Kaohsiung J Med Sci May 2007 • Vol 23 • No 5
232
People with spinal cord injury (SCI) exhibit deficits in volitional motor control and sensation that limit per-formance of daily tasks as well as the overall activity level [1]. Most patients who suffer from SCI experience some neurologic recovery and regain some muscle strength. Cheng et al [2] reported that the best prog-nosis is in patients who initially exhibit some spared
motor function. But another study showed that pa-tients with incomplete injuries merely recover faster than those with complete injuries, but their degree of recovery is not necessarily greater [3]. The relationship between the extent of strength recovery and spared motor function after injury has not been fully studied.
Poor physical fitness is usually found in persons with SCI due to their sedentary lives [4,5]. Many main long-term issues can be related to the alteration in body composition and metabolic function, including glucose intolerance, an unfavorable lipid profile, a decrease in lean body mass, and reduced physical condition-ing [6]. Compared with healthy populations, people with SCI were fatter according to their body mass
Received: September 6, 2006 Accepted: December 11, 2006 Address correspondence and reprint requests to: Dr Mao-Hsiung Huang, Department of Physical Medicine and Rehabilitation, Kaohsiung Medical University Hospital, 100 Tzyou 1stRoad, Kaohsiung 807, Taiwan.
E-mail: [email protected]
E
FFECTS OF
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UNCTIONAL
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LECTRICAL
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TIMULATION ON
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EAK
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ORQUE AND
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ODY
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OMPOSITION IN
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ATIENTS WITH
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NCOMPLETE
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ORD
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NJURY
Chin-Wei Liu,1Shih-Ching Chen,2Chia-Hsin Chen,1,3Tien-Wen Chen,4Jia-Jin Jason Chen,5Chun-Sheng Lin,1and Mao-Hsiung Huang1,3
1Department of Physical Medicine and Rehabilitation, Kaohsiung Medical University Hospital, 2Department of Physical Medicine and Rehabilitation, Taipei Medical University Hospital, 3Department of Rehabilitation, Faculty of Medicine, College of Medicine, Kaohsiung Medical
University, 4Department of Physical Medicine and Rehabilitation, Kaohsiung Municipal
Hsiao-Kang Hospital, Kaohsiung Medical University, and 5Institute of Biomedical Engineering, National Cheng Kung University, Taiwan.
The aim of this study was to investigate the change in body composition, leg girths, and muscle strength of patients with incomplete spinal cord injury (SCI) after functional electrical stimulation cycling exercises (FESCE). Eighteen subjects with incomplete SCI were recruited. Each patient received FESCE three times per week for 8 weeks. Body composition, thigh and calf girths of bilat-eral legs, muscle strength of bilatbilat-eral knee flexors and extensors were measured before and after 4 and 8 weeks of FESCE. A significant increase in bilateral thigh girth after 4 weeks of FESCE and significant increase in muscular peak torque of knee flexion and extension were found after 8 weeks of training. Besides, lean body mass increased significantly after complete treatment. FESCE can increase the thigh girth and muscular peak torque of patients with incomplete spinal cord injury.
Key Words:body composition, functional electrical stimulation, peak torque, spinal cord injury
Table 1.Patient characteristics
Subject Age (yr) Sex Weight (kg) Time since Neurologic ASIA class
injury (yr) level
1 52 M 64.1 3 T5 C 2 46 M 68.3 5 C4 C 3 32 M 63.2 2 T10 B 4 28 M 61.5 3 T12 C 5 45 M 78.8 4 C4 D 6 29 M 104.4 6 C7 D 7 33 F 62.2 1 T12 B 8 52 M 65.5 2 T5 B 9 46 F 53.4 4 T11 C 10 33 M 67.2 2 T10 C 11 33 M 78.8 5 T12 B 12 54 M 66.6 2 C4 D 13 26 M 77.3 2 L1 B 14 48 M 69.4 3 C3 D 15 61 M 74.4 9 C5 C 16 29 M 87.6 2 C4 D 17 46 M 78.3 1 T12 B 18 27 M 84.6 2 T7 C Mean 40.0± 11.3 M:F (16:2) 73.8± 13.9 3.2± 2.1 C:T:L (7:10:1) B:C:D (6:7:5)
Age, weight, and time since injury shown as mean±standard deviation. ASIA=American Spinal Injury Association; M=male; F=female.
