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PLOS One logoLink to PLOS One
. 2022 Dec 30;17(12):e0278592. doi: 10.1371/journal.pone.0278592

Why health system diagnosis delay among tuberculosis patients in Illubabor, Oromia region, South West Ethiopia? A qualitative study

Jira Wakoya Feyisa 1, Jiregna Chalcisa Lemu 2, Megersa Dinku Hunde 2, Robera Demissie Berhanu 2, Debela Dereje Jaleta 2, Diriba Kumara Abdisa 3, Tadesse Sime Garedow 2, Keno Melkamu Kitila 4,*
Editor: Yasir Bin Nisar5
PMCID: PMC9803213  PMID: 36584005

Abstract

Background

The main target of tuberculosis control and prevention is to detect incident cases as quickly as possible and also to prevent the occurrence of disease. It is also the responsibility of the health facility to screen the contacts, identifying children for prophylactic therapy. However, the target is difficult to meet due to issues within health facilities that cause health system diagnostic delays. Despite this, there is no information explored why health system diagnostic delays among tuberculosis patients.

Method

A qualitative study was conducted by using different data collection methods and sources. Seventeen DOT providers, five laboratory professionals, six program managers, and seven Tuberculosis patients were interviewed. In addition, 22 governmental health facilities were observed for the availability of resources. Data obtained from the in-depth interviews was transcribed, coded, categorized, and thematized manually.

Result

Health system Diagnosis delays reasons were related with sample collection procedures, poor competency of health professionals, in addition to absences or scarcity of health professionals, medical products, and basic infrastructure. We found 18 health facilities without skilled personnel in the OPD, 7 health facilities with a broken microscope, and almost all health facilities without a separate room for sputum examination. Furthermore, 12 (54.5%) and 14 (63.6%) health facilities lacked access to water and electric power, respectively.

Conclusion

Many reasons for TB diagnosis delays have been identified in the study area. Poor competence of health workers and scarcity of resources were identified. Depending on the finding, we suggest strengthening the health workers’ training. Concrete strategies need to be designed to retain professionals. Training on human resource planning and budget preparation is needed for front-line managers. Managers have to work on the maintenance of diagnostic tools and facilitate transportation. The rural health facilities need to use another alternative power source.

Introduction

Tuberculosis has been declared a global public health emergency for the past 25 years because it is the prominent reason of death from infectious disease among adults [1], with 7.1 million tuberculosis cases in 2019 [2]. Early diagnosis of TB cases are the cornerstones of global TB control initiatives [3]. Despite breakthroughs in knowledge regarding the importance of early case detection and treatment, the health system continues to miss millions of tuberculosis cases, resulting in long-term transmission and a rise in the pool of people at risk of contracting and developing the disease [4].

The gap between a patient’s first visit to a health care facility with symptoms of tuberculosis and the diagnosis of tuberculosis is referred to as the health system diagnostic delay. Actually it will be considered as health system delay if it is not detected on the first visit [5]. Early diagnosis of tuberculosis cases has been identified as a key impediment to TB control, particularly in low-income countries such as Ethiopia [6]. It causes a severe acute phase of the disease. Furthermore, despite "free services" for TB, it results in TB patients suffering significant pre-diagnosis costs for care seeking [7–9].

According to the findings of a systematic review and meta-analysis, health system diagnosis delays ranged from 2 to 128.5 days, whereas they ranged from 6 to 28 days in other studies conducted in Ethiopia among tuberculosis patients [10, 11]. The number and type of providers encountered prior to TB diagnosis, educational status, level of severity, types of symptoms, and first visited health facility are all factors that contribute to health system diagnosis delay [9, 12–14].

The Ethiopian government has prioritized the control of tuberculosis (TB) and has placed TB prevention and control as one of the country’s priority health initiatives in the country’s Health Sector Transformation Plan (HSTP) [8]. In Ethiopia, TB case notification has been mostly based on passive and community-based enhanced TB case finding, with a focus on diagnosing TB among those who actively seek medical care with TB symptoms or who are recognized in the community by health extension workers. With this technique, the program was able to detect less than two-thirds of the annual projected TB cases, necessitating the implementation of additional but effective strategies in order to meet the lofty targets set by END TB by 2035 [15].

Furthermore, in order to improve timely case detection, care, and prevention of further transmission while maximizing resources, the national TB control program needed to re-orient the approach with an additional systematic and targeted screening strategy among close and household contacts of infectious TB cases, among high-risk populations, and for key populations where TB usually concentrates. Moreover, since 2013, Ethiopia has been establishing a public-private-mix (PPM) initiative to include the private medical sector in providing TB services. However, only a tiny percentage of the private sector is participating [16].

Despite the growing number of quantitative studies on health system diagnosis delays, there is limited information on the causes of health system diagnosis delays explored qualitatively. As far as we know, no studies have been undertaken in the study area. Furthermore, contributing factors differ across societies, types of health facilities visited, and geographical regions between population groups in the same local settings and disease categories. Localized studies are needed to uncover area and population-specific characteristics linked to extended TB health system diagnosis delays. As a result, the goal of this study was to find out why health care providers in the Illubabor zone take so long to diagnose tuberculosis patients.

In the fight against tuberculosis, it’s critical to have a good understanding of what causes health system diagnosis delays. The findings of this study could help in the development of treatments targeted at increasing early diagnosis of tuberculosis cases in order to commence effective chemotherapy and reduce the risk of disease transmission in the public as well as the burden of morbidity in patients. Similarly, the research can assist healthcare practitioners in providing appropriate information to improve TB diagnosis in time, particularly in the study areas.

Furthermore, the findings of this study can be used by the Illubabor Zone Health Department to build and develop a local plan and implementation strategy to reduce health system diagnosis delays. Finally, the study is important in that it provides information to government policymakers, program planners, and non-governmental organizations (NGOs) so that they can develop relevant interventional strategies. It may also encourage other researchers and policymakers to conduct more extensive research in this area.

Methods and materials

Study setting and period

The study took place in Illubabor Zone health facilities in the Oromia region, South-West Ethiopia, from March 15, 2021, to October 1, 2021. The zone is 600 kilometers from Ethiopia’s capital city, Finfinnee/Addis Ababa. In 2021, there were 13 rural districts and one town administration in the Illubabora Zone. Currently, forty (40) public health facilities and five private clinics in the Illubabor zone provide DOT diagnosis and treatment.

Sample size and sampling techniques

In-depth interview

Through a purposive selection using an intensity sampling technique, twenty-eight health professionals with at least six months of experience in diagnosing and treating tuberculosis, or leading a tuberculosis control program, were included in the study [5]. We picked this sampling technique because it allowed us to reach out to people with a lot of knowledge, allowing us to acquire a complete picture of the reasons behind tuberculosis diagnosis delays. Seventeen DOT providers, five laboratory experts, six program managers, and seven tuberculosis patients (a total of 35 key informants) were interviewed to learn more about the delays in tuberculosis diagnosis. These groups were chosen because they were thought to be knowledgeable about their jobs. When two or more DOT providers were present at the same location, the more experienced provider was chosen. Seven TB patients on treatment were selected for in-depth interviews from seven treatment sites using a "maximum variation" sampling technique, which allowed access to patients with a variety of background characteristics [17].

Facility observation

Seven districts and one town administration were chosen by the lottery method among 13 districts and one town administration [11]. Consequently, 22 governmental health facilities, including two hospitals, eight urban health centers (placed in districts or zonal towns), and 12 rural health centers were chosen from the sampled districts. Thus, different types of health facilities were included from a variety of districts to obtain a comprehensive picture of the presence or absence of necessary infrastructure and other resources for TB case diagnosis. To acquire a comprehensive picture of the presence or absence of necessary infrastructure and other resources for TB diagnosis, various types of health facilities from a variety of areas were included during observation.

Data collection method and tool

Piloted interview guide questions were utilized for both the KIIs and the observations. We employed a variety of approaches to collect data. First, key informants in charge of directing or coordinating tuberculosis control programs at various levels, as well as those responsible for delivering DOT at the facility level and TB patients, were interviewed. All of the participants were approached face-to-face, and none of them declined to participate in the study. The interview guide was translated into Afan Oromo by an English language expert who is also an Afan Oromo native speaker and then re-translated into English.

The authors conducted in-depth interviews using the local language to learn about health workers’ and patients’ experiences and perspectives on the reasons for diagnosis delays. Various people were interviewed in order to gain as many opinions as possible on the study’s ultimate goal. After transcribing the day’s work and preliminary analysis, redundancy of responses was considered saturated and was deleted every evening.

