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. 2023 Nov 8;3(11):e0002567. doi: 10.1371/journal.pgph.0002567

Uptake of diabetic retinopathy screening at a secondary level facility in Malawi

Thokozani Zungu 1,2,*,#, Shaffi Mdala 1,2,#, Petros Kayange 1,2, Elizabeth Fernando 2, Halima Twabi 3, Arnold Jumbe 4, Johnstone Kumwenda 1,2, Adamson Muula 1
Editor: Nasheeta Peer5
PMCID: PMC10631633  PMID: 37939026

Abstract

Diabetic retinopathy (DR) is a common microvascular complication of long-standing diabetes mellitus (DM). DR screening is a cost-effective intervention for preventing blindness from DR. We conducted a cross-sectional study to investigate the uptake and the predictors of uptake of annual DR screening in an opportunistic DR screening programme at a secondary-level diabetes clinic in Southern Malawi. Consecutive patients were interviewed using a structured questionnaire to record their demographic characteristics, medical details and data regarding; the frequency of clinic visits, knowledge of existence of DR screening services and a history of referral for DR screening in the prior one year. Univariate binary logistic regression was used to investigate predictors of DR screening uptake over the prior one year. Explanatory variables that had a P-value of < 0.1 were included into a multivariate logistic regression model. All variables that had a p-value of <0.05 were considered to be statistically significant. We recruited 230 participants over three months with a median age of 52.5 years (IQR 18–84) and a median duration of diabetes of 4 years (IQR 1–7). The average interval of clinic visits was 1.2 months (SD ± 0.43) and only 59.1% (n = 139) of the participants were aware of the existence of diabetic retinopathy screening services at the facility. The uptake for DR screening over one year was 20% (n = 46). The strongest predictors of uptake on univariate analysis were awareness of the existence of DR screening services (OR 10.05, P <0.001) and a history of being referred for DR screening (OR 9.02, P <0.001) and these remained significant on multivariable analysis. Interventions to improve uptake for DR screening should promote referral of patients for DR screening and strengthen knowledge about the need and availability of DR screening services.

Introduction

More than 24 million adults aged 20–79 in Africa have diabetes mellitus (DM) and this figure is estimated to increase to 33 million by 2030 and 55 million by 2045 [1]. Diabetic retinopathy (DR) is a common complication of DM among adults and its prevalence in sub-Saharan Africa is increasing. It is estimated that a third of persons living with DM in the region have DR and 10% have sight-threatening DR [2]. DR is usually asymptomatic in its early stages and it may thus not be noticed until a patient’s vision is affected and the risk of blindness is high [3, 4].

There is strong evidence that DR screening is a cost-effective intervention for the prevention of visual impairment and blindness from diabetes [5]. However, DR screening uptake is often low even in well-resourced settings [68]. Some of the factors that have been reported to be associated with non-attendance for DR screening include younger age, lack of ocular symptoms, fear and low socioeconomic status. Other factors include long duration of diabetes, type of diabetes (with people with type 1 DM being less likely to attend screening), lack of awareness of DR and its risks and poor access to DR screening centres [9, 10]. There is also evidence that a referral by a primary health care professional for a patient to attend DR screening encourages screening attendance [1013].

For high income countries, systematic DR screening is utilised to achieve a high coverage of DR screening [14]. This is organised at the population level and it utilises a register of people living with diabetes to manage a call and recall system to ensure that all eligible people are offered or reminded of an appointment for screening [13]. However, most countries in Sub Saharan Africa lack the resources required to set up and maintain systematic DR screening programmes [15]. Thus, opportunistic screening for DR is often utilised in most screening programmes in the region.

Opportunistic screening involves providing DR screening to patients with diabetes upon their presentation to a health facility to seek DM care [15]. Considering the shortage of health facilities, personnel skilled in DR screening and the poor accessibility to facilities offering this service, diabetic retinopathy may go unnoticed in most patients. Thus most patients present to eye health facilities only after experiencing considerable vision loss [2]. It is thus important to establish interventions that may promote the uptake of DR screening in an opportunistic DR screening programme.

