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The incidence of sarcopenia among hospitalized older patients: results from the Glisten studyAnna Maria Martone1, Lara Bianchi2, Pasquale Abete3, Giuseppe Bellelli4, Mario Bo5, Antonio Cherubini6, Francesco Corica7, Mauro Di Bari8, Marcello Maggio9, Giovanna Maria Manca10, Emanuele Marzetti1, Maria Rosaria Rizzo11, Andrea Rossi12, Stefano Volpato2,13,*, Francesco Landi1 the GLISTEN Group Investigators1
Version of Record online: 14 SEP 2017
How to Cite
2017) The incidence of sarcopenia among hospitalized older patients: results from the Glisten study. Journal of Cachexia, Sarcopenia and Muscle, doi: 10.1002/jcsm.12224., , , , , , , , , , , , , , and (
evidence is emerging on the importance of lean body mass during periods
of illness and recovery. The preservation of lean body mass during such
periods of intense stress impacts both patient and treatment outcomes.
However, data concerning the incidence of sarcopenia among older people
during hospitalization are scarce. The objective of this study was to
evaluate the development of sarcopenia in a sample of hospitalized older
used data of 394 participants from the multicentre Italian Study
conducted by the Gruppo Lavoro Italiano Sarcopenia—Trattamento e
Nutrizione (GLISTEN) in 12 Acute Care Wards (Internal Medicine and
Geriatrics) of University Hospitals across Italy. This study was
designed to determine the prevalence of sarcopenia at hospital admission
and the change in muscle mass and strength during hospitalization.
Sarcopenia was defined as low skeletal mass index (kg/m2)
along with either low handgrip strength or slow walking speed [European
Working Groups on Sarcopenia in Older People (EWGSOP) criteria].
Estimation of skeletal muscle mass was performed by bioelectrical
impedance analysis (BIA).
mean age of the 394 enrolled patients (including 211 females who
accounted for 53% of the sample) was 79.6 ± 6.4 years. Among those
without sarcopenia at hospital admission, 14.7% of the study sample met
the EWGSOP sarcopenia diagnostic criteria at discharge. The incidence of
sarcopenia during hospitalization was significantly associated with the
number of days spent in bed but was not correlated with the total
length of hospital stay. In particular, patients who developed
sarcopenia spent an average of 5.1 days in bed compared with 3.2 days
for those with no sarcopenia at discharge (P = 0.02). Patients
with sarcopenia showed a significantly lower body mass index compared
with non-sarcopenic peers (25.0 ± 3.8 kg/m2 vs. 27.6 ± 4.9 kg/m2, respectively; P < 0.001).
Similarly, the skeletal mass index at admission was significantly lower
among patients who developed sarcopenia during hospital stay.
sarcopenia during hospital stay is relatively common and is associated
with nutritional status and the number of days of bed rest.
is one of the most important risk factors for mobility impairment,
falls, disability, loss of independence, hospitalization, and death
among older people.
The concept of sarcopenia is encountered increasingly often in research
and clinical practice, not only in geriatric medicine but also in other
specialties. New evidence is emerging on the importance of lean body mass during periods of illness and recovery.
Sarcopenia is considered a geriatric syndrome described as the
impairment of muscle function due to the loss of skeletal muscle mass,
which occurs during the aging process.[3, 4]
clinical implications of sarcopenia have been consistently described
across different settings, including community dwelling samples, nursing
homes, and acute care units.[5, 6]
According to a recent systematic review, the prevalence of sarcopenia
is significantly high in most of the geriatrics settings, but
estimations impressively vary across studies because of different
population characteristics, diagnostic criteria, and methods used to
assess muscle mass and physical performance. When assessed according to
the European Working Groups on Sarcopenia in Older People (EWGSOP)
prevalence rates range from 1 to 29% among community-dwelling
populations and from 17.4 to 32.8% among institutionalized persons. More recently, Bianchi and colleagues demonstrated that among older Italian patients admitted to hospital, sarcopenia, defined according to the EWGSOP criteria, was very common, and its prevalence raised steeply with increasing age in both genders.
