Frailty, sarcopenia and osteoporosis | Medicina Clínica (English Edition)

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Adapted from Cruz et al.<a class="elsevierStyleCrossRef" href="#bib0060">12</a> BIA: bioelectrical impedance; DXA: dual energy level X-ray absorptiometry; EWGSOP: European Working Group on Sarcopenia in Older People. SARC-F: Strength Assistance in walking, Rise from chair, Climb stairs, and Falls; TUG: Timed Up and Go." ] ] ] "textoCompleto" => "IntroductionFrailty, understood as physical or systemic frailty, is a syndrome of the elderly that leads to increased mortality and hospitalisation. With age there is also a progressive loss of skeletal muscle mass and strength known as sarcopenia. This disorder is closely related to the pathophysiology of frailty and can also be considered as a geriatric syndrome. On the other hand, osteoporosis, in its involutional form -by far the most common- is a disease of the elderly, particularly affecting women. Two main factors participate in the development of osteoporotic fractures: bone weakness and trauma. Both aspects may be related to sarcopenia and frailty. In fact, this relationship has been studied in a number of studies, which have not always focused on the same aspects. Given the above, there is an interest in clarifying how sarcopenia and frailty are related to osteoporosis.FrailtyConcept, definition and diagnostic criteriaThe term frailty emerged at the end of the last century to describe a clinical syndrome that represents a continuum from the healthy older adult to the extremely vulnerable with high risk of death and low chance of recovery.<a class="elsevierStyleCrossRef" href="#bib0005">1</a> Subsequently, Morley et al.,<a class="elsevierStyleCrossRef" href="#bib0010">2</a> in 2013 defined frailty as a multidimensional geriatric syndrome, characterised by an increased vulnerability of an individual to develop increased dependency or mortality when exposed to a stressor. More recently, the EU Joint Action 724099/ADVANTAGE<a class="elsevierStyleCrossRef" href="#bib0015">3</a> has defined frailty as "a state characterised by a progressive decline in physiological systems related to ageing, leading to a reduction in intrinsic capacity, which confers extreme vulnerability to stressors, increasing the risk of various negative health events". Frailty can be physical, psychosocial or a combination of both, and is a dynamic situation that can improve or worsen over time. There are multiple tools for diagnosing frailty, although the Fried score is probably the most widely used.<a class="elsevierStyleCrossRef" href="#bib0020">4</a> For these authors, a diagnosis of frailty can be made for people with at least three of the following five criteria: unintentional loss of 4.5 kg of weight or more in the last year, weakness - loss of strength, self-reported feelings of exhaustion or lack of energy, and decreased physical activity and gait speed. When one or two criteria are met, patients are classified as "pre-fragile". Other diagnostic tools are the Rockwood frailty index,<a class="elsevierStyleCrossRef" href="#bib0025">5</a> the Frailty Trait Scale (FTS<a class="elsevierStyleCrossRef" href="#bib0030">6</a> and the FRAIL frailty index.<a class="elsevierStyleCrossRef" href="#bib0035">7</a>Epidemiology and aetiopathogenesisThe reported prevalence of frailty is highly variable, due to the different criteria used to define frailty and the characteristics of the persons assessed (age, sex, race, degree of dependency, etc.). It is higher when using the Rockwood Index and increases exponentially with age, being more common in women than in men by a ratio of 2:1.<a class="elsevierStyleCrossRef" href="#bib0005">1</a> In a systematic review published a few years ago,<a class="elsevierStyleCrossRef" href="#bib0040">8</a> the prevalence of frailty described in the papers included in the review ranged from 2% to 48%, with an overall prevalence of 18% (confidence interval [CI]: 15 %–21 %). This study analysed 68 publications involving more than 10,000 people from different European countries. The characteristics of the persons included (age, sex, origin -community, nursing-homes etc.) and the diagnostic criteria were not homogeneous, although Fried's criteria were used in slightly more than half of these studies. When only the community population was analysed, not including dependent individuals, the prevalence of frailty was 12%.<a class="elsevierStyleCrossRef" href="#bib0040">8</a> In Spain, the prevalence at community level ranges from 2.5% to 38%, depending on age, sex and criteria applied.<a class="elsevierStyleCrossRef" href="#bib0005">1</a>In a study carried out by our group in 1.000 people belonging to the Camargo cohort,<a class="elsevierStyleCrossRef" href="#bib0045">9</a> living in the community and with a mean age of 72 years, the prevalence of frailty (using Fried's criteria) reached 12.1% of the population studied, being higher in women than in men (13.8% vs. 6.8%; p = 0.01).Frailty is a clinical syndrome that affects many systems. There is a clear relationship between frailty, muscle structure and function. However, although sarcopenia appears to be one of the risk factors and sometimes marks the beginning of the process known as the "frailty cycle", it is important to remember that although they overlap to some extent, they are not entirely coincidental and should be understood as distinct entities. The importance of frailty lies in its association with mortality, disability, falls, hospitalisation or admission to nursing homes.<a class="elsevierStyleCrossRefs" href="#bib0005">1,3</a> Its pathogenesis involves a number of age-related changes affecting several systems, the most prominent of which are cardiovascular, musculoskeletal, respiratory, endocrine (sex hormones, insulin sensitivity, growth hormone [GH], vitamin D), and immunological (low-grade inflammation) (<a class="elsevierStyleCrossRef" href="#fig0005">Fig. 1</a>).<a class="elsevierStyleCrossRef" href="#bib0050">10</a> The role of the central nervous system, although little known, seems to be relevant, and some recent studies suggest the involvement of certain brain areas related to executive functions in the generation of the syndrome.<a class="elsevierStyleCrossRef" href="#bib0005">1</a><elsevierMultimedia ident="fig0005"></elsevierMultimedia>SarcopeniaConcept, definition and diagnostic criteriaThe term sarcopenia - from the Greek sarx (flesh) and penia (poverty) - refers to the loss of muscle mass and strength that occurs during ageing. This term was introduced in 1989 by Irwin Rosenberg to describe the loss of muscle mass that occurs over the years.<a class="elsevierStyleCrossRef" href="#bib0055">11</a> However, decreased muscle mass alone is not a good predictor of mortality and disability. Thus, in addition to the loss of muscle mass, muscle function was subsequently impaired.<a class="elsevierStyleCrossRef" href="#bib0060">12</a> Sarcopenia is currently included in muscle diseases and is coded as a disease entity in the International Classification of Diseases, 10th edition (ICD-10) since 2016.<a class="elsevierStyleCrossRef" href="#bib0065">13</a> About 10 years ago, the European Working Group on Sarcopenia in Older People (EWGSOP) established diagnostic criteria based on the measurement of muscle mass, muscle strength and physical performance, which have been widely accepted<a class="elsevierStyleCrossRef" href="#bib0070">14</a> (<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>). Sarcopenia is considered to exist when patients have low muscle mass and one of the following two conditions: reduced muscle strength or poor physical performance. If muscle mass is reduced and muscle strength and physical performance are normal, the patient can be diagnosed with "presarcopenia". When all three parameters are altered, we speak of "severe sarcopenia". The European Society for Clinical Nutrition and Metabolism (ESPEN) and the Special Interest Groups (SIG<a class="elsevierStyleCrossRef" href="#bib0075">15</a> have also endorsed these criteria. Another definition is provided by the International Working Group on Sarcopenia (IWGS),<a class="elsevierStyleCrossRef" href="#bib0080">16</a> which is based on the measurement of muscle mass and gait speed. For the Foundation for the National Institutes of Health (FNIH),<a class="elsevierStyleCrossRef" href="#bib0085">17</a> the criteria should be based on the presence of low levels of muscle mass and strength.<elsevierMultimedia ident="tbl0005"></elsevierMultimedia>The EWGSOP updated the diagnostic criteria for sarcopenia syndrome in 2019 (EWGSOP 2),<a class="elsevierStyleCrossRef" href="#bib0090">18</a> proposing new cut-off points and a stepwise diagnostic approach through an algorithm (<a class="elsevierStyleCrossRef" href="#fig0010">Fig. 2</a>). Strength is the first parameter to be assessed, and if it is decreased, muscle mass is measured, making a diagnosis of sarcopenia if it is also decreased. If the patient also suffers from poor physical performance, this is referred to as severe sarcopenia. This consensus also contemplates the distinction between primary and secondary sarcopenia, the latter being considered when there are causal factors beyond age, such as inflammatory processes or malignant states. It also refers to acute or chronic sarcopenia, where chronic sarcopenia is defined as sarcopenia that has been present for more than six months.<elsevierMultimedia ident="fig0010"></elsevierMultimedia>Epidemiology and aetiopathogenesisAs with frailty, published prevalence values for sarcopenia are highly variable and depend on the criteria used for diagnosis, the techniques used to measure the different variables and the profile of the individuals included in the studies. When assessed using the EWGSOP scale, it is estimated to affect 5%–13% of people between 60–70 years of age. It is higher in men and increases with age.<a class="elsevierStyleCrossRef" href="#bib0095">19</a> In a systematic review analysing five studies, the prevalence of sarcopenia according to EWGSOP criteria was 4.3%, 5.6%, 11.2%, 15.9% and 31.9%.<a class="elsevierStyleCrossRef" href="#bib0100">20</a> Mayhew et al.