| | Nutrient Supplementation Post Ambulation in Persons With Incomplete Spinal Cord Injuries: A Randomized, Double-Blinded, Placebo-Controlled Case SeriesAbstract Nash MS, Meltzer NM, Martins SC, Burns PA, Lindley SD, Field-Fote EC. Nutrient supplementation post ambulation in persons with incomplete spinal cord injuries: a randomized, double-blinded, placebo-controlled case series. ObjectiveTo examine effects of protein-carbohydrate intake on ambulation performance in persons with incomplete spinal cord injury (SCI). DesignDouble-blinded treatment with washout and placebo crossover. SettingAcademic medical center. ParticipantsThree subjects aged 34 to 43 years with incomplete SCI at C5-T4. InterventionsSubjects walked to fatigue on 5 consecutive days. On fatigue, participants consumed 48g of vanilla-flavored whey and 1g/kg of body weight of carbohydrate (CH2O). Weekend rest followed, and the process was repeated. A 2-week washout was interposed and the process repeated using 48g of vanilla-flavored soy. Main Outcome MeasuresOxygen consumed (V̇o2; in L/min), carbon dioxide evolved (V̇co2), respiratory exchange ratio (RER: V̇co2/V̇o2), time (in minutes), and distance walked (in meters) were recorded. Caloric expenditure was computed as V̇o2 by time by 21kJ/L (5kcal/L) of oxygen consumed. Data were averaged across the final 2 ambulation sessions for each testing condition. ResultsDespite slow ambulation velocities (range, .11–.34m/s), RERs near or above unity reflected reliance on CH2O fuel substrates. Average ambulation time to fatigue was 17.8% longer; distance walked 37.9% longer, and energy expenditure 12.2% greater with the whey and CH2O supplement than with the soy drink. ConclusionsWhey and CH2O ingestion after fatiguing ambulation enhanced ensuing ambulation by increasing ambulation distance, time, and caloric expenditure in persons with incomplete SCI. INCOMPLETE SPINAL CORD injuries (SCI) and diseases bring about varying degrees of muscle paralysis and diminished locomotor function.1 Lost or diminished motor function occurring after SCI impairs performance of daily activities,2 fosters physical deconditioning,3 and hastens multisystem decline that accompanies aging with a physical disability.4 In doing so it decays the quality and longevity of life for many persons with SCI. Reconditioning exercises undertaken by persons with SCI often reverse unhealthy and diminished functional states imposed by paralysis,5 mirroring exercise benefits attained by those without disability. Unfortunately, altered contractile properties of muscle after SCI often limit the ability of weakened muscle to undergo aggressive exercise and satisfy vigorous functional performance needs.6 These muscle alterations include transformation to fibers having fast contractile properties and favored use of glycolytic energy substrates. In such cases the relative intensity of muscle actions increases to the point of early fatigue while still performing relatively little physical work.7 The mixture of muscle fuels can be examined during exercise by monitoring the respiratory exchange ratio (RER), an index of fuel use derived from the quotient of carbon dioxide evolved (V̇co2) to oxygen consumed (V̇o2), which increases as proportional use of muscle fuel shifts from low-intensity use of fatty fuels to high-intensity use of carbohydrates. Unity of the RER (ie, 1.0), and values above this level, indicate an increasing reliance on carbohydrate substrates (ie, muscle glycogen and blood glucose), and generally forecasts impending fatigue. Considerable research and clinical effort has focused on locomotor rehabilitation of persons with incomplete SCI as a pathway to improved function and enhanced health.8, 9 To date, however, dietary, pharmacologic, and nutrient modification that optimize physical performance for those with SCI have met with limited scrutiny, compared with the extensive research base and well-established benefits of immediate postexercise nutrient supplementation in persons without disability. In many cases of intense exercise the combined intake of carbohydrate (CH2O) and protein immediately after muscle fatigue hastens recovery from intense physical activity, and improves performance during ensuing exercise bouts.10 The most effective supplement combination for achieving this benefit in persons without disability is whey protein and CH2O,11, 12 which serves as the basis for testing of potential benefits in persons with SCI. The purpose of this case series was to examine whether postexercise nutrient supplementation