{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,30]],"date-time":"2026-09-30T20:36:02Z","timestamp":1790800562170,"version":"4.1.0"},"reference-count":101,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,7,27]],"date-time":"2023-07-27T00:00:00Z","timestamp":1690416000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Funda\u00e7\u00e3o de Amparo \u00e0 Pesquisa do Estado de Minas Gerais","award":["APQ 01637-17"],"award-info":[{"award-number":["APQ 01637-17"]}]},{"name":"Conselho Nacional de Desenvolvimento Cient\u00edfico e Tecnol\u00f3gico","award":["APQ 01637-17"],"award-info":[{"award-number":["APQ 01637-17"]}]},{"name":"Coordena\u00e7\u00e3o de Aperfei\u00e7oamento de Pessoal de N\u00edvel Superior","award":["APQ 01637-17"],"award-info":[{"award-number":["APQ 01637-17"]}]},{"name":"Universidade Federal de Minas Gerais","award":["APQ 01637-17"],"award-info":[{"award-number":["APQ 01637-17"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["TropicalMed"],"abstract":"<jats:p>A remarkable characteristic of infectious diseases classified as Neglected Tropical Diseases (NTDs) is the fact that they are mostly transmitted in tropical and subtropical regions with poor conditions of sanitation and low access to healthcare, which makes transmission areas more likely to overlap. Two of the most important NTDs, schistosomiasis and leishmaniasis, despite being caused by very different etiological agents, have their pathogenesis heavily associated with immune-mediated mechanisms, and Schistosoma spp. and Leishmania spp. have been shown to simultaneously infect humans. Still, the consequences of Schistosoma\u2013Leishmania coinfections remain underexplored. As the inflammatory processes elicited by each one of these parasites can influence the other, several changes have been observed due to this coinfection in naturally infected humans, experimental models, and in vitro cell assays, including modifications in susceptibility to infection, pathogenesis, prognostic, and response to treatment. Herein, we review the current knowledge in Schistosoma\u2013Leishmania coinfections in both human populations and experimental models, with special regard to how schistosomiasis affects tegumentary leishmaniasis, discuss future perspectives, and suggest a few steps to further improve our understanding in this model of parasite\u2013host\u2013parasite interaction.<\/jats:p>","DOI":"10.3390\/tropicalmed8080383","type":"journal-article","created":{"date-parts":[[2023,7,28]],"date-time":"2023-07-28T02:08:00Z","timestamp":1690510080000},"page":"383","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":5,"title":["Schistosoma and Leishmania: An Untold Story of Coinfection"],"prefix":"10.3390","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-0501-2508","authenticated-orcid":false,"given":"Genil Moror\u00f3 Ara\u00fajo","family":"Camelo","sequence":"first","affiliation":[{"name":"Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte 31270-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4194-7578","authenticated-orcid":false,"given":"Jeferson Kelvin Alves de Oliveira","family":"Silva","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte 31270-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Stefan Michael","family":"Geiger","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte 31270-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maria Norma","family":"Melo","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte 31270-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7670-5216","authenticated-orcid":false,"given":"Deborah Aparecida","family":"Negr\u00e3o-Corr\u00eaa","sequence":"additional","affiliation":[{"name":"Department of Parasitology, Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte 31270-901, Brazil"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,7,27]]},"reference":[{"key":"ref_1","unstructured":"WHO (2020). Ending the Neglect to Attain the Sustainable Development Goals: A Road Map for Neglected Tropical Diseases 2021\u20132030, World Health Organization."},{"key":"ref_2","unstructured":"WHO (2021). Neglected tropical diseases: Impact of COVID-19 and WHO\u2019s response\u20142021 update. Wkly. Epidemiol. Rec., 96, 461\u2013468."