Evidence Review
Sugar or High Fructose Corn Syrup—What Should Nurses Teach Patients and Families? Linda L. Sobel, RN, PhD • Elizabeth Dalby, BS
ABSTRACT Keywords high fructose corn syrup, blood glucose levels, high sugar, lipids
Background: There is lack of consensus in the lay literature to support consumption of table sugar as a preferred sweetener when compared to high fructose corn syrup (HFCS). Aims: The purpose of this study was to search the literature for evidence to determine the health effects of consumption of table sugar (sucrose) and HFCS on blood glucose, lipid levels, obesity, and appetite as well as to make recommendations for patient and family teaching of those at risk for developing negative health outcomes, including coronary heart disease. Methods: Nursing and health-related databases, including CINAHL, PubMed, Cochrane Central Registry of Controlled Trials, and Health and Wellness were searched for research articles, which were compared and evaluated for purpose, sample size, procedure, findings, and level of evidence. Findings: Five studies that met inclusion criteria were evaluated. No difference was found in changes in blood glucose levels, lipid levels, or appetite between table sugar consumption and HFCS consumption. When only fructose was consumed, lipid levels were significantly increased. Linking Evidence to Action: The evidence suggests that fructose, found in both table sugar and HFCS, has a negative effect on health outcomes. Clinicians should teach patients and families that all sugar consumption should be closely monitored and kept below the 40 g/day recommended by the World Health Organization.
BACKGROUND As concern about the ever-increasing incidence of obesity and development of Type 2 diabetes mellitus continues to escalate, the role of high fructose corn syrup (HFCS) as a food additive and sweetener has been examined more carefully. Popular lay literature ascribes many ill effects of HFCS consumption, but with little cited research to support these claims. When nurses and other clinicians teach patients and families about health dietary choices, they commonly provide information about saturated and unsaturated fats, fiber, caloric consumption, and salt. Sugar may be discussed within the context of diabetes mellitus education, but HFCS is rarely mentioned, often because of an assumption that HFCS is a fructose product that does not have the same effects on metabolism as table sugar.
What is Table Sugar? Table sugar, also known as sucrose, is one of three common disaccharides found in a typical diet. Other common disaccharides are maltose and lactose. Disaccharides are two conjoined carbohydrate molecules. Maltose is composed of two glucose molecules and lactose is composed of glucose and galactose. Sucrose is chemically composed of glucose and fructose in equal proportions (Gropper, Smith, & Groff, 2009)
126
Sucrose is extracted from sugar cane or beet juice, and is the common sugar we sprinkle on our food and add to our drinks and baked goods. Sucrose is also naturally found in fruit and fruit juice, honey, agave nectar, and maple syrup (Gropper et al., 2009).
Absorption and utilization of glucose and fructose. Glucose is absorbed from the duodenum into the vascular space with the aid of a hexose transporter that regulates the rate of absorption. As blood glucose levels rise, insulin is released from the pancreas to facilitate diffusion of glucose into muscle and fat cells, where glucose is converted to pyruvate through a process of glycolysis before entering the Citric Acid cycle for conversion to energy for cellular work (Gropper et al., 2009). Fructose differs from glucose in that it can enter glycolysis directly, and is not subject to the rate-limiting action of the hexose transporter (Gropper et al., 2009). Fructose is absorbed into the small intestine via passive diffusion. To maintain passive diffusion, blood concentration of fructose must remain low (Gropper et al., 2009). To maintain low fructose concentrations, the liver immediately takes up fructose to allow for continued fructose absorption from the gut. Unlike glucose, fructose does not stimulate insulin release. When fructose is absorbed by the liver, it readily enters the metabolic pathway and, if no energy is needed, is converted into a Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Evidence Review substance called acetyl CoA. When acetyl CoA builds up in liver cells, metabolism is pushed toward triglyceride production and formation of very low density lipoproteins (VLDLs) for transfer of these triglycerides into the bloodstream. Accordingly, consumption of large amounts of fructose has been associated with marked increases in serum triglyceride and VLDL levels (Parks & Hellerstein, 2000).
WHAT IS HFCS? HFCS is a processed caloric sweetener derived from corn, first introduced into the American diet in the early 1970s, that has become an industrially popular substitute for crystalline sucrose in the United States (Bray, Nielsen, & Popkin, 2004; White, 2008). After initial purification, an enzyme is added to corn starch to break the starch chains into simple sugars, most of which are glucose. In a series of steps using synthetic enzymes, a majority of this glucose is converted to fructose, a chemical similar to glucose that is found naturally in fruit. Usually this product is then mixed with low fructose corn syrup to create a mixture that is anywhere from 42% to 55% fructose to glucose, depending on its application in either solid food or in liquids. HFCS is valued by the food industry for its stability, its ability to dissolve easily in liquids, and, most of all, its low cost. It is important to note that HFCS and corn syrup are different products. Corn syrup is 100% glucose and contains no fructose (White, 2008). In recent years, the lay literature has targeted HFCS as a perpetrator of various health problems related to its consumption. Many claim that HFCS is metabolized differently than sucrose because HFCS is composed of free glucose and fructose molecules instead of bound fructose and glucose. Some simply claim there may be byproducts present in HFCS that influence triglyceride and lipid levels, and satiety or appetite. Alternatively, there are those who report that HFCS is not different than table sugar and that the public need not be concerned about consuming foods and beverages to which HFCS has been added. Currently, there is no literature comparing HFCS and table sugar to guide nurses and other clinicians as they teach their patients and families to consume healthy diets.
PURPOSE The purpose of this research is to synthesize the literature comparing the relationships of HFCS consumption and table sugar consumption with increased blood glucose levels, appetite, lipidemia or triglyceride levels, and obesity or weight gain in healthy adults. A PICO format (Fineout-Overholt, Melnyk, & Schultz, 2005) was used to develop the research question: Is there a relationship in (P) healthy adults who (I) consume HFCS (C) compared to those who consume table sugar and (O) blood glucose levels, appetite, lipidemia or triglyceride levels and obesity or weight gain. Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
DEFINITION OF TERMS HFCS is a mixture of glucose and fructose and is used as a sweetening additive for food and beverages. HFCS added to beverages is usually 45% glucose and 55% fructose, whereas HFCS added to food is usually 53% glucose and 42% fructose (Hein, Storey, White, & Lineback, 2005). Blood glucose level is the amount of glucose found in a sample of blood, obtained by either a finger-stick or venous sampling, and measured as mg/dl (Kee, 2005). Lipoprotein levels are the measure of varied lipids including plasma cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), VLDL, and plasma triglyceride (Kee, 2005). Appetite is conceptually defined as the desire or motivation to eat, measured by a 10-cm or 100-mm visual analog scale (VAS) ranging from “not at all” on the left to “extremely” on the right (Soenen & Westerterp-Plantenga, 2007). Appetite and food intake are also measured by evaluation of gherlin levels, a hormone produced in the stomach, which increases with hunger and may stimulate appetite, and is associated with increased short-term appetite and increased food intake (Wren et al., 2001). Overweight and obesity are defined as abnormal or excessive fat accumulation that may impair health. Body mass index (BMI) is a simple index of weight-for-height that is commonly used to classify overweight and obesity in adults. It is defined as a person’s weight in kilograms divided by the square of his height in meters (kg/m2 ). The WHO defines overweight as a BMI greater than or equal to 25, and obesity as a BMI greater than or equal to 30 (World Health Organization, 2013).
