Globally, obesity rates remain high and rates of related co-morbidities, e.g., metabolic syndrome and type 2 diabetes, continue to escalate. Poor diet, lifestyle, and an aging population has led to the emergence of “sarcopenic obesity” - characterized by low skeletal muscle mass/strength, combined with excess body fat, much of which is visceral. Surrounding the body's critical organs, visceral fat stimulates systemic inflammation and is an increasingly serious risk factor for cardiovascular disease and diabetes. Nutrition survey data suggest that populations are becoming overfed, yet undernourished, contributing simultaneously to a greater prevalence of sarcopenic obesity and elevated rates of chronic disease and nutrient inadequacy. Nutrition and public health policies need to evolve, including finding an alternative to BMI for assessing healthy body weight, raising awareness of the importance of sustainable physical activity with aging, emphasizing the nutrient density of the diet, and greater consideration of dietary protein and bioactive nutrient intake.
In some countries, the prevalence of overweight exceeds 60% of the population (in 2014, 1.9 billion adults were overweight; 600 million were obese; WHO, 2015 ; WHO, 2016). This epidemic of overweight and obesity over the past several decades has conspired with a rapidly aging population (United Nations, 2013) and declining physical activity levels (Hallal et al., 2012), resulting in an alarming rise in the rate of lifestyle-related, non-communicable disease (NCD-RisC, 2016). Paralleling these trends is a decline in the quality of the diet in many developed countries. For example, in the U.S., portion sizes have increased, increasing the energy density of the diet (Duffey and Popkin, 2011 ; Miller et al., 2009), yet the nutrient density of diets has declined (Miller et al., 2009).
These megatrends (lack of exercise, poor diet and aging) have led to the emergence of a previously silent phenomenon known as sarcopenic obesity (SO). SO is described as a syndrome characterized by the rise of body fat mass in parallel with excessive low muscle mass, with underlying elements such as endocrine, inflammatory, and lifestyle disruptions (Wannamethee and Atkins, 2015 ; Zamboni et al., 2008). SO is highly correlated with metabolism-related disease, chronic disease and functional disabilities, and has been described as “thin outside, fat inside” or “TOFI” (Stenholm et al., 2008). SO prevalence varies around the world, and tends to be greater in the elderly, those who are sedentary and with low protein intake (Tyrovolas et al., 2016). In a recently published meta-analysis involving 12 prospective cohort studies, over 35,000 participants and >14,000 deaths, Tian and Xu concluded that SO is associated with an increased risk of death (Tian & Xu, 2016).
SO is a unique type of obesity, distinct from that characterized by excess subcutaneous fat. SO’s distinguishing factor is the high level of visceral, or organ fat, which is known to be highly inflammatory. The excessive disposition of visceral fat can be attributed to a variety of etiological factors, e.g., age, genetics, gender, hormone, ethnicity, diet and other environmental and lifestyle variables (Tchernof & Despres, 2013).
Subjects with SO are considered to be in a hyper-inflammed state, contributing to an increased risk for chronic disease (Wannamethee & Atkins, 2015) as well as oxidative stress, both of which impair insulin sensitivity and growth hormone secretion and then enable the development and progression of muscle loss and consequent sarcopenia (Wannamethee and Atkins, 2015 ; Zamboni et al., 2008). In brief, SO is associated with a higher risk of frailty, disability, morbidity, and mortality than obesity or sarcopenia alone (Kohara, 2014). Thus, the efforts taken to promote healthy aging must consider both preventing obesity and maintaining or increasing muscle mass and function.
At the same time, SO subjects are metabolically compromised due to a decided decline in skeletal muscle mass, which in turn contributes to a reduction in the basal metabolic rate (Waters, Baumgartner, Garry, & Vellas, 2010). Externally, these subjects may appear normal and even appear to maintain a normal weight. Indeed, according to magnetic resonance imaging (MRI) scans, subjects may have a normal body mass index (BMI), and yet be diagnosed with SO. Comparing MRI scans of subjects with the same BMI but vastly different levels of visceral fat and skeletal muscle mass can reveal major disparities in inflammatory states and health status (Thomas, Frost, Taylor-Robinson, & Bell, 2012).