The data gathering team consisted of Principal Investigators (male lecturers) with secondary level qualifications (MPH). The study offered confidentiality to participants, and the interviews took place in a private setting. We did our best to make the study participants feel at ease by engaging them in small conversation for the first few minutes. To ensure triangulation of the data with the record, the team captured the data and took notes, including memos of participant behaviour and context. The interviews were done as a dialogue rather than asking and answering questions. The interviews lasted 60 to 90 minutes and were audio-taped and transcribed verbatim, with descriptive field notes written after each of the interviews.

Second, governmental health facilities were inspected using a predetermined checklist to gain an overview of the current condition in terms of the availability of necessary infrastructure and other resources, such as electricity, human resources, and TB diagnostic reagents. It was conducted by observing the TB room, laboratory room, outpatient department (OPD), patient waiting area, and general infrastructure, as well as interviewing the responsible individuals in the relevant facilities’ units. Each facility’s observation lasted 50 to 70 minutes. The authors were in charge of the facility inspection. The data gathering methods were created using national and WHO TB control program guidelines, as well as existing research [6–8].

Data analysis, data quality control and trustworthiness

The data analysis for the in-depth interview began with daily transcription and preliminary analysis during the data collection phase. The writers transcribed all of the audio-taped interviews and then double-checked the transcript by listening to the recordings. Descriptive notes were recorded when reviewing the transcripts. This included the addition of new probing questions as well as the consolidation of some of the interview guide’s other questions. A health management specialist who is a native speaker of the local language (Afan Oromo) assessed de-identified audio-taped interviews for peer debriefing (transcripts).

The data coding and categorization were done manually by the authors. The material was identified and analyzed using a thematic analysis approach. The information was organized into sample collection procedures, poor competency of health professionals, absences/scarcity of health professionals, scarcity of medical products/technologies, and absence/scarcity of basic infrastructures. Finally, we attempted to provide a general picture of what all of the survey participants described as their perspectives and experiences with regard to the reasons for TB diagnosis delays. The information was supplied in the form of descriptions of events and experiences that were pertinent to the study’s goal [9].

The frequency of presence and absence of specified resources, as well as an acid fast bacilli (AFB) reagent stock-out, were checked and computed using facility observation data. Narrative data was also compiled based on observations of each health institution and its surroundings. As a result, the observations from the facilities were used to confirm the conclusions from the in-depth interviews, as well as to enhance and deepen the data interpretation.

Triangulating data sources and data collection methods helps to challenge data from a variety of sources. The information gathered from many people at various levels was used to obtain experiences of those working in the TB control program, as well as the patients who received care [10]. The interviewers (authors) also made every effort to ensure that their relationship with the study participants was founded on trust so that they felt safe.

The interviewers were familiar with the local languages and cultures, and they believed they had established an "optimal" (insider-outsider) distance from the study [11]. They considered themselves insiders because they spoke the native languages fluently, which helped them grasp the situation. By not collaborating with DOT providers and program administrators, the outsider status was kept in part.

Ethics approval and consent to participate

Ethical approval was obtained from the Research and community Service Coordination Office (RCS) of Mettu University Faculty of Public Health and Medical Sciences with Ref. No RCS/114/13. Before the start of data collection, written informed consent was obtained from each of the study participants after information was provided about the nature and the study’s goal. Participants were informed that they have the right not to participate in the study or can withdraw at any time. Furthermore, privacy and confidentiality were ensured by using numbers to identify and describe the study participants.

Results

Background characteristics of the study participants

From total 35 study participants took part in the in-depth interview, 28(80%) are health professionals, of which 23(82.8%) of them were male and 19(66.7%) of them were between the ages of 25 and 34. In terms of educational attainment, 20(72.8%) had a bachelor’s degree, and 19(68.2%) had > 5 years of work experience for their current position or responsibility (Table 1).

Table 1. Characteristics of the study participants for in-depth interviews in the Illubabor Zone, 2021.

Characteristics of respondents Categories Frequency Percentage
Health workers(n = 28)
Sex Male 23 82.8%
Female 5 17.2%
Age ≤24 -
25–34 19 66.7%
≥35 9 33.7%
Education level Diploma 4 13.6%
Bachelor degree 20 72.8%
Masters 4 13.6%
Experience <2 years - -
Years 9 31.8%
>5 years 19 68.2%
Patients(n = 7)
Sex Male 3 42.9%
Female 4 57.1%
Age <24 2 28.6%
24–34 2 28.6%
>35 3 42.8%
Type of TB Pulmonary TB 6 85.7%
Extra pulmonary TB 1 14.3%
Duration of treatment ≤2 months 3 42.8%
>2months 4 57.2%
Residence Urban 5 71.4%
Rural 2 28.6%

Qualitative findings

From the analysis of the in-depth interviews, five major themes were identified. The major themes were: sample collection procedures, poor competency of health professionals, absences/scarcity of health professionals, scarcity of medical products/technologies and absence/scarcity of basic infrastructures. Each was narrated with expressive quotes from participants.

The sample collection method

Some laboratory professionals reported that the current approach to sputum collection might lead them to report false negative results. They explained that in the previous approach (spot-morning-spot), morning sample had a high chance of getting the mycobacterium tuberculosis under the microscope. They mentioned that the morning sample was highly concentrated. In contrast to this, the current approach (spot-spot) is susceptible to collecting saliva only, which has a low probability of getting the mycobacterium tuberculosis under the microscope. One participant stated:" We are collecting saliva, which is inappropriate sample."

Consequently, the participants suggested that more advanced research has to be done. According to their reports, the difference between the results of a sample from spot-spot and spot morning spot was significant. One participant said:"… As to me, it is better to conduct sophisticated research."

Poor competency of health professionals

Most of the study participants mentioned poor competency of health workers who were failing to request a necessary diagnostic investigation. They emphasized patients are suffering in the health facilities after consulting the health professionals.

One participant said:"… in our health facility, diagnosis delays are happening because of misdiagnosis at OPD level.”

Additionally, respondents reported that the laboratory professionals’ slide preparation led them to false negative reports. That means they are not preparing the slide with the appropriate procedure. One participant said:"… for instance, if you observe their slide preparation, it is very poor in some health centers."

The participants (program managers, DOT providers, and laboratory professionals) described possible causes for the lack of health workers’ competency. The first reason mentioned was an absence of in-service TB training for all general practitioners, health officers, and laboratory professionals to provide quality TB services for their clients. One participant explained:"… concerning the quality starting from the OPD, they are not well updated with the new algorism method, including the general practitioner.” Another participant said, "According to our health center, only one health professional was trained on tuberculosis from the outpatient department." AS participants said if the managers think proactively, it is possible to give training for all health workers.

The Second complaints by seniors about professionals’ competency were that higher education institutions are not producing competent graduates. They also underscored that the ministries of health and education have to take the necessary measures to correct the issues. One participant said:"… compared with the past, higher education institutions are producing professionals with unsatisfactory skills."

The third reasons raised by the participants were non-utilization of national TB control program guideline. According to their idea among health professionals who have taken the training most of them are not doing accordingly. Even they have already dumped the guidelines to their home from which have taken the training. They are not doing according to guidelines which leading them to inappropriate history taking so that they miss right diagnosis and, miss diagnosis is the possible reason for diagnosing the other upper respiratory tract infections. Then prescribing antibiotics for the patients and patients back home without having the right diagnosis and treatment and then come back again after days or weeks for the patient is not relieved form his/her complaint. These not utilizing guidelines in turn explained due to the lack of close supervision.

Evidence from observation mentioned, that national TB control program(NTCP) guideline was not available in 16(72.7%) outpatient departments, 18(81.8%) laboratory rooms, and 12(54.5%) TB rooms of the facilities.

Absence/Scarcity of health professionals

A majority of the study participants among the DOT providers and program managers at various levels reported that there was a scarcity or absence of trained health professionals, particularly in the outpatient and laboratory departments, which caused TB diagnosis delay.

One participant explained, "The main reason for diagnosis delays happening in our health facilities is the scarcity of laboratory health professionals."

Moreover, our findings from observations at health facilities show that there was an absence of trained professionals at OPD in 18(81.8%) of the facilities. The respondents gave emphasis on the reason for health professional scarcity, which they mentioned as the cause of diagnosis delay. The scarcity of health professionals is related to high turnover as a result of joining non-governmental institutions, education, and transfers to urban health facilities. The other reason for the delay in diagnosis is related to the absence of recruitment as per usual. The government is not recruiting health professionals immediately after graduation as a result of the scarcity of budgets. Additionally, significant numbers of university graduates are not passing the competency exam. According to the participant’s explanation, this condition is creating a huge gap in the midst of high professional demands.

