Abstracts

Background

Tuberculosis (TB) continues to be an important public health issue and is still considered the main cause of death by an infectious agent in the world. In 2018, approximately 10 million people around the world became ill and a total of 1.4 million deaths was registered due to TB ¹1. World Health Organization. Global tuberculosis report 2019. https://apps.who.int/iris/bitstream/handle/10665/329368/9789241565714-eng.pdf?ua=1 (accessed on 26/Dec/2019).
https://apps.who.int/iris/bitstream/hand... . In response to this, the World Health Organization (WHO) adopted the End TB Strategy which sets challenging objectives - including the early diagnosis of the disease in high risk groups - to eliminate the epidemic worldwide ²2. World Health Organization. Global strategy and targets for tuberculosis prevention, care and control after 2015. https://apps.who.int/iris/handle/10665/162760 (accessed on 16/Dec/2019).
https://apps.who.int/iris/handle/10665/1... . Among the high risk groups, the Indigenous population presents the highest prevalence of TB ³3. Tollefson D, Bloss E, Fanning A, Redd JT, Barker K, McCray E. Burden of tuberculosis in indigenous peoples globally: a systematic review. Int J Tuberc Lung Dis 2013; 17:1139-50.. This could be explained by accelerated social and cultural changes, higher malnutrition prevalence, and the deficient health care services provided for this high-risk group ⁴4. Lacerda SNB, Temoteo RCA, Figueiredo TMRM, Luna FDT, Sousa MAN, Abreu LC, et al. Individual and social vulnerabilities upon acquiring tuberculosis: a literature systematic review. Int Arch Med 2014; 7:35..

In 2019, Colombia registered 14,684 TB cases and the national incidence rate was 27.3 cases per 100,000 inhabitants. Nationwide, 4.9% of the cases occurred among the indigenous population ⁵5. Instituto Nacional de Salud. Informe de evento: tuberculosis, periodo epidemiológico XIII https://www.ins.gov.co/buscador-eventos/Informesdeevento/TUBERCULOSIS_PE_XIII_2019.pdf (accessed on 26/Jul/2020).
https://www.ins.gov.co/buscador-eventos/... . Cauca is the Colombian department with the second highest proportion of indigenous people; in 2018, this population represented 26.4% of the diagnosed TB cases ⁶6. Gobernación del Cauca. Registros del Programa Departamental de Tuberculosis. Popayán: Gobernación del Cauca; 2017.. The Department of Cauca has, as part of a TB control program, a policy of searching for the respiratory symptomatics (RS), such as persistent cough and sputum production for more than 15 days; the objective is to identify the affected people in the early stages, and provide them with treatment ⁷7. Solari L, Alarcón JO, Piscoya J, Tejada R. Sintomáticos respiratorios en personas atendidas en establecimientos de salud del minsiterio de salud en Lima, Perú. Rev Peru Med Exp Salud Pública 2019; 36:207-13.. These operational activities are conducted by the health care providers of the Colombian Health System ⁸8. Vargas-Zea N, Castro H, Rodríguez-Páez F, Téllez D, Salazar-Arias R. Colombian health system on its way to improve allocation efficiency-transition from a health sector reform to the settlement of an HTA agency. Value Health Reg Issues 2012; 1:218-22..

