RESEARCH Current Research
Trends in Nutrient Intake among Adults with Diabetes in the United States: 1988-2004 REENA OZA-FRANK, MS, MPH, RD; YILING J. CHENG, PhD; K. M. VENKAT NARAYAN, MD; EDWARD W. GREGG, PhD
ABSTRACT Background Weight loss through dietary modification is key to type 2 diabetes self-management, yet few nationally representative data exist on dietary trends among people with diabetes. Objective To examine dietary changes, via nutrient intakes, among US adults with diabetes between 1988 and 2004. Design Nutrition data from the cross-sectional National Health and Nutrition Examination Surveys (Phase I: 1988-1990 and Phase II: 1991-1994) and 1999-2004 of adults with self-reported diabetes were examined. Twentyfour– hour dietary recall data were used to assess changes in energy; carbohydrate; protein; total, saturated, polyunsaturated, and monounsaturated fat; cholesterol; fiber; sodium; and alcohol intake. Statistical analyses Consumption of total energy and specific nutrients per day were estimated by survey, controlled for age and sex, using multiple linear regression and adjusted means (with standard errors). Results Between 1988 and 2004 there was no significant change in self-reported total energy consumption among adults with self-reported diabetes (1,941 kcal/day in 1988-1990 to 2,109 kcal/day in 2003-2004, P for trend⫽ 0.22). However, there was a significant increase in the consumption of carbohydrate (209 g/day in 1988-1990 to 241 g/day in 2003-2004; P for trend⫽0.02). In analyses stratified by age group, changes in dietary consumption
R. Oza-Frank is a graduate student, Nutrition and Health Sciences Program, Graduate Division of Biomedical and Biological Sciences, Emory University, Atlanta, GA. Y. J. Cheng and E. W. Gregg are epidemiologists, Division of Diabetes Translation, National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Atlanta, GA. K. M. V. Narayan is a professor, Nutrition and Health Sciences Program, Graduate Division of Biochemical and Biological Sciences, the Hubert Department of Global Health, Rollins School of Public Health, and the School of Medicine, Emory University, Atlanta, GA. Address correspondence to: Reena Oza-Frank, MS, MPH, RD, Emory University, 1518 Clifton Rd, NE, Room 757G, Atlanta, GA 30322. E-mail:
[email protected] Manuscript accepted: December 19, 2008. Copyright © 2009 by the American Dietetic Association. 0002-8223/09/10907-0004$36.00/0 doi: 10.1016/j.jada.2009.04.007
© 2009 by the American Dietetic Association
were noted among persons aged 45 to 64 years; specifically, increases in total energy (1,770 to 2,100 kcal/day, P for trend ⫽0.01) and carbohydrate consumption (195 to 234 g/day, P for trend⫽0.02). Conclusions Despite recommendations to lose weight, daily energy consumption by individuals with diabetes showed no significant change, except in individuals aged 45 to 64 years, where an increase was observed. Overall, there was an increase in carbohydrate consumption. Emphasizing the equal importance of energy reduction and changes in dietary composition for people with diabetes is important for optimal self-management. J Am Diet Assoc. 2009;109:1173-1178.
O
ne in three people born in the United States in 2000 are projected to develop type 2 diabetes at some point in their lifetime (1) and more than 23 million currently have the disease (2). Its prevalence has increased 120% in the past 25 years (3), and it is projected that there will be 48 million individuals with type 2 diabetes in the United States by 2050 (4). More than 80% of individuals with type 2 diabetes are overweight or obese (5). Weight loss through dietary modification and exercise are key first steps in diabetes self-management (6). The main strategy recommended for weight loss in individuals with overweight or obesity is to reduce energy intake by 500 to 1,000 kcal/day (6), with the goal of a 1 to 2 lb weight loss per week (7). Even moderate weight loss (5% of body weight) improves control of hypertension and decreases insulin resistance (8). Observational studies suggest that, in individuals with type 2 diabetes, weight loss may reduce cardiovascular disease (CVD) and allcause mortality, although this has not been documented in clinical trials (9). In the general US population, mean energy intake and portion sizes increased between 1971 and 2000 (5,10) and both have been cited as explanations for the observed increasing trends in body weight (10). During the same time period, decreases in percent dietary fat, saturated fat, cholesterol, and discretionary salt intakes have been observed, suggesting that some improvements in diet quality have occurred (11). Individuals with diabetes may experience confusion regarding optimal nutrition-related practices that have a direct influence on disease management. Few nationally representative data exist on nutrient trends among people with type 2 diabetes. We used nationally representative data to study differences in nutrient intake among people with type 2 diabetes between 1988 and 2004, a period of increasing awareness of the public health problem of type 2 diabetes (12).
