NEWS & VIEWS
3.
4.
5.
6.
syndrome: the complete task force report. Fértil. Steril. 91, 456-488 (2009). Legro. R.S. et ai. Diagnosis and treatment of polycystic ovary syndrome: an Endocrine Society clinical practice guideline. J. din. Endocrinoi. Metab. http://dx.doi.org/lO.121O/ jc.2013-2350. Moghetti, P. etai. Divergences in insuiin resistance between the different phenotypes of the polycystic ovary syndrome. J. din. Endocrinoi. Metab. 98,628-637 (2013). Palomba, S. et ai. Pregnancy in women with polycystic ovary syndrome: the effect of different phenotypes and features on obstetric and neonatal outcomes, fert/7. Steril. 94, 1805-1811 (2010). Kaira, S. K. etal. Is the fertile window extended in women with polycystic ovary syndrome? Utilizing the Society for Assisted Reproductive Technology registry to assess the impact of
reproductive aging on live-birth rate. Fertii. Steril. 100.208-213 (2013). Orio. F. etai. Cardiovascular risk in women with polycystic ovary syndrome. Fertii. Steril. 86 (Suppl. 1), S20-S21 (2006). Puurunen, J. et ai. Statin therapy worsens insulin sensitivity in women with poiycystic ovary syndrome (PCOS): a prospective. randomized, double-blind, placebo-controlled study. J. din. Endocrinoi. Metab. http:// dx.doi.org/10.1210/jc.2013-2674. Palomba, S. et ai. Evidence-based and potentiai benefits of metformin in the polycystic ovary syndrome: a comprehensive review. Endocr. Rev. 30.1-50 (2009). 10. Misso, M. L. etai. Metformin versus clomiphene citrate for infertility in non-obese women with polycystic ovary syndrome: a systematic review and meta-analysis. Hum. Reprod. Update 19,2-11 (2013).
OBESITY
Have new guidelines overiooked the roie of diet composition? Arne Astrup and Jennie Brand-Miller
New US guidelines for the management of overweight and obesity have disregarded robust evidence from intervention triais demonstrating the importance of dietary factors for weight control and disease prevention. This omission implies that diet composition does not matter, a stance that is potentiaiiy counterproductive for prevention and treatment strategies. Astrup, A. & Brand-Miller. J. Nat. Rev. Endocrinoi. 10.132-133 (2014): published online 14 January 2014: doi:10.1038/nrendo.2013.271
Assessing the scientific robustness of strategies designed to encourage weight loss (and its subsequent maintenance) and to improve risk factors among individuals who are overweight or obese can be difficult. The demand for successful weight-loss strategies is great as most US and European adults are overweight, and 20-35% are obese. These two conditions are recognized to cause reduced quality of life, increased disease load and premature mortality and, therefore, represent a major economic burden for society. A group of leading US experts has produced a set of guidelines for the management of overweight and obesity on behalf of the American Heart Association (AHA), the American College of Cardiology (ACC) and The Obesity Society (TOS).' These guidelines provide an evidence base to check the validity ofthe various ways to achieve and maintain weight loss and as such are most welcome. Nevertheless, they fall short because the importance of diet composition has been completely overlooked. The AHA-ACC-TOS guidelines comprise a comprehensive, yet condensed, list of almost all relevant treatment modalities, excluding weight-loss drugs, but including
132
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bariatric surgery. Strength of evidence for the efficacy of each treatment option is rated by the guideline development panel as 'low', 'moderate' or 'high', which is the standard approach taken in guideline development. However, the required evidence underpinning these rankings is strikingly different from that used in systematic reviews and meta-analyses. The obvious reason for this discrepancy is that the AHA-ACC-TOS evidence synthesis applied rules for quality assessment required by the US Institute of Medicine. These rules were developed specifically for drug trials and exclude randomized controlled trials (RCTs) with a retention rate below 90% for 'compléter' analyses or below 80% for 'intention-to-treat' analyses. The Institute of Medicine criteria are clearly appropriate for their intended purpose; however, if applied to dietary intervention trials, they exclude a vast body of evidence. Trials of dietary interventions require participants to consume all meals every day over a period of several months in compliance with one particular diet composition. Consequently, retention rate should not be used solely as an indicator of trial
