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This study evaluates the effectiveness of various diagnostic methods for sarcopenia and nutritional status in outpatients with liver cirrhosis. It finds that the SARC-F tool is inadequate for screening, while the chair sit-and-stand test is the most effective for identifying low muscle strength. The study suggests excluding SARC-F and SARC-CalF from screening protocols, and highlights calf circumference as a viable alternative when more sophisticated methods like DXA are unavailable.

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0% found this document useful (0 votes)
14 views29 pages

Co WM 05585 02

This study evaluates the effectiveness of various diagnostic methods for sarcopenia and nutritional status in outpatients with liver cirrhosis. It finds that the SARC-F tool is inadequate for screening, while the chair sit-and-stand test is the most effective for identifying low muscle strength. The study suggests excluding SARC-F and SARC-CalF from screening protocols, and highlights calf circumference as a viable alternative when more sophisticated methods like DXA are unavailable.

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vivianelimalive
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Evaluación de la sarcopenia y del

estado nutricional en pacientes


ambulatorios con cirrosis
hepática: concordancia de
métodos diagnósticos

Evaluating sarcopenia and


nutritional status in outpatients
with liver cirrhosis: concordance
of diagnostic methods

10.20960/nh.05585

01/28/2025
OR 5585

Evaluating sarcopenia and nutritional status in outpatients


with liver cirrhosis: concordance of diagnostic methods

Evaluación de la sarcopenia y del estado nutricional en pacientes


ambulatorios con cirrosis hepática: concordancia de métodos
diagnósticos

Marina Demas Rezende Gischewski¹, Fernanda Lívia Cavalcante


Araujo², Aryana Isabelle de Almeida Neves Siqueira¹, Alina Joana da
Silva Wallraf³, João Araújo Barros Neto², Nassib Bezerra Bueno 3,
Juliana Célia de Farias Santos¹, Fabiana Andréa Moura¹,³

¹Pós-Graduação em Ciências Médicas (PPGCM/UFAL); ²Faculdade de


Nutrição (FANUT); ³Pós-Graduação em Nutrição (PPGNUT).
Universidade Federal de Alagoas (UFAL). Maceió, AL. Brazil

Received: 25/10/2024
Accepted: 11/12/2024
Correspondence: Fabiana Andréa Moura. Pós-Graduação em
Nutrição (PPGNUT). Universidade Federal de Alagoas (UFAL). Av.
Lourival Melo Mota, s/n - Tabuleiro do Martins. Maceió, AL. Brazil
e-mail: [email protected]

Acknowledgments: programa de Iniciação Científica. All patients with


liver cirrhosis of Hospital.

Authors´ contribution: conceptualization, data curation and


methodology, M. D. R. G., N. B. B., R. M. A. F. W., and F. A. M.;
investigation, M. D. R. G., F. L. C. A., A. I. A. N. S., A. J. S. W., and F. A.
M.; collection of data and materials, M. D. R. G., A. I. A. N. S., A. J. S.
W., and F. A. M.; writing original draft preparation, M. D. R. G., F. L. C.
A., N. B. B., J. C. F. S., and F. A. M.; writing, review and editing, M. D.R.
G., N. B. B., J. C. F. S., and F. A. M. All authors have read and agreed
to the published version of the manuscript.
Funding sources: this work was supported by FAPEAL number (60030-
0000000161/2022).

Institutional Review Board Statement: it was approved by the Ethics


Committee no. 5.432.777 on May 26, 2022.

Informed consent statement: all participants in this study signed the


Informed Consent Form (ICF).

Data availability statement: this is an unpublished work, not under


submission process in any other scientific journal. All data is privately
accessible.

Highlights: a) SARC-F tool is inadequate for sarcopenia screening


outpatients with liver cirrhosis; b) chair sit-and-stand test proved to
be the most effective tool for identifying low muscle strength; c) CC is
a viable alternative for muscle mass assessment when DXA or CT are
unavailable.

Conflict of interest: the authors declare that they have no conflict of


interest.

Artificial intelligence: the authors declare not to have used artificial


intelligence (AI) or any AI-assisted technologies in the elaboration of
the article.

