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© 2005 The American Society for Nutritional Sciences J. Nutr. 135:1183-1189, May 2005


Nutritional Epidemiology

Identification of a Food Pattern Characterized by High-Fiber and Low-Fat Food Choices Associated with Low Prospective Weight Change in the EPIC-Potsdam Cohort1

Mandy Schulz*,2, Ute Nöthlings*,{dagger}, Kurt Hoffmann*, Manuela M. Bergmann* and Heiner Boeing*

* Department of Epidemiology, German Institute of Human Nutrition Potsdam-Rehbruecke, Germany, and {dagger} Cancer Research Center of Hawaii, Honolulu

2To whom correspondence should be addressed. E-mail: mschulz{at}mail.dife.de.


    ABSTRACT
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The aim of the study was to identify a dietary pattern predictive of subsequent annual weight change by using dietary composition information. Study subjects were 24,958 middle-aged men and women of the European Prospective Investigation into Cancer and Nutrition–Potsdam cohort. To derive dietary patterns, we used the reduced rank regression method with 3 response variables presumed to affect weight change: fat density, carbohydrate density, and fiber density. Annual weight change was computed by fitting a linear regression line to each person’s body weight data (baseline, and 2- and 4-y follow-up) and determining the slope. In linear regression models, the pattern score was related to annual weight change. We identified a food pattern of high consumption of whole-grain bread, fruits, fruit juices, grain flakes/cereals, and raw vegetables, and of low consumption of processed meat, butter, high-fat cheese, margarine, and meat to be predictive of subsequent weight change. Mean annual weight gain gradually decreased with increasing pattern score (P for trend < 0.0001), i.e., subjects scoring high for the pattern maintained their weight or gained significantly less weight over time compared with subjects with an opposite pattern. However, the prediction of annual weight change by the food pattern was significant only in nonobese subjects. In this study population, we identified a food pattern characterized by high-fiber and low-fat food choices that can help to maintain body weight or at least prevent excess body weight gain.


KEY WORDS: • food pattern • weight change • reduced rank regression • European Prospective Investigation into Cancer and Nutrition • EPIC-Potsdam study

Weight gain results from an imbalance between energy intake and energy expenditure. Current recommendations to avoid weight gain include limiting dietary energy from fat to 35% and meeting at least 45% of energy requirements with carbohydrates (1). However, considering the dramatic development of obesity rates in the United States and other westernized countries, despite a decline in fat intake as a percentage of total energy over the past decades (24), the applicability and the success of these recommendations may be debatable. The question arises as to whether the focus of body-weight control should be on energy density or on more practical characteristics of diet, such as the choice of specific foods or food groups. Although a number of reviews of the association between fat intake and body-weight development revealed a direct association (58), the scientific evidence has been challenged (911).

In recent years, the integration and the compression of full dietary information using dietary pattern approaches to assess the association between diet and body-weight development has become of increasing interest among nutritional epidemiologists (12). From cross-sectional studies, we learned that no consistent associations could be identified between BMI or obesity and dietary patterns (13). However, a prospective study design relating baseline dietary information to subsequent change in body weight may shed new light on the association between diet and body weight. To date, prospective investigations to examine this association are scarce. For subjects of the Baltimore Longitudinal Study of Aging, a healthy cluster and a reduced-fat dairy, fruits, and fiber pattern were associated with significantly lower weight gains over time (14,15). A longitudinal study of food-intake patterns and BMI change in Danish adults revealed inconsistent and only minor associations. For instance, a dietary pattern characterized by high intakes of whole-grain products, fruits, and vegetables (labeled as "green" dietary pattern) was not associated at all with prospective weight change (16). Cluster analysis and factor analysis constituted the prevailing approaches of dietary pattern analysis in previous studies (12).

The aim of the present study was to identify a food pattern based on dietary composition information to predict subsequent annual weight change over a 4-y follow-up period in a German middle-aged population of the European Prospective Investigation into Cancer and Nutrition (EPIC)3-Potsdam study (17). We applied a new dietary pattern approach, reduced rank regression (RRR), proposed for nutritional epidemiology research by Hoffmann et al. (18), which has proven useful in identifying dietary patterns in relation to chronic diseases (18,19) and which is superior to principal component analysis (PCA) if variation in the selected nutrient densities is more relevant for weight change than the unspecified variation in intake of all foods (20).


