Journals of Gerontology: MEDICAL SCIENCES Cite journal as: J Gerontol A Biol Sci Med Sci. 2014 January;69(1):61–62 doi:10.1093/gerona/glt185
© The Author 2013. Published by Oxford University Press on behalf of The Gerontological Society of America. All rights reserved. For permissions, please e-mail: [email protected].
Editorial
Obesity in the Sarcopenia Era Stephen B. Kritchevsky Sticht Center on Aging, Wake Forest School of Medicine, Winston-Salem, North Carolina. Address correspondence to Stephen Kritchevsky, PhD, Sticht Center on Aging, Medical Center Boulevard, Winston-Salem, NC 27157. Email: [email protected]
Decision Editor: Stephen Kritchevsky, PhD
W
ith the coining of the term “sarcopenia,” lean body mass has been a major focus of aging research for the past 25 years. The motivating idea is that weakness, a hallmark of physical disability, is determined by skeletal muscle mass. Therefore, a logical strategy to prevent disability would be to slow or reverse age-related decreases in muscle mass (1). However, evidence shows that the situation is more nuanced than originally expected. In communitydwelling older adults, the linkage between lean mass and strength is not especially strong, and some interventions that are effective in increasing lean mass do not appear to affect strength (2,3). Furthermore, intentional weight loss in obese older adults does not necessarily reduce muscle strength, despite significant reductions in muscle mass (4). In contrast to what might be predicted by the sarcopenia hypothesis, there have been five moderate to large clinical trials showing that weight loss improves physical performance and that this effect is additive to the benefits of exercise (5–9). Furthermore, the degree of functional improvement is correlated with the extent of adipose tissue loss (10). The benefits of physical activity seem to be blunted in obese older adults (11), and high levels of adiposity accelerate aging-related loss of lean mass (12). Concerns that intentional weight loss might predispose overweight or obese older persons to a higher mortality risk appear unwarranted (13). Excess adipose tissue and obesity have emerged as strong contributors to physical limitation and functional decline (14). In the Framingham Study, for example, Visser et al. (15) found that those in the highest tertile of fat mass were more than 160% more likely to have self-reported disability compared with those in the bottom tertile. There was no association between disability and lean mass. Adiposity and obesity lead to disability through both direct and indirect pathways. From a biomechanical perspective, obesity increases the effort required to move for given strength; it also alters the gait mechanics impairing walking efficiency
(16,17). Obesity is a strong contributor to the most prevalent disabling health conditions—osteoarthritis, heart disease, diabetes, and stroke, and is a strong driver of multimorbidity (18). Obesity is associated with high levels of circulating inflammatory cytokines (eg, interleukin-6 and c-reactive protein), which predict functional decline in older adults (19). With aging, there is a tendency to deposit fat in and around organs. Specific functional and metabolic derangements have been seen with fat deposited in and around skeletal muscle, the heart, and the liver (20–22). Although this deposition is higher in obese individuals, the organ-specific associations are largely independent of whole body measures of obesity. This issue of the Journal presents several articles on obesity and related health outcomes to focus attention on this important area. These articles report data from the United States, France, Finland, and Iceland showing the impact of obesity on the longevity of older black Americans (23); the long-term functional impact of midlife obesity on frailty in old age (24); the impact of metabolic syndrome, a major obesity-related health condition, on incident mobility and instrumental activities of daily living limitation (25); and the age-dependent nature of the relationship between body mass index and cardiovascular disease and its risk factors (26). Three papers substantially advance the conversation on body composition and health and function. Tseng et al. (27) present data showing that body composition measures help explain gender differences in physical performance between older men and women. Manini et al. (28) present data from a trial of caloric restriction with exercise showing that the extent of reductions in both intramuscular and subcutaneous calf fat were correlated with increased walking speed. Finally, the report from Murphy et al. (29) points to a new research direction by linking the density of fat as assessed by CT to mortality risk. The paper includes data from nonhuman primates that explore the possible mechanistic basis for this novel finding. Denser fat is associated with small adipocyte 61
Downloaded from http://biomedgerontology.oxfordjournals.org/ at University of Hawaii - Manoa on June 29, 2015
Received October 16, 2013; Accepted October 16, 2013
62 KRITCHEVSKY
size, and lower leptin and higher adiponectin expression in fat cells. It is not, however, associated with inflammation at either the adipose tissue or the systemic level, suggesting there are additional health biomarkers linked to adipose tissue still to be elucidated. In the United States, 40.8% of 65- to 74-year-olds and 27.8% of those 75+ are obese, making it more common than sarcopenia in community-dwelling older adults (30). Given obesity’s high prevalence in older adults, and its strong association with functional impairment, it deserves the focused attention of medical gerontology.