<a class="elsevierStyleCrossRef" href="#bib0105">21</a> found that using the EWGSOP/Asian Working Group for Sarcopenia (AWGS) definition, the estimated prevalence was 12.9% (CI 9.9%–15.9%). According to EWGSOP criteria, the prevalence of sarcopenia in our study of the Camargo cohort<a class="elsevierStyleCrossRef" href="#bib0110">22</a> was 14.1% (13.0% in women and 17.7% in men). Locquet et al.,<a class="elsevierStyleCrossRef" href="#bib0115">23</a> using criteria comparable to ours and in an age-matched population, established a sarcopenia prevalence of 14.9%.Studies assessing the incidence of sarcopenia are relatively rare, although the incidence ranges from 1.6 to 3.6% per year using the EWGSOP criteria. As with prevalence, incidence increases with age.<a class="elsevierStyleCrossRef" href="#bib0060">12</a>Muscle mass and strength, as well as BMD, peak in youth and, after a period of plateau, begin to decline gradually. This loss of muscle mass and strength leads to an increased risk of falls, functional impairment, frailty and mortality.<a class="elsevierStyleCrossRef" href="#bib0060">12</a>There are many factors that may influence the development of this condition, and they are far from being fully understood (<a class="elsevierStyleCrossRef" href="#fig0015">Fig. 3</a>). Ageing causes an imbalance between the anabolic and catabolic pathways of muscle proteins, leading to an overall loss of skeletal muscle. Cellular changes in sarcopenic muscle include a reduction in the size and number of myofibrils, particularly affecting type II fibres.<a class="elsevierStyleCrossRef" href="#bib0060">12</a> This loss of fast motor units leads to a decrease in muscle strength which is reflected in the performance of certain movements, such as sitting in a chair, climbing stairs, or maintaining posture after losing balance. In addition, satellite cell dysfunction also appears to be linked to the development of sarcopenia.<a class="elsevierStyleCrossRef" href="#bib0120">24</a> Several elements are involved in this loss of muscle mass and strength, including environmental and hormonal factors, as well as those related to the muscle and its vascularisation or to the action of certain cytokines and growth factors.<a class="elsevierStyleCrossRefs" href="#bib0060">12,24</a> Finally, some studies suggest that the intercommunication between muscle and bone is mediated by endocrine factors, such as myostatin, irisin, osteocalcin and many others, although the relevance of this communication in the pathogenesis of sarcopenia is not fully understood.<a class="elsevierStyleCrossRefs" href="#bib0060">12,25</a><elsevierMultimedia ident="fig0015"></elsevierMultimedia>Relationship between frailty and osteoporosisAlthough we know that frailty and osteoporosis share risk factors (age, low body mass index [BMI], sedentary lifestyle, unbalanced nutrition, polypharmacy, etc.) the exact relationship between them is not well defined.<a class="elsevierStyleCrossRef" href="#bib0130">26</a> This is due, at least in part, to the different criteria used to define frailty and osteoporosis, and the heterogeneity of the populations in which they have been studied.Systemic frailty is considered to be a risk factor for fracture, probably due to the increase in falls it entails.<a class="elsevierStyleCrossRefs" href="#bib0005">1,26</a> Therefore, some of the studies have looked at the relationship with fractures in general. For example, in a systematic review that included six studies involving a total of about 100.000 people, frailty was found to be a significant predictor of future fractures among community-dwelling older people (odds ratio [OR]: 1.70, CI: 1.34–2.15, p < 0.0001).<a class="elsevierStyleCrossRef" href="#bib0135">27</a> Another paper using data from the Canadian Multicentre Osteoporosis Study (CaMos) found a significant hazard ratio (HR) of 1.18 for hip fractures and 1.30 for clinical vertebral fractures for each 0.10 increase in the frailty index.<a class="elsevierStyleCrossRef" href="#bib0140">28</a>In a recent study of more than 25,000 people in the Canadian Longitudinal Study on Aging (CLSA), frailty, as assessed by the Rockwood index, was independently associated with fracture incidence over three years of follow-up.<a class="elsevierStyleCrossRef" href="#bib0145">29</a> In fact, some authors have proposed that the frailty index would be comparable to the FRAX tool in predicting the risk of major osteoporotic and hip fractures, so that assessment of the degree of frailty could help to evaluate the risk of fracture in the elderly.<a class="elsevierStyleCrossRef" href="#bib0150">30</a>We observed a prevalence of osteoporotic fractures of 22.5% in frail people and 15.6% in non-frail people in the 1,000 people studied in our Camargo cohort study.<a class="elsevierStyleCrossRef" href="#bib0045">9</a> On the other hand, 16.5% of those with osteoporotic fractures and 11.1% of those without fractures were frail. The OR, adjusted for age and sex, was 1.57 (CI: 0.99–2.51), at the limit of statistical significance (p = 0.056).The results were less conclusive when the association sought was not that of frailty status with the development of fractures, but rather frailty with bone mineral density (BMD). Sternberg et al.<a class="elsevierStyleCrossRef" href="#bib0155">31</a> assessed frailty using Fried's criteria or the Vulnerable Elders Survey (VES-13) and found no significant association with BMD at baseline (although, interestingly, they found a significant association with the decrease in BMD observed after one year). Frisoli et al.<a class="elsevierStyleCrossRef" href="#bib0160">32</a> also found no association with frailty in a population of people with osteopenia or osteoporosis. One study has estimated subjectively assessed frailty,<a class="elsevierStyleCrossRef" href="#bib0165">33</a> without finding an association with BMD, but with hip fracture. In contrast, Kenny et al.<a class="elsevierStyleCrossRef" href="#bib0170">34</a> have found associations between BMD and two of the components of frailty, namely grip strength and gait speed.In our study of the Camargo cohort mentioned above,<a class="elsevierStyleCrossRef" href="#bib0045">9</a> we observed that the prevalence of densitometric osteoporosis in people with frailty was 21.7%, and in people without frailty, 20.2%. Conversely, frailty was present in 12.7% of patients with osteoporosis and 11.8% of those without. The OR was far from significant (p = 0.71), thus no association between frailty and osteoporosis was observed. Consistent with this, there were also no significant differences between BMD values of frail and non-frail patients.<a class="elsevierStyleCrossRef" href="#bib0045">9</a>Therefore, despite the heterogeneity of the studies, the existence of frailty appears to be associated with an increased risk of fractures, while the possible association between bone mass and frailty is less clear.Relationship between sarcopenia and osteoporosis. Sarcopenic obesitySarcopenia and osteoporosis may equally coincide because both are associated with ageing, but also because they may have other common aetiological factors (e.g. physical inactivity) and even because muscle changes may have an impact on bone and vice versa.<a class="elsevierStyleCrossRef" href="#bib0125">25</a> This has led to consider the existence of a mixed syndrome encompassing the two processes. Some authors have suggested the term "sarco-osteopenia" or “osteosarcopenia” to designate a disorder characterised by the coexistence of sarcopenia and bone mass with a T-score < −1.0 (osteopenia and osteoporosis). On the other hand, other authors only consider patients with sarcopenia and osteoporosis (T < −2,5),<a class="elsevierStyleCrossRefs" href="#bib0060">12,22</a> to whom the term "sarco-osteopenia" should not be applied, but rather "sarcopenic osteoporosis".We have already noted that sarcopenia - and to a lesser extent osteoporosis and even osteopenia - has been defined in different ways, so it is not surprising that data on the epidemiology of sarco-osteopenia vary widely from one study to another. Again, the different characteristics of the persons assessed (age, gender, country of origin, etc.) contribute to this variability. For example, in a systematic review published in 2018,<a class="elsevierStyleCrossRef" href="#bib0175">35</a> the prevalence of sarco-osteopenia (T < −1.0) was reported to range from 5 to 37%. In this review, a meta-analysis was conducted including 17 studies. Nine of them were able to estimate the prevalence of sarcopenia in patients with osteoporotic fractures, which was 46% (CI: 44–48; p < 0.001). The relative risk of fracture in sarcopenic vs. non-sarcopenic individuals, calculated based on data from four of the studies, was 1.37 (CI 1.18–1.59, p0_" 0.001). Finally, femoral neck BMD and femoral neck T-score (assessed from five and three studies, respectively) were significantly lower in people with sarcopenia (−0.07 g/cm2 [95% CI: 0.08−0.06] in the former and −0.34 [CI: 0.46−0.23] in the latter).The prevalence of sarcopenic osteoporosis (sarcopenia and T score < −2.5 T) is less well studied. Locquet et al.<a class="elsevierStyleCrossRef" href="#bib0115">23</a> found significantly lower figures than those described for sarco-osteopenia (4.5%). The prevalence of sarcopenic osteoporosis in the Japanese adult population living in the community (osteoporosis + sarcopenia according to AWGS) reached about 5%,<a class="elsevierStyleCrossRef" href="#bib0180">36</a> while in China it was 12.6% in older people with an average age of 75 years.<a class="elsevierStyleCrossRef" href="#bib0185">37</a> In a study conducted in Austria in a geriatric population<a class="elsevierStyleCrossRef" href="#bib0190">38</a> -elderly people over 80 years of age on average- the prevalence of sarcopenic osteoporosis (EGSWOP) was 14.2%, with no gender difference. In the study conducted by our group in Cantabria,<a class="elsevierStyleCrossRef" href="#bib0110">22</a> the prevalence of sarcopenic osteoporosis was 2.8%, closer to the figures of Locquet et al.<a class="elsevierStyleCrossRef" href="#bib0115">23</a> and Yoshimura et al.