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(Arteriosclerosis, Thrombosis, and Vascular Biology. 1996;16:1388-1392.)
© 1996 American Heart Association, Inc.

Articles

Ultrasonographically Assessed Maximum Carotid Artery Wall Thickness in Mexico City Residents and Mexican Americans Living in San Antonio, Texas

Association With Diabetes and Cardiovascular Risk Factors

Ming Wei; Clicerio Gonzalez; Steven M. Haffner; Daniel H. O'Leary; Michael P. Stern

the Division of Clinical Epidemiology (M.W., S.M.H., M.P.S.), Department of Medicine, University of Texas Health Science Center at San Antonio, San Antonio; the Centro de Estudios en Diabetes (C.G.), American British Cowdray Hospital, and Endocrinology and Metabolism Service, Division of Internal Medicine, Specialty Hospital of The National Medical Center, Mexican Social Security Institute, Mexico City; and the Department of Radiology (D.H.O'L.), New England Medical Center, Tufts University School of Medicine, Boston, Mass.

Correspondence to Ming Wei, MD, Division of Clinical Epidemiology, Department of Medicine, University of Texas Health Science Center at San Antonio, San Antonio, TX 78284-7873.

	Abstract

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Measurements of carotid artery wall thickness are often used as a surrogate for atherosclerosis. However, few studies have performed these measurements in populations of Mexican origin. Since Mexicans in Mexico City consume high-carbohydrate diets and have carbohydrate-induced dyslipidemia (high triglyceride and low HDL cholesterol levels) compared with Mexican Americans living in San Antonio, Tex, we questioned whether they also had more atherosclerosis than San Antonio Mexican Americans. Mean maximum intimal-medial thickness (IMT) of the common (CCA) and internal (ICA) carotid arteries were measured in 867 subjects aged 35 to 64 years (40% men) in two Mexican-origin populations, one from San Antonio (n=202) and the other from Mexico City (n=665). IMTs in the two cities were compared, and their associations with cardiovascular risk factors were analyzed. Older age, male sex, high levels of total cholesterol, low levels of HDL cholesterol, and high systolic blood pressure were positively associated with both CCA IMT and ICA IMT. Cigarette smoking was significantly associated with ICA IMT. CCA and ICA IMTs in diabetic subjects were thicker than in nondiabetic subjects in both men and women (all P<=.05). CCA IMT was thicker in the San Antonio than the Mexico City subjects after adjustment for cardiovascular risk factors (0.81 versus 0.76 mm in men and 0.77 versus 0.71 mm in women; P<.001 for city difference). San Antonio men also had thicker ICA IMT than their counterparts in Mexico City (0.88 versus 0.83 mm), but the reverse was true for women (0.73 versus 0.77 mm; interaction between sex and city, P<.05). Our results indicate that men had higher carotid IMTs than women. CCA IMT was thicker in San Antonio Mexican Americans than in Mexico City residents. The differences in ICA IMTs between San Antonio and Mexico City were inconsistent. Thus, since Mexico City residents consume high-carbohydrate diets, the data do not support an atherogenic effect of such diets. The interaction between sex and city on ICA IMT deserves further study.

Key Words: artery wall thickness • Mexican American • Mexico • risk factors

	Introduction

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Ultrasonographically assessed carotid artery wall thickness has been shown to be a safe, valid method for evaluating atherosclerosis.^{1 2 3 4 5 6 7 8 9 10} Several reports have provided evidence of a close relationship between carotid artery wall thickness and cardiovascular risk factors, such as high serum cholesterol, low HDL-C, cigarette smoking, and high SBP.^{11 12 13 14 15 16 17 18 19 20 21 22 23} Few studies, however, have investigated carotid artery wall thickness in populations of Mexican origin, who are of interest because they have been reported to have lower rates of cardiovascular disease but higher rates of diabetes than non-Hispanic whites.^{24 25 26} Furthermore, residents in Mexico City consume more carbohydrate and less fat and have higher TG and lower HDL-C levels than their Mexican American counterparts living in San Antonio, Tex.^{27 28} We have shown²⁷ that Mexico City subjects consume 65% of calories from carbohydrate and 19% from fat, whereas San Antonio Mexican American subjects consume 50% of calories from carbohydrate and 32% from fat. Since carbohydrate-induced lipemia (high TG and low HDL levels) has been postulated as a cardiovascular risk factor,^{29 30} we investigated whether there is a difference in carotid artery wall thickness between these two Mexican-origin populations.

