A. M. Abbatecola et al.

Age and Ageing 2014; 43: 548–553 © The Author 2013. Published by Oxford University Press on behalf of the British Geriatrics Society.
doi: 10.1093/ageing/aft196 All rights reserved. For Permissions, please email: journals.permissions@oup.com
Published electronically 22 December 2013

Body composition markers in older persons

with COPD
ANGELA MARIE ABBATECOLA1,†, ALESSIA FUMAGALLI2,†, LIANA SPAZZAFUMO3, VALERIA BETTI1,
CLEMENTINA MISURACA1, ANDREA CORSONELLO4, ANTONIO CHERUBINI5, ENRICO E. GUFFANTI2,
FABRIZIA LATTANZIO1

1
Scientific Direction – Italian National Research Center on Aging (INRCA), Via S. Margherita n. 5, Ancona 6100, Italy
2
Unit of Pulmonary Rehabilitation, Research Hospital of Casatenovo, Italian National Research Centre on Aging (INRCA),
Casatenovo, Italy
3
Statistic and Biometry Center, Department of Gerontology Research, Italian National Research Center on Aging, (INRCA),
Ancona, Italy
4
Unit of Geriatric Pharmacoepidemiology, Research Hospital of Cosenza, Italian National Research Center on Aging (INRCA),
Cosenza, Italy
5
Geriatric Hospital, IRCCS, Italian National Research Center on Aging (INRCA), Ancona, Italy
Address correspondence to: A. M. Abbatecola. Tel: +39 071 8004628; Fax: +39 071 35944.
E-mail: angela_abbatecola@yahoo.com

Abstract
Background: Body composition has been shown to be correlated with physical performance, but data in older persons with
diverse chronic diseases are lacking.
Objective: We aimed at investigating the associations of body composition to gait speed and nutritional status of older people
in different stages of chronic obstructive pulmonary disease (COPD).
Design, setting and subjects: Cross-sectional analysis of data from Pulmonary Rehabilitation Geriatric Unit at INRCA in
Casatenovo, Italy including 132 consecutively admitted COPD patients (mean age: 75 years) with data on body composition,
walking speed and respiratory parameters.
Methods: Body mass parameters were assessed using bioelectrical impedance analysis. Pulmonary function tests included
spirometry and arterial blood gases. Differences among body composition markers were compared according to gender.
Separate multivariate linear regression models with gait speed as the dependent variable were used to test for independent asso-
ciations with body composition markers after adjusting for multiple confounders.
Results: Walking speed deteriorated with increasing severity of COPD. Men were heavier and had more lean mass than
women. Participants in the fastest gait tertile were younger, had lower body mass index and fat mass (FM); higher lean-to-fat
ratio and albumin levels and better respiratory function (FEV1, FVC) compared with those in the slower tertiles. Total body
FM was an independent determinant of walking speed, while fat-free mass and lean-to-fat ratio were not.
Conclusions: Excess body fat may be harmful for physical functioning among elders with COPD.

Keywords: ageing, body fat, COPD, gait speed, indicators, older people

Introduction disease (COPD). Loss of body weight and depletion of

Decreased skeletal muscle is one of the most investigated
extra-pulmonary features in chronic obstructive pulmonary
†
These authors contributed equally to the manuscript.
fat-free mass (FFM) are common and severe risk factors for
mortality in COPD [1, 2]. Population-based studies have
shown higher COPD-related mortality rates in underweight
and normal weight than in overweight and obese [3, 4].
Malnutrition along with the inability of respiratory muscles to

