© 1995 American Heart Association, Inc.
Articles |
LDL Size and Subclass Pattern in Mexico City Residents and San Antonio Mexican Americans
From the Division of Clinical Epidemiology (S.M.H., H.M., M.P.S.), Department of Medicine, University of Texas Health Science Center at San Antonio; the Centro de Estudios en Diabetes (C.G.), American British Cowdray Hospital, Mexico City; and the Medlantic Research Institute (B.V.H.), Washington, DC.
Correspondence to Steven M. Haffner, MD, Department of Medicine, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Dr, San Antonio, TX 78284-7873.
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Abstract Recent studies suggest that a relative abundance of small dense LDL is a risk factor for coronary heart disease. We compared LDL size in Mexico City residents (n=191) and San Antonio Mexican Americans (n=282), two genetically similar populations that differ markedly in dietary behaviors: in Mexico City
62% of
calories are from carbohydrate and 19% from fat, and in San Antonio
40% of calories are from carbohydrate and 40% from fat. Mean
LDL size in Mexico City was 258.6±0.9 Å, and in San Antonio,
255.9±0.6 Å (P=.013). After adjustment for the higher
triglyceride and lower HDL cholesterol levels
(the two most important predictors of LDL size) in Mexico City, LDL
size was significantly lower in San Antonio than in Mexico City by
-8.33±0.84 Å (P<.001). Our data suggest that the
higher triglyceride concentrations in Mexico City residents
that are associated with a higher carbohydrate diet may not be
associated with atherogenic changes in LDL.
Key Words: LDL composition • ethnicity • Mexican Americans • diet
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Increased concentration of LDL-C is widely recognized as a risk factor for coronary heart disease.1 2 There is considerable heterogeneity in the size and density of LDL particles.3 4 Small dense LDL particles are thought to be more atherogenic than larger LDL particles, although this association may not be statistically independent of TG concentration.5 6 7 Austin et al6 have found that most individuals can be assigned to one of two LDL subclass patterns (A or B); relatively few subjects have an intermediate pattern (I). Small dense LDL (type B) is associated with diabetes, hyperinsulinemia, higher TG and lower HDL-C concentrations, and male gender.7 8 9 10 11 12 13 14
LDL heterogeneity may also have a genetic basis. In two family studies, LDL subclass pattern was found to have a strong genetic determinant.15 16 Nishina et al17 have provided evidence for linkage between the proposed gene for LDL type B and the LDL receptor locus located on the short arm of chromosome 19. However, relatively few studies of LDL composition have compared populations with different environmental and genetic backgrounds. Campos et al18 report higher concentrations of small dense LDL in rural and urban subjects from Puriscal, Costa Rica, than in Caucasian subjects from Framingham, Mass.