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RESEARCH DESIGN AND METHODS The National Health and Nutrition Examination Surveys (NHANES) are a series of cross-sectional health examination surveys representing the US civilian, noninstitutionalized populations conducted by the National Center for Health Statistics of the Centers for Disease Control and Prevention. NHANES III data were collected in two phases: Phase I 1988-1990 and Phase II 1991-1994 (13); after 1994, NHANES continuous surveys were released in 2-year segments. Specifically, NHANES 1999-2000 (14), 2001-2002 (15), and 2003-2004 (16) data were used for this analysis. Each survey followed a stratified multistage probability design. The survey combines face-toface interviews with health examinations. The health examinations take place in the mobile examination center where an interview is conducted to collect a 24-hour dietary recall. Response rates for mobile examination center-examined individuals for the survey years of interest were all approximately 80% (13-16). Informed consent was obtained from all participants and these documents were approved by the National Center for Health Statistics Institutional Review Board (17). Study Population Analyses were restricted to nonpregnant adults aged 20 to 74 years who had a reliable self-reported 24-hour dietary recall (all relevant variables associated with the 24-hour recall contain a value) and self-reported having diabetes in response to the question “Have you EVER been told by a doctor or health professional (other than during pregnancy) that you have diabetes or sugar diabetes?” The final analytic sample comprised 1,404 respondents (NHANES III Phase I n⫽329, NHANES III Phase II n⫽322, NHANES 1999-2000 n⫽237, NHANES 20012002 n⫽254, and NHANES 2003-2004 n⫽262). Dietary Assessment Methodology NHANES III used a computer-assisted, automated, interactive method developed by the University of Minnesota’s Nutrition Coordinating Center in collaboration with National Center for Health Statistics staff to collect dietary information in the form of a 24-hour recall. Dietary recalls collected for NHANES 1999-2001 used a computer-assisted dietary interview that included a four-step multiple pass approach (18). A five-step multiple pass approach with dietary recall methods that are part of the integrated US Department of Agriculture (USDA) and NHANES protocol of What We Eat In America was used for NHANES 2002 and 2003-2004 (15,16). Both approaches were designed to enhance complete and accurate food recall and reduce respondent burden. For nutrient analyses, the USDA 1994-1998 survey nutrient database was used before 2001 and after 2001, the USDA Food and Nutrient Database for Dietary Studies (version 1, USDA Agricultural Research Service, Beltsville, MD) was used. Diet data from NHANES I and II were not included in the analyses because the dietary interview methodologies and technical databases that were used to report NHANES I and II were considerably different from those used in more recent surveys. For example, the 24-hour recalls in NHANES I and II contained fewer data for
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weekend days (13-16), and food consumption patterns and behaviors may differ on weekends compared to weekdays. Statistical Analysis Data from each survey and survey phase were combined for trend analysis. Sampling weights that account for unequal probabilities of selection resulting from sample design, nonresponse, and planned oversampling of certain subgroups were calculated to make weighted results representative of the US population. All analyses were performed using SAS callable SUDAAN (release 9.0.1, 2005, Research Triangle Institute, Research