0% found this document useful (0 votes)
18 views11 pages

Skeletal Muscle As A Pro and Anti Inflammatory Tissue: Insights From Children To Adults and Ultrasound Findings

Texto didáctico

Uploaded by

Magali Pacheco
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
0% found this document useful (0 votes)
18 views11 pages

Skeletal Muscle As A Pro and Anti Inflammatory Tissue: Insights From Children To Adults and Ultrasound Findings

Texto didáctico

Uploaded by

Magali Pacheco
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
You are on page 1/ 11

Journal of Ultrasound (2024) 27:769–779

https://doi.org/10.1007/s40477-024-00917-5

REVIEW PAPER

Skeletal muscle as a pro‑ and anti‑inflammatory tissue: insights


from children to adults and ultrasound findings
Armando Di Ludovico1 · Saverio La Bella1 · Francesca Ciarelli1 · Francesco Chiarelli1 · Luciana Breda1 ·
Angelika Mohn1

Received: 12 March 2024 / Accepted: 11 May 2024 / Published online: 21 June 2024
© The Author(s) 2024

Abstract
Previously regarded as a movement and posture control agent, the skeletal muscle is now recognized as an endocrine organ
that may affect systemic inflammation and metabolic health. The discovery of myokines such as IL-6, released from skeletal
muscle in response to physical exercise, is now one of the most recent insights. Myokines are the mediators of the balance
between the pro-inflammatory and anti-inflammatory responses. This underscores the muscle function as a determinant of
good health and prevention of diseases. Advances in ultrasound technology improved evaluation of muscle thickness, compo-
sition, and determining fat distribution. Combining imaging with molecular biology, researchers discovered the complicated
interplay between muscle function, cytokine production and general health effects.The production of myokines with exercise
showcasing the adaptability of muscles to high-stress conditions and contributing to metabolism and inflammation regula-
tion. These findings have significant implications in order to provide improvement in metabolic and inflammatory diseases.

Keywords Ultrasound · Myokines · Adipokines · Obesity · Inflammation

Introduction imaging is considered as an essential tool for assessing


the degree of muscle contractions, which was lacking in
Scientific current research especially in the last decade the traditional functions that were simple motion evalua-
revealed outstanding data that changed our perception about tions [5]. Furthermore, research validating the competen-
the skeletal muscles as a simple contractile tissue secretariat cies of ultrasound in assessing body composition, as well
to the more complex endocrine organ [1]. This result springs as other parameters as muscle thickness, body fat distribu-
from a growing knowledge that the human body may pro- tion, and even structural changes, is an evident prove for the
duce and release cytokines: interleukin-6 (IL-6) and some advanced of modern diagnostic technique [6]. Ultrasound
others in response to exercise [2]. This process play a critical and a molecular biology provide a better evaluation of the
function in maintaining the metabolic balance and immune endocrine role of the muscle more especially in the context
reactions, placing the skeletal muscle in at the forefront of of ageing and chronic inflammation diseases. The associa-
research into the exploration of homeostasis and the inter- tion between the role of muscles, inflammation and chronic
actions between the immune system by mediating cytokine diseases is becoming more understood through studies that
production and signal pathways [3]. investigate muscle cytokines production, such as IL-6, and
The broader understanding of the topic derived from the implications of this process to chronic diseases [6]. For
extensive studies is invaluable; the use of ultrasound contrib- example, a study conducted by Pedersen and Febbraio,
uted to the enhancement of that field and issues of muscle showed that muscle release IL-6 during exercise, with posi-
structure and function have now become much clearer [4]. tive impact on inflammation and metabolism. Furthermore,
Substantiated by the work of Hodges et al. the ultrasound Casey et al. showed that inflammation-associated skeletal
muscle-derived cytokines participates in both systemic and
local inflammation [7]. Such information showed how mus-
* Armando Di Ludovico cle cells are not just absorbing the immune system but are
[email protected] also interacting with it, implying an important significance.
1 In conclusion, advancement in ultrasound and molecular
Department of Pediatrics, University of Chieti, Chieti, Italy

