Original Paper
Cerebrovasc Dis 2015;39:170–175
DOI: 10.1159/000375155
Resting Energy Expenditure in Patients with Stroke
during the Subacute Phases – Relationships with
Stroke Types, Location, Severity of Paresis, and
Activities of Daily Living
Michiyuki Kawakami a Meigen Liu a Ayako Wada b Tomoyoshi Otsuka b
Atsuko Nishimura a   
a
  Department of Rehabilitation Medicine, Keio University School of Medicine, Shinjuku-ku, Tokyo, and b Department of
Rehabilitation Medicine, National Higashisaitama Hospital, Saitama, Japan
Key Words
Activities of daily living · Diet · Energy metabolism ·
Rehabilitation · Stroke
Abstract
Background: The energy demands in patients with stroke
during the subacute phases are unclear. However, this infor-
mation is essential for appropriate clinical and nutritional
management. The aims of this study were to determine the
resting energy expenditure (REE) during the subacute phas-
es, examine its relationships with stroke types, location, se-
verity of hemiparesis, and activities of daily living (ADL), and
evaluate whether estimation of REE from the Harris–Bene-
dict equation (HB) requires the addition of a ‘stress factor’ to
capture possible additional REE imposed by stroke. Meth-
ods: We measured REE in 95 patients with subacute stroke
(53.5 ± 16.6 days post-stroke) with indirect calorimetry, and
compared it with predicted values of energy expenditure es-
timated from the HB (expressed as percentage). Patients
were admitted for rehabilitation of their first ischemic or
nonsurgical hemorrhagic stroke. The severity of hemiparesis
was assessed with the motor items of the Stroke Impairment
© 2015 S. Karger AG, Basel
1015–9770/15/0394–0170$39.50/0
E-Mail karger@karger.com
www.karger.com/ced
Received: October 16, 2014
Accepted: January 12, 2015
Published online: February 26, 2015
Assessment Set (SIAS). The ADL was assessed with the Func-
tional Independence Measure (FIM). We compared REE and
%HB of the two groups divided by hemiparesis severity and
ADL limitation using the Student’s t-test, and those of the
five groups divided by stroke location. The correlations
between REE and the motor items of the SIAS and the FIM
score were assessed with the Spearman rank correlation
test. A multiple regression analysis for REE was conducted.
Results: The average body weight (BW) was 57.1 ± 11.3 kg.
The average body mass index (BMI) was 22.5 ± 4.0. The mean
REE (%HB) was 1,271 ± 284 kcal/day (106.0 ± 17.3%). REE and
%HB of the low ADL group was less than that of the high ADL
group (p < 0.05). The REE had a positive correlation with the
FIM score (rs = 0.51, p < 0.01). The motor items of the SIAS
were not significantly correlated with REE. BW, FIM, and
stroke location were independent predictors of REE. Conclu-
sions: Analysis of energy expenditure suggests that stroke
patients are not hypermetabolic during the subacute phase.
The ‘stress factor’ in stroke patients during the subacute
phase was 1.0–1.1. This finding provides important informa-
tion for improving nutritional management during the sub-
acute phase in patients with stroke. © 2015 S. Karger AG, Basel
Michiyuki Kawakami, MD, PhD
Department of Rehabilitation Medicine
Keio University School of Medicine
35 Shinanomachi, Shinjuku-ku, Tokyo 160–8582 (Japan)
E-Mail michiyukikawakami @ hotmail.com
 Introduction
Elevated metabolic rates of 130–200% of the predicted
values have been well described for some disease states,
including burns [1], sepsis [2], trauma [2], and head in-
jury [3]. These changes are considered to reflect increased
oxygen consumption associated with injury severity. Hy-
permetabolism is defined as an increase in metabolic rate,
which is predicted from equations accounting for age,
sex, height, and weight [4]. There are limited data on the
energy expenditure patterns of patients after stroke. Rest-
ing energy expenditure (REE) of 15 patients with acute
stroke was reported to range from 95–107% of the pre-