    SUBJECTS AND METHODS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
    Study population. The study population was composed of men and women of the EPIC-Potsdam cohort (21), a German population sample of 27,548 participants contributing to the large multicenter EPIC cohort study (22). The baseline examination of the study participants took place between August 1994 and September 1998. Follow-up questionnaires were sent to the participants in 2-y intervals, with response rates > 96% (23).

Approval for all study procedures was given by the Ethical Committee of the State of Brandenburg, Germany, and informed consent was obtained from all study participants.

For this analysis, men aged 24–69 y and women aged 19–70 y, with complete data on body weight at baseline and who returned the first and second follow-up questionnaire, were eligible (n = 25,079). Pregnant women either at baseline or at follow-up were excluded from the analysis (n = 118), as well as 3 subjects with implausible follow-up weights, leaving 24,958 subjects for the statistical analysis. The mean follow-up time was 4.4 y, ranging between 1.6 and 7.5 y.

    Assessment of body weight and diet. Baseline body weight was measured without shoes and in light clothes on a calibrated scale to the nearest 0.1 kg by trained technicians. Weight at follow-up examinations at 2 y and 4 y was self-reported by the participants in the respective follow-up questionnaires.

A self-administered, validated FFQ was applied to obtain information on the habitual diet of the past 12 mo before baseline (24). The FFQ consisted of 148 items, included questions about individual portion sizes, and additional questions about fat content of certain food items. The food items were collapsed into 49 food groups based on culinary usage or nutrient profiles (25), and absolute intakes in gram per day were computed. Dietary changes that occurred during follow-up were assessed at both follow-up examinations. Subjects were asked if they had changed their dietary habits compared with that of 2 y ago (yes; yes, partly; no). The answers "yes" and "yes, partly" were collapsed to yes for the analysis.

Information about sociodemographic characteristics, physical activity, medications, previous illnesses, and occupation were assessed at baseline with a questionnaire and in a face-to-face interview. Self-reports on incident diseases were obtained at each follow-up and subsequently were verified.

    Statistical analysis. Weight change per year was computed by fitting a linear regression line to each person’s body weight data and determining the slope. A positive value indicates weight gain over time, whereas a negative value indicates weight loss.

To identify a food pattern that is related to annual weight change we applied the dietary pattern technique RRR. The RRR method uses both data from the study and prior knowledge to derive dietary patterns and therefore represents a so-called a posteriori method. A detailed description of the method can be found in Hoffmann et al. (18). Briefly, RRR extracts factors that maximize the proportion of explained variation in a set of response variables, which are considered to be related to the outcome of interest. In the present study, the nutrient densities of the dietary variables total fat, total carbohydrates, and fiber (g fat per 1 MJ, g carbohydrates per 1 MJ, and g fiber per 1 MJ), which are presumed to affect prospective weight change (2632), were chosen as response variables. Three factors were extracted. The first RRR factor explained 53.4% of total variation in all 3 response variables (43.0% of variation in fiber density, 52.0% of variation in fat density, and 65.3% of variation in carbohydrate density). The subsequent 2 RRRs explained only 20.5% and 9.5%, respectively, of response variation and therefore were not further examined. We applied the RRR method to the entire study population, as well as separately, to males and females. Because the overall pattern did not markedly differ from the gender-specific patterns, indicated by the very similar factor loadings for men and women, the overall pattern was used (Table 1). To better translate the derived dietary pattern score to a food pattern and eventually to other studies, the dietary pattern score was shortened and simplified. For this purpose, the 10 food groups that contributed most to interindividual variation in the dietary pattern score (5 food groups being directly associated with the score and 5 food groups being inversely associated with the score) were identified. The proportion of variance explained by the single food groups was obtained by multiplying the standardized score parameter with the correlation coefficient between the dietary pattern score and each food group times 100 [for details see (19)]. Also, these 10 food groups were used to derive a so-called simplified food pattern to construct a less population-dependent pattern variable of similar content as the original dietary pattern score. The simplified pattern score represents the sum of the standardized food group variables, which explained most of the interindividual variation in the original dietary pattern score. The method and its applicability have been described in detail by Schulze et al. (33). The simplified pattern score defined by the food groups given in Table 1 was used to evaluate the association between the pattern and the annual weight change and, through the remainder of the text, is referred to as the food pattern.


