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Carbohydrate Intake Is Associated with Diet Quality and Risk Factors for Cardiovascular Disease in U.S. Adults: NHANES III

Department of Food Science and Human Nutrition, Michigan State University, East Lansing, MI, (E.J.Y., J.K., W.O.S.), KOREA
Division of Food Science and Human Nutrition, Hoseo University, Chungnam, (H.K.C.), KOREA
Department of Food Science and Human Nutrition, Ewha Woman’s University (W.Y.K.), Seoul, KOREA

Address reprint requests to: Won O. Song, PhD, MPH, RD, Professor of Human Nutrition, and Associate Dean, 7 Human Ecology, Michigan State University, East Lansing, MI 48824-1224. E-mail: song{at}msu.edu

	ABSTRACT

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Objectives: To determine if carbohydrate intake, as a % of energy, was related to diet quality and risk factors for cardiovascular disease (CVD) in adults in a cross-sectional and population-based study in the U.S.

Methods: Data from the third National Health and Nutrition Examination Survey (NHANES III, 1988–1994) were utilized. The nationally representative sample of the U.S. population (3,754 men, 4,074 women, ages 25 to 64 years) was divided into quintiles of carbohydrate intake (% of energy), which was examined in relation to risk factors for CVD: systolic blood pressure, body mass index (BMI), and concentrations of serum triglyceride, serum total and HDL cholesterol and plasma glucose.

Results: When covariates (age, ethnicity, smoking, alcohol intake and total energy intake) were adjusted in multivariate analyses, carbohydrate intakes (% of energy) were inversely associated with BMI and serum total cholesterol concentration in men and BMI in women and positively associated with serum triglyceride concentration in women. When total sugar intake (% of energy) was further controlled as a step to understand the quality of carbohydrate, carbohydrate intakes (% of energy) was a stronger predictor of BMI and plasma glucose in men and BMI in women. A high carbohydrate diet (>57.4% of energy in men and >59.1% of energy in women) was associated with a low serum HDL-cholesterol concentration in men and high serum triglyceride in women.

Conclusion: Moderately high carbohydrate (50% to 55% of energy) diets were associated with low CVD risks with favorable lipid profiles.

Key words: carbohydrates, cardiovascular disease, NHANES III, triglyceride, BMI, cholesterol, glucose

	INTRODUCTION

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Cardiovascular disease (CVD) is the major cause of morbidity and mortality in American adults [1]. The risk of CVD rises with increasing age, body weight, blood pressure, cigarette smoking, alcohol intake and dyslipidemia [2,3]. Epidemiological studies have shown that elevated concentrations of serum total cholesterol and LDL-cholesterol are independent risk factors for CVD [4,5]. In efforts to reduce the risk of CVD, high-carbohydrate, low-fat diets have been recommended in the U.S. This advice is largely based on population observational studies in which low fat intake was associated with low risk for CVD, presumably by way of lower LDL-cholesterol levels [6]. In a recent human study [7], however, total fat replaced by carbohydrate intake resulted in an elevated plasma concentration of fasting triglyceride, decreased HDL-cholesterol and elevated triglyceride-rich lipoproteins, which may counteract the benefits of lowering LDL-cholesterol and lead to high risks for developing CVD [8,9]. A high fasting plasma triglyceride concentration is associated with postprandial lipemia, high plasminogen activator inhibitor-I concentration and smaller and denser LDL particles in plasma [10]. Even though LDL-cholesterol concentrations are similar on diets high in carbohydrate or monounsaturated fatty acids, the smaller LDL particles accompanying high-carbohydrate diets are indicative of higher levels of LDL apolipoprotein B [6]. Furthermore, on a high-carbohydrate diet, apolipoprotein B levels in triglyceride-rich lipoproteins are also higher than on a monounsaturated fatty acid rich diet. High-carbohydrate, low-fat diets also increase insulin concentrations [11], which have been reported to increase risk of CVD [12]. It is speculated that insulin-resistance is associated with the untoward effects on glucose, insulin and lipoprotein metabolism when the individual consumes a high-carbohydrate, low-fat diet [13].

