Oral creatine supplementation enhances upper extremity work capacity in persons with cervical-level spinal cord injury☆1☆2☆3☆4☆5☆6☆7☆8

Article Outline

• Abstract
• Methods
  • Subjects
  • Experimental procedure
  • Peak arm ergometry test
  • Measurements
  • Statistical analysis
• Results
• Discussion
• Conclusion
• References
• Copyright

Abstract 

Jacobs PL, Mahoney ET, Cohn KA, Sheradsky LF, Green BA. Oral creatine supplementation enhances upper extremity work capacity in persons with cervical-level spinal cord injury. Arch Phys Med Rehabil 2002;83:19-23. Objective: To examine the effects of short-term creatine monohydrate supplementation on the upper extremity work capacity of persons with cervical-level spinal cord injury (SCI). Design: Randomized, double-blind, placebo-controlled, crossover design study. Consists of 2 treatment phases lasting for 7 days, separated by a 21-day washout period. Setting: University research laboratory trial. Participants: Sixteen men with complete cervical-level SCI (C5-7). Intervention: Subjects were randomly assigned to 1 of 2 groups and received either 20g/d of creatine monohydrate supplement powder or placebo maltodextrin powder for the first treatment phase; the treatment was reversed in the second phase. Incremental peak arm ergometry tests, using 2-minute work stages and 1-minute recovery periods, were performed immediately before and after each treatment phase (total of 4 assessments). The initial stage was performed unloaded, with power output progressively increased 10 watts/stage until subjects had achieved volitional exhaustion. Main Outcome Measures: Peak power output, time to fatigue, heart rate, and metabolic measurements, including oxygen uptake (V̇O₂), minute ventilation, tidal volume (V_T), and respiration frequency. Results: Significantly greater values of VO₂, VCO₂, and V_T at peak effort after creatine supplementation (P < .001). Conclusions: Creatine supplementation enhances the exercise capacity in persons with complete cervical-level SCI and may promote greater exercise training benefits. © 2002 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation

Keywords:  Creatine, Dietary supplementation, Exercise tolerance, Rehabilitation, Spinal cord injuries

Creatine is a naturally occurring substance found primarily in skeletal muscle and synthesized endogenously by the liver, kidneys, and pancreas. Creatine can be obtained by eating meat and fish products, or it can come from supplementation powders. It exists primarily in 2 main forms: a free form and in a phosphorylated form as phosphocreatine. Approximately 60% of muscle creatine exists as phosphocreatine, which aids in the fast resynthesis of adenosine triphosphate (ATP) during short-term, high-intensity exercise. The mechanism involved is the transfer of a phosphate group from phosphocreatine to adenosine diphosphate via creatine kinase to replenish ATP, which is consumed quickly during high-intensity exercise. Dietary supplementation of creatine is beneficial in improving strength, power, and recovery from high-intensity exercise in unimpaired persons.¹, ², ³, ⁴, ⁵

Persons with spinal cord injury (SCI) have decreased upper extremity work capacity.⁶, ⁷, ⁸, ⁹ In particular, persons with cervical-level SCI have limited proficiency in the repeated tasks of daily living that require physical strength, power, and/or endurance. Increased muscular strength and/or endurance in persons with SCI would benefit them greatly by reducing the relative physical strain involved daily in their lives. Additionally, greater muscular strength and stamina would permit them to be more independent and active, with a resulting improvement in their overall health and quality of life.

When compared with able-bodied individuals, persons with cervical-level SCI have dramatically less upper body strength and a greatly reduced work capacity, which limits their independence and promotes inactivity. Creatine supplementation increases muscular performance and the ability to perform repeated bouts of high-intensity activity in persons without disability.⁵, ⁶, ⁷, ⁸, ⁹ However, the application of this supplement in research studies has generally been limited to athletic populations. It is possible that deconditioned populations, particularly those with diminished dietary intake of creatine, may especially benefit from creatine supplementation. This investigation sought to determine the effects of oral creatine supplementation on work capacity in persons with complete cervical-level SCI.