with whey protein and CH2O administered immediately after fatiguing ambulation enhances locomotor performance over a 2-week period. Methods  Ambulation Testing and Supplementation Study participants were experienced in overground locomotion through participation in an earlier research study, but were not actively ambulating when studied. More than 3 months had passed since they had participated in these studies. They were not enrolled in concurrent studies, undergoing structured therapy, or independently exercising in a home-based program. They wore a safety harness and used a rolling walker during testing, but were not provided additional body weight support. Assistive devices used during ambulation are shown in table 1 and were kept constant throughout all testing. Ambulation was performed to fatigue over a 24-m (80-ft) long indoor oval track on 5 consecutive days. Fatigue was determined by the inability of participants to take additional steps. Weekend rest followed, and the process was repeated for another 5 days. Within 5 minutes of experiencing fatigue participants consumed a blended drink containing 48g of vanilla-flavored wheya and 1g/kg of body weight CH2O (maltodextrinb). This combination drink, given immediately after fatiguing exercise, is known to rapidly replete muscle glycogen. A 2-week washout period was interposed and the process repeated using 48g of vanilla-flavored soy proteinc to which 2 packets of a commercial non-nutritive sweetener (Splendad) were added. By contrast, soy protein is slowly absorbed by the body and is not recognized as an aid in recovery from fatiguing exercise. Supplements had similar vanilla flavor, were blended to form similar liquid volumes, and were equally sweetened. There was a slight difference in texture that alerted participants to their difference, but not their identity. The order of supplementation was determined by chance, and the drink composition was unidentified for participants and investigators involved in data collection. Metabolic Monitoring Participants wore a Hans-Rudolph soft maske over their nose and mouth during each session. Oxygen consumed (V̇o2; in L/min), carbon dioxide evolved (V̇co2), and RER (V̇co2/V̇o2) were assessed by open-circuit spirometry using a portable metabolic analyzer carried on body harness (fig 1) and set to average responses over a 1-minute time interval. After preparation for metabolic monitoring participants sat quietly for 5 minutes while baseline data were collected. They then walked to fatigue, accompanied by an investigator. Time (in minutes) and distance walked (in meters) were recorded. Caloric expenditure was computed as the product of V̇o2, time, and a constant reflecting 21kJ (5kcal) burned per liter oxygen consumed.13 Data Management Data for each test condition were averaged across the final 2 days of ambulation and expressed both as individual participant responses and pooled data. The use of an average expressed over the last 2 days decreased the likelihood of bias imposed by factors that might enhance or limit performance on a single day. Differences between test conditions (whey and CH2O vs soy) were computed as percentage differences. Discussion The key observation of this study is that 3 persons with incomplete injuries walked longer distances and at greater caloric expenditure before sustaining fatigue after 2 weeks of whey and CH2O supplementation, whereas a blinded control condition failed to bring about this change. Although the specific benefit to muscle was not studied, the short duration of testing would argue against muscle strengthening known to accompany longer-term supplementation with whey protein,10, 14 and favor enhanced repletion of muscle glycogen typically depleted during repeated exhaustive exercise. Most studies of sublesional muscle after SCI in humans report fibers that are smaller than those above lesion, and than those of persons without SCI.15, 16, 17 These fibers have less contractile protein,15 produce lower peak contractile forces,18 and transform toward fast phenotypic protein expression.17, 19, 20 By increasing their fast myosin heavy chain isoforms,20, 21 muscles located below lesion level increase their reliance on glycogen fuels and decrease their resistance to fatigue.17, 22 This reliance was seen in study participants who walked at slow speeds but had RERs that rapidly approached or exceeded unity (1.0), indicating that despite slow walking the work is challenging. Muscle glycogen is an obligate fuel normally used to support moderate to high