Vol.:(0123456789)
770 Journal of Ultrasound (2024) 27:769–779

biology have improved our understanding of the skeletal Adipokines and myokines in obesity: impact
muscle, no longer considered with the only role of a organ on metabolic health
of movement but also with a influencer of inflammation,
metabolic balance, and overall health [8]. In this paper we With the more advances of obesity research, the role of
explored literature from childhood to adulthood in order muscle and fat cytokines in systemic inflammation and the
to obtain a full picture of how skeletal muscle’s and fat related development of metabolic diseases have become
cytokines change over time in regulating metabolic and pro apparent [20]. With the more advances of obesity research,
and anti-inflammatory balance. An improving in understand- the role of muscle and fat cytokines in systemic inflamma-
ing this process, may provide an improvement in diagnostic tion and the related development of metabolic diseases have
and therapeutic assessment of health diseases related to an become apparent [21]. One of many adipokines, consist-
imbalance between muscle and fat cytokines production [9]. ency levels of TNF-α, IL-6, and IL-1β, are usually increased
among overweight individuals and they are related to insulin
resistance, a process in which adipokines cause change in the
Myokines way insulin is transmitted. However, the quoted cytokines,
one, can inhibit insulin receptor substrates and, two, acti-
Skeletal muscle tissue showed a pro- an anti-inflammatory vate serine kinase pathways, that result in the reduction of
role, with implication from childhood to adulthood [10]. insulin signaling [22]. Moreover, this increased production
IL-6 is a principal myokine secreted from skeletal muscles of pro-inflammatory cytokines leads to the transformation
during exercise and it is important for balancing inflam- of macrophages into adipose tissue, where they take part
matory and anti-inflammatory reactions [11]. In addition, in the inflammatory process [23]. Thus, a person who is
IL-6 increases insulin sensitivity and regulates the immune overweight or obese is more likely to have a deficit in anti-
response [12]. Skeletal muscle is also another producer inflammatory adipokines like adiponectin, and will, there-
of other significant myokines that include IL-8, IL-15, fore, have insulin resistance in higher levels that are also
and Fstl1 [1]. IL-8 is an angiogenesis promoting cytokine inversely related to the amount of fat stored in the body [24].
required for the formation of new vascular networks in While the reduction in adiponectin level is worrisome, due
muscle tissue and therefore muscle growth. One of IL-15 to its association with increased likelihood of metabolic syn-
main functions is to stimulate muscle growth as well as fat drome, cardiovascular disease, and type 2 diabetes, the rest
metabolism [13, 14]. The function of Fstl1 is to promote of the alterations are still to be studied [25]. On the other
tissue repair and regeneration [15]. Besides their specific hand, muscle tissue not only serves as a metabolic organ,
functions, the muscle myokines together enhance lipolysis but also a secretmem exerted in physical activity is raised
and endothelial function, vital for cardiovascular health [16]. in muscle tissue it additionally acts as an endocrine organ
The ultrasonography allowed monitoring of changes similar to a pancreas, producing myokines during physical
in muscle structure and function, thus revealing an exclu- activity. Acting in an array of autocrines, paracrines, and
sive view on the endocrine role of skeletal muscles [17]. endocrines have been demonstrated for these muscle-ori-
Ultrasound gives a good assessment of muscle thickness gin cytokines [1]. This group of myokines comprises IL-6,
and echostructure. Ultrasound also gives certain additional IL-15, and irisin proteins, which are secreted into the blood
indirect data concerning muscles state and metabolic activi- stream under muscle contractions. These proteins play an
ties associated with secretion of myokines [18]. Ultrasound active role in the metabolic homeostasis. For example, IL-6
is a detailed muscle thickness and structural change quan- that is released by muscle during the exercise and has lipo-
tifying tool, demonstrating how the skeletal muscle is a lytic and fatty acid oxidation effects [19]. An adipokine has
dynamic reactor to physical triggers with its endocrine role its negative side when released by an adipose tissue that
being underlined. The linkage of physical activity, myokine induces an inflammation, however in other situation body
secretion, and systemic health responses shows that muscles becomes anti-inflammatory when this adipokine is released
are crucial in metabolism maintenance and overall systemic by muscles during the mass [26]. IL-15 was linked to muscle
inflammation control [19]. Ultrasound studies findings, for growth and also the process of ‘browning’ of white fat where
example changes in muscle composition, and myokine secre- the white fat is converted into active brown fat through this
tion patterns, demonstrate not only exercise effect on the mechanism. This is an adipose tissue type that is more effi-
muscle but also its endocrine effect that is verifiable from cient in calorie burning [27]. Irisin; a myokine, a cleaved
childhood to adulthood (Fig. 1). membrane protein of FNDC5, has some proven to increase
the energy expenditure and thus might act as an important
anti-obesity and metabolic diseases factor [28].
Journal of Ultrasound (2024) 27:769–779 771

Fig. 1  Impact of muscle and fat mass on human health. The muscle growth, angiogenesis, energy storage, and tissue cell repair. Fat mass
tissue and fat tissues differ in their response to inflammation. Elevated accumulation cause adipokines release, leading to proinflammatory
myokines levels such as IL-6, IL-8, IL-15, and Fstl1 promote muscle state and increased insulin resistance

The balance between the adipokines, the myokines intri- control their over-production or blocking the receptors to
cately controls the general metabolism on the systemic level stop their damaging effect [31]. But the physical activity
thus setting a complex between calorie burning, inflamma- as the exercise has also other effects. It decreases the level
tion and metabolic-health rates. Conversely, the white adi- of adipose tissue, which is associated with proinflamma-
pose tissue produces the pro-inflammatory cytokines that tory states. Further to this, physical activity enhances the
cause toxinization of insulin receptor and result in higher positive effects of myokines. An example of this is that,
insulin resistance in muscles [29]. This is an indication that one should keep their muscles and be fit, always as this is
adipokines and myokines are both equal in modifying the very important to overall health [16].
metabolism. Yet, myokines, a product of exercise secretion, All things considered, the balance of the adipokine and
might control these counter effects through enhancement of the myokine is very important in the field of metabolic
insulin response sensitivity and genesis of anti-inflammatory homeostasis, especially in the course of obesity diseases
reactions [30]. [32]. There are lots of factors that push this balance, which
These pathways implicate and characterize the intri- include the diet, activity, and the genetic predisposition,
cate networks of cytokines that need to be determined and their disturbance leads to systemic inflammation and
in order to create potent management of obesity and its insulin resistance, which are the key features of obesity.
metabolic dysfunctions. Alternatives to therapeutic inter- The data indicates that inequalities are inbuilt and have
vention in this regard may involve targeting cytokines to always remained in the course of social life [33].
772 Journal of Ultrasound (2024) 27:769–779

Muscle inflammation in multi‑age oxidative capacity, it becomes quite understandable why


