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* Departments of Family and Preventive Medicine, Reproductive Medicine, and Medicine, University of California, San Diego, CA;
Arizona Cancer Center, University of Arizona, Tucson, AZ;
** Stanford Center for Research in Disease Prevention, Stanford University; and
MD Anderson Cancer Center, University of Texas, Houston, TX
2To whom correspondence should be addressed. E-mail: clrock{at}ucsd.edu.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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KEY WORDS: • carbohydrate • dietary fat • triacylglycerol • diet intervention • cancer
The relation between dietary fat intake and the risk and progression of breast cancer has been the focus of numerous observational studies (1). Diet intervention trials are currently testing whether reduced intake of dietary fat can reduce risk for primary breast cancer (2), and whether postdiagnosis dietary modification can reduce risk for cancer recurrence (3,4). Energy from carbohydrate has replaced energy from fat in the diet in response to efforts to promote reduced fat intake in the intervention studies targeting breast cancer survivors (4,5).
In the analysis of the results of these studies, an important question is whether the intervention efforts successfully achieve a reduction in fat intake. The interpretation of self-reported data on dietary intakes collected using available methodologies (including dietary records, recalls, and FFQ) is constrained by several well-described limitations (6–8). In diet intervention trials, repeated dietary assessment and monitoring may affect the accuracy of reported intakes, and participants who are the focus of intervention efforts may be more likely to report diets in agreement with the goals of the intervention. Thus, dietary biomarkers can be useful to further define exposures and adherence (9).
A specific biological marker of total fat intake has not been identified or established (10). However, altering the proportion of energy intake from carbohydrate and fat has been shown to affect fasting plasma triacylglycerol concentration in numerous controlled feeding studies (11,12). Further, the magnitude of change in carbohydrate and fat intakes that promotes a change in triacylglycerol concentration in these studies appears to encompass the range being tested for effect on disease outcome in the intervention trials. In cross-sectional studies, lower levels of fat intake (13) and higher levels of carbohydrate intake (14) were associated with increased fasting plasma triacylglycerol concentrations in population-based cohorts. Also, HDL cholesterol concentration exhibited an inverse relation with carbohydrate intake and a direct relation with fat intake in several observational studies (11–14).
Several factors may influence the usefulness of these nonspecific markers of change in the relative intakes of carbohydrate and fat. As reviewed by Parks and Hellerstein (11), the majority of the clinical studies demonstrating the effect of modifying carbohydrate and fat intakes on plasma triacylglycerol and HDL cholesterol concentrations involved small numbers of subjects who were examined over a relatively short period of time, using formula diets rather than regular whole food and usual eating patterns. In addition, the effect of increasing carbohydrate intake on these lipids was shown to be modified by dietary fiber (11), which is often concurrently increased in association with guidance toward reduced fat intake in diet intervention trials (5), as well as by the type of carbohydrate consumed. Further, subject characteristics, such as age, degree of adiposity, baseline plasma triacylglycerol concentration, and degree of insulin resistance, may influence the lipid response to replacing fat with carbohydrate in the diet.
The purpose of this study was to examine the effect of intervention efforts promoting a low-fat diet on selected plasma lipid concentrations in subjects participating in a randomized, controlled trial to test the effect of diet on risk for recurrence and overall survival in women previously treated for breast cancer. The dietary goals for the intervention group in this study included a reduction in dietary fat intake and increased intakes of dietary fiber, vegetables, and fruit. We hypothesized that participants in the intervention group would exhibit increased fasting plasma triacylglycerol and reduced HDL cholesterol concentrations at 1 y postrandomization in response to the intervention efforts, reflecting a reduction in fat intake and an increase in carbohydrate intake.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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50 y old at enrollment and the first 100 women who were >50 y old. Additionally, women were selected who had not changed their tamoxifen usage from baseline to 12 mo; thus, tamoxifen use remained constant over the time period of interest. This medication is known to alter plasma lipid concentrations and thus could interfere with the analysis. None of the women in this study had been prescribed insulin for control of diabetes because this was an exclusion criterion for participation in the WHEL Study (3). Six women were subsequently dropped from this analysis due to insufficient data, and one woman was excluded as an outlier because she had a baseline triacylglycerol concentration that was more than five times the SD.
Procedures.
