Artigo original
Impact of COVID-19 on the registration of tegumentary leishmaniasis cases in Maranhão, Brazil
Impacto da COVID-19 no registro de casos de leishmaniose tegumentar no Maranhão, Brasil
Impacto de la COVID-19 en el registro de casos de leishmaniasis tegumentaria en Maranhão, Brasil
Impact of COVID-19 on the registration of tegumentary leishmaniasis cases in Maranhão, Brazil
Revista de Epidemiologia e Controle de Infecção, vol. 13, núm. 3, pp. 164-170, 2023
Universidade de Santa Cruz do Sul

Recepción: 04 Mayo 2023
Aprobación: 28 Agosto 2023
Abstract: Background and Objectives: Elucidating the potential impact of COVID-19 on surveillance interventions and programs, such as the tegumentary leishmaniasis one, during the first year of the pandemic can help understand its consequences for notification systems, which can inform immediate public policy and health education actions, as well as highlight the need to implement new strategies to strengthen epidemiological surveillance services. The objective of the present study was to analyze the possible impact of the COVID-19 pandemic on the number of cases of tegumentary leishmaniasis in Maranhão, Brazil. Methods: Ecological study of confirmed cases of tegumentary leishmaniasis in the period from January 2015 to December 2020. Data were obtained from the Brazilian Information System for Notifiable Diseases. The P-score metrics were used to evaluate the possible underreporting of tegumentary leishmaniasis. Results: In the period from 2015 to 2020, 7,886 new cases of the disease were registered. For the year 2020, 1,346 cases were expected, but 1,158 were notified, which represented a decrease of 13.94%. The regional health centers of São Luís, São João dos Patos, and Presidente Dutra showed the greatest drops in possible expected new cases. Conclusion: The challenges in diagnosing tegumentary leishmaniasis cases seem to have intensified in the context of COVID-19 in Maranhão, which signals an important alert for health services and managers.
Keywords: Epidemiology, Neglected Diseases, Coronavirus, Health Services.
Resumo: Justificativa e Objetivos: O potencial impacto da COVID-19 nas intervenções e nos programas de vigilância, como a leishmaniose tegumentar, durante o primeiro ano da pandemia, auxilia no entendimento das consequências da pandemia nos sistemas de notificação, com o intuito de subsidiar ações imediatas de políticas públicas e educação em saúde, além de evidenciar a necessidade de implementação de novas estratégias de fortalecimento dos serviços de vigilância epidemiológica. Este estudo teve como objetivo analisar o possível impacto da pandemia da COVID-19 no número de registros de casos de leishmaniose tegumentar no Maranhão, Brasil. Métodos: Trata-se de um estudo ecológico dos casos confirmados de leishmaniose tegumentar no período de janeiro de 2015 a dezembro de 2020. Os dados foram obtidos do Sistema de Informação de Agravos de Notificação. A métrica P-score foi utilizada para avaliar os possíveis subregistros de leishmaniose tegumentar. Resultados: No período de 2015 a 2020, foram registrados 7.886 casos novos da doença. Para o ano de 2020, eram esperados 1.346 casos, porém 1.158 foram notificados, o que representa uma diminuição de 13,94%. As regionais de saúde de São Luís, São João dos Patos e Presidente Dutra apresentam as maiores quedas de possíveis novos casos esperados. Conclusão: Os desafios no diagnóstico dos casos de leishmaniose tegumentar parecem ter se intensificado no contexto da COVID-19 no Maranhão, o que sinaliza um alerta importante para os serviços de saúde e gestores.
Palavras-chave: Epidemiologia, Doenças negligenciadas, Coronavírus, Serviços de Saúde.
