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Psychosomatic Medicine 69:537-542 (2007)
© 2007 American Psychosomatic Society

ORIGINAL ARTICLES

Depression is a Risk Factor for Poor Glycemic Control and Retinopathy in African-Americans With Type 1 Diabetes

Monique S. Roy, MD, Alec Roy, MD and Mahmoud Affouf, PhD

From the University of Medicine and Dentistry (M.S.R.), New Jersey Medical School, Institute of Ophthalmology and Visual Science, Newark, New Jersey; Psychiatry Service (A.R.), Veterans Administration Medical Center, East Orange, New Jersey; and Department of Mathematics (M.A.), Kean University, Union, New Jersey.

Address correspondence and reprint requests to Monique S. Roy, Department of Ophthalmology, UMDNJ-New Jersey Medical School, 90 Bergen Street, Room 6164, Newark, NJ 07101-1709. E-mail address: Roymo{at}umdnj.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Objective: To examine longitudinal data about depression in relationship to glycemic control and as a risk factor for diabetic retinopathy (DR). Depression is a common psychiatric disorder among diabetic persons and has been shown in cross-sectional studies to be associated with the vascular complications of diabetes.

Methods: A total of 483 African-American patients with Type 1 diabetes had a baseline examination and 6-year follow-up examination. Evaluations at both visits included administering the Beck Depression Inventory (BDI), a detailed ophthalmologic examination, retinal photographs, and measurement of glycosylated hemoglobin as an index of glycemic control. Six-year progression of DR between baseline and follow-up visits was evaluated from the change in retinopathy severity using the Early Treatment of Diabetic Retinopathy Study grading scale.

Results: Patients with high BDI scores at both baseline and 6-year follow-up visits had significantly higher baseline glycosylated hemoglobin values (p = .01), and were more likely to show progression of DR (odds ratio (OR) = 2.44; 95% confidence interval (CI): 1.01–5.88; p = .049) and progression to proliferative diabetic retinopathy (PDR) (OR = 3.19; 95% CI: 1.30–7.87; p = .01) than patients with low BDI scores at both visits. This was independent of baseline medical risk factors for DR.

Conclusion: Six-year longitudinal data indicate that depression is significantly associated with both poor glycemic control and higher 6-year progression to PDR in African-Americans with Type 1 diabetes.

Key Words: depression • diabetes • glycemic control • retinopathy

Abbreviations: AER = albumin excretion rate; BDI = Beck Depression Inventory; CI = confidence interval; DR = diabetic retinopathy; HbA1C = hemoglobin A1C; HPA = hypothalamo-pituitary-adrenal; OR = odds ratio; PDR = proliferative diabetic retinopathy.


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Depression is a common psychiatric disorder among diabetic persons. Several studies have reported that 10% to 25% of persons with diabetes develop a major depressive episode at some time (1–7). In recent years, studies in persons with either diabetes or other medical diseases have demonstrated that comorbid depression adversely affects outcome (8–12). In a meta-analysis of studies of diabetic patients in whom depression was assessed, depression was found to be significantly associated with diabetic vascular complications (13).

One major adverse vascular complication of diabetes is diabetic retinopathy (DR), the leading cause of new cases of legal blindness in Americans aged 20 to 64 years (14). We previously examined the medical risk factors for DR in 725 African-American patients with Type 1 diabetes (15). We found that poor glycemic control assessed from glycosylated hemoglobin levels, systemic hypertension, and proteinuria are the main medical risk factors associated with DR (15–17). However, these risk factors accounted for only 37% of the variance in the severity of DR among our African-American patients. We subsequently carried out a 6-year follow-up of these diabetic patients (18). At both the baseline and 6-year follow-up visits, patients completed the Beck Depression Inventory (BDI) (19).

The studies included in De Groot's meta-analysis of depression in relationship to diabetic vascular complications were cross-sectional in design (13). In that meta-analysis report, a need was identified for prospective studies to also investigate pathways that might mediate the association between depression and diabetic complications. Therefore, we decided to examine the longitudinal data from our 6-year follow-up of diabetic African-American patients to determine if depression affects glycemic control and progression of DR. We hypothesized that our Type 1 diabetic patients with high BDI scores at both visits would have significantly higher glycosylated hemoglobin levels and have greater progression of DR over the 6-year follow-up period. To test these hypotheses, we a) examined the association of BDI scores with glycemic control as evaluated from glycosylated hemoglobin data at both visits, and b) carried out logistic regression analyses using BDI scores and our previously reported medical risk factors in relationship to 6-year progression of DR (18).


