Abstract

This study aimed to describe the prevalence of leprosy and verify the factors associated with multibacillary clinical types in a Family Health Strategy priority setting to control and monitor the disease in northeastern Brazil. This cross-sectional study used data from the Notifiable Diseases Information System related to leprosy cases notified in Imperatriz, Maranhão, between 2008 and 2017. The prevalence was determined yearly and for the period. Poisson regression models with a significance level of 5% were employed to associate the variables and the multibacillary clinical types. Most of the 2,476 leprosy cases analyzed referred to multibacillary clinical types. The prevalence ranged from 7.8 and 15.6/10,000 inhabitants, with high and very high endemicity levels. The variables male, age groups between 30 and 59 years and ≥60 years, schooling <8 years, level 2 physical disability, types 1 and 2 reactive episodes, and urban residence area showed significant associations (p≤0.05) with multibacillary clinical types. Such findings can serve as a basis for elaborating and implementing leprosy control and surveillance measures, gearing actions to the most vulnerable groups, and becoming more effective.

Keywords
Leprosy; Epidemiology; Family Health Strategy

Introduction

One of the oldest diseases affecting men, leprosy is associated with social inequality and unfavorable socioeconomic conditions, such as illiteracy, poor housing conditions, lack of basic sanitation, disorderly urban growth, and ineffective health services¹1 World Health Organization (WHO). Guidelines for the diagnosis, treatment and prevention of leprosy [Internet]. Geneva: WHO; 2018 [cited 2021 Feb 16]. Available from: https://apps.who.int/iris/handle/10665/274127
https://apps.who.int/iris/handle/10665/2...

2 Rodrigues RN, Leano HA, Bueno IC, Araújo KM, Lana FC. Áreas de alto risco de hanseníase no Brasil, período 2001-2015. Rev Bras Enferm 2020; 73(3): e20180583.^-33 Souza CD, Magalhães MA, Luna CF. Hanseníase e carência social: definição de áreas prioritárias em estado endêmico do Nordeste brasileiro. Rev Bras Epidemiol 2020; 3: e200007.. Despite having been eliminated as a public health problem in many countries (prevalence <1 case per 10,000 inhabitants) since 2000, leprosy persists as a neglected disease⁴4 Brasil. Ministério da Saúde (MS). Guia prático sobre a hanseníase [Internet]. Brasília: MS; 2017 [acessado 2021 fev 16]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2017/novembro/22/Guia-Pratico-de-Hanseniase-WEB.pdf
https://portalarquivos2.saude.gov.br/ima...

5 Barbosa CC, Bonfim CV, Brito CM, Ferreira AT, Gregório VR, Oliveira AL, Portugal JL, Medeiros ZM. Spatial analysis of reported new cases and local risk of leprosy in hyper-endemic situation in Northeastern Brazil. Trop Med Int Health 2018; 23: 748-757.^-66 Mitjà O, Marks M, Bertran L, Kollie K, Argaw D, Fahal AH, Fitzpatrick C, Fuller LC, Isquierdo BG, Hay R, Ishii N, Johnson C, Lazarus JV, Meka A, Murdoch M, Ohene SA, Small P, Steer A, Tabah EN, Tiendrebeogo A, Waller L, Yotsu R, Walker SL, Asiedu K. Integrated Control and Management of Neglected Tropical Skin Diseases. PLoS Negl Trop Dis [Internet]. 2017 [acess 2021 Feb 16]. Available from: https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd. 0005136
https://journals.plos.org/plosntds/artic... in developing countries, causing physical and social limitations to their carriers, growing costs to health services, and stagnating outlook of social inequalities in these locations⁵5 Barbosa CC, Bonfim CV, Brito CM, Ferreira AT, Gregório VR, Oliveira AL, Portugal JL, Medeiros ZM. Spatial analysis of reported new cases and local risk of leprosy in hyper-endemic situation in Northeastern Brazil. Trop Med Int Health 2018; 23: 748-757.^,66 Mitjà O, Marks M, Bertran L, Kollie K, Argaw D, Fahal AH, Fitzpatrick C, Fuller LC, Isquierdo BG, Hay R, Ishii N, Johnson C, Lazarus JV, Meka A, Murdoch M, Ohene SA, Small P, Steer A, Tabah EN, Tiendrebeogo A, Waller L, Yotsu R, Walker SL, Asiedu K. Integrated Control and Management of Neglected Tropical Skin Diseases. PLoS Negl Trop Dis [Internet]. 2017 [acess 2021 Feb 16]. Available from: https://journals.plos.org/plosntds/article?id=10.1371/journal.pntd. 0005136
https://journals.plos.org/plosntds/artic... .

In 2018, data from the World Health Organization (WHO) revealed that 208,619 new cases of the disease were detected globally, distributed in 161 countries, with a detection rate of 2,74 cases per 100 thousand inhabitants and a prevalence of 0,29 cases per 10 thousand inhabitants⁷7 World Health Organization (WHO). Global leprosy update, 2018: moving towards a leprosy free world. Wkly Epidemiol Rec [Internet]. 2019 [cited 2021 Feb 16]; 94(35;36): 389. Available from: https://apps.who.int/iris/handle/10665/326776
https://apps.who.int/iris/handle/10665/3... . Compared to the previous year, the overall prevalence rate decreased by 4%, but countries in the Americas, the Mediterranean, and the Western Pacific showed growing rates, reaching 0,58 cases per 10 thousand inhabitants⁷7 World Health Organization (WHO). Global leprosy update, 2018: moving towards a leprosy free world. Wkly Epidemiol Rec [Internet]. 2019 [cited 2021 Feb 16]; 94(35;36): 389. Available from: https://apps.who.int/iris/handle/10665/326776
https://apps.who.int/iris/handle/10665/3... .