One participant stated:"… the reason for health professionals’ scarcity could be the unemployment of university graduates immediately after graduation."

Consequently, almost all the participants stated that high work overload is making it challenging to diagnose TB early. According to their reports, health professionals are not doing their work with adequate time because their intention was just to address the high patient flow.

One participant said, "… because of high patient flow, we are missing the opportunity to request an appropriate laboratory investigation, which is the reason for misdiagnosis."

One patient said, "… I visited three health facilities before my case was known; just as I entered the examination room, the health professionals gave me a prescription without asking me to address a lot of patients in the waiting area."

The participants reported that the work load was caused by the absence of the required health worker-to-population ratio standard by WHO. The DOT providers emphasized that their managers were ordering them to clerk more than sixty patients per day. This problem in turn happened as a result of not strictly requesting workers, and on the other hand, when the front line manager requests human power, the higher managers raise the budget scarcity issue. Accordingly, if the problem is not resolved, early tuberculosis diagnosis is out of the question, as per the participants.

Scarcity of medical products/technologies

The absence of diagnostic tools like updated or functional microscopes, X-rays, functioning Gene expert machines, and a shortage of AFB reagents were major reasons for the delayed diagnosis of TB, as reported by many of the laboratory professionals and program managers.

One participant mentioned that "the absence of diagnostic tools like X-ray, AFB reagents, and microscopes is the reason for the delay in diagnosis of TB."

From observation, in 7(31.8%) health facilities, microscopes were not functional and only 2(9.1%) health facilities had X-rays. The AFB reagents were not available in the drugstores of most health facilities: acid alcohol in 15(68.2%), carbol-fuchsion in 17(77.3%), and methylene blue in 14(63.6%) health facilities on the day of observation. Functional weighing scales and masks were not present in 11(50%) and 13(59.1%) of the TB rooms of the facilities, respectively. Nevertheless, these resources are supposed to be available in all 22 health facilities.

According to participants, the possible causes of the shortage of reagents were a failure to timely distribute them to the health facilities, which was related to the absence of timely requests. Even though the reagents are prepared in decentralized local regions, the transportation mechanism does not maintain their quality. Additionally, participants were complaining about the lack of a vehicle or motorcycle for the laboratory department to bring the reagents to the Zonal level.

"Most of the time, we are not supplied with AFB reagent on time, and even when it comes, they only supply us with local bottles that are not packed appropriately," one participant explained.

Participants also mentioned the cause of scarce diagnostic tools like microscopes and gene experts as the absence of timely maintenance for failed machines. One participant said, "Now the time you are interviewing me, the Gen expert machine is not functioning, which is only found in hospitals and used for all health centers in the zone.”

One patient undergoing directed observed treatment describes his ordeal: […].My result was delayed after I came to the health facility because of the machine not functioning, which is used for drug initiation. […](A TB patient)

Participants explained the lack of timely machine maintenance as not having trained technicians who maintain it. They stated that now they are calling for technicians from Addis to fix these machines. As a result, delays happen until the technician comes from a long distance. One participant stated: "We are calling the technicians from Addis Abeba to fix the machines which are resulting in the tuberculosis diagnosis delay."

The other idea, according to the participants, was that most of the microscopes being used in their healthcare set up are out-dated. They emphasized that our country is not using advanced technologies that are coming with new versions of machines. For this reason, they mentioned these out-dated machines may be the possible cause of the TB diagnosis delay. One participant mentioned that, "to your surprise, most of the microscopes working in our health facilities are out-dated.”

Absence/Scarcity of basic infrastructure

Most of the participants mentioned the absence of adequate rooms, water supply, and electricity. Several rural health centers lacked clean water, electricity, a patient waiting area, and a sputum collection area.

From observation, there were no waiting areas for patients in 7(31.8%) of the health facilities. Of those who had patient waiting areas, none of the health facilities had a separate waiting area for TB patients. Moreover, no health centre had a sputum collection area, and only one hospital had a separate laboratory room for sputum examination. The 12(54.5%) and 8(36.4%) health facilities didn’t have water supply and electricity, respectively.

The majority of study participants mentioned that limitations in laboratory room space and a separate sputum collection area were the causes of delayed diagnostics at health facilities. They said this could happen as a matter of poor building design. This led patients to give the samples using the same window. They said since limited space increases the chance of transmission for other patients, we appoint suspected cases after a certain time when patient flow decreases. One participant said, "We are intentionally delaying the diagnosis of TB to decrease the chance of index case contact with other patients because they bring samples via one window.”

Several participants gave emphasis to the absence of electricity and a standby generator as major factors in the diagnosis delay.

One participant explained, "One day I had scheduled the suspected TB patients for the next day because there was no light."

One patient said: […]. In fact, my results were delayed in the health facility due to appointments. [..]. (A TB patient)

According to the participants, the causes of limited basic infrastructure like water and electricity are scarcity of budget allocation and low community participation in fostering the basic infrastructure. Other issues identified were a lack of engagement with other aiding agencies or non-governmental organizations. Also, a lack of regular supervision was raised by participants. Most of them reported a lack of vehicles as the main obstacle to conducting supervision. Also, the COVID-19 impact was mentioned significantly. When the pandemic struck the country, most of the usual plans were disrupted.

Discussion

The present study explored laboratory professionals’, DOT providers’, patients’, and program managers’ views and experiences related to health system diagnosis delays among TB patients in Southwest Ethiopia. Our findings suggest that there are different reasons for Health system diagnosis delays in the study area. The major reasons were issues related to sample collection methods, poor competency of health professionals, absences /scarcity of health professionals, absences or scarcity of medical products or technologies, and absences or scarcity of basic infrastructure.

As mentioned by laboratory professionals, the current sputum collection method (spot-spot) has been leading them to Health system diagnosis delay. The different studies’ findings, including systematic review and meta-analysis, were against this finding [18–20]. Early morning sputum samples (EMS) are generally considered to yield a greater number of positive results than spot samples and to have higher sensitivity and specificity for culture, yet the published data to support this assumption is scarce. Moreover, spot samples were found to be at least as good as EMS for identifying M. tuberculosis prior to and during TB treatment and do not support the superiority of EMS over spot samples in a clinical trial setting. Spot-spot sputum sample collection also reduces the number of visits by patients and helps in preventing drop-outs. Possible explanations related to the spot-spot sample collection method’s delay might be the volume and quality of the sputum sample collected, the time to pro- cessing and transport conditions, and the proficiency of the laboratory professionals [19]. We propose that patients receive education before or during a spot sputum collection, including instructions on how to create sputum, advice on breathing exercises, and training for laboratory workers.

Poor competency of healthcare providers was another reason explained for contributing to health system diagnosis delays among tuberculosis patients. The discovery is supported by laboratory research [21, 22].The possible justifications are: skilled laboratory professionals can conduct diagnostic procedures correctly; competent health care providers working at OPD can take an appropriate history and do physical diagnosis accordingly so that he/she can request an accurate investigation. In this study, participants mentioned pre-service insufficient quality of education, a lack of all-inclusive in-service training, and not utilizing TB guidelines. Therefore, we suggest that health facilities at all levels should consider equipping health workers via training. Also, the ministries of health and education need to do more in collaboration to produce competent workers.

As mentioned by the TB control program coordinators, the health workers were diagnosing TB without special training on Tuberculosis. This finding is similar to studies conducted in different resource-limited countries [8, 23, 24]. They explained it as a result of turnovers of trained workers, which in turn happened because health workers transferred to the urban setting and were interested in joining non-governmental organizations. However, to accelerate progress towards universal health coverage and the UN Sustainable Development Goals, ensuring equitable access to health workers within strengthened health systems has planned strategic directions [25]. So, the scarcity of trained health care workers will have a negative effect on early TB diagnosis after patients visit health facilities [26]. This finding indicates that many things are expected from managers to make available health workers at all levels. For example, a sound retention strategy may motivate health workers to work in rural and remote health facilities.

Another reason mentioned for the scarcity of trained health professionals was the absence of timely recruitment, which is again due to budget scarcity and the need to request the needed health work force timely. This may also increase Health system diagnosis delays in health facilities. As a result, strategic health workforce management and the acquisition of new employees on a regular basis are needed [27]. For this reason, we suggest that training be given on human resource planning and budget preparation for the low-level managers so that such a problem can be tackled.