Malawi is a low-income country in Southern Africa with 28 districts and a population of 19.9 million of whom 84% live in rural areas [16]. The prevalence of DM among adults is 2% in rural areas and 3% in urban areas and the Ministry of Health has a Non-communicable diseases policy which includes DM management [17]. In the country’s national DR screening programme, ophthalmic clinical officers (OCOs) and optometrists perform opportunistic DR screening using direct ophthalmoscopy with pharmacological pupillary dilatation. This is done among patients attending diabetes clinics in the country’s twenty-four district hospitals, which are all secondary-level facilities that serve largely rural populations. Patients identified with treatable DR are referred for treatment to the country’s four tertiary level hospitals, which are located in the country’s four cities. There are no resources for DR screening in primary level health facilities.

The uptake of DR screening at any level of the health system in Malawi had not been reported prior to this study. The aim of this study was to describe the uptake and factors associated with uptake of DR screening in an opportunistic DR screening programme at a secondary level diabetes clinic in Southern Malawi.

Materials and methods

Ethics statement

The study protocol was reviewed and approved by the College of Medicine Research and Ethics Committee, Malawi, P.10/19/2803 and adhered to the tenets of the Declaration of Helsinki for research involving human participants. A participant information sheet was used to explain about the study’s purpose and its procedures during the health education talks that the patients attend in a group before being seen in the clinic. Thereafter, the patients were individually invited to a private room where they were given a chance to ask questions about the study, written informed consent was obtained and data collection interviews were held. The collected data was de-identified upon transcription onto a data collection sheet. All hard copy records were kept in a lockable cabinet and the data was entered into a Microsoft Excel spreadsheet (S1 Table).

All explanations about the study and the informed consent process were done by a study nurse from Queen Elizabeth Central Hospital, which is the referral facility for Thyolo District Hospital.

Study setting

This was a cross-sectional study that was carried out over 3 months in the diabetes clinic at Thyolo district hospital between the months of October 2020 to December 2020. The diabetes clinic is run on one day per week and about thirty patients with diabetes are seen in each clinic. The hospital is a secondary-level government-run health facility in Southern Malawi and it serves a rural population of about 721,456 people [18]. All healthcare services in public hospitals in Malawi, including DR screening and treatment, are government-funded and are provided at no cost to patients at the point of delivery. Besides ophthalmoscopy, DR screening includes visual acuity checks and anterior segment examination with a slit lamp to screen for other visually significant eye diseases that may affect patients with DM such as glaucoma, cataract and refractive error. In contrast to tertiary hospitals, there are no facilities for checking intraocular pressure or for performing ancillary tests such as perimetry in all the 24 district hospitals. At the time of the study, the diabetes clinic at Thyolo district hospital had a total of 700 patients on its register of patients.

As part of routine care, a group-based health education session is delivered by a nurse during each clinic and it includes information for patients on the need for annual DR screening. The nurse-led diabetes health education is meant to reduce the amount of time that the clinician running the diabetes clinic spends on counselling each patient about the complications of DM and the need for DR screening. DR screening is performed in the eye clinic at the facility and patients attend screening according to the schedule advised to them during the nurse-led group health education sessions.

The patient waiting time is prolonged for not less than one hour for patients undergoing DR screening. This is because they undergo pupillary dilatation with 1% tropicamide eye drops before fundoscopy and they also wait on a queue along with patients awaiting to be attended to for other ocular conditions in the eye clinic.

Subjects

The study included all consecutive patients aged at least 18 years old who attended the diabetes clinic at the hospital over the study period. The majority of the patients had a relative who had escorted them to the hospital and these signed as witnesses to the informed consent. Patients who had no witnesses were given an appointment to take part in the study on the following week after returning with a witness. Participants or witnesses who were illiterate signed the consent forms with a thumb print and the only criterion for exclusion was a refusal to participate in the study.

Data collection

A nurse interviewed each participant and ascertained the following data from the history and clinical records of each participant included in the study: age, sex, level of education, history of hypertension, type of diabetes, duration of diabetes, HIV status and the intervals at which the patient visited the clinic over the past 12 months. The nurse also asked each participant if they were aware of the existence of DR screening services at the facility, whether they had been individually referred by the DM clinician for DR screening within the prior 12-month period and whether they attended DR screening over the prior 12 months. After the interview, the visual acuity of each study participant was measured by an OCO using a Snellen chart.

Statistical analysis

The data collected was entered and managed using a Microsoft excel spread sheet and statistical analysis was performed using STATA 17. The main outcome variable was the uptake of DR screening (which was defined as the proportion of patients who had a diabetic eye examination over the past one year).