ABSTRACT
Introduction and objectives: malnutrition and sarcopenia are
prevalent in individuals with cirrhosis, but their diagnosis remains
challenging due to limited access to suitable methods across different
levels of healthcare. This study aimed to identify the most effective
method for diagnosing sarcopenia in outpatients with liver cirrhosis
and to evaluate the concordance between subjective and objective
diagnostic methods. Patients and methods: patients aged ≥ 18
years with a diagnosis of cirrhosis (regardless of etiology) under
outpatient care were included. Exclusion criteria were: a) neoplasia,
b) acute liver failure, c) pregnancy/lactation, d) HIV infection, e)
special situations requiring liver transplantation, and f) history of
organ failure. Nutritional and sarcopenia assessments used subjective
methods, including the Royal Free Hospital-Nutritional Prioritizing Tool
(RFH-NPT), SARC-F, SARC-Calf, and RFH-Global Assessment (RFH-GA);
and objective methods, including anthropometry, handgrip strength
(HGS), the sit-and-stand test (15s), and appendicular skeletal muscle
mass index (ASMI) by Dual-Energy X-ray Absorptiometry (DXA).
Concordance between ASMI and traditional methods was analyzed.
Significance was set at p < 0.05.
Results: a total of 45 patients were analyzed, with alcoholic liver
disease being the most frequent etiology (44.4 %). The sit-and-stand
test (15s) combined with muscle depletion by DXA diagnosed the
most cases of sarcopenia (42.2 %). Moderate agreement was found
between muscle depletion and isolated calf circumference (CC) (κ =
0.581; p < 0.001).
Conclusions: our study suggests excluding SARC-F and SARC-CalF
from sarcopenia screening in outpatients with cirrhosis. While ASMI
remains the most reliable diagnostic method, CC may serve as a
feasible alternative when DXA is unavailable.

Keywords: Nutritional status. Liver disease. Malnutrition. Muscular


atrophy and liver transplant.

RESUMEN
Introducción y objetivos: la desnutrición y la sarcopenia son
prevalentes en individuos con cirrosis, pero su diagnóstico sigue
siendo un desafío debido al acceso limitado a métodos adecuados en
los diferentes niveles de atención en salud. Este estudio tuvo como
objetivo identificar el método más efectivo para diagnosticar
sarcopenia en pacientes ambulatorios con cirrosis hepática y evaluar
la concordancia entre los métodos de diagnóstico subjetivos y
objetivos.
Pacientes y métodos: se incluyeron pacientes de ≥ 18 años con
diagnóstico de cirrosis (independientemente de la etiología) en
atención ambulatoria. Los criterios de exclusión fueron: a) neoplasia,
b) insuficiencia hepática aguda, c) embarazo/lactancia, d) infección
por VIH, e) situaciones especiales que requirieran trasplante hepático
y f) antecedentes de insuficiencia orgánica. Las evaluaciones de
desnutrición y sarcopenia utilizaron métodos subjetivos, como el
Royal Free Hospital-Nutritional Prioritizing Tool (RFH-NPT), SARC-F,
SARC-Calf y RFH-Global Assessment (RFH-GA); y métodos objetivos
como antropometría, fuerza de agarre manual (HGS), prueba de
sentarse y levantarse (15s) e índice de masa muscular esquelética
apendicular (ASMI) por absorciometría dual de rayos X (DXA). Se
analizó la concordancia entre ASMI y los métodos tradicionales. Se
estableció significancia en p < 0.05.
Resultados: se analizaron un total de 45 pacientes, siendo la
enfermedad hepática alcohólica la etiología más frecuente (44.4 %).
La prueba de sentarse y levantarse (15s) combinada con la depleción
muscular medida por DXA diagnosticó la mayor cantidad de casos de
sarcopenia (42.2 %). Se observó una concordancia moderada entre la
depleción muscular y la circunferencia de la pantorrilla aislada (CC) (κ
= 0.581; p < 0.001).
Conclusiones: nuestros hallazgos sugieren excluir SARC-F y SARC-
CalF del cribado de sarcopenia en pacientes ambulatorios con cirrosis.
Aunque ASMI sigue siendo el método diagnóstico más confiable, la CC
puede servir como alternativa viable cuando DXA no esté disponible.
Palabras clave: Estado nutricional. Enfermedad hepática.
Desnutrición. Atrofia muscular. Trasplante hepático.

