Integrated control of neglected tropical diseases in Brazil: document review of a national campaign in light of WHO recommendations

Control integrado de las enfermedades tropicales desatendidas en Brasil: revisión documental de una campaña nacional a la luz de las recomendaciones de la OMS

Controle integrado de doenças tropicais negligenciadas no Brasil: revisão documental de uma campanha nacional considerando as recomendações da OMS

Rosa Castália Ribeiro Soares Amanda Gabriela de Carvalho João Gabriel Guimarães Luz Ana Luiza Zílio Lucas Eliane Ignotti About the authors

ABSTRACT

Objective.

To describe the results of a national campaign aimed at the integrated control of neglected tropical diseases in Brazil in light of the World Health Organization (WHO) official documentation related to the integration of strategies for the prevention, control, and elimination or eradication of neglected tropical diseases.

Methods.

A document review that included official WHO documents published between 2007 and 2020 and campaign results extracted from the official technical report produced by the Brazilian Ministry of Health.

Results.

The integrated control of neglected tropical diseases was gradually incorporated in the WHO documentation over time. Preventive chemotherapy through mass drug administration, intensified case management, and integrated vector management were extensively recommended as strategies for integrated control. The Brazilian campaign was carried out in four iterations between 2013 and 2017. Children aged 5 to 14 years enrolled in municipal public schools nationwide were targeted. In summary, a total of 1 074 and 73 522 new cases of leprosy and trachoma, respectively, were detected. Nearly 18 million doses of preventive chemotherapy for soil-transmitted helminthiasis were administered. More than 700 cases of schistosomiasis were diagnosed and treated.

Conclusions.

The integrated strategies implemented in Brazil throughout the campaign generated results aligned with the WHO recommendations for the control of neglected tropical diseases, especially those regarding mass drug administration, active case detection, and intensified case management. Therefore, the continuity of the campaign with adequate evaluation tools must be encouraged as a constant public health policy in the Brazilian government agenda.

Keywords
Neglected diseases; communicable disease control; health policy; document analysis; Brazil

RESUMEN

Objetivo.

Describir los resultados de una campaña nacional dirigida al control integrado de las enfermedades tropicales desatendidas en Brasil, a la luz de la documentación oficial de la Organización Mundial de la Salud (OMS) relacionada con la integración de estrategias para la prevención, el control y la eliminación o erradicación de las enfermedades tropicales desatendidas.

Métodos.

Revisión documental que comprendió documentos oficiales de la OMS publicados entre el 2007 y el 2020, así como los resultados de las campañas, extraídos del informe técnico oficial elaborado por el Ministerio de Salud de Brasil.

Resultados.

Con el tiempo, la OMS ha ido incorporando gradualmente en sus documentos el concepto de control integrado de las enfermedades tropicales desatendidas. Tanto los tratamientos quimioprofilácticos mediante la administración masiva de medicamentos como la intensificación del tratamiento de los casos y el control integrado de vectores han sido recomendados ampliamente como estrategias para el control integrado. En Brasil, la campaña se llevó a cabo en cuatro ediciones, realizadas entre el 2013 y el 2017. Las actividades estuvieron dirigidas a la población escolar de entre 5 y 14 años de las escuelas públicas municipales de todo el país. En resumen, se detectaron 1 074 y 73 522 casos nuevos de lepra y tracoma, respectivamente; se administraron casi 18 millones de dosis de tratamiento quimioprofiláctico contra las geohelmintiasis; y se diagnosticaron y trataron más de 700 casos de esquistosomiasis.

Conclusiones.

Las estrategias integradas aplicadas en Brasil en el transcurso de la campaña permitieron obtener resultados acordes con las recomendaciones de la OMS para el control de las enfermedades tropicales desatendidas, especialmente en lo relativo a la administración masiva de medicamentos, la búsqueda activa de casos y la intensificación de su tratamiento. Por lo tanto, es necesario fomentar la continuidad de la campaña con herramientas de evaluación adecuadas, como una política constante en materia de salud pública dentro de la agenda del Gobierno de Brasil.

Palabras clave
Enfermedades desatendidas; control de enfermedades transmisibles; política de salud; análisis de documentos; Brasil

RESUMO

Objetivo.

Descrever os resultados de uma campanha nacional voltada ao controle integrado de doenças tropicais negligenciadas no Brasil considerando os documentos oficiais da Organização Mundial da Saúde (OMS) que tratam da integração de estratégias para a prevenção, o controle e a eliminação ou erradicação de doenças tropicais negligenciadas.

Métodos.

Realizou-se uma revisão documental que incluiu documentos oficiais da OMS publicados entre 2007 e 2020 e resultados de campanhas extraídos do relatório técnico oficial produzido pelo Ministério da Saúde do Brasil.

Resultados.

O controle integrado de doenças tropicais negligenciadas foi gradualmente incorporado à documentação da OMS ao longo do tempo. A quimioterapia preventiva por meio da administração em massa de medicamentos, a intensificação da gestão de casos e o manejo integrado de vetores foram amplamente recomendados como estratégias para o controle integrado. A campanha brasileira foi realizada em quatro iterações entre 2013 e 2017. O público-alvo foram crianças de 5 a 14 anos matriculadas em escolas públicas municipais de todo o país. Em resumo, foi detectado um total de 1 074 e 73 522 novos casos de hanseníase e tracoma, respectivamente. Foram administradas cerca de 18 milhões de doses de quimioterapia preventiva para helmintíase transmitida pelo solo. Mais de 700 casos de esquistossomose foram diagnosticados e tratados.

Conclusões.

As estratégias integradas implementadas no Brasil ao longo da campanha geraram resultados alinhados com as recomendações da OMS para o controle de doenças tropicais negligenciadas, especialmente aquelas relativas à administração em massa de medicamentos, à detecção ativa de casos e à intensificação da gestão de casos. Portanto, a continuidade da campanha com ferramentas de avaliação adequadas deve ser incentivada como uma política de saúde pública constante na agenda do governo brasileiro.

