Cascading Screening for Diabetic Retinopathy at the University Teaching Hospitals: strategies to overcome barriers

Kangwa I. M. Muma1,2,3, Jessie I. M. Nyalazi2, Chisomo Mbewe2, Timothy Kangwa2, George Zulu2, Grace Chipalo – Mutati2,3 and Gardner Syakantu4

1National Eye Health Coordination, Directorate of Clinical Care and Diagnostic Services, Ministry of Health, Lusaka, Zambia

2University Teaching Hospitals – Eye Hospital, Lusaka, Zambia

3Department of Ophthalmology, School of Medicine and Clinical Sciences, Levy Mwanawasa Medical University, Lusaka, Zambia

4School of Medicine and Clinical Sciences, Levy Mwanawasa Medical University, Lusaka, Zambia

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Objective: To develop a diabetic retinopathy strategy for early detection of sight-threatening diabetic retinopathy in Zambia.

Background: The Ministry of Health (MoH), Zambia, embarked on a programme to scale up the initiative for Universal Health Coverage of services across the continuum of health care throughout the country. The University Teaching Hospitals (UTHs) was tasked to play a pivotal role in this noble cause in line with MoH’s vision of bringing health as close to the family as possible. A National Diabetic Retinopathy Screening (DRS) programme was commenced in 2012 in collaboration with the Frimley Park Hospital of the United Kingdom (UK).

Methods: The DRS programme is based on fundus camera screening using the UK protocol. This is both community and hospital based. The idea was to develop strategies that would ensure the capture of all diabetic patients in the country and have them screened for diabetic retinopathy (DR). A national Diabetes Mellitus (DM) register was also to be created where all the DM patients would be registered and accounted for. The UTHs – Eye Hospital (UTHs – EH) was to implement the programme at the University Teaching Hospitals (UTHs), in Lusaka Province and oversee the roll out the national DRS programme through the National Eye Health Coordination (NEHC) office. In this endeavour, in 2018, the UTHs – EH introduced a weekly DRS screening clinic at the medical clinic of the UTHs – Adult Hospital (UTHs – AH) to increase the uptake of DRS by all the DM patients attending the diabetic clinic.

Results: A total of 1517 DM patients had both their eyes screened for DR at the UTHs from January 2016 to June 2019 of which nine hundred and ninety-three (993) were screened at the UTHs – EH compared to 524 (34.5%) screened at the UTHs – AH. Screening at UTHs – AH started in 2018. For the years 2016 and 2017, 36.9% (560/1517) participants were screened compare to 43.2% (656/1517) in 2018 of which 50.6% (332/656) were screened at the UTHs – AH and 49.4% (324/656) at the UTHs – EH. Quarters one and two of 2019 saw 63.8% (192/301) participants screened at UTHs – AH compared to 36.2% (109/301) at the UTHs – EH. Overall, 57.2% (524/957) participants were screened at the UTHs – AH in 2018 and 2019 implying that the setting up of this service significantly increased the uptake of DRS by 57.2%, p < 0.0001. There was an increase of the patients attended to by 63.7% from 102 in quarters one and two in 2016 to 167 in the same quarters in 2019. The hosting of the DRS clinic by the medical clinic also enhanced collaboration in the management of DR between ophthalmologists and physicians at the UTHs. Nine hundred and twenty-two (922) participants screened had DR making the prevalence of DR 60.8%.

Conclusion: The 57% more DM patients screened at the UTHs – AH demonstrated a huge need of following the DM patients to the medical clinic in order to increase the uptake and compliance to have DR screening. Thinking without the box strategies including collaboration of all disciplines involved in the DM management is vital in scaling up the DRS and preventing blindness due to DR. The study demonstrated the importance of creating convenience for the patients and making the service not only relevant but readily available to the public.

Keywords: Diabetes Mellitus, Diabetic Retinopathy, Diabetic Retinopathy Screening, Prevalence



Diabetes mellitus (DM), commonly known as diabetes, is a group of metabolic disorders characterized by high blood sugar due to either the pancreas not producing enough insulin (TYPE 1), or the cells of the body not responding properly to the insulin produced (TYPE 2) [1]. With the rise of a more sedentary lifestyle in both developed and developing countries, the global prevalence of DM is increasing rapidly. Diabetes prevalence in Zambia was reported at 6.2% in the population aged 20 to 79 years [3].

