Facilitators and barriers to TB care during the COVID-19 pandemic

Abstract

BACKGROUND:

Knowledge about factors influencing access and adherence to TB care, and on the impact of the COVID-19 pandemic on TB care in resource-restricted settings is scarce. We conducted this study in Atsimo-Andrefana, a rural region in southern Madagascar where TB prevalence, poverty and food insecurity rates are high. We aimed to determine facilitators and barriers to access to and provision of TB care in rural Madagascar during the COVID-19 pandemic.

METHODS:

We conducted qualitative focus group discussions (FGDs) and in-depth interviews (IDIs) with patients with TB, community health workers, facility-based health workers, public health officials and non-governmental organisation staff. We analysed interviews using thematic analysis.

RESULTS:

We conducted 11 FGDs and 23 IDIs. We identified three main barriers to access and adherence to TB care: 1) stigma, 2) indirect treatment costs, and 3) food insecurity. The facilitator perceived as most influential was high health worker motivation. The effects of the COVID-19 pandemic on TB care varied between stake-holders; some health workers described delays in TB diagnosis and increased workload.

CONCLUSIONS:

To improve access and adherence to TB care, both indirect treatment costs and stigma need to be reduced; undernourished patients with TB should receive food support.

Although curable and preventable, 10 million people fell ill with TB globally in 2020.¹ Low- and middle-income countries are disproportionately affected by the disease.¹ The COVID-19 pandemic set back the fight against TB, with approximately 1.4 million fewer people receiving TB care in 2020 compared to 2019.² In rural settings, challenges to accessing and adhering to TB treatment are numerous, including financial, social and geographical barriers.³

In Madagascar, TB prevalence is high, at 238 cases per 100,000 people;⁴ effective treatment coverage is only 59%. Barriers to TB care in Madagascar are compounded by high poverty rates. Nationally, 79% of the population live below the international poverty line (1.90 USD/day, 2011 purchasing power parity).⁶

To improve TB care, knowledge about relevant facilitators and barriers affecting access to and provision of care is needed. Assessing both patients’ and healthcare providers’ perspectives is essential to understand their interrelatedness, identify action points, and design effective and context-sensitive interventions. Similarly, evidence regarding the impact of the COVID-19 pandemic on TB care in rural regions is needed to improve the resilience of TB care programmes for future crises.

In this qualitative study, we analysed factors influencing access to and provision of TB care in rural Madagascar, acknowledging the interaction between patients’ and healthcare providers’ perspectives based on the access to care model.⁷ This also study provides insights into the implications of COVID-19 on TB care. We expect our results to inform policy and practice for TB care in rural Madagascar and similar settings.

METHODS

Study setting

We conducted this study in Atsimo-Andrefana, a region in southern Madagascar with a population of around 2 million people; 86% of whom live in rural areas.⁸ Extreme weather conditions, such as droughts, floods and heat waves decrease soil quality and water access, limiting agricultural gain and development. Chronic malnutrition is prevalent in the study area; there was a famine during data collection.^9,10

In Madagascar, TB care is funded by the Global Fund and provided free of charge by a countrywide network of state-funded, faith-based, and private diagnostic and treatment centres (locally known as Centres Diagnostic et de Traitement, CDTs). CDTs are supported by local treatment centres (locally known as Centres de Traitement, CTs), which are mostly basic health posts. All TB care activities are conceived, coordinated and supervised by the national TB programme (Programme National de Lutte contre la Tuberculose, PNLT). Figure 1 shows the typical journey of a TB patient in Madagascar.

FIGURE 1.

Stakeholders in TB care (white boxes) and patient journey through levels of care (black boxes) for drug-susceptible TB care in Madagascar according to the national TB strategy.¹¹ To access TB care, presumptive patients with TB either directly access the nearest treatment centre (CDT) or are identified and referred by CHWs or facility-based health workers. To ensure treatment adherence and safety, the national TB strategy requires directly observed treatment during the intense phase (first 2 months) of treatment. CHWs are responsible for reminding patients of treatment monitoring by smear microscopy at 2, 5 and 6 months of treatment. In case of continued positive sputum results after 5 months of treatment, patients are referred to higher-level health facilities for drug susceptibility testing. PNLT = Programme National de Lutte contre la Tuberculose; CHW = community health worker; CDT = Centres Diagnostic et de Traitement; CT = Centres de Traitement.