548

adapt to the increase in the ventilatory load [5] may contrib-
ute to exercise limitation [6]. Current COPD guidelines con-
sider nutritional monitoring an important part of routine
evaluation in patients [7].
While the role of low FFM seems to have a consistent
impact on negative health outcomes, a potential role of fat
mass (FM) on clinical functional parameters in older patients
is highly contradictory. In middle-age adults, the relation
between body mass index (BMI) and overall mortality is
U-shaped with an increased risk in the lowest and highest
percentiles [8]. In older hospitalised persons, the risk of
mortality is lower with increasing body weight [9]. Fat tissue
seems to have a different effect on physical function decline
across age [10] and COPD [11].
Reduced gait speed is considered a determinant of dis-
ability and mortality in elders [12]. Considering that there is
limited literature testing the association between body com-
position markers and gait speed in older COPD persons, we
present data from a clinical study testing associations among
nutritional parameters and anthropometric indexes on gait
speed in older COPD patients.
Methods
One hundred and thirty-two patients with COPD (mean age
75 ± 6 years) consecutively admitted to the inpatient
Pulmonary Rehabilitation Geriatric Unit at INRCA in
Casatenovo, Italy from 1 June to 30 September 2009 were
enrolled. All patients were admitted for one cycle of physioki-
nesitherapy and gave written informed consent approved by
INRCA Institutional Review Board. All patients had the
following characteristics: age ≥65 years, clinical stability of
COPD and chronic treatment for COPD [7]. The exclusion
criteria included pulmonary infection (<4 weeks), bronchial
reversibility > 12% after administration of β-agonists, renal,
hepatic or acute heart failure, cancer, drugs known to inter-
fere with water–mineral homeostasis and/or any signs of
oedema or dehydration. All patients underwent nutritional,
body composition and respiratory evaluations (including
arterial blood gas analysis of paO2 and paCO2) at the time of
admission.
BODE index
The BODE index [13] is a multidimensional assessment
score ranging from 0 to 10 (with higher values indicating
greater COPD severity) based on the sum of cut-off scores
for body-mass index (B), degree of airflow obstruction (O)
[14, 15], functional dyspnoea (D) [16] and exercise capacity as
measured by the 6-min walking test (6MWT) (E) [17]. The
BODE index has been shown to be effective in predicting
the mortality in patients with COPD [13]. The BODE score
was calculated as the sum of scores assigned for each individ-
ual tasks. For BMI (kg/m2), patients were assigned a score 0
for BMI ≤ 21 or 1 for BMI > 21; airflow obstruction was
assessed using FEV1 (% of predicted) [14, 15] and patients
Body composition markers in older persons
were scored 0 for FEV1 ≥ 65 = 0, 1 for FEV1 = 50–64, 2
for FEV1 = 36–49 and 3 for FEV1 ≤ 35; dyspnoea was
assessed using the Modified Medical Research Council
(MMRC) Dyspnea scale [16] and patients were assigned
score 0 for MMRC = 0–1, 1 for MMRC = 2, 2 for
MMRC = 3 and 3 for MMRC = 4; metres walked during the
6MWT were scored as follows [17]: ≥350 = 0; 250–349 = 1;
150–249 = 2 and ≤149 = 3.
Exercise capacity
6MWT was applied according to ATS criteria [17]. After the
test, the distance in metres walked in 6 min was recorded for
each patient. Gait speed (m/s) was calculated by dividing the
distance walked during 6MWT by time [18].
Bioelectrical impedance analysis
Bioelectrical impedance analysis (BIA) was performed using
a tetrapolar 101 System Analyzer (Akern, Florence, Italy)
with the emission of a low electrical current (500–800 mA
and 50 kHz). As previously described, patients were studied
in the supine position with electrodes connected to the
hands and feet [19]. The patient’s right side was standardised
for the test. Resistance (R) and capacitance (Xc) were direct-
ly measured in ohms (V) at 50 kHz and 800 mA using the
BIA (RJL Systems). Phase angle (PA) measures using the
BIA reflect the relative contributions of fluid (resistance)
and cellular membranes (capacitance) of the body. It was
calculated using the following equation: PA: (resistance/
capacitance) × (180/π). Sex-specific regression equations
derived for COPD patients are lacking, but we employed
the same sex-specific equations as previously reported in
a validation study in Italy [19]. FM (kg) was calculated as
total body weight (kg) minus FFM (kg). We also calculated
the lean-to-fat ratio (FFM/FM) as reported in a previous
study [20].
Pulmonary function tests
Function testing included spirometry and arterial blood gas
analysis. Forced expiratory volume in 1 s (FEV1) and forced
vital capacity (FVC) were measured with VMax Sensor
Medics spirometer.
Global initiative for chronic obstructive lung disease
Global initiative for chronic obstructive lung disease (GOLD)
staging system divides the severity of COPD into four stages
(mild, moderate, severe, very severe) based on airflow limita-
tion (obstruction) during pulmonary function tests. Based on
FEV1, FEV1/FVC ratio, COPD severity was staged based on
NHLBI/WHO GOLD criteria (Stages I–IV) [21].
549
A. M. Abbatecola et al.