METHODS Using Cooper’s (1998) framework for synthesizing literature, a systematic review of the health-related research literature was conducted to retrieve evidence to support the influence of HFCS on health outcomes. The framework identifies five stages of research synthesis: (a) problem formulation; (b) search for literature addressing the problem, also known as data collection; (c) data evaluation of quality and level of evidence; (d) analysis and interpretation of findings; and (e) presentation and dissemination. Cooper’s framework supports the review and synthesis of separate research studies examining the relationships between HFCS and blood glucose levels, lipid or triglyceride levels, appetite and obesity as compared to consumption of table sugar in adult humans. The initial search for literature addressing health effects of HFCS was done with no year limitations in order to identify appropriate databases and keywords. These terms were then used to develop search criteria to include all published articles between 1983 and 2010. A third review was conducted in 2011 with no new additional research noted.
Electronic Search for Literature This systematic review included a comprehensive search of CINHAL, PubMed, Cochrane Central Registry of Controlled
127
Sugar or High Fructose Corn Syrup
Trials, and Health and Wellness databases. Search terms were: high fructose corn syrup, sugar, high fructose corn syrup and blood glucose levels, high fructose corn syrup and lipid and triglyceride levels, high fructose corn syrup and appetite, high fructose corn syrup and obesity, and high fructose corn syrup and nursing. In addition, the term sugar was searched with each of the previously noted terms. Reference lists of research reports were reviewed and useful articles were retrieved. The search began with inclusion of all retrieved articles. To review a comprehensive population of studies, 60 articles were retrieved, fully read, and critiqued. Opinion articles, letters to the editor, animal studies, and others not presenting original research were excluded, as was research involving unhealthy individuals, individuals with diabetes mellitus, and children and adolescents. After exclusion criterion was applied, research articles published between 1990 and 2010 were thoroughly reviewed for inclusion. Research from varied health-related disciplines was reviewed including dietetics, exercise physiology, and diabetes care. No nursing research literature was found to compare the effects of HFCS and sugar on health.
Data Evaluation of Quality and Level of Evidence For each study included in this systematic investigation, the reviewer extracted: author names, journal title and publication year, study purpose, description of the sample, research procedure, and relevant findings. In addition, in an attempt to evaluate research studies for the best evidence available to answer the PICO question, levels of evidence as described by Fineout-Overholt et al. (2005) were determined. Of the 60 articles retrieved, five met the inclusion criteria. Abstracts of acceptable studies were evaluated for level of evidence and findings by two independent reviewers. Disagreements were discussed until consensus was reached. Two studies (Melanson et al., 2007; Stanhope et al., 2008) examined two outcome variables of interest to this review; blood glucose, and appetite. In addition, Stanhope et al. (2008) compared the association of sucrose and HFCS to triglyceride levels. No studies comparing sucrose and HFCS and a relationship specifically to weight gain were found. Most studies were excluded because they were opinion articles, studies that examined other outcomes than the ones identified for this systematic review, or animal studies. The accepted studies (Akhavan & Anderson, 2007; Melanson et al., 2007; Mitchell, Braun, Pizza, & Forrest, 2000; Soenen, 2007; Stanhope et al., 2008) are summarized in Table 1. Publication dates ranged from 2000 to 2008. Much of the earlier research focused on evaluation of fructose consumption by persons with Type 1 diabetes mellitus. This earlier work was excluded because it focused on nonhealthy adults. All studies used cross-sectional designs. No longitudinal designs were found. All five studies were ranked as Level III evidence (Fineout-Overholt et al., 2005). Three studies (Melanson et al., 2007; Mitchell et al., 2000; Stanhope et al., 2008) were supported by CocaCola and PepsiCola.
128
ANALYSIS AND INTERPRETATION OF FINDINGS Selected research was reviewed and critiqued to summarize the association between consumption of HFCS and sugar and blood glucose levels, lipid levels, appetite, and weight gain and/or obesity. Research findings were closely examined for level of evidence, sample size, study purpose, study procedure, and findings (Table 1).
Blood Glucose Three of the selected studies compared HFCS and sucrose (Melanson et al., 2007; Mitchell et al., 2000). Mitchell et al. (2000) examined a variety of sweetening substances, including sugar, a 900 cc HFCS solution, a 675 cc HFCS solution, and a water placebo. Blood glucose levels were measured at 15minute increments for 60 minutes. No significant differences in blood glucose levels were found at the end of 60 minutes for any sweetening solutions. At the end of 60 minutes, the sugar solution groups’ blood glucose levels and the HFCS groups’ blood glucose levels were comparable to the water group. Although HFCS solutions generally contain either 42% fructose or 55% fructose, the amount of fructose in the HFCS solution in this study is not indicated. Melanson et al. (2007) examined the effects of beverages sweetened with HFCS or sucrose on blood glucose and other responses in healthy normal-weight women. Participants were randomized to consume either a HFCS beverage containing 55% fructose or a sugar-sucrose beverage containing 50% fructose. Beverages were consumed with three meals, breakfast, lunch, and dinner. No significant difference in blood glucose levels was found between the two groups, suggesting no difference in blood glucose responses after consumption of either table sugar or HFCS. These studies demonstrate no difference between serum blood sugar response after consumption of table sugar and HFCS. That is to say, both table sugar and HFCS had the same effect on blood glucose levels. Stanhope et al. (2008) compared the metabolic and endocrine effects of sucrose and HFCS. Thirty-five participants were randomly assigned to consume sucrose sweetened beverages and HFCS sweetened beverages. Although the actual amount of sucrose and HFCS consumed is unclear (25% of energy expenditure), no difference was found in blood glucose levels after consumption of sucrose and of HFCS.
Appetite Four selected studies were reviewed to assess the evidence comparing the effect of sucrose or table sugar and HFCS consumption on appetite. Melanson et al. (2007) and Soenen (2007) both compared the effect of HFCS consumption and sucrose consumption on appetite, as measured with a 10-cm VAS, and by evaluation of gherlin levels. Gherlin is a hormone secreted in the stomach. Increased gherlin levels have been associated with short-term hunger and food intake (Wren et al., 2001). Melanson et al. (2007) studied 30 lean women, and reported a Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Evidence Review Table 1. Summary of Studies Comparing Effect of Sucrose and HFCS on Blood Glucose, Appetite, and Triglyceride and Lipid Levels
Study
LoE
Purpose
Sample
Procedure
Findings
Blood Glucose Level Mitchell et al. (2000) CocaCola sponsored study
lll
Influence of HFCS and other 10 trained healthy sweeteners on glycemic male runners response & exercise-induced hypoglycemia
Compared sucrose (table No difference in blood sugar) and HFCS glucose levels beverages during exercise
Melanson et al. (2007) Pepsi Cola sponsored study
III
Effect of HFCS and sucrose 30 healthy women on blood sugar, insulin, leptin, ghrelin, & appetite
Compared sucrose (table No difference in blood sugar) diet with HFCS glucose levels diet
Stanhope et al. (2008) Pepsi Cola sponsored study
III
Comparison of metabolic/endocrine effects of HFCS with sucrose
Compared sucrose (table No difference in blood sugar) sweetened glucose levels beverages to HFCS sweetened beverages
Melanson et al. (2007)
III
Effect of HFCS and sucrose 30 healthy women on blood sugar, insulin, leptin, ghrelin, & appetite
Compared sucrose diet (50% fructose) with HFCS diet (55% fructose)
Akhavan et al. (2007)
III
Effect of HFCS and sucrose 12 healthy men on blood sugar, insulin, leptin, ghrelin, & appetite
Compared water, 20% No difference with other glucose: 80% fructose solutions for appetite and sucrose (50% or ghrelin fructose)
Soenen et al. (2007)
III
Compare effect of HFCS, sucrose, milk on satiety
15 healthy men Compared HFCS G45:F55, No difference in satiety 15 healthy women sucrose, milk
Stanhope et al. (2008)
III
Comparison of metabolic/endocrine effects of HFCS with sucrose
16 healthy women 18 healthy men
lll
Compared diet containing No difference in 18 healthy men Comparison of HFCS and triglyceride levels sucrose sweetened 16 healthy women sucrose on glucose, beverages and diet insulin, leptin, ghrelin and containing HFCS triglyceride levels sweetened beverages
16 healthy women 18 healthy men
Appetite No difference in appetite
Compared sucrose (table No difference in gherlin sugar) sweetened levels beverages to HFCS sweetened beverages
Triglyceride/Lipid Level Stanhope et al. (2008)
slight but significant increase in appetite in the sucrose group, but Soenen et al. (2007) found no difference in reported appetite between the groups. Akhavan and Anderson (2007) examined the effect of sucrose, a glucose35:fructose65 beverage, a glucose20:fructose80 beverage, HFCS (glucose45:fructose55), and other combinations of glucose and fructose, on appetite as measured by a VAS and gherlin level. Results of a 10-cm VAS and gherlin hormone level demonstrated no differences in measured appetite from baseline after administration of any of the sucrose or glucose:fructose solutions, suggesting that neither sucrose consumption nor HFCS consumption influence appetite. Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Stanhope et al. (2008) measured gherlin levels and found no difference in appetite between sucrose and HFCS consumption. Thus, no evidence was found supporting a difference between table sugar consumption and HFCS consumption on appetite.