The screening activities for TB include searching for the RS (through sample collection) and conducting the necessary laboratory studies for diagnoses. The active search for the RS has been promoted as one of the main strategies for the detection of new TB cases in different countries of the Americas; this is done by establishing an indicator based on a targeted number of samples to be collect from RS each year ⁹9. Spagnolo LML, Tomberg JO, Martins MDR, Antunes LB, Gonzales RIC. Detecção da tuberculose: a estrutura da atenção primária à saúde. Rev Gaúch Enferm 2018; 39:e20180157.. It is estimated that RS are prevalent in 5% of the population aged over 15 years who are attended by the health care providers in their outpatient clinics; thus the same number is established as the targeted amount of samples to be collected each year ⁷7. Solari L, Alarcón JO, Piscoya J, Tejada R. Sintomáticos respiratorios en personas atendidas en establecimientos de salud del minsiterio de salud en Lima, Perú. Rev Peru Med Exp Salud Pública 2019; 36:207-13.^,1010. Ministerio de Salud y Protección Social. Lineamiento técnico operativo del Programa Nacional de Tuberculosis. https://www.minsalud.gov.co/Normatividad_Nuevo/Resoluci%C3%B3n%20No.%20227%20de%202020.pdf (accessed on 02/Apr/2020).
https://www.minsalud.gov.co/Normatividad... ^,1111. Romani Romani FR, Roque Henríquez J, Catacora López F, Hilasaca Yngas G. Conocimientos, percepciones y prácticas de personal de salud en la detección de sintomáticos respiratorios en una región de muy alto riesgo de trasmisión de tuberculosis en el Perú. An Fac Med (Perú) 2016; 77:123-7.. The prevalence of RS, however, greatly varies, ranging from 2% to 10% in Colombia, as well as in other countries under similar conditions ¹²12. Daza Arana JE, Cubides Munévar AM, Lozada Ramos H. Prevalencia de sintomáticos respiratorios y factores relacionados en dos territorios vulnerables de Santiago de Cali. Hacia Promoc Salud 2016; 21:63-76.^,1313. Cubides Munevar Á, Daza Arana J, García Puerta M, Zapata Ossa H, Arena Quintana B, Palacio S. Sintomáticos respiratorios desde un enfoque poblacional. Rev Cuba Salud Pública 2018; 44:153-68.^,1414. Moreira CMM, Zandonade E, Lacerda T, Maciel ELN. Sintomáticos respiratórios nas unidades de atenção primária no Município de Vitória, Espírito Santo, Brasil. Cad Saúde Pública 2010; 26:1619-26..

Colombia has yet to achieve its established goals. Only a maximum of 42% of the expected identification of RS has been reached ¹³13. Cubides Munevar Á, Daza Arana J, García Puerta M, Zapata Ossa H, Arena Quintana B, Palacio S. Sintomáticos respiratorios desde un enfoque poblacional. Rev Cuba Salud Pública 2018; 44:153-68.^,1515. Ministerio de Salud y Protección Social. Plan estratégico hacia el fin de la tuberculosis, 2016-2025. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/INEC/INTOR/Plan-estrategico-fin-tuberculosis-colombia-2016-2025.pdf (accessed on 28/Sep/2018).
https://www.minsalud.gov.co/sites/rid/Li... . Additionally, the percentage of positive RS cases for acid-fast bacilli (AFB), collected via smear test, has been decreasing from 3.1%, in 2001, to 1.8%, in 2015 ¹⁶16. Ministerio de Salud y Protección Social. Circular externa n. 000055 de 2016. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/DE/DIJ/circular-externa-55-de-2016.pdf (accessed on 14/Oct/2018).
https://www.minsalud.gov.co/sites/rid/Li... .

In the indigenous population, the amount of RS is conditioned by factors such as housing conditions, public utilities, access to drinking water, and means of transportation ¹⁷17. Aguirre S, Cuellar CM, Herrero MB, Cortesi GC, Romero NG, Alvarez M, et al. Prevalence of tuberculosis respiratory symptoms and associated factors in the indigenous populations of Paraguay (2012). Mem Inst Oswaldo Cruz 2017; 112:474-84.. Moreover, the different meanings attributed to TB, by the indigenous populations, may influence their knowledge, attitudes, and practices toward the disease; possibly affecting the early detection of this disease ¹⁸18. Munoz Sanchez AI, Rubiano Mesa YL. Meanings of "tuberculosis" in rural indigenous communities from a municipality in the Colombian Amazon. Invest Educ Enferm 2017; 35:165-73.. Brazilian health services have documented operational weaknesses associated to the way that local health services are organized for the implementation of systematic routines in the search of RS within indigenous populations ¹⁹19. Nobrega RG, Nogueira JDA, Netto AR, Duarte de Sa L, da Silva ATMC, Villa TCS. The active search for respiratory symptomatics for the control of tuberculosis in the Potiguara Indigenous Scenario, Paraiba, Brazil. Rev Latinoam Enferm 2010; 18:1169-76..