We randomly selected three out of nine rural districts in the Atsimo-Andrefana Region to allow for regional variation of experiences. We approached all (n = 6) CDTs providing care for drug-susceptible TB patients in the selected districts. CDTs were situated in urban settings, with population sizes ranging from 20,000 to 50,000. However, their catchment area also includes surrounding rural populations. There were four public CDTs. Local treatment centres (CTs) were not included in this study, as none of these facilities in the selected district were actively providing TB care at the time of the study.

Participants

We conducted qualitative in-depths interviews (IDIs) and focus group discussions (FGDs) with patients with TB and community health workers (CHWs). We conducted IDIs with facility-based health workers (FBHWs), public health officials from the national TB programme and non-governmental organisation (NGO) staff working in TB programmes.

We recruited patients with TB, CHWs and FBHWs by visiting the included facilities during TB treatment days. After obtaining approval from the facility head, we invited all patients who had received treatment for drug-susceptible disease during the previous 12 months to participate in this study. CHWs attached to the selected CDTs were approached during routine CHW training sessions and FBHWs at the CDTs either by visiting them at their facility or via phone or email. CHWs and FBHWs were invited to participate if they were involved in TB care provision at the time of the interview. We recruited regional public health officials coordinating or supporting TB care activities in the study region by contacting them via phone or email. We used snowball sampling to identify and recruit regional NGO staff working in the TB field.

We included all consenting participants who were fluent in French or Malagasy and over 18 years of age. All participants were explicitly informed that participation in the study was voluntary and that they could withdraw at any time without negative consequences. We obtained informed consent from each participant prior to study enrolment.

Data collection

Two researchers fluent in the local Malagasy dialects and French and with experience in qualitative data collection methods conducted all IDIs and FGDs. To ensure data validity and reliability, both researchers participated in a 3-day training on aspects of TB care, qualitative research methods, ethics and aims of this study. Interviews were conducted in person at a location of the participant’s choosing and audio-taped with the participant’s permission. Data were collected between October 2020 and January 2021.

We used interview guides based on available literature on access to TB care with open-ended questions, including areas for probing. For each group of participants, we conceived separate guides to elucidate their distinct roles in TB care. The IDIs and FGDs conducted with CHWs and FBHWs commenced with questions on the participant’s responsibilities in TB care, followed by the participant’s perspectives on facilitators and barriers experienced in providing TB care, and concluded with the participant’s perception of the effects of the COVID-19 pandemic on TB care. FGDs conducted with patients included open-ended questions on the participant’s personal experience in the TB care system, facilitators and barriers they encountered, and their suggestions for improving access along the TB care cascade. IDIs conducted with public health officials and NGO staff focused on the participant’s responsibilities in the national TB care system, the overarching barriers and facilitators on an administrative and political level and suggestions for improvement.

For community health workers, facility-based health workers, public health officials and NGO staff, data collection was considered complete once all eligible and consenting participants for a respondent group had been interviewed (e.g., all regional public health officials active in TB care). For patients, we continued recruitment until code saturation was reached, i.e., no higher-level concept and additional definitions of concepts for the codebook emerged from the analysis of the FGDs.

Data analysis

Trained interpreters first transcribed the recordings ad verbatim and then translated them to English for analysis. A native Malagasy speaker conducted random spot checks of the validity of transcripts and translations by comparing them to the audio recordings. All identifying information was pseudonymised by the researchers before transcription and translation. All data were stored in digital format in a password-protected database. Access was only granted to the research team. Three researchers (HW, LT, MF) coded all interviews separately, followed by cross-coding to ensure consistent coding practices. We used a deductive approach based on thematic analysis.¹¹ Emerging themes were discussed, and transcripts recoded as the codebook was refined to capture variability in perceptions and experiences. We grouped codes into sub-themes, which were consecutively allocated to the five dimensions of the access to care model, as described by Levesque et al.⁷. The sub-themes were then structured by facilitators and barriers to access and adherence to TB care and grouped into five over-arching themes, allowing for a comprehensive overview of factors. We used Dedoose v9.0.17 (University of California Los Angeles, Los Angeles, CA, USA) for data analysis.

Ethical approval

Ethical approval for this study was obtained from the University of Heidelberg Ethics Committee, Heidelberg, Germany, under the registration number S-624/2020.

RESULTS

In total, we conducted 11 FGDs including 59 participants and 23 IDIs (Table).

TABLE.

