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PLOS Global Public Health logoLink to PLOS Global Public Health
. 2022 Mar 16;2(3):e0000249. doi: 10.1371/journal.pgph.0000249

Understanding reasons for suboptimal tuberculosis screening in a low-resource setting: A mixed-methods study in the Kingdom of Lesotho

Afom T Andom 1,2,*, Hannah N Gilbert 2, Melino Ndayizigiye 1, Joia S Mukherjee 2,3,4, Jonase Nthunya 1, Tholoana A Marole 1, Mary C Smith Fawzi 2, Courtney M Yuen 2,3
Editor: Megan Coffee5
PMCID: PMC10021370  PMID: 36962295

Abstract

Lesotho has one of the highest tuberculosis (TB) incidence rates in the world, estimated at 654/100,000 population. However, TB detection remains low, with only 51% of people with TB being diagnosed and treated. The aim of this study was to evaluate implementation of TB screening and identify drivers of suboptimal TB screening in Lesotho. We used a convergent mixed methods study design. We collected data on the number of health facility visits and the number of clients screened for TB during March-August, 2019 from one district hospital and one health center. We conducted interviews and focus group discussions with patients and health workers to elucidate the mechanisms associated with suboptimal screening. Out of an estimated 70,393 visitors to the two health facilities, only 22% of hospital visitors and 48% of health center visitors were asked about TB symptoms. Only 2% of those screened at each facility said that they had TB symptoms, comprising a total of 510 people. Lack of training on tuberculosis screening, overall staff shortages, barriers faced by patients in accessing care, and health care worker mistrust of tuberculosis screening procedures were identified as drivers of suboptimal TB screening. TB screening could be improved by ensuring the availability of well-trained, incentivized, and dedicated screeners at health facilities, and by providing TB screening services in community settings.

Introduction

Globally, around 30 percent of people with tuberculosis (TB) are neither diagnosed nor treated [1]. Timely detection of TB and immediate initiation of effective treatment are important to save lives, reduce morbidity from the disease, and control transmission [2, 3]. In settings with high TB burdens, actively screening key populations for TB is a critical step for closing the TB diagnosis gap [4]. In settings with high TB burdens, one population that can benefit from systematic TB screening is people attending health facilities. In settings with high HIV prevalence, health facility attendees include large numbers of people living with HIV, making facility-based screening particularly effective for TB detection. Prevalence surveys in sub-Saharan African countries have repeatedly found that many people with undiagnosed TB had in fact sought care for their symptoms [5]. Screening health facility attendees has been shown to increase overall TB diagnoses in the population in countries with high TB and HIV burdens [6, 7]. However, even though countries may have policies for screening health facility attendees, incomplete implementation leads to missed diagnoses [8, 9].

Lesotho has the highest TB incidence globally, with an estimated 654 cases per 100,000 population annually [1]. The prevalence of multidrug resistant TB (MDR-TB) is among the highest in sub-Saharan Africa, and HIV is a major driver of the TB epidemic given the adult HIV prevalence of 21% [10]. In Lesotho, the estimated TB detection rate is only 51%, meaning that approximately half of TB patients are neither diagnosed nor treated [1]. The high prevalence of HIV co-infection among TB patients (62%) [1] is a challenge for TB diagnosis since people living with HIV often have paucibacillary or extrapulmonary disease that is less likely to be detected by sputum testing [11]. In Lesotho, there is no routine TB active case-finding outside health facilities, but screening of health facility clients is indicated in the national guidelines [12].

With this high rate of TB in the Kingdom, it is vital that every person presenting for care for whatever reason be screened for TB symptoms, tested if symptoms are present and given treatment if diagnosed. We therefore conducted a mixed methods study to evaluate TB screening and understand the reasons for suboptimal screening in two health facilities in Berea district in the Kingdom of Lesotho.

Materials and methods

Ethics statement

This study was approved by the National Health Research Ethics Committee of the Kingdom of Lesotho (ID91-2020) and by Harvard Medical School Institutional Review Board (protocol: IRB20-0109). All people who participated in the interviews and focus group discussions provided written informed consent.

Study design

We conducted a convergent mixed methods study [13] to assess the TB care cascade from screening through treatment completion in two health facilities in Lesotho. This paper focuses on screening, which is the initial step of the care cascade. Qualitative methods and results are reported according to Consolidated Criteria for Reporting Qualitative Research (COREQ) guidelines.

Study setting

The study was conducted in Berea Hospital and Khubetsoana Health Center. Berea Hospital is a district-level referral hospital located approximately 40 km from Maseru, the capital city of Lesotho. Khubetsoana Health Center is a primary-level facility near the outskirts of Maseru. Both facilities offer TB diagnostic and treatment services.

Lesotho’s national TB guidelines indicate that people presenting to health facilities with persistent cough or other TB symptoms should be registered as having “presumptive TB” and should be asked to submit sputum for testing [12]. The guidelines indicate that TB screeners (often lay people) should identify people who are coughing in health facility waiting areas, that people living with HIV should be screened at every clinical encounter, and that TB screening should be routine in all health facility departments. All those with TB are initiated on treatment, which is available for free throughout the country.

