Tuberculosis Knowledge, Attitudes, and Practice in Middle- and Low-Income Countries: A Systematic Review

Tuberculosis (TB) is the leading cause of death from an infectious agent in the world. Most tuberculosis cases are concentrated in low- and middle-income countries. The aim of this study is to better understand tuberculosis-related knowledge about TB disease, prevention, treatment and sources of information, attitudes towards TB patients and their stigmatization and prevention, diagnosis and treatment practices in the general population of middle- and low-income countries, with a high tuberculosis burden, and provide evidence for policy development and decision-making. A systematic review of 30 studies was performed. Studies reporting on knowledge, attitudes, and practices surveys were selected for systematic review through database searching. Population knowledge about TB signs and symptoms, prevention practices, and treatment means was found inadequate. Stigmatization is frequent, and the reactions to possible diagnoses are negative. Access to health services is limited due to difficulties in transportation, distance, and economic cost. Deficiencies in knowledge and TB health-seeking practices were present regardless of the living area, gender, or country; however, it seems that there is a frequent association between less knowledge about TB and a lower socioeconomic and educational level. This study revealed gaps in knowledge, attitude, and practices in focused in middle- and low-income countries. Policymakers could take into account the evidence provided by the KAP surveys and adapt their strategies based on the identified gaps, promoting innovative approaches and empowering the communities as key stakeholders. It is necessary to develop education programs on symptoms, preventive practices, and treatment for TB, to reduce transmission and stigmatization. It becomes also necessary to provide communities with innovative healthcare solutions to reduce their barriers to access to diagnosis and treatment.


Introduction
Tuberculosis (TB) is a bacterial disease caused by mycobacterium tuberculosis that is spread through sputum when an infected person coughs, spits, or sneezes [1]. Every year 1.5 million people die from TB, making it the leading cause of death from an infectious agent worldwide. Most TB cases are concentrated in low-and middle-income countries [1]. Geographically, most people who developed TB in 2019 were in the WHO regions of South-East Asia (44%), Africa (25%), and the Western Pacifc (18%) [2].
TB is a preventable and treatable disease mainly through promoting early screening and treatment for active TB, by addressing comorbidities and health risks as well as social determinants of the disease, and by promoting access to health care [3]. TB is a disease of poverty, and people afected by TB often face economic distress, vulnerability, marginalization, stigma, and discrimination [2]. Lack of awareness and insufcient knowledge about the symptoms of tuberculosis lead to a delay in seeking health care [4]. Terefore, disease control is improved, and treatment outcomes rely on improving awareness regarding TB [5].
To assess the awareness about TB, the best tool used is the knowledge, attitudes, and practice (KAP) survey. Tis is a representative study of a specifc population to assess what is known, believed, and done in relation to TB [6].
KAP surveys can identify common knowledge gaps, cultural beliefs, or behavioral patterns that may facilitate or pose problems for TB control eforts. Tese surveys address key barriers to accessing TB care and completing treatment. Te data collected provides government TB programs with the fundamental information needed to make strategic decisions [6].
Despite the fact that most of the cases are found in South-East Asia, most systematic reviews about tuberculosis' KAP surveys conducted in this region were addressed to healthcare workers [7,8] while those addressed to the general population were focused on specifc issues such as stigma [9], adherence to treatment [10], or centered in a limited geographical area [11]. Te aim of this study was to better understand TB-related knowledge about disease, prevention, treatment, and sources of information; attitudes towards TB patients and their stigmatization and prevention, diagnosis and treatment practices, stigma-related attitudes; and prevention, diagnosis and treatment-related practices doing a systematic review of published KAP studies addressed to the general population of middle-and low-income countries, where 80% of cases and deaths are found [1], in order to provide evidence that could help policy strategies and decision-making.

Search Methods.
A systematic review was conducted following the Preferred Reporting Items for Systematic Review and Meta-Analyses (PRISMA) guidelines and checklist [12] to identify evidence about knowledge, attitudes, and practices related to TB (see Table S1). Only peerreviewed and published journal articles were reviewed. Literature search was performed in PubMed, Embase, and Scielo using Medical Subject Heading (MeSH) Search terms, and free language terms were used to maximize retrieval of potentially relevant studies. "Tuberculosis," "Health Knowledge, Attitudes and Practices" terms were used. Te search strategy is presented in Table S2.

Eligibility Criteria.
To be eligible, articles have had to include research implemented in middle-or low-income countries according to the World Bank Classifcation [13]. Studies were also included if they were original research using quantitative knowledge, attitudes, and practices surveys or mixed methods. Studies could be published in Spanish, English, French, or Portuguese. Te search was limited to articles published between January 1, 2010, and January 1, 2021. Articles were excluded if they did not use a KAP questionnaire, and the study participants were health professionals or medical students if the article was an opinion piece, conference abstract, or other systematic reviews.