Palavras-chave
Doenças negligenciadas; controle de doenças transmissíveis; política de saúde; análise documental; Brasil

Neglected tropical diseases (NTD) are a diverse group of treatable and preventable communicable diseases listed by the World Health Organization (WHO) from the early 2000s. The list currently includes more than 20 human and zoonotic diseases, which occur predominantly in developing countries of Africa, Asia, and the Americas (11. World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565.
https://apps.who.int/iris/handle/10665/3...
). Within these areas, NTDs affect more than 1 billion people, especially those living in precarious socioeconomic conditions with a lack of basic sanitation and drinking water coverage and limited access to primary health care services (11. World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565.
https://apps.who.int/iris/handle/10665/3...
, 22. World Health Organization. Integrating neglected tropical diseases into global health and development: fourth WHO report on neglected tropical diseases. Geneva: WHO; 2017. Available from: https://apps.who.int/iris/handle/10665/255011.
https://apps.who.int/iris/handle/10665/2...
). If left undiagnosed and untreated, NTDs may result in physical deformities, disability, and death. This impacts on stigmatization, discrimination, social exclusion, and loss of productivity, and compromises family and government budgets. Annually, more than 200 000 deaths and 19 million disability-adjusted life years (DALYs) are related to NTDs worldwide (33. World Health Organization. Neglected tropical diseases. Geneva: WHO; 2021. Available from: https://www.who.int/health-topics/neglected-tropical-diseases#tab=tab_2.
https://www.who.int/health-topics/neglec...
).

Children are disproportionately at higher risk than adults for some NTDs, such as soil-transmitted helminthiasis (STH) and dengue (44. Hotez PJ, Odom John AR, LaBeaud AD. Pediatric tropical medicine: The neglected diseases of children. PLoS Negl Trop Dis. 2019;13(5):e0007008. https://doi.org/10.1371/journal.pntd.0007008.
https://doi.org/10.1371/journal.pntd.000...
). In addition to being commonly affected by more than one disease (55. Steinmann P, Utzinger J, Du ZW, Zhou XN. Multiparasitism a neglected reality on global, regional and local scale. Adv Parasitol. 2010;73:21–50. https://doi.org/10.1016/S0065-308X(10)73002-5.
https://doi.org/10.1016/S0065-308X(10)73...
), children are highly susceptible to the deleterious consequences of malnutrition and impairment of physical and cognitive development (66. Brandão E, Romero S, da Silva MAL, Santos FLN. Neglected tropical diseases in Brazilian children and adolescents: data analysis from 2009 to 2013. Infect Dis Poverty. 2017;6(1):154. https://doi.org/10.1186/s40249-017-0369-0.
https://doi.org/10.1186/s40249-017-0369-...
). Together, ascariasis, hookworm infection, trichuriasis, and dengue annually affect more than 80 million children under 5 years of age, which represents 65% of global DALYs in this age group (44. Hotez PJ, Odom John AR, LaBeaud AD. Pediatric tropical medicine: The neglected diseases of children. PLoS Negl Trop Dis. 2019;13(5):e0007008. https://doi.org/10.1371/journal.pntd.0007008.
https://doi.org/10.1371/journal.pntd.000...
).

In the last two decades, WHO has made considerable efforts to reduce the burden of NTDs and, consequently, to achieve one of the Sustainable Development Goals (SDGs) (77. Bangert M, Molyneux DH, Lindsay SW, Fitzpatrick C, Engels D. The cross-cutting contribution of the end of neglected tropical diseases to the sustainable development goals. Infect Dis Poverty. 2017;6(1):73. https://doi.org/10.1186/s40249-017-0288-0.
https://doi.org/10.1186/s40249-017-0288-...
). Thus, WHO has released technical guidelines for endemic countries with recommendations for integrated approaches targeting the control, prevention, and elimination or eradication of NTDs in the general population and/or target groups (11. World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565.
https://apps.who.int/iris/handle/10665/3...
).

Brazil has been identified as one of the most relevant hotspots for NTDs worldwide (88. Hotez PJ. Ten Global “Hotspots” for the Neglected Tropical Diseases. PLoS Negl Trop Dis. 2014;8(5):e2496. https://doi.org/10.1371/journal.pntd.0002496.
https://doi.org/10.1371/journal.pntd.000...
). Fourteen NTDs are endemic in Brazil, with heterogeneous distribution across the country (99. Lindoso JA, Lindoso AA. Neglected tropical diseases in Brazil. Rev Inst Med Trop Sao Paulo. 2009;51(5):247–253. https://doi.org/10.1590/s0036-46652009000500003.
https://doi.org/10.1590/s0036-4665200900...
, 1010. Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Articulação Estratégica de Vigilância em Saúde. Guia de Vigilância em Saúde. Brasília: Ministério da Saúde; 2022. Available from: https://bvsms.saude.gov.br/bvs/publicacoes/guia_vigilancia_saude_5ed_rev_atual.pdf.
https://bvsms.saude.gov.br/bvs/publicaco...
), although the highest detection rates are observed in municipalities of the North and Northeast regions (1111. Hotez PJ, Fujiwara RT. Brazil's neglected tropical diseases: an overview and a report card. Microbes Infect. 2014;16(8):601–606. https://doi.org/10.1016/j.micinf.2014.07.006.
https://doi.org/10.1016/j.micinf.2014.07...
). Following recommendations of the Pan American Health Organization (PAHO) aimed at the elimination or reduction of NTDs and other poverty-related infections (1212. Pan American Health Organization. Elimination of Neglected Diseases and Other Poverty-Related Infections [Resolution CD49.R19]. 49th PAHO Directing Council, 61st Session of the Regional Committee of the World Health Organization for the Americas; 28 September–2 October 2009. Washington, DC: PAHO; 2009. Available from: https://www.paho.org/en/documents/cd49r19-resolution-elimination-neglected-diseases-and-other-poverty-related-infections.
https://www.paho.org/en/documents/cd49r1...
), in 2012 the Brazilian Ministry of Health (MoH) launched the Integrated Plan of Strategic Actions to Eliminate Leprosy, Filariasis, Schistosomiasis, and Onchocerciasis as a Public Health Problem, Trachoma as a Cause of Blindness, and Control of Soil-Transmitted Helminths (1313. Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância em Doenças Transmissíveis. Plano integrado de ações estratégicas de eliminação da hanseníase, filariose, esquistossomose e oncocercose como problema de saúde pública, tracoma como causa de cegueira e controle das geohelmintíases: plano de ação 2011-2015. Brasília: Ministério da Saúde; 2012. Available from: https://bvsms.saude.gov.br/bvs/publicacoes/plano_integrado_acoes_estrategicas_2011_2015.pdf.
https://bvsms.saude.gov.br/bvs/publicaco...
). Among other populations, this Integrated Plan (IP) targeted school-age children for preventive chemotherapy delivered through mass anthelmintic administration combined with early case detection and treatment of targeted NTDs. These strategic actions were carried out nationwide during a national campaign in four iterations between 2013 and 2017 (1414. Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Coordenação Geral de Hanseníase e Doenças em Eliminação. Informe Técnico e Operacional V Campanha Nacional de Hanseníase, Verminoses, Tracoma e Esquistossomose. Brasília: Ministério da Saúde; 2017. Available from: http://www.riocomsaude.rj.gov.br/Publico/MostrarArquivo.aspx?C=ipu4TlJo5Ts%3D.
http://www.riocomsaude.rj.gov.br/Publico...
). After this period, the actions were discontinued.