Quantitative data collection and analysis

We sought to assess the proportion of people who attended the two health facilities during March-August 2019 who were screened for TB. To define the target population, we estimated the total visits to each health center during the analytic period based on monthly reports to the district health management office, summing up the total visits made to the outpatient department, ART clinic, antenatal clinic, under-five clinic, and family planning clinic. We collected data on the number of clients screened for TB from the paper-based TB screening register, and we collected data on the number of clients with TB symptoms from the paper-based presumptive TB register. We manually counted the number of people entered into each register by month and entered the data as aggregate numbers into a Microsoft Excel spreadsheet for analysis. We calculated the percentage of people screened by dividing the number screened by the total estimated visits to the health facilities, assuming that each visit corresponded to a single visitor who should be screened (i.e., a person accessing health services for him/herself or a guardian bringing a child to access services).

Qualitative data collection

Purposeful sampling was used to identify participants for qualitative data collection. To maximize variation, we included participants who had a wide range of experiences with TB care in Lesotho. The participants of both the interviews and focus group discussions (FGDs) were recruited with the help of the nurse managers in both health facilities and then, the research assistant explained the purpose of the study to the potential participants via a telephone call. The majority of the people contacted for the interviews and focus group discussions participated in the study, but we did not collect information on the number who refused.

Overall, there were 53 participants. We conducted a single round of semi-structured in-depth interviews with 15 health care workers; variation was ensured by purposefully sampling for a variety of professional backgrounds (district health manager = 1, TB program coordinators = 2, village health workers = 4, TB screeners = 4, laboratory personnel = 2, and implementing partners = 2). Two FGDs were conducted with nurses; each FGD included 7 participants. We also conducted a single round of semi-structured in-depth interviews with 24 patients.

All interviews and FGDs were conducted by local research assistants (JN, TAM), one of whom was male and one of whom was female. Both were university graduates with over 5 years of research experience and training in qualitative data collection methods. The research assistants did not previously know any of the participants. Interviews took place in a private room at the study health facilities, and were conducted in Sesotho or English, according to the participant’s stated preference. Interviews and FGDs took place in a private room out of earshot of others in the selected health facilities. Prior to the interview or FGD, the research assistants provided a standard introduction to the purpose of the study. No one else was present besides the research assistants and participants. Interviews and FGDs lasted on average between 60 and 90 minutes and were audio-recorded with permission. Field notes were also taken by the research assistants to aid in the transcription process.

Interviews and FGDs followed semi-structured interview guides (S1 Text) that were developed for each population by the lead author (AA, a medical doctor with 4 years of experience working in Lesotho) and second author (HG, a medical anthropologist). The study guide was piloted before the start of the data collection. Topics for health worker interviews and FGDs with nurses addressed training, supervision, supplies, and practices related to screening and diagnostic testing. The patient interview guide covered topics related to care-seeking experiences including access to services and treatment, as well as barriers and facilitators to receiving appropriate diagnosis and care. Because the study as a whole sought to assess the entire care cascade, interview guides explored different steps along the cascade, but this manuscript focuses only on the parts of the interviews relevant to screening. AA and HG regularly reviewed transcripts to monitor data quality and ensure fidelity to the research aims. Transcripts were not returned back to the participants for comments.

Qualitative data analysis

We used an inductive, thematic content analysis approach to identify key concepts related to gaps in TB screening [14]. A subset of transcripts was open coded by AA to identify content related to barriers and facilitators to appropriate screening. HG reviewed the open coding results; discrepancies were resolved through discussion, and the final concepts were developed into a draft codebook. The codebook was piloted and revised by AA and HG; the final codebook consisted of 38 codes and was used to code the dataset using Dedoose version 8 qualitative data management software. Coded data were analyzed inductively by AA to identify an initial set of descriptive themes which were labeled, defined, and supported with excerpts from the data. The initial draft of the thematic categories was created by AA and reviewed by HG. Employing an iterative process, AA and HG examined links between initial thematic categories to develop a set of increasingly higher-level concepts; saturation was reached when no higher-level concepts emerged. This resulted in four comprehensive thematic categories that that were defined and elaborated by AA to explain low TB screening in health facilities (S1 Table). Findings were not shared with patient participants, but health system participants will have access to the findings when they are shared with the two participating health facilities and the TB program at the Ministry of Health.

Results

Screening coverage

District reports recorded 45,699 visits to Berea Hospital and 24,694 visits to Khubetsoana Health Center during the 6-month analysis period. Based on the TB screening register, we estimate that only 22% (n = 9,841) of hospital visitors and 48% (n = 11,840) of visitors at the health center were asked about TB symptoms. Only 2% (n = 218 in the hospital, n = 292 in the health facility) of these individuals were listed in the presumptive TB register as having reported symptoms.

Barriers to effective TB screening

Our study’s qualitative portion revealed four thematic categories that help explain the low percentage of visitors screened for TB and the low percentage reporting symptoms in Berea district. The thematic categories are: (1) Overall staff shortage in health facilities; (2) Lack of adequate training for screeners; (3) Structural barriers create delays that shape patients’ care priorities and (4) Internal mistrust among health care workers about the accuracy of screening, which leads to redundant procedures. Fig 1 shows how these emergent themes intersect.

Fig 1. Conceptual framework for how barriers to implementing TB screening in health facilities result in missed TB diagnoses.

Fig 1

Major thematic categories from qualitative analysis are shown in rectangles.