In Sub-Saharan countries like Ethiopia, most health facilities use AFB smear microscopy for TB diagnosis [22]. But, this study revealed that there were shortages of microscopies related to absence of maintenance, and similarly, the Gene Expert machines, which are being utilized for anti-TB initiation, were not working during the data collection period. Previous studies also reported similar findings [7, 8]. Because of malfunctioning microscopies, patients would be left without getting an accurate diagnosis; on the other hand, they might be referred to another health facility for laboratory investigation. Furthermore, if the Gene expert is no longer able to provide an immediate solution, patients may be transferred to another hospital to begin anti-TB treatment. These conditions worsen TB diagnosis delays. In Ethiopia, the health sector transformation plan has also prioritized access to more sensitive screening tools, such as chest X-ray and GeneXpert, for diagnosing tuberculosis [28]. However, access to updated tools (such as a fluorescence microscope) [29] and a lack of timely diagnostic machine maintenance are to blame. We suggest that the Federal Ministry of Health and Regional Health Bureau have to work on the maintenance of malfunctioning diagnostic tools. This could be realized by working with biomedical engineers so that they can avail themselves of professionals needed to maintain malfunctioning tools. In one or the other ways, the respective stakeholders sought to update the laboratory machines with time.

Laboratory professionals acknowledged interruptions of AFB reagents as a reason for diagnostic delays in health facilities. Similar findings are reported by different studies [14, 23, 29]. Due to the absence of AFB reagents, patients would be referred to hospitals and higher-level private health institutions where they could be available. The possible reasons mentioned by participants for not availing of reagents in a regular manner were a lack of a motorbike for this purpose and not requesting them on time. This implies the managers are expected to facilitate transport mechanisms and strengthen regular monitoring so that they can close the gap, increasing the chance of Health system diagnosis delay.

The current study has identified inadequate room to perform laboratory activities, an absence of electricity and running water. This finding is similar to studies done in other resource-limited countries [14, 24]. It is justifiable that using a microscope is not possible without electricity, which could have a high potential to create diagnostic delay. Even though Ethiopia has the goal of achieving universal access to electricity by 2025, only 44% of urban and 31% of rural Ethiopians have access to electricity [30]. In such a context, until the goal is achieved, we suggest that the rural health facility needs to use another alternative power source like solar energy, biogas, or generator.

Inadequate working space, the absence of a sputum collection area, and a separate laboratory room for sputum examination were identified as means of diagnosis delay in health facilities. This finding is also supported by previous studies [14]. The participants explained that delays can occur as a result of space constraints due to fears of cross-contamination among suspected patients and others. Laboratory professionals were postponing suspected patients for some hours after the other patients were seen. This scenario might lead the patients to dropout and return another time with a delayed case created as a result of a health facility problem. We propose that the existing health facilities need to be redesigned in order to curb the problem. So the strategic road map, which involves different stakeholders, needs to be developed.

As a limitation, the present study excluded the views of health extension workers. We interviewed patients who had visited public health facilities, but not those individuals who had visited private clinics, and observation was not done for private clinics. Thus, we might miss essential information regarding factors affecting diagnosis delays in private clinics. Moreover, the responses from the study participants might tend to be positive and may not fully address their concerns (social desirability bias) since most of the interviews were conducted at health facilities. We attempted to reduce this bias by informing them about the objective of the study, assuring their confidentiality and using indirect questioning, which meant asking about what others thought and felt. As strength of the study, we used in-depth interviews and facility observations. In addition, we have included health centers, primary hospitals, and specialized hospitals. This helped to provide a great number of data sources and triangulation methods.

Conclusion

Many reasons for TB diagnosis delays have been identified in the study area. Poor competencies of health professionals, absences or scarcity of health professionals, scarcity of medical products or technologies, and absences or scarcity of basic infrastructures were identified. The limited basic infrastructure identified included running water, electric power, and room. Scarce medical products were the absence of updated or functional microscope machines and timely maintenance of diagnostic tools.

Preventing delays in diagnosis of tuberculosis is a crucial measure in achieving the Stop Tuberculosis strategy. Therefore, we suggest strengthening the health workers’ in-service and pre-service training. Concrete strategies need to be designed to acquire and maintain adequate and competent professionals. Training has to be given on human resource planning and budget preparation for the low-level managers. The Federal Ministry of Health and Regional Health Bureaus have to work on the maintenance of malfunctioning diagnostic tools, which could be realized in collaboration with biomedical engineers. The managers are expected to facilitate transport mechanisms to avail reagents and strengthen regular monitoring so that they can close the gap. Rural health care facilities must use an alternative power source such as solar energy, biogas, or generators. Finally, we propose that the existing health facilities need to be redesigned in order to curb the problem related to the room.

Supporting information

S1 Checklist. Checklist for facility observation.

(PDF)

S2 Checklist. Consolidated criteria for reporting qualitative research (COREQ) checklist.

(DOCX)

S1 Questionnaire. Interview guide English version.

(PDF)

Acknowledgments

We would like to thank the Illubabor Zone health department and respective district health offices. We would also like to thank the study participants and all others involved in any process of the study for providing us with the necessary support and information.

Data Availability

Data cannot be shared publicly because of the nature of the data being qualitative that contains personal quotes and clues to where the study occurred and can be potentially identifiable. However, data is available on request to the chair of Research and community Service Coordination Office (RCS) of Mettu University Faculty of Public Health and Medical Sciences (E-mail:mohammed.amin@meu.edu.et).

Funding Statement

The authors received no specific funding for this work.