dicted values [5]. Furthermore, in a much larger sample
population, the REE of stroke patients during the acute
phase was 10% higher than those predicted by the Har-
ris–Benedict equation (HB) [6]. Finally, the REE in 14
patients with mechanically ventilated nontraumatic in-
tracranial hemorrhage during the acute phase was report-
ed to be 126% of that predicted by the HB [7]. Thus, the
REE of stroke patients during the acute phase was rela-
tively higher than that calculated with HB. However,
there have been a few studies describing the energy ex-
penditure patterns in patients with stroke during the sub-
acute and chronic phases.
The metabolic rate typically peaks within several days
after injury and gradually declines to pre-injury levels in
the absence of infections or complications. However, it is
unclear whether stroke results in a similar pattern of meta-
bolic perturbation. Many stroke patients have functional
disturbance, including hemiparesis and dysphagia. Deter-
mination of the energy requirements is important for un-
derstanding the metabolic demands of stroke and for guid-
ing effective nutritional interventions for rehabilitation
during the subacute phase. Precise determination of ener-
gy expenditure in these subjects is important to guide ef-
fective nutritional interventions and to avoid the dangers
of underfeeding or overfeeding, as many stroke survivors
exhibit high-blood pressure, diabetes mellitus, hyperlipid-
emia, and obesity. Kono reported that lifestyle intervention
including nutritional therapy is beneficial for reducing the
incidence of new vascular events and improving vascular
risk factors in patients with ischemic stroke [8].
The HB, defined as the amount of energy (kcal/day)
needed to sustain all life processes under resting, thermo-
neutral conditions, is widely used in clinical practice and
research to estimate REE [9]. REE typically represents
75–90% of the total daily energy expenditure. The re-
mainder is accounted for by thermogenesis from nutri-
tional intake, shivering/nonshivering thermogenesis, and
Resting Energy Expenditure after Stroke
physical activity [10–12]. Significant deviation from the
estimated REE, as predicted by the HB, is assumed to re-
sult from the effects of an injury. The additional energy
demands imposed by hypermetabolism associated with
various diseases and injuries have led to the adjustment
of the equation with appropriate ‘stress factors’. These
factors enable more accurate predictions of total energy
requirements than when the HB is used alone. A ‘stress
factor’, however, does not exist for stroke, especially dur-
ing the subacute phase. Nutrition therapy during the sub-
acute phase is important as stroke patients with hemipa-
resis require intensive rehabilitation during this period.
There are a few studies describing the energy expenditure
patterns in patients with stroke during the subacute phase
and no report on relationships of energy expenditure
with stroke type, location, severity of hemiparesis, and
activities of daily living (ADL). The aims of the study were
to (1) describe the energy expenditure of patients with
stroke during the subacute phase; (2) examine the rela-
tionships between energy expenditure with stroke type,
stroke location, severity of hemiparesis, and ADL; and (3)
develop a ‘stress factor’ appropriate for use with the HB
in patients with stroke.
Materials and Methods
We recruited 95 consecutive patients who had been treated for
subacute stroke at a rehabilitation unit of National Higashisaitama
Hospital between July 2008 and March 2010 after being transferred
from acute care hospitals. The subacute phase in this study was
defined as the days from stroke onset between 30 and 90 days by
using previous study [13] as reference. Criteria for inclusion in the
study were (1) patients admitted for rehabilitation of their first
ischemic or nonsurgical hemorrhagic stroke, confirmed by either
