|Year : 2018 | Volume
| Issue : 3 | Page : 196-200
Prevalence of diabetic retinopathy among children with type 1 diabetes mellitus treated by insulin
Emad E.M Elgemai1, Nema H Zeriban2, Shaimaa S Soliman3
1 Department of Ophthalmology, Magrabi Eye Hospital, Damanhour Teaching Hospital, Tanta, Egypt
2 Department of Pediatrics, Damanhour Teaching Hospital, Tanta, Egypt
3 Department of Public Health and Community Medicine, Faculty of Medicine, Menofia University, Menofia, Egypt
|Date of Submission||06-Mar-2018|
|Date of Acceptance||24-May-2018|
|Date of Web Publication||24-Sep-2018|
Emad E.M Elgemai
Department of Ophthalmology, Magrabi Eye Hospital, Damanhour Teaching Hospital, 31511 Tanta
Source of Support: None, Conflict of Interest: None
Purpose Among children and young adults, type 1 diabetes mellitus (DM) is the commonest type to occur as a result of defects in insulin secretion and/or insulin action. It is usually treated by insulin or insulin analogs. This work was done to study the prevalence of diabetic retinopathy (DR) among diabetic children with type 1 DM treated with insulin.
Patients and methods This is a cross-sectional study that was carried out in Damnhour Teaching Hospital. It included 115 children with type 1 DM from 6 to 14 years of age. All patients were subjected to full fundus examination and were then classified according to its results into patients with DR and patients without DR. Risk factors associated with retinopathy were assessed in those patients.
Results The mean age of the patients was 9.70±1.94 years and 55.7% were males. DR was found in 12 (10.4%) patients, eight of whom had retinopathy in one eye and four had retinopathy in both eyes. Mild nonproliferative DR was found in 11/230 (4.8%) eyes and moderate nonproliferative DR was found in 5/230 (2.2%) eyes. A significant positive correlation was found between the grade of retinopathy and the duration of diabetes (r=0.37; P<0.01), fasting blood glucose (r=0.36; P<0.01), and glycosylated hemoglobin (r=0.38; P<0.01).
Conclusion The prevalence of DR was 10.4% among all studied patients and 7.0% among all studied eyes. The grade of retinopathy was directly related to the duration of DM, fasting blood glucose, and glycosylated hemoglobin levels.
Keywords: children, diabetes mellitus, diabetic retinopathy, insulin, prevalence
|How to cite this article:|
Elgemai EE, Zeriban NH, Soliman SS. Prevalence of diabetic retinopathy among children with type 1 diabetes mellitus treated by insulin. Delta J Ophthalmol 2018;19:196-200
|How to cite this URL:|
Elgemai EE, Zeriban NH, Soliman SS. Prevalence of diabetic retinopathy among children with type 1 diabetes mellitus treated by insulin. Delta J Ophthalmol [serial online] 2018 [cited 2019 Mar 18];19:196-200. Available from: http://www.djo.eg.net/text.asp?2018/19/3/196/242144
| Introduction|| |
Type 1 diabetes mellitus (DM) is a clinical syndrome characterized by relative or absolute deficiency of insulin owing to either autoimmune destruction of pancreatic B-cells or genetic factors. Therapy for type 1 DM is mainly insulin. Old insulin formulations depend on a mixture of intermediate-acting and short-acting insulin, which may result in poor glycemic control and fluctuation of blood glucose levels with increased risk of complications .
The microvascular affection that occurs owing to DM usually includes the retinal capillaries and venules and can result in diabetic retinopathy (DR). This retinal microvascular complication is the commonest microvascular disease seen in children and adolescents having type 1 diabetes and is considered the leading cause of acquired blindness in young adults in the USA ,.
The risk factors for the development of DR include long duration of diabetes, poor glycemic control, hypertension, hyperlipidemia, and genetic predisposition ,,,. In addition, overweight (higher body mass index) and family history of diabetes or its complications are common risk factors .
The prevalence of DR and its related risk factors varies widely in different studies. Few studies reported that mild DR occurred in children with short duration of DM as 1–2 years, but most studies reported that a duration of at least 3 or more years is required for the development of DR with a typical duration of 8–10 years ,,,. Generally, in many studies, the prevalence of DR ranged from 0 to 28% ,,,,.
The prevalence of DR is significantly influenced by the long-term metabolic control. One study demonstrated this relationship when they found that patients with lower glycosylated hemoglobin (HbA1c) (<7.5%) had developed DR after an average of 18.3 years, which was longer than patients with HbA1c greater than or equal to 7.5% who had developed DR after an average of 15.5 years .