Brazil remains on the list of 23 priority countries for controlling the disease and, together with India and Indonesia, was responsible for about 80% of new cases registered in 2018⁷7 World Health Organization (WHO). Global leprosy update, 2018: moving towards a leprosy free world. Wkly Epidemiol Rec [Internet]. 2019 [cited 2021 Feb 16]; 94(35;36): 389. Available from: https://apps.who.int/iris/handle/10665/326776
https://apps.who.int/iris/handle/10665/3... ^,88 Brasil. Ministério da Saúde (MS). Departamento de Condições Crônicas e Infecções Sexualmente Transmissíveis. Boletim epidemiológico de hanseníase [Internet]. Brasília: MS; 2020 [acessado 2021 fev 17]. Disponível em: http://www.aids.gov.br/pt-br/pub/2020/boletim-epidemiologico-de-hanseniase-2020
http://www.aids.gov.br/pt-br/pub/2020/bo... . Furthermore, it still ranks first in the Americas, contributing to 93% of newly registered cases in 2018, with a prevalence of 1,48 cases per 10,000 inhabitants⁷7 World Health Organization (WHO). Global leprosy update, 2018: moving towards a leprosy free world. Wkly Epidemiol Rec [Internet]. 2019 [cited 2021 Feb 16]; 94(35;36): 389. Available from: https://apps.who.int/iris/handle/10665/326776
https://apps.who.int/iris/handle/10665/3... ^,88 Brasil. Ministério da Saúde (MS). Departamento de Condições Crônicas e Infecções Sexualmente Transmissíveis. Boletim epidemiológico de hanseníase [Internet]. Brasília: MS; 2020 [acessado 2021 fev 17]. Disponível em: http://www.aids.gov.br/pt-br/pub/2020/boletim-epidemiologico-de-hanseniase-2020
http://www.aids.gov.br/pt-br/pub/2020/bo... . In the last five years, the highest concentration of cases occurred in the North, Northeast, and Midwest regions of the country⁸8 Brasil. Ministério da Saúde (MS). Departamento de Condições Crônicas e Infecções Sexualmente Transmissíveis. Boletim epidemiológico de hanseníase [Internet]. Brasília: MS; 2020 [acessado 2021 fev 17]. Disponível em: http://www.aids.gov.br/pt-br/pub/2020/boletim-epidemiologico-de-hanseniase-2020
http://www.aids.gov.br/pt-br/pub/2020/bo... .

In the case of endemic federative units, Maranhão stands out in the Northeast Region of Brazil, with a mean detection rate of new cases of 79,7 per 100 thousand inhabitants and a mean prevalence of 4,33 cases per 10,000 inhabitants⁸8 Brasil. Ministério da Saúde (MS). Departamento de Condições Crônicas e Infecções Sexualmente Transmissíveis. Boletim epidemiológico de hanseníase [Internet]. Brasília: MS; 2020 [acessado 2021 fev 17]. Disponível em: http://www.aids.gov.br/pt-br/pub/2020/boletim-epidemiologico-de-hanseniase-2020
http://www.aids.gov.br/pt-br/pub/2020/bo... between 2014 and 2018. Among Maranhão municipalities, Imperatriz had an incidence rate of 73,87 per 100 thousand inhabitants⁹9 Serra MA, Santos CS, Lima Neto PM, Oliveira KG, Oliveira FJ, Gordon AS, Matos DP, Lima RJCP, Bezerra JM, Dias ICCM, Santos FS, Costa ACPJ, Santos Neto M, Silva, AR. Araújo MFM. Factors associated with multibacillary leprosy in a priority region for disease control in Northeastern Brazil: a retrospective observational study. J Trop Med [Internet] 2019 [cited 2021 Feb 16]. Available from: https://www.mendeley.com/catalogue/18bedf85-c42f-3ece-b740-119392049bd9/
https://www.mendeley.com/catalogue/18bed... at the end of 2017, a priority for controlling and surveillance of the disease.

Due to the magnitude of leprosy as a Brazilian public health problem, the National Leprosy Control Program of the Brazilian Ministry of Health recommended that the disease control actions be decentralized to Primary Health Care (PHC) and coordinated by the Family Health Strategy (ESF) to facilitate people’s access to services, ensure care quality, and reduce the disease’s endemic levels¹⁰10 Savassi LCM, Modena CM. Hanseníase e a atenção primária: desafios educacionais e assistenciais na perspectiva de médicos residentes. Hansen Int 2015; 40(2): 2-16.. Despite this regulation, clinical practice and scientific investigations continue to cause difficulties for the early diagnosis and timely treatment of the disease, prevention, and monitoring of physical disabilities, besides contact surveillance, which has resulted in motor and neurological sequelae in the affected population¹¹11 Neta OAG, Arruda GMMS, Carvalho MMB, Gadelha RRM. Percepção dos profissionais de saúde e gestores sobre a atenção em hanseníase na Estratégia Saúde da Família. Rev Bras Promoc Saúde 2017; 30(2):239-248..

According to the WHO, for operational treatment purposes, Paucibacillary (PB) patients are those with up to five skin lesions and negative intradermal skin smear microscopy, when available. Multibacillary (MB) patients are those with six or more skin lesions or positive intradermal skin smear microscopy¹1 World Health Organization (WHO). Guidelines for the diagnosis, treatment and prevention of leprosy [Internet]. Geneva: WHO; 2018 [cited 2021 Feb 16]. Available from: https://apps.who.int/iris/handle/10665/274127
https://apps.who.int/iris/handle/10665/2... ^,44 Brasil. Ministério da Saúde (MS). Guia prático sobre a hanseníase [Internet]. Brasília: MS; 2017 [acessado 2021 fev 16]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2017/novembro/22/Guia-Pratico-de-Hanseniase-WEB.pdf
https://portalarquivos2.saude.gov.br/ima... . The MB classification stands out because it is the most severe forms of the disease, directly related to the greater transmissibility of Mycobacterium leprae, until treatment with polychemotherapy (PCT) is started¹²12 Espíndola MF, Nascimento JL, Gomes AC, Costa AL, Garcia FN, Rodrigues MC, Regis GJS, Vilas Boas, GF, Arruda EL. Perfil epidemiológico da hanseníase no período de 2015 a 2018 no município de Goianésia (GO). Br J Health Rev 2020; 3(2): 2600-2611..