Participants were randomly assigned to 1 of 2 study groups, stratified by stage of disease, age, and clinic site. The comparison group was advised to consume a diet consistent with current general dietary recommendations for cancer prevention (5 servings of vegetables and fruit daily, 20 g fiber/d, and 30% energy from fat). The intervention group was encouraged to consume 5 vegetable servings/d, 3 fruit servings/d, 480 mL vegetable juice/d, 30 g fiber/d, and 15–20% energy from fat. Dietary recommendations provided to both groups were consistent with current recommendations to control blood lipids. An intensive telephone-based diet counseling program, 12 group cooking classes, and printed materials were used to achieve diet modification in the intervention group (3). The participants in the comparison group were invited to attend 4 cooking classes unrelated to the intervention targets and were provided standard dietary guidance materials available from governmental agency sources (3).
Relevant to this substudy, the protocol involved clinic visits at enrollment and 1 y, during which a fasting blood sample was collected, height and weight were measured using standard procedures, and BMI (kg/m2) was computed.
Dietary and physical activity data. The primary method of dietary assessment in this study consisted of repeated 24-h dietary recalls. Details regarding this dietary assessment methodology are described elsewhere (3,15). Briefly, each study participant provided four 24-h dietary recalls including two weekdays and two weekend days over a 3-wk period. Trained dietary assessors, who were unaware of the intervention or comparison group assignment of the participants, collected these data during telephone interviews. Nutrient calculations were performed using the Nutrition Data System for Research software, developed by Nutrition Coordinating Center, University of Minnesota (Food and Nutrient Database 31, version 4.03, released November 2000).
At baseline and 1 y, the frequency, duration, and intensity of physical activity were assessed by questionnaire and converted into metabolic equivalents (METs). Total energy expenditure was obtained by weighting time spent per week by METs: mild physical activity was weighted 3 METs, moderate activity was weighted 5 METs, and vigorous activity was weighted 8 METs. Walking METs were assigned by walking speed. Unknown speed or 3.33 km/h (2 mph) walking was weighted 2 METs, 5 km/h (3 mph) walking was weighted 3 METs, 6.67 km/h (4 mph) walking was weighted 4 METs, and 
8.33 km/h (5 mph) walking was weighted 6 METs (16). METs were not assigned for hours spent sitting or sleeping.
Biochemical measurements. Blood samples collected were immediately placed on ice, protected from light, and separated within 1 h after collection, using centrifugation at 2300 x g at 4°C for 10 min. Aliquots of plasma and serum were stored at -80°C in cryogenic tubes until analysis.
Measurements of lipids were performed using an Abbott VP instrument (Abbott Laboratories) as described in the Lipid Research Clinic Manual of Laboratory Operations (17). The interassay CV was 0.8% for total cholesterol, 1.7% for total triglycerides, and 2.4% for HDL cholesterol. Apoprotein (apo)-A1, apo-B and lipoprotein (a) were determined by automated analysis using a Roche COBAS BIO instrument (Basel, Switzerland) with kits (#86111, #86070, and #86071, respectively) from Diasorin. LDL cholesterol values were calculated by the Friedewald equation (18). LDL cholesterol could not be calculated for 7 subjects because triacylglycerol concentration was >4.516 mmol/L in these cases and the equation is not valid under those circumstances (19,20). Thus, the final sample size is 393 for triacylglycerol and HDL cholesterol analysis and 386 for LDL cholesterol analysis.
We also examined fasting serum insulin concentration as a surrogate for insulin resistance (21). A double antibody RIA, with <0.2% cross-reactivity with human proinsulin, was used for the analysis of insulin (Linco Research). The intra-assay CV was 3.2%, and the interassay CV was 3.9%. Data on serum insulin concentration were not available for 2 subjects due to aliquot limitations.
Statistical analysis. Dietary values were log-transformed to ensure that they conformed to the Shapiro-Wilk test for normality, and paired t tests were conducted to examine changes in dietary intakes from baseline to 12 mo in the two study groups. Some of the plasma measurements (e.g., triacylglycerol, insulin) were not adequately normalized by log transformation. Therefore, differences between plasma lipids, lipoproteins, and insulin from baseline to 12 mo in the two study groups were tested using the Wilcoxon signed rank test on log-transformed values in each of the two study groups. The symmetry of the distributions was verified using quantile-quantile plots. Linear regression was used to analyze 12-mo triacylglycerol concentration as a function of the percentage of energy from fat, percentage of energy from carbohydrate, starch to sugar ratio (as a percentage of total carbohydrate), dietary fiber intake, age, BMI, degree of weight change, and baseline triacylglycerol and 12-mo fasting insulin concentrations. All analyses were performed using the Statistical Analysis System (version 8.01, 1999, SAS Institute).
