ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Feasey N, Wansbrough-Jones M, Mabey DCW, Solomon A, 2010. Neglected tropical diseases. Brit Med Bull93: 179–200.
-
2.
Bern C, Desjeux P, Cano J, Alvar J, 2012. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7: e35671.
-
3.
Torres-Guerrero E, Quintanilla-Cedillo MR, Ruiz-Esmenjaud J, Arenas R, 2017. Leishmaniasis: a review. F1000 Res 6: 1–15.
-
4.
Marsden PD, 1986. Mucosal leishmaniasis (“espundia” Escomel, 1911). Trans R Soc Trop Med Hyg 80: 859–876.
-
5.
Reithinger R et al., 2007. Cutaneous leishmaniasis. Lancet Infect Dis 2017: 7.
-
6.
Bezerra JMT, de Araújo VEM, Barbosa DS, Martins-Melo FR, Werneck GL, Carneiro M, 2018. Burden of leishmaniasis in Brazil and federated units, 1990–2016: Findings from Global Burden of Disease Study 2016. PLoS Negl Trop Dis 12: 1–19.
-
7.
Villasboas L et al., 2010. Miltefosine in the treatment of cutaneous leishmaniasis caused by Leishmania braziliensis in Brazil: a randomized and controlled trial. PLoS Negl Trop Dis 4:e912.
-
8.
Guimaraes LH et al., 2016. Atypical manifestations of cutaneous leishmaniasis in a region endemic for Leishmania braziliensis: clinical, immunological and parasitological aspects. PLoS Negl Trop Dis 10: 1–14.
-
9.
Novais FO et al., 2014. Human classical monocytes control the intracellular stage of Leishmania braziliensis by reactive oxygen species. J Infect Dis 209: 1288–1296.
-
10.
Scott P, Novais FO, 2016. Cutaneous leishmaniasis: immune responses in protection and pathogenesis. Nat Rev Immunol 16: 581–592.
-
11.
Bacellar O et al., 2002. Up-regulation of Th1-type responses in mucosal leishmaniasis patients. Infect Immun 70: 6734–6740.
-
12.
Hotez PJ, Bottazzi ME, Franco-paredes C, Ault SK, Periago MR, 2008. The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS Negl Trop Dis 2: e300.
-
13.
Brooker S et al., 2007. Age-related changes in hookworm infection, anaemia and iron deficiency in an area of high Necator americanus hookworm transmission in south-eastern Brazil. Trans R Soc Trop Med Hyg 101: 146–154.
-
14.
Casapia M, Joseph SA, Nunez C, Rahme E, Gyorkos TW, 2006. Parasite risk factors for stunting in grade 5 students in a community of extreme poverty in Peru. Int J Parasitol 36: 741–747.
-
15.
Ezeamama AE et al., 2006. Helminth infection and cognitive impairment among Filipino children. Am J Trop Med Hyg 72: 540–548.
-
16.
Khuroo MS, 1996. Ascariasis. Gastroenterol Clin North Am 25: 553–577.
-
17.
Maizels RM, Yazdanbakhsh M, 2003. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3: 733–744.
-
18.
Díaz A, Allen JE, 2007. Mapping immune response profiles: the emerging scenario from helminth immunology. Eur J Immunol 3: 3319–3326.
-
19.
Smallwood TB, Giacomin PR, Loukas A, Mulvenna JP, Clark RJ, Miles JJ, 2017. Helminth immunomodulation in autoimmune disease. Front Imunol 8: 453.
-
20.
Medeiros M et al., 2003. Schistosoma mansoni infection is associated with a reduced course of asthma. J Allergy Clin Immunol 111: 947–951.
-
21.
Araujo MI et al., 2000. Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int Arch Allergy Immunol 123: 145–148.
-
22.
Newlove T et al.2011. Antihelminthic therapy and antimony in cutaneous leishmaniasis: a randomized, double-blind, placebo-controlled trial in patients co-infected with helminths and Leishmania braziliensis. 84: 551–555.