Thus, it is necessary to prioritize search campaigns within vulnerable populations, such as the indigenous groups, in order to improve the indicators ¹⁵15. Ministerio de Salud y Protección Social. Plan estratégico hacia el fin de la tuberculosis, 2016-2025. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/INEC/INTOR/Plan-estrategico-fin-tuberculosis-colombia-2016-2025.pdf (accessed on 28/Sep/2018).
https://www.minsalud.gov.co/sites/rid/Li... . This implies the need for effective, culturally-adapted screening strategies, allowing an increase in the number of identified TB cases ²⁰20. Vyas A, Creswell J, Codlin AJ, Stevens R, Rao VG, Kumar B, et al. Community-based active case-finding to reach the most vulnerable: tuberculosis in tribal areas of India. Int J Tuberc Lung Dis 2019; 23:750-5..

This study aimed to evaluate the implementation process and the screening for pulmonary tuberculosis (PTB) within the Indigenous population of the Department of Cauca, from 2016 to 2018, to identify possible barriers in the implementation of the identifying strategies of new PTB cases.

Methods

Study design

A mixed methodology was used with a sequential explanatory design. In the first phase, screening indicators for PTB within the Department of Cauca’s indigenous population were estimated and created. In the second phase, with a qualitative approach, we attempted to explain the findings of the first phase, based on the health care providers perspective ²¹21. Creswell J, Plano V. Designing and conducting mixed methods research. 2nd Ed. Thousand Oaks: SAGE; 2011..

Study location

The study was conducted within the Department of Cauca, located in the Southwestern Colombia. In this region, 21% of its inhabitants are self-reported indigenous people. The department also has the second highest number of indigenous population in Colombia ²²22. Departamento Administrativo Nacional de Estadística. Grupos étnicos. https://www.dane.gov.co/index.php/estadisticas-por-tema/demografia-y-poblacion/grupos-etnicos (accessed on 21/Oct/2018).
https://www.dane.gov.co/index.php/estadi... . Within this population some tribes are highly acknowledge, such as the Nasa tribe, located in the Northern, the Northeastern, and the Eastern area of the department. Other noteworthy tribe within the department are the Misak tribe, located in the Eastern area; the Yanaconas tribe, towards the South; the Kokonucos tribe, towards the central part of the department; the Ingas, in the Southern end; the Totoroes in the Eastern; and the Eperara-Siapidara people, in the Western area ²³23. Gobernación del Cauca. Análisis de situación de salud con el modelo de los determinantes sociales de salud del Departamento del Cauca. https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/ED/PSP/asis-cauca-2019.zip (accessed on 26/Jul/2020).
https://www.minsalud.gov.co/sites/rid/Li... .

Participants

In the first phase, the indigenous population from the Department of Cauca who tested positive for PTB, during 2016-2018, were included. In the second phase, an extreme case sampling process was conducted. In this sample, the health care providers with the highest (n = 4) and lowest (n = 5) incidence of PTB in the indigenous population during the timeframe of the study were included ²⁴24. Ulin P, Robinson E, Tolley E. Investigación aplicada en salud pública: métodos cualitativos. Washington DC: Organización Panamericana de la Salud; 2006.. For each healthcare institution, the coordinators and assistants of the TB program were selected. Nine program coordinators and 11 nursing assistants from eight selected municipalities, which included both state-managed health care providers and indigenous-managed health care providers, were interviewed. These types of health care providers institutions differ on administrative aspects and on the services provided. The state-managed health care providers institutions are public, whereas the indigenous-managed health care providers institutions belong to the indigenous tribes. Additionally, in the latter, some elements of traditional medicine, such as provision of plant-based medicines and rituals performed by traditional healers, are included in their health care service model.

Variables and data collection

Three indicators were elaborated to assess the PTB screening process conducted by the Department of Cauca within its indigenous population: (i) percentage of RS identified by health services; (ii) percentage of RS examined by health services; and (iii) positivity index of the AFB smear test. The percentage of RS identified by the health services was defined as the number of people categorized as RS (via active and passive search) over the total amount of RS expected. The percentage of RS that were examined was calculated as the number of identified patients with at least one AFB smear divided by the total amount of RS identified. Finally, the positivity index of the AFB smear test was defined as the amount of RS and at least one positive AFB smear test divided by the total of RS that were examined by the health services ²⁵25. Malacarne J, Heirich AS, Cunha EAT, Kolte IV, Souza-Santos R, Basta PC. Performance of diagnostic tests for pulmonary tuberculosis in indigenous populations in Brazil: the contribution of rapid molecular testing. J Bras Pneumol 2019; 45:e20180185..

