Skip to main content
The Journal of Spinal Cord Medicine logoLink to The Journal of Spinal Cord Medicine
. 2018 Jan 15;42(3):272–280. doi: 10.1080/10790268.2017.1412562

Arm crank ergometry improves cardiovascular disease risk factors and community mobility independent of body composition in high motor complete spinal cord injury

James J Bresnahan 1,2,, Gary J Farkas 2, Jody L Clasey 3,4, James W Yates 3,4, David R Gater 2
PMCID: PMC6522950  PMID: 29334345

Abstract

Objective: Evaluate the effect of aerobic exercise using arm crank ergometry (ACE) in high motor complete (ISNCSCI A/B) spinal cord injury (SCI) as primarily related to cardiovascular disease (CVD) risk factors and functional mobility and secondarily to body composition and metabolic profiles.

Design: Longitudinal interventional study at an academic medical center.

Methods: Ten previously untrained participants (M8/F2, Age 36.7 y ± 10.1, BMI 24.5 ± 6.0) with high motor complete SCI (C7-T5) underwent ACE exercise training 30 minutes/day × 3 days/week for 10 weeks at 70% VO2Peak.

Outcome Measures: Primary outcome measures were pre- and post-intervention changes in markers of cardiovascular fitness (graded exercise testing (GXT): VO2, VO2Peak, respiratory quotient [RQ], GXT time, peak power, and energy expenditure [EE]) and community mobility (time to traverse a 100ft-5° ramp, and 12-minute WC propulsion test). Secondary outcome measures were changes in body composition and metabolic profiles (fasting and area under the curve for glucose and insulin, homeostasis model assessment [HOMA] for %β-cell activity [%β], %insulin sensitivity [%S], and insulin resistance [IR], and Matsuda Index [ISIMatsuda]).

Results: Resting VO2, relative VO2Peak, absolute VO2Peak, peak power, RQ, 12-minute WC propulsion, fasting insulin, fasting G:I ratio, HOMA-%S, and HOMA-IR all significantly improved following intervention (P < 0.05). There were no changes in body composition (P>0.05).

Conclusions: Ten weeks of ACE at 70% VO2Peak in high motor complete SCI improves aerobic capacity, community mobility, and metabolic profiles independent of changes in body composition.

Introduction

Respiratory and renal conditions have historically been the most prevalent cause of morbidity and mortality in the spinal cord injury (SCI) population.1 However, with improvements in medicine and our understanding in secondary complications that result from SCI, life expectancy has been on the rise and age-related comorbidities have become a greater determinant of survival. In fact, recent studies suggest that cardiovascular disease (CVD) is at greater prevalence in chronic SCI than the able-bodied (AB) population and is a leading cause of mortality in this population.1–3

Obesity is a well-recognized CVD risk factor and is more likely to occur in SCI because of the relative loss of metabolically active lean body mass (LBM), subsequent increase in body fat mass (FM), as well as blunting of the sympathetic nervous system.4,5 These changes lead to greater percent fat mass (%FM) in sedentary SCI men and women when compared to physically active age and gender matched individuals with SCI, as well as AB controls.2,6–9 Excess body fat has been shown to mediate metabolic syndrome via abnormal lipid and glucose profiles, cardiovascular inflammation, insulin resistance, hypertension, and thromboemboli.9–12 Metabolic syndrome is widespread in the SCI population.13–16 These risk factors have become targets of therapeutic interventions, such as exercise.17

The American College of Sports Medicine (ACSM) recommends 150 minutes of exercise per week to improve CVD risk factors.18 SCI Action Canada recommends 40 minutes/week of moderate-to-vigorous aerobic physical activity, while the American Congress of Rehabilitation Medicine (ACRM) recommends ≥ 40–60 minutes/week of moderate-to-vigorous aerobic activity.19,20 Both organizations call for more comprehensive exercise research in the SCI population.

Exercise limitations within the SCI population are numerous,21 but an inexpensive and widely used exercise modality for this population is arm crank ergometry (ACE). A quantifiable measure of cardiovascular health and maximal cardiorespiratory work is peak oxygen consumption (VO2Peak) which has previously been demonstrated as markedly reduced in SCI compared to the AB population.22 VO2Peak declines with age due to changes in body composition and cardiovascular health in the AB population.23

Only 25% of relatively young patients with SCI demonstrate aerobic capacity that is sufficient to meet the demands of independent mobility and living (> 15 ml/kg/min).24 Moreover, in SCI above T6, VO2Peak is inversely related to the level of injury (LOI) as a result of the limited volume of working abdominal musculature, ventilatory musculature, and circulatory dyskinesis.25–27 Previous research has demonstrated that exercise in the SCI population can improve aerobic capacity.25,27–31

ACE has occasionally shown the ability to augment some measures of metabolic profiles,32–35 however, these findings are inconsistent.33,36,37 Upper body exercise appears to improve hepatic insulin sensitivity but the effect on peripheral insulin sensitivity is poorly understood.38–40 The intensity, frequency, and duration of ACE needed to alter metabolic profiles is in need of further research.

Previous research on exercise in the SCI population has often failed to adequately control for completeness and level of injury. To our knowledge, no previous investigations have studied a range of CVD risk factors (GXT, two measures of community mobility, total and regional body composition, lipid profiles, and OGTT with measures of hepatic and peripheral insulin sensitivities) this extensively in high-motor complete injuries. In this study, we aimed to (1) evaluate the effects of ACE in high motor complete SCI as related to markers of aerobic fitness and community mobility and (2) examine effects of such exercise intervention on body composition and metabolic profiles. We hypothesized that following the ACE exercise intervention, markers of aerobic fitness, community mobility, body composition, and metabolic profiles would significantly improve.

Methods

Study design

Participants were recruited from the host institution to undergo aerobic exercise training and evaluation of CVD risk factors, which included aerobic capacity, community mobility, body composition, and serum metabolic profile markers for a longitudinal interventional study. All participants underwent complete physical examination by a physiatrist and 12-lead electrocardiogram prior to participation. Participants who met the inclusion criteria were defined as men and women, 18–55 years old with a C7-T4 motor complete SCI (ISNCSCI A or B) for greater than 6 months. Exclusion criteria included those individuals in an exercise program within the past 3 months; had known CVD, diabetes mellitus (type one or type two), hypothyroidism, and/or renal disease; uncontrolled autonomic dysreflexia; recent venous thromboembolism; pressure injury > grade II; or heterotopic ossification involving the upper extremities. This study was approved by the Intuitional Review Board at the host institution and all participants completed informed consent prior to the start of the study.

