(Stroke. 1997;28:1710-1716.)
© 1997 American Heart Association, Inc.
Articles |
Microalbuminuria and Carotid Artery Intima-Media Thickness in Nondiabetic and NIDDM Subjects
The Insulin Resistance Atherosclerosis Study (IRAS)
From the Department of Medicine, Division of Clinical Epidemiology, University of Texas Health Science Center at San Antonio (L.M., S.M.H.); Department of Public Health Sciences, Bowman Gray School of Medicine, Winston-Salem, NC (D.J.Z., G.H.); Department of Radiology, New England Medical Center, Boston, Mass (D.H. O'L.); and Medlantic Research Institute, Penn Medical Laboratory, Washington, DC (D.C.R.).
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Abstract |
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Background and Purpose Microalbuminuria is associated with cardiovascular mortality in subjects with non–insulin-dependent diabetes mellitus (NIDDM). However, little is known about this association in nondiabetic subjects. Specifically, it is not known whether microalbuminuria is related to an early stage of atherosclerosis manifested as increased intima-media thickness (IMT) of carotid arteries. We investigated the relationship between microalbuminuria and carotid artery IMT in 991 nondiabetic and 450 NIDDM subjects aged 40 to 69 years.
Methods Microalbuminuria was defined as
albumin-to-creatinine ratio 
2 mg/mmol in a
morning spot urine sample. B-mode ultrasound was used to assess the IMT
of the common and internal carotid arteries.
Results Altogether 13.9% of nondiabetic and 27.6% of NIDDM subjects had microalbuminuria, and 31.1% of nondiabetic and 50.8% of NIDDM subjects had hypertension. Subjects with microalbuminuria had greater common carotid artery (CCA) IMT than those without microalbuminuria (nondiabetic: 0.84±0.02 versus 0.80±0.01 mm, P=.010; NIDDM: 0.89±0.02 versus 0.86±0.01 mm, P=.152; combined: 0.86±0.01 versus 0.82±0.01, P=.005). The association of microalbuminuria and CCA IMT was independent of age, sex, ethnicity, smoking, and lipoprotein levels. Although further adjustment for hypertension in the multivariate linear regression analysis attenuated the difference in CCA IMT between subjects with and without microalbuminuria, this difference continued to be significant (combined: 0.86±0.01 versus 0.83±0.01, P=.015). In contrast to CCA IMT, microalbuminuria was not related to ICA IMT.
Conclusions Microalbuminuria was associated with increased CCA IMT. This relationship was only partly mediated by hypertension. Thus, microalbuminuria is related to atherosclerosis at an early stage of the disease process.
Key Words: atherosclerosis • carotid arteries • risk factors • microalbuminuria • ultrasonics
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Introduction |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Microalbuminuria is associated with cardiovascular mortality in patients with NIDDM1 2 3 4 and in the elderly.5 6 Little is known about the relationship between microalbuminuria and atherosclerotic vascular disease in nondiabetic subjects. Nevertheless, in one study microalbuminuria has been shown to be related to excess prevalence of coronary heart disease and peripheral vascular disease in nondiabetic subjects.7 Cardiovascular events and mortality, however, represent a late stage in the atherosclerotic process. Long before cardiovascular events occur, atherosclerosis has manifested as asymptomatic intimal thickening of the arterial wall. Atherosclerosis is a process simultaneously involving multiple arterial beds, and recent studies using ultrasound have shown that carotid atherosclerosis, expressed as increased IMT of carotid arteries, correlates with coronary disease.8 9 10 It has previously been hypothesized that microalbuminuria is a marker of generalized vascular disease and increased vascular permeability that might predispose to greater penetration of atherogenic lipoprotein particles into arterial wall.11 If microalbuminuria is a sign of generalized vascular disease, microalbuminuria could be related to carotid artery IMT.
Some preliminary data in NIDDM patients suggest that urinary albumin excretion may indeed be associated with carotid artery IMT.12 13 In one study, NIDDM patients with an increased albumin excretion rate had increased IMT of the CCA independent of blood pressure level.12 In another study in NIDDM patients with treated hypertension, urinary albumin excretion rate was also related to IMT of the CCA.13 However, these previous studies included NIDDM patients with both microalbuminuria and macroalbuminuria. Therefore, it is unclear whether the relationship between albumin excretion rate and carotid IMT in NIDDM patients was mainly explained by macroalbuminuria and overt diabetic nephropathy. It is not known whether microalbuminuria is associated with carotid IMT in nondiabetic subjects.