The expected amount of RS corresponds to the overall prevalence of RS for this population, estimated through population projections by calculating 2.5% of the total indigenous population over 15 years of age, according to the guidelines of the TB national program ¹⁰10. Ministerio de Salud y Protección Social. Lineamiento técnico operativo del Programa Nacional de Tuberculosis. https://www.minsalud.gov.co/Normatividad_Nuevo/Resoluci%C3%B3n%20No.%20227%20de%202020.pdf (accessed on 02/Apr/2020).
https://www.minsalud.gov.co/Normatividad... . The RS identified by the health services were estimated by applying the percentage of the indigenous population to the total of identified RS in the general population. The RS who were examined by the health services were estimated by applying the proportion of indigenous population to the total of RS examined in the general population.

The type of health insurance of the patients diagnosed with PTB was registered. The subsidized, contributive, and special insurance correspond to people who are insured by the state or with their own resources, respectively. Those uninsured are people who are not covered by the health insurance system; diagnostic and treatment activities, however, are covered by the state.

All indicators were estimated with aggregate data from the Colombian National Administrative Statistics Department ²²22. Departamento Administrativo Nacional de Estadística. Grupos étnicos. https://www.dane.gov.co/index.php/estadisticas-por-tema/demografia-y-poblacion/grupos-etnicos (accessed on 21/Oct/2018).
https://www.dane.gov.co/index.php/estadi... , and the records from the TB control program of the Department of Cauca. All the consulted databases were unified in a single spreadsheet on Microsoft Excel (https://products.office.com/).

For the second phase, the perceptions of key agents on the implementation of the screening process of RS were explored by semi-structured interviews ²⁴24. Ulin P, Robinson E, Tolley E. Investigación aplicada en salud pública: métodos cualitativos. Washington DC: Organización Panamericana de la Salud; 2006.. Field work was carried out by staff trained in Social Sciences who were knowledgeable about the screening process and external to the TB program in the region.

Analysis of the information

Absolute and percentage frequencies of the social and demographical characteristics were reported (sex, age at diagnosis, corresponding case municipality, and health insurance), as well as related program (HIV coinfection, notification period, program entering conditions, and AFB smear result) of the indigenous RS who had a positive AFB smear test during the study period. The cases in which the AFB smear test was positive for PTB were geographically referenced to the corresponding municipality and the belonging indigenous tribe. The screening indicators within the indigenous population were estimated and reported in percentages. For the analysis of the data, Microsoft Excel and statistical package Stata 14 (https://www.stata.com) were used.

In the qualitative phase a thematic analysis was performed ²⁶26. Fereday J, Muir-Cochrane E. Demonstrating rigor using thematic analysis: a hybrid approach of inductive and deductive coding and theme development. Int J Qual Methods 2006; 5:80-92.. The audio recordings were transcribed verbatim in Microsoft Word (https://products.office.com/). Then, the transcriptions were coded and analyzed through the Atlas.ti program, version 8 (http://atlasti.com/). A previously defined code book was created according to prior identified categories for the RS screening and were included in the semi-structured interviews guide. The codes used for the current analysis are: contact with health services, planning of the search, and implementation of the planned strategies. The creation of emerging codes was allowed ²⁷27. Hernández R, Fernández C, Baptista P. Metodología de la investigación. 5th Ed. México DF: McGraw-Hill; 2010.. Finally, the integration and triangulation between the results of the indicators and the qualitative findings were performed ²¹21. Creswell J, Plano V. Designing and conducting mixed methods research. 2nd Ed. Thousand Oaks: SAGE; 2011..

To report the qualitative results and to maintain confidentiality, the letter “C” was assigned to the personnel who coordinates the program, letter “A” to the assistant personnel, followed by letter “S” or “I” depending on the type of health care providers (“S” for State-managed health care providers and “I” for an indigenous-managed health care providers). The letters “H” or “L” were then assigned if there was a high incidence or low incidence within the municipality, and finally a corresponding consecutive number was assigned in the order in which the key agents were interviewed.

Ethical considerations

The study was approved by the Research Ethics Committee of the National Faculty of Public Health of the University of Antioquia and exonerated of revision by the Ethics Revision Committee of the Pan-American Health Organization (PAHOERC).