Relative to non-Hispanic whites, Mexican Americans are more obese,19 20 have higher TG concentrations,19 and have a higher prevalence19 21 and incidence22 of diabetes, hyperinsulinemia,23 and insulin resistance,24 and lower lipoprotein(a)25 concentrations. Mexican Americans have a considerable native American genetic admixture21 but a relatively similar diet to non-Hispanic whites in terms of percent of total kilocalories derived from carbohydrate, fat, and protein.26 LDL size in Mexican Americans is smaller than in non-Hispanic whites,13 although this difference is accounted for by the higher TG concentrations of Mexican Americans. Despite a higher predicted risk of cardiovascular mortality based on logistic regression coefficients for risk factors as derived from the Framingham study,27 Mexican American men have a lower prevalence of myocardial infarction and Mexican American women have a similar prevalence of myocardial infarction relative to their non-Hispanic white counterparts.28
Low-income Mexicans residing in Mexico City and low-income Mexican Americans residing in San Antonio are genetically similar, but Mexicans are less obese and more physically active than Mexican Americans.29 Mexicans also have higher TG and lower HDL-C concentrations and about one third less diabetes than Mexican Americans.29 Major differences in fat and carbohydrate intake as a percent of total kilocalories were observed between these populations, with Mexico City residents consuming approximately 18% to 21% of calories from fat, 58% to 62% from carbohydrate, and 15% to 17% from protein compared with 39% to 43% from fat, 38% to 42% from carbohydrate, and 14% to 17% from protein among Mexican Americans living in San Antonio.30
In this article we report on differences in LDL size between low-income Mexicans in Mexico City and low-income Mexican Americans in San Antonio. The higher TG and lower HDL-C levels in Mexicans occur in spite of less obesity and greater physical activity and are accompanied by higher carbohydrate consumption, suggesting an effect of the high-carbohydrate diet.31 32 We therefore asked whether the moderately increased TG levels associated with a high-carbohydrate diet are less likely to be associated with small dense LDL than the hypertriglyceridemia associated with obesity, glucose intolerance, and a high-fat diet.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
San Antonio
The San Antonio Heart Study is a population-based study of diabetes and cardiovascular disease in Mexican Americans and non-Hispanic whites. From 1979 through 1982 (phase I) and from 1984 through 1988 (phase II), we randomly selected households from several San Antonio, Tex, census tracts including low-income (barrio), middle-income (transitional), and high-income (suburban) tracts.19 23 The low-income neighborhoods were exclusively Mexican American, the middle-income neighborhoods were approximately 50% Mexican American and 50% non-Hispanic white, and the upper income neighborhoods were composed of 10% Mexican Americans and 90% non-Hispanic whites. All men and nonpregnant women 25 through 64 years of age who resided in the randomly selected households were eligible to participate. Mexican Americans were defined as individuals whose ancestry and cultural traditions derived from a Mexican national origin.33 Detailed descriptions of the phase I and II surveys are available.19 23 This study was approved by the Institutional Review Board of the University of Texas Health Science Center at San Antonio. All subjects gave informed consent.
In October 1987 we began an 8-year follow-up of the phase I cohort to determine the incidence of non–insulin-dependent diabetes mellitus and cardiovascular disease.22 This survey was completed in November 1990. Beginning in October 1991, we began a similar 8-year follow-up study of participants in phase II. This follow-up will be finished in the fall of 1996. To date, subjects have been reexamined from the first census tract of the phase II follow-up (a middle-income neighborhood; n=366) and the second census tract (a lower income barrio neighborhood; n=300). The overall response rate was 65%. Since the present article compares Mexican Americans residing in San Antonio with a low-income 35- to 64-year-old Mexican population residing in Mexico City, only the 35- to 64-year-old Mexican American subjects living in the low-income barrio examined in the 8-year follow-up of the phase II cohort (n=282) are included in this report. These 282 subjects were the entire sample of subjects who had contingency samples available in the second target area of the San Antonio Heart Study. Samples for this study were collected from April 1992 through October 1992.
Mexico City
In Mexico City, six low-income neighborhoods (colonias) were
selected for the study. Complete enumeration of the colonias was
performed between November 1989 and November 1991, and 3517 eligible
individuals (35- to 64-year-old men and nonpregnant women) were
identified. Of these 3517 subjects, 3319 (94.4%) completed a home
interview; of these 3319 subjects, 2198 (66.2%) completed a medical
examination at a clinic (overall response, 62.5%). Samples for this
substudy were collected between November 1991 and November 1992.
Physical Measurements
At both study sites, height, weight, waist and hip
circumferences, and skin reflectances were measured.34 35
BMI was calculated as weight in kilograms divided by height in meters
squared and was used as an index of overall adiposity. WHR was used as
a measure of upper body fat distribution.35 Skin
reflectance was measured with a Photovolt reflectance meter by using
three tristimulus filters on the inner aspect of the right arm, a
sun-shielded site.21 34 Lower reflectance values
indicate darker skin color. Percentage native American
admixture34 was calculated with a modification of
Bernstein's formula,
(m=[Rn-Rs]/[RI-Rs]),
where m is the percent native American admixture, Rn is the
skin reflectance of the hybrid population, and Rs and
RI are the skin reflectance values of the Spanish and
native American parental populations, respectively (33.3% and 12.3%,
respectively).