Exercise intervention

Qualified participants underwent ACE exercise training with a Monark Rehab Trainer 881E ACE (Patterson Medical, Warrenville,IL) for 30 minutes/day×3 days/week for 10 weeks at 70% VO2Peak. 90-minutes per week was chosen to more closely mimic the ACSM exercise guidelines for AB individuals while taking into account the significant sympathetic and cardiopulmonary disadvantages.18 In AB individuals, HR is a reliable indicator of oxygen uptake, however, in SCI individuals, this relationship does not hold true secondary to sympathetic blunting.22 Training intensity was assigned in the current study on the basis of the peak power output and rate of perceived exertion (RPE) at 70% VO2peak. VO2Peak & peak power were re-assessed at the end of week 5 to allow any necessary adjustments in absolute exercise intensity to maintain relative intensity at the appropriate level. Exercise sessions occurred at the exercise physiology laboratory at the host institution. Each exercise training session had a 5-minute warm-up consisting of 5 watts ACE performed at 50 RPM and a similar 5-minute cool-down period. Participants initially began exercising for shorter bouts with brief rest periods, allowing for the accumulation of total duration of 30 minutes of exercise. During the first week exercise sessions consisted of three 10-minute exercise bouts, while in the second week, exercise sessions consisted of two 15-minute bouts with a 5-minute rest period. From weeks 4–10 participants trained 30 minutes consecutively without rest at their designated intensity level. HR, BP, and RPE were monitored in each patient throughout every session. All subjects met physiological criteria for VO2Peak during Pre- and Post-testing, including Peak HR with drop in SBP, Respiratory Exchange Ratio > 1.1 and Borg Rate of Perceived Exertion (RPE) > 19. Transportation was arranged for subjects. It was predetermined that subjects would be removed from participation if they missed more than six of the thirty sessions due to the aims of the current study.

Graded exercise testing

Participants underwent a maximal graded exercise test (GXT) with a Physio-Dyne Max-1® (AEI Technologies, Naperville, IL) metabolic measurement system. To determine resting oxygen consumption (VO2), resting respiratory quotient (RQ; defined as the ratio of carbon dioxide production to oxygen consumption), and energy expenditure (EE) subjects were tested in a supine position and abided by the best practice guidelines for measurement of resting metabolic rates.41 VO2Peak, GXT time, and peak power (POpeak) were recorded with a standard ACE protocol one week before and within 4–7 days after the training intervention. Blood pressure was monitored throughout and heart rate was monitored via a lead II electrocardiogram (Quinton Q710 ECG system, Milwaukee, WI). Initial resistance of 5 watts was applied with metronome guided crank rate of 50 RPM. A warm-up stage of 2 minutes was used at this work rate, with subsequent 60-second stages of 5-watt increments employed until exhaustion. Respiratory exchange ratio, heart rate (HR), blood pressure (BP), and RPE was monitored during GXT. All participants were tested in their own stabilized wheelchair with appropriate seating, truncal stability, leg wraps, abdominal binder, and protective hand mitts that were secured to the ACE pedals.

Community mobility

Community mobility was assessed before and after the 10-week intervention with a 12-minute propelled distance performed on a 290-meter rubberized, level, indoor track as described and validated by Franklin et al.,42 as well as timed ascent up a 100-foot 5° ramp. Testing was performed in a lightweight wheelchair (Quickie, Southwest Medical, Phoenix, Arizona) adjusted to the participants’ height, arm length, and girth. All tests were timed and closely supervised by an exercise physiologist.

Body composition analysis and metabolic profiles

Body composition analysis was performed by measurement of total and regional values for the following variables: bone mineral content (BMC), bone mineral density (BMD), percent fat mass (%FM), fat mass (FM), and lean body mass (LBM) as determined by Dual Energy X-ray Absorptiometry (DXA; Lunar DPX-L, Lunar Corporation, Madison, Wisconsin) before and after the 10-week intervention. Every effort was taken to mimic the original participants’ position on the scanner at both evaluation time points. Scans were performed after lying flat for at least 20 minutes to minimize fluid shift. All scans were performed and analyzed by a certified DXA operator using Lunar software.

After a 12-hour fast, an indwelling Teflon catheter (DuPont, Wilmington, Delaware) was placed in an antecubital vein of one arm to collect 4-ml blood sample that was used to collect total cholesterol (TC), high-density lipoprotein-cholesterol (HDL-C), low-density lipoprotein-cholesterol (LDL-C), and triglycerides (TG).

A standard 75-g oral glucose tolerance test (OGTT) was administered between the hours 0700 and 1000 according to previously published methods.43 Briefly, 3 mL blood samples were taken at rest and at 0, 30, 60, 90, 120, and 180 minutes after the ingestion of 100 g glucose in a 10-ounce solution to evaluate the responses of glucose, plasma insulin, and the glucose:insulin (G:I) ratio. All blood collected during the study was immediately placed on ice, transferred to a chemistry pathology laboratory, centrifuged, aliquoted, and analyzed in accordance with CDC and standard practice guidelines.

The serum concentrations of glucose, triglycerides, cholesterol, LDL-C, and HDL-C were determined using colorimetric assays at the host institution (General Clinical Research Center [GCRC] Core Laboratory, Lexington, KY), while plasma insulin concentration was measured using a radioimmunoassay kit (GCRC core laboratory, Lexington, KY). The glucose and insulin area under the curve (AUC) was computed via the trapezoidal rule.43

The Homeostatic Model Assessment (HOMA) of insulin resistance (IR), percent β-Cell function (%β), percent fasting insulin sensitivity (%S), and the Matsuda Insulin Sensitivity (ISIMatsuda) were calculated.44,45 All carbohydrate and lipid measurements were performed one week before and 4-to-7 days after the 10-week intervention.

Statistical analysis

Normality was assessed with Shapiro-Wilks test. Wilcoxon signed rank tests were used to evaluate the effectiveness of exercise on GXT, body composition, community mobility, and metabolic biomarkers before and after the 10-week intervention. Level of significance was set at P < 0.05 and all analyses were performed with IBM SPSS Statistics 24 (PASW, SPSS Inc., IBM, Armonk, New York).