concerning the incidence of sarcopenia among older people during
hospital stay are scarce. In older patients, besides the negative effect
of the acute event, hospitalization itself might represent an
additional stressor in terms of reduced caloric intake, extremely low
physical activity, or prolonged bed rest. For example, experimental
studies suggest that in healthy older people, prolonged bed rest is
associated with significant decrease in muscle protein synthesis, lower
extremity lean mass, and strength.[10, 11]
The aim of this study was to evaluate the onset of sarcopenia in a
sample of hospitalized older patients. We conducted a multicentre
observational study of older patients admitted to 12 acute care wards in
Italy. The primary objective of this study was to estimate the
incidence and the clinical correlates of sarcopenia in a large sample of
hospitalized older patients without sarcopenia at the time of hospital
are from the Gruppo Lavoro Italiano Sarcopenia—Trattamento E Nutrizione
(GLISTEN) project, an observational study performed in geriatric and
internal medicine acute care wards of 12 Italian hospitals (Monza,
Turin, Ferrara, Verona, Parma, Florence, Ancona, Rome, Napoli I, Napoli
II, Cagliari, Messina). Methodology of the GLISTEN project has been
described in detail elsewhere.
In brief, the study was designed to investigate the prevalence and
clinical correlates of sarcopenia in older hospitalized patients in
Italy and to estimate the incidence of sarcopenia during hospital stay.
All participating centres obtained ethical approval from their
institutions, and all participants signed a written consent.
Study design, data collection, and sample
All patients aged 65 years or more (n = 655)
consecutively admitted to participating wards from February 2014 to May
2014 entered the study protocol. The only exclusion criterion was the
unwillingness to take part to the study. For the present study, we
included only patients without sarcopenia at baseline assessment (n = 428).
Six patients died during the hospital stay, and 28 were not included
for missing values in the variables of interest. The final sample was
therefore comprised of 394 participants (Figure 1).
Application of the EWGSOP algorithm for sarcopenia case finding in the GLISTEN sample.
patients were assessed within the first 2 days of hospital admission
and followed until discharge (within 24 h of hospital discharge).
Participants underwent comprehensive geriatric assessment (CGA),
including demographic characteristics, functional status, cognitive and
mood assessment, medications use, admission and discharge diagnoses, and
biochemical tests. A variety of information sources, such as direct
observation, interviews with the patient, family, friends or formal
service providers, and review of clinical records, both medical and
nursing, were used. Finally, objective measurers of physical performance
(handgrip strength and 4 m usual walking speed test) were assessed at
hospital admission and before discharge.
Assessment of sarcopenia
was defined, according to EWGSOP criteria, as the presence of low
muscle mass plus low muscle strength or low physical performance.
mass was measured by bioelectrical impedance analysis (BIA).
Bioelectrical impedance analysis resistance (Ohms, Ω) was obtained using
a Quantum/S Bioelectrical Body Composition Analyser (Akern Srl,
Florence, Italy) with an operating frequency of 50 kHz at 800 mA.
Whole-body BIA measurements were taken between the right wrist and ankle
with the patient in a supine position. Muscle mass was estimated using the equation developed by Janssen and colleagues[13, 14]:
height is measured in cm; BIA resistance is measured in Ω; for gender,
men = 1 and women = 0; and age is measured in years. This BIA equation
was developed and cross-validated against magnetic resonance imaging
measures of whole-body muscle mass.
The skeletal muscle index [SMI (kg/m2)] was obtained dividing absolute muscle mass by squared height. Using the cutoffs indicated in the EWGSOP consensus paper, low muscle mass was classified as SMI less than 8.87 and 6.42 kg/m2
in men and women, respectively. These cutoffs were similar to those
obtained among 2276 elderly women and 2223 elderly men from the Third
National Health and Nutrition Examination Survey (NHANES III).[15, 16]
strength was assessed by grip strength, measured using a hand-held
dynamometer (JAMAR hand dynamometer Model BK-7498, Fred Sammons Inc.,
Brookfield, IL). Three trials for each hand were performed, and the
highest value of the strongest hand was used in the analyses.
BMI-adjusted values were used to identify low muscle strength.
