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. 2024 May 31;19(5):e0300152. doi: 10.1371/journal.pone.0300152

Assessing the influence of the health system on access to cervical cancer prevention, screening, and treatment services at public health centers in Addis Ababa, Ethiopia

Kemal Hussein 1,*, Gilbert Kokwaro 1, Francis Wafula 1, Getnet Mitike Kassie 2
Editor: Dawit Wolde Daka3
PMCID: PMC11142424  PMID: 38820249

Abstract

Background

Cervical cancer is the second leading cause of cancer death among Ethiopian women. This study aimed to assess the influence of the health system on access to cervical cancer prevention, screening, and treatment services at public health centers in Addis Ababa, Ethiopia.

Methods

This study used a cross-sectional survey design and collected data from 51 randomly selected public health centers in Addis Ababa. Open Data Kit was used to administer a semi-structured questionnaire on Android tablets, and SPSS version 26 was used to analyze the descriptive data.

Results

In the study conducted at 51 health centers, cervical cancer prevention and control services achieved 61% HPV vaccination for girls, 79% for cervical cancer awareness messages, 80% for precancer lesion treatment, and 71% for cervical screening of women. All health centers were performing cervical screening mostly through visual inspection with acetic acid due to the inconsistent availability of HPV DNA tests and the lack of Pap smear tests. In 94% of health centers, adequate human resources were available. However, only 78% of nurses, 75% of midwives, 35% of health officers, and 49% of health extension workers received cervical cancer training in the 24 months preceding the study. Women had provider choices in only 65% of health centers, and 86% of the centers lacked electronic health records. In 41% of the health centers, the waiting time was 30 minutes or longer. About 88% and 90% of the facilities lacked audio and video cervical cancer messages, respectively.

Conclusion

This study revealed that the annual cervical cancer screening achievement was on track to fulfill the WHO’s 90-70-90 targets by 2030. We recommend that decision-makers prioritize increasing HPV vaccination rates, enhancing messaging, reducing wait times, and implementing electronic health records to improve access to cervical cancer services in Addis Ababa.

Introduction

Though cervical cancer is a preventable disease and curable (with early detection, timely diagnostic follow-up, and effective treatment) it continues to be a public health problem resulting in the premature death of women mainly in low-income countries globally [1]. In 2020, for instance, globally, 604, 127 new cervical cancer cases were reported with 341,831 deaths of which 117,316 incidences and 76, 745 deaths occurred in Africa [2]. Cervix uteri cancer accounted for 23.3% of all new cases of cancer in females in Sub-Saharan Africa (SSA) in 2020 [3]. In 2020, the age-standardized incidence rate (ASIR) for Eastern Africa was 40 cases per 100,000 women [2]. This is ten-fold higher than the incidence rate of lower than four per 100,000 women set by the WHO Global Strategy [1]. The pooled incidence proportion of estimates of high-risk human papillomavirus (HPV) infection among SSA women was 34% [4].

Each year, hospital data in Ethiopia revealed over 150,000 new cases of cancer, which account for 4% of all deaths [5]. In 2020 in Ethiopia, cervical cancer was the second most prevalent type of cancer among women, affecting 7,445 women and responsible for 5,338 deaths [6]. The ASIR was 24.6 per 100,000 Ethiopian females in 2019 [7]. The country had 36.9 million women aged 15 years and older who were at risk of developing cervical cancer, and an estimated 3.8% of women in the general population harbor cervical HPV16/18 infection [8]. In Addis Ababa, the most common cancers in women were breast (33%), and cervix uteri cancer (14.3%) [9, 10].

According to the 2017 WHO report policymakers and partners at the national and international levels paid insufficient attention to cancer [11]. Ethiopia regretfully also devoted little attention to cancer despite it being a significant public health issue [5, 9]. To prepare the way for the eradication of cervical cancer in the twenty-first century, WHO urges nations to achieve the 90-70-90 cervical cancer targets by 2030. At the age of 15, 90% of girls take the HPV vaccine in full, 70% of women undergo cervical screening at the age of 35 and 45, and 90% of women with precancerous lesions or invasive cancer receive treatment [1]. To combat cancer, the Ethiopian National Cancer Control Plan (NCCP) was put into effect in 2015 [9]. However, the healthcare system in the country still had to contend with issues like low levels of public awareness about cancer, a shortage of diagnostic and treatment facilities, a shortfall of oncology specialists, and a poor referral system [12]. Only 9% of health facilities offered diagnosis and treatment for cervical cancer in 2018 [13]. In 2014, just 8% of facilities had guidelines for the diagnosis and treatment of cancer, and 4% of those facilities had staff who had undergone cancer in-service training [14]. The estimated pooled prevalence of cervical cancer screening service utilization was 5.47% [15]. In 2020, there were still reports of high cervical cancer morbidity and mortality rates [6].

Our study aimed to assess the health system’s influence on access to cervical cancer prevention, screening, and treatment services at public health centers in Addis Ababa. The study took into account components of the earlier conceptual frameworks to examine the health system’s "inputs" and "outputs" related to services for cervical cancer [16, 17]. “Quality healthcare in Ethiopia” calls for comprehensive care that is timely, affordable, efficient with its use of resources, effective, safe, and patient-centered [18]. Similarly, in this study, a "quality cervical cancer service" refers to how well the desired health outcomes (target achievement, timeliness, patient-centeredness, availability, and equity) are improved by providing women with services for prevention, screening, and treatment. While "equity" seeks to provide high-quality healthcare services to all people without distinction based on their geographical location, gender, income, or disabilities [19].