In the United States of America (USA) and UK, diabetic retinopathy is an important cause of visual impairment and blindness among adults aged 20–74 years [4]. About 50–73% of those with visual impairment or blindness because of DR can be prevented by early detection and treatment of risk factors, and by photocoagulation [5,6]. With timely laser treatment and intravitreal anti-vascular endothelial growth factor (VEGF) therapy, severe vision loss from DR can be reduced by 90% [7,8,9]. Diabetic retinopathy is not only a blinding condition but also affects visual functions that affect performance of daily activities like contrast sensitivity [10].

In the Copperbelt province of Zambia, a population-based study on 2153 diabetic participants identified at various health centres and recruited in the DRS programme found some form of DR in 52% of participants and 36% had sight-threatening DR [11]. The reported prevalence rate was higher than most estimates from other studies; be it hospital-based or population-based. Several classification systems exist for grading severity of DR. In Zambia the United Kingdom Diabetic Retinopathy Grading System (UKDRGS) using fundus photos is used (Table 1). In this study, the UKDRGS was used [11].

Table 1: Grading of DR based on retinal images

R0 None No abnormalities / No DR
R1 Background Microaneurysm(s) Retinal haemorrhage(s) Venous loop Any exudate in the presence of other features of DR Any number of cotton wool spots (CWS) in presence of other features of DR
R2 Pre-proliferative Venous beading Venous reduplication Multiple blot haemorrhages Intraretinal microvascular abnormality (IRMA)
R3 Proliferative  
 R3aNew vessels on disc (NVD)New vessels elsewhere (NVE)New pre-retinal or vitreous haemorrhageNew pre-retinal fibrosisNew tractional retinal detachment
 R3sStable pre-retinal fibrosis + peripheral retinal scatter laserStable fibrous proliferation + peripheral retinal scatter laserStable R2 features + peripheral retinal scatter laserR1 features + peripheral retinal scatter laser
 M0No maculopathyAny microaneurysm or haemorrhage within 1DD of the centre of the fovea if associated with a best VA of ≤ 6/12 where the cause of the reduced vision is known and is not diabetic macular oedema.
 M1Exudate within 1-disc diameter (DD) of the centre of the foveaGroup of exudates within the maculaRetinal thickening within 1DD of the centre of the fovea (if stereo available)Any microaneurysm or haemorrhage within 1DD of the centre of the fovea only if associated with a best VA of ≤ 6/12 (if no stereo)CSMO – Retinal thickening at or within 500 microns of the centre of the maculaCSMO – Hard exudates at or within 500 microns of the centre of the macula, if associated with thickening of the adjacent retina (not residual hard exudates remaining after disappearance of retinal thickening) hard exudates remainingCSMO – A zone or zones of retinal thickening one-disc area or larger, any part of which is within one-disc diameter of the centre of the macula.
 P0No evidence of previous photocoagulation (default)
 P1Focal/grid to macula or peripheral scatter
 UAn image set that cannot be graded

(Core NDESP team, 2012)

African studies have shown low numbers of diabetic participants having routine eye examinations. A study done in Tanzania looking at participants not being part of any screening programme for DR found that only 29% of participants had had an eye examination in the previous year [12]. Similarly, in a South African study, 48.3% of participants had their last eye examination more than a year and a half period [13]. However, in a Saudi Arabian study, about 95% of participants had regular eye examinations, much higher than in the African set up [14].

A multiple case study by Poore et al. (2014) evaluating DR screening programmes in 2014 in Botswana, Ghana, Tanzania and Zambia noted a lack of local data in Africa on the scale of DR problem and that even in participants that were screened, uptake of referrals to the eye department was the main challenge [15].

Mild and moderate non-proliferative DR can be managed by good systemic glycaemic control and regular ophthalmoscopy examinations. Severe Non-proliferative DR, proliferative DR and centre-involving macular oedema require urgent treatment to prevent vision loss. With the advent of retinal laser photocoagulation therapy and anti- Vascular Endothelial Growth Factor (VEGF) agents, DR and maculopathy can be treated to prevent blindness if detected early enough [16]. Studies such as the Early Treatment of Diabetic Retinopathy Study (ETDRS) have shown that treatment with retinal laser photocoagulation can reduce the incidence of severe vision loss in participants with sight-threatening DR [17].