Back to Article Outline

Methods 

Subjects 

Sixteen men with complete cervical-level SCI (American Spinal Injury Association [ASIA] classes A and B) at levels C5-7 volunteered to participate in the study. They ranged in age from 22 to 53 years (mean age ± standard deviation [SD], 35.3 ± 8.6yr), and had a mean body mass of 71.4 ± 11.3kg. All subjects were familiar with arm ergometry, having experienced it during their rehabilitation, and intermittently thereafter. Their SCI level was assessed by using the ASIA Impairment Scale. This protocol was approved by the University of Miami Medical Sciences Subcommittee for the Protection of Human Subjects, and all subjects were informed of the purpose, possible risks, and benefits before giving written consent to participate.

Experimental procedure 

This crossover design study was double-blind, with random assignment of subjects into 2 treatment groups. The study protocol consisted of 2 treatment phases lasting for 7 days, separated by a 21-day washout period (fig 1).

• 
  • View Large Image
  • Download to PowerPoint

• Fig. 1. 

  Experimental design.

A 3-week washout period is adequate to allow serum creatine levels to return to baseline levels.¹⁰, ¹¹ Group 1 participants received creatine monohydrate supplement powder^a during phase I of the study and placebo maltodextrin powder^a during phase II, whereas persons in group 2 received converse treatment in a standard crossover procedure. Both supplements were similar in color and texture, thereby blinding the participants as to which supplement they had received. Subjects were instructed to take 1 teaspoon of the respective supplement with 8 ounces of water, 4 times daily for each 7-day treatment period. They were required to perform a total of 4 separate incremental upper extremity exercise tests during the 5-week study period. These exercise tests were performed on days 1 and 7 in both phases of the study.

Peak arm ergometry test 

Peak arm ergometry (AE) tests were performed before and after both supplementation periods. Subjects abstained from caffeine, nicotine, alcohol, and strenuous exercise for 12 hours before testing. The peak AE tests were performed on a Monarch 881 arm ergometer^b by using a progressive discontinuous protocol recommended by Franklin.¹² Each stage consisted of 2 minutes of exercise followed by a 1-minute recovery period. The initial workload was unloaded with power output progressively increased by 10 watts per subsequent stage. Subjects were guided with a metronome to maintain the desired cadence of 50rpm throughout the AE test. Subjects continued AE testing with increasing workloads to the point of volitional exhaustion, or until they were unable to maintain the 50-rpm cadence. Subjects were given verbal encouragement throughout each test to provide motivation and promote maximal effort. Termination points for these peak AE tests were those recommended by the American College of Sports Medicine (ACSM).¹³

Measurements 

Metabolic activity was monitored continuously throughout the AE tests via open circuit spirometry with a MMC Horizon System,^c which was calibrated before each test with standard gases and known volumes of air. Heart rate (HR) data were collected during the incremental AE tests with a FX-406U Cardimax 12-lead electrocardiograph.^d Ratings of perceived exertion (RPEs) were assessed immediately after each 2-minute work interval with a 6- to 20-point Borg Scale.

Statistical analysis 

Data were analyzed according to recommended methods for a 2-period crossover design¹⁴, ¹⁵, ¹⁶ using SPSS, version 8.0,^e and A Primer of Biostatistics¹⁴ on an IBM-compatible computer. These methods included analysis of variance for repeated measures with post hoc t tests (Bonferroni correction method applied to multiple comparisons) and applications of the t test to assess for treatment effects, period effects, and carry-over effects. In all cases, statistical significance was accepted at a P value of .05 or less.

Back to Article Outline

Results 

Demographic data, following random group assignment, are presented in table 1.

Table 1. Descriptive characteristics of research participants in groups 1 and 2

Note. Values are mean ± SD.

There were no significant differences between groups in subject age, body mass, or duration of SCI. The 16 subjects completed the study protocol without adverse effects from either treatment or the testing procedures. All subjects, in each of the 4 tests, reported an exertion level of 17 or greater (very hard) on the Borg RPE Scale, suggesting that they reached appropriate endpoints for test termination. Statistical analysis revealed no significant effects of test order (period effects) in any of the physiologic outcomes measured.

Peak physiologic responses to the AE tests are presented with reference to the supplementation received, regardless of group or order (table 2).

Table 2. Peak physiologic responses of 16 subjects with cervical-level SCI to graded peak AE testing after creatine and placebo supplementation

Note. Values are mean ± SD.