index (BMI) and were significantly less lean with more adipose tissue [7]. A study by Maggioni et al [8] showed that total fat mass in the SCI group was significantly higher than in the able-bodied group (31.1% vs. 20.8%). Another study by Spungen et al [9] also indicated that the SCI group was 13± 1% fatter per unit of BMI (kg/m2) compared with the healthy group. Increased
incidence of some disorders including diabetes melli-tus, hypertension, and hyperlipidemia may be related to adverse changes in body composition that result from immobilization and skeletal muscle denerva-tion because of SCI [10,11]. Therefore, further control of the change in body composition in SCI patients is indicated.
Functional electrical stimulation (FES) is potentially useful in the rehabilitation of patients with SCI. Proven benefits include improvement in bone density, deep venous thrombosis, edema, and amelioration of spas-ticity [12,13]. Clinical studies have shown that by applying FES to the paralyzed muscles, functional contractions are produced that satisfy the physiologic motor demand as well as maintain the activity of the degenerative target, thus resulting in an improve-ment in patients’ functions [14]. As a result, FES cycling exercises (FESCE) involving the contraction of the muscles of the paralyzed limbs in individuals with SCI may help to decrease muscle atrophy [15]. Erika
et al [16] reported that FESCE increases skeletal mus-cle cross-sectional area with no change in adipose tis-sue in both the thigh and leg. Timson [17] also reported that this type of exercise induced greater muscle hyper-trophy in animals and humans than aerobic exercise. However, few reports have discussed the effect of FESCE on muscular strength and body composition in SCI patients with different grades. Therefore, in the present study, we tried to investigate the effect of FESCE in patients with various degrees of incom-plete SCI, and changes in their thigh and calf girth, peak muscular contractile forces, body composition, and BMI. The relationship between strength recovery and the spared motor function was also studied.
M
ETHODSSample and data sources
Eighteen subjects with age ranging from 26 to 61 years and with incomplete SCI were recruited. The basic data collected (Table 1) were age, gender, weight, time since injury, level of injury, degree of injury (American Spinal Injury Association [ASIA] class) [18] ASIA B: sensory but not motor functional is preserved below the level (6 subjects); ASIA C: motor function is pre-served and more than half of the key muscles below
the level have a muscle grade < 3 (7 subjects); ASIA D: motor function is preserved and at least half the key muscles below the level have a muscle grade ≥ 3 (5 subjects). The inclusion criteria for the subjects were: (1) at least 1 year after SCI, to avoid the possi-bility of the patient still being in the spinal shock stage; (2) subject able to tolerate electrical stimulation; (3) subject has minimal-to-moderate spasticity and no con-tracture of knees or ankles; (4) radiologic examination of the entire lower extremities was unremarkable, indi-cating absence of metallic implants, recent fracture, and any other defect; and (5) subject is medically sta-ble with a cooperative attitude. All the participants gave informed consent for the study and the protocol was approved by the Ethical Review Committee of Kaohsiung Medical University.
Outcome measurement
The thigh and calf girths, body weight, BMI, body com-position, and muscle peak torque of knee flexors and knee extensors were measured before and after FESCE.
Measurement of body composition
and BMI
The assessment of body composition from bioelectri-cal impedance analysis (BIA) is a recently developed technique. BIA is considered to be a simple, nontrau-matic, and reliable method to analyze body composi-tion [19]. An eight-polar tactile-electrode impedance meter (Inbody 3.0, Biospace, Seoul, Korea) was used in this study [20]. This instrument makes use of eight tactile electrodes: two are in contact with the palm and thumb of each hand and two with the anterior and posterior aspects of the sole of each foot. As many SCI subjects did not have enough muscle power to stand unassisted, all the subjects maintained a sitting position to measure the weight and body composition. The total body weight was measured on a standard weight scale before the body composition measure-ment. The body composition included body fat mass (kg), fat percentage (%), body lean mass (kg), and bone mass (kg). In addition, the height was self-reported and the BMI (kg/m2) of these subjects were derived
from the given data.