Both the source and the amount of carbohydrate intake are potentially important. Simple sugars have a greater effect on raising triglyceride and total cholesterol than starch and a substantial effect on lowering HDL-cholesterol [14]. Dietary fiber, on the other hand, has shown a triglyceride-lowering effect, partially protecting against the triglyceride-raising effects of sucrose [14]. Dietary fiber, however, has shown no effects on preventing the cholesterol raising effect or the HDL-cholesterol lowering effect of sucrose [14,15].

High-carbohydrate intakes may not be entirely neutral with respect to CVD when high intakes are ingested for prolonged periods. The issues of optimal carbohydrate and fat intakes are obviously complex. We thus aimed to examine the association between carbohydrate intake, compounded with sugar intake, and risk of CVD in a large nationally representative sample of the U.S. population. The goal is to extend our understanding of the optimal proportion of carbohydrate intake (% of energy) to reduce risks for CVD.

	METHODS

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Description of Dataset
Included in the study were participants in the third National Health and Nutrition Examination Survey (NHANES III, 1988–94), conducted by the National Center for Health Statistics (NCHS). The purpose of the survey was to obtain nationally representative information on the health and nutritional status of the non-institutionalized population, ages two months and older. A total of 33,998 persons were surveyed after being selected by the stratified multistage probability sampling design. In the survey, data were collected via standardized questionnaires, physical examination and phlebotomy. Additional details about the NHANES III have been previously reported [16].

The subjects included in this study were men (n = 3,754) and women (n = 4,074), ages 25 to 64 years. The subjects excluded were those with unreliable and incomplete dietary data as coded by NCHS (n = 325), pregnant (n = 168) and lactating (n = 71) women, subjects who reported changing their diet because of any medical reasons or health conditions during the past one year (n = 2,061), subjects with implausibly low or high daily energy intakes (<500 kcal/day and >7,500 kcal/day for men, >5,000 kcal/day for women; n = 151), subjects with implausibly high sugar intake (>90% energy intake from sugars, n = 9) or high alcohol consumption (>66% energy from alcohol, n = 7), individuals taking medication for heart diseases (ICD code 429.9, n = 242) or medication for hyperlipidemia (drug classification code 912, n = 178), subjects who were told by a physician that they had heart attack or stroke (n = 439), or diabetes or were taking insulin (n = 688), subjects with BMI >62 kg/m² (n = 7) and subjects with serum triglyceride >900 mg/dL (n = 20). The subjects included in this study fasted at least ten hours and six hours for morning and evening blood samples, respectively. Details of the laboratory analytical methods and dietary survey methods about the NHANES III have been reported elsewhere [17].

Data Analyses
High carbohydrate intake was examined in relation to the known risk factors for cardiovascular diseases: age, ethnicity, education, income, cigarette smoking, alcohol intake, physical activity, body mass index (BMI), waist-to-hip ratio, systolic blood pressure, diastolic blood pressure, serum triglyceride, serum total cholesterol, serum HDL-cholesterol, serum insulin and plasma glucose. Since LDL-cholesterol was calculated from measured values of total cholesterol, triglycerides and HDL-cholesterol in NHANES III, LDL-cholesterol had collinearity with other blood lipid variables, so we used only the measured blood lipid variables (total cholesterol, triglycerides, and HDL-cholesterol) in our analyses. Based on a review of the literature [2,18], univariate analyses and change of the effect estimates by differences less than 1% in multivariate analyses, we selected 10 risk factors: age, ethnicity, cigarette smoking, alcohol intake, BMI, systolic blood pressure, serum triglyceride, serum total cholesterol, serum HDL-cholesterol and plasma glucose. Finally, we examined the relationship between carbohydrate intake and six primary risk factors: BMI, systolic blood pressure, serum triglyceride, serum total cholesterol, serum HDL-cholesterol and plasma glucose, while controlling for age, ethnicity, cigarette smoking, alcohol and total energy intake.

All statistical analyses were carried out with SAS (SAS Institute Inc.) and SUDAAN (Research Triangle Institute) software. SUDAAN was used to account for the complex sample design effect of the national survey. All analyses accounted for appropriate sample weights to adjust for unequal probabilities for selection and non-respondent characteristics. We used multiple linear regression and multiple logistic regression models to draw inferences for each gender separately.

