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AMERICAN JOURNAL OF LIFESTYLE MEDICINE OnlineFirst, published on August 19, 2010 as doi:10.1177/1559827610378960

vol. X • no. X American Journal of Lifestyle Medicine

John S. White, PhD, John P. Foreyt, PhD, Kathleen J. Melanson, PhD, RD, LD, and Theodore J. Angelopoulos, PhD, MPH High- Corn : Controversies and Common

Abstract: High-fructose is Keywords: high-fructose corn syrup; controversies that started in 2004 when often mischaracterized and misunder- HFCS; ; ; ; Bray et al1 suggested that there might be stood. This sweetener was introduced sweeteners; a link between high-fructose corn syrup into the supply in the consumption and obesity. in the late 1960s as a liquid sweet- igh-fructose corn syrup is one In their 2004 article published in the ener alternative to sucrose and existed of the most misunderstood food American Journal of Clinical Nutrition, in relative obscurity for many years. Hingredients in all of nutrition. Bray and colleagues1 argued that the dra- It carries the designations “Generally High-fructose corn syrup (HFCS) was first matic increase in the prevalence of obe- Recognized As Safe” (GRAS) and developed in the mid-1960s and, because sity in the United States over the past “natural” from the US Food and Drug of its unique physical and functional 30 years occurred during the same time- Administration. In 2004, several inves- properties, was widely embraced by food frame as a corresponding increase in the tigators suggested that high-fructose corn syrup might be linked to the increased prevalence of obesity in the United States. Subsequent human stud- High-fructose corn syrup is one ies have shown no unique link between high-fructose corn syrup and obesity. In of the most misunderstood food composition, high-fructose corn syrup, sucrose, , invert , and con- ingredients in all of nutrition. centrated are essentially interchangeable, and human studies to date have shown no significant dif- formulators. The use of high-fructose consumption of high-fructose corn syrup. ferences in metabolic, endocrine, hor- corn syrup has had rapid growth over the Even though a temporal association does monal, or appetitive responses to these past 30 years principally as a replacement not establish cause and effect and high- caloric sweeteners. This review explores for sucrose (table sugar). Its use reached fructose corn syrup and sucrose are vir- the metabolic and nutritional effects a peak in 1999 but has been in decline tually the same from a composition and of high-fructose corn syrup with a par- since then. Having existed as a benign biochemical point of view, a number of ticular emphasis on its relationship to and noncontroversial for more researchers began to investigate whether sucrose, the sweetener it replaced in than 30 years, high-fructose corn syrup there was something unique about high- many food products. has recently been caught up in a series of fructose corn syrup when compared to

DOI: 10.1177/1559827610378960. Manuscript received April 12, 2010; revised June 3, 2010; accepted June 28, 2010. From White Technical Research, Argenta, Illinois (JSW); Department of Medicine, Behavioral Medicine Research Center, Baylor College of Medicine, Houston, Texas (JPF); Department of Nutrition and Food Sciences, University of Rhode Island, Kingston (KJM); and Department of Health Professions, Center for Lifestyle Medicine, University of Central Florida, Orlando (TJA). Address correspondence to Theodore J. Angelopoulos, PhD, MPH, Department of Health Professions, Center for Lifestyle Medicine, University of Central Florida, PO Box 162205, Orlando, FL 32816; e-mail: [email protected]. For reprints and permissions queries, please visit SAGE’s Web site at http://www.sagepub.com/journalsPermissions.nav. Copyright © 2010 The Author(s)

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Table 1. Composition of Common Nutritive Sweeteners

Component HFCS-42, % HFCS-55, % Corn Syrup, % Fructose, % Sucrose, % Invert Sugar, %a Honey, %

Fructose 42 55 0 100 50 45 49

Glucose 53 42 100 0 50 45 43

Others 5b 3b 0 0 0 10c 5d

Moisture 29 23 20 5 5 25 18

From White J. Straight talk about high fructose corn syrup: what it is and what it ain’t. Am J Clin Nutr. 2008;88(suppl):1716S. Used with permission of author. HFCS, high-fructose corn syrup. aSucrose-based sweetener in which the bond between and fructose is partially or fully hydrolyzed (inverted) by or (). bReadily hydrolyzable of glucose. cUnhydrolyzed sucrose. dSucrose and minor amounts of other .

