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Cognitive Decline in Older Mexican Americans with Diabetes
Anna M Rotkiewicz-Piorun, MD; Soham Al Snih, MD, PhD; Mukaila A Raji, MD, MSc; Yong-Fang Kuo, PhD; and Kyriakos S Markides, PhD Texas City and Galveston, Texas
Financial support: This study was supported by grants AG10939, AG17638 and P60AG17231 from the National Institute on Aging United States, and in part by the UTMB Center for Population Health and Health Disparities 1P50CA105631 Dr Al Snih was supported by a fellowship from the National Institute on Disability and Rehabilitation Research H133P040003 Dr Rajis work is supported by the Bureau of Health Professions Geriatric Academic Career Award 1 K01 HP 00034-01 Preliminary results of the study were presented as a poster at the 2005 annual meeting of the American Geriatrics Society in Orlando, FL Objective: To examine social, demographic and health factors associated with cognitive decline over a seven-year period among older Mexican Americans with diabetes Methods: A population-based sample of 808 noninstitutionalized Mexican Americans aged 65 years with diabetes who had a Mini-Mental State Examination MMSE
17 at baseline from the Hispanic Established Population for the Epidemiological Study of the Elderly H-EPESE Measurements included sociodemographics, diabetic treatment received oral hypoglycemic or insulin, self-reported medical conditions, self-reported diabetes-related complications, high depressive symptoms and ADL limitations Results: The mean MMSE score at baseline was 253 SD37 The rate of decline in cognitive function MMSE during the follow-up period was 037 point per year Using general linear mixed models, we found that being male, and having high depressive symptoms and diabetic complications kidney impairment, circulation problems or limb amputation were factors significantly associated with greater declines in MMSE score over time Conclusion: Circulation problems, kidney impairment and depression are the major factors associated with cognitive decline in older Mexican Americans with diabetes Key words: diabetes cognitive decline elderly health Mexican Americans
2006 From a Private Practice, Texas City, TX Rotkiewicz-Piorun; Rehabilitation Sciences Division, School of Allied Health Sciences Al Snih, assistant professor, Memory Loss Clinics Raji, associate professor
and director, UTMB Geriatric Fellowship Training Program Raji, associate director, Sealy Center on Aging Al Snih, fellow, Department of Internal Medicine/Geriatrics Division Kuo, assistant professor and Preventive Medicine and Community Health Markides, professor, The University of Texas Medical Branch, Galveston Kuo, senior biostatistician Send correspondence and reprint requests for J Natl Med Assoc 2006;98:18401847 to: Dr Soham Al Snih, Sealy Center on Aging, The University of Texas Medical Branch Galveston, TX 77555-0460; phone: 409 747-3580; fax: 409 772-8931; e-mail: soalsnih@utmbedu
INTRODUCTION
iabetes was diagnosed in 78 million people in United States in 1993 and by the year 2003 the number increased to 138 million1 The overall prevalence of diabetes in 2003 was 173 among persons aged 65 years old and 151 among persons aged 75 years old1 However, the prevalence varies by ethnicity and gender Among subjects 75 years, 269 of Hispanic men and 214 of Hispanic women were diagnosed with diabetes Similarly, 208 of black men, 203 of black women, 17 of white men and 130 of white women were diagnosed with diabetes1 The number of Americans diagnosed with diabetes is projected to
increase 165, from 11 million in 2000 to 29 million in 2050, and the largest percent of increase will be among those aged 75 years2 The older Hispanic population is projected to grow faster than other groups from just over 2 million in 2003 to 76 million by the year 2030, and 15 million in 205024 The burden of diabetes is greatest in this population4 The burden arises in part from diabetes complications, such as peripheral vascular disease, kidney impairment, depression, heart attack, stroke, vision impairment, neuropathy and cognitive impairment5 Cognitive impairments–mild or severe–and diabetes are associated with increased risk of disability and nursing home placement6-7 Several studies have found accelerated cognitive decline and increased incidence of dementia among subjects with diabetes in comparison to subjects without diabetes8-10 Leibson and colleagues9 found that the risk of cognitive impairment among subjects with diabetes differs by gender Men with diabetes
D
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were twice as likely to develop Alzheimers disease as men without diabetes
Women also experienced elevated risk, but it was not statistically significant Elias and colleagues10 found that hypertensive subjects with diabetes
are at greatest risk for poor performance on tests measuring visual organization and memory and that subjects treated with diabetes insulin have poorer cognitive performance than those on oral hypoglycemics or diet