populations physical exercise improves energy utilization efficiency
[41]. These adaptations result from the increased produc-
Childhood tion of anti-inflammatory myokines and reduced metabo-
lism of cytokines which are known for chronic inflamma-
The growth period especially post muscle inflammation tion and are dysregulated metabolically [42].
can become the life-defining period for body development
and physiologic maturity [34]. Myokines, for instance Elderly population
IL-6, are in the lead of their function in co-ordination of
balancing a pro-inflammatory response and an anti-inflam- Echo muscle thickness evaluation is a powerful tool that is
matory response within the muscle tissue [7]. The second- used by the clinicians for diagnosis of sarcopenia in older
ary molecules may be also very active in the mediation of patients. These assessments allow one to see structural
the tissue stress adaptations to the physiological stresses changes in atrophic or inflamed muscles, offering an early
like exercise, maintaining intrinsic repair and regeneration reaction to defects that might cause muscle function to dete-
capacities, and finally triggering the process of renewal riorate, result in sarcopenia, and account for health-related
that follows traumatic injuries [35]. The signalling system diseases and disorders [43]. Despite of all, changes in skel-
of this complex is one of the most important features, ena- etal muscle myokines secretion and inflammations over the
bling the organism to deliver a fast and controlled response life show that at all stages of our lives keel physiological
to any type of damage and stress, in this way, the system system to normal [44, 45].
will be trustworthy to protect muscle physiology from a
variety of problems [36, 37]. Even though amino acids are
the most essential, this phase becomes even more critical, Imaging muscle inflammation
because here myokines interact with hormones and growth across the lifespan
factors, which are key drivers of muscle growth. They pro-
mote the proliferation of the satellite cell, their differentia- Insight into ultrasonography amalgamation of a wide range
tion of the newly formed cells and their direct incorpora- of advanced imaging techniques beyond visualization, which
tion into the muscle fibers [38]. Stimulated by increased aids in ecological assessment of inflammation due to obesity
myokine levels, the muscle tissue releases growth factors in skeletal muscles [46]. The application of ultrasonography
that are involved in immediate repair and prepare the tis- at various life stages shows how it provides images of mus-
sues for future stressers so instead of responding a once off cles and muscle cell function, which allows clinicians and
repair they create an environment that supports long-term researchers the safest and most effective way of observing
health [39]. the relationship between anatomical structure and pathologi-
cal process [44].
The grayscale analysis, as a crucial element of ultrasono-
Adulthood graphic research, was specially created to investigate muscle
echogenicity [47]. This technique includes the use of quanti-
As individuals move into adulthood, the consequences of tative methods to determine the echogenicity (echogenicity
muscle inflammation evolve [36]. The modern life style is a feature that indicates how dehydrated and degenerated
in which ‘laziness’ rather than physical activity is typical the muscle is, mostly caused by the fibrous tissues and the
is the total opposite of the physiological need of physical amount of fat deposit in the muscle), associated with the
exertion which is one of the determining factors in the pro- concentration of fibrous tissues and the amount of fat deposit
inflammatory state of muscle tissue. Systematic physical in the muscle [48]. Such modifications demonstrate chronic
activity supports healthy regulation of muscle secretion inflammation; the latter is associated with echogenicity
myokine muscle generators what is important for main ant- increasing, which is a sign of leaving normal muscle tis-
inflammatory conditions in the muscles tissue [16]. This sue behind [49]. Using ultrasonography, caliper is able to
adaptation is very crucial for the maintenance of metabolic effectively determine changes in tissues as quantitative data
health as it can help in increased insulin sensitivity, mini- allows to assess healthiness of the tissue and reveal early
mize the risk of chronic metabolic diseases, and improve- signs of histopathological alterations [17]. The road of life
ment of body’s homeostasis [40]. When physical exercise is marked with diverse challenges for the skeletal muscle
is seen as an application that goes beyond the mere reduc- from the increase in the demands as a child to the wearer
tion of inflammatory markers to the induction of beneficial out of the adulthood and to the physical test of maintaining
adaptations in the muscle fibers and an enhancement of the integrity muscle with age. In particular, kids at an early age
should be identified of inflammatory that comes out through
Journal of Ultrasound (2024) 27:769–779 773

ultrasonography and you should keep it as minimal as pos- individual, from birth to old age [57]. Ultrasonography is
sible to prevent it from having a negative effect on growth not only a crucial part of detection, but also of the moni-
and development [50]. The muscle ultrasound technique for toring process, as well as the story of how active muscle
evaluating the changes in muscle echogenicity and volume fibers work with their environment and coping with chronic
can provide an early detection of inflammatory myopathies inflammation while growing.
that would allow the clinicians to intervene in the disease
state and, as a result, an effective targeted treatment to alter
the course of the disease [49]. Ultrasound findings in obesity‑induced
While moving into adulthood the role of muscles changes muscle changes
from maturing to using them right and fighting inflammation
[51]. There ultrasonography rules as a measure of effective- The application of ultrasonography provides non-inva-
ness of muscle tissue rehab exercises. The underlying mech- sive information about skeletal muscle and adipose tissue
anisms of muscle-mediated anti-inflammatory effects can be throughout the lifespan (Table 1) [4]. These methods are
demonstrated through ultrasonography in a defined image based on the observation and classification of the progress of
[52]. This measurement is apparent while the muscle is in obesity-related changes in muscle and fat tissue in the body
motion as a result of physical activity. Ultrasound provides by utilizing a variety of scales and measurements. This sug-
as a mirror reflecting the tissue's reactions to exercise, where gests the interventions can be designed in a way which will
the improvements in muscle architecture and a decline in aim at various stages of life (Table 2) [58].
the level of inflammatory markers are demonstrated and as Contrast-enhanced ultrasound, a highly accurate very
a result it becomes obvious that physical activity preserves widely measuring technique, yields precise values of the
the organism against inflammation [52]. cross-sectional area (CSA) and thickness of important mus-
The golden years, as always, spawn their own issues, with cles in the leg, like the rectus femoris or gastrocnemius [59].
sarcopenia and gradual muscle mass and function loss being These are the techniques to compare the measured results
the leading ones [53]. Ultrasonography using a feature that with the normal data in the children’s age group to identify
provides with muscle mass and quality assessment becomes the abnormalities. An example is the Heckmatt scale, it was
an unreplaceable tool in detecting age-related pathology originally designed to evaluate muscle quality in patients
[54]. The ultrasonography method that includes the assess- with specific neuromuscular diseases [60]. It provides an
ment of body areas, such as muscle thickness, area of cross- assessment of muscle quality evaluating echogenicity from
section, and intramuscular fat concentration, provides a normal group to severe group and higher score indicates
comprehensive picture on the structural changes due to age more fat and connective tissues were infiltrated into the mus-
and helps to define the influence of age on muscle alterations cles [60].
[55]. Elastosonography can as well analyze muscle stiffness Indeed, the absence of differences from well-regulated
that may appears during fibrosis [56]. echo patterns and CSA measurements during this stage
In summary, from childhood to the elderly population, represents the loss of muscle strength due to obesity [61].
ultrasonography with the help of the utility of the technique In this stage the Doppler ultrasound technology is used to
provides a comprehensive depiction of the muscle health assess the perfusion and microvascularity of muscle [62]. A
[57]. It goes beyond classic imaging features and provides a Doppler ultrasound measures peak systolic velocity (PSV)
unique approach to observe how the inflammatory changes and end-diastolic velocity (EDV) and these values are an
in the muscles due to obesity lasts throughout the life of an indicator of the quality of the blood flow. Resistive indices,

Table 1  Muscular ultrasound changes in children and adult


Age group Ultrasound findings Implication References

Children Increased echogenicity Indicative of inflammatory myopathies and suggests the presence of fibrous [74, 75]
tissue and intramuscular fat, impacting muscle growth and metabolic health
Children Reduced muscle volume May indicate muscle atrophy or diminished muscle development due to [74, 75]
inflammation
Adults Increased echogenicity Correlates with intermuscular adipose infiltration and fibrosis, linked to [76, 77]
insulin resistance and decreased muscle function
Adults Changes in muscle architecture Visualized alterations can indicate ongoing inflammatory processes, poten- [76, 78]
tially affecting muscle strength and endurance
Children and adults Changes in muscles thickness Indirectly reflects muscle health, metabolic activity, and the secretion of [17, 18]
and echo intensity myokines within the muscle
Table 2  Ultrasound metrics: assessment of muscle and fat tissue
774