The limitations of BMI as a tool to assess obesity and the silent, and non-obvious nature of SO raise important public policy questions. BMI is relied on worldwide by health and authoritative bodies to assess the overweight and obesity status of populations. While both practical and cost effective, it can underestimate underlying body fat and cannot address body fat and muscle mass redistribution that is characteristic of SO. Clearly, a different metric is needed, if not at the population level, at least at the individual level, to better assess health status by taking into account lean body mass and body fat distribution.
High protein diets
Dietary protein intake is essential to sustain life and promote health throughout the human life course. Quantitatively, protein intake typically peaks for both men and women in early adulthood and progressively declines with advancing age, concurrent with reductions in lean body mass (especially skeletal muscle), total body energy expenditure, and dietary energy intake (Berner et al., 2013 ; Fulgoni, 2008). Older adults are at increased risk for suboptimal protein intakes (Berner et al., 2013) that contribute to reduced skeletal muscle size and function (Castaneda, Charnley, Evans, & Crim, 1995). The current Recommended Dietary Allowance (RDA) for protein, based on short-term nitrogen balance, is 0.8 g/kg/d (IOM, 2005). This amount of protein prevents muscle catabolism in older adults (Campbell, Trappe, Wolfe, & Evans, 2001), but may not maximally promote muscle anabolism (Bauer et al., 2013). Protein metabolism (Conley et al., 2013; Rafii et al., 2015; Rafii et al., 2016 ; Tang et al., 2014) and muscle health and functional outcomes data (Bauer et al., 2013 ; Moore et al., 2015) are progressively becoming available to aid scientists in updating recommended intakes for protein (Bauer et al., 2013), including adults with SO, sarcopenia and obesity.
Older adults in the United States consume about 65% of daily protein intake from animal-based foods, including 40% from flesh foods (meats, poultry, pork, and fish) and 25% from dairy and egg sources (Smit, Nieto, Crespo, & Mitchell, 1999). Grains (18%), vegetables (9%), legumes/soy/nuts/seeds (4%), and fruits (3%) are the predominant plant-based sources of protein typically consumed by older adults. Ingestion of protein-rich foods of animal origin is helpful since animal-based proteins are considered complete proteins because they contain all of the required essential amino acids. However, it is certainly possible to consume sufficient quantities of essential amino acids when consuming a variety of protein-rich plant-based proteins, especially as part of a lacto-ovo-vegetarian diet. Indeed, the capacity of older adults to retain or increase lean mass and skeletal muscle size was comparable when lacto-ovo-vegetarian or omnivorous (meat-containing) diets with sufficient total protein intake were consumed (Haub, Wells, Tarnopolsky, & Campbell, 2002).
Data from epidemiological and randomized controlled feeding studies support that daily protein intakes moderately above the RDA (>1.0 g/kg/d) promote a more favorable body composition, including a higher lean mass to fat mass ratio, and reduced loss of lean body mass during purposeful weight loss (Campbell et al., 2015; Campbell and Leidy, 2007 ; Kim et al., 2016). Indeed, when older adults consume lower amounts of dietary energy, either due to reduced energy requirements or purposeful weight loss to promote improved cardio-metabolic health (Villareal, Apovian, Kushner, & Klein, 2005), it is advisable to consume protein intakes of >1.0 g/kg/d. This dietary recommendation may be achieved by continuing to consume nutrient-rich, high-protein foods and reducing intakes of nutrient-poor refined carbohydrates and added sugars.