quality, but rather as a primary outcome that provides a measure ofthe success and acceptability ofthe diet.' However, no critical assessment of diet adherence (for example, measurement of urinary nitrogen excretion among individuals following a high-protein diet) was made for the few trials of dietary intervention accepted by the AHA-ACCTOS panel for inclusion in the data analysis. This omission increases the risk of reaching a false-negative conclusion. Given these shortcomings, the AHAACC-TOS guidelines leave obese individuals with the options of calorie counting, exercise and behaviour modification (to learn to comply with the first two approaches), perhaps leading primary health-care professionals to prescribe drugs or bariatric surgery more readily. The guidelines state "A variety of dietary approaches can produce weight loss in overweight and obese adults. All of the following dietary approaches are associated with weight loss if reduction in dietary energy intake is achieved." In our opinion, this advice is not helpful. Readers should be informed whether one diet composition enhances satiety or reduces hunger better than another, and thereby reduces energy intake spontaneously. Particularly surprising is the fact that the AHA-ACC-TOS panel give a low rating for the achievement of weight loss to diets with a high protein content (and corresponding reduction of carbohydrate) or a low glycaemic index (Gl) and/or glycaemic load (GL). This rating is in marked contrast to the findings of published systematic reviews and meta-analyses. For example, a meta-analysis of 23 RCTs comprising a total of 1,141 nondiabetic individuals with obesity and evaluating low-carbohydrate diets (regardless of the composition and degree of carbohydrate restriction) showed that diets high in protein but low in carbohydrate produced a 7.0 kg weight loss over 6-12 months, and that this difference was maintained for up to 2 years.' In a second study, Kreiger et al used metaregression of RCTs to determine the effect of changes in dietary protein and carbohydrate contents during energy restriction.** These investigators included a total of 87 RCTs, equivalent to 165 intervention groups, with diets providing at least 4,200 kj ( 1,000 kcal) daily. Diets that provided less than 35-41% of energy from carbohydrate were associated with a 1.7 kg greater weight loss, a 0.7 kg greater loss of fat-free mass and a 2.1 kg greater loss of fat mass than were diets with a higher percentage of energy derived from carbohydrate. In studies of >12 weeks'
www.nature.com/nrendo
NEWS & VIEWS Box 11 Diet composition matters • High protein intake with proportionately less energy from carbohydrate enhances satiety and produces a spontaneous reduction in energy intake, leading to Increased short-term and long-term loss of body fat • Low glycaemic index (Gl) and glycaemic load (GL) diets incorporating carbohydrate-based foods that are slowly digested and elicit reduced postprandial glycaemia are linked to substantial fat loss, even when consumed ad libitum i • Diets characterized by modestly high protein intake and carbohydrate foods with a iow Gl improve weight-loss maintenance, markers of inflammation, diabetes mellitus and cardiovascular risk
duration, the observed effects increased to 6.6 kg weight loss and 5.6 kg greater loss of fat mass among individuals receiving the reduced carbohydrate diets. Protein intakes of > 1.05 g/kg were associated with 0.60 kg of additional fat-free mass retention compared to diets with protein intakes below this level. Taken together, these two studies indicate that an appreciable body of evidence supports increased dietary protein content as a method to enhance weight loss among overweight and obese individuals, both in the short term and long term. Carbohydrates present in different foods have distinct physiological effects, including those on postprandial glycaemia and insulinaemia, which can