Scale Population Description Anatomical structures Normal range Variations from normal

Heckmatt Scale [60] Children Assesses muscle echogenicity Quadriceps, especially the rectus Grade 0 (normal) to Grade 1 Higher grades indicate increased fat
from normal to increased fibro- femoris, due to its accessibility (slight increase) and connective tissue, suggesting
sis and fat infiltration and size muscle pathology
Medial gastrocnemius, for its
propensity to show changes in
echogenicity due to its composi-
tion and function
Muscle Quality Index (MQI) [79] Adults Combines measurements of Biceps brachii and triceps brachii MQI < 25 (lower intramuscular Higher MQI scores may indicate
muscle size with the degree of in the upper extremities fat) sarcopenia or increased fat
intramuscular fat for an overall Rectus femoris and biceps femoris infiltration
assessment of muscle quality in the lower extremities, due to
their size and role in locomotion
Elastic modulus [77] Adults Quantifies muscle stiffness, Accessible and sizeable muscles < 8 kPa (indicative of normal tis- Increased values suggest greater tis-
often used in the assessment of such as the rectus femoris or sue stiffness) sue stiffness and potential fibrosis
fibrosis biceps brachii
These measurements are also use-
ful in deeper muscles, but acces-
sibility and the depth at which
reliable measurements can be
obtained may limit their use
Shear wave speed [77] Adults Measures the speed of shear Accessible and sizeable muscles 1–3 m/s (indicative of normal Higher values suggest increased
waves through muscle, related such as the rectus femoris or tissue elasticity) muscle stiffness and potential
to stiffness and used to assess biceps brachii pathology
fibrosis These measurements are also use-
ful in deeper muscles, but acces-
sibility and the depth at which
reliable measurements can be
obtained may limit their use
Peak systolic velocity (PSV) [80] All ages Assesses the maximum blood Measurements are often taken Generally ranges between 30 Lower values may indicate reduced
flow velocity in muscle during in the major arteries supplying to 100 cm/s, but this can vary muscle perfusion and potential
the contraction phase of the the muscle groups, such as the widely based on the artery's size pathology
heartbeat femoral artery for the lower and the patient's hemodynamic
limb muscles status
The brachial artery can be used
for upper limb muscle assess-
ments
Journal of Ultrasound (2024) 27:769–779
Journal of Ultrasound (2024) 27:769–779 775

unlike measuring the flexibility of the vascular system or

ance, which may reflect pathology


Lower values may indicate reduced
muscle perfusion during relaxa-
show rigidity [63].

suggest altered vascular resist-


Values outside the normal range
For mid life adults, where obesity has a better chance
to intensify its impact, Ultrasound is used as a tracker to
Variations from normal

measure changes over time. B-mode ultrasound is valuable


and the temperature of muscle texture and internal fat can
be seen with this [64]. In case of sonoelastography, which
not only helps assembling shot qualitative and shot qualita-
tive assessments of tissue stiffness but also reveals fibrosis
tion

[65]. Adopting standardized methods of assessment among


parameters like modulus of elasticity or shear wave so as to
again depending on the specific
vessel and physiological condi-

give the density the material in numerical form makes the


Often ranges from 5 to 20 cm/s,

tions at the time of measure-

0.5–0.7 (indicative of normal

stiffness observed in the muscle tissue easier. The higher


the value of fibrosis and inflammation, the better is the pres-
ence in the tissue for which it caters, therefore, the values
vascular resistance)

provide crucial insights into the condition of the tissue [66].


Regarding obesity, or sarcopenia in aging, ultrasound test
Normal range

will delineate muscle cross-sectional area and thickness.


This can be useful in sarcopenia and weight-related muscle
ment

changes diagnosis and treatment that help detect them at


the early stages. Sarcopenia is a condition of the muscle
the muscle can also be assessed
in the major arteries supplying

loss related to age and weakening of muscles employed in


the muscle groups, such as the

supplying the muscle group of

Small peripheral arteries within


for upper limb muscle assess-
The brachial artery can be used

Similarly to PSV and EDV, RI


Measurements are often taken

if the resolution of the ultra-


interest, such as the femoral
femoral artery for the lower

measurements are typically

sound machine is sufficient

weight-bearing activities. This assessment, in most cases,


taken in arteries within or

artery for the lower limbs

is based on the Muscle Quality Index (MQI) which consid-


Anatomical structures

ers muscle size as well as the degree and fat deposition in


muscle [67]. MQI is the highly important parameter that not
limb muscles

only estimates intramuscular fat status but also muscle area.


Among the most important tasks of the study is the process
ments

of assessing intervention efficiency when it comes to suc-


cessful prevention or treatment of sarcopenia [67].
In all the age groups the evaluation of subcutaneous and
Measures the blood flow velocity
in muscle during the relaxation

Calculates the ratio of peak sys-

intrabdominal adiposity via ultrasound is very key under-


tolic velocity minus end-dias-
tolic velocity to peak systolic
velocity, indicating muscle

standing of adiposity distribution, which doctors normally


refer to body’s underlying fat metabolism related disorders
phase of the heartbeat

[64]. Measuring subcutaneous fat (SAT) thickness at the


vascular resistance

standardised anatomical sites, such as the abdomen or thigh,


enables systemic SAT distribution assessment and provides
Population Description

an opportunity to reveal the association of metabolic risk


factors with SAT accumulation [64, 68]. Sonoelastography
does not only help in producing qualitative and quantita-
tive parameters of tissue stiffness, but also detects fibrosis
All Ages
End-diastolic velocity (EDV) [80] All ages

[65]. Adopting the standardized approaches for evaluation


for such parameters as modulus of elasticity or shear wave
to convert the density of the material into numerical form
makes the stiffness observed in the muscle tissue more
accessible. The higher the value of fibrosis and inflamma-
tion, the better is the presence in the tissue it is providing for,
Resistive Index (RI) [62]

hence, the values are very important for the state of tissue
Table 2  (continued)