-
23.
O’Neal SE et al., 2007. Influence of helminth infections on the clinical course of and immune response to Leishmania braziliensis cutaneous leishmaniasis. J Infect Dis 195: 142–148.
-
24.
Intituto Brasileiro de Geografia e Estatística , 2011. Sinopse Do Censo Demográfico 2010. Rio de Janeiro, Brazil: Ministério do Planejamento, Orçamento e Gestão.
-
25.
Nitahara A, 2019. Estimativa da população do Brasil passa de 210 milhões, diz IBGE. Brasilia, Brazil: Agência Brasil.
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26.
Tabarelli M, Venceslau A, Cezar M, Paul J, Peres CA, 2010. Prospects for biodiversity conservation in the Atlantic Forest: lessons from aging human-modified landscapes. Biol Conserv 143: 2328–2340.
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27.
Gramiccia M, Gradoni L, 2005. The current status of zoonotic leishmaniases and approaches to disease control. Int J Parasitol 35: 1169–1180.
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28.
Weirather JL et al., 2011. Serial quantitative PCR assay for detection, species discrimination, and quantification of Leishmania spp. in human samples. J Clin Microbiol 49: 3892–3904.
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29.
WHO , 2013. Schistosomiasis: progress report 2001–2011, strategic plan 2012–2020. Geneva, Switzerland: World Health Organization.
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30.
WHO , 1991. Basic laboratory methods in medical parasitology. Geneva, Switzerland: World Health Organization.
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31.
Silva S et al., 2018. Molecular epidemiology and in vitro evidence suggest that Leishmania braziliensis strain helps determine antimony response among American tegumenary leishmaniasis patients. Acta Trop 178: 34–39.
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32.
Amorim CF et al., 2019. Variable gene expression and parasite load predict treatment outcome in cutaneous leishmaniasis. Sci Transl Med 11: 1–10.
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33.
Vita GF et al., 2016. Status of American tegumentary leishmaniasis in the state of Rio de Janeiro, Brazil, from 2004 to 2013. Rev Inst Med Trop São Paulo 55: 1–8.
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34.
Barreto ML et al., 2007. Effect of city-wide sanitation programme on reduction in rate of childhood diarrhoea in northeast Brazil: assessment by two cohort studies. Lancet 370: 1622–1628.
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35.
Langdon K, Phie J, Thapa CB, Biros E, Loukas A, 2018. Helminth-based therapies for rheumatoid arthritis: a systematic review and meta-analysis. Int Immunopharmacol 66: 366–372.
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36.
Senna TC et al., 2019. Clinical features and therapeutic response in adult and pediatric patients with American tegumentary leishmaniasis in Rio de Janeiro. Trans R Soc Trop Med Hyg 114: 1–6.
-
37.
Schriefer A et al., 2004. Multiclonal Leishmania braziliensis population structure and its clinical implication in a region of endemicity for American tegumentary leishmaniasis. Infect Immun 72: 508–514.
-
38.
Queiroz A et al., 2012. Association between an emerging disseminated form of leishmaniasis and Leishmania (Viannia) braziliensis strain polymorphisms. J Clin Microbiol 50: 4028–4034.
-
39.
Costa DL et al., 2013. Characterization of regulatory T cell (Treg) function in patients infected with Leishmania braziliensis. Hum Immunol 74: 1491–1500.
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40.
Machado GU, Prates FV, Machado PRL, 2019. Disseminated leishmaniasis: clinical, pathogenic, and therapeutic aspects. An Bras Dermatol 94: 9–16.
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41.
Jirmanus L et al., 2012. Epidemiological and clinical changes in American tegumentary leishmaniasis in an area of Leishmania (viannia) braziliensis transmission over a 20-year period. Am J Trop Med Hyg 86: 426–433.
-
42.
