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Published in: BMC Neurology 1/2018

Open Access 01-12-2018 | Research article

Effect of tendon vibration during wide-pulse neuromuscular electrical stimulation (NMES) on muscle force production in people with spinal cord injury (SCI)

Authors: Vanesa Bochkezanian, Robert U. Newton, Gabriel S. Trajano, Amilton Vieira, Timothy S. Pulverenti, Anthony J. Blazevich

Published in: BMC Neurology | Issue 1/2018

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Abstract

Background

Neuromuscular electrical stimulation (NMES) is commonly used in skeletal muscles in people with spinal cord injury (SCI) with the aim of increasing muscle recruitment and thus muscle force production. NMES has been conventionally used in clinical practice as functional electrical stimulation (FES), using low levels of evoked force that cannot optimally stimulate muscular strength and mass improvements, and thus trigger musculoskeletal changes in paralysed muscles. The use of high intensity intermittent NMES training using wide-pulse width and moderate-intensity as a strength training tool could be a promising method to increase muscle force production in people with SCI. However, this type of protocol has not been clinically adopted because it may generate rapid muscle fatigue and thus prevent the performance of repeated high-intensity muscular contractions in paralysed muscles. Moreover, superimposing patellar tendon vibration onto the wide-pulse width NMES has been shown to elicit further increases in impulse or, at least, reduce the rate of fatigue in repeated contractions in able-bodied populations, but there is a lack of evidence to support this argument in people with SCI.

Methods

Nine people with SCI received two NMES protocols with and without superimposing patellar tendon vibration on different days (i.e. STIM and STIM+vib), which consisted of repeated 30 Hz trains of 58 wide-pulse width (1000 μs) symmetric biphasic pulses (0.033-s inter-pulse interval; 2 s stimulation train; 2-s inter-train interval) being delivered to the dominant quadriceps femoris. Starting torque was 20% of maximal doublet-twitch torque and stimulations continued until torque declined to 50% of the starting torque. Total knee extensor impulse was calculated as the primary outcome variable.

Results

Total knee extensor impulse increased in four subjects when patellar tendon vibration was imposed (59.2 ± 15.8%) but decreased in five subjects (− 31.3 ± 25.7%). However, there were no statistically significant differences between these sub-groups or between conditions when the data were pooled.

Conclusions

Based on the present results there is insufficient evidence to conclude that patellar tendon vibration provides a clear benefit to muscle force production or delays muscle fatigue during wide-pulse width, moderate-intensity NMES in people with SCI.