INTRODUCTION
The liver is the principal metabolic organ in the human body,
responsible for numerous complex biochemical processes involving
the metabolism of carbohydrates, proteins, and lipids; storage and
activation of vitamins; detoxification and excretion of endogenous
and exogenous products, among others. As liver function declines,
systemic overload increases, leading to a depletion in nutritional
status, which is evident even in the early stages of liver disease (1).
Sarcopenia, recognized as a muscular disease characterized by a
reduction in both the quality and quantity of muscle mass, has an
estimated prevalence of 37.5 % in patients with cirrhosis. When
present, it increases the mortality risk of this population by 2.6 times
(2).
Aiming at screening for sarcopenia and identifying the risk of poor
functional outcomes, the European Working Group on Sarcopenia in
Older People 2 (EWGSOP2) in 2019 suggested an algorithm involving
the following steps: (i) screening, using the SARC-F questionnaire
which subjectively assesses strength, assistance with walking, getting
up from a chair, climbing stairs, and falls; (ii) assessment of muscle
strength through methods such as handgrip strength (HGS) and the
chair stand test; (iii) evaluation of muscle quantity and quality using
body composition methods (3). As an alternative to SARC-F, Barbosa-
Silva et al. (2016) proposed the SARC-Calf tool, which adds calf
circumference to the subjective criteria of SARC-F (4).
Due to the symptomatic characteristics of patients with cirrhosis, such
as ascites and edema, the step of assessing muscle quality and
quantity becomes challenging, as it hinders the use of bioelectrical
impedance analysis, increasing the reliance on imaging methods such
as dual-energy X-ray absorptiometry (DXA) and computed
tomography (CT), which are costly and difficult to access in clinical
practice (5).
Given the challenges and uncertainties in assessing the presence of
sarcopenia in patients with cirrhosis, as well as the impact of its
development on the quality of life and survival of these individuals,
early identification is essential to establish effective clinical and
nutritional treatment. In this context, the objective of this study is to
identify the best method for diagnosing sarcopenia in patients with
cirrhosis, as well as to evaluate the concordance of subjective and
anthropometric methods – classically used in the assessment of these
patients – with sarcopenia diagnosed by DXA.

PATIENTS AND METHODS


Study design
This is a cross-sectional study conducted in the Infectious and
Parasitic Diseases Department of Professor Alberto Antunes University
Hospital, Maceió/Alagoas, Brazil, from October 2022 to November
2023.

Study groups
Patients aged ≥ 18 years and less than 70 years, of both sexes,
diagnosed with liver cirrhosis, were eligible for participation and
divided into two groups. One group had score Model for End-Stage
Liver Disease-sodium (MELD-Na) ≥ 15, eligible for Liver Transplant
(LT), while the other group had MELD-Na ≤ 14, with portal
hypertension. Eligible criteria for portal hypertension were ascites
presence, splenomegaly, esophagogastric varices, or the presence of
portosystemic collaterals (patent paraumbilical vein, splenorenal
collaterals, dilated left gastric veins, and short veins). Exclusion
criteria included: (a) neoplasia; (b) acute liver failure; (c) pregnant
and lactating women; (d) human immunodeficiency virus infection; (e)
patients listed for liver transplantation due to special conditions
(intractable pruritus, recurrent cholangitis, refractory ascites,
persistent hepatic encephalopathy); (f) history of organ failure
affecting nutritional status, such as renal replacement therapy,
respiratory, and cardiac failure.

Sample size
This is an exploratory study derived from an original research project
aiming to identify the prevalence of sarcopenia among LT candidates.
A relative risk of 3 for sarcopenia prevalence was expected,
considering a baseline prevalence of 25 % in the control group
(patients with liver cirrhosis but without LT indication). Assuming
80 % power and a 5 % alpha level, 19 patients were required in each
group (Group 1: MELD-Na ≤ 14; Group 2: MELD-Na ≥ 15).

Evaluation of liver disease severity


The severity of liver disease in patients was assessed MELD-Na scores
and participants were categorized into two groups: ≤ 14, indicating
patients not eligible for LT, and ≥ 15, indicating patients eligible for
LT. These scores were determined through a clinical evaluation
conducted by a specialized medical professional, combined with
laboratory test results obtained at the time of consultation.

Sociodemographic data and clinical assessment


Personal history, current disease history, presence of signs and
symptoms, prior hospitalizations related to hepatic disease
decompensation, lifestyle habits, etiology, and time of diagnosis were
collected using a standard form.

Nutritional/functional assessment
Nutritional and functional tests applied to individuals can be
visualized in table I.
Equipment and techniques
Weight and height measurements followed the technique
recommended by Lohman (1988), using a Filizola® digital scale and a
metal anthropometer (6). Arm circumference (AC) and calf
circumference (CC) were measured with a non-extensible tape
measure, while triceps skinfold (TSF) was assessed with a Lange®
caliper (6). Tetrapolar bioelectrical impedance analysis (BIA) by
Sanny® was used to determine the phase angle (PA). Appendicular
Skeletal Muscle Mass (ASM) was obtained through Dual-Energy X-ray
Absorptiometry (DXA) analysis using the Lunar Prodigy Primo system
from GE HealthCare, with a full-body anteroposterior incidence, and
the patient lying supine with extended legs, feet together, arms
extended alongside the body, without adornments. Muscle strength
was identified through the Individual performance in handgrip
strength (HGS) using the Jamar® dynamometer, measured three
times on the dominant hand by a trained professional.