The dietary intakes were estimated from 24-hour dietary recalls. Since the 24-hour dietary recall method is not appropriate to characterize individual diets, we grouped carbohydrate intake by quintiles. To compute age and ethnicity adjusted daily mean nutrient intakes by quintiles of carbohydrate intake (% of energy), nutrient variables were treated as dependent variables in a linear regression, with the adjustment factors as independent variables.

Means, odds ratios (ORs) and 95% confidence intervals (CIs) of six risk factors (BMI, systolic blood pressure, serum triglyceride, serum total cholesterol, serum HDL-cholesterol and plasma glucose) were calculated by quintiles of carbohydrate intake (% of energy) after multivariate adjustment for potentially confounding variables (age, ethnicity, cigarette smoking, alcohol intake and total energy intake). The adjusted means of the six risk factors were computed by using linear regression. The adjusted ORs and 95% CIs by quintiles of carbohydrate intake (% of energy) were computed by using logistic regression. The continuous variables were categorized into five age categories (30, 40, 50, 60, >60 years), three smoking status groups (current, past, non-smoker) and four alcohol intake groups (none, <20, 20–40, >40 g/day in men; none, <4, 4–10, >10 g/day in women) based on the distribution of the data. Total energy intake was entered into the models as a continuous variable. The six risk factors were divided into two groups (risk vs. non-risk) to compute the ORs. The cut-off points used were BMI 30 kg/m², systolic blood pressure <140 mmHg (subjects taking anti-hypertensive drugs (n = 450) were also categorized into the risk group), serum triglyceride <200 mg/dL, serum total cholesterol <240 mg/dL, serum HDL-cholesterol 35 mg/dL and plasma glucose <110 mg/dL [19]. In computing the ORs, the lowest quintile of carbohydrate intake (% of energy) was the reference group (OR = 1.0). As a step toward understanding the effects of the quality of carbohydrate, the analyses were repeated controlling for total sugar intake and fiber intake by adding total sugar intake as a % of energy (sum of sucrose, galactose, maltose, glucose, fructose and lactose) and fiber intake (g/day) to the full multivariate model to investigate whether the relationship of carbohydrate intake to CVD risk was affected by total sugar or fiber intakes. A test for trend was conducted after assigning the mean value of each quintile of carbohydrate intake and modeling this value as a continuous variable.

	RESULTS

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The weighted sample was 75.7% White, 10.6% Black, 6.0% Mexican American and 7.9% other ethnicities in men, and 75.0% White, 12.1% Black, 5.0% Mexican American and 8.0% other ethnicities in women. Tables 1 and 2 show the mean age, smoking status, alcohol intake and nutrient intakes for men and women, respectively. The mean age according to carbohydrate intake (% of energy) from the lowest to highest quintiles ranged from 39 to 40 years in men and from 40 to 41 years in women. Both men and women with high intakes of carbohydrate smoked less and consumed less alcohol. The pattern of nutrient intakes adjusted for age and ethnicity according to the quintiles of carbohydrate intake (% of energy) were similar for both men and women. A higher carbohydrate intake (% of energy) was associated with lower intakes of energy, total fat, cholesterol, protein, vitamin B₁₂ and zinc, but higher intakes of fiber and total sugar in both men and women. When compared with dietary guidelines [20], folic acid and fiber intakes were below the recommended intake in all groups. Zinc intake was below the recommended amount in both men (4th and 5th quintiles of carbohydrate intake) and women. Vitamin E and calcium intakes in the 4th and 5th quintiles of carbohydrate intake in women were less than the recommended amounts. Total sugar intakes (% of energy) in the 4th and 5th quintiles of carbohydrate intake (% of energy) were high with >50% of total carbohydrate intake. Although fiber intakes differed between the 1st and 5th quintiles of carbohydrate intake, daily fiber intakes were well below the recommended intake of 25–30 g/day in both men (16–22 g/day) and women (12–16 g/day).

When total sugar intake (% of energy) was adjusted for in men, the association of BMI and plasma glucose with carbohydrate intake (% of energy) was strengthened (Table 3). This suggests that total sugar intake (% of energy) could be a substantial factor in the relationship between carbohydrate intake and BMI as well as carbohydrate intake and plasma glucose in men. When dietary fiber intake (g/day) was further adjusted for, the association of BMI and serum total cholesterol with carbohydrate (% of energy) in men was attenuated.

