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Journal of the American College of Nutrition, Vol. 17, No. 3, 250-255 (1998)
Published by the American College of Nutrition

Original Paper

Relation of Serum Ascorbic Acid to Serum Lipids and Lipoproteins in US Adults

Joel A. Simon, MD, MPH, FACN, and Esther S. Hudes, PhD, MPH

General Internal Medicine Section, Medical Service, Veterans Affairs Medical Center, San Francisco, CA, (J.A.S)
Department of Epidemiology and Biostatistics, University of California, (J.A.S., E.S.H.) San Francisco, CA

Address reprint requests to: Joel A. Simon, MD, MPH, General Internal Medicine Section (111A1), San Francisco VA Medical Center, 4150 Clement Street, San Francisco, CA 94121


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Objective: To examine the relation of serum ascorbic acid level to serum lipid and lipoprotein levels among a random sample of the US adult population.

Methods: Using linear regression, the relation of serum ascorbic acid level to serum lipid and lipoprotein levels was examined among 5,412 women and 5,116 men enrolled in the Second National Health and Nutrition Examination Survey (NHANES II), 1976–1980. Age, race, body mass index, level of physical activity, level of education, alcohol intake, and dietary energy, cholesterol, and fat intakes, and other potential confounders were included in the multivariate models.

Results: Serum ascorbic acid level was independently associated with high-density lipoprotein cholesterol (HDL-C) among women; each 1 mg/dl increase in serum ascorbic acid level (range 0.1 to 2.7 mg/dl) was associated with a 2 mg/dl increase in HDL-C level (p=0.001). Because other investigators have demonstrated an inverse relation between ascorbic acid intake or blood levels and total serum cholesterol in individuals with elevated total serum cholesterol levels, we analyzed four subgroups of NHANES II participants with total serum cholesterol levels >200 mg/dl. Among women with total serum cholesterol levels >=200 mg/dl, each 1 mg/dl increase in serum ascorbic acid level was independently associated with an increase of 2 to 3 mg/dl in HDL-C level (p<=0.05). Serum ascorbic acid level was not significantly associated with other serum lipids or lipoproteins.

Conclusions: If the observed associations are linked causally, they would suggest that ascorbic acid is a factor in cholesterol homeostasis among women and may be particularly important for women at increased risk for coronary heart disease.

Key words: ascorbic acid, cholesterol, lipids, vitamin C


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
In experimental animals, ascorbic acid affects the catabolism of cholesterol to bile acids [1–7]. Administration of ascorbic acid attenuates the expected rise in serum cholesterol in cholesterol-fed rabbits [8–12] and exerts a hypolipidemic effect in guinea pigs [6,13–15]. Some observational studies have found significant negative correlations between ascorbic acid status and total serum cholesterol [16,17] and others have reported positive correlations between ascorbic acid status and high-density lipoprotein cholesterol (HDL-C) [18–21]. Several observational studies in humans have reported an inverse association between ascorbic acid intake and cardiovascular disease [22–24], although these associations have not been found consistently [25,26].

To examine the relation between serum ascorbic acid level, which reflects usual dietary intake, and serum lipid and lipoprotein levels, we analyzed data from the Second National Health and Nutrition Examination Survey (NHANES II). NHANES II collected serum ascorbic acid and serum lipid and lipoprotein levels on a representative sample of over 10,000 Americans.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
Subjects
NHANES II was a national probability survey of over 20,000 Americans conducted between 1976 and 1980 that employed a stratified, cluster sampling design to over-sample populations of special interest [27]. Participants, whose age ranged from 3 to 74 years, were interviewed and examined by study personnel at two visits [27]. Complete data from 10,528 adult participants between the ages of 20 and 74 years were available for these analyses. We excluded participants who were missing data on variables likely to be associated with serum lipid levels, such as body mass index, smoking, exercise, alcohol consumption, and dietary fat intake. Participants who reported use of lipid-lowering medication were also excluded.

Measurements
NHANES II questionnaire data included self-reported age, race, sex, years of education completed, level of leisure time physical activity, history of smoking, diabetes mellitus, level of alcohol intake, menopausal status, and use of cholesterol-lowering medications and oral contraceptives. All participants were asked whether they used hormones, but use of estrogen replacement therapy was not specifically ascertained. For women who were >40 years old and who had no history of thyroid disease, we considered a positive response to the use of hormones to denote use of estrogen replacement therapy. Nutrition data were collected using a food frequency questionnaire and 24-hour diet recall. We calculated body mass index (weight in kg/height in m2) from weight and height data recorded during the physical examination. The questionnaires, dietary methods, and examination procedures used in NHANES II have been described elsewhere in detail [27].