<a class="elsevierStyleCrossRef" href="#bib0180">36</a> In contrast to other studies,<a class="elsevierStyleCrossRef" href="#bib0195">39</a> we did not find a statistically significant association between sarcopenia and osteoporosis (the OR, adjusted for sex and age, was 1.03 [CI: 0.66–1.62; p = 0.89]), although we did find a relationship between muscle mass and hip BMD. Other authors have found similar relationships between low muscle mass and bone mass,<a class="elsevierStyleCrossRef" href="#bib0200">40</a> as well as between decreased muscle strength and decreased BMD in the spine.<a class="elsevierStyleCrossRef" href="#bib0205">41</a>In our study,<a class="elsevierStyleCrossRef" href="#bib0110">22</a> the prevalence of fractures in patients with sarcopenic osteoporosis was 35.7%, significantly higher than that of patients with sarcopenia without osteoporosis (16.8%; p < 0.01); p < 0.01), but not in of patients with osteoporosis without sarcopenia (26.1%; p = 0.45). Nor did we find significant differences between the prevalence of fractures in patients with sarcopenia (20.6%) and patients without it (15.7%). Therefore, our data do not support that sarcopenia increases the risk of fractures and suggest that the increase in fractures in patients with sarcopenic osteoporosis is mainly due to osteoporosis. In fact, a review of studies on this subject, to which we have already referred,<a class="elsevierStyleCrossRef" href="#bib0100">20</a> shows that the effect of sarcopenia on the development of fractures is controversial, with data published in both directions. Beaudart et al.<a class="elsevierStyleCrossRef" href="#bib0210">42</a> also point out that the evidence for the relationship between sarcopenia and fractures is not consistent. In a recent study involving middle-aged people (interquartile range [IQR]: 51–63 years) from the UK Biobank cohort, with a low prevalence of sarcopenia (0.3%) (EWGSOP 2), the risk of fracture was increased (HR = 1.30 [CI: 1.08–1.56]) in people with sarcopenia, although no significant differences were observed in the risk of major osteoporotic fracture (clinical vertebral, proximal humerus, distal radius or hip fracture) (HR = 1.18 [0.93–1.49]).<a class="elsevierStyleCrossRef" href="#bib0215">43</a> Finally, another recent study of older men from the Osteoporotic Fractures in Men Study (MrOs) cohort, with a follow-up of about six years, found no interaction between bone and muscle in predicting fractures. For the former, total, trabecular and cortical volumetric density and cortical area were assessed by high-resolution peripheral quantitative computed tomography (HR-pQCT), and for the latter, volume and density at the tibia level by HR-pQCT, mass by dilution of labelled creatine (Cr-D3), and strength (fist and legs).<a class="elsevierStyleCrossRef" href="#bib0220">44</a>In recent years there has been increasing concern about the possible association of sarcopenia with obesity, as ageing is associated with a decrease in muscle mass and an increase in fat mass. This has led to the coining of the term 'sarcopenic obesity'. Obesity can have a detrimental effect on muscle by infiltrating it with fat. Impaired muscle function, in turn, can facilitate falls and ultimately increase -at least theoretically- the risk of fractures. Moreover, if sarcopenia tends to be related to osteoporosis on the one hand and obesity on the other, it is conceivable that there is also a tendency for all three conditions to be associated. The term "osteosarcopenic obesity" has been coined to denote the association of obesity, sarcopenia and osteopenia/osteoporosis.The prevalence of sarcopenic obesity is highly variable. A German study<a class="elsevierStyleCrossRef" href="#bib0225">45</a> of women over 70 years of age, using the EWGSOP definition of sarcopenia, found a prevalence of sarcopenic obesity of 0% when obesity was measured by BMI and 2.3% when obesity was measured by percentage of fat mass. A recent study in India<a class="elsevierStyleCrossRef" href="#bib0230">46</a> applying the EWGSOP 2 sarcopenic obesity definition criteria for sarcopenia found a prevalence of sarcopenic obesity in the population over 65 years of age of 3.8% in women and 6.7% in men when obesity was diagnosed by BMI, and 5.7% in women and again 6.7% in men when diagnosed by fat percentage. In a recent systematic review analysing more than 100 studies involving nearly 170,000 older people of both sexes (70.6 ± 7.5 years), the estimated prevalence of sarcopenic obesity was 9%.<a class="elsevierStyleCrossRef" href="#bib0235">47</a>In our study,<a class="elsevierStyleCrossRef" href="#bib0110">22</a> the prevalence of sarcopenic obesity was 1.4% when obesity was diagnosed by BMI and 5.9% when diagnosed by percentage fat mass. Furthermore, the OR for the association between sarcopenia and obesity defined by BMI was 0.18 (p < 0.0001) and 0.58 (p = 0.003) for the association between sarcopenia and obesity defined by percentage fat mass. Therefore, it seems that sarcopenia and obesity tend not to coincide, as if the presence of one reduces the chances of suffering from the other. In the systematic review just discussed,<a class="elsevierStyleCrossRef" href="#bib0235">47</a> an association of obesity with a 34% reduction in the risk of sarcopenia was observed (OR: 0.66, CI: 0.48−0.91, p < 0.001). The authors point out that this lower risk of sarcopenia in obese people may help to explain the so-called "obesity paradox", whereby in certain chronically ill people, obesity is not only not associated with increased mortality, but is associated with decreased mortality.<a class="elsevierStyleCrossRef" href="#bib0240">48</a>On the other hand, in the individuals assessed in the Camargo cohort<a class="elsevierStyleCrossRef" href="#bib0110">22</a> no association between sarcopenia, obesity and osteoporosis (T score < −2.5) was observed when obesity was diagnosed by BMI, while when it was diagnosed by fat percentage, eight individuals were identified in whom all three conditions coincided. This represents a very low prevalence in the population as a whole (0.8%). We are not aware of any studies that have addressed this association. However, data on the association of obesity, sarcopenia and BMD have been published with a T score < −1.0. As expected, the values are higher and, moreover, highly variable, depending on the criteria used to define the various disorders and, on the population, studied.<a class="elsevierStyleCrossRef" href="#bib0245">49</a>ConclusionsThere is a great deal of confusion about the prevalence data for the entities considered, due to the large disparity in the values published by different authors, which is largely explained by the diversity of the criteria used to define them, in addition to the inherent diversity of the populations studied. In our experience, frailty appears to be associated with an increased risk of fractures (which may be related to the associated increase in falls), while the possible association between bone mass and frailty is less clear. The likely association of frailty with fractures may suggest that frailty should be included among the factors to be considered in fracture risk tools. However, given that the strength of the association is not yet well established, and that frailty may be associated with other factors related to the development of fractures, such as falls, studies are needed to ensure the usefulness of such inclusion. On the other hand, although sarcopenia is often associated with lower bone mass in the medical literature, the prevalence of sarcopenic osteoporosis we observed is low, and we did not observe a trend for sarcopenia and osteoporosis to be significantly associated. Nor have we observed that sarcopenia clearly increases the risk of fracture. The prevalence of sarcopenic obesity is also very low, and the frequency of obesity in sarcopenic patients is lower than in the general population (although in a small percentage of cases the opposite is true, resulting in so-called "sarcopenic obesity"). Finally, the coexistence of sarcopenia, osteoporosis and obesity in community-dwelling people is quite unusual.FundingThe study has been partly funded with support from the Institute of Health Carlos III, Ministry of Science and Innovation (PI21/00532) which includes ERDF funds.Ethical considerationsNot required as it is a review.Conflict of interestThe authors declare that they have no conflict of interest." "textoCompletoSecciones" => array:1 [ "secciones" => array:14 [ 0 => array:3 [ "identificador" => "xres2207088" "titulo" => "Abstract" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0005" ] ] ] 1 => array:2 [ "identificador" => "xpalclavsec1851665" "titulo" => "Keywords" ] 2 => array:3 [ "identificador" => "xres2207087" "titulo" => "Resumen" "secciones" => array:1 [ 0 => array:1 [ "identificador" => "abst0010" ] ] ] 3 => array:2 [ "identificador" => "xpalclavsec1851664" "titulo" => "Palabras clave" ] 4 => array:2 [ "identificador" => "sec0005" "titulo" => "Introduction" ] 5 => array:3 [ "identificador" => "sec0010" "titulo" => "Frailty" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0015" "titulo" => "Concept, definition and diagnostic criteria" ] 1 => array:2 [ "identificador" => "sec0020" "titulo" => "Epidemiology and aetiopathogenesis" ] ] ] 6 => array:3 [ "identificador" => "sec0025" "titulo" => "Sarcopenia" "secciones" => array:2 [ 0 => array:2 [ "identificador" => "sec0030" "titulo" => "Concept, definition and diagnostic criteria" ] 1 => array:2 [ "identificador" => "sec0035" "titulo" => "Epidemiology and aetiopathogenesis" ] ] ] 7 => array:2 [ "identificador" => "sec0040" "titulo" => "Relationship between frailty and osteoporosis" ] 8 => array:2 [ "identificador" => "sec0045" "titulo" => "Relationship between sarcopenia and osteoporosis. Sarcopenic obesity" ] 9 => array:2 [ "identificador" => "sec0050" "titulo" => "Conclusions" ] 10 => array:2 [ "identificador" => "sec0055" "titulo" => "Funding" ] 11 => array:2 [ "identificador" => "sec0060" "titulo" => "Ethical considerations" ] 12 => array:2 [ "identificador" => "sec0065" "titulo" => "Conflict of interest" ] 13 => array:1 [ "titulo" => "References" ] ] ] "pdfFichero" => "main.pdf" "tienePdf" => true "fechaRecibido" => "2023-07-16" "fechaAceptado" => "2024-03-07" "PalabrasClave" => array:2 [ "en" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Keywords" "identificador" => "xpalclavsec1851665" "palabras" => array:6 [ 0 => "Frailty" 1 => "Sarcopenia" 2 => "Osteoporosis" 3 => "Obesity" 4 => "Bone mass" 5 => "Fractures" ] ] ] "es" => array:1 [ 0 => array:4 [ "clase" => "keyword" "titulo" => "Palabras clave" "identificador" => "xpalclavsec1851664" "palabras" => array:6 [ 0 => "Fragilidad" 1 => "Sarcopenia" 2 => "Osteoporosis" 3 => "Obesidad" 4 => "Masa ósea" 5 => "Fracturas" ] ] ] ] "tieneResumen" => true "resumen" => array:2 [ "en" => array:2 [ "titulo" => "Abstract" "resumen" => "Frailty, sarcopenia and osteoporosis are entities specific to the elderly, who share some risk factors. For this reason, their relationship has been studied in different works, which have provided disparate results, probably because these studies have not always focused on the same aspects. This article reviews the relationship of frailty and sarcopenia with osteoporosis." ] "es" => array:2 [ "titulo" => "Resumen" "resumen" => "La fragilidad, la sarcopenia y la osteoporosis son entidades propias de las personas de edad avanzada, que comparten algunos factores de riesgo. Por ello, se ha estudiado su relación en distintos trabajos, que han aportado resultados dispares, probablemente porque estos estudios no siempre se han centrado en los mismos aspectos. En este artículo se revisa la relación de la fragilidad y la sarcopenia con la osteoporosis." ] ] "multimedia" => array:4 [ 0 => array:8 [ "identificador" => "fig0005" "etiqueta" => "Figure 1" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr1.jpeg" "Alto" => 1211 "Ancho" => 1200 "Tamanyo" => 128466 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0005" "detalle" => "Figure " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Chart of the aetiopathogenesis of frailty. Adapted from Angulo et al.<a class="elsevierStyleCrossRef" href="#bib0050">10</a>" ] ] 1 => array:8 [ "identificador" => "fig0010" "etiqueta" => "Figure 2" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr2.jpeg" "Alto" => 1108 "Ancho" => 1400 "Tamanyo" => 151573 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0010" "detalle" => "Figure " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Diagnostic algorithm for sarcopenia according to the European Working Group on Sarcopenia in Older People, second version (EWGSOP 2). Adapted from Cruz et al.<a class="elsevierStyleCrossRef" href="#bib0060">12</a> BIA: bioelectrical impedance; DXA: dual energy level X-ray absorptiometry; EWGSOP: European Working Group on Sarcopenia in Older People. SARC-F: Strength Assistance in walking, Rise from chair, Climb stairs, and Falls; TUG: Timed Up and Go." ] ] 2 => array:8 [ "identificador" => "fig0015" "etiqueta" => "Figure 3" "tipo" => "MULTIMEDIAFIGURA" "mostrarFloat" => true "mostrarDisplay" => false "figura" => array:1 [ 0 => array:4 [ "imagen" => "gr3.jpeg" "Alto" => 675 "Ancho" => 1500 "Tamanyo" => 94862 ] ] "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0015" "detalle" => "Figure " "rol" => "short" ] ] "descripcion" => array:1 [ "en" => "Factors involved in the development of sarcopenia. Adapted from Cruz et al.<a class="elsevierStyleCrossRef" href="#bib0060">12</a>" ] ] 3 => array:8 [ "identificador" => "tbl0005" "etiqueta" => "Table 1" "tipo" => "MULTIMEDIATABLA" "mostrarFloat" => true "mostrarDisplay" => false "detalles" => array:1 [ 0 => array:3 [ "identificador" => "at0020" "detalle" => "Table " "rol" => "short" ] ] "tabla" => array:2 [ "leyenda" => "BIA: bioelectrical impedance; DXA: dual energy level X-ray absorptiometry; EWGSOP: European Working Group on Sarcopenia in Older People; SMI: muscle mass index (limb muscle mass/height2); SPPB: Short Physical Performance Battery." "tablatextoimagen" => array:1 [ 0 => array:2 [ "tabla" => array:1 [ 0 => """ <table border="0" frame="\n \t\t\t\t\tvoid\n \t\t\t\t" class=""><thead title="thead"><tr title="table-row"><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Criteria \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Assessment method \t\t\t\t\t\t\n \t\t\t\t\t\t</th><th class="td" title="\n \t\t\t\t\ttable-head\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t" scope="col" style="border-bottom: 2px solid black">Cut-off points \t\t\t\t\t\t\n \t\t\t\t\t\t</th></tr></thead><tbody title="tbody"><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Muscle mass \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">DXA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">SMI: \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Males: 7.23–7.26 g/m2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Females: 5.50–5.67 kg/m2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">SMI: \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">BIA \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Males: 8.87 kg/m2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t"> \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Females: 6.42 kg/m2 \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Muscular strength \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Manual gripping force (dynamometer) \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Males: <30 kg Females: <20 kg \t\t\t\t\t\t\n \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">Physical performance \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">SPPB Walking speed \t\t\t\t\t\t\n \t\t\t\t</td><td class="td" title="\n \t\t\t\t\ttable-entry\n \t\t\t\t " align="left" valign="\n \t\t\t\t\ttop\n \t\t\t\t">SPPB ≤8 4 m distance: <0.8 m/s \t\t\t\t\t\t\n \t\t\t\t</td></tr></tbody></table> """ ] "imagenFichero" => array:1 [ 0 => "xTab3601139.png" ] ] ] ] "descripcion" => array:1 [ "en" => "Cut-off points for diagnosis of sarcopenia proposed by the European Working Group on Sarcopenia in Older People (EWGSOP).<a class="elsevierStyleCrossRef" href="#bib0070">14</a>" ] ] ] "bibliografia" => array:2 [ "titulo" => "References" "seccion" => array:1 [ 0 => array:2 [ "identificador" => "bibs0005" "bibliografiaReferencia" => array:49 [ 0 => array:3 [ "identificador" => "bib0005" "etiqueta" => "1" "referencia" => array:1 [ 0 => array:2 [ "contribucion" => array:1 [ 0 => array:2 [ "titulo" => "La fragilidad, una perspectiva a lo largo del tiempo" "autores" => array:1 [ 0 => array:2 [ "etal" => false "autores" => array:1 [ 0 => "L. 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Frailty, sarcopenia and osteoporosis

Fragilidad, sarcopenia y osteoporosis

José Manuel Olmos Martíneza,b,c,

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josemanuel.olmos@scsalud.es

Corresponding author.

, Paula Hernández Martínezd, Jesús González Macíasb

a Servicio de Medicina Interna, Hospital Universitario Marqués de Valdecilla, Santander, Cantabria, Spain

b Departamento de Medicina y Psiquiatría, Universidad de Cantabria, Santander, Cantabria, Spain

c Instituto de Investigación Valdecilla (IDIVAL), Cantabria, Spain

d Servicio de Medicina Interna, Hospital Sierrallana, Cantabria, Spain

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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Diagnostic algorithm for sarcopenia according to the European Working Group on Sarcopenia in Older People&#44; second version &#40;EWGSOP 2&#41;&#46; Adapted from Cruz et al&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> BIA&#58; bioelectrical impedance&#59; DXA&#58; dual energy level X-ray absorptiometry&#59; EWGSOP&#58; European Working Group on Sarcopenia in Older People&#46;</p> <p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">SARC-F&#58; Strength Assistance in walking&#44; Rise from chair&#44; Climb stairs&#44; and Falls&#59; TUG&#58; Timed Up and Go&#46;</p>"
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    "textoCompleto" => "<span class="elsevierStyleSections"><span id="sec0005" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0025">Introduction</span><p id="par0005" class="elsevierStylePara elsevierViewall">Frailty&#44; understood as physical or systemic frailty&#44; is a syndrome of the elderly that leads to increased mortality and hospitalisation&#46; With age there is also a progressive loss of skeletal muscle mass and strength known as sarcopenia&#46; This disorder is closely related to the pathophysiology of frailty and can also be considered as a geriatric syndrome&#46; On the other hand&#44; osteoporosis&#44; in its involutional form -by far the most common- is a disease of the elderly&#44; particularly affecting women&#46; Two main factors participate in the development of osteoporotic fractures&#58; bone weakness and trauma&#46; Both aspects may be related to sarcopenia and frailty&#46; In fact&#44; this relationship has been studied in a number of studies&#44; which have not always focused on the same aspects&#46; Given the above&#44; there is an interest in clarifying how sarcopenia and frailty are related to osteoporosis&#46;</p></span><span id="sec0010" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0030">Frailty</span><span id="sec0015" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0035">Concept&#44; definition and diagnostic criteria</span><p id="par0010" class="elsevierStylePara elsevierViewall">The term frailty emerged at the end of the last century to describe a clinical syndrome that represents a continuum from the healthy older adult to the extremely vulnerable with high risk of death and low chance of recovery&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> Subsequently&#44; Morley et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0010"><span class="elsevierStyleSup">2</span></a> in 2013 defined frailty as a multidimensional geriatric syndrome&#44; characterised by an increased vulnerability of an individual to develop increased dependency or mortality when exposed to a stressor&#46; More recently&#44; the EU Joint Action 724099&#47;ADVANTAGE<a class="elsevierStyleCrossRef" href="#bib0015"><span class="elsevierStyleSup">3</span></a> has defined frailty as &#34;a state characterised by a progressive decline in physiological systems related to ageing&#44; leading to a reduction in intrinsic capacity&#44; which confers extreme vulnerability to stressors&#44; increasing the risk of various negative health events&#34;&#46; Frailty can be physical&#44; psychosocial or a combination of both&#44; and is a dynamic situation that can improve or worsen over