The aim of this study was to investigate the relationship between microalbuminuria and carotid IMT in nondiabetic and NIDDM subjects participating in the IRAS. If microalbuminuria was related to increased IMT of carotid arteries in the general population, albumin excretion rate could be used to identify individuals with a high risk of coronary artery disease who would be likely to benefit from aggressive risk factor intervention.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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The IRAS is a multicenter epidemiological study aiming to explore relationships among insulin resistance, cardiovascular risk factors, and disease in blacks, Hispanics, and non-Hispanic whites across a broad range of glucose tolerance. A full description of the design and methods of the IRAS has been published.14 In brief, this study was conducted at four clinical centers. Clinical centers in Oakland and Los Angeles, Calif, studied non-Hispanic whites and blacks recruited from Kaiser Permanente, a nonprofit health maintenance organization. Clinical centers in San Antonio, Tex, and San Luis Valley, Colo, studied non-Hispanic whites and Hispanics recruited from two ongoing population-based studies (the San Antonio Heart Study15 and the San Luis Valley Diabetes Study16 ). Recruitment was tailored to yield approximately equal numbers of participants by ethnicity, sex, and glucose tolerance categories (NIDDM, IGT, and normal glucose tolerance). To recruit an adequate number of subjects with IGT, sampling strategies were focused on methods that would maximize the number of IGT participants. San Antonio and San Luis Valley centers drew random samples from participant lists from their respective ongoing population studies, which resulted in selection of a disproportionate number of participants with previously documented IGT. Oakland and Los Angeles centers enriched their samples of persons with IGT by oversampling from lists of nondiabetic persons with elevated levels of fasting plasma glucose (ie, 6.1 to 7.2 mmol/L). A total of 3416 potential participants were contacted to obtain the final sample of 1625, for an overall recruitment rate of 48%. However, despite the oversampling of IGT subjects, nondiabetic subjects in the IRAS have fasting glucose levels similar to those of the corresponding ethnic group in the population-based NHANES and HHANES surveys.14 Diabetic subjects who had taken insulin or who had fasting plasma glucose levels
300 mg/dL (16.7
mmol/L) were not eligible for this study. The final study sample included 613 non-Hispanic whites, 548 Hispanics, and 464 blacks.14 Individuals with normal glucose tolerance constituted the largest segment of the study sample (44%), followed by diabetic subjects (33%) and people with IGT (23%). Altogether 991 nondiabetic subjects and 450 subjects with NIDDM had data on carotid IMT and urinary albumin excretion rate, and they constitute the study population for this report.
The IRAS examination required two visits (
1 week apart [range, 2 to
28 days]), each lasting 4 hours. Height, weight, and girths (waist
at the umbilicus and hips) were measured following a standardized
protocol. Body mass index (weight [in kilograms] divided by height
[in meters] squared) was used as an estimate of overall adiposity.
The WHR was used as an estimate of body fat distribution. Blood
pressure was measured with the subject in the sitting position with a
mercury sphygmomanometer after a 5-minute rest. Three readings were
taken, and the average of the second and third measurements was used in
statistical analyses. A subject was defined as having
hypertension if his/her systolic blood pressure was >140
mm Hg, diastolic blood pressure was >90 mm Hg, or
he/she was currently taking medicine for hypertension.
B-mode real-time ultrasound was used to assess the IMT of the carotid artery by use of a protocol identical to that used in the Cardiovascular Health Study.17 Briefly, a bilateral assessment of the IMT was made in the CCA and ICA. For the CCA, bilateral images were obtained 1 cm proximal to the dilatation of the carotid bulb at a single (lateral) angle. For the ICA, the sonographer sought the site of maximal IMT in the region between the dilatation of the carotid bulb and the ICA 1 cm distal to the tip of the flow divider. For the ICA, three images were obtained (bilaterally) at the site of maximal thickness at different interrogation angles (posterior, lateral, and anterior).
