Clinical Nutrition 32 (2013) 772e776

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Clinical Nutrition
journal homepage: http://www.elsevier.com/locate/clnu

Original article

Sarcopenia: Prevalence and prognostic significance in hospitalized

patients
Salah Gariballa a, b, *, Awad Alessa a
a
Internal Medicine, Faculty of Medicine & Health Sciences, United Arab Emirates University (UAEU), UAE
b
University of Sheffield, UK

a r t i c l e i n f o s u m m a r y

Article history: Background: Sarcopenia is prevalent in older populations with many causes and varying outcomes
Received 9 October 2012 however information for use in clinical practice is still lacking.
Accepted 18 January 2013 Aims: The aim of this report is to identify the clinical determinants and prognostic significance of sar-
copenia in a cohort of hospitalized acutely ill older patients.
Keywords: Methods: Four hundred and thirty two randomly selected patients had their baseline clinical charac-
Sarcopenia
teristic data assessed within 72 h of admission, at 6 weeks and at 6 months. Nutritional status was
Older people
assessed from anthropometric and biochemical data. Sarcopenia was diagnosed from low muscle mass
Outcome
Nutrition
and low muscle strength-hand grip using anthropometric measures based on the European Working
Acute illness Group criteria.
Results: Compared with patients without sarcopenia, those diagnosed with sarcopenia 44 (10%) were
more likely to be older, have more depression symptoms and lower serum albumin concentration. The
length of hospital stay (LOS) was significantly longer in patients diagnosed with sarcopenia compared
with patients without sarcopenia [mean (SD) LOS 13.4 (8.8) versus 9.4 (7) days respectively, p ¼ 0.003].
The risk of non-elective readmission in the 6 months follow up period was significantly lower in patients
without sarcopenia compared with those diagnosed with sarcopenia (adjusted hazard ratio .53 (95% CI:
.32 to .87, p ¼ 0.013). The death rate was also lower in patients without sarcopenia 38/388 (10%),
compared with those with sarcopenia 12/44 (27%), p-value ¼ .001.
Conclusion: Older people with sarcopenia have poor clinical outcome following acute illness compared
with those without sarcopenia.
Ó 2013 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.

1. Introduction An important example of this challenge is sarcopenia, a condition

An important challenge of modern medicine is to distinguish
physiological changes associated with the process of ageing from
disease and adverse life style factors whose cumulative effects ac-
count for many of the adverse events in older people. Although
a number of these changes and events lead to progressive decline in
health many are responsive to treatment. This has created a need
for additional knowledge of age-related changes, which has
importance in the treatment and prevention of disease, and in
maintaining good health and quality of life in an ageing population.
* Corresponding author. Department of Internal Medicine, Faculty of Medicine
and Health Sciences, United Arab Emirates University, PO Box 17666, Al-Ain, UAE.
Tel.: þ971 37137659; fax: þ971 37672995.
E-mail address: s.gariballa@uaeu.ac.ae (S. Gariballa).
which is prevalent in older populations with many causes and
varying outcomes.1 It is a syndrome characterized by progressive
decline in skeletal mass, decreased strength and functional status
and associated with physical disability, poor quality of life and
death.2,3 There are a number of mechanisms involved in the aeti-
ology and pathogenesis of sarcopenia and their contribution vary
over time. Recognizing underlying causes is expected to help guide
treatment and therefore minimize adverse outcomes.4e6 Currently
the presence of low muscle mass and low muscle function (strength
or performance) are used for the diagnosis of sarcopenia.2,5,6
Although sarcopenia has emerged as an acceptable syndrome
which predict outcomes not many data on hospitalized patients are
available. Furthermore a valid and reproducible measurement
technique of sarcopenia suitable for clinical practice is still a chal-
lenge. The aim of this report is to measure the prevalence and
prognostic significance of sarcopenia in a cohort of acutely ill older
patients.

0261-5614/$ e see front matter Ó 2013 Elsevier Ltd and European Society for Clinical Nutrition and Metabolism. All rights reserved.
http://dx.doi.org/10.1016/j.clnu.2013.01.010

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2. Methods 2.3. Statistical analyses

