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Curr Opin Clin Nutr Metab Care. Author manuscript; available in PMC 2009 Jan 30.
Published in final edited form as:
Curr Opin Clin Nutr Metab Care. 2008 Nov; 11(6): 693–700.
doi: 10.1097/MCO.0b013e328312c37d
PMCID: PMC2633408
NIHMSID: NIHMS63521
PMID: 18827572

Sarcopenic obesity - definition, etiology and consequences

Sari Stenholm, PhD,1,2 Tamara B. Harris, MD, MS,3 Taina Rantanen, PhD,4 Marjolein Visser, PhD,5 Stephen B. Kritchevsky, PhD,6 and Luigi Ferrucci, MD, PhD1
Author information Copyright and License information PMC Disclaimer

Abstract

Purpose of the review

Older obese persons with decreased muscle mass or strength are at special risk for adverse outcomes. We discuss potential pathways to muscle impairment in obese individuals and the consequences that joint obesity and muscle impairment may have on health and disability. Tantamount to this discussion is whether low muscle mass or, rather, muscle weakness should be used for the definition.

Recent findings

Excess energy intake, physical inactivity, low-grade inflammation, insulin resistance and changes in hormonal milieu may lead to the development of so called ‘sarcopenic obesity’. It was originally believed that the culprit of age-related muscle weakness was a reduction in muscle mass, but it is now clear that changes in muscle composition and quality are predominant. We propose that the risk of adverse outcomes, such as functional limitation and mortality, is better estimated by considering jointly obesity and muscle strength rather than obesity and muscle mass and the term “sarcopenic obesity” should be revisited.

Summary

Recognition of obese patients who have associated muscle problems is an essential goal for clinicians. Further research is needed to identify new target for prevention and cure of this important geriatric syndrome.

Keywords: adipose tissue, body composition, disability, muscle strength, obesity, older people, sarcopenia

Introduction

This review focuses on a specific feature of obesity, which has been termed “sarcopenic obesity” [1, 2**]. In any healthy young and older individuals bone and muscle grow in harmony with change in weight. This harmony is maintained by gravity stimulating the mechanoreceptors in bone and muscle that modulate the production of growth factors [3, 4]. This adaptive physiological mechanism may be impaired in some older individuals who become frankly obese without a parallel growth of muscle mass and increment of strength. As a consequence, obese persons may end up having too low muscle strength relative to their body size.

We begin by exploring the current definition of and discuss why the term ‘sarcopenia’, examined within the limits of its etymological roots, is a source of confusion in this field. Next, we will examine the hypothetical pathways that can lead to the obesity/muscle impairment syndrome. Finally, we review the literature on the consequences of sarcopenic obesity in terms of functional and health-related outcomes.

Searching for a definition based on pathophysiology and associated risk

The development of a research agenda on the combined effect of muscle impairment and obesity is hampered by the lack of a widely agreed operational definition. The definitions of muscle impairment and obesity in older persons are controversial and their clustering and synergy in a syndromic entity remain hypothetical.

Obesity is defined as abnormal or extensive fat accumulation that negatively affects health [5]. According to the World Health Organization [5], obesity is defined as Body Mass Index (BMI) ≥ 30 kg/m 2 and central obesity as a waist circumference greater than 102 cm in men and 88 cm in women. Whether these criteria are appropriate for older individuals has been questioned.

The term sarcopenia comes from the Greek words sarx (meaning flesh) and penia (meaning loss) was originally meant to represent age-related loss of muscle mass with aging [6-9]. At the time this concept was coined, scientists believed that the age-associated decline of muscle strength was largely due to a parallel decline of muscle mass [10, 11], and therefore the study of muscle mass was in some way equivalent to the study of muscle function. Baumgartner et al. [12] defined sarcopenia as “appendicular skeletal muscle mass divided by body height squared in meters (muscle mass index)” two standard deviations or more below reference values from young, healthy individuals measured with dual X-ray absorptiometry (DXA). In 2002, Janssen et al. proposed to convert absolute skeletal muscle mass (kg) to percentage of weight (muscle mass / body mass × 100) and to define sarcopenia as more than one standard deviation below the reference values from young, healthy individuals measured with bioelectrical impedance. Criteria for the sarcopenia proposed more recently are based on the amount of lean mass lower than expected for a given amount of fat mass using residuals from linear regression models [13] and ratio between appendicular lean mass and appendicular fat (Harris et al. unpublished data).

The idea that decline in muscle function is largely explained by the parallel decline in mass has not been proven true. Both muscle mass and muscle strength decline with aging, but the decline in strength exceeds what is expected based on the decline in mass [14, 15*, 16]. The progressive mismatch between mass and strength occurs because of a progressive deterioration of muscle “quality”, including decrease in fiber size and number, intrinsic reduction of contractility in the intact fibers [17, 18], fat micro and macro-infiltration [19, 20], increase in collagen, modification of the motor unit, and impaired neurological modulation of contraction [21]. Evidence has also emerged that muscle strength is more important than muscle mass as a determinant of functional limitation and poor health in older age [14, 22-24].

In the complex choice between muscle mass and muscle strength as valid markers of age-related muscle impairment, it is useful to recapitulate the methodological work that led to the definition of osteoporosis. Initially bone mineral density was proposed as a diagnostic marker of osteoporosis because it reflected morphometric changes in bone that occurred over the lifetime and was accelerated by menopause. Subsequent studies demonstrated that bone mineral density discriminated individuals at high risk of fracture [25]. Later studies have indicated that not only bone structure, but bone quality, may contribute to fracture risk, along with functional aspects of health such as weight loss and frailty [25, 26]. Similarly, age-related changes in muscle tissue are mostly interesting because of their functional consequences. It is now clear that muscle macro-architecture reflects only poorly the amount of actively contracting proteins. Consistently, studies have found that muscle mass is only a poor cross-sectional and longitudinal correlate of physical function [14, 23, 27].

Sarcopenic obesity

In spite of the limitation discussed above, most of the literature focuses on the obesity/low muscle mass combination (Table 1), appropriately defined as sarcopenic obesity.