Lopes DM, Oliveira SC, Page B, Carvalho LP, Carvalho EM, Cardoso LS, 2019. Schistosoma mansoni rSm29 antigen induces a regulatory phenotype on dendritic cells and lymphocytes from patients with cutaneous leishmaniasis. Front Immunol 9: 1–13.
-
43.
Tarafder MR, Carabin H, Joseph L, Balolong E, Olveda R, McGarvey ST, 2010. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a “gold standard.” Int J Parasitol 40: 399–404.
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44.
Chidambaram M et al., 2017. Evaluation of the utility of conventional polymerase chain reaction for detection and species differentiation in human hookworm infections. Trop Parasitol 7: 111–116.
-
45.
Camacho E, Rastrojo A, Sanchiz Á, González-De La Fuente S, Aguado B, Requena JM, 2019. Leishmania mitochondrial genomes: maxicircle structure and heterogeneity of minicircles. Genes (Basel) 10: 758.
-
46.
Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J, 2008. Helminth infections: the great neglected tropical diseases. J Clin Invest 118: 1311–1321.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1233 | 480 | 16 |
| Full Text Views | 189 | 22 | 0 |
| PDF Downloads | 103 | 17 | 0 |
Influence of Intestinal Helminth Burden on Clinical Manifestations, Therapeutic Response, and Leishmania braziliensis Load in Patients with New World Cutaneous Leishmaniasis
Brady Page
Brady Page
Department of Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusettes;
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Alex Lago
Alex Lago
Serviço de Imunologia, Complexo Hospitalar Universitário Prof. Edgard Santos, Universidade Federal da Bahia (UFBA), Salvador, Brazil;
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Juliana Almeida Silva
Juliana Almeida Silva
Serviço de Imunologia, Complexo Hospitalar Universitário Prof. Edgard Santos, Universidade Federal da Bahia (UFBA), Salvador, Brazil;
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Albert Schriefer
Albert Schriefer
Serviço de Imunologia, Complexo Hospitalar Universitário Prof. Edgard Santos, Universidade Federal da Bahia (UFBA), Salvador, Brazil;
Instituto Nacional de Ciência e Tecnologia em Doenças Tropicais, CNPq, Ministério de Ciência, Tecnologia e Inovação, Bahia, Brazil;
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Instituto Nacional de Ciência e Tecnologia em Doenças Tropicais, CNPq, Ministério de Ciência, Tecnologia e Inovação, Bahia, Brazil;
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Jamile Lago
Jamile Lago
Serviço de Imunologia, Complexo Hospitalar Universitário Prof. Edgard Santos, Universidade Federal da Bahia (UFBA), Salvador, Brazil;
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Lívia Oliveira
Lívia Oliveira
Serviço de Imunologia, Complexo Hospitalar Universitário Prof. Edgard Santos, Universidade Federal da Bahia (UFBA), Salvador, Brazil;
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Luiz Henrique Guimarães
Luiz Henrique Guimarães
Universidade Federal do Sul da Bahia, Ilhéus, Brazil;
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Marshall Glesby
Marshall Glesby
Division of Infectious Diseases, Department of Medicine, Weill Cornell Medical College, New York, New York;
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Edgar M. Carvalho
Edgar M. Carvalho
Serviço de Imunologia, Complexo Hospitalar Universitário Prof. Edgard Santos, Universidade Federal da Bahia (UFBA), Salvador, Brazil;
Instituto Nacional de Ciência e Tecnologia em Doenças Tropicais, CNPq, Ministério de Ciência, Tecnologia e Inovação, Bahia, Brazil;
Instituto Gonçalo Moniz, Fudação Oswaldo Crux (Fiocruz), Salvador, Brazil
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Instituto Nacional de Ciência e Tecnologia em Doenças Tropicais, CNPq, Ministério de Ciência, Tecnologia e Inovação, Bahia, Brazil;
Instituto Gonçalo Moniz, Fudação Oswaldo Crux (Fiocruz), Salvador, Brazil
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ABSTRACT.