Ethical considerations
All patients provided written informed consent. The study was
conducted following the ethical guidelines of the 1975 Helsinki
Declaration. The protocol was approved by the Ethics Committee on
May 26, 2022 (Opinion Number 5432777).

Statistical analysis
We utilized the Statistical Package for Social Science (SPSS®), version
26.0, for all analyses. Descriptive statistics included frequencies,
absolute and relative values (n/percentage), with continuous variables
reported as mean and standard deviation. The kappa concordance
test (κ) was used to evaluate the agreement between methods,
interpreted as poor (< 0.0), slight (0.01-0.2), fair (0.21-0.4), moderate
(0.41-0.6), substantial (0.61-0.8), and almost perfect (0.81-1.00) (15).
We initially compared individual diagnostic methods with muscle
mass as assessed by DXA. Subsequently, we combined techniques for
assessing muscle strength and mass to determine whether any of
these combinations showed concordance with the sarcopenia
diagnosis obtained via DXA. The alpha value was set at 5 %

RESULTS
We analyzed 45 patients, with the majority being male (68.9 %), and
a mean age of 47.5 ± 14.2 years. Most resided in rural areas (60 %),
and 57.8 % reported being married or in a stable relationship.
The most common etiology of liver disease was alcoholic (44.4 %).
Among the individuals analyzed, approximately 37.8 % had
comorbidities such as systemic arterial hypertension (SAH), diabetes
mellitus (DM), obesity, dyslipidemia, and hypothyroidism.
Additionally, 46.7 % reported episodes of hepatic decompensation in
the last 6 months, including upper gastrointestinal bleeding (UGIB),
ascites, and hepatic encephalopathy (HE) (Table II). Among these,
28.6 % reported a combination of ascites and HE, and 19 % had UGIB,
ascites, and HE in the last 6 months. The presence of ascites and/or
edema at the time of data collection is detailed in table II.
The prevalence rates of sarcopenia risk, low muscle strength, and
reduced muscle mass are shown in table III. The SARC-Calf identified
more patients at risk for sarcopenia compared to the SARC-F, with
rates of 20.5 and 13.3, respectively. It is noteworthy that, due to the
presence of lower limb edema and the consequent inability to
measure CC, the SARC-Calf was applied to fewer patients than the
SARC-F (86.7 of those evaluated).
The prevalence of low muscle strength was identified in 91.1 by the
chair stand test compared to 15.6 by handgrip strength. Therefore,
the chair stand test proved to be a more efficient screening method
for sarcopenia than handgrip strength, identifying nearly six times
more patients with reduced strength than dynamometry.
Muscle depletion was highly prevalent, observed in 40 % of the
evaluated patients. Interestingly, using the sarcopenia diagnostic
protocol suggested by EWGSOP2, the prevalence of sarcopenia varied
widely depending on the combination of assessment tools used. It
ranged from 2.6 % (SARC-Calf + HGS + ASM/ASMI) to 20.0 % (SARC-
Calf + Chair sit-and-stand test (15s) + ASM/ASMI), indicating
significant variability in the diagnosis of sarcopenia among
outpatients with cirrhosis. When positivity in any of the forms (SARC-F
or SARC-Calf) and strength tests (HGS or chair sit-and-stand test) was
considered, the prevalence increased to 24.4 %.
Notably, the combination of the chair stand test with reduced muscle
mass (ASM/ASMI) identified 44.4 % of patients with cirrhosis as having
both low strength and low muscle mass, classifying them as
sarcopenic. Furthermore, those identified with muscle depletion by
DXA were the same individuals classified as sarcopenic, indicating
that reduced muscle mass in this group necessarily reflects low
strength. This finding aligns with the sarcopenia screening sequence,
where decreased strength precedes muscle mass reduction, and
underscores the importance of assessing muscle mass in these
individuals.
To determine the best method for diagnosing sarcopenia in
outpatients with cirrhosis, we compared different muscle and
nutritional assessment techniques with muscle depletion diagnosed
by DXA. The concordance analysis (Table IV) showed that among
anthropometric assessments, CC demonstrated the highest
agreement with muscle depletion ( = 0.581; p < 0.001), successfully
identifying 60 % of patients with reduced muscle mass
(MMEA/IMMEA). This indicates that CC is the most reliable
anthropometric measure for identifying muscle depletion in this
population when DXA is unavailable.
Other anthropometric measures, such as AC ( = 0.341; p = 0.019)
and MMAC adequacy ( = 0.348; p = 0.014), showed fair agreement
with DXA being less effective than CC. BMI displayed slight agreement
( = 0.120; p = 0.198), highlighting its limited utility in detecting
sarcopenia in patients with cirrhosis.
Regarding subjective nutritional assessments, the RFH-GA ( = 0.364;
p = 0.014) and RFH-NPT ( = 0.143; p = 0.289) showed a fair level of
agreement with muscle depletion. These findings suggest that while
subjective assessments may offer some insights, they cannot replace
more objective measures, particularly DXA and CC, in accurately
diagnosing sarcopenia.
Therefore, identifying muscle depletion using CC, especially in
settings without DXA, appears to be a practical and effective
approach for diagnosing sarcopenia in outpatients with cirrhosis.