Table 1

Comparison of different sarcopenic obesity definitions and prevalences

Definition of sarcopenic obesityNMean age (SD)Prevalence*
New Mexico Aging Process Study [1]
  • -
    Sarcopenia: skeletal muscle mass -2 SD below mean of young population or < 7.26 kg/m2 in men and < 5.45 kg/m2 in women.
  • -
    Obesity: percentage body fat greater than median or > 27% in men and 38% in women.
83160 and overM: 4.4%
F: 3.0%
NHANES III [28]
  • -
    Sarcopenia: two lower quintiles of muscle mass (<9.12 kg/m2 in men and <6.53 kg/m2 in women)
  • -
    Obesity: two highest quintiles of fat mass (>37.16% in men and > 40.01% in women).
M: 1391
F: 1591		M: 76.3 (1.7†)
F: 77.3 (2.2†)		M: 9.6%
F: 7.4%
[31]
  • -
    Sarcopenia: two lower quintiles of muscle mass (<5.7 kg/m2)
  • -
    Obesity: two highest quintiles of fat mass (>42.9%)
F: 16771.7 (2.4)F: 12.4%
*Age and gender adjusted prevalence.
†Standard error

Like sarcopenia, sarcopenic obesity was first defined by Baumgartner [1] as a muscle mass index less than 2 SD below the sex-specific reference for a young, healthy population. In 2002, Davison et al. [28] defined sarcopenic obesity using anthropometrics and bioelectrical impedance. Definitions based on strength are more recent and present intrinsic challenges. The usual normalization of strength by body size or by fat mass conceals part of the discrepancy between the “engine” and the “mass to be moved” which is the “raison d’être” for discussing sarcopenic obesity. Thus, operational definitions based on crude rather than “normalized” strength have been proposed (Stenholm et al. unpublished data) [29**, 30*]. Although there are no generally accepted criteria for low muscle strength, measuring strength is easier and cheaper than measuring muscle mass. The use of more sophisticated methods such as DXA or computed tomography should also be kept as an option in more thorough clinical examination and especially in establishing the effectiveness of interventions.

In studies using muscle mass as an indicator of sarcopenia, sarcopenic obesity prevalence ranges from 4 to 12 percent [1, 28, 31] (Table 1.). Based on BMI and hand grip strength measurements in four epidemiological studies, sarcopenic obesity can be roughly estimated between 4 to 9 percent (Table 2.).

Table 2

Prevalence of obesity and impaired muscle strength and odds-ratios for obesity associated with impaired muscle strength in four epidemiological studies of persons aged 65 years and older†.

Impaired strengthNot impaired muscle strengthImpaired vs. not impaired strength
Mean age (SD)ObeseNot obeseObeseNot obeseOR (95 % CI) *
BLSA (N = 1026)75.8 (7.1)
N (%)45 (4.4)296 (28.9)114 (11.1)571 (55.7)1.95 (1.01-3.79)
Age-adjusted prevalence (%)
male / female		M: 3.5
F: 6.6		M: 30.5
F: 28.2		M: 15.2
F: 9.4		M: 47.7
F: 59.0
Health 2000 Survey (N = 1413)76.4 (7.6)
N (%)129 (9.1)335 (23.7)267 (18.9)682 (48.3)2.62 (1.69-4.06)
Age-adjusted prevalence (%)
male / female		M: 6.1
F: 11.0		M: 29.6
F: 20.0		M: 15.3
F: 21.2		M: 49.0
F: 47.8
InCHIANTI (N = 856)74.3 (6.9)
N (%)74 (8.6)218 (25.5)139 (16.2)425 (49.7)1.96 (1.17-3.30)
Age-adjusted prevalence (%)
male / female		M: 6.3
F: 8.7		M: 30.5
F: 21.6		M: 13.6
F: 18.3		M: 50.6
F: 48.9
LASA (N = 1189)75.8 (7.2)
N (%)85 (7.2)281 (23.6)219 (18.4)604 (50.8)1.20 (0.74-1.95)
Age-adjusted prevalence (%)
male / female		M: 5.1
F: 8.9		M: 26.2
F: 21.4		M: 11.3
F: 24.4		M: 57.4
F: 45.2
*Adjusted for age, gender, body weight.
†Details of the studies:

BLSA (Baltimore Longitudinal Study on Aging), USA (1959-2007) [104]:

Impaired strength: lower gender-specific tertile of hand grip strength (<33 kg in men and <20 kg in women); Obese: BMI ≥ 30 kg/m2

Health 2000 Survey, Finland (2000-01) [105]:

Impaired strength: lower gender-specific tertile of hand grip strength (<322 N in men and <176 N in women); Obese: BMI ≥ 30 kg/m2

InCHIANTI, Italy (1998-2000) [106]:

Impaired strength: lower gender-specific tertile of hand grip strength (<32 kg in men and <18 kg in women); Obese: BMI ≥ 30 kg/m2

LASA (Longitudinal Aging Study Amsterdam), Netherlands (2001-02) [107, 108]:

Impaired strength: lower gender-specific tertile of hand grip strength (< 33 kg in men and < 20 kg in women); Obese: BMI ≥ 30 kg/m2

Pathways to the obesity/muscle impairment syndrome

Age-related changes in body composition

Longitudinal studies have shown that fat mass increases with age and is higher among later birth cohorts peaking at about age 60-75 years [32-34], whereas muscle mass and strength starts to decline progressively around the age of 30 years with a more accelerated loss after the age of 60 [35-37]. Visceral fat and intramuscular fat tend to increase, while subcutaneous fat in other regions of the body declines [38-41]. Furthermore, fat infiltration into muscle is associated with lower muscle strength and leg performance capacity [20, 42*].

The increase in body weight and fatness are probably due to progressive decline in total energy expenditure stemming from decreased physical activity and reduced basal metabolic rate [43] in the presence of increased or stable caloric intake exceeding basal and activity-related needs. Aging is also associated with a decline in a variety of neural, hormonal and environmental trophic signals to muscle. Physical inactivity, hormonal changes, pro-inflammatory state, malnutrition, loss of alpha-motor units in the central nervous system, and altered gene expression accelerate the loss of muscle mass and mass-specific strength [7, 44-46].