time&#46; There are multiple tools for diagnosing frailty&#44; although the Fried score is probably the most widely used&#46;<a class="elsevierStyleCrossRef" href="#bib0020"><span class="elsevierStyleSup">4</span></a> For these authors&#44; a diagnosis of frailty can be made for people with at least three of the following five criteria&#58; unintentional loss of 4&#46;5&#160;kg of weight or more in the last year&#44; weakness - loss of strength&#44; self-reported feelings of exhaustion or lack of energy&#44; and decreased physical activity and gait speed&#46; When one or two criteria are met&#44; patients are classified as &#34;pre-fragile&#34;&#46; Other diagnostic tools are the Rockwood frailty index&#44;<a class="elsevierStyleCrossRef" href="#bib0025"><span class="elsevierStyleSup">5</span></a> the Frailty Trait Scale &#40;FTS<a class="elsevierStyleCrossRef" href="#bib0030"><span class="elsevierStyleSup">6</span></a> and the FRAIL frailty index&#46;<a class="elsevierStyleCrossRef" href="#bib0035"><span class="elsevierStyleSup">7</span></a></p></span><span id="sec0020" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0040">Epidemiology and aetiopathogenesis</span><p id="par0015" class="elsevierStylePara elsevierViewall">The reported prevalence of frailty is highly variable&#44; due to the different criteria used to define frailty and the characteristics of the persons assessed &#40;age&#44; sex&#44; race&#44; degree of dependency&#44; etc&#46;&#41;&#46; It is higher when using the Rockwood Index and increases exponentially with age&#44; being more common in women than in men by a ratio of 2&#58;1&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a> In a systematic review published a few years ago&#44;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> the prevalence of frailty described in the papers included in the review ranged from 2&#37; to 48&#37;&#44; with an overall prevalence of 18&#37; &#40;confidence interval &#91;CI&#93;&#58; 15 &#37;&#8211;21 &#37;&#41;&#46; This study analysed 68 publications involving more than 10&#44;000 people from different European countries&#46; The characteristics of the persons included &#40;age&#44; sex&#44; origin -community&#44; nursing-homes etc&#46;&#41; and the diagnostic criteria were not homogeneous&#44; although Fried&#39;s criteria were used in slightly more than half of these studies&#46; When only the community population was analysed&#44; not including dependent individuals&#44; the prevalence of frailty was 12&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0040"><span class="elsevierStyleSup">8</span></a> In Spain&#44; the prevalence at community level ranges from 2&#46;5&#37; to 38&#37;&#44; depending on age&#44; sex and criteria applied&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><p id="par0020" class="elsevierStylePara elsevierViewall">In a study carried out by our group in 1&#46;000 people belonging to the Camargo cohort&#44;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> living in the community and with a mean age of 72 years&#44; the prevalence of frailty &#40;using Fried&#39;s criteria&#41; reached 12&#46;1&#37; of the population studied&#44; being higher in women than in men &#40;13&#46;8&#37; vs&#46; 6&#46;8&#37;&#59; p&#160;&#61;&#160;0&#46;01&#41;&#46;</p><p id="par0025" class="elsevierStylePara elsevierViewall">Frailty is a clinical syndrome that affects many systems&#46; There is a clear relationship between frailty&#44; muscle structure and function&#46; However&#44; although sarcopenia appears to be one of the risk factors and sometimes marks the beginning of the process known as the &#34;frailty cycle&#34;&#44; it is important to remember that although they overlap to some extent&#44; they are not entirely coincidental and should be understood as distinct entities&#46; The importance of frailty lies in its association with mortality&#44; disability&#44; falls&#44; hospitalisation or admission to nursing homes&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;3</span></a> Its pathogenesis involves a number of age-related changes affecting several systems&#44; the most prominent of which are cardiovascular&#44; musculoskeletal&#44; respiratory&#44; endocrine &#40;sex hormones&#44; insulin sensitivity&#44; growth hormone &#91;GH&#93;&#44; vitamin D&#41;&#44; and immunological &#40;low-grade inflammation&#41; &#40;<a class="elsevierStyleCrossRef" href="#fig0005">Fig&#46; 1</a>&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a> The role of the central nervous system&#44; although little known&#44; seems to be relevant&#44; and some recent studies suggest the involvement of certain brain areas related to executive functions in the generation of the syndrome&#46;<a class="elsevierStyleCrossRef" href="#bib0005"><span class="elsevierStyleSup">1</span></a></p><elsevierMultimedia ident="fig0005"></elsevierMultimedia></span></span><span id="sec0025" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0045">Sarcopenia</span><span id="sec0030" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0050">Concept&#44; definition and diagnostic criteria</span><p id="par0030" class="elsevierStylePara elsevierViewall">The term sarcopenia - from the Greek <span class="elsevierStyleItalic">sarx</span> &#40;flesh&#41; and <span class="elsevierStyleItalic">penia</span> &#40;poverty&#41; - refers to the loss of muscle mass and strength that occurs during ageing&#46; This term was introduced in 1989 by Irwin Rosenberg to describe the loss of muscle mass that occurs over the years&#46;<a class="elsevierStyleCrossRef" href="#bib0055"><span class="elsevierStyleSup">11</span></a> However&#44; decreased muscle mass alone is not a good predictor of mortality and disability&#46; Thus&#44; in addition to the loss of muscle mass&#44; muscle function was subsequently impaired&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> Sarcopenia is currently included in muscle diseases and is coded as a disease entity in the International Classification of Diseases&#44; 10th edition &#40;ICD-10&#41; since 2016&#46;<a class="elsevierStyleCrossRef" href="#bib0065"><span class="elsevierStyleSup">13</span></a> About 10 years ago&#44; the <span class="elsevierStyleItalic">European Working Group on Sarcopenia in Older People</span> &#40;EWGSOP&#41; established diagnostic criteria based on the measurement of muscle mass&#44; muscle strength and physical performance&#44; which have been widely accepted<a class="elsevierStyleCrossRef" href="#bib0070"><span class="elsevierStyleSup">14</span></a> &#40;<a class="elsevierStyleCrossRef" href="#tbl0005">Table 1</a>&#41;&#46; Sarcopenia is considered to exist when patients have low muscle mass and one of the following two conditions&#58; reduced muscle strength or poor physical performance&#46; If muscle mass is reduced and muscle strength and physical performance are normal&#44; the patient can be diagnosed with &#34;presarcopenia&#34;&#46; When all three parameters are altered&#44; we speak of &#34;severe sarcopenia&#34;&#46; The European Society for Clinical Nutrition and Metabolism &#40;ESPEN&#41; and the Special Interest Groups &#40;SIG<a class="elsevierStyleCrossRef" href="#bib0075"><span class="elsevierStyleSup">15</span></a> have also endorsed these criteria&#46; Another definition is provided by the <span class="elsevierStyleItalic">International Working Group on Sarcopenia</span> &#40;IWGS&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0080"><span class="elsevierStyleSup">16</span></a> which is based on the measurement of muscle mass and gait speed&#46; For the <span class="elsevierStyleItalic">Foundation for the National Institutes of Health</span> &#40;FNIH&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0085"><span class="elsevierStyleSup">17</span></a> the criteria should be based on the presence of low levels of muscle mass and strength&#46;</p><elsevierMultimedia ident="tbl0005"></elsevierMultimedia><p id="par0035" class="elsevierStylePara elsevierViewall">The EWGSOP updated the diagnostic criteria for sarcopenia syndrome in 2019 &#40;EWGSOP 2&#41;&#44;<a class="elsevierStyleCrossRef" href="#bib0090"><span class="elsevierStyleSup">18</span></a> proposing new cut-off points and a stepwise diagnostic approach through an algorithm &#40;<a class="elsevierStyleCrossRef" href="#fig0010">Fig&#46; 2</a>&#41;&#46; Strength is the first parameter to be assessed&#44; and if it is decreased&#44; muscle mass is measured&#44; making a diagnosis of sarcopenia if it is also decreased&#46; If the patient also suffers from poor physical performance&#44; this is referred to as severe sarcopenia&#46; This consensus also contemplates the distinction between primary and secondary sarcopenia&#44; the latter being considered when there are causal factors beyond age&#44; such as inflammatory processes or malignant states&#46; It also refers to acute or chronic sarcopenia&#44; where chronic sarcopenia is defined as sarcopenia that has been present for more than six months&#46;</p><elsevierMultimedia ident="fig0010"></elsevierMultimedia></span><span id="sec0035" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0055">Epidemiology and aetiopathogenesis</span><p id="par0040" class="elsevierStylePara elsevierViewall">As with frailty&#44; published prevalence values for sarcopenia are highly variable and depend on the criteria used for diagnosis&#44; the techniques used to measure the different variables and the profile of the individuals included in the studies&#46; When assessed using the EWGSOP scale&#44; it is estimated to affect 5&#37;&#8211;13&#37; of people between 60&#8211;70 years of age&#46; It is higher in men and increases with age&#46;<a class="elsevierStyleCrossRef" href="#bib0095"><span class="elsevierStyleSup">19</span></a> In a systematic review analysing five studies&#44; the prevalence of sarcopenia according to EWGSOP criteria was 4&#46;3&#37;&#44; 5&#46;6&#37;&#44; 11&#46;2&#37;&#44; 15&#46;9&#37; and 31&#46;9&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> Mayhew et al&#46;<a class="elsevierStyleCrossRef" href="#bib0105"><span class="elsevierStyleSup">21</span></a> found that using the EWGSOP&#47;Asian Working Group for Sarcopenia &#40;AWGS&#41; definition&#44; the estimated prevalence was 