Most apparently healthy adults consume the same pattern of foods throughout adulthood with more protein and energy typically consumed at dinner than lunch, followed by breakfast (Howarth, Huang, Roberts, Lin, & McCrory, 2007). This skewed within-day pattern of protein typically only includes one meal with sufficient protein (25–30 g/meal) to maximally stimulate muscle protein synthesis (Paddon-Jones et al., 2008 ; Thalacker-Mercer and Drummond, 2014). A skewed protein intake pattern is hypothesized to reduce the daily rate of skeletal muscle protein synthesis, compared to eating three meals daily with at least 25–30 g protein, which may in the long-term compromise the ability of older adults to retain lean body mass and muscle size. However, there are no published longitudinal randomized controlled trials assessing whether the within-day distribution of equal quantities of daily protein intake affect lean body mass and muscle size in older adults.
Enthusiasm for highly prescriptive use of high-protein diets (including within-day dietary patterning) to promote the retention of lean body mass, including muscle mass, and function in older adults (Paddon-Jones et al., 2008 ; Thalacker-Mercer and Drummond, 2014) must be supported by high-quality longitudinal research, not just theories, hypotheses or extrapolations from short-term studies. At present, the quantity of protein consumed daily is more important than the within-day pattern of consumption to promote the retention of lean body mass, which includes skeletal muscle, in older adults.
Consumption of fruits and vegetables is associated with a reduced risk for obesity as reported in a study using the data of the Nurses’ Health Study I, II; Health Professionals Follow-up Study (Bertoia et al., 2015). Emerging data also suggests the benefit of their consumption can be extended to sarcopenia and thus SO. Kim, Lee, Kye, Chung, and Kim (2015) found in a cross-sectional study that frequent vegetable and fruit consumption was inversely associated with sarcopenia in older Korean adults. Furthermore, fruit and vegetable intakes were found to inversely associate with functional limitations and disability in the Atherosclerosis Risk in Communities Study (Houston, Stevens, Cai, & Haines, 2005).
Even though the low calories and high nutrient density are probably accountable for the noted effects, bioactives which can be defined as “A type of chemical found in small amounts in plants and certain foods that have actions in the body that may promote good health (NCI, 2016)” may exert bioactions that prevent obesity and sarcopenia. There are thousands of phytochemicals with putative actions in health promotion and prevention, which can be simply categorized into phenolics, alkaloids, carotenoids, organosulfur compounds, nitrogen containing compounds, etc. (Liu, 2004).
Some bioactives have been illustrated in the literature for their benefits in normal measures of body weight and abdominal fat. Zhang et al. (2012) reported that daily consumption of a green tea beverage containing 609.3 mg catechins and 68.7 mg caffeine for 12 weeks decreased body weight and induced visceral fat loss in Chinese adults with central adiposity. Resveratrol, which is a polyphenol commonly found in red wine and red grapes, was found to decrease the adipocyte size of abdominal subcutaneous adipose tissue in healthy obese men, suggesting the compound could enhance adipogenesis (Konings et al., 2014). In addition to their beneficial effect on body weight and fat, polyphenols can augment fat-free mass. Aubertin-Leheudre, Lord, Khali, and Dionne (2007) reported that 6 month supplementation of 70 mg/d isoflavones increased fat-free mass and muscle mass index in obese-sarcopenic postmenopausal women.
Combining both physical activity and dietary regimen in lifestyle modification for the improvement of body composition and fat distribution is recognized to yield the best outcomes. Maki et al. (2009) observed that consumption of green tea (625 mg of catechins with 39 mg caffeine/d) for 12 weeks enhanced the exercise-induced reduction in abdominal fat and subcutaneous abdominal fat area in overweight and obese adults during exercise-induced weight loss while green tea alone did not have a significant effect. After taking soy isoflavones (75 mg of isoflavone conjugates/day) and walking exercise (45 min/d, 3 d/wk) either together or alone for 1 year, both treatments alone decreased the abdominal fat of postmenopausal Japanese women, but there was no interaction between them (Wu et al., 2006). It is possible that exercise type (aerobic vs. resistance) may affect the magnitude of interaction between physical activity and bioactives in body composition. Indeed, Cardoso, Salgado, Cesar, and Donado-Pestana (2013) found that there was a synergy between resistance exercise and green tea catechins in the improvement of body fat and waist circumference, lean body mass, and muscle strength in overweight or obese women. As sarcopenia is defined based on both muscle function and mass, it is critical to demonstrate the benefit of bioactives on muscle function. In an exercise plan, taking curcumin (200 mg/d) for 3 months improved muscle strength and physical performance in older people as compared to the exercise alone (Franceschi et al., 2016).