Before beginning the survey in Mexico City, the Mexico City clinic staff traveled to San Antonio and participated in a week-long joint-training session with the San Antonio staff. The training session followed procedures that we have used at approximately 6-month intervals since 1979 during fieldwork for the San Antonio Heart Study. Descriptions of these training procedures are available.36 Midway through the survey in Mexico City, one of the Spanish-speaking San Antonio clinic workers traveled to Mexico City for several days to observe the Mexico City staff making anthropometric and blood pressure measurements. She then demonstrated her own technique, after which a debriefing session was held and minor differences in technique were discussed and reconciled.
Blood Chemistry Measurements
At the examination in both cities, blood specimens were obtained
after a 12- to 14-hour fast, and a second specimen was obtained 2 hours
after administration of a 75-g glucose-equivalent load (Orangedex;
Custom Laboratories). Laboratory procedures for both studies were
performed in the Division of Clinical
Epidemiology Laboratory in San Antonio, or, in
the case of LDL subfractions, in the laboratory of the Medlantic
Research Institute, Washington, DC. In both San Antonio and Mexico City
samples were stored at -70°C. The specimens from Mexico were
shipped to San Antonio and subsequently to Washington, DC, on dry ice.
Insulin was measured by using a commercial radioimmunoassay
(Diagnostic Products Corp).23 Diabetes
mellitus was diagnosed according to the criteria of the World Health
Organization (fasting plasma glucose 
140 mg/dL and/or 2-hour glucose
200 mg/dL).37 Subjects who did not meet these criteria
but who were being treated with oral antidiabetic agents or insulin
were also considered to have diabetes. Fasting lipid and lipoprotein
levels were also measured.19 LDL subfraction measurements
were performed on a random subsample of 191 individuals residing in the
fourth and fifth colonias in Mexico City and on all 282 subjects (who
had available contingency samples) examined in the low-income
barrio in San Antonio.
LDL size and subclass assessment were determined on plasma samples according to the method of Krauss and Burke.4 Plasma samples for determination of LDL size were stored at -70°C (without thawing) until the analyses for LDL size were performed, an average of 7 months later; storage times ranged from 3 to 10 months. Gradient gels were obtained from Isolab, Inc. Measurement of particle sizes was calibrated by using LDL subfractions whose molecular diameter had been determined by analytical ultracentrifugation (courtesy of Dr R. Krauss, Donner Laboratories). Subjects were classified into three groups on the basis of the size and shape of the major peak. A major gradient peak >257 Å with skewing toward smaller particles was classified as pattern A. A predominant peak <253.5 Å with skewing toward larger particles was classified as pattern B. Subjects were classified as pattern I if the size of the predominant peak was between 253.5 and 257 Å unless the size was very close to the cutpoints and the peak had the shape of the A or B pattern. The mean sizes of the A, I, and B peaks were 264.7±0.3, 255.3±0.4, and 244.5±0.4 Å, respectively. The interassay coefficient of variation for eight control pools (240 to 263 Å) ranged from 1.8% to 3.6%.
Nutritional Analysis
Food frequency questionnaires were developed independently for
the San Antonio and Mexico City populations following the approach
suggested by Willett et al.38 Although the two
questionnaires had identical formats, the individual food items
differed and reflected the foods most commonly consumed in the
respective study sites. Both questionnaires were designed to capture
about 85% of the total daily intake of kilocalories, protein, fat, and
carbohydrate. The table of nutrient values available for the Mexico
City questionnaire provided adequate information for kilocalories,
protein, total fat, and total protein but not for sucrose or refined
sugars or type of fat. The validation of the food frequency instrument
has been described in detail.30
Statistical Methods
Statistical techniques included ANOVA, multiple linear
regression, 
2 tests, and Spearman correlation
coefficients.39 We confirmed that LDL size was normally
distributed by using normal probability plots. The skewness of the LDL
predominant peak size in the San Antonio Heart Study population was
-0.16 and its kurtosis was -0.71, values that also suggest
an approximately normal distribution. TG concentrations were
logarithmically transformed to reduce skewness and kurtosis.