influence the rate of digestion, appetite (hunger and satiety), fuel partitioning and metabolic rate. The quality of carbohydrate—defined by Gl and GL—is most relevant to individuals who are overweight and at increased risk of diabetes mellitus. The Gl is a food classification derived from the postprandial blood glucose response relative to a reference food, gram for gram of carbohydrate. The GL —the mathematical product ofthe Gl and the amount of carbohydrate—encapsulates both the quality and quantity of carbohydrate, and is the single best predictor of postprandial glycaemia. In overweight and insulin-resistant individuals consuming high Gl and/or GL diets, glycaemic spikes and insulin demand are excessively increased. Yet the evidence to show efficacy of low-GI and/or low-GL diets for weight loss was rated as iow by the AHAACC-TOS guidelines panel because many ofthe relevant RCTs were excluded from the analysis. For example, a meta-analysis of 24 prospective cohort studies with 7.5 million person-years of follow-up indicated that
NATURE REVIEWS ENDOCRiNOLOGY
high dietary GL was positively associated with a 1.45 relative risk of type 2 diabetes mellitus per 100 g increment in GL.^ High dietary Gl and GL can also increase the risk of coronary heart disease events.^ Metaanalyses of RCTs indicate that ad libitum low-GI and/or low-GL diets promote faster weight loss and greater loss of body fat than do conventional diets.' Women following ad libitum low-GI or low-GL diets for 12 weeks lost 80% more fat mass than those on a conventional low-fat diet." Female sex, insulin resistance and/or hyperinsulaemia might increase the risk of poor outcomes on high Gl and/or GL diets. Compared with a conventional low-fat diet, following a low-GL diet produced markedly greater decreases in weight (-5.8 versus -1.2 kg) and body fat (-2.6% versus -0.9%) at 18 months among obese adults aged 18-35 years with high levels of insulin secretion.' Reduced energy expenditure following a period of weight loss is thought to contribute to weight regain. Ebbeling et al. found that the drop in resting energy expenditure was greatest for conventional low-fat diets (205 kcal per day on average) and least for low-GI or low-GL diets (138-166 kcal per day).'" In a European study of 548 individuals, completion rate and maintenance of weight loss were highest among participants assigned to a high-protein and/or low-GI diet, whereas conventional dietary advice was associated with immediate weight regain.- Taken together, the various studies outlined above demonstrate the importance of considering dietary composition in any weight-management programme (Box 1).
íÍThenewAHA-ACC-TOS guidelines misinform both clinicians and the public... 99 The USA and Mexico currently top the global league table of obesity. This alarming situation will be difficult to reverse unless the relevant national experts acknowledge that diet composition matters, both for the prevention and management of obesity. Yes, weight loss can be achieved by any means of energy restriction, but the challenge is to achieve sustainable weight loss and prevent weight regain without increasing the risk of chronic disease. To conclude that all calories are equal and that diet composition is of no consequence is to imply that individuals struggling to lose or control weight may continue to consume a diet characterized by high-energy density and high GL as long as
it is energy-restricted. The new AHA-ACCTOS guidehnes misinform both clinicians and the public and will not help to solve the global obesity problem. Department ot Nutrition, Exercise and Sports, Faculty of Science, University of Copeniiagen, Rolighedsvej 30, DK-1958 Frederiksberg C, Denmari< (A. Astrup). Charles Perkins Centre and Schooi of Molecular Bioscience, University of Sydney, Biochemistry Building, G08, Sydney 2006, NSW, Australia (J. Brand-Miller). Correspondence to: A. Astrup [email protected] Competing interests
A. Astrup declares associations with the following companies: Gerson Lehrman Group, Global Dairy Platform, Jenny Craig. McCain Foods, McDonald's. J. Brand-Miller declares an association with the following organization: the Glycémie Index Foundation. See the articie online for fuii details of the relationships. 1.
