Special Section: Sarcopenia
An Overview of Sarcopenic Obesity

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Abstract

Sarcopenic obesity (SO) refers to the copresence of sarcopenia and obesity. In this condition, a disproportion exists between the amount of lean mass relative to fat mass. Research on SO is important because the presence of both sarcopenia and obesity may have important health consequences. However, SO research has been hampered by the disparate number of definitions of SO. Various definitions of sarcopenia include ratios of appendicular mass to height2 or body weight, measures of muscle strength, or physical function. More recent definitions incorporate all 3. Obesity is usually defined by high body mass index, but some studies have relied on percent body fat or visceral fat. Depending on the definition, the prevalence of SO ranges from 0% to 41% in older populations. The loss of lean mass and increase in fat mass with advancing age may share common etiologic pathways. Declines in physical activity can lead to poor muscle strength, lower muscle mass, and increased fat infiltration; all of which could lead to increases in fat mass. The increases in fat mass and accompanying increases in adipokines and inflammation may further adversely affect muscle quality. SO has been related to an increased risk of mobility disability, above and beyond sarcopenia, or obesity alone. Additional research is needed to further our understanding of the pathophysiology of SO and its consequences. Interventions aimed at reducing SO may improve physical function as well as reduce disability and death.

Introduction

Current demographic trends in which both the size and proportion of the older population, especially the oldest old, are increasing at unprecedented rates will have a profound public health impact. Coupled with this increase is the epidemic of obesity: of US adults overall, 35% were obese with a body mass index (BMI) ≥30 kg/m2 (1). Unsurprisingly, but of substantial societal importance, there was a significant increase in obesity among women aged 60 and older from 2003–04 to 2011–12: from 31.5% to 38.1%, p = 0.006. The convergence of these 2 trends could have a major impact on disability, morbidity, and mortality among older adults. This is especially important because skeletal muscle mass declines with aging. This decline in muscle mass with aging coupled with an increase in obesity and fat mass could have important consequences among older adults.

Sarcopenic obesity (SO) refers to the copresence of both sarcopenia and obesity (2). A disproportion exists between the amount of lean mass compared with fat mass where the fat mass exceeds the weight that lean mass could support. In short, there is too little muscle relative to size (3). Research into the physiology, epidemiology, and consequences of SO has been and remains hampered by lack of consensus regarding the definition of SO. Obesity is traditionally defined by the BMI. According to the World Health Organization, obesity refers to a BMI of at least 30 kg/m2 and central obesity, as a waist circumference greater than 102 cm in men and 88 cm in women (4). However among older adults, BMI may be overestimated because of height loss. This overestimation is most predominant in women 85 yr and older, leading to an overestimation of 0.9 (standard deviation [SD]: 0.7) kg/m2 (5).

The term sarcopenia comes from the Greek words sarx (meaning flesh) and penia (meaning loss) and was originally thought of as a loss of lean mass that occurs with aging. Current definitions of sarcopenia, however, include not only muscle mass but also measures of weakness and physical function. Various sarcopenia consensus definitions exist as follows.

The Foundation for the National Institutes of Health (FNIH) biomarkers consortium, the FNIH Sarcopenia Project, recently evaluated 9 different large cohorts to evaluate criteria for clinically relevant weakness and low lean mass (6). The pooled sample included 26,625 subjects (57% women); mean age, 75.2 ± 5.9 yr. The pooled samples were race/ethnically diverse, from many different geographic locations, and represented a wide range of physical function. The FNIH Sarcopenia Project developed evidence-based cutpoints for weakness (grip strength <26 kg for men and <16 kg for women) and for low appendicular lean mass (ALM) adjusted for BMI (<0.789 for men and <0.512 for women) 7, 8. Because low muscle mass by itself is not consistently associated with disability and other adverse outcomes, the FNIH Sarcopenia Project recommends that the criteria for low muscle mass should be determined based on weakness and not low muscle mass. Low muscle mass appears to be a problem only if it is accompanied with weakness (6). They also identified a more severe form of sarcopenia that includes poor physical function (gait speed of ≤0.8 m/s), and the aforementioned grip strength, and ALM cutpoints.