Trial registration

ACTRN12618000022​268. Date: 11/01/2018. Retrospectively registered.
Literature
1.
go back to reference Tewarie RDS, Hurtado A, Bartels RHMA, Grotenhuis JA, Oudega M. A clinical perspective of spinal cord injury. Neurorehabil. 2010;27(2):129–39. Tewarie RDS, Hurtado A, Bartels RHMA, Grotenhuis JA, Oudega M. A clinical perspective of spinal cord injury. Neurorehabil. 2010;27(2):129–39.
2.
go back to reference Oyster ML, Karmarkar AM, Patrick M, Read MS, Nicolini L, Boninger ML. Investigation of factors associated with manual wheelchair mobility in persons with spinal cord injury. Arch of Phys Med and Rehab. 2011;92(3):484–90.CrossRef Oyster ML, Karmarkar AM, Patrick M, Read MS, Nicolini L, Boninger ML. Investigation of factors associated with manual wheelchair mobility in persons with spinal cord injury. Arch of Phys Med and Rehab. 2011;92(3):484–90.CrossRef
3.
go back to reference Hosseini SM, Oyster ML, Kirby RL, Harrington AL, Boninger ML. Manual wheelchair skills capacity predicts quality of life and community integration in persons with spinal cord injury. Arch of Phys Med and Rehab. 2012;93(12):2237–43.CrossRef Hosseini SM, Oyster ML, Kirby RL, Harrington AL, Boninger ML. Manual wheelchair skills capacity predicts quality of life and community integration in persons with spinal cord injury. Arch of Phys Med and Rehab. 2012;93(12):2237–43.CrossRef
4.
go back to reference Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB, Newman AB, et al. Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci. 2009;64((11):1183–9.CrossRef Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB, Newman AB, et al. Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci. 2009;64((11):1183–9.CrossRef
6.
go back to reference Orlando G, Balducci S, Bazzucchi I, Pugliese G, Sacchetti M. Neuromuscular dysfunction in type 2 diabetes: underlying mechanisms and effect of resistance training. Diabetes-Metab Res Rev. 2016;32(1):40–50.CrossRefPubMed Orlando G, Balducci S, Bazzucchi I, Pugliese G, Sacchetti M. Neuromuscular dysfunction in type 2 diabetes: underlying mechanisms and effect of resistance training. Diabetes-Metab Res Rev. 2016;32(1):40–50.CrossRefPubMed
7.
go back to reference Andrade SD, da Silva JN. The effects of resistance training in osteoporosis: a systematic review. RBNE. 2015;9(50):144–9. Andrade SD, da Silva JN. The effects of resistance training in osteoporosis: a systematic review. RBNE. 2015;9(50):144–9.
8.
go back to reference Clark JE, Goon DT. The role of resistance training for treatment of obesity related health issues and for changing health status of the individual who is overfat or obese: a review. J Sports Med Phys Fitness. 2015;55(3):205–22.PubMed Clark JE, Goon DT. The role of resistance training for treatment of obesity related health issues and for changing health status of the individual who is overfat or obese: a review. J Sports Med Phys Fitness. 2015;55(3):205–22.PubMed
9.
go back to reference Caserotti P, Aagaard P, Larsen JB, Puggaard L. Explosive heavy-resistance training in old and very old adults: changes in rapid muscle force, strength and power. Scand J Med Sci Sports. 2008;18(6):773–82.CrossRefPubMed Caserotti P, Aagaard P, Larsen JB, Puggaard L. Explosive heavy-resistance training in old and very old adults: changes in rapid muscle force, strength and power. Scand J Med Sci Sports. 2008;18(6):773–82.CrossRefPubMed
10.
go back to reference Barbeau H, Ladouceur M, Mirbagheri MM, Kearney RE. The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies. Brain Res. 2002;40(1–3):274–91.CrossRef Barbeau H, Ladouceur M, Mirbagheri MM, Kearney RE. The effect of locomotor training combined with functional electrical stimulation in chronic spinal cord injured subjects: walking and reflex studies. Brain Res. 2002;40(1–3):274–91.CrossRef
11.