No significant treatment effects were noted between baseline, either supplement, or washout tests in the measures of HR, respiratory exchange ratio (RER), or minute ventilation (V̇_E). However, significant differences were observed among these assessment points in the measures of oxygen uptake (V̇O₂), carbon dioxide production (V̇CO₂), tidal volume (V_T), and ventilatory frequency (f) (P values < .001). Mean peak VO₂ after creatine supplementation was 12.81mL · kg⁻¹ · min⁻¹ compared with the placebo value of 10.8mL · kg⁻¹ · min⁻¹, representing an increase of 18.6%. Post hoc analysis revealed that, in each case, the values associated with the creatine supplementation period were significantly different from the other 3 test points. After taking the creatine monohydrate supplement, subjects reached significantly greater peak values of VO₂, VCO₂, and V_T. The peak VO₂ values of the 2 subject groups, at each of the 4 test points, are shown in figure 2.

• 
  • View Large Image
  • Download to PowerPoint

• Fig. 2. 

  Peak oxygen uptake response to graded peak AE testing in subjects with cervical-level SCI (mean ± SD) receiving dietary supplementation of (A) creatine followed by placebo and (B) placebo followed by creatine. * P < .001; creatine versus baseline; creatine versus placebo.

Fourteen of the 16 subjects displayed increased peak VO₂ values after creatine supplementation (range, .25-4.80mL · kg⁻¹ · min⁻¹). The 2 individuals whose peak values decreased had extremely small changes (.05-33mL · kg⁻¹ · min⁻¹). The gains in peak VO₂ were accompanied by statistically significant increases in peak power output (P ≤ .05) and a trend for increased time to fatigue (P = .086). Significantly lower peak values (P < .001) of ventilatory frequency were noted after creatine supplementation in comparison with the other 3 test points.

Back to Article Outline

Discussion 

Our findings indicate that persons with cervical-level SCI can significantly increase their upper extremity work capacity through dietary creatine supplementation. The relative gains in peak V̇O₂ were dramatic (18.6%), suggesting substantial enhancement in these persons' abilities to perform critical activities. However, the absolute magnitude of the changes in peak work capacity (approximately 2mL · kg⁻¹ · min⁻¹) may leave persons unfamiliar with the SCI population questioning the clinical significance. Previous investigations have reported modest effects of exercise training in cervical-level SCI. Gass et al¹⁷ reported a 3.2mL · kg⁻¹ · min⁻¹ gain in peak VO₂ after 7 weeks of exercise conditioning by their subjects. Hopman et al¹⁸ found a difference of 5.4mL · kg⁻¹ · min⁻¹ between groups of untrained and chronically trained persons with cervical SCI. In comparison with these training studies, our short-term supplementation study provided respectable results.

Our results contrast with the findings of other studies, which failed to show any change in maximal oxygen uptake after creatine supplementation in persons without disability.¹⁹, ²⁰ Nelson et al¹⁹ found no increase in V̇O₂max during leg cycling after creatine supplementation; however, the anaerobic threshold was increased. Similarly, Barnett et al²⁰ reported no increase in V̇O₂max during leg cycle ergometry after creatine supplementation and no increase in multiple sprint performance. In contrast, Jacobs et al²¹ reported an increase in oxygen uptake and time to fatigue during supramaximal leg cycle ergometry in their subjects after 7 days of creatine ingestion.

We are unaware of any studies that examined the effects of creatine supplementation in arm ergometry or within a population of persons with SCI. Our protocol consisted of 2-minute work stages with a 1-minute recovery period between each incremental stage. Although we used a standard ramped protocol, it was discontinuous and was a model of intermittent exercise. Several studies have shown a positive effect of creatine supplementation on high-intensity, intermittent, leg cycle exercise.²², ²³, ²⁴, ²⁵, ²⁶ A recent study by Rico-Sanz and Marco²⁶ showed that 5 days of oral creatine supplementation enhanced oxygen uptake during leg cycling for 3-minute alternating bouts at 30% and 90% of maximal power output until exhaustion. Oxygen consumption was increased during the first 2 work bouts performed at 90%, and time to exhaustion was increased after creatine supplementation. It is believed that these effects are related to increased aerobic phosphorylation and flux through the creatine kinase system.

