Electrically induced cycling and nutritional counseling for counteracting obesity after spinal cord injury: A pilot study

Abstract

Objective: The purpose of this pilot study was to determine the preliminary efficacy of interval functional electrical stimulation (FES) cycling combined with nutritional counseling in obese adults with SCI.

Setting: Community-based individuals with chronic SCI.

Participants: Ten participants with chronic SCI.

Interventions: Participants were divided into 2 groups (1) FES cycling and nutritional counseling (FES & Nutri) and (2) nutritional counseling only (Nutri Only). The FES & Nutri group performed high intensity interval FES cycling for 30 min 3 times per week for 8 weeks and received nutritional counseling for 30 min once per week for 8 weeks. The Nutri Only group received the nutritional counseling only.

Outcome Measures: Body composition (fat mass, lean mass, body fat percentage), blood glucose levels.

Results: Participants in the FES & Nutri group had a statistically significant greater decrease in body fat percentage (M = −1.14) compared to those in the Nutri Only group (M = +0.28) and gained more lean mass in their legs (M = +0.66 kg) compared to the Nutri Only group (M = –1.05 kg).

Discussion/Conclusion: The statistically significant decrease in body fat percentage for the FES & Nutri group provides evidence that further study is merited. Future studies should include larger numbers of participants and the possible introduction of a preliminary strengthening program before initiating interval FES cycling. In addition, an increase in exercise volume and a greater role for nutritional counseling should be considered in order to optimize the treatment for obesity.

Introduction

Thanks to medical advances and improved injury surval rates, spinal cord injury (SCI) has essentially been converted to a long-term chronic disability.¹ Consequently, increased longevity in this population has been accompanied by many negative health conditions, with obesity being a major health disparity.^2,3 It is reported that about 66–75% of those with SCI are either overweight or obese.^2–5 Additionally, because greater obesity is related to greater disability and chronic diseases, the risk of cardiometabolic diseases, including heart disease, stroke and type II diabetes, are elevated to more than twice that of the able-bodied population.^6–9 One reason for the high rate of obesity after SCI is the loss of muscle mass. Shortly after the injury, those with SCI experience rapid and significant skeletal muscle atrophy below the level of injury^10–13 resulting in skeletal muscle cross-sectional areas of 45–80% less than that of able-bodied individuals.^11,14 Therefore, after SCI, the loss of metabolically active muscle mass results in a 26% reduction in basal metabolic rate.^14–16 This is important because basal metabolic rate accounts for ∼65% of the total daily energy expenditure and plays a major role in the positive energy balance that results in obesity after SCI.¹⁶ In addition to decreased muscle mass, individuals with SCI are typically among the most sedentary, thus further lowering energy expenditure creating an unhealthy energy balance.^17,18

In light of these factors, it is important to develop exercise programs capable of increasing energy expenditure via increased physical activity and reversing the loss of muscle mass in order to decrease obesity and cardiometabolic disease risk in people with SCI. There is clear evidence that physical activity can play an important role in decreasing the risk of obesity and cardiometabolic disease.¹⁹ In particular, high-intensity interval training (HIIT) has been shown to decrease cardiovascular and metabolic risk among able-bodied individuals in a shorter period of time than standard non-interval exercise programs.^20,21 For example, Karstoft et al.²⁰ compared interval walking to continuous walking in able-bodied adults with type II diabetes over a 6-month period. The continuous walking group walked for 60 min 5 days per week at a moderate intensity while the interval training group alternated between 3 min of high intensity walking and 3 min of low intensity walking 5 days per week. The walking intensities were determined by oxygen uptake (VO_2peak) testing and energy expenditure, with moderate intensity being set at 55% and high intensity at 70% of VO_2peak. Although, the mileage was the same for both groups, the interval training group lost 4.3 ± 1.2 kg total body weight and 3.1 ± 0.7 kg body fat mass, whereas no changes in body composition were found in the continuous walking group or the non-walking control group. In a similar study, Gillen et al.²¹ used leg cycling 3 times per week for 12 weeks in both the continuous and interval training able-bodied groups and determined intensity levels based on heart rate. The interval training group performed 3 maximal effort cycling sessions of 20 s each separated by 2 min low intensity cycling, while the continuous group cycled steady at 70% of maximal heart rate for 45 min. Both groups improved similarly in insulin sensitivity, cardiorespiratory fitness, and skeletal muscle mitochondrial content; however, the interval training group achieved these benefits with a five-fold lower exercise volume and training time.