Diabetic Retinopathy Screening

Timely screening and treatment for DR can prevent morbidity. As early DR is asymptomatic, the International Diabetic Foundation (IDF) guidelines recommend early detection of DR by means of DR screening which is very effective in the proper management of DR [19]. It is only through screening that diagnosis and treatment can be made at an early stage and prevent sight threatening DR [20]. The importance of eye screening programme is to reduce the risk of sight loss amongst people with diabetes by the prompt identification and effective treatment if necessary, of sight-threatening DR, at the appropriate stage during the disease process [21].

Feasible and efficacious methods for increasing screening follow-up rates include patient education, a streamlined referral and scheduling process, and collaboration with local ophthalmologists and primary care providers [18]. Diabetic patients should be educated on the importance of regular eye examinations to detect early retinopathy [18, 20]. Even with the control of retinopathy risk factors such as high blood pressure, high serum cholesterol, poor diabetic control, smoking, obesity, and renal disease, regular ocular examination is highly recommended [20]. This is because long duration of the disease is probably the most significant risk factor for retinopathy [21]. Since diabetes is by nature a chronic ailment, most patients ultimately develop retinopathy in the course of the disease.

Prevention of visual loss in DR has improved considerably during the last decade, especially in northern Europe due to robust screening programmes in place [22]. Patient compliance with DR screening is not optimal, as shown by attendance rates ranging from 32 to 85% [24,25,26,27,28]. To increase DR screening attendance, insight into incentives and barriers to retinopathy screening is necessary. However, longer diabetes duration, older age and diabetes-related visual problems are associated with screening compliance [28,29]. In the USA, financial barriers are also often reported [27,28,29,30]. Nevertheless, the main barrier for compliance was the patient’s belief that they do not have DR [31]. Other factors were embarrassment about poor glycaemic control and fear of ophthalmological examination and treatment [32]. Many conclude that patients’ lack of awareness (due to lack of education/ information) is the main obstacle to attend a screening programme [26,32,33,34,35]. In view of the major investments in screening and treatment programmes, developing interventions to reduce non-compliance should be a priority [23]. another barrier is the making of appointments for eye screening at the eye facilities which be situated far from the medical clinic and could have a programme that is not aligned to favour immediate attention of the DM patients. There is also the barrier of travelling long distances to go for eye check-up. These barriers result in low uptake and follow-up rates of DM patients for DR [22].

Several types of screening programmes have been designed throughout the world to meet the DR problem. We report on our active screening programme for diabetic eye disease and describe the sight and eye condition of the diabetic patients who have been involved in this programme.


Study design

This was a retrospective study.

Study duration

January 2016 to June, 2019

Study site

The study was carried out at the University Teaching Hospitals (UTHs) in Lusaka. The DM patients in this study were recruited weekly from the medical clinic (clinic 5) of the Adult Hospital and the outpatient clinic at the Eye Hospital.

Study population

All diabetes mellitus patients seen at the medical and eye clinics at the UTHs

Inclusion criteria

All patients with a diagnosis of diabetes mellitus attending the medical clinic at the UTHs – AH and UTHs – EH were eligible for DR screening programme and could participate. Fundus photographs taken were graded in accordance with the DR grading system used in the UK National Health service (NHS). Visual impairment data were collected from visual acuity measurements recorded using Snellen chart.

Exclusion criteria

None was excluded

Study sample

All diabetes mellitus patients seen at the medical clinic and the eye clinic who have not had it done and those due for their annual DRS. For the study, no patient was recruited more than once.

Sampling technique

Every consecutive diabetic patient meeting inclusion criteria was included in the study.

Data collection instruments

A researcher-administered questionnaire adapted from the current form used in screening programme at UTHs – Eye Hospital and Adult Hospital. The questionnaire contained information regarding the demographic characteristics of the patients, the relevant diabetic medical and ocular history. A section for the findings of blood pressure, visual acuity and retinopathy grading was included. Other tools included a Snellen chart with pinhole, Digital Retinography System (DRS, Centervue, Italy) fundus camera and manual Sphygmomanometer

Data collection procedure 


Diabetic patients’ records were recruited to be included in the study at the adult hospital weekly medical clinic for diabetes and other endocrinology conditions.