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TABLE 1 Food groups comprising the simplified dietary pattern, their mean intake by men and women, and factor loadings1

 
For descriptive purposes, the mean intakes of the 10 food groups were calculated across quintiles of the food pattern score, as well as sample means, standard deviations, and frequencies for sample characteristics (general and dietary characteristics). Tests for linear trend were performed by using the quintile number as an independent variable in a linear regression model (continuous variables) and a test of independency ({chi}2 test) was performed for categorical variables.

Analysis of covariance was used separately for men and for women to compare mean outcome levels between quintiles of the food pattern, adjusted for effects of the covariates (34). We first evaluated the impact of potential effect modifiers on the association between the food pattern and the annual weight change by fitting models, including interaction terms for the simplified pattern quintile variable, with the following variables: age at baseline (median split: <50, 50+ y), BMI status (<25, 25 to 30, 30+), and change in diet (yes, no). There was evidence of effect modification by age, BMI status, and dietary change after baseline (each P-value of interaction term < 0.05 except for age) on mean weight change per year. Thus, mean outcome levels are presented in strata of age categories, BMI status, and dietary change. In addition, the impact of potential confounders was assessed on an individual basis and then in the stratified models. Relevant confounders that were retained in the final analysis included leisure time physical activity, change in smoking status after baseline, occupation at baseline, and number of incident diseases. In addition to these variables, the stratification variables were included as covariates in the full model. The women’s models additionally controlled for hormone replacement therapy at baseline. We also adjusted our models for total energy intake to separate the quantitative effect of diet and the qualitative effect expressed by the simplified pattern. However, this adjustment had no effect on the risk estimates and was left out from the final models.

All statistical tests were two-sided, and a P-value of <0.05 was considered significant. The statistical analysis was performed using SAS for Windows V8 (SAS Institute).


    RESULTS
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Baseline characteristics of the study population are presented across quintiles of the food-pattern score (Table 2). Except for age (continuous), all sample characteristics were associated with the food pattern. Worth mentioning is the distribution of dietary characteristics across the food-pattern quintiles: while relative fat intake (measured as percent energy from fat sources) decreased from 40.3% in the first quintile to 32.4% in the 5th quintile, total energy intake decreased as well, and both carbohydrate and fiber consumption increased across quintiles. Focusing on the key foods, as the food-pattern score increased, the intake of whole-grain bread, fresh fruit, fruit juices, grains and cereals, and raw vegetables gradually increased as well, whereas the intake of processed meat, butter, high-fat cheese, margarine, and meat decreased. Subjects with a high food-pattern score consumed a diet characterized by high-fiber, high-carbohydrate, and low-fat food choices in contrast to those having a low food-pattern score, whose diet was high-fat, low-carbohydrate, and low-fiber food.


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TABLE 2 Sample characteristics across quintiles of the (simplified) food pattern score, EPIC-Potsdam Study, n = 24,9581, 2

 
After the mean follow-up time of 4.4 y, the mean annual weight change in our study population was marginal (0.07 kg/y) but ranged from –13.6 to 7.5 kg/y. In crude analyses, annual weight change gradually decreased (from 0.15 to 0.0 kg/y) from the lowest to the highest quintile of the food-pattern score (data not shown).