Jensen, M. D. et ai. 2013 AHA/ACC/TOS guideline for tine management of overweight and obesity in aduits: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines and The Obesity Society. / Am. Coii. Cardioi. http://dx.doi.Org/10.1016/j.jacc.2013.ll.004. 2. Larsen. I M. et ai. Diets with higii or low protein content and glycémie index for weight-loss maintenanoe. N. Engi.J. Med. 363, 2102-2113 (2010). 3. Santos, F. L., Esteves, S. S., da Costa Pereira. A., Yancy, W. S. Jr & Nunes, J. P Systematic review and meta-analysis of dinicai trials ofthe effects of low carbohydrate diets on cardiovascular risk factors. Obes. Rev. 13,1048-1066 (2012). 4. Krieger, J. W., Sitren, H. S., Daniels, M. J. & Langkamp-Henken, B. Effects of variation in protein and carbohydrate intake on body mass and composition during energy restriction: a meta-regression. Am.J. din. Nutr. 83, 260-274 (2006). 5. Livesey.G., Taylor, R., Livesey, H. & Liu, S. Is there a dose-response relation of dietary glycémie load to risk of type 2 diabetes? Metaanalysis of prospective cohort studies. Am. J. din. Nutr. 97, 584-596 (2013). 6. Mirrahimi, I. A. et ai. Associations of glycémie index and load with coronary heart disease events: a systematic review and meta-analysis of prospeetive eohorts. J.Am. HeartAssoc. 1, e000752 (2012). 7. Thomas, D. E., Elliott, E. J. & Baur, L Low glyeaemie index or iow giyeaemie load diets for overweight and obesity. Cochrane Database of Systematic Reviews, Issue 3. Art. No.: CD005105. http://dx.doi.org/10.1002/ 14651858.CD005105.pub2. 8. MeMillan-Price. J. et al. Comparison of 4 diets of varying glycémie load on weight loss and cardiovaseular risk reduction in overweight and obese young adults: a randomised eontrolled trial. Arch, intern. Med. 166,1466-1475 (2006). 9. Ebbeling, C. B., Leidig, M. M.. Feldman, H. A., Lovesky, M. M. & Ludwig, D. S. Effeets of a lowglyeemie load vs low-fat diet in obese young adults: a randomized trial. JAMA 297, 2092-2102 (2007). 10. Ebbeling. C. B. et ai. Effeets of dietary eomposition on energy expenditure during weigiit-ioss maintenanee. JAMA 307. 2627-2634 (2012).
VOLUME 10
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133
Copyright of Nature Reviews Endocrinology is the property of Nature Publishing Group and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
3.
4.
5.
6.
syndrome: the complete task force report. Fértil. Steril. 91, 456-488 (2009). Legro. R.S. et ai. Diagnosis and treatment of polycystic ovary syndrome: an Endocrine Society clinical practice guideline. J. din. Endocrinoi. Metab. http://dx.doi.org/lO.121O/ jc.2013-2350. Moghetti, P. etai. Divergences in insuiin resistance between the different phenotypes of the polycystic ovary syndrome. J. din. Endocrinoi. Metab. 98,628-637 (2013). Palomba, S. et ai. Pregnancy in women with polycystic ovary syndrome: the effect of different phenotypes and features on obstetric and neonatal outcomes, fert/7. Steril. 94, 1805-1811 (2010). Kaira, S. K. etal. Is the fertile window extended in women with polycystic ovary syndrome? Utilizing the Society for Assisted Reproductive Technology registry to assess the impact of
reproductive aging on live-birth rate. Fertii. Steril. 100.208-213 (2013). Orio. F. etai. Cardiovascular risk in women with polycystic ovary syndrome. Fertii. Steril. 86 (Suppl. 1), S20-S21 (2006). Puurunen, J. et ai. Statin therapy worsens insulin sensitivity in women with poiycystic ovary syndrome (PCOS): a prospective. randomized, double-blind, placebo-controlled study. J. din. Endocrinoi. Metab. http:// dx.doi.org/10.1210/jc.2013-2674. Palomba, S. et ai. Evidence-based and potentiai benefits of metformin in the polycystic ovary syndrome: a comprehensive review. Endocr. Rev. 30.1-50 (2009). 10. Misso, M. L. etai. Metformin versus clomiphene citrate for infertility in non-obese women with polycystic ovary syndrome: a systematic review and meta-analysis. Hum. Reprod. Update 19,2-11 (2013).