Statistical analyses were performed on the natural logarithms
and the results were then back transformed into their natural units for
presentation in the tables. The effect of city on LDL
subclass pattern A or B adjusted for other covariates was determined by
multiple logistic regression; subjects with pattern I were excluded
from these analyses. Interactions between study site and other
variables (eg, obesity, body fat distribution, and glucose and TG
levels) were examined by using both logistic regression
analysis and ANOVA. There were no statistically significant
interactions (P>.30).
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Table 1
shows the anthropometric, demographic, and
metabolic characteristics of subjects in Mexico City and
San Antonio. Subjects from Mexico City were significantly more likely
to be male, younger, less obese, and have lower 2-hour glucose, 2-hour
insulin, HDL-C, LDL-C, and TC concentrations than subjects from San
Antonio. Subjects in Mexico City also had significantly higher TG
levels and WHR and were less likely to be diabetic than subjects from
San Antonio. Thirty-two percent of the subjects from Mexico City
had LDL subclass pattern B compared with 40% from San Antonio
(P=.038). LDL size in Mexico City subjects was 258.6±0.9 Å
compared with 255.9±0.6 Å in San Antonio subjects
(P=.013). Skin reflectance was not significantly different
in the two cities.
|
Table 2 shows Spearman correlations between LDL size and
selected variables overall and for the two cities separately. In
the overall population, LDL size was significantly inversely correlated
with insulin, TG, TC, and LDL-C levels and positively correlated with
HDL-C level. Correlations between LDL size and metabolic
variables were similar in subjects residing in Mexico and San
Antonio. Increased TG and decreased HDL-C concentrations are the
strongest correlates of small dense LDL.9 11 13 Thus, the
lower HDL-C and higher TG concentrations in Mexico City relative to San
Antonio may have attenuated the difference in LDL size between the two
cities.
|
Table 3 shows LDL size by city and selected
variables. After cross-classification according to TG or HDL-C
level, LDL size was significantly lower in San Antonio than in Mexico
City and was significantly related to male gender, diabetic status,
BMI, and fasting glucose, fasting insulin, TG, and HDL-C levels.
|
Table 4 shows multiple linear regression
analyses with LDL size as a dependent variable in two
different models. In model 1, age, city, and gender are the only
independent variables, and in model 2, BMI, WHR, skin color, TC,
HDL-C, LDL-C, TG, fasting glucose, 2-hour glucose, fasting insulin, and
2-hour insulin were also permitted to enter as independent
variables. In no case did both the fasting and 2-hour glucose or
insulin enter into the same regression model. In model 1, male gender
and residence in San Antonio significantly predicted small dense LDL.
In model 2, high TG and low HDL-C concentrations, male gender, fasting
glucose, and residence in San Antonio predicted small dense LDL.
Residence in San Antonio was associated with a 8.33-Å decrease in LDL
size. We also reanalyzed model 2 separately for men and
women. LDL size was significantly lower in San Antonio than in Mexico
City in both women (-5.3±1.0 Å, P=<0.01) and men
(-9.2±1.2 Å, P<.001). We also repeated the multiple
regression analyses with the sample confined to nondiabetic
subjects (n=402). LDL size was again significantly lower in San Antonio
than in Mexico City (-8.1±0.9 Å, P<.001).