Given the age-related changes in body composition, obesity and low muscle mass (or low muscle strength) may coexist in same person simply by chance. However, there is some evidence for a causal link between obesity and low strength.

Physical activity

Sedentary life-style is an important risk factor for weight gain [47]. Obese persons also tend to be less physically active and this may contribute to decreased muscle strength [48]. Finally, muscle atrophy leads to reduction in metabolic rate both at rest and during physical activity and may further aggravate the sedentary state, all of which can cause weight gain. Two recent studies have shown that weight loss intervention combining diet and exercise among older obese people improves muscle strength and muscle quality in addition to fat loss confirming the hypothesis about tight connection between adiposity and impaired muscle function [49, 50*].

Inflammation

It is now evident that adipose tissue is an active metabolic tissue that secretes hormones and proteins. For example, in adipose tissue, either adipocytes directly or infiltrating macrophages produces pro-inflammatory cytokines, such as interleukin(IL)-6 and tumor necrosis factor(TNF)-α [51] and adipokines, such as leptin and adiponectin, that up-regulate the inflammatory response [51, 52*, 53], which, again, may contribute to muscle mass and strength decline [54-58]. Cesari et al. [55*] reported that pro-inflammatory cytokines were positively associated with fat mass and negatively with muscle mass. In the InCHIANTI study, Schrager et al. [29] found that obese community-dwelling older persons with low muscle strength had elevated levels of CRP and IL-6 compared to those with normal strength. Thus, a pro-inflammatory state may be one of the key factors in creating a vicious cycle of decreased muscle strength among obese persons.

Insulin resistance

Studies in animals and humans have found that inflammatory molecules mediate obesity-related insulin resistance through a cross-talk between cytokine receptors and insulin receptor signaling pathways [59, 60]. It has been hypothesized that muscle fat infiltration causes insulin resistance in obese individuals [61, 62] and this hypothesis has been partially confirmed in humans [63-65].

Since insulin is a powerful anabolic signal on proteins [66, 67], insulin resistance in obese individuals may promote muscle catabolism. Studies have shown that insulin resistance is an independent correlate of poor muscle strength [68-70] and older diabetic patients show accelerated loss of leg muscle strength and quality [71*]. Furthermore, resistance training improves insulin sensitivity and glycemic control [61, 72].

Growth hormone and testosterone

Increased adiposity is often associated with high circulating free fatty acids [73, 74], which inhibit growth hormone production and decrease plasma insulin-like growth factor I (IGF-I) [75, 76]. Recent study showed that sarcopenic obese persons had depressed growth hormone secretion compared to obese persons [77]. Similarly, obese individuals tend to have lower testosterone [78]. Noteworthy, low levels of these anabolic hormones have been reported positively associated with low muscle strength [7, 79-81] and may therefore contribute to muscle impairment in obese individuals [82].

Malnutrition and weight loss

Weight gain results from the misbalance between energy intake and expenditure. Older persons tend to obtain too little proteins in their diet [83] which may impair protein muscle turnover, especially during periods of weight loss [84-86] which is often coincident with accelerated sarcopenia.

Association between obesity and muscle impairment

Clearly, our discussion on the possible origins of sarcopenic obesity is in no way exhaustive and several other mechanisms could be hypothesized. Based on the research summarized above, it is reasonable to hypothesize that low muscle strength and obesity may be pathophysiologically connected which makes them more likely to be associated than expected by chance alone.

We examined the hypothesis that obesity (BMI ≥ 30 kg/m2) and low muscle strength (lowest sex-specific hand grip strength tertile) are connected in four epidemiological studies that included persons aged 65 years and older. The reason why we choose muscle strength and not muscle mass in this analysis has been addressed above. Consistently across the four studies, participants with poor muscle strength were approximately two times more likely to be obese compared to those with normal strength when adjusted for age, gender and body weight (Table 2.). It is also evident that obesity and poor strength are not necessarily coexistent and can occur in isolation.

Consequences of obesity/muscle impairment syndrome

Obesity is a strong risk factor for poor health, reduced functional capacity and quality of life in older persons [5, 87, 88*, 89]. Analogously, low muscle strength has proven to be strong predictor of functional capacity, institutionalization and mortality [23, 90]. Initial evidence indicates that when obesity and muscle impairment co-exist they act synergistically on the risk of developing multiple health related outcomes [91**, 92]. Noteworthy, most of what we know currently is based on a definition of sarcopenic obesity that uses low muscle mass as a criterion.

It is intuitive that individuals with disproportionally poor muscle strength compared to their large body are more at risk of being disabled and of developing disability in the future. Ongoing studies within Baltimore Longitudinal Study on Aging are exploring the effect of obesity and poor muscle strength on the biomechanics and energetic expenditure of gait. Given the same task (workload) the energy expenditure, oxygen consumption and muscle force required for an obese person are higher than those required by a normal weight persons, potentially limiting their physical performance [93, 94].

Few studies have examined the combined effect of obesity and muscle mass or strength in older persons on physical functioning or disability. Studies based on muscle mass and obesity provides conflicting data. In the New Mexico Elder Health Survey sarcopenic obese participants were more likely to be disabled than participants who were just obese or sarcopenic [1]. In the 8-year follow-up of the New Mexico Aging Process Study, Baumgartner et al. [95] demonstrated that older participants with sarcopenic obesity at baseline had over 2-fold higher risk of developing IADL disability than those who were not sarcopenic obese at baseline. However, two other cross-sectional studies based on NHANES III [28] and a sample of older women in Verona [31] did not find an association between sarcopenic obesity and poor physical functioning. In fact, they only observed an association between obesity and functional decline, not with low muscle mass. In their studies Davison et al. and Zoico et al. both used same categorization to define sarcopenic obesity based on the estimated fat and muscle mass quintiles. The use of muscle mass, rather than a functional measure such as strength, as an indicator of sarcopenia may possibly explain why they did not find association with physical functioning, although the Baumgartner definition was based on muscle mass and obesity.