CT or MRI, and (2) patients who took oral medication. Patients
were excluded if they: (1) had sustained a subarachnoid hemor-
rhage; (2) had an episode of infection; (3) were comatose; (4) had
no neurological deficits or experienced a transient ischemic attack;
(5) had severe higher cortical dysfunctions; (6) had major system-
ic illnesses; (7) had been tube-fed or received parenteral nutrition;
or (8) were ventilator-dependent and/or receiving oxygen therapy.
Major systemic illnesses included sepsis, carcinoma with or
without chemotherapy, chronic renal failure requiring dialysis,
congestive heart failure with pulmonary edema, or respiratory dis-
orders, such as severe asthma or pneumonia, which were clinically
determined by the investigators and which could possibly raise
REE. Twenty-five control subjects of similar age range were also
recruited. Twenty-five patients with chronic stroke were recruited
from the outpatient clinic of National Higashisaitama Hospital
from July 2008 to March 2010. They had been followed up for
medications and clinical examinations. The chronic phase was de-
fined as duration from stroke onset over 6 months. The other cri-
teria for inclusion and exclusion were identical to the aforemen-
tioned criteria.
Cerebrovasc Dis 2015;39:170–175 171
DOI: 10.1159/000375155
 Stroke location (right or left hemisphere, basal ganglia/thala-
mus, cerebellum, or brain stem) and stroke type (ischemic or hem-
orrhagic) were confirmed by either MRI or CT imaging. The sever-
ity of hemiparesis was assessed with the motor items of the Stroke
Impairment Assessment Set (SIAS) [14] by three physiatrists. The
scores range from 0–5, with 0 indicating complete paralysis, 3 in-
dicating the ability to complete the task with difficulty, and 5 indi-
cating no paresis. The motor items consist of five items (knee-
mouth, finger function, hip-flexion, knee-extension, and foot-
pat), with a full score of 25 points. The FIM score and SIAS were
assessed on the day when REE was measured using indirect calo-
rimetry. The patients were divided into two groups (severe group,
mild group) according to the severity of hemiparesis assessed with
the median score from this study population of the SIAS motor
items. The ADL was assessed with the Functional Independence
Measure (FIM) by trained physiatrists, nurses, or therapists. Pa-
tients were divided into ‘low ADL’ or ‘high ADL’ groups by the
median FIM score from this study population [15].
We measured REE using indirect calorimetry (Metavine; Vine,
Tokyo, Japan) [16]. The characteristic of this type of portable calo-
rimetry is that resting metabolism is calculated by measuring oxy-
gen uptake and ventilation based on a fixed resting respiratory
quotient (RQ) of 0.82. Several studies have reported that Metavine
measurement of REE gave a similar result as other indirect calo-
rimetry methods that use in vivo gas (O2 and CO2) analyses, show-
ing excellent concurrent validity and intra-class reliability [16].
Measurements were performed within 2 days from admission, be-
fore the start of full-fledged rehabilitation. Measurements were
performed in the supine position at least 2 h after meal consump-
tion and after the patient had been recumbent for at least 30 min.
We compared REE measurements with the predicted values of
energy expenditure obtained with the HB, and results were ex-
pressed as a percentage. The HB uses patient sex, height, weight,
and age to estimate basal energy expenditure expected under
normal, non-illness situations [9]. The HBs for the predicted REE
of males and females were as follows: male: 66.5 + [13.8 * weight
(kg)] + [5.0 * height (cm)] − [6.8 * age (years)]; female: 655 + [9.6 *
weight (kg)] + [1.8 * height (cm)] − [4.7 * age (years)].
This study was approved by the Ethics Committee of National
Higashisaitama Hospital and in accordance with the Declaration
of Helsinki. Informed consent was obtained from all participants