Measurement of blood pressure, VA with pinhole to get the Best Corrected Visual Acuity (BCVA) was done. Ophthalmic nurses from the Eye hospital trained in fundus imaging and DR grading were used as research assistants. Then the patients’ pupils were dilated with a mydriatic that had a combination of tropicamide 0.8% and phenylephrine 5%. 1 eye drop was instilled in each eye and repeated as needed to achieve adequate pupillary dilatation.

DRS fundus camera was used to capture retinal images on patients dilated with mydriatically dilated pupils. Both colour and red-free retinal images were captured from both eyes and graded to assess the severity of retinopathy. The worse eye or the eye with a gradable image was used in the analysis. The principle investigator read all retinal images and graded using the international classification of DR. One ophthalmologist reviewed randomly selected images to ensure quality and adherence to the international standard and protocol for the study.

Sight-threatening DR was defined as any of the following: moderate pre-proliferative retinopathy or worse (level 40–71 +); macular exudates in a circinate pattern or within one disc diameter of the foveal centre or clinically significant macular oedema (level 3–4: sight-threatening maculopathy); or other diabetes-related retinal vascular disease: central or branch retinal artery occlusion, central or branch retinal vein occlusion.

Data analysis

Data was collected and entered in Excel spread sheet. Analysis was then done using SPSS version 24. Continuous variables were tested for normality using Shapiro-Wilk test. The chi square and Mann-Whitney tests were used to compare no DR to DR depending on the type of variable. To determine the correlation between two normally distributed independent variables Pearson coefficient was used; while Spearman coefficient was used for non-normally distributed variables. In the final analysis to rule out confounders, a multiple logistic regression model was constructed using a cut off of 20% for the variables. Age, HbA1c (in some patients) and use of Anti-HTN medication were included in the final analysis due to significant associations found in several other studies. The model helped identify factors that were associated with DR after adjusting for baseline characteristics. A p-value <0.05 was regarded as significant.

Ethical considerations

The University of Zambia Biomedical Research Ethics Committee (UNZABREC) approved the study (reference number 169-2019) and was carried out in compliance with the Helsinki Declaration (2006). Further approval was obtained from Ministry of Health of Zambia through the UTHs to use the data capture records.

Limitations of the study

This study was a retrospective one and some data could not be found.


Demographic details

A total of 1517 diabetic patients were screened from January 2016 to June 2019. Of the 1517 patients 93.8% had at least one eye of gradable quality for statistical analysis. The male patients represented 36.3% (550/1517) and the female counterparts 63.7% (967/1517). Mean age was 55. (SD 14.1), median age was 58 (SD14.1) and range was 66 years. Mean reported duration of diagnosed diabetes was 4 years (SD 3.1), median was 5 years and range was 45 years.

Table 2: Gender versus Screening Centre, N = 1,517

SexScreening CentreTotal
Eye HospitalAdult Hospital

Table 3: Year Seen versus Screening Centre, N = 1,517

Year ScreenedScreening CentreTotal
Eye HospitalAdult Hospital

Figure 1: Year seen versus Screening Centre

Table 4: Age Group versus Screening Centre, N = 1,517

Age GroupScreening CentreTotal
Eye HospitalAdult Hospital
10 – 19221.5120.8342.3
20 – 29211.4251.6463.0
30 – 39614.0513.41127.4
40 – 4915710.41137.527017.9
50 – 5926017.11258.238525.3
60 – 6930620.21248.143028.3
≥ 7016610.9744.924015.8

Figure 2: Participants attended to according to age group

The clinical characteristics of the patients included in statistical analysis were: type 1 diabetes 10.5% (160/1517), type 2 diabetes 80.6% (1223/1517) and unspecified diabetes 8.9% (134/1517). The females had more type 2 diabetes at 63.8% (780/1223) than their male counterparts, 36.2% (443/1223). However, there was no statistical difference between the females and the males, p = 0.665; table 5. The type 2 diabetes patients had suffered more from hypertension 43.7% (534/1223) than the type 1 patients 25.0% (40/160) and this was statistically significant, p < 0.001; table 5.