Results

Participant demographics

Ten patients (M8/F2; Age: 36.7 ± 12.5 years; BMI: 24.5 ± 6.0 kg/m2) were included in the study. Thirty percent of the patients were classified as cervical injuries, while 70% were classified as high thoracic injuries. Eight patients were classified as ISNCSCI A and two were ISNCSCI B. Four participants dropped out of the study due to non-compliance. Specifically, these subjects had issues associated with work, family and community responsibilities, and social activities that took precedent over attending exercise sessions. Table 1 presents participant demographic data.

Table 1. Participant demographics.

            Weight (kg) BMI (kg/m2)
Age Sex LOI ISNCSCI TSI (years) Height (cm) Pre Post Pre Post
30 M T2 A 30 168.0 100.5 NF 35.6 NF
52 F T4 A 34 155.9 64.0 61.00 26.6 25.4
51 M T1 A 32 188.0 66.0 68.30 18.7 19.3
22 M T4 A 1 175.0 68.5 NF 22.3 NF
38 M C7 A 0.6 185.0 109.5 112.50 32.0 32.7
26 M T5 A 1 180.0 63.4 60.90 19.6 18.8
23 F C7 B 5 168.0 50.0 50.00 17.7 17.7
36 M C7 B 4 178.0 90.0 91.00 28.4 28.7
55 M T2 A 15 180.3 67.3 NF 20.7 NF
26 M T4 A 1.5 201.0 95.3 NF 23.6 NF
Mean
36.7 NA NA NA 12.4 178.1 77.5 74.0 24.5 23.8

LOI, level of injury; ISNCSCI, international standard of neurological classification for spinal cord injury; TSI, time since injury; NF, no follow-up.

Graded exercise test

Post-intervention resting VO2 (172.5 ± 50.0 vs. 195.3 ± 44.6 mL/min, P = 0.046), resting respiratory quotient (0.96 ± 0.15 vs. 0.77 ± 0.02, P = 0.028), absolute VO2peak (784.2 ± 279.6 vs. 918.5 ± 310.0 mL/min, P = 0.028), relative VO2peak (10.8 ± 3.6 vs. 12.8 ± 4.0 mL/kg/min, P = 0.027), and peak power (40 ± 16 vs. 54 ± 17 W, P = 0.026) significantly improved when compared to their baseline data. All other parameters did not change and are shown in Table 2.

Table 2. Graded exercise testing before and after intervention.

  Pre-intervention Post-intervention P-value
Resting VO2 (ml/min) 172.5 ± 50.0 195.3 ± 44.6 0.046
VO2peak (ml/min)a 784.2 ± 279.6 918.5 ± 310.0 0.028
VO2peak (ml/kg/min)b 10.8 ± 3.6 12.8 ± 4.0 0.027
Peak Power (W) 40 ± 16 54 ± 17 0.026
GXT Time (min)c 23.2 ± 7.8 24.0 ± 4.7 0.920
Peak Heart Rate (BPM) 147.8 ± 23.2 151.2 ± 24.2 0.750
Resting Respiratory Quotient 0.96 ± 0.15 0.77 ± 0.02 0.028
Energy Expenditure (kcal/day) 1206.67 ± 336.19 1310.00 ± 301.13 0.075

aAbsolute peak oxygen consumption; brelative peak oxygen consumption; cgraded exercise test.

Community mobility

The 12-minute wheelchair propulsion (2062 ± 1167 vs. 2398 ± 1260 feet, P = 0.028; Table 3) significantly increased following the exercise intervention. There was no significant difference between pre and post-intervention measurement of time to traverse a 100-foot 5° ramp (18.8 ± 7.8 vs. 18.2 ± 10.3 sec, P = 0.463; Table 3).

Table 3. Community mobility before and after intervention.

  n Pre-intervention Post-intervention P-value
12-minute Propulsion (feet) 6 2062 ± 1167 2398 ± 1260 0.028
100 feet-5° Incline (seconds) 6 18.8 ± 7.8 18.2 ± 10.3 0.463

WC, wheelchair.

Body composition and metabolic profiles

There was no significant difference in body composition following the exercise intervention (P > 0.05; Table 4.) Post-intervention fasting insulin (12.23 ± 5.58 vs. 7.65 ± 2.34 μU/ml, P = 0.028), fasting G:I ratio (9.77 ± 4.49 vs. 13.69 ± 3.29, P = 0.028), HOMA-%S (73.3 ± 31.6 vs. 105.6 ± 27.1; P = 0.046) and HOMA-IR (1.6 ± 0.7 vs. 1.0 ± 0.3; P = 0.046) significantly improved from baseline, while HOMA-%β, Glucose AUC, Insulin AUC, and ISIMatsuda did not significantly differ following the exercise intervention (P > 0.05). TG profiles improved, but did not reach significance following the intervention (P > 0.05). Metabolic profile measurements are presented in Table 5.

Table 4. Body composition.

    Pre-intervention Post-intervention P-value
Arms FM (g) 1509 ± 1026 1520 ± 756 0.600
LBM (kg) 4.12 ± 1.50 4.33 ± 1.64 0.917
%FM 26.85 ± 15.54 26.37 ± 14.00 0.600
BMC (g) 300 ± 115 345 ± 126 0.249
BMD (g/cm2) 1.02 ± 0.16 1.04 ± 0.17 0.345
Legs FM (g) 8336 ± 3696 8273 ± 3916 0.345
LBM (kg) 12.35 ± 33.51 12.47 ± 38.74 0.917
%FM 39.45 ± 9.36 38.93 ± 8.44 0.225
BMC (g) 717 ± 467 698 ± 393 0.600
BMD (g/cm2) 0.96 ± 0.34 0.96 ± 0.32 0.753
Trunk FM (g) 13, 671 ± 7521 13, 574 ± 7108 0.917
LBM (kg) 25.20 ± 63.43 25.18 ± 67.91 0.600
%FM 33.23 ± 10.68 31.95 ± 8.99 0.753
BMC (g) 1063 ± 331 1064 ± 324 0.753
BMD (g/cm2) 0.96 ± 0.09 0.96 ± 0.09 1.000
Total Body FM (g) 25, 059 ± 11, 891 24, 810 ± 11, 826 0.753
LBM (kg) 44.31 ± 10.26 44.83 ± 11.41 0.753
%FM 34.91 ± 34.91 34.46 ± 34.46 0.345
BMC (g) 2635 ± 869 2661 ± 879 0.463
BMD (g/cm2) 1.13 ± 0.15 1.12 ± 0.15 0.752

%FM, % fat mass; BMC, bone mineral content; BMD, bone mineral density; FM, fat mass; LBM, lean body mass.

