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Arteriosclerosis, Thrombosis, and Vascular Biology. 1997;17:820-825

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(Arteriosclerosis, Thrombosis, and Vascular Biology. 1997;17:820-825.)
© 1997 American Heart Association, Inc.

Articles

Associations Between Diet and the Hyperapobetalipoproteinemia Phenotype Expression in Children and Young Adults

The Cardiovascular Risk in Young Finns Study

Ilpo O. Nuotio; Olli T. Raitakari; Kimmo V.K. Porkka; Leena Räsänen; Teemu Moilanen; ; Jorma S.A. Viikari

From the Department of Medicine (I.O.N, J.S.A.V.), the Cardiorespiratory Research Unit (I.O.N), and the Department of Clinical Physiology, University of Turku (O.T.R.); the Department of Medicine (K.V.K.P.) and the Division of Nutrition, University of Helsinki (L.R.); and the Medical School, University of Tampere and Tampere University Hospital (T.M.), Finland.

Correspondence to Ilpo O. Nuotio, MD, Cardiorespiratory Research Unit, University of Turku, Kiinamyllynkatu 10, FIN-20520 Turku, Finland. E-mail ilpo.nuotio{at}ktl.fi


*    Abstract
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 *Abstract
down arrowIntroduction
 down arrowMethods
 down arrowResults
 down arrowDiscussion
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Abstract The effect of diet on blood lipids has been under intensive study during recent decades. However, diet in the context of the hyperapobetalipoproteinemia (hyperapoB) phenotype has received less attention. The hyperapoB phenotype is commonly encountered in patients with premature coronary heart disease. It is defined as a combination of an increased concentration of apolipoprotein B (apo B), a normal concentration of LDL cholesterol (LDL-C), and as a result, a low LDL-C/apo B ratio. We studied the associations between diet and blood lipids in a cohort of 534 children and young adults 9 to 24 years old. The ratio of polyunsaturated to saturated fats (P/S ratio) correlated (r=-0.19, P<.001) with the LDL-C/apo B ratio. This association was also found when the model was adjusted with triglycerides (r=-0.24, P<.001). A change in the P/S ratio from 0.10 to 0.60 corresponded to a decrease of 0.12 in the LDL-C/apo B ratio, and in the highest apo B decile, the P/S value was higher in hyperapoB individuals (0.33) than in others (0.28, P=.019). Our results imply that the fatty acid composition of the diet may be one of the environmental factors that influence the hyperapoB phenotype expression.


Key Words: diet • lipids • hyperapobetalipoproteinemia • serum fatty acids • lipoproteins


*    Introduction
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 *Introduction
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The hyperapoB phenotype is commonly encountered in patients with premature coronary heart disease.1 2 3 It is defined as a combination of an increased concentration of LDL apo B and a normal concentration of LDL-C,1 resulting in a low ratio of LDL-C to LDL apo B.4 5 High triglyceride values, low HDL-C values, and expression of the small, dense LDL particle are often seen in hyperapoB patients.4 6 7 It is regarded as a familial lipoprotein disorder, although the genetic basis is probably heterogeneous.5 8 However, environmental factors also are associated with hyperapoB phenotype. We have recently shown that oral contraceptive use and alcohol consumption are associated with hyperapoB phenotype expression.9 In addition, many factors that raise the triglyceride level are probably associated with hyperapoB phenotype expression as well as with that of the small, dense LDL particle phenotype.9 10

The effect of diet on lipid values has been intensively studied in the past four decades.11 12 Common findings have been the cholesterol-increasing effect of SFAs and the cholesterol-decreasing effect of the PUFAs.11 12 Carbohydrates and especially saccharose in the diet have caused high triglyceride values,13 14 whereas PUFAs in the diet have lowered triglyceride levels.11 More recently, SFAs have also been associated with LDL particle size.15 In animal studies, PUFAs have decreased the LDL size,16 17 18 and the composition of LDL particles has changed to contain less cholesterol and more protein.17 18 19 The close association between the small, dense LDL particle and hyperapoB, as well as their common lipid determinants, therefore implied that dietary fat might also be associated with hyperapoB phenotype expression. Because triglycerides associate with both the small, dense LDL particle and the hyperapoB phenotype, the carbohydrates were also of interest.


