Skeletal Muscle Mass Indices in
Healthy Adults
Heliodoro Alema´n-Mateo1 and Roxana E. Ruiz Valenzuela2
1
Departamento de Nutricio´n y Metabolismo, Coordinacio´n de Nutricio´n, Centro de
Investigacio´n en Alimentacio´n y Desarrollo (CIAD), A.C. Hermosillo, Sonora, Me´xico
2
Departamento de Salud, Universidad Iberoamericana, Ciudad de Me´xico-Tijuana, Tijuana,
Baja California, Me´xico
INTRODUCTION
Skeletal muscle (SM) increases during postnatal development through a process of
hypertrophy of the individual muscle fibers; a similar process may be induced in adult
SM in response to contractile activity like strength exercises, and to androgens and
β-adrenergic agonists [1]. SM remains relatively constant during the third and fourth decades of life but begins to decline at B45 years of age in both genders [2]. In other words,
age exerts a strong influence on SM, but gender does as well [38]. Several studies have
demonstrated the effects of age and gender on SM, and some have examined the effects
on its distribution [2,56]. Perhaps the most relevant study on this issue was published by
Janssen et al. [2], who used an in vivo method to study body composition using, particularly, magnetic resonance imaging (MRI) to provide precise and reliable measurements of
SM and its distribution in a broad sample of Caucasian men and women. The results of
this study reported new findings on the behavior of SM mass during the lifecycle in both
men and women subjects.
Due to the growing awareness of the importance of SM on functionality and other clinical entities in older age groups [916], there is a need to establish reference values for relative SM in young adult populations using the most precise and accurate methods
available, and considering the factors of age, gender, and ethnicity. It is important to stress
that few countries have been able to conduct national-level studies of this kind [10,1719].
Some published works based on small samples of healthy young adult subjects reported
data on SM [2,6,2021] and proposed cutoff points for diagnosing sarcopenia—i.e., low
SM mass—and sarcopenia syndrome [9,10,17,2242]. To our knowledge, 21 cutoff points
3
Nutrition and Skeletal Muscle
DOI: https://doi.org/10.1016/B978-0-12-810422-4.00001-4 © 2019 Elsevier Inc. All rights reserved.
based on SM exist; specifically, 17 dual-energy X-ray absorptiometry (DXA)-derived
appendicular skeletal muscle mass (ASM) indices, 3 DXA-derived total SM (TSM) indices,
and one DXA-derived total lean body mass (LBM) index for younger adult populations
around the world [9,17,2236], together with seven indices derived from bioelectrical
impedance analysis (BIA) [10,3742], one that used an ultrasound technique [43], and one
MRI-derived TSM index (TSMI) [19]. Before presenting the main results of the published
ASM, TSM, and LBM indices, we will first review the biological bases that underlie them.
THE BIOLOGICAL BASES THAT UNDERLIE THE INDICES
Indices are association measurements that can be very useful in classifying nutritional
status or, as in the present case, the stadia of SM, evaluating the chronicity of the skeletal
muscle loss and assessing the efficacy of nutrition on loss of SM during the intervention
therapy. They may also serve to quantify various components of body mass. Indices of this
kind are usually divided into (1) those relative to weight and height and (2) those relative to
body composition. SM indices are the ones most closely related to body composition that
are used to diagnose presarcopenia and sarcopenia syndrome in geriatric populations. As
mentioned above, SM tissue is dependent on age, gender, body weight, height, and ethnicity
[2,56]. It is important to note that much of our current understanding of SM is based on
studies that used DXA and MRI, two in vivo methods for analyzing body composition
[2,56] that can accurately measure total or regional SM. DXA- derived lean tissue in arms
and legs or ASM account for .75% of total SM [44], which constitutes the primary portion
of SM involved in ambulation, physical activities, and functionality across the lifespan.
To clarify the origin of an index, particularly ASM, we examined the main findings
reported by Gallagher et al. [6], who assessed SM components by DXA in 148 healthy
adult women (80 African-Americans, 68 Caucasians) and 136 healthy adult men (72
African-Americans, 64 Caucasians) with an age range of 21.167.5 years. First, they noted
a significant negative correlation between ASM and age in all four groups. After adjusting
for age, they determined that ASM was significantly and positively correlated with body
weight and height in both ethnic groups, and in both men and women. Using multiple
regression models, they then explored the independent effects of height, weight, age, gender, and ethnicity on ASM. In their predicted ASM model, height and weight explained
64% and 67%, respectively, of ASM variance in the African-American and Caucasian
women, and 63% and 39%, respectively, in the African-American and Caucasian men.
Smaller contributions were found for age. Interestingly, after adjusting for height, body
weight, and age, an effect of gender was also found, as the men were found to have
greater ASM than the women in both groups of subjects across the entire age range.