Results

During the study period, 123 cases tested positive for PTB in the AFB smear test within the indigenous population of the Department of Cauca. In total, 34 cases of PTB, not confirmed by the AFB smear test, were excluded. According to the indigenous people, 71.5% (n = 88) acknowledged themselves as Nasa people.

In total, 61% (n = 75) were men and the median age was 40 years (IQR: 25-61). The highest amount of cases were diagnosed in 2017 (n = 52); 93.5% (n = 115) of patients were covered by the subsidized insurance; and 92.7% (n = 114) were new cases. In 30.1% (n = 37) of the cases, the diagnosis by AFB smear test was observed with more than 10 bacillus (Table 1).

Figure 1 shows the geographical distribution of the cases in the indigenous population. The cases were mostly distributed in the Northeastern area of the department, predominantly by the Nasa indigenous tribe. Toward the West, cases were registered in the Eperara-Siapidara tribe.

From the total of expected RS in indigenous population (n = 16,711), the health care providers were able to identify 42.3%, and from these identified RS (n = 7,064), they were able to examine 93.2% with at least one AFB smear diagnosis. The positivity index for the AFB smear test reported for the indigenous population during the study period was 1.87% (Table 2).

Explanations of the results of the implementation of the screening process in PTB

Indicator 1: percentage of RS identified

Goal of RS perceived as overestimated: among most interviewees there is a perception that the targeted amount for RS is overestimated, making it difficult to comply with the established goals.

“...here we have never been able to reach the goal, at least since I’ve been working here, we have never been able to (...) actually yes; the goal is a bit too high for the population and that is also why we haven’t been able to reach it” (ASH03).

Insufficient personnel for search: the effective personnel of health care providers institution are insufficient to complete all the activities that are assigned to them, resulting in a perceived work overload. This leads them to prioritize other activities, such as vaccination and follow-ups of pregnant women and children. Thus, the search for RS is delayed or is passively carried out.

“...the biggest difficulty is that one, who supports us to do the search?, because we have cases, we know who, we know where we can go, we also did a study, we know which are the areas where there have been more cases that we can go visit, but we don’t have anybody to do the visit, nobody to do what needs to be done, that’s what we are missing” (CSH01).

High search costs in areas of difficult geographical access: in some cases, the interviewed coordinating personnel stated that the costs generated in the search of RS exceed the perceived economic return on the health insurance’s part. This occurs more frequently in municipalities where roads are scarce or in which the access is by river.

“...generally, there are more than 300 people who live in that zone and is the place with the most tuberculosis cases, we’ve even had deaths due to tuberculosis, even though it’s true that the cost is equivalent to land transportation, by river you also have to walk and that takes an entire day” (CSH09).

Requesting permissions from the indigenous authorities: in order to search for RS, it is necessary to have consent from the indigenous authorities, hampering some State-managed health care providers actions, sometimes not been able to obtain permission or taking too long to obtain it.

“...it’s there where we can’t cross their paths, because there is an Indigenous reservation (...) and it’s there where most of the cases are, but it’s also there where we are not allowed to cross” (CSL02).

Stigma and fear of TB diagnosis: among the testimonies it is mentioned that on some occasions, people are used to denying symptoms when inquired about them. This is due to the TB stigma that remains among the indigenous tribes. The fear of being rejected by their peers makes people afraid of being diagnosed with TB.

“...they [people with TB] may mistrust us, no! If this staff member [program assistant] found out that I have the disease, she is going to tell, since she is going to visit such village, she is going to tell the neighbors, and like this, so they have the doubt as to how are they going to receive me, are they going to set me aside? Are they going to discriminate against me? Anyhow!” (AIL01).

Traditional medicine, self-medication, and beliefs: for most interviewees, practices that hinders the identification of RS includes the manufacturing of homemade remedies, infusions from plants, and the potential visit to the traditional healers. In the indigenous health care providers this kind of practices are reinforced by their health providing model. Self-medication is also an easily accessible first resort, before consulting a physician.

“...the farther the area is from the downtown, the more they believe on ancestral wisdom, they prefer using plants and all that, is only when they continue feeling sick that they seek a medical consultation” (CIL04).

Indicator 2: percentage of examined RS

Aversion to sputum collection: according to what the key agents said, the collection of the three sputum smears to be examined poses a challenge. This is due to the dislike or disgust provoked by the collection of sputum and the containers meant for doing so.