},{"key":"ref_3","unstructured":"WHO (2012). Accelerating Work to Overcome the Global Impact of Neglected Tropical Diseases\u2014A Roadmap for Implementation, World Health Organization."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/bs.apar.2021.08.007","article-title":"Towards global control of parasitic diseases in the COVID-19 era: One Health and the future of multisectoral global health governance","volume":"114","author":"Ung","year":"2021","journal-title":"Adv. Parasitol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1093\/trstmh\/traa157","article-title":"Neglected tropical disease control in a world with COVID-19: An opportunity and a necessity for innovation","volume":"115","author":"Brooker","year":"2021","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"236","DOI":"10.1093\/trstmh\/traa202","article-title":"Disruptions to schistosomiasis programmes due to COVID-19: An analysis of potential impact and mitigation strategies","volume":"115","author":"Kura","year":"2021","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"694","DOI":"10.1016\/j.pt.2021.05.003","article-title":"The impact of COVID-19 on neglected parasitic diseases: What to expect?","volume":"37","author":"Miguel","year":"2021","journal-title":"Trends Parasitol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"106859","DOI":"10.1016\/j.actatropica.2023.106859","article-title":"Impact of the COVID-19 pandemic on the actions of the Schistosomiasis Control Program in an endemic area in Northeastern Brazil","volume":"240","author":"Dantas","year":"2023","journal-title":"Acta Trop."},{"key":"ref_9","unstructured":"WHO (2021). Schistosomiasis and soil-transmitted helminthiases: Progress report, 2020. Wkly. Epidemiol. Rec., 96, 585\u2013595."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1128\/CMR.00137-14","article-title":"Advances in the Diagnosis of Human Schistosomiasis","volume":"28","author":"Weerakoon","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"89","DOI":"10.3389\/fimmu.2013.00089","article-title":"The Schistosoma Granuloma: Friend or Foe?","volume":"4","author":"Hams","year":"2013","journal-title":"Front. Immunol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"3157","DOI":"10.4049\/jimmunol.172.5.3157","article-title":"The Pathogenesis of Schistosomiasis Is Controlled by Cooperating IL-10-Producing Innate Effector and Regulatory T Cells","volume":"172","author":"Hesse","year":"2004","journal-title":"J. Immunol."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2253","DOI":"10.1016\/S0140-6736(13)61949-2","article-title":"Human schistosomiasis","volume":"383","author":"Colley","year":"2014","journal-title":"Lancet"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"383","DOI":"10.1016\/j.idc.2012.03.004","article-title":"Schistosomiasis","volume":"26","author":"Gryseels","year":"2012","journal-title":"Infect. Dis. Clin. N. Am."},{"key":"ref_15","doi-asserted-by":"crossref","unstructured":"Scorza, B.M., Carvalho, E.M., and Wilson, M.E. (2017). Cutaneous Manifestations of Human and Murine Leishmaniasis. Int. J. Mol. Sci., 18.","DOI":"10.3390\/ijms18061296"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"750","DOI":"10.12688\/f1000research.11120.1","article-title":"Leishmaniasis: A review","volume":"6","author":"Arenas","year":"2017","journal-title":"F1000Research"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"S359","DOI":"10.1590\/S0102-311X1994000800014","article-title":"Tegumentary and visceral leishmaniases in Brazil: Emerging anthropozoonosis and possibilities for their control","volume":"10","author":"Marzochi","year":"1994","journal-title":"Cad. Saude Publica"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"536","DOI":"10.4269\/ajtmh.1991.44.536","article-title":"Leishmaniasis in Bahia, Brazil: Evidence that Leishmania amazonensis Produces a Wide Spectrum of Clinical Disease","volume":"44","author":"Barral","year":"1991","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"e54","DOI":"10.1086\/340261","article-title":"Epidemiologic and Immunologic Findings for the Subclinical Form of Leishmania braziliensis Infection","volume":"34","author":"Follador","year":"2002","journal-title":"Clin. Infect. Dis."