Ten years after the launch of the IP and the completion of the first iteration of the national campaign, the relevance and adequacy of the actions performed have not yet been addressed. An analysis of these actions from the perspective of the WHO recommendations can be useful to identify successes and gaps related to the IP and the national campaign, as well as to support the possibility of continuing the integration of NTDs as a priority item in the Brazilian government agenda. Thus, the objective of this study was to examine the feasibility of integrated interventions aimed at the prevention, control, or elimination of NTDs by reviewing the conduct and results of the Brazilian national campaign in light of official WHO documentation.

MATERIALS AND METHODS

This was a document review to summarize the results of the national campaign aimed at the integrated control of NTDs in Brazil. This campaign was one strategy to implement the IP in coherence with WHO recommendations. The results of this review are presented from the perspective of the timeline of WHO official documentation related to the integration of strategies for the prevention, control, and elimination or eradication of NTDs and published from 2007 to 2020.

The WHO documentation was accessed in May 2022 from the WHO official website (www.who.int). With the exception of the Global Plan to Combat Neglected Tropical Diseases 2008–2015, all documents were accessed through the following pathway on the website: Health Topics > Neglected Tropical Diseases > WHO Resolutions and Decisions > Resolutions and Decisions on Neglected Tropical Diseases: 1948–2020 > Full List of NTD WHA Resolutions > All. Documents published between 2007 and 2020 of the following types were included: brochure and flyer, global strategy, governing bodies documentation, and report. The selected documents were organized chronologically and categorized according to their nature; i.e., plan, resolution, report, or roadmap. In sequence, the objectives and the main integrated strategies recommended for the prevention, control, and elimination or eradication of NTDs presented in each document were extracted. The document research was facilitated using a retrospective strategy, as the more recent publications referred to previous ones. No publication about the topic was excluded.

The IP and the official technical report with the results of the national campaign were accessed from the MoH Brazil official website (www.gov.br/saude/pt-br). For the IP, information was collated on the objectives, proposed integration strategies, and targeted NTDs with their respective goals. The following information regarding the national campaign was collated: dates of each iteration, strategies adopted for each disease/group of diseases, and main results (i.e., number of municipalities and schools included; number of screened, suspected, and confirmed cases of leprosy; number of screened, confirmed, and treated cases of trachoma and their contacts; and number of individuals who received preventive chemotherapy for STH).

Although leprosy and STH are widely distributed across Brazil, most of the cases are concentrated in the North and Midwest regions. The updated trachoma distribution was unknown before the campaign, so municipalities with poverty pockets were targeted and the campaign allowed access the truly endemic areas. Based on the poverty and life conditions criteria, all municipalities that participated in the campaign were areas with occurrence of leprosy, STH, and trachoma. For schistosomiasis, only endemic areas were considered, which have a focal distribution in Brazil. The IP mapped the geographic distribution of each disease as well the combinations of diseases (1313. Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância em Doenças Transmissíveis. Plano integrado de ações estratégicas de eliminação da hanseníase, filariose, esquistossomose e oncocercose como problema de saúde pública, tracoma como causa de cegueira e controle das geohelmintíases: plano de ação 2011-2015. Brasília: Ministério da Saúde; 2012. Available from: https://bvsms.saude.gov.br/bvs/publicacoes/plano_integrado_acoes_estrategicas_2011_2015.pdf.
https://bvsms.saude.gov.br/bvs/publicaco...
).

RESULTS

The WHO documentation timeline is depicted in Figure 1. In 2007, WHO released the Global Plan to Combat Neglected Tropical Diseases 2008–2015 (1515. World Health Organization. Global plan to combat neglected tropical diseases 2008–2015. Geneva: WHO; 2007. Available from: https://apps.who.int/iris/handle/10665/69708.
https://apps.who.int/iris/handle/10665/6...
), which addressed the first steps toward the integrated control of NTDs. Three years later, Working to Overcome the Global Impact of Neglected Tropical Diseases: First WHO Report on Neglected Tropical Diseases (1616. World Health Organization. Working to overcome the global impact of neglected tropical diseases: first WHO report on neglected tropical diseases. Geneva: WHO; 2010. Available from: https://apps.who.int/iris/handle/10665/44440.
https://apps.who.int/iris/handle/10665/4...
) was published. This report recommended the combination of the following strategies, considered to be the backbone for the prevention and control of NTDs: preventive chemotherapy; intensified case management; vector control; provision of safe water, sanitation, and hygiene (WASH); and veterinary public health. Based on the Global Plan, in 2012, WHO published Accelerating Work to Overcome the Global Impact of Neglected Tropical Diseases: A Roadmap for Implementation (1717. World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases: a roadmap for implementation. Geneva: WHO; 2012. Available from: https://apps.who.int/iris/handle/10665/70809.
https://apps.who.int/iris/handle/10665/7...
), which presented clearer and more specific targets for each disease. In the following year, the World Health Assembly, through Resolution WHA66.12/2013 (1818. World Health Organization. Neglected tropical diseases [Resolution WHA66.12]. 66th World Health Assembly; 27 May 2013. Geneva: WHO; 2013. Available from: https://apps.who.int/iris/bitstream/handle/10665/150163/A66_R12-en.pdf.
https://apps.who.int/iris/bitstream/hand...
), reinforced the relevance of previous documents (i.e., the 2007 Global Plan and 2012 Roadmap) and urged Member States to expand and implement interventions focused on NTDs to achieve the preestablished goals. In 2017, Integrating Neglected Tropical Diseases into Global Health And Development: Fourth WHO Report on Neglected Tropical Diseases (22. World Health Organization. Integrating neglected tropical diseases into global health and development: fourth WHO report on neglected tropical diseases. Geneva: WHO; 2017. Available from: https://apps.who.int/iris/handle/10665/255011.
https://apps.who.int/iris/handle/10665/2...
) was published. The document recommended an innovative focus on the integrated management of NTDs that affect the skin. Eight years after the first edition, WHO released the second and the most recent Roadmap on NTDs, Ending the Neglect to Attain the Sustainable Development Goals: A Road Map for Neglected Tropical Diseases 2021–2030 (11. World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565.
https://apps.who.int/iris/handle/10665/3...
).

