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See corresponding editorial on page 711.
Increased consumption of refined carbohydrates and the epidemicof type 2 diabetes in the United States: an ecologic assessment1–3 Lee S Gross, Li Li, Earl S Ford, and Simin Liu ABSTRACT
1991 and 1999, and currently Π60% of US adults are overweight Background: Type 2 diabetes is an epidemic that is affecting an
(3, 7). These increases cannot be explained by the aging of the ever-increasing proportion of the US population. Although con- population alone, because similar increases are also being seen in sumption of refined carbohydrates has increased and is thought to be related to the increased risk of type 2 diabetes, the ecologic effect of The cause of type 2 diabetes is multifactorial. Factors such as changes in the quality of carbohydrates in the food supply on the risk changes in exercise patterns and the ethnic composition of the US of type 2 diabetes remains to be quantified.
population are likely contributors to the rising trends in diabetes, Objective: The objective was to examine the correlation between
but there have been many debates in the scientific literature about consumption of refined carbohydrates and the prevalence of type 2 the effects of specific dietary macronutrients on the risk of obe- sity and type 2 diabetes (9 –12). Recent data suggest that a high Methods: In this ecologic correlation study, the per capita nutrient
intake of refined carbohydrates may increase the risk of insulin consumption in the United States between 1909 and 1997 obtained resistance (13–16). Although an increase in the intake of refined from the US Department of Agriculture was compared with the carbohydrates in the form of processed grains, soft drinks, sweet- prevalence of type 2 diabetes obtained from the Centers for Disease eners, and refined flours in the US food supply has been reported, scant quantitative data exist to determine whether such changes Results: In a univariate analysis, a significant correlation with dia-
in dietary composition are related to the current epidemic of betes prevalence was observed for dietary fat (r ҃ 0.84, P  0.001), obesity and type 2 diabetes in the United States. To address this carbohydrate (r ҃ 0.55, P  0.001), protein (r ҃ 0.71, P  0.001), issue, we examined almost one century of dietary data and the fiber (r ҃ 0.16, P ҃ 0.03), corn syrup (r ҃ 0.83, P  0.001), and total history behind changes in the US diet. We conducted a multi- energy (r ҃ 0.75, P  0.001) intakes. In a multivariate nutrient- variate analysis of the correlation between changes in the prev- density model, in which total energy intake was accounted for, corn alence of type 2 diabetes and changes in dietary patterns in the syrup was positively associated with the prevalence of type 2 dia- betes (␤ ҃ 0.0132, P ҃ 0.038). Fiber (␤ ҃ Ҁ13.86, P  0.01) wasnegatively associated with the prevalence of type 2 diabetes. Incontrast, protein (P ҃ 0.084) and fat (P ҃ 0.79) were not associated with the prevalence of type 2 diabetes when total energy was con- We obtained estimates of the prevalence of type 2 diabetes in the United States from the National Health Interview Surveys Conclusions: Increasing intakes of refined carbohydrate (corn
maintained by the Centers for Disease Control and Prevention’s syrup) concomitant with decreasing intakes of fiber paralleled the Diabetes Surveillance System (4, 17). Such data are available for upward trend in the prevalence of type 2 diabetes observed in the 1935 and then annually beginning in 1957 and are based on United States during the 20th century.
self-reports of having received a diagnosis of type 2 diabetes. In 1997, adoption of the type 2 diabetes diagnostic criteria of theWorld Health Organization effectively increased the prevalence KEY WORDS
Type 2 diabetes, obesity, dietary fiber, refined of type 2 diabetes in the United States after that year (18). We carbohydrate, dietary carbohydrate, glycemic index 1 From the Inter-Medic Medical Group, North Port, FL (LSG); the De- partment of Family Medicine, University Hospitals of Cleveland, Case West- INTRODUCTION
ern Reserve University (LL); the Centers for Disease Control and Prevention, Obesity and type 2 diabetes are occurring at epidemic rates in Atlanta (ESF); the Division of Preventive Medicine, Brigham and Women’s the United States (1–3). From 1935 to 1996, the prevalence of Hospital, Harvard Medical School, Boston (SL); and the Department of diagnosed type 2 diabetes climbed nearly 765% (4). Currently, Epidemiology, Harvard School of Public Health, Boston (SL).