Theme 1: Overall staff shortages in health facilities

A. Workforce is not tailored to health facility needs

Health care worker participants acknowledged that there were significant staffing gaps at health facilities across the district. They attributed these shortages in part to hiring policies at the central level, noting that staff distribution across different health facilities in the district was not based on the actual on-the-ground needs of a given clinic. Every clinic was allotted the same number of health care workers regardless of the volume of patients or the catchment population. There is a high expectation for the volume of work that health facilities are expected to perform. While new programs are continuously being added, there is no corresponding increase in the number of staff.

“If there is ANC [antenatal clinic] care day… you may find that it’s not easy for you to supervise or mentor that nurse on your program [TB program] because he/she is dealing with another patient. You understand that in this case the nurse is working at ANC and also dealing with TB patients; the supervisor is not able to talk to her about the TB program while she is still busy helping patients at MCH [maternal-child health]. It is not easy to talk to the nurse because the work will be overwhelming”.

[Health worker, ID# 1]

"This [allocation of human resources] was done by the Ministry of Haealth. I don’t know what they were basing themselves on when they came up with it. Different clinics have different catchment areas. For example, Khubetsoana, Ha Koali, and Mahlatsa have different catchment areas, but the staffing is the same; it is like they decided that all clinics will have the same number of nurses without considering the catchment areas, performance indicators, OPD attendance, and how many people are on TB treatment. It’s like the staffing is not based on our data. It’s like they just decided that at the hospital, we need five doctors and 100 nurses just like that.”

[Health worker, ID #2]

One consequence of understaffing is that all staff are expected to provide all forms of care, regardless of their training or affiliation with a given program. Under this work-sharing model, each staff member switches between programs on any given day to ensure that all activities in the facility are covered. The expectation that staff swap roles to meet care demands means that staff must often work without taking any breaks. Staff who complete night shifts cannot return home in the morning because nobody can take over their shift. When staff fall ill they hesitate to take sick leave because they know that this will result in a lack of coverage at the facility. The work-life balance of the staff is significantly compromised. Participants noted that this leads to burnout and negatively affects their ability to do their job.

“Because of the population we are serving, we are still understaffed. For example, the TB department is at the back in this facility; those who are already on treatment–we do not book them on daily basis, and we only book them on Tuesday and Wednesday. This is because we are short of nurses and we cannot afford to have a nurse who works only with TB patients. This is one of the restrictions we have of not having enough human resources.”

[Nurse, FGD, Khubetsoana Health Center]

“I feel like each program has to have a health care worker that focuses on working on it so they don’t have to work on multiple programs at the same time but still bearing in mind that they will have to go on leave whether sick leave or any other leave. They are working at night and have to be off the following day… and in the clinics those things are not happening. You are on call, you deliver two pregnant women, in the morning there is a long queue waiting for you outside and you have to carry on doing your work.

[Health worker, ID #2]

B. Lack of ownership over screening activities

Health care worker participants pointed out that no single individual was formally designated as responsible for carrying out TB screening, which is commonly performed at entry points to the health facility and in waiting areas before a patient sees their caregiver. Screening activities are shared among multiple clinic employees. At any given time, the screening could be performed by an implementing partner, a village health worker, a lay counselor, or other staff members.

Screening activities are generally allocated on a day-to-day basis, and the responsibility for screening often falls to an employee whose primary position is to support another non-TB program. While staff understand that they are required to screen when asked to do so, they do not see it as their job. Participants expressed concerned that this lack of “ownership” stemming from the shared nature of screening activities effectively eliminates the traceability of screening activities and results in an overall decline in the quality of TB screening.

“We have a challenge with the TB screening–that is why we are not getting most of the patients with TB. Because we do not have trained TB screeners, people who are doing the screening are just the facilities’ employees. Moreover, they take turns in the screening of TB; if this week is lay counselor, the other week will be the VHWC [village health worker coordinator]. It is just nobody’s department, so the screening is not done correctly; there is nobody who owns the screening department because no one is trained about screening. That is where the challenge is, and that is why at times when you find samples collected, nobody is feeling responsible because they will say, ‘[he/she was] not there that week, it was so-and-so.’ So screening is not owned by the TB screening department. If there were trained TB screeners, it would have been beneficial.”

[Health worker, ID #14]

“I do it because I find it necessary to do so and because of the staff shortages. It is not in my job description, but because the VHW [village health worker] was already doing that, I had to continue screening patients.”

[Health worker, ID # 6]

"There is no specific person assigned for TB screening. Anybody on duty, that is the one screening for TB, hence why it is sometimes not properly done. Few people are…screened at MCH, only from implementing partners."

[Nurse, FGD, Berea Hospital]

Theme 2: Lack of adequate training for screeners

Employees from other programs who were asked to perform TB screening in addition to their work explained that they were not formally trained on how to screen for TB. They were provided with screening tools but did not receive specific training on how to use them correctly. The TB screening tools are closed-ended questionnaires that ask about key symptoms such as fever, cough, weight loss, and night sweating. These ad-hoc screeners learned about screening on the job, either through informal feedback from colleagues or observing nurses when they screened patients. Continuous refresher training was also not offered.

“I think the gap is visible when the TB screeners are not clear on what to do or how to screen TB in the facilities—especially the lay counselors. If somebody has not been trained or lacks a refresher, the results of the screening by the screener will usually be bad because he/she may miss some patients who have TB and say that they are not presumptive TB patients. So that will impact badly on TB detection.”

