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Optimization of Protocols Using Neuromuscular Electrical Stimulation for Paralyzed Lower-Limb Muscles to Increase Energy Expenditure in People With Spinal Cord Injury

Optimization of Protocols Using Neuromuscular Electrical Stimulation for Paralyzed Lower-Limb... ORIGINAL RESEARCH ARTICLE Optimization of Protocols Using Neuromuscular Electrical Stimulation for Paralyzed Lower-Limb Muscles to Increase Energy Expenditure in People With Spinal Cord Injury Yiming Ma, MEd, Sonja de Groot, PhD, Ad Vink, MSc, Wouter Harmsen, PhD, Christof A.J. Smit, PhD, Janneke M. Stolwijk-Swuste, PhD, Peter J.M. Weijs, PhD, and Thomas W.J. Janssen, PhD Objective: The aim of this study was to evaluate whether using surface What Is Known neuromuscular electrical stimulation (NMES) for paralyzed lower-limb � Neuromuscular electrical stimulation (NMES) could muscles results in an increase in energy expenditure and whether the lead to a significant increase in energy expenditure number of activated muscles and duty cycle affect the potential increase. for weight management in able-bodied people. Using Design: This was a cross-sectional study. NMES to activate paralyzed lower-limb muscles for in- Results: Energy expenditure during all NMES protocols was signifi- creasing energy expenditure and subsequently weight cantly higher than the condition without NMES (1.2 ± 0.2 kcal/min), management in people with spinal cord injury has not with the highest increase (+51%; +0.7 kcal/min, 95% confidence in- been fully investigated. terval, 0.3–1.2) for the protocol with more muscles activated and the What Is New duty cycle with a shorter rest period. A significant decrease in muscle contraction size during NMES was found with a longer stimulation � Using NMES for paralyzed lower-limb muscles can sig- time, more muscles activated, or the duty cycle with a shorter rest period. nificantly increase energy expenditure with the highest Conclusion: Using NMES for paralyzed lower-limb muscles can signif- increase for the protocol with more muscles activated icantly increase energy expenditure compared with sitting without and the duty cycle with a shorter rest period (+51%). � Muscle fatigue occurred significantly with the more NMES, with the highest increase for the protocol with more muscles ac- intense NMES protocols. tivated and the duty cycle with a shorter rest period. Muscle fatigue oc- � Future studies should further optimize the NMES param- curred significantly with the more intense NMES protocols, which might eters and investigate the long-term effects of NMES. cause a lower energy expenditure in a longer protocol. Future studies should further optimize the NMES parameters and investigate the long-term effects of NMES on weight management in people with SCI. Reducing energy intake and increasing energy expendi- Key Words: Spinal Cord Injury, Neuromuscular Electrical ture or a combination are the possibilities of reaching a Stimulation, Lower-Limb Muscles, Energy Expenditure healthy energy balance. The SCI affects resting energy ex- (Am J Phys Med Rehabil 2023;102:489–497) penditure, which is markedly lower (14%–27%) in people with SCI compared with the able-bodied population. Resting energy expenditure is the greatest proportion (60%–80%) of besity is a common secondary health complication in peo- the total daily energy expenditure especially in very sedentary 3,4 O ple with spinal cord injury (SCI), with about two of every individuals. Because resting energy expenditure is low in three persons with SCI being obese and at risk for the meta- SCI, rather extreme dietary requirements, with very low energy bolic consequences of obesity. Therefore, it is necessary to reach intake, might cause a lower suboptimal protein and micronu- a healthy energy balance and prevent weight gain or achieve trient intake, resulting in a higher risk of malnutrition and weight loss, respectively, in people with SCI. subsequent health complications. The other way to achieve From the Faculty of Behavioural and Movement Sciences, Vrije Universiteit formal analysis, writing–original draft, writing–review and editing. WH: Amsterdam, Amsterdam Movement Sciences, Amsterdam (YM, SdG, AV, software, validation, resources, investigation, formal analysis, writing–original WH, TWJJ); Amsterdam Rehabilitation Research Center | Reade, Amsterdam draft, writing–review and editing. CAJS: writing–review and editing. JMS-S: (YM, SdG, CAJS, JMS-S, TWJJ); Tolbrug Rehabilitation/Jeroen Bosch Hospi- writing–review and editing. PJMW: formal analysis, data curation, writing– tal, `s Hertogenbosch (CAJS); Center of Excellence for Rehabilitation Medicine, review and editing, visualization, supervision. TWJJ: conceptualization, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht Uni- resources, formal analysis, data curation, writing–review and editing, versity and De Hoogstraat Rehabilitation, Utrecht (JMS-S); Faculty of Sports visualization, supervision. and Nutrition, Center of Expertise Urban Vitality, Amsterdam University of Ap- Financial disclosure statements have been obtained, and no conflicts of interest have been plied Sciences, Amsterdam (PJMW); and Department of Nutrition and Dietet- reported by the authors or by any individuals in control of the content of this article. ics, Amsterdam University Medical Centers, Vrije Universiteit Amsterdam, Supplemental digital content is available for this article. Direct URL citations appear Amsterdam Movement Sciences, Amsterdam, the Netherlands (PJMW). in the printed text and are provided in the HTML and PDF versions of this article All correspondence should be addressed to: Yiming Ma, MEd, Vrije Universiteit on the journal’s Web site (www.ajpmr.com). Amsterdam, Amsterdam Movement Sciences, Van der Boechorststraat 7, 1081 Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. This is BT Amsterdam, the Netherlands. an open-access article distributed under the terms of the Creative Commons Data availability: The datasets generated and/or analyzed during the current study are Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), available from the corresponding author on reasonable request. where it is permissible to download and share the work provided it is properly Author contributions: YM: software, validation, formal analysis, data curation, cited. The work cannot be changed in any way or used commercially without writing–original draft, writing–review and editing, visualization. SdG: permission from the journal. methodology, formal analysis, data curation, writing–review and editing, ISSN: 0894-9115 visualization, supervision. AV: software, validation, resources, investigation, DOI: 10.1097/PHM.0000000000002120 American Journal of Physical Medicine & Rehabilitation � Volume 102, Number 6, June 2023 www.ajpmr.com 489 Ma et al. Volume 102, Number 6, June 2023 a healthy energy balance, increasing energy expenditure, might tion below the ischial tuberosity and a redistribution of sitting therefore be more rational. By participating in physical exer- pressure away from the ischial tuberosity area, which could con- 19–23 cises such as arm cranking, weight training, or wheelchair tribute to a lower sitting pressure variance. Basedonthe ra- sports, people with SCI can gain muscle mass and strength tionale of sitting pressure relief by NMES, it is expected that 6,7 and reduce fat mass. However, not all people with SCI when muscle fatigue occurs, muscle contractions will become are able or inclined to engage in physical exercise and it was less powerful and subsequently cause less reduction in sitting 18,19 also reported that the energy expenditure in response to exer- pressure variance. Because muscle fatigue can remarkably 14,24 cises could be rather limited in people with SCI, especially in reduce the efficacy of NMES, it is important to detect pos- 1,8 those with a high degree of paralysis, making it difficult siblemusclefatigue during NMES. to sufficiently increase energy expenditure using only the For able-bodied individuals, studies have shown that NMES nonparalyzed muscles. could lead to a significant increase in energy expenditure for 25,26 Activating the larger paralyzed muscles below the lesion weight management. However, using NMES to activate using surface neuromuscular electrical stimulation (NMES) paralyzed lower-limb muscles for increasing energy expendi- or functional electrical stimulation is a possible way to increase ture and, subsequently, weight management in people with SCI 17,27 energy expenditure without many practical barriers and much has not been fully investigated. The purpose of this study, discomfort. Although functional electrical stimulation–induced therefore, was to evaluate whether using NMES for paralyzed cycling and rowing have been reported to increase energy lower-limb muscles results in a significant increase in energy expenditure and muscle mass in the lower limbs in people expenditure compared with a no NMES condition and how 9,10 with SCI, some drawbacks such as the adequate time for the number of activated muscles (gluteals, hamstrings, quadri- training responses to occur and the extra set-up time and pro- ceps, and calves vs. gluteals and hamstrings only) and duty cy- fessional assistance still limit its availability and accessibility cle (1:4 s vs. 1:8 s)affectthisincrease. 