“...they [people with TB] feel embarrassed to collect the sputum because they have always told me that they don’t want to collect that ugly sputum, they’ve always told me that” (ASH08).

Mistrust towards non-indigenous health staff: despite language not being a barrier for communication among the interviewees, it’s easier for the indigenous individual to trust and to express everything they want or feel with someone who speaks their own language. When the information is laid out by an indigenous person, it is better received and better accepted than when it is laid out by a health worker who does not belong to their communities.

“...they express better in their language, then they do speak out their minds but for them to do the same with the physician, they can’t express themselves the same and say everything that is happening to them” (AIH02).

Indicator 3: positivity index

Incorrect identification of RS: in the interviews we identified that the assistants take smears from people who do not meet the RS criteria, regarding cough and expectoration for more than 15 days. This situation might be motivated by the necessity to meet the monthly goals that are imposed by the health care providers institution. Consequently, resources are lost, some smears are of poor quality, and there is fatigue among the personnel in charge of analyzing the AFB smear.

“...if the person has some symptoms, cough for more than three days, the phlegm, then we do the collection. And the same goes for the other people who are symptomatic, those who we can see are coughing a lot, for more than three days, then we ask them for the smear” (AIL04).

“...they [nursing assistants] generally - to comply with the goals - and I emphasize to them, they bring me a lot of saliva and I tell them that we have to get the ones who truly are symptomatic, not just to comply with the goal, I am going to capture anybody and they are going to bring me smears that are not going to be worth and I’ll waste supplies and time” (CIL04).

Failures in the collection and transportation of smears: the staff coordinating the program acknowledges flaws in the technique used for fixation and extensions of the smears in the slides, thus making it difficult to process them. Besides, the conditions under which the smears are transported do not guarantee clear readings by the health care providers labs.

“The transportation of the smears is done in an archaic fashion, we do not have a special container set to certain temperature. It has happened to us that the assistant did collect the smears, arrived at the hospital and they were tipped over, so they were worthless” (CSL02).

No differences were found in the testimonies of the interviewees from municipalities with high and low incidence of TB or between the State-managed and indigenous-managed health care providers.

Discussion

This study made us aware of the possible barriers in the strategies used for the screening process of the TB control program, within the indigenous population of the Department of Cauca, during 2016-2018. The percentage of identified RS and the positivity index of the AFB smear test were the indicators with the lowest performance. The low percentage of identified RS might be explained by the stipulation of overestimated goals; insufficient personnel to conduct active searches; high costs to reach areas of difficult access; need for permissions from Indigenous authorities; culturally ingrained stigma; use of traditional medicine and self-medication; and the patients’ personal beliefs. While the low positivity index of the AFB smear test may be explained by other barriers, such as incorrect RS identification and failures in the collection and transportation of smears.

A study conducted in Paraguay ¹⁷17. Aguirre S, Cuellar CM, Herrero MB, Cortesi GC, Romero NG, Alvarez M, et al. Prevalence of tuberculosis respiratory symptoms and associated factors in the indigenous populations of Paraguay (2012). Mem Inst Oswaldo Cruz 2017; 112:474-84., in 19 indigenous communities, reported a RS prevalence of 5.7%. Another study, conducted in the Department of Vaupés (Colombia) ²⁸28. García I, De la Hoz F, Reyes Y, Montoya P, Guerrero MI, León CI. Prevalencia de sintomáticos respiratorios, de infección y enfermedad tuberculosa y factores asociados: estudio basado en población, Mitú, Vaupés, 2001. Biomedica 2004; 24:124-31., reported a RS prevalence of 4.4% (95%CI: 2.9-6.7) within their indigenous population. Our findings suggest that the percentage of expected RS within the indigenous population in Colombia would be underestimated (2.5%). However, operational staffs think otherwise. In 2020, the program guidelines were updated to contemplate the idea of adjusting the RS identification goal, considering the sample collection history of the regions ¹⁰10. Ministerio de Salud y Protección Social. Lineamiento técnico operativo del Programa Nacional de Tuberculosis. https://www.minsalud.gov.co/Normatividad_Nuevo/Resoluci%C3%B3n%20No.%20227%20de%202020.pdf (accessed on 02/Apr/2020).
https://www.minsalud.gov.co/Normatividad... . This might contribute to readjusting the goal of the RS indicator according to each context. Furthermore, community-wide active search strategies must be strengthened and continued. In countries like India, the active search strategies, by community health care workers, have proven successful within indigenous population ²⁰20. Vyas A, Creswell J, Codlin AJ, Stevens R, Rao VG, Kumar B, et al. Community-based active case-finding to reach the most vulnerable: tuberculosis in tribal areas of India. Int J Tuberc Lung Dis 2019; 23:750-5.. These models are similar to the ones in which nursing assistants remain on field and is usually the model adopted by the health care providers that are run by indigenous tribes in the Department of Cauca.