OBESITY
Have new guidelines overiooked the roie of diet composition? Arne Astrup and Jennie Brand-Miller
New US guidelines for the management of overweight and obesity have disregarded robust evidence from intervention triais demonstrating the importance of dietary factors for weight control and disease prevention. This omission implies that diet composition does not matter, a stance that is potentiaiiy counterproductive for prevention and treatment strategies. Astrup, A. & Brand-Miller. J. Nat. Rev. Endocrinoi. 10.132-133 (2014): published online 14 January 2014: doi:10.1038/nrendo.2013.271
Assessing the scientific robustness of strategies designed to encourage weight loss (and its subsequent maintenance) and to improve risk factors among individuals who are overweight or obese can be difficult. The demand for successful weight-loss strategies is great as most US and European adults are overweight, and 20-35% are obese. These two conditions are recognized to cause reduced quality of life, increased disease load and premature mortality and, therefore, represent a major economic burden for society. A group of leading US experts has produced a set of guidelines for the management of overweight and obesity on behalf of the American Heart Association (AHA), the American College of Cardiology (ACC) and The Obesity Society (TOS).' These guidelines provide an evidence base to check the validity ofthe various ways to achieve and maintain weight loss and as such are most welcome. Nevertheless, they fall short because the importance of diet composition has been completely overlooked. The AHA-ACC-TOS guidelines comprise a comprehensive, yet condensed, list of almost all relevant treatment modalities, excluding weight-loss drugs, but including
132
MARCH 2014
VOLUME 10
bariatric surgery. Strength of evidence for the efficacy of each treatment option is rated by the guideline development panel as 'low', 'moderate' or 'high', which is the standard approach taken in guideline development. However, the required evidence underpinning these rankings is strikingly different from that used in systematic reviews and meta-analyses. The obvious reason for this discrepancy is that the AHA-ACC-TOS evidence synthesis applied rules for quality assessment required by the US Institute of Medicine. These rules were developed specifically for drug trials and exclude randomized controlled trials (RCTs) with a retention rate below 90% for 'compléter' analyses or below 80% for 'intention-to-treat' analyses. The Institute of Medicine criteria are clearly appropriate for their intended purpose; however, if applied to dietary intervention trials, they exclude a vast body of evidence. Trials of dietary interventions require participants to consume all meals every day over a period of several months in compliance with one particular diet composition. Consequently, retention rate should not be used solely as an indicator of trial
quality, but rather as a primary outcome that provides a measure ofthe success and acceptability ofthe diet.' However, no critical assessment of diet adherence (for example, measurement of urinary nitrogen excretion among individuals following a high-protein diet) was made for the few trials of dietary intervention accepted by the AHA-ACCTOS panel for inclusion in the data analysis. This omission increases the risk of reaching a false-negative conclusion. Given these shortcomings, the AHAACC-TOS guidelines leave obese individuals with the options of calorie counting, exercise and behaviour modification (to learn to comply with the first two approaches), perhaps leading primary health-care professionals to prescribe drugs or bariatric surgery more readily. The guidelines state "A variety of dietary approaches can produce weight loss in overweight and obese adults. All of the following dietary approaches are associated with weight loss if reduction in dietary energy intake is achieved." In our opinion, this advice is not helpful. Readers should be informed whether one diet composition enhances satiety or reduces hunger better than another, and thereby reduces energy intake spontaneously. Particularly surprising is the fact that the AHA-ACC-TOS panel give a low rating for the achievement of weight loss to diets with a high protein content (and corresponding reduction of carbohydrate) or a low glycaemic index (Gl) and/or glycaemic load (GL). This rating is in marked contrast to the findings of published systematic reviews and meta-analyses. For example, a meta-analysis of 23 RCTs comprising a total of 1,141 nondiabetic individuals with obesity and evaluating low-carbohydrate diets (regardless of the composition and degree of carbohydrate restriction) showed that diets high in protein but low in carbohydrate produced a 7.0 kg weight loss over 6-12 months, and that this difference was maintained for up to 2 years.' In a second study, Kreiger et al used metaregression of RCTs to determine the effect of changes in dietary protein and carbohydrate contents during energy restriction.