Materials and methods

Study settings and period

Ethiopia’s three-tiered health service delivery system includes primary, secondary, and tertiary-level care. The primary healthcare institutions (health centers), which each provide services to up to 40,000 people in urban settings, are at the bottom of the tier structure [20]. The location of this study was Addis Ababa, the capital city of Ethiopia, which has 126 woredas (districts) and 11 sub-cities. According to UN population forecasts, Addis Ababa’s metro area had a population of 5,228,000 in 2022 [21]. To uncover problems in a health system setup with reasonably enough resources and to suggest workable solutions that may be extended to other places while taking contextual variables into account, this urban scenario was selected. The study’s data collection period was from July 15, 2022, until August 31, 2022.

Study design and participants

This study employed a cross-sectional survey design to assess the influence of the health system on access to prevention, screening, and treatment of cervical cancer at public health centers in Addis Ababa. The study population was 90 public health centers actively providing cervical cancer prevention, screening, and treatment services. Study participants comprised 51 cervical cancer focal persons appointed by the 51 health centers chosen for the study. Nurses, midwives, and health officers who supervise, manage, and coordinate cervical cancer services are the focal individuals in Addis Ababa’s health center settings.

Sample size and sampling procedure

The sample size for health centers was determined using n0 = z2 * p * q / e2 [22]. Where: n0 = sample size, z = 1.96 for a confidence level (α) of 95%, p = proportion (0.09) [13], q = 1-p (0.91), e = margin of error (5%). Thus, the initial sample size (n0) consisted of 126 facilities. Since the population size is small to the sample size, the sample size was adjusted using n = (n0/(1+(n0-1)/N))) [22]. Where n is the adjusted sample size and N is the population size. A proportionate number of 51 health centers were randomly selected using Microsoft Excel out of a total of 90 public health centers actively providing cervical cancer services in 11 sub-cities. The list was obtained from the Addis Ababa City Administration Health Bureau. Additionally, after considering the "cervical cancer focal person position" in the health centers, 51 healthcare workers (nurses, midwives, and health officers) were chosen for face-to-face interviews using a semi-structured questionnaire (S1 File). The focal persons were individuals responsible for managing or coordinating cervical cancer services. However, the number of cervical cancer service providers was different from a health center to a health center.

Data collection procedure

The following two components were part of this study’s data collection process:

  1. Face-to-face interviews: The data were collected from the 51 health centers through face-to-face interviews with cervical cancer focal persons by five trained data collectors (public health experts) using an Open Data Kit (ODK) tool installed with an English language semi-structured questionnaire (S1 File). The semi-structured questionnaire was read out to cervical cancer focal persons and explained (translated) in Amharic (local language) to avoid any misunderstanding. The survey was focused on health system “inputs” (providers, equipment, tests and vaccines, financing, and health information systems), and “outputs” (target achievement of services, availability of screening options, timeliness of services, patient-centeredness, and equity) of cervical cancer services.

  2. Secondary data review: This involved a review of existing data related to cervical cancer. A checklist (for percentage achievement of public awareness, HPV vaccination, screening, and treatment) was used for the data extraction by examining records from the cervical cancer register, the extended program on immunization (EPI) register, and administrative reports. The cervical cancer register provided information on the number of women who were screened for cervical cancer and who received treatment. The EPI registration was checked to ascertain the number of girls who received the HPV vaccine. Administrative reports, on the other hand, provided information on public awareness messages related to cervical cancer.

Study variables

To assess the health system inputs and outputs influencing access to cervical cancer prevention, screening, and treatment services, the study took into account a number of different variables. These indicators assisted in determining whether cervical cancer services were comprehensive, timely, patient-centered, and equitable to the population.

  1. Health system inputs: The health system’s "inputs" were determined by taking into account 1) Human resources: The availability of staff for services related to cervical cancer screening and treatment (nurses, midwives, and/or health officers); 2) Physical/Infrastructure: Availability of screening devices, diagnostic tests (HPV DNA tests and Pap smear tests), treatment equipment, and HPV vaccine; 3) Information: Health information systems that facilitate the collection, management, and analysis of data related to cervical cancer screening and treatment (cervical cancer register, EPI register, and administrative reports); and 4) Financial: Funding (infrastructure, supplies, and operational costs), user fees, and transportation costs.

  2. Health system outputs: The measurement of health system “output” indicators to cervical cancer screening and treatment included 1) Target Achievement: Measuring the percentage of HPV vaccination, screening, and treatment achievement (performance per annual plan) towards meeting the WHO 90-70-90 cervical cancer targets [1]; 2) Availability: Assessing the availability of screening and testing (visual inspection with acetic acid, HPV DNA tests, and Pap smear tests); 3) Timeliness: Assessing the time required for screening and treatment services; 4) Patient-centeredness: Assessing whether patient preferences and needs were considered by providing various testing options; and 5) Equity: Evaluating the provision of cervical cancer prevention, screening, and treatment services without variation based on socioeconomic status, ability to pay, or geographical location.