or their proxies.
Statistical Analyses
Comparability of the two groups (patients during the subacute
phase and controls) with respect to age, gender, BMI, stroke type
and severity of hemiparesis was established using the Student’s
t-test, the Chi-square test and Mann-Whitney U test , setting the
significance level at less than 0.05. We compared the REE and %HB
of the two groups using the Student’s t-test. We compared REE and
%HB of the two groups divided by stroke type, hemiparesis sever-
ity, and ADL limitation using the Student’s t-test. ANOVA was
used to compare REE and %HB of the five groups divided by stroke
location. The correlations between REE and the motor items of the
SIAS and the FIM score were assessed with the Spearman rank cor-
relation test. After assessing the multicollinearity, a multiple re-
gression analysis for REE was conducted. Variables that were re-
lated to REE at p < 0.10 in the analysis of the above were entered
in addition to sex, age, height, and body weight. Sex was dummy
coded as 0 for females and 1 for males. Stroke type was dummy
172 Cerebrovasc Dis 2015;39:170–175
DOI: 10.1159/000375155
coded as 0 for hemorrhagic stroke and 1 for ischemic stroke. As for
stroke location, the presence of a lesion for each five locations was
dummy coded as 0 for ‘no’ and 1 for ‘yes’. Variables were then se-
lected using the backward method (the significance level required
for retention in the model was 0.20).
Results
Between July 2008 and March 2010, 125 patients were
admitted to the hospital with a clinical diagnosis of their
first stroke, 30 of who were not eligible for recruitment.
The reasons for exclusion were severe higher cortical dys-
function in eight patients, tube-feeding in 11 patients,
and an episode of infection in 11 patients. As a result, a
total of 95 patients with subacute stroke were included for
the study, with 53 males (56%) and 42 females (44%), and
a mean age of 67.9 ± 12.2 years. The average body weight
(BW) was 57.1 ± 11.3 kg. The average body mass index
(BMI) was 22.5 ± 4.0. Sixty-one patients (64%) had isch-
emic strokes and 34 (36%) had hemorrhagic strokes.
Stroke locations included 16 (17%) with right hemi-
sphere, 24 (25%) with left hemisphere, 37 (39%) with bas-
al ganglia/thalamus, four (4%) with cerebellar, and 14
(15%) with brain stem lesions. The median number of
days from onset to the REE measurement was 51 (range:
31–90). The median score of the SIAS motor items was 14
(range: 0–25). The median FIM score was 76 (range: 24–
124). All patients were fed orally, but seven patients took
modified food to facilitate swallowing, for example, pro-
cessed food in a blender and thickened water.
Twenty-five patients in the chronic phase entered the
study as controls, with 11 males (44%) and 14 females
(56%), and a mean age of 70.1 ± 11.6. The average BW
was 55.5 ± 11.0 kg. The average BMI was 23.2 ± 3.9. Sev-
enteen patients (68%) had ischemic strokes and eight
(32%) had hemorrhagic strokes. Stroke locations in-
cluded seven (28%) with right hemisphere, seven (28%)
with left hemisphere, nine (36%) with basal ganglia/
thalamus, and two (8%) with brain stem lesions. The
median number of months from onset to the REE mea-
surement was 55 (range: 7–233). Seven patients took
modified food.
There were no differences between participants and
controls in age, gender, BMI, stroke type, or severity of
hemiparesis (table 1). The mean REEs of the patients dur-
ing the subacute phase and controls were 1,271 ± 284
kcal/day and 1,128 ± 231 kcal/day, respectively. The mean
%HBs of patients during the subacute phase and controls
were 106.0 ± 17.3% and 100.6 ± 17.7%, respectively. REE
Kawakami/Liu/Wada/Otsuka/Nishimura
 Table 1. Demographics of the study sample. Comparison between stroke patients during the subacute phase and
controls (during chronic phase) with regard to age, gender, BMI, stroke type, or severity of hemiparesis