To evaluate the association between the identified food pattern and the annual weight change, we used a linear regression model approach and estimated mean weight change per year as a function of the food-pattern score controlled for other covariates (Table 3). Mean annual weight change across strata of male and female study subjects ranged from –0.36 kg/y for obese women to 0.33 kg/y for normal-weight men. With all subjects, after adjustment for covariates, we saw a weight gain of 0.12 kg/y among subjects in the lowest quintile of the food-pattern score and a nearly stable weight among subjects of the highest quintile. The annual weight changes in the 4th and 5th quintile of the food-pattern score were significantly different from the annual weight change in the first quintile. This means that subjects with a diet characterized by high intakes of whole-grain bread, fresh fruit, fruit juices, grains and cereals, and raw vegetables, and by low intakes of processed meat, butter, high-fat cheese, margarine, and meat generally maintained their body weight, whereas subjects without these dietary habits were more likely to gain weight. This association was found for all subjects combined, as well as for males and females separately. However, the association of the food pattern and the annual weight change differed according to strata of the effect modifying variables.


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TABLE 3 Adjusted mean weight change per year by quintiles of the (simplified) food pattern score, overall, by gender and stratification variables, EPIC-Potsdam Study, n = 24,9581, 2

 
Among men, the food-pattern score was associated with weight change per year in the older age group (50+ y) but not in the younger age group. Also, for BMI, the food-pattern score was highly predictive (P = 0.0055) of annual weight change in the overweight group and predictive (P = 0.0668) in the normal-weight group but had no predictive value in the obese subjects. Of note, although overweight and especially normal-weight men on average gained weight, obese men reported body weights indicating a weight loss over time. Among normal-weight men, the mean weight gain in the higher quintiles of the food pattern was substantially lower than the mean weight gain in the lowest quintile. In obese males, annual weight change did not differ among quintiles of the food-pattern score. A change in diet during follow-up changed the impact of the food pattern on annual weight change in that the food pattern was significantly associated with weight change only among those who reported to have changed their diet (P = 0.0005).

In females, the most pronounced difference in predictability of the food pattern was found in BMI status. The food pattern predicted annual weight change for the normal-weight range (P < 0.0001) better than for the group of obese women (P = 0.1841). Worth mentioning is the direction of the weight change across BMI classes; whereas normal-weight and overweight women on average gained weight over time, the obese women reported a weight loss. The weight gained among normal-weight women with a high food-pattern score was significantly lower than the weight gain of women of the lowest quintile of the food-pattern score. A change in diet did not affect the association of the food pattern with annual weight change. However, those who changed their diet, on average, maintained their body weight and even lost some weight with an increasing food-pattern score, whereas women with no change in diet on average gained weight with significantly lower weight gains in the upper quintiles than in the bottom quintile of the food-pattern score.


    DISCUSSION
 TOP
 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
In the present study, we identified a food pattern characterized by high-fiber and high-carbohydrate food choices, such as whole-grain bread, fresh fruit, fruit juices, grains and cereals, raw vegetables, and by high-fat food choices, such as processed meat, butter, high-fat cheese, margarine, and meat, which predicted annual weight change over a 4-y period in a German adult population. Subjects with higher intakes of the high-fiber and high-carbohydrate foods and lower intakes of the high-fat foods were found to be weight stable or had substantially lower weight gains than subjects with an opposite food pattern. However, the identified food pattern was less predictive of annual weight change in obese subjects than in normal-weight and overweight subjects.

We compared our findings with findings from previous studies of dietary patterns and prospective weight change. There are at least 3 studies (1416) to date that examined empirically derived dietary patterns in relation to prospective weight change. The analyses by Newby et al. [cluster analysis (14), factor analysis (15)] of the Baltimore study to derive dietary patterns each identified a healthy dietary pattern, characterized by high intake of high-fiber grains and cereals, reduced fat dairy, fruits, and vegetables, and by low intake of refined grains, meats, soda, and high-fat dairy, which was associated with substantially less weight gain over time. Our findings are in agreement with these studies, assuming that dietary practices of subjects in the highest quintile of the food-pattern score of the present study resemble those in the healthy dietary pattern in the Baltimore study. A study (16) from Denmark found no association of a "green" dietary pattern, characterized by a high consumption of whole grains, fruits, and vegetables, and thus resembles a high score of the food pattern identified in the present study, with prospective weight change. This study suffered from a high drop-out rate at follow-up examination, which may have diluted the association under investigation. Other points of reference are studies that identified food groups predictive of prospective weight gain. In a previous study (35), we showed that, among women, high-fat foods such as fats, sauces, and meat predicted subsequent weight gain, whereas the consumption of cereals was predictive of weight loss. Although in this study we did not use the full dietary information in a pattern approach but used single food-group intakes, it strengthens the importance of the food pattern identified in the present study with regard to body-weight development. Further studies integrating food-intake information were equivocal: some studies found evidence that consumption of meat or sweets was related to increases in body weight (36,37), whereas other investigators reported opposite or null associations between examined food groups and weight change (38,39).