It has been found that daily dietary supplementation with 4 g of fish oil-derived n-3 polyunsaturated fatty acids (PUFA) stimulates muscle protein synthesis by increasing the efficiency of amino acid incorporation into muscle protein (Smith et al., 2011) and increases muscle mass and muscle strength in healthy older adults (Smith et al., 2015). Others have shown that dietary supplementation with 2 g of fish oil-derived n-3 PUFA improves neuromuscular function (shortened neuromuscular delay) in healthy older women (Rodacki et al., 2012). In addition, it has been found that supplementation with n-3 PUFA augments brachial artery dilation, vascular conductance, and blood flow during muscle contraction in healthy people and rats (Stebbins et al., 2010 ; Walser et al., 2006), which may be important to ensure adequate oxygen and nutrient delivery to muscle.
These findings suggest fish oil-derived n-3 PUFAs as a potential novel nutritional strategy to counteract the age-associated decline in skeletal muscle mass and function without potential adverse or possibly even beneficial effects on cardiometabolic health (Avanzini et al., 2013; He et al., 2016; Lalia and Lanza, 2016; Leslie et al., 2015; Miller et al., 2014; Rizos et al., 2012 ; Yang et al., 2016).
Thus, it appears that bioactives present in certain foods and supplements can have a role in prevention and protection against sarcopenic obesity. However, more evidence must be gathered from clinical studies with considerations given to type and dose of bioactives, interaction with exercise, robust study design, subject type (genetics, ethnicity, age, gender, and existence of sarcopenia or central adiposity) (Goisser et al., 2015).
Starting in late middle-age, skeletal muscles undergo a progressive series of changes, including atrophy, infiltration with non-contractile fat and connective tissue, reduced capillary density, decreased mitochondrial content, and motor unit and neuromuscular junction remodeling. These alterations adversely affect endurance and the ability of muscle to generate and maintain force, which can have adverse effects on activities of daily living (such as walking, climbing stairs, and lifting items) and quality-of-life. Older adults whose muscle mass and physical abilities (walking speed and/or strength) fall below certain threshold values are considered “sarcopenic” and are at increased risk for falls, hospitalization, frailty, loss of independence, and mortality (Cruz-Jentoft et al., 2010 ; Fielding et al., 2011). Obesity, which has become very prevalent in older adults, often masks the age-associated loss of muscle mass and aggravates the effect of aging on muscle quality and function (Choi et al., 2016; Lafortuna et al., 2014 ; Villareal et al., 2004).
The loss of skeletal muscle mass is observed in many pathophysiological conditions including, aging and obesity (Akhmedov and Berdeaux, 2013; Lessard et al., 2016 ; Rivas et al., 2016). The loss of muscle mass and function with aging is characterized by a mismatch between skeletal muscle protein synthesis and breakdown (Gordon et al., 2013; Haran et al., 2012 ; Rivas et al., 2014). The concurrence of obesity and sarcopenia, increases the risk of metabolic impairments and physical disability more than just either sarcopenia or obesity alone (Anton et al., 2013 ; Nilsson et al., 2013). Similar to obesity, body fat redistribution occurs during aging placing older adults at a greater risk for the accumulation of abdominal fat, which contributes to unhealthy metabolic conditions and reductions in insulin sensitivity (Anton et al., 2013 ; Ferrucci and Alley, 2007). Sarcopenia and obesity magnify one another as the loss of muscle reduces the mass of available insulin-responsive tissue, promoting insulin resistance, which, in turn, promotes the metabolic syndrome and obesity (Anton et al., 2013 ; Ferrucci and Alley, 2007).