Quality
Assessment. Te quality of the included studies was assessed with the NIH quality assessment tool for cohort, and cross-sectional studies [14] modifed for crosssectional studies. We assessed the representativeness of the study population, participation rate, correct recruitment, sample size justifcation, correct outcome defnition and assessment, and confounding variables measurement. Each study included was assessed independently by two reviewers and was assigned a quality score ranging from 0 to 9. Quality was rated as 0 for poor (0-2 out of 9 points), + for fair (3-6 out of 9 points), or ++ for good (7-9 out of 9 points). While for the included studies with a mixed methods design, the mixed methods appraisal tool (MMAT) [15] was used to assess their quality, considering whether each study justifed the rationale for the design, whether they integrated and interpreted quantitative and qualitative results, whether they explained any inconsistencies found, and whether they assessed the adequacy of the qualitative and quantitative components.

Data Collection and Analysis.
Two reviewers conducted the search independently using the same eligibility criteria to evaluate the studies. Study data were extracted by each reviewer and verifed by both of them. Conficts were solved by a discussion with a third reviewer. After agreeing on the full-text eligible articles, each reviewer completed the information collection sheet including the name of the frst author, year of publication, country and setting (urban/ rural/both), sample size, survey location (home/community/ hospital/health center), the aim of the study and outcomes classifed by knowledge, attitudes, and practices reported in the survey by the participants. First, we have made a descriptive analysis of the frequencies of the studies settings (region, country, rural/urban, survey location), type of survey (quantitative or not), sample size, target population and subject (knowledge, attitudes, practices), and year of publication of each survey and summarized them in totals, percentages, and mean. We also summarized the responses collected in each study by subject (knowledge, attitudes, or practices) reporting their totals and percentages.

Results
Six hundred and four (N � 604) records were identifed through a search in the aforementioned databases. Twentyfve were the articles included in the qualitative reading after full-text assessment for eligibility and, fve records that met the inclusion criteria were added after being identifed in the references of completed read articles. Finally, a total of thirty (N � 30) articles were included ( Figure 1).
Most of the studies reviewed were conducted in Africa (56.7%) ( Table 1). Of the 30 studies, all of them were crosssectional studies, 24 were quantitative studies, and 6 were mixed, all of them used the knowledge, attitudes, and practices (KAP) questionnaire as a survey tool. Te studies were mainly addressed to the general population (63.4%). Te mean sample size was 1557, and the median sample size was 699.   Table 2 shows a detailed summary of the study settings, aims, and outcomes of reviewed studies.

Knowledge about TB.
All of the 30 studies included provided information on the responses of their participants regarding knowledge.
Regarding knowledge about TB treatment, the most frequently mentioned in the studies was "modern drugs" or "modern treatments" by 50% of the studies [16, 17, 19, 22, 25-27, 33, 34, 36, 37, 39, 42, 44, 45]. However, misconceptions and traditional treatments were also frequently mentioned. Te most common incorrect forms of treatment mentioned were "traditional medicine," "herbal remedies," and "roots, blood, skin cuts," and other incorrect treatments mentioned were "resting," "religious treatment," and "burning swelling sites with heated metals" [22]. Only two studies [25,27] mention that a part of their population did not know any treatments for TB.
When asked about the place where to obtain treatment, 17% of the studies conducted in Africa reported "health centers" and "traditional healers" in a study from Asia [36] (Table 3).

Attitudes regarding TB
3.2.1. Stigma. Stigmatization towards TB patients was present in 20 (67%) of the included studies, showing high levels of stigmatization in 37% of them "more than 50% of the population feels rejection towards TB patients, would not support them, and think that TB is an illness that one should be ashamed of" [17,22,23,25,35,36,39,41,42,44,45]. It is important to highlight that many of these studies were conducted only in rural areas [17,22,23,25,44] while the studies that presented lower levels of stigmatization were conducted mostly in urban areas [19,21,26,31] or in both [32,33,36,38].
In addition, only 3 studies showed that some of the participants would be willing to reveal having TB to their families or friends [30,34,42].

Health-Seeking Practices. Of the included studies, 20%
reported that the majority of the studied population said that they used to go to health centers or the Community Health Worker (CHW) to seek health care at least once a year [19, 25-27, 34, 42]. Terefore, when asked what they would do if they had symptoms of TB, the most common answers were "go to a health care facility," "go to the Community Health Worker (CHW)," or "go to the hospital" [16, 19, 22, 24-26, 30, 32, 33, 36, 37, 42, 44, 45] although 9% of the studies showed that most participants only would go to the hospital when traditional or self-treatment failed and the symptoms were persistent or incapacitating [27,37,45] ( Table 4).

Delay.
Out of the 30 selected studies, only 2 (7%) analyzed that the average delay of treatment seeking among the population was 7 days after symptoms onset, one in a rural area of Asia, Myanmar [44] and one in rural Africa, Ethiopia [25].