go back to reference Harvey LA, Fornusek C, Bowden JL, Pontifex N, Glinsky J, Middleton JW, et al. Electrical stimulation plus progressive resistance training for leg strength in spinal cord injury: a randomized controlled trial. Spinal Cord. 2010;48(7):570–5.CrossRefPubMed Harvey LA, Fornusek C, Bowden JL, Pontifex N, Glinsky J, Middleton JW, et al. Electrical stimulation plus progressive resistance training for leg strength in spinal cord injury: a randomized controlled trial. Spinal Cord. 2010;48(7):570–5.CrossRefPubMed
12.
go back to reference Thrasher TA, Ward JS, Fisher S. Strength and endurance adaptations to functional electrical stimulation leg cycle ergometry in spinal cord injury. Neurorehabil. 2013;33(1):133–8. Thrasher TA, Ward JS, Fisher S. Strength and endurance adaptations to functional electrical stimulation leg cycle ergometry in spinal cord injury. Neurorehabil. 2013;33(1):133–8.
13.
go back to reference American College of Sports Medicine. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2009;41(3):687–708.CrossRef American College of Sports Medicine. Progression models in resistance training for healthy adults. Med Sci Sports Exerc. 2009;41(3):687–708.CrossRef
14.
go back to reference Ahtiainen JP, Pakarinen A, Alen M, Kraemer WJ, Hakkinen K. Muscle hypertrophy, hormonal adaptations and strength development during strength training in strength-trained and untrained men. Eur J Appl Physiol. 2003;89(6):555–63.CrossRefPubMed Ahtiainen JP, Pakarinen A, Alen M, Kraemer WJ, Hakkinen K. Muscle hypertrophy, hormonal adaptations and strength development during strength training in strength-trained and untrained men. Eur J Appl Physiol. 2003;89(6):555–63.CrossRefPubMed
15.
go back to reference Enoka R. Neuromechanics of human movement 2002. Enoka R. Neuromechanics of human movement 2002.
17.
go back to reference Alon G. Guest editorial - Use of neuromuscular electrical stimulation in neureorehabilitation: A challenge to all. J Rehabil Res Dev. 2003;40(6):IX–XII.CrossRefPubMed Alon G. Guest editorial - Use of neuromuscular electrical stimulation in neureorehabilitation: A challenge to all. J Rehabil Res Dev. 2003;40(6):IX–XII.CrossRefPubMed
18.
go back to reference Hillegass EA, Dudley GA. Surface electrical stimulation of skeletal muscle after spinal cord injury. Spinal Cord. 1999;37(4):251–7.CrossRefPubMed Hillegass EA, Dudley GA. Surface electrical stimulation of skeletal muscle after spinal cord injury. Spinal Cord. 1999;37(4):251–7.CrossRefPubMed
19.
go back to reference Gregory CM, Recruitment BCS. Patterns in human skeletal muscle during electrical stimulation. Phys Ther. 2005;85(4):358–64.PubMed Gregory CM, Recruitment BCS. Patterns in human skeletal muscle during electrical stimulation. Phys Ther. 2005;85(4):358–64.PubMed
20.
go back to reference Gorgey AS, Mahoney E, Kendall T, Dudley GA. Effects of neuromuscular electrical stimulation parameters on specific tension. Eur J Appl Physiol. 2006;97(6):737–44.CrossRefPubMed Gorgey AS, Mahoney E, Kendall T, Dudley GA. Effects of neuromuscular electrical stimulation parameters on specific tension. Eur J Appl Physiol. 2006;97(6):737–44.CrossRefPubMed
21.
go back to reference Ibitoye MO, Hamzaid NA, Hasnan N, Abdul Wahab AK, Davis GM. Strategies for rapid muscle fatigue reduction during fes exercise in individuals with spinal cord injury: a systematic review. PLoS One. 2016;11(2):e0149024.CrossRefPubMedPubMedCentral Ibitoye MO, Hamzaid NA, Hasnan N, Abdul Wahab AK, Davis GM. Strategies for rapid muscle fatigue reduction during fes exercise in individuals with spinal cord injury: a systematic review. PLoS One. 2016;11(2):e0149024.CrossRefPubMedPubMedCentral
22.
go back to reference Bickel CS, Gregory CM, Dean JC. Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal. Eur J Appl Physiol. 2011;111(10):2399–407.CrossRefPubMed Bickel CS, Gregory CM, Dean JC. Motor unit recruitment during neuromuscular electrical stimulation: a critical appraisal. Eur J Appl Physiol. 2011;111(10):2399–407.CrossRefPubMed
23.