11,12 in daily use. Compared with functional electrical stimu- lation, NMES is a different form of paralyzed muscle activa- METHODS tion that could be less time-consuming and could even be applied during daily activities or during the night without Participants the requirement of external equipment other than a portable 11,13 Nine men with an SCI for at least 6 mos and untrained for stimulator and electrodes. If this form of NMES-induced NMES participated in this study. Exclusion criteria were pres- contractions could lead to an increased energy expenditure, sure sores, a flaccid paralysis, a known intolerance for NMES, this method could be beneficial to long-term weight manage- a history of severe autonomic dysreflexia, or severe cognitive ment in people with SCI. or communicative disorders. This study was approved by the Different stimulation parameters such as the target muscles 14 Medical Ethical Committee of Vrije Universiteit Amsterdam and duty cycle can induce different effects. The lower-limb Medical Center (NL22712.029.08) and Reade, center for reha- muscles, including gluteals, hamstrings, quadriceps, and calves, bilitation and rheumatology. All participants signed an informed are naturally exposed to muscle atrophy owing to the loss of cen- 15,16 consent before the start of the experiments. This study conforms tral activation and immobilization after SCI. Activating these to all STROBE guidelines and reports the required information large, clinically important muscles may result in a significant 17 accordingly (see Supplementary Checklist, Supplemental Digi- increase in energy expenditure. Another important stimula- tal Content 1, http://links.lww.com/PHM/B869). tion parameter is duty cycle. Duty cycle describes the actual muscle activation and rest periods of an NMES program. The- Design oretically, duty cycle with a shorter rest period could induce There were five test conditions, including one without NMES more intense muscle contractions and subsequently contribute and four with NMES. Energy expenditure without NMES was to a higher increase in energy expenditure. However, it could measured in a resting sitting position for 5 mins before NMES also lead to greater muscle fatigue, which reduces energy ex- 18,19 protocols started. Participants received NMES during four dif- penditure and the efficacy of NMES. It is still not clear ferent 10-min protocols while sitting still on their wheelchair. what is the optimal stimulation-rest ratio to increase energy ex- The stimulated muscles were gluteals (Gl), hamstrings (Ham), penditure for people with SCI. quadriceps (Qua), and calves (Ca) vs. Gl and Ham only. The Lower-limb muscle fatigue can also influence the stimula- duty cycle was 1:4 s or 1:8 s. Energy expenditure was measured tion effects. With NMES, it was reported that selective recruit- continuously during all conditions, that is, with and without ment of the large and fast motor units would result in a more NMES. The order in which the NMES protocols were provided rapid fatigue than with voluntary exercise because the axons was randomized by simple randomization to avoid the effect of of the larger motor units have less resistance to electrical current. muscle fatigue. Muscle fatigue was measured by the changes in Thus, the predominance activation of type II fibers in people the muscle contraction size and sitting pressure variance. During with SCI during NMES could lead to greater muscle fatigue. all measurements, participants were instructed to sit as still as Relevant factors such as training history, percentage of type II fi- possible and not to speak. The placement of the electrodes for bers, time since injury, and placement of electrodes could cause 14,18 NMES is showninFigure1. a different time to fatigue during NMES. For hamstrings and quadriceps, changes in muscle contraction size, measured Electrical Stimulation by a muscle contraction sensor, can be an indicator of muscle fa- tigue. For gluteals, studies have shown that utilizing NMES to The muscles were electrically stimulated with a biphasic, activate gluteals could result in a sizeable sitting pressure reduc- squared, and balanced stimulation pattern provided by a 490 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Electrical Stimulation in People With SCI portable eight-channel stimulator (NeuroPro, Berkelbike BV, 4 mins of the resting condition (the first minute was discarded Sint-Michielsgestel, the Netherlands). To induce a tetanic mus- to allow for determining energy expenditure in a stable state) cle contraction and activate a maximum number of muscle fi- and during the last 7 mins of each NMES protocol (the first bers with less chance of skin pain, a stimulation frequency of 3 mins were discarded to allow for determining energy expen- 28,29 70 Hz and a pulse duration of 0.5 msecs were applied. Be- diture in a stable state). fore starting the actual NMES protocols, the stimulation cur- rent amplitude was determined for each participant and muscle Muscle Fatigue group separately. Current amplitude (35–120 mA) was individ- When muscles fatigue, the muscle contractions in response ually set to induce visible muscle contractions at comfortable to NMES become less powerful. A muscle contraction results levels, but low enough to prevent very strong contractions that in an increase in the muscle’s circumference compared with rest. could potentially disturb daily activity performance or even Therefore, a system was developed to monitor the changes in the force the participant out of the wheelchair. In this way, a circumference of the upper leg to evaluate the degree of fatigue of clinically relevant current level was achieved. To avoid un- the hamstrings and quadriceps during the NMES protocols. A wanted movements (knee extension) during NMES, the feet Futek load cell (LSB200, 25 lb, JR S-beam load cell), measuring were fixed to the footrests of the wheelchair with a Velcro strap. forces in one direction during rest and muscle contractions, was The duration of each NMES protocol was 10 mins, followed by integrated into a Velcro strap with an elastic end and placed a 10-min rest. around the right upper leg (Fig. 1, right). When muscles contract because of NMES, the upper-leg muscle circumference in- Energy Expenditure creases as the muscles become shorter and thicker, and the elas- The primary outcome in this study was the energy expen- tic part will be more elongated, resulting in a force difference on diture calculated from the oxygen consumption (VO )and car- the load cell. With muscle fatigue negatively affecting muscle bon dioxide production (VCO ) gatheredwithanon-line gas contractions, a less pronounced change in muscle circumfer- analysis system (Oxycon alpha, Mijnhardt BV, Bunnik, the ence and, subsequently, a smaller force difference will occur. Netherlands). Gas and volume calibration was performed be- The data were obtained with a data acquisition system of Na- fore each measurement. All the measurements were done un- tional Instruments (NI USB-6009 DAQ) and LabView software der the same conditions. The energy expenditure in kcal/min (Student Edition 8.2). was calculated using the Weir equation. A second parameter to estimate fatigue of the gluteals and Energy expenditure (kcal/min) = 3.94 VO +1.11 VCO hamstrings was sitting pressure variance, measured using a 2 2 With Matlab software (R2018b), mean energy expendi- pressure mapping system (mFLEX, Vista Medical, Canada). ture was calculated for rest without NMES during the last This system measures the pressure of an area of 533  533 mm FIGURE 1. The placement of the electrodes for gluteals, hamstrings (electrodes with solid outline, left), calves (electrodes with dashed outline, left) stimulation and for quadriceps stimulation (electrodes with dashed outline, right) and the contraction sensor (right). © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 491 Ma et al. Volume 102, Number 6, June 2023 with a total of 1024 (32 32) pressure sensors and was placed on changes in muscle contraction size and sitting pressure variance the cushion of the participant’s wheelchair. During a during the NMES protocols. nonactive period, most pressure will be located around the buttocks. When the gluteals and hamstrings contract, the total Statistical Analysis pressure will be more distributed to the surrounding area and The normality of the data was checked by Shapiro-Wilk will therefore result in a lower pressure variance during an acti- tests and Q-Q plots and all data were normally distributed (or vation period than in rest. Fatigue will make the muscle con- approximately). Repeated-measures analysis of variance to- tractions less powerful, resulting in less pronounced changes of gether with post hoc tests was used to check the systematic pressure distribution and therefore less decrease in pressure vari- differences between (1) energy expenditure without and with ance. This method was applied only for the protocols with gluteal NMES during all protocols; (2) energy expenditure with NMES and hamstring activation because activation of quadriceps and in different protocols; (3) the muscle contraction size during all calves lifts the legs and has a disruptive effect on sitting pressure protocols and the interaction effects (2  2  2, stimulation variance. With Matlab software, the changes in sitting pressure time, muscles and duty cycle); and (4) the sitting pressure vari- variance were analyzed. ance during the 1:4 s GlHam and 1:8 s GlHam protocols and The measurements of muscle contraction size and sitting the interaction effects (2  2, stimulation time, duty cycle). pressure variance were started at least 1 min before the first All statistical analyses were performed using SPSS software NMES protocol started. The start and end time of each NMES (version 25, IBM, Somers, NY). A P value <0.05 was consid- protocol was recorded. The raw force data were filtered with