2.1. Subjects
Four hundred and thirty two unselected acutely ill older pa-
tients who took part in a randomized controlled trial with complete
data were included.7 Inclusion criteria were: age  65 years; stable
medical condition and able to sign an informed written consent
form. Patients excluded from the study were those with severe
medical or psychiatric illness including those with malignancy,
severe dementia and living in institution. The study received local
research ethics committee approval.
All patients had baseline clinical assessment such as de-
mographic and medical data, current diagnosis, history of chronic
illnesses, smoking, alcohol and drug intake, nutritional status and
disability measured using the Barthel score. The Barthel scores 10
functions on a scale 0 (fully dependent) to 20 (independent). The
Barthel Score posses certain advantage, including completeness,
sensitivity to change suitability for statistical manipulation and
greater familiarity due to more widespread use. It is also a more
reliable and less subjective score for assessing disability.8 Nutri-
tional status was assessed from anthropometric, haematological
and biochemical data.7 All anthropometric measurements were
performed using standard methods with intra observer’s differ-
ences assessed prior to the commencement of the study. Mid-arm
circumference (MAC) and triceps skin folds (TSF) were measured
by a flexible tape and Happened Skin fold callipers accurate to
.2 mm (Practical Metrology Sussex UK) respectively and the mean
of three measures was recorded. Dietary intakes were measured
using a validated food diary.6 The local Pathology Laboratory
performed routine tests including haemoglobin, albumin and
transferrin measurements. C-reactive protein (CRP) concentration,
a marker of tissue inflammation (severity of illness) was meas-
ured by a modified latex-enhanced immuno-turbidimetric assay
(normal range £ 10 mg/L). The inter-assay coefficient of variation
(C.V.) was 3.9%.
2.2. Diagnosis of sarcopenia2,3
The European Working Group on Sarcopenia in Older people
(EWGSOP) criteria was used to diagnose sarcopenia. The EWGSOP
recommends using the presence of both low muscle mass and low
muscle function (strength or performance) for the diagnosis of
sarcopenia. For this study we used the anthropometric measures of
low muscle mass and low muscle strength-hand grip as a measure
of muscle function.
Statistical analyses were performed with SPSS software, version
19.0 (SPSS Inc., Chicago). Descriptive tests (mean [SD]) were used to
describe the baseline characteristics of the subjects. Independent
student-t test was used to test between group differences with a p-
value of <.05 regarded as statistically significant. A Cox propor-
tional hazards model was used to examine the 6-month risk of non-
elective readmission and mortality between patients with sarco-
penia and those without sarcopenia after adjusting for other clin-
ical risk indicators including age, disability (Barthel score),
smoking, body mass index (BMI), tissue inflammation (CRP)] and
serum albumin. Risks of readmission and 6-month mortality pre-
sented graphically using the KaplaneMeier (KeM) survival curve
and assessed using the log rank test.
3. Results
All 432 acutely ill older patients who took part in a previously
published randomized controlled trial with complete data were
included in this analysis.7 Forty- four out of 432 patients (10%) were
diagnosed with sarcopenia. Table 1 shows baseline clinical char-
acteristics according to the presence of the diagnosis of sarcopenia
including gender, smoking, alcohol consumption, disability,
depression and quality of life scores, tissue inflammation (CRP),
haemoglobin, albumin and transferrin. Compared with patients
without sarcopenia, those diagnosed with sarcopenia were more
likely to be older, have more depression symptoms and lower
serum albumin concentration. Stratification of subjects into groups
according to body mass index (BMI) categories revealed that 62%
(13/21) of those underweight (BMI < 18.5) had sarcopenia com-
pared with 13% (22/174) of those with normal weight (BMI 18.5e
24.99) and 2% (4/199) in overweight/obese patients (BMI  25)
[p ¼ 0.001].
The length of hospital stay (LOS) was significantly longer in
patients diagnosed with sarcopenia compared with patients
without sarcopenia [mean (SD) LOS 13.4(8.8) versus 9.4(7) days
respectively, mean difference 4 days (95% C.I 2e6), p .003]. Cox
regression analysis showed that the risk of non-elective read-
mission in the 6 months follow up period was significantly lower in
patients without sarcopenia compared with those diagnosed with
sarcopenia after adjustment for other clinical risk indicators, with
a hazard ratio of .53 (95% CI: .32 to .87, p ¼ 0.013) (Table 2). Sig-
nificantly higher number of patients with sarcopenia 24/44 (55%)
were readmitted to hospital in the 6 months follow up period
compared with those without sarcopenia 125/388 (32%), p ¼ 0.001
(Fig. 1). After adjustment for other clinical risk indicators Cox

Table 1
2.2.1. Muscle strength-hand grip
Baseline characteristics of subjects according to presence or absence of sarcopenia.
This was measured using a handgrip dynamometer (Practical
Metrology, Sussex, and UK). Subjects used their dominant hand Variable Sarcopenia Not sarcopenia
(n ¼ 44) (n ¼ 388)
unless this was unusable (arms in plaster, recent stroke weakness).
Three measurements were taken and the mean calculated. Using Age (SD) * 79 (7) 77 (6)
Gender, female 29 (66) 176 (45)
the cut-off points of the EWGSOP low muscle strength was classi-
Smoking Never smoked 17 (39) 118 (30)
fied as muscle strength-hand grip less than 30 kg and 20 kg in men Ex smoker 16 (36) 200 (52)
and women respectively. Current smoker 11 (25) 70 (18)
Alcohol  14 units 5 (11) 51 (13)
Barthel score 15.3 (4.8) 16.1 (4.6)
Geriatric depression score * 21.2 (4) 20 (3)
2.2.2. Muscle mass assessment
SF-36 score 75 (19) 80 (21)
The muscle mass was measured by mid-arm muscle circum- C-reactive protein mg/L 51 (59) 52 (74)
ference (MAMC) using the following formula: Haemoglobin g/dl 12.3 (2) 12.7 (2)
MAMC ¼ MAC  (3.14  triceps skin fold thickness). Low muscle Albumin g/L * 35.5 (5) 38 (5)
mass was classified as MAMC less 21.1 cm and 19.2 cm in men and Transferrin g/L 2.03 (.58) 2.17 (.49)