|
Table 5 shows the results of multiple logistic
regression analyses with LDL subclass pattern B or A as the
dependent variable. Independent variables in the two models
were identical to those used in Table 4
. In model 1, male gender and
residence in San Antonio predicted pattern B. In model 2, high TG and
fasting glucose concentrations, low HDL-C level, male gender, and
residence in San Antonio significantly predicted pattern B.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Subjects living in Mexico City, despite being less obese, have higher TG and lower HDL-C concentrations than Mexican Americans living in San Antonio.29 Campos et al18 also report higher TG and lower HDL-C concentrations in subjects from Puriscal, Costa Rica, than in Caucasian subjects living in Framingham, Mass. Like Mexicans residing in Mexico City,30 subjects in Costa Rica also eat a high-carbohydrate diet.18 However, urban subjects in Costa Rica eat a diet higher in fat (28.9±5.9%) and lower in protein (10.3±2.6%) than do subjects in Mexico City (fat, 19.4%, and protein, 15.2%). High-carbohydrate diets are associated with increased TG levels in most31 32 40 41 but not all42 studies.
Unadjusted LDL size is significantly higher in Mexico City Mexicans than in low-income Mexican Americans living in San Antonio. Both groups have similar levels of native American admixture29 as assessed by skin reflectance, and thus ethnicity is probably not the cause of this difference. However, after adjustment for the higher TG and lower HDL-C levels in Mexico City, the city difference in LDL size became even greater. In both Mexicans and Mexican Americans, high TG and low HDL-C levels were associated with small dense LDL.
In their report of increased small LDL in subjects in Costa Rica compared with Caucasians living in Framingham, Mass, Campos et al18 did not adjust for the higher TG and lower HDL-C levels in the Costa Rican populations relative to the Framingham population. We have shown13 similar results in that Mexican Americans have smaller LDL than non-Hispanic whites in San Antonio; differences in LDL size can be explained by the relative dyslipidemia in the former group.
There was no significant association between dietary carbohydrates and
LDL particle size (Table 2). However, while food frequency data may
adequately assess the diet of groups, it may not be sufficiently
accurate to assess the diets of individuals. In contrast to the report
by Campos et al,18 higher carbohydrate intake in the
present study was inversely associated with LDL particle size in
women but not men. It is difficult to compare their data and ours,
since dietary fat and protein intake also differed between the two
populations. The metabolic mechanisms underlying the
significant association between TG concentrations and small dense LDL
are not well understood. One possibility is that some forms of
hypertriglyceridemia, such as that which
occurs with central obesity, are associated with increased
production rates of apoB as well as TGs, thus resulting in an
LDL particle enriched in apoB.16 In contrast, increased
dietary carbohydrate, which leads to the overproduction of
VLDL TGs but not VLDL apoB, leads to large TG-rich particles whose
metabolism results in larger LDL particles.42
A second weakness of the present report is that our study is
ecological. While the populations in San Antonio and Mexico City appear
to be genetically similar and we describe the differences in LDL
composition to the marked nutritional differences between the
population, we did not perform a dietary intervention.
A number of reports suggest a strong relation between coronary heart disease and a preponderance of small dense LDL that is independent of the absolute concentration of LDL-C.5 6 7 However, the association between LDL composition and coronary heart disease is not usually statistically independent of the TG concentration, which is not surprising given the strong correlation (r=-.65) between TG and LDL size. It is also not clear whether the association between coronary heart disease and small dense LDL is due to small dense LDL itself or to other correlates of small dense LDL such as low HDL-C or insulin resistance.