An important aspect of the present study is that the association of the food pattern we identified with annual weight change of the subsequent 4-y period was confined to nonobese subjects. This merits special attention, because the impact of a diet characterized by high-fiber low-fat food choices on weight change appears to be prevention of weight gain instead of predicting weight loss. The obese individuals of the present study reported follow-up weights that were lower than their measured baseline weights, indicating a weight loss. This might be the reason why we did not find an association among the obese subjects. Another possible explanation can be misclassification bias of either the exposure (diet) or the outcome (annual weight change). It is known that diet is reported biased, especially for foods considered salubrious (fruits and vegetables) or foods considered unhealthy (fats and meat). This phenomenon is even more pronounced among overweight subjects (40,41). Correspondingly, overweight subjects tend to underreport their body weight (42). Because we had to rely on self-reported weights at follow-up, underreporting may have introduced misclassification of the outcome, which, as a result, diluted any potential association between diet and weight change detected. Furthermore, there is always the possibility of residual confounding, and we can never rule out that unmeasured or imprecisely measured factors have confounded the association.

By choosing energy density variables as the base for the identification of the dietary pattern in the present study, we assumed that the composition of the diet may affect body-weight development. This assumption affected the selection of the food groups representing the food pattern and is subject to discussion. There are at least 7 prospective investigations examining the association between dietary composition and subsequent weight change. Attention focused on the effect of dietary fat as percent energy in relation to weight change. However, results are inconclusive: whereas some studies detected a positive association (27,29,32,43,44), others reported no association (45,46). At least one study reported an inverse association between percent energy from carbohydrates or fiber density and prospective weight change (29). Although it is a highly debated topic, whether total energy intake or the relative contribution of macronutrients to energy is to be recommended to avoid weight gain, our results suggest that dietary behavior, which reflects the current recommendation to limit fat intake to 35% of energy and to increase fiber intake (1), can avoid or at least minimize weight gain in an adult population.

We applied a new dietary-pattern approach to examine the association between dietary habits and prospective weight change by focusing on dietary composition. The benefit of using RRR compared with directly choosing energy densities as predictors of prospective weight change is that the effect of increasing or decreasing the usual intake of a specific food group on body weight can be estimated. This advantage follows from the fact that for any change of habitual dietary intake, the corresponding change of pattern score can be calculated. The RRR method is a powerful technique, because it combines both a priori and a posteriori information of the exposure-outcome association by defining a set of variables assumed to be linked to the outcome and explaining variation in those variables with the dietary information at hand. This is novel in nutritional epidemiology and has proven informative in examining associations between dietary patterns and some outcome (18,19). Previous pattern approaches, with the exception of confirmatory factor analysis, used only either a priori information or the data at hand.

A question often raised, given the more data-driven nature of the RRR method, as well as of other pattern methods, is to what extent is the identified dietary pattern entirely unique to the underlying study population, and thus of limited value for inferences. Because of this and the ease of understanding and of disseminating the dietary pattern into public health practices, we chose the simplified food-pattern approach. Using this approach, the major weakness of the pattern technique was limited by concisely naming the contributing food groups, along with their intakes and direction of association with the pattern score. Thus, the food pattern identified in the present study is easily reproducible in other study populations with similar quality of dietary variables.