sucrose, which might create a unique the modern scientific understandings of supplied in liquid form rather than the hazard for obesity or other metabolic high-fructose corn syrup, with particular solid form of sucrose) and other beneficial problems. This was particularly important emphasis on the comparison of high- physical and functional properties, the use because many of the hypotheses to date fructose corn syrup to sucrose, the sub- of high-fructose corn syrup achieved sub- had been based on comparisons of pure stance it was designed to replace in cer- stantial growth over the next 30 years. fructose to pure glucose, which are not tain and beverages. High-fructose corn syrup served indus- common in the food supply.2-4 try in relative obscurity for many years. There is now abundant research demon- This is not surprising, given that it is vir- Discussion of the strating no short-term differences between tually identical to sucrose: both con- Scientific Evidence high-fructose corn syrup and sucrose in sist of roughly equal amounts of glucose any parameter yet measured in human We address issues related to high- and fructose (see Table 1), have equal beings.2,4-10 This includes work in both fructose corn syrup by posing and , have equal per gram, lean5,8-10 and obese6,7 individuals. In addi- answering a series of commonly asked and are metabolized virtually identically. tion, the published proceedings from sev- questions about this sweetener. In our During this time, multiple expert scientific eral different conferences that brought discussion, we draw on published panels concluded that sucrose, high- together leading researchers in the field of research and published proceedings from fructose corn syrup, and their compo- nutritive sweeteners have provided uni- 2 important, contemporary symposia on nents, fructose and glucose, did not pose form scientific opinion that, from a meta- sweeteners. any significant health risk with the sole bolic standpoint, there is nothing unique exception of promoting dental caries.4,19-22 linking high-fructose corn syrup to obe- What Is High-Fructose Added sugars have since been catego- sity or other metabolic problems when Corn Syrup? rized as “discretionary calories,” and compared to other nutritive sweeteners, High-fructose corn syrup is a liquid moderate intake is recommended.17,23,24 including sucrose, honey, and fruit sweetener developed as a liquid alterna- The question addressed in this article is concentrates.3,8,11-15 Both the American tive to sucrose (table sugar).18 It is used whether any one caloric sweetener, spe- Medical Association,16 which explored in many foods and beverages to enhance cifically high-fructose corn syrup, is meta- whether there was a unique link between flavors or sweetness. In baked goods, it bolically or nutritionally unique. high-fructose corn syrup and obesity, and enhances moisture retention and brown- Glucose, fructose, and sucrose from fruit the American Dietetic Association have ing. Early developmental work on high- or honey have been part of the human concluded that high-fructose corn syrup is fructose corn syrup started in the 1960s, diet for millennia. Sucrose has been pro- not a unique cause of obesity.17 and commercial applications began in the duced commercially from The purpose of the current review is to late 1960s and early 1970s. Because of and sugar beets for hundreds of years provide practicing physicians and allied a variety of properties such as ease of and continues to serve as the bench- health care workers with a summary of handling (high-fructose corn syrup is mark against which other sweeteners are