In conclusion, we have shown that Mexican Americans living in San Antonio have a preponderance of smaller denser LDL than genetically similar Mexicans living in Mexico City once differences in HDL-C and TG concentrations are controlled for. Our data suggest that elevations in TG levels induced by high-carbohydrate diets may be less likely to produce atherogenic changes in LDL composition than the hypertriglyceridemia that is associated with high-fat diets, further supporting recommendations of lowering the fat in the diet of subjects at risk of atherosclerosis. One may postulate two opposing tendencies: hypertriglyceridemia tends to decrease LDL size, but a high-carbohydrate diet tends to increase it. Depending on the net balance of forces, the effect on LDL size could go in either direction.
|
Selected Abbreviations and Acronyms |
|---|
|
|
Acknowledgments |
|---|
This work was supported by grants R01-HL-24799 and R37-HL-36820 from the National Heart, Lung, and Blood Institute. Administrative support was provided by the Fundación Mexicana para la Salud. The Centro de Estudios en Diabetes has received support from Consejo Asesor en Epidemiología and has a cooperative agreement with the Universidad Autónoma de México.
Received June 28, 1995; accepted September 19, 1995.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Castelli WP, Garrison RJ, Wilson PWF, Abbott RD, Kalousdian S, Kannel WB. Incidence of coronary heart disease and lipoprotein cholesterol levels: the Framingham Heart Study. JAMA. 1986;256:2835-2838.
2. Kannel WB, Castelli WP, Gordon T, McNamara PM. Serum cholesterol, lipoproteins, and the risk of coronary heart disease: the Framingham Study. Ann Intern Med. 1971;74:1-12.
3. Shen MMS, Krauss RM, Lindgren FT, Forte TM. Heterogeneity of serum low density lipoproteins in normal human subjects. J Lipid Res. 1981;22:236-244. [Abstract]
4. Krauss RM, Burke DJ. Identification of multiple subclasses of plasma low density lipoproteins in normal humans. J Lipid Res. 1982;23:97-104. [Abstract]
5. Crouse JR, Parkes JS, Schey HM, Kahl FR. Studies of low density lipoprotein molecular weight in human beings with coronary artery disease. J Lipid Res. 1985;26:566-574. [Abstract]
6.
Austin MA, Breslow JL, Hennekens CH, Buring JE,
Willett WC, Krauss RM. Low density lipoprotein subclass patterns
and risk of myocardial infarction. JAMA. 1988;260:1917-1921.
7.
Campos H, Genest JJ, Blijlevens G, McNamara JR, Janner
JN, Ordovas JM, Wilson PWF, Schaefer EJ. Low-density
lipoprotein particle size and coronary artery disease.
Arteriosclerosis. 1992;12:187-195.
8. Barakat HK, Carpenter JW, McLendon VD, Khazanie P, Leggett N, Heath J, Marks R. Influence of obesity, impaired glucose tolerance, and NIDDM on LDL structure and composition: possible link between hyperinsulinemia and atherosclerosis. Diabetes. 1990;39:1527-1533. [Abstract]
9.
McNamara JR, Campos H, Ordovas JM, Peterson JM, Wilson
PWF, Schaefer EJ. Effect of gender, age, and lipid status on
low-density lipoprotein subfraction distribution: results of the
Framingham Offspring Study.
Arteriosclerosis. 1987;7:483-490.
10.
Swinkels DW, Demacker PNM, Hendriks JCM, Van't Laar
A. Low-density lipoprotein subfractions and relationship of
other risk factors for coronary artery disease in healthy
individuals. Arteriosclerosis. 1989;9:604-613.
11.
Selby JV, Austin MA, Newman B, Zhong D, Quesenberry CP,
Mayer EJ, Krauss RM. LDL subclass phenotypes and the
insulin resistance syndrome in women.
Circulation. 1993;88:381-387.
12.
Feingold KB, Grunfeld C, Pang M, Doerrler W, Krauss
RM. LDL subclass phenotypes and triglyceride
metabolism in non–insulin-dependent
diabetes. Arterioscler Thromb. 1992;12:1496-1502.
13.
Haffner SM, Mykkänen L, Valdez RA, Paidi M, Stern
MP, Howard BV. Low-density lipoprotein subclass pattern in a
biethnic population.
Arteriosclerosis. 1993;13:1623-1630.