Downloaded from http://biomedgerontology.oxfordjournals.org/ at University of Hawaii - Manoa on June 29, 2015
References 1. Dutta C, Hadley EC. The significance of sarcopenia in old age. J Gerontol A Biol Sci Med Sci. 1995;50:1–4. 2. Goodpaster BH, Park SW, Harris TB, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61:1059–1064. 3. Giannoulis MG, Sonksen PH, Umpleby M, et al. The effects of growth hormone and/or testosterone in healthy elderly men: a randomized controlled trial. J Clin Endocrinol Metab. 2006;91:477–484. 4. Marsh AP, Shea MK, Vance Locke RM, et al. Resistance training and pioglitazone lead to improvements in muscle power during voluntary weight loss in older adults. J Gerontol A Biol Sci Med Sci. 2013;68:828–836. 5. Messier SP, Loeser RF, Miller GD, et al. Exercise and dietary weight loss in overweight and obese older adults with knee osteoarthritis: the Arthritis, Diet, and Activity Promotion Trial. Arthritis Rheum. 2004;50:1501–1510. 6. Villareal DT, Chode S, Parimi N, et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med. 2011;364:1218–1229. 7. Rejeski WJ, Brubaker PH, Goff DC Jr, et al. Translating weight loss and physical activity programs into the community to preserve mobility in older, obese adults in poor cardiovascular health. Arch Intern Med. 2011;171:880–886. 8. Rejeski WJ, Ip EH, Bertoni AG, et al. Look AHEAD Research Group. Lifestyle change and mobility in obese adults with type 2 diabetes. N Engl J Med. 2012;366:1209–1217. 9. Messier SP, Mihalko SL, Legault C, et al. Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial. JAMA. 2013;310:1263–1273. 10. Beavers KM, Miller ME, Rejeski WJ, Nicklas BJ, Krichevsky SB. Fat mass loss predicts gain in physical function with intentional weight loss in older adults. J Gerontol A Biol Sci Med Sci. 2013;68:80–86. 11. Koster A, Patel KV, Visser M, et al. Health, Aging and Body Composition Study. Joint effects of adiposity and physical activity on incident mobility limitation in older adults. J Am Geriatr Soc. 2008;56:636–643. 12. Koster A, Ding J, Stenholm S, et al. Health ABC study. Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults? J Gerontol A Biol Sci Med Sci. 2011;66:888–895. 13. Shea MK, Nicklas BJ, Houston DK, et al. The effect of intentional weight loss on all-cause mortality in older adults: results of a randomized controlled weight-loss trial. Am J Clin Nutr. 2011;94:839–846.
14. Rejeski WJ, Marsh AP, Chmelo E, Rejeski JJ. Obesity, inten tional weight loss and physical disability in older adults. Obes Rev. 2010;11:671–685. 15. Visser M, Harris TB, Langlois J, et al. Body fat and skeletal muscle mass in relation to physical disability in very old men and women of the Framingham Heart Study. J Gerontol A Biol Sci Med Sci. 1998;53:M214–M221. 16. Runhaar J, Koes BW, Clockaerts S, Bierma-Zeinstra SM. A systematic review on changed biomechanics of lower extremities in obese individuals: a possible role in development of osteoarthritis. Obes Rev. 2011;12:1071–1082. 17. Ko S, Stenholm S, Ferrucci L. Characteristic gait patterns in older adults with obesity–results from the Baltimore Longitudinal Study of Aging. J Biomech. 2010;43:1104–1110. 18. van den Bussche H, Koller D, Kolonko T, et al. Which chronic diseases and disease combinations are specific to multimorbidity in the elderly? Results of a claims data based cross-sectional study in Germany. BMC Public Health. 2011;11:101. 19. Brinkley TE, Hsu FC, Beavers KM, et al. Total and abdomi nal adiposity are associated with inflammation in older adults using a factor analysis approach. J Gerontol A Biol Sci Med Sci. 2012;67:1099–1106. 20. Beavers KM, Beavers DP, Houston DK, et al. Associations between body composition and gait-speed decline: results from the Health, Aging, and Body Composition study. Am J Clin Nutr. 2013;97:552–560. 21. Ding J, Hsu FC, Harris TB, et al. The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am J Clin Nutr. 2009;90:499–504. 22. Asrih M, Jornayvaz FR. Inflammation as a potential link between nonalcoholic fatty liver disease and insulin resistance. J Endocrinol. 2013;218:R25–R36. 23. Singh PN, Clark RW, Herring P, Sabaté J, Shavlik D, Fraser GE. Obesity and life expectancy among long-lived black adults. J Gerontol A Biol Sci Med Sci. 2014;69. 24. Stenholm S, Strandberg TE, Pitkälä K, Sainio P, Heliövaara M, Koskinen S. Midlife obesity and risk of frailty in old age during a 22-year follow-up in men and women: The Mini-Finland Follow-up Survey. J Gerontol A Biol Sci Med Sci. 2014;69. 