It is possible that our finding that creatine supplementation increased VO₂peak may not result solely from the exercise protocol or the population, but may be related to the mode of exercise. To our knowledge, ours is the only study that has investigated the effects of VO₂peak after creatine supplementation with AE test. The exercise activity most similar to arm ergometry is kayaking, which depends primarily on the upper body and trunk musculature. McNaughton et al²⁷ studied the effects of 5-day creatine loading on maximal kayak performance in trials of 90, 150, and 300 seconds, and showed an increase in total work performance in all 3 trials. Blood lactate concentrations were no different in the placebo or control group for the 90-second test, however, they were significantly greater during the postsupplementation 150-second test. After creatine ingestion, total work for the 90-second bout increased, with no change in blood lactate, which suggests that ATP is being regenerated at a higher rate as a result of an increase in phosphocreatine resynthesis. Total work and blood lactate levels increased in the creatine group during the 150-second bout of kayaking, which McNaughton attributed to an increased buffering capacity of the muscle with creatine supplementation. These effects may also be present during the AE test.

Persons with cervical-level SCI typically attribute local muscular fatigue and soreness in the arms and shoulders, rather than cardiorespiratory fatigue, as the reason they are unable to continue a maximal AE test. With creatine supplementation, there may be a greater contribution of energy derived from phosphagen and oxidative metabolism and less from anaerobic glycolysis, causing reduced muscle acidosis.¹⁹, ²² Creatine may help delay the onset of fatigue experienced with high-intensity arm exercise, thus, permitting these subjects to increase work capacity and, consequently, peak oxygen consumption. Alternatively, creatine supplementation may simply improve the buffering capacity of muscle and thus allow subjects to perform more work before local fatigue occurs.

The difference in the musculature used during arm and leg cycling cannot be ignored as a potential factor in the discrepancies between our results and those of other studies of creatine supplementation and VO₂peak. The upper extremity musculature used during AE has greater percentages of fast-twitch muscle fibers than in the lower body musculature.²⁸ Creatine is found in greater quantities within fast-twitch muscle fibers than in slow-twitch fibers.², ²⁹ Therefore, creatine supplementation may be of greater benefit to the larger type II muscle fibers, which use greater percentages of phosphagens than do slow-twitch fibers. Increased peak oxygen consumption during AE after creatine supplementation may be because of the recruitment of fast-fatigable fibers that likely have increased concentrations of total creatine¹⁰, ¹¹, ³⁰, ³¹ and an increased capacity to resynthesize phosphocreatine during recovery.³²

It is possible that certain muscles used predominantly during the AE test, such as the triceps, undergo alterations after SCI at the C5-6 level that particularly limit the performance of this exercise. Persons with cervical-level SCI exhibit reduced strength in the triceps, which may result from a reduction in functional motoneurons.³³ Subjects in our study may have had partial denervation of the triceps muscles that would contribute to heightened muscle fatigue rates during AE. It is possible that if these muscles have limited voluntary control, the fiber types within the muscle may shift to faster, more fatigable fibers because of disuse or limited innervation. Creatine supplementation may help the existing motoneuron pool in the triceps to recover more quickly during the 1-minute rest period. If the fiber types of partially denervated triceps do shift toward faster, more fatigable fibers, it is likely that they will show an increased response to creatine, making supplementation extremely beneficial during AE, when the triceps perform a large portion of the work. Also, it is possible that creatine supplementation can increase recovery in the fully functional motoneurons in the triceps and increase work capacity. More study is needed to determine the change, if any, in the fiber-type characteristics within partially denervated muscles. The effect of creatine supplementation on fatigue rates of the triceps in persons with cervical-level SCI also requires further study.

One unexpected finding of this study concerned respiratory function at peak effort. Although V̇_E was not affected by the supplementation procedures, the 2 contributing factors of respiration, V_T and f, were inversely influenced. Creatine supplementation appears to increase tidal volume and to reduce respiratory rate at peak exercise in persons with cervical-level SCI. One hypothesis is that creatine may increase energy production in the major ventilatory muscles that remain intact in this population. Further study is needed to determine whether creatine can enhance the capacity of the respiratory muscles in a population in which peak ventilation may be somewhat compromised.

This study may have been limited by our use of volitional exhaustion as the endpoint for peak exercise testing. However, there were no significant differences in mean peak HRs across all 4 treatments and these values were within the range of maximal predicted HR for this population. Additionally, the subjects' self-reported RPE values were greater than 17 in each test, indicating their perception of effort as “very hard.” Therefore, both the peak HR and RPE values are in accord with the ASCM guidelines¹³ and are appropriate termination points for maximal exercise testing.