women respectively.2,3 *P < 0.05.

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774 S. Gariballa, A. Alessa / Clinical Nutrition 32 (2013) 772e776
Table 2
The Cox’s proportional hazard analysis of the relationship between sarcopenia and other prognostic variables and hospitalised patients’ 6-month non-elective readmission.
Variable Regression coefficient
Age (years) .003
Barthel score (0e20) .017
Smoking (never, ex, current) .162
BMIþ .025
BMI 2 (BMI-mean BMI)2 .023
Sarcopenia (yes/no) .645
C-reactive protein (mg/L) .004
Serum albumin (g/L) .013
*P < 0.05, þ BMI ¼ Body mass index.
regression also suggests that the hazard or risk of dying, up to 6
months was less in patients without sarcopenia compared with
those diagnosed with sarcopenia, hazard ratio .45 (95% CI: .21e.97),
p ¼ 0.043) (Table 3). Fig. 2 shows the death rate was higher in the
sarcopenia patients 12/44 (27%), compared with those without
sarcopenia 38/388 (10%), p-value ¼ .001.
4. Discussion
This study shows that older patients with the diagnosis of sar-
copenia had poor clinical outcome over 6-month period following
acute illness compared with those without sarcopenia after
adjusting for a number of important poor prognostic indicators.
Sarcopenia leads to impaired ability to perform activities of daily
living, disabilities, loss of independence, increased risk of falls,
fractures and death. Despite recent scientific interest in the subject,
information on sarcopenia among acutely ill older patients and it is
clinical implication and management is limited. We are not aware
of any previous study which has attempted to measure the preva-
lence of sarcopenia and associated morbidity in acutely ill hospi-
talized older patients. A recent study assessed sarcopenia in
a community free-living subjects using the EWGSOP algorithm
similar to the one used in our study revealed that sarcopenia was
highly prevalent among older persons and that sarcopenic subjects
were three time more likely to fall during a 2-year follow up period
regardless of age, gender and other confounding factors.3 Another
study which only measured muscle strength showed that lower
handgrip strength in older patients is correlated with poor func-
tional, psychological and social health.9 Other available studies in
Fig. 1. KaplaneMeier curve for 6 months non-elective readmission.
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Standard error P value Hazard ratio for unit change 95% C.I
.015 .836 1.00 .97e1.03
.023 .477 1.02 .97e1.06
.137 .237 1.18 .90e1.54
.043 .570 1.03 .974e1.12
.293 .937 .98 .55e1.74
.259 .013* .53 .32e.87
.002 .032* .996 .99e1.00
.023 .579 .99 .94e1.03
older people either considered muscle strength or muscle mass
separately as biomarkers or end points.
Well recognized risk factors for sarcopenia include chronic
diseases and inflammation. In this study the prevalence of sarco-
penia in hospitalized older patients was determined from baseline
clinical data on admission. Many of these patients were admitted
with acute illness and had a prolonged stay in hospital. Acute illness
and other diseases of ageing lead to tissue inflammation and ne-
crosis, which result in inflammatory responses. Such inflammatory
responses result in release of markers such as C-reactive proteins
and cytokines. These inflammatory markers have been shown to
decrease food intake and also reduce body weight and muscle
function therefore contributing to development of malnutrition
and sarcopenia in older people. With development of malnutrition
and worsening sarcopenia a vicious circle develops in which older
people develop recurrent illnesses leading to further inflammatory
responses, malnutrition and sarcopenia.6,10 We have previously
shown that the increased inflammatory response in older patients
is not just confined to the period of acute illness which led to the
hospital admission but also present but to a lesser extent at 6 weeks
and at 6 months of follow up in the community.10 This continuous
erosion of nutritional reserves as a result of inflammation leads to
metabolic, physiological and functional impairments which might
be responsible for the poor clinical outcome seen in this study. We
have also found significantly increased prevalence of sarcopenia in
underweight patients compared to those with normal or increased
body weight at admission but this did not influence clinical out-
come. Although patients with no weight loss, anorexia or meas-
urable inflammatory response may well be sarcopenic, sarcopenia
may be accelerated after an acute inflammatory stress. Furthermore
overweight/obese patients may still be sarcopenic due to muscle
loss despite increased fat mass and this often made worse by sys-
temic inflammatory response due to underlying disease.6
Besides poor nutritional status sarcopenia may be related to
other clinical risk indicators such as underlying disease state, drugs,
or functional capacity. In this study we have attempted to adjust for
a number of clinical prognostic factors. In addition all patients with
severe medical and psychiatric illnesses such as liver, gastro-
intestinal, kidney or neoplasm or living in an institution were
excluded from this study. Those excluded were more likely to have
sarcopenia and this might have therefore underestimated the
prevalence of sarcopenia in our study.
Other methodological issues may have affected our results
including the heterogeneous nature of the hospitalized patient’s
population and the use of hand grip strength and muscle mass but
not physical performance to diagnose sarcopenia. Another impor-
tant limitation is inherent difficulties in measuring anthropometric
indices to calculate muscle mass in ageing patients. The purpose of
assessing intra observer’s differences on anthropometric mea-
surements and the use of regression analysis was to overcome
some of these weaknesses. Although a wide range of valid and
reliable techniques are available for measurement of muscle mass
 S. Gariballa, A. Alessa / Clinical Nutrition 32 (2013) 772e776 775