** These investigators included a total of 87 RCTs, equivalent to 165 intervention groups, with diets providing at least 4,200 kj ( 1,000 kcal) daily. Diets that provided less than 35-41% of energy from carbohydrate were associated with a 1.7 kg greater weight loss, a 0.7 kg greater loss of fat-free mass and a 2.1 kg greater loss of fat mass than were diets with a higher percentage of energy derived from carbohydrate. In studies of >12 weeks'
www.nature.com/nrendo
NEWS & VIEWS Box 11 Diet composition matters • High protein intake with proportionately less energy from carbohydrate enhances satiety and produces a spontaneous reduction in energy intake, leading to Increased short-term and long-term loss of body fat • Low glycaemic index (Gl) and glycaemic load (GL) diets incorporating carbohydrate-based foods that are slowly digested and elicit reduced postprandial glycaemia are linked to substantial fat loss, even when consumed ad libitum i • Diets characterized by modestly high protein intake and carbohydrate foods with a iow Gl improve weight-loss maintenance, markers of inflammation, diabetes mellitus and cardiovascular risk
duration, the observed effects increased to 6.6 kg weight loss and 5.6 kg greater loss of fat mass among individuals receiving the reduced carbohydrate diets. Protein intakes of > 1.05 g/kg were associated with 0.60 kg of additional fat-free mass retention compared to diets with protein intakes below this level. Taken together, these two studies indicate that an appreciable body of evidence supports increased dietary protein content as a method to enhance weight loss among overweight and obese individuals, both in the short term and long term. Carbohydrates present in different foods have distinct physiological effects, including those on postprandial glycaemia and insulinaemia, which can influence the rate of digestion, appetite (hunger and satiety), fuel partitioning and metabolic rate. The quality of carbohydrate—defined by Gl and GL—is most relevant to individuals who are overweight and at increased risk of diabetes mellitus. The Gl is a food classification derived from the postprandial blood glucose response relative to a reference food, gram for gram of carbohydrate. The GL —the mathematical product ofthe Gl and the amount of carbohydrate—encapsulates both the quality and quantity of carbohydrate, and is the single best predictor of postprandial glycaemia. In overweight and insulin-resistant individuals consuming high Gl and/or GL diets, glycaemic spikes and insulin demand are excessively increased. Yet the evidence to show efficacy of low-GI and/or low-GL diets for weight loss was rated as iow by the AHAACC-TOS guidelines panel because many ofthe relevant RCTs were excluded from the analysis. For example, a meta-analysis of 24 prospective cohort studies with 7.5 million person-years of follow-up indicated that
NATURE REVIEWS ENDOCRiNOLOGY
high dietary GL was positively associated with a 1.45 relative risk of type 2 diabetes mellitus per 100 g increment in GL.^ High dietary Gl and GL can also increase the risk of coronary heart disease events.^ Metaanalyses of RCTs indicate that ad libitum low-GI and/or low-GL diets promote faster weight loss and greater loss of body fat than do conventional diets.' Women following ad libitum low-GI or low-GL diets for 12 weeks lost 80% more fat mass than those on a conventional low-fat diet." Female sex, insulin resistance and/or hyperinsulaemia might increase the risk of poor outcomes on high Gl and/or GL diets. Compared with a conventional low-fat diet, following a low-GL diet produced markedly greater decreases in weight (-5.8 versus -1.2 kg) and body fat (-2.6% versus -0.9%) at 18 months among obese adults aged 18-35 years with high levels of insulin secretion.' Reduced energy expenditure following a period of weight loss is thought to contribute to weight regain. Ebbeling et al. found that the drop in resting energy expenditure was greatest for conventional low-fat diets (205 kcal per day on average) and least for low-GI or low-GL diets (138-166 kcal per day).'" In a European study of 548 individuals, completion rate and maintenance of weight loss were highest among participants assigned to a high-protein and/or low-GI diet, whereas conventional dietary advice was associated with immediate weight regain.- Taken together, the various studies outlined above demonstrate the importance of considering dietary composition in any weight-management programme (Box 1).