Cut-points were similar to those obtained among 469 men and 561 women
(age range from 20 to 102 years) from the InCHIANTI study population.
speed was evaluated measuring participants' usual gait speed (in meters
per second) over a 4 m course. A cutoff point of 0.8 m/s or less
identified participants with low physical performance.
variables (age, gender, smoking habit, education) were assessed through
clinical interview at hospital admission. Functional status in basic
activities of daily living (ADL) was measured according to the
participants' self-reported difficulty in performing each of six
activities: getting in and out of a bed, bathing, dressing, eating,
continence, and using the toilet. Severe ADL disability was defined as
the presence of difficulty in three or more activities. Cognitive functioning was assessed using the Short Portable Mental Status Questionnaire.
Patients with scores ≥ 3 were considered to be cognitively impaired.
Depression was assessed by means of the 15-item Geriatric Depression
Scale, where the cutoff of > 5 points suggests significant depressive
hospital stay, days of bed rest were considered those spent in the bed
for 24 h. The days of fasting were considered according to the
non-consumption of at least two main meals.
Diagnoses of specific
medical conditions were gathered from the patient, attending physicians,
and by a careful review of medical charts; comorbidity was assessed
using the Charlson Comorbidity Index by adding scores assigned to
specific discharge diagnoses. Assessors recorded all drugs currently
taken by the participants at admission: brand name, formulation, and
daily dosage were registered. All drugs were coded according to the
Anatomical Therapeutic and Chemical codes. The number of drugs taken was
the present study, we selected all patients without sarcopenia at
baseline (hospital admission). After excluding six patients who died
during hospital stay and 28 for missing values, the final sample was
composed of 394 participants. Patients with incident sarcopenia during
hospital stay were identified using the algorithm developed by the
EWGSOP for sarcopenia case-finding and screening in practice (Figure 1).
Data were analysed to obtain descriptive statistics. Continuous
variables are presented as mean ± standard deviation. Differences in
socio-demographic, functional, and clinical characteristics between
patients with or without incident sarcopenia were analysed in different
ways. Quantitative parameters with normal distribution were tested by
one-way analysis of variance, after a pretest for homogeneity of
variances. If distribution was not normal, the non-parametric
Kruskal–Wallis rank test was used. Categorical variables were analysed
by the χ2 test. A P value lowers than 0.05 was chosen for statistical significance.
relationship between incident sarcopenia and clinical and functional
variables was estimated by deriving odds ratios (ORs) from multiple
logistic regression models. Sarcopenia was included as the dependent
variable in such models. Based on previous researches, we considered
age, gender, length of hospital stay, functional ability (ADL score),
cognitive performance, comorbidity, and BMI as factors potentially
associated with incident sarcopenia and included them as independent
variables in the models. We provide estimates of association while
adjusting for potential confounders by deriving crude and adjusted ORs
and the corresponding 95% confidence intervals (CIs) from these models.
All analyses were performed using SPSS software (version 11.0, SPSS
Inc., Chicago, IL).
mean age of the 655 enrolled patients in the GLISTEN study (including
340 females who accounted for 51.9% of the sample) was 81.0 ± 6.8 years
(82.3 ± 6.6 and 79.6 ± 6.0, in women and men, respectively). Sarcopenia
at hospital admission was diagnosed in 227 (34.7%) patients (Figure 1).
Among patients without sarcopenia at hospital admission (n = 394), 58 participants (14.7%) met the EWGSOP sarcopenia diagnostic criteria at hospital discharge (Figure 1).
More than 50% of those who developed sarcopenia during hospital stay
showed over 10% muscle mass loss compared with baseline values.
Patients who developed sarcopenia (Table 1) were significantly older than those who did not (82.0 ± 7.2 vs. 79.2 ± 6.2 years, respectively; P < 0.01).
Participants with incident sarcopenia during hospital stay showed
significantly lower baseline BMI compared with patients who did not
develop sarcopenia (25.0 ± 3.8 kg/m2 vs. 27.6 ± 4.9 kg/m2, respectively; P < 0.001).
Similarly, SMI at hospital admission was significantly lower among
patients who developed sarcopenia during hospital stay (8.4 ± 1.5 kg/m2 vs. 9.0 ± 1.8 kg/m2, respectively; P = 0.01).