[Health worker, ID # 1]

“The people who screen for TB in Berea hospital have never received specific training on how to screen TB. They have just been given the screening tools to screen patients for TB.”

[Nurse, FGD, Berea Hospital]

“We got it [training] once or maybe two times, but usually what happens is that we have meetings as VHWs [village health workers], and during those meetings we discuss different topics and this helps us remember what we had forgotten. And when we have a problem with certain topics, we ask the nurse to help us with them.”

[Health worker, ID#8]

Health care workers and the management team members were concerned that poorly trained screeners could not uniformly apply the screening tool. Furthermore, without training on how to deliver the screening tool, some participants worried that screeners were not properly explaining questions to patients. This could result in inaccurate answers to the screening question, leading to missed opportunities to identify people with symptoms, inaccurate documentation of symptoms, and compromised care. Patients with active TB could return home without a proper diagnosis.

“We miss most of the patients. Most of the TB patients are missed during the screening, and they go home with TB, which was not detected during the screening because of the way they ask questions. Patients respond, and [screeners] miss them, and they go home without being known that they have presumptive TB. Furthermore, they go home and the disease spreads to the families and communities. Later on, they come back very ill, and sometimes they are too ill even to complete the treatment and die in the process because they missed the first time they went to the facility during the screening."

[Health worker ID #14]

“The weakness may be the staff members [TB screeners] not asking the patients the screening questions in a standardized way; they ask them differently on different days."

[Health worker, ID #1]

“Because of lack of training we are missing TB cases. This will result in the rapid transmission of tuberculosis infection and this can be exacerbated with lack of knowledge on how to prevent TB infections. Lack of training also affects in the documentation of the outcome of tuberculosis treatment, particularly on the outcome of ‘died’ [for] TB patients.”

[Nurse, FGD, Berea Hospital]

While participants acknowledge that training is essential for effective and efficient TB screening, there are simply no funds available to train staff on screening procedures.

“I think the ministry always mentions the issues of not having funds. Otherwise, every facility could choose people who could be trained for TB screening. But it is the challenge of unavailable funds for the training.”

[Health worker, ID #14]

“We are actually trained by the national TB and Leprosy program, and we do the step-down trainings if we have been trained. But you may find that there are some hindering issues like hiccups with the funds when we have to decentralize the trainings.”

[Health worker, ID#1]

“Like I said it is finances, human resources–these are the things we lack. So, if we could get support when it comes to these we can be very effective.”

[Health worker, ID#2]

Theme 3: Structural barriers create delays that shape patients’ care priorities

A. Long travel and clinic wait times negatively impact how patients feel when visiting a health facility

Patients and health workers in our sample described the challenges that patients faced when attending health facilities. They had to travel long distances to the facility and often woke up early and left their homes before mealtime. Many had to walk long distances as part of their journey and often struggled to pay for transport. Upon arrival at the facility, many patients were already weak and fatigued, and they knew that they would face an additional hours-long wait before a provider could see them.

“We always queue for a long time at the gate. It brings a lot of fatigue and dizziness.”

[Patient, Berea hospital, ID#7]

“We have a great problem. A person is already very sick, like I have told you that sometimes I even struggled to have food, I have already left home having not taken enough food. When you get to the facility, you get here at 8:00 am only to get consultations at 12 [noon].”

[Patient, Khubetsoana health center, ID#9]

It takes many hours [to go to the facility] because the cars [did not] come straight here [facility], as they wait for passengers.

[Patient, Berea hospital, ID#10]

“Most of the time, [it] is the distance that [hinders] the patient’s accessibility of the facility. Most of the facilities are not accessible because most of the people have to travel for some distance to reach the facility.”

[Health worker, ID#15]

B. Health care workers recognize that long wait times compromise screening

Health care workers understood that patients were focused on seeing their providers as quickly as possible to receive care and begin their challenging trip home. From their view, patients prioritized being seen by the clinician and viewed screening activities as a potential delay that added additional wait time to their already hours-long wait for care. Health care workers expressed concern that, in their view, patients provided answers to a screening question that would not prolong their time at the clinic by requiring them to visit the TB clinic for sputum collection.

“Another one is when they come here for services –just as you saw that long queue outside the gate, I think that happens in almost all clinics–there is always a long queue. People know that they are going to be screened for TB, and if they answer “yes” to one of the questions, that means you are going to take longer to get services because they make you give the sputum and wait for the results and all that.”

[Health worker, ID # 2]

“The patients complain that the counselors or TB screeners make them wait too long, therefore waste their time. For example, I often overheard the patients talking on the corridors complaining that the TB screeners waste their time; therefore, the patients would rather respond ‘no, no, no’ on each and every screening question asked.”

[Nurse, FGD, Khubetsoana Health Center]

“Once a patient has any TB symptoms, he/she is ordered to send the sputum to the TB clinic, so this makes patients unwilling to give out all the answers when being screened.” [Nurse, FGD, Berea Hospital]

Theme 4: Internal mistrust about the accuracy of screening leads to redundancy

After a patient passes through the TB screening process, they will be able to see their provider. While screening should have already been carried out by a screener when they entered the heatlh facility, nurses reported that they do not trust the screeners’ assessment. They therefore take on the additional task of of re-screening patients for TB during their clinical visit. When nurses re-screen patients during clinical consultations, this adds time to the patient visit, and also overloads nurses who are already stretched thin by their clinical duties. This creates service inefficiencies, with highly trained clinicians performing work that could be carried out by minimally trained screeners.