Weight Gain and Obesity No research with adults was found. Forshee, Anderson, and Storey (2007) reported no evidence to support an association between greater weight gain with HFCS consumption than with consumption of table sugar in children.
129
Sugar or High Fructose Corn Syrup
Triglyceride Levels Only one study was found that compared the relationship between HFCS, sucrose, and fructose on triglyceride levels (Stanhope et al., 2008). As noted above, 34 healthy subjects (18 men and 16 women) consumed diets based on calculated energy requirements, of which 25% of the calories came from sugar in the form of sucrose, HDCS, glucose, or fructose sweetened beverages. No differences between consumption of sucrose containing beverages or HFCS were found in plasma triglyceride, cholesterol, LDL, or HDL levels. Fasting triglyceride levels of all participants were increased the morning following consumption of both sucrose and HFCS. This study suggests that there is no difference between the effect of sucrose and HFCS on triglyceride levels. However, it is important to note that triglyceride levels were elevated with both sweeteners, suggesting that both may be harmful, especially in persons trying to exert dietary control of lipids and triglyceride.
What About Fructose? The review of the literature comparing table sugar and HFCS literature led to a further inquiry of the association between fructose and triglyceride levels. The research describing an association between sweeteners and elevated postprandial lipidemia or triglyceride has focused on the fructose of sucrose (glucose plus 50% fructose) and the fructose of HFCS (glucose plus 42–55% fructose). Chong, Fielding, and Frayn (2007) examined the association of elevated plasma lipid level. Fructose solutions were administered, to 14 healthy male subjects, followed by measured plasma triacylglycerol and plasma VLDL-triacylglycerol. Plasma triglycerol levels were significantly higher after consumption of fructose as compared to glucose, and remained higher for a longer period of time. Bantle, Raatz, Thomas, and Georgopoulos (2000) and Stanhope et al. (2008) compared glucose diets and fructose diets and reported significantly increased mean plasma postprandial triglyceride, VLDL-tricylglycerol, LDL cholesterol in the male subjects, with increases being more pronounced in overweight and obese individuals. Of interest, in two studies including female subjects (Bantle et al., 2000; Stanhope et al., 2008) both premenopausal and perimenopausal women taking estrogen reported no differences in plasma lipid levels between the glucose groups and the fructose groups. Other research (Swarbrick, 2008; Teff et al., 2004) examining the relationships between fructose consumption and elevated triglyceride levels consistently demonstrate compelling evidence that increased consumption of either table sugar or HFCS leads to elevated triglyceride levels in healthy adult. After conducting a meta-analysis of 42 studies, Livesay and Taylor (2008) concluded that a significant rise in postprandial triglycerides can be seen after 50 g or more of fructose is consumed, and noted that more than 50% of the adult population consumes this amount of fructose each day. Most recently, Welsh et al. (2010) reported findings from a national survey indicating
130
a significant correlation between added sugars and increased blood lipid levels among U.S. adults.
DISCUSSION The relationship between HFCS consumption and health outcomes has been broadly discussed in popular literature and in discipline-based research literature. Much of the popular literature attributes the rising incidence of obesity and development of Type 2 diabetes mellitus to HFCS. This literature proposes that HFCS affects hormone levels that control appetite, thus preventing individuals from feeling full or sated after eating. However, little evidence exists to associate consumption of HFCS with higher blood glucose levels, changes in appetite, weight gain, or elevated lipid or triglyceride levels when compared to consumption of table sugar. However, compelling evidence does exist suggesting that greater changes in lipid and triglyceride levels may be associated with consumption of fructose in healthy adults. Because the glucose in table sugar does not seem to be associated with changes in lipid levels, it may be the fructose in both table sugar and in HFCS that leads to elevated lipid and triglyceride levels. What this may mean is that increased sugar or HFCS consumption and associated increased fructose consumption leading to elevated triglyceride levels, may play a significant role in development of coronary artery disease and perhaps the development of hyperinsulinemia and Type 2 Diabetes mellitus.
RECOMMENDATIONS FOR PRACTICE Basciano, Federico, and Adeli (2005) reported that Western diets contain 85–100 g of fructose. Most of the added sugar is in the form of table sugar and HFCS. Other sweeteners including molasses, honey, and maple syrup are consumed to a smaller degree. Johnson et al. (2009), on behalf of the American Heart Association, recommended limiting the consumption per day of added sugar to 100 calories or about five teaspoons for women and 144 calories or nine teaspoons for men. Sufficient evidence exists to support the need for clinicians to include discussions about any type of sugar consumption with all patients and families, but especially with patients manifesting risk factors associated with development of metabolic syndrome, coronary artery disease, and hypertension. As clinicians teach patients and families about the health effects of both sugar and HFCS, the emphasis should be placed on the amount of fructose contained in foods. It is important to note that nutritional labels only indicate grams of sugar in food products, and that the amount of fructose is not indicated. In addition, recommendations from government and scientific organizations for sugar consumption are difficult to interpret for teaching patients and families. Determining how much sugar is equal to 100 calories, or converting grams of sugar to teaspoons of sugar can be cumbersome. Clinicians should know that one teaspoon of sugar is equivalent to 4 g and that, depending on the food or beverage, either 42% of the sugar Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Evidence Review for solid products or 55% of the sugar for beverages may be fructose. Thus, one 12-ounce can of sweetened soda contains about eight teaspoons of added sugar for about 130 calories, 32 g of sugar and 16 g of fructose. Patients and families can be shown how to read nutritional labels to choose foods and beverages with lower amounts of sugar, and to avoid foods and beverages containing HFCS and sugar. Recently, some producers of foods and beverages have replaced HFCS with sugar; however, it must be noted that these foods and beverages continue to contain large amounts of table sugar and, thus, large amounts of fructose. Juices containing large amounts of added sugar can be diluted before consumption or avoided. Between-meal snacks containing sugar can be replaced with foods with no sugar, like nuts and vegetables.
RECOMMENDATIONS FOR FUTURE RESEARCH Most of the studies reviewed did not assess outcomes longitudinally over time. Longitudinal studies may be useful for examining the long-term effects of added sweeteners as well as the effect of decreasing daily sugar consumption. Additional research is needed examining the influence of removing or limiting sugar and HFCS from diets on triglyceride levels.
LIMITATIONS Limitations of this review should be noted. Convenience sampling was used and sample sizes in each of the studies were small—ranging from 10 to 30 participants. The few studies available comparing differences between table sugar consumption and HFCS make it difficult to develop generalizable conclusions. However, the consistency of the findings in the reviewed studies suggests that further research with only shortterm outcomes measures may not be necessary. Finally, because no longitudinal designs were used, it is not possible to determine long-term effects.