Triangle Park, NC). All reported P values are two sided. Results were considered significant if P⬍0.05. Multiple linear regression was used and predicted marginals (with standard errors) were computed to estimate the total energy consumption per day and consumption of each specified nutrient per day by time period, controlling for age and sex. Predicted marginals (a type of direct standardization in which the predicted values from the linear regression models are averaged over the covariate distribution of the population [19]) were also used to test for trend across the survey years of interest. Although potential nonlinear effects of age were considered ([agemean age] and [age-mean age]2), results did not change with the inclusion of these variables and thus age was kept as a continuous variable. Race/ethnicity was included as an independent factor in all regressions; however, it was not significant and thus the results do not include race/ethnicity. Significance of interaction terms of survey period with sex, race/ethnicity (non-Hispanic white, non-Hispanic African American, Hispanic, other), age group (20 to 44 years, 45 to 64 years, 65 to 74 years), and body mass index (BMI) category (normal weight 18.5 to 24.9, overweight 25 to 29.9, and obese ⬎30) were assessed separately to determine if changes throughout the 16-year period and between the first and last surveys differed by these categories when the outcome variable was total energy. Trends were also examined by sex, race/ethnicity, age group, and BMI separately for clinical significance of changes in diet. Because the objective was to examine trends in absolute nutrient intake (vs trends in the proportions of total energy), total energy was not included in the nutrient-specific regressions. Because the analyses presented here are based on secondary data analyses, standard errors were computed. Standard errors and corresponding P values are shown, which is equivalent to showing confidence intervals (95% confidence interval⫽estimate⫾standard error [1.96]). If standard error/confidence intervals have been constructed, it is thought that power calculations yield no additional insights (20). RESULTS The characteristics of respondents with self-reported diabetes in the NHANES survey phases and surveys are shown in Table 1. From 1988 to 2004, there was no significant change in age- and sex-adjusted total energy consumption among people with self-reported diabetes (1,941 kcal/day to 2,109 kcal/day, P for trend⫽0.22) (Ta-
Table 1. Characteristics of self-reported diabetes respondents to the third National Health and Nutrition Examination Survey (NHANES) (Phase I: 1988-1990 and Phase II: 1991-1994) to NHANES 2003-2004a NHANES 1988-1990 (nⴝ329)
Characteristic
NHANES 1991-1994 (nⴝ322)
NHANES 1999-2000 (nⴝ237)
NHANES 2001-2002 (nⴝ254)
NHANES 2003-2004 (nⴝ262)
4™™™™™™™™™™™™™™™™™™™™™™™™™ mean⫾standard error ™™™™™™™™™™™™™™™™™™™™™™™™™ 3 Age (%) 20-44 y 45-64 y 65-74 Sex (% women) Race (% white) High school education (%) Height (cm) Weight (kg) Body mass indexb Taking insulin (%) Taking oral hypoglycemic agents (%) a
32.0⫾5.3 46.5⫾4.6 21.2⫾3.1 33.1⫾4.5 74.1⫾3.8 31.0⫾4.1 170.9⫾1.2 88.6⫾2.0 30.4⫾0.7 31.7⫾4.7 38.4⫾4.6
28.7⫾5.8 56.4⫾5.6 14.9⫾3.1 39.1⫾5.4 70.9⫾3.9 36.4⫾5.9 169.1⫾1.0 88.6⫾2.0 31.0⫾0.6 25.1⫾4.5 53.3⫾5.1
22.2⫾3.6 56.4⫾4.5 21.4⫾2.3 31.5⫾3.4 61.6⫾6.7 25.0⫾5.7 169.2⫾0.9 94.3⫾2.7 32.8⫾0.8 30.5⫾5.3 60.2⫾6.8
30.3⫾4.5 56.5⫾4.3 13.2⫾2.3 30.6⫾2.9 58.5⫾4.2 23.5⫾3.0 170.7⫾0.8 92.6⫾2.1 31.8⫾0.7 20.0⫾2.9 70.2⫾3.6
21.1⫾2.6 58.0⫾2.1 20.9⫾2.7 36.3⫾2.5 69.4⫾6.2 22.6⫾3.0 170.7⫾0.5 94.7⫾2.7 32.5⫾0.9 23.0⫾3.0 65.6⫾4.2
All estimates are weighted to be representative of the US noninstitutionalized population aged 20 to 74 years. Calculated as kg/m2.