intensity contraction of innervated muscle,23 and it is the preferred fuel for both innervated and paralyzed muscle undergoing fatiguing contraction.24, 25, 26 Glycogen breakdown is greater in paralyzed than in innervated muscle when undergoing contraction.19, 22 When glycogen is depleted from innervated or paralyzed muscle the capacity to perform additional voluntary or involuntary activity at moderate and higher work intensities is either completely lost or severely limited.10, 27 This makes rapid replenishment of depleted or exhausted glycogen stores critical if, and when, additional bouts of work are performed.10, 12, 28 Enhanced recovery from glycogen-depleting exercise in persons without disability is readily achieved by immediate CH2O administration, which is superior to both no supplementation and supplementation with electrolytes in water.10, 12, 29 Immediate postactivity ingestion of this nutrient appears critical for successful glycogen repletion.10, 30 This generally rules out ingestion of bulk food to achieve the same benefit, because the immediacy of muscle CH2O uptake is stalled by time required for nutrient digestion, intestinal transit, and blood-borne transport. Addition of protein to the supplement mix increases the glycogen resynthetic capacity of ingested carbohydrates by stimulating an insulin response considered permissive for rapid glycogen repletion.31 It also provides an amino acid reservoir that delays postexercise protein catabolism and enhances protein anabolism.29, 32 Whey protein generally satisfies this need, because it is easily digested, contains high concentrations of branch-chain amino acids used for muscle repair, and rapidly crosses from the intestinal tract into the circulation. By contrast, soy is slowly ingested, and its uptake exceeds the critical timing need for protein uptake, which explains its selection as a control condition for this study. The incorporation of locomotor training in rehabilitation of persons with incomplete SCI has received widespread research attention and has achieved diverse performance outcomes.1, 8, 33, 34, 35, 36, 37 Not all persons who undergo the process become functional ambulators, because walking requires greater muscle forces and more prolonged endurance than many persons can achieve before experiencing fatigue. Surprisingly, no studies have mentioned dietary enhancements or nutrient supplementation as tools to improve performance outcomes, even though enhanced strength, endurance, ambulation time and speed, and motor efficiency have been primary experimental goals of treatment.1, 8, 35, 36, 37, 38, 39 By contrast, considerable success has been achieved in enhancing exercise performance of healthy persons without disability, the frail elderly, and people with chronic infections through use of postexercise nutrient supplementation.10, 40 The performance-enhancing effects of these supplements underpin a joint position of the American Dietetic Association, Dietitians of Canada, and American College of Sports Medicine that “… physical activity, athletic performance, and recovery from exercise are enhanced by optimal nutrition …, ”41(p2130) and who jointly “… recommend appropriate selection of food and fluids, timing of intake, and supplement choices for optimal health and exercise performance.”42(p1543) To our knowledge none of these recommendations have been incorporated or examined for efficacy in persons with SCI undergoing locomotor training. Several studies on persons with SCI have examined pharmacologic approaches to increasing ambulation time and efficiencies, with most efforts focusing on antispasmodic medications having adrenergic, serotonergic, and γ-aminobutyric acid agonist properties,43 although responses to these drugs have been mixed and their universal use limited. Benefits on muscle strengthening have been reported for the β2-selective adrenergic agonist metaproterenol.44 The nutritional food supplement creatine monohydrate has been used for short periods of time to increase motor function of weakened upper muscles in persons with tetraplegia, but with mixed outcomes45, 46; however, no evidence suggests that activity-induced creatine deficiency is a cause of muscle weakness or premature fatigue in persons with SCI. The α1 sympathomimetic agent midodrine reportedly enhances exercise performance in persons with tetraplegia,47 although the benefits of treatment have been attributed to enhanced pressor responses in persons having cardiovascular autonomic dysfunction from injuries above the T1 level. Again, no