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measured. Worldwide, 9 times as much very different from “regular” corn syrup The hypothesis that the replace- sucrose is consumed as high-fructose and pure fructose: corn syrup is glu- ment of sucrose by HFCS in bev- corn syrup. It would likely surprise many cose based with no fructose and low erages plays a positive role in to learn that even in the United States, sweetness, whereas the latter contains obesity is not supported on the more sucrose is consumed per capita than no glucose and is used only in specialty basis of its composition, bio- high-fructose corn syrup.15,23,25 The fact applications. The name high-fructose logic actions, or short-term effects that obesity is as prevalent in countries corn syrup does not mean the fructose on food intake. Had the hypoth- that use little or no high-fructose corn content is much higher than other sweet- esis been phrased in the con- syrup as in the United States substantially eners, but that name was given because verse, namely that replacing HFCS weakens the Bray hypothesis1 of a unique its fructose content is higher than the with sucrose in beverages would link between high-fructose corn syrup corn syrup from which it was derived. be seen as a to the obe- and obesity. These distinctions are particularly impor- sity epidemic, its merit would High-fructose corn syrup proved to tant because considerable confusion have been seen more clearly. Put be an attractive alternative to sucrose has risen in both the medical literature simply, a proposal that a return because of its stability in acidic foods and lay literature, where improper refer- to sucrose containing beverages and beverages (eg, soft ). It is ences and comparisons between regular would be a credible solution to the also an ingredient derived from corn, a corn syrup, pure fructose, and high- obesity epidemic would have been dependable and renewable agricultural fructose corn syrup are frequently made. met with outright dismissal. material grown abundantly in the mid- The proper comparison is between high- What Are the Findings western region of the United States. In a fructose corn syrup and sucrose. of Current Research sense, high-fructose corn syrup should on High-Fructose Corn be viewed as “corn sugar.” From this per- Is Consumption of High- Syrup and Sucrose? spective, it could properly be viewed as Fructose Corn Syrup The original Bray hypothesis1 received a reasonable agricultural alternative to Linked to Obesity? additional traction from research per- sugar (sucrose) produced from sugarcane As indicated earlier, Bray et al1 sug- formed by Teff et al,27 who employed a and sugar beets. gested in 2004 that there might be a model in which individuals consumed How Does the Composition link between increased consumption of 25% of calories either as pure fructose of High-Fructose Corn high-fructose corn syrup and dramatic or pure glucose in the context of mixed- Syrup Compare With Other increases in obesity in the United States. meals over 1 day. Individuals Nutritive Sweeteners? These authors subsequently acknowl- who consumed 25% of calories from glu- It is important to understand that edged that their opinion piece was cose experienced a spike in glu- essentially all nutritive sweeteners in intended to be provocative and stir a sci- cose and when compared to common use in the American diet are entific debate. Indeed it did. Multiple individuals who consumed 25% of cal- similar combinations of glucose and fruc- studies from a variety of research labo- ories from pure fructose. The reduction tose. Two main forms of high-fructose ratories,2,5-10 as well as proceedings from in meal-dependent insulin secretion in corn syrup are in common use. HFCS-55, 2 major symposia on nutritive sweeten- individuals who consumed 25% of calo- which is composed of 55% fructose, 42% ers3,8,11-15 have all uniformly concluded ries from pure fructose resulted in sup- glucose, and 3% glucose polymers, is the that, based on current science, there is no pressed circulating levels of leptin and form of high-fructose corn syrup com- unique association between high-fructose less ghrelin suppression. It was argued monly used in soft drinks. HFCS-42, con- corn syrup and obesity. Furthermore, the on the basis of this experiment that con- sisting of 42% fructose, 53% glucose, and American Medical Association studied sumption of fructose could lead to over- 5% glucose polymers, is the common this issue for over a year and concluded consumption of calories by attenuating form of high-fructose corn syrup used in that high-fructose corn syrup “does not insulin and leptin concentrations, as well baked goods. appear to contribute more to obesity than as ghrelin suppression.27 When these Table 1 provides the carbohydrate other caloric sweeteners.”16 Finally, the experiments were repeated using real- composition of common nutritive sweet- American Dietetic Association17 stated, world diets comparing 25% of calories eners. As can be observed from the data “No persuasive evidence supports the from high-fructose corn syrup to 25% of in this table, HFCS-55 and HFCS-42 are claim that the high fructose corn syrup is calories from sucrose in the context of very similar in composition to sucrose, a unique contributor to obesity.” mixed-nutrient meals over the course of invert sugar, and honey. From a prac- Perhaps the most succinct synop- a day, all of the differences in short-term tical standpoint, all 4 of these nutritive sis of this issue came from G. Harvey regulating levels disap- sweeteners are essentially interchange- Anderson26 in an editorial for the peared.5 The contrast between these 2 able in many foods and beverages. High- American Journal of Clinical Nutrition, sets of experiments carried out with virtu- fructose corn syrup and sucrose are both where he wrote: ally identical research procedures but