b
Table 2. Total energy and nutrient consumption among all respondents with self-reported diabetes in a 24-hour recall from the third National Health and Nutrition Examination Survey (NHANES) (Phase I: 1988-1990 and Phase II: 1991-1994) to NHANES 2003-2004a Nutrient
NHANES 1988-1990
NHANES 1991-1994
NHANES 1999-2000
NHANES 2001-2002
NHANES 2003-2004
Total energy (kcal) Carbohydrate (g) Protein (g) Total fat (g) Saturated fat (g) Polyunsaturated fat (g) Monounsaturated fat (g) Total cholesterol (mg) Fiber (g) Sodium (mg) Alchohol (g)
4™™™™™™™™™™™™™™™™™™™™™™™™ mean⫾standard error ™™™™™™™™™™™™™™™™™™™™™™™™3 1,941⫾87 1,980⫾70 2,058⫾71 1,948⫾68 2,109⫾80 209⫾8 226⫾9 240⫾8 227⫾9 241⫾9 90⫾6 82⫾4 88⫾3 82⫾4 85⫾4 79⫾4 83⫾4 84⫾5 78⫾4 85⫾4 26⫾1 26⫾1 26⫾1 23⫾1 27⫾1 15⫾1 19⫾1 19⫾1 17⫾1 18⫾1 32⫾3 32⫾2 32⫾2 29⫾2 32⫾2 352⫾41 301⫾26 313⫾21 326⫾29 322⫾21 17⫾1 18⫾1 19⫾2 16⫾1 16⫾1 3,544⫾186 3,657⫾187 3,717⫾169 3,359⫾133 3,491⫾109 8⫾2 4⫾1 3⫾1 8⫾2 10⫾4
P for Trend 0.218 0.020 0.536 0.663 0.973 0.184 0.592 0.722 0.371 0.396 0.406
a Estimates were derived from regression models with each variable in the Table as a continuous outcome; independent variables were sex and age (in all models), and survey (NHANES III Phase I: 1988-1990, NHANES III Phase II: 1991-1994, NHANES 1999-2000, NHANES 2001-2002, NHANES 2003-2004) as trend. The estimates are predicted marginal⫾standard error from weighted regression models that included respondents with reliable dietary recall data (n⫽1,404). NOTE: Information from this table is available online at www.adajournal.org as part of a PowerPoint presentation.
ble 2). Based on the observed small changes in total energy per day between NHANES III Phases I and II and the most recent survey showing a particularly high estimate, possibly indicating a potential upward trend in total energy consumption, a post-hoc test was conducted to confirm the lack of a significant trend for total energy consumption. Specifically, both NHANES III phases were combined, as were NHANES 2001-2004. Results showed a similar, although nonsignificant, trend (1,962 kcal/day to 2,036 kcal/day (P for trend⫽0.22), strengthening the evidence for a lack of change in total energy consumption. Overall age- and sex-adjusted carbohydrate consumption increased from 209 g in 1988-1990 to 241 g in 2003-2004 (P for trend⫽0.02). For all the remaining macronutrients
and micronutrients, no significant changes in consumption were observed. Despite the increasing trend in absolute consumption of carbohydrates in people with diabetes, macronutrient percentage of daily energy consumption did not significantly differ among the surveys (Figure 1). From 1988 to 2004, carbohydrate percentage remained stable, protein went from 19.1% in 1988-1990 to 15.6% in 2003-2004 and total fat went from 38.4% in 1988-1990 to 34.5% in 20032004. As a percentage of total energy, saturated fat slightly changed from 12.6% in 1988-1990 to 11.2% in 2003-2004, polyunsaturated fat remained stable, and monounsaturated fat went from 15.4% in 1988-1990 to 12.9% in 2003-2004 (data not shown). Trends for macro-
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Figure 1. Macronutrient intake as a percentage of total energy among all respondents with self-reported diabetes in a 24-hour recall from the National Health and Nutrition Examination Survey (NHANES) III (Phase I: 1988-1990 and Phase II: 1991-1994) to NHANES 2003-2004. The percentages were calculated from the predicted marginals from weighted regression models that included respondents with complete covariate information (n⫽1,404). Predicted marginals were derived from regression models with each variable as a continuous outcome; independent variables were sex and age (in all models), total energy, and survey (NHANES III Phase I, NHANES III Phase II, NHANES 19992000, NHANES 2001-2002, or NHANES 2003-2004) as trend. NOTE: This figure is available online at www.adajournal.org as part of a PowerPoint presentation. nutrient percentage of total energy and type of fat percentage were not significantly different by sex, race/ethnicity, age group, and BMI category (data not shown) among people with self-reported diabetes. None of the interactions tested were statistically significant. Specifically, no change in total energy intake was observed throughout the 16-year period across sex (adjusted for age), any race/ethnic groups (adjusted for age and sex), those aged 20 to 44 years or 65 to 74 years, or among BMI categories (adjusted for age and sex). Despite a nonsignificant interaction between survey and age group, results