CONCLUSIONS Nurses, nutritionists, and other clinicians have a responsibility to share accurate, evidence-based information with patients and families, and to provide information that will help with health promotion decision making. This review provides evidence to support teaching that informs patients and families of the risks of both sugar and HFCS consumption and the benefits of reducing that consumption whenever possible. WVN
LINKING EVIDENCE TO ACTION r Assess patient and family knowledge of differences and similarities between table sugar and high fructose corn syrup (HFCS).
Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
r Discuss possible associations of both table sugar and HFCS and coronary artery disease and metabolic syndrome.
r Identify ways to limit both table sugar and HFCS from patient and family diets such as: – Reading nutritional labels and ingredient lists to identify table sugar and HFCS food and beverage sources – Choosing foods and beverages based on their lesser amount of sugar – Diluting fruit juices with water to limit table sugar and HFCS consumption – Replacing snacks containing added table sugar or HFCS with nuts, vegetables, or dairy products.
r Discuss patient and family considerations and preferences for implementation of dietary changes
Author information Linda L. Sobel, Associate Professor of Nursing, James Madison University, Harrisonburg, VA,USA; Elizabeth Dalby, Lab Coordinator, Krasnow Institute of Advanced Studies, George Mason University, Fairfax, VA, USA. Address correspondence to Dr. Linda L. Sobel, James Madison University, MSC 4305, Harrisonburg, VA 22807; sobelll@ jmu.edu. Accepted 2 September 2013 C 2014, Sigma Theta Tau International Copyright
References Akhavan, T., & Anderson, G. H. (2007). Effects of glucose-tofructose ratios in solutions on subjective satiety, food intake, and satiety hormones in young men. The American Journal of Clinical Nutrition, 86(5), 1354–1363. Bantle, J. P., Raatz, S. K., Thomas, W., & Georgopoulos, A. (2000). Effects of dietary fructose on plasma lipids in healthy subjects. American Journal of Clinical Nutrition, 72(5), 1128– 1134. Basciano, H., Federico, L. & Adeli, K. (2005). Fructose, insulin resistance, and metabolic dyslipidemia. Nutrition & Metabolism, 2(5), 5–14. Bray, G. A., Nielsen, S. J., & Popkin, B. M. (2004). Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity [corrected; published erratum appears in American Journal of Clinical Nutrition, 80(4), 1090]. American Journal of Clinical Nutrition, 79(4), 537–543. Chong, M. F., Fielding, B. A., & Frayn, K. N. (2007). Mechanisms for the acute effect of fructose on postprandial lipemia. The American Journal of Clinical Nutrition, 85(6), 1511–1520. Cooper, H. M. (1998). Synthesizing research: A guide for literature reviews (3rd ed.). Thousand Oaks, CA: Sage Publications.
131
Sugar or High Fructose Corn Syrup
Fineout-Overholt, E., Melnyk, B. M., & Schultz, A. (2005). Transforming health care from the inside out: Advancing evidencebased practice in the 21st century. Journal of Professional Nursing, 21(6), 335–344.
Parks, E. J., & Hellerstein, M. K. (2000). Carbohydrate-induced hypertriacyglycerolemia: Historical perspective and review of biological mechanisms. American Journal of Clinical Nutrition, 71(2), 412–433.
Forshee, R. A., Anderson, P. A., & Storey, M. L. (2007). Sugarsweetened beverages and body mass index in children and adolescents: A meta-analysis. The American Journal of Clinical Nutrition, 87(6), 1662–1671.
Soenen, S. & Westerterp-Plantenga, M. (2007). No differences in satiety or energy intake after high-fructose corn syrup, sucrose, or milk preloads. The American Journal of Clinical Nutrition, 86(6), 1586–1594.
Gropper, S. S., Smith, J. L., & Groff, J. L. (2009). Micronutrients and their metabolism—Carbohydrates. In Advanced nutrition and human metabolism (pp. 66–71). Belmont, CA: Wadsworth Cengage Learning.
Stanhope, K. L., Griffen, S. C., Bair, B. R., Swarbrick, M. M., Keim, N. L., & Havel, P. J. (2008). Twenty-four-hour endocrine and metabolic profiles following consumption of high-fructose corn syrup-, sucrose-, fructose-, and glucose-sweetened beverages with meals. The American Journal of Clinical Nutrition, 87(5), 1194–1203.
Hein, G. L., Storey, M. L., White, J. S., & Lineback, D. R. (2005). Highs and lows of high fructose corn syrup: A report from the center for food and nutrition policy and its Ceres Workshop. Nutrition Today, 40(6), 253–256. Johnson, R. K., Appel, L. J., Brands, M., Howard, B. V., Lefevre, M., Lustig, R. H., . . . on behalf of the American Heart Association Nutrition Committee of the Council on Nutrition, Physical Activity, and Metabolism and the Council on Epidemiology and Prevention. (2009). Dietary sugars intake and cardiovascular health: A scientific statement from the American Heart Association. Circulation, 120(11), 1011– 1020. Kee, J. L. (2005). Laboratory and diagnostic tests (7th ed.). Upper Saddle River, NJ: Pearson Prentice Hall. Livesay, G., & Taylor, R. (2008). Fructose consumption and consequences for glycation, plasma triacyglycerol, and body weight: Meta-analysis and meta-regression models of intervention studies. American Journal of Clinical Nutrition, 88(5), 1419– 1437. Melanson, K. J., Zukley, L., Lowndes, J., Nguyen, V., Angelopoulos, T. J., & Rippe, J. M. (2007). Effects of high-fructose corn syrup and sucrose consumption on circulating glucose, insulin, leptin, and ghrelin and on appetite in normal-weight women. Nutrition, 23(2), 103–112. Mitchell, J. B., Braun, W. A., Pizza, F.X., & Forrest, M. (2000). Pre-exercise carbohydrate and fluid ingestion: Influence of glycemic response on 10-km treadmill running performance in the heat. Journal of Sports Medicine and Physical Fitness, 40, 41– 50.
132
Swarbrick, M. M. (2008). Consumption of fructose-sweetened beverages for 10 weeks increases postprandial triacylglycerol and apolipoprotein-B concentrations in overweight and obese women. British Journal of Nutrition, 100(5), 947–952. Teff, K. L., Elliot, S. S., Tschop, M., Kieffer, T. J., Radar, D., Heiman, M., . . . Havel, P. J. (2004). Dietary fructose reduces circulating insulin and ghrelin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. Journal of Clinical Endocrinology and Metabolism, 89(6), 2963–2972. Welsh, J. A., Sharma, A., Abramson, J. L., Vaccarino, V., Gillespie, C. & Vos, M. B. (2010). Caloric sweetener consumption and dyslipidemia among us adults. Journal of the American Medical Association, 303(15), 1490–1497. White, J. S. (2008). Straight talk about high-fructose corn syrup: What it is and what it ain’t. American Journal of Clinical Nutrition, 88(6), 1716S-1721. World Health Organization. (2013). Obesity and overweight. Fact sheet no.311. Retrieved from http://www.who.int/mediacentre/ factsheets/fs311/en/ Wren, A. M., Seal, L. J., Cohen, M. A., Brynes, A. E., Frost, G. S., Murphy, K. G., . . . Bloom, S. R. (2001). Ghrelin enhances appetite and increases food intake in humans. Journal of Clinical Endocrinology Metabolism, 86(12), 59–92.