Table 1 Baseline characteristics and mean standard deviation of MMSE score for older Mexican Americans with diabetes Explanatory Variables Overall Age, Mean SD 75 75 Gender Female Male Education Years 8 8 Marital Status Married Unmarried Medical Conditions Hypertension Yes No Stroke Yes No Heart Attack Yes No Depression CES-D 16 16 Obesity BMI 30 Kg/m2 30 Kg/m2 ADL Limitations 1 None Diabetic Complications Eye Problem Yes No Kidney Problem Yes No Circulation Problem or Amputation Yes No Treatment Disease Insulin Use Yes No Disease Duration 10 years 10 years N 808 100 725 58 558 691 250 309 485 600 323 400 618 769 186 231 472 584 336 416 MMSE Score, Mean SD 249 38 254 36 238 38 246 38 253 36 242 37 271 32 254 36 241 38
580 718 228 282 65 80 743 920 112 139 694 861 196 244 608 756 299 392 464 608 117 145 691
855
247 37 254 38 243 41 249 37 250 39 249 37 243 36 251 38 250 37 249 37 237 39 251 37
251 318 539 682 86 108 707 892 292 369 500 631
248 35 249 38 243 36 250 38 245 37 251 38
194 242 609 758 259 336 511 664
252 37 248 38 253 36 247 38
p value 0001; SD: standard deviation; MMSE: Mini Mental State Examination; CES-D: Center for Epidemiologic Studies Depression Scale; ADL: activities of daily living; BMI: body mass index
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It is not clear why diabetes confers an increased risk of cognitive impairments, but several medical conditions that coexist with type-2 diabetes in older people have been implicated as risk factors for dementia These include stroke, hypertension and depression11,12 For example, Wu and colleagues,6 in a cohort of Latinos aged 60, found that greater cognitive decline is associated with presence of diabetic complications such as retinopathy, nephropathy, amputations and stroke Boston and colleagues13 found that significantly more subjects with vascular dementia had diabetes compared to subjects with
Alzheimers disease and nondemented subjects MacKnight and colleagues14 also found an association between diabetes and vascular cognitive impairment but not with Alzheimers disease Few longitudinal studies, however, have examined risk factors for cognitive decline over time in patients with diabetes at the population level6,8-10,15 It is also not
clear whether the risk of cognitive impairment is associated with type-2 diabetes or whether it is due to other conditions affecting cognitive function or treatment of diabetes Possible reasons for inconsistent findings include tests that assess some but not all aspects of cognition, differences in the test sensitivity assessments of cognitive function, and differences in inclusion criteria and study design time of observation, populations observed, statistical methods used Very little is known about risk of cognitive decline in very old people, especially in the population with a very high prevalence of diabetes: the older Mexican Americans The purpose of this study is to examine predictors of cognitive decline over a seven-year period among older Mexican Americans with diabetes This study is important in this population for several
reasons Mexican Americans with diabetes have greater fasting glycemia than non-Hispanic whites, higher prevalence of cogni-
Table 2 General linear mixed models estimates for cognitive decline among older Mexican Americans with diabetes N808 Explanatory Variables Intercept Time Years Age at Baseline Years Gender Male Education Years Marital Status Married Hypertension Stroke Heart Attack Depression CES-D score Obesity BMI 30 Kg/m2 ADL Limitations Diabetic Complications Eye problem Kidney problem Circulation problem or amputation Diabetic Treatment Insulin Use Disease Duration 10 Years Gender Male Time Education Years Time Marital Status Married Time Hypertension Time Stroke Time Heart Attack Time Depression CES-D score Time Obesity BMI 30 Kg/m2 Time ADL Limitations Time Diabetic Complications Eye problem time Kidney problem time Circulation problem or amputation time Diabetic Treatment Insulin Use Time Disease Duration 10 Years Time
p value 0001; p value 001; p value 005
Model 1 Estimate SE 2463 017 -038 004 -009 002 010 025 036 003 063 024 -080 025 -111 036 041 031 -003 001 011 021 -029 007
Model 2 Estimate SE 2459 017 -032 006 -009 002 010 027 035 003 056 026
-072 026 -096 042 021 035 -001 001 003 023 -025 010
-003 023 -060 032 -036 023 -017 025 104 026
-026 027 -016 038 -011 025 007 028 105 027 -015 009 0003 001 003 009 -009 011 -006 012 015 010 -001 0004 007 008 -0002 003
014 008 -020 010 -024 009 -015 009 -006 008
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tive impairment, severe peripheral macrovascular disease such as limb amputations and microvascular diseases such as retinopathy and nephropathy as well as higher rates of microalbuminuria and proteinuria16 Specifically, we examine whether the underlying pathogenesis of cognitive decline in subjects with diabetes should be attributed mostly to micro- and macrovascular diseases and whether the magnitude of difference in cognitive score between subjects with and without risk factors for dementia become clinically meaningful Understanding factors associated with impaired cognition among older patients with diabetes is key toward the developing and testing of interventions to reduce or stop cognitive disability in this population
jects in the fourth wave Subjects excluded N71 from the