Noteworthy is that Brazil recorded an increased proportion of MB among the number of new cases. In 2009, the rate was 57,2%, hiking to 77,2% in 2018. This increase was notable in all regions of the country and in the state of Maranhão, which showed a proportion of 80,8%⁸8 Brasil. Ministério da Saúde (MS). Departamento de Condições Crônicas e Infecções Sexualmente Transmissíveis. Boletim epidemiológico de hanseníase [Internet]. Brasília: MS; 2020 [acessado 2021 fev 17]. Disponível em: http://www.aids.gov.br/pt-br/pub/2020/boletim-epidemiologico-de-hanseniase-2020
http://www.aids.gov.br/pt-br/pub/2020/bo... .

Thus, it is imperative to know and analyze epidemiological aspects of the reported leprosy cases, concerning total cases under treatment in priority locations for monitoring the disease, in order to understand the factors associated with the clinical types with a greater possibility of spreading the disease, providing subsidies for more effective health planning and interventions. Thus, we aimed to determine the prevalence of leprosy and verify the factors associated with MB clinical types.

Methods

This is a cross-sectional study¹³13 Rouquayrol MZ, Silva MG. Rouquayrol epidemiologia & saúde. 8ª ed. Rio de Janeiro: MedBook; 2018. conducted in Imperatriz (MA), a territorial area of 1,368.988 km² and an estimated population of 258,016 inhabitants in 2018, with over 94% of these residing in the urban area¹⁴14 Instituto Brasileiro de Geografia e Estatística (IBGE). População - Imperatriz, MA [Internet]. Brasília: IBGE; 2018 [acessado 2021 fev 16]. Disponível em: https://cidades.ibge.gov.br/brasil/ma/imperatriz/panorama
https://cidades.ibge.gov.br/brasil/ma/im... . The municipality is located 626 km from the state capital, São Luís, and is the second-largest population, commercial, and service center in Maranhão¹⁴14 Instituto Brasileiro de Geografia e Estatística (IBGE). População - Imperatriz, MA [Internet]. Brasília: IBGE; 2018 [acessado 2021 fev 16]. Disponível em: https://cidades.ibge.gov.br/brasil/ma/imperatriz/panorama
https://cidades.ibge.gov.br/brasil/ma/im... ^,1515 Santos LS, Nunes FG. Imperatriz do Maranhão: proposição para a compreensão do processo de ocupação e consolidação da cidade. GeoTextos 2018; 14(2): 117-141..

All leprosy cases notified to the Notifiable Diseases Information System (SINAN) from January 2008 to December 2017, collected in February 2019 at the Health Surveillance Service (SVS) of the Regional Health Management Unit of Imperatriz were included. After data collection, duplicate records were excluded (74; 2,90%) and with a “diagnostic error” closure status (8; 0,31%).

Sociodemographic variables were selected for investigation, such as age, gender, ethnicity/skin color, and education, besides clinical-epidemiological variables, such as entry type, operational classification, clinical form, number of affected nerves, physical disability at diagnosis, number of registered contacts, number of contacts examined, residence area, and closure status.

A descriptive analysis of the data was performed, by determining the absolute and relative frequencies of the sociodemographic and clinical-epidemiological variables, according to the operational classification (MB/PB). The mean, median, mode, and standard deviation were calculated for the age variable. The age variable was also categorized into four intervals (<15 years, 15-29 years, 30-59 years, and ≥ 60 years).

The prevalence rate for every 10,000 inhabitants was determined for each year under investigation, considering all cases under treatment on December 31 of the assessment year, divided by the total population of the same place and period¹⁶16 Brasil. Ministério da Saúde (MS). Diretrizes para vigilância, atenção e eliminação da hanseníase como problema de saúde pública [Internet]. Brasília: MS; 2016 [acessado 2021 fev 17]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2016/fevereiro/04/diretrizes-eliminacao-hanseniase-4fev16-web.pdf
https://portalarquivos2.saude.gov.br/ima... , according to population estimates by the Brazilian Institute of Geography and Statistics (IBGE)¹⁴14 Instituto Brasileiro de Geografia e Estatística (IBGE). População - Imperatriz, MA [Internet]. Brasília: IBGE; 2018 [acessado 2021 fev 16]. Disponível em: https://cidades.ibge.gov.br/brasil/ma/imperatriz/panorama
https://cidades.ibge.gov.br/brasil/ma/im... .

The endemicity parameters were used to classify the prevalence findings, as expressed in the Indicators for Monitoring the Progress of Leprosy Elimination as a Public Health Problem in the Guidelines for the Surveillance, Care, and Elimination of Leprosy as a Public Health Problem¹⁶16 Brasil. Ministério da Saúde (MS). Diretrizes para vigilância, atenção e eliminação da hanseníase como problema de saúde pública [Internet]. Brasília: MS; 2016 [acessado 2021 fev 17]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2016/fevereiro/04/diretrizes-eliminacao-hanseniase-4fev16-web.pdf
https://portalarquivos2.saude.gov.br/ima... , and low endemicity was considered in the locations with less than 1,0 cases per 10,000 inhabitants; medium endemicity 1,0-4,9 cases per 10,000 inhabitants; high endemicity 5,0-9,9 cases per 10,000 inhabitants; very high endemicity 10,0-19,9 cases per 10,000 inhabitants; and hyperendemic locations ≥ 20,0 cases per 10,000 inhabitants.