Measurement of thigh and calf girths
The measurements of thigh and calf girths were per-formed as follows: the subject kept a supine position with full relaxation of the lower limb muscles. The thigh
girth was measured with a flexible meter at 20 cm above the adductor tubercle, and calf girth was meas-ured at 10 cm below the tibial tubercle [21]. Every measurement was performed at the start of FES to avoid the influence of possible exercise-induced mus-cle swelling [22]. In order to optimize the accuracy of these measurements, the average of three measure-ments was taken at each location.
Measurement of isometric peak torque of
knee flexors and knee extensors
The voluntary torque capacity was evaluated to meas-ure the peak torque of the knee flexors and knee exten-sors with the modified isometric mode by using a Kin-Com dynamometer (Kin-Com 505, Chattanooga, TN, USA) under the trigger of electrical stimulation [23,24]. During isometric contraction, the knee muscle maintained a constant length as resistance was applied and no change in joint position occurred. Volitional isometric strength of the bilateral knee flexors and extensors were assessed with the subject seated on the dynamometer with the knee positioned at 100° from the horizontal position [25]. The subjects’ hips were positioned at about 85° of flexion. Meanwhile, the trunk, pelvis, thigh, and legs were stabilized with straps. Surface electrodes of the electrical stimulation machine were attached to the muscle belly of bilateral quadriceps and hamstrings. Patients tried to do max-imum muscular contraction of knee flexors and exten-sors on their own, in coordination with being triggered by the electrical stimulation at the same time with the same stimulation current density (140 mA) [26]. Each maximal volitional isometric torque of knee flexors and extensors was recorded as the average of five repeated measurements. The effect of gravity was also corrected for by subtracting the torque generated by the weight of the limb and the lever arm of the apparatus [27]. In order to avoid the extra torque induced by the sporadic spasms, lower stimulation intensities were chosen in these small number of cases. Besides that, in order to minimize possible effects of muscle tempera-ture before and after training, the room temperatempera-ture was kept constant at 20°C during the testing procedure.
FESCE training
FES-induced cycling exercise was performed by apply-ing 5× 7 cm surface electrodes to the muscle belly of bilateral quadriceps and hamstrings to achieve a se-quential rhythmic cycling motion. The sites of electrode
Table 3.Changes in girth of upper and lower legs (cm) in SCI subjects*
Before FESCE After 4 wks of FESCE After 8 wks of FESCE
Right thigh girth 48.2± 5.5 49.6± 5.2† 50.3± 5.1‡
Left thigh girth 47.4± 5.9 49.0± 5.4† 49.8± 5.2‡
Right calf girth 34.2± 3.8 34.5± 3.2 34.6± 3.3
Left calf girth 33.6± 4.9 33.8± 3.7 34.1± 3.9
*Data are presented as mean± standard deviation; †significant difference (p< 0.05) between the values before FESCE and those after 4 weeks of FESCE; ‡significant difference (p< 0.05) between the values before FESCE and those after 8 weeks of FESCE. FESCE = func-tional electrical stimulation cycling exercises; SCI = spinal cord injury.
placement were not only easily accessible but also relatively close to the motor points, which needed less stimulation current to generate a satisfactory contrac-tion. The pulse frequency was set at 30 Hz, rectangu-lar pulse duration of 300μs, and current variation of 10–132 mA, which was controlled by a microprocessor in order to maintain a pedaling rate of 45 rpm [28,29]. Although the equipment contained an arm-crank struc-ture, it could only be used to help establish cycling by an SCI individual and to warm up before electrical stimulation. Patients received the FESCE thrice a week for 8 weeks. Each session lasted 30 minutes with warm-up and cool-down periods of 3 minutes. Evaluations were performed before and after 4 and 8 weeks of training.