Resumen: Justificación y Objetivos: El posible impacto de la COVID-19 en las intervenciones y programas de vigilancia, como el de la leishmaniasis tegumentaria, durante el primer año de la pandemia, ayuda a comprender las consecuencias de la pandemia en los sistemas de notificación, con el fin de subsidiar las acciones inmediatas de política pública y educación para la salud, además de resaltar la necesidad de implementar nuevas estrategias para fortalecer los servicios de vigilancia epidemiológica. Este estudio tuvo como objetivo analizar el posible impacto de la pandemia de COVID-19 en el número de registros de casos de leishmaniasis tegumentaria en Maranhão, Brasil. Métodos: Se trata de un estudio ecológico de los casos confirmados de leishmaniasis tegumentaria desde enero de 2015 hasta diciembre de 2020. Los datos se obtuvieron del Sistema de Información de Enfermedades de Declaración Obligatoria. Se utilizó la métrica P-score para evaluar los posibles subregistros de leishmaniasis tegumentaria. Resultados: Entre 2015 y 2020, se registraron 7.886 nuevos casos de la enfermedad. Para 2020 se esperaban 1.346 casos, pero se notificaron 1.158, lo que representa una disminución del 13,94%. Los centros regionales de salud de São Luís, São João dos Patos y Presidente Dutra presentaron las mayores caídas en los posibles nuevos casos esperados. Conclusión: Los desafíos en el diagnóstico de los casos de leishmaniasis tegumentaria parecen haberse intensificado en el contexto de la COVID-19 en Maranhão, lo que señala una alerta importante para los servicios y gestores de salud.
Palabras clave: Epidemiología, Enfermedades Desatendidas, Coronavirus, Servicios de Salud.
INTRODUCTION
Between December 18 and 29, 2019, five atypical pneumonia cases were reported in inpatients in the city of Wuhan, China.1,2 On December 30, 2019, these cases were notified at the World Health Organization (WHO). On January 7, 2020, a new type of coronavirus (CoV) was isolated. At that time, it was designated 2019-nCoV, a term subsequently changed by WHO to severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2), responsible for the coronavirus disease-2019 (COVID-19).3,4
The COVID-19 pandemic exposed the inequalities in access to health services all over the world5. Turning attention to this health issue affected care measures to prevent and treat other pathologies, such as tegumentary leishmaniasis (TL), which delayed its timely diagnosis and led to an increase in disabling and severe complications, especially in vulnerable populations.6,7
In South America, the first reported cases of COVID-19 occurred in Brazil, which was one of the countries most affected by the disease, with over 7,716,184 cases and around 195,725 deaths in 20208. In this period, attention was focused on and adjusted to fighting this pandemic. In the Brazilian state of Maranhão, the efforts to prevent a growth in the number of cases of this disease caused the authorities to declare a state of emergency, which made it possible to implement several measures, including increasing the number of hospital beds specifically for patients with this infection in intensive care units and wards, concert and lesson cancellations, as well as restrictions in interstate transportation. This quick response to the increase in COVID-19 cases may have originated gaps in access to health services by patients with TL9. The objective of the present study was analyzing the possible impact of COVID-19 on the number of reported TL cases in Maranhão, Brazil.
METHODS
Study area
Maranhão is located in the Brazilian Northeast Region. The state has an area of 333,367 km2, an estimated population in 2020 of 7,114,598 people, and a demographic density of 19.81 people per km2. It is bordered to the west by Pará, to the southwest by Tocantins, to the north by the Atlantic Ocean, and the southeast and east by Piauí.10
The state is divided into 19 health regions (São Luís, Chapadinha, Itapecuru, Rosário, Timon, Pinheiro, Viana, Açailândia, Imperatriz, Barra do Corda, Presidente Dutra, São João dos Patos, Bacabal, Codó, Pedreiras, Santa Inês, Zé Doca, Balsas, and Caxias), delimited based on municipalities, population, and demographic density, for the provision of actions and minimum services in each area (Figure 1).11

Study type
This was an ecological study that analyzed confirmed TL cases and incidence rates in Maranhão and its health regions between January 2015 and December 2020.