Table 5: Type of DM versus other parameters

 DM Typep
Type IType IINot Known
            n        %         n      %              n       % 
Sex      0.665
Age group      <0.001
 10 – 193119.4%30.2%00.0% 
 20 – 292012.5%211.7%53.7% 
 30 – 391811.3%816.6%139.7% 
 40 – 492918.1%22218.2%1914.2% 
 50 – 592314.4%33027.0%3223.9% 
 60 – 692314.4%36830.1%3929.1% 
Duration      0.493
 ≤ 57647.5%57947.3%7455.2% 
 > 5 – 104125.6%28923.6%3324.6% 
 > 10 – 152415.0%17013.9%1410.4% 
 > 20106.3%1189.6%75.2% 
 Not known95.6%675.5%64.5% 
Hypertension      <0.001
Family history      0.011

Family history of diabetes was positive in 51.5% (781/1517) and 48.5% (736/1517) reported no family history of diabetes. Family history was statistically significantly different between the types 1 and 2 diabetic patients with 53.2% (649/1223) of type 2 diabetes having a positive family history compared to 40.5% (64/160) of the type 1 cohort; table 5.  Of the 160 type 1 diabetes patients, 89.4% (143/160) were on insulin compared to 32.3% (395/1223) of the type 2 diabetes patients. The majority 61.0% (746/1223) of the type 2 diabetes patients while 2.6% (32/1223) were on both oral hypoglycaemics and insulin.

Diabetic retinopathy

The prevalence of DR was graded based on the worst affected eye and the results are shown in Table 6. Sixty point eight per cent (60.8% (922/1517)) of all DM patients (type 1, type 2 and type unspecified) showed evidence of DR. Forty one per cent of patients graded (41.0% (623/1517)) had sight threatening DR. Five point seven per cent (5.7% (86/1517)) of all patients were graded as having proliferative DR which was distributed as 3.8% in type 1 diabetics (6/160) compared to 5.8% (71/1223) of type 2 diabetics (p = <0.001).

Prevalence of sight threatening DR was 31.3% (50/160) in type 1 diabetics compared to 43.1% (526/1517) of type 2 (p = <0.001).

Table 6: Prevalence of DR

             No DR              DR
nPrevalence %nPrevalence %
Age Group    
 10 – 19264.480.9
 20 – 29284.7182.0
 30 – 39579.6556.0
 40 – 4913823.213214.3
 50 – 5914925.023625.6
 60 – 6912821.530232.8
Family History    
 Yes 21035.342045.6
 ≤ 538865.234137.0
 > 5 – 1013122.023225.2
 > 10 – 15467.716217.6
 > 20183.011712.7
 Not known122.0707.6
DM Type    
 Type I7913.3818.8
 Type II46377.876082.4
 Not Known538.9818.8


The DR screening programme at the UTHs meets the World Health Organization criteria for screening programmes, which stipulates that early DR must be recognized, acceptable treatment options available and recognize DR as an important public health concern [36]. Efforts to increase patient screening   for   DR   should   accompany efforts to increase patient education regarding the disease. This is the practice currently at the UTHs. Despite efforts to educate people about DR in USA in 2012, the national survey showed that 73% of adults aged 40 and over with DR were unaware of their condition [37]. At the UTHs only 25.7% of the participants were not aware of the DR challenge. This was particularly so in patients with less severe DR, shorter diabetes duration, and lack of a recent eye examination just as was reported in other studies [37]. This shows that eye health education and promotion must be an ongoing programme. Some studies have shown that follow-up rates increase most with education. A randomized, controlled study in 1999 showed that intensive education to an intervention group increased follow-up appointment rates to about 54%, from about 27% [38]. This should include the sensitisation and education of physicians and nurses dealing with DM patients in the medical departments. This proved to be very crucial in improving uptake at the UTHs by setting up a DR screening facility at the medical clinic. Health promotion was also critical in this exercise which further improved the uptake of the DR screening services.

Current DR screening guidelines recommend a retinal examination of at least once per year in type 1 diabetics 5 years after diagnosis whereas Type 2 diabetes patients should be examined immediately at the time of diagnosis and at least annually thereafter. More frequent examinations are advised for patients with progressing retinopathy [10]. The retinal examination should be conducted by an ophthalmologist, optometrist or a medical licentiate in ophthalmology (known as ophthalmic medical practitioner (OMP)) who should look through a dilated pupil using the indirect or direct ophthalmoscope or slit lamp biomicroscopy [10]. This is the practice at the UTHs.