evidence suggests that ambulation deficiencies in those with SCI are caused by circulatory dysregulation or are corrected by use of α1 selective adrenergic agonists. Study Limitations We note a number of study limitations. The study population is a small case-series and therefore subject to selection bias. In this first study examining this topic, we did not control for dietary intake, but instructed participants to maintain their habitual food choices. A treatment group for CH2O alone was not included, and thus, the extent to which whey enhanced the postulated effect of CH2O ingestion cannot be determined. Instead, we elected to examine whether the combination of whey and CH2O appeared beneficial, and then backtrack through its nutritional elements. Whereas protein content was matched in the two study supplements, the CH2O was not, which makes room for the possibility that CH2O alone was responsible for the case observations. No muscle biopsies were taken to confirm glycogen depletion after fatiguing exercise, or greater glycogen storage after treatment. Participants were studied without body weight support, which differs from the partially unloaded state commonly used to train persons with incomplete SCI. We note that postural hypotension and other circulatory dysfunction accompanying SCI may have contributed to the fatigue patterns.48 Despite these limitations, the magnitude of change observed under blinded placebo-controlled conditions is encouraging; it exceeds in magnitude and speed of change the benefits provided by other ergogenic aids tested for those with SCI and provides a basis for more systematic study in a larger test population. Conclusions Intake of whey and CH2O after fatiguing ambulation enhanced ensuing ambulation by persons with incomplete SCI. Apparent reliance on CH2O substrates, and known benefits of whey and CH2O in postactivity CH2O repletion, suggest a mechanism of action. Ease of digestion and minimal adverse effects were noted. Future research directions could reasonably include studies examining mechanisms of total or subtotal fatigue during locomotory training, as well as investigations of anticatabolic effects of protein supplementation during exhaustive exercise. Confirmation of this benefit requires investigation in a larger study population. Suppliers References 1. 1Field-Fote EC. Combined use of body weight support, functional electric stimulation, and treadmill training to improve walking ability in individuals with chronic incomplete spinal cord injury. Arch Phys Med Rehabil. 2001;82:818–824. Abstract | Full Text |
Full-Text PDF (71 KB)
|
CrossRef
2. 2Field-Fote EC. Spinal cord control of movement: implications for locomotor rehabilitation following spinal cord injury. Phys Ther. 2000;80:477–484. MEDLINE 3. 3Washburn RA, Figoni SF. Physical activity and chronic cardiovascular disease prevention in spinal cord injury: a comprehensive literature review. Top Spinal Cord Injury Rehabil. 1998;3:16–32. 4. 4Gerhart KA, Bergstrom E, Charlifue SW, Menter RR, Whiteneck GG. Long-term spinal cord injury: functional changes over time. Arch Phys Med Rehabil. 1993;74:1030–1034. MEDLINE |
CrossRef
5. 5Jacobs PL, Nash MS, Rusinowski JW. Circuit training provides cardiorespiratory and strength benefits in persons with paraplegia. Med Sci Sports Exerc. 2001;33:711–717. MEDLINE 6. 6Castro MJ, Apple DF, Hillegass EA, Dudley GA. Influence of complete spinal cord injury on skeletal muscle cross-sectional area within the first 6 months of injury. Eur J Appl Physiol Occup Physiol. 1999;80:373–378. MEDLINE 7. 7Shields RK, Law LF, Reiling B, Sass K, Wilwert J. Effects of electrically induced fatigue on the twitch and tetanus of paralyzed soleus muscle in humans. J Appl Physiol. 1997;82:1499–1507. 8. 8Dobkin BH, Harkema S, Requejo P, Edgerton VR. Modulation of locomotor-like EMG activity in subjects with complete and incomplete spinal cord injury. J Neurol Rehabil. 1995;9:183–190. 9. 9Wirz M, Colombo G, Dietz V. Long term effects of locomotor training in spinal humans. J Neurol Neurosurg Psychiatry. 2001;71:93–96. MEDLINE |
CrossRef
10. 10Ivy JL, Goforth HW, Damon BM, McCauley TR, Parsons EC, Price TB. Early postexercise muscle glycogen recovery is enhanced with a carbohydrate-protein supplement. J Appl Physiol. 2002;93:1337–1344. 11. 11Ivy JL. Dietary strategies to promote glycogen synthesis after exercise. Can J Appl Physiol. 2001;26(Suppl):S236–S245. 12. 12Ivy JL. Glycogen resynthesis after exercise: effect of carbohydrate intake. Int J Sports Med. 1998;19(Suppl 2):S142–S145.