Data source
The data on confirmed new TL cases included in the present study were obtained at the Brazilian Information System for Notifiable Diseases (Sinan, as per its acronym in Portuguese) using the digital platform of the Informatics Department of the Brazilian Unified Health System (Datasus, as per its abbreviation in Portuguese), which is part of the Ministry of Health, on December 5, 2021. The accessed item was “Notifiable diseases”, followed by “2007 onwards”, via TabNet, a tabulation tool.12 COVID-19 cases confirmed in 2020 were obtained directly from the CORONAVÍRUS BRASIL panel, updated by the Health Surveillance Secretariat8. Confirmed cases in patients who did not live in Maranhão were excluded. The estimated population was obtained from projections for all the years from 2015 to 2020 by the Brazilian Institute of Geography and Statistics.
Data analysis
Data were analyzed by using the P-score metric, which was originally developed to assess mortality increase. However, it proved useful for identifying the underreporting of events in public health.13 P-score is defined as the percentage difference between the reported number of cases or incidence and the expected number of cases or incidence divided by the reported number of cases or incidence, which is then multiplied by 100. The expected value was considered the average in the period from 2015 to 2019, previous to the COVID-19 pandemic. Incidence was obtained by dividing the number of annual cases in Maranhão or its health regions by the number of people and then multiplying the value by 100,000. The results were expressed as positive and negative percentage values, which indicated increase and reduction, respectively. Office Excel software (Microsoft Corporation) version 2016 was used to treat the data.
Ethical aspects
The present study used secondary aggregate data, with no identification of any patients. Therefore, the proposal did not require approval by a research ethics committee. The study was conducted in accordance with the ethical standards imposed by Ministry of Health Resolutions 466/2012, 510/2016, and 580/2018. The principles of the Declaration of Helsinki were also observed.
RESULTS
Between 2015 and 2020, 7,886 new TL cases were reported in Maranhão, of which 72.9% (5,747) occurred in the male population. For 2020, 1,346 new cases were expected (18.9 per 100 thousand people). However, the actual number was 1,158 (16.3 per 100 thousand people). This meant a reduction of 13.94% in the number of new cases and 14.57% in incidence. The highest drop in the number of new cases was observed in women (-24.34%). The probable number of undiagnosed cases for 2020 was 188 (Figure 2).

Analysis of the absolute numbers of the health regions indicated that São Luís (-69.63%), São João dos Patos (-54.02%), Presidente Dutra (-45.95%), and Codó (-41.56%) showed a decrease in the number of reported new cases. The health region of Viana experienced an 80% increase in the number of reported cases in comparison with the expected number for the same period (Figure 3).

Seven health regions (Açailândia, Bacabal, Pedreiras, Rosário, Santa Inês, Timon, and Viana) had an increase in the number of reported TL cases over the pandemic year of COVID-19 (2020) in comparison with the pre-pandemic period examined in the present study (2015-2019). Analysis of TL incidence in 2020 showed that the health regions most affected by this disease were Açailândia, Rosário, and Zé Doca (Table 1).