},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Salam, N., Al-Shaqha, W.M., and Azzi, A. (2014). Leishmaniasis in the Middle East: Incidence and Epidemiology. PLoS Negl. Trop. Dis., 8.","DOI":"10.1371\/journal.pntd.0003208"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1047","DOI":"10.1016\/j.ijpara.2021.05.009","article-title":"Comparative genomics of Leishmania isolates from Brazil confirms the presence of Leishmania major in the Americas","volume":"51","author":"Baptista","year":"2021","journal-title":"Int. J. Parasitol."},{"key":"ref_22","first-page":"401","article-title":"Global leishmaniasis surveillance: 2019\u20132020, a baseline for the 2030 roadmap","volume":"96","author":"Jain","year":"2021","journal-title":"Wkly. Epidemiol. Rec."},{"key":"ref_23","first-page":"575","article-title":"Global leishmaniasis surveillance: 2021, assessing the impact of the COVID-19 pandemic","volume":"97","author":"Jain","year":"2022","journal-title":"Wkly. Epidemiol. Rec"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Alvar, J., V\u00e9lez, I.D., Bern, C., Herrero, M., Desjeux, P., Cano, J., Jannin, J., and den Boer, M. (2012). Who Leishmaniasis Control the WHO Leishmaniasis Control Team Leishmaniasis Worldwide and Global Estimates of Its Incidence. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0035671"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"581","DOI":"10.1038\/nri.2016.72","article-title":"Cutaneous leishmaniasis: Immune responses in protection and pathogenesis","volume":"16","author":"Scott","year":"2016","journal-title":"Nat. Rev. Immunol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"138","DOI":"10.1038\/sj.icb7100011","article-title":"Balancing immunity and pathology in visceral leishmaniasis","volume":"85","author":"Stanley","year":"2006","journal-title":"Immunol. Cell Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"155339","DOI":"10.1016\/j.cyto.2020.155339","article-title":"Chemokines in Leishmaniasis: Map of cell movements highlights the landscape of infection and pathogenesis","volume":"147","author":"Pereira","year":"2021","journal-title":"Cytokine"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"S23","DOI":"10.1017\/S003118200001698X","article-title":"Concomitant infections, parasites and immune responses","volume":"122","author":"Cox","year":"2001","journal-title":"Parasitology"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1016\/S0020-7519(97)00189-6","article-title":"Multiparasite communities in animals and humans: Frequency, structure and pathogenic significance","volume":"28","author":"Petney","year":"1998","journal-title":"Int. J. Parasitol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1016\/j.pt.2009.03.001","article-title":"Parasite adaptations to within-host competition","volume":"25","author":"Mideo","year":"2009","journal-title":"Trends Parasitol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"142","DOI":"10.1086\/509808","article-title":"Influence of Helminth Infections on the Clinical Course of and Immune Response to Leishmania braziliensis Cutaneous Leishmaniasis","volume":"195","author":"Machado","year":"2007","journal-title":"J. Infect. Dis."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"630934","DOI":"10.3389\/fimmu.2021.630934","article-title":"Previous History of American Tegumentary Leishmaniasis Alters Susceptibility and Immune Response Against Schistosoma mansoni Infection in Humans","volume":"12","author":"Miranda","year":"2021","journal-title":"Front. Immunol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1781","DOI":"10.1111\/jdv.15521","article-title":"Cutaneous schistosomiasis and leishmaniasis coinfection: A case report","volume":"33","author":"Gregorio","year":"2019","journal-title":"J. Eur. Acad. Dermatol. Venereol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"42","DOI":"10.1016\/j.actatropica.2015.10.015","article-title":"Intestinal helminth coinfection is associated with mucosal lesions and poor response to therapy in American tegumentary leishmaniasis","volume":"154","author":"Pimentel","year":"2016","journal-title":"Acta Trop."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1","DOI":"10.15761\/CCRR.1000422","article-title":"Massive Splenomegaly: A Case Report of Visceral Leishmania and Schistosomiasis Co-infection and a Review of Infectious Causes of Massive Splenomegaly","volume":"4","author":"Paran","year":"2018","journal-title":"Clin. Case Rep. Rev."