Background
Continued transmission by individuals not diagnosed and treated rapidly and appropriately is a major driver of the tuberculosis (TB) epidemic. Yet, nearly 3 million of the estimated 9 million TB cases worldwide are “missing”, either because they were not notified by health systems or not diagnosed [
1]. There are two over-arching reasons for under-diagnosis: failure of patients to access TB diagnostic services and failure of providers to diagnose and treat TB among patients who do access TB diagnostic services. The latter represents a failure of the health system and, if addressed, an opportunity to increase TB case detection and treatment rates.
Studies of the quality of TB evaluation (
i.e., diagnostic workup of patients with symptoms suggestive of TB) in high burden countries have generally shown poor adherence to international or national guidelines. The International Standards for TB Care (ISTC), Edition 3. TB CARE I, The Hague, 2014 which have been endorsed by nearly all TB programs worldwide, recommend that at a minimum all patients in high burden countries with cough of at least 2 weeks’ duration should have at least two sputum smears examined for acid-fast bacilli (AFB) and be treated for TB if sputum AFB smear-positive. In Uganda, which is one of the 22 high TB burden countries according to the World Health Organization (WHO), we found that only 21% of patients with cough greater than 2 weeks’ duration were referred for sputum smear microscopy, 73% of patients referred completed sputum smear examination, and 71% of patients with a positive sputum examination were initiated on TB treatment [
2]. Similar findings of providers not following guidelines for TB diagnosis and treatment have been reported from the public and private sector in many other high burden countries [
3-
9].
While previous research, including quantitative [
10-
12], qualitative [
13-
19], and mixed methods approaches [
20], has assessed barriers patients face in accessing primary care centers that provide TB diagnostic services, less is known about barriers providers in these settings face in adhering to guidelines for evaluating patients for TB. The two studies evaluating provider perspectives have focused on their perceptions about patient barriers to accessing TB care [
19,
21]. Less well understood are the determinants of provider adherence to TB evaluation guidelines. In particular, there is increasing recognition that guideline implementation is heavily dependent on provider behavior and in order to improve the quality of care, understanding and subsequently changing provider behavior is required.
To inform the development of clinic-level interventions to improve implementation of TB evaluation guidelines, we conducted a qualitative study of front-line providers involved in TB evaluation at six primary health centers in rural Uganda. We used a theory-informed approach to elicit key determinants of the current behavior of health center staff involved in TB diagnosis and treatment. We focused on health system (clinic-level) and contextual barriers to changing provider behavior in relation to key processes associated with TB diagnosis, and used the PRECEDE framework to classify modifiable barriers as predisposing, enabling and reinforcing factors that could be targeted with clinic-level interventions [
22].
Discussion
We report a descriptive qualitative analysis of barriers to uptake of internationally recommended TB evaluation practices by providers at routine health centers in a high TB prevalence country. We found that health center staff perceived many of the same barriers reported previously by studies eliciting patient perspectives, including the time and costs associated with seeking and completing TB evaluation and stigma against patients with TB [
10,
31,
32]. In addition, we identified specific health system factors that can be targeted for interventions. These ranged from behaviors relevant to the providers and other staff at the clinics (
e.g., lack of training, low motivation of staff, and poor coordination of services) to direct availability of resources (
e.g., stock-outs of supplies and drugs), both of which contribute to sub-standard TB evaluation. Next steps will focus on creating a series of targeted intervention strategies that have potential to modify provider behavior by addressing key predisposing, enabling, and reinforcing factors within this clinical setting.
Patient barriers to TB evaluation impacting initial access to TB diagnostic services have received considerable attention over the past several years. For example, previous studies have identified how long distances to health centers, direct and opportunity costs associated with seeking TB evaluation, and repeated visits to private practitioners or traditional healers delay TB evaluation [
10,
31]. These factors were well recognized by providers in our study and our findings indicate that providers clearly sense that these barriers continue to impact their ability to deliver high quality TB evaluation even after patients arrive at the clinic. To mitigate economic and geographic barriers, the WHO has recently endorsed a smear microscopy strategy in which two sputum specimens are collected and examined at the initial patient visit instead of over several days [
33]. Our findings reinforce that TB programs in high burden countries should take steps to enable diagnosis of TB followed by initiation of treatment at a single health center visit, either through same-day microscopy or, where feasible, through use of novel semi-automated molecular diagnostic tests [
34]. If implemented successfully, “test and treat” strategies are likely to have considerable impact on TB incidence and/or mortality [
35].