among those aged 45 to 64 years were of clinical importance. Adjusted for sex, total energy intake increased from 1,771 to 2,100 (P for trend⫽0.01) (Figure 2). Total carbohydrate consumption also increased from 195 g to 234 g (P for trend⫽0.02) (data not shown). Increases in total fat consumption were borderline significant (73 g to 87 g; P for trend⫽0.05) (data not shown). No other nutrients showed significant changes in this age group. This age group showed no change in percentage of energy from carbohydrates (44%) and fat (37%), and percentage of energy from protein went from 18% to 16%. Very small changes were seen in the percentage of energy from the different types of fat (data not shown). DISCUSSION Among adults with diabetes, there was no statistically significant evidence that total energy consumption
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changed between 1988 and 2004; however, carbohydrate consumption increased. In addition, among those aged 45 to 64 years, increases in consumption of total energy, carbohydrates, and fat were observed. Previous studies report increases in energy intake among the general US population (5,10,12), even when adjusted for diabetes status (21). Despite the lack of a significant trend in total energy intake in this study, the observed nonsignificant increases in energy intake could have clinical importance. Specifically, as little as an extra 10 kcal/day of unexpended energy is equivalent to an extra pound (0.45 kg) of weight per year (10). The proportion of energy from carbohydrates in this population were within the American Diabetes Association recommendations (⬍50% to 60% of total energy) (8). Although total carbohydrate consumption increased, there was no evidence of changes in fiber consumption, indicating the source of the increased carbohydrate is not coming from the recommended high-fiber sources of carbohydrates. There was a nonsignificant decrease in protein consumption; yet the population remained within the bounds recommended by the American Diabetes Association. A low-fat (eg, 25% to 30% of energy from fat and ⬍7% of total energy from saturated fat [8]) diet is considered the conventional therapy for treating and preventing CVD and obesity (8,21), regardless of diabetes status. In this population, percentage of energy from total fat was ⬎30% and ⬎10% for saturated fat, indicating that American Diabetes Association recommendations for either are not being met, but both percentages appear to be following a decreasing trend. Monounsaturated fat remained ⬍20% and polyunsaturated fat remained at ⬍10% of total energy. This could be a result of education to change dietary fat composition. Trans fat has been associated with increased risk of CVD (22); however, data on trans-fat consumption were not available in NHANES and thus were not used for these analyses. American Diabetes Association recommendations for cholesterol and sodium consumption are also not being met. Cholesterol consumption is still ⬃100 mg over the ⬍200 mg/day (8) recommendation and sodium consumption is ⬃1,000 mg over the 2,400 mg/day (6 g salt) recommendation. This may indicate the need for more intensive education for meeting recommended levels. The optimal macronutrient distribution of weight-loss diets has not been established, but there is consensus that the ideal diet varies by circumstances (8). The current American Diabetes Association recommendations are based on evidence regarding the effects of diet in reducing several CVD risk factors that are important for patients with type 2 diabetes because of their increased risk of CVD (8). Due to a lack of research in individuals with type 2 diabetes, current recommendations for nutrition therapy in type 2 diabetes, especially in relation to vascular complications, are not based on evidence from research in patients with type 2 diabetes (23). Interestingly, the results of our study indicate that the population is adhering well to most of the general macronutrient distribution recommendations, but more energy is being consumed during the time period represented. This additional energy is not coming from an increase in alcohol intake. Therefore, this discrepancy could be a result of