Table 5. Metabolic profiles before and after intervention.

  Pre-intervention Post-intervention P-value
Total cholesterol (mg/dl) 174.00 ± 22.69 175.50 ± 16.50 0.750
HDL-C (mg/dl) 36.33 ± 6.31 34.83 ± 7.31 0.066
% HDL-C 21.33 ± 4.03 19.83 ± 4.17 0.074
LDL-C (mg/dl) 104.83 ± 14.93 116.83 ± 17.98 0.116
TG (mg/dl) 164.50 ± 132.05 120.00 ± 57.85 0.600
OGTT
Fasting glucose (mg/dl) 99.83 ± 14.80 99.00 ± 10.43 0.917
Fasting Insulin (μU/ml) 12.23 ± 5.58 7.65 ± 2.34 0.028
Fasting G:I 9.77 ± 4.49 13.69 ± 3.29 0.028
Glucose AUC 914.67 ± 236.60 968.58 ± 236.60 0.249
Insulin AUC 440.88 ± 212.88 464.76 ± 152.95 0.917
HOMA and ISIMatsuda
HOMA-%β 111.4 ± 48.7 82.4 ± 19.1 0.116
HOMA-%S 73.3 ± 31.6 105.6 ± 27.1 0.046
HOMA-IR 1.6 ± 0.7 1.0 ± 0.3 0.046
ISIMatsuda 3.4 ± 1.6 3.6 ± 0.8 0.345

% β: %Beta cell activity; %S: %insulin sensitivity; AUC: area under the curve; HDL-C, high-density lipoprotein-cholesterol; HOMA: homeostasis modeal assessment; ISI: Insulin sensitivity index; LDL-C, low-density lipoprotein-cholesterol; TG, triglycerides; Fasting G:I, fasting glucose to insulin ratio.

Discussion

This study focused on evaluating the effects of ten weeks of ACE on cardiovascular disease risk factors and community mobility. The main findings from this study suggest ten weeks of ACE significantly improve markers of aerobic fitness, 12-minute wheelchair propulsion, and some metabolic markers of cardiovascular fitness. All results were independent of significant changes in body composition.

Peak oxygen consumption and power output are considered reliable indexes of cardiorespiratory health and ACE is the most established and widely validated upper extremity exercise test.30,46–48 Peak oxygen consumption is markedly reduced in SCI compared to the AB population.22,49 Our study and previous research has shown ACE provides reliable changes in aerobic fitness in the SCI population.25,36,50 El-Sayed et al. showed 12 weeks of ACE at 60–65% VO2peak in chronic SCI improves aerobic fitness but did not control for completeness or level of injury.32 Similarly, Sutbeyaz et al.51 showed 6 weeks of ACE at 75% VO2peak in chronic SCI improves aerobic fitness in subjects with T6–12 injuries. de Groot et al.35 demonstrated 8 weeks of high intensity ACE showed more dramatic changes in VO2peak than low intensity ACE, and DiCarlo52 showed that 8 weeks of ACE in cervical SCI subjects improved VO2peak. However, none of these studies controlled for completeness of injury. Despite an overall lack of homogeneity, systematic reviews agree that ACE improves aerobic fitness.53–56

It is well established in SCI literature that a level-dependent impairment of the respiratory system exists. More cranial injuries display worse functional outcomes in numerous pulmonary measures.57–59 This level dependent impairment is due to obstructive and restrictive lung disease caused by denervation of the pulmonary musculature, denervation of stabilizing abdominal musculature, and sympathetic blunting.60 Motor-incomplete individuals (ISNCSCI C or D) have some pulmonary and skeletal muscle function below the LOI, while those individuals with a motor-complete injury (ISNCSCI A or B) do not. Individuals with incomplete injuries and/or lower LOI, may have disproportionate increases in cardiorespiratory function and therefore skew the outcomes of studies. The current study controls for completeness by only including motor complete injuries and controls for LOI by only including individuals of the same functional level, C7-T5, a level that is higher than what is needed to approach pulmonary function in the able bodied individual (T6–8).57 The current study showed a 13% and 19% increase in resting VO2 and relative VO2peak, respectively, demonstrating the subjects increased ability to uptake, transport, and utilized oxygen after 10 weeks of training at 70% VO2peak. It currently remains unclear whether the improvements in aerobic fitness stem from (1) physiological adaptions in heart rate, stroke volume, and/or cardiac output, (2) improvements in a-VO2 differences (oxygen extraction in the peripheral tissues), or (3) neurological adaptions in the brain and/or cord. However, a combination of these factors is more likely.61

The physical strain of performing activities of daily living (ADLs) and community mobility is related to level of injury and physical capacity.24,25,49,62,63 Individuals with a higher physical capacity (higher VO2peak) are better able to perform ADLs, navigate the community, and have fewer medical complications.24,25,49,62–64 The 12-minute wheelchair propulsion test is a reliable and cheap measure of community mobility.42 DiCarlo showed 8 weeks of ACE improved 12 minute wheelchair propulsion from 1.18 to 2.1km on average in a cohort of eight subjects with cervical SCIs, but included congenital lesions and did not control for completeness.52 The current study noted an average increase in propulsion of 336 feet, or 14%, a significant improvement that further validates the use of ACE to improve community mobility.

Sedentary individuals with SCI have poor metabolic profiles compared to the AB population,2 while active individuals with SCI have more favorable profiles.65,66 HOMA is a tool used to analyze fasting glucose and insulin levels. %β and %S are inversely related. HOMA-IR is the ratio of %β to %S. The average person in a population is represented by %β and %S of 100%, with an IR of 1.0. HOMA-IR highly correlates to insulin resistance measured by more invasive methods such as hyperinsulinemic-euglycemic clamp and intravenous glucose tolerance test.67 The HOMA-IR cut-off value consistent with 66th percentile of insulin resistance in the AB population is HOMA-IR > 2.73.68 HOMA measures are suggestive of fasting hepatic insulin sensitivity,69–71 while Matsuda Index is a measure of whole body peripheral insulin sensitivity adaptations.72 The current study found significant changes in post-intervention HOMA-%S (73.% to 105.6%) and HOMA-IR (1.6 to 1.0), which are consistent with previous research examining the effect of upper body exercise on hepatic insulin sensitivity.38,39,73

Approximately 70% of glucose intolerance post-SCI is due to intramuscular fat (IMF) accumulation and skeletal atrophy of the thighs.74 One proposed mechanism to improve glucose tolerance is to decrease IMF by increasing LBM and decreasing FM.75 Functional electrical stimulation (FES) of the lower extremities has the potential to alter cardiometabolic profiles from a multifaceted approach; skeletal muscle hypertrophy, non-insulin dependent glucose uptake, peripheral insulin sensitivity, and alteration of total and regional body composition. Previous studies have shown FES can increase regional and total body LBM as well as alter glucose and insulin metabolism, although they have not consistently shown a decrease in IMF.36,76,77 ACE does not appear to activate enough muscle mass in the upper extremities to cause changes in body composition53,78 but improvement in metabolic profile has been reported without changes in body composition,33 and is supported by the findings of this study.