doi 10.1111/wvn.12027 WVN 2014;11:126–132
Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Sugar or High Fructose Corn Syrup—What Should Nurses Teach Patients and Families? Linda L. Sobel, RN, PhD • Elizabeth Dalby, BS
ABSTRACT Keywords high fructose corn syrup, blood glucose levels, high sugar, lipids
Background: There is lack of consensus in the lay literature to support consumption of table sugar as a preferred sweetener when compared to high fructose corn syrup (HFCS). Aims: The purpose of this study was to search the literature for evidence to determine the health effects of consumption of table sugar (sucrose) and HFCS on blood glucose, lipid levels, obesity, and appetite as well as to make recommendations for patient and family teaching of those at risk for developing negative health outcomes, including coronary heart disease. Methods: Nursing and health-related databases, including CINAHL, PubMed, Cochrane Central Registry of Controlled Trials, and Health and Wellness were searched for research articles, which were compared and evaluated for purpose, sample size, procedure, findings, and level of evidence. Findings: Five studies that met inclusion criteria were evaluated. No difference was found in changes in blood glucose levels, lipid levels, or appetite between table sugar consumption and HFCS consumption. When only fructose was consumed, lipid levels were significantly increased. Linking Evidence to Action: The evidence suggests that fructose, found in both table sugar and HFCS, has a negative effect on health outcomes. Clinicians should teach patients and families that all sugar consumption should be closely monitored and kept below the 40 g/day recommended by the World Health Organization.
BACKGROUND As concern about the ever-increasing incidence of obesity and development of Type 2 diabetes mellitus continues to escalate, the role of high fructose corn syrup (HFCS) as a food additive and sweetener has been examined more carefully. Popular lay literature ascribes many ill effects of HFCS consumption, but with little cited research to support these claims. When nurses and other clinicians teach patients and families about health dietary choices, they commonly provide information about saturated and unsaturated fats, fiber, caloric consumption, and salt. Sugar may be discussed within the context of diabetes mellitus education, but HFCS is rarely mentioned, often because of an assumption that HFCS is a fructose product that does not have the same effects on metabolism as table sugar.
What is Table Sugar? Table sugar, also known as sucrose, is one of three common disaccharides found in a typical diet. Other common disaccharides are maltose and lactose. Disaccharides are two conjoined carbohydrate molecules. Maltose is composed of two glucose molecules and lactose is composed of glucose and galactose. Sucrose is chemically composed of glucose and fructose in equal proportions (Gropper, Smith, & Groff, 2009)
126
Sucrose is extracted from sugar cane or beet juice, and is the common sugar we sprinkle on our food and add to our drinks and baked goods. Sucrose is also naturally found in fruit and fruit juice, honey, agave nectar, and maple syrup (Gropper et al., 2009).
Absorption and utilization of glucose and fructose. Glucose is absorbed from the duodenum into the vascular space with the aid of a hexose transporter that regulates the rate of absorption. As blood glucose levels rise, insulin is released from the pancreas to facilitate diffusion of glucose into muscle and fat cells, where glucose is converted to pyruvate through a process of glycolysis before entering the Citric Acid cycle for conversion to energy for cellular work (Gropper et al., 2009). Fructose differs from glucose in that it can enter glycolysis directly, and is not subject to the rate-limiting action of the hexose transporter (Gropper et al., 2009). Fructose is absorbed into the small intestine via passive diffusion. To maintain passive diffusion, blood concentration of fructose must remain low (Gropper et al., 2009). To maintain low fructose concentrations, the liver immediately takes up fructose to allow for continued fructose absorption from the gut. Unlike glucose, fructose does not stimulate insulin release. When fructose is absorbed by the liver, it readily enters the metabolic pathway and, if no energy is needed, is converted into a Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Evidence Review substance called acetyl CoA. When acetyl CoA builds up in liver cells, metabolism is pushed toward triglyceride production and formation of very low density lipoproteins (VLDLs) for transfer of these triglycerides into the bloodstream. Accordingly, consumption of large amounts of fructose has been associated with marked increases in serum triglyceride and VLDL levels (Parks & Hellerstein, 2000).
WHAT IS HFCS? HFCS is a processed caloric sweetener derived from corn, first introduced into the American diet in the early 1970s, that has become an industrially popular substitute for crystalline sucrose in the United States (Bray, Nielsen, & Popkin, 2004; White, 2008). After initial purification, an enzyme is added to corn starch to break the starch chains into simple sugars, most of which are glucose. In a series of steps using synthetic enzymes, a majority of this glucose is converted to fructose, a chemical similar to glucose that is found naturally in fruit. Usually this product is then mixed with low fructose corn syrup to create a mixture that is anywhere from 42% to 55% fructose to glucose, depending on its application in either solid food or in liquids. HFCS is valued by the food industry for its stability, its ability to dissolve easily in liquids, and, most of all, its low cost. It is important to note that HFCS and corn syrup are different products. Corn syrup is 100% glucose and contains no fructose (White, 2008). In recent years, the lay literature has targeted HFCS as a perpetrator of various health problems related to its consumption. Many claim that HFCS is metabolized differently than sucrose because HFCS is composed of free glucose and fructose molecules instead of bound fructose and glucose. Some simply claim there may be byproducts present in HFCS that influence triglyceride and lipid levels, and satiety or appetite. Alternatively, there are those who report that HFCS is not different than table sugar and that the public need not be concerned about consuming foods and beverages to which HFCS has been added. Currently, there is no literature comparing HFCS and table sugar to guide nurses and other clinicians as they teach their patients and families to consume healthy diets.
PURPOSE The purpose of this research is to synthesize the literature comparing the relationships of HFCS consumption and table sugar consumption with increased blood glucose levels, appetite, lipidemia or triglyceride levels, and obesity or weight gain in healthy adults. A PICO format (Fineout-Overholt, Melnyk, & Schultz, 2005) was used to develop the research question: Is there a relationship in (P) healthy adults who (I) consume HFCS (C) compared to those who consume table sugar and (O) blood glucose levels, appetite, lipidemia or triglyceride levels and obesity or weight gain. Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
DEFINITION OF TERMS HFCS is a mixture of glucose and fructose and is used as a sweetening additive for food and beverages. HFCS added to beverages is usually 45% glucose and 55% fructose, whereas HFCS added to food is usually 53% glucose and 42% fructose (Hein, Storey, White, & Lineback, 2005). Blood glucose level is the amount of glucose found in a sample of blood, obtained by either a finger-stick or venous sampling, and measured as mg/dl (Kee, 2005). Lipoprotein levels are the measure of varied lipids including plasma cholesterol, high-density lipoprotein (HDL), low-density lipoprotein (LDL), VLDL, and plasma triglyceride (Kee, 2005). Appetite is conceptually defined as the desire or motivation to eat, measured by a 10-cm or 100-mm visual analog scale (VAS) ranging from “not at all” on the left to “extremely” on the right (Soenen & Westerterp-Plantenga, 2007). Appetite and food intake are also measured by evaluation of gherlin levels, a hormone produced in the stomach, which increases with hunger and may stimulate appetite, and is associated with increased short-term appetite and increased food intake (Wren et al., 2001). Overweight and obesity are defined as abnormal or excessive fat accumulation that may impair health. Body mass index (BMI) is a simple index of weight-for-height that is commonly used to classify overweight and obesity in adults. It is defined as a person’s weight in kilograms divided by the square of his height in meters (kg/m2 ). The WHO defines overweight as a BMI greater than or equal to 25, and obesity as a BMI greater than or equal to 30 (World Health Organization, 2013).
METHODS Using Cooper’s (1998) framework for synthesizing literature, a systematic review of the health-related research literature was conducted to retrieve evidence to support the influence of HFCS on health outcomes. The framework identifies five stages of research synthesis: (a) problem formulation; (b) search for literature addressing the problem, also known as data collection; (c) data evaluation of quality and level of evidence; (d) analysis and interpretation of findings; and (e) presentation and dissemination. Cooper’s framework supports the review and synthesis of separate research studies examining the relationships between HFCS and blood glucose levels, lipid or triglyceride levels, appetite and obesity as compared to consumption of table sugar in adult humans. The initial search for literature addressing health effects of HFCS was done with no year limitations in order to identify appropriate databases and keywords. These terms were then used to develop search criteria to include all published articles between 1983 and 2010. A third review was conducted in 2011 with no new additional research noted.