FIGURE 1.
Timeline of the World Health Organization (WHO) documentation related to the integration of strategies for the prevention, control, and elimination or eradication of neglected tropical diseases (2007–2020), and the Integrated Plan and national campaign aimed at integrated control of neglected tropical diseases in Brazil

Table 1 summarizes the objectives of each document and the main integrated strategies that have been recommended for the prevention, control, and elimination or eradication of NTDs. With the exception of Resolution WHA66.12/2013, all documents were exhaustive regarding preventive chemotherapy through mass drug administration (MDA) and integrated vector management. Although the First WHO Report on NTDs recommended intensified case management in combination with the other key strategies, integrated case detection and management – specifically for skin NTDs – was only recommended years later by the Fourth WHO Report on NTDs and the second edition of the Roadmap. Additionally, the Roadmap from 2020 recommended a combined search for suspected cases and contacts of NTDs in specific populations. Integration strategies related to WASH and veterinary public health were recommended by the WHO reports released in 2010 and 2017 and by the roadmaps launched in 2012 and 2020. A One Health approach was included from 2017 onward in all of these documents. Except for the Global Plan, all documents recommended the incorporation of activities aimed at the control of NTDs into national health systems, both in primary care centers and in preexisting control programs, as stated in Resolution WHA66.12/2013. For that, the development of an integrated online platform for data management and surveillance was recommended in three documents (namely, the Global Plan, the Fourth Report, and the most recent Roadmap).

TABLE 1.
Summary of World Health Organization publications from 2007 to 2020, with objectives and main integrated strategies for the prevention, control, and elimination or eradication of neglected tropical diseases

The IP was launched by the MoH in 2012 with the general objective defined as the promotion of the development and implementation of effective and evidence-based integrated and interprogrammatic public policies to reduce the burden of diseases in elimination. For this purpose, the active case detection and timely treatment as well as interventions with collective preventive treatment within the scope of primary health care were recommended. The selection of target diseases was based on the classification of NTDs and other poverty-related infections in accordance with PAHO Resolution CD49.R19. Thus, the following diseases were included with their respective goals: (i) leprosy, schistosomiasis, lymphatic filariasis, and onchocerciasis: elimination as a public health problem; (ii) STH: control with drastic load reduction; and (iii) trachoma: elimination as a cause of blindness.

TABLE 2.
Summary of the main results of the four iterations of the national campaign aimed at integrated control of neglected tropical diseases in Brazil, 2013–2017

The strategic actions proposed by the IP were performed as a national campaign in four iterations conducted from 2013 to 2017 (Figure 1). The target audience was children aged 5–14 years enrolled in municipal public schools. For leprosy, cases were first screened through the completion of a self-image form by parents or guardians. After analysis of the form, suspected cases were referred for medical consultation at health units. In case of confirmation of leprosy, treatment was started immediately. For trachoma, cases were actively detected by external eye examination. Confirmed cases and the respective household contacts were treated. The investigation of schistosomiasis was carried out through parasitological examination of feces with treatment of positive cases, and MDA according to the local positivity rate. For STH, preventive chemotherapy was administered to students under the supervision of primary health care professionals.

Table 2 summarizes the main results of the national campaign according to each iteration/year. The percentage of Brazilian municipalities participating in the campaign increased over the first three iterations, with a peak of 41.1% (2 292/5 570) in the third iteration. The number of participating schools also increased over time, from 21 745 in 2013 to 37 212 in 2015. A total of 1 074 leprosy cases were detected, with a mean of 268.5 cases per iteration and a peak of 354 cases in the second iteration. Regarding trachoma, a total of 73 522 new cases were detected, with a mean of 18 380.5 cases per iteration, and the highest number of cases were also detected in the second iteration (25 173). Nearly 18 million doses of preventive chemotherapy for STH were administered. The number of children reached with mass anthelmintic administration increased sharply over the first three iterations of the campaign and decreased slightly in the fourth iteration. Actions targeting schistosomiasis were performed only in the last two iterations of the campaign; a total of 365 and 381 cases were diagnosed and treated in the third and fourth iterations, respectively.

From the first to the last iteration, the number of municipalities participating in the campaign increased, distributed across all 27 states. However, most were located in the North, Northeast, and Midwest regions, which are recognized as the most NTD-endemic geographic areas in the country (1313. Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância em Doenças Transmissíveis. Plano integrado de ações estratégicas de eliminação da hanseníase, filariose, esquistossomose e oncocercose como problema de saúde pública, tracoma como causa de cegueira e controle das geohelmintíases: plano de ação 2011-2015. Brasília: Ministério da Saúde; 2012. Available from: https://bvsms.saude.gov.br/bvs/publicacoes/plano_integrado_acoes_estrategicas_2011_2015.pdf.
https://bvsms.saude.gov.br/bvs/publicaco...
).

DISCUSSION

This article provides a historical overview of the WHO documentation related to the prevention, control, and elimination or eradication of NTDs. Additionally, we described the results of the national strategy aimed at integrating control of NTDs among Brazilian schoolchildren from 2013 to 2017. In summary, the integrated strategies recommended by the IP and implemented in Brazil throughout the campaign were feasible and generated results aligned with the WHO recommendations for the control of NTDs. These findings were similar to those of studies on integrated control strategies for NTDs in Mali (1919. Dembélé M, Bamani S, Dembélé R, Traoré MO, Goita S, Traoré MN, et al. Implementing preventive chemotherapy through an integrated National Neglected Tropical Disease Control Program in Mali. PLoS Negl Trop Dis. 2012;6(3):e1574. https://doi.org/10.1371/journal.pntd.0001574.
https://doi.org/10.1371/journal.pntd.000...
) and India (2020. Mani TR, Rajendran R, Sunish IP, Munirathinam A, Arunachalam N, Satyanarayana K, et al. Effectiveness of two annual, single-dose mass drug administrations of diethylcarbamazine alone or in combination with albendazole on soil-transmitted helminthiasis in filariasis elimination programme. Trop Med Int Health. 2004;9(9):1030–1035. https://doi.org/10.1111/j.1365-3156.2004.01298.x.
https://doi.org/10.1111/j.1365-3156.2004...
).