Data quality control

In this study, the quality of the data was controlled utilizing a variety of techniques. Five public health professionals were selected for data collection based on their prior experience with quantitative data collection using the Open Data Kit (ODK) platform. Then, using the data collection guidelines, a half-day of training was given to the data collectors. The semi-structured questionnaire that was pre-installed on the ODK tool was the main topic of discussion. The data collectors offered comments on how to make the tool more effective at answering the study questions. The semi-structured questionnaire’s validity was further evaluated based on how well it addressed the study questions through field testing. For this, the tool underwent pretesting at the Felege Meles Health Center in Addis Ababa before the actual data collecting began. The tool was modified in response to field feedback. Real-time data synchronization and collection were made accessible through the ODK central server. The questions pre-programmed on the ODK allowed for the validation of the tools’ consistency, integrity, validity, and comprehensiveness. The data manager also supervised the daily ODK server data collection and consistency. Data auditing was done before data collection was complete to maintain the required sample size. Any discrepancies were fixed after determining the sample size before data analysis. At the same time, to guarantee the reliability of the study’s findings, thorough data, and ongoing data comparisons were used.

Data processing and analysis

To make sure that the data was correct, trustworthy, and prepared for descriptive analysis, the following approach was employed. Data auditing was done before data collection was finished to make sure the required sample size was kept. This process included checking the collected data for accuracy, consistency, and completeness. Any discrepancies or missing data points were fixed. The data was exported to Excel CSV format after the data auditing procedure was finished. To further clean and analyze the data, SPSS Version 26 was employed. At this step, extra verifications and checks were done on the data to make sure it was accurate and consistent. This made it possible to find mistakes and fix them, deal with missing values, and recode variable replies so that they are in the correct format. The dataset was cleaned and then made ready for additional analysis. In this step, certain variables of interest were chosen and the data was formatted in a way that is suitable for analysis. Descriptive statistics (frequency, proportion or percentage, mean, and standard deviation) were used to summarize the data. Graphs and tables were used to recap the percentage and attributes of the cervical cancer focal persons’ responses, as well as the secondary data extracted from health centers’ cervical cancer register, EPI register, and administrative reports.

Ethical consideration

Ethical approvals of the study were obtained from 1) Strathmore University Institutional Scientific and Ethical Review Committee (SU-IERC1373/22), and 2) Addis Ababa City Administration Health Bureau Ethical Clearance Committee (A/A/0024/227). Support letters were also provided by 11 sub-cities in Addis Ababa and produced to the respective health centers for permission to collect data. The cervical cancer focal persons were briefed on the purpose and objective of the research. The written informed consent was obtained from respondents before the interview. The collected data was kept confidential, and no names were displayed in the study.

Results

Health system inputs/functions

The survey showed that 94.1% of the health centers had adequate staff for cervical cancer services. There was at least one nurse, one midwife, and one health officer trained in cervical cancer management in 20, 17, and 13 health centers, respectively. Among the 51 health centers surveyed, the providers who received cervical cancer training in the 24 months preceding the study were 40 (78.4%) nurses, 38 (74.5%) midwives, 18 (35.3%) health officers, and 25 (49%) health extension workers (HEWs). All the fifty-one health centers were providing community services through HEWs. Public education was the main role for HEWs in 48 (94%) facilities, followed by referral linkage of women (92%). The HEWs public engagement areas were mostly in community outreach (100%) and at schools (71%). Table 1 shows speculums were available in 51 (100%), a cryotherapy machine with CO2 gas supply in 50 (98%), acetic acid in 50 (98%), and the HPV vaccine in 28 (54.9%) facilities. The cervical cancer prevention and control guidelines were available throughout the fifty-one facilities, and the majority of them had adequate Information, Education, and Communication (IEC)/ Social and Behavior Change Communication (SBCC) materials including posters, flyers, and brochures. Audio and video messages were unavailable in 45 (88.2%) and 46 (90.2%) facilities, respectively. Paper-based referral forms were available throughout the health centers though only 26 (51%) of them received no feedback.

Table 1. Availability of equipment, vaccines, and supplies at health centers in Addis Ababa (n = 51).

Variables Count Percent
Speculum
Available 51 100.0
Cryotherapy machine with CO2 gas supply
Available 50 98.0
Not available 1 2.0
Acetic acid
Available 50 98.0
Not available 1 2.0
HPV vaccine
Available 28 54.9
Not available 23 45.1
IEC/SBCC material (poster)
Available 47 92.2
Not available 4 7.8
IEC/SBCC material (audio)
Available 6 11.8
Not available 45 88.2
IEC/SBCC material (video)
Available 5 9.8
Not available 46 90.2
IEC/SBCC material (flyer)
Available 39 76.5
Not available 12 23.5
IEC/SBCC material (brochure)
Available 44 86.3
Not available 7 13.7
Cervical cancer prevention and control guideline
Available 51 100.0
Referral forms
Available 51 100.0

The cervical cancer screening and treatment services at public health centers were provided for free. It was covered by the government, development partners, and community-based health insurance funds. Only 33% of the fifty-one facilities reported a shortage of funds. There were no transportation incentives for the linkage of the most at-risk women to facilities. Thirty-three (64.7%) of the health centers indicated that there was inadequate transportation for cases that were referred to hospitals. Nevertheless, 39 (76.5%) of the facilities’ distances to specialized care were determined to be less than 10 km. Patient follow-up telephone calls were practiced by 39 (76.5%) health centers, especially for re-screening testing. Cervical cancer screening and treatment, and EPI services registration books were available in all health centers.

Health system outputs/performance

Target achievement of services

Messages on cervical cancer awareness were delivered to 79.1% of women, 61.2% of girls aged 15 were fully vaccinated against cervical cancer, 71.1% of women screened for cervical cancer, and 79.8% of women treated for precancer lesions (Table 2).

