Clinical Profile of Elderly Patients (Over 90 Years) with Type 2 Diabetes Seen at a Diabetes Center in South India

Abstract

Background:

The current life expectancy in India is <70 years. Type 2 diabetes mellitus (T2DM) is known to reduce life expectancy by 6–8 years. Hence elderly people with T2DM in India would be rare. We report on the clinical profile of Asian Indian patients with T2DM who lived beyond 90 years of age and compared them with T2DM patients aged 50 to 60 years.

Methods:

From the diabetes electronic medical records of >470,000 diabetes patients, we identified T2DM patients who had lived ≥90 years and compared them with those in the 50–60 years age group, matched for gender and duration of diabetes. Clinical data included age at last visit, age at diagnosis, duration of diabetes, family history, smoking and alcohol, details of medications, body mass index (BMI), and blood pressure. Biochemical data included fasting and postprandial plasma glucose, glycated hemoglobin, fasting and stimulated C-peptide levels, lipid profile, and renal function studies. Assessment of retinopathy, nephropathy, neuropathy, coronary artery disease (CAD), and peripheral vascular disease (PVD) was also done.

Results:

A total of 325 T2DM patients aged ≥90 years and 278 T2DM patients aged between 50 and 60 years were selected for the study. Patients aged ≥90 years had higher systolic blood pressure (P < 0.001) and lower BMI (P < 0.001) than those between 50 and 60 years. Prevalence of retinopathy (29.7% vs. 53.5%) and macroalbuminuria (3.7% vs. 16.0%) was lower in the ≥90 years T2DM patients than in the 50–60 years age group. However, prevalence of neuropathy (89.8% vs. 50.8%), PVD (13.5% vs. 2.0%), and CAD (60.3% vs. 32.0%) was higher among the ≥90 years patients. Eighty-five percent of the T2DM aged ≥90 years were on oral hypoglycemic agents (OHAs), (of whom 64.9% were on sulfonylurea), 12% were on insulin, and 3% on diet alone. Among the 50–60 years old, 87.8% were on OHAs and 12.2% on insulin.

Conclusions:

This is the first report on the clinical profile of Asian Indians with T2DM aged ≥90 years, and significant differences are seen in their clinical profile compared with younger T2DM patients.

Introduction

According to the 2011 census, only 5.5% of the population of India was in the geriatric age group, defined as ≥65 years of age.^1

–4The current life expectancy in India is 67 years for males and 69 years for females.⁵ Type 2 diabetes mellitus (T2DM) is known to reduce life expectancy, on an average, by 6–8 years.⁶ Thus, one would expect that T2DM at very elderly age groups would be uncommon in India.

As the life expectancy increases, the prevalence of T2DM also could be expected to increase parallelly, as age is a nonmodifiable risk factor for T2DM. Although a few studies have reported on the very elderly with T2DM,^7
–9 they have focused mainly on the prevalence of diabetes and very few have reported on clinical features of these patients. Moreover, diabetes that sets in at a very old age appears to be a milder form of T2DM and Ahlqvist et al.¹⁰ have termed this as mild age-related diabetes (MARD). Reports on T2DM patients who have lived beyond 90 years of age are rare. In this study, we report on a series of Asian Indian patients with T2DM, who are known to have lived >90 years of age and compare their clinical profile with T2DM patients in the 50–60 years age group who were matched for gender and duration of diabetes. We believe this is the first report on Indian nonagenarians with T2DM.

Research Design and Methods

From the diabetes electronic medical records (DEMR) of >470,000 patients with diabetes registered at our center in southern India, we identified 325 individuals with T2DM who were known to have lived ≥90 years of age. We then matched these individuals with a group of 278 individuals aged between 50 and 60 years with T2DM who were matched for gender and duration of diabetes. Wherever possible, the patients were contacted and the latest clinical and biochemical data as well as assessment of micro and macrovascular complications were done. In others, who had died or were unable to come for the follow-up visit, the latest data available in the DEMR were used for the analysis.

Institutional Ethics Committee approval was obtained for the study. Only those who had provided written informed consent to use anonymized medical data were included in the study.

Clinic procedures

At each clinic visit, patients underwent an evaluation according to a standard protocol followed at the center. In brief, this involves elicitation of detailed history including details of medications used, exercise, and dietary assessment. Waist circumference was measured and body mass index (BMI) was calculated as the ratio of weight in kilogram divided by of height in meters squared. Blood pressure was measured using standardized techniques. Assessment of biochemical parameters includes fasting plasma glucose (FPG), postprandial plasma glucose (PPG) after a standardized breakfast, glycated hemoglobin (HbA1c), and lipid profile. Assessment of complications was done wherever possible. All details were entered in the DEMR at each visit. The clinic visit concluded with a consultation with a physician.