References

  • 1.Nathavitharana RR, Bond P, Dramowski A, Kotze K, Lederer P, Oxley I, et al. Agents of change: The role of healthcare workers in the prevention of nosocomial and occupational tuberculosis. Presse Med. 2017;46(2):e53–62. doi: 10.1016/j.lpm.2017.01.014 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Organization WH. Global tuberculosis report 2013. World Health Organization; 2013. [Google Scholar]
  • 3.Organization WH. The global plan to stop TB 2011–2015: transforming the fight towards elimination of tuberculosis. 2010. [Google Scholar]
  • 4.Organization WH. World malaria report 2015. World Health Organization; 2016. [Google Scholar]
  • 5.Shiferaw MB, Zegeye AM. Delay in tuberculosis diagnosis and treatment in Amhara state, Ethiopia. 2019;19(1). [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Gebremariam G, Asmamaw G, Hussen M, Hailemariam MZ, Asegu D, Astatkie A, et al. Impact of HIV status on treatment outcome of tuberculosis patients registered at Arsi Negele Health Center, Southern Ethiopia: a six year retrospective study. PLoS One. 2016;11(4):e0153239. doi: 10.1371/journal.pone.0153239 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Wale W. A Study On The Situation Of Hiv/Aids Mainstreaming: The Case Of Federal Non Health Public Sector Ministries In Addis Ababa. St. Mary’s University; 2013. [Google Scholar]
  • 8.Ereso BM, Yimer SA, Gradmann C, Sagbakken M. Barriers for tuberculosis case finding in Southwest Ethiopia: a qualitative study. PLoS One. 2020;15(1):e0226307. doi: 10.1371/journal.pone.0226307 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Taylor SJ, Bogdan R, DeVault M. Introduction to qualitative research methods: A guidebook and resource. John Wiley & Sons; 2015. [Google Scholar]
  • 10.Rashid M, Hodgson CS, Luig T. Ten tips for conducting focused ethnography in medical education research. Med Educ Online. 2019;24(1):1624133. doi: 10.1080/10872981.2019.1624133 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Elfil M, Negida A. Sampling methods in clinical research; an educational review. Emergency. 2017;5(1). [PMC free article] [PubMed] [Google Scholar]
  • 12.Kalan ME, Sis HY, Kelkar V, Harrison SH, Goins GD, Jafarabadi MA, et al. The identification of risk factors associated with patient and healthcare system delays in the treatment of tuberculosis in Tabriz, Iran. BMC Public Health. 2018;18(1):1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Awoke N, Dulo B, Wudneh F. Total delay in treatment of tuberculosis and associated factors among new pulmonary TB patients in selected health facilities of Gedeo zone, southern Ethiopia, 2017/18. Interdiscip Perspect Infect Dis. 2019. doi: 10.1155/2019/2154240 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Cattamanchi A, Miller CR, Tapley A, Haguma P, Ochom E, Ackerman S, Davis JL, Katamba A, Handley MA. Health worker perspectives on barriers to delivery of routine tuberculosis diagnostic evaluation services in Uganda: a qualitative study to guide clinic-based interventions. BMC health services research. 2015. Dec;15(1):1–0. doi: 10.1186/s12913-014-0668-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Wondale B, Medihn G, Teklu T, Mersha W, Tamirat M, Ameni G. A retrospective study on tuberculosis treatment outcomes at Jinka General Hospital, southern Ethiopia. BMC Res Notes. 2017;10(1):1–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Reves R, Angelo S. As Ethiopia moves toward tuberculosis elimination, success requires higher investment. Center for Strategic and International Studies (CSIS); 2016. [Google Scholar]
  • 17.Locke K. Qualitative research and evaluation methods. Organ Res Methods. 2002;5(3):299. [Google Scholar]
  • 18.Datta S, Shah L, Gilman RH, Evans CA. Comparison of sputum collection methods for tuberculosis diagnosis: a systematic review and pairwise and network meta-analysis. Lancet Glob Heal [Internet]. 2017;5(8):e760–71. Available from: doi: 10.1016/S2214-109X(17)30201-2 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Murphy ME, Phillips PPJ, Mendel CM, Bongard E, Bateson ALC, Hunt R, et al. Spot sputum samples are at least as good as early morning samples for identifying Mycobacterium tuberculosis. BMC Med. 2017;15(1):1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Firdaus S, Kaur IR, Kashyap B, Avasthi R, Singh NP. Front loading sputum microscopy–an alternative approach for diagnosis of pulmonary tuberculosis. J Clin Tuberc Other Mycobact Dis [Internet]. 2017;8:6–12. Available from: doi: 10.1016/j.jctube.2017.05.002 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Getnet F, Demissie M, Assefa N, Mengistie B, Worku A. Delay in diagnosis of pulmonary tuberculosis in low-and middle-income settings: systematic review and meta-analysis. BMC pulmonary medicine. 2017. Dec;17(1):1–5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Peri AM, Bernasconi DP, Galizzi N, Matteelli A, Codecasa L, Giorgio V, et al. Determinants of patient and health care services delays for tuberculosis diagnosis in Italy: a cross-sectional observational study. BMC infectious diseases. 2018. Dec;18(1):1–1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Gebreegziabher SB, Bjune GA, Yimer SA. Total delay is associated with unfavorable treatment outcome among pulmonary tuberculosis patients in west Gojjam zone, Northwest Ethiopia: a prospective cohort study. PLoS One. 2016;11(7):e0159579. doi: 10.1371/journal.pone.0159579 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 24.Dabaro D. J Clin Tuberc Other Mycobact Dis Factors a ff ecting tuberculosis case detection in Kersa District, South West. J Clin Tuberc Other Mycobact Dis [Internet]. 2017;9(January):1–4. Available from: 10.1016/j.jctube.2017.08.003 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.WHO. Global strategy on human resources for health: Workforce 2030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Harries AD, Lin Y, Kumar AM, Satyanarayana S, Takarinda KC, Dlodlo RA, et al. What can National TB Control Programmes in low-and middle-income countries do to end tuberculosis by 2030?. F1000Research. 2018;7. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Sink HL, Langley CJ Jr. A managerial framework for the acquisition of third-party logistics services. J Bus Logist. 1997;18(2):163. [Google Scholar]
  • 28.Health Sector transformation plan. 2021;25. [Google Scholar]
  • 29.Abayneh M, Hailemariam S, Asres A. Low Tuberculosis (TB) Case Detection: A Health Facility-Based Study of Possible Obstacles in Kaffa Zone, Southwest District of Ethiopia. Can J Infect Dis Med Microbiol. 2020;2020. doi: 10.1155/2020/7029458 [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Utilities E. Engendering Utilities Partner Profile Eeu, Ethiopia Usaid partners with Ethiopian Electric Utility (EEU) to improve. 2020;18–21. [Google Scholar]

Decision Letter 0

Yasir Bin Nisar

1 Jun 2022

PONE-D-22-11392Why Tuberculosis diagnosis and treatment delay in health system: a qualitative study of patients, health workers and program managers’ perspectivesPLOS ONE

Dear Dr. Kitila,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’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.

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Comments to the Author

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Reviewer #2: Partly

**********

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Reviewer #1: N/A

Reviewer #2: N/A

**********

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Reviewer #1: No

Reviewer #2: Yes

**********

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Reviewer #2: No

**********

5. Review Comments to the Author

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Reviewer #1: Dear Editor,

Thank you for giving me the opportunity to review the article “Why Tuberculosis diagnosis and treatment delay in health system: a qualitative study of patients, health workers and program managers’ perspectives”. I have read the article with great interest. However, major revisions are needed in the methods and writing style before it can be considered for publication. Some of the comments are as follows:

1. The article needs to be read and revised by a native English speaker.

2. The title of the article needs to be revised/rewritten.

3. Reviewer comment: In the introduction section and throughout the manuscript, definition of health system delay, “Early diagnosis and initiation of tuberculosis treatment” “Late detection and Treatment” are not clear.

4. Methods and Materials

Study setting and period

Study period has been written in the reverse order “from October 15, 2021, to March 1, 2021”.

5. Sample size and sampling techniques

In-depth interview

It is not mentioned that 28 health professionals were chosen out of how many health professionals?

6. Why was the criteria of 6 months of experience in TB for health professionals chosen?

7. What was the criteria for choosing different numbers of interviewees (Seventeen DOT providers, five laboratory experts, six program managers, and seven tuberculosis patients for the study?

8. Facility Observation

Who observed, what was their qualification, how frequently for how long they observed the facilities?

9. Interviewers

What was their qualification, were they trained in interviews and were their methods checked?

10. Finally, until the publication was approved,???? the authors had regular conversations and consultations about the design, data analysis, and result interpretations. Unclear and unnecessary information is given.

11. Ethics approval and consent to participate

Were the participants compensated for their time? Was any incentive given to the study participants?

12. The sample collection method is not clear regarding different collection procedures such as “spot spot” and “spot morning spot”techniques.

13. Criteria of trained professional in OPD has not been mentioned.

14. Discussion

First paragraph, No new finding has been reported as a result of the study. Scarcity of infrastructure is already known.

15. Were the skills of the lab professionals checked?

16. Conclusion is too long in abstract and end of discussion. Needs to be rewritten.

Best Regards

Brekhna

Reviewer #2: While this is an important research topic and very relevant for LMICs, this paper does not add any new information, nor is there any innovative idea or concept explored. It adds to the pool of the existing knowledge.

The paper has used purely qualitative methods, that include interviews and observations, as mentioned by authors. It would have been enriched had it been a mixed methods study, with some quantitative data on coverage, the duration between care seeking and confirmation of diagnosis, proportion of the total cases that were diagnosed at the first visit or required more than 1 visit, the data from facilities which were commonly visited by patients or any surveillance data from the community that collected information on TB prevalence.

Since it is purely a qualitative study, focus group discussions would have added greater insights into a larger number of key informants.

Additionally, as we know TB management has several challenges, the paper could have adopted a more comprehensive approach by addressing some more barriers if not all. Although the study has addressed the important barriers such as delays in diagnosis, lack of adherence to TB treatment guideline, poor infrastructure, lack of appropriate diagnostic tools, staff shortage etc., there are others, such as unregulated private health care leading to widespread irrational use of first-line and second-line anti-TB drugs; spreading HIV infection; poverty; lack of political will and administrative challenges. There are issues related to intermittent supplies of Anti-TB drugs, intermittent supplies of laboratory reagents, poor TB data documentation, lack of health worker motivation and commitment, lack of awareness, knowledge, stigma associated with the infection, long distance to health facilities limiting access, adverse drug reaction, and poor household income. Poor compliance to complete and appropriate treatment with a high proportion of defaulters, also leads to an increased pool of infective and drug resistant cases. There may be TB cases who do not report to hospital for care-seeking, due to lack of knowledge or fear of stigma, which also need urgent attention. There may be a need of active surveillance. It would be very useful to incorporate this additional information in case the study has collected these.

Coming to the specific comments, it would be helpful if the challenges could be categorized as 1) patient level 2) provider level 3) facility level 4) health systems level and 5) policy level. Currently there seems to be substantial overlap.

The term participants and lab professionals have been interchangeably used. It is not clear as which responses are provided by which category of respondents, whether it is reported by the program managers, or the DOT providers, or the lab experts or the patients. Table 1 needs to be categorized accordingly. We do not know the education of patients. It is also not clear why duration of treatment is categorized as less than and more than 2 months, what is the mean duration of treatment?