16 million Americans have type 2 diabetes, one-third of whom Supported by a CI-8 Clinical Investigator Award from Damon Runyon do not even know that they have the disease (5). Recent data 3 Address reprint requests to LS Gross, Inter-Medic Medical Group, 2630 suggest that 47 million Americans have the metabolic syn- drome—an insulin resistance syndrome that is associated with an increased risk of type 2 diabetes (6). The prevalence of adult obesity increased a staggering 57% in the brief period between Accepted for publication November 6, 2003.
Am J Clin Nutr 2004;79:774 –9. Printed in USA. 2004 American Society for Clinical Nutrition REFINED CARBOHYDRATES AND TYPE 2 DIABETES therefore excluded data from later than 1997. The diagnosticcriteria for type 2 diabetes also changed in 1979 (19). However,the rate of increase in the prevalence of type 2 diabetes actuallydecreased somewhat from the previous 2 decades after thischange in 1979, which suggested that the increase in prevalenceof diabetes beyond 1979 was not an artifact of that change. Thus,these data were included in our analysis.
The prevalence of obesity was based on the measured height and weight of a random sample of the civilian noninstitutional-ized population aged ͧ 20 y, and is reported as a percentage ofthe US population with a body mass index (BMI; kg/m2) of ͧ 30.
The data came from the National Health Examination Survey(NHES 1960 –1962); the first, second, and third National Healthand Nutrition Examination Surveys (NHANES I, 1971–1974; FIGURE 1. Change in total carbohydrate consumption (F) and the per-
NHANES II, 1976 –1980; NHANES III, 1988 –1994); and centage of carbohydrate from fiber (vertical bars) in the United States be-tween 1909 and 1997 (17).
Unless stated otherwise, the nutrient content of the US food supply and other nutrition data were obtained from the National In a multivariate nutrient-density model (Table 1)—in which
Nutrient Data Bank, which is maintained by the Center for Nu- total energy, corn syrup, fiber, fat, and protein intakes were trition Policy and Promotion and the Economic Research Service simultaneously included— corn syrup was positively associated of the US Department of Agriculture (20). Nutrient data are based with the prevalence of type 2 diabetes (␤ ҃ 0.0132, P ҃ 0.038), on food disappearance and were calculated with the use of food whereas dietary fiber (␤ ҃ Ҁ13.86, P  0.01) was negatively availability data from the Economic Research Service and on the associated with the prevalence of type 2 diabetes. In contrast, the basis of the nutrient content of the edible portion of the available percentages of energy from protein (P ҃ 0.083) and fat (P ҃ food supply as calculated by the Nutrient Data Laboratory of the 0.79) were not associated with the prevalence of type 2 diabetes Agricultural Research Service. These food-composition data are after adjustment for total energy intake and other dietary vari- the numerical foundation of essentially all public and private ables in the multivariate nutrient-density model.
work in the field of human nutrition (20).
Until 1980, the total energy intake remained relatively con- Regression analysis was performed to examine the correlation stant. Between 1980 and 1997, however, total energy intake between macronutrient consumption and disease rates. A multi- increased by Π500 kcal/d. This increase was due primarily to variate nutrient-density model was used to control for total en- increases in dietary carbohydrate. Specifically, 428 kcal (nearly ergy intake (21). In particular, corn syrup was selected to repre- 80% of the increase in total energy) came from carbohydrates, 64 sent refined carbohydrates in the model, because it is a highly kcal (12% of the increase in total energy) came from protein, and refined substance that is consumed in vast quantities in the only 45 kcal (8% of the increase in total energy) came from fat.