The integrated control of NTDs was gradually incorporated in WHO documentation over time. While the initial documents provided general and theoretical aspects on the theme, the first Roadmap published in 2012 proposed specific action plans to be adopted by endemic countries. Based on this Roadmap, the London Declaration on NTDs was endorsed by a coalition of public and private organizations, companies, and institutions (2121. Uniting to Combat Neglected Tropical Diseases. London Declaration on Neglected Tropical Diseases: Ending the Neglect & Reaching 2020 Goals. London: Uniting to Combat Neglected Tropical Diseases; 2012. Available from: https://unitingtocombatntds.org/en/neglected-tropical-diseases/resources/london-declaration-on-neglected-tropical-diseases/.
https://unitingtocombatntds.org/en/negle...
). Taken together, these documents constituted important tools to enhance the control of NTDs (2222. Tristao I, Cali J. It Can be Done: An Integrated Approach for Controlling and Eliminating Neglected Tropical Diseases. Washington, DC: Inter-American Development Bank; 2014. Available from: https://publications.iadb.org/en/it-can-be-done-integrated-approach-controlling-and-eliminating-neglected-tropical-diseases.
https://publications.iadb.org/en/it-can-...
), which was subsequently incorporated in the SDGs (77. Bangert M, Molyneux DH, Lindsay SW, Fitzpatrick C, Engels D. The cross-cutting contribution of the end of neglected tropical diseases to the sustainable development goals. Infect Dis Poverty. 2017;6(1):73. https://doi.org/10.1186/s40249-017-0288-0.
https://doi.org/10.1186/s40249-017-0288-...
), specifically SDG target 3.3. This target is measured by SDG indicator 3.3.5, which refers to the number of people in need of interventions against NTDs (2323. United Nations, Department of Economic and Social Affairs. Transforming our World: The 2030 Agenda for Sustainable Development. New York: United Nations; 2015. Available from: https://sustainabledevelopment.un.org/post2015/transformingourworld/publication.
https://sustainabledevelopment.un.org/po...
). Given this indicator, the Brazilian national campaign notably covered millions of schoolchildren across the country toward the elimination of leprosy, schistosomiasis, and trachoma, and the control of STH.

The analysis of WHO documentation demonstrated that preventive chemotherapy through MDA has been widely recommended as a crucial strategy for integrated control. Within the scope of our review, this was addressed for the first time in the 2007 Global Plan (1515. World Health Organization. Global plan to combat neglected tropical diseases 2008–2015. Geneva: WHO; 2007. Available from: https://apps.who.int/iris/handle/10665/69708.
https://apps.who.int/iris/handle/10665/6...
); however, the concomitant mass treatment of STH and trachoma was mentioned earlier by WHO (2424. World Health Organization. Preventive chemotherapy in human helminthiasis. Coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. Geneva: WHO; 2006. Available from: https://apps.who.int/iris/handle/10665/43545.
https://apps.who.int/iris/handle/10665/4...
). The campaign caried out in Brazil adopted MDA as a key strategy; thus, almost 18 million Brazilian children underwent preventive treatment for STH. Studies have stressed the efficacy (2525. Makaula P, Kayuni SA, Mamba KC, Bongololo G, Funsanani M, Musaya J, et al. An assessment of implementation and effectiveness of mass drug administration for prevention and control of schistosomiasis and soil-transmitted helminths in selected southern Malawi districts. BMC Health Serv Res. 2022;22(1):517. https://doi.org/10.1186/s12913-022-07925-3.
https://doi.org/10.1186/s12913-022-07925...
) and cost-effectiveness (2626. Turner HC, Truscott JE, Fleming FM, Hollingsworth TD, Brooker SJ, Anderson RM. Cost-effectiveness of scaling up mass drug administration for the control of soil-transmitted helminths: a comparison of cost function and constant costs analyses. Lancet Infect Dis. 2016;16(7):838–846. https://doi.org/10.1016/S1473-3099(15)00268-6.
https://doi.org/10.1016/S1473-3099(15)00...
) of such a strategy in decreasing the burden of STH. Therefore, it is highly likely that Brazilian children reached in the campaign were spared the deleterious effects of these infections. Moreover, it is likely that the frequent chains of transmission were interrupted after the large-scale intervention (2727. Jardim-Botelho A, Brooker S, Geiger SM, Fleming F, Lopes ACS, Diemert DJ, et al. Age patterns in undernutrition and helminth infection in a rural area of Brazil: associations with ascariasis and hookworm. Trop Med Int Health. 2008;13(4):458–467. https://doi.org/10.1111/j.1365-3156.2008.02022.x.
https://doi.org/10.1111/j.1365-3156.2008...
, 2828. Luz JGG, Carvalho AG, Marques AP, Marcondes AA, Roma JHF, Castro LS, et al. Intestinal parasitic infections and associated risk factors in preschoolers from different urban settings in Central-Western Brazil. Asian Pac J Trop Dis. 2017;7(7):405–410. https://doi.org/10.12980/apjtd.7.2017D7-90.
https://doi.org/10.12980/apjtd.7.2017D7-...
). For STH, some strategies to mitigate the risk of resistance should be applied to community-wide deworming adopted to interrupt transmission (2929. Pilotte N, Manuel M, Walson JL, Ajjampur SSR. Community-wide mass drug administration for soil-transmitted helminths – risk of drug resistance and mitigation strategies. Front Trop Dis. 2022;3:897155. https://doi.org/10.3389/fitd.2022.897155.
https://doi.org/10.3389/fitd.2022.897155...
).