It is known that scarcity of health providing personnel or their lack of continuity in the program often affects the activities associated to the TB control programs; all of which influences the perception that users have regarding the quality of the health services that they receive ²⁹29. Marahatta SB, Yadav RK, Giri D, et al. Barriers in the access, diagnosis and treatment completion for tuberculosis patients in central and western Nepal: a qualitative study among patients, community members and health care workers. PLoS One 2020; 15:e0227293.. Additionally, we also have to consider the lack of financial resources, facilities, and supplies that health providers usually face ³⁰30. Ereso BM, Yimer SA, Gradmann C, Sagbakken M. Barriers for tuberculosis case finding in Southwest Ethiopia: a qualitative study. PLoS One 2020; 15:e0226307.. Keeping all of this in mind, the scarcity of financial resources, which may be due to the high expenses associated with conducting the search in areas of difficult access, was identified as a possible explanation for the low percentage of RS identified. This coincides with the geographical distribution observed in our findings in which indigenous people, such as the Eperara-Siapidara and the Inga, find themselves in zones of difficult access within the Department of Cauca. Moreover, most cases diagnosed with TB are covered by an insurance that is subsidized by the State, reflecting the indigenous population’s limited ability to pay.

Stigma and fear of being diagnosed with TB are important factors that restrict the ability to comply with the program activities. In Uganda, 30.6% of the patients were found to hide their diagnosis from their families and that up to 12.3% of them suffered negative experiences due to severe stigmatization ³¹31. Nyangoma M, Bajunirwe F, Atwine D. Non-disclosure of tuberculosis diagnosis by patients to their household members in south western Uganda. PLoS One 2020; 15:e0216689.. Fear of TB diagnosis in indigenous people is influenced by negative experiences lived within the activities of TB control program and by beliefs on the origin of the disease ²⁹29. Marahatta SB, Yadav RK, Giri D, et al. Barriers in the access, diagnosis and treatment completion for tuberculosis patients in central and western Nepal: a qualitative study among patients, community members and health care workers. PLoS One 2020; 15:e0227293.. In the local context, the authorities of the Arhuaco tribe in Sierra Nevada of Santa Marta report fear of TB diagnosis, since they perceive the activities of TB control program as a threat to their culture ³²32. Organización Panamericana de la Salud. Enfoque intercultural: prevención de la tuberculosis en pueblos indígenas. Washington DC: Organización Panamericana de la Salud; 2009.. Additionally, fear of TB infection can affect relationships between health workers, patients and their families, and the community ³³33. Ascuntar JM, Gaviria MB, Uribe L, Ochoa J. Fear, infection and compassion: social representations of tuberculosis in Medellin, Colombia, 2007. Int J Tuberc Lung Dis 2010; 14:1323-9.. These factors request for the health system agents to work harder in order to implement strategies to reduce stigmatization around TB since, as shown in this study, it becomes a barrier for RS identification. These strategies should be directed not only at the community but also at the health care providers, minimizing attitudes that may generate stigma. The staff should include those who speak the native language, since communication in their own language generates more confidence, in agreement with what was reported by the interviewees.