Ultrasound images were recorded on super VHS tape and transferred to a central reading facility (D.H.O'L., principal investigator) for measurement of the IMT. Ultrasound data were read in a manner blinded to clinical information. For each of the eight available images, the maximal IMT was taken over a 1-cm segment of the arterial wall distant from the skin surface ("far wall"). Two summary measures were calculated: (1) the mean of the two CCA sites and (2) the mean of the six ICA sites. To allow equal weighing of the right and left arteries in the presence of missing data, the mean value of the available measures on the right ICA and the mean value of the available measures of the left ICA were calculated, and then the mean of these two means was used in the analysis. This approach is similar to that used to provide an index of atherosclerosis in other epidemiological studies17 18 and clinical trials.19 20
Participants were asked before each visit to fast for 12 hours, to abstain from heavy exercise and alcohol for 24 hours, and to refrain from smoking the morning of the examination. For the oral glucose tolerance test, a 75-g glucose load (Orangedex, Customs Laboratories) was administered over a period of <10 minutes. Blood was collected before ingestion and 2 hours after the glucose load. Glucose tolerance status was based on the World Health Organization criteria.21
Insulin sensitivity was assessed by an FSIGT22 with minimal model analyses.23 Two modifications of the original protocol were used. An injection of regular insulin, rather than tolbu- tamide, was used to ensure adequate plasma insulin levels for the accurate computation of insulin sensitivity across a broad range of glucose tolerance.24 This was because of the blunted or absent insulin response in diabetic subjects. In addition, the reduced sampling protocol (which required 12 rather than 30 plasma samples and shows results similar to the full protocol25 ) was used because of the large number of subjects. Glucose in the form of a 50% solution (0.3 g/kg) and regular human insulin (0.03 U/kg) were injected through an intravenous line at 0 and 20 minutes, respectively. Blood was collected at -5, 2, 4, 8, 19, 22, 30, 40, 50, 70, 100, and 180 minutes for plasma glucose and insulin concentrations. Insulin sensitivity, expressed as the insulin sensitivity index (SI), was calculated by mathematical modeling methods (MINMOD, version 3.0 [1994]). This modified version of the FSIGT protocol used in the IRAS has recently been compared with the hyperinsulinemic euglycemic clamp and shown to be a valid measure of insulin resistance.26
The IRAS protocol was approved by local institutional review committees, and all subjects gave informed consent.
Plasma glucose was measured with the glucose oxidase technique on an automated autoanalyzer (Yellow Springs) at the central IRAS laboratory at the University of Southern California, Los Angeles. Plasma lipoprotein measurements were obtained from fasting single fresh plasma samples with the use of Lipid Research Clinic methods. Plasma lipoproteins were measured at the central IRAS laboratory at Medlantic Research Institute, Washington, DC. LDL and HDL were isolated by preparative ultracentrifugation, and VLDL (top) and bottom fractions were measured for cholesterol and triglyceride concentrations. HDL cholesterol was measured in the presence of MnCl2 and heparin in which non-HDL lipoproteins were precipitated, leaving HDL in the supernatant. The supernatant was removed after centrifugation, and the cholesterol content was measured on a separate autoanalyzer channel set to measure low cholesterol values. LDL was calculated as the difference between the HDL cholesterol and the bottom cholesterol. Triglycerides were measured enzymatically after correction for free glycerol.
Urinary albumin concentration was assessed in a morning spot
urine sample. Urinary albumin was measured from samples stored
at -20°C by a commercial immunoprecipitation assay (Incstar SPQ test
system) with a sensitivity of 5.8 mg/dL and intra-assay and
interassay coefficients of variation of 1.46% and 1.77%,
respectively. Urinary creatinine was determined by a
modified Jaffe method.27 Urinary albumin and
creatinine for all samples were measured at the central
IRAS laboratory at the Medlantic Research Institute, Washington, DC. We
have external quality control data of urinary albumin and
creatinine measurements in the IRAS. From 170 blind
duplicate specimens, the external coefficient of variation for urinary
albumin measurements was 12% and for urinary
creatinine measurements was 17%; correlation between the
two blind duplicate measurements for urinary albumin was 0.82
and for urinary creatinine was 0.71. Because we used a
morning spot urine sample and its collection time may vary between
subjects, the ACR was used as a measure of albumin excretion.