Continuous variables were summarised as means or medians at 95% confidence intervals and univariate logistic regression was used to investigate the association between uptake of DR screening and the following explanatory variables; age, sex, highest level of education attended, type of diabetes, duration of diabetes, awareness about DR screening services, history of referral by a clinician for DR screening, intervals of clinic visits, history of hypertension, HIV status and the presenting visual acuity. Variables that had a p-value of <0.05 were considered to be statistically significant. Explanatory variables that had a p-value of < 0.1 on univariate analysis were included into a multivariate logistic regression model.

Results

Participant characteristics

We recruited 230 participants over a three-month period and all eligible participants consented to participate in the study. The median age of the patients’ population was 52.5 years (IQR 18–84). The majority of the participants were female (56.5%) and most had attended varying levels of formal education except for 31 participants (13.5%). Most patients had type 2 DM (n = 214, 93%) and 139 patients (60.4%) had a history of hypertension. The median duration of diabetes for the study population was 4 years (IQR 1–7) and the average interval of clinic visits was 1.2 months (SD ± 0.43). Although 59.1% (n = 139) of the population were aware of the existence of diabetic retinopathy screening services at the facility, only 33.9% (n = 78) had been referred by a clinician for DR screening in the prior 12 month period and the uptake of DR screening was 20% (n = 46), Table 1.

Table 1. Patients’ characteristics and association with uptake of DR screening (n = 230).

Variable Summary of characteristics DR screening in past 12 months (uptake), n (%)    
  n (%) Screened, n = 46 (20.0) Not screened, n = 184 (80.0) OR (95% CI)* P–value*
Age (mean ±SD) 52.5 ± 12.9 55.8±12.5 51.7±12.9 1.03 (1.00–1.05) 0.057
Sex
Female 130 (56.5) 23 (10) 107 (46.5) 1  
Male 100 (43.5) 23 (10) 77 (33.5) 1.39 (0.73–2.65) 0.320
Level of education attended
No formal education 31 (13.5) 3 (1.3) 28 (12.2) 1
Primary school 122 (53) 27 (11.7) 95 (41.3) 2.65 (0.75–9.40) 0.131
Secondary school 60 (26.1) 12 (5.2) 48 (20.9) 2.33 (0.61–8.99) 0.218
Post-secondary education 17 (7.4) 4 (1.7) 13 (5.7) 2.87 (0.56–14.73) 0.560
Type of diabetes
    Type 1 16 (7) 4 (1.7) 12 (5.2) 1
    Type 2 214 (93) 42 (18.3) 172 (74.8) 0.73 (0.22–2.39) 0.605
Duration of diabetes (median years, IQR) 4 (1–7) 6 (2–11) 3 (1–7) 1.07 (1.02–1.12) 0.009
Diagnosis of hypertension 
    No hypertension 91 (39.6) 12 (5.2) 79 (34.4) 1  
    Hypertension 139 (60.4) 34 (14.8) 105 (45.6) 2.13 (1.04–4.38) 0.039
HIV status          
Non-reactive 174 (75.7) 38 (16.5) 136 (59.2) 1
    Reactive 41 (17.8) 7 (3) 34 (14.8) 0.74 (0.30–1.79) 0.501
Unknown 15 (6.5) 1 (0.4)   14 (6.1)    
Monthly intervals of clinic visits (mean ± SD) 1.2 ± 0.43 1.3±0.47 1.2±0.42 1.79 (0.90–3.56) 0.098
Awareness about existing DR screening services
    Not aware 94 (40.9) 4 (1.7) 90 (39.1) 1  
    Aware 136 (59.1) 42 (18.3) 94 (40.9) 10.05 (3.46–29.18) <0.001
Referral for DR screening in past 12 months
    Not referred  152 (66.1)  12 (5.2) 140 (60.9)  1  
    Referred 78 (33.9) 34 (14.8) 44 (19.1) 9.02 (4.30–18.90) <000.1
Presenting visual acuity (VA) in the better eye
    6/6–6/18 (Normal Vision) 181 (78.7) 34 (14.8) 147 (63.9) 1
    <6/18–6/60 (Visual impairment) 28 (12.2) 5 (2.2) 23 (10) 0.94 (0.33–2.65) 0.907
    <6/60–3/60 (Severe Visual impairment) 13 (5.7) 4 (1.7) 9 (3.9) 1.92 (0.56–6.61) 0.300
    <3/60 –NPL (Blindness) 8 (3.4) 3 (1.3) 5 (2.2) 2.59 (0.59–11.39) 0.207