[66]. Specifically, the prevalence of obesity, or sarcopenia


in elderly, ultrasound test can define muscle cross-sectional
area and thickness should be performed. The latter can be of
great value in identifying diagnosis and treatment of sarco-
Scale

penia and weight-related muscle changes that appear at the


776 Journal of Ultrasound (2024) 27:769–779

first stages. Sarcopenia is defined by age-associated loss of The crosstalk between muscle mediated cytokines and
muscle mass and deterioration of muscles utilized in load- the systemic inflammation is critical for it places the skeletal
dependent activities. This assessment frequently includes the muscle as the main actor not only through movement but an
Muscle Quality Index (MQI), which considers muscle size active participant of metabolic well-being and of immunity
and simultaneously the amount and deposition of in Muscle responses regulation [42]. Systematic implementation of
[67]. Metabolic Quality Index (MQI) is a crucial parameter approaches designed for physiologic changes proposed for
that evaluates not only the condition of intramuscular fat but muscle in a way would make muscle tissue healthier, result-
also muscle area. The process of assessing intervention effi- ing in not only healthier metabolic profiles but also reduced
ciency in successful prevention or treatment of sarcopenia is chronic inflammation-associated diseases [73].
one of the most important tasks of the study [67].
In all the age groups auditioning subcutaneous and intrab-
Author contributions ADL wrote the manuscript and realized the fig-
dominal adiposity via ultrasound provides very key under- ure and table. SLB and FC (Francesca Ciarelli) wrote the manuscript.
standing of adiposity distribution, which physician refer to FC (Francesco Chiarelli), LB and AM coordinated, reviewed, and
as underlying body fat metabolism related diseases [64]. approved the final version of the manuscript. All authors have read and
Measuring subcutaneous fat (SAT) thickness at the standard- agreed to the published version of the manuscript. All authors take full
responsibility for the integrity and accuracy of all aspects of the work.
ised anatomical sites, such as the abdomen or thigh, enables
SAT distribution throughout the body estimation and pro- Funding Open access funding provided by Università degli Studi G.
vides an opportunity to reveal the association of metabolic D’Annunzio Chieti Pescara within the CRUI-CARE Agreement. This
risk factors with SAT accumulation [68]. manuscript received no external funding.
Through the physician’s interpretation, validation of Data availability Not applicable to this article as no datasets were gen-
index and scale, physical examination that is then confirmed erated or analyzed during the current study.
by ultrasonography, doctors can now identify, determine and
measure the pathological changes in the body tissues due to Declarations
muscle inflammation in obesity [69]. The analysis of differ-
Conflict of interest The authors declare that they have no competing
ent life stages allows us to comprehend the developing pat- interest.
tern as well as the effects of the obesity on skeletal muscles,
and the clinicians attain the age-specific tailored approaches Ethical approval All performed procedures were in accordance with
for personalised interventions in order to minimize the harm. the ethical standards of the institutional and/or national research com-
mittee and with the 1964 Helsinki Declaration and its later amendments
or comparable ethical standards.

Informed consent Not applicable.


Conclusion
Open Access This article is licensed under a Creative Commons Attri-
Skeletal muscle is not a straightforward one but a rather bution 4.0 International License, which permits use, sharing, adapta-
tion, distribution and reproduction in any medium or format, as long
complex one, which is constantly changing in terms of as you give appropriate credit to the original author(s) and the source,
inflammatory response. It can synthesize cytokines which provide a link to the Creative Commons licence, and indicate if changes
regulate many body functions and have effects on certain were made. The images or other third party material in this article are
parts. These molecules, global inflammation mediators, included in the article’s Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in
include IL-6 that play an important role in muscle health the article’s Creative Commons licence and your intended use is not
and prevention of chronic ailments [70]. It is the endocrine permitted by statutory regulation or exceeds the permitted use, you will
function of muscle and physical activity that necessitates need to obtain permission directly from the copyright holder. To view a
exercise as a role promoting muscle health and disease pre- copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
vention through control of cytokine production [1]. Muscles
can be seen clearly in ultrasound examinations while they
are becoming inflamed. Such studies are the most known
ways of monitoring inflammation of muscles. They could References
enable the medical staff to find out how to best aid their
1. Hoffmann C, Weigert C (2017) Skeletal muscle as an endocrine
patients through their observation of the sound of the muscle organ: the role of myokines in exercise adaptations. Cold Spring
cells contracting and that is associated with the inflamma- Harb Perspect Med 7(11):a029793. https://​doi.​org/​10.​1101/​cshpe​
tion [71]. rspect.​a0297​93
2. Fischer CP (2006) Interleukin-6 in acute exercise and training:
Besides muscle mass assessment by ultrasonography
what is the biological relevance? Exerc Immunol Rev 12:6–33
methods, sarcopenia detection is important in evaluation of 3. Nelke C, Dziewas R, Minnerup J, Meuth SG, Ruck T (2019)
muscle health and inflammation related diseases [72]. Skeletal muscle as potential central link between sarcopenia and
Journal of Ultrasound (2024) 27:769–779 777