Electronic Search for Literature This systematic review included a comprehensive search of CINHAL, PubMed, Cochrane Central Registry of Controlled
127
Sugar or High Fructose Corn Syrup
Trials, and Health and Wellness databases. Search terms were: high fructose corn syrup, sugar, high fructose corn syrup and blood glucose levels, high fructose corn syrup and lipid and triglyceride levels, high fructose corn syrup and appetite, high fructose corn syrup and obesity, and high fructose corn syrup and nursing. In addition, the term sugar was searched with each of the previously noted terms. Reference lists of research reports were reviewed and useful articles were retrieved. The search began with inclusion of all retrieved articles. To review a comprehensive population of studies, 60 articles were retrieved, fully read, and critiqued. Opinion articles, letters to the editor, animal studies, and others not presenting original research were excluded, as was research involving unhealthy individuals, individuals with diabetes mellitus, and children and adolescents. After exclusion criterion was applied, research articles published between 1990 and 2010 were thoroughly reviewed for inclusion. Research from varied health-related disciplines was reviewed including dietetics, exercise physiology, and diabetes care. No nursing research literature was found to compare the effects of HFCS and sugar on health.
Data Evaluation of Quality and Level of Evidence For each study included in this systematic investigation, the reviewer extracted: author names, journal title and publication year, study purpose, description of the sample, research procedure, and relevant findings. In addition, in an attempt to evaluate research studies for the best evidence available to answer the PICO question, levels of evidence as described by Fineout-Overholt et al. (2005) were determined. Of the 60 articles retrieved, five met the inclusion criteria. Abstracts of acceptable studies were evaluated for level of evidence and findings by two independent reviewers. Disagreements were discussed until consensus was reached. Two studies (Melanson et al., 2007; Stanhope et al., 2008) examined two outcome variables of interest to this review; blood glucose, and appetite. In addition, Stanhope et al. (2008) compared the association of sucrose and HFCS to triglyceride levels. No studies comparing sucrose and HFCS and a relationship specifically to weight gain were found. Most studies were excluded because they were opinion articles, studies that examined other outcomes than the ones identified for this systematic review, or animal studies. The accepted studies (Akhavan & Anderson, 2007; Melanson et al., 2007; Mitchell, Braun, Pizza, & Forrest, 2000; Soenen, 2007; Stanhope et al., 2008) are summarized in Table 1. Publication dates ranged from 2000 to 2008. Much of the earlier research focused on evaluation of fructose consumption by persons with Type 1 diabetes mellitus. This earlier work was excluded because it focused on nonhealthy adults. All studies used cross-sectional designs. No longitudinal designs were found. All five studies were ranked as Level III evidence (Fineout-Overholt et al., 2005). Three studies (Melanson et al., 2007; Mitchell et al., 2000; Stanhope et al., 2008) were supported by CocaCola and PepsiCola.
128
ANALYSIS AND INTERPRETATION OF FINDINGS Selected research was reviewed and critiqued to summarize the association between consumption of HFCS and sugar and blood glucose levels, lipid levels, appetite, and weight gain and/or obesity. Research findings were closely examined for level of evidence, sample size, study purpose, study procedure, and findings (Table 1).
Blood Glucose Three of the selected studies compared HFCS and sucrose (Melanson et al., 2007; Mitchell et al., 2000). Mitchell et al. (2000) examined a variety of sweetening substances, including sugar, a 900 cc HFCS solution, a 675 cc HFCS solution, and a water placebo. Blood glucose levels were measured at 15minute increments for 60 minutes. No significant differences in blood glucose levels were found at the end of 60 minutes for any sweetening solutions. At the end of 60 minutes, the sugar solution groups’ blood glucose levels and the HFCS groups’ blood glucose levels were comparable to the water group. Although HFCS solutions generally contain either 42% fructose or 55% fructose, the amount of fructose in the HFCS solution in this study is not indicated. Melanson et al. (2007) examined the effects of beverages sweetened with HFCS or sucrose on blood glucose and other responses in healthy normal-weight women. Participants were randomized to consume either a HFCS beverage containing 55% fructose or a sugar-sucrose beverage containing 50% fructose. Beverages were consumed with three meals, breakfast, lunch, and dinner. No significant difference in blood glucose levels was found between the two groups, suggesting no difference in blood glucose responses after consumption of either table sugar or HFCS. These studies demonstrate no difference between serum blood sugar response after consumption of table sugar and HFCS. That is to say, both table sugar and HFCS had the same effect on blood glucose levels. Stanhope et al. (2008) compared the metabolic and endocrine effects of sucrose and HFCS. Thirty-five participants were randomly assigned to consume sucrose sweetened beverages and HFCS sweetened beverages. Although the actual amount of sucrose and HFCS consumed is unclear (25% of energy expenditure), no difference was found in blood glucose levels after consumption of sucrose and of HFCS.
Appetite Four selected studies were reviewed to assess the evidence comparing the effect of sucrose or table sugar and HFCS consumption on appetite. Melanson et al. (2007) and Soenen (2007) both compared the effect of HFCS consumption and sucrose consumption on appetite, as measured with a 10-cm VAS, and by evaluation of gherlin levels. Gherlin is a hormone secreted in the stomach. Increased gherlin levels have been associated with short-term hunger and food intake (Wren et al., 2001). Melanson et al. (2007) studied 30 lean women, and reported a Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Evidence Review Table 1. Summary of Studies Comparing Effect of Sucrose and HFCS on Blood Glucose, Appetite, and Triglyceride and Lipid Levels
Study
LoE
Purpose
Sample
Procedure
Findings
Blood Glucose Level Mitchell et al. (2000) CocaCola sponsored study
lll
Influence of HFCS and other 10 trained healthy sweeteners on glycemic male runners response & exercise-induced hypoglycemia
Compared sucrose (table No difference in blood sugar) and HFCS glucose levels beverages during exercise
Melanson et al. (2007) Pepsi Cola sponsored study
III
Effect of HFCS and sucrose 30 healthy women on blood sugar, insulin, leptin, ghrelin, & appetite
Compared sucrose (table No difference in blood sugar) diet with HFCS glucose levels diet
Stanhope et al. (2008) Pepsi Cola sponsored study
III
Comparison of metabolic/endocrine effects of HFCS with sucrose
Compared sucrose (table No difference in blood sugar) sweetened glucose levels beverages to HFCS sweetened beverages
Melanson et al. (2007)
III
Effect of HFCS and sucrose 30 healthy women on blood sugar, insulin, leptin, ghrelin, & appetite
Compared sucrose diet (50% fructose) with HFCS diet (55% fructose)
Akhavan et al. (2007)
III
Effect of HFCS and sucrose 12 healthy men on blood sugar, insulin, leptin, ghrelin, & appetite
Compared water, 20% No difference with other glucose: 80% fructose solutions for appetite and sucrose (50% or ghrelin fructose)
Soenen et al. (2007)
III
Compare effect of HFCS, sucrose, milk on satiety
15 healthy men Compared HFCS G45:F55, No difference in satiety 15 healthy women sucrose, milk
Stanhope et al. (2008)
III
Comparison of metabolic/endocrine effects of HFCS with sucrose
16 healthy women 18 healthy men
lll
Compared diet containing No difference in 18 healthy men Comparison of HFCS and triglyceride levels sucrose sweetened 16 healthy women sucrose on glucose, beverages and diet insulin, leptin, ghrelin and containing HFCS triglyceride levels sweetened beverages
16 healthy women 18 healthy men
Appetite No difference in appetite
Compared sucrose (table No difference in gherlin sugar) sweetened levels beverages to HFCS sweetened beverages
Triglyceride/Lipid Level Stanhope et al. (2008)
slight but significant increase in appetite in the sucrose group, but Soenen et al. (2007) found no difference in reported appetite between the groups. Akhavan and Anderson (2007) examined the effect of sucrose, a glucose35:fructose65 beverage, a glucose20:fructose80 beverage, HFCS (glucose45:fructose55), and other combinations of glucose and fructose, on appetite as measured by a VAS and gherlin level. Results of a 10-cm VAS and gherlin hormone level demonstrated no differences in measured appetite from baseline after administration of any of the sucrose or glucose:fructose solutions, suggesting that neither sucrose consumption nor HFCS consumption influence appetite. Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Stanhope et al. (2008) measured gherlin levels and found no difference in appetite between sucrose and HFCS consumption. Thus, no evidence was found supporting a difference between table sugar consumption and HFCS consumption on appetite.