A major consenquence of SCI is that paralysis limits voluntary exercise with the legs. In addition, the 60–90% prevalence of shoulder pain in persons with chronic SCI often limits the possibility of regular arm exercise.^22–27 To curcumvent these problems, functional electrical stimulation (FES) has been shown to be a safe and effective way to exercise paralyzed leg muscles in clinical and home settings.^17,28–30 As a result of developing a new protocol, which incorporates resistance-guided (RG) HIIT into FES cycling (RG-HIIT-FES),^31,32 we postulated that it may provide equal or greater benefits with less exercise time commitment, by analogy to HIIT programs used by able-bodied individuals. Resistance was used as the determinant of exercise intensity because heart rate has been shown to be an ineffective method for monitoring exercise intensity with injuries at T6 and above.³³

While FES cycling has been shown to help improve muscle mass in paralyzed limbs, there have also been reports of concomittent increases of caloric intake which could produce unanticipated consequences for programs trying to create a more healthy lean to fat mass ratio.³⁴ To limit unhealthy dietary fluctuations, the authors of the present study included nutritional counseling concerning healthy food choices and portions.

The purpose of this study was to determine the preliminary efficacy of RG-HIIT-FES cycling combined with nutritional counseling in obese adults with SCI in order to provide a new direction for weight control programs and a basis for developing evidence-based practice information.

Methods

Participants

Thirteen non-ambulatory chronically spinal injured participants with American Spinal Injury Association Impairment Scores A-C were enrolled with 3 participants not completing the study due to injury, pain or other factors unrelated to the study. The 10 remaining participants were divided into 2 groups (1) FES cycling and nutritional counseling (FES & Nutri) and (2) nutritional counseling only (Nutri Only). The 2 groups were matched by level of injury (2 tetraplegia and 3 paraplegia per group), years since injury (FES & Nurti group mean 11.6 yrs and Nutri Only group mean 9.8 yrs) and body mass index (29.04 and 27.33 kg/m² respectively). Table 1 provides a summary of participant characteristics.

Table 1. Participant characteristics.

ID	Group	LOI	AIS	YPI (yrs)	Sex	Age (yrs)	Ht (meters)	Wt (kgs)
1	FES & Nutri	T9	A	12	M	35	1.84	134.01
2	FES & Nutri	C6	B	9	F	34	1.67	76.57
3	FES & Nutri	C6	C	7	F	27	1.62	63.59
4	FES & Nutri	T11	B	13	F	33	1.57	63.54
5	FES & Nutri	T12	C	17	F	42	1.73	85.18
6	Nutri only	T10	A	25	F	36	1.62	104.46
7	Nutri only	C5	B	2	M	45	1.88	83.87
8	Nutri only	T10	B	5	M	23	1.78	67.86
9	Nutri only	T12	C	19	F	65	1.66	62.37
10	Nutri only	C5	A	8	F	40	1.69	82.19

LOI, level of injury; AIS, ASIA impairment scale; YPI, Years post injury; Ht, Height; Wt, Weight.

All participants read and completed an informed consent form and participants participating in FES cycling were examined by their physicians and presented a medical clearance form signed by their physician.

Body composition measurements

Participants were weighed using a Scale-Tronix Wheelchair Scale (Welch Allyn, Skaneatelest Falls, NY). The weight of the wheelchair alone subtracted from the combined weight of the participant and wheelchair provided the weight of the participant. An electrical powered lift (Invacare, Reliant 450) was used to provide safe transfers for all participants from the participant’s wheelchair to testing locations (e.g. exam table and body composition scanner). An anthropometric measuring rod was used to measure height. The left leg was extended to a straight position and ankle dorsiflexed to 90 degrees to enable an accurate measurement from the bottom of the foot to top of the head. A Lunar Prodigy Advance Absorptiometry (DXA) scanner (General Electric, Madison, WI) was used to measure body composition before and after the 8 week program. After transfer on to the DXA scanner, participants were asked to remain supine with arms at their sides without movement for 7–10 min. Their legs were strapped at the proximal and distal position with a slight internal rotation of the hips when possible, as recommended by the International Society for Clinical Densitometry and for the safety of the participant in the event of an untimely muscle spasm. All metal artifacts, rings, buckles and the like, were removed prior to scanning. Measurements concerning, body fat percentage, fat mass, total and legs lean mass and bone mineral density were determined by the DXA Lunar software version 10.5.