Leishmania braziliensis is the most important cause of cutaneous leishmaniasis (CL) in the Americas. A Th1-type immune response is required to control Leishmania infection, but an exaggerated inflammatory response leads to the development of ulcers seen in CL. Infection with intestinal helminths has the potential to inhibit the Th1 response in a manner that depends both on the species of helminth present as well as the burden of helminthiasis. We conducted a prospective cohort study of CL patients from an endemic area between January and December 2017 with either negative or high intestinal helminth burden to characterize relationships between helminth burden, L. braziliensis quantification within CL lesions, clinical aspects of CL, and therapeutic response. Of 234 participants with leishmaniasis who underwent stool examination at the time of diagnosis, 45% had detectable helminth infection. The overall cure rate after 90 days was 66%, with a median time to resolution of disease of 40 days (interquartile range: 30–65 days). There was no significant association between the type of helminth infection or the magnitude of intestinal helminth burden at the time of diagnosis and L. braziliensis genomic DNA (gDNA) detected in biopsies from CL lesions. Likewise, there was no association between helminth burden and response to treatment after 90 days. Considering quantification of parasite DNA in CL lesions, participants who were cured at 90 days had a median of 0.017 ng/mg gDNA, and participants who failed therapy had a median of 0.091 ng/mg gDNA (P = 0.03). The results indicate that cutaneous Leishmania load may influence therapeutic response in CL.
Author Notes
Financial support: This work was supported through the Fulbright-Fogarty Fellowship in Public Health by grants from the Fulbright Program, U.S. Department of State. and the Fogarty International Center, U.S. National Institutes of Health.
Authors’ addresses: Brady Page, Department of Medicine, Massachusetts General Hospital, Boston, MA, E-mail: bradylpage@gmail.com. Alex Lago, Juliana Almeida Silva, Albert Schriefer, Jamile Lago, and Edgar M. Carvalho, Serviço de Imunologia, Complexo Hospitalar Universitário Prof. Edgard Santos, Universidade Federal da Bahia (UFBA), Salvador, Bahia, Brazil, E-mails: alex-lago@hotmail.com, july-meida@yahoo.com.br, nab.schriefer@gmail.com, Jamile.lago@hotmail.com, livia.alves.oliveira@hotmail.com, and imuno@ufba.br. Luiz Henrique Guimarães, Universidade Federal do Sul da Bahia, Itabuna, Bahia, Brazil, E-mail: luizhenriquesg@yahoo.com.br. Marshall Glesby, Division of Infectious Diseases, Department of Medicine, Weill Cornell Medical College, New York, NY, E-mail: mag2005@med.cornell.edu.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Feasey N, Wansbrough-Jones M, Mabey DCW, Solomon A, 2010. Neglected tropical diseases. Brit Med Bull93: 179–200.
-
2.
Bern C, Desjeux P, Cano J, Alvar J, 2012. Leishmaniasis worldwide and global estimates of its incidence. PLoS One 7: e35671.
-
3.
Torres-Guerrero E, Quintanilla-Cedillo MR, Ruiz-Esmenjaud J, Arenas R, 2017. Leishmaniasis: a review. F1000 Res 6: 1–15.
-
4.
Marsden PD, 1986. Mucosal leishmaniasis (“espundia” Escomel, 1911). Trans R Soc Trop Med Hyg 80: 859–876.
-
5.
Reithinger R et al., 2007. Cutaneous leishmaniasis. Lancet Infect Dis 2017: 7.
-
6.
Bezerra JMT, de Araújo VEM, Barbosa DS, Martins-Melo FR, Werneck GL, Carneiro M, 2018. Burden of leishmaniasis in Brazil and federated units, 1990–2016: Findings from Global Burden of Disease Study 2016. PLoS Negl Trop Dis 12: 1–19.
-
7.
Villasboas L et al., 2010. Miltefosine in the treatment of cutaneous leishmaniasis caused by Leishmania braziliensis in Brazil: a randomized and controlled trial. PLoS Negl Trop Dis 4:e912.