Biochemical methods

Plasma glucose (hexokinase method), serum cholesterol (cholesterol oxidase–peroxidase–amidopyrine method), triglycerides (glycerol phosphate oxidase–peroxidase–amidopyrine method), and high-density lipoprotein (HDL) cholesterol (direct method–polyethylene glycol–pretreated enzymes) were measured using Hitachi-912 Autoanalyzer (Hitachi, Mannheim, Germany) using kits supplied by Roche Diagnostics (Mannheim, Germany) and low-density lipoprotein (LDL) cholesterol was calculated using the Friedewald formula.¹¹ Urinary albumin concentration was measured in a fasting urine sample using an immunoturbidometric assay (Hitachi 902 autoanalyzer; Roche Diagnostics). The intra- and interassay coefficients of variation (CVs) for the biochemical assays ranged between 3.1% and 7.6%. Fasting and stimulated (90 min after a standard breakfast consisting of 300 calories and 60 g of carbohydrates) C-peptide levels were estimated by the electrochemiluminescence method using an Elecsys 2010 machine (Hitachi).^12,13 HbA1c was estimated by high-performance liquid chromatography using the Variant machine (Bio-Rad, Hercules, CA). The CV for the HbA1c assay was <3.5%. Our laboratory is certified by the College of American Pathologists as well as the National Accreditation Board for Testing and Calibration of Laboratories.

Definitions

Diabetes was diagnosed if the FPG level was ≥126 mg/dL (7.0 mmol/L) and/or 2 h postload glucose level was ≥200 mg/dL (11.1 mmol/L) and/or if the patient had been prescribed pharmacotherapy (oral hypoglycemic agents [OHAs] and/or insulin) for diabetes by a physician.¹⁴ T2DM was diagnosed by absence of ketosis, good β-cell reserve as shown by fasting [C-peptide assay] [>0.6 pmol/mL], and stimulated C peptide >1.0 pmol/mL and response to OHAs for at least 2 years.^12,13 Hypertension was diagnosed based on drug treatment for hypertension or if blood pressure was 140/90 mmHg.¹⁵

Hypercholesterolemia was defined as total cholesterol levels ≥200 mg/dL (5.2 mmol/L), hypertriglyceridemia as serum triglyceride ≥150 mg/dL (1.7mmol/L), high LDL cholesterol as LDL cholesterol levels ≥100 mg/dL (2.6 mmol/L), and low HDL cholesterol, as HDL cholesterol levels <40 mg/dL (1.0 mmol/L) in men and <50 mg/dL (1.3 mmol/L) in women.¹⁶

Assessment of complications

Assessment of diabetes complications was done as given hereunder, usually at baseline and yearly thereafter, or at the earliest subsequent follow-up visit, in patients who failed to report for the annual visit.

Retinopathy

A comprehensive ocular examination was performed and visual acuity was recorded using an illuminated Snellen chart. A detailed retinal (fundus) examination using direct and indirect ophthalmoscopy was performed by a retinal specialist trained in grading of retinal lesions. Retinal (fundus) photography was performed using four-field stereo color retinal photography (model FF 450 Pluscamera; Carl Zeiss, Jena, Switzerland) whenever possible. An early treatment diabetic retinopathy study grading system that has been modified and standardized in other population-based studies was used for the diagnosis of diabetic retinopathy.¹⁷

Nephropathy

Urinary albumin concentration was measured in a fasting urine sample using an immunoturbidometric assay (Hitachi 902 autoanalyzer; Roche Diagnostics). Microalbuminuria was diagnosed if the albumin excretion was between 30 and 299 g/mg creatinine. Macroalbuminuria was diagnosed if albumin excretion was ≥300 g/mg creatinine. Nephropathy was defined as presence of either micro- or macroalbuminuria.¹⁸

Neuropathy

Neuropathy was assessed using a biothesiometer. Vibratory perception threshold of the great toes was measured in a standardized manner by a single observer, and neuropathy was diagnosed if the mean vibratory perception threshold was ≥20 V.¹⁹