Table 2. Achievement (%) of cervical cancer services at health centers in Addis Ababa (n = 51).
Achievement* Minimum Maximum Mean Std. Deviation
% of women reached with cervical cancer awareness messages. 20 99 79.1 22.4
% of girls fully vaccinated against cervical cancer at the age of 15. 0 99 61.2 25.6
% of women screened for cervical cancer. 13 99 71.1 24.3
% of women with positive cervical screening treated. 1 99 79.8 33.3

*Achievement: Performance per plan for July 1, 2021 to June 30, 2022.

Equity, availability, patient-centeredness, and timeliness of services

Efforts have been made by the government to attain equitable free cervical cancer services through at least 90 active public health centers spread out in 11 sub-cities in Addis Ababa with no discrimination due to income, gender, place of residence, and ethnicity of users. This was demonstrated by the cervical screening, preventive, and treatment services offered in the 51 health centers examined. Since Pap smear tests were not available in health centers, women were referred for testing in private diagnostics or the Family Guidance Association of Ethiopia costing USD10 per test. The turnaround time (TAT) was ranging from 15 to 30 days in 49 (96.1%) of the health centers. Whereas the TAT for the visual inspection with the acetic acid test was 1 minute in 48 (94.1%) of the health centers. HPV DNA test was unavailable throughout the 51 health centers. During the January 2022 campaign, 35,099 vials of HPV vaccine were wasted due to contamination and breakage, and 4,240 vials of vaccine as a result of the Vaccine Vial Monitor (VVM) change. In 41 (80.4%) of the health centers, women had ongoing relationships with the healthcare providers and were given a chance to choose the providers in 33 (64.7%) of the facilities. The average waiting time for cervical cancer screening and treatment was 30 minutes or longer in 41% of facilities. E-registers were not available in the majority of the facilities (86.3%).

Major challenges and improvement areas for cervical cancer services

The survey showed that 96.1% of health centers admitted to facing challenges in delivering public education with 58.8% mentioning inadequate media coverage as the major underlying factor. The women’s transportation cost (35.3%) and the facility’s distance (29.4%) were additional concerns. Training to providers was recommended by 80.4% of the cervical cancer focal persons with 76.5% suggesting improved media coverage (Table 3).

Table 3. Prevention, screening, and community linkage challenges, and improvement areas at health centers (n = 51).

Variables Count Percent
Prevention and screening service challenge*
Education 49 96.1
Religious factors 7 13.7
Stigma 9 17.6
Language barrier 5 9.8
Lack of space for screening 10 19.6
Unavailability of SBCC/IEC materials 6 11.8
Inadequate media coverage (TV, radio) 30 58.8
Major challenges on community linkage*
Transportation cost 18 35.3
Distance to the facility 15 29.4
Capacity of HEWs 3 5.9
Fear of procedure 8 15.7
Lack of awareness 12 23.5
Areas of improvement in cervical cancer services*
Provide transportation allowance 11 21.6
Shorten waiting time 8 15.7
Provide staff training 41 80.4
Improve diagnostic capacity 31 60.8
Ensure preference for a provider 13 25.5
Spouse or partner support 21 41.2
Promote media coverage 39 76.5
Facilitate suitable room 7 13.7
Include routine HPV vaccine service 4 7.8

*Participants provided more than one response.

Discussion

This study looked at the effect of the health system on access to cervical cancer services from the primary healthcare perspective. It is the first survey to examine the "inputs" and "outputs" of the health system regarding public health centers’ response and dedication to the fight against cervical cancer. The study revealed the prevailing health system challenges deterring the provision of the highest possible coordinated and integrated cervical cancer services at the facilities.

Health system inputs

In-service training had been given to 35% of health officers and 49% of health extension workers (HEWs) in the 24 months before the study. This supports previous studies conducted in Addis Ababa, Ethiopia, which found that more than half (52%) of HEWs lacked an appropriate understanding of cervical cancer and its screening [23, 24]. In addition, only 16% of health centers and hospitals’ staff who provide services for cervical cancer in East Gojjam Zone, northwest Ethiopia, had undergone in-service training [25]. However, our study revealed a better development than a previous study conducted in Ethiopia, which discovered that only 4% of the employees in the health facilities had undergone in-service training on cancer in 2014 [14]. All health centers possessed guidelines for preventing and managing cervical cancer. Again this showed significant improvement compared to a prior study in Ethiopia, which discovered that only 8% of healthcare facilities held cancer guidelines in 2014 [14]. The lack of audio materials in 88% and video recordings in 90% of facilities, may have had a detrimental impact on the public awareness achievement of 79% shown in this study. This confirms the limited community awareness identified by previous studies conducted in Ethiopia [12, 26], and other countries [2729]. The decision-makers may take into account online learning modules to satisfy the current demands for in-service training. For a routine immunization campaign aimed at 14-year-old girls, the quadrivalent HPV vaccine was introduced in Ethiopia in December 2018 [30]. However, this was given in campaigns and the HPV vaccine was available in 54.9% health centers only. In 35% of health centers, the cost of transportation was a significant barrier to connecting women in the community with services for cervical cancer. This probably contributed to Ethiopia’s previously reported low cervical cancer screening service utilization of 5.47% [15]. Lessons from the HIV programs may also be applied to the design and implementation of transportation incentives, particularly for connecting the most vulnerable women to health centers.