*Univariate logistic regression, CI: confidence interval

Predictors of uptake of diabetic retinopathy screening

Table 1 also shows the factors associated with DR screening over 12 months. The strongest predictors of uptake of DR screening over one year were being aware of the existence of DR screening services (OR 10.05, 95% CI: 3.46–29.18) and a history of being individually referred by a clinician for DR screening within the year (OR 9.02, 95% CI: 4.30–18.90). Participants who had a diagnosis of hypertension had twice the odds (OR 2.13, 95% CI: 1.04–4.38) of having undergone DR screening in the prior 12 months compared to those who did not have hypertension. There was also an association between DR screening uptake and the duration of diabetes with the odds increasing by 1.07 times each year (P = 0.009). The association between being screened for DR in the past year and increasing age was non-significant (OR 1.03, 95% CI: 1.00–1.05) and there was no significant association with the participants’ level of education, type of diabetes and the presenting visual acuity.

On multivariate analysis, the only factors that remained as significant independent determinants of uptake of DR screening were awareness of the existence of DR screening services at the health facility (P = 0.021) and being individually referred for DR screening within the year (P < 0.001), Table 2.

Table 2. Factors associated with uptake of diabetic retinopathy screening.

Variable OR (95% C.I) P–value
Age 1.02 (0.99–1.05) 0.263
Duration of Diabetes 1.04 (0.98–1.10) 0.223
Awareness about DR screening services
    Not aware 1.00
    Aware 3.98 (1.23–12.90) 0.021
Referral for DR screening
    Not individually referred 1.00
    Individually referred 4.80 (2.11–10.96) <0.001
Intervals of clinic visits 1.40 (0.63–3.10) 0.409
Diagnosis of hypertension 
    No Hypertension 1.00
    Hypertension 1.04 (0.42–2.56) 0.934

Discussion

There is limited data from sub-Saharan Africa on the uptake of DR screening. A systematic review on the barriers and enablers for access to DR screening services in different income settings identified only three primary studies from low-income countries of which two were from sub-Saharan Africa [19]. The uptake of DR screening was low across the studies and this is in line with the findings from our study where only a fifth of the patients had undergone DR screening in the past year. Our findings are comparable to reports from Tanzania, where the uptake for DR screening at a tertiary eye hospital in the past 12 months was found to be 29% [20]. Similarly, the uptake for DR screening among patients attending 9 diabetes clinics across three counties in Kenya was low, with only 13% having undergone screening in the prior one year [13].

One of the possible reasons for the low uptake of DR screening in our study is the rural setting of the study. Although nurse-led patient education on the need for DR screening is delivered to the diabetes clinic attendants, this does not address the inherent barriers that are experienced by patients living in rural communities, such as limited transportation and access to health care services [21]. Rural residence has not been reported to be a predictor of DR screening uptake in the previous African studies [13, 20]. This could have been due to the low numbers of rural-based patients who had undergone DR screening in the studies. Otherwise it has been reported from China and the United Kingdom that rural populations have lower access to DR screening facilities compared to urban populations and consequently have a lower uptake of DR screening [16, 22].

The longer waiting time that patients experience when they attend DR screening in the general eye clinic after the diabetes clinic is another possible reason for the low uptake of DR screening in our study. Long patient waiting time has been reported to be a deterrent for patients to utilise DR screening services in Africa [23]. A possible intervention to reduce the patient waiting time is the integration of DR screening into the diabetes clinic. This eliminates the need for patients to make a second visit to the eye clinic and ensures that DR screening is offered as part of the continuum of care in the diabetes clinic [24]. We thus suggest studies investigating the feasibility of integrating DR screening into diabetes clinics in secondary-level health facilities.

Other important patient-related factors that have been described to be barriers to accessing DR screening in low income countries include; a lack of knowledge on ocular complications of DM, lack of awareness about the importance of eye examination and lack of knowledge about availability of eye clinics [19]. In our study, being aware of the existence of DR screening services at the hospital was strongly associated with uptake for DR screening. Our findings suggest that health education on the availability of DR screening services has an important role in promoting uptake of DR screening in an opportunistic DR screening model.