Poisson regression models with robust adjustment of variance were used to verify the factors associated with the MB clinical types. Sociodemographic and clinical-epidemiological with a p-value ≤ 0,20 were included in the adjusted model. The prevalence ratios (PR) and the respective 95% confidence intervals were estimated directly by the model’s regression coefficients¹⁷17 Barros AJ, Hirakata VN. Alternatives for logistic regression in crosssectional studies: an empirical comparison of models that directly estimate the prevalence ratio. BMC Med Res Methodol 2003; 3:21.. On that occasion, “unknown” data was deleted. Data were tabulated in Microsoft Office Excel® 2019 spreadsheets and tests performed using the IBM Statistical Package for Social Science® (SPSS®), version 24,0, at a 5% significance level.

The Research Ethics Committee of the Federal University of Maranhão (UFMA) approved the research according to the human research guidelines and regulatory standards of Resolutions 466/2012 and 510/2016.

Results

A total of 2,550 leprosy cases were reported to SINAN in Imperatriz during the investigation, and 2,468 cases were considered for the investigation after applying the exclusion criteria (duplicity and diagnostic error). Of these, 1,662 (67,34%) were classified as MB and 806 (32,66%) as PB. The prevalence ranged from 7,8 to 15,6 per 10,000 inhabitants over the study period. Prevalence declined over the years until 2014 and remained stable until the end of the analyzed period after that (Figure 1).

The minimum age of the cases was 3 years and the maximum age 97 years, with a mean of 41,3 years, a standard deviation of 19,2, a median of 41, and a mode of 28 years. Comparing sociodemographic characteristics by operational classification, we observed a predominance of MB cases in males (76,43%), age group ≥ 60 years (77,52%), brown (69,54%), schooling <8 years (72,58%), and significant percentages of ignored information on variables such as ethnicity/skin color (68,42%) and education (68,82%) (Table 1).

As for the clinical-epidemiological characteristics of MB cases compared to PB, there was a predominance of other re-entries (90,90%) as entry type, dimorphic clinical type (70,70%), from two to five affected nerves (67,96%), level 2 physical disability (91,36%), type 2 reactional episode (93,33%), more than five registered and examined contacts (67,36% and 72,28%, respectively), urban residents (67,59%) and closure due to cure (68,07%). Significant percentage values of “unknown” data were also observed in the records of MB cases, specifically in variables such as entry type (82,35%), affected nerves (67,30%), physical disability (74,07%), reactional episode (64,34%), number of registered contacts (75,00%), number of contacts examined (71,09%), and exit type (67,74%) (Table 2).

In the crude analysis, the significant associations (p≤0,20) for the MB operational classification were age groups 30-59 years and ≥ 60 years, male, brown, schooling < 8 years, levels 1 and 2 physical disability, types 1 and 2 reactional episodes and, urban residence area. In the adjusted analysis, the significant associations (p≤0,05) for the MB type were male, age groups from 30 to 59 years and ≥ 60 years, schooling < 8 years, level 2 physical disability, type 1 and 2 reactional episodes, and urban residence area (Table 3).

Discussion

A progressive decline was observed in the prevalence of leprosy over the analyzed period, with a maximum value of 15.6 per 10,000 inhabitants in 2008 and a minimum of 7.8 per 10,000 inhabitants in 2016, and the municipality was classified as having high and very high endemicity levels¹⁶16 Brasil. Ministério da Saúde (MS). Diretrizes para vigilância, atenção e eliminação da hanseníase como problema de saúde pública [Internet]. Brasília: MS; 2016 [acessado 2021 fev 17]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2016/fevereiro/04/diretrizes-eliminacao-hanseniase-4fev16-web.pdf
https://portalarquivos2.saude.gov.br/ima... , with rates above the elimination target established by the WHO¹⁸18 World Health Organization (WHO). Global leprosy strategy 2016-2020: accelerating towards a leprosy-free world [Internet]. New Delhi: WHO; 2017 [cited 2021 Feb 16]. Available from: https://apps.who.int/iris/handle/ 10665/254907
https://apps.who.int/iris/handle/ 10665/... . Such findings raise the need for regular analysis of epidemiological and operational indicators to assess the effectiveness of control measures and disease progression¹⁹19 Brasil. Ministério da Saúde (MS). Estratégia nacional para o enfrentamento da hanseníase (2019-2022) [Internet]. Brasília: MS; 2019 [acessado 2021 fev 16]. Disponível em: http://portalarquivos2.saude.gov.br/images/pdf/2019/marco/27/Estrategia-Nacional-CGHDE-Consulta-Publica-27mar.pdf
http://portalarquivos2.saude.gov.br/imag... . The leprosy prevalence rate is an essential indicator to support the formulation of disease control strategies and actions to provide patients with timely treatment, discontinue the transmission chain, and prevent physical disabilities²⁰20 Ribeiro MD, Silva JC, Oliveira SB. Estudo epidemiológico da hanseníase no Brasil: reflexão sobre as metas de eliminação. Rev Panam Salud Publica 2018; 42:e42..

A study conducted by Ribeiro et al.²⁰20 Ribeiro MD, Silva JC, Oliveira SB. Estudo epidemiológico da hanseníase no Brasil: reflexão sobre as metas de eliminação. Rev Panam Salud Publica 2018; 42:e42. revealed a similar national trend of decreasing prevalence from 2005 to 2015, with a heterogeneous distribution among the Brazilian regions, with the North, Northeast, and Midwest regions responsible for the endemic burden the national territory and the managing Maranhão state for the high prevalence rates of the Northeast Region.

The country’s substantial territorial extension and the socioeconomic inequalities between regions explaining such heterogeneity and the most socioeconomically disadvantaged locations were considered of greater endemicity. Implementing PCT and other preventive measures, such as examining contacts and early detection, were listed as positive factors for the reduction²⁰20 Ribeiro MD, Silva JC, Oliveira SB. Estudo epidemiológico da hanseníase no Brasil: reflexão sobre as metas de eliminação. Rev Panam Salud Publica 2018; 42:e42..

