primary amoebic meningoencephalitis by Naegleria fowleri: pathogenesis and treatments. Biomolecules 11: 1320. https://doi.org/10.3390/biom11091320
[38] Das S.R. 1972. Isolation of Naegleria and Hartmannella amoebae from Beckenham (London) soils and their pathogenicity in mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 66(4): 663–664. https://doi.org/10.1016/0035-9203(72)90313-6
[39] Dyková I., Kostka M., Wortberg F., Nardy E., Pecková H. 2010. New data on aetiology of nodular gill disease in rainbow trout, Oncorhynchus mykiss. Folia Parasitologica (Praha). 57(3): 157–163.
[40] Vannetti S.M., Wynne J.W., English C., Huynh C., Knüsel R., de Sales-Ribeiro C., Widmer M., Delalay G., Schmidt-Posthaus H. 2023. Amoeba species colonizing the gills of rainbow trout (Oncorhynchus mykiss) in Swiss aquaculture. Journal of Fish Diseases 46(9): 987–999. https://doi.org/10.1111/jfd.13819
[41] Kožíšek F., Rychlíková E., Pumann P. 2019. 16 victims and 16 years for elucidating the case. A reminder of the worst Czech bathing water epidemic in Ústí nad Labem, Hygiena 64(2): 52–58. https://doi.org/10.21101/hygiena.a1708
[42] Apley J., Clarke S.K., Roome A.P., Sandry S.A., Saygi G., Silk B., Warhurst D.C. 1970. Primary amoebic meningoencephalitis in Britain. British Medical Journal 1(5696): 596–599. https://doi.org/10.1136/bmj.1.5696.596
[43] Cope J.R., Ali I.K. 2016. Primary amebic meningoencephalitis: what have we learned in the last 5 years?. Current Infectious Disease Reports 18(10): 31. https://doi.org/10.1007/s11908-016-0539-4
[44] Grace E., Asbill S., Virga, K. 2015. Naegleria fowleri: pathogenesis, diagnosis, and treatment options. Antimicrobial Agents and Chemotherapy 59(11): 6677–6681. https://doi.org/10.1128/AAC.01293-15
[45] Rojas-Hernández S., Rodríguez-Monroy M.A., Moreno-Fierros L., Jarillo-Luna A., Carrasco-Yepez M., Miliar-García A., Campos-Rodríguez R. 2007. Nitric oxide production and nitric oxide synthase immunoreactivity in Naegleria fowleri. Parasitology Research 101(2): 269–274. https://doi.org/10.1007/s00436-007-0495-x
[46] Cervantes-Sandoval I., Serrano-Luna J.D.J., García-Latorre E., Tsutsumi V., Shibayama M. 2008. Characterization of brain inflammation during primary amoebic meningoencephalitis. Parasitology. International 57(3): 307–313. https://doi.org/10.1016/j.parint.2008.01.006
[47] Song K.J., Jang Y.S., Lee Y.A., Kim K.A., Lee S.K., Shin M.H. 2011. Reactive oxygen species-dependent necroptosis in Jurkat T cells induced by pathogenic free-living Naegleria fowleri. Parasite Immunology 33(7): 390–400. https://doi.org/10.1111/j.1365-3024.2011.01297.x
[48] De Oca A.C., Carrasco-Yépez M., Campos-Rodríguez R., Pacheco-Yépez J., Bonilla-Lemus P., Pérez-López J., Rojas-Hernández S. 2016. Neutrophils extracellular traps damage Naegleria fowleri trophozoites opsonized with human IgG. Parasite Immunology 38(8): 481–495. https://doi.org/10.1111/pim.12337
[49] Bellini N.K., Santos T.M., da Silva M.T.A., Thiemann O.H. 2018. The therapeutic strategies against Naegleria fowleri. Experimental Parasitology 187: 1–11. https://doi.org/10.1016/j.exppara.2018.02.010
[50] De Fuentes-Vicente J.A., Vidal-López D.G., Flores-Villegas A.L., Moreno-Rodríguez A., De Alba-Alvarado M.C., Salazar-Schettino P.M., Rodríguez-López M.H., Gutiérrez-Cabrera A.E. 2019. Trypanosoma cruzi: a review of biological and methodological factors in Mexican strains. Acta Tropica 195: 51–57. https://doi.org/10.1016/j.actatropica.2019.04.024
[51] Herrera L. 2014. Trypanosoma cruzi, the causal agent of Chagas disease: boundaries between wild and domestic cycles in Venezuela. Frontiers in Public Health 2: 259. https://doi.org/10.3389/fpubh.2014.00259