Increased carotid artery IMT at one site is only modestly correlated with thickened artery walls at other carotid sites.³¹ However, most studies report the CCA IMT only or the average of the CCA and ICA IMTs. Information on the relation of risk factors to arterial IMT at different carotid sites may increase our understanding of atherosclerosis. We therefore assessed city differences and associations with risk factors separately for the CCA and ICA.

	Methods

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The Mexico City Diabetes Study was designed to provide information about the prevalence of diabetes, cardiovascular disease, and cardiovascular risk factors among residents of Mexico City. A total of six "colonias" (equivalent to U.S. census tracts) in Mexico City were selected for study, and a complete enumeration was performed in each area. All 35- to 64-year-old men and nonpregnant women were considered eligible (n=3505). Of these, 2258 (64.4%) completed a clinic examination, of whom 302 met study criteria for type II diabetes. A 3.25-year follow-up examination was begun on April 16, 1993. All prevalent diabetic subjects were recalled first, of whom 218 (72.2%) returned for follow-up examination. Follow-up of the nondiabetic participants was then begun and is now complete for 480 of 661 subjects from the first two of the six colonias in the original study. US examination was available at follow-up on 480 nondiabetic and 185 diabetic subjects. The cardiovascular risk factor profile was quite similar in the US sample and the original study population (data not shown).

The San Antonio sample consisted of Mexican Americans who participated in the IRAS. The IRAS sampling design called for one third of subjects to be diabetic. San Antonio IRAS participants were derived from the San Antonio Heart Study cohort, a random sample of the San Antonio population. Diabetic and nondiabetic subjects were recalled separately in random order. The present analyses are based on the 202 San Antonio subjects (55 diabetics) who were Mexican Americans and between 35 and 64 years of age. Again, the cardiovascular risk factor profile was quite similar in the US sample and the original San Antonio Heart Study population (data not shown). All survey and examination procedures were approved by the Institutional Review Boards of the University of Texas Health Science Center at San Antonio, and all subjects gave informed consent.

Diabetes was defined according to the plasma glucose criteria of the World Health Organization, ie, fasting plasma glucose 140 mg/dL and/or 2-hour postload glucose level 200 mg/dL.³² Subjects who did not meet these criteria but who gave a history of diabetes and reported current therapy with either oral antidiabetic agents or insulin were also considered to have diabetes. Plasma cholesterol, TG, and HDL-C levels were measured by using enzymatic procedures.³³

Measurement of Carotid Artery Wall Thickness
Carotid artery wall thickness was measured from US recordings made with a Toshiba SSA-270A imaging unit. The imaging protocol involved obtaining a single longitudinal lateral view of the distal 10 mm of the right and left CCAs and three longitudinal views (anterior, lateral, and posterior obliques) in different imaging planes of each ICA. Carotid ultrasonography was performed by certified sonographers who attended a week-long training course in San Antonio and received training in the IRAS ultrasonography protocol. This protocol is essentially identical to the protocol used in the Cardiovascular Health Study.⁹ All US readings were read by a single reader from the Ultrasound Reading Center at the Geisinger Medical Center, Danville, Pa, which developed standardized protocols for both scanning and interpretation of carotid ultrasonographic images. The images were digitized, and a single reader drew lines at the lumen-intimal, medial-adventitial, and adventitial-periadventitial interfaces on the near and far walls. Maximum IMT for each segment was determined by using a specially designed computer program. To quantify the degree of IMT of the carotid artery wall, the maximum wall thickness of the CCA was defined as the mean of the maximum wall thicknesses of the far wall on the left and right sides; the maximum wall thickness of the ICA was defined in the same way, with the results of the three views averaged for the right and left sides separately.^{7 9 34 35 36 37} The use of a single reader and the reading of both studies during the same approximate time frame eliminated concerns about interreader variability and temporal drift.