Finally, the English language needs improvement, there is lack of consistency in the grammar, use of language and spellings in the abstract, methods and materials and discussions; seems that the sections are written by different persons.

**********

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Reviewer #1: Yes: Brekhna Aurangzeb

Reviewer #2: Yes: Sarmila Mazumder

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PLoS One. 2022 Dec 30;17(12):e0278592. doi: 10.1371/journal.pone.0278592.r002

Author response to Decision Letter 0


23 Jun 2022

Response to Reviewers

Response to Reviewer 1

1. The article needs to be read and revised by a native English speaker.

Response: Yes, I have invited the English language expert to read and revise the manuscript. Consequently, the necessary improvement has been made.

2. The title of the article needs to be revised/rewritten

Response: Tuberculosis diagnosis delay: a qualitative study of patients, health workers, and program managers’ perspectives

3. Reviewer comment: In the introduction section and throughout the manuscript, definition of health system delay, ‘’Early diagnosis and initiation of tuberculosis treatment’’ ‘’Late detection and Treatment’’ are not clear.

Response: Regarding TB delay, there are three terms.

1. Patient delays are defined as the time interval from the onset of symptoms of tuberculosis until the first visit to any formal health care facility above median days from the onset of the symptoms as cut-off points

2. Health system delays: is the time interval from the patient’s first visit to the formal health care facility to the commencement of treatment, and time longer than the median days will be considered indicative of health system delays (diagnosis delay plus treatment delay).

3. Total health system delay is the time interval from the first onset of symptoms to the commencement of treatment, or the sum of patient delay and healthcare system delay.

In this manuscript, the title has focused on health system delays (diagnosis delay plus treatment delay). At the beginning, the authors' intention was to explore the reasons for health system delay (both reasons for diagnosis delay and treatment delay), but since all participants mentioned no reasons related to treatment delay, we have modified the title (see track change). Based on the comments We have modified the introduction section (see track change version).

4. Methods and Materials

Study setting and period

Study period has been written in the reverse order ‘’from October 15, 2021, to March 1, 2021’’.

Response: We have corrected the order accordingly (see line 68 from the track change).

5. Sample size and sampling technique

In-depth interview

It is not mentioned that 28 health professionals were chosen out of how many health professionals?

Response: Actually, Illubabor Zone has 13 districts and one town administration. Out of these, six districts and one town were selected randomly. As mentioned in the manuscript, the health professionals involved were program managers, laboratory professionals, and DOT providers. Regarding the six program managers, one was from the Zonal CDC focal person and the other five were from selected district health offices. Regarding the DOT providers, 17 were included out of 82 DOT providers in the seven districts. Five of 36 laboratory experts were from seven health facilities.

6. Why was the criteria of 6 months of experience in TB for health professionals chosen?

Response: After six months, we expect any health professional to know their work environment. In Ethiopia, they can give enough information about the reasons for the TB diagnosis delay.

7. What was the criteria for choosing different numbers of interviewees(Seventeen DOT providers, five laboratory experts, six program)

Response: For triangulation, different numbers of health professionals were interviewed.

8. Facility Observation

Who observed, what was their qualification, how frequently for how long they observed the facilities?

Response: At each facility, observations were conducted for 50 to 70 minutes by the authors. They had masters in educational qualifications (see 124 & 125 lines from the track change version).

9. Interviewers

What was their qualification, were they trained in interviews and were their methods checked?

Response: The interviewers were the authors (originators of the research idea).We had a common understanding of data collection procedures.

10. Finally until the publication was approved? ??? the authors had regular conversations and consultations about the design, data analysis, and result interpretations. Unclear and unnecessary information is given.

Response: We have removed it. See track change version.

11. Ethics approval and consent to participate

Were the participants compensated for their time?

Was any incentive given to the study participants?

Response: Any incentives were not given to participants.

12. The sample collection method is not clear regarding different collection procedures such as ‘’spot spot’’ and ‘’spot morning spot’’ techniques.

Response: A spot morning spot technique is for sputum microscopy. One spot sample is collected at the time of the first visit of a patient to the laboratory. Two sputum (spot and early morning) samples were collected the next day.

In 2011, WHO advice was revised with a recommendation of a two-‘spot-spot’ strategy collected on the same day. According to the participants, after the TB diagnosis technique changed from spot morning spot to spot-spot it has been contributing to the diagnosis delay.

13. A criteria of trained professional in OPD has not been mentioned.

Response: Any health professional who has taken any type of in-service TB training is considered a trained health professional.

14. Discussion

First paragraph, No new finding has been reported as a result of the study. Scarcity of infrastructure is already known.

Response: OK, This research topic is new. Because previous studies were conducted quantitatively and others were conducted on factors affecting case identification. But, this research explored reasons for diagnosis delays qualitatively. In particular, it is helpful for the study area. Because contributing factors differ across societies, types of health facilities visited, and geographical regions between population groups in the same local settings and disease categories. Localized studies are needed to uncover area and population-specific characteristics linked to extended TB diagnosis delays.

15. Were the skills of the lab professionals checked?

Response: Dear Reviewer, The study's intention is not to measure (check) the skills of lab professionals. We have just recorded factors delaying TB diagnosis by participants.

16. Conclusion is too long in abstract and end of discussion. Needs to be rewritten.

Response: Thank you. It has been modified accordingly; see track change version.

Response to Reviewer 2

1st paragraph comment: While this is an important research topic and very relevant for LMICs, this paper does not add any new information, nor is there any innovative idea or concept explored. It adds to the pool of the existing knowledge.

Response: Thank you for your critical comments. But, the previous studies focused on factors affecting case detection. In this study, we focused on factors affecting TB diagnosis delay. That means factors which could delay diagnosis after the patients reach health facilities.

2nd paragraph comment: The paper has used purely qualitative methods,that include interviews and observations, as mentioned by authors. It would have been enriched had it been a mixed methods study, with some quantitative data on coverage, the duration between care seeking and confirmation of diagnosis, proportion of the total cases that were diagnosed at the first visit or required more than 1 visit, the data from facilities which were commonly visited by patients or any surveillance data from the community that collected information on TB prevalence.

Response: The quantitative studies were conducted by other researchers who measured the duration between care seeking and confirmation of diagnosis. But, in this study, our aim was to explore qualitatively "why TB diagnosis delays after patients reach the health facilities."

3rd comment: Since it is purely a qualitative study, focus group discussions would have added greater insights into a larger number of key informants.

Response: As we have mentioned in the method section, the participants were included from different districts, which are from distant geographic locations from each other’s. So, it was difficult to bring them together for focus group discussion, and we preferred interviewing them individually.

4th paragraph comment: Additionally, as we know TB management has several challenges, the paper could have adopted a more comprehensive approach by addressing some more barriers if not all. Although the study has addressed the important barriers such as delays in diagnosis, lack of adherence to TB treatment guideline, poor infrastructure, lack of appropriate diagnostic tools, staff shortage etc., there are others, such as unregulated private health care leading to widespread irrational use of first-line and second-line anti-TB drugs; spreading HIV infection; poverty; lack of political will and administrative challenges. There are issues related to intermittent supplies of Anti-TB drugs, intermittent supplies of laboratory reagents, poor TB data documentation, lack of health worker motivation and commitment, lack of awareness, knowledge, stigma associated with the infection, long distance to health facilities limiting access, adverse drug reaction, and poor household income. Poor compliance to complete and appropriate treatment with a high proportion of defaulters, also leads to an increased pool of infective and drug resistant cases. There may be TB cases who do not report to hospital for care-seeking, due to lack of knowledge or fear of stigma, which also need urgent attention. There may be a need of active surveillance. It would be very useful to incorporate this additional information in case the study has collected these.

Response: Dear Reviewer, the above reasons could be an answer to "why low TB case notification". As a result, it covers a wide range of topics, including barriers to TB diagnosis before and after patients visit health facilities. In our case, we focused on delay of TB diagnosis. That means when our concern was on delay time of diagnosis whereas the above might be focused on low case detection.

5th comment: Coming to the specific comments, it would be helpful if the challenges could be categorized as 1) patient level 2) provider level 3) facility level 4) health systems level and 5) policy level. Currently there seems to be substantial overlap.

Response: The proposed categories are good. But, based on the collected data, the procedure of thematic qualitative analysis leads us to the thematic mentioned in the result section. Moreover, when we evaluated our data to adjust according to the comments, some categories couldn’t be identified from the data, like patient level, health system level, and policy level.