25. Carriere I, Pérès K, Ancelin ML, et al. Metabolic syndrome and disability: findings from the Prospective Three-City Study. J Gerontol A Biol Sci Med Sci. 2014;69. 26. Canning KL, Brown RE, Jamnik VK, Kuk JL. Relationship between obesity and obesity-related morbidities weakens with aging. J Gerontol A Biol Sci Med Sci. 2014;69. 27. Tseng LA, Delmonico MJ, Visser M, et al. Body composition explains sex differential in physical performance among older adults. J Gerontol A Biol Sci Med Sci. 2014;69. 28. Manini TM, Buford TW, Lott DJ, et al. Effect of dietary restriction and exercise on lower extremity tissue compartments in obese, older women: a pilot study. J Gerontol A Biol Sci Med Sci. 2014;69. 29. Murphy RA, Register TC, Shively CA, et al. Adipose tissue density, a novel biomarker predicting mortality risk in older adults. J Gerontol A Biol Sci Med Sci. 2014;69. 30. Fakhouri TH, Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of Obesity Among Older Adults in the United States, 2007–2010. NCHS data brief, no 106. Hyattsville, MD: National Center for Health Statistics; 2012.
© The Author 2013. Published by Oxford University Press on behalf of The Gerontological Society of America. All rights reserved. For permissions, please e-mail: [email protected].
Editorial
Obesity in the Sarcopenia Era Stephen B. Kritchevsky Sticht Center on Aging, Wake Forest School of Medicine, Winston-Salem, North Carolina. Address correspondence to Stephen Kritchevsky, PhD, Sticht Center on Aging, Medical Center Boulevard, Winston-Salem, NC 27157. Email: [email protected]
Decision Editor: Stephen Kritchevsky, PhD
W
ith the coining of the term “sarcopenia,” lean body mass has been a major focus of aging research for the past 25 years. The motivating idea is that weakness, a hallmark of physical disability, is determined by skeletal muscle mass. Therefore, a logical strategy to prevent disability would be to slow or reverse age-related decreases in muscle mass (1). However, evidence shows that the situation is more nuanced than originally expected. In communitydwelling older adults, the linkage between lean mass and strength is not especially strong, and some interventions that are effective in increasing lean mass do not appear to affect strength (2,3). Furthermore, intentional weight loss in obese older adults does not necessarily reduce muscle strength, despite significant reductions in muscle mass (4). In contrast to what might be predicted by the sarcopenia hypothesis, there have been five moderate to large clinical trials showing that weight loss improves physical performance and that this effect is additive to the benefits of exercise (5–9). Furthermore, the degree of functional improvement is correlated with the extent of adipose tissue loss (10). The benefits of physical activity seem to be blunted in obese older adults (11), and high levels of adiposity accelerate aging-related loss of lean mass (12). Concerns that intentional weight loss might predispose overweight or obese older persons to a higher mortality risk appear unwarranted (13). Excess adipose tissue and obesity have emerged as strong contributors to physical limitation and functional decline (14). In the Framingham Study, for example, Visser et al. (15) found that those in the highest tertile of fat mass were more than 160% more likely to have self-reported disability compared with those in the bottom tertile. There was no association between disability and lean mass. Adiposity and obesity lead to disability through both direct and indirect pathways. From a biomechanical perspective, obesity increases the effort required to move for given strength; it also alters the gait mechanics impairing walking efficiency
(16,17). Obesity is a strong contributor to the most prevalent disabling health conditions—osteoarthritis, heart disease, diabetes, and stroke, and is a strong driver of multimorbidity (18). Obesity is associated with high levels of circulating inflammatory cytokines (eg, interleukin-6 and c-reactive protein), which predict functional decline in older adults (19). With aging, there is a tendency to deposit fat in and around organs. Specific functional and metabolic derangements have been seen with fat deposited in and around skeletal muscle, the heart, and the liver (20–22). Although this deposition is higher in obese individuals, the organ-specific associations are largely independent of whole body measures of obesity. This issue of the Journal presents several articles on obesity and related health outcomes to focus attention on this important area. These articles report data from the United States, France, Finland, and Iceland showing