United States in the form of soft drinks, commercial baked goods, This represents a relative increase in consumption of dietary ready-to-eat breakfast cereals, and many other commercially carbohydrates from 48% to 54% of total energy intake over a processed food products. Similarly, dietary fiber was selected 20-y period and a relative decrease in dietary fat from 41% to because it generally is removed during the refining process. All 37% of total energy intake. During the same period, the preva- P values are two sided. The statistical analysis was performed lence of type 2 diabetes increased by 47% and the prevalence of with the use of EPI-INFO (2002; Centers for Disease Control and obesity increased by 80%, indicating a significant positive cor- relation between the percentage of energy from refined carbo-hydrates and the prevalence of type 2 diabetes and obesity.
The total per capita use of caloric sweeteners increased by 86% between 1909 and 1997, and the type of sweeteners used also changed dramatically. Corn syrup sweeteners, which were al- Dietary carbohydrate steadily decreased from 500 g/d in 1909 most nonexistent at the beginning of the century, now comprise to 374 g/d in 1963, largely because of a decrease in the consump-tion of whole grains. Simultaneously, dietary fiber decreased at a greater rate— by nearly 40%. Since 1963, the consumption of Multivariate nutrient-density model for examining the associations carbohydrates steadily increased back to 500 g/d; however, fiber between trends in nutrients and the prevalence of type 2 diabetes in the consumption did not increase proportionately. This finding re- flects an increased consumption of refined carbohydrates over
this time period (Figure 1). From 1963 to 1997, the consumption
of total fat increased nearly 30%, protein consumption increased 8%, and total energy consumption increased 9%.
In a univariate analysis of the available data for the period between 1909 and 1997, a significant correlation with the prev- alence of type 2 diabetes was observed for intakes of dietary fat (r ҃ 0.84 P  0.001), carbohydrate (r ҃ 0.55, P  0.001), protein 1 A positive ␤ coefficient indicates an increased risk of type 2 diabetes, (r ҃ 0.71, P  0.001), fiber (r ҃ 0.16, P ҃ 0.027), corn syrup whereas a negative coefficient indicates a decreased risk of type 2 diabetes.
(r ҃ 0.83, P  0.001), and total energy (r ҃ 0.75, P  0.001).
All values are adjusted for each other. Energy value used for fiber ҃ 4 kcal/g.
FIGURE 4. Increasing prevalence of type 2 diabetes (vertical bars) in the
United States between 1960 and 1997 with increasing carbohydrate intake(F) (14, 17).
FIGURE 2. Change in total carbohydrate consumption in the United
States between 1909 and 1997, reflected by the replacement of whole grains ately to the increase in consumption of refined carbohydrates in (smaller circles) with corn syrup (larger circles) (17).
the United States (Figures 4 – 6) .
Our data also indicate that modern carbohydrates are consid- Π20% of the total daily carbohydrate intake and 10% of the daily erably different from those consumed before the beginning of the total energy intake, which represents an increase of Π2100%.
20th century and that the US food supply has become reliant on These sweeteners have surpassed sucrose as the leading sweet- highly refined carbohydrates as significant sources of energy.
ener in the US food industry and account for much of the rebound The refining process has changed the composition and thus the increase in carbohydrate consumption after the mid-1960s, quality of carbohydrates (22). For example, processing whole largely replacing the losses due to whole grains (Figure 2). There
grains into white flour actually increases the caloric density by was a significant correlation between the percentage of carbo- Œ 10%, reduces the amount of dietary fiber by 80%, and reduces hydrate from corn syrup and the prevalence of type 2 diabetes the amount of dietary protein by almost 30% (23). Refining (r ҃ 0.85, P  0.001; Figure 3).