Glucose control

Blood glucose and hemoglobin A1c (HbA1c) levels were examined to determine effects on short- and long-term glucose regulation. To do this, portable automated glucose testing PTS Diagnostics and A1cNow devices were used to analyze blood samples obtained from a finger stick performed in the left hand prior to and after the 8 week program.

Maximal FES cycling resistance test

Prior to the Maximal FES Cycling Resistance Test, surface electrodes were placed on the quadriceps, hamstring, and gluteal muscle groups as described in recent publications.^17,35 Once electrodes and leads were attached, electrical stimulation was applied to each muscle group individually beginning with low level intensity then increasing until a comfortable vigorous muscle contraction was induced. This process determined the initial electrical intensity parameters used for the insuing test. Participants cycled from their own wheelchair with safety hook attachments securing the wheelchair to the cycle. Participants were velcro strapped onto the FES cycle pedals at the forefoot, heel, and just below the knee. The Resistance Guided FES Cycling Maximal Test began with a 2 min passive cycling warm-up and then the electricity was ramped up to the prior determined electrical intensities up to 140 mA. Participants cycled at 35 rpm and the resistance, starting at 0.5 Nm, increased by 0.5–2 Nm each minute (depending on individual tolerance) until the participant could no longer cycle without motor support. Test termination was determined when the cycling speed dropped 10 rpm or when the display panel cogwheel indcator showed that motor support was needed for continued cycling. At this point, a passive cool-down period began for 2 min to restore resting levels. The maximal level of resistance reached while cycling for 30 s without motor support was considered the participants cycling resistance maximum.

RG-HIIT-FES cycling program

Preparation for the RG-HIIT-FES cycling sessions was the same as mentioned above for the maximal cycling resistance test. Participants were asked to empty their bladder prior to cycling. Vital signs (heart rate and blood pressure) were checked at rest, and again every 5 min or sooner as needed during the cycling session. Participants cycled 3 times per week for 8 weeks with at least one rest day after a cycling day. Each participant was asked to perform the RG-HIIT-FES cycling protocol with a 30-second high intensity interval at 80% of the highest resistance tolerated during the initial resistance guided FES cycling maximal test followed by a 30 s low intensity bout where the resistance is decreased to 0.5 Nm, the lowest level the RT300 cycle will allow. Sessions continued for 30 min alternating between high and low intensity intervals. During high intensity intervals, electical stimulation was at 100% of the prior determined effective intensity level, not to exceed 140 mA, which is the RT300 maximum. During low intensity intervals, electrical stimulation intensity was decreased by 50%. Pulse width was constant at 350 µs for greater muscle recovery between sessions,³⁶ while frequency was maintained at 40 Hz. A 2-minute passive cycling warm-up and 2-minute passive cycling cool-down bracketed the RG-HIIT-FES cycling sessions. The rationale for cycling at 35 rpm stems from our observations that some individuals were so deconditioned that their stimulated muscles were incapable of generating output sufficient for cycling at faster speeds without motor support at the lowest cycle resistance 0.5 Nm. Thus, the speed of cycling was thought to be low enough to allow electricity-induced muscle contractions to cycle against resistance on their own. However, 2 of the 5 participants in the FES & Nutri group were not initially able to cycle at a resistance greater than 0.5 Nm using a speed of 35 rpm, thus while the strength of muscle contractions alternated between high and low intensity due to the electrical stimulation changes between high and low intensity phases, the resistance remained unchanged between intervals until enough strength was gained to cycle against greater resisitance levels without motor support. These changes ocurred at cycling sessions 12 and 14 respectively. All participants completed a total of 24 cycling sessions.

The first FES cycling session for each participant was completed in the university laboratory so that the participants response via vital signs HR, BP, rating of perceived exertion could be monitored to ensure safety and exercise tolerance. Participants then completed the remaining FES cycling sessions in their own home and results were monitored via internet connection. If the participants had there own FES cycles, the interval FES cycling program was uploaded to their cycle. If the participant did not own an FES cycle, an RT300 FES cycle was placed in their home for the duration of the program. None of the participants had participated in FES cycling for at least 3 months prior to the start of the program.