Peripheral vascular disease

Peripheral vascular disease (PVD) was diagnosed by measurement of ankle–brachial pressure index (ABPI) using a Doppler probe. Blood pressure recordings were made of the brachial pulses in the upper limb. Similar recordings were made of the dorsalis pedis and posterior tibial pulses in the lower limb by inflating the cuff proximal to the ankle, and the mean of these two readings was taken as the ankle pressure. ABPI <0.9 was considered diagnostic of PVD.²⁰

Coronary artery disease

Coronary artery disease (CAD) was diagnosed based on a documented history of myocardial infarction or drug treatment for CAD and/or Minnesota codes 1-1-1 to 1-1-7, [Q wave changes] 4-1 to 4-2 [ST segment depression] or 5-1 to 5-3 [T wave abnormalities] on the electrocardiogram or history of revascularization, stenting, and coronary bypass graft.²¹

Statistical analysis

Continuous variables are presented as mean (standard deviation) and categorical variables, as proportions. Student's t-test was used for continuous variables and the chi-square test for categorical variables. P value <0.05 was considered as statistically significant. All statistical analyses were conducted using the Statistical Package for the Social Sciences (version 15.0; SPSS, Inc., Chicago, IL).

Results

A total of 603 patients were included for the study, 325 aged ≥90 years and 278 between 50 and 60 years. Table 1 lists the clinical and biochemical characteristics of the two groups of patients. The mean ages of the two groups were 93.3 ± 2.8 years and 58 ± 2.3 years, respectively. The mean ages at diagnosis of diabetes were 69 ± 14 years and 37 ± 10 years, respectively, in the two groups. The patients aged ≥90 years had higher systolic blood pressure and HDL cholesterol levels, but lower BMI, FPG, PPG, HbA1c, and serum triglycerides than those aged 50–60 years. Mean C-peptide levels were not different between the two groups. Significantly rates of family history of diabetes (23% vs. 54.2%) and lower obesity (27.7% vs. 62.5%) were observed in the ≥90 years group than the 50–60 years age group. The prevalence of hypertension was 68% in the ≥90 years age group and 62.9% in the 50–60 years age group (P = 0.055).

Table 1.

Clinical and Biochemical Characteristics of the Type 2 Diabetes Mellitus Patients (Aged ≥90 Years and 50–60 Years)

Variables	T2DM patients aged ≥90 years (n = 325)	T2DM patients aged 50–60 years (n = 278)	P
Gender (males)	202 (71.1)	189 (68.0)	0.418
Age (years)	93.3 ± 2.8	58 ± 2.3	<0.001
Age at onset (years)	69.0 ± 14.0	37 ± 10	<0.001
Duration of diabetes (years)	23 ± 14	22 ± 10	0.321
Systolic blood pressure (mmHg)	139 ± 18	132 ± 16	<0.001
Diastolic blood pressure (mmHg)	80 ± 8	81 ± 8	0.137
BMI (kg/m²)	24.0 ± 4.0	26 ± 4	<0.001
FPG (mg/dL)	160 ± 72	179 ± 77	<0.003
PPG (mg/dL)	258 ± 95	275 ± 102	0.042
HbA1c (%)	8.5 ± 2.2	9.0 ± 1.4	0.001
Serum creatinine (mg/dL)	0.98 ± 0.32	0.84 ± 0.42	0.003
Fasting C-peptide (pmol/mL)	1.0 ± 0.6	1.0 ± 0.4	1.00
Stimulated C-peptide (pmol/mL)	2.0 ± 0.9	2.0 ± 0.8	1.00
Serum cholesterol (mg/dL)	182 ± 46	173 ± 48	0.025
Serum triglycerides (mg/dL)	144 ± 81	169 ± 112	0.003
HDL-cholesterol (mg/dL)	44 ± 11	38 ± 8	<0.001
LDL-cholesterol (mg/dL)	105 ± 37	100 ± 37	0.143
Treatment [n (%)]
Diet only [n (%)]	10 (3.0)	0 (0.0)	—
Sulfonylurea [n (%)]	211 (64.9)	122 (43.9)	<0.001
Metformin [n (%)]	38 (11.7)	86 (31.0)	<0.001
Sulfonylurea + metformin [n (%)]	20 (6.2)	17 (6.1)	0.984
DPP4 inhibitors	7 (2.2)	19 (6.8)	0.005
Insulin [n (%)]	39 (12.0)	34 (12.2)	0.931
Statins [n (%)]	89 (27.0)	40 (14.4)	<0.001
Aspirin [n (%)]	46 (14.1)	71 (25.5)	<0.001
Antihypertensive drugs [n (%)]	146 (44.6)	111 (39.9)	0.216
Current smoking [n (%)]	29 (9.0)	39 (14.0)	0.048
Alcohol [n (%)]	21 (6.4)	35 (12.6)	0.014
Overweight^* (23.0–24.9 kg/m²)	63 (19.4)	51 (18.4)	0.741
Obese^* (≥25.0 kg/m²)	90 (27.7)	173 (62.5)	<0.001
Positive family history of diabetes [n (%)]	75 (23.0)	142 (54.2)	<0.001
Hypertension [n (%)]	221 (68.0)	175 (62.9)	0.055
Hypercholesterolemia (≥200 mg/dL)	100 (30.8)	70 (26.1)	0.028
Hypertriglyceridemia (≥150 mg/dL)	96 (29.5)	114 (42.5)	0.040
Low HDL cholesterol (<40 mg/dL for males; <50mg/dL for females)	126 (38.8)	193 (72.3)	<0.001
High LDL cholesterol (≥100mg/dL)	135 (41.5)	133 (50.6)	0.526