Statistical analysis
Paired t test was used to analyze changes in thigh and calf girths, body composition, BMI, and muscle peak torque after 4 and 8 weeks of training, respectively. A statistically significant difference was set at p< 0.05. Analysis of variance was used to analyze the differ-ent percdiffer-entages of strength recovery among incom-plete SCI levels (ASIA B–D). Statistical significance between group means was determined by Scheffe’s tests (p< 0.05). Furthermore, the relationship between
initial strength in the pretraining period and percent-age of strength gain after the 8-week training course was performed by Pearson correlations. All analyses were performed with the SPSS program (SPSS Inc., Chicago, IL, USA).
R
ESULTSChanges in body composition and BMI
The changes in body composition before and after training are given in Table 2. Total body weight increased from 73.8±13.9kg to 75.0±14.3kg (p=0.062). Mild increase in body lean mass (from 51.6± 7.1 to 52.8± 8.2) was found after 8 weeks of FESCE (p = 0.03). However, there were no other marked differences in body composition, including body fat mass, fat percentage, bone mass and BMI.
Changes in upper and lower leg girths
Changes in thigh and calf girths are shown in Table 3. The 18 patients showed significant increase in bilateral thigh girth after 4 weeks of training (p< 0.05). Mean thigh girth increased from 48.2± 5.5 cm to 49.6 ± 5.2 cm for the right leg, and 47.4± 5.9 cm to 49.0 ± 5.4 cm for the left leg. Thereafter, there was only a mild increase
Table 2.Changes in body composition after training in SCI subjects*
Before FESCE After 4 wks of FESCE After 8 wks of FESCE
Total body weight (kg) 73.8± 13.9 73.9± 13.7 75.0± 14.3
Body fat mass (kg) 18.6± 8.6 18.7± 8.5 18.7± 8.4
Body lean mass (kg) 51.6± 7.1 52.3± 7.5 52.8± 8.2†
Percentage fat mass (%) 25.3± 7.1 25.4± 6.9 24.9± 6.6
Bone weight (kg) 3.5± 0.4 3.5± 0.4 3.6± 0.4
BMI (kg/m2) 25.4± 3.9 25.5± 3.8 25.7± 3.5
*Data are presented as mean± standard deviation; †significant difference (p< 0.05) between the values before FESCE and those after 8 weeks of FESCE. FESCE = functional electrical stimulation cycling exercises; SCI = spinal cord injury.
when FESCE continued. A slight increase in calf girth from 34.2± 3.8 cm to 34.6 ± 3.3 cm in the right leg and 33.6± 4.9 to 34.1 ± 3.9 cm in the left leg occurred after 8 weeks of training. However, the slight increase in calf girth was not statistically significant (p> 0.05).
Changes in mean peak torque
Changes in isometric peak torque in bilateral knee flex-ors and knee extensflex-ors are shown in Table 4. There was no significant increase in mean peak torque after 4 weeks of FESCE; however, there was significant in-crease (p< 0.05) in mean peak torque of bilateral knee flexors and right knee extensors after 8 weeks of train-ing. Although there was little improvement in peak torque of the left knee extensors after training, the
strength of the left knee extensors demonstrated an increasing trend (p= 0.067) after 8 weeks of FESCE.
Correlation between SCI severity and
FESCE training
Further analysis was performed with reference to the subjects with different grades of motor function (ASIA B–D). The results of isometric peak torques and the percentage of torque gains in bilateral knee flexors and knee extensors of these three groups are shown in Table 5. Although the subjects all had peak torque increase after completing FESCE training, subjects in the ASIA D group had a higher percentage of strength gains in bilateral knee extensors and flex-ors than those in the ASIA B and C groups (p< 0.05)
Table 4.Isometric peak torques of knee extensors and flexors before and after training in SCI subjects*
Peak torque (Nm) Before FESCE After 4 wks of FESCE After 8 wks of FESCE
Right knee extensor 45.9± 32.8 47.6± 34.8 52.6± 40.7†‡
Left knee extensor 37.9± 26.8 38.3± 32.1 38.9± 29.9
Right knee flexor 16.1± 11.9 16.5± 10.2 17.7± 11.6†‡
Left knee flexor 15.1± 6.3 15.2± 6.1 16.9± 6.8†‡
*Data are presented as mean± standard deviation; †significant difference (p< 0.05) between the values after 4 weeks of FESCE and those after 8 weeks of FESCE; ‡significant difference (p< 0.05) between the values before FESCE and those after 8 weeks of FESCE. FESCE = functional electrical stimulation cycling exercises; SCI = spinal cord injury.