Comment: The term participants and lab professionals have been interchangeably used. It is not clear as which responses are provided by which category of respondents, whether it is reported by the program managers, or the DOT providers, or the lab experts or the patients. Table 1 needs to be categorized accordingly.

Response: In the manuscript, where we have used "health professionals," it represents the ideas of all health professionals, but where we have used "lab professionals," it represents only the ideas of lab professionals.

Comment: We do not know the education of patients. It is also not clear why duration of treatment is categorized as less than and more than 2 months, what is the mean duration of treatment?

Response: TB treatment phases are categorized into two phases. Duration of treatment less than 2 months is categorized as an intensive phase, whereas duration of treatment greater than 2 months is categorized as a continuation phase.

Comment: Finally, the English language needs improvement, there is lack of consistency in the grammar, use of language and spellings in the abstract, methods and materials and discussions; seems that the sections are written by different persons.

Response: Yes, we have improved it accordingly.

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 1

Yasir Bin Nisar

2 Sep 2022

PONE-D-22-11392R1Tuberculosis diagnosis delay: a qualitative study of patients, health workers and program managers’ perspectivesPLOS ONE

Dear Dr. Kitila,  Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’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 1 October 2022. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ 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 academic 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'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Yasir Bin Nisar, Ph.D

Academic Editor

PLOS ONE

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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

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

**********

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

Reviewer #1: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). 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

**********

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

PLOS ONE 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: No

**********

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: Overall comments;

It is an important article that explains qualitative aspects of delay in diagnosis of TB in low middle income countries. The authors have revised it significantly. However, I still feel the English language and expression needs improvement at multiple points. There are multiple typo errors: in some places there is a space between bracket and figures and in certain places without a space, which needs to be corrected. Please add the revision of methods suggested by the reviewers in the manuscript.

Abstract:

Comment No 1:

Background: “The main target of Tuberculosis control and prevention is to detect incident cases as early as possible”. However, the target is hard to meet due to problems that exist within health facilities, which lead to diagnostic delays. Despite this, there is no information explored why diagnosis delays among Tuberculosis patients.” This statement is not correct. The main target of TB control and prevention is not only to detect incident cases as quickly as possible but also to prevent occurrence of disease. This is also the responsibility of the health facility to screen the contacts, identify cases and prevent spread in children by identifying children for prophylactic therapy.

Some examples of the problems stated above are;

Comment No 2

Results: Diagnosis delays have been identified as a result of issues with sample collection procedures, poor competency of health professionals, absences/scarcity of health professionals, and scarcity of medical products and absence/scarcity of basic infrastructure. This sentence can be rephrased to avoid repetition of absence/ scarcity.

Comment No 3; Result: “We found 18 health facilities without skilled personnel in the OPD, seven health facilities with a broken microscope, and almost all health facilities without a

separate room for sputum examination”. Grammatical correction needs to be done 7 health facilities had a broken microscope?

Comment no 4: Conclusion: Many reasons for TB diagnosis delays have been identified in the study area. Poor competence of health workers and scarcity of resources were identified. Depending on the finding, we suggest strengthening the health workers’ training. Concrete strategies need to be designed to retain Professionals. Training on human resource planning and budget preparation is needed for low level managers. The meaning of low level managers is not clear.

Introduction:

Comment No 5: Introduction line 3; why expected 10.4 million cases? When the year is already complete and should have the actual figures. Also, why has the statistics of 2016 been mentioned instead of the latest? Please put the latest statistics.

Comment No 6; “The time elapsed between seeking health care and receiving a diagnosis is defined as diagnosis delay” Why is definition in the past tense in introduction?

Comment No 7; “Diagnosis of tuberculosis cases has been identified as a key impediment

to TB control, particularly in low-income countries such as Ethiopia”. Probably the author wants to state that early diagnosis or prompt diagnosis is a key impediment to ......

Comment No 8; “Because, it causes more acute sickness, a longer period of infection, and worse treatment outcomes such as mortality and drug resistance”. Please replace with it causes severe acute phase of the disease.

Comment No 9:

Furthermore, despite "free service" for TB, it results in TB patients suffering significant pre-diagnosis costs for care seeking. Add s to service.

Comment No 10:

According to the findings of a systematic review and meta-analysis, diagnosis delays ranged

from 2 to 128.5 days, whereas they ranged from 6 to 28 days in other studies conducted in

Ethiopia among tuberculosis patients (10, 11). Is 2 or 6 days counted as diagnostic delay or is it normal time taken to diagnose TB????

**********

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.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Brekhna Aurangzeb

**********

[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 One. 2022 Dec 30;17(12):e0278592. doi: 10.1371/journal.pone.0278592.r004

Author response to Decision Letter 1


8 Sep 2022

Response to Reviewers

Reviewer #1: Overall comments;

It is an important article that explains qualitative aspects of delay in diagnosis of TB in low middle income countries. The authors have revised it significantly. However, I still feel the English language and expression needs improvement at multiple points. There are multiple typo errors: in some places there is a space between bracket and figures and in certain places without a space, which needs to be corrected. Please add the revision of methods suggested by the reviewers in the manuscript.

Response: Thank you. We have modified accordingly.

Abstract:

Comment No 1:

Background: “The main target of Tuberculosis control and prevention is to detect incident cases as early as possible”. However, the target is hard to meet due to problems that exist within health facilities, which lead to diagnostic delays. Despite this, there is no information explored why diagnosis delays among Tuberculosis patients.” This statement is not correct. The main target of TB control and prevention is not only to detect incident cases as quickly as possible but also to prevent occurrence of disease. This is also the responsibility of the health facility to screen the contacts, identify cases and prevent spread in children by identifying children for prophylactic therapy.

Response: Yes, it has been corrected accordingly. see first paragraph on page 2.

Some examples of the problems stated above are;

Comment No 2

Results: Diagnosis delays have been identified as a result of issues with sample collection procedures, poor competency of health professionals, absences/scarcity of health professionals, and scarcity of medical products and absence/scarcity of basic infrastructure. This sentence can be rephrased to avoid repetition of absence/ scarcity.

Response: Yes, it has been rephrased accordingly. See the result part of abstract.

Comment No 3; Result: “We found 18 health facilities without skilled personnel in the OPD, seven health facilities with a broken microscope, and almost all health facilities without a

separate room for sputum examination”. Grammatical correction needs to be done 7 health facilities had a broken microscope?

Response: Yes, it has been rephrased accordingly. See the result part of abstract.

Comment no 4: Conclusion: Many reasons for TB diagnosis delays have been identified in the study area. Poor competence of health workers and scarcity of resources were identified. Depending on the finding, we suggest strengthening the health workers’ training. Concrete strategies need to be designed to retain Professionals. Training on human resource planning and budget preparation is needed for low level managers. The meaning of low level managers is not clear.

Response: Low level managers mean frontline managers. Now we have replaced with frontline managers. Check the last line of conclusion in the Abstract

Introduction:

Comment No 5: Introduction line 3; why expected 10.4 million cases? When the year is already complete and should have the actual figures. Also, why has the statistics of 2016 been mentioned instead of the latest? Please put the latest statistics.

Response: we have updated the information. check second page, line three

Comment No 6; “The time elapsed between seeking health care and receiving a diagnosis is defined as diagnosis delay” Why is definition in the past tense in introduction?

Response: We have modified accordingly. Check second paragraph, line one under the introduction.

Comment No 7; “Diagnosis of tuberculosis cases has been identified as a key impediment

to TB control, particularly in low-income countries such as Ethiopia”. Probably the author wants to state that early diagnosis or prompt diagnosis is a key impediment to ......

Response: You are right. We have corrected accordingly.

Comment No 8; “Because, it causes more acute sickness, a longer period of infection, and worse treatment outcomes such as mortality and drug resistance”. Please replace with it causes severe acute phase of the disease.

Response: Yes, we have replaced accordingly. check second paragraph, fourth line under the introduction.

Comment No 9:

Furthermore, despite "free service" for TB, it results in TB patients suffering significant pre-diagnosis costs for care seeking. Add s to service.

Response: Good. it is corrected.

Comment No 10:

According to the findings of a systematic review and meta-analysis, diagnosis delays ranged

from 2 to 128.5 days, whereas they ranged from 6 to 28 days in other studies conducted in

Ethiopia among tuberculosis patients (10, 11). Is 2 or 6 days counted as diagnostic delay or is it normal time taken to diagnose TB????

Response: Actually the ranges are mentioned to show the existing days of delay from the literature. But different literatures utilized the median as cut point.