Statistical analysis significant differences for FM (kg) (23.1 versus 24.8,

Statistical analyses were performed using SPSS version 15.0
(SPSS, Chicago). Demographic and clinical characteristics were
investigated across COPD stages according to GOLD stages I
(less) to IV (very severe) with the analysis of variance
(ANOVA)-based test for trend. Comparison of body compos-
ition markers between gender was performed using Student’s t
testing. Clinical and anthropometric parameters were tested
across tertiles of gait speed using ANOVA. Descriptive results
of continuous variables are presented as means ± SD. Partial
correlations investigated the relationship between walking speed
and PA, body composition markers, respiratory function inde-
pendently of age and weight in the entire study population.
Separate multivariate linear regression models were used to test
for independent associations between gait speed as the depend-
ent variable and body composition parameters (FFM, FM,
FFM/FM), age, gender, BMI, PA, albumin, FEV1 and the
number of comorbidities. To avoid collinearity, we included
body weight in our model testing the association with FFM and
not in those with FM or FFM/FM as dependent variables.
Albumin was included as a confounder because it is a widely
known marker of malnutrition.
Results
Our study population consisted of 132 persons (mean age
75 ± 6 years) with COPD in diverse stages [I (n = 12), II
(n = 59), III (n = 49), IV (n = 12)]. The mean walking dis-
tance and walking speed were lower across increased COPD
severity (Table 1). We confirmed a significant decline in PA
across COPD stages suggesting that lower PAs may be asso-
ciated with decreased cell integrity (Table 1). Even though we
used sex-specific regression equations (see methods), we
tested for differences in body composition markers accord-
ing to gender. In men versus women, we did not find any
P = 0.365), BMI (26.3 versus 26.1, P = 0.884) or FFM/FM
(2.53 versus 2.79; P = 0.669), but men were significantly
heavier (kg) (74.0 versus 63.8, P = 0.001) and had more
FFM (kg) (50.8 versus 40.0, P = < 0.001) than women. In
addition, there was not a significant difference in PA (5.05
versus 4.7, P = 0.096) between genders.
Table 2 describes clinical and anthropometric characteris-
tics across tertiles of walking speed. Individuals in the fastest
tertile of walking speed were younger, showed lower FM,
higher FFM/FM and had better lung performance than
those in slower tertiles.
Age- and body weight-adjusted correlations among
walking speed and clinical parameters showed that walking
speed correlated with PA (r = 0.180, P = 0.050), FM (r =
−0.137, P = 0.035), pO2 (r = 0.384, P < 0.001), pCO2 (r =
−0.192, P = 0.029), FVC (r = 0.265, P = 0.002) and FEV1
(r = 0.361, P < 0.001). There were no significant correlations
between walking speed, FFM, FFM/FM and albumin.
The relationship between FM and walking speed inde-
pendent of multiple confounders was tested in a multivariate
linear regression model (Table 3). The same analysis was per-
formed including FFM and FFM/FM separately (Table 3).
With regard to body composition markers, we found that
only FM was an independent determinant of walking speed.
In all models, age and FEV1 continued to be independent
determinants of walking speed (Table 3).
Discussion
In this study, we investigated the correlations of lean and FM
on walking speed and gait speed in older COPD patients. We
found that FM was an independent determinant for slower
walking speed, while lean mass was not. The importance of
limitation in mobility using diverse walking speed distances