Health system outputs

In comparison to the annual plan for 2022, 61% of girls received the full HPV vaccination by the age of 15 to fulfill the WHO target of 90% by 2030 [1]. Only 29.4% of health centers’ HPV immunization programs involved HEWs. Additionally, the survey found high HPV vaccine loss (39, 339 vials). To advance towards reaching the WHO target of 90% by 2030, further efforts were needed through routine immunization programs, effective supply chain management, and improved HEWs participation. In comparison to the WHO goal of 70% by 2030, a higher screening success rate (71%) has been attained. Per the cervical cancer guidelines algorithm, the turnaround time (TAT) for counseling, screening, and treating women was less than 15 minutes [30]. However, the health centers had no technical capacity and infrastructure, and poor access to Pap smear testing. It was performed outside the facilities with a TAT of up to a month and out-of-pocket charges. These findings uphold the previous Ethiopian studies that reported inadequate diagnostic and treatment centers for cancer [12, 13]. Furthermore, three-fourths of the patients had delayed diagnostic confirmation (more than 30 days) in a different study conducted in Addis Ababa, Ethiopia [31]. Previous research suggested combining a Pap smear test with visual inspection using acetic acid (VIA) to boost the success rate of cervical cancer screening [32, 33]. The challenges encountered with Pap smear testing could be lessened with proper lab networking, test cost assistance, and a shorter TAT. In addition, implementing Pap smear testing in facilities could enhance screening and lead to better achievement for treating precancer lesions than what this study found (80%).

To reduce long wait times, health facility managers could have set timelines and monitored the services from triage to screening clinics with improved provider preference assurances. Offering accurate, thorough, and standardized patient condition information was difficult because most health centers (86%) still needed electronic health records (EHRs). Moreover, clinical records of patients were not electronically referred from health centers to hospitals and vice versa. Though all health centers managed paper-based referrals no feedback was received in 51% of the health centers which demanded a health system practice redesign to access to the patient’s clinical records. According to a Tanzanian study, similar issues were encountered in this regard [28]. A robust information system is essential for enabling the integration and coordination of patient-centered care as well as round-the-clock provider access [26, 34]. Furthermore, this may facilitate regular evaluation of patient-reported indicators to determine whether patient-centered care is being provided and to fix any gaps in the health system [35].

Equity of services

Equity of services has been given top priority in the Ethiopian Health Sector Transformation Plan II [19]. It places a strong emphasis on making sure that nobody is prevented from accessing essential healthcare because of their location or other traits, such as being a woman or a member of a disadvantaged group. The expansion of equitable health services at health centers was one of the main strategies of the health transformation plan. As a result, throughout eleven sub-cities of Addis Ababa, the Addis Ababa City Administration Health Bureau has made notable strides in guaranteeing the availability and accessibility of cervical cancer screening and treatment services in at least ninety health centers. Our study showed that services for cervical cancer prevention and control were offered throughout the 51 health centers. By achieving equity, Addis Ababa may be able to ensure that everyone has an equal opportunity to gain from cervical cancer prevention, early detection, and treatment. On the other hand, the replies from 76.5% of the health centers indicated that women had to travel up to 10 kilometers for specialized care, which is only provided in secondary and tertiary hospitals. According to a study from Zimbabwe, women should be provided with transportation to health facilities so they can undergo cervical cancer treatment [27].

Areas of improvement

Training for healthcare providers, spreading messages of public awareness, and improving diagnostic capabilities at health centers were all highlighted as key health system deficiencies that need to be addressed. These priorities were also identified by several earlier research [12, 14, 2527, 29, 36]. Prior research suggested coordinated efforts to lower barriers to screening services, primarily by utilizing the media to create demand and offering training to healthcare providers [26, 37, 38]. Other studies conducted in Ethiopia and Central America proposed improving HPV DNA testing through the self-collection of samples to enhance screening in high-burden and resource-limited settings [39, 40]. Furthermore, a study carried out in Jimma, southwest Ethiopia, suggested that initiatives be taken to enhance women’s views, comprehension, and satisfaction regarding cervical cancer screening services [41].

Strengths and limitations of the study

The study has a variety of benefits regarding the health system’s influence on the provision of services for cervical cancer prevention and control in settings with limited resources. It offers insightful information about the “inputs” and “outputs” of the healthcare system about cervical cancer services. However, the study also revealed several restrictions that need to be taken into account. The inability to evaluate the aspects of the health system that have an impact on the provision of cervical cancer services at private health institutions is the first restriction. Since the study concentrated on situations with few resources, private health centers may have a big impact on how cervical cancer services are provided. The absence of these facilities could preclude the study from giving a complete picture of the health system and its impact on cervical cancer services. Another restriction is the generalizability of the study’s findings. Since the study was conducted in Addis Ababa, its findings might apply to major urban settings, but they might not fairly represent the challenges that other regions and rural parts of the country face. When extrapolating the results beyond the study’s confines, care should be used because different places may have different infrastructures and access to services. Last but not least, the study did not completely address the issues with Pap smear testing’s technical capabilities and infrastructure, nor did not look into any missed chances with the HPV vaccination program. Comprehending the complete range of cervical cancer preventive and control services requires an understanding of these factors. However, due to budget limitations, the study was unable to investigate these areas, which restricts the findings’ comprehensiveness. It is crucial to be aware of these limitations when evaluating the study’s results and choosing how to move forward with cervical cancer prevention and control activities in settings with limited resources. A more nuanced understanding of the aspects of the health system that have an impact on the delivery of cervical cancer services could be provided by additional research that takes these constraints into account and contributes to the development of useful reform measures.