12&#46;9&#37; &#40;CI 9&#46;9&#37;&#8211;15&#46;9&#37;&#41;&#46; According to EWGSOP criteria&#44; the prevalence of sarcopenia in our study of the Camargo cohort<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> was 14&#46;1&#37; &#40;13&#46;0&#37; in women and 17&#46;7&#37; in men&#41;&#46; Locquet et al&#46;&#44;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> using criteria comparable to ours and in an age-matched population&#44; established a sarcopenia prevalence of 14&#46;9&#37;&#46;</p><p id="par0045" class="elsevierStylePara elsevierViewall">Studies assessing the incidence of sarcopenia are relatively rare&#44; although the incidence ranges from 1&#46;6 to 3&#46;6&#37; per year using the EWGSOP criteria&#46; As with prevalence&#44; incidence increases with age&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a></p><p id="par0050" class="elsevierStylePara elsevierViewall">Muscle mass and strength&#44; as well as BMD&#44; peak in youth and&#44; after a period of plateau&#44; begin to decline gradually&#46; This loss of muscle mass and strength leads to an increased risk of falls&#44; functional impairment&#44; frailty and mortality&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a></p><p id="par0055" class="elsevierStylePara elsevierViewall">There are many factors that may influence the development of this condition&#44; and they are far from being fully understood &#40;<a class="elsevierStyleCrossRef" href="#fig0015">Fig&#46; 3</a>&#41;&#46; Ageing causes an imbalance between the anabolic and catabolic pathways of muscle proteins&#44; leading to an overall loss of skeletal muscle&#46; Cellular changes in sarcopenic muscle include a reduction in the size and number of myofibrils&#44; particularly affecting type II fibres&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> This loss of fast motor units leads to a decrease in muscle strength which is reflected in the performance of certain movements&#44; such as sitting in a chair&#44; climbing stairs&#44; or maintaining posture after losing balance&#46; In addition&#44; satellite cell dysfunction also appears to be linked to the development of sarcopenia&#46;<a class="elsevierStyleCrossRef" href="#bib0120"><span class="elsevierStyleSup">24</span></a> Several elements are involved in this loss of muscle mass and strength&#44; including environmental and hormonal factors&#44; as well as those related to the muscle and its vascularisation or to the action of certain cytokines and growth factors&#46;<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">12&#44;24</span></a> Finally&#44; some studies suggest that the intercommunication between muscle and bone is mediated by endocrine factors&#44; such as myostatin&#44; irisin&#44; osteocalcin and many others&#44; although the relevance of this communication in the pathogenesis of sarcopenia is not fully understood&#46;<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">12&#44;25</span></a></p><elsevierMultimedia ident="fig0015"></elsevierMultimedia></span></span><span id="sec0040" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0060">Relationship between frailty and osteoporosis</span><p id="par0060" class="elsevierStylePara elsevierViewall">Although we know that frailty and osteoporosis share risk factors &#40;age&#44; low body mass index &#91;BMI&#93;&#44; sedentary lifestyle&#44; unbalanced nutrition&#44; polypharmacy&#44; etc&#46;&#41; the exact relationship between them is not well defined&#46;<a class="elsevierStyleCrossRef" href="#bib0130"><span class="elsevierStyleSup">26</span></a> This is due&#44; at least in part&#44; to the different criteria used to define frailty and osteoporosis&#44; and the heterogeneity of the populations in which they have been studied&#46;</p><p id="par0065" class="elsevierStylePara elsevierViewall">Systemic frailty is considered to be a risk factor for fracture&#44; probably due to the increase in falls it entails&#46;<a class="elsevierStyleCrossRefs" href="#bib0005"><span class="elsevierStyleSup">1&#44;26</span></a> Therefore&#44; some of the studies have looked at the relationship with fractures in general&#46; For example&#44; in a systematic review that included six studies involving a total of about 100&#46;000 people&#44; frailty was found to be a significant predictor of future fractures among community-dwelling older people &#40;<span class="elsevierStyleItalic">odds ratio</span> &#91;OR&#93;&#58; 1&#46;70&#44; CI&#58; 1&#46;34&#8211;2&#46;15&#44; p&#160;&#60;&#160;0&#46;0001&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0135"><span class="elsevierStyleSup">27</span></a> Another paper using data from the Canadian Multicentre Osteoporosis Study &#40;CaMos&#41; found a significant hazard ratio &#40;HR&#41; of 1&#46;18 for hip fractures and 1&#46;30 for clinical vertebral fractures for each 0&#46;10 increase in the frailty index&#46;<a class="elsevierStyleCrossRef" href="#bib0140"><span class="elsevierStyleSup">28</span></a></p><p id="par0070" class="elsevierStylePara elsevierViewall">In a recent study of more than 25&#44;000 people in the Canadian Longitudinal Study on Aging &#40;CLSA&#41;&#44; frailty&#44; as assessed by the Rockwood index&#44; was independently associated with fracture incidence over three years of follow-up&#46;<a class="elsevierStyleCrossRef" href="#bib0145"><span class="elsevierStyleSup">29</span></a> In fact&#44; some authors have proposed that the frailty index would be comparable to the FRAX tool in predicting the risk of major osteoporotic and hip fractures&#44; so that assessment of the degree of frailty could help to evaluate the risk of fracture in the elderly&#46;<a class="elsevierStyleCrossRef" href="#bib0150"><span class="elsevierStyleSup">30</span></a></p><p id="par0075" class="elsevierStylePara elsevierViewall">We observed a prevalence of osteoporotic fractures of 22&#46;5&#37; in frail people and 15&#46;6&#37; in non-frail people in the 1&#44;000 people studied in our Camargo cohort study&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> On the other hand&#44; 16&#46;5&#37; of those with osteoporotic fractures and 11&#46;1&#37; of those without fractures were frail&#46; The OR&#44; adjusted for age and sex&#44; was 1&#46;57 &#40;CI&#58; 0&#46;99&#8211;2&#46;51&#41;&#44; at the limit of statistical significance &#40;p&#160;&#61;&#160;0&#46;056&#41;&#46;</p><p id="par0080" class="elsevierStylePara elsevierViewall">The results were less conclusive when the association sought was not that of frailty status with the development of fractures&#44; but rather frailty with bone mineral density &#40;BMD&#41;&#46; Sternberg et al&#46;<a class="elsevierStyleCrossRef" href="#bib0155"><span class="elsevierStyleSup">31</span></a> assessed frailty using Fried&#39;s criteria or the <span class="elsevierStyleItalic">Vulnerable Elders Survey</span> &#40;VES-13&#41; and found no significant association with BMD at baseline &#40;although&#44; interestingly&#44; they found a significant association with the decrease in BMD observed after one year&#41;&#46; Frisoli et al&#46;<a class="elsevierStyleCrossRef" href="#bib0160"><span class="elsevierStyleSup">32</span></a> also found no association with frailty in a population of people with osteopenia or osteoporosis&#46; One study has estimated subjectively assessed frailty&#44;<a class="elsevierStyleCrossRef" href="#bib0165"><span class="elsevierStyleSup">33</span></a> without finding an association with BMD&#44; but with hip fracture&#46; In contrast&#44; Kenny et al&#46;<a class="elsevierStyleCrossRef" href="#bib0170"><span class="elsevierStyleSup">34</span></a> have found associations between BMD and two of the components of frailty&#44; namely grip strength and gait speed&#46;</p><p id="par0085" class="elsevierStylePara elsevierViewall">In our study of the Camargo cohort mentioned above&#44;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a> we observed that the prevalence of densitometric osteoporosis in people with frailty was 21&#46;7&#37;&#44; and in people without frailty&#44; 20&#46;2&#37;&#46; Conversely&#44; frailty was present in 12&#46;7&#37; of patients with osteoporosis and 11&#46;8&#37; of those without&#46; The OR was far from significant &#40;p&#160;&#61;&#160;0&#46;71&#41;&#44; thus no association between frailty and osteoporosis was observed&#46; Consistent with this&#44; there were also no significant differences between BMD values of frail and non-frail patients&#46;<a class="elsevierStyleCrossRef" href="#bib0045"><span class="elsevierStyleSup">9</span></a></p><p id="par0090" class="elsevierStylePara elsevierViewall">Therefore&#44; despite the heterogeneity of the studies&#44; the existence of frailty appears to be associated with an increased risk of fractures&#44; while the possible association between bone mass and frailty is less clear&#46;</p></span><span id="sec0045" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0065">Relationship between sarcopenia and osteoporosis&#46; Sarcopenic obesity</span><p id="par0095" class="elsevierStylePara elsevierViewall">Sarcopenia and osteoporosis may equally coincide because both are associated with ageing&#44; but also because they may have other common aetiological factors &#40;e&#46;g&#46; physical inactivity&#41; and even because muscle changes may have an impact on bone and vice versa&#46;<a class="elsevierStyleCrossRef" href="#bib0125"><span class="elsevierStyleSup">25</span></a> This has led to consider the existence of a mixed syndrome encompassing the two processes&#46; Some authors have suggested the term &#34;sarco-osteopenia&#34; or &#8220;osteosarcopenia&#8221; to designate a disorder characterised by the coexistence of sarcopenia and bone mass with a T-score &#60;&#160;&#8722;1&#46;0 &#40;osteopenia and osteoporosis&#41;&#46; On the other hand&#44; other authors only consider patients with sarcopenia and osteoporosis &#40;T &#60; &#8722;2&#44;5&#41;&#44;<a class="elsevierStyleCrossRefs" href="#bib0060"><span class="elsevierStyleSup">12&#44;22</span></a> to whom the term &#34;sarco-osteopenia&#34; should not be applied&#44; but rather &#34;sarcopenic osteoporosis&#34;&#46;</p><p id="par0100" class="elsevierStylePara elsevierViewall">We have already noted that sarcopenia - and to a lesser extent osteoporosis