not permitted.

It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA

© 2016 EDIZIONI MINERVA MEDICA European Journal of Physical and Rehabilitation Medicine 2017 April;53(2):219-27
Online version at http://www.minervamedica.it DOI: 10.23736/S1973-9087.16.03804-1

ORIGINAL ARTICLE

The effects of upper extremity aerobic exercise in patients

with spinal cord injury: a randomized controlled study
Halil AKKURT  1, Hale U. KARAPOLAT  1 *, Yesim KIRAZLI  1, Timur KOSE 2

1Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Ege University, İzmir, Turkey; 2Department of Biostatistics
and Medical Informatics, Faculty of Medicine, Ege University, İzmir, Turkey
*Corresponding author: Hale U. Karapolat, Department of Physical Medicine and Rehabilitation, Faculty of Medicine, Ege University, 35100 Bornova,
Izmir, Turkey. E-mail: hale.karapolat@ege.edu.tr

ABSTRACT
BACKGROUND: Immobility and secondary complications, including cardiopulmonary disease, pressure ulcers, and pain, occur in patients with
spinal cord injury (SCI). These patients also have difficulty coping with the strain of daily activities. Thus, it is important for SCI patients to
engage in aerobic exercise in order to be able to cope adequately with the strain of activities and SCI-related complications.
AIM: The aim of this study was to investigate the effects of arm aerobic exercise on the parameters of cardiopulmonary function, quality of life,
degree of disability, psychological state, and metabolic syndrome.
DESIGN: This study was a single blind, randomized, controlled trial.
SETTING: This study was conducted in a university hospital.
POPULATION: SCI patients were randomly assigned to an intervention group (N.=17) or a control group (N.=16). Arm ergometer exercises
(three days/week; 1.5 hours/week 50-70% pVO2) and general exercises (two sessions/day; 5 days/week), were assigned to the intervention group
for 12 weeks. The control group was assigned general exercises only during this trial.
METHODS: Before the rehabilitation (Week 0), after six weeks, and after the rehabilitation (Week 12), all patients were evaluated for functional
status (maximal oxygen uptake [pVO2], power output [PO], and Functional Independence Measurement), pulmonary function (FEV1%, FVC%,
FEV1/FVC%), quality of life (World Health Organization Measure of Quality of Life, short form, Turkish version), metabolic syndrome param-
eters (triglycerides, total cholesterol, high-density lipoprotein cholesterol, low-density lipoprotein cholesterol, fasting blood sugar, waist circum-
ference, and systolic and diastolic blood pressure), degree of disability (Craig Handicap Assessment and Reporting Technique, short form), and
psychological status (Center for Epidemiologic Studies Depression Scale and Hospital Anxiety and Depression Scale).
RESULTS: At the end of the study, increases of 39.6% and 45.4% in the pVO2 and PO levels, respectively, were found. Additionally, no statisti-
cally significant difference was found in the intervention group after the rehabilitation compared to the levels before rehabilitation (P<0.05).
However, no statistically significant differences in functional status, quality of life, psychological state, level of disability, or metabolic syndrome
parameters were found in the intervention group (P>0.05). The control group, on the other hand, showed no clinically significant differences in
any of the parameters (P>0.05).
CONCLUSIONS: Short-term arm aerobic exercise performed by patients with SCI improves their exercise capacities. These patients require
longer rehabilitation programs to receive more benefits from aerobic exercise training.
CLINICAL REHABILITATION IMPACT: Adding arm cranking exercise training to the rehabilitation program of patients with spinal cord inju-
ry demonstrated improved exercise capacity; however, further studies are needed to assess the effects of exercise training on other health issues.
(Cite this article as: Akkurt H, Karapolat HU, Kirazlı Y, Kose T. The effects of upper extremity aerobic exercise in patients with spinal cord injury: a
randomized controlled study. Eur J Phys Rehabil Med 2017;53:219-27. DOI: 10.23736/S1973-9087.16.03804-1)
Key words: Spinal cord injuries - Exercise - Ergometry.

S
or other proprietary information of the Publisher.

pinal cord injury (SCI), along with the physical, tions, it can cause morbidity and mortality.1 With SCI
psychosocial, and economic problems which ac- patients, other organs and anatomic structures may also
company it, is an illness with relevant personal and have been injured, and various complications, such as
social repercussions. Moreover, due to its complica- cardiopulmonary, urinary bladder, intestine, and sexual