go back to reference Bickel CS, Slade JM, VanHiel LR, Warren GL, Dudley GA. Variable-frequency-train stimulation of skeletal muscle after spinal cord injury. J Rehabil Res Dev. 2004;41(1):33–40.CrossRefPubMed Bickel CS, Slade JM, VanHiel LR, Warren GL, Dudley GA. Variable-frequency-train stimulation of skeletal muscle after spinal cord injury. J Rehabil Res Dev. 2004;41(1):33–40.CrossRefPubMed
24.
go back to reference Adams GR, Harris RT, Woodard D, Dudley GA. Mapping of electrical muscle stimulation using MRI. J Appl Physiol. 1993;74(2):532–7.CrossRefPubMed Adams GR, Harris RT, Woodard D, Dudley GA. Mapping of electrical muscle stimulation using MRI. J Appl Physiol. 1993;74(2):532–7.CrossRefPubMed
25.
go back to reference Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R. Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord. 1997;35(2):86–91.CrossRefPubMed Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R. Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord. 1997;35(2):86–91.CrossRefPubMed
26.
go back to reference Pelletier CA, Hicks AL. Muscle fatigue characteristics in paralyzed muscle after spinal cord injury. Spinal Cord. 2011;49(1):125–30.CrossRefPubMed Pelletier CA, Hicks AL. Muscle fatigue characteristics in paralyzed muscle after spinal cord injury. Spinal Cord. 2011;49(1):125–30.CrossRefPubMed
27.
go back to reference Karu ZZ, Durfee WK, Barzilai AM. Reducing muscle fatigue in fes applications by stimulating with N-let pulse trains. IEEE Trans Biomed Eng. 1995;42(8):809–17.CrossRefPubMed Karu ZZ, Durfee WK, Barzilai AM. Reducing muscle fatigue in fes applications by stimulating with N-let pulse trains. IEEE Trans Biomed Eng. 1995;42(8):809–17.CrossRefPubMed
28.
go back to reference Gorgey AS, Poarch HJ, Dolbow DR, Castillo T, Gater DR. Effect of adjusting pulse durations of functional electrical stimulation cycling on energy expenditure and fatigue after spinal cord injury. J Rehab Res Dev. 2014;51(9):1455–68.CrossRef Gorgey AS, Poarch HJ, Dolbow DR, Castillo T, Gater DR. Effect of adjusting pulse durations of functional electrical stimulation cycling on energy expenditure and fatigue after spinal cord injury. J Rehab Res Dev. 2014;51(9):1455–68.CrossRef
29.
go back to reference Borde R, Hortobagyi T, Granacher U. Dose-response relationships of resistance training in healthy old adults: a systematic review and meta-analysis. Sports Med. 2015;45(12):1693–720.CrossRefPubMedPubMedCentral Borde R, Hortobagyi T, Granacher U. Dose-response relationships of resistance training in healthy old adults: a systematic review and meta-analysis. Sports Med. 2015;45(12):1693–720.CrossRefPubMedPubMedCentral
30.
go back to reference Schoenfeld BJ, Ogborn D, Krieger JW. Dose-response relationship between weekly resistance training volume and increases in muscle mass: a systematic review and meta-analysis. J Sports Sci. 2017;35(11):1073–82.CrossRefPubMed Schoenfeld BJ, Ogborn D, Krieger JW. Dose-response relationship between weekly resistance training volume and increases in muscle mass: a systematic review and meta-analysis. J Sports Sci. 2017;35(11):1073–82.CrossRefPubMed
31.
go back to reference Bickel CS, Yarar-Fisher C, Mahoney ET, McCully KK. Neuromuscular electrical stimulation–induced resistance training after SCI: a review of the Dudley protocol. Top Spinal Cord Inj Rehabil. 2015;21(4):294–302.CrossRefPubMedPubMedCentral Bickel CS, Yarar-Fisher C, Mahoney ET, McCully KK. Neuromuscular electrical stimulation–induced resistance training after SCI: a review of the Dudley protocol. Top Spinal Cord Inj Rehabil. 2015;21(4):294–302.CrossRefPubMedPubMedCentral
32.
go back to reference Dudley GA, Castro MJ, Rogers S, Apple DF. A simple means of increasing muscle size after spinal cord injury: a pilot study. Eur J Appl Physiol Occup Physiol. 1999;80(4):394–6.CrossRefPubMed Dudley GA, Castro MJ, Rogers S, Apple DF. A simple means of increasing muscle size after spinal cord injury: a pilot study. Eur J Appl Physiol Occup Physiol. 1999;80(4):394–6.CrossRefPubMed
33.