Overnight ACR correlates well with albumin excretion
rate,28 29 and ACR measured in a single untimed urine
specimen has been shown to be an effective means for identifying
diabetic patients who are at risk of developing overt
nephropathy.30 An overnight ACR 2
mg/mmol predicts an albumin excretion rate >30
µg/min with a high sensitivity and
specificity.28
Statistical Methods
Means, SDs, and other basic descriptive statistics were
calculated to describe the study population (Table 1
). Subjects
exhibiting macroalbuminuria (ACR 20 mg/mmol) were
excluded from these analyses (11 nondiabetic and 25 NIDDM
subjects). For analyses shown in Tables 2 and 3, subjects were
divided into those with microalbuminuria (ACR 2
mg/mmol) and those without microalbuminuria (ACR <2
mg/mmol). For variables that were not normally distributed
(triglycerides, ACR), log transformation was used for
statistical testing. Student's t test or
2 test was used to test differences between
subjects with microalbuminuria and subjects without
microalbuminuria (Tables 2 and 3). Multiple linear
regression was employed to relate the presence of
microalbuminuria to carotid IMT with adjustment for
potential confounding variables (Table 4). Three linear regression
models were used to adjust for the following: (1) age, sex, ethnicity,
and clinic; (2) age, sex, ethnicity, clinic, LDL
cholesterol, HDL cholesterol, loge
triglyceride, and smoking; and (3) age, sex, ethnicity,
clinic, LDL cholesterol, HDL cholesterol,
loge triglyceride, smoking, and
hypertension.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Characteristics of the study population are shown in Table 1
. The mean age of nondiabetic subjects
was 54.8 years, and that of NIDDM subjects was 57.3 years. Equal
proportions of the study subjects were black, Hispanic, and
non-Hispanic white. The prevalence of hypertension was 31.1% in
nondiabetic and 50.8% in NIDDM subjects. Altogether 13.9% of
nondiabetic and 27.6% of NIDDM subjects were found to have
microalbuminuria (2 mg/mmol< ACR <20
mg/mmol). The CCA IMT (0.87±0.24 versus 0.79±0.20 mm,
P<.001) and ICA IMT (0.94±0.42 versus 0.84±0.35 mm,
P<.001) were significantly greater in NIDDM subjects than
in nondiabetic subjects.
Table 2 shows characteristics of
nondiabetic subjects according to the presence or absence of
microalbuminuria. Nondiabetic subjects with
microalbuminuria were more obese (higher body mass index)
than those without microalbuminuria. Furthermore, subjects
with microalbuminuria had higher systolic and
diastolic blood pressure and a higher prevalence of
hypertension than subjects without microalbuminuria.
Subjects with microalbuminuria did not differ from those
without microalbuminuria in regard to body fat distribution
(WHR), smoking, prevalence of IGT, or concentrations of total
cholesterol, LDL cholesterol, HDL
cholesterol, and triglycerides. Nondiabetic
subjects with microalbuminuria had significantly greater
CCA IMT than nondiabetic subjects without microalbuminuria.
However, ICA IMT was not different in nondiabetic subjects with
microalbuminuria compared with those without
microalbuminuria.
Table 3 shows characteristics of NIDDM
subjects according to the presence or absence of
microalbuminuria. NIDDM subjects with
microalbuminuria were more obese than those without
microalbuminuria. In addition, subjects with
microalbuminuria had a longer duration of diabetes and
higher fasting and 2-hour plasma glucose levels than those without
microalbuminuria. NIDDM subjects with
microalbuminuria had also higher prevalence of hypertension
and higher systolic blood pressure and total
cholesterol and triglyceride levels than those
without microalbuminuria. NIDDM subjects with
microalbuminuria did not differ from those without
microalbuminuria in regard to body fat distribution,
smoking, LDL cholesterol levels, or HDL
cholesterol levels. NIDDM subjects with
microalbuminuria had greater CCA IMT than those without
microalbuminuria (difference, 0.03 mm, which is
60% of the difference seen in nondiabetic subjects), but this
difference was not statistically significant. ICA IMT was not different
in NIDDM subjects with microalbuminuria compared with those
without microalbuminuria.