Although awareness of the existence of DR screening services was an important predictor of uptake for DR screening in our study, only 59.1% of the participants had knowledge about the existence of the screening services at the facility. This is despite the observation that the patient population visited the diabetes clinic at average intervals of 1.2 months and that they routinely received group health education on the need for DR screening and the existence of the service. This suggests that the health education model being implemented through group counselling may have a low coverage among the patient population. This warrants research into the feasibility of integrating alternative health education models such as personalised counselling for DR into DM clinics. Personalised health education for DM and DR offered by primary health care workers in a rural setting was demonstrated to be effective in improving uptake for DR screening in India [25]. Another intervention that has been shown to be acceptable in an African setting is health education led by peers who have had DR screening [13, 20]. Thus, we suggest research into the effectiveness of peer-led health education to increase uptake of DR screening.

Besides awareness of the existence of DR screening services at the facility, the only other factor associated with uptake of DR screening on multivariate analysis was being individually referred by a clinician for DR screening and this was the strongest predictor of uptake. This is comparable to findings from Kenya where patients who had been referred for an eye examination had higher odds of having had a fundoscopy in the prior 12 months compared to those who had not been referred [13].

Our findings highlight that it may not be sufficient to provide group education to patients on when and where they should go for DR screening, rather it is also important to ensure that each patient with DM is individually referred by a DM clinician for screening. However, previous research from Africa has shown that less than a fifth of physicians caring for people living with DM refer their patients for DR screening [26]. In line with this, only a third of the participants in our study reported that they had been individually referred for DR screening by a clinician. This highlights a poor linkage between DM care and DR screening services. An intervention that has been suggested to promote both referral and screening for DR is integration of DR services into DM services to ensure that patients access them as one service [27].

Patients that have a longer history of DM (particularly of at least 10 years) have a higher risk of developing sight-threatening DR [28]. Thus it may be expected that they are more likely to be referred for DR screening or to have a higher perceived need for undergoing DR screening. Long duration of DM was reported to be a strong predictor of uptake of DR screening in Kenya, India and among non-indigenous populations in Australia [13, 29, 30]. However, comparable to findings from Tanzania, long duration of DM was not an independent predictor of DR screening uptake in our study [20]. One possible explanation for this is the shorter median duration of DM of 4 years among our patient population.

Comorbidity has been shown to increase health care utilisation in general among patients with DM [31]. In Kenya, comorbid hypertension was a predictor for having ever had an eye examination but not for eye examination within 12 months [13]. From our study, although a diagnosis of hypertension was an independent predictor of uptake of DR screening, this was not significant on multivariate analysis. In addition, HIV infection, another chronic comorbidity, had no association with uptake of DR screening.

Our study has some limitations. Due to the cross-sectional study design, a temporal relationship between the predictors of DR screening uptake and the uptake of DR screening could not be established. In addition, the association between the variables are subject to being significantly influenced by the small number of participants that underwent DR screening. Thus, the observations that age, level of education and visual acuity were not significantly associated with uptake of DR screening should be interpreted with caution. Previous reports from Kenya, Nigeria and mostly high income countries have shown that increasing age and low visual acuity are associated with increased attendance for DR screening [13, 19, 32, 33]. In contrast, low educational attainment and poor literacy have been reported to be associated with poor knowledge of DR and a lower uptake of DR screening irrespective of a country’s income level [19].

Another limitation of our study is that it did not have a qualitative component looking into the patient-related reasons for attendance or non-attendance to DR screening especially among the patients who were aware of the existence of DR services. In addition, due to lack of facilities for performing HbA1C at the study location, we could not investigate the relationship between uptake of DR screening and patients’ glycaemic control.

One strength of this study is that it is the first study to report on the uptake of DR screening at secondary level health facility in Malawi and the findings add to the limited body of literature on the uptake of DR screening in low income countries. Our findings are of value to policy makers and programme managers planning to improve diabetic retinopathy screening programmes in similar settings.