"Even after the counselor or TB screener has screened the patient, the nurse also screens the patient again. This is done because a patient can provide a ’no’ answer to the counselor when being screened, only to admit to having such a symptom when they get to the nurses. So, we always make sure that we ask signs and symptoms of TB at every point that the patient gets to."

[Nurse, FGD, Khubetsoana Health Center]

“[We] re-screen the patient because the patient may be carrying a note that shows that he/she has been screened for TB, but if the clinician feels like re-screening the patient, they do so.”

[Health worker, ID #1]

Moreover, nurses reported screening for TB in the consultation room only if they suspect TB based on physical manifestations, which means that they could be catching the disease only in later stages.

“Loss of weight is one of the skills I use to assess a presumptive TB patient. Sometimes once the patient gets into the consulting room, as a nurse, you recognize that the patient is emaciated. Sometimes just by looking at the patient’s clothes, you will see that they no longer fit on the owner of the clothes. Another assessment is just the physical appearance; like when a patient has [miliary] TB, he/she will not mention night sweats. It is only when I recognize these that I will know the patient is a presumptive TB patient.” [Nurse, FGD, Berea Hospital]

Discussion

In this facility-based study, we found that poorly implemented screening procedures are likely to be a major contributor to missed TB diagnoses among people accessing the health system. We found that less than a third of visitors at the district referral hospital and around half of the visitors at the health center were asked about TB symptoms. While we do not know the reason for this difference, is possible that TB screening activities are less emphasized at the hospital based on the assumption is that patients would have already been screened at their local health center prior to referral to the hospital. Four main obstacles to effective TB screening were identified: an overall staff shortage in the health facilities, lack of adequate training for screeners and health workers in the health facilities, structural barriers create delays that shape patients’ care priorities, and health care workers’ mistrust of the initial screening process.

Our findings showed that the overall shortage of staff and lack of trained TB screeners contributed to the low completion of TB screening. These factors have been found to be major barriers to effective TB screening in other settings as well, contributing to poor service quality, long health service delays, low patient satisfaction, and high staff turnover [15, 16]. One potential solution to the lack of ownership over TB screening activities described by the health care workers in our study would be to introduce trained layperson or community health worker TB screeners into health facilities, which has been shown to increase TB diagnoses [6, 17]. This would require additional resources, as screeners are likely to be more effective if properly compensated [18]; however, using community health workers for activities that do not require a nurse or doctor has been shown to be cost-effective across a variety of health conditions and interventions [19]. Moreover, it would be necessary to integrate TB screening efficiently into the patients’ visits so that sputum collection does not prolong the time that patients spend at the clinic.

Another potential strategy for improving TB screening in the context of understaffed health facilities is better integration of health services. In our study, health care workers mentioned that having insufficient staff to cover multiple vertical programs attending to different health conditions contributed to a lack of prioritization of TB screening–a separate activity not tied to the other programs. Integrating TB screening into standard health facility intake procedures could increase coverage with minimal additional time required [20]. Alternatively, TB screening could be incorporated as a standard evaluation procedure at every clinical encounter, as has been done successfully for people accessing HIV care in many sub-Saharan African settings [21]. Since health care workers indicated that TB screening within the context of the clinical evaluation sometimes occurs already, standardizing and monitoring the process could replace a separate screening procedure. Making screening and sputum collection part of a standard intake or evaluation procedure could potentially also reduce the disincentive for patients to respond positively to TB screening if it reduces the perception of TB screening as an additional activity that prolongs the time spent at the health facility.

While symptom-based screening in health facilities is potentially low-cost and high-yield, it is likely not sufficient to close the gap in TB detection in Lesotho or other similar settings. Known barriers to TB diagnosis in Lesotho include poor access to health care in rural areas [22] and suboptimal logistics for sputum testing [23]. Thus, efforts to improve TB detection cannot be limited to health facilities. Bringing active case-finding services into communities can help to improve TB diagnosis among people who face barriers to accessing health facilities [24]. Indeed, over half of the people with respiratory symptoms identified by the 2019 Lesotho TB prevalence survey had not sought care for their symptoms [25]. Moreover, symptom screening has serious limitations, as prolonged cough has poor sensitivity while broad symptom criteria have poor specificity [4]. Chest radiography offers high sensitivity and specificity as a screening tool, and computer-aided detection software can help to make mass radiographic screening feasible [26]. In settings with high TB burdens, community-based mobile radiography units have been used to reach populations that face barriers to accessing health facilities [27] and have been shown to increase population-level case notifications [28].

Our findings identified gaps in five of the six domains of the WHO framework for the building blocks of health systems (leadership and governance, service delivery, health informatics, health financing, human resources, and pharmacy and supplies) [29, 30]. We found deficiencies in human resources, access to quality TB services, adequate funds for training and hiring of staff, and governance and leadership in prioritizing and allocating the workforce. Moreover, the distribution of staff in the health facilities was not based on the need and patient workload, so data usage for program optimization was low. Weak health systems significantly impact TB programs [31]. Sufficient and equitable staffing, adequate supply of essential commodities, and proper monitoring and evaluation of performance through effective data utilization is critical for eliminating TB.