There are only few studies about the combined effect of obesity and muscle impairment where muscle impairment was defined by poor muscle strength. In the cross-sectional Finnish Health 2000 Survey persons with combination of increased fat percentage and decreased muscle strength had higher prevalence of walking limitation compared to those with only high fat percentage or low muscle strength [30]. In the InCHIANTI study we showed recently that older persons with high BMI and low strength experience a steeper decline in walking speed and have higher probability of mobility disability than those with either poor muscle strength or obesity alone (Stenholm et al. unpublished data).

The mortality risk associated with obesity coupled with poor strength was studies by Rantanen et al. [90] who examined hand grip strength and body mass index as predictors of 30-year all-cause mortality in initially healthy men. These authors found that overweight persons in the lowest grip strength tertile had 1.39 times higher mortality risk compared to normal weight persons in the highest grip strength tertile. Increased mortality related to sarcopenic obesity is an important finding and sheds light over the dilemma related to body composition and mortality. Previous studies have shown that muscle strength is a strong predictor of mortality [24, 90, 96, 97], whereas the relationship between obesity and mortality remains controversial [98, 99*, 100]. In old age, obesity may protect against mortality, but if combined with low muscle strength, the risk of mortality may exceed the protective effect. Future studies should examine this topic with large samples including also oldest old people and sample sizes that allow analyzing cause-specific mortality.

Many open questions remain on the genesis and the consequences of the obesity/muscle impairment syndrome in older persons that should be addressed in future research. For example, it will be important to examine gender differences in the development and consequences of this condition. Women are known to have more fat mass as well as lower absolute and relative muscle strength than men [42, 101], and may therefore be more prone to develop obesity and poor strength. Based on our descriptive analysis in four different data sets, the association seems to be more common in women than in men. This is in line with recent obesity-studies showing that the consequences of obesity may be more severe in women than in men [89, 102, 103]. In obese women even small decline in muscle strength may cause difficulties in bearing their excess weight and in moving efficiently.

We have excluded from this review the potential association between sarcopenic obesity and specific obesity-related illnesses, because Dominguez et al. [91] have reviewed the cardiometabolic consequences of sarcopenic obesity, especially in reference to diabetes and cardiovascular diseases. Future studies are needed to understand the effect of disproportionate amount of fat and muscle strength, on cardiovascular, metabolic and musculoskeletal diseases.

In this review we have tried to avoid as much as possible the use of the term “sarcopenic obesity” to describe the combination of obesity and low muscle strength. However, some misuse of this term is almost unavoidable and reflects the true confusion in the literature. A central issue in future discussion about the obesity/muscle impairment geriatric syndrome is a search for new, more comprehensive terminology that takes into account the findings of research conducted in the last decade.

Conclusions

The imbalance between obesity and muscle impairment, either defined by low muscle mass or poor muscle strength is associated with important, negative health outcomes in older individuals. Recent epidemiological studies suggest that this syndrome is related to accelerated functional decline and high risk of diseases and mortality and, therefore, the identification of affected older patients should be an essential goal for clinicians. Expanding our understanding of the complex etiology of the obesity/muscle impairment syndrome and identifying therapeutic targets may offer a tremendous opportunity to limit the expansion of disability that the joined effects of the demographic transformation and the ongoing obesity epidemic will certainly determine. More collaboration between researchers in different fields is needed to fulfill these goals.

Acknowledgements

This research was partly supported by the Intramural Research Program, National Institute on Aging, NIH. The Baltimore Longitudinal Study of Aging was supported by the Intramural Research Program of the NIH, National Institute on Aging. The InCHIANTI Study was supported as a “targeted project” (ICS 110.1/RS97.71) by the Italian Ministry of Health, and in part by the U.S. National Institute on Aging (Contracts N01-AG-916413 and N01-AG-821336), and by the Intramural Research Program of the NIH, National Institute on Aging (Contracts 263 MD 9164 13 and 263 MD 821336). The Longitudinal Aging Study Amsterdam is financially supported by the Dutch Ministry of Public Health, Welfare and Sports. This work was also supported by grant from the Finnish Academy (no. 125494). None of the sponsoring institutions interfered with the collection, analysis, presentation, or interpretation of the data reported here. Authors have no conflicts of interest.

References and recommended reading

Papers of particular interest, published within the annual period of review, have been highlighted as:

* of special interest

** of outstanding interest

1. Baumgartner RN. Body composition in healthy aging. Ann N Y Acad Sci. 2000;904:437–448. [PubMed] [Google Scholar]
2** Zamboni M, Mazzali G, Fantin F, et al. Sarcopenic obesity: a new category of obesity in the elderly. Nutr Metab Cardiovasc Dis. 2008;18:388–395. [PubMed] [Google Scholar]
Review article where authors discuss about definition, pathogenesis, clinical implications and treatment of sarcopenic obesity.
3. Russo CR, Ricca M, Ferrucci L. True osteoporosis and frailty-related osteopenia: two different clinical entities. J Am Geriatr Soc. 2000;48:1738–1739. [PubMed] [Google Scholar]
4. Maggi S, Lauretani F, Ferrucci L, et al. The quality of bone: a “magic natural alloy” Aging Clin Exp Res. 2004;16(Suppl):3–9. [PubMed] [Google Scholar]
5. WHO . Obesity: Preventing and managing the global epidemic. Report of a WHO Consultation. WHO Technical Report Series 894; Geneva, Switzerland: 2000. [PubMed] [Google Scholar]
6. Rosenberg IH. Sarcopenia: origins and clinical relevance. J Nutr. 1997;127:990S–991S. [PubMed] [Google Scholar]
7. Marcell TJ. Sarcopenia: causes, consequences, and preventions. J Gerontol A Biol Sci Med Sci. 2003;58:M911–916. [PubMed] [Google Scholar]
8. Thomas DR. Loss of skeletal muscle mass in aging: examining the relationship of starvation, sarcopenia and cachexia. Clin Nutr. 2007;26:389–399. [PubMed] [Google Scholar]
9. Rosenberg I. Epidemiologic and methodologic problems in determining nutritional status of older persons. Am J Clin Nutr. 1989;50:1131–1133. [PubMed] [Google Scholar]
10. Doherty TJ, Vandervoort AA, Brown WF. Effects of ageing on the motor unit: a brief review. Can J Appl Physiol. 1993;18:331–358. [PubMed] [Google Scholar]
11. Campbell MJ, McComas AJ, Petito F. Physiological changes in ageing muscles. J Neurol Neurosurg Psychiatry. 1973;36:174–182. [PMC free article] [PubMed] [Google Scholar]
12. Baumgartner R, Koehler K, Gallagher D, et al. Epidemiology of sarcopenia among the elderly in New Mexico. Am J Epidemiol. 1998;147:755–763. [PubMed] [Google Scholar]
13. Newman AB, Kupelian V, Visser M, et al. Sarcopenia: alternative definitions and associations with lower extremity function. J Am Geriatr Soc. 2003;51:1602–1609. [PubMed] [Google Scholar]
14. Lauretani F, Russo C, Bandinelli S, et al. Age-associated changes in skeletal muscles and their effect on mobility: an operational diagnosis of sarcopenia. J Appl Physiol. 2003;95:1851–1860. [PubMed] [Google Scholar]
15* 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;61A:M1059–M1064. [PubMed] [Google Scholar]
Based on the Health ABC study, this study provides further evidence that the loss of muscle strength is much more rapid than the concomitant loss of muscle mass, suggesting a significant decline in the quality of muscle.
16. Hughes VA, Frontera WR, Wood M, et al. Longitudinal muscle strength changes in older adults: influence of muscle mass, physical activity, and health. J Gerontol A Biol Sci Med Sci. 2001;56:B209–B217. [PubMed] [Google Scholar]
17. Lexell J, Taylor CC, Sjöström M. What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15-to 83-year-old men. J Neurol Sci. 1988;84:275–294. [PubMed] [Google Scholar]
18. Larsson L, Li X, Frontera WR. Effects of aging on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol. 1997;272:C638–649. [PubMed] [Google Scholar]
19. Sipilä S, Suominen H. Knee extension strength and walking speed in relation to quadriceps muscle composition and training in elderly women. Clin Physiol. 1994;14:433–442. [PubMed] [Google Scholar]
20. Goodpaster BH, Carlson CL, Visser M, et al. Attenuation of skeletal muscle and strength in the elderly: The Health ABC Study. J Appl Physiol. 2001;90:2157–2165. [PubMed] [Google Scholar]
21. Delbono O. Neural control of aging skeletal muscle. Aging Cell. 2003;2:21–29. [PubMed] [Google Scholar]
22. Visser M, Newman AB, Nevitt MC, et al.Health, Aging, and Body Composition Study Research Group Reexamining the sarcopenia hypothesis. Muscle mass versus muscle strength. Ann N Y Acad Sci. 2000;904:456–461. [PubMed] [Google Scholar]
23. Visser M, Goodpaster BH, Kritchevsky SB, et al. Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci. 2005;60:M324–M333. [PubMed] [Google Scholar]
24. Newman AB, Kupelian V, Visser M, et al. Strength, but not muscle mass, is associated with mortality in the health, aging and body composition study cohort. J Gerontol A Biol Sci Med Sci. 2006;61A:M72–M77. [PubMed] [Google Scholar]
25. NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy Osteoporosis Prevention, Diagnosis, and Therapy. JAMA. 2001;285:785–795. [Google Scholar]
26. Dennison E, Cole Z, Cooper C. Diagnosis and epidemiology of osteoporosis. Curr Opin Rheumatol. 2005;17:456–461. [PubMed] [Google Scholar]
27. Visser M, Deeg DJ, Lips P, et al. Skeletal muscle mass and muscle strength in relation to lower-extremity performance in older men and women. J Am Geriatr Soc. 2000;48:381–386. [PubMed] [Google Scholar]
28. Davison KK, Ford E, Cogswell M, Dietz W. Percentage of body fat and body mass index are associated with mobility limitations in people aged 70 and older from NHANES III. J Am Geriatr Soc. 2002;50:1802–1809. [PubMed] [Google Scholar]
29** Schrager MA, Metter EJ, Simonsick E, et al. Sarcopenic obesity and inflammation in the InCHIANTI study. J Appl Physiol. 2007;102:919–925. [PMC free article] [PubMed] [Google Scholar]
Using cross-sectional data from InCHIANTI this study found that obesity directly affects inflammation which in turn negatively affects muscle strength. This finding suggests that the role of inflammation may be important to the development and progression of sarcopenic obesity.
30* Stenholm S, Rantanen T, Heliövaara M, Koskinen S. The mediating role of C-reactive protein and handgrip strength between obesity and walking limitation. J Am Geriatr Soc. 2008;56:462–469. [PubMed] [Google Scholar]