Participants included in the study to assess facilitators and barriers along the TB care cascade in rural Madagascar

	FGDs n (total number of participants)	IDIs n
Patients with TB	6 (32)
CHWs	5 (27)
FBHWs
Physicians		7
Laboratory technicians		7
Public health officials		5
NGO staff		4
Total	11 (59)	23

FGD = focus group discussion; IDI = in-depth interviews; CHW = community health worker; FBHW = facility-based health workers; NGO = non-governmental organisation.

Factors influencing the access and adherence to TB care

We identified five main themes affecting access and adherence to TB care. We present the main themes grouped by the access to care model.⁷ Figure 2 shows the main themes identified. Results regarding the impact of COVID-19 on TB care are reported in a separate paragraph.

FIGURE 2.

Access to care model for TB care in Atsimo-Andrefana, Madagascar (adopted from Levesque et al.⁷). Data for this figure was drawn from 11 focus group discussions with 32 patients, and 27 CHWs and 7 individual interviews with FBHWs. Themes were identified and categorised by three researchers (HW, LT, MF). FBHW = facility-based health worker; CHW = community health worker; HCP = healthcare personnel.

Health literacy

FBHWs and CHWs reported that patients often did not retain disease- and treatment-related information, possibly indicating challenges in health literacy. FBHWs and CHWs deemed community sensitisation to be essential to improve health literacy. However, CHWs felt overburdened by the high workload due to their various duties and lack of financial incentives for their work.

Patients felt confident in their knowledge about the duration of care. However, several patients expressed misconceptions about TB transmission (for e.g., that TB was passed down by one’s ancestors). This could further underline possible challenges to health literacy.

I got mine from my ancestors who had tuberculosis. And that was passed on to the descendant. (Patient 01)

Motivation to deliver TB care

FBHWs expressed high intrinsic motivation and reported behaviours exceeding job-related responsibilities to ensure continuous, high-quality care. In areas where health facilities lacked medical staff, laboratory technicians were actively involved in TB treatment, patient education, and follow-up. Similarly, CHWs also reported monitoring directly observed treatment (DOT), thereby exceeding their programmatically allocated responsibilities.¹²

FBHWs reported the degree of training they received to be essential for their work motivation; training in TB care in the study area was offered by the government and NGOs. Lack of training, aggravated by pandemic control measures, was reported as an important demotivating factor for many FBHWs.

In the past, we had 3 days of training, [..], whereas now (since the COVID-19 pandemic) it’s reduced to 2 days. And the 2 days didn’t happen. (CHW-01)

While traditional healing practices and self-medication without medical prescription are broadly available in the study area, patients did not report using either of them. FBHWs, however, mentioned these factors as being reasons for delayed treatment seeking, possibly indicating social desirability bias among patients.

There are many people with TB who are satisfied with traditional medicine [...] and who die without having gone to a medical (TB care) centre. (FBHW-01)

A barrier to access TB care deemed decisive by participants was stigmatisation. We identified two forms of stigma as drivers for social exclusion of patients: enacted and perceived stigma. Enacted stigma, mainly shown through acts of discrimination from community members, prevented patients with TB from seeking social interaction, increasing the psychological disease burden. Psychological distress, in turn, prevented patients from seeking care. In contrast, perceived stigma, meaning a TB patient’s fear of stigmatisation by a health worker, motivated patients to withhold personal information, such as names or addresses. This, in turn, rendered health workers unable to identify patients for follow-up. These acts of stigmatisation were predominantly described by health workers, whereas patients tended to only describe the effects of stigma (e.g., not being allowed to sell produce at the market).

When the community knows that a patient has tuberculosis then the patient is excluded. For example, if the patient is selling tea and coffee, […] they don’t drink there anymore. (FBHW-02)

Infrastructure

Insufficient infrastructure, such as poor road networks, combined with the distance between rural communities and health facilities were reported as major barriers for patients and health workers.

For FBHWs, the interplay between geographical barriers and lack of means of transportation complicated the transfer of TB samples to reference laboratories, delaying diagnosis and care. It also complicated home visits by CHWs for vulnerable patients, who were unable to seek treatment at a health facility.

There is a (geographical) distance between the patients and the (health) centre. [..] The (health) centre is far away and they will not come there. (NGO staff-01)

We come to those who can’t walk, and we make them take their medication every morning during first 2 months. (CHW-02)

Shortages in laboratory reagents, medication and personal protective equipment were reported by FBHWs to have caused delays in diagnosis and treatment. In addition, FBHWs reported health facility overcrowding and insufficient room to isolate patients with TB, endangering patients and staff.