Nutritional counseling

Data Collection: A Registered Dietitian supervised the collection of dietary intake data from participants using the USDA 24-hour recall, multi-pass 5-step method (an established and ideal approach for short-term dietary intake assessment).^37–39 Data were collected via telephone on two nonconsecutive weekdays and one weekend day, pre- and post-intervention. A nutrient analysis was conducted to determine average daily total energy, macronutrient, and other nutrient intake.

Intervention: Participants received a brief introductory nutrition education session at enrollment regarding portion sizes and food reporting to improve dietary data collection accuracy. Nutrition counseling was delivered to maintain participant dietary intake throughout the course of the study based on the individualized, calculated needs of the participants. The nutritional counseling was not provided to alter caloric intake, but rather to ensure that individuals maintained their normal caloric intake throughout the study so as not to confound the effects of the FES-HIIT cycling program. Based on current guidelines, participants in both groups were monitored for adherence to the following diet: a caloric prescription of 22.7 or 27.9 kilocalories per kilogram of body weight for tetraplegic or paraplegic participants, respectively, 0.8–1.0 grams of protein per kilogram of body weight per day, and 1 milliliter of fluid per kilogram of body weight plus 500 milliliters per day.⁴⁰ Participants received weekly nutrition counseling sessions via telephone to support the participants’ goals to meet prescribed recommendations.

Statistical analysis

Because the analysis of covariance (ANCOVA) is often used in designs such as this study, the researchers tested the ANCOVA assumptions of homogeneity of variance and homogeneity of slopes, and both of these assumptions were violated on the collected data. Thus the gain score approach using an independent sample t-test was used which according to Glinger et al.⁴¹ is the next best option. Accordingly, the researchers used the gain score difference between pretest and posttest scores to determine if there was a difference between FES & Nutri and Nutri Only groups. The gain scores for each measurement were treated as the dependent variable, and the control and treatment groups were considered the two groups of the independent variable. The Independent sample t-test was used to determine if there was a statistical difference in the gain score between the Nutri Only (control) group and FES & Nutri (treatment) group based on body fat percentage, legs lean mass, total lean mass, total fat mass, body mass index (BMI), legs fat mass, and weight.

For the independent sample t-test, Levene’s test of equal variances was not violated for each dependent variable; thus, t statistics and p values were assessed assuming equal variances.

Results

Body composition

The major findings of body composition in this study were that a significant difference existed between the FES & Nutri and Nutri Only groups on body fat percentage (t = −0.628, P = 0.030) and legs lean mass (t = 4.060, P = 0.004). For body fat percentage, participants in the FES & Nutri group had a loss of body fat percentage (M = −1.14) while those in the Nutri Only group had a slight gain (M = +0.28). Additionally, participants in the FES & Nutri group gained lean mass in their legs (M = +0.66 kg) while the Nutri Only group continued to lose leg lean mass (M = −1.05 kg) over the 8 week study.

The FES & Nutri group also showed a greater decrease for weight, BMI and total fat mass as well as a greater increase in total lean mass than the Nutri Only group however, these results were determined not to be statistically significant. Tables 2 and 3 show pre and post program body composition measures and individual changes by participant are displayed in Table 4.

Table 2. Changes in body composition.

ID	Group	Wt (kg)	BMI (kg/m2)	BF%*	TLM (kg)	TFM (kg)	LLM* (kg)	LFM (kg)
1	FES & Nutri	−7.41	−2.2	−1.8	−1.71	−5.21	−0.12	−0.02
2	FES & Nutri	−4.6	−0.1	−1.7	+1.82	−0.68	+1.26	+0.25
3	FES & Nutri	+1.6	0	−1.1	+2.05	+0.18	+0.92	+0.29
4	FES & Nutri	−0.14	−0.1	−1.1	+0.24	−0.86	+0.18	+0.27
5	FES & Nutri	−1.13	−0.4	0	−0.19	−0.24	+1.03	+1.91
6	Nutri Only	−0.9	−0.3	+1.2	−2.35	+1.89	−2.22	−2.37
7	Nutri Only	+0.5	+0.1	+1.3	+0.22	+1.92	−2.65	+0.31
8	Nutri Only	+0.2	+0.5	−0.2	+0.32	−0.12	−0.94	−0.48
9	Nutri Only	−0.6	−0.2	+0.1	−0.82	−0.62	−0.66	−1.13
10	Nutri Only	−0.9	−0.4	−1.0	−0.40	−1.24	−1.19	−1.48

BMI, Body mass index; BF%, Body fat percentage; TLM, Total lean mass; TFM, Total fat mass; LLM, Legs lean mass; LFM, Legs fat mass; *, Statistically Significant.