immune senescence. EBioMedicine 49:381–388. https://​doi.​org/​ 21. Coelho M, Oliveira T, Fernandes R (2013) State of the art paper
10.​1016/j.​ebiom.​2019.​10.​034 biochemistry of adipose tissue: an endocrine organ. Arch Med
4. Pillen S, Van Alfen N (2011) Skeletal muscle ultrasound. Neurol Sci 2:191–200. https://​doi.​org/​10.​5114/​aoms.​2013.​33181
Res 33(10):1016–1024. https://​doi.​org/​10.​1179/​17431​32811Y.​ 22. Cao H (2014) Adipocytokines in obesity and metabolic dis-
00000​00010 ease. J Endocrinol 220(2):T47–T59. https://​doi.​org/​10.​1530/​
5. Hodges PW, Pengel LHM, Herbert RD, Gandevia SC (2003) JOE-​13-​0339
Measurement of muscle contraction with ultrasound imaging. 23. Surmi B, Hasty A (2008) Macrophage infiltration into adipose
Muscle Nerve 27(6):682–692. https://d​ oi.o​ rg/1​ 0.1​ 002/m
​ us.1​ 0375 tissue: initiation, propagation and remodeling. Future Lipidol
6. Miclos-Balica M et al (2021) Reliability of body composition 3(5):545–556. https://​doi.​org/​10.​2217/​17460​875.3.​5.​545
assessment using A-mode ultrasound in a heterogeneous sam- 24. Freitas Lima LC et al (2015) Adipokines, diabetes and athero-
ple. Eur J Clin Nutr 75(3):438–445. https://​doi.​org/​10.​1038/​ sclerosis: an inflammatory association. Front Physiol. https://​
s41430-​020-​00743-y doi.​org/​10.​3389/​fphys.​2015.​00304
7. Nara H, Watanabe R (2021) Anti-inflammatory effect of muscle- 25. Lei X, Qiu S, Yang G, Wu Q (2023) Adiponectin and metabolic
derived interleukin-6 and its involvement in lipid metabolism. Int cardiovascular diseases: therapeutic opportunities and chal-
J Mol Sci 22(18):9889. https://​doi.​org/​10.​3390/​ijms2​21898​89 lenges. Genes Dis 10(4):1525–1536. https://​doi.​org/​10.​1016/j.​
8. Casey P et al (2022) The current use of ultrasound to measure gendis.​2022.​10.​018
skeletal muscle and its ability to predict clinical outcomes: a 26. Taylor EB (2021) The complex role of adipokines in obesity,
systematic review. J Cachexia Sarcopenia Muscle 13(5):2298– inflammation, and autoimmunity. Clin Sci 135(6):731–752.
2309. https://​doi.​org/​10.​1002/​jcsm.​13041 https://​doi.​org/​10.​1042/​CS202​00895
9. Gomarasca M, Banfi G, Lombardi G (2020) Myokines: the 27. Pierce JR, Maples JM, Hickner RC (2015) IL-15 concentrations
endocrine coupling of skeletal muscle and bone. Advances in in skeletal muscle and subcutaneous adipose tissue in lean and
clinical chemistry, vol 94. Elsevier, Amsterdam, pp 155–218. obese humans: local effects of IL-15 on adipose tissue lipolysis.
https://​doi.​org/​10.​1016/​bs.​acc.​2019.​07.​010 Am J Physiol-Endocrinol Metab 308(12):E1131–E1139. https://​
10. Severinsen MCK, Pedersen BK (2020) Muscle–organ crosstalk: doi.​org/​10.​1152/​ajpen​do.​00575.​2014
the emerging roles of myokines. Endocr Rev 41(4):594–609. 28. Arhire LI, Mihalache L, Covasa M (2019) Irisin: a hope in under-
https://​doi.​org/​10.​1210/​endrev/​bnaa0​16 standing and managing obesity and metabolic syndrome. Front
11. De Melo Madureira ÁN, De Oliveira JRS, De Menezes Lima Endocrinol 10:524. https://​doi.​org/​10.​3389/​fendo.​2019.​00524
VL (2022) The role of IL-6 released during exercise to insu- 29. Rodríguez A, Becerril S, Ezquerro S, Méndez-Giménez L, Früh-
lin sensitivity and muscle hypertrophy. Mini-Rev Med Chem beck G (2017) Crosstalk between adipokines and myokines in fat
22(18):2419–2428. https://​doi.​org/​10.​2174/​13895​57522​66622​ browning. Acta Physiol 219(2):362–381. https://​doi.​org/​10.​1111/​
03091​61245 apha.​12686
12. Kistner TM, Pedersen BK, Lieberman DE (2022) Interleukin 6 30. Gonzalez-Gil AM, Elizondo-Montemayor L (2020) The role
as an energy allocator in muscle tissue. Nat Metab 4(2):170– of exercise in the interplay between myokines, hepatokines,
179. https://​doi.​org/​10.​1038/​s42255-​022-​00538-4 osteokines, adipokines, and modulation of inflammation for
13. Lin W et al (2023) Functional role of skeletal muscle-derived energy substrate redistribution and fat mass loss: a review. Nutri-
interleukin-6 and its effects on lipid metabolism. Front Physiol ents 12(6):1899. https://​doi.​org/​10.​3390/​nu120​61899
14:1110926. https://​doi.​org/​10.​3389/​fphys.​2023.​11109​26 31. Clemente-Suárez VJ et al (2023) The role of adipokines in health
14. Quinn LS, Anderson BG (2011) Interleukin-15, IL-15 recep- and disease. Biomedicines 11(5):1290. https://​doi.​org/​10.​3390/​
tor-alpha, and obesity: concordance of laboratory animal and biome​dicin​es110​51290
human genetic studies. J Obes 2011:1–8. https://​d oi.​o rg/​1 0.​ 32. Pelczyńska M et al (2023) The role of adipokines and myokines
1155/​2011/​456347 in the pathogenesis of different obesity phenotypes—new per-
15. Forcina L, Cosentino M, Musarò A (2020) Mechanisms regulat- spectives. Antioxidants 12(12):2046. https://d​ oi.o​ rg/1​ 0.3​ 390/a​ ntio​
ing muscle regeneration: insights into the interrelated and time- x1212​2046
dependent phases of tissue healing. Cells 9(5):1297. https://​doi.​ 33. Schwartz MW et al (2017) Obesity pathogenesis: an endocrine
org/​10.​3390/​cells​90512​97 society scientific statement. Endocr Rev 38(4):267–296. https://​
16. Leal LG, Lopes MA, Batista ML (2018) Physical exercise- doi.​org/​10.​1210/​er.​2017-​00111
induced myokines and muscle-adipose tissue crosstalk: a review 34. Jung U, Choi M-S (2014) Obesity and its metabolic complica-
of current knowledge and the implications for health and meta- tions: the role of adipokines and the relationship between obesity,
bolic diseases. Front Physiol 9:1307. https://​doi.​org/​10.​3389/​ inflammation, insulin resistance, dyslipidemia and nonalcoholic
fphys.​2018.​01307 fatty liver disease. Int J Mol Sci 15(4):6184–6223. https://d​ oi.o​ rg/​
17. Wijntjes J, Van Alfen N (2021) Muscle ultrasound: present state 10.​3390/​ijms1​50461​84
and future opportunities. Muscle Nerve 63(4):455–466. https://​ 35. Dalle Carbonare L et al (2023) Crosstalk between bone and mus-
doi.​org/​10.​1002/​mus.​27081 cles during physical activity. Cells 12(16):2088. https://​doi.​org/​
18. Sanz-Paris A et al (2021) Muscle thickness and echogenicity 10.​3390/​cells​12162​088
measured by ultrasound could detect local sarcopenia and mal- 36. Costamagna D, Costelli P, Sampaolesi M, Penna F (2015) Role of
nutrition in older patients hospitalized for hip fracture. Nutri- inflammation in muscle homeostasis and myogenesis. Mediators
ents 13(7):2401. https://​doi.​org/​10.​3390/​nu130​72401 Inflamm 2015:1–14. https://​doi.​org/​10.​1155/​2015/​805172
19. Balakrishnan R, Thurmond DC (2022) Mechanisms by which 37. Muñoz-Cánoves P, Scheele C, Pedersen BK, Serrano AL (2013)
skeletal muscle myokines ameliorate insulin resistance. Int J Interleukin-6 myokine signaling in skeletal muscle: a double-
Mol Sci 23(9):4636. https://​doi.​org/​10.​3390/​ijms2​30946​36 edged sword? FEBS J 280(17):4131–4148. https://​doi.​org/​10.​
20. Kawai T, Autieri MV, Scalia R (2021) Adipose tissue inflam- 1111/​febs.​12338
mation and metabolic dysfunction in obesity. Am J Physiol 38. Ahmad SS et al (2023) The roles of growth factors and hormones
Cell Physiol 320(3):C375–C391. https://​doi.​org/​10.​1152/​ajpce​ in the regulation of muscle satellite cells for cultured meat produc-
ll.​00379.​2020 tion. J Anim Sci Technol 65(1):16–31. https://​doi.​org/​10.​5187/​
jast.​2022.​e114
778 Journal of Ultrasound (2024) 27:769–779