We further examined the relationship between
microalbuminuria and CCA IMT by linear regression
analyses. In nondiabetic subjects, microalbuminuria
was associated with CCA IMT independently of age, sex, ethnicity,
clinic, LDL cholesterol concentration, HDL
cholesterol concentration, triglyceride
concentration, and smoking (Table 4, model
2). After these adjustments, the mean IMT
of the CCA was 0.84 mm in subjects with
microalbuminuria and 0.80 mm in those without
microalbuminuria. After further adjustment for hypertension
this association became statistically nonsignificant, but subjects with
microalbuminuria still had 0.03 mm thicker CCA IMT
than those without microalbuminuria. In NIDDM subjects, the
association between microalbuminuria and IMT of the CCA did
not reach statistical significance (Table 4). However, the difference
between adjusted mean IMT of the CCA between NIDDM subjects with and
without microalbuminuria was of same magnitude as in
nondiabetic subjects (0.03 to 0.04 mm). If nondiabetic and NIDDM
subjects were pooled, microalbuminuria was associated with
CCA IMT independently of age, sex, ethnicity, clinic, LDL
cholesterol concentration, HDL cholesterol
concentration, triglyceride concentration, and smoking
(Table 4, model 2). Even after further adjustment for hypertension, the
difference in IMT of the CCA between subjects with and without
microalbuminuria remained significant (0.86±0.01 versus
0.83±0.01 mm, P=.015) in the pooled model. We also
performed a multiple linear regression analysis similar to
model 3 but substituted hypertension by systolic blood
pressure, and the results were essentially similar (data not shown). An
interaction term of diabetes status by microalbuminuria was
entered into the multiple linear regression model 3 in the pooled
population; this interaction term was not statistically significant
(P=.899), suggesting that the association of
microalbuminuria with increased IMT of the CCA was not
different in nondiabetic and NIDDM subjects.
We have previously reported that insulin sensitivity was related
to the carotid IMT in the IRAS cohort.31 Furthermore,
microalbuminuria was associated with decreased insulin
sensitivity in the IRAS cohort (L. Mykkänen, D.J. Zaccaro, L.E.
Wagenknecht, D.C. Robbins, M. Gabriel, and S.M. Haffner, unpublished
data, 1997). Therefore, we performed an additional multiple linear
regression analysis, adjusting for insulin sensitivity index
(SI) and all the variables included in model 3 shown in
Table 4. After further adjustment for SI, the difference in
IMT of the CCA between subjects with and without
microalbuminuria remained unchanged in the model combining
nondiabetic and NIDDM subjects (0.86±0.01 versus 0.83±0.01 mm,
P=.015).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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This study showed that microalbuminuria is associated with increased carotid artery IMT in nondiabetic and NIDDM subjects. This relation was only partly mediated by hypertension. Thus, microalbuminuria is related to atherosclerosis at an early stage of the disease process and not only to symptomatic coronary heart disease and peripheral vascular disease, as shown previously.7
The increase in CCA IMT related to microalbuminuria
(0.05 mm in nondiabetic and 0.03 mm in NIDDM subjects) was of
the same magnitude as the difference in carotid artery IMT between
nondiabetic and NIDDM subjects in the present study (Table 4, model
1) and in several previous studies.32 33 Previously, a
difference of 0.06 to 0.07 mm in the carotid IMT has been reported
between subjects with and without prevalent heart
disease34 or smoking.35
Microalbuminuria was associated with increased IMT of the CCA but not of the ICA. The fact that this finding was similar in nondiabetic and in NIDDM subjects suggests that the difference between the CCA and the ICA was not due to chance alone. The carotid bifurcation at sites with low mean shear stress and oscillation in shear stress direction is a prime area for atherosclerotic lesions.36 37 Therefore, in the IRAS cohort increased IMT related to the development of atherosclerosis was more likely to be detected in the ICA images, including the bifurcation region, than in the CCA images. This likelihood was further strengthened by the IRAS scanning protocol, which focused on the point of maximal IMT in the ICA images, whereas the CCA images were taken at a fixed point below the dilatation of the carotid bulb. Furthermore, a larger number of images were averaged for the ICA IMT compared with the CCA IMT in the IRAS protocol, which should yield higher accuracy. Therefore, we think that risk factors for increased IMT may be different in the CCA and in the ICA. We have previously reported that insulin sensitivity was more strongly related to ICA IMT than to CCA IMT in the IRAS cohort.31 This is in agreement with an earlier study suggesting different risk factor patterns for early atherosclerosis in the CCA, carotid bulb, and common femoral artery.38
What could explain the association between microalbuminuria and increased IMT? There are several possibilities, and some of these may operate simultaneously. First, microalbuminuria may be a marker of generalized vascular disease, as suggested earlier.11 If this is the case, the development of atherosclerosis indexed by increased IMT would temporally precede microalbuminuria. Second, microalbuminuria per se could be a risk factor for atherosclerosis. Third, the relation between microalbuminuria and increased IMT might be explained by adverse changes in cardiovascular risk factors in subjects with microalbuminuria. Fourth, microalbuminuria and increased IMT both could be related to a third factor, such as insulin resistance.