analysis were significantly more likely to be older; to have lower levels of education; to be unmarried; to have ever had a stroke, heart attack, high depressive symptoms, eye and kidney problems; or to be disabled At the end of the follow-up 20002001, 462 572 subjects were reinterviewed, 29 36 subjects refused to be reinterviewed, 59 73 subjects were lost to follow-up, and 259 319 subjects were confirmed dead through the National Death Index NDI and reports from relatives
MEASURES Diabetes Mellitus
We assessed diabetes by asking if subjects had ever been told by a doctor that they had diabetes Respondents who reported a diabetes diagnosis were asked about disease duration 10 years vs 10 years and treatment received categorized as: none, oral hypoglycemic, insulin or oral hypoglycemic/insulin combination Respondents were asked if they had problems with their kidneys, eyes or circulation or if they have any amputations due to their diabetes
METHODS Sample and Procedures
Data used were from the Hispanic Established Population for the Epidemiological Study of the Elderly HEPESE, a longitudinal study of Mexican Americans aged 65, residing in Texas, New Mexico, Colorado, Arizona and
California The sample and its characteristics have been described elsewhere17,18 The present study used baseline data 19931994 and data obtained from a twoyear follow-up 19951996, a five-year follow-up 19981999 and a seven-year follow-up assessment 20002001 Of the 3,050 subjects interviewed at baseline, 879 subjects had a self-reported diagnosis of diabetes over the four waves Excluding subjects with MMSE 17 at baseline yielded a final sample of 808 subjects: 600 subjects in the first wave, 100 subjects in the second wave, 65 subjects in the third wave and 43 sub-
Cognitive Function
Cognitive function was assessed with the Mini Mental State Examination MMSE instrument19-20 Interviewers were thoroughly trained in administration and scoring of the MMSE, both through workshops and videotaped instruction The English and Spanish versions of the MMSE were adopted from the Diagnostic Interview Scale DIS used in prior community survey studies20 This Spanish version of the MMSE has met standard cri-
Figure 1 Predicted MMSE score over seven-year period for older Mexican Americans with diabetes with and without circulation problems N808 26 25 Estimated MMSE Score 24 23 22 21 20 0 1 2 3 4
Follow-Up Time Year 5 6 7
Without circulation problems With circulation problems
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teria for development of translated tests, including formal translation, back-translation and consensus by committee for final item content21 Additionally, the Spanish MMSE has been successfully used in community surveys of Mexican Americans22 Scores have a potential range of 030, with lower scores indicating poorer cognitive ability Because of the low educational attainment and advanced age of our subjects average education49 years; average age725, we identified individuals as having cognitive impairment if their MMSE score was 18 at baseline23 This study included only subjects with a MMSE cutoff score of 18, similar to past studies of populations with lower educational attainment and in certain ethnic minorities with low English literacy23
Statistical Analysis
General linear mixed model using the MIXED procedure in SAS was used to examine the factors associated with decline in cognitive function over a seven-year period among older Mexican Americans with diabetes
All variables were analyzed as time-dependent covariates potential to change as time progresses except age, education and gender The mixed model was chosen for analysis because it best handles unbalanced data, allowing for modeling of time-dependent change in variables as well as time-dependent change in magnitude of association between variables Also, because H-EPESE data comprised repeated measures over seven years, mixed models allow for more flexibility in modeling the effects of time on outcome28-29 Two mixed models were constructed to test the relationship between the predictor variables and cognitive decline over the seven-year period Model 1 included age, gender, marital status, years of formal education and time Model 2 included interaction terms each predictor variable x time, medical conditions, ADL limitations, high depressive symptoms, BMI, diabetic complications and disease duration along with the variables in Model 1 Interaction terms assess the association between each predictor variable and slope of cognitive function over time The time interactions represent the estimated effect of each predictor variable on rate of change in cognitive function All analyses were
performed using the SAS System for Windows, Version 91 SAS Institute, Cary, NC
Covariates
Baseline sociodemographic variables included age, gender, marital status and years of formal education We assessed 
the presence of medical conditions by asking if respondents had ever been told by a doctor that they had hypertension, heart attack or stroke Body mass index BMI was computed by dividing measured weight in kilograms by height in meters squared Kg/m2 Participants with BMIs of 30 were considered obese24 Functional disability was assessed by seven items from a modified version of the Katz Activities of Daily Living ADL scale25 ADLs include walking across a small room, bathing, grooming, dressing, eating, transferring from a bed to a chair, and using the toilet Any ADL limitation was dichotomized as: no help needed/needing help with or unable to perform 1 ADL activities Depressive symptomatology was measured with the Center for Epidemiologic Studies Depression Scale CES-D26 A score of 16 indicates high depressive symptomatology27