*    Methods
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 *Methods
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The Cardiovascular Risk in Young Finns Study is a multicenter follow-up study of atherosclerosis precursors in Finnish children and young adults.20 21 A total of 3596 subjects, 3, 6, 9, 12, 15, and 18 years old, participated in the main cross-sectional study in 1980. Equal numbers of boys and girls, rural and urban, and eastern and western Finns were recruited, and they were chosen in a random fashion from the national population register. For the present study, all subjects (n=534) with complete data on serum lipids, apolipoproteins, anthropometric variables, and diet were selected from the second follow-up study year, 1986. The representativeness of the subpopulation participating in the 1986 dietary survey has been reported earlier.22 As in the earlier reports of the Cardiovascular Risk in Young Finns Study,23 in this study the subjects lost to follow-up were older and tended to have a higher BMI.

All lipid measurements were done in the laboratory of the Research and Development Center of the Social Insurance Institution (Turku, Finland), which continuously cross-checks the accuracy, precision, and between- and within-run variability of serum lipid determinations with the WHO reference laboratory. All venous blood samples were taken after 12 hours of fasting. Standard enzymatic methods were used for the determination of serum cholesterol (Boehringer CHOD-PAP) and triglycerides (Boehringer). Serum HDL cholesterol was measured from the serum supernatant after precipitation of VLDLs and LDLs with dextran sulfate (DS-500) and MgCl2.24 The concentration of LDL-C was calculated by the Friedewald formula.25 Apos A-I and B were determined by immunoturbidimetry.26 The serum cholesteryl ester fatty acid composition was analyzed with a gas chromatograph (Hewlett-Packard Co) equipped with an OV-351 fused silica capillary column (Nordion Instruments).27 Height was measured by Seca anthropometer and weight by Seca weighing scale. BMI was calculated from the formula BMI=weight (kg)/[height (m)]2. Diet was assessed with the 48-hour recall method.28

The following dietary variables were used in the analyses: daily energy; the values of protein, carbohydrates, saccharose, and fat expressed as percentages of total energy intake; the values of PUFAs, MUFAs, and SFAs expressed as mass per 1000 kcal; the P/S ratio; and the cholesterol mass per 1000 kcal. In the LDL-C/apo B ratio, the levels of LDL-C were transformed to grams per liter. The lipid values were standardized to age- and sex-specific Fisher's z scores by extracting the mean and dividing by the SD in each given sex/age group.29 Loge transformation was applied in regression analyses to triglycerides, the P/S ratio, and the diet percentage of saccharose.

Statistical analyses were performed with version 6.10 of the SAS software.29 Comparisons between sexes were made with the Wilcoxon test for nonparametric and Student's t test for parametric data. The associations between diet, serum cholesteryl ester fatty acids, and standardized lipid variables were measured by the Spearman rank-order correlation coefficient with partial correlation analyses of apo B and the LDL-C/ apo B ratio. Differences between the P/S ratio groups and the saccharose groups were evaluated with ANOVA and ANCOVA after evaluations with the Bonferroni test in multiple comparisons of groups. The relationships between apo B, the LDL-C/ apo B ratio, saccharose, and the P/S ratio were subsequently studied with multiple linear regression, and the stepwise selection technique was used, with a significance level of 0.15 as the model entry criterion. The independent variables were sex, age, BMI, and those chosen on the basis of Spearman's correlations results.

The LDL-C and apo B percentile points (90th age- and sex-specific percentiles) were generated from the maximal available combined LDL-C and apo B data (n=1137) of the follow-up study year, 1986. On the basis of these percentile values, all subjects were classified into three groups: normal apo B (apo B <90th age- and sex-specific percentile), hyperapoB (apo B >=90th but LDL-C <90th age- and sex-specific percentile), and the high LDL-C/high apo B group (both LDL-C and apo B >=90th age- and sex-specific percentile). In the highest apo B decile, the differences in the P/S ratios and energy percentages of saccharose were studied with the Wilcoxon test between the hyperapoB group and the high LDL-C/high apo B group.


*    Results
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In females (Table 1Down), the serum lipid values were higher than in males, with the exception of LDL-C/apo B ratios. Males (Table 2Down) consumed more energy, and higher percentages of this energy were derived from protein, fat, PUFAs, and MUFAs. Females consumed relatively more carbohydrates and saccharose than males.