In women, when total sugar intake (% of energy) was adjusted for, the association of BMI with carbohydrate intake (% of energy) was strengthened (Table 4). After the additional adjustment for dietary fiber intake (g/day), the association of triglyceride with carbohydrate intake (% of energy) in women increased.

	DISCUSSION

 
Current trends to decrease CVD risks emphasize the importance of increasing carbohydrate intake, predominantly from whole grains, and reducing dietary fat and saturated fat intake. Among populations that differ in eating habits, those with a higher consumption of total fat usually have a higher prevalence of obesity [21,22]. High-carbohydrate, low-fat diets are attractive because of their reduced energy density [23] and theoretical considerations of higher metabolic cost than high-fat diets in relation to weight loss [24]. In our results, BMI of those with high-carbohydrate, low-fat diets were significantly lower than those with low carbohydrate diets. The risk for CVD may be reduced by high carbohydrate diets at least through decreased BMI.

Several dietary factors, including the amount and type of dietary fat, cholesterol, fiber and minerals, affect blood pressure [25]. Svetkey et al. [26] reported that the DASH (the Dietary Approaches to Stop Hypertension) combination diet (55% carbohydrate, 27% fat, 31 g fiber) lowered blood pressure compared to a control diet (48% carbohydrate, 37% fat, 9 g fiber). In our results, higher carbohydrate intakes (% of energy) were associated with lower intakes of total fat and total cholesterol and higher intakes of fiber. However, carbohydrate intakes (% of energy) were not associated with systolic blood pressure in both men and women.

Recommendations to decrease fat intake are based on the evidence that high saturated fat and cholesterol in a high fat diet raise serum LDL-cholesterol levels, thereby increasing risk of CVD. Our findings are not in conflict with this evidence. In our study, high-carbohydrate, low-fat diets were positively associated with serum triglyceride and negatively associated with serum HDL-cholesterol. Substantial evidence exists that high-carbohydrate, low-fat diets alter lipoprotein, glucose, and insulin metabolism and thereby increase the risk of CVD [12]. Stampfer et al. [27] reported that CVD risks increase with higher serum triglyceride levels and lower HDL-cholesterol. Willett [28] also noted that HDL-cholesterol is strongly protective against CVD and that the serum total cholesterol level does not represent the complete effect of blood lipids on the risk of CVD. Triglyceride concentrations were significantly higher (p <0.001) when subjects consumed diets containing 60% carbohydrate (25% fat) compared to 40% carbohydrate (45% fat) in a trial of postmenopausal women [29]. Fat restricted diets (18% to 30% energy) given to hypercholesterolemic men for one year resulted in decreased total cholesterol, LDL-cholesterol and HDL-cholesterol and increased triglyceride [30]. Knopp et al. [30] noted that a low-fat diet compared with a moderate-fat diet offers few advantages with potentially undesirable effects.

In our study, serum total cholesterol was inversely associated with carbohydrate intake (% of energy) in men and no association in women. Odds ratios for serum HDL-cholesterol did not differ among quintiles of carbohydrate intake (% of energy), with no trend for serum HDL-cholesterol among the quintiles in either men or women. However, the mean HDL-cholesterol value in the 5th quintile of carbohydrate intake (>57.4%) was significantly lower than those in the 1st quintile of carbohydrate intake (38.7%) in men. The carbohydrate intake (% of energy) was positively associated with serum triglyceride level in women, but not in men.

According to the USDA’s Continuing Survey of Food Intakes by Individuals [31], dietary carbohydrate intake increased to about 52% of energy intake from 45%, and fat intake decreased from 40% to 33% of energy intake from the 1960s to 1995. The plethora of fat-free foods offers people the opportunity to consume more sugar, not complex carbohydrate and fiber. In our results, total sugar intake substantially contributed to carbohydrate intake. Total sugar intakes in those consuming >50.8% of energy from carbohydrate in men (>52.4% in women) were high at over 50% of total carbohydrate intake. Sugar intake, partially sucrose, has been reported to have a greater triglyceride and cholesterol-raising effect than starch [32]. When healthy young men altered their usual high fat Western diets (40% carbohydrate, 39% fat) to very low fat, low or moderate sucrose diets (70% carbohydrate with 0% or 18% sucrose, 15% fat), triglyceride concentrations changed little; however, very low fat diets with high sucrose (32% to 52% of total energy) resulted in elevated serum triglyceride [14] and decreased HDL-cholesterol concentrations. Liu et al. [33] reported that dietary glycemic load is positively associated with risk of CVD. Sugar intake can increase blood triglyceride level and decrease HDL-cholesterol more so than grain intake. Therefore, high-carbohydrate, low-fat diets with high sugar content may counteract the benefit of lowering risk for CVD.