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 219

not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AKKURT AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY
function disorders and problems associated with in-
activity, may be involved in the condition. Over years
of compromised physical ability, SCI patients often
experience psychological and social problems that af-
fect their quality of life.1, 2 Aerobic exercise is of ut-
most importance for SCI patients to gain independence
in their activities of daily living, to prevent complica-
tions that may occur secondary to the illness, and to be
able to sustain an active lifestyle. No matter how much
locomotor training is performed during rehabilitation,
most patients remain dependent on a wheelchair. After
being discharged from the hospital, patients may not
be well adapted to their environment and may struggle
with certain acquired skills. For this reason, in order for
patients to engage in social participation, have a high
quality of life, and live independently, they should have
good arm endurance. It is also known, based on the re-
views 3, 4 mention that that exercising increases the ex-
ercise capacity of the upper extremities. However, there
are only a small number of studies dealing with patient
morbidities, such as cardiopulmonary risk factors, psy-
chological state, quality of life, and degree of disability,
or the effect of increased functionality on the patient’s
independence, self-efficiency, and well-being.5, 6 To the
best of our knowledge, no studies have considered all of
the comorbidity factors of exercising as a whole in SCI
patients. As such, the primary aim of our study was to
investigate the effects of upper extremity exercises on
the patient’s exercise capacity. Our secondary aim was
to discover the effects of upper extremity exercises on
other health issues including cardiopulmonary risk fac-
tors, metabolic syndrome, psychological state, quality
of life, and degree of disability.
Materials and methods
People with SCI who had been rehabilitated at the
Physical Medicine and Rehabilitation Departments of
the Faculty of Medicine at Ege University were includ-
ed in the study. Participants were included if: 1) they
were aged between 15 and 65 years; 2) all lesions were
traumatic; 3) lesion levels were C7-L5; 4) they were at
least one month post-injury; 5) they were physically ac-
or other proprietary information of the Publisher.
tive in training and outdoor mobility less than two hours
a week; 6) they received medical approval for participa-
tion in physical activity; 7) they had the ability to read
and write the Turkish language. Exclusion criteria were:
220 European Journal of Physical and Rehabilitation Medicine April 2017
other secondary health problems (i.e., pressure sores,
bladder infections, cardiovascular diseases or contrain-
dication for exercise), according to the American Col-
lege of Sports Medicine guidelines 7 as well as any other
medical conditions that did not allow the performance
of physical activities.
The study was a two-arm, 12-week, single-blind, ran-
domized controlled trial. This study was approved by
the local ethics committee of our institution. Informed
consent forms were obtained from all participants. All
participants underwent outcome measurement sessions
during a four week, nonintervention baseline phase. Af-
ter baseline measurements were recorded, 40 patients
were assigned to one of the following two treatment
groups on the basis of a computer-generated minimiza-
tion method: an intervention group (N.=20) or a control
group (N.=20).
Intervention
All supervised intervention sessions were performed
in the same human performance laboratory, with each
participant having the same amount of supervision and
interaction with the investigation. Patients in the inter-
vention group performed general rehabilitation exercis-
es and aerobic exercise with the arm ergometer (Mas-
terScreen CPX with metabolic cart and Monark 831
E; Viasys Healthcare, Jaeger, Würzburg, Germany) for
12 weeks. The patients in the control group performed
only the general rehabilitation exercises for 12 weeks.
General rehabilitation exercise programs were adapted
according to the patients’ neurological levels and sub-
ject skills. The exercise sessions consisted of two ses-
sions/day, five days/week, for 12 weeks. Exercises were
given prone, supine, quadruped, full and half kneeling,
and standing. The following activities were given to the
patients: passive, active-assisted, active range of mo-
tion exercises, strengthening exercises for the upper
and lower body (the pectorals, deltoids, triceps, biceps,
latissimus dorsi, wrist flexors, wrist extensors, torso
flexors, torso extensors, quadriceps, hamstrings, and
gastrocnemius), one-repetition maximum (50%1RM),
core and balance exercises, and if possible locomotor
training (with or without body weight supported). The
patients in the intervention group were administered an
additional exercise program involving arm ergometer
rowing and breathing exercises three days/week, 1.5
not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY AKKURT
hours/week for 12 weeks. The exercise with arm ergom-
eter was performed so that pVO2 was at 50-70% and a
Borg scale score of lightly hard–moderately hard.13‑15
The breathing exercises included pursed lip breathing,
segmental breathing, diaphragmatic breathing, volun-
tary isocapnic hyperpnea, and air shifting (ten repeti-
tions, two sessions/day, seven days/week).
Baseline measurements
All baseline assessments were conducted by the same
investigator, who was blind to the patients’ group as-
signments. The following demographic characteristics
were considered: age, gender, marital status, occupation,
Body Mass Index (BMI), presence of comorbidities, du-
ration of disease, smoking status, and medications used.
The neurologic levels of the patients were assessed us-
ing the American Spinal Injury Association Scale 8 and
ambulation was assessed using the Functional Ambula-
tion Scale.9 The patients were recorded separately based
on whether they used wheelchairs, long leg braces plus
walker, short leg braces plus crutches, crutches alone,
or no devices.
All of the patients were assessed before the rehabili-
tation (Week 0), at week six (Week 6), and after the re-
habilitation (Week 12).
Primary outcome measures
Functional status was assessed using a cardiopul-
monary exercise test and the Functional Independence
Measurement (FIM).10
The exercise capacity, which was measured accord-
ing to the cardiopulmonary function test, entailed a
multistep progressive protocol using a MasterScreen
CPX with metabolic cart and Monark 831 E arm ergom-
eter (Viasys Healthcare, Jaeger, Würzburg, Germany).
Patients in wheelchairs remained seated in their wheel-
chairs. A metronome was added to the ergometer so
the subjects would not drop below the 50-rpm turning
speed during the test. A power output of 30 W was used
for two minutes and then increased by 10 W every two
minutes. Twelve derivation electrocardiogram records
or other proprietary information of the Publisher.
were observed during the test. Blood pressure measure-
ments were taken before and after the test. Peak oxygen
uptake (pVO2) and carbon dioxide output (VCO2) were
analyzed breath-by-breath and in 30-second intervals
Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine
by taking their average values from the expiration air
with the metabolic measurement device. Calibrations
were carried out with standard O2 and CO2 gases with
known pretest concentrations. The test was discontin-
ued in the event of serious angina, restrictive symptoms
(dyspnea, dizziness, etc.), ventricular tachycardia, con-
duction abnormalities (second and third degree heart
blocks), ischemic ECG changes, rise or fall in systolic
blood pressure >20 mmHg, or oxygen saturation <80%.
No complications developed in any of the patients dur-
ing the tests. pVO2 (mL/kg/min) and work output load
(PO, watt) values were recorded.
The FIM is a generic and global activity scale that
measures an individual’s independence in conducting
his or her daily fundamental physical and cognitive
activities. The FIM measures 81 items in two areas:
1) physical/motor function (13 items) and 2) cognitive/
psychosocial function (5 items). The items are divided
into six subgroups according to activities, four physical
and two cognitive. Each item is scored on a scale of one
to seven, with “level 1” indicating that the patient needs
complete help and “level 7” indicating complete inde-
pendence. The total FIM score varies between 18 and
126. We used the total FIM score in this study.10
Secondary outcome measures
The respiratory function tests were carried out using
a spirometer (SensorMedics 2400; US) in a sitting po-
sition. Forced vital capacity (FVC, mL), forced expi-
ration volume in one second (FEV1, mL), and FEV1/
FVC% rate were recorded.
Quality of life was assessed using the World Health
Organization Measure of Quality of Life, Short Form,
Turkish version (WHOQOL-Bref-Tr).11 The WHO-
QOL-Bref consists of 26 questions that cover generally
perceived quality of life. A national question was added
to the WHOQOL-Bref-Tr version during its validity
studies, so it contains 27 questions. In this study, the pa-
tients were asked to consider the previous 15 days when
answering the questions. Except for two general ques-
tions, the questions measure physical health, mental
health, social environment, and national environment
domain scores. The WHOQOL-Bref-Tr is scored on a
0-20 scale; as the physical health, mental health, social
environment, and national environment scores increase,
the quality of life score also increases.
221
not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AKKURT AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY

Disability was assessed using the Craig Handi- Table I.—Comparison of demographic data of intervention and
cap Assessment and Reporting Technique, short form control group.
(CHART-sf). The CHART-sf is a quality of life criteria Intervention group Control group
(N.=17) (N.=16)
form that evaluates the parameters of physical indepen-
Age (years), median [range] 33 [15-42] 37 [19-62]
dence, cognitive independence, mobility, social cohe- Gender
sion, occupation, and economic independence. This tool Male 16 (94.1%) 13 (81.3%)
is scored according to the patient’s participation level: a Female 1 (5.4%) 3 (18.8%)
high level of participation results in a high score and dis- Marital status
Married 8 (47.1%) 12 (75%)
ability results in a low score. Each parameter is scored Single 9 (52.9%) 4 (25%)
on a 0-100 scale. The maximum score of 100 represents Occupation
Unemployed 12 (70.6%) 8 (50.0%)
the participation level of a person without any disabil- Employed 1 (5.9%) 2 (12.5%)
ity. We used the CHART’s total score in our study.12 Retired 3 (17.6%) 4 (25%)
Psychological status was assessed using the Center Housewife 1 (5.9%) 2 (12.5%)
Comorbid disease
for Epidemiologic Studies Depression Scale (CES- Yes 0 (0%) 2 (12.5%)
D) and the Hospital Anxiety and Depression Scale No 17 (100%) 14 (87.5%)
(HADS). The CES-D is a self-report scale designed Smoking
Yes 4 (26.7%) 11 (68.8%)
to measure depressive symptoms in the general popu- No 13 (76.5%) 5 (31.3%)
lation. The scale consists of 20 questions designed to Neurological status
measure the patient’s experience in the previous week, C7 0 (0%) 1 (6.3%)
T3 1 (5.9%) 0 (0%)
scored on a four-point scale from 0-3, with a total score T5 0 (0%) 1 (6.3%)
of 0-60. Higher scores indicate greater severity of de- T6 1 (5.9%) 0 (0%)
T8 1 (5.9%) 0 (0%)
pression.13 The HADS consists of 14 items relating to T9 2 (11.8%) 2 (12.5%)
anxiety and depression. Each item is scored on a 0-3 T10 0 (0%) 1 (6.3%)
scale; higher scores indicate greater severity of anxiety T11 1 (5.9%) 1 (6.3%)
T12 5 (29.4%) 6 (37.5%)
and/or depression.14 L1 3 (17.6%) 1 (6.3%)
Metabolic syndrome parameters, including triglyc- L2 1 (5.9%) 2 (12.5%)
erides (TG, mg/dL), total cholesterol (T-chol, mg/dL), L3 2 (11.8%) 1 (6.3%)
ASIA Grade
high-density lipoprotein (HDL, mg/dL), low-density li- A 9 (52.9%) 10 (62.5%)
poprotein (LDL, mg/dL), fasting blood sugar (glucose, B 1 (5.9%) 0 (0%)
C 5 (29.4%) 5 (31.3%)
mg/dL), waist circumference (cm), and systolic (SBP) D 2 (11.8%) 1 (6.3%)
and diastolic (DBP) blood pressure (mm/Hg) were re- Complete 9 (52.9%) 10 (62.5%)
corded. Incomplete 8 (47.1%) 6 (37.5%)
Device
Wheelchair 10 (58.8%) 8 (50%)
Long leg braces + walker 5 (29.4%) 6 (37.5%)
Statistical method Short leg braces + crutches 0 (0%) 1 (6.3%)
Crutches 1 (5.9%) 0 (0%)
No device 1 (5.9%) 1 (6.3%)
The data obtained in the study were evaluated with the FAS stage
SPSS for Windows v.20.0 program; P<0.05 was accept- 0 10 (58.8%) 8 (50%)
ed as significant. The nominal variables from the demo- 1 5 (29.4%) 6 (37.5%)
2 0 (0%) 1 (6.3%)
graphic data of both groups were assessed with the chi- 3 1 (5.9%) 0 (0%)
square test, and the metric variables were assessed with 4 1 (5.9%) 1 (6.3%)
5 - -
the Mann-Whitney U-test. The Friedman test was used
BMI (kg/m2), 23.88 [30.42-16.65] 24.66 [16.71-29.07]
for in-group comparisons of Weeks 0, 6, and 12. When a median [max-min]
difference was found at the end of this test, the Wilcoxon Duration of disease (months), 15 [144-2] 15 [120-3]
or other proprietary information of the Publisher.

test was applied. Basal values between the two groups
and differences at Weeks 0-6, 0-12, and 6-12 were as-
sessed with the Mann–Whitney U-test. The Bonferroni
test was used for the comparison of the two groups.
median [max-min]
Where not otherwise stated, values are expressed as number of patients (percentage).
ASIA: American Spinal Injury Association Scale; FAS: Functional Assessment
Scale; BMI: Body Mass Index.
No statistically significant intergroup difference versus baseline (P>0.05).