The expanded diagnostic network and access to treatment facilitated by the decentralization of leprosy control activities with actions integrated with PHC through the ESF in Brazil is essential for the control of the disease and has was relevant in southern and southeastern settings of the country, which have reached the goal advocated by the WHO regarding the disease’s prevalence indicator¹⁹19 Brasil. Ministério da Saúde (MS). Estratégia nacional para o enfrentamento da hanseníase (2019-2022) [Internet]. Brasília: MS; 2019 [acessado 2021 fev 16]. Disponível em: http://portalarquivos2.saude.gov.br/images/pdf/2019/marco/27/Estrategia-Nacional-CGHDE-Consulta-Publica-27mar.pdf
http://portalarquivos2.saude.gov.br/imag... .

In the Northeast Region, a study investigating the relationship between leprosy and ESF coverage in Paraíba’s municipalities indicated that increased ESF coverage contributed significantly to the disease’s higher rate of detection, reinforcing that PHC-based services are crucial for the early diagnosis and timely treatment²¹21 Araújo KMFFA, Lana FCF. Relação da hanseníase com a cobertura da estratégia saúde da família e condições socioeconómicas. Ciencia y Enfermeria 2020; 26(1): 1-9..

In 2008, ESF estimated population coverage was 61,59% in Imperatriz. In 2017, it declined to 58,43%²²22 Brasil. Ministério da Saúde (MS). Cobertura da Atenção Básica [Internet]. Brasília: MS; 2020 [acessado 2021 fev 16]. Disponível em: https://egestorab.saude.gov.br/paginas/acessoPublico/relatorios/relHistoricoCoberturaAB.xhtml
https://egestorab.saude.gov.br/paginas/a... , below the Brazilian average, 63,91% that year, and with a team composed of a doctor, nurse, nursing technician or assistant and community health workers (ACS), possibly with a linked Oral Health team. Besides this setting, the professional team turnover, the incipient active search actions in children under 15 years of age, and the early detection of cases have favored the maintenance of the epidemiological chain of the disease²³23 Gordon AS, Gomes JM, Costa AC, Serra MA, Santos Neto M, Xavier MB. Incidência de hanseníase em menores de 15 anos acompanhados no município de Imperatriz, Maranhão, entre 2004 e 2010. Arq Cienc Saúde Unipar 2017; 21(1):19-24., hindering its elimination and, consequently, favoring underreporting.

Thus, the need to expand the disease diagnostic and monitoring actions emerges in all ESF teams linked to the municipality’s reference center, besides considering improvements in elements, such as the availability of human resources, technical capacity, and sensitivity of the teams and definition of workflows and processes, essential for the control and surveillance of the disease and timely for the qualification of professional practices given the specificities of the territory. ESF professionals also need to improve the quality of care offered to users and facilitate the guidance of patients and relatives in treatment, recovery, and self-care.

The ACS are professionals included in the ESF who can actively contribute to leprosy control actions due to their proximity to the population. They are the main executors of the active search for suspected dermatological cases in the population since the home visit is a working tool that builds bonds of trust with families, observes their habits, detects problems, exchanges information, and transmits health guidelines²⁴24 Vieira NF, Lanza FM, Martínez-Riera JR, Nolasco A, Lana FCF. Orientación de la atención primaria en las acciones contra la lepra: factores relacionados con los profesionales. Gaceta Sanitaria 2020; 34:120-126.^,2525 Lanza FM, Lana FCF. O processo de trabalho em hanseníase: tecnologias e atuação da equipe de saúde da família. Texto Contexto Enferm 2011; 20(Esp):238-246..

Thus, the guidelines provided by ACS during home visits can be the primary strategy to promote and maintain community awareness regarding leprosy²⁵25 Lanza FM, Lana FCF. O processo de trabalho em hanseníase: tecnologias e atuação da equipe de saúde da família. Texto Contexto Enferm 2011; 20(Esp):238-246.. While not assessing the ACS role in the context of Imperatriz, this investigation raises reflections on the importance of professional training and performance in the fight against leprosy. From this perspective, the active search assumes a hegemonic role because it is a device that allows the early identification of cases and their increase in the community and identifies patients’ abandonment of treatment¹⁰10 Savassi LCM, Modena CM. Hanseníase e a atenção primária: desafios educacionais e assistenciais na perspectiva de médicos residentes. Hansen Int 2015; 40(2): 2-16.^,1111 Neta OAG, Arruda GMMS, Carvalho MMB, Gadelha RRM. Percepção dos profissionais de saúde e gestores sobre a atenção em hanseníase na Estratégia Saúde da Família. Rev Bras Promoc Saúde 2017; 30(2):239-248..

In this study, most reported cases were MB, with a predominance of dimorphs, similar to other studies²⁶26 Mendes AO, Costa CE, Silva RC, Campos SA, Cunha VM, Silva GC, Silva MCS. Caráter clínico-epidemiológico e grau de incapacidade física nos portadores de hanseníase no município de Barbacena - MG e macrorregião no período de 2001 a 2010. Rev Med Minas Gerais 2014; 24(4):486-494.^,2727 Reis MC, Raposo MT, Alencar CH, Ramos Júnior AN, Heukelbach J. Incapacidades físicas em pessoas que concluíram a poliquimioterapia para hanseníase em Vitória da Conquista, Bahia, Brasil. Acta Fisiatr 2018; 25(2):78-85.. This shows a persistent high circulation of the bacillus, which challenges leprosy control, especially for operational reasons, such as early detection, long-term treatment, contact examination, and the disease’s social stigma.