Participants with greater impairments in daily activities (by means ADL
score) and cognitive performance (according to the SPMSQ score) showed
higher incidence of sarcopenia at discharge. Finally, the incidence of
sarcopenia during hospitalization was significantly associated with the
number of days spent in bed, while it was only marginally correlated
with the total length of hospital stay. In particular, patients with
incident sarcopenia spent an average of 5.4 ± 6.7 days in bed (more than
28% of the length of hospital stay) compared with 3.2 ± 5.3 days (18%
of the length of hospital stay) among participants without sarcopenia at
discharge (P = 0.02).Table 1. Selected general characteristics and comorbidities of study participants according to the incidence of sarcopenia
After multivariable adjustment, (Table 2)
we found an increased and independent likelihood of developing
sarcopenia during hospital stay with ADL disability (OR: 1.23; 95% CI
1.01–1.49) and length of bed rest (OR: 1.05; 95% CI 1.01–1.12).
Conversely, a decreased probability of being sarcopenic at hospital
discharge was detected with increasing BMI (OR: 0.92; 95% CI 0.86–0.98)
and baseline SMI (OR: 0.43; 95% CI 0.29–0.61).Table 2. Unadjusted and adjusted models for risk of incident sarcopenia in the study population.
evaluation of the impact of hospitalization on the onset of sarcopenia
among frail older patients is an important and intricate issue. In the
present study, we explored the incidence of sarcopenia during hospital
stay and the association of different domains with incident sarcopenia
in a large sample of hospitalized older patients. Our data show that
sarcopenia develops in approximately 15% of hospitalized elderly
patients. Considering that, at the time of hospital admission, the
prevalence of sarcopenia is around 35%;
this means that half of the patients present with sarcopenia at
discharge. Furthermore, our findings show that the days of bed rest and
baseline disability exert an important influence on the onset of
sarcopenia, independent of age, gender, and other clinical and
functional variables. Greater muscle mass and good nutritional status at
hospital admission emerged as protective factors against incident
Sarcopenia is caused by the simultaneous reduction in
the number of muscle fibres and atrophy of the remaining myocytes,
likely as a result of lower rate of myofibrillar protein synthesis and
enhanced myonuclear elimination via an apoptosis-like mechanism.[21, 22]
These phenomena reflect a progressive reduction of anabolism and
increased catabolism, along with reduced muscle regeneration capacity.
Histological sections of aged muscles have also shown increased
infiltration of non-contractile tissue (i.e. collagen and fat).
Muscle mass loss is linked, although not linearly, with reduced force generation and impaired muscle performance.
Many factors are involved in the age-dependent muscle decline: the
aging processes itself, genetic susceptibility, behavioural factors
(e.g. less-than-optimal diet, prolonged bed rest, sedentary lifestyle),
chronic health conditions, and several drugs.
In this respect, it is important to highlight that our results show
that the days of inactivity are an important risk factor for the onset
of sarcopenia. On the other hand, in agreement with previous
we found a significant association between baseline BMI and SMI value
the incidence of sarcopenia, with patients with higher BMI and greater
SMI having a lower likelihood of developing sarcopenia during hospital
stay. Malnutrition per se is a powerful risk factor for sarcopenia and
might well explain the increased prevalence and incidence of sarcopenia
in patients with lower BMI.
Loss of appetite and/or reduction of food intake, usually observed
during hospitalization, can lead to muscle wasting, decreased
immunocompetence, and an increased rate of disease complications. In
particular, a reduction in food intake along with physical inactivity
leads to significant losses in muscle mass and strength.
composition and function are regulated by muscle protein turnover rate.