14. Haffner SM, Mykkänen L, Stern MP, Paidi M, Howard BV. Greater effect of LDL size in women than in men. Diabetes Care. 1994;10:1164-1771.
15. Austin MA, King MC, Vranizan MC, Newman B, Krauss RM. Inheritance of low density lipoprotein subclass patterns: results of complex segregation analysis. Am J Hum Genet. 1988;43:838-846. [Medline] [Order article via Infotrieve]
16.
Austin MA, Brunzell JD, Fitch WL, Krauss RM.
Inheritance of low-density lipoprotein subclass patterns in
familial combined hyperlipidemia.
Arteriosclerosis. 1990;10:520-530.
17.
Nishina PM, Johnson JP, Naggert JK, Krauss RM.
Linkage of atherogenic lipoprotein phenotype to the low density
lipoprotein receptor on the short arm of chromosome 19.
Proc Natl Acad Sci U S A. 1992;89:708-712.
18.
Campos H, Willett WC, Peterson RM, Siles X, Bailey SM,
Wilson PWF, Posner BM, Ordovas JM, Schaefer EJ. Nutrient intake
comparisons between Framingham and rural and urban Puriscal, Costa
Rica. Arterioscler Thromb. 1991;11:1089-1099.
19.
Stern MP, Rosenthal M, Haffner SM, Hazuda HP, Franco
LJ. Sex difference in the effects of sociocultural status on
diabetes and cardiovascular risk factors in Mexican
Americans: the San Antonio Heart Study. Am J
Epidemiol. 1984;120:834-851.
20. Haffner SM, Stern MP, Hazuda HP, Pugh JA, Patterson JK, Malina R. Upper body and centralized adiposity in Mexican Americans and non-Hispanic whites: relationships to body mass index and other behavioral and demographic variables. Int J Obes. 1986;10:493-502. [Medline] [Order article via Infotrieve]
21. Gardner LI, Stern MP, Haffner SM, Gaskill SP, Hazuda HP, Relethford JH, Eifler CW. Prevalence of diabetes in Mexican Americans: relationship to percent of gene pool derived from native American sources. Diabetes. 1984;33:86-92. [Abstract]
22. Haffner SM, Hazuda HP, Mitchell BD, Patterson JK, Stern MP. Increased incidence of type II diabetes mellitus in Mexican Americans. Diabetes Care. 1991;14:102-108. [Abstract]
23. Haffner SM, Stern MP, Hazuda HP, Pugh JA, Patterson JK. Hyperinsulinemia in a population at high risk for non-insulin dependent diabetes mellitus. N Engl J Med. 1986;315:220-224. [Abstract]
24. Haffner SM, Stern MP, Dunn JF, Mobley M, Blackwell J, Bergman RN. Diminished insulin sensitivity and increased insulin response in non-obese, non-diabetic Mexican Americans. Metabolism. 1990;39:842-847. [Medline] [Order article via Infotrieve]
25.
Haffner SM, Gruber K, Morales PA, Hazuda HP, Valdez R,
Stern MP. Lp(a) concentrations in Mexican Americans and
non-Hispanic whites: the San Antonio Heart Study. Am J
Epidemiol. 1992;136:1060-1068.
26.
Haffner SM, Knapp JA, Stern MP, Young EA.
Dietary intakes of macronutrients among Mexican Americans and Anglo
Americans: the San Antonio Heart Study. Am J Clin
Nutr. 1985;42:1266-1275.
27.
Mitchell BD, Stern MP, Haffner SM, Hazuda HP, Patterson
JK. Risk factors for cardiovascular mortality in
Mexican Americans and non-Hispanic whites: the San Antonio Heart
Study. Am J Epidemiol. 1990;131:423-433.
28.
Mitchell BD, Hazuda HP, Haffner SM, Patterson JK, Stern
MP. Myocardial infarction in Mexican Americans and non-Hispanic
whites: the San Antonio Heart Study.