Indeed, insulin sensitivity was related to the carotid IMT in the IRAS cohort, as reported earlier,31 and microalbuminuria was associated with decreased insulin sensitivity in the IRAS (L. Mykkänen, D.J. Zaccaro, L.E. Wagenknecht, D.C. Robbins, M. Gabriel, and S.M. Haffner, unpublished data, 1997). However, insulin resistance did not explain the relationship between microalbuminuria and CCA IMT. Findings of the present study support the third possibility. Lipid and lipoprotein levels were not different between nondiabetic subjects with and without microalbuminuria in the present study, but subjects with microalbuminuria had significantly higher systolic and diastolic blood pressure levels and higher prevalence of hypertension than those without microalbuminuria. Further adjustment for hypertension in the multiple linear regression analysis attenuated the difference in IMT of the CCA between subjects with and without microalbuminuria, but even after this adjustment the difference in CCA IMT between subjects with and without microalbuminuria was significant if nondiabetic and NIDDM subjects were pooled. Thus, the relationship between microalbuminuria and IMT was partly explained by elevated blood pressure. Subjects with hypertension have previously been shown to have increased IMT of the CCA39 40 41 and increased urinary albumin excretion rate.42 43 44 However, hypertension did not explain completely the difference in CCA IMT between subjects with and without microalbuminuria in the present study. Thus, it is possible that microalbuminuria is a marker of generalized vascular disease, as suggested earlier.11
A limitation of the IRAS is that the study sample was not randomly selected from the general population but instead was recruited from identified subgroups of ethnicity and glucose tolerance status to allow valid comparisons among and within these subgroups. Moreover, the response rate to the IRAS examination, while excellent, indicates that the final cohort does not strictly represent a general population sample. However, the IRAS population was drawn from existing population-based studies (San Antonio Heart Study and San Luis Valley Diabetes Study) or from health maintenance organization populations (Oakland and Los Angeles, Calif) that were basically representative of the general population. Furthermore, the focus of the present report is on the relationship of microalbuminuria and IMT, which both were measured in the study participants, rather than a description of the distribution of these factors in the general population. Therefore, we think that the results of the present study are applicable to a wider community beyond the IRAS population.
In conclusion, we showed that microalbuminuria was associated with increased IMT of the CCA in nondiabetic subjects, which was partly mediated by hypertension. A similar relationship was also seen in NIDDM subjects, but it did not reach statistical significance. Thus, microalbuminuria is related to atherosclerosis at an early stage of the disease process.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This study was supported by National Heart, Lung, and Blood Institute grants HL47887, HL47889, HL47890, HL47892, HL47902, and the General Research Centers Program (NCRR GCRC, M01 RR431, M01 RR011346).
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Footnotes |
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Reprint requests to Leena Mykkänen, MD, Department of Medicine, Division of Clinical Epidemiology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78284-7873.
Received April 16, 1997; revision received June 5, 1997; accepted June 5, 1997.
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