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3158","DOI":"10.3389\/fimmu.2018.03158","article-title":"Modulation of Allergic Reactivity in Humans Is Dependent on Schistosoma mansoni Parasite Burden, Low Levels of IL-33 or TNF-\u03b1 and High Levels of IL-10 in Serum","volume":"9","author":"Resende","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1186\/1475-2875-3-43","article-title":"Increase of malaria attacks among children presenting concomitant infection by Schistosoma mansoni in Senegal","volume":"3","author":"Sokhna","year":"2004","journal-title":"Malar. J."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Capron, M., B\u00e9ghin, L., Leclercq, C., Labreuche, J., Dendooven, A., Standaert, A., Delbeke, M., Porcherie, A., Nachury, M., and Boruchowicz, A. (2019). Safety of P28GST, a Protein Derived from a Schistosome Helminth Parasite, in Patients with Crohn\u2019s Disease: A Pilot Study (ACROHNEM). J. Clin. Med., 9.","DOI":"10.3390\/jcm9010041"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"551","DOI":"10.4269\/ajtmh.2011.10-0423","article-title":"Antihelminthic Therapy and Antimony in Cutaneous Leishmaniasis: A Randomized, Double-Blind, Placebo-Controlled Trial in Patients Co-Infected with Helminths and Leishmania braziliensis","volume":"84","author":"Newlove","year":"2011","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"700","DOI":"10.1016\/j.micinf.2010.04.012","article-title":"Innate immunogenicity and in vitro protective potential of Schistosoma mansoni lung schistosomula excretory\u2013secretory candidate vaccine antigens","volume":"12","author":"Tallima","year":"2010","journal-title":"Microbes Infect."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"90","DOI":"10.1128\/iai.60.1.90-94.1992","article-title":"Comparison of irradiated-cercaria schistosome vaccine models that use 15- and 50-kilorad doses: The 15-kilorad dose gives greater protection, smaller liver sizes, and higher gamma interferon levels after challenge","volume":"60","author":"Reynolds","year":"1992","journal-title":"Infect. Immun."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"2764","DOI":"10.1002\/eji.200324143","article-title":"Pivotal roles of the parasite PGD2 synthase and of the host D prostanoid receptor 1 in schistosome immune evasion","volume":"33","author":"Angeli","year":"2003","journal-title":"Eur. J. Immunol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"824","DOI":"10.1096\/fj.15-277822","article-title":"The helminth T2 RNase \u03c91 promotes metabolic homeostasis in an IL-33- and group 2 innate lymphoid cell-dependent mechanism","volume":"30","author":"Hams","year":"2016","journal-title":"FASEB J."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1673","DOI":"10.1084\/jem.20082460","article-title":"Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses","volume":"206","author":"Everts","year":"2009","journal-title":"J. Exp. Med."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7554\/eLife.41337","article-title":"Programmed genome editing of the omega-1 ribonuclease of the blood fluke, Schistosoma mansoni","volume":"8","author":"Ittiprasert","year":"2019","journal-title":"eLife"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"442","DOI":"10.4049\/jimmunol.167.1.442","article-title":"Lacto-N-fucopentaose III Found on Schitosoma mansoni Egg Antigens Functions as Adjuvant for Proteins by Inducing Th2-Type Response","volume":"167","author":"Okano","year":"2001","journal-title":"J. Immunol."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"6712","DOI":"10.4049\/jimmunol.163.12.6712","article-title":"Induction of Th2 responses and IgE is largely due to carbohydrates functioning as adjuvants on Schistosoma mansoni egg antigens","volume":"163","author":"Okano","year":"1999","journal-title":"J. Immunol."