Statistical Methods
Based on a two-sided test with a .05 significance level and 80% power, the magnitude of the crude differences that could be detected between study subjects in the two cities was 0.044 mm for CCA IMT and 0.067 mm for ICA IMT. Variation in crude IMT and covariate-adjusted means were assessed by using ANCOVA. Since both US samples were stratified by diabetic status, although in slightly different ways, analyses are presented either separately for diabetic and nondiabetic subjects or adjusted for diabetes by using ANCOVA. Multivariate analyses were initially performed by using general linear regression models. Analyses were repeated by using log-transformation to normalize the distribution of TGs and IMTs. All probability values were calculated by using two-tailed tests. All statistical analyses were performed by using SAS software.

	Results

Top Abstract Introduction Methods Results Discussion References

 
Table 1 presents the mean age and unadjusted cardiovascular risk factors according to sex, city, and diabetic status. The mean age of diabetic subjects was similar in the two cities for both sexes. However, nondiabetic subjects in San Antonio were significantly older than nondiabetic subjects in Mexico City for both sexes. Despite the fact that subjects in Mexico City had consistently lower BMIs in every comparison, they nevertheless had significantly lower HDL-C levels and higher TG levels than subjects in San Antonio. This pattern is similar to that reported for the original parent populations.²⁸ These tendencies appear more clearly in the age- and diabetes-adjusted analyses presented in Table 2, which also shows that men had higher SBP and DBP, higher TG levels, and lower BMI and levels of HDL-C than women. More men were current cigarette smokers than women. These tendencies were consistent in both cities. Table 3 shows age-adjusted average CCA IMT and ICA IMT according to sex, city, and diabetic status. Using two-way ANCOVA with city and diabetic status as grouping variables, the main effect of diabetic status was significant, with diabetic subjects showing thicker IMTs in both men and women. Both CCA and ICA IMT were modestly correlated in these data (r=.3, P<.001).

View this table: [in this window] [in a new window]   Table 1. Selected Characteristics of Study Subjects in San Antonio and Mexico City by Sex and Diabetic Status

View this table: [in this window] [in a new window]   Table 2. Age- and Diabetes-Adjusted Risk Factors by Sex and City

View this table: [in this window] [in a new window]   Table 3. Age-Adjusted Carotid Artery Wall Thickness by Sex, City, and Diabetic Status

The age- and diabetes-adjusted and full risk factor–adjusted CCA and ICA IMTs according to city and sex are presented in Table 4. Even though subjects in Mexico City had higher levels of TGs and lower levels of HDL-C (Table 2), they had thinner CCA IMTs than subjects in San Antonio (0.76 versus 0.81 mm in men and 0.71 versus 0.77 mm in women; P<.0001 for city difference). For ICA IMT, an interaction between city and sex was detected: in San Antonio men had thicker (0.88 versus 0.83 mm) and women had thinner (0.73 versus 0.77 mm) ICA IMTs (P<.05 for the interaction between sex and city). CCA and ICA IMTs in men were thicker than in women, both in Mexico City and San Antonio (all P<.01). Table 5 shows the association of risk factors with carotid wall thickness. Since tests for interactions between sex and risk factors in their associations with carotid artery wall thickness were not significant, we pooled the sexes to increase statistical power. Older age, male sex, diabetes, high SBP, and low HDL-C were significantly associated with both CCA and ICA IMTs. However, a significant association between current cigarette smoking and carotid artery wall thickness was demonstrated only for ICA IMT, and a significant relationship between TC level and carotid artery wall thickness was seen only in CCA IMT in multivariate analysis. Overall, the combination of age, sex, and other risk factors explained 22% of the variance in CCA IMT and 12% of that in ICA IMT.

View this table: [in this window] [in a new window]   Table 4. Mean Maximum Carotid Artery Wall Thickness by Sex and City

View this table: [in this window] [in a new window]   Table 5. Associations Between Risk Factors and Maximum Carotid Artery Wall Thicknesses (Continuous Variable) in Multiple Regression Analysis Models

	Discussion

Top Abstract Introduction Methods Results Discussion References

 
Subjects in Mexico City had thinner CCA IMTs than those in San Antonio, even though they had higher TG and lower HDL-C levels; the latter are presumably due to the Mexico City residents' high carbohydrate intake, which leads to carbohydrate-induced lipemia.^{27 28} This dietary and lipid pattern is common in developing countries, where cardiovascular disease rates are low.^{38 39 40 41} However, some have expressed concern that this dyslipidemic pattern may potentially accelerate atherosclerosis.^{29 30} In addition to the established atherogenicity of low HDL levels, high TG levels have been associated with small dense LDL⁴² and increased levels of plasminogen activator inhibitor,⁴² both of which are considered to enhance atherogenesis. The present data of thinner CCA IMT and inconsistent differences in ICA IMT in Mexico City do not support the hypothesis that a high-carbohydrate diet would have an atherogenic effect. The present results are also consistent with our finding⁴³ that the hypertriglyceridemia associated with a high-carbohydrate diet may be less likely to produce atherogenic changes in LDL composition (ie, small dense LDL) than the hypertriglyceridemia associated with a high-fat diet.