CrossRef
13. 13American College of Sports Medicine. In: Resource manual for guidelines for exercise testing and prescription. 7th ed.. Baltimore: Lippincott Williams & Wilkins; 2005;. 14. 14Wolfe RR. Protein supplements and exercise. Am J Clin Nutr. 2000;72:551S–557S. MEDLINE 15. 15Castro MJ, Apple DF, Staron RS, Campos GE, Dudley GA. Influence of complete spinal cord injury on skeletal muscle within 6 mo of injury. J Appl Physiol. 1999;86:350–358. 16. 16Burnham R, Martin T, Stein R, Bell G, MacLean I, Steadward R. Skeletal muscle fibre type transformation following spinal cord injury. Spinal Cord. 1997;35:86–91. MEDLINE 17. 17Castro MJ, Apple DF, Rogers S, Dudley GA. Influence of complete spinal cord injury on skeletal muscle mechanics within the first 6 months of injury. Eur J Appl Physiol. 2000;81:128–131. MEDLINE 18. 18Rochester L, Chandler CS, Johnson MA, Sutton RA, Miller S. Influence of electrical stimulation of the tibialis anterior muscle in paraplegic subjects. 1. Contractile properties. Paraplegia. 1995;33:437–449. MEDLINE 19. 19Andersen JL, Mohr T, Biering-Sorensen F, Galbo H, Kjaer M. Myosin heavy chain isoform transformation in single fibres from m. vastus lateralis in spinal cord injured individuals: effects of long-term functional electrical stimulation (FES). Pflugers Arch. 1996;431:513–518. MEDLINE |
CrossRef
20. 20Talmadge RJ, Castro MJ, Apple DF, Dudley GA. Phenotypic adaptations in human muscle fibers 6 and 24 wk after spinal cord injury. J Appl Physiol. 2002;92:147–154. 21. 21Castro MJ, Apple DF, Melton-Rogers S, Dudley GA. Muscle fiber type-specific myofibrillar Ca(2+) ATPase activity after spinal cord injury. Muscle Nerve. 2000;23:119–121.
CrossRef
22. 22Kjaer M, Dela F, Sorensen FB, et al. Fatty acid kinetics and carbohydrate metabolism during electrical exercise in spinal cord-injured humans. Am J Physiol Regul Integr Comp Physiol. 2001;281:R1492–R1498. MEDLINE 23. 23Hultman EH. Carbohydrate metabolism during hard exercise and in the recovery period after exercise. Acta Physiol Scand Suppl. 1986;556:75–82. MEDLINE 24. 24Kim CK, Bangsbo J, Strange S, Karpakka J, Saltin B. Metabolic response and muscle glycogen depletion pattern during prolonged electrically induced dynamic exercise in man. Scand J Rehabil Med. 1995;27:51–58. MEDLINE 25. 25Lees SJ, Franks PD, Spangenburg EE, Williams JH. Glycogen and glycogen phosphorylase associated with sarcoplasmic reticulum: effects of fatiguing activity. J Appl Physiol. 2001;91:1638–1644. 26. 26Sinacore DR, Delitto A, King DS, Rose SJ. Type II fiber activation with electrical stimulation: a preliminary report. Phys Ther. 1990;70:416–422. MEDLINE 27. 27Doyle JA, Sherman WM, Strauss RL. Effects of eccentric and concentric exercise on muscle glycogen replenishment. J Appl Physiol. 1993;74:1848–1855. 28. 28van Loon LJ, Saris WH, Kruijshoop M, Wagenmakers AJ. Maximizing postexercise muscle glycogen synthesis: carbohydrate supplementation and the application of amino acid or protein hydrolysate mixtures. Am J Clin Nutr. 2000;72:106–111. MEDLINE 29. 29Rasmussen BB, Tipton KD, Miller SL, Wolf SE, Wolfe RR. An oral essential amino acid-carbohydrate supplement enhances muscle protein anabolism after resistance exercise. J Appl Physiol. 2000;88:386–392. 30. 30Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M. Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol. 2001;535:301–311. MEDLINE |
CrossRef
31. 31Biolo G, Declan Fleming RY, Wolfe RR. Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. J Clin Invest. 1995;95:811–819. MEDLINE |
CrossRef