Although same-day microscopy and semi-automated molecular tests clearly represent an important way forward to simplifying the diagnostic process, many health system barriers not unique to TB diagnosis are likely to blunt the impact of introducing new diagnostic strategies or tests if not addressed. Stock-outs of supplies and drugs and malfunctioning equipment are common at health centers in low-income countries [
36]. Stock-outs not only affect the ability of staff to deliver quality care but also reinforce negative community perceptions about government health facilities, leading to patients seeking care in settings where TB testing and treatment are not routinely offered. Ministries of Health must also address barriers that may underlie the guideline concordant behaviors that will increase diagnostic service provision. These include low motivation of staff at government health facilities, partially related to concerns about the risk of acquiring TB infection from patients. Data are limited but suggest these concerns are real – health care workers in high burden countries have a 3-fold higher risk of developing TB and 6-fold higher risk of developing multidrug-resistant TB than the general population [
37]. Last, poor coordination of clinic staff and services (including volunteers) was perceived as a key barrier to delivering high quality care. More attention is needed to how the timing and location of services impacts patients’ ability to receive all required care prior to completing their health center visit.
In order to build on the findings of these interviews, we propose some specific intervention strategies for application in field studies to address factors operating at multiple levels in the setting in which interventions are planned [
38]. In this study we organized our qualitative findings on barriers into possible intervention components, using predisposing, enabling and reinforcing factors as intervention targets. This approach is based on a substantial literature that applies the PRECEDE model to planning health promotion activities in health care settings [
39]. Our results suggest that a multi-faceted intervention to improve adherence to recommended TB evaluation practices should jointly address one of more of the following factors: 1) guideline training, leadership and peer support activities (such as mentoring/peer coaching, patient advocates, and/or opinion leaders) and visual job aides/referral materials to target knowledge, motivation of staff, stigma toward TB patients, and self-efficacy (
i.e., predisposing factors); 2) adequate staff training in microscopy skills, patient counseling, and care coordination; utilization of tools such as checklists or mHealth strategies to improve supply management; same-day diagnosis and treatment of TB; task-shifting, including utilizing community health workers for community-based sputum collection, co-training of all staff as counselors, implementing cough screening by registration clerks (
i.e. enabling factors), 3) performance feedback, recognition, and incentives to increase accountability (
i.e., reinforcing factors). While what we presented in this paper focuses on interventions based at the health center, additional interventions that improve patient access and strengthen the larger health system are clearly needed to maximize the quality of TB evaluation services.
Our study has several potential limitations. First, the generalizability of our findings could be limited in that our study included health centers in a single country. However, the sampled health centers are from six geographically distinct districts in Uganda and provide similar services as district health centers found throughout sub-Saharan Africa. Second, our sampling of health center staff was incomplete and included only those available during site visits, limiting our ability to stratify our results by provider type. Finally, it is possible that staff were more comfortable highlighting certain barriers (such as supplies) over others (such as internal problems) that could jeopardize their standing if discussed with supervisors.
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made.
The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder.
Competing interests
This study was supported by the following grants from the National Institutes of Health: K23 AI080147 (JLD), K23 HL94141 (AC), R21 AI096158 (AC MH), and UL1 RR024131, P30DK092924 (MH), P60MD006902 (MH), and by the National Center for Advancing Translational Sciences, National Institutes of Health, through UCSF-CTSI Grant Number UL1 TR000004. The funding sources had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
The authors declare they have no competing interests.
Authors’ contributions
Conceived and designed the study: AC, AK, LD, MH. Data collection: AT, PH, EO, MH. Data analysis: AC, CRM, MH, SA. Manuscript preparation and editing: AC, CRM, MH, SA. Manuscript review: All authors. ICMJE criteria for authorship read and met. All authors agree with the manuscript’s results and conclusions. All authors read and approved the final manuscript.