Table 5.Results of isometric peak torque gains in knee extensors and flexors after training (Nm)*
ASIA B group (n= 6) ASIA C group (n= 7) ASIA D group (n= 5) Right knee extensor
Before FESCE 22.1± 11.9 44.6± 26.3 76.3± 36.4
After FESCE 22.8± 9.8 47.4± 31.4 95.8± 39.7
Strength gains (%) 3.2 6.3 25.6‡§
Left knee extensor
Before FESCE 18.2± 6.2 38.7± 9.7 52.6± 11.3
After FESCE 18.5± 5.8 42.5± 15.1 58.5± 14.4
Strength gains (%) 1.6 9.8† 11.2‡
Right knee flexor
Before FESCE 11.7± 5.6 14.4± 11.7 21.1± 10.9
After FESCE 12.2± 9.1 16.7± 13.1 25.9± 11.8
Strength gains (%) 4.3 15.9† 22.7‡§
Left knee flexor
Before FESCE 12.1± 6.2 16.2± 6.3 16.9± 5.5
After FESCE 12.6± 5.1 17.5± 7.8 21.1± 5.9
Strength gains (%) 4.1 8.0 24.9‡§
*Isometric torques presented as mean± standard deviation; †significant difference (p< 0.05) of strength gains (%) between ASIA B group and ASIA C group; ‡significant difference (p< 0.05) of strength gains (%) between ASIA B group and ASIA D group; §significant difference (p< 0.05) of strength gains (%) between ASIA C group and ASIA D group. ASIA = American Spinal Injury Association; FESCE = functional electrical stimulation cycling exercises.
after 8 weeks of FESCE, and those in the ASIA C group had better results compared with the ASIA B group.
Relationship between changes in muscle
peak torque and initial severity
of paresis
Correlations between initial peak torque before train-ing and the percentage of changes in knee muscular strength after 8 weeks of training were analyzed to determine the impact of initial motor function on the potential for recovery. Pearson correlation coeffi-cients were 0.86 (p= 0.013 for right knee extensor), 0.65 (p= 0.048 for left knee extensor), 0.5l (p = 0.032 for left knee flexor), and 0.49 (p= 0.062 for right knee flexor). These results showed that the percentage of strength gains during FESCE was positively related to the spared muscle function before FESCE, implying that patients who had higher residual muscle strength might achieve better results from training.
D
ISCUSSIONMany reports on body composition assessment in SCI subjects usually show that total fat mass is signif-icantly higher and total lean mass signifsignif-icantly lower than in healthy people [30,31]. But only a few studies have examined the issue of body composition change in SCI patients after FESCE. Hjeltnes et al [32] reported that lean body mass increased and fat mass decreased for SCI patients after 8 weeks of FESCE. The body com-position in their study was evaluated by dual-energy X-ray absorptiometry (DEXA), which showed increase in lean body mass from 66.2± 2.6% to 68.2 ± 2.1% (p< 0.05), with a decrease in whole body fat content from 29.7± 2.6% to 27.8 ± 2.1% (p < 0.05) after training. However, those results came from the analysis of a small group of patients (n=5). In the present study, 8 weeks of FESCE resulted in a mild increase in lean body mass from 51.6± 7.1 kg to 52.8 ± 8.2 kg (p < 0.05), but no significant change in fat body mass. Although there were some differences in the results between the two studies, this possibly resulted from various FES training intensities and differences in the evalua-tion equipment. Body composievalua-tion in incomplete SCI subjects always deteriorates as a consequence of both neurologic injury and activity deficiency. Our data sug-gest that FESCE partially improves lean body mass within 8 weeks of training. In addition, analysis of
the relationships between the increment in lean body mass and gains in peak torque of bilateral legs after the 8-week training course were performed. Pearson cor-relation coefficients were 0.53 (p= 0.061) for right knee extensor, 0.41 (p= 0.093) for left knee extensor, 0.63 (p=0.078) for right knee flexor, and 0.55 (p=0.073) for left knee flexor. The positive correlation trend demonstrated the possibility that increase in lean body mass may bring about the regaining of muscle strength. Further study for understanding the rela-tionship is warranted.