Impaired muscle protein synthesis may be due to many factors including
inadequate nutritional intake, deficit in post-absorptive protein
synthesis, and reduced anabolic response to nutrient ingestion,
especially amino acids.[28, 29]
It has been shown that physical exercise and targeted oral nutritional
supplementation may improve muscle health through various mechanisms.
findings have potentially relevant clinical implications. Physical
inactivity during in-hospital bed rest and malnutrition can have a
negative synergistic effect on muscle protein synthesis, favouring the
subsequent onset of sarcopenia. The preservation of muscle mass and
function is increasingly recognized as a crucial factor for promoting
healthy aging and better outcomes in different healthcare settings. As
such, sarcopenia represents an ideal target for interventions aimed at
preventing or postponing the occurrence of negative health-related
events in late life. At present, multicomponent interventions, involving
the combination of physical activity and nutrition (in particular
adequate protein intake) are the only ‘interventions’ to prevent
In particular, an adequate nutritional support and an early
mobilization program during hospital stay are essential for preventing
sarcopenia. For this reason, it is very important to promptly arrange
rehabilitation services for frail older inpatients to avoid bed
immobilization and treat potentially disabling conditions. Programs that
meet these needs can reduce the number of severely disabled persons, or
at least delay their entering a critically disabled state.
interpreting our findings, some limitations should be considered. First,
as in all observational studies, results may be confounded by
unmeasured factors. However, our homogeneous population of hospitalized
older people minimizes the possibility that patients without sarcopenia
at hospital discharge had substantially better healthcare or health
knowledge than those with incident sarcopenia. However, because of the
use of an extensive multidimensional assessment approach, the present
study could comprehensively investigate the different domains
influencing the incidence of sarcopenia. This made it possible to
control for a large number of potential confounders. Despite this
effort, it is still possible that differences between study groups may
have biased the results and conclusions. For example, biomarkers that
potentially correlate with sarcopenia (i.e. vitamin D and inflammatory
markers) were not considered. Second, the use of BIA for muscle mass
assessment presents some drawbacks mainly due to hydration problems
frequently observed in older persons that may result in underestimation
of body fat and overestimation of fat-free mass. On the other hand, BIA
is inexpensive, easy to use, readily reproducible, and appropriate for
both ambulatory and bedridden patients, considered as a portable
alternative to dual energy X-ray absorptiometry.[31, 32] As such, its standardized use may favour the widespread assessment of body composition in everyday clinical practice.
Another important limitation that needs to be considered in the
interpretation of the results is the lack of data about daily food
intake. Even though the days of fasting did not significantly differ
between patients who developed sarcopenia and those who did not, it is
possible that the intake of specific nutrients (e.g. protein intake or
oral supplementation) might be different. Finally, we were not able to
formally differentiate cases of sarcopenia from cases of cachexia, a
condition highly prevalent in acute care wards. Although after the
exclusion of cases with very low BMI ( < 20 kg/m2), the
prevalence of sarcopenia at hospital admission was not substantially
modified (31.9%), the possibility cannot be ruled out that we
overestimated the true prevalence of sarcopenia.
these limitations, our data support the concept that there is an urgent
need to screen for sarcopenia at an early stage—for example, at
hospital admission and/or during hospital stay—to initiate prevention
and specific interventions to avoid the debilitating consequences of
this condition. For the construction of a practical conceptual model,
sarcopenia may be considered the central element of the physical frailty
By establishing a specific biological basis (i.e. skeletal muscle
decline) of physical frailty, new approaches may be determined for the
development of interventions designed to reduce or reverse this
conclusion, the results of this study show that the number of patients
who develop sarcopenia during hospitalization is relatively high. The
onset of sarcopenia is directly related to the nutritional status and
the number of days of bed rest. This is of particular interest
considering that during a period of acute illness, the loss of lean body
mass can both affect the patient's recovery outcomes and treatment
plans. Preventing the loss of muscle mass during hospitalization,
through specific nutritional programs and early mobilization, might
improve disease-specific and functional outcomes.[38, 39]
authors certify that they comply with the ethical guidelines for
publishing in the Journal of Cachexia, Sarcopenia and Muscle: update
Conflict of interest
Maria Martone, Lara Bianchi, Pasquale Abete, Giuseppe Bellelli, Mario
Bo, Antonio Cherubini, Francesco Corica, Mauro Di Bari, Marcello Maggio,
Giovanna Maria Manca, Emanuele Marzetti, Maria Rosaria Rizzo, Andrea P.
Rossi, Stefano Volpato, and Francesco Landi declare that they have no
conflict of interest.