Implications for policy and practice

The primary aim of the National Cancer Control Plan (NCCP) is to engage the entire health system, including primary healthcare facilities such as health centers. It is the responsibility of the decision-makers at the national and regional levels to monitor the entire system, pinpoint its flaws, and create plans to enhance health performance outcomes. While decision-makers concentrate on the NCCP’s overarching objectives, healthcare professionals working in health centers are dedicated to providing patient-centered integrated and coordinated standard cervical cancer care that caters to the requirements of both individual service users and communities. This study looked at how health centers responded to and were committed to the NCCP’s overarching goals by evaluating the current service provision, organizational capacity, information, and patient participation. It highlighted weaknesses in the healthcare system, including low rates of HPV vaccination, a lack of screening choices caused by the sporadic availability of HPV DNA tests, a lack of access to Pap smear tests, insufficient staff capacity building, and lengthy wait times. The results of the study could potentially provide a foundation for tackling the challenges that are encountered in other forms of cancer. This may spur additional studies to look into and fill in these gaps so that everyone afflicted by cancer can receive thorough and patient-centered care. Researchers can contribute to a deeper understanding of the health system’s strengths and shortcomings in providing effective cancer prevention, treatment, and control measures by extending the scope of their research beyond cervical cancer and investigating the execution of NCCP goals for other cancers. Lastly, this research can support policy initiatives by directing focus, establishing priorities, and revamping the nation’s cancer care delivery system.

Conclusions

To deal with cancer, the Ethiopian government has put the National Cancer Control Plan into effect. Free and equitable cervical cancer screening and treatment services were provided in over 90 health centers located throughout eleven Addis Ababa sub-cities. The programs, which were primarily aimed at women in the 30 to 49 years old age range, were bolstered by public awareness messages. Additionally, campaigns were used to immunize females against HPV. However, there were still challenges in the way of achieving higher HPV vaccination rates, which call for consistent access to vaccines with minimal wastes. Moreover, there were gaps in training for healthcare professionals, offering testing options and provider preferences, reducing wait times, and implementing electronic health records, and raising awareness campaigns primarily via audio and video messages, and television media. Addressing the inconsistent accessibility of HPV DNA testing could enhance screening services [39, 40]. The adoption of electronic health records is the primary means of enhancing the referral pathways between health centers and hospitals to better coordinate and integrate services. Reducing wait times, enhancing public awareness, and fulfilling patient needs and preferences may be achieved by increasing providers’ capacity and improving service coordination at facilities. The WHO 90-70-90 targets for cervical cancer can be met by 2030 with the provision of high-quality services at healthcare institutions and the combined efforts of communities, service users, and decision-makers.

Supporting information

S1 File. Semi-structured questionnaire.

(DOCX)

pone.0300152.s001.docx (28.4KB, docx)
S2 File. Health centers survey tables and figures.

(DOCX)

pone.0300152.s002.docx (472.1KB, docx)
S3 File. Health centers survey data_PLoS.

(SAV)

pone.0300152.s003.sav (39.2KB, sav)

Acknowledgments

We are grateful to the Addis Ababa City Administration Health Bureau for approving the study, as well as the 11 Addis Ababa sub-cities for facilitating access, providing letters of support to the health centers, and offering ongoing assistance during the study. Additionally, we would like to thank all of the study participants, particularly the cervical cancer focal persons who supplied pertinent data. Furthermore, we would like to express our sincere gratitude to all data collectors who helped with the validation of the study’s questionnaire and data collection.

Data Availability

All relevant data are within the manuscript and its Supporting information files.

Funding Statement

The author(s) received no specific funding for this work.

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Decision Letter 0

Dawit Wolde Daka

3 Aug 2023

PONE-D-23-08979Health system factors affecting equitable access to quality cervical cancer services at public health centers in Addis Ababa, EthiopiaPLOS ONE

Dear Dr. Hussein,

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. Up on my own review and the reviewers comments I recommend Major Revision to this manuscript. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Please pay attention to editor and reviewers comments below.

==============================

ACADEMIC EDITOR: Please pay attention to the following points in addition to feedback given by reviewers:

  • There are major flaws in grammar and language throughout this paper. In the revised version, try to address this. Authors are highly recommended to get editions services of this manuscript with experts, to have a qualified scientific paper. 

  • The abstract section of the paper  should clearly show the rationale for this paper, and how the proposed aim was answered. But, this issues are shallow and lacks clarity. The method section in the main body is not also clearer and doesn't help for replication. Therefore,  authors are suggested to revise this section and better if the methods is re-organized in the follows sections: study settings and period, Study design and participants, data collection,  study variables,  data quality control, data processing and analysis,  ethical consideration 

  • In the topics and aim of the paper, key terms like equity, quality of cervical cancer services and the like are described.  However, authors didn't adequately define this terms in any section of the paper,  not described the measurement methods employed, and displayed the measured results.  Though two frameworks are employed in the current paper, how this framework employed to guide the measurements lacks clarity. Please provide explanations to this, and as well address this issues within the manuscript. 

  • Make sure that the manuscript has addressed the journals requirements in terms of contents, particularly after the conclusions section of the paper. Refer the journal guideline and correct this part. 

  • Change the citation formats to square brackets (e.g., [1]).

  • Adequately discuss the present study findings with that of literature in other settings(out of Ethiopia). Discuss the strength and limitations of the study, focusing on the methods used, and have a separate section to discuss the policy and practice implications of the study. 