Another measure widely performed in the Brazilian campaign was the active case detection of leprosy and trachoma. This measure was first highlighted in WHO documentation in 2010 as one of the five strategies considered the backbone for the prevention and control of NTDs. Nonetheless, it was clearly defined later in the 2020 Roadmap as a combined search for and contact with suspected NTD cases in a defined population (11. World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565.
https://apps.who.int/iris/handle/10665/3...
). This strategy plays a crucial role in the early diagnosis and prevention of physical disabilities (11. World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565.
https://apps.who.int/iris/handle/10665/3...
, 3030. Pedrosa VL, Dias LC, Galban E, Leturiondo A, Palheta J Jr, Santos M, et al. Leprosy among schoolchildren in the Amazon region: A cross-sectional study of active search and possible source of infection by contact tracing. PLoS Negl Trop Dis. 2018;12(2):e0006261. https://doi.org/10.1371/journal.pntd.0006261.
https://doi.org/10.1371/journal.pntd.000...
), and for leprosy and trachoma is also highly desirable to prevent further transmission (3030. Pedrosa VL, Dias LC, Galban E, Leturiondo A, Palheta J Jr, Santos M, et al. Leprosy among schoolchildren in the Amazon region: A cross-sectional study of active search and possible source of infection by contact tracing. PLoS Negl Trop Dis. 2018;12(2):e0006261. https://doi.org/10.1371/journal.pntd.0006261.
https://doi.org/10.1371/journal.pntd.000...
). Leprosy cases were referred to be treated in the health system, probably due to the long regimen of multidrug therapy. On the other hand, trachoma cases and their contacts were managed within the scope of the campaign with a single dose of azithromycin. This approach also covers the WHO recommendation regarding intensified case management. It is noteworthy that schistosomiasis cases were also managed during the campaign. These patients were only identified in the two last iterations, probably due to the more restricted geographic distribution of schistosomiasis in Brazil (3131. Scholte RGC, Gosoniu L, Malone JB, Chammartin F, Utzinger J, Vounatsou P. Predictive risk mapping of schistosomiasis in Brazil using Bayesian geostatistical models. Acta Trop. 2014;132:57–63. https://doi.org/10.1016/j.actatropica.2013.12.007.
https://doi.org/10.1016/j.actatropica.20...
).

Considering the current recommendation to prevent, control, and eliminate NTDs, since 2018 WHO has recommended the use of post-exposure chemoprophylaxis in the form of single-dose rifampicin (PEP-SDR) to contacts of leprosy cases (3232. World Health Organization. Guidelines for the diagnosis, treatment and prevention of leprosy. Geneva: WHO; 2018. Available from: https://apps.who.int/iris/handle/10665/274127.
https://apps.who.int/iris/handle/10665/2...
). This recommendation is also included in the Roadmap (11. World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565.
https://apps.who.int/iris/handle/10665/3...
). In addition, other target populations and diseases may be eligible for integrated programs, such as for vector-borne (3333. Rodrigues TOR, Perri SHV, Nunes CM, Valladão GMR, Gallani SU, Pinheiro SR, et al. Ações educativas para o controle de vetores da dengue e leishmaniose visceral. Vet Zootec. 2011;18(3):462–472.) or skin-related (3434. Carvalho AG, Tiwari A, Luz JGG, Nieboer D, Steinmann P, Richardus JH, et al. Leprosy and cutaneous leishmaniasis affecting the same individuals: A retrospective cohort analysis in a hyperendemic area in Brazil. PLoS Negl Trop Dis. 2021;15(12):e0010035. https://doi.org/10.1371/journal.pntd.0010035.
https://doi.org/10.1371/journal.pntd.001...
) NTDs.

Although the strategies implemented in Brazil generated results that apparently corresponded to the WHO recommendations, there was a lack of systematic monitoring of the actions. Even with the insertion of data in information systems by the managers of the municipalities where the actions were developed, the MoH did not perform a detailed evaluation and measurement of the goals. It means that work with cross-cutting indicators is dependent on the official data of each disease program, but not from the campaign.

The data obtained were presented summarily in the report used as the basis for this review (1414. Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Coordenação Geral de Hanseníase e Doenças em Eliminação. Informe Técnico e Operacional V Campanha Nacional de Hanseníase, Verminoses, Tracoma e Esquistossomose. Brasília: Ministério da Saúde; 2017. Available from: http://www.riocomsaude.rj.gov.br/Publico/MostrarArquivo.aspx?C=ipu4TlJo5Ts%3D.
http://www.riocomsaude.rj.gov.br/Publico...
) or analyzed in regional studies (3535. Blank NPC, Freitas BHBM, Bortolini J. Busca ativa de hanseníase em escolas de Cuiabá, Mato Grosso, Brasil. Adolesc Saude. 2018;15(3):15–26.). This was by far one of the main limitations of the campaign, as well as of this study. In addition, the discontinuity of actions deserves to be pointed out. It is very likely that this occurred due to management transitions at the federal level that culminated in the weakening of the agenda aimed at combating NTDs nationwide.

Despite these limitations, the IP and the campaign represented a major and innovative step in the fight against NTDs in Brazil. The campaign proved feasible and was in accordance with the IP as well as the WHO recommendations for the control of NTDs, especially those regarding MDA, active case detection, and intensified case management. Therefore, the continuity of the campaign with adequate evaluation tools must be encouraged as a constant public health policy in the Brazilian government agenda.

Given the high endemicity of NTDs in Brazil (99. Lindoso JA, Lindoso AA. Neglected tropical diseases in Brazil. Rev Inst Med Trop Sao Paulo. 2009;51(5):247–253. https://doi.org/10.1590/s0036-46652009000500003.
https://doi.org/10.1590/s0036-4665200900...
) and the higher coverage and sustainability of integrated control, these measures should be targeted as a priority in the planning of public health policies. To this end, the strengthening of public–private partnerships is encouraged to ensure the implementation, maintenance, and systematic evaluation of actions. In parallel, efforts must be made to design public policies aimed at achieving the other SDGs, such as those directly related to the reduction of inequalities and eradication of poverty. Taken together, these measures represent a feasible way to reduce the burden of NTDs in the country.

Disclaimer.

Authors hold sole responsibility for the views expressed in the manuscript, which may not necessarily reflect the opinion or policy of the RPSP/PAJPH and/or the Pan American Health Organization (PAHO).

  • Author contributions.
    All authors conceived the original idea and collected the data. AGC and JGGL analyzed the data and interpreted the results. All authors wrote the paper and reviewed and approved the final version.
  • Conflict of interest.
    None declared.