DISCUSSION
Studies confirm that early identification of nutritional risk, as well as
risk of sarcopenia and sarcopenia itself, is crucial for ensuring
accurate treatment, potential reversal of the condition, improved
prognosis, and quality of life for the affected individual (16-18). When
proposing to identify nutritional risk or sarcopenia risk, screening
instruments are used to maximize true positives within a sample, with
subsequent steps aiming to discard false positives (19,20).
Individuals with cirrhosis experience a progressively worsening
condition, often leading to episodes of decompensation that
frequently require hospitalization, thereby increasing morbidity and
mortality rates. Key complications include ascites, UGIB, and HE,
which elevate the mortality risk by 5 to 10 times in this population
(21). The average survival for patients experiencing these
complications is merely 1 to 2 years, while compensated individuals
have a survival expectancy of 10 to 12 years (22). Given its impact on
global health (as the 11th leading cause of death, accounting for 2
million fatalities) and its substantial cost (with $32.5 million spent in
the US alone in 2016) (21), preventing hepatic decompensation
through pharmacological or non-pharmacological interventions is
crucial to reduce hospitalizations, healthcare expenses, and improve
patients' quality of life.
Nutritional status is heavily impacted by cirrhosis progression.
Reduced food intake, energy-protein imbalances, altered
macronutrient and micronutrient metabolism, diminished absorptive
capacity, as well as muscle dysfunction and sarcopenia, are common
nutritional complications seen in individuals with cirrhosis (23).
As cirrhosis negatively impacts nutritional status, the presence of
nutritional and functional deficits also adversely affects the clinical
progression of patients with cirrhosis. This influence extends to
quality of life, with increased risks of infection, HE, ascites, and
mortality, making it a prognostic factor for individuals with liver
cirrhosis (24). However, the identification of nutritional deficits,
especially malnutrition and sarcopenia, remains a challenge in
cirrhosis due to the frequent occurrence of fluid retention (edema and
ascites) in these patients. This retention hampers the use of more
affordable and accessible anthropometric and body composition
measures, such as weight, CC, and bioimpedance, across various
clinical nutrition monitoring settings for these patients.
The EWGSOP2 recommends using the SARC-F tool for sarcopenia risk
screening (3). In a study involving patients with cirrhosis, Singla et al.
(2024) demonstrated good sensitivity of the SARC-F score for bedside
screening in the Indian population (25). However, a meta-analysis by
Voelker et al. (2021) suggested applying sarcopenia diagnostic
criteria independently of risk screening due to the SARC-F's low
sensitivity, which may lead to the detection of only severe cases (26).
Our findings support this, as the SARC-F and SARC-Calf showed low
efficacy in identifying individuals with low muscle strength and
depletion in outpatients with cirrhosis, indicating that these tools
should not be solely relied upon for sarcopenia diagnosis in this
population.
Our study is pioneering in that it evaluates sarcopenia prevalence
using different methods and assesses the agreement between
sarcopenia diagnosis, based on decreased strength (sit-to-stand test)
and muscle mass (DXA), and various nutritional and functional
assessment methods in outpatients with cirrhosis. Following the
diagnostic criteria for sarcopenia, decreased strength precedes
skeletal muscle depletion, which is why strength tests, such as the sit-
to-stand test and HGS, should precede body composition assessment.
In our work, we found that relying on HGS could result in a high
number of false negatives, potentially depriving many patients with
cirrhosis of timely and appropriate interventions involving physical
exercise and nutritional adjustments, which are currently the main
treatment options, given the lack of effective pharmacological
treatments (27).
Although HGS is widely used to measure strength, its limitations are
evident, as it primarily assesses hand and forearm muscles, which are
not critical for activities that involve supporting body weight. Despite
showing moderate correlation with strength in other body
compartments (28), HGS might not be as effective as the sit-to-stand
test, which is a more comprehensive tool for assessing functional
capacity and muscle power (3). Additionally, several mechanisms
contribute to muscle strength impairment in patients with cirrhosis,
including muscle quality changes, hormonal alterations, electrolyte
imbalances, and systemic complications (8,16,29).
DXA, a recommended method for body composition assessment,
accurately evaluates muscle mass and is suitable for individuals with
cirrhosis, especially since it can bypass ascites interference when
using appendicular skeletal muscle mass (ASM/ASMI) (3,16). Our
study confirmed the high prevalence of muscle depletion in
outpatients with cirrhosis, reinforcing the importance of incorporating
muscle mass measurement for sarcopenia diagnosis.
The sit-to-stand test emerged as a highly effective screening tool for
probable sarcopenia, as it identified the largest number of individuals
with low muscle strength. Its simplicity, requiring only a chair and
timer, makes it more accessible than HGS, and it can be employed
across different healthcare settings (30). In contrast CC proved to be
the most viable alternative for muscle mass assessment when DXA is
unavailable, demonstrating the best agreement with ASM/ASMI.
Interestingly, while the SARC-Calf incorporates CC as part of its
assessment - adding 10 points to the final score –, our findings
showed that CC alone presented a stronger correlation with muscle
depletion (ASM/ASMI) compared to SARC-Calf. This suggests that
isolating CC as an independent measure may enhance its utility in
clinical practice, particularly when the broader SARC-Calf framework
shows limitations in identifying low muscle strength and quality.
This association between CC and muscle mass was also identified by
Kawakami et al. (2020) in their study of Japanese adults, where CC
positively correlated with muscle mass measured by bioimpedance or
DXA, regardless of the presence of obesity. Therefore, CC can be
considered a useful diagnostic marker for sarcopenia (31).
However, it is important to acknowledge the limitations of using CC in
patients with lower limb edema, a common condition in cirrhosis.
Given this, the chair sit-and-stand test is recommended as an
alternative when edema precludes CC measurement, based on the
strong agreement observed in our study regarding sarcopenia
diagnosis.