Regular physical activity and high protein intake (1.2–1.6 g per kg per day) are recommended to prevent and treat sarcopenia (Bauer et al., 2013; Baum et al., 2016; Landi et al., 2016 ; Phillips et al., 2016). However, few older adults regularly engage in physical activity and high protein intake does not improve muscle strength and increases the risk of developing insulin resistance and type 2 diabetes (Krebs et al., 2002; Levine et al., 2014; Linn et al., 1996; Linn et al., 2000; Robinson et al., 2014; Sluijs et al., 2010; Smith, Yoshino, et al., 2015; Smith et al., 2016; Tinker et al., 2011 ; Wang et al., 2010). Diet-induced weight loss, although very effective in ameliorating the cardiometabolic abnormalities associated with obesity (Fabbrini and Klein, 2008; Gallagher and LeRoith, 2015; Kirk and Klein, 2009; Klein et al., 2002; Klein et al., 2004; Parker and Folsom, 2003 ; Wolin et al., 2010) is often not recommended for obese older adults because of the adverse effect of diet-induced weight loss on lean body and muscle mass.
A characteristic metabolic feature of both aging and obese skeletal muscle is an increase in intramyocellular lipid (IMCL) content (Lessard et al., 2007; Rivas, Morris, et al., 2011; Rivas et al., 2009; Rivas et al., 2012 ; Rivas et al., 2016). Increases in IMCL content may play an important mechanistic role in the development of the muscle’s resistance to anabolic stimuli and the progression of sarcopenia with aging and muscle atrophy in obesity (Kalyani et al., 2014; Kalyani et al., 2015 ; Rivas et al., 2012). In fact, even in otherwise healthy older humans there have been shown to be increases in the accumulation of bioactive lipid species, associated with anabolic resistance in these individuals, compared to their young cohorts (Rivas et al., 2012). Therefore, reducing the accumulation of excess lipid storage both centrally and within insulin sensitive peripheral tissue could provide a critical benefit in reversing the progression of SO.
Over the last 30 years, the scientifically verified benefits of regular physical activity (PA) have been demonstrated and proven through small intervention studies, randomized clinical trials (RCT) and large, well-designed epidemiological studies in both humans and animals (Chee et al., 2016; Harber et al., 2012; Lessard et al., 2007; Lessard et al., 2011; Pahor et al., 2014; Rivas, Lessard, et al., 2011 ; Rouffet et al., 2013). These include, but are not limited to, cardiovascular enhancements (Earnest et al., 2013), cognitive improvements (Lautenschlager et al., 2008), lowered risk of osteoporosis (Wilks et al., 2009), and decreased falls and injuries from falls (Gillespie et al., 2012 ; Rubenstein et al., 2000). In addition, exercise is an effective treatment for many of the chronic diseases that increase with age, including obesity, diabetes/pre-diabetes and sarcopenia, providing a definitive rationale for exercise prescription in an elderly population (Booth et al., 2000; Campbell et al., 2009; Fiatarone et al., 1990 ; Lee et al., 2012). A recent multicenter RCT was conducted comparing a moderate intensity PA with an educational program in 1635 sedentary and functionally limited older persons, over a follow-up period of approximately 3 years. The primary results showed that PA reduced the incidence of major mobility disability over a mean follow-up period of 2.6 years, with largest benefits among participants with the most severe functional impairment at baseline (Pahor et al., 2014). These results show, at least in this population, the benefit of long-term moderate intensity PA.