222 European Journal of Physical and Rehabilitation Medicine April 2017

not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY AKKURT

Results significant improvement in pVO2 and PO at Weeks 0-6

A total of 45 patients were eligible for the study and
fulfilled the inclusion criteria. Five patients refused to
participate in the study, and the remaining 40 patients
were randomized into the intervention group (N.=20) or
the control group (N.=20). Three patients in interven-
tion group failed to complete the program due to diffi-
culty commuting to the hospital. In control group, three
patients withdrew (lost to follow-up) and one patient
was unwilling to complete the final assessments. Thus,
17 patients in intervention group and 16 patients in con-
trol group completed the study.
The demographic data of the two groups are shown in
Table I. The demographic and clinical data at baseline
showed no significant differences between intervention
and control group (P>0.05).
Primary outcomes
The pVO2 and PO values of the patients in the aero-
bic intervention group increased after the rehabilitation
by 39.6% and 45.4%, respectively, compared to their
pre-rehabilitation values. The intervention difference
analysis showed that intervention group demonstrated
and at Weeks 6-12 (P<0.05, Table II). However there
were no statistically significant differences in the con-
trol group in regard to pVO2 and PO values during the
assessment periods (P>0.05). No difference was found
significant in both groups in accordance with FIM in the
assessment periods (P>0.05, Table II).
Secondary outcomes
There were no statistically significant intergroup dif-
ferences at Weeks 0-6, Weeks 6-12 and Weeks 0-12,
both in the intervention group and the control group with
regard to respiratory function tests (FEV1), FVC, FEV1/
FVC (Table III), disability levels (Chart-sf: physical,
cognitive, mobility, work, social domains) (Table IV),
quality of life (WHOQOL-Bref-Tr: physical, cognitive,
mobility, work, social domains) (Table V), psychologi-
cal status (HADS, CES-D) (Table VI), or metabolic
syndrome parameters (Tchol, TG, HDL, LDL, glucose,
waist circumference, SBP, DBP) (Table VII) (P>0.05).
Also, in the control group, no significant differences
were found in any of the parameters at the end of the
rehabilitation (P>0.05).

Table II.—Comparison of functional status of intervention group and control group.

P0 P1 P2
Intervention group (N.=17) Control group (N.=16)
Median value* value* value*
[max-min] (Weeks (Weeks (Weeks
Week 0 Week 6 Week 12 Week 0 Week 6 Week 12 0-6) 0-12) 6-12)
pVO2 19.1 [35.9-5.6] 22.1 [34.5-12.8] 23.4 [33.2-15.5] 15.45 [31.3-11.4] 16.8 [22.4-11] 16.8 [30.5-9.7] 0.03 0.02 0.30
(mL/kg/min)
PO (W) 76 [97-40] 94 [121-54] 98 [146-68] 56 [127-29] 67.5 [86-30] 70 [139-31] 0.04 0.02 0.28
FIM 63 [118-50] 63 [118-50] 62.5 [118-50] 73.5 [119-50] 72 [94-56] 74 [119-56] 1.000 1.000 1.000
*Intergroup difference.
pVO2: peak oxygen uptake (mL/kg/min); PO: work output load (W); FIM: Functional Independence Measurement (total score).

Table III.—Comparison of respiratory function tests at Weeks 0, 6, and 12 of intervention group and control group.
Respiratory func- Intervention group (N.=17) Control group (N.=16)
tion tests Week 0 Week 6 Week 12 Week 0 Week 6 Week 12
FEV1 (mL) 3.5 [3.7-2.3]* 3.44 [4.0-2.6] 3.36 [3.9-2.5] 2.63 [4.9-1.7]* 2.9 [4.83-1.83] 2.8 [4.9-1.6]
FEV1 (%) 85 [116-54] 86 [108-62] 85 [104-58] 78 [119-47] 79 [115-38] 83 [118-54]
FVC (mL) 3.8 [4.7-2.5] 4.08 [4.6-2.9] 4.111 [4.53-2.6] 3.2 [5.5-1.8] 3.3 [5.55-1.5] 3.4 [5.9-2.1]
FVC (%) 82 [124-49] 84 [117-66] 83.5 [115-51] 83.5 [125-39] 78 [118-34] 85 [122-56]
or other proprietary information of the Publisher.

FEV1/FVC 86.76 [98.2-73.6] 84.08 [95.1-74.4] 83.25 [96.0-67.9] 83.2 [98.3-75.2] 81.8 [92.42-72.41] 82.7 [90.5-73.2]
Values are expressed as median [max-min].
FEV1: forced expiration volume in one second; FVC: forced vital capacity.
*The FEV1 value is significantly better in the exercise group at baseline (P<0.05).
Non-significant statistical intergroup difference (P>0.05) at Weeks 0-6, Weeks 6-12 and at Weeks 0-12.

Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine 223

not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AKKURT AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY

Table IV.—Comparison of disability of intervention group and control group.