Attachment

Submitted filename: Response to Reviewers.docx

Decision Letter 2

Yasir Bin Nisar

26 Sep 2022

PONE-D-22-11392R2Tuberculosis diagnosis delay: a qualitative study of patients, health workers and program managers’ perspectivesPLOS ONE

Dear Dr. Kitila, 

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’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 Nov 10 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 plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ 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 academic 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'.

If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions see: https://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols. Additionally, PLOS ONE offers an option for publishing peer-reviewed Lab Protocol articles, which describe protocols hosted on protocols.io. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols.

We look forward to receiving your revised manuscript.

Kind regards,

Yasir Bin Nisar, Ph.D

Academic Editor

PLOS ONE

Additional Editors Comments:

Thank you for giving me the opportunity to review the article “Why Tuberculosis diagnosis and treatment delay in health system: a qualitative study of patients, health workers and program managers’ perspectives”. I have read the article with great interest. However, major revisions are needed in the methods and writing style before it can be considered for publication. Some of the comments are as follows:

1. The article needs to be read and revised by a native English speaker.

2. The title of the article needs to be revised/rewritten.

3. Reviewer comment: In the introduction section and throughout the manuscript, definition of health system delay, “Early diagnosis and initiation of tuberculosis treatment” “Late detection and Treatment” are not clear.

4. Methods and Materials

Study setting and period

Study period has been written in the reverse order “from October 15, 2021, to March 1, 2021”.

5. Sample size and sampling techniques

In-depth interview

It is not mentioned that 28 health professionals were chosen out of how many health professionals?

6. Why was the criteria of 6 months of experience in TB for health professionals chosen?

7. What was the criteria for choosing different numbers of interviewees (Seventeen DOT providers, five laboratory experts, six program managers, and seven tuberculosis patients for the study?

8. Facility Observation

Who observed, what was their qualification, how frequently for how long they observed the facilities?

9. Interviewers

What was their qualification, were they trained in interviews and were their methods checked?

10. Finally, until the publication was approved,???? the authors had regular conversations and consultations about the design, data analysis, and result interpretations. Unclear and unnecessary information is given.

11. Ethics approval and consent to participate

Were the participants compensated for their time? Was any incentive given to the study participants?

12. The sample collection method is not clear regarding different collection procedures such as “spot spot” and “spot morning spot”techniques.

13. Criteria of trained professional in OPD has not been mentioned.

14. Discussion

First paragraph, No new finding has been reported as a result of the study. Scarcity of infrastructure is already known.

15. Were the skills of the lab professionals checked?

16. Conclusion is too long in abstract and end of discussion. Needs to be rewritten.

[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 One. 2022 Dec 30;17(12):e0278592. doi: 10.1371/journal.pone.0278592.r006

Author response to Decision Letter 2


3 Oct 2022

Response to Reviewers

1. The article needs to be read and revised by a native English speaker.

Response: Yes, I have invited the English language expert to read and revise the manuscript. Consequently, the necessary improvement has been made.

2. The title of the article needs to be revised/rewritten

Response: Of course, revised. See the track change

3. Reviewer comment: In the introduction section and throughout the manuscript, definition of health system delay, ‘’Early diagnosis and initiation of tuberculosis treatment’’ ‘’Late detection and Treatment’’ are not clear.

Response: see the second paragraph of track change under the introduction part.

4. Methods and Materials

Study setting and period

Study period has been written in the reverse order ‘’from October 15, 2021, to March 1, 2021’’.

Response: We have corrected the order accordingly (see study setting and period subsection).

5. Sample size and sampling technique

In-depth interview

It is not mentioned that 28 health professionals were chosen out of how many health professionals?

Response: Actually, Illubabor Zone has 13 districts and one town administration. Out of these, six districts and one town were selected randomly. As mentioned in the manuscript, the health professionals involved were program managers, laboratory professionals, and DOT providers. Regarding the six program managers, one was from the Zonal CDC focal person and the other five were from selected district health offices. Regarding the DOT providers, 17 were included out of 82 DOT providers in the seven districts. Five of 36 laboratory experts were from seven health facilities.

6. Why was the criteria of 6 months of experience in TB for health professionals chosen?

Response: After six months, we expect any health professional, know their work environment. They can give enough information about the reasons for the TB diagnosis delay.

7. What was the criteria for choosing different numbers of interviewees(Seventeen DOT providers, five laboratory experts, six program)

Response: For triangulation, different numbers of health professionals were interviewed.

8. Facility Observation

Who observed, what was their qualification, how frequently for how long they observed the facilities?

Response: At each facility, observations were conducted for 50 to 70 minutes by the authors. They had masters in educational qualifications (see 124 & 125 lines from the track change version).

9. Interviewers

What was their qualification, were they trained in interviews and were their methods checked?

Response: The interviewers were the authors (originators of the research idea).We had a common understanding of data collection procedures.

10. Finally until the publication was approved? ??? the authors had regular conversations and consultations about the design, data analysis, and result interpretations. Unclear and unnecessary information is given.

Response: We have removed it. See track change version.

11. Ethics approval and consent to participate

Were the participants compensated for their time?

Was any incentive given to the study participants?

Response: Any incentives were not given to participants.

12. The sample collection method is not clear regarding different collection procedures such as ‘’spot spot’’ and ‘’spot morning spot’’ techniques.

Response: A spot morning spot technique is for sputum microscopy. One spot sample is collected at the time of the first visit of a patient to the laboratory. Two sputum (spot and early morning) samples were collected the next day.

In 2011, WHO advice was revised with a recommendation of a two-‘spot-spot’ strategy collected on the same day. According to the participants, after the TB diagnosis technique changed from spot morning spot to spot-spot it has been contributing to the diagnosis delay.

13. A criteria of trained professional in OPD has not been mentioned.

Response: Any health professional who has taken any type of in-service TB training is considered a trained health professional.

14. Discussion

First paragraph, No new finding has been reported as a result of the study. Scarcity of infrastructure is already known.

Response: OK, This research topic is new. Because previous studies were conducted quantitatively and others were conducted on factors affecting case identification. But, this research explored reasons for diagnosis delays qualitatively. In particular, it is helpful for the study area. Because contributing factors differ across societies, types of health facilities visited, and geographical regions between population groups in the same local settings and disease categories. Localized studies are needed to uncover area and population-specific characteristics linked to extended TB diagnosis delays.

15.Were the skills of the lab professionals checked?

Response: Dear Reviewer, The study's intention is not to measure (check) the skills of lab professionals. We have just recorded factors delaying TB diagnosis by participants.

16.Conclusion is too long in abstract and end of discussion. Needs to be rewritten.

Response: Thank you. It has been modified accordingly; see unmarked version.

Attachment

Submitted filename: Response to Reviewer.docx

Decision Letter 3

Yasir Bin Nisar

21 Nov 2022

Why Health System Diagnosis Delay among Tuberculosis patients in Illubabor, Oromia Region, South West Ethiopia? A qualitative study

PONE-D-22-11392R3

Dear Dr. Kitila,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

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 onepress@plos.org.

Kind regards,

Yasir Bin Nisar, Ph.D

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

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

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

**********

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

Reviewer #1: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). 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

**********

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

PLOS ONE 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

**********

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: All the comments have been addressed satisfactorily. This article should be published as it addresses a pertinent issue .

**********

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.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Brekhna Aurangzeb

**********

Acceptance letter

Yasir Bin Nisar

23 Nov 2022

PONE-D-22-11392R3

Why Health System Diagnosis Delay among Tuberculosis patients in Illubabor, Oromia Region, South West Ethiopia? A qualitative study

Dear Dr. Kitila:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

PLOS ONE Editorial Office Staff

on behalf of

Dr. Yasir Bin Nisar

Academic Editor

PLOS ONE

Associated Data

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

    Supplementary Materials

    S1 Checklist. Checklist for facility observation.

    (PDF)

    S2 Checklist. Consolidated criteria for reporting qualitative research (COREQ) checklist.

    (DOCX)

    S1 Questionnaire. Interview guide English version.

    (PDF)

    Attachment

    Submitted filename: Response to Reviewers.docx

    Attachment

    Submitted filename: Response to Reviewers.docx

    Attachment

    Submitted filename: Response to Reviewer.docx

    Data Availability Statement

    Data cannot be shared publicly because of the nature of the data being qualitative that contains personal quotes and clues to where the study occurred and can be potentially identifiable. However, data is available on request to the chair of Research and community Service Coordination Office (RCS) of Mettu University Faculty of Public Health and Medical Sciences (E-mail:mohammed.amin@meu.edu.et).


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