Serum ascorbic acid levels were measured at the Centers for Disease Control by the dinitrophenyl-hydrazine method using a standardized protocol [28]. Because there were a small number of extreme serum ascorbic acid values of questionable validity (ranging as high as 18.1 mg/dl), we excluded participants with ascorbic acid levels in the top 0.5% of the sample (n=54). Ascorbic acid levels for the remaining 99.5% of the participants ranged from 0.1 to 2.7 mg/dl.

All lipid and lipoprotein samples were measured at the George Washington Lipid Research Clinic Laboratory and performed according to the Lipid Research Clinic Program protocols [29]. We analyzed the association between ascorbic acid and total non-fasting serum cholesterol levels, which have been reported to reflect fasting cholesterol levels accurately [30]. Smaller numbers of participants had measurements of HDL-C and triglycerides performed. We used standard equations to calculate low density lipoprotein cholesterol (LDL-C) levels [31]. We excluded 833 participants with serum triglyceride levels >400 mg/dl from the analyses of the relation of ascorbic acid to LDL-C because the estimation of LDL-C levels in such individuals cannot be made accurately using the Friedewald equation.

Statistical Methods
We examined the distribution of ascorbic acid concentrations and other variables of interest using sample weights. We used simple and multiple linear regression models to examine the associations of ascorbic acid level and other variables to serum lipid and lipoprotein levels. Level of education, level of physical activity, and alcohol consumption were analyzed as ordinal variables. We examined whether hormone use and menopausal status modified the association of ascorbic acid to total serum cholesterol and lipoprotein levels by including interaction terms in the multivariate models and by performing stratified analyses when interactions were detected.

Analyses were performed using Stata software that included survey commands for the analysis of complex survey data [32]. Stata uses the Taylor linearization method to estimate standard errors from complex surveys. We calculated regression coefficients and 95% confidence intervals to estimate the difference in serum lipid and lipoprotein level associated with each 1 mg/dl increase in serum ascorbic acid level. Two-tailed p values of <=0.05 were considered to be statistically significant, unadjusted for multiple comparisons [33].


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 
The characteristics of study participants, including mean age, serum ascorbic acid level, serum lipid and lipoprotein levels, and intake of calories, cholesterol, and fat are presented in Table 1. There were approximately equal numbers of women and men participants, who were, on average, middle-aged, non-obese, and white. Among participants >40 years, men had lower total serum cholesterol levels than women (225 mg/dl vs. 238 mg/dl, respectively); among participants <=40 years, sex-related differences in total serum cholesterol levels were smaller in magnitude (197 mg/dl vs. 192 mg/dl, respectively) (both p<0.0001).


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  		Table 1. Characteristics of the Study Subjects (n=10,528)*

 
Among women, serum ascorbic acid level was significantly associated with higher HDL-C levels in univariate, age-adjusted, and multivariate models (all p<=0.002). (Table 2) After controlling for the effects of age, race, body mass index, level of physical activity, current smoking, highest level of education achieved, intake of dietary fat, cholesterol, energy, and alcohol, and use of oral contraceptives, hormones, and menopausal status, each 1 mg/dl increase in serum ascorbic acid level was independently associated with a 2 mg/dl increase in HDL-C level. Among men, higher serum ascorbic acid levels were significantly associated with HDL-C levels in univariate and age-adjusted models (both p=0.04), but were no longer associated with HDL-C level after multivariate adjustment (p=0.26). Serum level of ascorbic acid was not significantly associated with any other serum lipid or lipoprotein level. (Table 2)


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  		Table 2. Difference in Serum Lipid and Lipoprotein Level (in mg/dl) for Each 1 mg/dl Increase in Serum Vitamin C Level{dagger}

 
We examined whether hormone use or menopausal status might modify the association of serum ascorbic acid level to serum lipid and lipoprotein levels. There was no evidence of such an interaction for menopausal status, however, we did detect an interaction between serum ascorbic acid and hormone use on HDL-C level (p=0.02). Performing analyses stratified by hormone use, we found that among women who used hormones (n=269), each 1 mg/dl increase in serum ascorbic acid level was marginally associated with a 3.9 mg/dl increase in HDL-C (p=0.08), whereas among women who did not use hormones (n=4395), each 1 mg/dl increase in serum ascorbic acid level was significantly associated with a 1.6 mg/dl increase in HDL-C (p=0.002).