Table 3
The Cox’s proportional hazard analysis of the relationship between sarcopenia and other prognostic variables and hospitalised patients 6-month mortality.

Variable Regression coefficient Standard error P value Hazard ratio for unit change 95% C.I
Age (years) .056 .028 .048* 1.06 1.00e1.12
Barthel score (0e20) .030 .034 .375 .97 .91e1.04
Smoking (never, ex, current) .638 .237 .007* 1.89 1.19e3.01
BMI .083 .079 289 1.09 .93e1.27
BMI2 (BMI-mean BMI)2 .517 .528 .328 .60 .21e1.68
Sarcopenia (yes/no) .792 .390 .043* .45 .21e.97
C-reactive protein (mg/L) .000 .002 .887 1.00 .99e1.01
Serum albumin (g/L) .111 .040 .005* .90 .83e.97

*P < 0.05.

such as DEXA, ultrasound CT and MRI ultimately cost eeffective-
ness and ease of use in all types of patient groups in different
healthcare settings including busy clinical practice will determine
whether these techniques are suited to clinical practice or only
remain useful for research. There is also some evidence from lon-
gitudinal studies that age-related decline in muscle strength far
exceeds the observed changes in muscle mass or size and that in-
terventions that maintain or even increase muscle mass may not
necessarily decrease or prevent muscle weakness in older adults.
This is clearly an area for future research.4,11e13
A number of treatment approaches for management of sarco-
penia in older people have been explored.14e16 Nutrition support
and exercise in particular deserve special attention in older people
with sarcopenia following acute illness. Firstly because acutely ill
older patients particularly those with the diagnosis of sarcopenia
are more likely to have premorbid decrease in physical activity,
muscle mass and function and therefore poor nutritional status.
Their nutritional status is likely to deteriorate further as the result
of the catabolism associated with the acute illness.17 This is
compounded further by the demands of the prolonged rehabil-
itation period in some patients. Secondly following acute illness
older people tend to slow down and many will not regain their
premorbid physical activity levels for some time after recovery
from acute illness. This is a very important area because physical
activity is an important aspect of health and confers benefit on
most risk factors of ageing, but also by increasing energy expen-
diture, leads to increased food intake and hence increased nutrient
intake if a mixed diet is consumed. Increased physical activity in
older people can therefore enable a diet of marginal nutrient
density to become adequate because of increased consumption.
More research is needed however on the effect of increased
physical activity and nutrient intake in particular protein and
amino acid supplement in the treatment of sarcopenia following
acute illness.1
In conclusion this study shows that sarcopenia is associated
with poor outcome in hospitalized older patients. It also highlights
two important challenges. The first is to find a valid, reliable, cost-
effective and a practical way of measuring sarcopenia in routine
clinical practice. In particular the use of anthropometry versus.
other techniques in the measurement of muscle mass. The second
is to determine the role of nutritional support coupled with
increased physical activity and other treatment modalities in
prevention and treatment of sarcopenia in older patients stratified
by the degree of inflammation, specific illness and severity of
sarcopenia. Meanwhile patients with the diagnosis of sarcopenia
may benefit from targeted nutritional screening, follow up and
intervention.
Author’s contribution
SG is the principal investigator and wrote the first draft of the
manuscript. AE contributed to analysis of the data and the discus-
sion. Both authors read and approved the final manuscript.
Conflict of interest

None.

Acknowledgement

The index study was funded by THE HEALTH FOUNDATION

project grant. Thank you to Sarah Forster for her help with data
collection.

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