Table 3. Pre-intervention body composition.

ID	Group	Wt (kg)	BMI (kg/m2)	BF%	TLM (kg)	TFM (kg)	LLM (kg)	LFM (kg)
1	FES & Nutri	134.01	39.5	44.3	70.57	56.02	10.90	14.52
2	FES & Nutri	76.57	27.4	54.9	32.64	39.77	9.20	12.64
3	FES & Nutri	63.59	24.1	40.1	36.00	24.10	11.61	8.80
4	FES & Nutri	63.54	25.6	40.2	35.95	24.15	8.60	9.00
5	FES & Nutri	85.18	28.6	53.2	37.37	42.55	8.56	11.50
6	Nutri Only	104.46	39.8	58.8	40.89	58.39	13.70	24.06
7	Nutri Only	83.87	23.7	41.4	45.28	32.01	14.71	11.43
8	Nutri Only	67.86	21.5	23.2	49.57	15.01	12.32	5.17
9	Nutri Only	62.37	22.5	44.4	33.38	26.63	8.03	11.40
10	Nutri Only	82.65	28.9	55.5	35.14	43.85	12.06	16.36

BMI, Body mass index; BF%, Body fat percentage; TLM, Total lean mass; TFM, Total fat mass; LLM, Legs lean mass; LFM, Legs fat mass.

Table 4. Post-intervention body composition.

ID	Group	Wt (kg)	BMI (kg/m2)	BF%	TLM (kg)	TFM (kg)	LLM (kg)	LFM (kg)
1	FES & Nutri	126.60	37.3	42.5	68.87	50.82	10.80	14.50
2	FES & Nutri	76.11	27.3	53.2	34.45	39.10	10.46	12.89
3	FES & Nutri	65.23	24.1	39.0	38.05	24.28	12.53	9.08
4	FES & Nutri	63.23	25.5	39.1	36.19	23.28	8.78	9.26
5	FES & Nutri	84.05	28.2	53.2	37.48	42.57	9.64	12.99
6	Nutri Only	103.56	39.2	61.0	38.54	60.27	11.47	21.69
7	Nutri Only	83.91	23.8	42.7	45.50	33.93	14.45	11.74
8	Nutri Only	68.04	21.5	23.0	49.88	14.89	11.39	4.70
9	Nutri Only	61.73	22.3	44.5	32.56	26.08	7.37	10.27
10	Nutri Only	81.53	28.5	54.5	35.53	42.62	10.88	14.88

BMI, Body mass index; BF%, Body fat percentage; TLM, Total lean mass; TFM, Total fat mass; LLM, Legs lean mass; LFM, Legs fat mass.

Blood glucose

There was a nominal drop in the mean blood glucose levels for the FES & Nutri group 101.8–97.8 mg/dl and the Nutri Only group 94.6–93 mg/dl, however neither change was found to be statistically significant P > 0.05. Pre and post HbA1c measures were only received from three participants from each group with a small decrease in mean for each group, FES & Nutri 5.43–5.13 and Nutri Only 5.37–5.27. These changes were also not statistically significant P > 0.05.

Nutritional intake

While there were nominal changes the Mann Whitney Test revealed no significant group differences (P = >0.05) in pre-intervention or post-intervention intake of kcals, fat and protein. Wilcoxon signed rank test showed no differences for either group pre-intervention or post-intervention intake of kcals, fat and protein. Similarly, there were no group or pre and post intervention differences in percent of energy or protein needs consumed (Table 5). This would indicate that the participants were generally compliant with the maintenance recommendations for the nutrition intervention. These results were provided by study participants over the telephone as a 3 day recall of food consumed pre and post intervention.