Limitations and perspectives


The data were collected from outpatients with cirrhosis, meaning that
in more severe or decompensated cases, alternative criteria might
provide more accurate sarcopenia diagnosis. The inclusion criteria for
this study aimed to minimize confounding factors, which may have
consequently limited the participation of more compromised
individuals, such as those with hepatocellular carcinoma, cardiac,
renal, and/or pulmonary complications, or hepatic encephalopathy.
Therefore, the findings may not fully represent patients with more
advanced disease stages. However, by including patients based on
MELD-Na scores, an internationally recognized measure of disease
severity, our results can be extrapolated to patients who do not
present terminal-stage conditions.
Moreover, although DXA was chosen over computed tomography (CT)
— the gold standard for muscle assessment in liver disease – due to
greater accessibility, this limitation was mitigated by evaluating
appendicular skeletal muscle mass (ASM) and its index (ASMI). We
acknowledge that CT imaging, particularly in advanced cirrhosis,
where it is often performed for hepatic lesion monitoring or pre-
transplant evaluation, could provide more precise muscle
assessments and should be considered in future studies.
Finally, the etiology of liver disease may significantly influence
nutritional status, especially in alcoholic cirrhosis, as alcohol
interferes with nutrient absorption, leading to chronic malnutrition
and exacerbating nutritional deficits. However, no specific tools
currently exist for nutritional risk or status assessment based on
disease etiology. Future assessment tools could consider
incorporating alcoholic cirrhosis as a criterion, emphasizing its
nutritional impact.

CONCLUSION
Our study demonstrates that the EWGSOP2 algorithm tends to
underdiagnose sarcopenia in outpatients with cirrhosis, primarily due
to the low sensitivity of the SARC-F tool in this population. Therefore,
we suggest that the screening step be excluded or that CC
measurement be used as an alternative, provided there is no lower
limb edema.
The chair sit-and-stand test emerged as the most reliable method for
identifying low muscle strength, effectively capturing a greater
number of individuals with probable sarcopenia than HGS.
Additionally, CC measurement showed moderate concordance with
ASM/ASMI and could serve as a practical alternative in the absence of
imaging methods, although it may miss a considerable number of
patients with muscle depletion. Hence, CC is not sufficient as a
standalone diagnostic measure for sarcopenia in this population.
Our findings reinforce the critical need for incorporating imaging
techniques such as DXA or CT in the comprehensive care of patients
with cirrhosis to ensure accurate identification and appropriate
intervention for sarcopenia. Despite the limited availability of DXA in
routine clinical settings, its role in accurately assessing muscle mass
highlights the necessity for its inclusion, even if performed with
reduced frequency.
In alignment with the Delphi consensus from the Global Leadership
Initiative in Sarcopenia (GLIS) (32), which emphasizes the practicality
and feasibility of sarcopenia assessment components, we propose
that combining CC and the chair sit-and-stand test can serve as
feasible alternatives for diagnosing and monitoring sarcopenia in
cirrhotic patients, particularly in resource-limited settings where
imaging methods are not readily accessible.