| Health regions | 2015-2019 (n) | 2020 (n) | Difference (n) | % | Incidence per 100,000 people (2020) |
| Açailândia | 116 | 139 | 23 | 54.51 | 46.37 |
| Bacabal | 55 | 77 | 22 | 58.33 | 28.54 |
| Balsas | 21 | 20 | -1 | 48.78 | 8.77 |
| Barra do Corda | 46 | 39 | -7 | 45.88 | 16.61 |
| Caxias | 28 | 27 | -1 | 49.09 | 8.79 |
| Chapadinha | 92 | 60 | -32 | 39.47 | 15.74 |
| Codó | 30 | 17 | -13 | 36.17 | 5.47 |
| Imperatriz | 98 | 72 | -26 | 42.35 | 13.21 |
| Itapecuru Mirim | 129 | 84 | -45 | 39.44 | 21.65 |
| Pedreiras | 44 | 63 | 19 | 58.88 | 28.75 |
| Pinheiro | 75 | 74 | -1 | 49.66 | 18.53 |
| Presidente Dutra | 36 | 19 | -17 | 34.55 | 6.52 |
| Rosário | 121 | 135 | 14 | 52.73 | 44.48 |
| Santa Inês | 116 | 130 | 14 | 52.85 | 32.85 |
| São João dos Patos | 50 | 19 | -31 | 27.54 | 7.69 |
| São Luís | 57 | 24 | -33 | 29.63 | 1.64 |
| Timon | 12 | 24 | 12 | 66.67 | 9.55 |
| Viana | 5 | 8 | 3 | 61.54 | 2.91 |
| Zé Doca | 203 | 122 | -81 | 37.54 | 40.25 |
DISCUSSION
The data on reported TL cases showed a higher predominance of new cases in men and a remarkable reduction in disease reporting over 2020, especially in the health regions in the north and south areas of Maranhão. The COVID-19 pandemic interfered with the timely diagnosis of other infectious diseases all over the world in 2020, especially those caused by vectors, such as dengue fever, malaria, and leishmaniases (both visceral and tegumentary).14,15,16 Maranhão had its first COVID-19 report on March 19, 2020, and was one of the first Brazilian states to implement lockdown and social distancing measures.17,18
Social restraints and isolation as a response to the increase in COVID-19 cases were a considerable logistic challenge to health surveillance services and impacted the underreporting of other infectious diseases, including TL.19 With the pandemic dissemination, the P-score metric became an important analysis tool that helps elucidate the consequences of COVID-19 for health services, since it allows a comparison of a certain disease status between municipalities, states, and countries.20
The female gender showed the highest potential drop in a number of reported new cases, and the male gender had the highest TL incidence. Tropical vector-borne diseases, such as TL, tend to afflict certain groups in situations of social vulnerability, that is, more susceptible to poverty.21 COVID-19 unevenly affects poorer men and women, increasing existing inequalities.22 Maranhão is considered the poorest state in Brazil.23 Therefore, neglecting the impact of sexual differences in health records can reinforce healthcare inequalities and reduce the efficacy of interventions.24,25
It is important to emphasize that permanent disfiguring scars, which occur when diagnosis is not timely, cause lifelong stigma and decrease quality of life. They are more harmful to women in situations of social vulnerability.26
Disease underreporting already existed before the COVID-19 pandemic. Dealing with this problem involves a complex process of getting to understand the coverage level of health surveillance services, as well as aspects related to management, interaction with healthcare teams, factors inherent in the identification of suspected cases, and timely diagnosis.27
Maranhão has a high TL burden, and the management of the disabilities and deformities caused by this disease is always an urgent matter.28 An absent or delayed diagnosis means reinforcing its stigma as a neglected tropical disease. In a context in which attention was focused on COVID-19, an assessment of the actual impact of TL control measures can be designed by analyzing reported new cases, with special emphasis on the detection delay period.29
The present study had limitations inherent in the use of secondary data, which is subject to incompleteness, transcription errors, and duplicity. P-score quality depends on the accuracy of the available data.30 However, it is important to stress the continuous updating of Sinan over the past years, which helped consolidate this system as the most important source of information/decision-making/action related to diseases in Brazil.31
Dealing with the COVID-19 pandemic was a challenge regarding reporting of new TL cases in Maranhão, mainly in the health regions of São Luís and São João dos Patos. In this context, it is important that health services, once back to their routine activities, be encouraged to intensify actions oriented toward TL prevention, active screening, diagnosis, and treatment.
REFERENCES
1. Kumar A, Singh R, Kaur J, et al. Wuhan to world: the COVID-19 pandemic. Front Cell Infect Microbiol 2021; 11: 1-21. https://doi.org/10.3389/fcimb.2021.596201.
2. Carlos WG, Dela-Cruz CS, Cao B, et al. Novel Wuhan (2019-nCoV) Coronavirus. Am J Respir Crit Care Med 2020; 201(4): P7-P8.