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  		Table 1. Clinical Characteristics of the Subjects


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  		Table 2. Composition of the Diet

In the total population, carbohydrates correlated (Table 3Down) negatively with total, LDL, and HDL cholesterol as well as with apolipoprotein A-I values and positively with triglycerides. The intake of saccharose behaved similarly, although the correlations with HDL-C and apo A-I were insignificant. PUFAs correlated negatively and SFAs correlated positively with total and LDL cholesterol values. In addition, the intake of SFAs correlated positively with HDL-C and apo A-I.


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  		Table 3. Spearman's Correlation Coefficients and Partial% Correlation Coefficients Between Dietary Variables and the Standardized§ Serum Lipids/Lipoproteins

The two factors composing the hyperapoB definition criteria (high apo B and low LDL-C/apo B ratio) were also associated with diet. Unadjusted values of apo B showed only a negative correlation with the P/S ratio. However, the LDL-C/apo B ratio was associated with several factors. Carbohydrates, saccharose, PUFAs, and the P/S ratio correlated negatively with the LDL-C/ apo B ratio. The percentages of total fat and SFAs correlated positively with the LDL-C/apo B ratio.

Since the total apo B values were influenced by triglyceride-carrying molecules (VLDL and IDL), the correlations were also studied with adjustment to triglyceride values (Table 3Up). In this manner, correlations to LDL apo B could also be estimated. This procedure revealed the negative correlation of carbohydrates and saccharose to apo B values. It also showed the positive correlation of total and saturated fat to apo B values. The association of carbohydrates with the LDL-C/apo B ratio disappeared, and the association of saccharose became weaker. However, the correlations between the dietary fat variables and the LDL-C/apo B ratio were unchanged. In both sexes, PUFAs and the P/S ratio correlated negatively and SFAs correlated positively with the LDL-C/apo B ratio.

The correlation between the P/S ratio and the LDL-C ratio was also studied in the highest and lowest apo B quartiles separately. No significant correlations were observed between apo B and the dietary fat values in these groups. However, in the highest apo B quartile, the correlation between the P/S ratio and the LDL-C/ apo B ratio differed (r=-.09, P=NS) from the correlation in the lowest apo B quartile (r=-.25, P<.01). The adjustment to triglyceride values reduced this difference (r=.18, P<.05 and r=.28, P<.01 for top and bottom quartiles, respectively). In addition, when the highest apo B quartile was limited to the percentile values 75% to 97.5%, there were no differences between the top and bottom quartiles regarding the triglyceride-adjusted correlations between the P/S ratio and the LDL-C/apo B ratio (r=.27, P<.01 and r=.28, P<.01 for top and bottom quartiles).

A correlation matrix (Table 4Down) was produced with the serum cholesteryl ester fatty acid values and the serum lipid values. Serum cholesteryl ester SFAs, MUFAs, and {omega}-3 PUFAs correlated positively and {omega}-6 PUFAs correlated negatively with the LDL-C/apo B ratio. Since correlations also existed with the triglycerides, these associations were revealed after adjustment to triglycerides. The dietary P/S ratio and serum cholesteryl ester SFAs, MUFAs, and {omega}-3–series PUFAs correlated negatively with the serum cholesteryl ester linoleic acid ({omega}-6 PUFA), which composed half of the cholesteryl ester fatty acids (mean, 51%; range, 38% to 66%).


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  		Table 4. Spearman's Correlation Coefficients and Partial% Correlation Coefficients Between Serum Cholesteryl Ester Fatty Acids and the Standardized§ Serum Lipids/Lipoproteins

The associations between the P/S ratio, apo B, and the LDL-C/apo B ratio were further evaluated by means of seven discrete P/S ratio groups (Table 5Down). The change in the P/S ratio mean from 0.15 to 0.55 corresponded to a decrease of 0.12 in the LDL-C/apo B ratio mean. Similarly, the associations between saccharose, apo B, and LDL-C/apo B were studied by means of six discrete saccharose groups (Table 6Down). The change in dietary saccharose mean from 6% to 18% corresponded to a decrease of 0.12 in the LDL-C/apo B ratio mean. There were no clear changes in apo B values between the P/S ratio groups or the saccharose groups.