and even osteopenia - has been defined in different ways&#44; so it is not surprising that data on the epidemiology of sarco-osteopenia vary widely from one study to another&#46; Again&#44; the different characteristics of the persons assessed &#40;age&#44; gender&#44; country of origin&#44; etc&#46;&#41; contribute to this variability&#46; For example&#44; in a systematic review published in 2018&#44;<a class="elsevierStyleCrossRef" href="#bib0175"><span class="elsevierStyleSup">35</span></a> the prevalence of sarco-osteopenia &#40;T &#60; &#8722;1&#46;0&#41; was reported to range from 5 to 37&#37;&#46; In this review&#44; a meta-analysis was conducted including 17 studies&#46; Nine of them were able to estimate the prevalence of sarcopenia in patients with osteoporotic fractures&#44; which was 46&#37; &#40;CI&#58; 44&#8211;48&#59; p &#60;&#160;0&#46;001&#41;&#46; The relative risk of fracture in sarcopenic vs&#46; non-sarcopenic individuals&#44; calculated based on data from four of the studies&#44; was 1&#46;37 &#40;CI 1&#46;18&#8211;1&#46;59&#44; p0&#95;&#34;&#160;0&#46;001&#41;&#46; Finally&#44; femoral neck BMD and femoral neck T-score &#40;assessed from five and three studies&#44; respectively&#41; were significantly lower in people with sarcopenia &#40;&#8722;0&#46;07&#160;g&#47;cm<span class="elsevierStyleSup">2</span> &#91;95&#37; CI&#58; 0&#46;08&#8722;0&#46;06&#93; in the former and &#8722;0&#46;34 &#91;CI&#58; 0&#46;46&#8722;0&#46;23&#93; in the latter&#41;&#46;</p><p id="par0105" class="elsevierStylePara elsevierViewall">The prevalence of sarcopenic osteoporosis &#40;sarcopenia and T score &#60; &#8722;2&#46;5&#160;T&#41; is less well studied&#46; Locquet et al&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> found significantly lower figures than those described for sarco-osteopenia &#40;4&#46;5&#37;&#41;&#46; The prevalence of sarcopenic osteoporosis in the Japanese adult population living in the community &#40;osteoporosis&#160;&#43;&#160;sarcopenia according to AWGS&#41; reached about 5&#37;&#44;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">36</span></a> while in China it was 12&#46;6&#37; in older people with an average age of 75 years&#46;<a class="elsevierStyleCrossRef" href="#bib0185"><span class="elsevierStyleSup">37</span></a> In a study conducted in Austria in a geriatric population<a class="elsevierStyleCrossRef" href="#bib0190"><span class="elsevierStyleSup">38</span></a> -elderly people over 80 years of age on average- the prevalence of sarcopenic osteoporosis &#40;EGSWOP&#41; was 14&#46;2&#37;&#44; with no gender difference&#46; In the study conducted by our group in Cantabria&#44;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> the prevalence of sarcopenic osteoporosis was 2&#46;8&#37;&#44; closer to the figures of Locquet et al&#46;<a class="elsevierStyleCrossRef" href="#bib0115"><span class="elsevierStyleSup">23</span></a> and Yoshimura et al&#46;<a class="elsevierStyleCrossRef" href="#bib0180"><span class="elsevierStyleSup">36</span></a> In contrast to other studies&#44;<a class="elsevierStyleCrossRef" href="#bib0195"><span class="elsevierStyleSup">39</span></a> we did not find a statistically significant association between sarcopenia and osteoporosis &#40;the OR&#44; adjusted for sex and age&#44; was 1&#46;03 &#91;CI&#58; 0&#46;66&#8211;1&#46;62&#59; p&#160;&#61;&#160;0&#46;89&#93;&#41;&#44; although we did find a relationship between muscle mass and hip BMD&#46; Other authors have found similar relationships between low muscle mass and bone mass&#44;<a class="elsevierStyleCrossRef" href="#bib0200"><span class="elsevierStyleSup">40</span></a> as well as between decreased muscle strength and decreased BMD in the spine&#46;<a class="elsevierStyleCrossRef" href="#bib0205"><span class="elsevierStyleSup">41</span></a></p><p id="par0110" class="elsevierStylePara elsevierViewall">In our study&#44;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> the prevalence of fractures in patients with sarcopenic osteoporosis was 35&#46;7&#37;&#44; significantly higher than that of patients with sarcopenia without osteoporosis &#40;16&#46;8&#37;&#59; p &#60;&#160;0&#46;01&#41;&#59; p &#60;&#160;0&#46;01&#41;&#44; but not in of patients with osteoporosis without sarcopenia &#40;26&#46;1&#37;&#59; p&#160;&#61;&#160;0&#46;45&#41;&#46; Nor did we find significant differences between the prevalence of fractures in patients with sarcopenia &#40;20&#46;6&#37;&#41; and patients without it &#40;15&#46;7&#37;&#41;&#46; Therefore&#44; our data do not support that sarcopenia increases the risk of fractures and suggest that the increase in fractures in patients with sarcopenic osteoporosis is mainly due to osteoporosis&#46; In fact&#44; a review of studies on this subject&#44; to which we have already referred&#44;<a class="elsevierStyleCrossRef" href="#bib0100"><span class="elsevierStyleSup">20</span></a> shows that the effect of sarcopenia on the development of fractures is controversial&#44; with data published in both directions&#46; Beaudart et al&#46;<a class="elsevierStyleCrossRef" href="#bib0210"><span class="elsevierStyleSup">42</span></a> also point out that the evidence for the relationship between sarcopenia and fractures is not consistent&#46; In a recent study involving middle-aged people &#40;interquartile range &#91;IQR&#93;&#58; 51&#8211;63 years&#41; from the <span class="elsevierStyleItalic">UK Biobank</span> cohort&#44; with a low prevalence of sarcopenia &#40;0&#46;3&#37;&#41; &#40;EWGSOP 2&#41;&#44; the risk of fracture was increased &#40;HR&#160;&#61;&#160;1&#46;30 &#91;CI&#58; 1&#46;08&#8211;1&#46;56&#93;&#41; in people with sarcopenia&#44; although no significant differences were observed in the risk of major osteoporotic fracture &#40;clinical vertebral&#44; proximal humerus&#44; distal radius or hip fracture&#41; &#40;HR&#160;&#61;&#160;1&#46;18 &#91;0&#46;93&#8211;1&#46;49&#93;&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0215"><span class="elsevierStyleSup">43</span></a> Finally&#44; another recent study of older men from the Osteoporotic Fractures in Men Study &#40;MrOs&#41; cohort&#44; with a follow-up of about six years&#44; found no interaction between bone and muscle in predicting fractures&#46; For the former&#44; total&#44; trabecular and cortical volumetric density and cortical area were assessed by high-resolution peripheral quantitative computed tomography &#40;HR-pQCT&#41;&#44; and for the latter&#44; volume and density at the tibia level by HR-pQCT&#44; mass by dilution of labelled creatine &#40;Cr-D3&#41;&#44; and strength &#40;fist and legs&#41;&#46;<a class="elsevierStyleCrossRef" href="#bib0220"><span class="elsevierStyleSup">44</span></a></p><p id="par0115" class="elsevierStylePara elsevierViewall">In recent years there has been increasing concern about the possible association of sarcopenia with obesity&#44; as ageing is associated with a decrease in muscle mass and an increase in fat mass&#46; This has led to the coining of the term &#39;sarcopenic obesity&#39;&#46; Obesity can have a detrimental effect on muscle by infiltrating it with fat&#46; Impaired muscle function&#44; in turn&#44; can facilitate falls and ultimately increase -at least theoretically- the risk of fractures&#46; Moreover&#44; if sarcopenia tends to be related to osteoporosis on the one hand and obesity on the other&#44; it is conceivable that there is also a tendency for all three conditions to be associated&#46; The term &#34;osteosarcopenic obesity&#34; has been coined to denote the association of obesity&#44; sarcopenia and osteopenia&#47;osteoporosis&#46;</p><p id="par0120" class="elsevierStylePara elsevierViewall">The prevalence of sarcopenic obesity is highly variable&#46; A German study<a class="elsevierStyleCrossRef" href="#bib0225"><span class="elsevierStyleSup">45</span></a> of women over 70 years of age&#44; using the EWGSOP definition of sarcopenia&#44; found a prevalence of sarcopenic obesity of 0&#37; when obesity was measured by BMI and 2&#46;3&#37; when obesity was measured by percentage of fat mass&#46; A recent study in India<a class="elsevierStyleCrossRef" href="#bib0230"><span class="elsevierStyleSup">46</span></a> applying the EWGSOP 2 sarcopenic obesity definition criteria for sarcopenia found a prevalence of sarcopenic obesity in the population over 65 years of age of 3&#46;8&#37; in women and 6&#46;7&#37; in men when obesity was diagnosed by BMI&#44; and 5&#46;7&#37; in women and again 6&#46;7&#37; in men when diagnosed by fat percentage&#46; In a recent systematic review analysing more than 100 studies involving nearly 170&#44;000 older people of both sexes &#40;70&#46;6&#160;&#177;&#160;7&#46;5 years&#41;&#44; the estimated prevalence of sarcopenic obesity was 9&#37;&#46;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">47</span></a></p><p id="par0125" class="elsevierStylePara elsevierViewall">In our study&#44;<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> the prevalence of sarcopenic obesity was 1&#46;4&#37; when obesity was diagnosed by BMI and 5&#46;9&#37; when diagnosed by percentage fat mass&#46; Furthermore&#44; the OR for the association between sarcopenia and obesity defined by BMI was 0&#46;18 &#40;p &#60;&#160;0&#46;0001&#41; and 0&#46;58 &#40;p&#160;&#61;&#160;0&#46;003&#41; for the association between sarcopenia and obesity defined by percentage fat mass&#46; Therefore&#44; it seems that sarcopenia and obesity tend not to coincide&#44; as if the presence of one reduces the chances of suffering from the other&#46; In the systematic review just discussed&#44;<a class="elsevierStyleCrossRef" href="#bib0235"><span class="elsevierStyleSup">47</span></a> an association of obesity with a 34&#37; reduction in the risk of sarcopenia was observed &#40;OR&#58; 0&#46;66&#44; CI&#58; 0&#46;48&#8722;0&#46;91&#44; p &#60;&#160;0&#46;001&#41;&#46; The authors point out that this lower risk of sarcopenia in obese people may help to explain the so-called &#34;obesity paradox&#34;&#44; whereby in certain chronically ill people&#44; obesity is not only not associated with increased mortality&#44; but is associated with decreased mortality&#46;<a class="elsevierStyleCrossRef" href="#bib0240"><span class="elsevierStyleSup">48</span></a></p><p