Krauss et al. [34] estimated the effects of isocaloric dietary substitutes on the risk of CVD. Replacing 4% of energy from saturated fat with an equivalent amount of energy from carbohydrate would reduce the risk of CVD by about 5%. On the other hand, replacing energy from unsaturated fat with energy from carbohydrate increases the rate of CVD. Therefore, a higher dietary intake of saturated fat and trans unsaturated fat were associated with an increased risk of CVD, whereas a higher intake of monounsaturated fat and polyunsaturated fat were associated with decreased risk. In our study, the ratio of polyunsaturated fat/saturated fat (P/S ratio) from highest to lowest quintiles of carbohydrate intakes (% of energy) were 0.66, 0.67, 0.71, 0.66 and 0.74 in men and 0.73, 0.70, 0.68, 0.71 and 0.76 in women. Because of the opposite effects of saturated fat and unsaturated fat on incidence for CVD, there are different opinions about total fat intake in relation to CVD.

Which dietary recommendation is ideal for reducing CVD? Various scientific organizations, including the American Heart Association [34,35] and the National Heart, Lung, and Blood Institute [36], have recommended reductions in dietary total fat and saturated fat intake to treat or prevent CVD. The suggested amounts are less than 30% of total energy intake from fat and 55% from carbohydrate. Lewis et al. [37] recommended that the low fat (27% energy), high carbohydrate (59% energy), high fiber (55 g/2500 kcal) diet produced the most favorable lipid profile. Any increase in complex carbohydrate must be associated with an increase in dietary fiber to prevent hypertriglyceridemia and a fall in HDL-cholesterol. However, Garg et al. [38] suggested that a high carbohydrate diet (55% carbohydrate, 30% fat) did not have advantages in lowering LDL-cholesterol levels compared to a high fat diet (40% carbohydrate, 45% fat consisting of 25% monounsaturated fat) in NIDDM patients. Jeppesen et al. [29] recommended that an isoenergetic diet containing 45% of energy from carbohydrate, 10% saturated fat, 10% polyunsaturated fat, 20% monounsaturated fat and 15% protein might be the best diet for all.

An increase in carbohydrate intake over 60% of energy might have greater effects on serum total cholesterol and weight control, but negative effects on serum triglyceride and HDL-cholesterol. In our study, high carbohydrate diets (>57.4% in men and >59.1% in women) were associated with a higher concentration of serum triglyceride and lower HDL-cholesterol. Moreover, the recommendation that all individuals should consume high-carbohydrate, low-fat diets can be questioned [30]. From previous evidence that insulin resistance and compensatory hyperinsulinemia were associated with lower HDL-cholesterol and higher triglyceride [39], it was predicted that the more insulin-resistant an individual, the greater would be the negative metabolic effects of high-carbohydrate, low-fat diets. Jensen et al. [40] concluded that LDL-cholesterol and triglyceride increased and HDL-cholesterol decreased significantly as a consequence of menopause. Based on Do et al. [3], HDL-cholesterol appears to be the only biological risk factor for CVD that changes as a direct consequence of menopause. Therefore, it was strongly suggested that the effects of a high-carbohydrate, low-fat diets on increasing the risks of CVD would be critically relevant in the insulin-resistant subjects and menopausal women.

	CONCLUSIONS

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In our study, high-carbohydrate, low-fat diets were inversely associated with BMI and serum total cholesterol in men and BMI in women. However, the highest quintile of carbohydrate intake (>57.4% in men and >59.1% in women) was associated with a higher concentration of serum triglyceride and lower HDL-cholesterol. Based on our findings, we conclude that diets moderately high in carbohydrate (50% to 55% of energy) are associated with low CVD risks with favorable lipid profiles. One should keep in mind that the sources of fat and carbohydrate have significant effects on risk factors for CVD.

Received December 10, 2001. Accepted July 3, 2002.

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