Extensive changes in FFM, such as those noted with FES-LCE, would be expected to cause a greater degree of change in metabolic profiles. The current study noted similar changes in metabolic profile to those with robust muscular hypertrophy of the thighs. FES-LCE does not reliably decrease FM,36,76,79,80 which may result from the lack of dietary control in study design. When diet is controlled for, lower extremity FES has been shown to increase LBM, decrease IMF, improve fasting insulin, glucose AUC, insulin AUC, and lipid profiles.81

Study limitations

This study is not without limitations. (1) This study is of small sample size with only six participants completing the entire study raising the possibility of a type 2 error. However, this sample size is consistent with exercise-based SCI research.36,37,43,81–84 (2) There is a lack of comparative control group. (3) ACE does not appear to cause body composition changes to the degree of FES-LCE, resistance training, or FES-rowing.33,36,81 However, FES equipment is more expensive than ACE, individuals have limited access to facilities with the equipment, transportation barriers, and environmental constraints limiting its use.85 SCI individuals appear to adhere to FES and ACE when they have the opportunity to do it in their home.40,85,86 (4) The diets of the enrolled participants were not controlled for. Lastly, (5) OGTT is not considered the gold standard in the assessment of carbohydrate metabolism, however the technique is less time consuming, less expensive, and is safer than the intravenous glucose tolerance test and hyperinsulinemic euglycemic clamp, especially for the SCI population.87,88

Conclusions

The findings suggest that ten weeks of 30minutes/day 3days/week ACE leads to an improvement in measures of cardiovascular fitness (resting VO2, absolute VO2peak, relative VO2peak, RQ, peak power), community mobility (12-minute WC propulsion), and metabolic profiles (fasting insulin, G:I ratio, HOMA-S, and HOMA-IR) independent of changes in body composition. This work emphasizes the importance of exercise as a means to reduce CVD risk factors and improve aerobic fitness and community mobility.

Disclaimer statements

Contributors None.

Ethics approval None.

Declaration of interest The authors report no declarations of interest.

Funding Statement

Supported by American Heart Association (9806232), National Center for Research Resources, National Institutes of Health (MO1RR02602), Veterans Affairs Rehabilitation Research and Development Service (B2247V), and National Institutes of Health (K23 RR16182).