The study has some limitations. Firstly, we conducted the study in only in two health facilities, so our findings may not be generalizable to the rest of the country. However, by conducting interviews and focus groups with both patients and a variety of healthcare workers, our data captured a range of experiences at both the community, local facility, and district level. Also, due to COVID-19 delays in accessing data at health facilities, this study employed a convergent design rather than the originally planned sequential design, so the quantitative data identifying the significant gap in TB screening was not apparent until after the qualitative data collection was complete. As a result, we did not probe as much as we could have about patients’ experiences and attitudes regarding screening, and we did not specifically recruit patients who had not been screened.

Another set of limitations stems from the paper-based data sources available for the quantitative assessment of screening coverage. To estimate the total number of visits, we assumed that each visit corresponded to a single individual eligible for screening, even though for child-focused services, each visit would involve multiple people, as children would be accompanied by adult guardians. Since cough-based screening is an adult-focused strategy, we believe that using total visits as a denominator is valid, as the total number of visits is likely to be close to the total number of adults coming to the health facility. However, this assumption reflects the lack of systematic screening of children for TB. Our assessment of the number of people screened based on screening registers is also subject to error in both directions. On the one hand, people who were screened twice–once by a screener and once during their clinical evaluation–could potentially be listed on the screening register twice. However, in practice, nurses who screen patients during the clinical evaluation often do not fill out the register. While there is thus substantial uncertainty around our estimate of screening coverage, the challenges revealed by our qualitative findings suggest that even if the registers underestimate the number of patients screened, the quality and consistency of screening is likely to be suboptimal. Finally, individual-level data extraction from paper registers was not feasible given the patient volumes of the health facilities. Thus, we were unable to collect data on important patient-level characteristics such as HIV status, which would have allowed us to assess whether TB screening differed among patient groups.

Conclusion

To close the TB diagnosis gap in Lesotho and other countries with high TB burdens, it is essential to improve TB screening services at health facilities and in communities. Within health facilities, it is necessary to ensure that the staff conducting this activity are properly trained on both adult and pediatric TB screening, and that the coverage and quality of screening is continuously monitored. Different screening models can be considered based on the local health system context; introducing a cadre of lay worker or community health worker screeners where they do not exist could help facility-based screening programs to operate more effectively, as could better integration of TB screening into HIV, antenatal, and other primary health care services. Moreover, active TB case-finding in communities can help to remove some of the structural barriers faced by patients and thus improve in TB detection. These investments are necessary in order to find people living with undiagnosed TB and prevent the unnecessary spread of TB in the community.

Supporting information

S1 Text. Interview guides.

(DOCX)

S1 Table. Supplementary quotations.

Supporting quotes for themes identified in qualitative analysis.

(XLSX)

Data Availability

All data supporting the findings of this study are available within the article and supplementary materials.

Funding Statement

This work was conducted with support from the Master of Medical Sciences in Global Health Delivery program of Harvard Medical School Department of Global Health and Social Medicine (ATA) and financial contributions from Harvard University and the Ronda Stryker and William Johnston MMSc Fellowship in Global Health Delivery (ATA). The content is solely the responsibility of the authors and does not necessarily represent the official views of Harvard University and its affiliated academic health care centers. Additional support was provided by Partners In Health – Lesotho (ATA). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLOS Glob Public Health. doi: 10.1371/journal.pgph.0000249.r001

Decision Letter 0

Megan Coffee, Julia Robinson

26 Oct 2021

PGPH-D-21-00687

Understanding reasons for low tuberculosis detection in a low-resource setting: a mixed-methods study in the Kingdom of Lesotho

PLOS Global Public Health

Dear Dr. Yuen,

Thank you for submitting your manuscript to PLOS Global Public Health. After careful consideration, we feel that it has merit but does not fully meet PLOS Global Public Health’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Please submit your revised manuscript by Dec 09 2021 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at globalpubhealth@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pgph/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

We look forward to receiving your revised manuscript.

Kind regards,

Megan Coffee, MD, PhD

Academic Editor

PLOS Global Public Health

Additional Editor Comments (if provided):

Thank you very much for your submission of your work on "Understanding reasons for low tuberculosis detection in a low-resource setting: a mixed-methods study in the Kingdom of Lesotho". I think the topic and approach are precisely what PLOS Global Health is looking to publish. You will see there are many thoughtful comments and suggestions to ensure the conclusions match the study findings. I hope you find these helpful.

There also are some minor corrections to ensure uniformity and precision in language, though the paper itself is very readable. Thank you and I hope we are able to go forward with this paper, guided by the suggestions included.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Does this manuscript meet PLOS Global Public Health’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: No

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Global Public Health does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: This paper is on an important topic from a high-burden setting and is an important piece of work utilizing a clever methodology. There are major problems, however, with the manuscript that need to be addressed prior to publication.