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Table I. Nutritional and functional tests applied in outpatients with
liver cirrhosis
Test Characteristics Categories
Objective diagnosis of the Depleted: ASM
Appendicular
amount of muscle mass, < 20 kg for men
Skeletal Muscle
obtained by densitometry and < 15 kg for
Mass (ASM) and
(DXA), summing the muscle women, OR
Appendicular
masses of the upper and lower ASMI < 7 kg/m²
Skeletal Muscle
limbs. and < 5.5 kg/m²
Mass Index
ASMI was calculates using for men and
(ASMI)
ASM/height² women (3)
Depleted: AC
Arm adequacy <
Circumference Objective diagnosis of 90 % (7)
(AC) adequacy malnutrition. Not depleted:
% AC adequacy <
90 %
BMI (kg/m²) Real weight (kg) - for patients Malnutrition:
without ascites or edema in BMI < 18.5
lower limbs; kg/m² for adults
Or, (11) and BMI <
Dry weight (kg) - for patients 22.0 kg/m² for
with ascites (deducting 5 %, 10 the aged (12)
%, or 15 % of the current
weight depending on the
ascites classification (mild, Not
moderate, or severe) [8]) or malnutrition:
edema in lower limbs BMI ≥ 18.5
(discounting 1 kg, 3 kg, or 6 kg, kg/m²) for
if edema classified as mild, adults and BMI
moderate, or severe, ≥ 22.0 kg/m² for
respectively [9]); the aged
And
Real height (m) – patients aged
< 60 years (measure
performed in foot);
Or,
Estimated height - patients
aged ≥ 60 years (classified as
elderly in Brazil), height was
estimated using the Chumlea
technique (10)
Depleted: CC <
Calf
Objective diagnosis of muscle 34 cm for men
Circumference
depletion and < 33 cm for
(CC) (cm)
women (4);
Low strength
Handgrip Muscle strength/functional muscle: HGS <
strength (HGS) capacity screening, using 27 kg for men
(kgf) dynamometer and < 16 kg for
women (4)
Mid-arm muscle
Objective diagnosis of muscle Depleted: TSF
circumference
depletion. Calculated using AC adequacy <
(MAMC)
and triceps skinfold 90 % (7);
adequacy (%)
Diagnosis of cellular integrity,
Phase Angle
calculated from the resistance __
(PA) (°)
and reactance obtained by BIA
Royal Free Nutritional risk assessment (a
Hospital combination of the following With nutritional
Nutritional criteria: alcoholic hepatitis, risk, RFH-NPT ≥
Prioritizing Tool tube feeding, fluid overload, 1 point (13)
(RFH-NPT) and dietary intake)
Royal Free Subjective malnutrition Malnutrition
Hospital Global diagnosis (a combination of the (14);
Assessment following criteria: BMI, MAMC, well-noutrished
(RFH-GA) and dietary intake)
Sarcopenia screening. It uses Risk of
scores referring to 5 domains sarcopenia:
that involve strength, difficulty SARC-F ≥ 4 (3)
SARC-F and walking, difficulty standing, points or SARC-
SARC-Calf difficulty climbing stairs and CalF ≥ 11 points
history of falls. For the SARC- (4)
CalF, the WC measurement
was added
Muscle strength/functional Low strength
capacity screening muscle: sit-to-
Sit-to-stand test
stand test < 5 in
15 seconds (4)
Diagnosed using muscle Sarcopenia:
strength/functional capacity HGS or sit-to-
(HGS or sit-to-stand test and stand test with
Sarcopenia appendicular skeletal muscle low strength
mass (ASM or ASMI) muscle, and
ASM or ASMI
depleted (4)
Table II. Sociodemographic and clinical characteristics in outpatients
with liver cirrhosis
Characteristics n (%)
37
Adult
(82.2)
Age group
8
Elderly
(17.8)
11
White
(24.4)
Race
34
Black/brown
(75.6)
24
≤ Elementary school incomplete
(53.3)
Schooling
21
Other
(46.7)
14
No
Alcohol (31.1)
consumption 31
Ex-alcohol consumer
(68.9)
20
Alcohol
(44.4)
6
Autoimmune hepatitis
(13.3)
6
Etiology of Cryptogenic hepatitis
(13.3)
cirrhosis
Metabolic dysfunction associated fatty
3 (6.7)
liver disease
Alcohol + hepatitis B infection 3 (6.7)
7
Other
(15.5)
MELD-Na ≤ 14 22
(48.9)
23
≥ 15
(51.1)
7
Upper gastrointestinal bleeding
(15.5)
11
Hepatic encephalopathy
(24.4)
Cirrhosis
20
complications Ascites
(44.4)
10
Edema
(22.2)
MELD-Na: Model for End-stage Liver Disease-Sodium.
Table III. Prevalence of sarcopenia risk, low strength muscle, and
muscle depletion in outpatients with liver cirrhosis
Individ No (n Yes (n
Risk of sarcopenia
uals [%]) [%])
SARC-F 45 39 6 (13.3)
(86.7)
SARC-CalF 39 31 8 (20.5)
(79.5)
SARC-F/SARC-CalF 33 12
(73.3) (26.7)
Strength muscle No (n Yes (n
[%]) [%])
Chair sit-and-stand test (15s) 45 4 (8.9) 41
(91.1)
Hand grip strength (HGS) 48 38 7 (15.6)
(84.4)
Chair sit-and-stand test (15s)/Hand 45 4 (8.9) 41
grip strength (91.1)
Muscle mass (DXA) No (n Yes (n
[%]) [%])
ASM 45 27 18
(60.0) (40.0)
ASMI 45 30 15
(66.7) (33.3)
ASM or ASMI 45 25 20
(55.6) (44.4)
Sarcopenia No (n Yes (n
[%]) [%])
EWGSOP2 protocol (SARC-F + HGS + 45 42 3 (6.7)
ASM/ASMI) (93.3)
EWGSOP2 protocol (SARC-CalF + 39 38 1 (2.6)
HGS + ASM/ASMI) (97.4)
EWGSOP2 protocol (SARC-F + Chair 45 40 5 (11.1)
sit-and-stand test (15s) + ASM/ASMI) (88.9)
EWGSOP2 protocol (SARC-CalF + 39 32 8 (20.0)
Chair sit-and-stand test (15s) + (80.0)
ASM/ASMI)
EWGSOP2 protocol (SARC-F/SARC- 45 34 11
CalF + HGS/Chair sit-and-stand test (75.6) (24.4)
(15s) + ASM/ASMI)
Chair sit-and-stand test (15s) + 45 25 20
ASM/ASMI (55.6) (44.4)
HGS + ASM/ASMI 45 38 7 (15.6)
(84.4)
ASM: appendicular skeletal muscle; ASMI: appendicular skeletal
muscle index; EWGSOP2: European Working Group on Sarcopenia in
Older People 2.