íÍThenewAHA-ACC-TOS guidelines misinform both clinicians and the public... 99 The USA and Mexico currently top the global league table of obesity. This alarming situation will be difficult to reverse unless the relevant national experts acknowledge that diet composition matters, both for the prevention and management of obesity. Yes, weight loss can be achieved by any means of energy restriction, but the challenge is to achieve sustainable weight loss and prevent weight regain without increasing the risk of chronic disease. To conclude that all calories are equal and that diet composition is of no consequence is to imply that individuals struggling to lose or control weight may continue to consume a diet characterized by high-energy density and high GL as long as
it is energy-restricted. The new AHA-ACCTOS guidehnes misinform both clinicians and the public and will not help to solve the global obesity problem. Department ot Nutrition, Exercise and Sports, Faculty of Science, University of Copeniiagen, Rolighedsvej 30, DK-1958 Frederiksberg C, Denmari< (A. Astrup). Charles Perkins Centre and Schooi of Molecular Bioscience, University of Sydney, Biochemistry Building, G08, Sydney 2006, NSW, Australia (J. Brand-Miller). Correspondence to: A. Astrup [email protected] Competing interests
A. Astrup declares associations with the following companies: Gerson Lehrman Group, Global Dairy Platform, Jenny Craig. McCain Foods, McDonald's. J. Brand-Miller declares an association with the following organization: the Glycémie Index Foundation. See the articie online for fuii details of the relationships. 1.
Jensen, M. D. et ai. 2013 AHA/ACC/TOS guideline for tine management of overweight and obesity in aduits: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines and The Obesity Society. / Am. Coii. Cardioi. http://dx.doi.Org/10.1016/j.jacc.2013.ll.004. 2. Larsen. I M. et ai. Diets with higii or low protein content and glycémie index for weight-loss maintenanoe. N. Engi.J. Med. 363, 2102-2113 (2010). 3. Santos, F. L., Esteves, S. S., da Costa Pereira. A., Yancy, W. S. Jr & Nunes, J. P Systematic review and meta-analysis of dinicai trials ofthe effects of low carbohydrate diets on cardiovascular risk factors. Obes. Rev. 13,1048-1066 (2012). 4. Krieger, J. W., Sitren, H. S., Daniels, M. J. & Langkamp-Henken, B. Effects of variation in protein and carbohydrate intake on body mass and composition during energy restriction: a meta-regression. Am.J. din. Nutr. 83, 260-274 (2006). 5. Livesey.G., Taylor, R., Livesey, H. & Liu, S. Is there a dose-response relation of dietary glycémie load to risk of type 2 diabetes? Metaanalysis of prospective cohort studies. Am. J. din. Nutr. 97, 584-596 (2013). 6. Mirrahimi, I. A. et ai. Associations of glycémie index and load with coronary heart disease events: a systematic review and meta-analysis of prospeetive eohorts. J.Am. HeartAssoc. 1, e000752 (2012). 7. Thomas, D. E., Elliott, E. J. & Baur, L Low glyeaemie index or iow giyeaemie load diets for overweight and obesity. Cochrane Database of Systematic Reviews, Issue 3. Art. No.: CD005105. http://dx.doi.org/10.1002/ 14651858.CD005105.pub2. 8. MeMillan-Price. J. et al. Comparison of 4 diets of varying glycémie load on weight loss and cardiovaseular risk reduction in overweight and obese young adults: a randomised eontrolled trial. Arch, intern. Med. 166,1466-1475 (2006). 9. Ebbeling, C. B., Leidig, M. M.. Feldman, H. A., Lovesky, M. M. & Ludwig, D. S. Effeets of a lowglyeemie load vs low-fat diet in obese young adults: a randomized trial. JAMA 297, 2092-2102 (2007). 10. Ebbeling. C. B. et ai. Effeets of dietary eomposition on energy expenditure during weigiit-ioss maintenanee. JAMA 307. 2627-2634 (2012).
VOLUME 10
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Copyright of Nature Reviews Endocrinology is the property of Nature Publishing Group and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.