Figure 2. Total energy among respondents by age group with self-reported diabetes in a 24-hour recall from National Health and Nutrition Examination Survey (NHANES) III [Phase I: 1988-1990 and Phase II: 1991-1994] to NHANES 2003-2004. The percentages were calculated from the predicted marginals from weighted regression models that included respondents with complete covariate information (n⫽1,404). Predicted marginals were derived from regression models with each variable as a continuous outcome; independent variables were sex and age (in all models), total energy, and survey (NHANES III Phase I, NHANES III Phase II, NHANES 1999-2000, NHANES 2001-2002, NHANES 2003-2004) as trend. NOTE: This figure is available online at www.adajournal.org as part of a PowerPoint presentation. differences in reporting dietary intake based on dietary recall methodology and/or changes in the nutrient database during the study period. Medications may influence weight gain in individuals with type 2 diabetes (8). Many patients with type 2 diabetes are already overweight at diagnosis and gain more weight while taking oral medications and/or insulin (8). Individuals with type 2 diabetes may also increase energy intake through possible overtreatment of medicationinduced hypoglycemia. Medications may also provide patients with a newfound freedom (8) when pharmacotherapy or insulin therapy is initiated. For example, motivation to change lifestyle behaviors may be low, leading to dietary recklessness. This emphasizes the need for an individualized nutrition and physical activity plan, possibly in addition to any medications that may be necessary. This study’s sample sizes were too small to stratify individuals with diabetes by medication type; however, including medication type as a control variable in analyses produced no change in results (data not shown). Of concern is the significant increase in total energy consumption observed among those aged 45 to 64 years. Prevalence of diabetes increases with age, which is particularly important considering those aged ⬎45 years are at the highest risk in developing diabetes (2). This increase might be coming from increases in absolute carbohydrates and fat. The proportion of total energy from carbohydrate was within recommendations; however, the proportion of energy from fat was greater than the American Diabetes Association–recommended amount throughout all survey phases and years. Limitations to our study include a lack of differentiation between type 1 and type 2 diabetes in the questionnaire. Because type 2 diabetes typically constitutes 95% of cases, it is presumed that the majority of cases were
type 2 diabetes (2). Only self-reported diabetes was considered, but the accuracy of self-reporting for diabetes is reasonably high in population surveys (24). Second, although studies have shown the dietary collection methods adopted after NHANES III accurately report energy intake in normal-weight subjects (25,26), persons who are weight conscious, overweight, or obese are likely to underreport their energy intake (10,25). This would bias the results of this study toward nonsignificant trends, a plausible explanation for the observed results. Studies have also reported a high occurrence of low-energy reporting in national survey data (27). Third, the nutrient database used for estimating energy and nutrient intake has expanded over the period of the five surveys, and values of some nutrients may be more accurate in later survey years because of improved analytic technology and foodsampling methods (28). Finally, the physical activity variable was not comparable in the same level of detail across surveys and was not included in analyses. CONCLUSIONS These results indicate that only those individuals with diabetes aged 45 to 64 years are similar to the general population in that they increased energy consumption between 1988 and 2004. Overall, individuals with diabetes are not following American Diabetes Association nutrition recommendations for optimal disease management or for weight loss. When tailoring dietary intake messages to individuals with type 2 diabetes, it is important to emphasize the equal importance of energy reduction and changing dietary composition along with physical activity to optimize weight loss and intake of essential nutrients. Improving nutrition, in conjunction with exercise and behavior therapy through individualized plans,
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are recommended lifestyle strategies for successful weight loss and management of diabetes. The findings and conclusions in this report are those of the authors and do not necessarily represent the official position of the Centers for Disease Control and Prevention. STATEMENT OF POTENTIAL CONFLICT OF INTEREST: No potential conflict of interest was reported by the authors.
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