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Turner, J.D., Jenkins, G.R., Hogg, K.G., Aynsley, S.A., Paveley, R.A., Cook, P.C., Coles, M.C., and Mountford, A.P. (2011). CD4+CD25+ Regulatory Cells Contribute to the Regulation of Colonic Th2 Granulomatous Pathology Caused by Schistosome Infection. PLoS Negl. Trop. Dis., 5.","DOI":"10.1371\/journal.pntd.0001269"},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Haeberlein, S., Obieglo, K., Ozir-Fazalalikhan, A., Chay\u00e9, M.A.M., Veninga, H., Van Der Vlugt, L.E.P.M., Voskamp, A., Boon, L., Haan, J.M.M.D., and Westerhof, L.B. (2017). Schistosome egg antigens, including the glycoprotein IPSE\/alpha-1, trigger the development of regulatory B cells. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006539"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"2174","DOI":"10.1002\/eji.200737063","article-title":"Immunopathology in schistosomiasis is controlled by antigen-specific regulatory T cells primed in the presence of TLR2","volume":"37","author":"Layland","year":"2007","journal-title":"Eur. J. Immunol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"5839","DOI":"10.4049\/jimmunol.176.10.5839","article-title":"Regulatory T Cell Responses Develop in Parallel to Th Responses and Control the Magnitude and Phenotype of the Th Effector Populatio","volume":"176","author":"Taylor","year":"2006","journal-title":"J. Immunol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"6734","DOI":"10.1128\/IAI.70.12.6734-6740.2002","article-title":"Up-Regulation of Th1-Type Responses in Mucosal Leishmaniasis Patients","volume":"70","author":"Bacellar","year":"2002","journal-title":"Infect. Immun."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"7853","DOI":"10.1128\/IAI.73.12.7853-7859.2005","article-title":"Decreased In Situ Expression of Interleukin-10 Receptor Is Correlated with the Exacerbated Inflammatory and Cytotoxic Responses Observed in Mucosal Leishmaniasis","volume":"73","author":"Faria","year":"2005","journal-title":"Infect. Immun."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1111\/j.1365-3083.2005.01707.x","article-title":"Mucosal Leishmaniasis Patients Display an Activated Inflammatory T-cell Phenotype Associated with a Nonbalanced Monocyte Population","volume":"63","author":"Gaze","year":"2005","journal-title":"Scand. J. Immunol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Ca\u00f1eda-Guzm\u00e1n, I.C., Salaiza-Suazo, N., Fern\u00e1ndez-Figueroa, E.A., Carrada-Figueroa, G., Aguirre-Garc\u00eda, M., and Becker, I. (2014). NK Cell Activity Differs between Patients with Localized and Diffuse Cutaneous Leishmaniasis Infected with Leishmania mexicana: A Comparative Study of TLRs and Cytokines. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0112410"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1111\/j.1365-2230.2005.01991.x","article-title":"Inducible nitric oxide synthase and cytokine pattern in lesions of patients with American cutaneous leishmaniasis","volume":"31","author":"Diaz","year":"2006","journal-title":"Clin. Exp. Dermatol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"446","DOI":"10.1590\/S0074-0276108042013008","article-title":"Chemokines and chemokine receptors expression in the lesions of patients with American cutaneous leishmaniasis","volume":"108","author":"Diaz","year":"2013","journal-title":"Mem. Inst. Oswaldo Cruz."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1220","DOI":"10.1016\/j.humimm.2010.09.002","article-title":"Chemokines and chemokine receptors coordinate the inflammatory immune response in human cutaneous leishmaniasis","volume":"71","author":"Campanelli","year":"2010","journal-title":"Hum. Immunol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"856","DOI":"10.1590\/S0074-02762011000700012","article-title":"Schistosoma mansoni antigens alter the cytokine response in vitro during cutaneous leishmaniasis","volume":"106","author":"Bafica","year":"2011","journal-title":"Mem. Inst. Oswaldo Cruz."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"520308","DOI":"10.1155\/2012\/520308","article-title":"Changes in T-Cell and Monocyte Phenotypes In Vitro by Schistosoma mansoni Antigens in Cutaneous Leishmaniasis Patients","volume":"2012","author":"Bafica","year":"2012","journal-title":"J. Parasitol. Res."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"743069","DOI":"10.1155\/2014\/743069","article-title":"Dendritic Cell Profile Induced by Schistosoma mansoni Antigen in Cutaneous Leishmaniasis Patients","volume":"2014","author":"Lopes","year":"2014","journal-title":"BioMed Res. Int."