Stroke patients during p value

the subacute phase the chronic phase
(n = 95) (n = 25)

Age, years 67.9±12.2 70.1±11.6 0.28†

Gender (male:female) 53:42 11:14 0.27*
BMI, kg/m2 22.5±4.0 23.2±3.9 0.41†
Stroke type (infarction:hemorrhage) 61:34 17:8 0.72*
The score of SIAS motor items 13.4±8.1 12.6±7.9 0.41‡

BMI = Body mass index; SIAS = Stroke Impairment Assessment Set. †  Student t-test. *  Chi-square test.
‡
 Mann-Whitney U test.

Table 2. Measured resting energy expenditure and percentage of Harris–Benedict equation for stroke patients
during the subacute and chronic phases

REE (kcal/24 h ± SD) REE (95% CI) % of HB ± SD % of HB (95% CI)

Subacute phase (n = 95) 1,271±284 1,212.2–1,330.7 106.0±17.3 102.4–109.7

Chronic phase (n = 25) 1,128±231 1,065.0–1,249.4 100.6±17.7 93.0–108.3

Table 3. Resting energy expenditure (kcal/day ± SD) and percent- Table 4. Resting energy expenditure (kcal/day ± SD) and percent-
age of Harris–Benedict equation (% ± SD) of patients with strokes age of Harris–Benedict equation (% ± SD) of patients with differ-
of varying severity of hemiparesis and degree of activities of daily ent stroke locations and types
living (ADL)
Location/type Resting energy Percentage of
Hemiparesis severity and REE % of expenditure Harris–Benedict equation
degree of ADL (kcal/24 h ± SD) HB ± SD
Right hemisphere 1,180.6±189.2 103.6±11.5
Severe hemiparesis Left hemisphere 1,165.9±245.5 101.1±16.2
(n = 45) 1,224.6±267.0 103.7±19.7 Basal ganglia/thalamus 1,344.3±285.6 108.2±19.8
Mild hemiparesis Cerebellar 1,441.7±420.4 116.3±20.5
(n = 50) 1,311.5±295.3 108.0±15.0 Brain stem 1,321.4±340.5 108.5±16.8
p value (Student t-test) 0.15 0.23 p value (ANOVA) 0.06 0.36
Low ADL (n = 49) 1,109.3±233.7 99.1±17.2 Infarct 1,229±270 106.0±16.9
High ADL (n = 46) 1,404.4±252.9 108.5±13.9 Hemorrhage 1,350±298 106.1±18.4
p value (Student t-test) <0.01 <0.01 p value (Student t-test) 0.07 0.97

and %HB were not significantly different between the two
groups (p = 0.18). Both parameters had large standard
deviations and wide 95% confidence intervals (table 2).
There were no differences in mean REE and %HB of pa-
tients during the subacute phase by the severity of hemi-
paresis, but %HB of the ‘low ADL’ group was lower than
that of the ‘high ADL’ group (p < 0.05) (table 3). The REE
had a positive correlation with the FIM score (rs = 0.51,
p < 0.01). The motor items of the SIAS were not signifi-
cantly correlated with REE (rs = 0.20, p = 0.07). There
were no differences in the mean REE and %HB of patients
during the subacute phase by stroke location and types
(table 4). Table 5 shows the results of the multiple regres-
sion analysis for REE. Sex, age, height, body weight, stroke