ORCID

James J. Bresnahanhttp://orcid.org/0000-0002-9712-4629

Gary J. Farkashttp://orcid.org/0000-0002-5482-6049

References

  • 1.Hagen EM, Lie SA, Rekand T, Gilhus NE, Gronning M.. Mortality after traumatic spinal cord injury: 50 years of follow-up. J Neurol Neurosurg Psychiatry 2010;81(4):368–73. [DOI] [PubMed] [Google Scholar]
  • 2.Bauman WA, Spungen AM.. Coronary heart disease in individuals with spinal cord injury: assessment of risk factors. Spinal Cord 2008;46(7):466–76. [DOI] [PubMed] [Google Scholar]
  • 3.Myers J, Lee M, Kiratli J.. Cardiovascular disease in spinal cord injury: an overview of prevalence, risk, evaluation, and management. Am J Phys Med Rehabil 2007;86(2):142–52. [DOI] [PubMed] [Google Scholar]
  • 4.Mollinger LA, Spurr GB, el Ghatit AZ, Barboriak JJ, Rooney CB, Davidoff DD, et al. Daily energy expenditure and basal metabolic rates of patients with spinal cord injury. Arch Phys Med Rehabil 1985;66(7):420–6. [PubMed] [Google Scholar]
  • 5.Sedlock DA, Laventure SJ.. Body composition and resting energy expenditure in long term spinal cord injury. Paraplegia 1990;28(7):448–54. [DOI] [PubMed] [Google Scholar]
  • 6.Cardus D, McTaggard W.. Body Composition in Spinal Cord Injury. Arch Phys Med Rehabil 1985;66(4):257–9. [DOI] [PubMed] [Google Scholar]
  • 7.Olle MM, Pivarnik JM, Klish WJ, Morrow JR.. Body composition of sedentary and physically active spinal cord injured individuals estimated from total body electrical conductivity. Arch Phys Med Rehabil 1993;74(7):706–10. [DOI] [PubMed] [Google Scholar]
  • 8.Kocina P.Body composition of spinal cord injured adults. Sport Med 1997;23(1):48–60. [DOI] [PubMed] [Google Scholar]
  • 9.Gater DR, Farkas GJ.. Alterations in body composition after SCI and the mitigating role of exercise. In: Taylor JA, Morse L, editors. The Physiology of Exercise in Spinal Cord Injury. New York, NY: Springer Healthcare LLC; 2017. p. 175–99. [Google Scholar]
  • 10.Matsuzawa Y.White adipose tissue and cardiovascular disease. Best Pract Res Clin Endocrinol Metab 2005Dec;19(4):637–47. [DOI] [PubMed] [Google Scholar]
  • 11.Jung UJ, Choi M-S.. Obesity and Its Metabolic Complications: The Role of Adipokines and the Relationship between Obesity, Inflammation, Insulin Resistance, Dyslipidemia and Nonalcoholic Fatty Liver Disease. Int J Mol Sci 2014;15(4):6184–223. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 12.Farkas G, Gater D.. Neurogenic obesity and systemic inflammation following spinal cord injury: a review. J Spinal Cord Med 2017;1–10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 13.Manns PJ, McCubbin JA, Williams DP.. Fitness, inflammation, and the metabolic syndrome in men with paraplegia. Arch Phys Med Rehabil 2005;86(6):1176–81. [DOI] [PubMed] [Google Scholar]
  • 14.Maruyama Y, Mizuguchi M, Yaginuma T, Kusaka M, Yoshida H, Yokoyama K, et al. Serum leptin, abdominal obesity and the metabolic syndrome in individuals with chronic spinal cord injury. Spinal Cord 2008;46(7):494–9. [DOI] [PubMed] [Google Scholar]
  • 15.Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Castillo C, Gater DR.. Effects of spinal cord injury on body composition and metabolic profile - part I. J Spinal Cord Med 2014;37(6):693–702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Castillo C, Miller JM, Moore J, Gater DR.. Metabolic Syndrome in Veterans with Spinal Cord Injury. J Spinal Cord Med 2007;30:403. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Parikh RM, Mohan V.. Changing definitions of metabolic syndrome. Indian J Endocrinol Metab 2012;16(1):7–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA, et al. Physical activity and public health: Updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc 2007;39(8):1423–34. [DOI] [PubMed] [Google Scholar]
  • 19.Martin Ginis K, Hicks A, Latimer A, Warburton D, Bourne C, Ditor D, et al. The development of evidence-informed physical activity guidelines for adults with spinal cord injury. Spinal Cord 2011;49(11):1088–96. [DOI] [PubMed] [Google Scholar]
  • 20.Evans N, Wingo B, Sasso E, Hicks A, Gorgey AS, Harness EB.. Exercise Recommendations and Considerations for Persons With Spinal Cord Injury. Arch Phys Med Rehabil 2015;96(9):1749–50. [DOI] [PubMed] [Google Scholar]
  • 21.Gorgey AS.Exercise awareness and barriers after spinal cord injury. World J Orthop 2014;5(3):158–62. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.McLean KP, Jones PP, Skinner JS.. Exercise prescription for sitting and supine exercise in subjects with quadriplegia. Med Sci Sports Exerc 1995;27(1):15–21. [PubMed] [Google Scholar]
  • 23.Sergi G, Coin A, Sarti S, Perissinotto E, Peloso M, Mulone S, et al. Resting VO2, maximal VO2 and metabolic equivalents in free-living healthy elderly women. Clin Nutr 2010;29(1):84–8. [DOI] [PubMed] [Google Scholar]
  • 24.Jansen T, Van Oers C, Van Der Woude L, Hollander P.. Physical strain in daily life of wheelchair users with spinal cord injuries. Med Sci Sports Exerc 1994;26(6):661–70. [DOI] [PubMed] [Google Scholar]
  • 25.Gater D, Ugdale V.. Physiological foundations for exercise prescription in tetraplegia. In: Shankar K, editor. Exercise Prescription. Philadelphia, PA: Hanley& Belfus; 1999. p. 199–246. [Google Scholar]
  • 26.Burkett LN, Chisum J, Stone W, Fernhall B.. Exercise capacity of untrained spinal cord injured individuals and the relationship of peak oxygen uptake to level of injury. Paraplegia 1990;28(8):512–21. [DOI] [PubMed] [Google Scholar]
  • 27.Van Loan MD, McCluer S, Loftin JM, Boileau RA.. Comparison of physiological responses to maximal arm exercise among able-bodied, paraplegics and quadriplegics. Paraplegia 1987;25(5):397–405. [DOI] [PubMed] [Google Scholar]
  • 28.Machač S, Radvanský J, Kolář P, Kříž J.. Cardiovascular response to peak voluntary exercise in males with cervical spinal cord injury. J Spinal Cord Med 2016;39(4):412–20. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Lassau-Wray E, Ward G.. Varying physiological response to arm-crank exercise in specific spinal injuries. J Physiol Anthropol Appl Human Sci 2000;19(1):5–12. [DOI] [PubMed] [Google Scholar]
  • 30.McConnell TJ, Horvat MA, Beutel-Horvat TA, Golding LA.. Arm crank versus wheelchair treadmill ergometry to evaluate the performance of paraplegics. Paraplegia 1989;27(4):307–13. [DOI] [PubMed] [Google Scholar]