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 
Study Population
From 1982, all patients admitted to the 116 hospitals in New Jersey with a discharge diagnosis of diabetes mellitus are reported to the New Jersey Department of Health. This information comprises the computerized New Jersey Hospital Discharge Data for patients with diabetes mellitus. In this database, 68,455 names of African-Americans with either a primary or secondary diagnosis of diabetes mellitus were listed. Included in the original cohort were patients with Type 1 diabetes identified from the random review of 13,615 patient charts from 31 hospitals located in the seven counties lying within a 20-mile radius of the New Jersey Medical School, Newark (20). Inclusion criteria were: acute onset of diabetes before 30 years of age, insulin therapy instituted within the first 6 months of the diagnosis of diabetes, and continuous insulin therapy from that time (21). Excluded were patients with Type 2 diabetes, those diagnosed after age 30 years whether or not they received insulin, and patients with maturity-onset diabetes of youth (21,22).

Of the 875 eligible patients, 725 participated in the baseline examination between 1993 and 1998, and 508 (70.1%) of these 725 participated in a 6-year follow-up examination between October 1999 and August 2004 (18,20). Of the 217 patients who did not have a follow-up examination, 44 (6.1%) patients could not be located, 34 (4.7%) patients refused examination, and 139 (19.2%) patients had died in the 6-year interval (18). Twenty-five (4.9%) of the remaining 508 participants seen at the 6-year follow-up were no longer receiving insulin at follow-up. Because they may not be truly insulin-dependent, they were excluded from the study, leaving 483 (82.4%) of the 508 patients available for incidence data analyses (18). The mean ± standard deviation time of follow-up was 6.1 ± 0.5 years and median time of follow-up was 5.96 years.

Procedures
Examinations at both visits followed a similar protocol, which had been approved by the Institutional Review Board of the University of Medicine and Dentistry of New Jersey, New Jersey Medical School, Newark, New Jersey. Patients were examined in the Eye Clinic at University Hospital in Newark at both initial visit and 6-year follow-up. On arrival, the patients provided informed written consent. At both visits, a structured clinical interview was conducted which included detailed medical and ophthalmologic histories and sociodemographic factors. The BDI was administered to patients ≥18 years of age (19).

Patients had a detailed eye examination including seven standard stereoscopic Diabetic Retinopathy Study retinal photographs (23). Blood pressure was measured twice in the sitting and standing positions. A venous blood sample was drawn for measurement of total glycosylated hemoglobin, using high-pressure liquid chromatography, and for high- and low-density lipoprotein and total cholesterol, using an enzymatic assay and separation spectrophotometry. The normal range for total glycosylated hemoglobin is 4.2% to 7.0% and the intra-assay coefficient of variation is 0.38% to 1.47%. The interassay coefficients of variation are 3% for values of 0.04 to 0.07, 2% for values 0.08 to 0.12, 1.5% for values 0.12 to 0.15, and 1% for values of >0.15. A 4-hour timed urine sample was obtained for measurement of albumin excretion rate (AER) and creatinuria using spectrophotometry. These data regarding medical risk factors in relationship to progression of DR have been previously reported (18).

DR Grading
Color fundus photographs obtained at both baseline and 6-year follow-up were graded in a blind fashion by the Wisconsin Fundus Photograph Reading Center in Madison, Wisconsin, to obtain gradings using the modified Airlie House classification of DR (24,25). The classification has 12 levels of DR severity (10 through 85) including proliferative DR (PDR), levels of ≥61. DR severity for a participant was determined from the grade of the worse eye. To evaluate the progression of DR, we used a 13-step scale similar to that described by Klein and associates (26). The data about the 6-year progression of DR have been previously reported (18).

Definitions
Socioeconomic factors included the patient's level of education (for those >25 years of age), personal income (for those >18 years of age), and family income. Patient's socioeconomic status was classified according to Goldthorpe and Hope social grading of occupations (27). Systemic hypertension was defined as present if at baseline either the systolic pressure was ≥140 mm Hg or the diastolic pressure was ≥90 mm Hg, or the patient was taking antihypertensive medication. Microproteinuria was defined as present if the baseline AER was 20 to 200 µg/min, and overt proteinuria was defined as present if the baseline AER was >200 µg/min.

Progression to PDR over the 6-year follow-up was calculated for all patients who did not have PDR at baseline. Progression of DR was calculated for patients who had no DR or nonproliferative DR (level < 61) at baseline and who progressed at least two steps between baseline and follow-up examinations (26). When examining two-step progression, patients with PDR at baseline were excluded. These data have been previously reported (18).