Table 1. Demographic and clinical characteristics according to GOLD stages of COPD (n = 132)
COPD groups
I (n = 12) II (n = 59) III (n = 49) IV (n = 12) P
....................................................................................
Age 74.8 ± 6.4 74.5 ± 5.3 74.7 ± 5.5 73.5 ± 9.9 0.936
Sex, m/f 6/6 36/23 34/15 10/2 0.518
Height (m) 1.64 ± 0.09 163.1 ± 1.0 165.3 ± 0.08 166.3 ± 0.08 0.551
Weight (kg) 88.4 ± 12.2 71.8 ± 16.4 70.5 ± 15.7 57.4 ± 15.8 0.002
BMI (kg/m2) 32.9 ± 5.6 27.0 ± 5.8 25.8 ± 5.6 20.5 ± 4.6 <0.001
FM (kg) 34.4 ± 9.9 24.5 ± 9.6 23.2 ± 9.5 16.5 ± 8.1 <0.001
FFM (kg) 53.9 ± 7.6 47.6 ± 10.0 47.3 ± 9.6 40.8 ± 9.7 0.052
PA (°) 5.95 ± 0.57 5.25 ± 0.80 4.72 ± 1.1 3.72 ± 1.0 <0.001
FEV1 82.3 ± 2.9 61.0 ± 8.1 41.8 ± 4.8 25.4 ± 3.6 <0.001
FVC 96.3 ± 4.1 75.7 ± 13.1 63.6 ± 13.0 47.2 ± 10.4 <0.001
Albumin (g/dl) 4.1 ± 0.2 3.8 ± 0.4 3.7 ± 0.5 3.5 ± 0.3 0.021
paO2 (mmHg) 72.1 ± 8.0 65.2 ± 11.4 59.1 ± 9.0 56.2 ± 10.6 <0.001
paCO2 (mmHg) 38.2 ± 4.6 41.9 ± 7.7 46.1 ± 6.2 50.2 ± 11.1 <0.001
6MWT (m) 475 ± 140 403 ± 118 357 ± 71 311 ± 68 0.001
Walking speed (m/s) 1.32 ± 0.39 1.12 ± 0.33 0.99 ± 0.20 0.86 ± 0.19 0.001

Data are presented as mean ± standard deviation. BMI, body mass index; FM, fat mass; FFM, free fat mass; FEV1, forced expiratory volume in 1 s; FVC, forced vital
capacity; paO2, partial pressure arterial oxygen; paCO2, partial pressure of arterial carbon dioxide; 6MWT, six minute walking test distance.

550
 Body composition markers in older persons

Table 2. Clinical characteristics of the study group of older persons with COPD across body walking speed tertiles
First tertile (n = 18) Second tertile (n = 74) Third Tertile (n = 40) P (for trend)
....................................................................................
Walking speed (m/s) 0.93 ± 0.13 1.10 ± 0.10 1.43 ± 0.23 <0.001
Age (years) 75.8 ± 6.1 74.9 ± 5.9 73.4 ± 5.3 0.040
Body weight (kg) 79.8 ± 16.7 70.7 ± 18.1 71.1 ± 15.1 0.123
BMI (kg/m2) 29.0 ± 6.0 26.6 ± 5.9 25.0 ± 5.3 0.025
FM (kg) 27.6 ± 8.7 23.8 ± 9.3 22.9 ± 10.2 0.028
FFM (kg) 52.2 ± 13.0 46.8 ± 8.8 48.1 ± 8.8 0.143
Lean-to-fat ratio 1.89 ± 0.9 1.97 ± 0.9 2.10 ± 0.6 0.040
PA (°) 4.7 ± 1.0 5.2 ± 1.0 5.4 ± 0.9 0.004
FEV1 47.7 ± 14.3 56.3 ± 16.1 57.8 ± 14.3 0.001
FVC 65.9 ± 15.9 74.4 ± 17.8 75.2 ± 15.2 0.007
Albumin (g/dl) 3.7 ± 0.5 3.8 ± 0.4 4.0 ± 0.3 0.018
BODE index 6.7 ± 1.4 5.4 ± 1.6 3.5 ± 1.9 <0.001
Number of comorbidities 3.0 ± 1.2 3.0 ± 1.3 2.8 ± 1.0 0.712

Data are presented as mean ± standard deviation. BMI, body mass index; FM, fat mass; FFM, free fat mass; FEV1, forced expiratory volume in 1 s; FVC, forced vital
capacity.