Intervention group (N.=17) Control group (N.=16)
Chart-sf item
Week 0 Week 6 Week 12 Week 0 Week 6 Week 12
Physical 60 [100-4] 52 [100-4] 65 [100-4] 12 [100-4] 46 [100-4] 36 [100-4]
Cognitive 37 [89-0] 37 [59-0] 46.5 [85-0] 15 [100-0] 26 [100-0] 41 [100-15]
Mobility 32 [92-12] 53 [90-15] 50.5 [76-6] 36 [100-0] 42 [67-6] 37 [100-10]
Work 0 [63-0] 0 [36-0] 0 [50-0] 6.25 [100-0] 43.8 [43-0] 10 [100-0]
Social 100 [100-64] 100 [100-61] 100 [100-64] 100 [100-64] 100 [100-61] 100 [100-82]
Values are expressed as median [max-min].
Chart-sf: Handicap Assessment and Reporting Technique, short form
No significant statistical intergroup difference (P>0.05) at Weeks 0-6, Weeks 6-12 and Weeks 0-12.

Table V.—Comparison of quality of life of intervention group and control group.

Intervention group (N.=17) Control group (N.=16)
WHOQOL-Bref-Tr item
Week 0 Week 6 Week 12 Week 0 Week 6 Week 12
Physical 11.4 [14.3-6.9] 11.4 [14.3-6.9] 10.9 [13.1-7.4] 10.86 [14.29-6.29] 10.86 [13.7-8.6] 10.9 [14.3-6.3]
Psychological 13.3 [17.3-10] 13.3 [17.3-10] 13.7 [17-5] 12 [15.3-7.3] 12 [14.7-7.3] 12.7 [17-9]
Social 20 [20-4] 12 [20-4] 12 [20-6.7] 10.7 [16-6.7] 10.67 [16-6.7] 14.7 [20-8]
Environment 11.6 [14.2-5.3] 11.56 [14.2-5.3] 12 [14.22-4] 12 [14.7-8] 12 [14.7-8] 12 [15.6-8.4]
Values are expressed as median [max-min].
WHOQOL-Bref-Tr: World Health Organization Measure of Quality of Life, Turkish version.
No significant statistical intergroup difference (P>0.05) at Weeks 0-6, Weeks 6-12 and Weeks 0-12.

Table VI.—Comparison of psychological aspects of intervention group and control group.

Intervention group (N.=17) Control group (N.=16)
Psychological symptoms
Week 0 Week 6 Week 12 Week 0 Week 6 Week 12
HADS 19 [29-5] 18 [29-9] 19 [39-14] 19.5 [28-15] 17.5 [24-14] 20 [29-12]
CES-D 19 [52-4] 15 [48-5] 16 [43-4] 21 [32-4] 26 [48-10] 24 [39-4]
Values are expressed as median [max-min].
CES-D: Center for Epidemiologic Studies Depression Scale; HADS: Hospital Anxiety Depression Scale.
No significant statistical intergroup difference (P>0.05) at Weeks 0-6, Weeks 6-12 and Weeks 0-12.

Table VII.—Comparison of metabolic syndrome parameters of intervention group and control group.
Intervention group (N.=17) Control group (N.=16)
Metabolic values
Week 0 Week 6 Week 12 Week 0 Week 6 Week 12
T-chol (mg/dL) 177 [267-140] 181 [258-137] 187 [284-187] 178 [241-119] 177 [282-119] 180 [276-117]
TG (mg/dL) 133 [221-69] 146 [231-42] 138.5 [260-50] 122 [314-49] 118 [313-44] 148 [292-67]
LDL (mg/dL) 111 [176-78] 112 [172-88] 111 [192-63] 112.5 [164-9] 115.5 [170-53] 109 [176-54]
HDL (mg/dL) 37 [67-28] 41 [55-28] 37 [78-26] 40.5 [65-28] 43 [67-35] 46 [57-33]
Glucose (mg/dL) 80 [105-52] 81 [96-58] 76.5 [96-63] 80.5 [99-53] 87 [111-74] 83 [120-71]
Waist circumference (cm) 86.5 [124-72] 90 [124-72] 91.25 [124-72] 94.5 [102-66] 94.5 [102-66] 96 [103-76]
SBP (mmHg) 100 [115-90] 100 [120-90] 100 [110-90] 100 [120-90] 100 [120-90] 100 [120-90]
DBP (mmHg) 60 [70-60] 60 [70-60] 60 [70-60] 60 [70-60] 60 [70-60] 60 [70-60]
T-chol: total cholesterol; TG: triglycerides; LDL: low-density lipoprotein; HDL: high-density lipoprotein; SBP: systolic blood pressure; DBP: diastolic blood pressure.
No significant statistical intergroup difference (P>0.05) at Weeks 0-6, Weeks 6-12 and Weeks 0-12.

Discussion their general rehabilitation exercises, no improvement

or other proprietary information of the Publisher.

was seen in their breathing function tests, quality of life,

Although an increase in aerobic capacity was seen at disability, psychological status, or metabolic syndrome
the end of our study in the patients with SCI after a 12- parameters.
week aerobic exercise with arm ergometer was added to The respiratory system disorders seen in SCI patients