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"173","DOI":"10.1016\/j.molimm.2017.11.018","article-title":"Susceptibility of dendritic cells from individuals with schistosomiasis to infection by Leishmania braziliensis","volume":"93","author":"Lopes","year":"2018","journal-title":"Mol. Immunol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fimmu.2018.03122","article-title":"Schistosoma mansoni rSm29 Antigen Induces a Regulatory Phenotype on Dendritic Cells and Lymphocytes From Patients with Cutaneous Leishmaniasis","volume":"9","author":"Lopes","year":"2019","journal-title":"Front. Immunol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"240512","DOI":"10.1155\/2012\/240512","article-title":"Dyarrheal Syndrome in a Patient Co-Infected with Leishmania infantum and Schistosoma mansoni","volume":"2012","author":"Cota","year":"2012","journal-title":"Case Rep. Med."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1016\/S0151-9638(06)70841-9","article-title":"Leishmania infantum\/HIV co-infection: Cutaneous lesions following treatment of visceral leishmaniasis","volume":"133","author":"Catorze","year":"2006","journal-title":"Ann. Dermatol. Venereol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"668","DOI":"10.1016\/S0035-9203(01)90110-5","article-title":"Davidson Ethiopian visceral leishmaniasis: Generic and proprietary sodium stibogluconate are equivalent; HIV co-infected patients have a poor outcome","volume":"95","author":"Ritmeijer","year":"2001","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"2686","DOI":"10.4049\/jimmunol.145.8.2686","article-title":"Activation of human monocyte-derived macrophages to kill schistosomula of Schistosoma mansoni in vitro","volume":"145","author":"James","year":"1990","journal-title":"J. Immunol."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"585","DOI":"10.1128\/CMR.05040-11","article-title":"Helminth Infections and Host Immune Regulation","volume":"25","author":"McSorley","year":"2012","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"890","DOI":"10.1016\/S0140-6736(94)90009-4","article-title":"Long-term effect of prenatal exposure to maternal microfilaraemia on immune responsiveness to filarial parasite antigens","volume":"343","author":"Steel","year":"1994","journal-title":"Lancet"},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"2960","DOI":"10.3389\/fimmu.2018.02960","article-title":"Maternal Schistosomiasis: Immunomodulatory Effects with Lasting Impact on Allergy and Vaccine Responses","volume":"9","author":"LaCorcia","year":"2018","journal-title":"Front. Immunol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1271","DOI":"10.1016\/j.jaci.2014.05.034","article-title":"Maternal immune response to helminth infection during pregnancy determines offspring susceptibility to allergic airway inflammation","volume":"134","author":"Straubinger","year":"2014","journal-title":"J. Allergy Clin. Immunol."},{"key":"ref_72","doi-asserted-by":"crossref","unstructured":"Cortes-Selva, D., Gibbs, L., Maschek, J.A., Nascimento, M., Van Ry, T., Cox, J.E., Amiel, E., and Fairfax, K.C. (2021). Metabolic reprogramming of the myeloid lineage by Schistosoma mansoni infection persists independently of antigen exposure. PLoS Pathog., 17.","DOI":"10.1371\/journal.ppat.1009198"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"338","DOI":"10.1007\/s004360050407","article-title":"Schistosoma haematobium, S. intercalatum, S. japonicum, S. mansoni, and S. rodhaini in mice: Relationship between patterns of lung migration by schistosomula and perfusion recovery of adult worms","volume":"84","author":"Rheinberg","year":"1998","journal-title":"Parasitol. Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1017\/S0031182000052689","article-title":"A comparative study of the life-histories of mammalian schistosomes","volume":"87","author":"Loker","year":"1983","journal-title":"Parasitology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1016\/0035-9203(80)90038-3","article-title":"Susceptibility to Leishmania mexicana of mice infected with Schistosoma mansoni","volume":"74","author":"Coelho","year":"1980","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"339","DOI":"10.1046\/j.1365-3024.2002.00473.x","article-title":"Schistosomiasis delays lesion resolution during Leishmania major infection by impairing parasite killing by macrophages","volume":"24","author":"Scott","year":"2002","journal-title":"Parasite Immunol."