-
8.
Guimaraes LH et al., 2016. Atypical manifestations of cutaneous leishmaniasis in a region endemic for Leishmania braziliensis: clinical, immunological and parasitological aspects. PLoS Negl Trop Dis 10: 1–14.
-
9.
Novais FO et al., 2014. Human classical monocytes control the intracellular stage of Leishmania braziliensis by reactive oxygen species. J Infect Dis 209: 1288–1296.
-
10.
Scott P, Novais FO, 2016. Cutaneous leishmaniasis: immune responses in protection and pathogenesis. Nat Rev Immunol 16: 581–592.
-
11.
Bacellar O et al., 2002. Up-regulation of Th1-type responses in mucosal leishmaniasis patients. Infect Immun 70: 6734–6740.
-
12.
Hotez PJ, Bottazzi ME, Franco-paredes C, Ault SK, Periago MR, 2008. The neglected tropical diseases of Latin America and the Caribbean: a review of disease burden and distribution and a roadmap for control and elimination. PLoS Negl Trop Dis 2: e300.
-
13.
Brooker S et al., 2007. Age-related changes in hookworm infection, anaemia and iron deficiency in an area of high Necator americanus hookworm transmission in south-eastern Brazil. Trans R Soc Trop Med Hyg 101: 146–154.
-
14.
Casapia M, Joseph SA, Nunez C, Rahme E, Gyorkos TW, 2006. Parasite risk factors for stunting in grade 5 students in a community of extreme poverty in Peru. Int J Parasitol 36: 741–747.
-
15.
Ezeamama AE et al., 2006. Helminth infection and cognitive impairment among Filipino children. Am J Trop Med Hyg 72: 540–548.
-
16.
Khuroo MS, 1996. Ascariasis. Gastroenterol Clin North Am 25: 553–577.
-
17.
Maizels RM, Yazdanbakhsh M, 2003. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol 3: 733–744.
-
18.
Díaz A, Allen JE, 2007. Mapping immune response profiles: the emerging scenario from helminth immunology. Eur J Immunol 3: 3319–3326.
-
19.
Smallwood TB, Giacomin PR, Loukas A, Mulvenna JP, Clark RJ, Miles JJ, 2017. Helminth immunomodulation in autoimmune disease. Front Imunol 8: 453.
-
20.
Medeiros M et al., 2003. Schistosoma mansoni infection is associated with a reduced course of asthma. J Allergy Clin Immunol 111: 947–951.
-
21.
Araujo MI et al., 2000. Inverse association between skin response to aeroallergens and Schistosoma mansoni infection. Int Arch Allergy Immunol 123: 145–148.
-
22.
Newlove T et al.2011. Antihelminthic therapy and antimony in cutaneous leishmaniasis: a randomized, double-blind, placebo-controlled trial in patients co-infected with helminths and Leishmania braziliensis. 84: 551–555.
-
23.
O’Neal SE et al., 2007. Influence of helminth infections on the clinical course of and immune response to Leishmania braziliensis cutaneous leishmaniasis. J Infect Dis 195: 142–148.
-
24.
Intituto Brasileiro de Geografia e Estatística , 2011. Sinopse Do Censo Demográfico 2010. Rio de Janeiro, Brazil: Ministério do Planejamento, Orçamento e Gestão.
-
25.
Nitahara A, 2019. Estimativa da população do Brasil passa de 210 milhões, diz IBGE. Brasilia, Brazil: Agência Brasil.
-
26.
Tabarelli M, Venceslau A, Cezar M, Paul J, Peres CA, 2010. Prospects for biodiversity conservation in the Atlantic Forest: lessons from aging human-modified landscapes. Biol Conserv 143: 2328–2340.
-
27.
Gramiccia M, Gradoni L, 2005. The current status of zoonotic leishmaniases and approaches to disease control. Int J Parasitol 35: 1169–1180.
-
28.