SCI results in a significant and dramatic loss of muscle mass and muscle strength that can have a harmful impact on the health of the individual. Muscle fiber cross-sectional area starts to decline within 1 month after SCI [33]. Electrical stimulation of the muscular paresis may improve the condition of mus-cle size and peak contractile forces. Dudley et al [34] demonstrated the effectiveness of a simple program of electrically induced knee extensions, performed twice-weekly over an 8-week period, dramatically revers-ing the muscle size of the quadriceps muscles in SCI patients. The present results also show that individu-als with incomplete SCI responded to the 8-week FES cycling program. The subjects showed significant increases in bilateral thigh girth even after 4 weeks of training. Although calf girth increased after training, this was not statistically significant, probably because the gastrocnemius and soleus muscles were not directly stimulated during the cycling exercise. It demonstrated that an FES training program involving the contrac-tion of the limb muscle with paresis in people with SCI may help not only to decrease muscle atrophy, but increase muscle size as well. Our subjects showed increases in the girth of bilateral thighs, which was compatible with the results that muscle hypertrophy and increase in the number of muscle fibers per motor unit were the reasons for strength gain after the FES cycling exercise [35]. Nevertheless, subjects did not show further increase in muscle mass after 8 weeks of training, probably because the workload was not incrementally increased during the study period.
In general, as the motor and sensory recovery essen-tially reach a plateau at the end of 1 year, it is logical to base the initial rehabilitation plans on a predicted 1-year recovery period [36]. It is interesting to note that there were substantial increases in the measured strength of the bilateral knee extensors and knee flex-ors in these SCI patients, whose average postinjury
time is about 3.2 years, after 8 weeks of FESCE. The result revealed that exercise by using the FES cycling system can improve muscle strength in patients with SCI postinjury for more than 1 year.
It is well known that the best prognosis is in patients who initially exhibit some spared motor func-tion and in those in whom neurologic recovery occurs early after injury [37]. The effect of FESCE has never been compared and discussed in relation to different degrees of incomplete SCI in previous studies. With regard to the effect of 8 weeks of FESCE on the sever-ity of injury, we found that the average strength increased from 1.6% to 4.3% in ASIA B group, 6.3% to 15.9% in ASIA C group, and 11.2% to 25.6% in ASIA D group in our study. The more residual muscle strength there was, the more percentage of strength was regained. It has been reported that age is an important factor in motor recovery and older patients show less functional motor recovery than younger patients [38]. In our study, each group was controlled by the mean age of SCI patients as far as possible in order to diminish the effect of age on recovery. The findings of our study demonstrated that the initial muscle strength of legs might be an effective predictor of muscle strength recovery after FES cycling training. Besides, FESCE could also provide an effective tran-sitional training for SCI patients in muscle torque increase before the operating electronic device usage at a later stage. There are still some limitations to our study: the permanent effect of FESCE and the other training parameter control such as duration and fre-quency of FESCE etc, which need further study for more efficiency and convenience for SCI patients. Moreover, in spite of various dietary needs of patients, the subjects’ diet intake should be controlled properly in order to avoid the influence on body weight and BMI during the study period.