Using these criteria for sarcopenia, the FNIH Sarcopenia Project compared the prevalence of sarcopenia with the International Working Group (9) and the European Working Group on Sarcopenia in Older Persons (EWGSOP) definitions (10). The International Working Group considers a gait speed of <1.0 m/s and ALM/ht2; men ≤7.23 kg/m2 and women ≤5.67 kg/m2. The EWGSOP considers gait speed of <0.8 m/s or grip strength of <30 kg in men and <20 kg in women. Severe sarcopenia is present if all 3 criteria are met (11). As shown in Fig. 1, the prevalence of sarcopenia alone varied substantially based on the definition from 0.5% to 5.3% in men and from 1.8% to 13.3% in women. The prevalence of severe sarcopenia using the EWGSOP was low; 0.7% in men and 2.9% in women.

As noted previously, SO is the combined condition meeting sarcopenia requirements in the presence of obesity. Waters and Baumgartner (12) described the body composition phenotype characteristics. As shown in Table 1, sarcopenic individuals have low body weight, low ALM, low BMI with low to normal fat mass, and waist circumference. In contrast, sarcopenia/obese individuals have normal/high weight, high fat mass, low ALM, normal to high BMI, and waist circumference. The original authors did not note that sarcopenic obese subjects may have high body weight or BMI, but this seems a reasonable possibility.

A summary of the prevalence of SO and the different definitions of SO is shown in Table 2. Note that this review was limited to large community cohorts.

As shown in Table 2, obesity was defined by total fat mass, percent body fat, BMI, visceral fat area, or waist circumference. Sarcopenia was defined in many studies using the ALM/height2 or ALM/weight ratios. With such a mass-based approach, a person is considered to be sarcopenic if their ratio is <2 SDs below a reference population. This is similar to the approach used to define osteoporosis: a bone mineral density level <2.5 SDs below the value from a young reference group population. However, the reference database for bone mineral density is the representative National Health and Examination Survey (NHANES) database. For sarcopenia, it is not clear which reference database was used and how generalizable it was. In some cases, simple grip or leg strength measures were used alone as a measure for sarcopenia. For the most part, dual-energy X-ray absorptiometry was used to define ALM although a few older studies used bioelectric impedance analysis. Subjects in these studies were primarily older than 60 yr, and many reported the prevalence combined in men and women. Studies were carried out in various countries, including the United States, Canada, China, Korea, France, and Holland.

Baumgartner (13) was the first to publish the prevalence of sarcopenia and SO in 883 Hispanic and non-Hispanic white men and women living in New Mexico (the New Mexico Elder Health Survey, 1992–1995). In the report, sarcopenia was defined as ALM (kg)/height2 (m2) being less than 2 SDs below the mean of a young reference group. The reference group was 229 non-Hispanic white men and women aged 18–40 recruited in New Mexico. Obesity was defined as a percentage of body fat > sex-specific medians (women, 38% and men, 27%). The prevalence of SO was quite low, 3%–4% but increased with age from about 2% among those aged <70 to 10% among those aged 80 or older.

Using data from the National Health and Nutrition Examination Surveys 1988–1994, 1526 women and 1391 men, aged 70, were studied (14). Percentage of body fat was estimated by a prediction equation that included waist and hip circumference, triceps skinfold, and sex. Muscle mass was also estimated using a prediction equation with height, age, resistance from bioelectrical impedance analysis, and sex. Those with the highest fat mass (top 40%) and lowest muscle mass (<40%) were considered to be SO. The prevalence of SO was 7.4% in women and 9.6% in men.

Newman et al (15) proposed that the definition of sarcopenia must be adjusted for not only height but also fat mass. Indeed, the definition of sarcopenia based on ALM adjusted for height and fat mass showed stronger correlations with lower physical function performance scores than adjusting for height only (24). The Newman studies were carried out in the Health Aging and Body Composition Study, a large cohort study from 2 US communities. Participants were aged 70–79, n = 2984; 52% women and 41% black. The prevalence of SO was 11% in men and 14.4% in women. Separate prevalence rates were not reported for whites and blacks.

A later study from Baumgartner et al (16) using a separate cohort of 451 individuals from New Mexico, mean age 72 yr, used the same definitions of sarcopenia and obesity as their previous study. In this study, the overall prevalence of SO was 5.8%; 61.5% of those with SO were men.