  • 31.Valent L, Dallmeijer A, Houdijk H, Talsma E, van der Woude L.. The effects of upper body exercise on the physical capacity of people with a spinal cord injury: a systematic review. Clin Rehabil 2007;21(4):315–30. [DOI] [PubMed] [Google Scholar]
  • 32.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(5):299–305. [DOI] [PubMed] [Google Scholar]
  • 33.Gorgey AS, Harnish CR, Daniels JA, Dolbow DR, Keeley A, Moore J, et al. A report of anticipated benefits of functional electrical stimulation after spinal cord injury. J Spinal Cord Med 2012;35(2):107–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Hooker S, Wells C.. Effects of low- and moderate-intensity training in spinal cord-injured persons. Med Sci Sports Exerc 1989;21(1):18–22. [DOI] [PubMed] [Google Scholar]
  • 35.de Groot P, Hjeltnes N, Heijboer A, Stal W, Birkeland K.. Effect of training intensity on physical capacity, lipid profile and insulin sensitivity in early rehabilitation of spinal cord injured individuals. Spinal Cord 2003;41(12):673–9. [DOI] [PubMed] [Google Scholar]
  • 36.Gorgey AS, Martin H, Metz A, Khalil RE, Gater DR.. Longitudinal changes in body composition and men with chronic spinal cord injury Longitudinal changes in body composition and metabolic profile between exercise clinical trials in men with chronic spinal cord injury. J Spinal Cord Med 2016;39(6):699–712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 37.Kjaer M, Pollack S, Mohr T, Weiss H, Gleim G, Bach F, et al. Regulation of glucose turnover and hormonal responses during electrical cycling in tetraplegic humans. Am J Physiol 1996;271(1):191–9. [DOI] [PubMed] [Google Scholar]
  • 38.Bakkum AJT, Paulson TAW, Bishop NC, Goosey-Tolfrey VL, Stolwijk-Swüste JM, Van Kuppevelt DJ, et al. Effects of hybrid cycle and handcycle exercise on cardiovascular disease risk factors in people with spinal cord injury: A randomized controlled trial. J Rehabil Med 2015;47(6):523–30. [DOI] [PubMed] [Google Scholar]
  • 39.Kim D-I, Lee H, Lee B-S, Kim J, Jeon JY, Bauman WA, et al. Effects of a 6-Week Indoor Hand-Bike Exercise Program on Health and Fitness Levels in People With Spinal Cord Injury: A Randomized Controlled Trial Study. Arch Phys Med Rehabil 2015;96(11):2033–40. [DOI] [PubMed] [Google Scholar]
  • 40.Nightingale TE, Walhin JP, Thompson D, Bilzon JLJ.. Impact of Exercise on Cardiometabolic Component Risks in Spinal Cord–injured Humans. Med Sci Sports Exerc 2017; doi: 10.1249/MSS.0000000000001390(July):epub ahead of print. [DOI] [PMC free article] [PubMed]
  • 41.Compher C, Frankenfield D, Keim N, Roth-Yousey L, Evidence Analysis Working Group Best Practice Methods to Apply to Measurement of Resting Metabolic Rate in Adults: A Systematic Review. J Am Diet Assoc 2006;106(6):881–903. [DOI] [PubMed] [Google Scholar]
  • 42.Franklin B, Swantek K, Grais S, Johnstone K, Gordon S, Timmis G.. Field test estimation of maximal oxygen consumption in wheelchair users. Arch Phys Med Rehabil 1990;71(8):574–8. [PubMed] [Google Scholar]
  • 43.Gorgey AS, Gater DR.. A Preliminary Report on the Effects of the Level of Spinal Cord Injury on the Association Between Central Adiposity and Metabolic Profile. PM&R 2011;3(5):440–6. [DOI] [PubMed] [Google Scholar]
  • 44.Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC.. Homeostasis model assessment: insulin resistance and B-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 1985;28(7):412–9. [DOI] [PubMed] [Google Scholar]
  • 45.Matsuda M, DeFronzo RA.. Insulin sensitivity indices obtained from oral glucose tolerance testing: comparison with the euglycemic glucose clamp. Diabetes Care 1999;22(9):1462–70. [DOI] [PubMed] [Google Scholar]
  • 46.Bar-Or O, Zwiren LD.. Maximal oxygen consumption test during arm exercise--reliability and validity. J Appl Physiol 1975;38(3):424–6. [DOI] [PubMed] [Google Scholar]
  • 47.Bobbert A.Physiologic comparison of 3 types of ergometer. J Appl Physiol 1960;15(6):1007–14. [Google Scholar]
  • 48.Drory Y, Ohry A, Brooks ME, Dolphin D, Kellermann JJ.. Arm crank ergometry in chronic spinal cord injured patients. Arch Phys Med Rehabil 1990;71(6):389–92. [PubMed] [Google Scholar]
  • 49.Collins EG, Gater D, Kiratli J, Butler J, Hanson K, Langbein WE.. Energy cost of physical activities in persons with spinal cord injury. Med Sci Sports Exerc 2010;42(4):691–700. [DOI] [PubMed] [Google Scholar]
  • 50.Hooker S, Greenwood J, Hatae D, Husson R, Matthiesen T, Waters A.. Oxygen uptake and heart rate relationship in persons with spinal cord injury. Med Sci Sports Exerc 1993;25(10):1115–9. [PubMed] [Google Scholar]
  • 51.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(3):273–6. [DOI] [PubMed] [Google Scholar]
  • 52.DiCarlo SE.Effect of arm ergometry training on wheelchair propulsion endurance of individuals with quadriplegia. Phys Ther 1988;68(1):40–4. [DOI] [PubMed] [Google Scholar]
  • 53.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 spinal cord injury: a systematic review. Spinal Cord 2011;49(11):1103–27. [DOI] [PubMed] [Google Scholar]
  • 54.Hoffman MD.Cardiorespiratory fitness and training in quadriplegics and paraplegics. Sport Med 1986;3(5):312–30. [DOI] [PubMed] [Google Scholar]
  • 55.Figoni SF.Perspectives on cardiovascular fitness and SCI. J Am Paraplegia Soc 1990;13(4):63–71. [DOI] [PubMed] [Google Scholar]
  • 56.Devillard X, Rimaud D, Roche F, Calmels P.. Effects of training programs for spinal cord injury. Ann Réadaptation Médecine Phys 2007;50(6):490–8. [DOI] [PubMed] [Google Scholar]
  • 57.West CR, Sheel AW, Romer LM.. Respiratory system responses to exercise in spinal cord injury. In: The Physiology of Exercise in Spinal Cord Injury2017. p. 51–75.
  • 58.Baydur A, Adkins RH, Milic-Emili J.. Lung mechanics in individuals with spinal cord injury: effects of injury level and posture. J Appl Physiol 2001;90(2):405–11. [DOI] [PubMed] [Google Scholar]
  • 59.Mueller G, de Groot S, van der Woude L, Hopman MTE.. Time-courses of lung function and respiratory muscle pressure generating capacity after spinal cord injury: a prospective cohort study. J Rehabil Med 2008;40(4):269–76. [DOI] [PubMed] [Google Scholar]
  • 60.Qiu S, Alzhab S, Picard G, Taylor JA.. Ventilation Limits Aerobic Capacity after Functional Electrical Stimulation Row Training in High Spinal Cord Injury Med Sci Sports Exerc. 2016;48(6):1111–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 61.Jacobs P, Nash M.. Exercise recommendations for individuals with spinal cord injury. Sport Med 2004;34(11):727–51. [DOI] [PubMed] [Google Scholar]