In conclusion, FES-induced cycling training pro-gram resulted in significant increase in thigh muscle mass after a 4-week period and muscle peak torque after 8 weeks of training. Besides, subjects with less muscle power loss have a correspondingly better muscle strength recovery.
A
CKNOWLEDGMENTSThe authors thank Dr Shih-Hung Chuang for his assis-tance with data collection and Mr Richard A. J. Hudson
for his assistance with editing. Besides that, they also thank the financial department of the National Science Council, Taiwan, for this research under the contract numbers NSC-89-2614-E-038-001, NSC-90-2614-E-038-001, and NSC-94-2314-B-037-006.
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EFERENCES1. Patric LJ, Mark SN. Exercise recommendations for individuals with spinal cord injury. Sports Med 2004; 34:727–51.
2. Cheng D, Crozier KS, Zorn G. Spinal cord injury: prog-nosis for ambulation based on recovery of quadriceps function. J Am Paraplegia Soc 1991;14:94–8.
3. Zorn GW, Crozier KS, Cheng LL. Quadriceps recovery in Frankel C spinal cord injury. J Am Paraplegia Soc 1991;14:90–3.
4. Washburn RA, Figoni SF. Physical activity and chronic cardiovascular disease prevention in spinal cord injury: a comprehensive literature review. Top Spinal Cord Injury
Rehabil 1998;3:16–32.
5. Bernard PL, Mercier J, Varray A. Influence of lesion level on the cardioventilatory adaptations in paraplegic wheelchair athletes during muscular exercise. Spinal
Cord 2000;38:16–25.
6. Stiens SA, Johnson MC II, Lyman PJ. Cardiac rehabili-tation in patients with spinal cord injuries. Phys Med
Rehabil Clin North Am 1995;6:263–96.
7. Spungen AM, Wang J, Pierson RN, et al. Soft tissue body composition differences in monozygotic twins discor-dant for spinal cord injury. J Appl Physiol 2000;88:1310–5. 8. Maggioni M, Bertoli S, Margonato V, et al. Body com-position assessment in spinal cord injury subjects. Acta
Diabetol 2003;40(Suppl 1):183–6.
9. Spungen AM, Adkins RH, Stewart CA, et al. Factors influencing body composition in persons with spinal cord injury: a cross-sectional study. J Appl Physiol 2003; 95:2398–407.
10. Mohr T, Dela F, Handberg A, et al. Insulin action and long-term electrically induced training in individuals with spinal cord injuries. Med Sci Sports Exerc 2001; 33:1247–52.
11. Phillips WT, Kiratli BJ, Sarkarati M, et al. Effect of spinal cord injury on the heart and cardiovascular fit-ness. Curr Probl Cardiol 1998;23:641–716.
12. Glaser RM, Janssen TWJ, Suryaprasad AG, et al. The physiology of exercise. In: Apple DF, ed. Physical
Fitness: A Guide for Individuals with Spinal Cord Injury.
Washington DC: Department of Veterans Affairs, 1997: 1–23.
13. Ragnarsson KT. Health maintenance and reduction of disability through physical exercise. In: Apple DF, ed. Physical Fitness: A Guide for Individuals with Spinal
Cord Injury. Washington DC: Department of Veterans
14. Baldi JC, Jackson RD, Moraille Rich, et al. Muscle atrophy is prevented in patients with acute spinal cord injury using functional electrical stimulation. Spinal Cord 1998; 36:463–9.
15. Willoughby DS, Priest JW, Nelson M. Expression of the stress proteins, ubiquitin, heat shock protein 72, and myofibrillar protein content after 12 weeks of leg cycling in persons with spinal cord injury. Arch Phys
Med Rehabil 2002;83:649–54.
16. Erika AM, Kurta L, Gentili A, et al. Increasing muscle mass in spinal cord injured persons with a functional electrical stimulation exercise program. Arch Phys Med
Rehabil 1999;80:1531–6.
17. Timson BF. Evaluation of animal models for the study of exercise-induced muscle enlargement. J Appl Physiol 1998;69:1935–45.