[52] Hemmige V., Tanowitz H., Sethi A. 2012. Trypanosoma cruzi infection: a review with emphasis on cutaneous manifestations. International Journal of Dermatology 51(5): 501–508. https://doi.org/10.1111/j.1365-4632.2011.05380.x
[53] Echavarría N.G., Echeverría L.E., Stewart M., Gallego C., Saldarriaga C. 2021. Chagas disease: chronic Chagas cardiomyopathy. Current Problems in Cardiology 46(3): 100507. https://doi.org/10.1016/j.cpcardiol.2019.100507
[54] Machado F.S., Dutra W.O., Esper L., Gollob K.J., Teixeira M.M., Factor S.M., Weiss L. M., Nagajyothi F., Tanowitz H.B., & Garg N.J. 2012. Current understanding of immunity to Trypanosoma cruzi infection and pathogenesis of Chagas disease. Seminars in Immunopathology 34(6): 753–770. https://doi.org/10.1007/s00281-012-0351-7
[55] Patz J.A., Githeko A.K., McCarty J.P., Hussein S., Confalonieri U. DeWet N. 2003. Climate change and infectious diseases. Climate Change and Human Health: Risks and Responses 2: 103–132.
[56] Van de Vuurst P. Escobar L.E. 2023. Climate change and infectious disease: a review of evidence and research trends. Infectious Diseases of Poverty 12(1): 51. https://doi.org/10.1186/s40249-023-01102-2
[57] Yadav N., Upadhyay R.K. 2023. Global effect of climate change on sea-sonal cycles, vector population and rising challenges of communicable diseases: a review. Journal of Atmospheric Science Research 6(1): 21–59. https://doi.org/10.30564/jasr.v6i1.5165
[58] Brasil L.S., Silvério D.V., Silva J.O.A., Santos W.S., de Melo L.V., Juen L., França F.M., Vieira T.B. 2025. Potential geographic displacement of Chagas disease vectors under climate change. Medical and Veterinary Entomology 39(4): 709–717. https://doi.org/10.1111/mve.12810
[59] Shikanai-Yasuda M.A., Carvalho N.B. 2012. Oral transmission of Chagas disease. Clinical Infectious Diseases 54(6): 845–852. https://doi.org/10.1093/cid/cir956
[60] De Souza W., Barrias E.S. 2020. May the epimastigote form of Trypanosoma cruzi be infective? Acta Tropica 212: 105688. https://doi.org/10.1016/j.actatropica.2020.105688
[61] Jimenez V. 2014. Dealing with environmental challenges: mechanisms of adaptation in Trypanosoma cruzi. Research in Microbiology 165(3): 155–165.https://doi.org/10.1016/j.resmic.2014.01.006
[62] Bern C., Kjos S., Yabsley M.J., Montgomery S.P. 2011. Trypanosoma cruzi and Chagas disease in the United States. Clinical Microbiology Reviews 24(4): 655–681. https://doi.org/10.1128/CMR.00005-11
[63] Tyler K.M., Engman D.M. 2001. The life cycle of Trypanosoma cruzi revisited. International Journal for Parasitology 31(5–6): 472–481. https://doi.org/10.1016/s0020-7519(01)00153-9
[64] Nunes M.C.P., Beaton A., Acquatella H., Bern C., Bolger A.F., Echeverría L.E., Dutra W.O., Gascon J., Morillo C.A., Oliveira-Filho J., Ribeiro A.L.P., Marin-Neto J.A., American Heart Association Rheumatic Fever, Endocarditis and Kawasaki Disease Committee of the Council on Cardiovascular Disease in the Young; Council on Cardiovascular and Stroke Nursing; and Stroke Council. 2018. Chagas cardiomyopathy: an update of current clinical knowledge and management: a scientific statement from the American Heart Association. Circulation 138(12): e169–e209. https://doi.org/10.1161/CIR.0000000000000599
[65] Añez N., Carrasco H., Parada H., Crisante G., Rojas A., Gonzalez N., Ramirez J.L., Guevara P., Rivero C., Borges R., Scorza J.V. 1999. Acute Chagas disease in western Venezuela: a clinical, seroparasitologic, and epidemiologic study. The American Journal of Tropical Medicine and Hygiene 60(2): 215–222. https://doi.org/10.4269/ajtmh.1999.60.215