Weight Gain and Obesity No research with adults was found. Forshee, Anderson, and Storey (2007) reported no evidence to support an association between greater weight gain with HFCS consumption than with consumption of table sugar in children.
129
Sugar or High Fructose Corn Syrup
Triglyceride Levels Only one study was found that compared the relationship between HFCS, sucrose, and fructose on triglyceride levels (Stanhope et al., 2008). As noted above, 34 healthy subjects (18 men and 16 women) consumed diets based on calculated energy requirements, of which 25% of the calories came from sugar in the form of sucrose, HDCS, glucose, or fructose sweetened beverages. No differences between consumption of sucrose containing beverages or HFCS were found in plasma triglyceride, cholesterol, LDL, or HDL levels. Fasting triglyceride levels of all participants were increased the morning following consumption of both sucrose and HFCS. This study suggests that there is no difference between the effect of sucrose and HFCS on triglyceride levels. However, it is important to note that triglyceride levels were elevated with both sweeteners, suggesting that both may be harmful, especially in persons trying to exert dietary control of lipids and triglyceride.
What About Fructose? The review of the literature comparing table sugar and HFCS literature led to a further inquiry of the association between fructose and triglyceride levels. The research describing an association between sweeteners and elevated postprandial lipidemia or triglyceride has focused on the fructose of sucrose (glucose plus 50% fructose) and the fructose of HFCS (glucose plus 42–55% fructose). Chong, Fielding, and Frayn (2007) examined the association of elevated plasma lipid level. Fructose solutions were administered, to 14 healthy male subjects, followed by measured plasma triacylglycerol and plasma VLDL-triacylglycerol. Plasma triglycerol levels were significantly higher after consumption of fructose as compared to glucose, and remained higher for a longer period of time. Bantle, Raatz, Thomas, and Georgopoulos (2000) and Stanhope et al. (2008) compared glucose diets and fructose diets and reported significantly increased mean plasma postprandial triglyceride, VLDL-tricylglycerol, LDL cholesterol in the male subjects, with increases being more pronounced in overweight and obese individuals. Of interest, in two studies including female subjects (Bantle et al., 2000; Stanhope et al., 2008) both premenopausal and perimenopausal women taking estrogen reported no differences in plasma lipid levels between the glucose groups and the fructose groups. Other research (Swarbrick, 2008; Teff et al., 2004) examining the relationships between fructose consumption and elevated triglyceride levels consistently demonstrate compelling evidence that increased consumption of either table sugar or HFCS leads to elevated triglyceride levels in healthy adult. After conducting a meta-analysis of 42 studies, Livesay and Taylor (2008) concluded that a significant rise in postprandial triglycerides can be seen after 50 g or more of fructose is consumed, and noted that more than 50% of the adult population consumes this amount of fructose each day. Most recently, Welsh et al. (2010) reported findings from a national survey indicating
130
a significant correlation between added sugars and increased blood lipid levels among U.S. adults.
DISCUSSION The relationship between HFCS consumption and health outcomes has been broadly discussed in popular literature and in discipline-based research literature. Much of the popular literature attributes the rising incidence of obesity and development of Type 2 diabetes mellitus to HFCS. This literature proposes that HFCS affects hormone levels that control appetite, thus preventing individuals from feeling full or sated after eating. However, little evidence exists to associate consumption of HFCS with higher blood glucose levels, changes in appetite, weight gain, or elevated lipid or triglyceride levels when compared to consumption of table sugar. However, compelling evidence does exist suggesting that greater changes in lipid and triglyceride levels may be associated with consumption of fructose in healthy adults. Because the glucose in table sugar does not seem to be associated with changes in lipid levels, it may be the fructose in both table sugar and in HFCS that leads to elevated lipid and triglyceride levels. What this may mean is that increased sugar or HFCS consumption and associated increased fructose consumption leading to elevated triglyceride levels, may play a significant role in development of coronary artery disease and perhaps the development of hyperinsulinemia and Type 2 Diabetes mellitus.
RECOMMENDATIONS FOR PRACTICE Basciano, Federico, and Adeli (2005) reported that Western diets contain 85–100 g of fructose. Most of the added sugar is in the form of table sugar and HFCS. Other sweeteners including molasses, honey, and maple syrup are consumed to a smaller degree. Johnson et al. (2009), on behalf of the American Heart Association, recommended limiting the consumption per day of added sugar to 100 calories or about five teaspoons for women and 144 calories or nine teaspoons for men. Sufficient evidence exists to support the need for clinicians to include discussions about any type of sugar consumption with all patients and families, but especially with patients manifesting risk factors associated with development of metabolic syndrome, coronary artery disease, and hypertension. As clinicians teach patients and families about the health effects of both sugar and HFCS, the emphasis should be placed on the amount of fructose contained in foods. It is important to note that nutritional labels only indicate grams of sugar in food products, and that the amount of fructose is not indicated. In addition, recommendations from government and scientific organizations for sugar consumption are difficult to interpret for teaching patients and families. Determining how much sugar is equal to 100 calories, or converting grams of sugar to teaspoons of sugar can be cumbersome. Clinicians should know that one teaspoon of sugar is equivalent to 4 g and that, depending on the food or beverage, either 42% of the sugar Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
Evidence Review for solid products or 55% of the sugar for beverages may be fructose. Thus, one 12-ounce can of sweetened soda contains about eight teaspoons of added sugar for about 130 calories, 32 g of sugar and 16 g of fructose. Patients and families can be shown how to read nutritional labels to choose foods and beverages with lower amounts of sugar, and to avoid foods and beverages containing HFCS and sugar. Recently, some producers of foods and beverages have replaced HFCS with sugar; however, it must be noted that these foods and beverages continue to contain large amounts of table sugar and, thus, large amounts of fructose. Juices containing large amounts of added sugar can be diluted before consumption or avoided. Between-meal snacks containing sugar can be replaced with foods with no sugar, like nuts and vegetables.
RECOMMENDATIONS FOR FUTURE RESEARCH Most of the studies reviewed did not assess outcomes longitudinally over time. Longitudinal studies may be useful for examining the long-term effects of added sweeteners as well as the effect of decreasing daily sugar consumption. Additional research is needed examining the influence of removing or limiting sugar and HFCS from diets on triglyceride levels.
LIMITATIONS Limitations of this review should be noted. Convenience sampling was used and sample sizes in each of the studies were small—ranging from 10 to 30 participants. The few studies available comparing differences between table sugar consumption and HFCS make it difficult to develop generalizable conclusions. However, the consistency of the findings in the reviewed studies suggests that further research with only shortterm outcomes measures may not be necessary. Finally, because no longitudinal designs were used, it is not possible to determine long-term effects.