Back to Article Outline

Conclusion 

This study found that there is increased upper extremity work capacity after creatine supplementation in subjects with cervical-level SCI. There are 4 ways that creatine supplementation, either alone or in combination, is believed to enhance peak oxygen consumption during the AE test. They are: (1) by increasing phosphocreatine resynthesis, primarily in type II muscle fibers, and directly enhancing the production of ATP; (2) by increasing phosphocreatine resynthesis, to act as a buffer by consuming protons and by reducing muscle acidosis in the arms and shoulders; (3) by further increasing energy production from the phosphagen and the oxidative systems, and decreasing the contribution from anaerobic glycolysis, specific to the intermittent exercise protocol that was used; and (4) by increasing the recovery of the motoneuron pool in the triceps that, in this population, may be reduced because of partial denervation.

Creatine supplementation appears to increase exercise capacity in persons with cervical-level SCI. It may aid in increasing power and stamina when used in conjunction with strength training, which would allow persons with SCI to be more independent and active and lead to an improvement in overall health and quality of life.

Back to Article Outline

References 

1. Balsom P, Soderlund K, Sjodin B, Ekblom B. Skeletal muscle metabolism during short duration high-intensity exercise: influence of creatine supplementation. Acta Physiol Scand. 1995;1154:303–310
   • View In Article
2. Casey A, Constantin-Teodosiu D, Howell D, Hultman E, Greenhaff P. Creatine ingestion favorably affects performance and muscle metabolism during maximal exercise in humans. Am J Physiol. 1996;271:E31–E37
   • View In Article
   • MEDLINE
3. Harris R, Viru M, Greenhaff P, Hultman E. The effect of oral creatine supplementation on running performance during maximal short term exercise in man. J Physiol. 1993;467:74P
   • View In Article
4. Earnest C, Snell P, Rodriguez R, Almada A, Mitchell T. The effect of creatine monohydrate ingestion on anaerobic power indices, muscular strength and body composition. Acta Physiol Scand. 1995;153:207–209
   • View In Article
   • MEDLINE
   • CrossRef
5. Greenhaff P, Bodin K, Harris R, et al.  The influence of oral creatine supplementation on muscle phosphocreatine resynthesis following intense contraction in man. J Physiol. 1993;467:75P
   • View In Article
6. Hopman MT, Oeseburg B, Binkhorst RA. Cardiovascular responses in paraplegic subjects during arm exercise. Eur J Appl Physiol. 1992;65:73–78
   • View In Article
7. Jehl JL, Gandmontagne M, Pastene G, Eyssette M, Flandrois R, Coudert J. Cardiac output during exercise in paraplegic subjects. Eur J Appl Physiol. 1991;62:256–260
   • View In Article
8. Lin KH, Lai JS, Kao MJ, Lien IN. Anaerobic threshold and maximal oxygen consumption during arm cranking exercise in paraplegia. Arch Phys Med Rehabil. 1993;74:515–520
   • View In Article
   • MEDLINE
   • CrossRef
9. Van Loan MD, McCluer S, Loftin JM, Boileau RA. Comparison of physiological responses to maximal arm exercise among able-bodied, paraplegics and quadriplegics. Paraplegia. 1987;25:397–405
   • View In Article
   • MEDLINE
   • CrossRef
10. Hultman E, Soderlund K, Timmons JA, Cederblad G, Greenhaff PL. Muscle creatine loading in men. J Appl Physiol. 1996;81:232–237
    • View In Article
    • MEDLINE
11. McKenna MJ, Morton J, Selig SE, Snow RJ. Creatine supplementation increases muscle total creatine but not maximal intermittent exercise performance. J Appl Physiol. 1999;87:2244–2252
    • View In Article
    • MEDLINE
12. Franklin BA. Exercise testing, training and arm ergometry. Sports Med. 1985;2:100–119
    • View In Article
    • MEDLINE
    • CrossRef
13. American College of Sports Medicine . Guidelines for exercise testing and training. 5th ed. Indianapolis (IN): : Saunders; 1990;
    • View In Article