Table 3. Multivariate linear regression models testing the COPD patients (mean age of 75 years) admitted for respira-
association of gait speed as the dependent variable on body tory rehabilitation on walking speed. This is a cross-sectional
composition, nutritional and respiratory markers study from an ongoing protocol testing for performance out-
comes in older persons with COPD, thus future findings will
B SE P
........................................ determine a predictive role of body composition measures
FM −0.009 0.004 0.025 on physical function in older persons. Our data also con-
Age −0.014 0.005 0.006 firmed that older persons in a more severe state of COPD
FEV1 0.007 0.002 <0.001 were more likely to walk slower.
FFMa 0.007 0.006 0.267 Loss of lean mass is now recognised as a major
Age −0.014 0.005 0.005
FEV1 0.007 0.002 <0.001
comorbidity of COPD and causes functional impairment
FFM/FMa 0.002 0.008 0.830 [2, 13, 24, 25]. Skeletal muscle wasting is a powerful predictor
Age −0.013 0.005 0.010 of mortality in COPD, independent of the lung function [11].
FEV1 0.007 0.002 <0.001 Clinically, rapid deteriorations in lean body mass have been
All models included BMI, gender, PA, number of comorbidities that did not described following an acute exacerbation of COPD, and par-
reach statistical significance. ticularly in more severe patients (FEV1 is <50%) [26].
a
Models also included body weight that did not reach statistical significance. In contrast to emphysema and small airway fibrosis, skel-
etal muscle wasting and functional impairment can be slightly
has been shown to be important even if not attributable to improved by nutritional intervention, physical training and
specific disease states in older persons [22]. Considering that anabolic steroids, indicating that it is potentially reversible
there are contradicting data on the role of FM-related clinical [27]. Considering the importance of physical performance
outcomes in older persons especially with chronic diseases, prediction on COPD outcomes, we hypothesised that lower
this study adds important detail for future longitudinal per- lean mass would have a negative association with gait speed.
spectives. A previous community dwelling cohort of older Our findings confirmed that the lean-to-fat ratio increased
persons suggested that the absolute amount of FM was nega- across walking speed tertiles even in COPD patients [23].
tively associated with physical performance, while lean mass However, the lean-to-fat ratio was not an independent deter-
is not as significant in absolute terms [23]. However, these minant of gait speed. These differences are most likely due to
authors did not aim at testing differences according to the fact that our study included only older patients (>65
chronic diseases. With regard to studies performed in years of age) with COPD, while the paper by Sternfeld et al.
patients with COPD, an important impact of lean mass has [23] included community dwelling individuals with ages
been shown to have an important impact on negative clinical ranging from 55 to 95 years (mean age of 69).
outcomes [2, 5]. Interestingly, a recent study found that the COPD individuals with less lean mass have been shown to
lean-to-fat ratio was associated with a greater walking dis- have more negative outcomes [24, 25]. Surprisingly, we did not
tance in younger men, but not in women with COPD [20]. find that lower lean mass was an independent determinant of
These same authors showed that higher measures of total slower gait speed in older COPD patients. This finding indi-
adiposity (BMI) and central adiposity were related to func- cates that other body composition factors may hold a greater
tional limitation in both genders. However, these data were impact on physical performance in older COPD patients. We
limited to a younger cohort of COPD patients (mean age of found that absolute FFM levels and a higher lean-to-fat ratio
58 years). We aimed at testing for differences in FM, lean were associated with faster walking speed. This finding to a
mass (fat-free mass) and lean-to-fat ratio in a sample of older certain extent reinforces that of previous studies showing that