the impact of obesity on the longevity of older black Americans (23); the long-term functional impact of midlife obesity on frailty in old age (24); the impact of metabolic syndrome, a major obesity-related health condition, on incident mobility and instrumental activities of daily living limitation (25); and the age-dependent nature of the relationship between body mass index and cardiovascular disease and its risk factors (26). Three papers substantially advance the conversation on body composition and health and function. Tseng et al. (27) present data showing that body composition measures help explain gender differences in physical performance between older men and women. Manini et al. (28) present data from a trial of caloric restriction with exercise showing that the extent of reductions in both intramuscular and subcutaneous calf fat were correlated with increased walking speed. Finally, the report from Murphy et al. (29) points to a new research direction by linking the density of fat as assessed by CT to mortality risk. The paper includes data from nonhuman primates that explore the possible mechanistic basis for this novel finding. Denser fat is associated with small adipocyte 61
Downloaded from http://biomedgerontology.oxfordjournals.org/ at University of Hawaii - Manoa on June 29, 2015
Received October 16, 2013; Accepted October 16, 2013
62 KRITCHEVSKY
size, and lower leptin and higher adiponectin expression in fat cells. It is not, however, associated with inflammation at either the adipose tissue or the systemic level, suggesting there are additional health biomarkers linked to adipose tissue still to be elucidated. In the United States, 40.8% of 65- to 74-year-olds and 27.8% of those 75+ are obese, making it more common than sarcopenia in community-dwelling older adults (30). Given obesity’s high prevalence in older adults, and its strong association with functional impairment, it deserves the focused attention of medical gerontology.
Downloaded from http://biomedgerontology.oxfordjournals.org/ at University of Hawaii - Manoa on June 29, 2015
References 1. Dutta C, Hadley EC. The significance of sarcopenia in old age. J Gerontol A Biol Sci Med Sci. 1995;50:1–4. 2. Goodpaster BH, Park SW, Harris TB, et al. The loss of skeletal muscle strength, mass, and quality in older adults: the health, aging and body composition study. J Gerontol A Biol Sci Med Sci. 2006;61:1059–1064. 3. Giannoulis MG, Sonksen PH, Umpleby M, et al. The effects of growth hormone and/or testosterone in healthy elderly men: a randomized controlled trial. J Clin Endocrinol Metab. 2006;91:477–484. 4. Marsh AP, Shea MK, Vance Locke RM, et al. Resistance training and pioglitazone lead to improvements in muscle power during voluntary weight loss in older adults. J Gerontol A Biol Sci Med Sci. 2013;68:828–836. 5. Messier SP, Loeser RF, Miller GD, et al. Exercise and dietary weight loss in overweight and obese older adults with knee osteoarthritis: the Arthritis, Diet, and Activity Promotion Trial. Arthritis Rheum. 2004;50:1501–1510. 6. Villareal DT, Chode S, Parimi N, et al. Weight loss, exercise, or both and physical function in obese older adults. N Engl J Med. 2011;364:1218–1229. 7. Rejeski WJ, Brubaker PH, Goff DC Jr, et al. Translating weight loss and physical activity programs into the community to preserve mobility in older, obese adults in poor cardiovascular health. Arch Intern Med. 2011;171:880–886. 8. Rejeski WJ, Ip EH, Bertoni AG, et al. Look AHEAD Research Group. Lifestyle change and mobility in obese adults with type 2 diabetes. N Engl J Med. 2012;366:1209–1217. 9. Messier SP, Mihalko SL, Legault C, et al. Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial. JAMA. 2013;310:1263–1273. 10. Beavers KM, Miller ME, Rejeski WJ, Nicklas BJ, Krichevsky SB. Fat mass loss predicts gain in physical function with intentional weight loss in older adults. J Gerontol A Biol Sci Med Sci. 2013;68:80–86. 11. Koster A, Patel KV, Visser M, et al. Health, Aging and Body Composition Study. Joint effects of adiposity and physical activity on incident mobility limitation in older adults. J Am Geriatr Soc. 2008;56:636–643. 12. Koster A, Ding J, Stenholm S, et al. Health ABC study. Does the amount of fat mass predict age-related loss of lean mass, muscle strength, and muscle quality in older adults? J Gerontol A Biol Sci Med Sci. 2011;66:888–895. 13. Shea MK, Nicklas BJ, Houston DK, et al. The effect of intentional weight loss on all-cause mortality in older adults: results of a randomized controlled weight-loss trial. Am J Clin Nutr. 2011;94:839–846.