==============================

Please submit your revised manuscript by Sep 17 2023 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.

We look forward to receiving your revised manuscript.

Kind regards,

Dawit Wolde Daka

Academic Editor

PLOS ONE

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When submitting your revision, we need you to address these additional requirements.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. 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: Partly

Reviewer #2: Yes

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

Reviewer #1: No

Reviewer #2: Yes

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3. 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

Reviewer #2: Yes

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4. 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

Reviewer #2: Yes

**********

5. Review Comments to the Author

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

Reviewer #1: Manuscript Number: PONE-D-23-08979

Manuscript Title: Health system factors affecting equitable access to quality cervical cancer services at public health centers in Addis Ababa, Ethiopia:

Dear Editor,

Thank you for inviting me to review the scientific quality of this article.

Dear Authors,

It is very interesting to get research done on this very interesting area of women's health.

However, I recommend you the following points be addressed before your article gets published

1. Either modify the title or re-do the analysis because there is no result to talk about the quality of service. Also, there is no strongly concluded point about equity to the service user.

2. The 150,000 new cases that Ethiopia reports is not clear. Line 46

3. Font Color of lines 56-59 is different: a light blue. Better to make it similar throughout the document. The sentence is direct copy and paste. Rephrase

4. I was expecting to read what “quality cervical cancer services” are mean in the introduction, particularly in Ethiopia. How did it become your concern? Any other previous evidence on the case and what is the gap?

Material and Method

1. The method needs rearrangement. For example, why data collection method under the session “Study design and period”?

2. Organization of Ethiopian health service delivery system line 93-95 needs reference.

3. It is described how the health facilities were sampled and selected. How about the service providers? Who were they? How were they selected? It should not be indicated under the session “Data collection procedure and data analysis”

4. The data collection procedure is not indicated well. Face-to-face interview? FGD? Checklist data extraction???

5. Avoid unnecessary repetitions. For example, the study period on lines 91 and 118.

6. The data analysis procedure lacks a detailed explanation. Is it not important to explain the used analysis method, and cutoff points,…the analysis is rough and do not fully support the study aims.

7. It is important to describe measurements in this study. For example,

o How the fulfillment of the input was measured? Was it the summation of all the available inputs or any of them? Was 100% input expected?

o What indicators were used to measure (effectiveness, availability, timeliness, and patient-centeredness): the Outputs?

o How was equity of cervical cancer services measured? When did you say there is equity in the services?

o What is quality service as per your study?

Result

1. What is the importance of writing in different colors again? Line 134-139

2. You have no data extraction method. How was the data for the information provided in Table 3 were obtained?

Discussion

1. Lines 192-194: “The study revealed that the prevailing health system challenges at the primary healthcare level had negatively impacted the quality of cervical cancer 194 services.” How can you say it affects the quality without showing the status of the quality of the service?

2. Ideas in lines 197-216 seem taken from literature; how does the idea on line 217 connect with it? Which findings are being compared?

3. Line 233-234, client report. Where did you get it? You have no client involvement or data extraction in the data collection method.

4. In general, I recommend doing the discussion ideally under sub-headings of input, output, and equity in access to cervical cancer screening. It is a copy of the result. Make it short and discuss using guidelines on recommended minimum importance.

Conclusions

Lines 312-313: do you have data on the poor engagement of school and drop-out girls?

Similarly, in lines 316-317; do you have information on “HPV DNA and Pap smear testing attract more women for screening”?

� the conclusion should be done depending only on the data that can be accessed in this manuscript. It seems discussion.

Reviewer #2: General Comments: Thank you for the updated manuscript. Any study on equitable access to quality cervical cancer services in LMIC countries is important as efforts are made to control/eliminate CC globally from the perspective of health system factors. The manuscript has paramount but needs modification to make it publishable.

I have pointed some out below but get this fixed throughout the manuscript.

Specific comments

Abstract

Lines 19-20: be consistent in the use of terms (women vs girls) use either of the two throughout your documents, again in the use of health center and health facilities

Introduction

1. Line 39: add references at the end of the paragraph.

2. Line 56-59: be alert while taking documents from other sources and I will recommend you to re-write again.

Methods

3. Lines 92 – 101: what is your study population: healthcare providers or health centers??

4. A proportionate number of 51 facilities were randomly selected using Microsoft Excel out of a total of 90 public health centers actively providing cervical cancer services. How do you select healthcare providers from each health center? Do you think equal numbers of healthcare providers were in each HC?

5. Line 113-114: you said cervical cancer service providers in facilities (11 nurses, 10 midwives, 4 health officers, and 26 cervical cancer focal persons) were approached

What is your justification to select nurses, midwifery, and health officers? Why not used cervical cancer focal persons throughout all health facilities

6. Line 114: add health be for the word facilities, again be consistent in the use of health centers and facilities( I recommend using health facilities throughout your documents)

7. You need to provide more details on the study recruitment process and data collection.

o How exactly were the healthcare providers recruited from 51 health centers?

o How do you select 51 health centers from 11 sub-cities? Clearly shown in sampling procedures

o Where was the data collected, and for how long? Etc. etc.

o Since these healthcare providers were not interviewed in the local language even if they were understanding English? What measures were in place to ensure that the translation process, did not affect the content of what was said?

o Lines 120: change ethical consideration to Ethics approval and consent to participate. I recommend you strictly follow journal guidelines

o Lines 125-126: All methods were performed in accordance with the relevant guidelines and regulations (Declaration of Helsinki). Do the PLoS One guidelines follow such terms?