go back to reference Gorgey AS, Mather KJ, Cupp HR, Gater DR. Effects of resistance training on adiposity and metabolism after spinal cord injury. Med Sci Sports Exerc. 2012;44(1):165–74.CrossRefPubMed Gorgey AS, Mather KJ, Cupp HR, Gater DR. Effects of resistance training on adiposity and metabolism after spinal cord injury. Med Sci Sports Exerc. 2012;44(1):165–74.CrossRefPubMed
34.
go back to reference Mahoney ET, Bickel CS, Elder C, Black C, Slade JM, Apple D, et al. Changes in skeletal muscle size and glucose tolerance with electrically stimulated resistance training in subjects with chronic spinal cord injury. Arch Phys Med Rehabil. 2005;86(7):1502–4.CrossRefPubMed Mahoney ET, Bickel CS, Elder C, Black C, Slade JM, Apple D, et al. Changes in skeletal muscle size and glucose tolerance with electrically stimulated resistance training in subjects with chronic spinal cord injury. Arch Phys Med Rehabil. 2005;86(7):1502–4.CrossRefPubMed
35.
go back to reference Erickson ML, Ryan TE, Backus D, McCully KK. Endurance neuromuscular electrical stimulation training improves skeletal muscle oxidative capacity in individuals with motor-complete spinal cord injury. Muscle Nerve. 2017;55(5):669–75. Erickson ML, Ryan TE, Backus D, McCully KK. Endurance neuromuscular electrical stimulation training improves skeletal muscle oxidative capacity in individuals with motor-complete spinal cord injury. Muscle Nerve. 2017;55(5):669–75.
36.
go back to reference Dudley-Javoroski S. Muscle and bone plasticity after spinal cord injury: review of adaptations to disuse and to electrical muscle stimulation. J Rehabil Res Dev. 2008;45(2):283–96.CrossRefPubMedPubMedCentral Dudley-Javoroski S. Muscle and bone plasticity after spinal cord injury: review of adaptations to disuse and to electrical muscle stimulation. J Rehabil Res Dev. 2008;45(2):283–96.CrossRefPubMedPubMedCentral
37.
go back to reference Hangartner TN, Rodgers MM, Glaser RM, Barre PS. Tibial bone density loss in spinal cord injured patients: effects of FES exercise. J Rehabil Res Dev. 1994;31(1):50–61.PubMed Hangartner TN, Rodgers MM, Glaser RM, Barre PS. Tibial bone density loss in spinal cord injured patients: effects of FES exercise. J Rehabil Res Dev. 1994;31(1):50–61.PubMed
38.
go back to reference Shields RK, Dudley-Javoroski S, Law LA. Electrically induced muscle contractions influence bone density decline after spinal cord injury. Spine. 2006;31(5):548–53.CrossRefPubMedPubMedCentral Shields RK, Dudley-Javoroski S, Law LA. Electrically induced muscle contractions influence bone density decline after spinal cord injury. Spine. 2006;31(5):548–53.CrossRefPubMedPubMedCentral
39.
go back to reference Glinsky J, Harvey L, Van Es P. Efficacy of electrical stimulation to increase muscle strength in people with neurological conditions: a systematic review. Physiother Res Int. 2007;12(3):175–94.CrossRefPubMed Glinsky J, Harvey L, Van Es P. Efficacy of electrical stimulation to increase muscle strength in people with neurological conditions: a systematic review. Physiother Res Int. 2007;12(3):175–94.CrossRefPubMed
40.
go back to reference Harvey LA. Physiotherapy rehabilitation for people with spinal cord injuries. J Physiother. 2016;62(1):4–11.CrossRefPubMed Harvey LA. Physiotherapy rehabilitation for people with spinal cord injuries. J Physiother. 2016;62(1):4–11.CrossRefPubMed
41.
go back to reference Ribot-Ciscar E, Butler JE, Thomas CK. Facilitation of triceps brachii muscle contraction by tendon vibration after chronic cervical spinal cord injury. J Appl Physiol. 2003;94(6):2358–67.CrossRefPubMed Ribot-Ciscar E, Butler JE, Thomas CK. Facilitation of triceps brachii muscle contraction by tendon vibration after chronic cervical spinal cord injury. J Appl Physiol. 2003;94(6):2358–67.CrossRefPubMed
42.