Usually, the first option is looking for relief of TB symptoms in traditional medicine before doing so in Western medicine ²⁹29. Marahatta SB, Yadav RK, Giri D, et al. Barriers in the access, diagnosis and treatment completion for tuberculosis patients in central and western Nepal: a qualitative study among patients, community members and health care workers. PLoS One 2020; 15:e0227293.^,3434. Nogueira LMV, Teixeira E, Basta PC, Motta MCS. Therapeutic itineraries and explanations for tuberculosis: an indigenous perspective. Rev Saúde Pública 2015; 49:96.. Traditional healers are people who are acknowledge as such by their community and their knowledge in the treatment of diseases is based on the oral tradition from generation to generation, without formal training in medicine. Evidence shows that 80% of the patients visit indigenous traditional healers before reaching out to a hospital ³⁵35. Gumede MV. Traditional healers: a medical practitioner's perspective. Johannesburg: Skotaville; 1990.. Beliefs around the disease may include abstract explanations, such as a form of punishment or a disease of the spirit ³⁴34. Nogueira LMV, Teixeira E, Basta PC, Motta MCS. Therapeutic itineraries and explanations for tuberculosis: an indigenous perspective. Rev Saúde Pública 2015; 49:96.. In this study, the use of traditional medicine, self-medication, and belief practices were also identified in the testimonies of the people interviewed. Not only does these practices hinder the rate of RS identification but they also become risk factors due to the delay in diagnosis ³⁶36. Storla DG, Yimer S, Bjune GA. A systematic review of delay in the diagnosis and treatment of tuberculosis. BMC Public Health 2008; 8:15..

One study, conducted in regions with a high risk of transmission in Peru, has reported that 99.3% of the total RS identified are examined with AFB smear test and the diagnostics performance of the test reaches 1.5% ³⁷37. Roque-Henríquez J, Catacora-López F, Hilasaca-Yungas G, Romaní-Romaní F. Evaluation of tuberculosis detection indicators in a region with high risk of transmission in Peru. Rev Peru Med Exp Salud Pública 2015; 32:504-8.; similar to our results. Note that, for the indicator of RS examined, at least one AFB smear test was considered (out of the three that are usually performed). On the other hand, a RS prevalence of 4.8% has been observed in indigenous communities from Brazil; however, the positivity index of the AFB smear test from RS was 3.7% ²⁵25. Malacarne J, Heirich AS, Cunha EAT, Kolte IV, Souza-Santos R, Basta PC. Performance of diagnostic tests for pulmonary tuberculosis in indigenous populations in Brazil: the contribution of rapid molecular testing. J Bras Pneumol 2019; 45:e20180185.. This reduction in the positivity index of the AFB smear test might be explained by the findings associated with the incorrect identification of the RS and the failures in the collection and transportation of the smears. Our study found that in some cases the criterion for cough with expectoration for more than 15 days was not met for sample collection. This factor negatively affect the quality of the collected samples and their positivity rate. According to the quantitative findings, a lower bacillary index is observed in the Eperara-Siapidara tribe, whose cases were located in the most remote regions and with greater difficulties of access and means of transportation.

The control program for TB does not categorize by ethnicity, those who were RS identified by the health services. That is the reason why we used data from the general population and the estimated proportion of indigenous people in the Department of Cauca ²²22. Departamento Administrativo Nacional de Estadística. Grupos étnicos. https://www.dane.gov.co/index.php/estadisticas-por-tema/demografia-y-poblacion/grupos-etnicos (accessed on 21/Oct/2018).
https://www.dane.gov.co/index.php/estadi... . This represents a limitation on the estimation of the indicators.

Conclusion

This study presented the barriers in the implementation of TB diagnosis programs within the indigenous population, in Cauca, as well as the results of three key indicators for TB detection in the area. The possible overestimation of the TB program goals; the lack of personnel; the lack of resources to reach geographically distant regions; cultural elements, such as the language barrier, stigma, self-medication, use of traditional medicine; and lack of adherence to official norms for samples collection were reported as barriers to the process of search and detection of active cases.

Based on this study we highlight the following recommendations to improve the implementation of the search and detection process for TB in indigenous populations of Colombia: adjust the goals for the identification of RS and diagnosis of TB based on the epidemiological findings reported; include additional data on sample characteristics, such as the indigenous tribe the patient belongs to, to identify risk and vulnerability factors when identifying RS; and improve and strengthen search and detection teams, by implementing interventions that have been successful in similar populations, such as the inclusion of indigenous social promoters, as well as providing culturally acceptable health services, as aspects related to the practice of traditional medicine.

Acknowledgments

We thanks the Pan American Health Organization (PAHO), the Alliance for Health Policy and Systems Research (AHPSR), the Special Training Program in Research of Tropical Diseases (TDR), the Mexican National Institute of Public Health (INSP), the National Faculty of Public Health of the University of Antioquia, and the Governor’s Office of the Department of Cauca - Health Bureau of the Department of Cauca, for the support and political willingness for this project.

References

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