a ered significant. second-order Butterworth band-pass filter (0.05–0.8 Hz). Matlab software was used to further analyze the data. For muscle RESULTS contraction size, all the peak and valley values of force in each protocol were determined at first. The peak values right before the valley values were then selected to calculate the Descriptives force differences between them. The force differences were used Table 1 shows the descriptives of all participants. Because -bx -ed to make a general fit exponential model with y = ae + c of measurement errors, the sitting pressure variance data of two function to check the values at specific time. Subsequently, participants were removed for analysis. the force differences at the start (5 s) and at 3 and at 10 mins in each NMES protocol were determined. A higher force differ- Changes in Energy Expenditure Among ence was associated with a larger change in muscle contraction Different Protocols size. Percentages of the difference at 3 and 10 mins relative to Energy expenditure (kcal/min) with or without NMES is the start value were calculated to indicate the changes in muscle shown in Figure 3. All NMES protocols resulted in a significant contraction size. increase in energy expenditure (1:4 s GlHamQuaCa: +51%; Similarly, all the peak and valley values of sitting pressure 1:8 s GlHamQuaCa: +44%; 1:4 s GlHam: +36%; 1:8 s GlHam: variance in each protocol were determined and the differences +25%) compared with the energy expenditure without NMES between them were used to make a general fit exponential -bx -ed (1.2 ± 0.2 kcal/min). Three participants showed a very positive model with y = ae + c function to check the values at spe- increase in energy expenditure compared with other partici- cific time. Subsequently, these differences at the start (5 s) and pants, with the highest increase (+106%, +171%, and +55%) at 3 and at 10 mins in each NMES protocol were determined. A during the protocol 1:4 s GlHamQuaCa (Fig. 4). When comparing higher difference was associated with a higher decrease in pres- between different protocols, the protocol 1:4 s GlHamQuaCa sure variance. Percentages of the difference at 3 and 10 mins rel- and 1:8 s GlHamQuaCa with more muscles activated showed a ative to the start value were calculated to indicate the changes in sitting pressure variance. Figure 2 shows the examples of the significantly higher increase in energy expenditure compared FIGURE 2. Examples of the changes in muscle contraction size (left, participant 4) and sitting pressure variance (right, participant 3) during NMES -bx -ed protocols. Lines are fit through the data by a general fit exponential model with y = ae + c function. Most of the participants showed similar trends as illustrated above. 492 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Electrical Stimulation in People With SCI TABLE 1. Descriptives of participants (n =9) Current Amplitude Participant Age, y Body Mass, kg Height, m Time Since Injury, yrs Lesion Level AIS Gl Ham, mA Qua, mA Ca, mA 158 86 1.85 1.5 C3–4 B 120 100 100 2 31 63 1.75 9 C5 A 90 80 90 349 63 1.87 22 C5–6 A 60 90 50 4 24 80 1.91 8 C6 B 75 90 70 541 81 1.70 14 C6–7 B 40 50 35 631 70 1.80 5 C7–8 A 60 60 40 728 92 1.86 4 T3–4 A 70 70 65 8 66 120 1.73 4 T9 B 50 40 45 9 29 73 1.84 11 T11 A 45 60 60 Mean (SD) 40 (15) 81 (18) 1.81 (0.71) 9 (6) 68 (25) 71 (20) 62 (22) Lesion level: C, cervical; T, thoracic. AIS indicates American Spinal Injury Association impairment scale; Gl, gluteals; Ham, hamstrings; Qua, quadriceps; Ca, calves. with the protocol 1:4 s GlHam (+11%) and 1:8 s GlHam muscles activated and the duty cycle with a longer rest period (+15%), respectively. However, no significant difference was (1:8 s GlHam) showed the smallest increase (+25%) in energy found between the protocol 1:8 s GlHamQuaCa and 1:4 s GlHam. expenditure (+0.4 kcal/min, 95% confidence interval, 0.1–0.6). Meanwhile, the protocol 1:4 s GlHam showed a significantly higher increase in energy expenditure than the protocol 1:8 s GlHam (+9%). Such difference was not found between the pro- Muscle Fatigue tocol 1:4 s GlHamQuaCa and 1:8 s GlHamQuaCa (Fig. 3). As shown in Table 2, a significantly larger decrease in the The protocol with more muscles activated and the duty cycle muscle contraction size was found with a longer stimulation with a shorter rest period (1:4 s GlHamQuaCa) showed the larg- time, more muscles activated, or the duty cycle with a shorter est increase (+51%) in energy expenditure (+0.7 kcal/min, 95% rest period, respectively (main effect). However, no interaction confidence interval, 0.3–1.2), whereas the protocol with fewer effect was found. FIGURE 3. Mean energy expenditure (kcal/min) during sitting without NMES and during different NMES protocols (n = 9). *P < 0.05 compared with the mean energy expenditure during sitting without NMES; **P < 0.05 compared with the mean energy expenditure during the protocol 1:4 s GlHamQuaCa; ***P < 0.05 compared with the mean energy expenditure during the protocol 1:8 s GlHam. © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 493 Ma et al. Volume 102, Number 6, June 2023 FIGURE 4. Individual differences in energy expenditure (kcal/min) during the different NMES protocols (n = 9). Percentages indicate the three participants who have very positive increases in energy expenditure during the protocol 1:4 s GlHamQuaCa. Table 3 shows the changes in the sitting pressure variance at low frequency (1 and 3 Hz) twitches with 50 and 100 mA of gluteals and hamstrings at 3 and at 10 mins. A significantly current amplitude in 10 participants with motor complete larger decrease in the sitting pressure variance was found with SCI. Although that finding is in line with the studies that have a longer stimulation time but not with the duty cycle with a recommended using a lower frequency while providing NMES 14,27 shorter rest period (main effect). No interaction effect was found. in people with SCI, it is still somewhat surprising because the very low frequencies (1 and 3 Hz) only induced twitches without the recruitment of all the muscle fibers. One of the DISCUSSION reasons could be, as reported by Petrie et al., that some key This study showed that using NMES for paralyzed lower-limb genes associated with oxidative transcription showed a fivefold muscles in people with SCI resulted in a significant increase in to sixfold increase during the lower-frequency (5 Hz) stimula- energy expenditure compared with sitting without NMES. The tion session compared with the higher-frequency (20 Hz) ses- protocol with more muscles activated and the duty cycle with a sion in people with motor complete injury. Another reason shorter rest period showed the largest increase in energy expen- might be that utilizing a low current frequency could attenuate diture. Based on muscle contraction size and sitting pressure the process of rapid muscle fatigue during NMES, which is the variance, muscle fatigue occurred significantly with the more main obstacle that hinders the efficacy of NMES in people intense protocols, which might be caused by a lower energy ex- with SCI because the recruitment pattern of motor units by penditure in a longer protocol. NMES would likely result in slightly greater fatigue than with In this study, the protocol 1:4 s GlHamQuaCa showed the voluntary contractions. Furthermore, because the recruitment largest increase in energy expenditure. Compared with a similar of fast motor units would depend on the percentage of fast motor 17 14 study, Woelfel et al. found a much larger increase in energy units in the muscles being stimulated, individuals with a differ- expenditure by applying NMES of quadriceps and hamstrings ent training history, percentage of type II fibers, or time since TABLE 2. Mean of the muscle contraction size at 3 and 10 mins compared with the start value in different NMES protocols and the main and interaction effects of all the variables (n =9) Muscle Contraction Size (% of Start), Mean (SD) P (Main Effect) P (Interaction Effect) Protocols 3 mins 10 mins ST M DC ST MST  DC M  DC ST  M  DC 1:4 s GlHam QuaCa 58 (19) 42 (19) <0.001 0.04 <0.001 0.58 0.62 0.51 0.86 1:8 s GlHam QuaCa 76 (14) 62 (16) 1:4 s GlHam 64 (21) 46 (25) 1:8 s GlHam 86 (13) 71 (22) Gl indicates gluteals; Ham, hamstrings; Qua, quadriceps; Ca, calves; ST, stimulation time; M, muscles; DC, duty cycle. 494 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Electrical Stimulation in People With SCI TABLE 3. Mean of the sitting pressure variance at 3 and 10 mins compared with the start value in different NMES protocols and the main and interaction effects of all the variables (n =7) Sitting Pressure Variance (% of Start), Mean (SD) P (Main Effect) P (Interaction Effect) Protocols 3 mins 10 mins Stimulation Time Duty Cycle Stimulation Time  Duty Cycle 1:4 s GlHam 93 (8) 79 (22) 0.03 0.64 0.64 1:8 s GlHam 94 (6) 82 (18) Gl indicates gluteals; Ham, hamstrings. 