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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In women who lost weight, this factor influenced the plasma triacylglycerol response. Women in the comparison group who lost 5% of initial body weight from baseline to 1 y (n = 20) exhibited a significant decrease in plasma triacylglycerol concentration (P < 0.05). Women in the intervention group who lost 5% of initial body weight from baseline to 1 y (n = 26) did not exhibit any change in plasma triacylglycerol concentration, suggesting that concurrent weight loss attenuated the effect of change in diet composition on response (data not shown).
In a linear regression analysis for 12-mo plasma triacylglycerol concentration, the percentage of energy from carbohydrate was a significant predictor of triacylglycerol concentration, but the percentage of energy from fat, the starch to sugar ratio, and fiber intake did not independently contribute to the variance (Table 4). As anticipated, plasma triacylglycerol concentration at enrollment was a significant predictor of the concentration at 12 mo. Also, triacylglycerol concentration was significantly associated with serum fasting insulin concentration and weight loss.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The identification of dietary biomarkers is currently considered an important research goal for nutritional epidemiology (23). These dietary biomarkers are particularly meaningful in intervention studies, because adherence is a crucial issue in the interpretation of the observed effect of the intervention on disease outcomes. The effect of reduced fat intake on breast cancer outcomes is currently being examined in clinical trials (2–4), and the identification and refinement of biological indicators relevant to fat and carbohydrate intakes would be useful. As validated by substantially increased plasma carotenoid concentrations (24–26), the WHEL Study diet intervention efforts were shown previously to result in a major increase in vegetable and fruit intake.
Increased plasma triacylglycerol and reduced HDL concentrations were observed quite consistently in response to increased carbohydrate and reduced fat intakes in controlled feeding studies in which energy balance was held constant (11,12). However, many issues relating to these lipid responses are still unresolved. The controlled feeding studies have predominantly involved formula feeding (rather than regular food) and have been of short duration (11). Other dietary factors (e.g., fiber, type of carbohydrate), weight loss despite efforts to achieve an isocaloric comparison, and various subject characteristics influence the response. Even in the studies in which subjects consumed regular whole foods rather than formula diets, the magnitude of the difference between the high-fat, low-carbohydrate and low-fat, high-carbohydrate conditions in these studies has typically been very large (11,12). This might suggest limited relevance to smaller changes in diet composition that are achievable and sustainable as a result of intervention efforts in disease prevention studies. For example, Parks et al. (27) observed a 60% increase in triacylglycerol concentration at 5 wk in response to a low-fat (15% of energy), high-carbohydrate (68% of energy) diet compared with a control diet (35% energy from fat, 50% energy from carbohydrate) based on whole foods, in which mono- and disaccharides were limited to 44% of energy and fiber was increased from 30 to 45 g/d during the experimental period. In other studies characterized by free-living subjects, regular whole foods, and increased dietary fiber, concurrent weight loss is often a confounding factor. Turley et al. (28) examined the effects of a self-selected high-fat (36% energy from fat, 43% energy from carbohydrate) and a low-fat (22% energy from fat, 59% energy from carbohydrate) diet on serum lipids in a 12-wk crossover study involving 38 men with moderately elevated serum total cholesterol concentration. Similar to the present study, the subjects in that study were advised to replace fat with carbohydrate from grains, vegetables, legumes, and fruit, although the subject characteristics were very different. Their intervention resulted in a mean weight loss of 1.5 kg and a 14% reduction in energy from fat, which was associated with a marginally significant reduction in HDL cholesterol concentration and no change in plasma triacylglycerol concentration.
In the present study, we detected a change in plasma triacylglycerol, HDL cholesterol, and apo-A1 concentrations in response to a 7% reduction in energy from fat and an 8% increase in energy from carbohydrate, in a target group in which most subjects did not exhibit weight loss. The women in this study generally had a favorable lipid profile at enrollment (22), and changes of a large magnitude in plasma lipid concentrations were not anticipated.