Patients reported that disease-related weakness negatively influenced their ability to regularly visit health facilities. CHWs reported delivering medication directly to weak patients. Home visits by CHWs were highly valued by the communities, allowing patients to continue treatment despite geographical and disease-related barriers.

That’s the main problem for us (patients with TB), we are too tired to go back here (health facility) every day. (Patient-02)

Socio-economic factors

Both FBHWs and public health officials reported funding gaps hampering service delivery. To bridge these gaps, FBHWs reported the need to pay for operational expenses, e.g., for sending reports or sharing clinical data, which should have been covered by PNLT funding. This not only impeded information sharing and clinical care but also considerably demotivated FBHWs. FBHWs also reported supporting patients’ indirect treatment costs from their own income, e.g., by paying for patients’ food, to ensure continuity of TB care, which they perceived as a major motivational challenge.

The barrier perceived as most impactful by patients was the costs associated with visiting treatment facilities. Despite treatment being free of charge, indirect costs such as transportation or concomitant drugs were prominent threats to TB treatment adherence. These barriers were aggravated by opportunity costs such as loss of income.

Quality of care

Across all levels of care, FBHWs reported TB treatment provision to be drastically impacted by the scarcity of healthcare staff, in turn increasing individual workload. CHWs perceived their role to be essential to foster patient-provider interaction and patient follow-up. FBHWs described clear and open communication with patients about their disease as an essential facilitator for treatment adherence, stating that they used the time patients spend in in-patient care to repeatedly educate them about their disease and to respond to questions, if any. FBHWs further highlighted the importance of building a respectful, trusting relationship with their patients, as they felt it enabled patients to be more open about treatment side effects and other issues, in turn improving treatment adherence and patient satisfaction.

We get ‘familiar’ with the patients. So that the patient doesn’t hide their problems from us or any side effects that they may be experiencing. (FBHW-02)

FBHWs and CHWs regularly exchanged treatment and diagnostic registers, as well as CHWs patient lists to cross-reference patient data and update each other on presumptive and confirmed patients with TB. However, dependence on paper-based systems, as well as geographical barriers such as bad road conditions, were perceived to slow down data sharing and reporting between levels of care.

Some reports come from very remote CDTs in the countryside. And if no one picks up or brings the report, then it is left there. (NGO staff-02)

While patients with TB indicated awareness of the importance of treatment adherence, they felt that chronic food insecurity limited their ability to engage in TB care. Patients felt pressured by the nutrition guidelines given by health workers and reported food scarcity as a limiting factor to their well-being, especially when suffering from treatment side effects.

It is recommended to us to eat well [..] but we can’t do it, we don’t have the resources. (Patient-03)

Impact of COVID-19 on TB care

While there was consensus on the negative impact of the COVID-19 pandemic, the perceived effect of the pandemic on TB care in the study region was varied. Some CHWs reported that community sensitisation activities had continued, while others said that public gatherings were forbidden, and sensitisation activities suspended. Similarly, some CHWs reported that they continued to visit vulnerable patients with TB at home ensuring treatment continuity, while others suspended all activities due to fear of infection.

Some FBHWs reported that there was little to no change in their daily routine nor TB patient numbers, while others reported a drop in the number of patients seeking care at facilities and that care provision was affected. Most FBHWs reported that personal protective equipment was distributed late and in insufficient quantities, meaning they did not feel protected against COVID-19 and were afraid to infect others, especially their families. This, in turn, decreased their work motivation and increasing their perceived stress levels

FBHWs reported an increased workload due to the pandemic; cooperation with other FBHWs was reduced due to pandemic control measures. There was consensus among FBHWs regarding the difficulty of distinguishing COVID-19 from other infections.

The problem with COVID-19 is that it combines the symptoms of all the diseases that I know. (FBHW-03)

The most frequently reported barrier due to the pandemic was the use of diagnostic tools usually reserved to detect TB drug resistance for COVID-19 diagnostics, which delayed the diagnosis of patients with presumptive drug-resistant TB.

DISCUSSION

Participants reported stigmatisation, indirect costs and food insecurity during TB treatment as major barriers to access and adherence to TB care. Other perceived barriers included lack of transportation, medical equipment and supplies, high workload among health workers, health worker shortages and insufficient training, as well as competing traditional healing practices. In contrast, health worker motivation was perceived as a key facilitator to access TB care. While the perceived effect of the COVID-19 pandemic was varied, a delay in TB diagnosis, especially of drug-resistant cases as diagnostic equipment was repurposed for COVID-19 detection, was a commonly expressed challenge.