removes many of the main ingredients, leaving a dietary sub- The multivariate nutrient-density model was modified to de- stance that is nearly pure starchy carbohydrate with fewer nutri- termine the “toxicity” of changing carbohydrate quality. This model included total carbohydrate, the percentage of carbohy- Corn refining in the United States began around the time of the drates from corn syrup, and the percentage of carbohydrates from Civil War with the development of cornstarch (25). In 1866, it fiber. In this model, corn syrup and fiber—potential indicators of was discovered that cornstarch could be converted to glucose, carbohydrate quality—accounted for 18% of the variability in and by 1882 the corn industry was manufacturing “refined corn the prevalence of diabetes when the intake of total carbohydrate sugar.” The remainder of the corn plant (fiber, germ, and protein) that was removed in the refining process was sold for animal feedor for the conversion to corn oil. Corn syrup technology advancedsignificantly with the introduction of enzyme-hydrolyzed prod- DISCUSSION
ucts. In 1921, crystalline dextrose hydrate was introduced. The In this ecologic analysis, in which national data from 1909 to purification and crystallization of glucose meant that, for the first 1997 were used, we found a strong association between an in- time, corn-based sweeteners could compete in some markets that creased consumption of refined carbohydrates in the form of corn had been the sole domain of the sugar industry. In the mid-1950s, syrup, a decreased consumption of dietary fiber, and an increas- the technology for commercially preparing low-conversion ing trend in the prevalence of type 2 diabetes in the United States products such as maltodextrin syrup was developed. The next during the 20th century. Furthermore, our data are consistent inthat obesity and the prevalence of diabetes increased proportion- FIGURE 3. Increasing prevalence of type 2 diabetes (vertical bars) in the
FIGURE 5. Increasing prevalence of obesity [BMI (in kg/m2) Π30;
United States between 1933 and 1997 with increasing per capita percentage vertical bars] in the United States between 1960 and 1997 with increasing of carbohydrate intake from corn syrup (F) (14, 17).
REFINED CARBOHYDRATES AND TYPE 2 DIABETES Health Interview Survey are self-reported, many studies haveindicated excellent agreement between self-reported data anddata from medical records concerning a person’s diabetes status(31–35). The issue of confounding with obesity, physical activ-ity, or both is challenging. Unfortunately, there is no uniformsource of consistent information about physical activity in theUnited States for the period studied. The Behavioral Risk FactorSurveillance Survey has only produced such data since the 1990s(36). Similarly, the first national obesity data were from the early1960s, which provide only 5 usable data points from the NationalHealth Examination Survey and NHANES studies since that FIGURE 6. Increasing prevalence of type 2 diabetes (vertical bars) in the
time. Use of such scant data to control for obesity would lack United States between 1966 and 1997 with increasing consumption of refinedgrains in the form of ready-to-eat cereals (F) (14, 17).
sufficient power to be meaningful. However, because obesity islikely an intermediary for the development of type 2 diabetes,control for this variable would likely negate the contribution of development involved the enzyme-catalyzed isomerization of any macronutrient. Thus, the control for obesity may be a case of glucose to fructose. The commercial production of high-fructose overadjustment. These potential confounders will hopefully be corn syrup (HFCS) began in 1967, at which time the fructose teased out by future prospective studies.
content of the syrup was Ȃ15%. Further research enabled the Classifying foods according to the physiologic effects ob- industry to develop a higher-conversion HFCS that had a fructose tained directly from metabolic experiments is useful in under- content of 42%. After a few more modifications, an HFCS with standing the health effects of diets (37). Indeed, the concept that a fructose content of 55% became the sweetener of choice for the carbohydrates vary in quality is not new (ie, carrots are not the soft drink and ice cream industries, and an HFCS with a fructose same as cake) and appears to have important clinical signifi- content of 90% became a frequent choice for use in “natural” and cance. The glycemic index (GI) is a relative in vivo measure of “light” foods. By 2002, HFCS sweeteners represented Œ 56% of the plasma glucose response to a standardized amount of carbo- hydrate. The glycemic load (GL) is a product of the GI and the The results of this ecologic study need to be interpreted in the total amount of carbohydrate consumed, incorporating the ef- context of the study’s strengths and weaknesses. Ecologic stud- fects of both the quality and quantity of carbohydrate intake. A ies, such as observational studies of individual persons, are sus- growing body of evidence suggests that a high dietary GL in- ceptible to confounding. The so-called ecologic fallacy may oc- creases the risk of obesity, glucose intolerance, dyslipidemia, cur when inferences are made about individual persons on the type 2 diabetes, and coronary heart disease (38 – 49).