There are many guidelines for the screening of pediatric DR. However, they are more or less similar in giving annual screening recommendation after 3–5 years of the initial diagnosis of the disease ,,.
This work was conducted to study the prevalence of DR among diabetic children having type 1 DM treated with insulin.
| Patients and methods|| |
This cross-sectional descriptive analytical study included 115 children with type 1 DM attending the Endocrine Clinic of Damanhour Teaching Hospital from the period of January 2016 to January 2017.
The inclusion criteria were as follows:
- Age from 1 to 16 years old.
- Type 1 DM; treated by insulin, documented by increased blood glucose level, increased HbA1c, low C-peptide levels and weight within normal percentiles to exclude type 2 DM.
All the cases were subjected to complete physical examination, anthropometric measures (weight, height, etc.), and biochemical examination [HbA1c, T4, thyroid-stimulating hormone (TSH), anti-tissue transglutaminase and urine for microalbuminuria]. Fundus examination was done by indirect ophthalmoscopy (under sedation if required) or slit lamp biomicroscopy using 90 D noncontact lens. It included examination of the optic disc, macula, retinal blood vessels, background, and fundus periphery to detect any signs of DR. The central macular thickness was measured by SD-OCT (Topcon 3D OCT 2000; Topcon, Tokyo, Japan).
DR was defined and classified according to the International Clinical Diabetic Retinopathy Disease Severity Scale by Wilkinson et al. :
No apparent retinopathy: no abnormalities.
- Mild nonproliferative diabetic retinopathy (NPDR): only microaneurysms.
- Moderate NPDR: more than just microaneurysms but less than severe NPDR.
- Severe NPDR: any of the following:
- More than 20 intraretinal hemorrhages in each of the four quadrants.
- Definite venous beading in two or more quadrants.
- Prominent intraretinal microvascular abnormalities in one or more quadrants with no signs of proliferative retinopathy.
- Proliferative diabetic retinopathy (PDR): one or both of the following:
- Vitreous/preretinal hemorrhage.
According to fundus examination, patients were divided into two groups:
- Group I: patients with no DR.
- Group II: patients with DR.
The study was approved by the Ethical Committee of the General Organization for Teaching Hospitals and Institutes (Damanhour Teaching Hospital). An informed consent was obtained from each participant’s legal guardian before all the steps of the interview process and examination procedures with adherence to the guidelines of the declaration of Helsinki.
Data were collected, tabulated and statistically analyzed by an IBM compatible personal computer with SPSS statistical package version 23 (SPSS Inc., released 2015, IBM SPSS statistics for windows, version 23.0; IBM Corp., Armonk, New York, USA). χ2-Test and Fisher’s exact test were used to study the association between qualitative variables. Student’s t-test was used for comparison of quantitative variables between two groups of normally distributed data, whereas Mann–Whitney’s test was used for comparison of quantitative variables between two groups of not normally distributed data. Pearson’s correlation was used to show correlation between two continuous normally distributed variables whereas Spearman’s correlation was used for not normally distributed ones. Two sided P value of less than 0.05 was considered statistically significant.
| Results|| |
This study included 115 patients (230 eyes) aged from 6 to 14 years old having type 1 DM. Their mean age was 9.70±1.94 years, and males represented 55.7% (64 cases) of all the participants. The patients’ characteristics are detailed in [Table 1]a and b.
A total of 12 (10.4%) patients were found to have DR. Eight patients (7.0%, representing 3.4% of all eyes) had retinopathy in one eye and the other four (3.5%, representing 1.7% of all eyes) had retinopathy in both eyes. Thus, the total number of eyes with retinopathy was 16 of 230 screened eyes (7.0% of all eyes).
Most eyes with retinopathy had a mild degree of NPDR, as it was present in 11 eyes (4.8% of total eyes and 68.8% of the 16 eyes with retinopathy). The other five eyes (2.2% of total eyes and 31.3% of the 16 eyes with retinopathy) had moderate degree of NPDR, whereas none of the eyes had PDR ([Table 1]b). In addition, eyes with retinopathy had significantly higher central macular thickness (315.65±42.34 μm) than the normal eyes (233.91±20.63 μm), with a P value less than 0.001.