3. Hu Z, Ge Q, Li S, et al. Forecasting and evaluating multiple interventions for COVID-19 worldwide. Front. Artif. Intell. 2020; 3: 1-11. https://doi.org/10.3389/frai.2020.00041.
4. Kim J, Chung Y, Jo HJ, et al. Identification of coronavirus isolated from a patient in Korea with COVID-19. Osong Public Health Res Perspect 2020; 11(1): 3-7. https://doi.org/10.24171/j.phrp.2020.11.1.02.
5. Thompson D, Barbu M, Beiu C, et al. The impact of COVID-19 pandemic on long-term care facilities worldwide: an overview on international issues. Biomed Res Int 2020. https://doi.org/10.1155/2020/8870249.
6. Paudel V. Tele-dermatology in clinical management of suspected cutaneous leishmaniasis in COVID-19 pandemic. Nepal Journal of Dermatology, Venereology & Leprology 2020; 18(1): 91-92.
7. Allahverdi S, Koruk I. Changes In Psychosocial Status And Quality Of Life In Pediatric Patients With Cutaneous Leishmaniasis. Eur. J. Public Health 2021; 31 (Supl 3): iii225- iii226.
8. BRASIL. Ministério da Saúde (2021). Secretaria de Vigilância à Saúde. Guia de vigilância epidemiológica: painel coronavírus [Internet]. Brasília: Ministério da Saúde; [cited 2021 Jun 24]. Available from: https://covid.saude.gov.br.
9. Almeida JS, Cardoso JA, et al. Epidemiological characterization of COVID-19 cases in Maranhão: A brief analysis. Rev Infec e Saúde 2020;6:10477. https://doi.org/10.26694/repis.v6i0.10477.
10. Instituto Brasileiro de Geografia e Estatística. IBGE (2020). Censo 2010. Brasília: Instituto Brasileiro de Geografia e Estatística; [cited 2021 Jun 5]. Available from: https://cidades.ibge.gov.br/brasil/ma/maranhão.
11. Secretaria de Estado do Planejamento e Orçamento. SEPLAN (2022). Regionalização da Saúde; [cited 2022 Feb 5]. Available from: https://seplan.ma.gov.br/uploads/seplan/docs/regionalizacao_saude_ma.pdf.
12. Sistema de Informação de Agravos de Notificação. Leishmaniose tegumentar americana – casos confirmados notificados no Sistema de Informação de Agravos de Notificação (Sinan) – Maranhão; [cited 2023 Oct 9]. Available from: http://tabnet.datasus.gov.br/cgi/deftohtm.exe?sinannet/cnv/ltama.def.
13. Souza MR, Paz WS, Sales VBS, et al. Impact of the COVID-19 Pandemic on the Diagnosis of Tuberculosis in Brazil: Is the WHO End TB Strategy at Risk? Front. Pharmacol 2022; 13: 891711. https://doi.org/10.3389/fphar.2022.891711.
14. Steffen R, Lautenschlager S, Fehr J. Travel restrictions and lockdown during the COVID-19 pandemic – impact on notified infectious diseases in Switzerland. J Travel Med 2020; 27 (8): 1-3. https://doi.org/10.1093/jtm/taaa180.
15. Reegan AD, Gandhi MR, Asharaja AC, et al. COVID-19 lockdown: impact assessment on Aedes larval indices, breeding habitats, effects on vector control programme and prevention of dengue outbreaks. Heliyon 2020; 6 (10):e05181. https://doi.org/10.1016/j.heliyon.2020.e05181.
16. Bağci ÖU. Impact of the COVID-19 duration on neglected parasitic diseases. Turkiye parazitolojii dergisi 2021; 45 (4): 317-325. https://doi.org/10.4274/tpd.galenos.2021.25744.
17. Silva AAM, Lima-Neto LG, Pedrozo-e-Silva CM, et al. Population-based seroprevalence of SARS-CoV-2 is more than halfway through the herd immunity threshold in the State of Maranhão, Brazil. medRxiv 2020. https://doi.org/10.1101/2020.08.28.20180463.