Finally, a significant effect of ethnicity on ASM was found, as the African-American men
and women had greater adjusted ASM than the Caucasian subjects [6].
Three years later, Janssen et al. [2] examined the influence of age, gender, body weight,
and height on TSM assessed by whole body MRI in a large, heterogeneous sample of 468
men and women aged 1888 years. It is important to mention that this study included
two additional ethnic groups—Asians and Hispanics—in assessing TSM and its distribution [2]. As in the case of Gallagher et al. [6], these researchers also reported a significant
4 1. SKELETAL MUSCLE MASS INDICES IN HEALTHY ADULTS
I. GENERAL ASPECTS: SKELETAL MUSCLE PHYSIOLOGY AND NUTRITION
effect of height, body weight, age, and gender on total and regional or appendicular SM.
In another significant finding related to this chapter, Janssen et al. [2], demonstrated that
the substantial increase in body weight observed between 18 and 40 years of age was not
associated with a corresponding increase in TSM. Instead, the absolute quantity of TSM
was maintained into the fifth decade of life, but with noticeable losses thereafter. This finding is important so as not to limit the cutoff points for SM mass indices for people aged
1840 years, as was originally proposed in Rosseta’s study [6], and the body composition
reference values from National Health and Nutrition Examination Survey [17] or Korean
studies [29,3334].
Numerous body composition indices have been generated by considering the biological
and statistical associations among certain aspects of body composition with age, and specific anthropometric variables; especially, the strong correlation between absolute SM and
height. Originally, in order to define low SM mass or sarcopenia, it was necessary to have
a measure related to the amount of existing SM [9], and as previously mentioned, the
absolute values of SM correlates strongly with height. Therefore, ASM (kg) divided by
height squared (ht2
) produces an index of relative appendicular SM mass that serves as an
indicator of muscularity. In fact, Baumgartner et al. [9] established that placing ht2 in the
denominator constituted the best common power for minimizing the correlation of the
index with height across all gender, ethnic and age groups, and study populations, since
adjusting TSM or ASM for size eliminates the differences in the amount of SM associated
with the greater height of young adults, as well as those related to gender and ethnicity.
The resulting index permits better comparisons than absolute values of SM or any other
parameter of body composition.
SM has also been adjusted by body weight following the same principle as adjustment
by ht2
. Following Janssen et al. [10], SM adjusted by body weight considered adjustments
for both stature and the mass of non-SM tissues (i.e., fat, organs, and bones) under the
assumption that most mobility tasks and daily living activities are strongly influenced by
body size. In older people, in addition to the adjustment by height, SM has also been
adjusted by fat mass. Originally, it was hypothesized that SM adjusted by height and fat
mass would better identify subjects with sarcopenia or with low SM than an index
adjusted only for ht2 and that individuals so identified as such might be at even greater
risk for poor lower extremity functioning [45].
With respect to the adjustments of absolute SM values by ht2
, body weight, fat mass, or
body mass index, a debate is ongoing as to which of these different indices is the best SM
parameter and, therefore, the one that should be included in the criteria to define sarcopenia. Based on their results, Han et al. [42] proposed using absolute SM adjusted by height,
because it correlated more closely with grip strength and with better muscular function
than SM adjusted by body weight. Therefore, they recommended utilizing SM adjusted by
height to diagnose sarcopenia syndrome.
To the best of our knowledge, no established cutoff points adequately identify the level
at which relative SM becomes deficient or low SM. In the most recent international consensus on the operational definition of presarcopenia and sarcopenia syndrome by the
European Working Group on Sarcopenia in Older People (EWGSOP) [46], the
International Working Group on Sarcopenia (IWGS) [47], and the Asian Working Group
for Sarcopenia (AWGS) [48], the cutoff values for each gender were redefined,
THE BIOLOGICAL BASES THAT UNDERLIE THE INDICES
5
I. GENERAL ASPECTS: SKELETAL MUSCLE PHYSIOLOGY AND NUTRITION
respectively, as values one or two standard deviations (SD) below the gender-specific
mean values of the reference data of a healthy young adult population [910,4648]. The
usefulness of these criteria and their corresponding cutoff points is based on a normal distribution which assumes that 68% of cases would fall within one standard deviation from
the mean, and that 95% of all cases would fall within two standard deviations. As a result,
the ASM index (ASMI) not only adjusts ASM according to height but also takes into
account the lower correlation between height and ASM; this means, a deficit, expressing
low appendicular SM mass or presarcopenia, or an excess, suggestive of high appendicular lean tissue or muscularity, expressed as high ASM. Finally, this criterion (22 SD of the
mean values of the genderethnic-specific SM indices from a young adult population) is
the one most often used and associated with impaired physical performance and physical
disability in geriatric populations



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