Based on the representative sample of older adults in Finland, this study found that combination of high fat percentage and low hand grip strength is associated with increased level of CRP as well as with walking limitation.
31. Zoico E, Di Francesco V, Guralnik JM, et al. Physical disability and muscular strength in relation to obesity and different body composition indexes in a sample of healthy elderly women. Int J Obes Relat Metab Disord. 2004;28:234–241. [PubMed] [Google Scholar]
32. Rissanen A, Heliövaara M, Aromaa A. Overweight and anthropometric changes in adulthood: a prospective study of 17,000 Finns. Int J Obes. 1988;12:391–401. [PubMed] [Google Scholar]
33. Droyvold WB, Nilsen TI, Kruger O, et al. Change in height, weight and body mass index: Longitudinal data from the HUNT Study in Norway. Int J Obes. 2006;30:935–939. [PubMed] [Google Scholar]
34. Ding J, Kritchevsky SB, Newman AB, et al. Effects of birth cohort and age on body composition in a sample of community-based elderly. Am J Clin Nutr. 2007;85:405–410. [PubMed] [Google Scholar]
35. Rantanen T, Masaki KT, Foley D, et al. Grip strength changes over 27 yr in Japanese-American men. J Appl Physiol. 1998;85:2047–2053. [PubMed] [Google Scholar]
36. Bassey EJ. Longitudinal changes in selected physical capabilities: muscle strength, flexibility and body size. Age Ageing. 1998;27:12–16. [PubMed] [Google Scholar]
37. Frontera WR, Hughes VA, Fielding RA, et al. Aging of skeletal muscle: a 12-yr longitudinal study. J Appl Physiol. 2000;88:1321–1326. [PubMed] [Google Scholar]
38. Beaufrere B, Morio B. Fat and protein redistribution with aging: metabolic considerations. Eur J Clin Nutr. 2000;54(Suppl 3):S48–53. [PubMed] [Google Scholar]
39. Enzi G, Gasparo M, Biondetti PR, et al. Subcutaneous and visceral fat distribution according to sex, age, and overweight, evaluated by computed tomography. Am J Clin Nutr. 1986;44:739–746. [PubMed] [Google Scholar]
40. Zamboni M, Armellini F, Harris T, et al. Effects of age on body fat distribution and cardiovascular risk factors in women. Am J Clin Nutr. 1997;66:111–115. [PubMed] [Google Scholar]
41. Horber FF, Gruber B, Thomi F, et al. Effect of sex and age on bone mass, body composition and fuel metabolism in humans. Nutrition. 1997;13:524–534. [PubMed] [Google Scholar]
42* Visser M, Kritchevsky SB, Goodpaster BH, et al. Leg Muscle Mass and Composition in Relation to Lower Extremity Performance in Men and Women Aged 70 to 79: The Health, Aging and Body Composition Study. J Am Geriatr Soc. 2002;50:897–904. [PubMed] [Google Scholar]
Muscle strength seems a more important determinant of incident mobility limitations than muscle mass in a large sample of well-functioning older men and women.
43. Elia M, Ritz P, Stubbs RJ. Total energy expenditure in the elderly. Eur J Clin Nutr. 2000;54:S92–S103. [PubMed] [Google Scholar]
44. Morley JE, Baumgartner RN, Roubenoff R, et al. Sarcopenia. J Lab Clin Med. 2001;137:231–243. [PubMed] [Google Scholar]
45. Doherty T. Aging and sarcopenia. J Appl Physiol. 2003;95:1717–1727. [PubMed] [Google Scholar]
46. Roubenoff R. Sarcopenia: Effects on Body Composition and Function. J Gerontol A Biol Sci Med Sci. 2003;58A:M1012–M1017. [PubMed] [Google Scholar]
47. LaMonte MJ, Blair SN. Physical activity, cardiorespiratory fitness, and adiposity: contributions to disease risk. Curr Opin Clin Nutr Metab Care. 2006;9:540–546. [PubMed] [Google Scholar]
48. Duvigneaud N, Matton L, Wijndaele K, et al. Relationship of obesity with physical activity, aerobic fitness and muscle strength in Flemish adults. J Sports Med Phys Fitness. 2008;48:201–210. [PubMed] [Google Scholar]
49. Wang X, Miller GD, Messier SP, Nicklas BJ. Knee strength maintained despite loss of lean body mass during weight loss in older obese adults with knee osteoarthritis. J Gerontol A Biol Sci Med Sci. 2007;62:866–871. [PubMed] [Google Scholar]
50* Frimel TN, Sinacore DR, Villareal DT. Exercise attenuates the weight-loss-induced reduction in muscle mass in frail obese older adults. Med Sci Sports Exerc. 2008;40:1213–1219. [PMC free article] [PubMed] [Google Scholar]
This randomized trial examined the effect of combined diet and exercise intervention on body composition and muscle strength among obese older people. During 6 months intervention persons in the diet + exercise group lost fat mass but increased muscle strength indicating a tight connection between adiposity and muscle impairment.
51. Fantuzzi G. Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol. 2005;115:911–919. quiz 920. [PubMed] [Google Scholar]
52* Fontana L, Eagon JC, Trujillo ME, et al. Visceral fat adipokine secretion is associated with systemic inflammation in obese humans. Diabetes. 2007;56:1010–1013. [PubMed] [Google Scholar]
This is among the first studies to examine the adipokine production by visceral fat in obese subjects. By examining blood samples from the portal vein and radial artery during open gastric bypass surgery they were able to show that plasma IL-6 concentrations were much higher in portal vein than in peripheral artery blood in obese subjects, demonstrating that visceral fat is an important source of IL-6 production in obese people
53. Hung J, McQuillan BM, Thompson PL, Beilby JP. Circulating adiponectin levels associate with inflammatory markers, insulin resistance and metabolic syndrome independent of obesity. Int J Obes. 2008;32:772–779. [PubMed] [Google Scholar]
54. Visser M, Pahor M, Taaffe DR, et al. Relationship of interleukin-6 and tumor necrosis factor-α with muscle mass and muscle strength in elderly men and women: The Health ABC Study. J Gerontol A Biol Sci Med Sci. 2002;57A:M326–M332. [PubMed] [Google Scholar]
55* Cesari M, Kritchevsky SB, Baumgartner RN, et al. Sarcopenia, obesity, and inflammation - results from the Trial of Angiotensin Converting Enzyme Inhibition and Novel Cardiovascular Risk Factors study. Am J Clin Nutr. 2005;82:428–434. [PubMed] [Google Scholar]