go back to reference Cotey D, Hornby TG, Gordon KE, Schmit BD. Increases in muscle activity produced by vibration of the thigh muscles during locomotion in chronic human spinal cord injury. Exp Brain Res. 2009;196(3):361–74.CrossRefPubMed Cotey D, Hornby TG, Gordon KE, Schmit BD. Increases in muscle activity produced by vibration of the thigh muscles during locomotion in chronic human spinal cord injury. Exp Brain Res. 2009;196(3):361–74.CrossRefPubMed
43.
go back to reference Collins DF. Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev. 2007;35(3):102–9.CrossRefPubMed Collins DF. Central contributions to contractions evoked by tetanic neuromuscular electrical stimulation. Exerc Sport Sci Rev. 2007;35(3):102–9.CrossRefPubMed
44.
go back to reference Gondin J, Giannesini B, Vilmen C, Dalmasso C, le Fur Y, Cozzone PJ, et al. Effects of stimulation frequency and pulse duration on fatigue and metabolic cost during a single bout of neuromuscular electrical stimulation. Muscle Nerve. 2010;41(5):667–78.PubMed Gondin J, Giannesini B, Vilmen C, Dalmasso C, le Fur Y, Cozzone PJ, et al. Effects of stimulation frequency and pulse duration on fatigue and metabolic cost during a single bout of neuromuscular electrical stimulation. Muscle Nerve. 2010;41(5):667–78.PubMed
45.
go back to reference Wegrzyk J, Foure A, Vilmen C, Ghattas B, Maffiuletti NA, Mattei JP, et al. Extra forces induced by wide-pulse, high-frequency electrical stimulation: occurrence, magnitude, variability and underlying mechanisms. Clin Neurophysiol. 2015;126(7):1400–12.CrossRefPubMed Wegrzyk J, Foure A, Vilmen C, Ghattas B, Maffiuletti NA, Mattei JP, et al. Extra forces induced by wide-pulse, high-frequency electrical stimulation: occurrence, magnitude, variability and underlying mechanisms. Clin Neurophysiol. 2015;126(7):1400–12.CrossRefPubMed
46.
go back to reference Magalhaes FH, Kohn AF. Vibration-induced extra torque during electrically-evoked contractions of the human calf muscles. J NeuroEng Rehabil. 2010;7 Magalhaes FH, Kohn AF. Vibration-induced extra torque during electrically-evoked contractions of the human calf muscles. J NeuroEng Rehabil. 2010;7
47.
go back to reference Trajano GS, Seitz LB, Nosaka K, Blazevich AJ. Can passive stretch inhibit motoneuron facilitation in the human plantar flexors? J Appl Physiol. 2014;117(12):1486–92.CrossRefPubMed Trajano GS, Seitz LB, Nosaka K, Blazevich AJ. Can passive stretch inhibit motoneuron facilitation in the human plantar flexors? J Appl Physiol. 2014;117(12):1486–92.CrossRefPubMed
48.
go back to reference Bongiovanni LG, Hagbarth KE. Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. J Physiol-London. 1990;423:1–14.CrossRefPubMedPubMedCentral Bongiovanni LG, Hagbarth KE. Tonic vibration reflexes elicited during fatigue from maximal voluntary contractions in man. J Physiol-London. 1990;423:1–14.CrossRefPubMedPubMedCentral
49.
go back to reference Neyroud D, Armand S, De Coulon G, Da Silva SRD, Wegrzyk J, Gondin J, et al. Wide-pulse-high-frequency neuromuscular electrical stimulation in cerebral palsy. Clin Neurophysiol. 2016;127(2):1530–9.CrossRefPubMed Neyroud D, Armand S, De Coulon G, Da Silva SRD, Wegrzyk J, Gondin J, et al. Wide-pulse-high-frequency neuromuscular electrical stimulation in cerebral palsy. Clin Neurophysiol. 2016;127(2):1530–9.CrossRefPubMed
50.
go back to reference Bochkezanian V, Newton RU, Trajano GS, Vieira A, Pulverenti TS, Blazevich AJ. Effect of tendon vibration during wide-pulse neuromuscular electrical stimulation (NMES) on the decline and recovery of muscle force. BMC Neurol. 2017;17(1):82.CrossRefPubMedPubMedCentral Bochkezanian V, Newton RU, Trajano GS, Vieira A, Pulverenti TS, Blazevich AJ. Effect of tendon vibration during wide-pulse neuromuscular electrical stimulation (NMES) on the decline and recovery of muscle force. BMC Neurol. 2017;17(1):82.CrossRefPubMedPubMedCentral
51.
go back to reference Bergquist AJ, Wiest MJ, Collins DF. Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: quadriceps femoris. J Appl Physiol. 2012;113(1):78–89.CrossRefPubMed Bergquist AJ, Wiest MJ, Collins DF. Motor unit recruitment when neuromuscular electrical stimulation is applied over a nerve trunk compared with a muscle belly: quadriceps femoris. J Appl Physiol. 2012;113(1):78–89.CrossRefPubMed