Conclusion

Our study showed that there was a low uptake of annual eye examinations through opportunistic DR screening at a secondary level diabetes clinic. Although awareness of DR screening services and a history of referral for screening were strong predictors of screening uptake, there was low awareness of the existence of DR screening services at the facility and most patients had not been referred for screening. Future research should investigate the feasibility of integrating DR counselling and screening services into routine DM care to promote DR screening uptake by increasing patient awareness and facilitating referrals.

Supporting information

S1 Checklist. STROBE statement.

(DOCX)

S1 Table. Variables collected as part of the study.

(XLSX)

Acknowledgments

We are grateful to Ms Asante Makuta for coordinating the implementation of the project. We are also thankful to Mr David Mtumodzi and Ms Myrnah Pendame for assisting in data collection.

Data Availability

The data for this this project is fully available without restriction through the following link DOI: https://doi.org/10.6084/m9.figshare.23710023.v1.

Funding Statement

This study was funded by the Non-communicable Diseases Building Research Capacity, Implementation and Translation Expertise consortium (NCD BRITE) mentored research grant to TZ for the period 2020 to 2022. The NCD BRITE consortium is supported by the National Heart, Lung, and Blood Institute of the National Institutes of Health under grant number 5U24HL136791 to AM. The funding covered participant compensation fees, communication costs and transportation costs for the study team. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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PLOS Glob Public Health. doi: 10.1371/journal.pgph.0002567.r001

Decision Letter 0

Nasheeta Peer

10 May 2023

PGPH-D-23-00555

Uptake of diabetic retinopathy screening at a secondary level facility in Malawi

PLOS Global Public Health

Dear Dr. Zungu,

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

Please submit your revised manuscript by Jun 24 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 globalpubhealth@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pgph/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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

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

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

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

We look forward to receiving your revised manuscript.

Kind regards,

Nasheeta Peer

Academic Editor

PLOS Global Public Health

Journal Requirements:

1. Please amend your detailed Financial Disclosure statement. This is published with the article. It must therefore be completed in full sentences and contain the exact wording you wish to be published.

a. State the initials, alongside each funding source, of each author to receive each grant.

b. State what role the funders took in the study. If the funders had no role in your study, please state: “The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.”

c. If any authors received a salary from any of your funders, please state which authors and which funders.

If you did not receive any funding for this study, please simply state: “The authors received no specific funding for this work.”

2. Please amend your Data Availability Statement and indicate where the data may be found.

Additional Editor Comments (if provided):

Introduction

Lines 64-71: please explain the reason for including a description of UK DR screening programme? Is it relevant to your context?

Lines 71-73: Why describe guidelines for a high-resource setting? Is it applicable to Malawi?

This section is too long; please shorten. The focus should be on Malawi with a clear motivation for conducting this study.

Lines 74-82: This may be incorporated into the Discussion section where it can be compared with the findings in this study. Describing screening in Tanzania and Kenya is not a motivation for this study conducted in Malawi.

Line 81: please improve your grammar – “blinding eye complications”.

Lines 103-105: The aims should be clearly articulated. E.g., “The aim of this study was to…”

Methods

Do patients pay for healthcare?

Does it cost more for DR screening?

Are the waiting times increased if patients undergo DR screening?

Do patients self-select for DR screening?

Are they not automatically provided with an appointment for DR screening?

Statistical analyses: what p-value level was considered statistically significant?

Results

Were only 230 patients seen at the clinic over a 3-month period - October 2020 to December 2020?

Table 1:

What does primary, secondary, etc. schooling refer to? This translates to how many years of schooling completed?

Use the word hypertension, not hypertensive.

Please include HbA1c levels, if available.

Table 1 and 3: please write 1.00 for the reference value for the logistic regression.

Note, this should be presented first.

Where is Table 2?

Discussion

Line 186: name the countries and describe the comparable, or otherwise, prevalence.

Lines 189-192: Please rephrase; there are numerous barriers, not a single one, for the absence of screening programmes.

Lines 203-204: What does “…health promotion on the need for DR screening” actually entail? Please provide more detail.

Why are all patients not routinely referred for DR screening at this diabetes clinic? How are patients selected for DR screening?

Line 220: What do you mean by ‘health care demand’?

Line 222: Uptake of what?

Line 224: replace ‘weak’ with non-significant’. What was the reason for this? Likely the small sample size. Please include.

Lines 232-233: Again, the small sample size with only 49 patients screened is likely the reason for the lack of significance and should be stated.

Line 235: please explain: ’among different races’ – why is race relevant to this study?