This is the first study to examine simultaneously obesity, sarcopenia and inflammatory factors. Cross-sectional study with 286 older men and women shows that C-reactive protein and IL-6 were positively associated with fat mass, but negatively related to lean mass. The results suggest that obesity-related inflammation may lead to sarcopenia and sarcopenic obesity.
56. Schaap LA, Pluijm SM, Deeg DJ, Visser M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med. 2006;119:526.e529–526.e517. [PubMed] [Google Scholar]
57. Barbieri M, Ferrucci L, Ragno E, et al. Chronic inflammation and the effect of IGF-I on muscle strength and power in older persons. Am J Physiol Endocrinol Metab. 2003;284:E481–487. [PubMed] [Google Scholar]
58. Roth SM, Metter EJ, Ling S, Ferrucci L. Inflammatory factors in age-related muscle wasting. Curr Opin Rheumatol. 2006;18:625–630. [PubMed] [Google Scholar]
59. Bastard JP, Maachi M, Lagathu C, et al. Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw. 2006;17:4–12. [PubMed] [Google Scholar]
60. Dyck DJ, Heigenhauser GJ, Bruce CR. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol (Oxf) 2006;186:5–16. [PubMed] [Google Scholar]
61. Goodpaster BH, Brown NF. Skeletal muscle lipid and its association with insulin resistance: what is the role for exercise? Exerc Sport Sci Rev. 2005;33:150–154. [PubMed] [Google Scholar]
62. Kelley DE, Slasky BS, Janosky J. Skeletal muscle density: effects of obesity and non-insulin-dependent diabetes mellitus. Am J Clin Nutr. 1991;54:509–515. [PubMed] [Google Scholar]
63. Goodpaster BH, Krishnaswami S, Resnick H, et al. Association between regional adipose tissue distribution and both type 2 diabetes and impaired glucose tolerance in elderly men and women. Diabetes Care. 2003;26:372–379. [PubMed] [Google Scholar]
64. Goodpaster BH, Thaete FL, Kelley DE. Thigh adipose tissue distribution is associated with insulin resistance in obesity and in type 2 diabetes mellitus. Am J Clin Nutr. 2000;71:885–892. [PubMed] [Google Scholar]
65. van Loon LJ, Goodpaster BH. Increased intramuscular lipid storage in the insulin-resistant and endurance-trained state. Pflugers Arch. 2006;451:606–616. [PubMed] [Google Scholar]
66. Biolo G, Declan Fleming RY, Wolfe RR. Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest. 1995;95:811–819. [PMC free article] [PubMed] [Google Scholar]
67. Fujita S, Rasmussen BB, Cadenas JG, et al. Effect of insulin on human skeletal muscle protein synthesis is modulated by insulin-induced changes in muscle blood flow and amino acid availability. Am J Physiol Endocrinol Metab. 2006;291:E745–754. [PMC free article] [PubMed] [Google Scholar]
68. Nomura T, Ikeda Y, Nakao S, et al. Muscle strength is a marker of insulin resistance in patients with type 2 diabetes: a pilot study. Endocr J. 2007;54:791–796. [PubMed] [Google Scholar]
69. Abbatecola AM, Ferrucci L, Ceda G, et al. Insulin resistance and muscle strength in older persons. J Gerontol A Biol Sci Med Sci. 2005;60A:1278–1282. [PubMed] [Google Scholar]
70. Guillet C, Boirie Y. Insulin resistance: a contributing factor to age-related muscle mass loss? Diabetes Metab. 2005;31(Spec No 2):5S20–25S26. [PubMed] [Google Scholar]
71* Park SW, Goodpaster BH, Strotmeyer ES, et al. Accelerated loss of skeletal muscle strength in older adults with type 2 diabetes: The Health, Aging, and Body Composition Study. Diabetes Care. 2007;30:1507–1512. [PubMed] [Google Scholar]
Based on 3 year follow-up of the Health ABC study, this is the first longitudinal study to show that type 2 diabetes is associated with accelerated loss of muscle strength and mass in older adults.
72. Eves ND, Plotnikoff RC. Resistance training and type 2 diabetes: Considerations for implementation at the population level. Diabetes Care. 2006;29:1933–1941. [PubMed] [Google Scholar]
73. Campbell PJ, Carlson MG, Nurjhan N. Fat metabolism in human obesity. Am J Physiol. 1994;266:E600–605. [PubMed] [Google Scholar]
74. Petersen KF, Befroy D, Dufour S, et al. Mitochondrial dysfunction in the elderly: possible role in insulin resistance. Science. 2003;300:1140–1142. [PMC free article] [PubMed] [Google Scholar]
75. Van Dam PS, Smid HE, de Vries WR, et al. Reduction of free fatty acids by acipimox enhances the growth hormone (GH) responses to GH-releasing peptide 2 in elderly men. J Clin Endocrinol Metab. 2000;85:4706–4711. [PubMed] [Google Scholar]
76. Weltman A, Weltman JY, Veldhuis JD, Hartman ML. Body composition, physical exercise, growth hormone and obesity. Eat Weight Disord. 2001;6:28–37. [PubMed] [Google Scholar]
77. Waters DL, Qualls CR, Dorin RI, et al. Altered growth hormone, cortisol, and leptin secretion in healthy elderly persons with sarcopenia and mixed body composition phenotypes. J Gerontol A Biol Sci Med Sci. 2008;63:536–541. [PubMed] [Google Scholar]
78. Allan CA, Strauss BJ, McLachlan RI. Body composition, metabolic syndrome and testosterone in ageing men. Int J Impot Res. 2007;19:448–457. [PubMed] [Google Scholar]
79. Ceda GP, Dall’Aglio E, Maggio M, et al. Clinical implications of the reduced activity of the GH-IGF-I axis in older men. J Endocrinol Invest. 2005;28:96–100. [PubMed] [Google Scholar]
80. Schaap LA, Pluijm SM, Smit JH, et al. The association of sex hormone levels with poor mobility, low muscle strength and incidence of falls among older men and women. Clin Endocrinol. 2005;63:152–160. [PubMed] [Google Scholar]
81. Cappola AR, Bandeen-Roche K, Wand GS, et al. Association of IGF-I levels with muscle strength and mobility in older women. J Clin Endocrinol Metab. 2001;86:4139–4146. [PubMed] [Google Scholar]
82. Chu L-W, Tam S, Kung AWC, et al. Serum Total and Bioavailable Testosterone Levels, Central Obesity, and Muscle Strength Changes with Aging in Healthy Chinese Men. J Am Geriatr Soc. 2008 in press. DOI: 10.1111/j.1532-5415.2008.01746.x. [PubMed] [Google Scholar]