WHO Asia Pacific Guidelines.

BMI, body mass index; DPP4, dipeptidyl peptidase 4; FPG, fasting plasma glucose; HbA1c, glycated hemoglobin; HDL, high-density lipoprotein; LDL, low-density lipoprotein; PPG, postprandial plasma glucose; T2DM, type 2 diabetes mellitus.

Treatment pattern was as follows in the ≥90 years age group and 50–60 years age group, respectively: sulfonylurea (gliclazide or glimiperide) (64.9% vs. 43.9%, P < 0.001), metformin (11.7% vs. 31.0%, P < 0.001), sulfonylurea and metformin combination (6.2% vs. 6.1%, P = 0.984), dipeptidyl peptidase 4 inhibitors (2.2% vs. 6.8%, P = 0.005), insulin (12.0% vs. 12.2%, P = 0.931), and diet alone patients aged (3% vs. 0%, P = 0.002). Thus, overall 85% of the T2DM ≥90 years were on OHAs, 12% on insulin, and 3% on diet alone, whereas in the 50–60 years age group, 87.8% were on OHAs alone and 12.2% on insulin.

Table 2 gives the prevalence of diabetes-related complications in the two groups. More patients aged ≥90 years had neuropathy (89.8% vs. 50.8%, P < 0.001), PVD (13.5% vs. 2.0%, P < 0.001), and CAD (60.3% vs. 32.0%, P < 0.001) than the 50–60 years age group. However, the prevalence of retinopathy (29.7% vs. 53.5%) and macroalbuminuria (3.7 vs. 16.0) was lower in the ≥90 years T2DM age group than in the 50–60 years age group.

Table 2.

Distribution of Diabetes Complications Among the Study Population

Complications	n	T2DM patients aged ≥90 years n (%) (n = 325)	n	T2DM patients aged 50–60 years n (%) (n = 278)	P
Retinopathy	172	51 (29.7)	256	137 (53.5)	<0.001
Proliferative diabetic retinopathy		8 (4.7)		19 (7.4)	0.248
Nonproliferative diabetic retinopathy		43 (25.0)		118 (46.1)	<0.001
Nephropathy	215	89 (41.3)	268	117 (43.6)	0.617
Microalbuminuria		81 (37.6)		74 (27.6)	0.019
Macroalbuminuria		8 (3.7)		43 (16.0)	<0.001
Neuropathy	217	195 (89.8)	248	126 (50.8)	<0.001
Peripheral vascular disease	207	28 (13.5)	254	5 (2.0)	<0.001
Coronary artery disease	179	108 (60.3)	241	77 (32.0)	<0.001

Discussion

The elderly population is growing both in developed and developing countries but at a faster rate in developing countries. Although increasing age is a risk factor for the development of T2DM and there are several reports on diabetes in elderly populations,^22,23 there are few describing the clinical profile of patients with T2DM aged ≥90 years, and none in Asian Indians, an ethnic group with lower life expectancy than Europeans.

Diabetes affects 10%–25% of elderly people (>65 years) worldwide, with particularly high rates in populations such as Pima Indians, Mexican Americans, and South Asians. Elderly persons with diabetes mellitus have considerable economic, social, and health burdens.²⁴

Diabetes can occur at increased frequency in older age groups due to decreased physical activity and other causes.²⁵ In one study,⁷ diabetes prevalence was 15.1% in elderly >65 years but only 7.6% in the very elderly, probably reflecting survivor bias. In this series of patients aged ≥90 years of age, the diagnosis was made before 70 years of age in 54%. Our T2DM patients with age ≥90 years had a significantly lower BMI than T2DM patients who were 50–60 years old. This could be due to poor eating habits, decreased appetite, and weight loss due to sarcopenia (muscle loss) or due to coexisting illness.^26
–28 Not unexpectedly, hypertension, peripheral neuropathy, PVD, and CAD were significantly higher in elderly patients as all these are age-related disorders.