18. American Spinal Injury Association. International
Stan-dards for Neurological Classification of Spinal Cord Injury,
revised 2002. Chicago, IL: American Spinal Injury Association, 2002.
19. Desport JC, Preux PM, Guinvarch S, et al. Total body water and percentage fat mass measurements using bioelectrical impedance analysis and anthropometry in spinal cord-injured patients. Clin Nutr 2000;19: 185–90.
20. Sartorio A, Malavolti M, Agosti F, et al. Body water dis-tribution in severe obesity and its assessment from eight-polar bioelectrical impedance analysis. Eur J Clin
Nutr 2005;59:155–60.
21. Arnold PB, McVey PP, Farrell WJ, et al. Grasso AR. Functional electric stimulation: its efficiency and safety in improving pulmonary function and musculoskeletal fitness. Arch Phys Med Rehabil 1992;73:665–8.
22. Willoughby DS, Priest JW, Jennings RA. Myosin heavy chain isoform and ubiquitin protease mRNA expression after passive leg cycling in persons with spinal cord injury. Arch Phys Med Rehabil 2000;81: 157–63.
23. Johnston TE, Smith BT, Betz RR. Strengthening of par-tially denervated knee extensors using percutaneous electric stimulation in a young man with spinal cord injury. Arch Phys Med Rehabil 2005;86:1037–42.
24. Huang MH, Lin YS, Yang RC, et al. A comparison of various therapeutic exercises on the functional status of patients with knee osteoarthritis. Semin Arthritis Rheum 2003;32:398–406.
25. Gerrits HL, de Haan A, Sargeant AJ, et al. Altered con-tractile properties of the quadriceps muscle in people with spinal cord injury following functional electrical stimulated cycle training. Spinal Cord 2000;38:214–23. 26. Gerrits HL, Dehaan A, Hopman MTE, et al. Contractile
properties of the quadriceps muscle in individuals with spinal cord injury. Muscle Nerve 1999;22:1249–56. 27. Belanger M, Stein RB, Wheeler GD, et al. Electrical
stimulation: can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch
Phys Med Rehabil 2000;81:1090–8.
28. BeDell KK, Scremin AM, Perell KL, et al. Effects of functional electrical stimulation-induced lower extremity cycling on bone density of spinal cord-injured patients.
Am J Phys Med Rehabil 1996;75:29–34.
29. Chen K, Chen SC, Tsai KH, et al. An improved design of home cycling system via functional electrical stimu-lation for paraplegics. J Indus Ergon 2004;34:223–35. 30. Maggioni M, Bertoli S, Margonato V, et al. Body
com-position assessment in spinal cord injury subjects. Acta
Diabetol 2003;40:183–6.
31. Bauman WA, Spungen AM, Adkins RH, et al. Metabolic and endocrine changes in persons aging with SCI.
Assist Technol 1999;11:88–96.
32. Hjeltnes N, Aksnes AK, Birkeland KI, et al. Improved body composition after 8 wk of electrically stimulated leg cycling in tetraplegic patients. Am J Physiol 1997; 273:1072–9.
33. Castro MJ, Apple JD, Hillegass EA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Physiol
Occup Physiol 1999;80:373–8.
34. Dudley GA, Gastro MJ, Rogers S. A simple means of increasing muscle size after spinal cord injury: a pilot study. Eur J Appl Physiol Occup Physiol 1999;80:394–6. 35. Mange KC, Marino RJ, Gregory PC. The course of motor
recovery at the zone of injury in complete spinal cord injury. Arch Phys Med Rehabil 1992;73:437–40.
36. Water RL, Adkins RH, Yakura JS. Motor and sensory recovery following complete tetraplegia. Arch Phys Med
Rehabil 1993;74:242–7.
37. Folman Y, Masri WE. Spinal cord injury: prognostic indicators. Injury 1989;20:92–5.
38. Welsh L, Rutherford OM. Effects of isometric strength training on quadriceps muscle properties in over 55 year olds. Eur J Appl Physiol 1996;72:219–23.
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