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different sugar comparisons (pure glu- A few animal studies have compared cose and pure fructose27 [not commonly effects of high-fructose corn syrup and Figure 1. found in the diet] or high-fructose corn sucrose over longer terms and have Per capita daily caloric intake (US 5 syrup and sucrose [commonly found raised questions about risks of obesity Department of Agriculture Economic in the diet]) underscores the danger of and with high-fructose Research Service loss-adjusted 29 extrapolating data from pure fructose and corn syrup. However, the doses used availability), 1970-2005. pure glucose into the real-world situation far exceed any that would be consumed of high-fructose corn syrup and sucrose. by humans. Longer-term human research 3000 In addition, in neither experiment did the is currently under way comparing the 2500 participants express differences in appe- effects of common sweeteners at typi- tite either during testing or the day after. cal intake levels in a broad range of test 2000 A comparison between high-fructose participants. 1500 corn syrup and sucrose has also been It must be recognized that most exper- made on appetite and caloric consump- imentation in support of a unique met- 1000 5 tion at subsequent meals. Recent research abolic role for high-fructose corn syrup 500 has shown no difference between high- in obesity and related diseases relies on fructose corn syrup and sucrose on appetite test diets featuring exaggerated amounts 0 1970 1980 1990 2000 2005 or caloric consumption at the next meal.9,10 of pure fructose at levels never encoun- It has also been argued that high- tered in the human diet. Marriott et al30 Per capita caloric intake fructose corn syrup consumption may recently estimated mean and 95th percen- increase levels of .28 If this tile intakes at 9% and <18% of total cal- were true, it would be cause for con- ories, respectively. Experimental diets cern because there is a purported link featuring 25% to 40% or 60+% of calories caloric intake. And although between elevated levels of uric acid and as fructose are commonly used in human consumption increased during this period— some underlying components of the and animal studies, respectively. Although along with all other macronutrients— 28 metabolic syndrome. Evidence for a exaggerated levels generate reportable it should be noted that as a percentage linkage between pure fructose consump- differences between fructose and controls, of total calories consumed, added sug- tion at high levels and increased uric acid they are not physiologically relevant to ars actually declined slightly, whereas levels comes from animal experiments humans and should not be used to judge added and flours/cereals modestly 28 performed by Johnson et al, in which risk or guide public health decisions. increased.32 Thus, Americans are eating laboratory rats were fed more than 60% more of everything than in 1970, when of calories from pure fructose. In this If High-Fructose Corn Syrup high-fructose corn syrup was introduced Is Not Causing the Obesity model, it was demonstrated that uric acid to the food and beverage industry.15 increases. However, research using high- Epidemic, What Is? fructose corn syrup and sucrose at 25% Numerous studies, including those pro- What Should the Lifestyle of calories (far above typical human con- viding the basis for the Dietary Guidelines Physician and Practitioners sumption levels) over the course of 1 day for Americans 200524 and the Surgeon Know About High-Fructose did not show any differences or abnor- General’s report on obesity,31 have pro- Corn Syrup in Sports Drinks? mal elevations in uric acid levels.6 vided compelling evidence that the obesity High-fructose corn syrup and other It has been suggested that high lev- epidemic in the United States (and other sweeteners are commonly found in els of fructose consumption may also industrialized countries) is multifactorial in sports performance drinks, where they cause abnormalities, particularly to origin and can be largely attributed to the have been proven to maintain glucose postprandial elevations in .10 significant increases in per capita and provide energy sub- Once again, data supporting this asser- intake and decreases in physical activity, strates to maintain or improve exercise tion come from experiments that use which have occurred in the United States performance over long durations. Of par- high levels of pure fructose (typically and other industrialized countries over the ticular importance, it has been shown 25% of calories). Recent experiments past 30 years. As can be seen in Figure 1, that consumption of the combination of comparing mixed-nutrient meals with average caloric consumption in the United glucose and fructose results in greater 25% of calories from either high-fructose States increased 25% between 1970 and exogenous carbohydrate oxidation and corn syrup or sucrose in both lean and 2005.32 Couple this increase in caloric con- better athletic performance than when obese women again showed no short- sumption with declines in levels of physical either is consumed term differences in triglycerides, nor were activity, and an environment is set up to alone.33,34 The added calories from high- there any significant elevations in post- promote weight gain. Today, added sugars fructose corn syrup or other carbohy- prandial triglycerides.7 account for approximately 17% of daily drates in these settings are probably less