[66] Pérez-Molina J.A., Molina I. 2018. Chagas disease. Lancet (London, England) 391(10115): 82–94. https://doi.org/10.1016/S0140-6736(17)31612-4
[67] Santos É., Menezes Falcão L. 2020. Chagas cardiomyopathy and heart failure: from epidemiology to treatment. Revista Portuguesa de Cardiologia 39(5): 279–289. https://doi.org/10.1016/j.repc.2019.12.006
[68] Ramírez-Toloza G., Ferreira A. 2017. Trypanosoma cruzi evades the complement system as an efficient strategy to survive in the mammalian host: the specific roles of host/parasite molecules and Trypanosoma cruzi calreticulin. Frontiers in Microbiology 1: 8: 1667. https://doi.org/10.3389/fmicb.2017.01667
[69] da Silveira A.B., Lemos E.M., Adad S.J., Correa-Oliveira R., Furness J.B., D’Avila Reis D. 2007. Megacolon in Chagas disease: a study of inflammatory cells, enteric nerves, and glial cells. Human Pathology 38(8): 1256–1264. https://doi.org/10.1016/j.humpath.2007.01.020
[70] Altclas J., Sinagra A., Jaimovich G., Salgueira C., Luna C., Requejo A., Milovic V., De Rissio A., Feldman L., Riart A. 1999. Reactivation of chronic Chagas disease following allogeneic bone marrow transplantation and successful pre-emptive therapy with benznidazole. Transplant Infectious Disease 1(2): 135–137. https://doi.org/10.1034/j.1399-3062.1999.010207.x
[71] Bern C., Montgomery S.P., Herwaldt B.L., Rassi A., Marin-Neto J.A., Dantas, R.O., Maguire J. H., Acquatella H., Morillo C., Kirchhoff L.V., Gilman R.H., Reyes P.A., Salvatella R., Moore, A.C. 2007. Evaluation and treatment of chagas disease in the United States: a systematic review. JAMA 298(18): 2171–2181.
[72] Araújo E.F., Chamlian E.G., Peroni A.P., Pereira W.L., Gandra S.M., Rivetti L.A. 2014. Cardiac resynchronization therapy in patients with chronic Chagas cardiomyopathy: long-term follow up. Revista Brasileira de Cirurgia Cardiovascular 29(1): 31–36. https://doi.org/10.5935/1678-9741.20140008
[73] Cafferata M.L., Toscani M.A., Althabe F., Belizán J.M., Bergel E., Berrueta M., Capparelli E.V., Ciganda Á., Danesi E., Dumonteil E., Gibbons L., Gulayin P.E., Herrera C., Momper J.D., Rossi S., Shaffer J.G., Schijman A.G., Sosa-Estani S., Stella, C.B., Klein K., Buekens P. 2020. Short-course benznidazole treatment to reduce Trypanosoma cruzi parasitic load in women of reproductive age (BETTY): a non-inferiority randomized controlled trial study protocol. Reproductive Health 17(1): 128. https://doi.org/10.1186/s12978-020-00972-1
[74] Sing A., Leitritz L., Bogner J.R., Heesemann J. 1999. First-glance diagnosis of Strongyloides stercoralis autoinfection by stool microscopy. Journal of Clinical Microbiology 37(5): 1610–1611. https://doi.org/10.1128/JCM.37.5.1610-1611.1999
[75] Greaves D., Coggle S., Pollard C., Aliyu S.H., Moore E.M. 2013. Strongyloides stercoralis infection. BMJ 347: f4610. https://doi.org/10.1136/bmj.f4610
[76] Ottino L., Buonfrate D., Paradies P., Bisoffi Z., Antonelli A., Rossolini G.M., Gabrielli S., Bartoloni A., Zammarchi L. 2020. Autochthonous human and canine Strongyloides stercoralis infection in Europe: report of a human case in an Italian teen and systematic review of the literature. Pathogens 9(6): 439. https://doi.org/10.3390/pathogens9060439
[77] Gregory B.T., Desouky M., Slaughter J., Hallem E.A., Bryant A.S. 2024. Thermosensory behaviors of the free-living life stages of Strongyloides species support parasitism in tropical environments. bioRxiv: the preprint server for biology 2024.09.12.612595. https://doi.org/10.1101/2024.09.12.612595
[78] Gordon C.A., Utzinger J., Muhi S., Becker S.L., Keiser J., Khieu V., Gray D.J. 2024. Strongyloidiasis. Nature Reviews. Disease Primers 10(1): 6. https://doi.org/10.1038/s41572-023-00490-x