Statistical Analyses
Patients who at both baseline and 6-year follow-up had a BDI score of either >14 or ≤14 were compared for baseline demographic and diabetic characteristics using the t test for continuous variables and {chi}2 tests for categorical variables. Incidence rates with 95% confidence intervals (CI) were calculated for progression of DR and progression to PDR.

Univariate logistic regression modeling was applied to BDI scores and baseline medical variables to estimate odds ratio (OR) and 95% CI to predict two end-points: progression of DR and progression to PDR. A p < .05 was considered significant. Multiple logistic regression models were used to examine independent associations between risk factors and progression of DR by entering baseline characteristics significant on univariate analysis and using both forward and backward selections. Generalized adjusted coefficients of determination (r2) were used to estimate the relative contribution of the baseline characteristics.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 NOTES
 REFERENCES
 
Of the 483 patients who had a 6-year follow-up, 409 had the BDI administered at baseline. Of these 409 patients, 99 (24.2%) had a BDI score of >14. At the 6-year follow-up, 443 of the 483 diabetic patients completed the BDI. Of these 443 patients, 100 (22.6%) had a BDI score of >14. There were 51 patients with a BDI score of >14, and 264 patients with BDI scores of ≤14 at both baseline and 6-year follow-up visits.

Relationship of BDI Scores and Baseline Demographic and Diabetic Characteristics
Patients with a BDI score of >14 at both baseline and 6-year follow-up visits (n = 51) had significantly higher baseline glycosylated hemoglobin values than the patients with BDI scores of ≤14 at both visits (n = 264) (p = .01) (Table 1). There were no other significant differences for baseline socioeconomic or clinical characteristics except for age and a history of smoking (Table 1). When BDI scores were examined separately either at baseline or follow-up, no significant relationship was found with either glycosylated hemoglobin or progression of DR (data not shown).


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  		TABLE 1. Diabetic Patients With BDI Scores of >14 and ≤14 at Both Baseline and 6-Year Follow-up Visits Compared for Baseline Demographic and Diabetic Characteristic

 

Depression and Baseline Risk Factors in Relationship to Progression of DR Univariate Analysis
Depression and Progression of DR
Patients who were depressed at both baseline and follow-up were on average three times more likely to show progression of DR (p = .01) or progression to PDR (p = .001) than nondepressed patients (Table 2).


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  		TABLE 2. Depression and Other Baseline Characteristics in Relationship to 6-Year Progression of DR: Univariate Analysis

 

Baseline Medical Risk Factors and Progression of DR
Patients in the upper two quartiles of glycosylated hemoglobin values at baseline were more likely to show progression of DR and progression to PDR at 6-year follow-up, as in our previous report in a slightly larger sample (18) (Table 2). Patients with baseline systemic hypertension or proteinuria were more likely to have progressed to PDR at 6-year follow-up (Table 2).

Multivariate Analysis
In the multiple logistic regression model, having a BDI score of >14 at both visits was significantly and independently associated with progression of DR (p = .049) and progression to PDR (p = .01) (Table 3). Baseline glycosylated hemoglobin values were significantly and independently associated with progression of DR and progression to PDR (all p < .001) (Table 3) similar to our previous report (18). Baseline duration of diabetes and systemic hypertension were significantly and independently associated with progression to PDR (18) (p < .001 and p < .001, respectively) (Table 3). Similar results were also found when patients depressed at both visits (n = 51) were compared with the rest of the patients (n = 432).


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  		TABLE 3. Depression and 6-Year Progression of DR and Progression to PDR: Multivariate Analysis

 

In the full model, baseline glycosylated hemoglobin values accounted for 21% and being depressed at both visits accounted for 6% of the progression of DR; baseline glycosylated hemoglobin values, hypertension, and duration of diabetes accounted for 21% and being depressed at both visits accounted for 6% of progression to PDR.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
NOTES
 REFERENCES
 
In the present 6-year longitudinal follow-up study of Type 1 diabetic African-Americans, we found that glycemic control, hypertension, and longer duration at baseline were medical risk factors strongly associated with 6-year progression to PDR, as previously reported (18). In addition, and to a lesser degree, being depressed at both baseline and follow-up was a new risk factor significantly and independently associated with progression of DR and progression to PDR in this population. Thus, our longitudinal data confirm and extend previous reports suggesting that depression in diabetic patients may have a significant negative impact on the morbidity of the diabetes. In particular, our data are consistent with the conclusion from a meta-analysis of 10 cross-sectional studies that depression in diabetic patients is significantly associated with DR (13).