52.
go back to reference Bax L, Staes F, Verhagen A. Does neuromuscular electrical stimulation strengthen the quadriceps femoris? Syst Rev Random Controlled Trials Sports Med. 2005;35(3):191–212. Bax L, Staes F, Verhagen A. Does neuromuscular electrical stimulation strengthen the quadriceps femoris? Syst Rev Random Controlled Trials Sports Med. 2005;35(3):191–212.
53.
go back to reference Edgerton VR, Roy RR. Activity-dependent plasticity of spinal locomotion: implications for sensory processing. Exerc Sport Sci Rev. 2009;37(4):171–8.PubMedPubMedCentral Edgerton VR, Roy RR. Activity-dependent plasticity of spinal locomotion: implications for sensory processing. Exerc Sport Sci Rev. 2009;37(4):171–8.PubMedPubMedCentral
54.
go back to reference Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR. Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci. 2004;27:145–67.CrossRefPubMed Edgerton VR, Tillakaratne NJ, Bigbee AJ, de Leon RD, Roy RR. Plasticity of the spinal neural circuitry after injury. Annu Rev Neurosci. 2004;27:145–67.CrossRefPubMed
55.
go back to reference Bergquist AJ, Clair JM, Lagerquist O, Mang CS, Okuma Y, Collins DF. Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol. 2011;111(10):2409–26.CrossRefPubMed Bergquist AJ, Clair JM, Lagerquist O, Mang CS, Okuma Y, Collins DF. Neuromuscular electrical stimulation: implications of the electrically evoked sensory volley. Eur J Appl Physiol. 2011;111(10):2409–26.CrossRefPubMed
56.
go back to reference Collins DF, Burke D, Gandevia SC. Large involuntary forces consistent with plateau-like behavior of human motoneurons. J Neurosci. 2001;21(11):4059–65.PubMed Collins DF, Burke D, Gandevia SC. Large involuntary forces consistent with plateau-like behavior of human motoneurons. J Neurosci. 2001;21(11):4059–65.PubMed
57.
go back to reference Fallon JB, Macefield VG. Vibration sensitivity of human muscle spindles and Golgi tendon organs. Muscle Nerve. 2007;36(1):21–9.CrossRefPubMed Fallon JB, Macefield VG. Vibration sensitivity of human muscle spindles and Golgi tendon organs. Muscle Nerve. 2007;36(1):21–9.CrossRefPubMed
58.
go back to reference Rehabilitation LJS. Following brain damage: some neurophysiological mechanisms. Physiological correlates of clinically observed changes in posture and tone following lesions of the central nervous system. Int Rehabil Med. 1981;4(4):195–9. Rehabilitation LJS. Following brain damage: some neurophysiological mechanisms. Physiological correlates of clinically observed changes in posture and tone following lesions of the central nervous system. Int Rehabil Med. 1981;4(4):195–9.
59.
go back to reference Xia R, Rymer WZ. Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord. 2005;43(1):14–21.CrossRefPubMed Xia R, Rymer WZ. Reflex reciprocal facilitation of antagonist muscles in spinal cord injury. Spinal Cord. 2005;43(1):14–21.CrossRefPubMed
60.
go back to reference Biering-Sorensen B, Kristensen IB, Kjaer M, Biering-Sorensen F. Muscle after spinal cord injury. Muscle Nerve. 2009;40(4):499–519.CrossRefPubMed Biering-Sorensen B, Kristensen IB, Kjaer M, Biering-Sorensen F. Muscle after spinal cord injury. Muscle Nerve. 2009;40(4):499–519.CrossRefPubMed
61.
go back to reference Kim HE, Corcos DM, Hornby TG. Increased spinal reflex excitability is associated with enhanced central activation during voluntary lengthening contractions in human spinal cord injury. J Neurophysiol. 2015;114(1):427–39.CrossRefPubMedPubMedCentral Kim HE, Corcos DM, Hornby TG. Increased spinal reflex excitability is associated with enhanced central activation during voluntary lengthening contractions in human spinal cord injury. J Neurophysiol. 2015;114(1):427–39.CrossRefPubMedPubMedCentral
62.
go back to reference Gordon T, Mao J. Muscle atrophy and procedures for training after spinal-cord injury. Phys Ther. 1994;74(1):50–60.CrossRefPubMed Gordon T, Mao J. Muscle atrophy and procedures for training after spinal-cord injury. Phys Ther. 1994;74(1):50–60.CrossRefPubMed