Recommendations: Please provide clear recommendations to improve DR at this clinic; these should be linked to your data.

What are areas for further research?

Include the small sample size as a major limitation.

Are there other such studies from Malawi or is it a first? Please include as a study strength.

You did not examine glycaemic control as a factor for DR; this is a limitation. If this data are available, please include in your analyses.

Line 249-254: Please move recommendations and future research to the Discussion section and link it directly to a study finding.

Lines 253-254: “alternative health education models” – the authors need to describe the current education model before advocating for a change.

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

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

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

Reviewer #1: Partly

Reviewer #2: Yes

Reviewer #3: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: Yes

**********

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

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

Reviewer #1: Yes

Reviewer #2: Yes

Reviewer #3: 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: The article addressed a relevant issue that requires more research, especially in low and middle-income countries.

However, the text lacks key contextual information to allow the readers to understand the many barriers people with diabetes face to access timely health care in Malawi.

For example, the article states that the prevalence of DM adults is 2% in rural areas and 3% in urban areas. However, the information comes from a cross-sectional study that, because of the sample size, provides only an estimate, shows that DM is a problem in the country and that there is a high prevalence of risk factors for developing diabetes.

There needs to be more information about Malawi’s health system: how many people have access to health insurance, out-of-pocket expenses, if the country has a DM program and policies, and if the DR screening program offers the exam free of cost. Also, there needs to be more information on the number of clinics that offer the DR screening programs, if these are located in urban or rural areas if there are regions or districts without facilities offering DR screening.

The methods part has to be reviewed and enriched. Authors stated that the protocol adhered to the tenets of the Declaration of Helsinki for research 123 involving human participants, and ethical approval was obtained from the College of 124 Medicine Research and Ethics Committee (study protocol number P.10/19/2803), however, there is no information about the procedure. Informed consent is a process that must respect the autonomy of the participants, and as for this research, recruitment happened within the clinics and has 0 refusal rate; there is a need to know if: recruiters were workers at the clinics, how power relations were addresses, how autonomy was guarantee (beyond the informed consent if for example people were informed about the research in the day of their visit to the clinic, and where invited to come back another day for be part of the research). There needs to be more information about who covered the screening costs. This information is critical to describe how the ethics of the research was guaranteed.

Reviewer #2: The article highlighted the importance of recognizing need for referrals and management for diabetic retinopathy management in underresourced settings. I would also comment if possible on the potential for scalability of this program in-country and methods for scalability and collaboration. It may also be helpful if doing further work after this study to collect information on HgA1c/glucose levels of patients that were referred or need referral for diabetic retinopathy screening. If possible, diabetic teaching and management could also be included during diabetic retinopathy screening as well.

Reviewer #3: Zungu T et al explore a key area in diabetes care of uptake of screening for diabetic retinopathy in a sub-Saharan African country.

Generally, the manuscript is well written with the rationale of the study well explained and the study methods used in data collection plus the exclusion and inclusion criteria well stated.

I have minor comments which the authors should respond to.

1. A more detailed description of the study site is needed. Does it serve a predominantly rural or urban area? How does have an effect on the observed low uptake of the screening services? Kindly elaborate.

2. For the section on predictors of screening services on page 9 and in Table 1 on page 10, add 95% CI to aid in better interpretation of the results.

3. Restrict your p-values to two decimal points apart from the highly significant ones of <0.001.

4. Could the authors also add a note on the availability and cost of treatment options of diabetes retinopathy in that hospital or in Malawi generally (both in the public and private sector) once a patient is diagnosed with severe forms of retinopathy like proliferative diabetic retinopathy.

5. On page 6, the authors highlighted how diabetic screening is done at the different healthcare levels. I would like to know if this screening also includes assessment of other forms of ocular conditions like glaucoma which is also an identifiable cause of blindness in patients with diabetes. If so, how is it done? If it is not done, explain why.

**********

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

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

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

Reviewer #1: No

Reviewer #2: No

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.

PLOS Glob Public Health. doi: 10.1371/journal.pgph.0002567.r003

Decision Letter 1

Nasheeta Peer

23 Aug 2023

PGPH-D-23-00555R1

Uptake of diabetic retinopathy screening at a secondary level facility in Malawi

PLOS Global Public Health

Dear Dr. Zungu,

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

Please submit your revised manuscript by Oct 07 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 globalpubhealth@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pgph/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

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

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

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

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

We look forward to receiving your revised manuscript.