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  		Table 5. Characteristics by Different P/S Ratio Groups


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  		Table 6. Characteristics by Different Saccharose Groups

The relations between the P/S ratio and saccharose percentage with the LDL-C/apo B ratio were also studied with linear regression analyses (Table 7Down). In the regression model, a change in the P/S ratio from 0.10 to 0.60 (percentile points 3% and 94%, respectively) corresponded to a decrease of 0.12 in the LDL-C/apo B ratio. The change in the percentage of saccharose in daily energy from 3% to 23% (percentile points 2.5% and 95%, respectively) similarly corresponded to a decrease of 0.11 in the LDL-C/apo B ratio. However, the inclusion of triglycerides in the model caused only minor changes in the R2 and the ß values of the P/S ratio (ß=-.064, R2=2.5%, P<.001) but substantially decreased the significance, the R2, and the coefficient ß of the saccharose percentage (ß=-.024, R2=0.3%, P=.102).


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  		Table 7. Stepwise Multiple Linear Regression Analyses: Changes in Apo B Level and LDL-C/Apo B Ratio Are Predicted From a Change in a Single Correlate

The validity of the regression model in the highest apo B decile was then tested between two groups: (1) the hyperapoB group (apo B>=90 and LDL-C<90th age- and sex-specific percentile) and (2) the high apo B and high LDL-C group (both apo B and LDL-C >=90 age- and sex-specific percentile). The Wilcoxon probability value was .019 (P/S ratio=0.33 and 0.28 in hyperapoB and high LDL-C/high apo B groups). Similar comparison with the saccharose percentage gave an insignificant probability value (P=.204).


*    Discussion
up arrowTop
 up arrowAbstract
 up arrowIntroduction
 up arrowMethods
 up arrowResults
 *Discussion
down arrowReferences
 
The associations between diet and hyperapoB phenotype expression have not been reported previously. In this study, the main findings were the associations of dietary SFAs, PUFAs, and the P/S ratio with the LDL-C/ apo B ratio. Similar associations were seen between serum cholesteryl SFAs, serum cholesteryl PUFAs, and the LDL-C/apo B ratio. Saccharose consumption was associated with the LDL-C/apo B ratio, and this relation was partly dependent on the triglyceride values. The change from 0.10 to 0.60 in the P/S ratio corresponded to a decrease of 0.12 in the LDL-C/apo B ratio in linear regression analysis and, in the highest apo B decile, the P/S ratio mean was higher in hyperapoB individuals than in others. When the highest and lowest apo B quartiles were studied separately, there seemed to be differences in correlations between the P/S ratio and the LDL-C/ apo B ratio. These differences were most likely due to the existence of mainly genetically determined high lipid/lipoprotein values in the highest apo B percentile points.

In this study and in common clinical practice, the apo B assay measures total apo B instead of LDL apo B.30 Total apo B is the sum of VLDL, IDL, and LDL apo B. IDL and especially VLDL are in turn the major carriers of triglycerides; therefore, individuals with high total apo B values are likely to have higher triglyceride values than individuals with only high LDL apo B values. However, the association between coronary heart disease and hyperapoB has been the same regardless of the apo B assay,2 3 and the overproduced particle in hyperapoB is, in fact, VLDL.31 Moreover, there are at the moment no reports evaluating the difference in apo B assays in hyperapoB. Therefore, some comparability between studies using total apo B or LDL apo B is lost, but the possible advantage of either apo B assay method cannot be evaluated at this time. However, all the models in this study were repeated with the triglyceride adjustment, which should also show the triglyceride- and VLDL-independent changes in the apo B level and the LDL-C/apo B ratio.

In experimental studies, carbohydrates and especially saccharose have increased triglyceride levels.11 13 14 Since the LDL-C/apo B ratio is linearly negatively correlated with the triglyceride levels,9 32 the negative association of carbohydrates with the LDL-C/apo B ratio was expected. This association was reduced when triglycerides were added to the model, and the negative relations with the apo B level were also revealed. The changes suggested that carbohydrates raised the VLDL apo B and lowered the LDL apo B level. Although the magnitude of the estimated decrease in the LDL-C/apo B ratio was almost of the same size as the estimated decrease associated with the change in the P/S ratio, no significant difference could be seen in the highest decile of apo B between the hyperapoB group and the rest. Therefore, the relation between the saccharose intake and the hyperapoB phenotype expression remains open.