A statistically significant association was observed for the gender variable, with a higher occurrence of MB types among men, with almost twice as much occurrence than women. Some authors have pointed out that both leprosy and MB types of the disease are more frequent in men than in women²⁸28 Souza EA, Ferreira AF, Boigny RN, Alencar CH, Heukelbach J, Martins-Melo FR, Barbosa JC, Ramos Jr AN. Hanseníase e gênero no Brasil: tendências em área endêmica da região Nordeste, 2001-2014. Rev Saude Publica 2018; 52:20.^,2929 Ramos AC, Yamamura M, Arroyo LH, Popolin MP, Chiaravalloti Neto F, Palha PF, Uchoa SAC, Pieri FM, Pinto IC, Fiorati RC, Queiroz AAR, Belchior AS, Santos DT, Garcia MCCG, Crispim, JA, Alves, LS, Berra TZ, Arcêncio RA. Spatial clustering and local risk of leprosy in São Paulo, Brazil. PLoS Negl Trop Dis [Internet]. 2017 [cited 2021 Feb 16]. Available from: https://repositorio.usp.br/item/002879810
https://repositorio.usp.br/item/00287981... . This predominance is probably linked to greater exposure to work-related activities, low demand for health services, low self-care level, and reduced access to information²⁸28 Souza EA, Ferreira AF, Boigny RN, Alencar CH, Heukelbach J, Martins-Melo FR, Barbosa JC, Ramos Jr AN. Hanseníase e gênero no Brasil: tendências em área endêmica da região Nordeste, 2001-2014. Rev Saude Publica 2018; 52:20..

The low adherence of the male public to health services may be related to the opening hours of the units, which can coincide with the exercise of work activities⁹9 Serra MA, Santos CS, Lima Neto PM, Oliveira KG, Oliveira FJ, Gordon AS, Matos DP, Lima RJCP, Bezerra JM, Dias ICCM, Santos FS, Costa ACPJ, Santos Neto M, Silva, AR. Araújo MFM. Factors associated with multibacillary leprosy in a priority region for disease control in Northeastern Brazil: a retrospective observational study. J Trop Med [Internet] 2019 [cited 2021 Feb 16]. Available from: https://www.mendeley.com/catalogue/18bedf85-c42f-3ece-b740-119392049bd9/
https://www.mendeley.com/catalogue/18bed... , which hinders men’s access and permanence at this care level³⁰30 Moreira RL, Fontes WD, Barboza TM. Dificuldades de inserção do homem na atenção básica a saúde: a fala dos enfermeiros. Esc Anna Nery 2014; 18(4): 615-621..

Studies have shown that women tend to attend health services more regularly and are more concerned with healthy habits³¹31 Levorato CD, Mello LM, Silva AS, Nunes AA. Fatores associados à procura por serviços de saúde numa perspectiva relacional de gênero. Cienc Saude Colet 2014; 19(4): 1263-1274.^,3232 Thompson AE, Anisimowicz Y, Miedema B, Hogg W, Wodchis WP, Aubrey-Bassler K. The influence of gender and other patient characteristics on health care-seeking behaviour: a Qualicopc Study. BMC Family Practice 2016; 17:38., which should also be considered regarding gender difference. In this sense, gender must be recognized as a determining factor for the occurrence and greater severity of the disease²⁸28 Souza EA, Ferreira AF, Boigny RN, Alencar CH, Heukelbach J, Martins-Melo FR, Barbosa JC, Ramos Jr AN. Hanseníase e gênero no Brasil: tendências em área endêmica da região Nordeste, 2001-2014. Rev Saude Publica 2018; 52:20., which points to the inevitability of differentiated strategies aimed at the male public, considering the diversity of leprosy’s outlook in the country. ESF professionals expanding service opening hours in the setting under investigation could be a strategic alternative for servicing this target audience.

A greater involvement was observed in the age groups 30-59 years (PR=1,60) and ≥ 60 years (PR=1,72), statistically associating with the MB clinical type. Greater possibility of contracting the most bacilliferous types with age is observed, similar to results in other studies³³33 Monteiro MJ, Santos GM, Barreto MT, Silva RV, Jesus RL, Silva HJ. Perfil epidemiológico de casos de hanseníase em um estado do Nordeste Brasileiro. Rev Aten Saude 2017; 15(54):21-28.^,3434 Oliveira AK, Freire FF, Nascimento MR. Incidência e perfil clínico-epidemiológico da hanseníase no Brasil. Revista Científica da Fasete [Internet]. 2018 [acessado 2021 Feb 16]. Disponível em: https://www.unirios.edu.br/revistarios/media/revistas/2018/20/incidencia_e_perfil_clinico_epidemiologico_da_hanseniase_no_brasil.pdf
https://www.unirios.edu.br/revistarios/m... . These findings also showed the predominance of leprosy in the economically active age group²⁹29 Ramos AC, Yamamura M, Arroyo LH, Popolin MP, Chiaravalloti Neto F, Palha PF, Uchoa SAC, Pieri FM, Pinto IC, Fiorati RC, Queiroz AAR, Belchior AS, Santos DT, Garcia MCCG, Crispim, JA, Alves, LS, Berra TZ, Arcêncio RA. Spatial clustering and local risk of leprosy in São Paulo, Brazil. PLoS Negl Trop Dis [Internet]. 2017 [cited 2021 Feb 16]. Available from: https://repositorio.usp.br/item/002879810
https://repositorio.usp.br/item/00287981... and are very relevant, since the production phase can be drastically interrupted due to the disease’s high disabling power.