Kind regards,

Nasheeta Peer

Academic Editor

PLOS Global Public Health

Journal Requirements:

Additional Editor Comments (if provided):

Introduction

Lines 99-116: Please shift most of this text on the Malawian context to the Methods section.

Results

The Editor disagrees with the Reviewer on the number of decimal places for p-values when reporting data. Please report all p-values to 3 decimal places in both tables and the main text, as is standard practice.

Discussion

Please improve the syntax of this section. There are many minor grammatical errors that need correction. I suggest a co-author (or anyone else) with an excellent grasp of the English language review this paper in detail for sentence construction, etc.

Lines 290-294: This is an overly long poorly constructed sentence extending over 5 lines with ‘findings’ used twice in the sentence. Please rework.

Lines 294-296: Are the findings from the literature comparable to this study or not? Please comment; that is the purpose of a Discussion.

Lines 297-305: How relevant is the urban-rural comparison to Malawi since most people (84%) live in rural areas? Please edit/rework the text.

Lines 310-314: Please improve the clarity of these sentences as well as the syntax.

Lines 330 and 441: Please replace ‘consumer’ with ‘patient’.

Areas for future research should be ‘suggested’ and not ‘recommended’; please reword accordingly (used in multiple texts). The authors should be more circumspect.

Line 370: replace ‘enough’ with ‘sufficient’.

Lines 370-372: Please improve the syntax.

Line 398: replace ‘condition’ with ‘comorbidity’ in keeping with the context of the paragraph.

Line 402-406: Please explain why a longer duration of diabetes would be associated with DR screening uptake. Simply reporting data from other studies does not contribute to a quality Discussion.

Line 407: Please include the reference for other low-income countries.

Lines 409-411: How does this impact/contribute to DR screening uptake?

Please be consistent with your spelling. I suggest using UK English uniformly e.g., ‘programme’, ‘glycaemic’, etc.

Line 420: ‘Commitment’ in terms of what? (Resources, funding, skills, etc.) Please expand briefly.

Line 424: improve the grammar; this is confusing.

Line 425: Replace ‘studied’ with ‘established’.

Line 429: Reports from which countries? Does it include Malawi?

Line 447: ‘secondary level’ what?

Lines 457-458: Is this feasible/ practical in Malawi where there is likely a shortage of skilled staff who are overburdened with a large volume of patients? The current trend is toward task-shifting i.e., to lower-level health personnel; however, the authors are now suggesting the reverse.

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

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

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

Reviewer #1: All comments have been addressed

Reviewer #3: All comments have been addressed

**********

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

Reviewer #1: Yes

Reviewer #3: Yes

**********

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

Reviewer #1: I don't know

Reviewer #3: Yes

**********

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

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

Reviewer #1: Yes

Reviewer #3: Yes

**********

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

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

Reviewer #1: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

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

Reviewer #1: The authors have addressed my coments regarding context, and ethics.

Reviewer #3: All comments raised have been addressed to my satisfaction.

**********

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

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

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

Reviewer #1: No

Reviewer #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.

PLOS Glob Public Health. doi: 10.1371/journal.pgph.0002567.r005

Decision Letter 2

Nasheeta Peer

13 Oct 2023

Uptake of diabetic retinopathy screening at a secondary level facility in Malawi

PGPH-D-23-00555R2

Dear Dr Zungu,

We are pleased to inform you that your manuscript 'Uptake of diabetic retinopathy screening at a secondary level facility in Malawi' has been provisionally accepted for publication in PLOS Global Public Health.

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

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

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

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

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

Best regards,

Nasheeta Peer

Academic Editor

PLOS Global Public Health

***********************************************************

Reviewer Comments (if any, and for reference):

Associated Data

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

    Supplementary Materials

    S1 Checklist. STROBE statement.

    (DOCX)

    S1 Table. Variables collected as part of the study.

    (XLSX)

    Attachment

    Submitted filename: Response to reviewers.docx

    Attachment

    Submitted filename: Response to reviewers.odt

    Data Availability Statement

    The data for this this project is fully available without restriction through the following link DOI: https://doi.org/10.6084/m9.figshare.23710023.v1.


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