14. Glantz SA. A primer for biostatistics. 4th ed. New York: : McGraw-Hill; 1997;
    • View In Article
15. Fleiss JL. The design and analysis of clinical experiments. New York: : Wiley & Sons; 1986;
    • View In Article
16. Pocock SJ. Clinical trials: a practical approach. Chichester (UK): : Wiley & Sons; 1983;
    • View In Article
17. Gass GF, Watson J, Camp EM, Court HJ, McPherson LM, Redhead P. The effects of physical training on high level spinal lesion patients. Scand J Rehabil Med. 1980;12:61–65
    • View In Article
    • MEDLINE
18. Hopman MT, Dallmeijer AJ, Snoek G, van der Woude LH. The effect of training on cardiovascular responses to arm exercise in individuals with tetraplegia. Eur J Appl Physiol. 1996;74:172–179
    • View In Article
19. Nelson A, Day R, Glickman-Weiss E, Hegstad M, Sampson B. Creatine supplementation raises anaerobic threshold. [abstract] FASEB J. 1997;11:A589
    • View In Article
20. Barnett C, Hinds M, Jenkins DG. Effects of oral creatine supplementation on multiple sprint cycle performance. Aust J Sci Med Sport. 1996;28:35–39
    • View In Article
    • MEDLINE
21. Jacobs I, Bleue S, Goodman J. Creatine ingestion increases anaerobic capacity and maximum accumulated oxygen deficit. Can J Appl Physiol. 1997;22:231–243
    • View In Article
    • MEDLINE
    • CrossRef
22. Prevost MC, Nelson AG, Morris GS. Creatine supplementation enhances intermittent work performance. Res Q Exerc Sport. 1997;68:233–240
    • View In Article
    • MEDLINE
23. Dawson B, Cutler M, Moody A, Lawrence S, Goodman C, Randall N. Effects of oral creatine loading on single and repeated maximal short sprints. Aust J Sci Med Sports. 1995;27:56–61
    • View In Article
    • MEDLINE
24. Balsom PD, Ekblom B, Soderlund K, Sjodin B, Hultman E. Creatine supplementation and dynamic high-intensity intermittent exercise. Scand J Med Sci Sports. 1993;3:143–149
    • View In Article
    • CrossRef
25. Vandebuerie F, Vanden Eynde B, Vandenberghe K, Hespel P. Effect of creatine loading on endurance capacity and sprint power in cyclists. Int J Sports Med. 1998;19:490–495
    • View In Article
    • MEDLINE
    • CrossRef
26. Rico-Sanz J, Marco TM. Creatine enhances oxygen uptake and performance during alternating intensity exercise. Med Sci Sports Exerc. 2000;32:379–385
    • View In Article
    • MEDLINE
    • CrossRef
27. McNaughton LR, Dalton B, Tarr J. The effects of creatine supplementation on high intensity exercise performance in elite performers. Eur J Appl Physiol. 1998;78:236–240
    • View In Article
    • CrossRef
28. Johnson MA, Polgar J, Weightman D, Appleton D. Data on the distribution of fibre types in thirty-six human muscles. An autopsy study. J Neurol Sci. 1973;18:111–129
    • View In Article
    • MEDLINE
    • CrossRef
29. Clark JF, Odoom J, Tracey I, et al.  Experimental observations of creatine and creatine phosphate metabolism. In:  Conway MA,  Clark JF editor. Creatine and creatine phosphate: scientific and clinical perspectives. San Diego: : Academic Pr; 1996;p. 33–50
    • View In Article
30. Harris R, Soderlund K, Hultman E. Elevation of creatine in resting and exercised muscle of normal subjects by creatine supplementation. Clin Sci. 1992;83:367–374
    • View In Article
31. Febbraio MA, Flanagan TR, Snow RJ, Zhao S, Carey MF. Effect of creatine supplementation on intramuscular TCr, metabolism and performance during intermittent, supramaximal exercise in humans. Acta Physiol Scand. 1995;155:387–395
    • View In Article
    • MEDLINE
    • CrossRef
32. Greenhaff P, Bodin K, Soderlund K, Hultman E. Effect of oral creatine supplementation on skeletal muscle phosphocreatine resynthesis. Am J Physiol. 1994;266:E725–E730
    • View In Article
    • MEDLINE
33. Thomas CK, Zaidner EY, Calancie B, Broton JG, Bigland-Ritchie BR. Muscle weakness, paralysis and atrophy after human cervical spinal cord injury. Exp Neurol. 1997;148:414–423
    • View In Article
    • MEDLINE
    • CrossRef