REFERENCES

  • 1.
    World Health Organization. Ending the neglect to attain the Sustainable Development Goals: a road map for neglected tropical diseases 2021–2030. Geneva: WHO; 2020. Available from: https://apps.who.int/iris/handle/10665/338565
    » https://apps.who.int/iris/handle/10665/338565
  • 2.
    World Health Organization. Integrating neglected tropical diseases into global health and development: fourth WHO report on neglected tropical diseases. Geneva: WHO; 2017. Available from: https://apps.who.int/iris/handle/10665/255011
    » https://apps.who.int/iris/handle/10665/255011
  • 3.
    World Health Organization. Neglected tropical diseases. Geneva: WHO; 2021. Available from: https://www.who.int/health-topics/neglected-tropical-diseases#tab=tab_2
    » https://www.who.int/health-topics/neglected-tropical-diseases#tab=tab_2
  • 4.
    Hotez PJ, Odom John AR, LaBeaud AD. Pediatric tropical medicine: The neglected diseases of children. PLoS Negl Trop Dis. 2019;13(5):e0007008. https://doi.org/10.1371/journal.pntd.0007008
    » https://doi.org/10.1371/journal.pntd.0007008
  • 5.
    Steinmann P, Utzinger J, Du ZW, Zhou XN. Multiparasitism a neglected reality on global, regional and local scale. Adv Parasitol. 2010;73:21–50. https://doi.org/10.1016/S0065-308X(10)73002-5
    » https://doi.org/10.1016/S0065-308X(10)73002-5
  • 6.
    Brandão E, Romero S, da Silva MAL, Santos FLN. Neglected tropical diseases in Brazilian children and adolescents: data analysis from 2009 to 2013. Infect Dis Poverty. 2017;6(1):154. https://doi.org/10.1186/s40249-017-0369-0
    » https://doi.org/10.1186/s40249-017-0369-0
  • 7.
    Bangert M, Molyneux DH, Lindsay SW, Fitzpatrick C, Engels D. The cross-cutting contribution of the end of neglected tropical diseases to the sustainable development goals. Infect Dis Poverty. 2017;6(1):73. https://doi.org/10.1186/s40249-017-0288-0
    » https://doi.org/10.1186/s40249-017-0288-0
  • 8.
    Hotez PJ. Ten Global “Hotspots” for the Neglected Tropical Diseases. PLoS Negl Trop Dis. 2014;8(5):e2496. https://doi.org/10.1371/journal.pntd.0002496
    » https://doi.org/10.1371/journal.pntd.0002496
  • 9.
    Lindoso JA, Lindoso AA. Neglected tropical diseases in Brazil. Rev Inst Med Trop Sao Paulo. 2009;51(5):247–253. https://doi.org/10.1590/s0036-46652009000500003
    » https://doi.org/10.1590/s0036-46652009000500003
  • 10.
    Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Articulação Estratégica de Vigilância em Saúde. Guia de Vigilância em Saúde. Brasília: Ministério da Saúde; 2022. Available from: https://bvsms.saude.gov.br/bvs/publicacoes/guia_vigilancia_saude_5ed_rev_atual.pdf
    » https://bvsms.saude.gov.br/bvs/publicacoes/guia_vigilancia_saude_5ed_rev_atual.pdf
  • 11.
    Hotez PJ, Fujiwara RT. Brazil's neglected tropical diseases: an overview and a report card. Microbes Infect. 2014;16(8):601–606. https://doi.org/10.1016/j.micinf.2014.07.006
    » https://doi.org/10.1016/j.micinf.2014.07.006
  • 12.
    Pan American Health Organization. Elimination of Neglected Diseases and Other Poverty-Related Infections [Resolution CD49.R19]. 49th PAHO Directing Council, 61st Session of the Regional Committee of the World Health Organization for the Americas; 28 September–2 October 2009. Washington, DC: PAHO; 2009. Available from: https://www.paho.org/en/documents/cd49r19-resolution-elimination-neglected-diseases-and-other-poverty-related-infections
    » https://www.paho.org/en/documents/cd49r19-resolution-elimination-neglected-diseases-and-other-poverty-related-infections
  • 13.
    Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância em Doenças Transmissíveis. Plano integrado de ações estratégicas de eliminação da hanseníase, filariose, esquistossomose e oncocercose como problema de saúde pública, tracoma como causa de cegueira e controle das geohelmintíases: plano de ação 2011-2015. Brasília: Ministério da Saúde; 2012. Available from: https://bvsms.saude.gov.br/bvs/publicacoes/plano_integrado_acoes_estrategicas_2011_2015.pdf
    » https://bvsms.saude.gov.br/bvs/publicacoes/plano_integrado_acoes_estrategicas_2011_2015.pdf
  • 14.
    Brazil. Ministério da Saúde. Secretaria de Vigilância em Saúde. Departamento de Vigilância das Doenças Transmissíveis. Coordenação Geral de Hanseníase e Doenças em Eliminação. Informe Técnico e Operacional V Campanha Nacional de Hanseníase, Verminoses, Tracoma e Esquistossomose. Brasília: Ministério da Saúde; 2017. Available from: http://www.riocomsaude.rj.gov.br/Publico/MostrarArquivo.aspx?C=ipu4TlJo5Ts%3D
    » http://www.riocomsaude.rj.gov.br/Publico/MostrarArquivo.aspx?C=ipu4TlJo5Ts%3D
  • 15.
    World Health Organization. Global plan to combat neglected tropical diseases 2008–2015. Geneva: WHO; 2007. Available from: https://apps.who.int/iris/handle/10665/69708
    » https://apps.who.int/iris/handle/10665/69708
  • 16.
    World Health Organization. Working to overcome the global impact of neglected tropical diseases: first WHO report on neglected tropical diseases. Geneva: WHO; 2010. Available from: https://apps.who.int/iris/handle/10665/44440
    » https://apps.who.int/iris/handle/10665/44440
  • 17.
    World Health Organization. Accelerating work to overcome the global impact of neglected tropical diseases: a roadmap for implementation. Geneva: WHO; 2012. Available from: https://apps.who.int/iris/handle/10665/70809
    » https://apps.who.int/iris/handle/10665/70809
  • 18.
    World Health Organization. Neglected tropical diseases [Resolution WHA66.12]. 66th World Health Assembly; 27 May 2013. Geneva: WHO; 2013. Available from: https://apps.who.int/iris/bitstream/handle/10665/150163/A66_R12-en.pdf
    » https://apps.who.int/iris/bitstream/handle/10665/150163/A66_R12-en.pdf
  • 19.
    Dembélé M, Bamani S, Dembélé R, Traoré MO, Goita S, Traoré MN, et al. Implementing preventive chemotherapy through an integrated National Neglected Tropical Disease Control Program in Mali. PLoS Negl Trop Dis. 2012;6(3):e1574. https://doi.org/10.1371/journal.pntd.0001574