},{"key":"ref_77","first-page":"80","article-title":"Studies on the interaction of Schistosoma mansoni and Leishmania major in experimentally infected Balb\/c mice","volume":"14","author":"Yole","year":"2007","journal-title":"Afr. J. Health Sci."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1016\/S1383-5769(99)00006-9","article-title":"Immune responses against protozoal and nematodal infection in mice with underlying Schistosoma mansoni infection","volume":"48","author":"Yoshida","year":"1999","journal-title":"Parasitol. Int."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"244","DOI":"10.1186\/1756-3305-6-244","article-title":"Combination therapy using Pentostam and Praziquantel improves lesion healing and parasite resolution in BALB\/c mice co-infected with Leishmania major and Schistosoma mansoni","volume":"6","author":"Kutima","year":"2013","journal-title":"Parasites Vectors"},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"712","DOI":"10.1016\/j.trstmh.2009.04.019","article-title":"Atypical manifestations of tegumentary leishmaniasis in a transmission area of Leishmania braziliensis in the state of Bahia, Brazil","volume":"103","author":"Machado","year":"2009","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"824","DOI":"10.4269\/ajtmh.1998.58.824","article-title":"Cutaneous scars in American tegumentary leishmaniasis patients: A site of Leishmania (Viannia) braziliensis persistence and viability eleven years after antimonial therapy and clinical cure","volume":"58","author":"Schubach","year":"1998","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"943","DOI":"10.2353\/ajpath.2006.051319","article-title":"The Schistosoma mansoni Hepatic Egg Granuloma Provides a Favorable Microenvironment for Sustained Growth of Leishmania donovani","volume":"169","author":"Hassan","year":"2006","journal-title":"Am. J. Pathol."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"93","DOI":"10.2307\/3283351","article-title":"An Experimental Model of the Production of Metastases in Murine Cutaneous Leishmaniasis","volume":"80","author":"Bertho","year":"1994","journal-title":"J. Parasitol."},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"771","DOI":"10.1017\/S0031182012002156","article-title":"Golden hamster (Mesocricetus auratus) as an experimental model for Leishmania (Viannia) braziliensis infection","volume":"140","author":"Valverde","year":"2013","journal-title":"Parasitology"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1007\/s11259-007-0040-5","article-title":"Setting New Immunobiological Parameters in the Hamster Model of Visceral Leishmaniasis for In Vivo Testing of Antileishmanial Compounds","volume":"31","author":"Alunda","year":"2007","journal-title":"Veter.-Res. Commun."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1590\/S0100-879X2004000400020","article-title":"Immunity and immunosuppression in experimental visceral leishmaniasis","volume":"37","author":"Goto","year":"2004","journal-title":"Braz. J. Med. Biol. Res."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1590\/S0074-02761988000200001","article-title":"Experimental canine mucocutaneous leishmaniasis (Leishmania braziliensis braziliensis)","volume":"83","author":"Pirmez","year":"1988","journal-title":"Mem. Inst. Oswaldo Cruz."},{"key":"ref_88","first-page":"83","article-title":"Domestic and wild animals naturally infected with Schistosoma mansoni in the Gezira Irrigated Scheme, Sudan","volume":"88","author":"Karoum","year":"1985","journal-title":"J. Trop. Med. Hyg."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"831","DOI":"10.4269\/ajtmh.1956.5.831","article-title":"The Relative Egg Producing Capacity of Schistosoma mansoni and Schistosoma japonicum","volume":"5","author":"Moore","year":"1956","journal-title":"Am. J. Trop. Med. Hyg."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"170","DOI":"10.1590\/S0037-86822007000200005","article-title":"Morbidity due to Schistosoma mansoni\u2013Entamoeba histolytica coinfection in hamsters (Mesocricetus auratus)","volume":"40","author":"Dolabella","year":"2007","journal-title":"Rev. Soc. Bras. Med. Trop."