Increased dietary fiber intake may have attenuated the plasma lipid response to increased carbohydrate intake in the present study, although the study was not designed to specifically test this effect. We did not identify an independent relation between fiber intake and plasma triacylglycerol concentration when considering the effect of other influencing factors in regression analysis. This suggests that increased plasma triacylglycerol concentration occurs in response to increased carbohydrate intake in spite of concurrently increased dietary fiber, as observed in controlled feeding studies (27). It has been suggested that minimizing intake of mono- and disaccharides may reduce the likelihood of increased triacylglycerol concentration in response to increased carbohydrate intake (11). Although the intervention group subjects reported a small but significant increase in the percentage of energy from mono- and disaccharides, these dietary constituents still contributed only 30% of total energy, and the change in the proportionate contribution of starch and sugars to total carbohydrate intake was relatively small. Another potentially influencing dietary factor is fish oil consumption, which has been shown to reduce plasma triacylglycerol concentration (29). In the present study, intakes of the major subtypes of dietary fat declined in response to the intervention, concurrent with the reduction in total fat intake (data not shown). However, change in carbohydrate intake (rather than change in fat intake) was the dietary factor that exhibited the strongest independent relation with plasma triacylglycerol concentration in the regression analysis that considered other influencing factors.
The relations between carbohydrate or fat intake and fasting triacylglycerol and HDL cholesterol concentrations have been examined in several cohorts in cross-sectional analysis (12). For example, fat intake was inversely associated with fasting plasma triacylglycerol concentration, adjusted for age, smoking status, alcohol consumption, physical activity, BMI, and energy intake, in 269 men in the Health Professionals Follow-up Study (13). More recently, Liu et al. (14) found carbohydrate intake to be directly related to fasting triacylglycerol concentration (but unrelated to HDL cholesterol concentration) in a sample of 280 women in the Nurses’ Health Study, using similar adjustment variables. The present study moves the development of this lipid pattern as a biological indicator of carbohydrate and fat intake one step further. These previous epidemiologic studies involved cross-sectional analysis, but the responsiveness of a dietary biomarker to change in diet composition is an important characteristic for intervention studies, and this was observed in the present study.
As expected, we identified an independent effect of weight loss on plasma triacylglycerol concentration in the women who lost weight. We also found baseline plasma triacylglycerol concentration and fasting serum insulin concentration to relate independently to triacylglycerol concentration after the low-fat diet intervention. In previous studies of healthy women, the degree of increase in triacylglycerol concentration in response to increased carbohydrate intake was observed to be directly related to insulin resistance (30). We used fasting insulin as a surrogate for insulin resistance in the present study because the use of more precise procedures for measuring insulin resistance is not feasible in this type of study. Fasting serum insulin, as well as other approaches based on fasting insulin and glucose concentrations, was used to identify insulin resistance in many other studies (21,31–33). Influencing factors such as baseline triacylglycerol concentration, weight change, adiposity, and insulin resistance modulate the response to increased carbohydrate and reduced fat intakes and should be considered in the interpretation of these plasma responses as biological indicators of dietary intake in individuals.
The degree of increase in plasma triacylglycerol and decrease in HDL cholesterol concentrations that was observed in response to the intervention was not of a degree that would indicate increased risk for cardiovascular disease as a result of the diet modification (22). The frequency of hypertriacylglycerolemia in the study groups did not change over time or differ in the intervention vs. the comparison group. Changes in total cholesterol, LDL cholesterol, apo-B, lipoprotein (a), and fasting insulin concentrations were not observed in either the intervention or the comparison group, and most importantly, the LDL cholesterol/HDL cholesterol ratio did not change. Because this ratio did not change, we conclude that the small changes in plasma lipid concentrations that were noted did not change the cardiovascular disease risk in these study participants (22).
In summary, modest changes in dietary carbohydrate and fat intakes as a result of intervention efforts to promote a low-fat dietary pattern were associated with increased plasma triacylglycerol and reduced HDL cholesterol and apo-A1 concentrations in women participating in a clinical trial that is testing the effect of diet modification on risk for breast cancer recurrence. The intervention effort was shown previously to result in substantially increased vegetable and fruit intake, associated with increased plasma carotenoid concentrations. The changes in the lipid pattern reported in the present study validate self-reported changes in fat and carbohydrate intakes.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Manuscript received 2 October 2003. Initial review completed 30 October 2003. Revision accepted 11 November 2003.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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