id="par0130" class="elsevierStylePara elsevierViewall">On the other hand&#44; in the individuals assessed in the Camargo cohort<a class="elsevierStyleCrossRef" href="#bib0110"><span class="elsevierStyleSup">22</span></a> no association between sarcopenia&#44; obesity and osteoporosis &#40;T score &#60; &#8722;2&#46;5&#41; was observed when obesity was diagnosed by BMI&#44; while when it was diagnosed by fat percentage&#44; eight individuals were identified in whom all three conditions coincided&#46; This represents a very low prevalence in the population as a whole &#40;0&#46;8&#37;&#41;&#46; We are not aware of any studies that have addressed this association&#46; However&#44; data on the association of obesity&#44; sarcopenia and BMD have been published with a T score &#60; &#8722;1&#46;0&#46; As expected&#44; the values are higher and&#44; moreover&#44; highly variable&#44; depending on the criteria used to define the various disorders and&#44; on the population&#44; studied&#46;<a class="elsevierStyleCrossRef" href="#bib0245"><span class="elsevierStyleSup">49</span></a></p></span><span id="sec0050" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0070">Conclusions</span><p id="par0135" class="elsevierStylePara elsevierViewall">There is a great deal of confusion about the prevalence data for the entities considered&#44; due to the large disparity in the values published by different authors&#44; which is largely explained by the diversity of the criteria used to define them&#44; in addition to the inherent diversity of the populations studied&#46; In our experience&#44; frailty appears to be associated with an increased risk of fractures &#40;which may be related to the associated increase in falls&#41;&#44; while the possible association between bone mass and frailty is less clear&#46; The likely association of frailty with fractures may suggest that frailty should be included among the factors to be considered in fracture risk tools&#46; However&#44; given that the strength of the association is not yet well established&#44; and that frailty may be associated with other factors related to the development of fractures&#44; such as falls&#44; studies are needed to ensure the usefulness of such inclusion&#46; On the other hand&#44; although sarcopenia is often associated with lower bone mass in the medical literature&#44; the prevalence of sarcopenic osteoporosis we observed is low&#44; and we did not observe a trend for sarcopenia and osteoporosis to be significantly associated&#46; Nor have we observed that sarcopenia clearly increases the risk of fracture&#46; The prevalence of sarcopenic obesity is also very low&#44; and the frequency of obesity in sarcopenic patients is lower than in the general population &#40;although in a small percentage of cases the opposite is true&#44; resulting in so-called &#34;sarcopenic obesity&#34;&#41;&#46; Finally&#44; the coexistence of sarcopenia&#44; osteoporosis and obesity in community-dwelling people is quite unusual&#46;</p></span><span id="sec0055" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0075">Funding</span><p id="par0140" class="elsevierStylePara elsevierViewall">The study has been partly funded with support from the <span class="elsevierStyleGrantSponsor" id="gs0005">Institute of Health Carlos III&#44; Ministry of Science and Innovation</span> &#40;<span class="elsevierStyleGrantNumber" refid="gs0005">PI21&#47;00532</span>&#41; which includes ERDF funds&#46;</p></span><span id="sec0060" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0080">Ethical considerations</span><p id="par0145" class="elsevierStylePara elsevierViewall">Not required as it is a review&#46;</p></span><span id="sec0065" class="elsevierStyleSection elsevierViewall"><span class="elsevierStyleSectionTitle" id="sect0085">Conflict of interest</span><p id="par0150" class="elsevierStylePara elsevierViewall">The authors declare that they have no conflict of interest&#46;</p></span></span>"
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          "titulo" => "Introduction"
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          "titulo" => "Frailty"
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              "titulo" => "Concept&#44; definition and diagnostic criteria"
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              "titulo" => "Epidemiology and aetiopathogenesis"
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          "titulo" => "Sarcopenia"
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              "titulo" => "Concept&#44; definition and diagnostic criteria"
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              "titulo" => "Epidemiology and aetiopathogenesis"
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          "titulo" => "Relationship between frailty and osteoporosis"
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        8 => array:2 [
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          "titulo" => "Relationship between sarcopenia and osteoporosis&#46; Sarcopenic obesity"
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          "titulo" => "Conclusions"
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            1 => "Sarcopenia"
            2 => "Osteoporosis"
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            1 => "Sarcopenia"
            2 => "Osteoporosis"
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            4 => "Masa &#243;sea"
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        "resumen" => "<span id="abst0005" class="elsevierStyleSection elsevierViewall"><p id="spar0035" class="elsevierStyleSimplePara elsevierViewall">Frailty&#44; sarcopenia and osteoporosis are entities specific to the elderly&#44; who share some risk factors&#46; For this reason&#44; their relationship has been studied in different works&#44; which have provided disparate results&#44; probably because these studies have not always focused on the same aspects&#46; This article reviews the relationship of frailty and sarcopenia with osteoporosis&#46;</p></span>"
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        "titulo" => "Resumen"
        "resumen" => "<span id="abst0010" class="elsevierStyleSection elsevierViewall"><p id="spar0040" class="elsevierStyleSimplePara elsevierViewall">La fragilidad&#44; la sarcopenia y la osteoporosis son entidades propias de las personas de edad avanzada&#44; que comparten algunos factores de riesgo&#46; Por ello&#44; se ha estudiado su relaci&#243;n en distintos trabajos&#44; que han aportado resultados dispares&#44; probablemente porque estos estudios no siempre se han centrado en los mismos aspectos&#46; En este art&#237;culo se revisa la relaci&#243;n de la fragilidad y la sarcopenia con la osteoporosis&#46;</p></span>"
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          "en" => "<p id="spar0005" class="elsevierStyleSimplePara elsevierViewall">Chart of the aetiopathogenesis of frailty&#46; Adapted from Angulo et al&#46;<a class="elsevierStyleCrossRef" href="#bib0050"><span class="elsevierStyleSup">10</span></a></p>"
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          "en" => "<p id="spar0010" class="elsevierStyleSimplePara elsevierViewall">Diagnostic algorithm for sarcopenia according to the European Working Group on Sarcopenia in Older People&#44; second version &#40;EWGSOP 2&#41;&#46; Adapted from Cruz et al&#46;<a class="elsevierStyleCrossRef" href="#bib0060"><span class="elsevierStyleSup">12</span></a> BIA&#58; bioelectrical impedance&#59; DXA&#58; dual energy level X-ray absorptiometry&#59; EWGSOP&#58; European Working Group on Sarcopenia in Older People&#46;</p> <p id="spar0015" class="elsevierStyleSimplePara elsevierViewall">SARC-F&#58; Strength Assistance in walking&#44; Rise from chair&#44; Climb stairs&#44; and Falls&#59; TUG&#58; Timed Up and Go&#46;</p>"
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          "leyenda" => "<p id="spar0030" class="elsevierStyleSimplePara elsevierViewall">BIA&#58; bioelectrical impedance&#59; DXA&#58; dual energy level X-ray absorptiometry&#59; EWGSOP&#58; European Working Group on Sarcopenia in Older People&#59; SMI&#58; muscle mass index &#40;limb muscle mass&#47;height<span class="elsevierStyleSup">2</span>&#41;&#59; SPPB&#58; Short Physical Performance Battery&#46;</p>"
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                  \t\t\t\t">Males&#58; 7&#46;23&#8211;7&#46;26&#160;g&#47;m<span class="elsevierStyleSup">2</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Females&#58; 5&#46;50&#8211;5&#46;67&#160;kg&#47;m<span class="elsevierStyleSup">2</span>&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">SMI&#58;&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
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                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">BIA&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t</td></tr><tr title="table-row"><td class="td-with-role" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Females&#58; 6&#46;42&#160;kg&#47;m<span class="elsevierStyleSup">2</span>&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Muscular strength&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">Males&#58; &#60;30 kg Females&#58; &#60;20 kg&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t ; entry_with_role_rowhead " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">Physical performance&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td><td class="td" title="\n
                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
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                  \t\t\t\t">SPPB Walking speed&nbsp;\t\t\t\t\t\t\n
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                  \t\t\t\t\ttable-entry\n
                  \t\t\t\t  " align="left" valign="\n
                  \t\t\t\t\ttop\n
                  \t\t\t\t">SPPB &#8804;8 4 m distance&#58; &#60;0&#46;8&#160;m&#47;s&nbsp;\t\t\t\t\t\t\n
                  \t\t\t\t</td></tr></tbody></table>
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Article information

ISSN: 23870206
Original language: English

DOI:10.1016/j.medcle.2024.03.004

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