Because ascorbic acid may be involved in cholesterol homeostasis and may lower cholesterol levels among individuals with high cholesterol levels, we analyzed subgroups of participants with total serum cholesterol levels >=200 mg/dl at several cut points ranging from 200 mg/dl to 260 mg/dl (Table 3). Among women, serum ascorbic acid remained significantly associated with HDL-C level in all multivariate models; each 1 mg/dl increase was associated with an approximately 2 to 3 mg/dl increase in HDL-C level (all p<=0.05). Serum ascorbic acid was not significantly associated with any other serum lipid or lipoprotein level, regardless of the cut point examined.


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  		Table 3. Difference in Serum Lipid and Lipoprotein Level (in mg/dl) for Each 1 mg/dl Increase in Serum Vitamin C Level among Participants with Total Cholesterol (TC) Levels >=200 mg/dl*

 

   DISCUSSION
 
Our main and most consistent finding was the independent association between serum ascorbic acid levels and serum HDL-C levels among women. This association was apparent even after controlling for the effects of dietary fat, cholesterol, and energy intake, as well as body mass index, alcohol consumption, smoking, physical activity, menopausal status, and use of oral contraceptives and hormones. The relation between serum ascorbic acid level and higher levels of HDL-C was present in all subgroups of women that we analyzed. These findings agree with those of several observational studies [19–21,34,35] and experimental studies among humans [18,36,37], but have not been observed uniformly [38–42]. We also examined NHANES II participants with elevated total serum cholesterol levels (>=200 mg/dl) because other investigators have reported that ascorbic acid administration may lower blood cholesterol levels in such individuals [43]. No significant relation was observed between serum ascorbic acid level and serum lipid levels in women or men.

In experimental animals, ascorbic acid is an important factor in cholesterol homeostasis [44]. A number of studies have reported that ascorbic acid administration lowers blood cholesterol levels in the guinea pig, an animal that like humans lacks the enzyme required for the hepatic synthesis of ascorbic acid [13–15]. Experiments in the guinea pig have shown that ascorbic acid is necessary in the rate-limiting step in the conversion of cholesterol to bile acids; the hepatic concentration of ascorbic acid affects the rate of cholesterol catabolism [5–7,45]. Other animal studies have reported that ascorbic acid administration attenuates the expected rise in serum cholesterol after cholesterol-feeding [9–12], increases LDL receptors [46], and may mobilize cholesterol from body stores [11,13,47–49].

Human studies examining the relation between ascorbic acid and serum lipids have been inconsistent [44]. One possible explanation for the inconsistent findings is that ascorbic acid lowers total serum cholesterol levels only among individuals with elevated cholesterol levels who have less than full tissue saturation of ascorbic acid [44]. Several studies have found that the administration of ascorbic acid to individuals with elevated total serum cholesterol levels (>200 mg/dl) lowers total serum cholesterol levels [40,43,50], particularly in individuals with less than full tissue saturation of ascorbic acid at baseline [50,51]. For individuals with total serum cholesterol levels <200 mg/dl, the administration of ascorbic acid does not produce a consistent effect. We, however, were unable to detect any significant inverse relation between serum ascorbic acid level and serum LDL-C, total cholesterol, and triglycerides in four subgroups with total serum cholesterol levels >200 mg/dl.

There are alternative explanations for our findings. Because we performed many comparisons, it is possible that some of the observed associations were the result of chance. A chance association seems unlikely to account for the relation between serum ascorbic acid level and HDL-C level among women in view of the strength and consistency of the findings. Serum ascorbic acid levels were consistently associated with higher HDL-C levels among women, even after adjustment for potential confounders. Although we controlled for the effect of many potential confounders including physical activity and level of education, we cannot exclude the possibility that serum ascorbic acid level is a healthy lifestyle marker for women. Finally, our study was a cross-sectional analysis and inferences about causality should be made cautiously. Our study has, however, two noteworthy strengths. The findings should be generalizable to the US population and most important, the measurement of serum ascorbic acid levels allows for a better estimate of ascorbic acid status compared with studies using dietary intake estimations only.


   CONCLUSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 CONCLUSION
ACKNOWLEDGMENTS
 REFERENCES
 
Although the results of our study should be interpreted cautiously, they do support prior evidence linking ascorbic acid with cholesterol homeostasis among women [52]. If increased ascorbic acid intake is related causally to higher HDL-C levels in women, it could be of potential importance for the prevention of coronary heart disease.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
REFERENCES
 
This study was supported by Public Health Service grant HL53479 and a research grant from Hoffmann-La Roche, Inc. We gratefully acknowledge Dr. Warren Browner for his comments and suggestions.

Received April 1, 1997. Accepted September 1, 1997.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 CONCLUSION
 ACKNOWLEDGMENTS
 REFERENCES
 

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