14,32 injury may have a different time to fatigue during NMES. A duty cycle. However, because a significant decrease in muscle third reason could be the position and numbers of electrodes contraction size might cause a lower energy expenditure, this during NMES. Four electrodes per leg were adhered over the finding needs to be confirmed in a longer NMES protocol. quadriceps and hamstrings in the study of Woelfel et al., Three participants showed very positive responses, whereas whereas in this study, two electrodes per leg were adhered over others only showed limited responses to NMES, which caused quadriceps and four electrodes per leg were adhered over glu- a rather lower increase in energy expenditure on a group level teals and hamstrings together. This might cause different re- (Fig. 4). The reason for this finding might be associated with 14,25 sponses to NMES. Despite the fact that tetanic contractions the stimulation intensity. As the current amplitude was individ- were induced in this study, even in the most intense protocol, ually set to induce visible muscle contractions at comfortable clear muscle contractions were found until the end. Thus, al- levels, the stimulation intensities of the three participants men- though muscle fatigue occurred in this study, the lower-limb tioned above were overall higher than the others. Time since in- muscles might still be further stimulated to gain more potential jury might be another reason because three participants who effects after 10 mins. In a recent study, Barton et al. tested showed limited responses to NMES had a longer duration of the effects of 12 wks of daily gluteal and hamstring NMES in injury. It was reported that even oxidative slow-twitch fibers people with SCI; with 50 Hz frequency and 1:4 s duty cycle ap- transitioned to a glycolytic fast-twitch phenotype, which indi- plied, participants were able to activate the lower-limb muscles cated the decrements in muscle oxidative capacity and losses with an adapted wearable clothing garment for 6 hrs per day in fatigue resistance in people with chronic SCI. Thus, through without any adverse events and subsequently gained positive ef- the combined effects of prolonged muscle atrophy and muscle fects of increasing thigh circumference and improving the risk phenotypic shift, people with a longer duration of injury without factors for developing pressure ulcers. Besides, a recent study exercise or training might show less responses to NMES. Le- showed that by using NMES-shorts to stimulate gluteals, ham- sion completeness could hypothetically be another reason to ex- strings, and quadriceps with 35 Hz frequency and 1:4 s duty cy- plain the lower increase in energy expenditure. Except for one cle, it was feasible to activate these muscles for 8 hrs overnight participant, the other three participants with American Spinal In- and it improved participants’ sleep quality with good usability. jury Association impairment scale B showed limited responses These advantages would likely increase participants’ adherence to NMES probably because they still had some sensory func- to the NMES regimen, which is important to gain and sustain tion, and thus, a high stimulation current amplitude could not adequate long-term benefits to weight management. be utilized. Besides, it should also be noted that NMES in this Another parameter that might influence the increase in en- study was applied in NMES-untrained people, and with long- ergy expenditure during NMES is the duty cycle. Although the term training, the fatigue resistance of lower-limb muscles 1:4 s duty cycle induced a greater decline in muscle contraction could be improved, which would increase the efficacy of size, it resulted in a larger increase in energy expenditure com- NMES. pared with the 1:8 s duty cycle. Dreibati et al. reported that in To determine whether the increase in energy expenditure able-bodied adults, increasing the rest time and decreasing the is helpful for weight management, an estimation of the energy NMES frequency might be beneficial for clinical rehabilitation excess was made using the results found in a previous study. programs because it could attenuate muscle fatigue. However, It was reported that body mass increased on average by 1.36 kg that study did not compare different duty cycles. A previous each year after injury. Assuming that this gain is caused by an in- study investigated the effects of duty cycle (1:1 s vs. 1:4 s) on crease in fat mass, the surplus of energy intake is 12,240 kcal/yr the interface pressure distribution and subsequent muscle or 34 kcal/day. Thus, theoretically, when extrapolating using the fatigue during NMES-induced gluteal and hamstring activa- protocol 1:4 s GlHamQuaCa, 49 mins of daily stimulation could tion in people with SCI and concluded that the 1:4 s duty cycle presumably reach that goal for weight management, which seems was recommended because of the less fatiguing effect. That a feasible time to achieve. It should be noted, however, that this finding indicated the advantage of increasing the rest time dur- is an extrapolation based on the 10-min protocols, and longer ing NMES. Based on the results of this study, although the protocols and long-term effects of NMES should be evaluated 1:4 s duty cycle caused a significant decrease in muscle con- to determine a more accurate estimation of daily stimulation traction size, the sitting pressure variance was not significantly time. When extrapolating the estimated energy excess to the different between the 1:4 s and 1:8 s duty cycles. As clear mus- study of Woelfel et al., the efficacy (1 Hz: 1 hr/day for 203 days; cle contractions were found until the end of each protocol, the 3 Hz: 20 min/day for 305 days) was higher than the estimation 1:4 s duty cycle could be more effective because it induced a above in this study because they found a larger increase in energy higher increase in energy expenditure compared with the 1:8 s expenditure in their protocols. However, their measurement © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 495 Ma et al. Volume 102, Number 6, June 2023 protocols are shorter (6 mins), and it is unknown whether the ACKNOWLEDGMENTS status of oxygen consumption would be sustained for a longer The authors thank the rehabilitation center Reade in period. When comparing with other exercise methods to in- Amsterdam which has contributed to the organization of mea- crease energy expenditure for people with SCI, it seems obvi- surements. They also thank China Scholarship Council (CSC), ous that arm cranking (32 W, 3.62–4.12 kcal/min), weight which has supported the PhD career of the corresponding author. training (2.44–3.65 kcal/min), and functional electrical stimu- The authors appreciate the cooperation of all the participants and lated cycling (4.8 kcal/min) could induce higher levels of energy the master’s students who performed the measurements. expenditure than the protocol 1:4 s GlHamQuaCa (1.9 kcal/min) 8,12 in this study. This protocol, however, still has great potential for weight management because it is low risk, low cost, and fea- REFERENCES sible for at-home use without any transfer, and more importantly, 1. Gater DR Jr.: Obesity after spinal cord injury. Phys Med Rehabil Clin N Am 2007;18:333–51, it is not an exercise or training and could be used during other vii 2. Buchholz AC, Pencharz PB: Energy expenditure in chronic spinal cord injury. daily activities or even during the night without much interfer- 13 Curr Opin Clin Nutr Metab Care 2004;7:635–9 ence. This can be very beneficial to long-term weight manage- 3. Farkas GJ, Pitot MA, Gater DR Jr.: A systematic review of the accuracy of estimated and ment in people with SCI. measured resting metabolic rate in chronic spinal cord injury. Int J Sport Nutr Exerc Metab A limitation of this study is the small sample size (n =9). 2019;29:548–58 4. 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Spinal Cord Ser Cases ther improve the important parameters for NMES protocol, in- 2020;6:5 cluding current frequency and intensity, duty cycle, fatigue sta- 14. Dolbow DR, Holcomb WR, Gorgey AS: Improving the efficiency of electrical stimulation tus, and duration of each session. If the sample size was large activities after spinal cord injury. Curr Phys Med Rehabil Rep 2014;2:169–75 15. Spungen AM, Adkins RH, Stewart CA, et al: Factors influencing body composition in enough, some subgroups of people with SCI (eg, age, motor persons with spinal cord injury: a cross-sectional study. J Appl Physiol (1985) 2003;95: completeness, and time since injury) could be analyzed sepa- 2398–407 rately to determine the optimal NMES parameters for different 16. Gorgey AS, Dudley GA: Skeletal muscle atrophy and increased intramuscular fat after incomplete spinal cord injury. Spinal Cord 2007;45:304–9 subgroups. Measurements such as muscle volumes, perimeter, 17. Woelfel JR, Kimball AL, Yen CL, et al: Low-force muscle activity regulates energy and length of limbs could give more insight into the optimal expenditure after spinal cord injury. Med Sci Sports Exerc 2017;49:870–8 stimulation intensity of NMES for increasing energy expendi- 18. Dreibati B, Lavet C, Pinti A, et al: Influence of electrical stimulation frequency on skeletal ture in people with SCI. Besides, the training effects of NMES muscle force and fatigue. Ann Phys Rehabil Med 2010;53:266–71, 271–7 19. Smit CA, Legemate KJ, de Koning A, et al: Prolonged electrical stimulation-induced gluteal such as muscle hypertrophy and improved muscle fatigue re- and hamstring muscle activation and sitting pressure in spinal cord injury: effect of duty cycle. sistance and how long-term NMES could contribute to weight J Rehabil Res Dev 2013;50:1035–46 management in people with SCI should be investigated. 20. 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Front Integr Neurosci 2014;8:36 © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 497 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png American Journal of Physical Medicine & Rehabilitation Wolters Kluwer Health

Optimization of Protocols Using Neuromuscular Electrical Stimulation for Paralyzed Lower-Limb Muscles to Increase Energy Expenditure in People With Spinal Cord Injury

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Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc.