[79] Chessell C., Rabuszko L., Richardson D., Llewellyn C. 2024. Factors associated with the sexual transmission of Strongyloides stercoralis in men who have sex with men: a systematic review. Journal of the European Academy of Dermatology and Venereology 38(4): 673–679. https://doi.org/10.1111/jdv.19664
[80] Centers for Disease Control and Prevention (CDC). 2012. Transmission of Strongyloides stercoralis through transplantation of solid organs – Pennsylvania. Morbity and Mortality Weekly Report 62(14): 264–266. https://www.cdc.gov/mmwr /preview/mmwrhtml/mm 6214a2.htm
[81] Czeresnia J.M., Weiss L.M. 2022. Strongyloides stercoralis. Lung 200(2): 141–148. https://doi.org/10.1007/s00408-022-00528-z
[82] Teixeira M.C., Pacheco F.T., Souza J.N., Silva M.L., Inês E.J., Soares N.M. 2016. Strongyloides stercoralis Infection in alcoholic patients. BioMed Research International 4872473. https://doi.org/10.1155/2016/4872473
[83] Zhao H., Bradbury R.S. 2024. Feline strongyloidiasis: an insight into its global prevalence and transmission cycle. One Health 19: 100842. https://doi.org/10.1016/j.onehlt.2024.100842
[84] de Oliveira L.C., Ribeiro C.T., Mendes D., Oliveira T.C., Costa-Cruz J.M. 2002. Frequency of Strongyloides stercoralis infection in alcoholics. Memorias do Instituto Oswaldo Cruz 97(1): 119–121. https://doi.org/10.1590/s0074-02762002000100021
[85] Yeh M.Y., Aggarwal S., Carrig M., Azeem A., Nguyen A., Devries S., Destache C., Nguyen T., Velagapudi M. 2023. Strongyloides stercoralis infection in humans: a narrative Rrview of the Mmst neglected parasitic disease. Cureus 15(10): e46908. https://doi.org/10.7759/cureus.46908
[86] Abrantes R., Barata R., Caeiro F., Ferreira A., Nolasco F. 2023. Strongyloides stercoralis after renal transplantation – a global threat. Nefrologia 43(6): 789–790. https://doi.org/10.1016/j.nefroe.2022.11.017
[87] Singh B., Verma S., Rashid K., Stoltzfus M.T. 2024. Loeffler’s syndrome induced by the transmigration of Strongyloides stercoralis to the lungs: a case report and literature review. Cureus 16(12): e75897. https://doi.org/10.7759/cureus.75897
[88] Bae K., Jeon K.N., Ha J.Y., Lee J.S., Na B.K. 2018. Pulmonary strongyloidiasis presenting micronodules on chest computed tomography. Journal of Thoracic Disease 10(8): E612–E615. https://doi.org/10.21037/jtd.2018.07.32
[89] Mejia R., Nutman T.B. 2012. Screening, prevention, and treatment for hyperinfection syndrome and disseminated infections caused by Strongyloides stercoralis. Current Opinion in Infectious Diseases 25(4): 458–463. https://doi.org/10.1097/QCO.0b013e3283551dbd
[90] Vadlamudi R.S., Chi D.S, Krishnaswamy G. 2006. Intestinal strongyloidiasis and hyperinfection syndrome. Clinical and Molecular Allergy 4: 8. https://doi.org/10.1186/1476-7961-4-8
[91] Cai S., Zhou M., Zhang Y., Luo W., Xie B. 2024. Residual gastritis associated with Strongyloides stercoralis infection: a case report. Medicine (Baltimore) 103(39): e39714. https://doi.org/10.1097/MD.0000000000039714
[92] Ashiri A., Rafiei A., Beiromvand M., Khanzadeh A., Alghasi A. 2021. Case report: challenges for the diagnosis and treatment of Strongyloides stercoralis in chronic obstructive pulmonary disease patients. American Journal of Tropical Medicine and Hygiene 106(2): 695–699. https://doi.org/10.4269/ajtmh.21-1011
[93] Hamze H., Tai T., Harris D. 2023. Strongyloides hyperinfection syndrome precipitated by immunosuppressive therapy for rheumatoid arthritis and COVID-19 pneumonia. Tropical Diseases, Travel Medicine and Vaccines 9(1): 15. https://doi.org/10.1186/s40794-023-00201-0