  • 62.Noreau L, Shephard RJ, Simard C, Paré G, Pomerleau P.. Relationship of impairment and functional ability to habitual activity and fitness following spinal cord injury. Int J Rehabil Res 1993;16(4):265–75. [DOI] [PubMed] [Google Scholar]
  • 63.Dallmeijer AJ, Hopman MT, van As HH, van der Woude LH.. Physical capacity and physical strain in persons with tetraplegia; the role of sport activity. Spinal Cord 1996;34(11):1173–6. [DOI] [PubMed] [Google Scholar]
  • 64.Hjeltnes N, Jansen T.. Physical endurance capacity, functional status and medical complications in spinal cord injured subjects with long-standing lesions. Paraplegia 1990;28(7):428–32. [DOI] [PubMed] [Google Scholar]
  • 65.Bostom A, Toner M, McArdle W, Montelion T, Brown C, Stein R.. Lipid and lipoprotein profiles relate to peak aerobic power in spinal cord injured men. Med Sci Sports Exerc 1991;23(4):409–14. [PubMed] [Google Scholar]
  • 66.Dallmeijer AJ, Hopman MTE, Van Der Woude LH V.. Lipid, lipoprotein, and apolipoprotein profiles in active and sedentary men with tetraplegia. Arch Phys Med Rehabil 1997;78(11):1173–6. [DOI] [PubMed] [Google Scholar]
  • 67.Wallace TM, Levy JC, Matthews DR.. Use and abuse of HOMA modeling. Diabetes Care 2004;27(6):1487–95. [DOI] [PubMed] [Google Scholar]
  • 68.Sumner AE, Cowie CC.. Ethnic differences in the ability of triglyceride levels to identify insulin resistance. Atherosclerosis 2008;196(2):696–703. [DOI] [PubMed] [Google Scholar]
  • 69.Haffner SM, Gonzalez C, Mlettlnen H, Kennedy E, Stern MP.. A Prospective Analysis of the HOMA Model The Mexico City Diabetes Study. Diabetes Care 1996;19(10):1138–41. [DOI] [PubMed] [Google Scholar]
  • 70.Radziuk J.Homeostastic Model Assessment and Insulin Sensitivity/Resistance. Diabetes 2014;63:1850–4. [DOI] [PubMed] [Google Scholar]
  • 71.Levy JC, Matthews DR, Hermans MP.. Correct Homeostasis Model assessment (HOMA) evaluation used the computer program. Diabetes Care 1998;21(12):2191–2. [DOI] [PubMed] [Google Scholar]
  • 72.Matsuda M, DeFronzo RA.. Insulin Sensitivity Indices Obtained From Oral Glucose Tolerance Testing. Diabetes Care 1999;22(9):1462–70. [DOI] [PubMed] [Google Scholar]
  • 73.Nightingale TE, Walhin JP, Thompson D, Bilzon JL.. Impact of Moderate-intensity exercise on metabolic health and aerobic capacity in persons with chronic paraplegia. Med Sci Sports Exerc 2016;48(5S):430.26460633 [Google Scholar]
  • 74.Elder CP, Apple DF, Bickel CS, Meyer RA, Dudley GA.. Intramuscular fat and glucose tolerance after spinal cord injury--a cr oss-sectional study. Spinal Cord 2004;42(12):711–6. [DOI] [PubMed] [Google Scholar]
  • 75.Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Castillo C, Gater DR.. Effects of spinal cord injury on body composition and metabolic profile – Part I. J Spinal Cord Med 2014;37(6):693–702. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 76.Griffin L, Decker M, Hwang J, Wang B, Kitchen K, Ding Z, et al. Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury. J Electromyogr Kinesiol 2009;19(4):614–22. [DOI] [PubMed] [Google Scholar]
  • 77.Jeon JY, Weiss CB, Steadward RD, Ryan E, Burnham RS, Bell G, et al. Improved glucose tolerance and insulin sensitivity after electrical stimulation-assisted cycling in people with spinal cord injury. Spinal Cord 2002;40(3):110–7. [DOI] [PubMed] [Google Scholar]
  • 78.Fisher JA, McNelis MA, Gorgey AS, Dolbow DR, Goetz LL.. Does Upper Extremity Training Influence Body Composition after Spinal Cord Injury? Aging Dis 2015;6(4):271–81. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Gorgey AS, Dolbow DR, Dolbow JD, Khalil RK, Gater DR.. The effects of electrical stimulation on body composition and metabolic profile after spinal cord injury--Part II. J Spinal Cord Med 2015;38(1):23–37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 80.Gater DR.Obesity After Spinal Cord Injury. Phys Med Rehabil Clin N Am 2007;18(2):333–51. [DOI] [PubMed] [Google Scholar]
  • 81.Gorgey AS, Mather KJ, Cupp HR, Gater DR.. Effects of resistance training on adiposity and metabolism after spinal cord injury. Med Sci Sports Exerc 2012;44(1):165–74. [DOI] [PubMed] [Google Scholar]
  • 82.Nash MS, Bilsker MS, Kearney HM, Ramirez JN, Applegate B, Green BA.. Effects of electrically-stimulated exercise and passive motion on echocardiographically-derived wall motion and cardiodynamic function in tetraplegic persons. Paraplegia 1995;33(2):80–9. [DOI] [PubMed] [Google Scholar]
  • 83.Rosety-Rodriguez M, Camacho A, Rosety I, Fornieles G, Rosety MA, Diaz AJ, et al. Low-grade systemic inflammation and leptin levels were improved by arm cranking exercise in adults with chronic spinal cord injury. Arch Phys Med Rehabil 2014;95(2):297–302. [DOI] [PubMed] [Google Scholar]
  • 84.Johnston TE, Marino RJ, Oleson C V, Schmidt-Read M, Leiby BE, Sendecki J, et al. Musculoskeletal Effects of 2 Functional Electrical Stimulation Cycling Paradigms Conducted at Different Cadences for People With Spinal Cord Injury: A Pilot Study. Arch Phys Med Rehabil 2016;97(9):1413–22. [DOI] [PubMed] [Google Scholar]
  • 85.Dolbow DR, Gorgey AS, Ketchum JM, Moore JR, Hackett LA, Gater DR.. Exercise Adherence During Home-Based Functional Electrical Stimulation Cycling by Individuals with Spinal Cord Injury. Am J Phys Med Rehabil 2012;91(11):922–30. [DOI] [PubMed] [Google Scholar]
  • 86.Gorgey AS, Lester RM, Wade RC, Khalil RE, Khan RK, Anderson ML, et al. A feasibility pilot using telehealth videoconference monitoring of home-based NMES resistance training in persons with spinal cord injury. Spinal Cord Ser Cases 2017;3. [DOI] [PMC free article] [PubMed]
  • 87.Bailey SN, Hardin EC, Kobetic R, Boggs LM, Pinault G, Triolo RJ.. Neurotherapeutic and neuroprosthetic effects of implanted functional electrical stimulation for ambulation after incomplete spinal cord injury. J Rehabil Res Dev 2010;47(1):7–16. [DOI] [PubMed] [Google Scholar]
  • 88.Doherty JG, Burns AS, O’Ferrall DM, Ditunno JF.. Prevalence of upper motor neuron vs lower motor neuron lesions in complete lower thoracic and lumbar spinal cord injuries. J Spinal Cord Med 2002;25(4):289–92. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Spinal Cord Medicine are provided here courtesy of Taylor & Francis

RESOURCES