In our study, San Antonio men had thicker but women had thinner ICA IMTs than their counterparts in Mexico City. These differences were not explained by differences in age, levels of TC, HDL-C, or TGs, or prevalence of smoking or diabetes between the two groups. One limitation in our study was that reproducibility between sonographers was not tested, so this source of measurement error could not be evaluated. However, both sonographers were extensively trained and certified in a common protocol.

Current population-based studies have documented that cardiovascular risk factors, including cigarette smoking, elevated SBP, high TC, and low HDL-C, are consistently associated with carotid artery wall thickness in the general population^{11 16 17 18 21 23} ; however, these studies contain few Hispanic individuals. Racial differences in carotid artery wall thickness have been found. For example, Tell et al²² report that whites have more carotid artery plaques than blacks. For white subjects, age, sex, diabetes, hypertension, and smoking history were significantly associated with CCA plaque thickness, but in black subjects only age and smoking were associated.²² Few studies based on populations of Mexican origin have thus far been reported. Our results corroborate findings of an association between carotid wall thickness and atherosclerosis risk factors after multivariate statistical adjustment. The effects of these risk factors on carotid artery wall thickness are similar to those reported for the general population of the U.S.^{17 21}

The ability to accurately predict wall thickness at one site given the wall thickness at another site is modest in our study, but is consistent with previous studies.³¹ Risk factors for carotid plaques may vary somewhat by arterial segment.^{12 22} Most previous carotid wall thickness–risk factor studies have used single CCA measurements or have combined a few sites into a single summary index. Comparisons of ICA and CCA IMTs are infrequent. In the present study, age, male gender, diabetes mellitus, SBP, TC, and HDL-C were all associated with both ICA and CCA IMT; smoking was significantly associated with ICA but not CCA IMT (Table 5). The association between smoking and carotid artery wall thickness seems to be stronger for the ICA than the CCA wall.⁹ It is also important to note that Mexican American smokers smoke, on average, only 9 cigarettes per day, and smokers in Mexico City smoke, on average, only 7 cigarettes per day (Table 2). The lack of a smoking effect on CCA IMT may be due to the low rate of cigarette consumption among Mexican smokers. Based on the patchy distribution of atherosclerosis in human arteries, the thickness at a given location of an artery should affect blood flow changes in the artery, and a greatly thickened arterial wall at one site may have a larger effect on local blood flow than modestly increased thickness at two sites. Therefore, we favor using both ICA IMT and CCA IMT separately as indicators of atherosclerosis, rather than the average of the thickness at both sites.

The reports of associations between diabetes and carotid artery wall thickness are controversial. Although a history of diabetes has not been independently associated with carotid wall thickness in some hospital-based studies,^{19 20} population-based studies have demonstrated that diabetes is a risk factor for maximal intimal-medial carotid thickening.^{11 23} Our data support such a relationship in populations of Mexican origin (Table 3).

	Selected Abbreviations and Acronyms

 

BMI = body mass index CCA = common carotid artery DBP = diastolic blood pressure HDL-C = HDL cholesterol ICA = internal carotid artery IMT = intimal-medial thickness IRAS = Insulin Resistance Atherosclerosis Study SBP = systolic blood pressure TC = total cholesterol TG = triglyceride US = ultrasound

	Acknowledgments

 
This study was supported by grants RO1HL24799, R37HL36820, and U01HL47902 from the National Heart, Lung, and Blood Institute, National Institutes of Health, the Consejo Nacional de Ciencia y Tecnologia (CONACYT) (2029/M9303), and the Fundacion Mexicana para la Salud. Dr Wei was supported by a training grant from the National Institutes of Health, Bethesda, Md.

Received August 7, 1995; revision received April 10, 1996;

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