Prevention Practices.
Five studies (17%) mentioned some prevention practices that the respondents were actively using, such as "avoid sharing food utensils" [22], "covering the mouth and nose when coughing" [21,31], "maintaining a correct ventilation of the house" [21,31], or "limiting contact with TB patients" [40]. Only one study [19] mentioned that a small percentage of the participants answered that TB could not be prevented (Table 4).

Critical Appraisal.
All the included studies had fair or good quality after the quality assessment. All the studies had a clearly stated research question and a specifed study population. Te main limitations of the included studies were related to the reporting of the sampling strategy, the participation rate, and the qualitative results in some of the studies with mixed methods. Te complete quality assessment tables are available in Table S3.

Discussion
Tuberculosis is a major cause of ill health, one of the top 10 causes of death worldwide and the leading cause of death from a single infectious agent [1]. TB treatment has prevented more than 60 million deaths, but many millions have also been left without diagnosis and care [2]. India, Indonesia, the Philippines, and South Africa are the four countries that account for 44% of global TB cases [2]. However, only 7 of the included studies (23%) were conducted in South-East Asia, highlighting a gap in KAP on TB research in the region.
Studies results showed how the awareness about TB in the general population of middle-and low-income countries is still insufcient. Tese defciencies implied inadequate attitudes and practices, causing delay in seeking treatment and increasing transmission [4,46,47].
Our review shows that inadequate knowledge and TB health-seeking practices were present regardless the gender, living area (urban or rural), or country. In addition, it seems that there is a frequent association between less knowledge about TB and a lower socioeconomic and educational level [47,48]. Low income and low education populations are more likely to have incorrect perceptions of TB, such as more incorrect responses to the causes, symptoms, and transmission and prevention. Low awareness about TB associated with being unemployed or not have completed high school education was also found in other two systematic reviews [47,48].
Te respondents knew that the best place to go to treat TB is the health services, where they could be treated with "modern drugs". However, this is not refected in their practices as they preferred to go to the traditional healers or even used self-treatment [17,27,34,39]. Barriers in accessing health services are among the most mentioned reasons why individuals did not frequent them when they present symptoms, as shown in a study conducted in Kenya where distance to the health centers was a factor in underdiagnoses and poorer treatment outcomes [49]. Te training of community health workers and the promotion of diagnosis in peripheral and rural areas could be recommended, as a way of bringing health care closer to the most remote areas.
Te presence of TB disease is often believed to be an event of which one should be ashamed of. Stigmatization of TB patients is found more frequent in rural areas than in urban areas. In Ethiopia, TB patients may deliberately hide their health status or try to live with TB without treatment to avoid stigma, being the source of infection to others [50]. In Nepal, TB is also a source of stigmatization and isolation, causing delays in seeking healthcare and treatment [51]. Delay in seeking treatment is among the most common practice that could lead to the spread of the disease in the community. Te most common causes for delay in seeking TB care found were difculties in transportation and lack of knowledge about where to search for treatment [25].
Te preferred sources of information about TB in this review were TV in urban and HEWs in rural areas. Studies have shown that mass media is an adequate source of information about TB [52,53]. Furthermore, more exposure to mass media when used to give information about TB translates into better knowledge and attitude, being TV the most popular mass-media source [53,54]. A study carried out in India showed that the rural population or those with a lower socioeconomic level have less access to the mass media and subsequently less access to information about TB [55], recommending that HEWs would be the most appropriate source of information for the rural population.
Te quality of evidence from some of the included studies was overall acceptable; yet, the main limitations of the included studies were that some did not report the rate of participation, and some studies did not explain the estimation of the sample size. Also, due to the inclusion criteria, there is little presence of studies conducted in the SEA region. Notwithstanding these limitations, the need to improve TB awareness and health-seeking behavior showed evident.

Conclusion
Tis study revealed gaps in TB knowledge, attitude, and practices in the general population in middle-and lowincome countries. Te evidence shown in this study should be considered to improve education programs on symptoms, preventive practices, and TB treatment in order to reduce stigma and the barriers associated with diagnosis and treatment access, using mass media in urban areas and HEWs in rural areas as sources of information, focusing on the most vulnerable population. Furthermore, successful control of TB relies on coherent, multifaceted communitybased health programs. Policymakers should take into account the relevant information provided by KAP surveys and adapt their strategies to evidence, promoting innovative approaches such as new mechanisms for drug distribution and diagnosis and empowering the communities as key stakeholders. Implementing community-directed programs would provide opportunities for government health services and other local social actors to work closely with the population directly afected, reaching as many people as possible, and taking into account socio-cultural and economic conditions.

Data Availability
No data were used in this study.

Ethical Approval
No ethical approval was required as this is a review article with no original research data.

Conflicts of Interest
Te authors declare that there are no conficts of interest.