Nevertheless, our application of the RRR method has several limitations. First, although we tried to define homogeneous food groups, the number and definitions of the food groups are somewhat arbitrary and may affect the derived patterns. Grouping may arbitrarily limit the variation, and groups composed of several foods are considered to be similar to groups consisting of only one food. Moreover, RRR and PCA work with the default of centered and scaled food groups, which implicitly gives equal weight to all food groups, regardless whether the foods are consumed frequently in high amounts or infrequently in small amounts. However, in contrast to PCA patterns, the RRR patterns are not affected by standardization of food groups, because they focus on the variation in the selected nutrient densities. Second, there is no well-accepted statistical criterion to specify the number of derived patterns. In the present study, we reported and analyzed only the first pattern. This seems to be unusual, because in previous PCA applications, at least 2 patterns were reported. However, the RRR method is a dimension-reduction procedure that starts from the dimension of responses, which is only 3 in our study and therefore is much lower than the number of food groups, which is the starting point of PCA. Therefore, a reduction from dimension 3 to 1 seems reasonable. Moreover, although the response variations explained by the second and third RRR patterns were 20.5% and 9.5%, respectively, both patterns explained together much less variation in responses than the first RRR pattern alone. Third, the choice of the 3 nutrient densities as responses in the RRR analysis is neither objective nor unique. Choosing different dietary components as responses will clearly result in distinct patterns that must not be related to subsequent weight gain or loss. However, minor changes of the set of response variables, such as adding a fourth nutrient density, will not have a dramatic effect on the results, by our calculations (not shown), and a comprehensive sensitivity analysis focused on this issue (19).

Given the relatively small mean weight change in our study, which appears to contrast the general raise of obesity rates (47), the question is whether the association we found between the food pattern and the annual weight change is relevant to other populations; to address this concern, consider the source of the follow-up information on weight presented in this study. These were self-reported and were compared with measured body weights at baseline. This is a clear limitation of the study. However, we still detected a significant association between the baseline diet and subsequent weight change, which is considered a rather conservative estimate of the true association, given the measurement error in the weight-change variable. Furthermore, our study population is a middle-aged population, which is not characterized by massive adult weight gain. In Germany, adult weight gain is seen among young men between the ages 30 y and 40 y (47). Because only a small percentage of our study population is in this age range, we did not expect to see large mean weight gains. We also compared our annual weight changes with weight changes measured in other studies. Togo et al. (16) reported a mean 5-y change in BMI of 0.2 kg/m2 among 60-y-old subjects. This would be 0.12 kg/y, assuming a mean height of 1.70 m and resembles our observed annual weight gain. The annual BMI change in the Baltimore study (14) was reported as 0.11 kg/m2 per year, which converts to about 0.32 kg/y for a person of average height. Unlike our study, in these studies, both baseline and follow-up weights were measured. Taking these weights into account, we do not find that the associations detected in the present study are of limited relevance. However, the absolute value of mean annual weight change of the present study needs to be interpreted with caution, because only baseline weights were measured.

In summary, from our data, we conclude that a food pattern characterized by low-fat, high-fiber, high-carbohydrate food choices, such as whole-grain bread, fruits, grains, and cereals, may help to maintain body weight or to prevent excess weight gain over time. Although the predictive value of this dietary pattern was confined to nonobese subjects, this study lends support to the current recommendations regarding macronutrient composition of the diet. Following the food pattern identified in the present study will help meet the recommendations for dietary fat, carbohydrate, and fiber intake and, consequently, may not result in excess energy intake and thus in weight gain. The association between dietary practices and weight change among obese individuals warrants further investigations.


    ACKNOWLEDGMENTS
 
We thank Matthias B. Schulze for valuable comments on this study.


    FOOTNOTES
 
1 The EPIC Potsdam Study was funded by the German Cancer Aid (Deutsche Krebshilfe) (grant 70-2488) and the European Community (grant SPC.2002332). Back

3 Abbreviations used: EPIC, European Prospective Investigation into Cancer and Nutrition; PCA, principal component analysis; RRR, reduced rank regression. Back

Manuscript received 21 October 2004. Initial review completed 16 November 2004. Revision accepted 23 January 2005.


    LITERATURE CITED
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 ABSTRACT
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 

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