Table 5. Mean nutritional intake (USDA 24-hr recall, multi-pass 5 step method).

	Energy (kcals)	Protein (g)	Fat (g)
FES & Nutri Pre-Test	1410	61	53
FES & Nutri Post-Test	1732	83	58
Nutri Only Pre-Test	1635	55	70
Nutri Only Post-Test	1530	74	57

Discussion

The authors postulated that a program of RG-HIIT-FES cycling and nutritional counseling may provide equal or greater benefits for battling obesity with less exercise time commitment, as an analogy to HIIT programs used by able-bodied individuals. The results of this pilot study indicate that this postulation was at least partially correct. There was a statistically significant decrease in mean body fat percentage which is important for battling obesity and possibly decreasing cardiometabolic disease risk. The increase in legs lean mass was expected due to the electrically induced exercise to the paralyzed muscles of the legs. This is important as Skold et al.⁴² & Demchak et al.⁴³ have demonstrated that FES legs cycling increases leg muscle volume and cross-sectional area versus non-treatment control groups. In addition, the results of the currently study show similarities with a recent case report where a 31 yr old male with T10 SCI, AIS B performed interval FES cycling 3 times per week for 8 weeks and increased total body lean mass and legs lean mass by 2.8% and 5.3% respectively. Vastus lateralus thickness increased by 59%⁴⁴.

There were additional nominal decreases in weight, total fat mass, BMI and blood glucose levels although these changes were not found to be statistically significant (all P > 0.05). The authors feel that the small number of participants and the low volume of exercise may have been a limitation in this regard. Likewise, blood glucose and HbA1c levels decreased in both groups with neither change being statistically significant.

These results provide evidence that a program of RG-HIIT-FES cycling and nutritional counseling can be beneficial for individuals with SCI, however, the authors recommend implementation of a primer exercise program of electrical stimulation to the paralyzed muscle groups to be used in the RG-HIIT-FES cycling program. Two individuals in the FES & Nutri group were not able to cycle against a resistance greater than 0.50 Nm at the outset of the program, thus for the first 12–14 sessions of the program the cycling resistance in both the high and low intensity intervals remained the same. Thus the only factor differentiating the high intensity and low intensity intervals for these two participants was the percentage of electrical stimulation used. The initial and final high intensity interval resistances for the FES & Nutri group were (0.50–1.04 Nm; 0.50–1.17 Nm; 1.00–2.12 Nm; 0.91–1.04 Nm 0.64–0.91 Nm). The authors also feel that the lack of exercise volume may have limited the benefits received by the FES & Nutri group. The U.S. Department of Health and Human Services “Physical Activity Guidelines for Adults with Disabilities” recommend at least 150 min a week of moderate-intensity exercise.⁴⁵

Additionally, it would likely be helpful for nutritional counseling to take on a larger role than just attempting to maintain the participants’ normal caloric intake and nutrition. As these individuals are obese, nutritional counseling should become more involved in sensibly decreasing caloric intake in order to provide greater assistance in battling obesity.

Limitations

There were only 10 total participants (n = 5 per group) which makes it difficult to generalize the results to the overall SCI population. The use of BMI as a matching factor was less accurate than using body fat percentage. The pre- and post-test 3 day dietary recall did not guarantee regular eating habits during the eight week program as they may have differed between the 2 testing periods. Lastly, the two groups were uneven in terms of intervention, one receiving the exercise intervention and nutritional counseling while the other received nutritional counseling only.

Conclusion

The statistically significant decrease in body fat percentage and increased legs lean mass for those utilizing RG-HIIT-FES cycling and nutritional counseling provides evidence that further study is merited. Blood glucose and HbA1c levels decreased in both groups although these changes lacked statistical significance. The nutritional counseling that was designed to maintain dietary intake levels throughout the program also saw a nominal increase in caloric consumption in the FES & Nutri group, however this was also not a statistically significant change. Future studies should include larger numbers of participants and the introduction of a preliminary strengthening program to better prepare participants for RG-HIIT-FES. In addition, an increase in exercise volume for more caloric expenditure and a greater role for nutritional counseling designed to decrease caloric intake should be considered in order to optimize the treatment for obesity.

Disclaimer statements

Contributors None.

Funding Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health via the Center for Clinical and Translational Research under number U54GM115428.

Conflicts of interest None.