18. Oliveira BLCA, Campos MAG, Queiroz RCS, et al. Prevalence and factors associated with covid-19 vaccine hesitancy in Maranhão, Brazil. Rev. Saúde Pública 2021; 55: 1-12. https://doi.org/10.11606/s1518-8787.2021055003417.
19. Ganesan B, Al-Jumaily A, Fong KNK, et al. Impact of Coronavirus Disease 2019 (COVID-19) Outbreak Quarantine, Isolation, and Lockdown Policies on Mental Health and Suicide. Front. Psychiatry 2021; 12: 565190. https://doi.org/10.3389/fpsyt.2021.565190.
20. Paz WS, Souza MR, Tavares DS, et al. Impact of the COVID-19 pandemic on the diagnosis of leprosy in Brazil: An ecological and population-based study. Lancet Reg Health Am 2022; 9: 100181. https://doi.org/10.1016/j.lana.2021.100181.
21. Weld ED, Waitt C, Barnes K, et al. Twice neglected? Neglected diseases in neglected populations. Br. J. Clin. Pharmacol. 2022; 88(2): 367-373. https://doi.org/10.1111/bcp.15148.
22. Buheji M, Cunha KC, Beka G, et al. The Extent of COVID-19 Pandemic Socio-Economic Impact on Global Poverty. A Global Integrative Multidisciplinary Review. Am. J. Econ. 2020; 10 (4): 213-224. https://doi.org/10.5923/j.economics.20201004.02.
23. Maas LWD, Assis LML, Tomás MC, et al. A pobreza no Maranhão: uma análise com base na perspectiva multidimensional. Soc. estado. 2022; 37 (2):407-433. https://doi.org/10.1590/s0102-6992-202237020002.
24. Patel JA, Nielsen FBH, Badiani AA, et al. Poverty, inequality and COVID-19: the forgotten vulnerable. Public Health 2020; 183: 110-111. https://doi.org/10.1016/j.puhe.2020.05.006.
25. García GSM, Souza EA, Araújo VM, et al. Territory, neglected diseases and the action of community and endemic combat agents. Rev. Saúde Pública 2022; 56: 27. https://orcid.org/0000-0002-0884-4721.
26. Grifferty G, Shirley H, McGloin J, et al. Vulnerabilities to and the Socioeconomic and Psychosocial Impacts of the Leishmaniases: A Review. Res. rep. trop. med. 2021; 12: 135- 151. https://doi.org/10.2147/RRTM.S278138.
27. Souza-Melo MAS, Silva LLM, Melo ALS, et al. Subnotificação no Sinan e fatores gerenciais e operacionais associados: revisão sistemática da literatura. Revista de Administração da UEG 2018; 9 (1): 26-43.
28. Farias FJAS, Silva EDC, Silva SA, et al. Epidemiological profile of American tegumentary leishmaniasis in the state of Maranhão in recent years. Revista Multidisciplinar em Saúde 2021; 2 (3). https://doi.org/10.51161/rems/1395.
29. Mazaherifar S, Solhjoo K, Abdoli A. Outbreak of cutaneous leishmaniasis before and during the COVID-19 pandemic in Jahrom, an endemic region in the southwest of Iran. Emerg. microbes & infect 2022; 11(1): 2218-2221. https://doi.org/10.1080/22221751.2022.2117099.
30. Bando DH, Rodrigues LA, Biesek L, et al. Spatial patterns and epidemiological characterization of suicides in the Chapecó micro-region, Santa Catarina, Brazil: an ecological study, 1996-2018. Epidemiol. Serv. Saúde 2023; 32(1): e2022593. https://doi.org/10.1590/S2237-96222023000100007.
31. Filho AMS, Vasconcelos CH, Dias AC, et al. Primary Health Care in Northern and Northeastern Brazil: mapping team distribution disparities. Ciênc. saúde coletiva 2022; 27(01): 377-386. https://doi.org/10.1590/1413-81232022271.39342020.