Osteosarcopenic obesity: a new face of an old problem
Although osteopenia/osteoporosis, sarcopenia, and obesity have been recognized and assessed for decades, the concurrent appearance of these problems has just begun to be discussed. From a historical perspective, the combination of sarcopenia and obesity termed sarcopenic obesity, was the first term to be introduced [33] and is extensively studied [21].
Sarcopenic obesity is an emerging health problem characterized by the simultaneous manifestation of excess body fat and low muscle mass/strength, and it has been described by Roubenoff as the confluence of two epidemics: the aging and the obesity epidemics [34]. Since there are no standard definitions for combined sarcopenia and obesity, a variety of indices has been used, and we refer the reader to an extensive review [21]. Regardless of indices used to define this condition, the majority of studies have found sarcopenic obesity to predict worse clinical outcomes when compared to sarcopenia or obesity in isolation [21, 34, 35].
The term “sarco-osteopenia” or “ sarco-osteoporosis” was first introduced by Binkley and Buehring [36]. The authors proposed that patients with both low bone and muscle mass/performance would be diagnosed with this condition. Therefore, sarco-osteopenia or sarco-osteoporosis is an interconnected syndrome which should be combined into a single term. Individuals presenting with sarco-osteopenia or sarco-osteoporosis would be at higher risk for falls and fractures and, hence, increased morbidity, reduced quality of life, and increased mortality [36].
Although the term has only recently been proposed, the association of muscle and bone mass has been extensively studied [37–41]. Specifically, the dominant role of muscle on BMD of various skeletal sites in younger and older women was reported earlier [3]. Furthermore, when there is a lack of weight training, muscle mass begins to decline during the third decade of life, and bone loss follows due to the lack of strain [42]. Even the various modes of habitual and low-impact physical activity (gardening, stair climbing, heavy housework) had a positive influence on bone in postmenopausal women [2].
As the prevalence of elderly individuals increases in the USA and throughout the world, so does the prevalence of sarcopenia and osteopenia/osteoporosis. The addition of obesity to these existing conditions exacerbates the metabolic abnormalities likely leading to reduced physical function and quality of life. Osteosarcopenic obesity represents a change in paradigm that has gone unrecognized until recently, due to the lack of accurate technology to assess human body composition, as sophisticated tools are needed to accurately assess fat, lean, and bone tissue compartments. Furthermore, as suggested by Stenholm et al. [43], although in healthy young and older individuals bone and muscle change concurrently with changes in body weight, this process may be impaired in some individuals when the excess of body weight occurs without concurrent increases in bone and muscle mass [43].
The association among bone, muscle, and fat mass was explored by Sowers et al. [37] in adult women. The authors categorized fat and lean tissue mass into tertiles, reporting a linear increase in mean femoral neck BMD for each tertile of muscle mass. Conversely, there was a nonlinear increase in BMD for each tertile of fat mass. BMD was similarly and equally greater in the high-muscle/low-fat and high-muscle/high-fat body composition types, suggesting that greater weight alone was not associated with increased BMD. Hence, if muscle does not grow in parallel with increased body weight, BMD is not optimized [37]. The authors concluded that low muscle mass was a risk factor for low BMD in young adult women, while higher fat mass was only protective when muscle mass was adequate.
Finally, as bone and muscle loss can appear concurrently with obesity, it is reasonable to propose a new term encompassing these three conditions. The acknowledgment of osteosarcopenic obesity as an emerging public health problem increases not only scientific but also public awareness for the identification, prognostic significance, public health costs, and ultimately the development of behavioral, nutritional, and possibly pharmacological interventions to prevent or reverse this condition.

Challenges of operationalization and applicability
Unfortunately, the advantage of proposing this new abnormal body composition phenotype introduces challenges to future research endeavors. Primarily, it leads to additional debate on the diagnosis of osteosarcopenic obesity, which in turn can impact risk prediction and treatment strategies. Although the definition of osteopenia/osteoporosis has been quite widely accepted, substantial debate still exists regarding the definition of sarcopenia and even obesity [21]. Likewise, the expected prevalence of osteosarcopenic obesity in the general population is uncertain. The combination of three diagnostic criteria (for abnormal bone, muscle, and fat) may limit the number of individuals presenting with this condition, which will impact the identification of this phenotype in non-epidemiological studies in healthy populations. On the contrary, we hypothesize that the prevalence of osteosarcopenic obesity will be pronounced in those presenting with clinical conditions (e.g., cancer, diabetes, etc.).
Additional opportunities exist to identify the onset, cause, and effect of this condition. Although osteosarcopenic obesity leads to health complications (Fig. 1), it is unclear if the health implications are a cause or consequence of osteosarcopenic obesity (Fig. 2). In fact, further studies are needed to investigate the occurrence of potential reverse causality. Importantly, although future studies are needed, we anticipate that this combined phenotype will represent an advantage for risk prediction and preventive/treatment strategies in primary and secondary/tertiary care.
Fig. 2 Hypothesized interrelationships between bone, muscle, and adipose tissue in the osteosarcopenic syndrome. IMAT, intramuscular adipose tissue; GH, growth hormone; IGF, insulin-like growth factor I; ROS, reactive oxygen species. Adapted from Zamboni et al. [35], Ezzat-Zadeh et al. [44], and Roubenoff [33]