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important than the performance bene- moderation, most notably the Dietary sweetened with fructose, glucose, sucrose, fits that come from the addition of these Guidelines for Americans 2005.24 or high-fructose corn syrup. Am J Clin Nutr. 2008;88(suppl):18335S. carbohydrates. 6. High-fructose corn syrup should not 4. Tappy L, Lê K-A. Metabolic effects of fruc- be confused with pure fructose or reg- tose and the worldwide increase of obe- Summary ular corn syrup. Research conducted sity. Physiol Rev. 2010;90:23-46. using a pure fructose model should 5. Melanson K, Zukley L, Lowndes J, With this background on high-fructose not be extrapolated to high-fructose Nguyen V, Angelopoulos T, Rippe J. corn syrup, what should lifestyle physi- corn syrup. In retrospect, high-fructose Effects of high-fructose corn syrup and cians and practitioners understand as key corn syrup was probably poorly sucrose consumption on circulating glu- cose, insulin, leptin, and ghrelin and messages to impart to their patients? named because the name implies that We suggest that the following key fac- on appetite in normal-weight women. it must contain a preponderance of Nutrition. 2007;23:103-112. tors be emphasized: fructose, but this is not the case. The 6. Lowndes J, Zukley L, Nguyen V, Angelo- 1. From a compositional standpoint, more proper comparison is between poulos T, Rippe J. The effect of high- high-fructose corn syrup and sucrose, fructose corn syrup on uric acid levels in high-fructose corn syrup, sucrose, obese women. Obesity. 2007;15(suppl):498-P. invert sugar, honey, and concen- both of which contain approximately 50% glucose and 50% fructose. 7. Zukley L, Lowndes J, Melanson K, trated fruit juices are all virtually inter- Nguyen V, Angelopoulos TJ, Rippe JM. changeable. All of these nutritive 7. The addition of carbohydrates to The effect of high-fructose corn syrup on sweeteners are composed of approx- sports drinks may provide a bene- triglycerides in obese females. Obesity. imately 50% glucose and 50% fruc- fit by maintaining glucose homeosta- 2007;15(suppl):500-P. tose. All are absorbed similarly, have sis, providing substrates for sustained 8. Angelopoulos TJ, Lowndes J, Zukley L, energy release and increased rates of et al: The effect of high-fructose corn syrup similar sweetness, and have the same consumption on triglycerides and uric acid. number of calories per gram. exogenous carbohydrate oxidation, J Nutr. 2009;139:1242S-1245S. which may be particularly valuable 2. From a metabolic standpoint, high- 9. Soenen S, Westerterp-Plantenga MS. No fructose corn syrup and sucrose are for endurance events. differences in satiety or energy intake virtually identical by all endpoints 8. Longer-term research is currently under after high-fructose corn syrup, sucrose, way comparing the effects of common or preloads. Am J Clin Nutr. measured to date. These include 2007;86:1586-1594. serum glucose and insulin, leptin and sweeteners at typical intake levels in a broad range of test participants. 10. Stanhope K, Griffen S, Bair B, Swarbrick M, ghrelin, triglycerides, and uric acid. Keim N, Havel P. Twenty-four-hour endo- 3. There is now overwhelming scien- crine and metabolic profiles follow- tific agreement that high-fructose corn As sources of authority, it is important ing consumption of high-fructose corn syrup is not a unique cause of obe- that physicians and other health care pro- syrup-, fructose-, and glucose-sweetened fessionals recognize that controversies beverages with meals. Am J Clin Nutr. sity when compared to other nutritive 2008;87:1194-1203. sweeteners at typical intake levels. arise and are perpetuated in nonrefereed venues such as the Internet. Now that 11. Fulgoni V. High-fructose corn syrup: The original hypothesis that high- everything you wanted to know, but fructose corn syrup was uniquely abundant science exists in the area of were afraid to ask. Am J Clin Nutr. related to obesity was based on a high-fructose corn syrup in general and 2008;88(suppl):1715S. temporal association and did not its comparison to sucrose in particular, 12. White J. Straight talk about high-fructose establish cause and effect. Numerous lifestyle physicians can serve as a trusted corn syrup: what it is and what it ain’t. Am J Clin Nutr. 2008;88:1716S-1721S. subsequent short-term metabolic trials source of commonsense advice in this important area. AJLM 13. Duffey KJ, Popkin BM. High-fructose corn and appetite studies now suggest that syrup: is this what’s for dinner? Am J Clin there is no unique link between high- Nutr. 2008;88(suppl):1722S-1732S. fructose corn syrup and obesity. References 14. Murphy SP. The state of the science on 4. Americans are eating more of dietary sweeteners containing fructose: 1. Bray GA, Nielsen SJ, Popkin BM. everything than they did 30 years summary and issues to be resolved. J Nutr. Consumption of high-fructose corn 2009;139:1269S-1270S. ago—and compared with 3 decades syrup in beverages may play a role in 15. White JS. Misconceptions about high- ago, added sugars now make up less the epidemic of obesity. Am J Clin Nutr. fructose corn syrup: is it uniquely respon- of the diet as a percentage of total 2004;79:537-543. sible for obesity, reactive dicarbonyl calories than fats and cereals. 2. Melanson K, Angelopoulos T, Nguyen V, compounds, and advanced end- 5. All nutritive sweeteners should be Zukley L, Lowndes J, Rippe J. High- products? J Nutr. 2009;139:1219S-1227S. fructose corn syrup, energy intake, and used in moderation, as should caloric 16. American Medical Association. Report 3 of appetite regulation. Am J Clin Nutr. the Council on Science and Public Health foods and ingredients from all mac- 2008;88(suppl):1738S. (A-08): The Health Effects of High Fructose ronutrient sources. Many strategies 3. Stanhope K, Havel P. Endocrine and met- Corn Syrup. Chicago: American Medical have been developed to promote abolic effects of consuming beverages Association; 2008.

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