Weirather JL et al., 2011. Serial quantitative PCR assay for detection, species discrimination, and quantification of Leishmania spp. in human samples. J Clin Microbiol 49: 3892–3904.
-
29.
WHO , 2013. Schistosomiasis: progress report 2001–2011, strategic plan 2012–2020. Geneva, Switzerland: World Health Organization.
-
30.
WHO , 1991. Basic laboratory methods in medical parasitology. Geneva, Switzerland: World Health Organization.
-
31.
Silva S et al., 2018. Molecular epidemiology and in vitro evidence suggest that Leishmania braziliensis strain helps determine antimony response among American tegumenary leishmaniasis patients. Acta Trop 178: 34–39.
-
32.
Amorim CF et al., 2019. Variable gene expression and parasite load predict treatment outcome in cutaneous leishmaniasis. Sci Transl Med 11: 1–10.
-
33.
Vita GF et al., 2016. Status of American tegumentary leishmaniasis in the state of Rio de Janeiro, Brazil, from 2004 to 2013. Rev Inst Med Trop São Paulo 55: 1–8.
-
34.
Barreto ML et al., 2007. Effect of city-wide sanitation programme on reduction in rate of childhood diarrhoea in northeast Brazil: assessment by two cohort studies. Lancet 370: 1622–1628.
-
35.
Langdon K, Phie J, Thapa CB, Biros E, Loukas A, 2018. Helminth-based therapies for rheumatoid arthritis: a systematic review and meta-analysis. Int Immunopharmacol 66: 366–372.
-
36.
Senna TC et al., 2019. Clinical features and therapeutic response in adult and pediatric patients with American tegumentary leishmaniasis in Rio de Janeiro. Trans R Soc Trop Med Hyg 114: 1–6.
-
37.
Schriefer A et al., 2004. Multiclonal Leishmania braziliensis population structure and its clinical implication in a region of endemicity for American tegumentary leishmaniasis. Infect Immun 72: 508–514.
-
38.
Queiroz A et al., 2012. Association between an emerging disseminated form of leishmaniasis and Leishmania (Viannia) braziliensis strain polymorphisms. J Clin Microbiol 50: 4028–4034.
-
39.
Costa DL et al., 2013. Characterization of regulatory T cell (Treg) function in patients infected with Leishmania braziliensis. Hum Immunol 74: 1491–1500.
-
40.
Machado GU, Prates FV, Machado PRL, 2019. Disseminated leishmaniasis: clinical, pathogenic, and therapeutic aspects. An Bras Dermatol 94: 9–16.
-
41.
Jirmanus L et al., 2012. Epidemiological and clinical changes in American tegumentary leishmaniasis in an area of Leishmania (viannia) braziliensis transmission over a 20-year period. Am J Trop Med Hyg 86: 426–433.
-
42.
Lopes DM, Oliveira SC, Page B, Carvalho LP, Carvalho EM, Cardoso LS, 2019. Schistosoma mansoni rSm29 antigen induces a regulatory phenotype on dendritic cells and lymphocytes from patients with cutaneous leishmaniasis. Front Immunol 9: 1–13.
-
43.
Tarafder MR, Carabin H, Joseph L, Balolong E, Olveda R, McGarvey ST, 2010. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a “gold standard.” Int J Parasitol 40: 399–404.
-
44.
Chidambaram M et al., 2017. Evaluation of the utility of conventional polymerase chain reaction for detection and species differentiation in human hookworm infections. Trop Parasitol 7: 111–116.
-
45.
Camacho E, Rastrojo A, Sanchiz Á, González-De La Fuente S, Aguado B, Requena JM, 2019. Leishmania mitochondrial genomes: maxicircle structure and heterogeneity of minicircles. Genes (Basel) 10: 758.
-
46.
Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J, 2008. Helminth infections: the great neglected tropical diseases. J Clin Invest 118: 1311–1321.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1233 | 480 | 16 |
| Full Text Views | 189 | 22 | 0 |
| PDF Downloads | 103 | 17 | 0 |