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"392","DOI":"10.2307\/3273883","article-title":"Comparative Susceptibility of Common Laboratory Animals to Experimental Infection with Schistosoma haematobium","volume":"40","author":"Moore","year":"1954","journal-title":"J. Parasitol."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"711","DOI":"10.4257\/oeco.2010.1403.07","article-title":"A review on the role of the water-rat Nectomys squamipes on the transmission dynamics of mansonic schistosomiasis: A long term multidisciplinary study in an endemic area","volume":"14","author":"Gentile","year":"2010","journal-title":"Oecol. Aust."},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1590\/1089-6891v16i331640","article-title":"Monitoring positivity for Schistosoma mansoni in rodents Holochilus sp. naturally infected","volume":"16","author":"Miranda","year":"2015","journal-title":"Cien. Anim. Bras."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1590\/S0036-46651984000600004","article-title":"Holochilus brasiliensis nanus Thomas, 1897: As an experimental model for filariasis, leishmaniasis and schistosomiasis","volume":"26","author":"Bastos","year":"1984","journal-title":"Rev. Inst. Med. Trop. Sao Paulo"},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Andrade, M.S., Courtenay, O., Brito, M.E.F., Carvalho, F.G., Carvalho, A.W.S., Soares, F., Carvalho, S.M., Costa, P.L., Zampieri, R., and Floeter-Winter, L.M. (2015). Infectiousness of Sylvatic and Synanthropic Small Rodents Implicates a Multi-host Reservoir of Leishmania (Viannia) braziliensis. PLoS Negl. Trop. Dis., 9.","DOI":"10.1371\/journal.pntd.0004137"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"592","DOI":"10.1093\/trstmh\/trt062","article-title":"Small mammals as hosts of Leishmania spp. in a highly endemic area for zoonotic leishmaniasis in north-eastern Brazil","volume":"107","author":"Lima","year":"2013","journal-title":"Trans. R. Soc. Trop. Med. Hyg."},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1017\/S0031182003004037","article-title":"Leishmania (Viannia) braziliensis-induced chronic granulomatous cutaneous lesions affecting the nasal mucosa in the rhesus monkey (Macaca mulatta) model","volume":"127","author":"Teva","year":"2003","journal-title":"Parasitology"},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1006\/expr.1996.0005","article-title":"Leishmania amazonensis: The Asian Rhesus Macaques (Macaca mulatta) as an Experimental Model for Study of Cutaneous Leishmaniasis","volume":"82","author":"Amaral","year":"1996","journal-title":"Exp. Parasitol."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"376","DOI":"10.1016\/j.exppara.2007.05.006","article-title":"The development of hepatic granulomas in 20 Krad irradiated Schistosoma mansoni cercaria vaccinated grivet monkeys (Cercopithecus aethiops aethiops)","volume":"117","author":"Torben","year":"2007","journal-title":"Exp. Parasitol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1080\/00034983.1982.11687512","article-title":"Natural infections of Schistosoma mansoni and S. haematobiumin Cercopithecus monkeys in Kenya","volume":"76","author":"Else","year":"1982","journal-title":"Ann. Trop. Med. Parasitol."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1002\/path.1700230308","article-title":"A comparative study of experimental bilharziasis in monkeys contrasted with the hitherto described lesions in man","volume":"23","author":"Fairley","year":"1920","journal-title":"J. Pathol. Bacteriol."}],"container-title":["Tropical Medicine and Infectious Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2414-6366\/8\/8\/383\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:20:40Z","timestamp":1760127640000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2414-6366\/8\/8\/383"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,27]]},"references-count":101,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,8]]}},"alternative-id":["tropicalmed8080383"],"URL":"https:\/\/doi.org\/10.3390\/tropicalmed8080383","relation":{},"ISSN":["2414-6366"],"issn-type":[{"value":"2414-6366","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,27]]}}}