Disparities   in   screening   rates   exist   between   ethnic, socioeconomic, and geographical groups nationally and in North Carolina [39]. A North Carolina survey of people with diabetes showed that approximately 70% of non-Hispanic whites and African Americans received eye examinations in the year before the survey, compared to 61% of Native Americans and 52% of Hispanics [39]. The study did not investigate the details of possible disparities among the people seeking DR services.

Screening rates also vary by geographic location, with rural populations having lower rates of screening, likely due to issues with access to care [40]. In this study 81.5% were from the urban setting and 18.5% from the rural setting/high density areas. Diabetes patients with retinopathy who have access to retinopathy screening at or near the office of their primary care provider may more likely be screened out of convenience compared with those who are referred to an eye health care specialist [41]. This tends to be the case in the hospital settings as well were we saw that uptake improved by 57% when the screening was introduced at the medical clinic. Other potential barriers to screening include financial difficulties and language differences [42]. This was not a barrier in our case.

Improving screening rates for DR can improve focus for research and inform policy. This can also help in enhancing interventions utilized in different communities to increase patient and provider awareness, collaboration with community-based programmes and disciplines, using electronic medical records and automatic reminders, utilizing mobile diabetes clinics, and providing services in multiple languages [42]. The University of North Carolina’s management of diabetes patients is a current example of a health care system utilizing electronic medical records, automatic reminders, and interdisciplinary collaboration [18]. The UTHs have to introduce electronic data capture and records for easy access and to prevent loss of records and to promote interdisciplinary collaboration. This should be escalated to the whole country in order to capture all DM patients and screen them for DR and later store data for planning and research purposes.

In   many   locations   around   North   Carolina, diabetes patients were seen for initial eye examinations; retaining these patients for their follow-up has been a bigger challenge [18]. This difficulty in following up with patients is not just a USA phenomenon; a study by Keenum et al. based largely on an African American population in an urban setting, less than 30% of the study participants adhered to their recommended follow-up ophthalmic examinations [43]. These patients had access to a health care centre housing both ophthalmology and primary care physicians in the same building that welcomed patients, including those without insurance [43]. Poor compliance was more so in younger patients [43]. This is what was implemented at the UTHs where a one stop DR screening clinic was created were patients were attended by the physicians and soon after that the ophthalmic team took over and conducted a thorough DR screening. This collaboration strategy led to uptake increase of 57%.

The strategy also created convenience for the patients to be attended to and patients were not required to make appointments of being attended at a later date at the UTHs EH.

The fact that this study minimized the access barriers to immediate screening and aided with scheduling follow-up, suggests that additional barriers to DR screening can be overcome through more collaboration with all the stakeholders dealing with DM. More research is needed to elucidate factors involved in low uptake and follow-up rates. Anecdotal data at the UTHs EH showed that only 25.0% of the DM patients adhered to the recommended follow up plans.


A one stop DR screening clinic is fundamental in improving the uptake of DR services. Cascading screening for DR requires effective strategies such collaboration between the physicians and the ophthalmologists within the hospital setting. This strategy increased uptake and follow up of DR patients at the UTHs by 57%. This led to early detection of DR and early intervention in case of sight threatening DR. Fundus photography improves DR screening and retention because screening will be done by other medical personnel and ophthalmologists will grade the photos later and come up with management plans.


Fundus photography telemedicine provides an alternative strategy for obtaining the retinal examination. This method involves a trained photographer taking retinal images and sending them to a remote trained reader (typically an ophthalmologist or DR graders) for interpretation. Fundus photography telemedicine has been shown to have acceptable sensitivity and specificity for screening of diabetic retinopathy compared to in-person screens. It is also cost-effective and generally well-liked by patients. System alerts can also be used in letting primary care providers know when eye examinations are due and when they have been completed, giving them the opportunity to remind and counsel patients. Putting up fundus photography across the country and training people to capture the images for transmission to the DR grading centre will prevent patients from travelling long distances to be screened.

One way of implementing tele-medicine and tele-screening is by utilisation of the training hubs for the Levy Mwanawasa Medical University (LMMU). This will enhance both training and screening of DM patients for DR and the images will be analysed and interpreted from the DR centre at LMMU.


Potential conflicts of interest. All authors have no relevant conflicts of interest.


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