o On line 174: table 3: I think you have used document review for data retrieval, my concern is what are your data collection methods( state clearly)

Results

General comments

If the socio-demographic variables were in your tools, better to add the description of socio-demographic characteristics of health care providers ( age, sex, profession, etc)

8. Lines 130-131: your description were 20, 17, and 13 health facilities. The total was 50 versus 51 health facilities.

9. Lines 131-132: Rephrase the sentence at lines 131 and 132 to make correct meaning

The recommendation is to minimize use respectively when your list of activities were more than three. In 40 (78.4%), 38 (74.5%), 18 132 (35.3%), and 25 (49%) facilities had nurses, midwives, health officers, and health extension 133 workers (HEWs) who received cervical cancer training, respectively

You can write as 40 (78.4%) nurses, 38 (74.5%) midwives, 18 (35.3%) health officers, and 25 (49%) health extension workers (HEWs) received cervical cancer training

10. Line: 142: table 1: revised all tables based on journal guidelines formats

11. Lines 161-165: this whole text descriptions were not in line with the tables and need to be corrected

12. Lines 170: How do you measure the effectiveness of services? needs operational definition in the methods part

Discussion and conclusions

Detail and clear description of each section

**********

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

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: No

Reviewer #2: No

**********

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PLoS One. 2024 May 31;19(5):e0300152. doi: 10.1371/journal.pone.0300152.r002

Author response to Decision Letter 0


16 Sep 2023

A rebuttal letter that responds to each point raised by the academic editor and reviewer(s) has been uploaded as a separate file labeled 'Response to Reviewers'.

Attachment

Submitted filename: Response to Reviewers.docx

pone.0300152.s004.docx (62.2KB, docx)

Decision Letter 1

Dawit Wolde Daka

15 Nov 2023

PONE-D-23-08979R1Health system factors affecting access to cervical cancer prevention, screening, and treatment services at public health centers in Addis Ababa, Ethiopia.PLOS ONE

Dear Dr. Hussein,

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 Dec 30 2023 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.

We look forward to receiving your revised manuscript.

Kind regards,

Dawit Wolde Daka

Academic Editor

PLOS ONE

Journal Requirements:

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

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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 #2: All comments have been addressed

Reviewer #3: (No Response)

**********

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 #2: Yes

Reviewer #3: Yes

**********

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

Reviewer #2: Yes

Reviewer #3: 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 #2: Yes

Reviewer #3: 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 #2: Yes

Reviewer #3: 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 #2: All my concerns were clearly stated and responded. Still your conclusion was so long and seems result , try to revised it.

Reviewer #3: (No Response)

**********

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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 #2: No

Reviewer #3: No

**********

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

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

Attachment

Submitted filename: The manuscript overall would benefit from some significant editing services.docx

pone.0300152.s005.docx (12.9KB, docx)
PLoS One. 2024 May 31;19(5):e0300152. doi: 10.1371/journal.pone.0300152.r004

Author response to Decision Letter 1


13 Dec 2023

Response to reviewers: A rebuttal letter that responds to each point raised by the reviewers has been uploaded as a separate file labeled 'Response to Reviewers'.

Attachment

Submitted filename: Response to reviewers.docx

pone.0300152.s006.docx (23.9KB, docx)

Decision Letter 2

Dawit Wolde Daka

22 Feb 2024

Assessing the influence of the health system on access to cervical cancer prevention, screening, and treatment services at public health centers in Addis Ababa, Ethiopia.

PONE-D-23-08979R2

Dear Dr. Hussein,

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,

Dawit Wolde Daka

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 #2: 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 #2: Partly

**********

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

Reviewer #2: 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 #2: 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 #2: 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 #2: The author will be alert during revision. Some part of the manuscript were totally changed and finally come to unclear concepts.

**********

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 #2: No

**********

Acceptance letter

Dawit Wolde Daka

7 May 2024

PONE-D-23-08979R2

PLOS ONE

Dear Dr. Hussein,

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

At this stage, our production department will prepare your paper for publication. This includes ensuring the following:

* All references, tables, and figures are properly cited

* All relevant supporting information is included in the manuscript submission,

* There are no issues that prevent the paper from being properly typeset

If revisions are needed, the production department will contact you directly to resolve them. If no revisions are needed, you will receive an email when the publication date has been set. At this time, we do not offer pre-publication proofs to authors during production of the accepted work. Please keep in mind that we are working through a large volume of accepted articles, so please give us a few weeks to review your paper and let you know the next and final steps.

Lastly, 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 customercare@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

Mr Dawit Wolde Daka

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 File. Semi-structured questionnaire.

    (DOCX)

    pone.0300152.s001.docx (28.4KB, docx)
    S2 File. Health centers survey tables and figures.

    (DOCX)

    pone.0300152.s002.docx (472.1KB, docx)
    S3 File. Health centers survey data_PLoS.

    (SAV)

    pone.0300152.s003.sav (39.2KB, sav)
    Attachment

    Submitted filename: Response to Reviewers.docx

    pone.0300152.s004.docx (62.2KB, docx)
    Attachment

    Submitted filename: The manuscript overall would benefit from some significant editing services.docx

    pone.0300152.s005.docx (12.9KB, docx)
    Attachment

    Submitted filename: Response to reviewers.docx

    pone.0300152.s006.docx (23.9KB, docx)

    Data Availability Statement

    All relevant data are within the manuscript and its Supporting information files.


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