The Invecchaire in Chianti on Aging in the Chianti Area Study is a prospective-based cohort study of 2 small towns in the Tuscany region of Italy (17). In 1998, 1270 persons aged 65 and older were randomly selected from the population. Of these, 378 men and 493 women had complete data for this analysis. Sarcopenia was defined by the lowest sex-specific tertile of grip strength. Obesity was defined either by a waist circumference in the upper sex-specific tertile or by a BMI of ≥30 kg/m2. The mean age at the time of examination was 74 yr. The prevalence of SO differed markedly by obesity indices: using waist circumference, the prevalence was 11% in men and 12% in women; using BMI, the prevalence was 5% and 41% in men and women, respectively. It is unclear why the prevalence of SO was so much larger if BMI was used.

Stenholm et al (3) described the prevalence of SO in 2 cohorts, the Baltimore Longitudinal Study on Aging (N = 1826; mean age: 75.8) and the Longitudinal Aging Study Amsterdam (n = 1189; mean age: 75.8). Sarcopenia was based on lowest sex-specific tertiles for ALM men (<33 kg) and women (<20 kg) and obesity, BMI ≥30 kg/m2. Prevalence in the Baltimore Longitudinal Study on Aging was 3.5% and 6.6% in men and women, respectively, and in Longitudinal Aging Study Amsterdam, 5.1% and 5.9%, respectively.

Data from the Canadian Study, Nutrition as a Determinant of Successful Aging, were reported by Bouchard et al (18). Nutrition as a Determinant of Successful Aging is an observational cohort study of 1793 community-dwelling men and women, aged 68–82 yr. SO was defined using the Baumgartner definition with a prevalence of SO in men (19%) and women (11%).

Rolland et al (19) described results from the French, EPIDemiologie de I’OSteoporose Study, a prospective study of 1308 women aged 75 and older. The Baumgartner definition of sarcopenia was used. Women were considered obese if their percentage body fat was ≥40% body fat. The prevalence of SO was quite low, 2.7%. This may reflect the overall low BMI (range mean: 20–24 kg/m2) in these French women.

Two studies from Korea reported the prevalence of SO. The Korean NHANES Study (2008–09) studied 4486 men and 5999 women, aged 20 and older (20). Women and men aged 20–39 yr formed the reference database. They defined sarcopenia in 2 ways (appendicular skeletal muscle [ASM]/height2 and ASM/weight). Waist circumference was used to define obesity. The overall prevalence of SO differed markedly by the definition of sarcopenia. Using the height-adjusted definition, the prevalence of SO was 0.2% in men and 0% in women. Using the weight-adjusted definition, the prevalence was 7.6% in men and 9.1% in women. The height-adjusted definition may underestimate the prevalence of SO, similar to findings by Newman et al (15). It is also useful to note that the BMI was quite low (22–24 kg/m2) compared with western populations. The prevalence of sarcopenia increased with age: men, 1.6% age 40–49 to 25.6%, aged 80 and older; women, 1.7%, aged 40–49 to 9.4%, aged 80 and older.

Using data from the Korean Longitudinal Study on Health and Aging, the prevalence of SO also differed markedly by whether ASM was adjusted for height or weight (21). Visceral fat was used to define obesity. Adjusting for height, the prevalence was 11%, compared with 41%, adjusting for weight.

Using NHANES data, 1999–2004, Levine and Crimmins (22) reported that the overall prevalence of SO was 10.4% in 2287 subjects, aged 60 and older, 56%, women. Most subjects (81%) were white, but they did not report the prevalence of SO separately by race/ethnicity.

In the Framingham cohort, mean age 78, the prevalence of SO was 8% in men and 4% in women (24). Finally, a smaller study of 101 Chinese men, aged 80 and older, the prevalence of SO was 4.9% (23).

In summary, the prevalence of SO varies markedly by the definition. The range is quite large depending on the population (0%–41%) and definition. Adjusting for height alone in the sarcopenia phenotype may lead to underestimation of the prevalence, and hence the recognition of its impact on function, morbidity, and mortality. Of importance, the prevalence of obesity is much greater than SO. For example, in NHANES, the prevalence of obesity without sarcopenia was 49%, compared with 10% for SO. Consensus definitions for both sarcopenia and SO are clearly needed to advance not only research but also clinical care of people with SO.

A full description of the pathogenesis of SO is beyond the scope of this review. However, multiple interactions between fat and muscle exist; a model indicating interrelationships between adipose tissue and muscle, which may underpin mechanisms leading to SO is reproduced (25) (Fig. 2). Aging is associated with reduced physical activity, which in turn leads to reductions in muscle mass, muscle strength, and even lower physical activity and decreased endurance. Poor muscle quality with increased fat infiltration could further increase inflammation. The decrease in physical activity may lead to weight gain, increased insulin resistance, and increased total abdominal fat with concomitant increases in inflammation. As fat mass increases, secretion of leptin and other adipokines and cytokines could also contribute to the development of SO. This vicious cycle between loss of lean mass and gain in fat mass could lead to increases in sarcopenia and SO.