Low schooling was significantly associated with MB types, and individuals with schooling < 8 years were more susceptible (PR=2,5), agreeing with the result found by Sousa et al.³⁵35 Sousa GC, Vieira FS, Oliveira DE, Costa ES, Moura ME. Caracterização clínico-epidemiológica de casos de hanseníase com incapacidades físicas. Rev Rene 2017; 18(1): 99-105.. Other studies showed a predominance of low schooling level with leprosy cases³⁶36 Basso ME, Silva RL. Perfil clínico-epidemiológico de pacientes acometidos pela hanseníase atendidos em uma unidade de referência. Rev Soc Bras Clin Med 2017; 15(1): 27-32.^,3737 Boigny RN, Souza EM, Romanholo HS, Araújo OD, Araújo TM, Carneiro MAG, Grijó MDF, Henz NLFB, Reis AS, Pinto, MSAP, Barbosa JC, Ramos Jr AN. Persistência da hanseníase em redes de convívio domiciliar: sobreposição de casos e vulnerabilidade em regiões endêmicas no Brasil. Cad Saude Publica 2019; 35(2):e00105318.. An aspect of concern of low schooling is that it is a risk for physical disabilities, since the increased schooling level of individuals tends to decrease the frequency of diagnoses with installed physical disabilities, and illiterate people and people with primary school level are more likely to be diagnosed with disabilities than those with high school education or higher³⁸38 Lages DS, Kerr BM, Bueno IC, Niitsuma EN, Lana FC. A baixa escolaridade está associada ao aumento de incapacidades físicas no diagnóstico de hanseníase no Vale do Jequitinhonha. HU Revista 2018; 44(3): 303-309.. In this line of reasoning, the relationship between schooling and leprosy can be explained by a lower level of understanding of the disease’s signs and symptoms, hindering treatment and self-care measures, besides this population’s difficult access to health services³⁹39 Souza DE. Determinação social da saúde: associação entre sexo, escolaridade e saúde autorreferida [tese]. Salvador: Instituto de Saúde Coletiva da UFBA; 2012.^,4040 Leano HA, Araújo KM, Bueno IC, Niitsuma EN, Lana FC. Fatores socioeconômicos relacionados à hanseníase: revisão integrativa da literatura. Rev Bras Enferm 2019; 72(5): 1474-1485..

Thus, the ESF’s health education is an essential factor in determining health²⁵25 Lanza FM, Lana FCF. O processo de trabalho em hanseníase: tecnologias e atuação da equipe de saúde da família. Texto Contexto Enferm 2011; 20(Esp):238-246.^,3939 Souza DE. Determinação social da saúde: associação entre sexo, escolaridade e saúde autorreferida [tese]. Salvador: Instituto de Saúde Coletiva da UFBA; 2012., making explicit the paramount importance of expanding public education investments and mitigating socioeconomic inequalities, increasing leprosy control, and improving the living conditions of the population.

In this study, level 2 physical disability was significantly associated with MB clinical types, suggesting a late diagnosis of leprosy, similar to data from other studies²⁶26 Mendes AO, Costa CE, Silva RC, Campos SA, Cunha VM, Silva GC, Silva MCS. Caráter clínico-epidemiológico e grau de incapacidade física nos portadores de hanseníase no município de Barbacena - MG e macrorregião no período de 2001 a 2010. Rev Med Minas Gerais 2014; 24(4):486-494.^,4141 Araújo EJ, Araújo OD, Araújo TM, Almeida PD, Sena IV, Neri EA. Pós-alta de hanseníase: prevalência de incapacidades físicas e sobreposição de doenças. Cogitare Enferm 2018; 23(4): e58080.

42 Darlong J, Govindharaj P, Darlong F, Mahato N. A study of untreated leprosy affected children reporting with Grade 2 disability at a referral centre in West Bengal, India. Lepr Rev 2017; 88: 298-305.^-4343 Portela NL, Sousa PH, Melo LN. Fatores associados à incapacidade física de casos novos de hanseníase em Paço do Lumiar - MA, 2006-2015. Hygeia 2018; 14(27): 80-88.. Deficiency, disability, and deformity are the leading causes of the stigma associated with the disease and significantly interfere with the quality of life of leprosy patients⁴⁴44 Reyila VP, Betsy A, Riyaz N, Sasidharanpillai S, Sherjeena PV, Majitha MP, Joseph DM. Clinico-epidemiological study of disability due to leprosy at the time of diagnosis among patients attending a tertiary care institution. Indian J Dermatol. 2019; 64(2):106-111.. Also, Leano et al.⁴⁰40 Leano HA, Araújo KM, Bueno IC, Niitsuma EN, Lana FC. Fatores socioeconômicos relacionados à hanseníase: revisão integrativa da literatura. Rev Bras Enferm 2019; 72(5): 1474-1485. emphasize that the severity of leprosy is shown in physical disabilities arising from untreated cases, which reduces or eliminates work and subsistence opportunities.

The evidence pointed out in Imperatriz leads to the discussion on achieving the 2016-2020 Global Strategy for Leprosy goals agreed by the WHO, whose fundamental principle was the early detection of all patients before the onset of disabilities⁴⁵45 World Health Organization (WHO). Global leprosy update, 2016: accelerating reduction of disease burden [Internet]. Geneva: WHO; 2017 [cited 2021 Feb 16]. Available from: https://apps.who.int/iris/bitstream/handle/10665/258841/WER9235.pdf?sequence=1
https://apps.who.int/iris/bitstream/hand... . Considering that early detection and reduction of disabilities seem to be related to efficient PHC services¹⁹19 Brasil. Ministério da Saúde (MS). Estratégia nacional para o enfrentamento da hanseníase (2019-2022) [Internet]. Brasília: MS; 2019 [acessado 2021 fev 16]. Disponível em: http://portalarquivos2.saude.gov.br/images/pdf/2019/marco/27/Estrategia-Nacional-CGHDE-Consulta-Publica-27mar.pdf
http://portalarquivos2.saude.gov.br/imag... ^,2020 Ribeiro MD, Silva JC, Oliveira SB. Estudo epidemiológico da hanseníase no Brasil: reflexão sobre as metas de eliminação. Rev Panam Salud Publica 2018; 42:e42., the importance of improving the provision of health services is emphasized concerning access, application of resources, and professional training. Thus, regular training directed to the needs of professionals working in the ESF in Imperatriz is required to offer more qualified care regarding the early detection of leprosy signs and symptoms.