[94] Buonfrate D., Bradbury R.S., Watts M.R., Bisoffi Z. 2023. Human strongyloidiasis: complexities and pathways forward. Clinical Microbiology Reviews 36(4): e0003323. https://doi.org/10.1128/cmr.00033-23
[95] Prendki V., Fenaux P., Durand R., Thellier M., Bouchaud O. 2011. Strongyloidiasis in man 75 years after initial exposure. Emerging Infectious Diseases 17(5): 931–932. https://doi.org/10.3201/eid1705.100490
[96] Karanam L.S.K., Basavraj G.K. Papireddy C.K.R. 2021. Strongyloides stercoralis hyper infection syndrome. Indian Journal of Surgery 83 (Suppl. 3): 582–586. https://doi.org/10.1007/s12262-020-02292-x
[97] Rodríguez-Guardado A., Álvarez-Martínez M.J., Flores M.D., Sulleiro E., Torrús-Tendero D., Velasco M., Membrillo F.J.; Imported Pathology Group of the SEIMC. 2023. Screening for strongyloidiasis in Spain in the context of the SARS-CoV-2 pandemic: results of a survey on diagnosis and treatment. Enfermedades Infecciosas y Microbiologia Clinica (Engl Ed) 41(6): 329–334. https://doi.org/10.1016/j.eimce.2022.08.006
[98] Miret R., Acosta-Rullan J.M., Toll A., Honeycutt G., Malhi M., Zorrilla C.A., Diaz R., Danckers M., Zapata D. 2025. The unwelcome guest: Strongyloides stercoralis hyperinfection in a patient with steroid-dependent asthma-COPD overlap syndrome (ACOS) – a case report and review of literature. Case Reports in Pulmonology: 3204304. https://doi.org/10.1155/crpu/3204304
[99] Schär F., Trostdorf U., Giardina F., Khieu V., Muth S., Marti H., Vounatsou P., Odermatt P. 2013. Strongyloides stercoralis: global distribution and risk factors. PLoS Neglected Tropical Diseases 7(7): e2288. https://doi.org/10.1371/journal.pntd.0002288
[100] Gelaye W., Williams N.A., Kepha S., Junior A.M., Fleitas P.E., Marti-Soler H., Damtie D., Menkir S., Krolewiecki A.J., van Lieshout L., Enbiale W. 2021. Stopping transmission of intestinal parasites (STOP) project consortium. Performance evaluation of Baermann techniques: the quest for developing a microscopy reference standard for the diagnosis of Strongyloides stercoralis. PLoS Neglected Tropical Diseases 15(2): e0009076. https://doi.org/10.1371/journal.pntd.0009076
[101] Albermann S., Vischer A., Vu X.L., Horat A., Grimm F., Nickel B., Gottstein B., Hirzel C., Oberli A. 2025. Serodiagnosis of strongyloidiasis in a low-endemic setting – a two-tiered test approach. Travel Medicine and Infectious Disease 67: 102890. https://doi.org/10.1016/j.tmaid.2025.102890
[102] Arifin N., Hanafiah K.M., Ahmad H., Noordin R. 2019. Serodiagnosis and early detection of Strongyloides stercoralis infection. Journal of Microbiology, Immunology and Infection 52(3): 371–378. https://doi.org/10.1016/j.jmii.2018.10.001
[103] Kadkhoda K., Gibson Jr., B. 2020. Evaluation of a new Strongyloides ELISA IgG test kit. Clinical Laboratory 66(12): https://doi.org/10.7754/Clin.Lab.2020.200319
[104] Hailu T., Nibret E., Amor A., Munshea A., Anegagrie M. 2020. Efficacy of single dose ivermectin against Strongyloides stercoralis infection among primary school children in Amhara National Regional State. Infectious Diseases (Auckl) 13: 1178633720932544. https://doi.org/10.1177/1178633720932544
[105] Buonfrate D., Salas-Coronas J., Muñoz J., Maruri B.T., Rodari P., Castelli F., Zammarchi L., Bianchi L., Gobbi F., Cabezas-Fernández T., Requena-Mendez A., Godbole G., Silva R., Romero M., Chiodini P.L., Bisoffi Z. 2019. Multiple-dose versus single-dose ivermectin for Strongyloides stercoralis infection (Strong Treat 1 to 4): a multicentre, open-label, phase 3, randomised controlled superiority trial. The Lancet. Infectious Diseases 19(11): 1181–1190. https://doi.org/10.1016/S1473-3099(19)30289-0