Regular physical activity in middle age is highly associated with healthy aging (Sabia et al., 2012 ; Sun et al., 2010). Even in individuals who are sedentary up until middle age it is not too late since exercising in old age leads to significant improvements to physical and cognitive health (Berk et al., 2006; Hamer et al., 2014 ; Lautenschlager et al., 2008). The metabolic benefits of increasing fatty acid oxidation in skeletal muscle, rather than accumulating intramuscular and adipose tissue stores around the major organs as well as lowered blood pressure helps to reduce the risk developing type 2 diabetes mellitus, cardiovascular disease and sarcopenia (Booth et al., 2000; Campbell et al., 2009; Fiatarone et al., 1990 ; Lee et al., 2012). This likely occurs, in part, through an increase in oxidative enzymes that facilitate the turnover and oxidation of fatty acid both at rest and during exercise (Devries et al., 2013; Dube et al., 2008; Margolis and Rivas, 2015 ; Samjoo et al., 2013).
Although there is abundant evidence demonstrating the benefits of increased PA, findings of some concern is a majority of individuals demonstrate low adherence to exercise prescription either because of psychological, physical or even genotypic/phenotypic obstacles (Colley et al., 2008; Hughes et al., 2009; Vasconcelos et al., 2016 ; Wasser et al., 2016). SO poses a special challenge for exercise prescription, because the difficulty of designing effective interventions for people with multiple comorbidities associated with both obesity and older age (Dufour et al., 2013; Goisser et al., 2015 ; Vasconcelos et al., 2016). For example, obesity in older adults is associated with increased stress on load-bearing joints from excess weight, mobility disabilities and insufficient aerobic fitness that is worsened with SO (Cauley, 2015; Dufour et al., 2013; Goisser et al., 2015 ; Vasconcelos et al., 2016). Therefore, the development of strategies to better promote sustainable physical activity are required. This could perhaps begin with tailoring exercise to the individual rather than dictating arbitrary recommendations for everyone. Adding plausibility to this concept is the fact that aside from the physical variability found in SO there are recognized deficits in the metabolic response of exercise or ‘exercise resistance’ in some individuals (Lessard et al., 2013). Making ‘exercise resistance’ a major consideration in the prescription of a new exercise regimen.
SO is the confluence of one natural process (aging) and one symptom of fast-paced modern living (obesity). The decrease in muscle mass with age, and the increase in visceral fat with poor dietary choices and lack of exercise, leads to a “fat frail” or TOFI population with the worst of both worlds, i.e., decreased muscle strength expected to carry increased body weight. And the problem worsens as a function of time; a vicious cycle of increasing body weight leading to sore joints leading to more inactivity leading to more muscle wastage leading to increasing body weight. Further, adipose tissue is much less metabolically active than muscle tissue; and adipose tissue has less insulin-responsiveness than muscle tissue promoting insulin resistance, which predisposes towards metabolic syndrome, obesity and diabetes (Roubenoff, 2004).
Diet, in addition to physical activity, play key roles in the prevention and management of SO. In many countries around the world, diets have become energy rich, yet nutrient poor, and populations are overfed, yet undernourished (Miller et al., 2009). In other words, diets are high in energy density and low in nutrient density, contributing to an increase in the intake of “empty” calories. To combat this trend, experts and nutrition policy makers have emphasized the importance of consuming high nutrient density diets (Drewnowski and Fulgoni, 2014; Troesch et al., 2015 ; U.S. DHHS & USDA, 2015). Consumption of diets rich in protein, bioactive food components, such as catechins from green tea and omega-3 fatty acids, along with resistance exercise have been studied as lifestyle approaches to prevent and combat SO.
Shao, A; Campbell, W; Chen, O; et al. The emerging global phenomenon of sarcopenic obesity: Role of functional foods; a conference report. Journal of Functional Foods. Volume 33, Pages 244–250 (2017). http://www.sciencedirect.com/science/article/pii/S1756464617301652.