Table IV. Concordance between muscular mass by dual-energy X-ray


absorptiometry (DXA) and anthropometrics assessment and
subjective instruments used in outpatients with liver cirrhosis
Muscular mass Concordanc
(ASM/ASMI) e
Adequa Deplet
Kapp
Total te ed p
a
n = 25 n = 20
Anthropometric assessment
Not 41
24 17
Malnutri (91.1)
(96.0) (85.0)
BMI (kg/m²) tion 0,120 0.198
Malnutri 4 (8.9) 3
1 (4.0)
tion (15.0)
Arm Not 20 15 5 0.34 0.019
circumference Malnutri (44.4) (60.0) (25.0) 1
adequacy tion
25
10 15
Malnutri (55.6)
(40.0) (75.0)
tion
Adequat 18 14 4
Muscular mass
e (40.0) (56.0) (20.0) 0.34
circumference 0.014
Deplete 27 11 16 8
adequacy
d (60.0) (44.0) (80.0)
Adequat 25 23 8
Calf e (64.1) (92.0) (40.0) 0.58 <
circumference Deplete 14 12 1 0.001
2 (8.0)
d (35.9) (60.0)
Subjective Nutritional Assessment
Without 15
10 5
nutrition (33.3)
(40.0) (25.0)
al risk
RFH-NPT 0.143 0.289
With 30
15 15
nutrition (66.7)
(60.0) (75.0)
al risk
Well 27
19 8
nourishe (60.0)
(76.0) (40.0) 0.36
RFH-GA d 0.014
4
Malnutri 18 11
8 (24.0)
tion (40.0) (60.0)
ASM: appendicular skeletal muscle mass; ASMI: appendicular skeletal
muscle mass index; BMI: body mass index; HGS: handgrip strength;
RFH-GA: Royal Free Hospital – Global Assessment; RFH-NPT: Royal
Free Hospital - Nutritional Prioritizing Tool.

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