Spearman correlation analysis revealed significant positive correlation between the grade of retinopathy from one side and each of the duration of DM, fasting blood glucose (FBG), and HbA1c from the other side (P<0.01 for all; [Table 2]).
|Table 2 Spearman correlation between grade of retinopathy and the patients’ characteristics|
Click here to view
There was no significant difference between patients without and patients with retinopathy regarding age, weight, BMI or laboratory investigations. However, the mean duration of DM, mean FBG, and mean HbA1c were significantly higher in patients with DR (P=0.009, 0.01, and 0.008, respectively; [Table 3]).
|Table 3 Comparison between patients without and patients with diabetic retinopathy regarding their personal and laboratory characteristics|
Click here to view
| Discussion|| |
DR is a potentially blinding complication of diabetes especially in children and young adults, hence the importance of screening and routine fundus examination . In the past few years, routine fundus examination has been added to the health insurance system for adults in Egypt. However, routine screening in the young age is still facing difficulties, may be because of caregiver incompliance or the incompliance of the child parents themselves.
Among the 115 screened children, 12 (10.4%) children were found to have DR in varying degrees. Four patients had bilateral DR and the other eight had unilateral DR, which equals 16 (7.0%) eyes with DR among the 230 screened eyes. Close results were stated by Silverstein et al.  in their statement of the American Diabetes Association about the care of children and adolescents with type 1 diabetes. They stated that retinopathy usually starts after puberty in those children. However, pre-Diabetes Control and Complications Trial found that 9.0% of children younger than 13 years had background DR with very low incidence of PDR. They recommended ophthalmological screening after the age of 10 years and for children who have diabetes for 3–5 years.
A study published more recently in the year 2015 by Tapley et al.  reported a lower prevalence rate than the current study. They studied 236 pediatric patients with either type 1 or type 2 DM and 5.5 years as a mean duration of DM. They detected DR in 3.8% of participants. In addition, Kernell et al. , in 1997, detected retinopathy in 5% of patients between 8 and 10 years of age, which is less than our results. However, a higher prevalence of DR was found by Eppens et al. , who found DR in 254 (20.0%) of 1264 patients with type 1 DM, with a mean age of 15.7 years.
In the present study, most of the affected eyes were having mild affection. Mild degree of DR was found in 11 eyes, whereas the other five eyes had a moderate degree; this represents 4.8 and 2.2% of the total screened eyes, respectively. Symmetrical affection was found in two patients with bilateral mild DR. The other two patients with bilateral affection had mild DR in one eye and moderate DR in the other eye. This is in agreement with Tapley et al. , who found that 4.3% of the affected eyes had unclassifiable/ungradable lesion followed by background DR in 3.0% of the affected eyes, with 0.9% of the eyes having PDR and 0.4% with maculopathy.In the current study, age and sex of the patients did not affect the presence of DR. Only, the duration of DM was the personal risk factor to be significantly associated with DR. The laboratory characteristics of the screened patients showed that FBG and HbA1c levels were significantly associated with the presence of DR. Other laboratory investigations like T4, TSH or microalbuminuria were not significantly associated with DR. Lueder et al. , in the clinical report of the American Academy of Pediatrics reported that age was not linked to DR, however, it was the duration of the disease which was linked to the development of DR, and children younger than 10 years were at minimal risk of developing DR. Some of these clinical aspects were studied by Eppens et al.  in their comparison between type 1 and type 2 DM. They found no significant difference between both types regarding age at last assessment or sex. They also found that the duration of DM and HbA1c were significantly higher in type 1 than type 2 DM. However, microalbuminuria was significantly higher in type 2 than type 1 DM.
Age of the patients and duration of DM were not correlated with the degree of DR, whereas the levels of FBG and HbA1c were highly correlated with the grade of DR. Significant positive correlations were present between the grade of DR and duration of DM, FBG, and HbA1c. Other laboratory markers like T4 or TSH were not correlated with the grade of DR. No previous study described the correlation between the grade of retinopathy and the laboratory results of the patients. This may be owing to the low prevalence of DR among children and adolescents with type 1 DM and because most of the cases have mild or background DR.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Fong DS, Aiello LP, Ferris FL. Diabetic retinopathy. Diabetes Care 2004; 27:2540–2553.
Lueder GT, Silverstein J, Section on Ophthalmology and Section on Endocrinology, American Association for Pediatric Ophthalmology and Strabismus. Clinical Report Guidance for the Clinician in Rendering Pediatric Care. Screening for retinopathy in the pediatric patient with type 1 diabetes mellitus. Pediatrics 2005; 116:270–273.
Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol 1984; 102:520–526.
Sultan MB, Starita C, Huang K. Epidemiology, risk factors and management of pediatrics diabetic retinopathy. Br J Ophthalmol 2012; 96:312–317.