83. Morley JE. Anorexia of aging: physiologic and pathologic. Am J Clin Nutr. 1997;66:760–773. [PubMed] [Google Scholar]
84. Dreyer HC, Volpi E. Role of protein and amino acids in the pathophysiology and treatment of sarcopenia. J Am Coll Nutr. 2005;24:140S–145S. [PMC free article] [PubMed] [Google Scholar]
85. Campbell WW, Leidy HJ. Dietary protein and resistance training effects on muscle and body composition in older persons. J Am Coll Nutr. 2007;26:696S–703S. [PubMed] [Google Scholar]
86. Houston DK, Nicklas BJ, Ding J, et al. Dietary protein intake is associated with lean mass change in older, community-dwelling adults: the Health, Aging, and Body Composition (Health ABC) Study. Am J Clin Nutr. 2008;87:150–155. [PubMed] [Google Scholar]
87. Houston DK, Stevens J, Cai J. Abdominal fat distribution and functional limitations and disability in a biracial cohort: the Atherosclerosis Risk in Communities Study. Int J Obes. 2005;29:1457–1463. [PubMed] [Google Scholar]
88* Alley DE, Chang VW. The changing relationship of obesity and disability, 1988-2004. JAMA. 2007;298:2020–2027. [PubMed] [Google Scholar]
Using data from NHANES this representative study shows that opposite to the decreased disability prevalence among non-obese, the obesity-associated disability has increased from 1988-1994 to 1999-2004.
89. Stenholm S, Sainio P, Rantanen T, et al. Effect of co-morbidity on the association of high body mass index with walking limitation among men and women aged 55 years and older. Aging Clin Exp Res. 2007;19:277–283. [PubMed] [Google Scholar]
90. Rantanen T, Harris T, Leveille SG, et al. Muscle Strength and Body Mass Index as Long-Term Predictors of Mortality in Initially Healthy Men. J Gerontol A Biol Sci Med Sci. 2000;55A:M168–M173. [PubMed] [Google Scholar]
91** Dominguez LJ, Barbagallo M. The cardiometabolic syndrome and sarcopenic obesity in older persons. J Cardiometab Syndr. 2007;2:183–189. [PubMed] [Google Scholar]
Changes in body composition and fat redistribution with aging are associated with obesity-related cardiometabolic risk factors. This article discusses the role of cardiometabolic syndrome in the development of sarcopenic obesity.
92. Aubertin-Leheudre M, Lord C, Goulet ED, et al. Effect of sarcopenia on cardiovascular disease risk factors in obese postmenopausal women. Obesity (Silver Spring) 2006;14:2277–2283. [PubMed] [Google Scholar]
93. Hulens M, Vansant G, Claessens AL, et al. Predictors of 6-minute walk test results in lean, obese and morbidly obese women. Scand J Med Sci Sports. 2003;13:98–105. [PubMed] [Google Scholar]
94. Hulens M, Vansant G, Lysens R, et al. Exercise capacity in lean versus obese women. Scand J Med Sci Sports. 2001;11:305–309. [PubMed] [Google Scholar]
95. Baumgartner RN, Wayne SJ, Waters DL, et al. Sarcopenic obesity predicts instrumental activities of daily living disability in the elderly. Obes Res. 2004;12:1995–2004. [PubMed] [Google Scholar]
96. Rantanen T, Volpato S, Ferrucci L, et al. Handgrip strength and cause-specific and total mortality in older disabled women: exploring the mechanism. J Am Geriatr Soc. 2003;51:636–641. [PubMed] [Google Scholar]
97. Gale CR, Martyn CN, Cooper C, Sayer AA. Grip strength, body composition, and mortality. Int J Epidemiol. 2007;36:228–235. [PubMed] [Google Scholar]
98. Zamboni M, Mazzali G, Zoico E, et al. Health consequences of obesity in the elderly: a review of four unresolved questions. Int J Obes (Lond) 2005;29:1011–1029. [PubMed] [Google Scholar]
99* Al Snih S, Ottenbacher KJ, Markides KS, et al. The Effect of Obesity on Disability vs Mortality in Older Americans. Arch Intern Med. 2007;167:774–780. [PubMed] [Google Scholar]
Large 7 year follow-up study based on EPESE study confirming earlier findings that obesity is more important risk factor for disability than for mortality.
100. Flegal KM, Graubard BI, Williamson DF, Gail MH. Excess deaths associated with underweight, overweight, and obesity. Jama. 2005;293:1861–1867. [PubMed] [Google Scholar]
101. Lafortuna CL, Maffiuletti NA, Agosti F, Sartorio A. Gender variations of body composition, muscle strength and power output in morbid obesity. Int J Obes. 2005;29:833–841. [PubMed] [Google Scholar]
102. Friedmann JM, Elasy T, Jensen GL. The relationship between body mass index and self-reported functional limitation among older adults: a gender difference. J Am Geriatr Soc. 2001;49:398–403. [PubMed] [Google Scholar]
103. Angleman SB, Harris TB, Melzer D. The role of waist circumference in predicting disability in periretirement age adults. Int J Obes. 2006;30:364–373. [PubMed] [Google Scholar]
104. Shock NW, Greulich R, Andres R, et al. Normal Human Aging: The Baltimore Longitudinal Study of Aging. U.S. Govt. Printing Office; Washington, DC: 1984. (NIH Publication 84-2450). 1984. [Google Scholar]
105. Aromaa A, Koskinen S. Baseline results of the Health 2000 health examination survey. Publications of the National Public Health Institute B12; Helsinki: 2004. Health and functional capacity in Finland. Available also at: http://www.ktl.fi/terveys2000/index.uk.html. [Google Scholar]
106. Ferrucci L, Bandinelli S, Benvenuti E, et al. Subsystems contributing to the decline in ability to walk: bridging the gap between epidemiology and geriatric practice in the InCHIANTI study. J Am Geriatr Soc. 2000;48:1618–1625. [PubMed] [Google Scholar]
107. Sonnenberg CM, Deeg DJ, Comijs HC, et al. Trends in antidepressant use in the older population: Results from the LASA-study over a period of 10 years. J Affect Disord. 2008 in press. DOI:10.1016/j.jad.2008.03.009. [PubMed] [Google Scholar]
108. Deeg DJ, van Tilburg T, Smit JH, de Leeuw ED. Attrition in the Longitudinal Aging Study Amsterdam. The effect of differential inclusion in side studies. J Clin Epidemiol. 2002;55:319–328. [PubMed] [Google Scholar]
-