39. Ost M, Coleman V, Kasch J, Klaus S (2016) Regulation of 56. Brandenburg JE et al (2014) Ultrasound elastography: the new
myokine expression: role of exercise and cellular stress. Free frontier in direct measurement of muscle stiffness. Arch Phys Med
Radic Biol Med 98:78–89. https://​doi.​org/​10.​1016/j.​freer​adbio​ Rehabil 95(11):2207–2219. https://​doi.​org/​10.​1016/j.​apmr.​2014.​
med.​2016.​02.​018 07.​007
40. Zhao X, An X, Yang C, Sun W, Ji H, Lian F (2023) The crucial 57. Nijholt W, Scafoglieri A, Jager-Wittenaar H, Hobbelen JSM, Van
role and mechanism of insulin resistance in metabolic disease. Der Schans CP (2017) The reliability and validity of ultrasound to
Front Endocrinol 14:1149239. https://​doi.​org/​10.​3389/​fendo.​ quantify muscles in older adults: a systematic review. J Cachexia
2023.​11492​39 Sarcopenia Muscle 8(5):702–712. https://​doi.​org/​10.​1002/​jcsm.​
41. El Assar M, Álvarez-Bustos A, Sosa P, Angulo J, Rodríguez- 12210
Mañas L (2022) Effect of physical activity/exercise on oxidative 58. Sizoo D, De Heide LJM, Emous M, Van Zutphen T, Navis G, Van
stress and inflammation in muscle and vascular aging. Int J Mol Beek AP (2021) Measuring muscle mass and strength in obesity:
Sci 23(15):8713. https://​doi.​org/​10.​3390/​ijms2​31587​13 a review of various methods. Obes Surg 31(1):384–393. https://​
42. Docherty S et al (2022) The effect of exercise on cytokines: doi.​org/​10.​1007/​s11695-​020-​05082-2
implications for musculoskeletal health: a narrative review. 59. Ong C, Lee JH, Leow MKS, Puthucheary ZA (2023) Muscle ultra-
BMC Sports Sci Med Rehabil 14(1):5. https://​doi.​org/​10.​1186/​ sound changes and physical function of critically ill children: a
s13102-​022-​00397-2 comparison of rectus femoris cross-sectional area and quadriceps
43. Barotsis N, Galata A, Hadjiconstanti A, Panayiotakis G (2020) thickness measurements. Crit Care Explor 5(6):e0937. https://d​ oi.​
The ultrasonographic measurement of muscle thickness in sar- org/​10.​1097/​CCE.​00000​00000​000937
copenia. A prediction study. Eur J Phys Rehabil Med. https://​doi.​ 60. Moreta MC et al (2020) Reliability and validity of the modified
org/​10.​23736/​S1973-​9087.​20.​06222-X Heckmatt scale in evaluating muscle changes with ultrasound in
44. Nagae M, Umegaki H, Yoshiko A, Fujita K (2023) Muscle ultra- spasticity. Arch Rehabil Res Clin Transl 2(4):100071. https://​doi.​
sound and its application to point-of-care ultrasonography: a nar- org/​10.​1016/j.​arrct.​2020.​100071
rative review. Ann Med 55(1):190–197. https://​doi.​org/​10.​1080/​ 61. Ponti F, De Cinque A, Fazio N, Napoli A, Guglielmi G, Bazzocchi
07853​890.​2022.​21578​71 A (2020) Ultrasound imaging, a stethoscope for body composition
45. Huang L et al (2022) Potential therapeutic strategies for skeletal assessment. Quant Imaging Med Surg 10(8):1699–1722. https://​
muscle atrophy. Antioxidants 12(1):44. https://​doi.​org/​10.​3390/​ doi.​org/​10.​21037/​qims-​19-​1048
antio​x1201​0044 62. Limberg JK et al (2020) Assessment of resistance vessel function
46. Deniz O et al (2020) Role of ultrasonography in estimating muscle in human skeletal muscle: guidelines for experimental design,
mass in sarcopenic obesity. J Parenter Enter Nutr 44(8):1398– Doppler ultrasound, and pharmacology. Am J Physiol Heart Circ
1406. https://​doi.​org/​10.​1002/​jpen.​1830 Physiol 318(2):H301–H325. https://​doi.​org/​10.​1152/​ajphe​art.​
47. Klawitter F, Walter U, Patejdl R, Endler J, Reuter DA, Ehler J 00649.​2019
(2022) Sonographic evaluation of muscle echogenicity for the 63. Boote EJ (2003) AAPM/RSNA physics tutorial for residents: top-
detection of intensive care unit-acquired weakness: a pilot single- ics in US: Doppler US techniques: concepts of blood flow detec-
center prospective cohort study. Diagnostics 12(6):1378. https://​ tion and flow dynamics. Radiographics 23(5):1315–1327. https://​
doi.​org/​10.​3390/​diagn​ostic​s1206​1378 doi.​org/​10.​1148/​rg.​23503​5080
48. Fionda L et al (2023) Comparison of quantitative muscle ultra- 64. Wagner DR (2013) Ultrasound as a tool to assess body fat. J Obes
sound and whole-body muscle MRI in facioscapulohumeral mus- 2013:1–9. https://​doi.​org/​10.​1155/​2013/​280713
cular dystrophy type 1 patients. Neurol Sci 44(11):4057–4064. 65. Winn N, Lalam R, Cassar-Pullicino V (2016) Sonoelastography
https://​doi.​org/​10.​1007/​s10072-​023-​06842-5 in the musculoskeletal system: current role and future directions.
49. Albayda J, Van Alfen N (2020) Diagnostic value of muscle World J Radiol 8(11):868. https://​doi.​org/​10.​4329/​wjr.​v8.​i11.​868
ultrasound for myopathies and myositis. Curr Rheumatol Rep 66. Taljanovic MS et al (2017) Shear-wave elastography: basic phys-
22(11):82. https://​doi.​org/​10.​1007/​s11926-​020-​00947-y ics and musculoskeletal applications. Radiographics 37(3):855–
50. Maurits NM, Beenakker EAC, Van Schaik DEC, Fock JM, Van 870. https://​doi.​org/​10.​1148/​rg.​20171​60116
Der Hoeven JH (2004) Muscle ultrasound in children: normal 67. Naimo MA, Varanoske AN, Hughes JM, Pasiakos SM (2021)
values and application to neuromuscular disorders. Ultrasound Skeletal muscle quality: a biomarker for assessing physical
Med Biol 30(8):1017–1027. https://​doi.​org/​10.​1016/j.​ultra​smedb​ performance capabilities in young populations. Front Physiol
io.​2004.​05.​013 12:706699. https://​doi.​org/​10.​3389/​fphys.​2021.​706699
51. Kunz HE, Lanza IR (2023) Age-associated inflammation and 68. Hoffmann J et al (2022) Measurement of subcutaneous fat tissue:
implications for skeletal muscle responses to exercise. Exp Ger- reliability and comparison of caliper and ultrasound via system-
ontol 177:112177. https://​doi.​org/​10.​1016/j.​exger.​2023.​112177 atic body mapping. Sci Rep 12(1):15798. https://​doi.​org/​10.​1038/​
52. Nader GA, Lundberg IE (2009) Exercise as an anti-inflammatory s41598-​022-​19937-4
intervention to combat inflammatory diseases of muscle. Curr 69. Simó-Servat A et al (2022) Usefulness of muscle ultrasound to
Opin Rheumatol 21(6):599–603. https://​doi.​org/​10.​1097/​BOR.​ study sarcopenic obesity: a pilot case–control study. J Clin Med
0b013​e3283​319d53 11(10):2886. https://​doi.​org/​10.​3390/​jcm11​102886
53. Larsson L et al (2019) Sarcopenia: aging-related loss of muscle 70. Belizário JE, Fontes-Oliveira CC, Borges JP, Kashiabara JA, Van-
mass and function. Physiol Rev 99(1):427–511. https://​doi.​org/​ nier E (2016) Skeletal muscle wasting and renewal: a pivotal role
10.​1152/​physr​ev.​00061.​2017 of myokine IL-6. Springerplus 5(1):619. https://​doi.​org/​10.​1186/​
54. Baek S-H, Sung JH, Park J-W, Son MH, Lee JH, Kim B-J (2023) s40064-​016-​2197-2
Usefulness of muscle ultrasound in appendicular skeletal mus- 71. Harris-Love M et al (2018) The comparative associations of ultra-
cle mass estimation for sarcopenia assessment. PLoS ONE sound and computed tomography estimates of muscle quality with
18(1):e0280202. https://​doi.​org/​10.​1371/​journ​al.​pone.​02802​02 physical performance and metabolic parameters in older men. J
55. Ismail C et al (2015) Diagnostic ultrasound estimates of muscle Clin Med 7(10):340. https://​doi.​org/​10.​3390/​jcm71​00340
mass and muscle quality discriminate between women with and 72. Kara M et al (2021) Diagnosing sarcopenia: functional perspec-
without sarcopenia. Front Physiol. https://​doi.​org/​10.​3389/​fphys.​ tives and a new algorithm from the ISarcoPRM. J Rehabil Med
2015.​00302 53(6):jrm00209. https://​doi.​org/​10.​2340/​16501​977-​2851
Journal of Ultrasound (2024) 27:769–779 779