224 European Journal of Physical and Rehabilitation Medicine April 2017

not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY AKKURT
are among the disorders that most frequently lead to
mortality, morbidity, and economic burden.15 The disor-
ders in these patients’ inspiratory muscles prevent deep
breathing, leading to dyspnea and/or lung collapse. In
addition, deficient expiratory muscles reduce coughing
and the discharge of secretions from the lungs, leading
to infections in the airways.15 The respiratory function
disorder seen in acute-stage SCI patients, particularly
in patients with cervical and upper thoracic vertebral
injuries, is reported to be associated with respiratory
muscle paralysis, whereas that of chronic-stage patients
is general microatelectases accompanying the respira-
tory muscle paralysis.16 While some studies have re-
ported that significant increases were observed in re-
spiratory function tests as a result of arm exercises,17, 18
other studies have reported that exercise is ineffective.15
However, in studies where aerobic arm exercise had
an impact on respiratory function, the SCI was at level
thoracic 12 (T12) or above.18, 19 Although improvement
in respiratory function has been seen due to the activa-
tion of accessory respiratory muscles as a result of arm
exercises, we linked the reason for not seeing such an
improvement in our study to the fact that most of our
patients had a neurological level of T12 or under, they
had the disease for longer than a year, and they were not
trained with an inspiratory or expiratory muscle trainer.
As a result, we think it would be useful to compare the
results of respiratory function tests when training SCI
patients with an inspiratory and/or expiratory muscle
trainer and when training them with aerobic exercise
only.
It has been reported that cardiovascular disease,
which is one of the causes of morbidity and mortality
in SCI, develops secondary to the inactivity associated
with SCI.20 Inactivity leads to lipid changes, abnormal
glucose hemostasis, increased obesity, and decreased
cardiac fitness. In addition, SCI-related cardiovascular
problems such as blood pressure abnormalities, deep
venous thrombosis, rhythm disturbances, and blunted
cardiovascular response to exercise 21 are observed in
SCI patients. Ordinary activities of daily living remain
insufficient for the continuation of cardiovascular fit-
ness in SCI patients; it has been reported that increased
or other proprietary information of the Publisher.
physical activity would reduce the risk of developing
cardiovascular diseases.22 Therefore, it is important to
encourage SCI patients to exercise. Due to motor fail-
ure in the lower extremities, upper extremity exercises
Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine
would be a logical choice for SCI patients. Aerobic arm
exercise has been shown to increase aerobic capacity by
an average of 20-50% in SCI patients in the short term
(4-20 weeks) by producing peripheral (skeletal muscle)
adaptation.23 Similarly, we found a significant increase
of 39.6% in the aerobic capacity of our patients. The
patients stated that due to this increase in exercising ca-
pacity, they were less tired at the end of their activities
of daily living (performing transfers and self-care), they
could sustain a certain activity longer, and they had in-
creased self-confidence.
SCI patients have lower quality of life compared with
their able-bodied counterparts.3 The impaired mobiliza-
tion of these patients and the secondary complications
that develop (cardiopulmonary, pressure ulcer, chronic
pain, etc.) may compromise aspects of psychological
well-being, social participation, and overall quality of
life.24‑26 Studies have shown that exercising has a posi-
tive impact on quality of life.27, 28 However, different
types of exercises were administered in these studies,
they used different measures of quality of life, and they
found that the relationship between physical activity
and quality of life appears to be robust. However, the
case study by Effing et al.29 did not result in quality
of life improvements. We also did not see any positive
effects of exercising on quality of life. We think the
reason for this finding was that the number of patients
was small, the duration of rehabilitation was short, the
patients could not be provided with the necessary so-
cial environment and support, and the patients’ func-
tional expectations could not be fulfilled. Assuming
that an exercise involving ambulation activities (e.g.,
body weight-supported treadmill training, overground
training) would have a more positive impact on quality
of life, we think there is a need for further studies ex-
ploring the effects of arm and leg ergometry on quality
of life in SCI.
Some patients with SCU undergo a depression attack
in the period following the injury. Studies have reported
that the rate of major depression is 22.30% in SCI pa-
tients, that such depression heals within 3-6 months, and
that patients who could not recover from it lacked suf-
ficient social support.30 While the meta-analysis showed
that exercise has a positive impact on depression,31
other studies have reported no positive impact on de-
pression.27, 32 We also did not see any positive impact of
exercising on depression at the end of our study. One of
225
not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AKKURT AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY
the reasons for this finding is that the depressive mood
of our patients was minimal at the beginning of the ill-
ness and there was very little room for improvement.
Considering that exercising is effective in patients with
greater depressive symptomatology, these findings are
not particularly surprising. We think that in addition to
exercise, a social environment where SCI patients can
come together can greatly improve the psychological
state of the patients.
When assessing disability in our study, we took into
consideration physical independence, cognitive inde-
pendence, mobility, occupation, social cohesion, and
economic independence, and we found no significant