63.
go back to reference Li Y, Li X, Harvey P, Bennett D. Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol. 2004;92(5):2694–703.CrossRefPubMed Li Y, Li X, Harvey P, Bennett D. Effects of baclofen on spinal reflexes and persistent inward currents in motoneurons of chronic spinal rats with spasticity. J Neurophysiol. 2004;92(5):2694–703.CrossRefPubMed
64.
go back to reference Magalhaes FH, de Toledo DR, Kohn AF. Plantar flexion force induced by amplitude-modulated tendon vibration and associated soleus V/F-waves as an evidence of a centrally-mediated mechanism contributing to extra torque generation in humans. J NeuroEng Rehabil. 2013;10:32.CrossRefPubMedPubMedCentral Magalhaes FH, de Toledo DR, Kohn AF. Plantar flexion force induced by amplitude-modulated tendon vibration and associated soleus V/F-waves as an evidence of a centrally-mediated mechanism contributing to extra torque generation in humans. J NeuroEng Rehabil. 2013;10:32.CrossRefPubMedPubMedCentral
65.
66.
go back to reference D'Amico JM, Condliffe EG, Martins KJB, Bennett DJ, Gorassini MA. Recovery of neuronal and network excitability after spinal cord injury and implications for spasticity. Front Integr Neurosci. 2014;8:36.PubMedPubMedCentral D'Amico JM, Condliffe EG, Martins KJB, Bennett DJ, Gorassini MA. Recovery of neuronal and network excitability after spinal cord injury and implications for spasticity. Front Integr Neurosci. 2014;8:36.PubMedPubMedCentral
67.
go back to reference Mizrahi J. Fatigue in functional electrical stimulation in spinal cord injury. J Electromyogr Kinesiol. 1997;7(1):1–2.CrossRefPubMed Mizrahi J. Fatigue in functional electrical stimulation in spinal cord injury. J Electromyogr Kinesiol. 1997;7(1):1–2.CrossRefPubMed
68.
go back to reference Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and neuromuscular electrical stimulation. Phys Ther. 1993;73(12):902–10.CrossRefPubMed Binder-Macleod SA, Snyder-Mackler L. Muscle fatigue: clinical implications for fatigue assessment and neuromuscular electrical stimulation. Phys Ther. 1993;73(12):902–10.CrossRefPubMed
69.
go back to reference Kent-Braun JA. Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol Occup Physiol. 1999;80(1):57–63.CrossRefPubMed Kent-Braun JA. Central and peripheral contributions to muscle fatigue in humans during sustained maximal effort. Eur J Appl Physiol Occup Physiol. 1999;80(1):57–63.CrossRefPubMed
70.
go back to reference Eklund G, Hagbarth KE, Hagglund JV, Wallin EU. The late reflex responses to muscle stretch - the resonance hypothesis versus the long-loop hypothesis. J Physiol-London. 1982;326(5):79–90.CrossRefPubMedPubMedCentral Eklund G, Hagbarth KE, Hagglund JV, Wallin EU. The late reflex responses to muscle stretch - the resonance hypothesis versus the long-loop hypothesis. J Physiol-London. 1982;326(5):79–90.CrossRefPubMedPubMedCentral
71.
go back to reference Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves DE, Jha A, et al. International standards for neurological classification of spinal cord injury (revised 2011). J Spinal Cord Med. 2011;34(6):535–46.CrossRefPubMedPubMedCentral Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves DE, Jha A, et al. International standards for neurological classification of spinal cord injury (revised 2011). J Spinal Cord Med. 2011;34(6):535–46.CrossRefPubMedPubMedCentral
Metadata
Title
Effect of tendon vibration during wide-pulse neuromuscular electrical stimulation (NMES) on muscle force production in people with spinal cord injury (SCI)
Authors
Vanesa Bochkezanian
Robert U. Newton
Gabriel S. Trajano
Amilton Vieira
Timothy S. Pulverenti
Anthony J. Blazevich
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Neurology / Issue 1/2018
Electronic ISSN: 1471-2377
DOI
https://doi.org/10.1186/s12883-018-1020-9

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