Poor glycemic control has been shown to be associated with all complications of diabetes (15–17). Thus, it is of interest that another result of the present study was that depression was significantly associated with higher baseline glycosylated hemoglobin, a measure of glycemic control. Similarly, Van Tilburg et al. found a significant association between BDI scores and hemoglobin A1C (HbA1C) levels in Type 1 diabetic persons (28). Lustman et al. found that HbA1C levels, controlled for weight and insulin dose, were significantly higher in depressed Type 1 diabetic persons compared with nondepressed patients (9). In that study, there was also a significant association between HbA1C levels and depression severity (9). Furthermore, the authors reported that, within the depressed diabetic group, there was a stepwise increase of adjusted HbA1C levels in relationship to depression severity. This may be analogous to the results of the present study in which depressed diabetic patients with BDI scores of >14 at both visits showed higher glycosylated hemoglobin levels.

However, that depression is associated with DR independently of glycemic control also raises the possibility of other mechanisms. Lustman et al. suggested that the depression-hyperglycemia relationship may not be mediated by diabetes self-care behavior and that other pathways, including pathophysiology, should be studied (9). The pathophysiology of depression may include changes in neurotransmitter function, changes in coagulation factors and vascular endothelial function, altered platelet function, alteration of immune and inflammatory responses, alteration in insulin resistance and glucose resistance, and dysregulation of the hypothalamo-pituitary-adrenal (HPA) axis (29–41).

HPA axis dysregulation and the resulting hypercortisolemia may be associated with changes in insulin resistance and steroid production (35,37). We have previously reported that Type 1 diabetic persons have mild chronic hypercortisolemia as shown by raised fasting morning plasma cortisol, increased urinary free cortisol, and altered endocrine responses to challenge with intravenous corticotropin-releasing hormone (42–44). Depression may also be associated with dysregulation of the noradrenergic system (45–47). Thus, it is noteworthy that, in patients with another diabetic vascular complication, i.e., coronary artery disease, depressive symptoms were found to be associated with significantly increased 24-hour urinary norepinephrine and cortisol excretion (48,49).

Limitations of the present study include the fact that our sample was African-American—thus limiting the ability to generalize to other populations. Also, although inclusion criteria for Type 1 diabetes were followed for the initial recruitment of patients, more recent reports suggest that diabetes in African-Americans may be a more complex disease (50,51). Further, our Type 1 diabetic patients had been admitted to the hospital at some time in the past, which might also limit the generalizability of the results to all Type 1 diabetic persons. However, the patients were randomly identified from a large database. Of note, 95% of Type 1 diabetic persons have reportedly had a diabetes-related admission at some time (52,53).

Another possible limitation is that we used the BDI, a self-report measurement of depression symptom severity, rather than an observer-rated assessment of depression like the Hamilton Depression Rating Scale. However, the BDI has been used widely to measure depressive symptoms in patients with other medical disorders such as coronary artery disease (54). In their meta-analysis, Barth et al. found that the low cut-off score of 10 on the BDI was sufficient to indicate an increased mortality risk from coronary disease (54). In the present study, we used a higher BDI cut-off score of >14, because we had used it in our previous studies on depression in diabetic patients (7). Also, in diabetic persons, the BDI somatic items may be a confound (55). However, it is noteworthy that BDI cut-off scores of 12 to 14 have been found to have high predictive value as a screening instrument for depressive disorders in both the general population and in diabetic patients (55,56). Nonetheless, further studies of the relationship of depression and diabetic complications might use a structured psychiatric interview to obtain current and lifetime history of depressive disorder including data about recurrent episodes and dysthymia.

Strengths of the present study include the longitudinal data about progression of DR obtained from the 6-year follow-up, the administration of the BDI on two occasions, that all participants had a detailed ophthalmologic evaluation, and that glycosylated hemoglobin—an index of glycemic control—was obtained on two separate visits. The possible clinical implications may include the identification and treatment of depression in Type 1 diabetic persons, particularly those with retinopathy, so that treatment of depression may be instituted. In this regard, it is noteworthy that the recent Pathways Study in largely Type 2 diabetic persons showed that depression in diabetic patients can be effectively treated (57).


   NOTES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
REFERENCES
 
Received for publication October 25, 2006; revision received March 30, 2007.

This research was supported by Grant RO1 EY 09860 from National Eye Institute, Bethesda, MD, and a Lew Wasserman Merit Award from Research to Prevent Blindness, Inc., New York, NY.

DOI:10.1097/PSY.0b013e3180df84e2


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 NOTES
 REFERENCES
 

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