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Abstract

ORIGINAL RESEARCH ARTICLE Optimization of Protocols Using Neuromuscular Electrical Stimulation for Paralyzed Lower-Limb Muscles to Increase Energy Expenditure in People With Spinal Cord Injury Yiming Ma, MEd, Sonja de Groot, PhD, Ad Vink, MSc, Wouter Harmsen, PhD, Christof A.J. Smit, PhD, Janneke M. Stolwijk-Swuste, PhD, Peter J.M. Weijs, PhD, and Thomas W.J. Janssen, PhD Objective: The aim of this study was to evaluate whether using surface What Is Known neuromuscular electrical stimulation (NMES) for paralyzed lower-limb � Neuromuscular electrical stimulation (NMES) could muscles results in an increase in energy expenditure and whether the lead to a significant increase in energy expenditure number of activated muscles and duty cycle affect the potential increase. for weight management in able-bodied people. Using Design: This was a cross-sectional study. NMES to activate paralyzed lower-limb muscles for in- Results: Energy expenditure during all NMES protocols was signifi- creasing energy expenditure and subsequently weight cantly higher than the condition without NMES (1.2 ± 0.2 kcal/min), management in people with spinal cord injury has not with the highest increase (+51%; +0.7 kcal/min, 95% confidence in- been fully investigated. terval, 0.3–1.2) for the protocol with more muscles activated and the What Is New duty cycle with a shorter rest period. A significant decrease in muscle contraction size during NMES was found with a longer stimulation � Using NMES for paralyzed lower-limb muscles can sig- time, more muscles activated, or the duty cycle with a shorter rest period. nificantly increase energy expenditure with the highest Conclusion: Using NMES for paralyzed lower-limb muscles can signif- increase for the protocol with more muscles activated icantly increase energy expenditure compared with sitting without and the duty cycle with a shorter rest period (+51%). � Muscle fatigue occurred significantly with the more NMES, with the highest increase for the protocol with more muscles ac- intense NMES protocols. tivated and the duty cycle with a shorter rest period. Muscle fatigue oc- � Future studies should further optimize the NMES param- curred significantly with the more intense NMES protocols, which might eters and investigate the long-term effects of NMES. cause a lower energy expenditure in a longer protocol. Future studies should further optimize the NMES parameters and investigate the long-term effects of NMES on weight management in people with SCI. Reducing energy intake and increasing energy expendi- Key Words: Spinal Cord Injury, Neuromuscular Electrical ture or a combination are the possibilities of reaching a Stimulation, Lower-Limb Muscles, Energy Expenditure healthy energy balance. The SCI affects resting energy ex- (Am J Phys Med Rehabil 2023;102:489–497) penditure, which is markedly lower (14%–27%) in people with SCI compared with the able-bodied population. Resting energy expenditure is the greatest proportion (60%–80%) of besity is a common secondary health complication in peo- the total daily energy expenditure especially in very sedentary 3,4 O ple with spinal cord injury (SCI), with about two of every individuals. Because resting energy expenditure is low in three persons with SCI being obese and at risk for the meta- SCI, rather extreme dietary requirements, with very low energy bolic consequences of obesity. Therefore, it is necessary to reach intake, might cause a lower suboptimal protein and micronu- a healthy energy balance and prevent weight gain or achieve trient intake, resulting in a higher risk of malnutrition and weight loss, respectively, in people with SCI. subsequent health complications. The other way to achieve From the Faculty of Behavioural and Movement Sciences, Vrije Universiteit formal analysis, writing–original draft, writing–review and editing. WH: Amsterdam, Amsterdam Movement Sciences, Amsterdam (YM, SdG, AV, software, validation, resources, investigation, formal analysis, writing–original WH, TWJJ); Amsterdam Rehabilitation Research Center | Reade, Amsterdam draft, writing–review and editing. CAJS: writing–review and editing. JMS-S: (YM, SdG, CAJS, JMS-S, TWJJ); Tolbrug Rehabilitation/Jeroen Bosch Hospi- writing–review and editing. PJMW: formal analysis, data curation, writing– tal, `s Hertogenbosch (CAJS); Center of Excellence for Rehabilitation Medicine, review and editing, visualization, supervision. TWJJ: conceptualization, Brain Center Rudolf Magnus, University Medical Center Utrecht, Utrecht Uni- resources, formal analysis, data curation, writing–review and editing, versity and De Hoogstraat Rehabilitation, Utrecht (JMS-S); Faculty of Sports visualization, supervision. and Nutrition, Center of Expertise Urban Vitality, Amsterdam University of Ap- Financial disclosure statements have been obtained, and no conflicts of interest have been plied Sciences, Amsterdam (PJMW); and Department of Nutrition and Dietet- reported by the authors or by any individuals in control of the content of this article. ics, Amsterdam University Medical Centers, Vrije Universiteit Amsterdam, Supplemental digital content is available for this article. Direct URL citations appear Amsterdam Movement Sciences, Amsterdam, the Netherlands (PJMW). in the printed text and are provided in the HTML and PDF versions of this article All correspondence should be addressed to: Yiming Ma, MEd, Vrije Universiteit on the journal’s Web site (www.ajpmr.com). Amsterdam, Amsterdam Movement Sciences, Van der Boechorststraat 7, 1081 Copyright © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. This is BT Amsterdam, the Netherlands. an open-access article distributed under the terms of the Creative Commons Data availability: The datasets generated and/or analyzed during the current study are Attribution-Non Commercial-No Derivatives License 4.0 (CCBY-NC-ND), available from the corresponding author on reasonable request. where it is permissible to download and share the work provided it is properly Author contributions: YM: software, validation, formal analysis, data curation, cited. The work cannot be changed in any way or used commercially without writing–original draft, writing–review and editing, visualization. SdG: permission from the journal. methodology, formal analysis, data curation, writing–review and editing, ISSN: 0894-9115 visualization, supervision. AV: software, validation, resources, investigation, DOI: 10.1097/PHM.0000000000002120 American Journal of Physical Medicine & Rehabilitation � Volume 102, Number 6, June 2023 www.ajpmr.com 489 Ma et al. Volume 102, Number 6, June 2023 a healthy energy balance, increasing energy expenditure, might tion below the ischial tuberosity and a redistribution of sitting therefore be more rational. By participating in physical exer- pressure away from the ischial tuberosity area, which could con- 19–23 cises such as arm cranking, weight training, or wheelchair tribute to a lower sitting pressure variance. Basedonthe ra- sports, people with SCI can gain muscle mass and strength tionale of sitting pressure relief by NMES, it is expected that 6,7 and reduce fat mass. However, not all people with SCI when muscle fatigue occurs, muscle contractions will become are able or inclined to engage in physical exercise and it was less powerful and subsequently cause less reduction in sitting 18,19 also reported that the energy expenditure in response to exer- pressure variance. Because muscle fatigue can remarkably 14,24 cises could be rather limited in people with SCI, especially in reduce the efficacy of NMES, it is important to detect pos- 1,8 those with a high degree of paralysis, making it difficult siblemusclefatigue during NMES. to sufficiently increase energy expenditure using only the For able-bodied individuals, studies have shown that NMES nonparalyzed muscles. could lead to a significant increase in energy expenditure for 25,26 Activating the larger paralyzed muscles below the lesion weight management. However, using NMES to activate using surface neuromuscular electrical stimulation (NMES) paralyzed lower-limb muscles for increasing energy expendi- or functional electrical stimulation is a possible way to increase ture and, subsequently, weight management in people with SCI 17,27 energy expenditure without many practical barriers and much has not been fully investigated. The purpose of this study, discomfort. Although functional electrical stimulation–induced therefore, was to evaluate whether using NMES for paralyzed cycling and rowing have been reported to increase energy lower-limb muscles results in a significant increase in energy expenditure and muscle mass in the lower limbs in people expenditure compared with a no NMES condition and how 9,10 with SCI, some drawbacks such as the adequate time for the number of activated muscles (gluteals, hamstrings, quadri- training responses to occur and the extra set-up time and pro- ceps, and calves vs. gluteals and hamstrings only) and duty cy- fessional assistance still limit its availability and accessibility cle (1:4 s vs. 1:8 s)affectthisincrease. 