551
A. M. Abbatecola et al.
higher levels of fat were associated with a greater likelihood of
disability, while lower levels of lean mass were not [20, 23, 28].
In a younger cohort of COPD adults, the accumulation of
greater FM, not the loss of lean, was strongly associated with
functional limitation in both sexes [20]. Our findings add
insight to a potential role played by FM alone on functional
decline in older COPD patients.
From the literature, it would appear that a decline in lean
mass is an important precursor of functional limitation at an
earlier age in COPD [20]; however, an increase in FM should
not be underestimated. Our study also showed that even
though nutritional parameters including albumin and PA
were significantly lower across COPD stages and tertiles of
gait speed, these same parameters were not independent
determinants of impaired mobility in fully adjusted models.
Our study had some limitations. One cannot rule out a
role played by increased inflammatory markers produced by
fat tissue on gait speed. Unfortunately, our protocol did not
include pro-inflammatory cytokines, such as interleukin- 6
(IL-6) or tumour necrosis factor-alpha (TNF-α). The proto-
col did include C-reactive protein (CRP), but this was found
not to be an independent determinant (data not shown).
Recent data from the Health ABC study highlighted that ex-
cessive abdominal visceral fat contributes to increased
plasma IL-6, which, in turn, was strongly associated with
mortality in older persons with COPD [29]. Another import-
ant limitation is our relatively small sample size. The small
number of participants in the first and fourth groups of the
GOLD stages should be noted and may explain why FFM
did reach statistical differences across COPD groups, but
considering that this study is continuously recruiting COPD
patients, future findings will explain this tendency.
Although fat tissue has been shown to hold a protective
role against morbidity in elders, increased FM suggests a
negative role on mobility in older COPD patients.
Key points
• Analysing gait speed in older patients with COPD.
• Impact of body composition on gait speed in COPD.
• FM is a determinant on slower gait speed in COPD.
Conflicts of interest
All authors declare no conflict of interest.
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Received 20 May 2013; accepted in revised form 4 October
2013

Age and Ageing 2014; 43: 553–558 © The Author 2013. Published by Oxford University Press on behalf of the British Geriatrics Society.
doi: 10.1093/ageing/aft197 All rights reserved. For Permissions, please email: journals.permissions@oup.com
Published electronically 12 December 2013

BODE index or geriatric multidimensional

assessment for the prediction of very-long-term
mortality in elderly patients with chronic
obstructive pulmonary disease? A prospective
cohort study
CLAUDIO PEDONE1,2, SIMONE SCARLATA3, FRANCESCO FORASTIERE4, VINCENZO BELLIA5,
RAFFAELE ANTONELLI INCALZI6,7

1
Cattedra di Geriatria, Università Campus Biomedico, Via dei Compositori 128, Roma 00128, Italy
2
Fondazione Alberto Sordi, Rome, Italy
3
Chair of Geriatrics, Unit of Respiratory Pathophysiology, Università Campus Bio Medico, Via A. del Portillo 200, Rome 00128, Italy
4
Osservatorio Epidemiologico del Lazio, Rome, Italy
5
Dipartimento di Medicina, Pneumologia, Endocrinologia, Fisiologia e Nutrizione Umana, Università di Palermo, Palermo, Italy
6
Department of Geriatrics, University Campus Bio-Medico, Via dei Compositori 130, Rome 00128, Italy
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Fondazione ‘S. Raffaele – Cittadella della Carità’, Taranto, Italy
Address correspondence to: S. Scarlata. Tel: +39 06 225411168; Fax: +39 06 22541456. Email: s.scarlata@unicampus.it

Abstract

Background: a multidimensional approach—the BODE index—has been proposed for prognostic purposes in chronic
obstructive pulmonary disease (COPD) and theoretically seems to be well suited for elderly people, but there is a lack of data

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