Resting Energy Expenditure after Stroke Cerebrovasc Dis 2015;39:170–175 173

DOI: 10.1159/000375155
Table 5. Multiple regression analysis of factors related to a resting
energy expenditure
Parameter Sβ p value
estimate
Body weight 11.99 0.522 <0.001
FIM 3.70 0.343 <0.001
Presence of a lesion in
left hemisphere 117.37 −0.187 0.018
R2 (Adjusted R2) 0.540 (0.522)
Sβ = Standard partial regression coefficients; FIM = Function-
al Independence Measure.
type, stroke location, and severity of hemiparesis (SIAS)
and ADL (FIM) were entered into the multiple regression
analysis. Multivariate analyses showed that BW (p <
0.001), FIM (p < 0.001), and left hemisphere (p < 0.05)
were independent predictors of REE.
Discussion
This is the first study with a relatively large sample to
report REE in patients with stroke during the subacute
phase. The primary finding of this study was that the REE
of stroke patients during the subacute phase was not high.
This is an interesting result because the results were a lit-
tle different from previous reports that the REE of Stroke
patients during the acute phase were 10–26% higher than
that calculated with HB [6, 7]. Finestone demonstrated
that mean %HB was 113.7 ± 12.9% (n = 47) at 90 days af-
ter stroke [6]. Although the REE measurements of stroke
patients were slightly higher than those of the present
study, the variation may largely be explained by differ-
ences in the proportion of obese patients between the two
studies. The difference between the two studies is small,
which seems to confirm these findings.
Independent predictors of REE during the subacute
phase in the present study included age, BW, ADL, and
stroke location. ADL limitation may be explained by a
decline in muscle mass. An investigation using dual en-
ergy X-ray absorptiometry (DXA) and magnetic reso-
nance imaging suggested that the relative mass of the in-
ternal organs contributed significantly to variations in
REE [17]. Skeletal muscle mass decreases after stroke [18,
19], which is considered to be due to prolonged immobil-
ity. As such, the REE and %HB of stroke patients with
‘low ADL’ may decrease.
174 Cerebrovasc Dis 2015;39:170–175
DOI: 10.1159/000375155
Stroke location was also an independent predictor of
REE and there was a negative correlation between left
hemisphere lesion and REE. The body activity amount
might decrease because of dominant hand dysfunction
and depression mood resulting from lesion of the left
hemisphere. Stroke survivors with injury to the left hemi-
sphere of the brain have a greater risk of post-stroke de-
pression [20]. However, this finding should be verified in
a larger within-subgroup sample, as there was an unbal-
anced sample with regard to stroke location.
There are a few studies that describe the energy expen-
diture patterns in patients with stroke during the chronic
phase. Leone et al. reported that REE of chronically tube-
fed stroke survivors was reduced, although no informa-
tion is available for orally-fed patients in the chronic
phase [21]. In our study, the REEs of 25 patients with
chronic stroke were measured in controls. Leone and
Pencharz demonstrated that the mean percentage of pre-
dicted REE was 90.1 ± 4.8% (n = 10) at 6–66 months after
stroke [21]. Although these REE measurements are lower
than those of the present study, the variation may be
largely explained by the different mode of feeding be-
tween the two studies (oral intake vs. tube feeding, respec-
tively), likely attributable to differences in the indepen-
dence in ADL (outpatients vs. inpatients of long-term
care floors, respectively). The participants in the present
study could walk independently and visit the outpatient
clinic. Thus, the muscle mass was likely to have been
maintained.
Based on these studies, the REE of stroke patients can
be summarized as follows: during the acute phase, REE
becomes higher; during the subacute and chronic phase,
REE shows a gradual decline and is restored to its prior
state. The ‘stress factor’ in stroke patients during the acute
phase was 1.1–1.2 and showed a gradual decline to 1.0–
1.1. This finding, however, should be verified in a pro-
spective cohort study.
There are some potential limitations of the present
study. First, the study was conducted only at one institu-
tion, and thus the results must be generalized with cau-
tion. The unbalanced sample with respect to stroke sever-
ity is also a limitation. As this study was performed in a
subacute rehabilitation unit, the study sample does not
include the most severe cases, for example bed-bound
patients and relatively mild cases that were discharged
home directly from the acute hospital. Second, this study
was cross-sectional, and a prospective cohort study from
the acute to chronic phase is necessary to demonstrate
the time course of REE in stroke patients. Despite these
limitations, we believe that the present findings provide
Kawakami/Liu/Wada/Otsuka/Nishimura
important information for improving nutritional man- Funding Sources
agement during the subacute phase in patients with
We have no funding source.
stroke.

Conclusions
Analysis of energy expenditure suggests that stroke
patients during the subacute phase are not hypermetabolic.
BW, FIM, and presence of a lesion in the left hemisphere
were independent predictors of REE. REE in stroke patients
during the subacute phase was 5% higher than that predict-
ed from HB, although individual REE variation was high. If
an accurate assessment of caloric requirement is necessary
for an individual patient, indirect calorimetry is indicated.
Statements of Authorship
M.K. and M.L. contributed to conception and design, data ac-
quisition, analysis, and interpretation, and drafting the manu-
script. A.W., T.O., and A.N. contributed to data acquisition. All
authors revised the article critically and approved the final version
for publication.
Disclosure Statement
All authors declare no conflicts of interest.

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Resting Energy Expenditure after Stroke Cerebrovasc Dis 2015;39:170–175 175

DOI: 10.1159/000375155
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