11,12 in daily use. Compared with functional electrical stimu- lation, NMES is a different form of paralyzed muscle activa- METHODS tion that could be less time-consuming and could even be applied during daily activities or during the night without Participants the requirement of external equipment other than a portable 11,13 Nine men with an SCI for at least 6 mos and untrained for stimulator and electrodes. If this form of NMES-induced NMES participated in this study. Exclusion criteria were pres- contractions could lead to an increased energy expenditure, sure sores, a flaccid paralysis, a known intolerance for NMES, this method could be beneficial to long-term weight manage- a history of severe autonomic dysreflexia, or severe cognitive ment in people with SCI. or communicative disorders. This study was approved by the Different stimulation parameters such as the target muscles 14 Medical Ethical Committee of Vrije Universiteit Amsterdam and duty cycle can induce different effects. The lower-limb Medical Center (NL22712.029.08) and Reade, center for reha- muscles, including gluteals, hamstrings, quadriceps, and calves, bilitation and rheumatology. All participants signed an informed are naturally exposed to muscle atrophy owing to the loss of cen- 15,16 consent before the start of the experiments. This study conforms tral activation and immobilization after SCI. Activating these to all STROBE guidelines and reports the required information large, clinically important muscles may result in a significant 17 accordingly (see Supplementary Checklist, Supplemental Digi- increase in energy expenditure. Another important stimula- tal Content 1, http://links.lww.com/PHM/B869). tion parameter is duty cycle. Duty cycle describes the actual muscle activation and rest periods of an NMES program. The- Design oretically, duty cycle with a shorter rest period could induce There were five test conditions, including one without NMES more intense muscle contractions and subsequently contribute and four with NMES. Energy expenditure without NMES was to a higher increase in energy expenditure. However, it could measured in a resting sitting position for 5 mins before NMES also lead to greater muscle fatigue, which reduces energy ex- 18,19 protocols started. Participants received NMES during four dif- penditure and the efficacy of NMES. It is still not clear ferent 10-min protocols while sitting still on their wheelchair. what is the optimal stimulation-rest ratio to increase energy ex- The stimulated muscles were gluteals (Gl), hamstrings (Ham), penditure for people with SCI. quadriceps (Qua), and calves (Ca) vs. Gl and Ham only. The Lower-limb muscle fatigue can also influence the stimula- duty cycle was 1:4 s or 1:8 s. Energy expenditure was measured tion effects. With NMES, it was reported that selective recruit- continuously during all conditions, that is, with and without ment of the large and fast motor units would result in a more NMES. The order in which the NMES protocols were provided rapid fatigue than with voluntary exercise because the axons was randomized by simple randomization to avoid the effect of of the larger motor units have less resistance to electrical current. muscle fatigue. Muscle fatigue was measured by the changes in Thus, the predominance activation of type II fibers in people the muscle contraction size and sitting pressure variance. During with SCI during NMES could lead to greater muscle fatigue. all measurements, participants were instructed to sit as still as Relevant factors such as training history, percentage of type II fi- possible and not to speak. The placement of the electrodes for bers, time since injury, and placement of electrodes could cause 14,18 NMES is showninFigure1. a different time to fatigue during NMES. For hamstrings and quadriceps, changes in muscle contraction size, measured Electrical Stimulation by a muscle contraction sensor, can be an indicator of muscle fa- tigue. For gluteals, studies have shown that utilizing NMES to The muscles were electrically stimulated with a biphasic, activate gluteals could result in a sizeable sitting pressure reduc- squared, and balanced stimulation pattern provided by a 490 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Electrical Stimulation in People With SCI portable eight-channel stimulator (NeuroPro, Berkelbike BV, 4 mins of the resting condition (the first minute was discarded Sint-Michielsgestel, the Netherlands). To induce a tetanic mus- to allow for determining energy expenditure in a stable state) cle contraction and activate a maximum number of muscle fi- and during the last 7 mins of each NMES protocol (the first bers with less chance of skin pain, a stimulation frequency of 3 mins were discarded to allow for determining energy expen- 28,29 70 Hz and a pulse duration of 0.5 msecs were applied. Be- diture in a stable state). fore starting the actual NMES protocols, the stimulation cur- rent amplitude was determined for each participant and muscle Muscle Fatigue group separately. Current amplitude (35–120 mA) was individ- When muscles fatigue, the muscle contractions in response ually set to induce visible muscle contractions at comfortable to NMES become less powerful. A muscle contraction results levels, but low enough to prevent very strong contractions that in an increase in the muscle’s circumference compared with rest. could potentially disturb daily activity performance or even Therefore, a system was developed to monitor the changes in the force the participant out of the wheelchair. In this way, a circumference of the upper leg to evaluate the degree of fatigue of clinically relevant current level was achieved. To avoid un- the hamstrings and quadriceps during the NMES protocols. A wanted movements (knee extension) during NMES, the feet Futek load cell (LSB200, 25 lb, JR S-beam load cell), measuring were fixed to the footrests of the wheelchair with a Velcro strap. forces in one direction during rest and muscle contractions, was The duration of each NMES protocol was 10 mins, followed by integrated into a Velcro strap with an elastic end and placed a 10-min rest. around the right upper leg (Fig. 1, right). When muscles contract because of NMES, the upper-leg muscle circumference in- Energy Expenditure creases as the muscles become shorter and thicker, and the elas- The primary outcome in this study was the energy expen- tic part will be more elongated, resulting in a force difference on diture calculated from the oxygen consumption (VO )and car- the load cell. With muscle fatigue negatively affecting muscle bon dioxide production (VCO ) gatheredwithanon-line gas contractions, a less pronounced change in muscle circumfer- analysis system (Oxycon alpha, Mijnhardt BV, Bunnik, the ence and, subsequently, a smaller force difference will occur. Netherlands). Gas and volume calibration was performed be- The data were obtained with a data acquisition system of Na- fore each measurement. All the measurements were done un- tional Instruments (NI USB-6009 DAQ) and LabView software der the same conditions. The energy expenditure in kcal/min (Student Edition 8.2). was calculated using the Weir equation. A second parameter to estimate fatigue of the gluteals and Energy expenditure (kcal/min) = 3.94 VO +1.11 VCO hamstrings was sitting pressure variance, measured using a 2 2 With Matlab software (R2018b), mean energy expendi- pressure mapping system (mFLEX, Vista Medical, Canada). ture was calculated for rest without NMES during the last This system measures the pressure of an area of 533  533 mm FIGURE 1. The placement of the electrodes for gluteals, hamstrings (electrodes with solid outline, left), calves (electrodes with dashed outline, left) stimulation and for quadriceps stimulation (electrodes with dashed outline, right) and the contraction sensor (right). © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 491 Ma et al. Volume 102, Number 6, June 2023 with a total of 1024 (32 32) pressure sensors and was placed on changes in muscle contraction size and sitting pressure variance the cushion of the participant’s wheelchair. During a during the NMES protocols. nonactive period, most pressure will be located around the buttocks. When the gluteals and hamstrings contract, the total Statistical Analysis pressure will be more distributed to the surrounding area and The normality of the data was checked by Shapiro-Wilk will therefore result in a lower pressure variance during an acti- tests