Ogle G, Middlehuurst A, Silink M, Hanas R. International society for pediatric and adolescent diabetes (ISPAD), International diabetes federation. IDF/ISPAD 2011 Global guideline for diabetes in childhood and adolescence. Available at: https://www.ispad.org/page/idfispad2011globalG?
Accessed April 2017.
Dorchy H, Claes C, Verougstraete C. Risk factors of developing proliferative retinopathy in type 1 diabetic patients: role of BMI. Diabetes Care 2002; 25:798–799.
Holl RW, Lang GE, Grabert M, Heinze E, Lang GK, Debatin KM. Diabetic retinopathy in pediatric patients with type-1 diabetes: effect of diabetes duration, prepubertal and pubertal onset of diabetes, and metabolic control. J Pediatr 1998; 132:790–794.
Donaghue KC, Fairchild JM, Chan A, Hing SJ, King J, Howard NJ, Silink M. Diabetes micro vascular complications in prepubertal children. J Pediatr Endocrinol Metab 1997; 10:579–585.
Verougstraete C, Toussaint D, De Schepper J, Haentjens M, Dorchy H. First microangiographic abnormalities in childhood diabetes − types of lesions. Graefes Arch Clin Exp Ophthalmol 1991; 229:24–32.
Malone JI, Grizzard S, Espinoza LR, Achenbach KE, van Cader TC. Risk factors for diabetic retinopathy in youth. Pediatrics 1984; 73:756–761.
Kristinsson JK, Gudmundsson JR, Stefansson E, Jonasson F, Gislason I, Thorsson AV. Screening for diabetic retinopathy: initiation and frequency. Acta Ophthalmol Scand 1995; 73:525–528.
Gallego PH, Wiltshire E, Donaghue KC. Identifying children at particular risk of long-term diabetes complications. Pediatr Diabetes 2007; 8(Suppl 6):40–48.
Massin P, Erginay A, Mercat-Caudal I, Vol S, Robert N, Reach G et al.
Prevalence of diabetic retinopathy in children and adolescents with type1 diabetes attending summer camps in France. Diabetes Metab 2007; 33:284–289.
Majaliwa ES, Munubhi E, Ramaiya K, Mpembeni R, Sanyiwa A, Mohn A, Chiarelli F. Survey on acute and chronic complications in children and adolescents with type 1 diabetes at Muhimbili National Hospital in Dar essalaam Tanzania. Diabetes Care 2007; 30:2187–2189.
Donaghue KC, Craig ME, Chan AK, Fairchild JM, Cusumano JM, Verge CF et al.
Prevalence of diabetes complications 6 years after diagnosis in an incident cohort of childhood diabetes. Diabet Med 2005; 22:711–718.
American Academy of Ophthalmology Retina Panel. Preferred practice pattern: diabetic retinopathy. San Francisco: American Academy of Ophthalmology; 2003. 1–63
Aiello LP, Gardner TW, King GL, Blankenship G, Cavallerano JD, Ferris FL, Klein R, American Diabetes Association. Diabetic retinopathy. Diabetes Care 2002; 25(Suppl 1):S90–S93.
American Academy of Pediatrics. Section on endocrinology and section on ophthalmology. Screening for retinopathy in the pediatric patient with type 1 diabetes mellitus. Pediatrics 1998; 101:313–314.
Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M et al.
Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 2003; 110:1677–1682.
Silverstein J, Klingensmith G, Copeland K, Plotnick L, Kaufman F, Laffel L et al.
Care of children and adolescents with type 1 diabetes. Diabetes Care 2005; 28:186–212.
Tapley JL, McGwin G Jr, Ashraf AP, MacLennan PA, Callahan K, Searcey K et al.
Feasibility and efficacy of diabetic retinopathy screening among youth with diabetes in a pediatric endocrinology clinic: a cross-sectional study. Diabetol Metab Synd 2015; 24:7–56.
Kernell A, Dedorsson I, Johansson B, Wickström CP, Ludvigsson J, Tuvemo T et al.
Prevalence of diabetic retinopathy in children and adolescents with IDDM: a population-based multicentre study prevalence of diabetic retinopathy in children and adolescents with IDDM. A population-based multicentre study. Diabetologia 1997; 40:307–310.
Eppens MC, Craig ME, Cusumano J, Hing S, Chan AK, Howard NJ et al.
Prevalence of diabetes complications in adolescents with type 2 compared with type 1 diabetes. Diabetes Care 2006; 29:1300–1306.
[Table 1], [Table 2], [Table 3]