First, and perhaps most importantly, the paper is really an exploration as to why the rates for TB SCREENING are low, not as to why the rates of TB detection are low. While it is great that the authors present all steps of the cascade from the quantitative analysis, the fact that they only explore the reasons behind low rates of screening in the qualitative assessment really means their paper should focus on this aspect of the cascade. Thus I would suggest that they reframe the entire paper in this way. This should start with the title--which should be changed to state it is TB SCREENING and not DETECTION that will be explored--and carry throughout the paper. I think this might help the authors focus the background and discussion more as well. And while I think it is worth presenting the whole cascade with its results, the authors really should try and target the paper more on TB screening. To this end, it would help to have something in the background about the health care resources/services available in Lesotho as well as other experiences with implementing TB symptom screening systematically (for example this has been done in South Africa for quite some time). I also think it would be important in the discussion section to talk about the limitations of TB symptom screening as part of the care cascade and how it misses many people with active TB, even when done systematically. I find it interesting, for example, that the authors note in their own introduction section in lines 41-43 that screening should preferably done with chest X-ray, thus suggesting they also see a limit to TB symptom screening. But since the bulk of the paper is about why TB symptom screening is not done, I would suggest the authors substantially revise the paper to focus on this. I suspect this will take a couple of rounds of revisions with reviewers, but I would encourage the authors to try and do this if they are willing as there are some rich and important findings in their study.

If the authors want to focus on other aspects of the care cascade, then there are some other findings that merit discussion that are completely unaddressed in their mixed methods. Their rates of sputum collection and submission are strikingly high as are their rates of treatment initiation, and this should be commented on if the authors chose to explore other aspects of the cascade. However, their rates of treatment completion are unacceptably low and this should also be explored. It was not clear to me if authors actually collected qualitative data on these aspects of the cascade and simply chose not to present them for reasons of space/economy or of the only collected qualitative data on why people did not undergo screening. If they have qualitative data on these other aspects of the cascade, they could certainly consider presenting them in a revised manuscript--although I suspect it could get quite lengthy.

My second major concern with the paper is that there seem to be some internal inconsistencies with the data shared in the qualitative assessments and the data in the quantitative cascade. This happens often in mixed methods research, as people are often inconsistent with reporting or understanding the motivations for their behaviors. But when this happens it must be addressed and explored in the discussion section. One example of this is the reported qualitative finding that nurses did not "trust" the screeners to really do the TB symptom screening and thus they re-screened the patients themselves. But if this is true--then it would mean that people were screened TWICE at the health facilities (once by screeners and once by nurses) and rather a higher rate of symptom screening should be reported (unless this is, of course, not really happening or not being "recorded" in a way that was captured in the data analysis). Another example is saying that patients have to wait for long periods of time when they come to the clinic but that they do not have time to undergo TB screening. If they are queued and waiting for a long time, could the screening not also be done then? During the early days of antiretroviral availability in Lesotho, for example, the long waiting times were used to do HIV education and counseling, as people were queuing for hours to wait for physicians. While it may be that people did not want to talk about TB or get "pulled" from the queue to do further TB testing, this should lead to a discussion on the need to better streamline TB screening and testing procedures for people. There are other instances of this throughout the paper that must be addressed in the discussion and limitations section, as some of what people appear to be reporting does not match what the numbers show. This is one of the beautiful things about mixed methods studies in that you have different information coming from different actors/sources. But these things must be discussed.

There is a different in the percentage of people screened for TB symptoms at the hospital versus the health center and the authors should comment on this in the discussion and present any qualitative data they might have that could illuminate the difference. One would expect a hospital to be better staffed and resourced than a health center--although perhaps they were also overwhelmed with too many critically ill patients? Whatever the reason, this should be noted and explored.

The interview guide should be included as an Annex.

There should be a COREQ checklist used to report on this qualitative study and that should be submitted with the revision and noted in the methods.

Was there any attempt in the estimates of number of people who should be screened for TB to account or adjust for TB screening in children, where different symptoms might suggest TB? Where sputum may be difficult to obtain? This should be mentioned since the authors note they used data from the vaccine and under 5 clinics to calculate the number of people who should have been screened for TB.

In line 278-279, the authors note that the "lack of specialization" may be one reason why TB screening was not done. I am not sure if this is their term of if this is what participants gave as a reason. It is worth exploring this further in the discussion as well, since one "goal" of a PHC is that everyone can do multiple jobs--and it is precisely this lack of "specialization" that is the goal in an integrated, holistic system. Screening for TB symptoms is not a complex intervention where "specialization" is needed. So how would this fit in with a whole UHC goal--which I know Lesotho has invested a lot in--as a way to improve TB care? Again, if this is what participants stated as a reason for not doing TB screening, then the authors should report it this way. But this is an important finding that then has implications for trying to get all PHC staff or community health workers to be able to do TB screening and shows the global move towards universal screening may not match with what people on the ground are seeing or want ("specialized people" to do screening).

Some of the language needs to be more scientific and less informal. For example, the test done to look for TB is a cartridge-based genotypic test and not a "GeneXpert" machine (line 45), it is not clear what a "mild" symptom is (line 42). The group that transports the sputum specimens is called Riders for Health (not Riders on Health, line 82). There is also some stigmatizing language used in the paper that should be addressed (i.e. while it is a common epidemiology term to refer to "TB cases" these are people who are living with TB--line 62).

I realize I am suggesting a major re-write/reconceptualization of this piece of work, but I would encourae the authors to consider it if they can. I think since the bulk of the qualitative data are presented on why people are not doing screening, then the paper should be revised around that. If the authors do want to focus on the whole cascade, then they need to present qualitative data on the other aspects of the cascade, because some of the steps are completed at a higher rate than would be expected (sputum collection, initiation in treatment) and others are also much lower than expected (treatment completion).