basis of solely population-level data. Our analysis may also have In several small-scale metabolic trials, refined grains have been limited by the use of food disappearance data at the popu- been shown to cause a significant increase in insulin secretion lation level that are indirectly related to intakes at individual and the postprandial glucose response (50 –54). In general, sub- levels. To address these issues, our analyses used only stituting high-fiber, low-GI foods for high-GI foods significantly population-level variables (energy from macronutrients) to pre- improves fasting insulin concentrations, the postprandial insulin dict the only ecologic outcome (population-level prevalence of response, glycemic control, and lipid profiles (55– 65). Corn type 2 diabetes). Because we avoided inferences about individualpersons from population data, no cross-level bias should occur syrup largely consists of the monosaccharide fructose, in contrast (26, 27). Also, because we applied food disappearance data only with sucrose—which is a disaccharide of fructose and glucose.
from within the United States and did not compare regional, Fructose, unlike sucrose, has been directly linked to insulin re- international, or ethnic group data, the bias, if any, would at least sistance in small human and animal studies and has been impli- be uniform for the same population. Although food disappear- cated in every metabolic abnormality associated with the meta- ance data are an indirect measure of individual consumption, bolic syndrome (66 – 69). Corn syrup is now endemic in the US these data have been calculated annually for more than a century, food supply, which places an unprecedented biochemical evo- making them the only consistent data available for identifying lutionary pressure for processing fructose.
Several prospective cohorts have incorporated the concept of To establish a causal diet-disease relation, however, one must GI in assessing the relations between dietary carbohydrate and examine evidence from a variety of sources and look for con- the risk of type 2 diabetes. In the Nurses’ Health Study, the gruence between these sources (28). This is especially important multivariate-adjusted relative risk of type 2 diabetes during 6 y of when interpreting population-level analyses of macronutrient follow-up was 1.37 (95% CI: 1.09, 1.71) for an increase in GI of intakes because the specific effects of individual macronutrients 15 units and was 1.47 (95% CI: 1.16, 1.86) for extreme quintiles and the generic effect of total energy intakes may not be evident of dietary GL. Women with both a high dietary GL and a low in individual-based studies with small sample sizes (29, 30). To cereal fiber intake were at an even higher risk of type 2 diabetes this end, such ecologic studies have advantages over population- (relative risk: 2.43; 95% CI: 1.12, 5.27) (70). In the Health Pro- based interventions for identifying potential diet-disease rela- fessionals’ Follow-up Study, the multivariate-adjusted relative risk was 1.37 (95% CI: 1.02, 1.83) in 6 y of follow-up for extreme Changes in diagnostic criteria and screening practices for type quintiles of dietary GL and 2.17 (95% CI: 1.04, 4.54) for the 2 diabetes may limit the ability to determine the extent of effect combination of a high GL and a low intake of cereal fiber (71). In due solely to dietary changes. To reduce this bias, we excluded the Iowa Women’s Health Study, however, neither the GI nor the data beyond 1997. Although prevalence data from the National GL were related to the risk of type 2 diabetes in 6 y of follow-up, although dietary fructose and glucose were significantly associ- physiological basis for carbohydrate exchange. Am J Clin Nutr 1981; Our analysis confirmed that during the past century, especially 15. Jenkins DA, Jenkins AL. The glycemic index, fiber, and the dietary treatment of hypertriglyceridemia and diabetes. J Am Coll Nutr 1987; the past 20 y, the American diet has undergone a dramatic change. Furthermore, our data indicate that, during the same 16. Brand Miller J. Importance of glycemic index in diabetes. Am J Clin Nutr period, type 2 diabetes has reached epidemic proportions, exert- ing a substantial health burden on society. These population- 17. Centers for Disease Control and Prevention. Diabetes surveillance 1999.
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Source: http://helios.hampshire.edu/~cjgNS/sputtbug/416K/Energy%20Reg/Gross.pdf