A statistically significant association was identified between type 1 and type 2 reactive episodes and the MB types, with respective PRs of 1,50 and 2,00. A similar result was found by Monteiro et al.⁴⁶46 Monteiro LD, Alencar CH, Barbosa JC, Braga KP, Castro MD, Heukelbach J. Incapacidades físicas em pessoas acometidas pela hanseníase no período pós-alta da poliquimioterapia em um município no Norte do Brasil. Cad Saude Publica 2013; 29(5): 909-920. in a study carried out in Tocantins, who recognize that MB cases are risk factors for the development of reactive episodes, which are more frequent in MB cases.

Correlating clinical types and reactive states is extremely important, as these episodes are complications during the disease and the leading causes of disability in these patients⁴4 Brasil. Ministério da Saúde (MS). Guia prático sobre a hanseníase [Internet]. Brasília: MS; 2017 [acessado 2021 fev 16]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2017/novembro/22/Guia-Pratico-de-Hanseniase-WEB.pdf
https://portalarquivos2.saude.gov.br/ima... ^,4747 Coelho Júnior LG, Machado GB, Faria TA. Reação hansênica tipo dois em paciente multibacilar, forma Virchowiana, em vigência de tratamento: relato de caso. Rev Med (São Paulo) 2015; 94(3): 197-200.. The clinical complications resulting from these intercurrences should be avoided by reinforcing the importance of prevention and a specific PCT, which provides new leprosy curative perspectives⁴⁷47 Coelho Júnior LG, Machado GB, Faria TA. Reação hansênica tipo dois em paciente multibacilar, forma Virchowiana, em vigência de tratamento: relato de caso. Rev Med (São Paulo) 2015; 94(3): 197-200. without the need to restart it, and they do not contraindicate it⁴4 Brasil. Ministério da Saúde (MS). Guia prático sobre a hanseníase [Internet]. Brasília: MS; 2017 [acessado 2021 fev 16]. Disponível em: https://portalarquivos2.saude.gov.br/images/pdf/2017/novembro/22/Guia-Pratico-de-Hanseniase-WEB.pdf
https://portalarquivos2.saude.gov.br/ima... .

The urban area showed statistical significance with the MB clinical types. Residents of these spaces were twice as likely to fall ill than rural residents, results that are in line with other studies⁴⁸48 Santos DA, Spessatto LB, Melo LS, Olinda RA, Lisboa HC, Silva MS. Prevalência de casos de hanseníase. Rev Enferm UFPE Online 2017; 11(Supl. 10):4045-4055.^,4949 Gonçalves NV, Alcântara RC, Sousa Júnior AS, Pereira AL, Miranda CS, Oliveira JSS, Melo ACBV, Guedes JA, Costa RJF, Costa SBN, Marcos W, Gomes RP, Oliveira RAC, Palácios VRCM. A hanseníase em um distrito administrativo de Belém, estado do Pará, Brasil: relações entre território, socioeconomia e política pública em saúde, 2007-2013. Rev Pan-Amaz Saude 2018; 9(2): 21-30., in which leprosy cases were identified essentially in urban settings.

The leprosy urbanization process in Brazil has escalated in the last decades, mainly due to the population’s unsafe living conditions and the restricted access to collective goods and services. These characteristics are related in the urban space weakened by the high population density and socioeconomic vulnerability, which together determine a general outlook of illness and death⁵⁰50 Barbosa DR, Almeida MG, Santos AG. Características epidemiológicas e espaciais da hanseníase no Estado do Maranhão, Brasil, 2001-2012. Med (Ribeirão Preto) 2014; 47(4): 347-356.. However, it is essential to highlight that the small number of cases reported in the rural area of the setting under investigation may be related to inequalities in access to health, the lower supply of health services in these areas, and the lower demand for these services by the rural population, when compared to the urban dwellers⁵¹51 Arruda NM, Maia AG, Alves LC. Desigualdade no acesso à saúde entre as áreas urbanas e rurais do Brasil: uma decomposição de fatores entre 1998 a 2008. Cad Saude Publica 2018; 34(6): e00213816.. These factors may result in some notifications below the actual existing value.

A finding that should be highlighted in this study is a large number of “unknown” responses in important information obtained from completing essential and mandatory fields, which means flaws in the notification of the disease or improper feeding, hindering screening and directing appropriate care to the disease carrier. The feeding of the information systems depends directly on the efforts of the municipalities and regions to provide the data³⁴34 Oliveira AK, Freire FF, Nascimento MR. Incidência e perfil clínico-epidemiológico da hanseníase no Brasil. Revista Científica da Fasete [Internet]. 2018 [acessado 2021 Feb 16]. Disponível em: https://www.unirios.edu.br/revistarios/media/revistas/2018/20/incidencia_e_perfil_clinico_epidemiologico_da_hanseniase_no_brasil.pdf
https://www.unirios.edu.br/revistarios/m... and the proper completion of the notification form by the ESF professionals involved in patient care.

One of the main limitations of this study is the use of secondary data that often lack information and show inconsistent data. Therefore, it is necessary to correctly complete the compulsory notification forms with consistent information so that these data provide subsidies for assessing the population’s health status and decision-making.

Conclusion

Most patients had the multibacillary clinical type, with greater involvement of the economically active population and a low schooling level. High and very high levels of endemicity were evidenced, which shows that health management and services still fail to control this disease through prevention, management, and curative actions.

Such findings raise the need to strengthen health surveillance actions, especially by the Family Health Strategy professionals linked to the reference center in Imperatriz, focusing on active search and early treatment to reduce physical disabilities and consequent harm to the quality of life of those with this condition.

Acknowledgments

The research was financed by the Foundation for the Support of Research and Scientific and Technological Development of Maranhão (FAPEMA), file reference UNIVERSAL 01036/19, and the Coordination for the Improvement of Higher Education Personnel - Brazil (CAPES), Finance Code 001. We are grateful to the Health Surveillance Service of the Regional Health Management Unit of Imperatriz for providing us with the data.

References

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History