An earlier study of the very elderly with diabetes showed that 24.4% were treated with OHAs, 2.2% with insulin, and the rest with diet.⁷ In our series, 85% of our T2DM patients ≥90 years were on OHAs and 12% were on insulin. Majority of the patients on OHAs were on modern sulfonylureas such as gliclazide and glimiperide. Use of sulfonylureas in the elderly age group is generally low because of fear of hypoglycemia. Hence it is reassuring that sulfonylureas such as gliclazide and glimiperide are tolerated by the elderly. Our findings are similar to a study from China that also showed that sulfonylurea was the most commonly used oral drug in elderly T2DM patients.²⁹ The main reasons for using insulin are comorbid conditions of patients which precluded the use of oral medications, or failure of oral medications in achieving glycemic control.

We found that both retinopathy and macroalbuminuria were less common among our patients aged ≥ 90 years than in the 50–60 years age group. This likely reflects the less severe hyperglycemia in the ≥90 years group or survival bias. Kidney disease in elderly patients may also reflect other causes of chronic kidney disease or age-related decline in renal function.³⁰ Not unexpectedly, neuropathy, PVD, and CAD were more common in the ≥90 years group than in the 50–60 years age group.

We had earlier reported on a comparison of long-term survivors and nonsurvivors with T2DM and showed that the survivors had better control of glycemia, blood pressure, and dyslipidemia.³¹ However, in that study, only duration of diabetes was used as the criterion and not the age of the patients, and hence very few patients with age >90 years were included in that report. This report differs from our earlier article in that it focuses on T2DM patients who lived beyond 90 years of age.

Motta et al.⁷ state that most of the very elderly patients have MARD that does not require treatment. They also state that long lasting diabetes is not compatible with extreme longevity. In this sense, the findings in this article are of significance, as our report includes patients with T2DM >90 years of age who had a mean duration of diabetes of 23 ± 14 years. This report therefore shows that survival of T2DM patients beyond 90 years of age is possible, even in Asian Indians whose current life expectancy is <70 years.

One of the strengths of our study is that it is the first report of Asian Indians with T2DM living >90 years of age. This was possible because of the large number of patients (>470,000) registered at our center and the availability of electronic medical records for nearly three decades at the center.³² We also report on a comparison with a group of T2DM patients who were on an average 35 years younger, but matched for gender and duration of diabetes.

One of the limitations of this study is that it is mostly a retrospective cross-sectional study done at a single diabetes center. Another limitation is the missing data for complications in those who could not be screened for the complications for various reasons, including frailty and loss to follow-up to the center. For the latter reason, the control of diabetes was also far from adequate. Finally, in keeping with the results of the recent CAROLINA study showing the safety and efficacy of sulfonylurea,³³ the majority of the elderly patients in this study were on modern sulfonylurea agents such as gliclazide and glimiperide. Future prospective studies on elderly T2DM patients could look at the best management options for this group of patients.

Footnotes

Acknowledgments

The authors thank the staff of Dr. Mohan's Diabetes Specialities Centre, Chennai, and the clinical epidemiology team of the Madras Diabetes Research Foundation for their help and all the participants who took part in the study. We thank Dr. Colin Palmer of the University of Dundee, Scotland, for providing us funds to conduct this study.

Author Disclosure Statement

No potential conflicts of interest relevant to this study was reported.

Authors' Contributions

V.M. conceived the study and involved in execution of the fieldwork, wrote parts of the article and revised all drafts of the article. C.S.S.R. was involved in the execution of the fieldwork and wrote parts of the article. R.M.A. provided scientific inputs and revised the drafts of the article. R.U., P.R., C.P., P.K.G., and R.P. gave valuable comments and suggestions for the writing of the article. S.J.R., G.U., K.G.V., R.A.K., and T.R. helped to collect data. U.V. did all the statistical analysis of the data. V.M., R.M.A., and. C.S.S.R. are the guarantors of this study and, as such, had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Funding Information

We received partial support from the University of Dundee, Scotland, through the NIHR grant. Project reference no: 16/136/102, NIHR Global Health Research Unit on Global Diabetes Outcomes Research.

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