14. Rejeski WJ, Marsh AP, Chmelo E, Rejeski JJ. Obesity, inten tional weight loss and physical disability in older adults. Obes Rev. 2010;11:671–685. 15. Visser M, Harris TB, Langlois J, et al. Body fat and skeletal muscle mass in relation to physical disability in very old men and women of the Framingham Heart Study. J Gerontol A Biol Sci Med Sci. 1998;53:M214–M221. 16. Runhaar J, Koes BW, Clockaerts S, Bierma-Zeinstra SM. A systematic review on changed biomechanics of lower extremities in obese individuals: a possible role in development of osteoarthritis. Obes Rev. 2011;12:1071–1082. 17. Ko S, Stenholm S, Ferrucci L. Characteristic gait patterns in older adults with obesity–results from the Baltimore Longitudinal Study of Aging. J Biomech. 2010;43:1104–1110. 18. van den Bussche H, Koller D, Kolonko T, et al. Which chronic diseases and disease combinations are specific to multimorbidity in the elderly? Results of a claims data based cross-sectional study in Germany. BMC Public Health. 2011;11:101. 19. Brinkley TE, Hsu FC, Beavers KM, et al. Total and abdomi nal adiposity are associated with inflammation in older adults using a factor analysis approach. J Gerontol A Biol Sci Med Sci. 2012;67:1099–1106. 20. Beavers KM, Beavers DP, Houston DK, et al. Associations between body composition and gait-speed decline: results from the Health, Aging, and Body Composition study. Am J Clin Nutr. 2013;97:552–560. 21. Ding J, Hsu FC, Harris TB, et al. The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am J Clin Nutr. 2009;90:499–504. 22. Asrih M, Jornayvaz FR. Inflammation as a potential link between nonalcoholic fatty liver disease and insulin resistance. J Endocrinol. 2013;218:R25–R36. 23. Singh PN, Clark RW, Herring P, Sabaté J, Shavlik D, Fraser GE. Obesity and life expectancy among long-lived black adults. J Gerontol A Biol Sci Med Sci. 2014;69. 24. Stenholm S, Strandberg TE, Pitkälä K, Sainio P, Heliövaara M, Koskinen S. Midlife obesity and risk of frailty in old age during a 22-year follow-up in men and women: The Mini-Finland Follow-up Survey. J Gerontol A Biol Sci Med Sci. 2014;69. 25. Carriere I, Pérès K, Ancelin ML, et al. Metabolic syndrome and disability: findings from the Prospective Three-City Study. J Gerontol A Biol Sci Med Sci. 2014;69. 26. Canning KL, Brown RE, Jamnik VK, Kuk JL. Relationship between obesity and obesity-related morbidities weakens with aging. J Gerontol A Biol Sci Med Sci. 2014;69. 27. Tseng LA, Delmonico MJ, Visser M, et al. Body composition explains sex differential in physical performance among older adults. J Gerontol A Biol Sci Med Sci. 2014;69. 28. Manini TM, Buford TW, Lott DJ, et al. Effect of dietary restriction and exercise on lower extremity tissue compartments in obese, older women: a pilot study. J Gerontol A Biol Sci Med Sci. 2014;69. 29. Murphy RA, Register TC, Shively CA, et al. Adipose tissue density, a novel biomarker predicting mortality risk in older adults. J Gerontol A Biol Sci Med Sci. 2014;69. 30. Fakhouri TH, Ogden CL, Carroll MD, Kit BK, Flegal KM. Prevalence of Obesity Among Older Adults in the United States, 2007–2010. NCHS data brief, no 106. Hyattsville, MD: National Center for Health Statistics; 2012.