Circulation. 1991;83:45-51.
29. Stern MP, González C, Mitchell BD, Villalpando E, Haffner SM, Hazuda HP. Genetic and environmental determinants of type II diabetes in Mexico City and San Antonio, TX. Diabetes. 1992;41:484-492. [Abstract]
30. Stern MP, Gonzáles C, Hernandez M, Knapp JA, Hazuda HP, Villalpando E, Valdez RA, Haffner SM, Mitchell BD. Performance of semiquantitative food frequency questionnaires in international comparisons: Mexico City versus San Antonio, Texas. Ann Epidemiol. 1993;3:300-307. [Medline] [Order article via Infotrieve]
31.
Ginsberg H, Olefsky JM, Kimmering G, Crapo P, Reaven
GM. Induction of
hypertriglyceridemia by a low fat diet in
normal humans. J Clin Endocrinol Metab. 1976;42:729-735.
32. Coulston AM, Liu GC, Reaven GM. Plasma glucose, insulin and lipid responses to high carbohydrate, low fat diets in normal humans. Metabolism. 1983;32:52-56. [Medline] [Order article via Infotrieve]
33.
Hazuda HP, Comeaux PJ, Stern MP, Haffner SM, Eifler CW,
Rosenthal M, Franco LJ. A comparison of three indicators for
identifying Mexican Americans in epidemiologic research: methodological
findings from the San Antonio Heart Study. Am J
Epidemiol. 1986;123:96-112.
34. Relethford JH, Stern MP, Gaskill SP, Hazuda HP. Social class, admixture, and skin color variation in Mexican Americans and Anglo Americans living in San Antonio, Texas. Am J Phys Anthropol. 1983;61:97-102. [Medline] [Order article via Infotrieve]
35. Haffner SM, Stern MP, Hazuda HP, Pugh JA, Patterson JK. Do upper body and centralized adiposity measure different aspects of regional body fat distribution? relationship to non-insulin dependent diabetes mellitus, lipids and lipoproteins. Diabetes. 1987;38:43-51.
36. Malina RM, Little BB, Stern MP, Gaskill SP, Hazuda HP. Ethnic and social class differences in selected anthropometric characteristics of Mexican American and Anglo adults: the San Antonio Heart Study. Hum Biol. 1983;55:867-881. [Medline] [Order article via Infotrieve]
37. World Health Organization Expert Committee. Second Report on Diabetes Mellitus. Geneva, Switzerland: World Health Organization; 1985. WHO technical report series No. 727.
38.
Willett W, Sampson L, Stampfer M, Rosner B, Bain C,
Witschi J, Hennekens C, Speizer F. Reproducibility and validity
of a semiquantitative food frequency questionnaire. Am J
Epidemiol. 1985;122:51-65.
39. SAS/STAT User's Guide. Release 6.03. Cary, NC: SAS Institute; 1988.
40. Antonis A, Bersohn I. The influence of diet on serum triglycerides in South African and Bantu prisoners. Lancet. 1961;1:3-9. [Medline] [Order article via Infotrieve]
41. Reaven GM, Lerner RL, Stern MP, Farquahar JW. Role of insulin in endogenous hypertriglyceridemia. J Clin Invest. 1967;46:1756-1767.
42. Abbott WGH, Swinburne B, Ruotolo G, Hara H, Patti L, Harper I, Grundy SM, Howard BV. Effect of a high-carbohydrate, low-saturated fat diet on apolipoprotein B and triglyceride metabolism in Pima Indians. J Clin Invest. 1990;86:642-650.
This article has been cited by other articles:
 |
|
 |
|
  K. R. Kulkarni, J. H. Markovitz, N. C. Nanda, and J. P. Segrest Increased Prevalence of Smaller and Denser LDL Particles in Asian Indians Arterioscler Thromb Vasc Biol, November 1, 1999; 19(11): 2749 - 2755. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||