differences after the rehabilitation. These results show
that as patients’ mobility increases, their physical inde-
pendence and success at work also increase, their feel-
ing of disability decreases, and the improvements in
their physical independence, mobility, work, and eco-
nomic independence decrease the feeling of disability
in general. However, although the exercise capacity of
the patients in our study increased, other functions, in-
cluding mobility and physical independence, did not,
because their walking function did not improve. In this
respect, we think that patients must be informed about
their illness and a cognitive-behavioral therapy should
be administered.
The immobilization experienced by patients with
SCI results in nutritional disorders, obesity, dyslip-
idemia, increased insulin resistance, and metabolic
syndrome. Fasting dyslipidemia, depressed HDL cho-
lesterol, and normal or low total cholesterol are often
seen in SCI patients.33 However, the role of exercise
training on metabolic disorders after an SCI has not
been well established,34, 35 possibly because the arm
has less muscle mass 36 and no high-intensity exer-
cises are performed.37 Similar to these studies, we
also did not find any changes in metabolic parameters
due to exercise. To clarify this result, there is a need
for further controlled, randomized studies, involving
a large number of patients, to investigate the effects
of high-intensity arm and leg ergometry on metabolic
parameters. To the best of our knowledge, no single
study has looked at changes in all parameters (car-
or other proprietary information of the Publisher.
diopulmonary, metabolic, physical function, quality
of life, and psychological well-being) simultaneously.
We hope our study will provide guidance for future
studies.
226 European Journal of Physical and Rehabilitation Medicine April 2017
Limitations of the study
The limitation of our study is that there was no long-
term follow-up of the patients. This is because the
patients lost motivation to exercise, as they could not
achieve the desired functional level (walking indepen-
dently) at the end of the exercises. Because we realized
that long-term follow-up could not produce sound re-
sults, the study was discontinued. However, because
exercise has been shown to generate an increase in mo-
tor functions due to the reorganization of the brain and
spinal cord, even in the chronic stage,3 we recommend
that the effects of exercising on the motor functions of
chronic-stage SCI patients be observed for a long time
(6 months and longer) in future studies. Unintentionally,
almost all of our subjects were paraplegic patients. We
think the reason was that the cause of trauma in most
of the patients included in the study was failure to wear
safety belts during motor vehicle accidents. Therefore,
we think it is important to conduct studies comparing
the effects of exercise in tetraplegic and paraplegic pa-
tients.
Conclusions
In conclusion, this study showed that short-term aer-
obic exercises administered to SCI patients increased
their exercise capacity. The reason for this finding might
be that exercising has a local effect rather than a central
one, because arm muscles have less muscle mass than
leg muscles do. A longer rehabilitation program may be
necessary to obtain more benefits from arm aerobic ex-
ercises in SCI patients. For this reason, there is a need
for further studies to compare the effects of arm and leg
ergometry.
References
1. Brurok B, Helgerud J, Karlsen T, Leivseth G, Hoff J. Effect of aero-
bic high-intensity hybrid training on stroke volume and peak oxygen
consumption in men with spinal cord injury. Am J Phys Med Rehabil
2011;90:407-14.
2. Knechtle B, Müller G, Willmann F, Eser P, Knecht H. Comparison
of fat oxidation in arm cranking in spinal cord-injured people versus
ergometry in cyclists. Eur J Appl Physiol 2003;90:614-9.
3. Kloosterman MG, Snoek GJ, Jannink MJ. Systematic review of the
effects of exercise therapy on the upper extremity of patients with
spinal-cord injury. Spinal Cord 2009;47:196-203.
4. Spooren AI, Janssen-Potten YJ, Kerckhofs E, Seelen HA. Outcome of
motor training programmes on arm and hand functioning in patients
with cervical spinal cord injury according to different levels of the
ICF: a systematic review. J Rehabil Med 2009;41:497-505.
not permitted. It is not permitted to remove, cover, overlay, obscure, block, or change any copyright notices or terms of use which the Publisher may post on the Article. It is not permitted to frame or use framing techniques to enclose any trademark, log
means which may allow access to the Article. The use of all or any part of the Article for any Commercial Use is not permitted. The creation of derivative works from the Article is not permitted. The production of reprints for personal or commercial use i
This document is protected by international copyright laws. No additional reproduction is authorized. It is permitted for personal use to download and save only one file and print only one copy of this Article. It is not permitted to make additional copies
(either sporadically or systematically, either printed or electronic) of the Article for any purpose. It is not permitted to distribute the electronic copy of the article through online internet and/or intranet file sharing systems, electronic mailing or any other
©
COPYRIGHT 2017 EDIZIONI MINERVA MEDICA
AEROBIC EXERCISE REHABILITATION IN SPINAL CORD INJURY AKKURT
5. El-Sayed MS, Younesian A. Lipid profiles are influenced by arm
cranking exercise and training in individuals with spinal cord injury.
Spinal Cord 2005;43:299-305.
6. Hicks AL, Martin KA, Ditor DS, Latimer AE, Craven C, Bugaresti J,
et al. Long-term exercise training in persons with spinal cord injury:
effects on strength, arm ergometry performance and psychological
well-being. Spinal Cord 2003;41:34-43.
7. Pescatello LS. American College of Sports Medicine ACSM’s guide-
lines for exercise testing and prescription. Ninth edition. Lippincott
Williams & Wilkins; 2013
8. Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves
DE, Jha A, et al. International standards for neurological classi-
fication of spinal cord injury (Revised 2011). J Spinal Cord Med
2011;34:535-46.
9. Holden MK, Gill KM, Magliozzi MR, Nathan J, Piehl-Baker L. Clin-
ical gait assessment in the neurologically impaired. Reliability and
meaningfulness. Phys Ther 1984;64:35-40.
10. Küçükdeveci AA, Yavuzer G, Elhan AH, Sonel B, Tennant A. Ad-
aptation of the Functional Independence Measure for use in Turkey.
Clin Rehabil 2001;15:311-9.
11. Eser SY, Fidaner H, Fidaner C, Elbi H. Measure of quality of life
WHOQOL- 100 and WHOQOL-Bref. Dergisi 1999;7(2 Suppl):5-13.
12. Dijkers M, Yavuzer G, Ergin S, Weitzenkamp D, Whiteneck GG. A
tale of two countries: environmental impacts on social participation
after spinal cord injury. Spinal Cord 2002;40:351-62.
13. Radloff LS, Teri L. Use of the Center for Epidemiological Studies
Depression Scale with older adults. Clin Gerontol 1986;5:119-36.
14. Aydemir Ö, Güvenir T, Küey L, Kültür S. Hastane Anxietysiyete ve
Depresyon Ölçeği Türkçe Formunun Geçerlik Güvenilirlik Çalışması.
Türk Psikiyatri Dergisi 1997;8:280-7.
15. Tamplin J, Berlowitz DJ. A systematic review and meta-analysis of
the effects of respiratory muscle training on pulmonary function in
tetraplegia. Spinal Cord 2014;52:175-80.
16. Galeiras Vázquez R, Rascado Sedes P, Mourelo Fariña M, Montoto
Marqués A, Ferreiro Velasco ME. Respiratory management in the pa-
tient with spinal cord injury. Biomed Res Int 2013;2013:168757.
17. Sutbeyaz ST, Koseoglu BF, Gokkaya NK. The combined effects of
controlled breathing techniques and ventilatory and upper extremity
muscle exercise on cardiopulmonary responses in patients with spinal
cord injury. Int J Rehabil Res 2005;28:273-6.
18. Le Foll-de Moro D, Tordi N, Lonsdorfer E, Lonsdorfer J. Ventila-
tion efficiency and pulmonary function after a wheelchair interval-
training program in subjects with recent spinal cord injury. Arch Phys
Med Rehabil 2005;86:1582-6.
19. Gómara-Toldrà N, Sliwinski M, Dijkers MP. Physical therapy after
spinal cord injury: a systematic review of treatments focused on par-
ticipation. J Spinal Cord Med 2014;37:371-9.
20. Jacobs PL, Nash MS. Exercise recommendations for individuals with
spinal cord injury. Sports Med 2004;34:727-51.
21. Phillips AA, Cote AT, Warburton DE. A systematic review of exercise
as a therapeutic intervention to improve arterial function in persons
living with spinal cord injury. Spinal Cord 2011;49:702-14.
22. Zwinkels M, Verschuren O, Janssen TW, Ketelaar M, Takken T;
Sport-2-Stay-Fit study group. Exercise training programs to improve
Conflicts of interest.—The authors certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript.
Article first published online: November 8, 2016. - Manuscript accepted: November 7, 2016. - Manuscript revised: October 5, 2016. - Manuscript received:
January 2, 2015.
or other proprietary information of the Publisher.
Vol. 53 - No. 2 European Journal of Physical and Rehabilitation Medicine
hand rim wheelchair propulsion capacity: a systematic review. Clin
Rehabil 2014;28:847-61.
23. Warburton DER, Krassioukov A, Sproule S, Eng JJ. Cardiovascular
Health and Exercise Following Spinal Cord Injury. In: Eng JJ, Teasell
RW, Miller WC, Wolfe DL, Townson AF, Hsieh JTC, et al., editors.
Spinal Cord Injury Rehabilitation Evidence. Volume 5.0. Vancouver:
ICORD; 2014, p. 1-48.
24. Post MW, van Leeuwen CM. Psychosocial issues in spinal cord in-
jury: a review. Spinal Cord 2012;50:382-9.
25. Dijkers M. Quality of life after spinal cord injury: a meta-analysis
of the effects of disablement components. Spinal Cord 1997;35:829-
40.
26. Community reintegration following spinal cord injury. In: Eng J, Tea-
sell R, Miller W, Wolfe DL, Townson AF, Hsieh JTC, et al., editors.
Spinal Cord Injury Rehabilitation Evidence. Volume 2.0. Vancouver:
ICORD; 2008. p. 4-66.
27. Hicks AL, Martin Ginis KA, Pelletier CA, Ditor DS, Foulon B, Wolfe
DL. The effects of exercise training on physical capacity, strength,
body composition and functional performance among adults with spi-
nal cord injury: a systematic review. Spinal Cord 2011;49:1103-27.
28. Ditor DS, Latimer AE, Ginis KA, Arbour KP, McCartney N, Hicks
AL. Maintenance of exercise participation in individuals with spinal
cord injury: effects on quality of life, stress and pain. Spinal Cord
2003;41:446-50.
29. Effing TW, van Meeteren NL, van Asbeck FW, Prevo AJ. Body
weight-supported treadmill training in chronic incomplete spinal cord
injury: a pilot study evaluating functional health status and quality of
life. Spinal Cord 2006;44:287-96.
30. Elliott TR, Kennedy P. Treatment of depression following spinal cord
injury: an evidence-based review. Rehabil Psychol 2004;49:134-9.
31. Devillard X, Rimaud D, Roche F, Calmels P. Effects of training pro-
grams for spinal cord injury. Ann Readapt Med Phys 2007;50:490-8.
32. Warms CA, Belza BL, Whitney JD, Mitchell PH, Stiens SA. Lifestyle
physical activity for individuals with spinal cord injury: a pilot study.
Am J Health Promot 2004;18:288-91.
33. Cowan RE, Nash MS. Cardiovascular disease, SCI and exer-
cise: unique risks and focused countermeasures. Disabil Rehabil
2010;32:2228-36.
34. Carlson KF, Wilt TJ, Taylor BC, Goldish GD, Niewoehner CB,
Shamliyan TA, et al. Effect of exercise on disorders of carbohydrate
and lipid metabolism in adults with traumatic spinal cord injury:
systematic review of the evidence. J Spinal Cord Med 2009;32:361-
78.
35. Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Gater DR. The
effects of electrical stimulation on body composition and meta-
bolic profile after spinal cord injury - Part II. J Spinal Cord Med
2015;38:23-37.
36. Dallmeijer AJ, van der Woude LH, Hollander AP, van As HH. Physi-
cal performance during rehabilitation in persons with spinal cord in-
juries. Med Sci Sports Exerc 1999;31:1330-5.
37. de Groot PC, Hjeltnes N, Heijboer AC, Stal W, Birkeland K. Effect of
training intensity on physical capacity, lipid profile and insulin sensi-
tivity in early rehabilitation of spinal cord injured individuals. Spinal
Cord 2003;41:673-9.
227