RESULTS
Table 1 shows baseline characteristics and mean standard deviation SD of MMSE score for older Mexican Americans with diabetes The average MMSE
score
Figure 2 Predicted MMSE score over seven-year period for subjects with and without kidney problems N808 26 25 Estimated MMSE Score 24 23 22 21 20 0 1 2 3 4 Follow-Up Time Year 5 6 7 Without kidney problems With kidney problems
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for subjects in the study was 249 with SD of 38 point The mean age of the sample was 726 years, 485 60 of the respondents were women and 472 584 were married Mean level of education was 49 years The most common medical conditions were hypertension 718 and stroke 80, 244 had high depressive symptoms CES-D 16, 145 reported any ADL limitations and 392 had a BMI 30 Kg/m2 Circulation problems or amputations were reported in 369 subjects, eye problems in 318 subjects and kidney problems in 108 subjects Insulin alone or in combination with hypoglycemic agents was used by 242 of subjects, 565 704 used oral hypoglycemics only and 44 59 were diet controlled only Diabetes duration 10 years was reported in 336 of the subjects There were no statistical differences in MMSE score at baseline for each predictor variable except for
years of education 8 years 242 37 vs 8 years 271 32; p value 0001 Table 2 presents the general linear model estimates for change in MMSE score as a function of covariates sociodemographic factors, medical conditions, diabetic complications, disease duration and treatment received In Model 1, the rate of decline in cognitive function was 038 per year Subjects with high level of education [estimate 036, standard error SE 003], married estimate 063, SE 024, and those with a disease duration 10 years estimate 104, SE 026 were significantly associated with higher MMSE score at each point time of follow-up intercept of MMSE score Older age estimate -009, SE 002, hypertension estimate -080, SE 025, stroke estimate -111, SE 036, high depressive symptoms estimate -003, SE 001 and increasing ADL limitations estimate -029, SE 007 were significantly associated with lower MMSE score at each follow-up intercept of MMSE score In Model 2, interaction terms were added There was a significant interaction term between covariates and time slope of MMSE score over time in subjects with high depressive symptoms estimate -001, SE 0004, kidney problem estimate -020, SE 010, and
circulation problem estimate -024, SE 006, indicating that subjects with depression and diabetic complications kidney and circulation problems had greater decline in MMSE score over time when compared with those without these complications To better illustrate and understand the decline in MMSE scores associated with diabetic complications, slopes of change in MMSE scores were created for every evaluated factor significantly associated with change in cognition over time in comparison to the reference slope Figures 1 and 2 show the estimated MMSE score over a seven-year period for subjects with circulation problems or amputation and kidney problems for those subjects with diabetes over the four waves Steepness of slope indicates the rate of cognitive
decline No significant differences in baseline MMSE scores are observed
DISCUSSION
This study examined social, demographic and health factors associated with cognitive decline over seven years among older Mexican Americans with diabetes Over the seven-year period of observation, having diabetic complications circulation and kidney problems and depression were the major factors associated with cognitive decline in older Mexican
Americans with diabetes Despite adjustment for prevalent comorbidities, these associations remained statistically significant Our study is comparable with previous studies conducted using the MMSE among older subjects with diabetes, but it also extends the results of previous longitudinal studies Past research suggests that diabetes coexisting with hypertension or stroke accelerates cognitive decline Haan and colleagues,11 in a cross-sectional study of community-dwelling elderly people 60 years, found that Hispanic and non-Hispanic whites alike have poorer cognitive performance in MMSE score when diabetes coexists with a history of stroke Using data from the Framingham Heart Study, Elias and colleagues10 found that those with both diabetes and hypertension had poorer performance on tests of visual organization and memory, while normotensives with diabetes did not They also found that patients on insulin performed worse in some neuropsychological tests involving verbal and visual memory No previous longitudinal studies, to our knowledge, have looked specifically at the relationship between peripheral vascular disease or kidney impairment and cognitive function in subjects with