Reviewer #2: Authors have made a good attempt on the subject matter. Issues requiring attention:

1. Authors need to ensure consistency in the use of British and American, in the abstract the authors have used Supervised the British way and Incentivized the American way

2. The conclusion of the study is not supported by the study findings. The authors have indicated in the conclusion that case finding could improve if health care workers are supervised. I did not see any data supporting this conclusion

3.In the discussion, the authors need to relate their findings with others studies. They made an attempt but not consistently.

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6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

Do you want your identity to be public for this peer review? If you choose “no”, your identity will remain anonymous but your review may still be made public.

For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLOS Glob Public Health. doi: 10.1371/journal.pgph.0000249.r003

Decision Letter 1

Megan Coffee

17 Jan 2022

PGPH-D-21-00687R1

Understanding reasons for suboptimal tuberculosis screening in a low-resource setting: a mixed-methods study in the Kingdom of Lesotho

PLOS Global Public Health

Dear Dr. Yuen,

Thank you for submitting your manuscript to PLOS Global Public Health. After careful consideration, we feel that your paper meets the criteria for publishing except for one small question detailed in the reviewer section, which we would like to ask a minor revision for. Do submit this and we will act right away on this.

Please submit your revised manuscript by Mar 03 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at globalpubhealth@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pgph/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

  • A marked-up copy of your manuscript that highlights changes made to the original version. You should upload this as a separate file labeled 'Revised Manuscript with Track Changes'.

  • An unmarked version of your revised paper without tracked changes. You should upload this as a separate file labeled 'Manuscript'.

Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

We look forward to receiving your revised manuscript.

Kind regards,

Megan Coffee, MD, PhD

Academic Editor

PLOS Global Public Health

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments (if provided):

Thank you very much for your submission. It has been a busy time for everyone in infectious diseases. We appreciate your patience and all the work you did to complete the revisions requested. We are looking forward to publishing this. If you are able to make the small revision or provide feedback on "visitors" raised by one of the reviewers, that is the only outstanding issue. We can move along quickly without sending out to further reviewers, just do reach back about the "visitors" comment.

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. Does this manuscript meet PLOS Global Public Health’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Global Public Health does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The authors have done an excellent job revising this paper, and they have addressed all the comments made by me and by the other reviewer. I realize this involved a substantial amount of work and re-analysis, and I am impressed at how thoughtfully and thoroughly the authors were able to update the paper. The work is much stronger now and makes a compelling piece of evidence on one aspect of the TB care cascade that is failing.

I have one very minor comment to make. The authors use the term "visitors" to the health facilities, and I understand this to mean people who are coming there to seek health care. However, when referring to the hospital, the term visitors could also mean people who are there to visit family members or other people who are sick in the hospital. Are these people also screened for TB? Should they be? Or do the authors mean to use the term "visitors" to convey people who come there seeking care? I realize this is minor, but the term should probably be clarified somewhere in the paper (i.e. a small sentence saying "We use the term "visitor" to denote people who came to the facility seeking health services" if this is in fact what is meant. I do note that the authors state that family members often brought children for care and those family members are screened as well, so maybe they do mean the term to encompass anyone entering the facility for any reason, and if so, this should be mentioned.).

Thank you for taking the comments into account and doing such a nice round of revisions.

Reviewer #2: The authors have addressed most the issues that were raised in the previous submission and the manuscript reads well. They may wish to correct a few issues:

1. In the abstract they have used TB screeners, this is not an official term in reference to the health care workers involved in screening for TB. The author may consider using the term clinical team

2. In line 83 the term once found positive for TB symptoms, can be substituted with TB presumptive

3. In line 108 - 112 the authors need to observe the space before the = sign

4. in line 477 I suggest that for the reference 29 and 30 they use close the square brackets for each reference as [29], [30]

Otherwise well done to the team

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

Do you want your identity to be public for this peer review? If you choose “no”, your identity will remain anonymous but your review may still be made public.

For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: Yes: Patrick Lungu

**********

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLOS Glob Public Health. doi: 10.1371/journal.pgph.0000249.r005

Decision Letter 2

Megan Coffee, Julia Robinson

13 Feb 2022

Understanding reasons for suboptimal tuberculosis screening in a low-resource setting: a mixed-methods study in the Kingdom of Lesotho

PGPH-D-21-00687R2

Dear Dr Yuen

We are pleased to inform you that your manuscript 'Understanding reasons for suboptimal tuberculosis screening in a low-resource setting: a mixed-methods study in the Kingdom of Lesotho' has been provisionally accepted for publication in PLOS Global Public Health.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. A member of our team will be in touch with a set of requests.

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they'll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact globalpubhealth@plos.org.

Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Global Public Health.

Best regards,

Megan Coffee, MD, PhD

Academic Editor

PLOS Global Public Health

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Reviewer Comments (if any, and for reference):

Associated Data

    This section collects any data citations, data availability statements, or supplementary materials included in this article.

    Supplementary Materials

    S1 Text. Interview guides.

    (DOCX)

    S1 Table. Supplementary quotations.

    Supporting quotes for themes identified in qualitative analysis.

    (XLSX)

    Attachment

    Submitted filename: Reviewer response.docx

    Attachment

    Submitted filename: Response to reviewers.docx

    Data Availability Statement

    All data supporting the findings of this study are available within the article and supplementary materials.


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