CONCLUSIONS Nurses, nutritionists, and other clinicians have a responsibility to share accurate, evidence-based information with patients and families, and to provide information that will help with health promotion decision making. This review provides evidence to support teaching that informs patients and families of the risks of both sugar and HFCS consumption and the benefits of reducing that consumption whenever possible. WVN
LINKING EVIDENCE TO ACTION r Assess patient and family knowledge of differences and similarities between table sugar and high fructose corn syrup (HFCS).
Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
r Discuss possible associations of both table sugar and HFCS and coronary artery disease and metabolic syndrome.
r Identify ways to limit both table sugar and HFCS from patient and family diets such as: – Reading nutritional labels and ingredient lists to identify table sugar and HFCS food and beverage sources – Choosing foods and beverages based on their lesser amount of sugar – Diluting fruit juices with water to limit table sugar and HFCS consumption – Replacing snacks containing added table sugar or HFCS with nuts, vegetables, or dairy products.
r Discuss patient and family considerations and preferences for implementation of dietary changes
Author information Linda L. Sobel, Associate Professor of Nursing, James Madison University, Harrisonburg, VA,USA; Elizabeth Dalby, Lab Coordinator, Krasnow Institute of Advanced Studies, George Mason University, Fairfax, VA, USA. Address correspondence to Dr. Linda L. Sobel, James Madison University, MSC 4305, Harrisonburg, VA 22807; sobelll@ jmu.edu. Accepted 2 September 2013 C 2014, Sigma Theta Tau International Copyright
References Akhavan, T., & Anderson, G. H. (2007). Effects of glucose-tofructose ratios in solutions on subjective satiety, food intake, and satiety hormones in young men. The American Journal of Clinical Nutrition, 86(5), 1354–1363. Bantle, J. P., Raatz, S. K., Thomas, W., & Georgopoulos, A. (2000). Effects of dietary fructose on plasma lipids in healthy subjects. American Journal of Clinical Nutrition, 72(5), 1128– 1134. Basciano, H., Federico, L. & Adeli, K. (2005). Fructose, insulin resistance, and metabolic dyslipidemia. Nutrition & Metabolism, 2(5), 5–14. Bray, G. A., Nielsen, S. J., & Popkin, B. M. (2004). Consumption of high-fructose corn syrup in beverages may play a role in the epidemic of obesity [corrected; published erratum appears in American Journal of Clinical Nutrition, 80(4), 1090]. American Journal of Clinical Nutrition, 79(4), 537–543. Chong, M. F., Fielding, B. A., & Frayn, K. N. (2007). Mechanisms for the acute effect of fructose on postprandial lipemia. The American Journal of Clinical Nutrition, 85(6), 1511–1520. Cooper, H. M. (1998). Synthesizing research: A guide for literature reviews (3rd ed.). Thousand Oaks, CA: Sage Publications.
131
Sugar or High Fructose Corn Syrup
Fineout-Overholt, E., Melnyk, B. M., & Schultz, A. (2005). Transforming health care from the inside out: Advancing evidencebased practice in the 21st century. Journal of Professional Nursing, 21(6), 335–344.
Parks, E. J., & Hellerstein, M. K. (2000). Carbohydrate-induced hypertriacyglycerolemia: Historical perspective and review of biological mechanisms. American Journal of Clinical Nutrition, 71(2), 412–433.
Forshee, R. A., Anderson, P. A., & Storey, M. L. (2007). Sugarsweetened beverages and body mass index in children and adolescents: A meta-analysis. The American Journal of Clinical Nutrition, 87(6), 1662–1671.
Soenen, S. & Westerterp-Plantenga, M. (2007). No differences in satiety or energy intake after high-fructose corn syrup, sucrose, or milk preloads. The American Journal of Clinical Nutrition, 86(6), 1586–1594.
Gropper, S. S., Smith, J. L., & Groff, J. L. (2009). Micronutrients and their metabolism—Carbohydrates. In Advanced nutrition and human metabolism (pp. 66–71). Belmont, CA: Wadsworth Cengage Learning.
Stanhope, K. L., Griffen, S. C., Bair, B. R., Swarbrick, M. M., Keim, N. L., & Havel, P. J. (2008). Twenty-four-hour endocrine and metabolic profiles following consumption of high-fructose corn syrup-, sucrose-, fructose-, and glucose-sweetened beverages with meals. The American Journal of Clinical Nutrition, 87(5), 1194–1203.
Hein, G. L., Storey, M. L., White, J. S., & Lineback, D. R. (2005). Highs and lows of high fructose corn syrup: A report from the center for food and nutrition policy and its Ceres Workshop. Nutrition Today, 40(6), 253–256. Johnson, R. K., Appel, L. J., Brands, M., Howard, B. V., Lefevre, M., Lustig, R. H., . . . on behalf of the American Heart Association Nutrition Committee of the Council on Nutrition, Physical Activity, and Metabolism and the Council on Epidemiology and Prevention. (2009). Dietary sugars intake and cardiovascular health: A scientific statement from the American Heart Association. Circulation, 120(11), 1011– 1020. Kee, J. L. (2005). Laboratory and diagnostic tests (7th ed.). Upper Saddle River, NJ: Pearson Prentice Hall. Livesay, G., & Taylor, R. (2008). Fructose consumption and consequences for glycation, plasma triacyglycerol, and body weight: Meta-analysis and meta-regression models of intervention studies. American Journal of Clinical Nutrition, 88(5), 1419– 1437. Melanson, K. J., Zukley, L., Lowndes, J., Nguyen, V., Angelopoulos, T. J., & Rippe, J. M. (2007). Effects of high-fructose corn syrup and sucrose consumption on circulating glucose, insulin, leptin, and ghrelin and on appetite in normal-weight women. Nutrition, 23(2), 103–112. Mitchell, J. B., Braun, W. A., Pizza, F.X., & Forrest, M. (2000). Pre-exercise carbohydrate and fluid ingestion: Influence of glycemic response on 10-km treadmill running performance in the heat. Journal of Sports Medicine and Physical Fitness, 40, 41– 50.
132
Swarbrick, M. M. (2008). Consumption of fructose-sweetened beverages for 10 weeks increases postprandial triacylglycerol and apolipoprotein-B concentrations in overweight and obese women. British Journal of Nutrition, 100(5), 947–952. Teff, K. L., Elliot, S. S., Tschop, M., Kieffer, T. J., Radar, D., Heiman, M., . . . Havel, P. J. (2004). Dietary fructose reduces circulating insulin and ghrelin, attenuates postprandial suppression of ghrelin, and increases triglycerides in women. Journal of Clinical Endocrinology and Metabolism, 89(6), 2963–2972. Welsh, J. A., Sharma, A., Abramson, J. L., Vaccarino, V., Gillespie, C. & Vos, M. B. (2010). Caloric sweetener consumption and dyslipidemia among us adults. Journal of the American Medical Association, 303(15), 1490–1497. White, J. S. (2008). Straight talk about high-fructose corn syrup: What it is and what it ain’t. American Journal of Clinical Nutrition, 88(6), 1716S-1721. World Health Organization. (2013). Obesity and overweight. Fact sheet no.311. Retrieved from http://www.who.int/mediacentre/ factsheets/fs311/en/ Wren, A. M., Seal, L. J., Cohen, M. A., Brynes, A. E., Frost, G. S., Murphy, K. G., . . . Bloom, S. R. (2001). Ghrelin enhances appetite and increases food intake in humans. Journal of Clinical Endocrinology Metabolism, 86(12), 59–92.
doi 10.1111/wvn.12027 WVN 2014;11:126–132
Worldviews on Evidence-Based Nursing, 2014; 11:2, 126–132. C 2014 Sigma Theta Tau International