73. Qiu Y et al (2023) Exercise sustains the hallmarks of health. J 79. Caamaño-Navarrete F, Jerez-Mayorga D, Alvarez C, Del-Cuerpo
Sport Health Sci 12(1):8–35. https://​doi.​org/​10.​1016/j.​jshs.​2022.​ I, Cresp-Barría M, Delgado-Floody P (2023) Muscle Quality
10.​003 Index in morbidly obesity patients related to metabolic syndrome
74. Zaidman CM, Van Alfen N (2016) Ultrasound in the assessment of markers and cardiorespiratory fitness. Nutrients 15(11):2458.
myopathic disorders. J Clin Neurophysiol 33(2):103–111. https://​ https://​doi.​org/​10.​3390/​nu151​12458
doi.​org/​10.​1097/​WNP.​00000​00000​000245 80. Adigozali H, Shadmehr A, Ebrahimi E, Rezasoltani A, Naderi F
75. VanHorn TA, Cartwright MS (2020) Neuromuscular ultrasound (2019) B mode, Doppler and ultrasound elastography imaging
in the pediatric population. Diagnostics 10(12):1012. https://​doi.​ on active trigger point in women with myofascial pain syndrome
org/​10.​3390/​diagn​ostic​s1012​1012 treated by dry needling. Muscle Ligaments Tendons J 09(03):417.
76. Khan IM et al (2015) Intermuscular and perimuscular fat https://​doi.​org/​10.​32098/​mltj.​03.​2019.​16
expansion in obesity correlates with skeletal muscle T cell
and macrophage infiltration and insulin resistance. Int J Obes Publisher's Note Springer Nature remains neutral with regard to
39(11):1607–1618. https://​doi.​org/​10.​1038/​ijo.​2015.​104 jurisdictional claims in published maps and institutional affiliations.
77. Ashir A et al (2023) Skeletal muscle assessment using quantitative
ultrasound: a narrative review. Sensors 23(10):4763. https://​doi.​
org/​10.​3390/​s2310​4763
78. Page P, Manske RC, Voight M, Wolfe C (2023) MSK ultra-
sound—an IJSPT perspective. Int J Sports Phys Ther. https://​doi.​
org/​10.​26603/​001c.​68184

You might also like