diabetes Indeed, few studies in the general population have explored the association of peripheral vascular disease with cognitive impairment30 Little is known about kidney impairment and cognitive performance,31 and no study to our knowledge has examined the latter in older diabetics with nephropathy Our research shines a new light on the impact of diabetic complications peripheral vascular disease and nephropathy, but not retinopathy on the decline in cognitive function It is well known that peripheral vascular disease is a risk factor for minor ischemic stokes and transit ischemic attacks TIA Peripheral vascular disease also adversely affects stroke outcomes Peripheral vascular disease is a marker of generalized atherosclerosis Moreover, this disease is often asymptomatic and underdiagnosed, as is kidney dysfunction As our study indicates, by the time diagnosis is made, patients may already have significant loss of cognitive function Therefore, effort should be concentrated on early detection of peripheral vascular disease and nephropathy by screening patients with diabetes with ankle-brachial index for signs of peripheral vascular disease and on
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urine analysis for microproteinuria; both tests are relatively inexpensive Next, aggressive management with antiplatelet medication aspirin, clopidogrel, statins, and optimal control of blood pressure and proteinuria by use of ACE inhibitors may slow progression of cognitive decline in older subjects with diabetes This study has some limitations First, the assessment of diabetes mellitus and its complications was by self-report Clinical observation may provide a different and more precise diagnosis However, the self-report approach has been documented to provide reliable information and a good agreement between self-reported diabetes and diabetes diagnosed by blood tests32 Second, by including in the sample subjects who were reinterviewed, we are examining the cohort of survivors over a seven-year period Subjects who were not interviewed at the last follow-up were significantly more likely to be male; to report high depressive symptoms, ADL disability, longer diabetes duration; to be in treatment with insulin; to have a BMI 30 Kg/m2; and to have more eye, kidney and circulation
problems when compared with those who were reinterviewed at the seven-year follow up Third, cognitive function is established by MMSE scores, which may not reflect all cognitive functions, especially executive function However, using conventional cut-off scores with adjustment for confounders, the MMSE has consistently yielded correct classification rates of 8090 when compared with physician assessment of cognitive impairment and dementia22 Our study has several strengths, including its large community-based sample, its prospective design and its exploration of potential factors affecting cognitive function in older Mexican Americans–a rapidly growing segment of the older population Another important strength is the use of mixed models, an analytic approach that allows use of all available data and evaluation of time-dependent effects By excluding severely impaired individuals, we were able to see a less rapid decline in MMSE for the group and to better estimate risk factors for decreased cognitive function This is the first study to demonstrate that in older Mexican Americans living with diabetes, circulation and kidney problems are major risk factors for cognitive decline over
time Our study also underscores the difference between factors influencing baseline cognition versus those factors influencing rate of cognitive decline, a difference that future intervention studies should consider In conclusion, increasing awareness of the associations among diabetes-related complications of circulation problems, kidney problems, and depression and cognitive decline can help clinicians screen for and manage these complications with the goal of preserving cognitive function and independent living in elderly patients with diabetes
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functional status among community elders Am J Public Health 1984;74:266-268 26 Radloff LS The CED-S Scale: a self-report depression scale for research in the general population J Appl Psychol Meas 1977;1:385-401 27 Boyd JH, Weissman M, Thompson W, et al Screening for depression in a community sample Arch Ger Psychiatry 1982;39:1195-1200 28 Liang KY, Zeger SL Longitudinal data analysis using generalized linear models Biometrika 1986;73:13-22 29 Zeger SL, Liang KY Longitudinal data analysis for discrete and continuous outcomes Biometrics 1968;42:121-30 30 Phillips NA, Mate-Kole CC Cognitive deficits in Peripheral Vascular Disease A Comparison of Mild Stroke Patients and Normal Control Subjects Stroke 1977;28:777-784 31 Viljoen M, Koorts AM A role for proinflammatory cytokines in the behavioral disturbances and cognitive decline in chronic renal failure patients Clinical Nephrology 2004;61:227-229 32 Midthjell K, Holmen J, Bjorndal A, et al Is questionnaire information valid in the study of chronic disease such as diabetes? The Nord-Trondelg diabetes study J Epidemiol Community Health 1992;46:537-542
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