In general, dietary SFAs (12:0, 14:0, and 16:0) increase and PUFAs decrease the LDL-C level in comparison with carbohydrates,11 12 whereas triglycerides are lowered by fat, especially by the {omega}-3–series PUFAs.11 12 Our findings also suggest that PUFAs decrease and SFAs increase more LDL-C than LDL apo B, the P/S ratio being the strongest indicator of this action. In addition, the serum cholesteryl ester fatty acids correlated similarly, although there were inconsistencies in the associations of triglycerides, the behavior of MUFAs, and the {omega}-3 PUFAs. These serum cholesteryl ester fatty acids probably reflect a variety of dietary items and not only the dietary fat composition. Much of the stearic acid (SFA) is rapidly converted to oleic acid (MUFA),33 and therefore, a part of the serum cholesteryl ester MUFAs can be derived from the SFAs. In addition, it has been speculated that the {omega}-6 PUFAs competitively displace the {omega}-3 PUFAs in the serum fatty acid pool.34

When the P/S ratio variable is used, the differing actions of 18:0 SFAs, MUFAs, and different types of PUFAs are ignored. In intervention studies, dietary variables reflect the intraindividual change in values. In our population-based study, there are no intraindividual changes, and the correlations of the different dietary percentage values mirror the sum of a change in one element and the simultaneous alterations in others. This may also explain some of the discrepancies in the serum cholesteryl ester fatty acid correlations. Since most of the other fatty acids correlate negatively with the linoleic acid, their positive correlation with the LDL-C/apo B ratio can be considered merely a reflection of the change in the linoleic acid concentration. Therefore, the consideration of counterparts, eg, PUFAs on SFAs or linoleic acid on the others, may be a relevant viewpoint in this cross-sectional population study. However, our findings do not exclude the possibility of substantial differences between individuals in response to the various dietary elements.

The variation at the plasma level in the LDL-C/apo B ratio may be seen in the changes in LDL particle composition. In animal studies, PUFAs have changed the LDL particle composition to contain less cholesterol and more protein17 18 19 and the LDL particle size has decreased.16 17 18 In human studies, the P/S ratio has been associated with lower small LDL mass,35 PUFAs have induced no change in the cholesterol/protein ratio in LDL36 or they have diminished the cholesterol/protein ratio,37 38 and SFAs have been associated with greater LDL particle size.15 The strongest relations of particle size have been reported to be with the free cholesterol concentration of the LDL particle,39 the plasma total triglyceride level,10 40 and others.41 42 Therefore, the LDL-C/apo B ratio does not necessarily correlate directly with the particle size, but similar changes in the LDL particle composition and in the LDL-C/apo B ratio are to be expected.

Some individuals who express the hyperapoB phenotype have a familial form of hyperapoB.3 This phenotype has been associated with other disease entities, eg, familial combined hyperlipidemia, diabetes, hypertension, and others.2 5 8 Its genetic basis is heterogeneous, and the definition criteria are probably in evolution.5 8 However, even though more precise diagnostic tools can be expected in the future,43 44 the two diagnostic criteria, high apo B level and low LDL-C/apo B ratio, are likely to remain in some use, eg, in preliminary screening of possibly affected individuals. Therefore, it is valuable to recognize the possible confounders that may cause individuals to express the hyperapoB phenotype. Our results suggest that the changes in the fatty acid composition of the diet may affect the hyperapoB phenotype expression.


*    Selected Abbreviations and Acronyms
 
apo = apolipoprotein
BMI = body mass index
HDL-C = HDL cholesterol
hyperapoB = hyperapobetalipoproteinemia
LDL-C = LDL cholesterol
MUFA = monounsaturated fatty acid
P/S ratio = ratio of polyunsaturated to saturated fatty acids
PUFA = polyunsaturated fatty acid
SFA = saturated fatty acid


*    Acknowledgments
 
This study was supported by grants from the Sigrid Juselius Foundation, the Medical Research Council of the Academy of Finland, the Ida Montin Foundation, and the University of Turku Foundation.

Received September 2, 1996; accepted September 9, 1996.


*    References
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 up arrowDiscussion
 *References
 

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