and Q-Q plots and all data were normally distributed (or vation period than in rest. Fatigue will make the muscle con- approximately). Repeated-measures analysis of variance to- tractions less powerful, resulting in less pronounced changes of gether with post hoc tests was used to check the systematic pressure distribution and therefore less decrease in pressure vari- differences between (1) energy expenditure without and with ance. This method was applied only for the protocols with gluteal NMES during all protocols; (2) energy expenditure with NMES and hamstring activation because activation of quadriceps and in different protocols; (3) the muscle contraction size during all calves lifts the legs and has a disruptive effect on sitting pressure protocols and the interaction effects (2  2  2, stimulation variance. With Matlab software, the changes in sitting pressure time, muscles and duty cycle); and (4) the sitting pressure vari- variance were analyzed. ance during the 1:4 s GlHam and 1:8 s GlHam protocols and The measurements of muscle contraction size and sitting the interaction effects (2  2, stimulation time, duty cycle). pressure variance were started at least 1 min before the first All statistical analyses were performed using SPSS software NMES protocol started. The start and end time of each NMES (version 25, IBM, Somers, NY). A P value <0.05 was consid- protocol was recorded. The raw force data were filtered with a ered significant. second-order Butterworth band-pass filter (0.05–0.8 Hz). Matlab software was used to further analyze the data. For muscle RESULTS contraction size, all the peak and valley values of force in each protocol were determined at first. The peak values right before the valley values were then selected to calculate the Descriptives force differences between them. The force differences were used Table 1 shows the descriptives of all participants. Because -bx -ed to make a general fit exponential model with y = ae + c of measurement errors, the sitting pressure variance data of two function to check the values at specific time. Subsequently, participants were removed for analysis. the force differences at the start (5 s) and at 3 and at 10 mins in each NMES protocol were determined. A higher force differ- Changes in Energy Expenditure Among ence was associated with a larger change in muscle contraction Different Protocols size. Percentages of the difference at 3 and 10 mins relative to Energy expenditure (kcal/min) with or without NMES is the start value were calculated to indicate the changes in muscle shown in Figure 3. All NMES protocols resulted in a significant contraction size. increase in energy expenditure (1:4 s GlHamQuaCa: +51%; Similarly, all the peak and valley values of sitting pressure 1:8 s GlHamQuaCa: +44%; 1:4 s GlHam: +36%; 1:8 s GlHam: variance in each protocol were determined and the differences +25%) compared with the energy expenditure without NMES between them were used to make a general fit exponential -bx -ed (1.2 ± 0.2 kcal/min). Three participants showed a very positive model with y = ae + c function to check the values at spe- increase in energy expenditure compared with other partici- cific time. Subsequently, these differences at the start (5 s) and pants, with the highest increase (+106%, +171%, and +55%) at 3 and at 10 mins in each NMES protocol were determined. A during the protocol 1:4 s GlHamQuaCa (Fig. 4). When comparing higher difference was associated with a higher decrease in pres- between different protocols, the protocol 1:4 s GlHamQuaCa sure variance. Percentages of the difference at 3 and 10 mins rel- and 1:8 s GlHamQuaCa with more muscles activated showed a ative to the start value were calculated to indicate the changes in sitting pressure variance. Figure 2 shows the examples of the significantly higher increase in energy expenditure compared FIGURE 2. Examples of the changes in muscle contraction size (left, participant 4) and sitting pressure variance (right, participant 3) during NMES -bx -ed protocols. Lines are fit through the data by a general fit exponential model with y = ae + c function. Most of the participants showed similar trends as illustrated above. 492 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Electrical Stimulation in People With SCI TABLE 1. Descriptives of participants (n =9) Current Amplitude Participant Age, y Body Mass, kg Height, m Time Since Injury, yrs Lesion Level AIS Gl Ham, mA Qua, mA Ca, mA 158 86 1.85 1.5 C3–4 B 120 100 100 2 31 63 1.75 9 C5 A 90 80 90 349 63 1.87 22 C5–6 A 60 90 50 4 24 80 1.91 8 C6 B 75 90 70 541 81 1.70 14 C6–7 B 40 50 35 631 70 1.80 5 C7–8 A 60 60 40 728 92 1.86 4 T3–4 A 70 70 65 8 66 120 1.73 4 T9 B 50 40 45 9 29 73 1.84 11 T11 A 45 60 60 Mean (SD) 40 (15) 81 (18) 1.81 (0.71) 9 (6) 68 (25) 71 (20) 62 (22) Lesion level: C, cervical; T, thoracic. AIS indicates American Spinal Injury Association impairment scale; Gl, gluteals; Ham, hamstrings; Qua, quadriceps; Ca, calves. with the protocol 1:4 s GlHam (+11%) and 1:8 s GlHam muscles activated and the duty cycle with a longer rest period (+15%), respectively. However, no significant difference was (1:8 s GlHam) showed the smallest increase (+25%) in energy found between the protocol 1:8 s GlHamQuaCa and 1:4 s GlHam. expenditure (+0.4 kcal/min, 95% confidence interval, 0.1–0.6). Meanwhile, the protocol 1:4 s GlHam showed a significantly higher increase in energy expenditure than the protocol 1:8 s GlHam (+9%). Such difference was not found between the pro- Muscle Fatigue tocol 1:4 s GlHamQuaCa and 1:8 s GlHamQuaCa (Fig. 3). As shown in Table 2, a significantly larger decrease in the The protocol with more muscles activated and the duty cycle muscle contraction size was found with a longer stimulation with a shorter rest period (1:4 s GlHamQuaCa) showed the larg- time, more muscles activated, or the duty cycle with a shorter est increase (+51%) in energy expenditure (+0.7 kcal/min, 95% rest period, respectively (main effect). However, no interaction confidence interval, 0.3–1.2), whereas the protocol with fewer effect was found. FIGURE 3. Mean energy expenditure (kcal/min) during sitting without NMES and during different NMES protocols (n = 9). *P < 0.05 compared with the mean energy expenditure during sitting without NMES; **P < 0.05 compared with the mean energy expenditure during the protocol 1:4 s GlHamQuaCa; ***P < 0.05 compared with the mean energy expenditure during the protocol 1:8 s GlHam. © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 493 Ma et al. Volume 102, Number 6, June 2023 FIGURE 4. Individual differences in energy expenditure (kcal/min) during the different NMES protocols (n = 9). Percentages indicate the three participants who have very positive increases in energy expenditure during the protocol 1:4 s GlHamQuaCa. Table 3 shows the changes in the sitting pressure variance at low frequency (1 and 3 Hz) twitches with 50 and 100 mA of gluteals and hamstrings at 3 and at 10 mins. A significantly current amplitude in 10 participants with motor complete larger decrease in the sitting pressure variance was found with SCI. Although that finding is in line with the studies that have a longer stimulation time but not with the duty cycle with a recommended using a lower frequency while providing NMES 14,27 shorter rest period (main effect). No interaction effect was found. in people with SCI, it is still somewhat surprising because the very low frequencies (1 and 3 Hz) only induced twitches without the recruitment of all the muscle fibers. One of the DISCUSSION reasons could be, as reported by Petrie et al., that some key This study showed that using NMES for paralyzed lower-limb genes associated with oxidative transcription showed a fivefold muscles in people with SCI resulted in a significant increase in to sixfold increase during the lower-frequency (5 Hz) stimula- energy expenditure compared with sitting without NMES. The tion session compared with the higher-frequency (20 Hz) ses- protocol with more muscles activated and the duty cycle with a sion in people with motor complete injury. Another reason shorter rest period showed the largest increase in energy expen- might be that utilizing a low current frequency could attenuate diture. Based on muscle contraction size and sitting pressure the process of rapid muscle fatigue during NMES, which is the variance, muscle fatigue occurred significantly with the more main obstacle that hinders the efficacy of NMES in people intense protocols, which might be caused by a lower energy ex- with SCI because the recruitment pattern of motor units by penditure in a longer protocol. NMES would likely result in slightly greater fatigue than with In this study, the protocol 1:4 s GlHamQuaCa showed the voluntary contractions. Furthermore, because the recruitment largest increase in energy expenditure. Compared with a similar of fast motor units would depend on the percentage of fast motor 17 14 study, Woelfel et al. found a much larger increase in energy units in the muscles being stimulated, individuals with a differ- expenditure by applying NMES of quadriceps and hamstrings ent training history, percentage of type II fibers, or time since TABLE 2. Mean of the muscle contraction size at 3 and 10 mins compared with the start value in different NMES protocols and the main and interaction effects of all the variables (n =9) Muscle Contraction Size (% of Start), Mean (SD) P (Main Effect) P (Interaction Effect) Protocols 3 mins 10 mins ST M DC ST MST  DC M  DC ST  M  DC 1:4 s GlHam QuaCa 58 (19) 42 (19) <0.001 0.04 <0.001 0.58 0.62 0.51 0.86 1:8 s GlHam QuaCa 76 (14) 62 (16) 1:4 s GlHam 64 (21) 46 (25) 1:8 s GlHam 86 (13) 71 (22) Gl indicates gluteals; Ham, hamstrings; Qua, quadriceps; Ca, calves; ST, stimulation time; M, muscles; DC, duty cycle. 