TB stigma is known to contribute to delayed healthcare seeking and reduced treatment adherence.¹³ While previous literature has identified TB stigma as an essential determinant of TB treatment uptake,^13–16 participants expressed an interrelation between stigma and socio-economic status, which ultimately led to an unwillingness to seek out and adhere to TB care in fear of social exclusion and financial impoverishment. Stigma was perceived to be exacerbated by misconceptions, e.g., about disease transmission. Previous research has shown that health education, e.g., through context-sensitive community outreach, can decrease TB misconceptions, positively impacting health-seeking behaviour and health outcomes.^17,18

While TB treatment is free at public health facilities in Madagascar, indirect treatment and opportunity costs were reported to be significant economic barriers for patients. Healthcare financing mechanisms should be improved to counter the financial burden of indirect treatments costs of TB care.^19–21 For example, subsidised food or transportation to health facilities may alleviate the financial burden of TB treatment.¹⁹

Patients with TB also expressed a lack of adequate and nutritious food to be a major barrier to treatment adherence. The link between TB and nutrition is well-established.²² As southern Madagascar is frequently hit by drought and was experiencing a famine with high rates of malnutrition at the time of data collection, this barrier merits particular attention.¹⁰ The future increase of extreme climatic events is likely to exacerbate both TB prevalence and food insecurity. This highlights the need to develop resilient food and agriculture systems, as well as food support programmes for patients with TB.

Health worker motivation to provide quality care was perceived as an important facilitator across the TB care cascade. High levels of health worker motivation and work ethos despite challenging working conditions have been found across other settings in sub-Saharan Africa.^23–25 Sufficient and timely financial compensation for their work was the most influential motivating factor for FBHWs,^23,24 a sentiment that was also echoed by health workers in our study. CHWs too reported high levels of motivation and of being frequently engaged in activities exceeding their job-related responsibilities. While this behaviour fills gaps in service delivery, it could potentially endanger patients’ well-being due to insufficient training in specific TB activities. For CHWs, who usually work as volunteers, financial constraints were particularly decisive in determining work motivation.²⁵ To ensure health worker motivation, policy makers need to ensure sufficient and timely payments of operating budgets and health worker salaries.

The reported effects of the COVID-19 pandemic on TB care varied among participant groups. There was consensus that the pandemic disrupted TB care at all levels of the care cascade. As described in other settings,²⁶ the use of TB-dedicated diagnostic equipment for COVID-19 was perceived as having a negative impact on the timeliness of TB diagnosis and thus, treatment initiation. Furthermore, health workers reported fear of infection with COVID due to insufficient supply of personal protective equipment, leading to the suspension of several TB activities. This shift of service delivery consequently may reduce quality of TB care and worsen health outcomes.²⁶ As echoed across settings,²⁷ the similarity in clinical manifestations of TB and COVID-19 was reported to pose difficulties in differentiating COVID-19 symptoms from other diseases, indicating a potential lack of training during the pandemic.

Our study had several limitations. While the study was conducted in an area with both rural and urban populations, perceptions and experiences in more urbanised areas likely differ; the generalisability of results may thus be limited. Similarly, due to ethnographic and structural differences, the application of our results to other rural areas could be limited. Generalisability may have been further limited by the use of purposive sampling. Due to the nature of the study setting, a random sampling approach was not feasible. Patient reports during FGDs may have been distorted by social desirability bias, facilitating groupthink, and thus, polarising results. This could be especially important regarding the small number of patients who admitted seeking care at traditional healers or self-medicating, although this is common in other settings^13,28,29 and was reported by HCPs and CHWs. Additionally, the strong association between stigma and TB may have limited patients’ willingness to participate due to fear of discrimination.

CONCLUSION

Our findings highlight the need for strategies to reduce TB stigma, such as community health education. Indirect costs of TB treatment should be reduced, with a special focus on transportation and nutritional support. Health worker motivation may be improved by ensuring timely salary payments, as well as by providing additional monetary or non-monetary incentives. The impact of the COVID-19 pandemic on TB care may be reduced by ensuring adequate availability of diagnostic equipment and health worker training.

Funding Statement

This study was financially supported by German Agency for International Cooperation (GIZ) on behalf of the German Federal Ministry for Economic Cooperation and Development (BMZ), and by DLR Project Management Agency on behalf of the German Federal Ministry of Education and Research (BMBF).