Roubenoff (26) coined the phrase that SO refers to the “fat frail.” The potential consequences of sarcopenia on physical function may be more severe in obese subjects. Sarcopenia and obesity may act synergistically on metabolic and physical functions imparting greater disability.

Cross-sectional studies have reported an association between SO and physical function. In both NHANES III and NHANES (1999–2004), subjects with SO were more likely to report difficulties with physical function. In the first NHANES report (14), women with both high body fat and low muscle mass were 2-fold more likely and men, 1.65-fold more likely to report functional limitations, but confidence intervals (CIs) were wide and not statistically significant. This may reflect low statistical power because the prevalence of SO was low (Table 2). The more recent NHANES Study (22) showed that the odds ratio of physical function problems in those with SO was 1.91 (95% CI: 1.53–2.38). Further adjusting for both insulin resistance and inflammation attenuated this association slightly suggesting that these factors are in the etiologic pathway. Of importance, however, the association remained statistically significant. Of interest, the association between sarcopenia alone and physical function was weaker, odds ratio = 1.58 (95% CI: 1.15–2.17).

In EPIDemiologie de I’OSteoporose Study (19), those with SO were 2.54 more likely to report any mobility difficulties (95% CI: 1.12–5.75) compared with normal individuals. In contrast, there was no association between sarcopenia and mobility impairment.

In the Framingham Study (24), men with SO were 2.5–3.0 times more likely to report difficulty walking, climbing stairs, or performing heavy work, but there was no association in women. Further understandings of whether sex influences these associations are needed. However, the authors used the ALM/height2 measure of sarcopenia in their SO definition, although stronger associations with mobility limitations were found when sarcopenia was defined using ALM adjusting for weight.

These previous studies were all limited by their cross-sectional design. The cohort study participants from New Mexico were followed for up to 8 yr (16). Subjects with SO were more likely to develop incident disability (hazard ratio: 2.63 (95% CI: 1.19–5.85) compared with those with normal lean mass and not obese. This was one of the first prospective studies to show that SO independently predicts disability. A prospective study of about 4000 individuals aged 65 and older from Hong Kong showed that the fat to muscle ratio was associated with new or worsening physical function 4 yrs later in both men and women (27). These associations were independent of many covariates, including age and specific comorbidities.

In the Invecchaire in Chianti on Aging in the Chianti Area Study, obese subjects with lower muscle strength experienced steeper declines in walking speed and were at high risk of developing new mobility disability over the 6-yr period in comparison to those without obesity or low muscle strength (28). The differences between these 2 groups were substantially higher in those 80 yrs and older.

Thus, the studies to date suggest that the combination of low lean mass measured in a variety of ways and obesity synergistically decreases physical function and increases the risk of disability. The results suggest that these effects are stronger than obesity alone or sarcopenia alone.

The younger age at the onset of obesity, currently observed in the United States, could lead to an increased burden of disability in future cohorts of elders (29). Obesity coupled with the loss of lean mass with age, that is, SO, could lead to dramatic increases in disability in future generations. However, SO research is in its infancy. Many studies have reported the prevalence of SO, but definitions vary, and thus the range in prevalence is wide. The research environment needs to develop a consistent definition of SO to be used across studies. The link between loss of lean mass and obesity suggests common etiologic pathways that need to be further clarified. SO is associated with an increased risk of disability and lower physical function. Osteoporotic fractures are also associated with poor physical function, and there is a paucity of research on the relationship of SO to skeletal health and other adverse outcomes. Interventions aimed at reducing SO may improve physical function as well as reduce disability and death.

Key Points

  • SO is the co-presence of sarcopenia and obesity.

  • The definitions of SO varied markedly. Research needs to identify a consistent definition to further study of the etiology and consequences of SO.

  • SO is associated with greater declines in physical function than obesity or sarcopenia alone.

  • Links between loss of muscle mass and increase in fat mass suggest common etiologic factors.

  • Further research is needed on the consequences of SO, including skeletal consequences, and to identify interventions aimed at reducing SO.

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    Disclosures: None to report.

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