494 www.ajpmr.com © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. Volume 102, Number 6, June 2023 Electrical Stimulation in People With SCI TABLE 3. Mean of the sitting pressure variance at 3 and 10 mins compared with the start value in different NMES protocols and the main and interaction effects of all the variables (n =7) Sitting Pressure Variance (% of Start), Mean (SD) P (Main Effect) P (Interaction Effect) Protocols 3 mins 10 mins Stimulation Time Duty Cycle Stimulation Time  Duty Cycle 1:4 s GlHam 93 (8) 79 (22) 0.03 0.64 0.64 1:8 s GlHam 94 (6) 82 (18) Gl indicates gluteals; Ham, hamstrings. 14,32 injury may have a different time to fatigue during NMES. A duty cycle. However, because a significant decrease in muscle third reason could be the position and numbers of electrodes contraction size might cause a lower energy expenditure, this during NMES. Four electrodes per leg were adhered over the finding needs to be confirmed in a longer NMES protocol. quadriceps and hamstrings in the study of Woelfel et al., Three participants showed very positive responses, whereas whereas in this study, two electrodes per leg were adhered over others only showed limited responses to NMES, which caused quadriceps and four electrodes per leg were adhered over glu- a rather lower increase in energy expenditure on a group level teals and hamstrings together. This might cause different re- (Fig. 4). The reason for this finding might be associated with 14,25 sponses to NMES. Despite the fact that tetanic contractions the stimulation intensity. As the current amplitude was individ- were induced in this study, even in the most intense protocol, ually set to induce visible muscle contractions at comfortable clear muscle contractions were found until the end. Thus, al- levels, the stimulation intensities of the three participants men- though muscle fatigue occurred in this study, the lower-limb tioned above were overall higher than the others. Time since in- muscles might still be further stimulated to gain more potential jury might be another reason because three participants who effects after 10 mins. In a recent study, Barton et al. tested showed limited responses to NMES had a longer duration of the effects of 12 wks of daily gluteal and hamstring NMES in injury. It was reported that even oxidative slow-twitch fibers people with SCI; with 50 Hz frequency and 1:4 s duty cycle ap- transitioned to a glycolytic fast-twitch phenotype, which indi- plied, participants were able to activate the lower-limb muscles cated the decrements in muscle oxidative capacity and losses with an adapted wearable clothing garment for 6 hrs per day in fatigue resistance in people with chronic SCI. Thus, through without any adverse events and subsequently gained positive ef- the combined effects of prolonged muscle atrophy and muscle fects of increasing thigh circumference and improving the risk phenotypic shift, people with a longer duration of injury without factors for developing pressure ulcers. Besides, a recent study exercise or training might show less responses to NMES. Le- showed that by using NMES-shorts to stimulate gluteals, ham- sion completeness could hypothetically be another reason to ex- strings, and quadriceps with 35 Hz frequency and 1:4 s duty cy- plain the lower increase in energy expenditure. Except for one cle, it was feasible to activate these muscles for 8 hrs overnight participant, the other three participants with American Spinal In- and it improved participants’ sleep quality with good usability. jury Association impairment scale B showed limited responses These advantages would likely increase participants’ adherence to NMES probably because they still had some sensory func- to the NMES regimen, which is important to gain and sustain tion, and thus, a high stimulation current amplitude could not adequate long-term benefits to weight management. be utilized. Besides, it should also be noted that NMES in this Another parameter that might influence the increase in en- study was applied in NMES-untrained people, and with long- ergy expenditure during NMES is the duty cycle. Although the term training, the fatigue resistance of lower-limb muscles 1:4 s duty cycle induced a greater decline in muscle contraction could be improved, which would increase the efficacy of size, it resulted in a larger increase in energy expenditure com- NMES. pared with the 1:8 s duty cycle. Dreibati et al. reported that in To determine whether the increase in energy expenditure able-bodied adults, increasing the rest time and decreasing the is helpful for weight management, an estimation of the energy NMES frequency might be beneficial for clinical rehabilitation excess was made using the results found in a previous study. programs because it could attenuate muscle fatigue. However, It was reported that body mass increased on average by 1.36 kg that study did not compare different duty cycles. A previous each year after injury. Assuming that this gain is caused by an in- study investigated the effects of duty cycle (1:1 s vs. 1:4 s) on crease in fat mass, the surplus of energy intake is 12,240 kcal/yr the interface pressure distribution and subsequent muscle or 34 kcal/day. Thus, theoretically, when extrapolating using the fatigue during NMES-induced gluteal and hamstring activa- protocol 1:4 s GlHamQuaCa, 49 mins of daily stimulation could tion in people with SCI and concluded that the 1:4 s duty cycle presumably reach that goal for weight management, which seems was recommended because of the less fatiguing effect. That a feasible time to achieve. It should be noted, however, that this finding indicated the advantage of increasing the rest time dur- is an extrapolation based on the 10-min protocols, and longer ing NMES. Based on the results of this study, although the protocols and long-term effects of NMES should be evaluated 1:4 s duty cycle caused a significant decrease in muscle con- to determine a more accurate estimation of daily stimulation traction size, the sitting pressure variance was not significantly time. When extrapolating the estimated energy excess to the different between the 1:4 s and 1:8 s duty cycles. As clear mus- study of Woelfel et al., the efficacy (1 Hz: 1 hr/day for 203 days; cle contractions were found until the end of each protocol, the 3 Hz: 20 min/day for 305 days) was higher than the estimation 1:4 s duty cycle could be more effective because it induced a above in this study because they found a larger increase in energy higher increase in energy expenditure compared with the 1:8 s expenditure in their protocols. However, their measurement © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 495 Ma et al. Volume 102, Number 6, June 2023 protocols are shorter (6 mins), and it is unknown whether the ACKNOWLEDGMENTS status of oxygen consumption would be sustained for a longer The authors thank the rehabilitation center Reade in period. When comparing with other exercise methods to in- Amsterdam which has contributed to the organization of mea- crease energy expenditure for people with SCI, it seems obvi- surements. They also thank China Scholarship Council (CSC), ous that arm cranking (32 W, 3.62–4.12 kcal/min), weight which has supported the PhD career of the corresponding author. training (2.44–3.65 kcal/min), and functional electrical stimu- The authors appreciate the cooperation of all the participants and lated cycling (4.8 kcal/min) could induce higher levels of energy the master’s students who performed the measurements. expenditure than the protocol 1:4 s GlHamQuaCa (1.9 kcal/min) 8,12 in this study. 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Front Integr Neurosci 2014;8:36 © 2022 The Author(s). Published by Wolters Kluwer Health, Inc. www.ajpmr.com 497

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