    » https://doi.org/10.1371/journal.pntd.0001574
  • 20.
    Mani TR, Rajendran R, Sunish IP, Munirathinam A, Arunachalam N, Satyanarayana K, et al. Effectiveness of two annual, single-dose mass drug administrations of diethylcarbamazine alone or in combination with albendazole on soil-transmitted helminthiasis in filariasis elimination programme. Trop Med Int Health. 2004;9(9):1030–1035. https://doi.org/10.1111/j.1365-3156.2004.01298.x
    » https://doi.org/10.1111/j.1365-3156.2004.01298.x
  • 21.
    Uniting to Combat Neglected Tropical Diseases. London Declaration on Neglected Tropical Diseases: Ending the Neglect & Reaching 2020 Goals. London: Uniting to Combat Neglected Tropical Diseases; 2012. Available from: https://unitingtocombatntds.org/en/neglected-tropical-diseases/resources/london-declaration-on-neglected-tropical-diseases/
    » https://unitingtocombatntds.org/en/neglected-tropical-diseases/resources/london-declaration-on-neglected-tropical-diseases/
  • 22.
    Tristao I, Cali J. It Can be Done: An Integrated Approach for Controlling and Eliminating Neglected Tropical Diseases. Washington, DC: Inter-American Development Bank; 2014. Available from: https://publications.iadb.org/en/it-can-be-done-integrated-approach-controlling-and-eliminating-neglected-tropical-diseases
    » https://publications.iadb.org/en/it-can-be-done-integrated-approach-controlling-and-eliminating-neglected-tropical-diseases
  • 23.
    United Nations, Department of Economic and Social Affairs. Transforming our World: The 2030 Agenda for Sustainable Development. New York: United Nations; 2015. Available from: https://sustainabledevelopment.un.org/post2015/transformingourworld/publication
    » https://sustainabledevelopment.un.org/post2015/transformingourworld/publication
  • 24.
    World Health Organization. Preventive chemotherapy in human helminthiasis. Coordinated use of anthelminthic drugs in control interventions: a manual for health professionals and programme managers. Geneva: WHO; 2006. Available from: https://apps.who.int/iris/handle/10665/43545
    » https://apps.who.int/iris/handle/10665/43545
  • 25.
    Makaula P, Kayuni SA, Mamba KC, Bongololo G, Funsanani M, Musaya J, et al. An assessment of implementation and effectiveness of mass drug administration for prevention and control of schistosomiasis and soil-transmitted helminths in selected southern Malawi districts. BMC Health Serv Res. 2022;22(1):517. https://doi.org/10.1186/s12913-022-07925-3
    » https://doi.org/10.1186/s12913-022-07925-3
  • 26.
    Turner HC, Truscott JE, Fleming FM, Hollingsworth TD, Brooker SJ, Anderson RM. Cost-effectiveness of scaling up mass drug administration for the control of soil-transmitted helminths: a comparison of cost function and constant costs analyses. Lancet Infect Dis. 2016;16(7):838–846. https://doi.org/10.1016/S1473-3099(15)00268-6
    » https://doi.org/10.1016/S1473-3099(15)00268-6
  • 27.
    Jardim-Botelho A, Brooker S, Geiger SM, Fleming F, Lopes ACS, Diemert DJ, et al. Age patterns in undernutrition and helminth infection in a rural area of Brazil: associations with ascariasis and hookworm. Trop Med Int Health. 2008;13(4):458–467. https://doi.org/10.1111/j.1365-3156.2008.02022.x
    » https://doi.org/10.1111/j.1365-3156.2008.02022.x
  • 28.
    Luz JGG, Carvalho AG, Marques AP, Marcondes AA, Roma JHF, Castro LS, et al. Intestinal parasitic infections and associated risk factors in preschoolers from different urban settings in Central-Western Brazil. Asian Pac J Trop Dis. 2017;7(7):405–410. https://doi.org/10.12980/apjtd.7.2017D7-90
    » https://doi.org/10.12980/apjtd.7.2017D7-90
  • 29.
    Pilotte N, Manuel M, Walson JL, Ajjampur SSR. Community-wide mass drug administration for soil-transmitted helminths – risk of drug resistance and mitigation strategies. Front Trop Dis. 2022;3:897155. https://doi.org/10.3389/fitd.2022.897155
    » https://doi.org/10.3389/fitd.2022.897155
  • 30.
    Pedrosa VL, Dias LC, Galban E, Leturiondo A, Palheta J Jr, Santos M, et al. Leprosy among schoolchildren in the Amazon region: A cross-sectional study of active search and possible source of infection by contact tracing. PLoS Negl Trop Dis. 2018;12(2):e0006261. https://doi.org/10.1371/journal.pntd.0006261
    » https://doi.org/10.1371/journal.pntd.0006261
  • 31.
    Scholte RGC, Gosoniu L, Malone JB, Chammartin F, Utzinger J, Vounatsou P. Predictive risk mapping of schistosomiasis in Brazil using Bayesian geostatistical models. Acta Trop. 2014;132:57–63. https://doi.org/10.1016/j.actatropica.2013.12.007
    » https://doi.org/10.1016/j.actatropica.2013.12.007
  • 32.
    World Health Organization. Guidelines for the diagnosis, treatment and prevention of leprosy. Geneva: WHO; 2018. Available from: https://apps.who.int/iris/handle/10665/274127
    » https://apps.who.int/iris/handle/10665/274127
  • 33.
    Rodrigues TOR, Perri SHV, Nunes CM, Valladão GMR, Gallani SU, Pinheiro SR, et al. Ações educativas para o controle de vetores da dengue e leishmaniose visceral. Vet Zootec. 2011;18(3):462–472.
  • 34.
    Carvalho AG, Tiwari A, Luz JGG, Nieboer D, Steinmann P, Richardus JH, et al. Leprosy and cutaneous leishmaniasis affecting the same individuals: A retrospective cohort analysis in a hyperendemic area in Brazil. PLoS Negl Trop Dis. 2021;15(12):e0010035. https://doi.org/10.1371/journal.pntd.0010035
    » https://doi.org/10.1371/journal.pntd.0010035
  • 35.
    Blank NPC, Freitas BHBM, Bortolini J. Busca ativa de hanseníase em escolas de Cuiabá, Mato Grosso, Brasil. Adolesc Saude. 2018;15(3):15–26.

Publication Dates

  • Publication in this collection
    20 Oct 2023
  • Date of issue
    2023

History

  • Received
    03 Jan 2023
  • Accepted
    12 July 2023
Organización Panamericana de la Salud Washington - Washington - United States
E-mail: contacto_rpsp@paho.org