32. 32Biolo G, Tipton KD, Klein S, Wolfe RR. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol. 1997;273:E122–E129. MEDLINE 33. 33Field-Fote EC, Lindley SD, Sherman AL. Locomotor training approaches for individuals with spinal cord injury: a preliminary report of walking-related outcomes. J Neurol Phys Ther. 2005;29:127–137. MEDLINE 34. 34Dietz V, Nakazawa K, Wirz M, Erni T. Level of spinal cord lesion determines locomotor activity in spinal man. Exp Brain Res. 1999;128:405–409. MEDLINE |
CrossRef
35. 35Field-Fote E. Spinal cord stimulation facilitates functional walking in a chronic, incomplete spinal cord injured subject [letter]. Spinal Cord. 2002;40:428. MEDLINE |
CrossRef
36. 36Harkema SJ, Hurley SL, Patel UK, Requejo PS, Dobkin BH, Edgerton VR. Human lumbosacral spinal cord interprets loading during stepping. J Neurophysiol. 1997;77:797–811. MEDLINE 37. 37Wernig A, Nanassy A, Muller S. Laufband (treadmill) therapy in incomplete paraplegia and tetraplegia. J Neurotrauma. 1999;16:719–726. MEDLINE |
CrossRef
38. 38Dietz V, Wirz M, Colombo G, Curt A. Locomotor capacity and recovery of spinal cord function in paraplegic patients: a clinical and electrophysiological evaluation. Electroencephalogr Clin Neurophysiol. 1998;109:140–153. MEDLINE 39. 39Hesse S. Locomotor therapy in neurorehabilitation. NeuroRehabilitation. 2001;16:133–139. MEDLINE 40. 40Evans WJ. Protein nutrition and resistance exercise. Can J Appl Physiol. 2001;26(Suppl):S141–S152. 41. 41Joint Position Statement: Nutrition and athletic performance. American College of Sports Medicine, American Dietetic Association, and Dietitians of Canada. Med Sci Sports Exerc. 2000;32:2130–2145. MEDLINE |
CrossRef
42. 42Position of the American Dietetic Association, Dietitians of Canada, and the American College of Sports Medicine (Nutrition and athletic performance). J Am Diet Assoc. 2000;100:1543–1556. Abstract | Full Text |
Full-Text PDF (1779 KB)
|
CrossRef
43. 43Norman KE, Pepin A, Barbeau H. Effects of drugs on walking after spinal cord injury. Spinal Cord. 1998;36:699–715. MEDLINE 44. 44Signorile JF, Banovac K, Gomez M, Flipse D, Caruso JF, Lowensteyn I. Increased muscle strength in paralyzed patients after spinal cord injury: effect of beta-2 adrenergic agonist. Arch Phys Med Rehabil. 1995;76:55–58. Abstract |
Full-Text PDF (408 KB)
|
CrossRef
45. 45Jacobs 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. Abstract | Full Text |
Full-Text PDF (56 KB)
|
CrossRef
46. 46Kendall RW, Jacquemin G, Frost R, Burns SP. Creatine supplementation for weak muscles in persons with chronic tetraplegia: a randomized double-blind placebo-controlled crossover trial. J Spinal Cord Med. 2005;28:208–213. MEDLINE 47. 47Nieshoff EC, Birk TJ, Birk CA, Hinderer SR, Yavuzer G. Double-blinded, placebo-controlled trial of midodrine for exercise performance enhancement in tetraplegia: a pilot study. J Spinal Cord Med. 2004;27:219–225. MEDLINE 48. 48Ditor DS, Kamath MV, Macdonald MJ, Bugaresti J, McCartney N, Hicks AL. Reproducibility of heart rate variability and blood pressure variability in individuals with spinal cord injury. Clin Auton Res. 2005;15:387–393. MEDLINE |
CrossRef
a Department of Neurological Surgery, Miller School of Medicine, University of Miami, Miami, FL b Department of Rehabilitation Medicine, Miller School of Medicine, University of Miami, Miami, FL c Department of Physical Therapy, Miller School of Medicine, University of Miami, Miami, FL d The Miami Project to Cure Paralysis, Miller School of Medicine, University of Miami, Miami, FL e Sargent College of Health and Rehabilitation Sciences, Boston University, Boston, MA.  Reprint requests to Mark S. Nash, PhD, Dept of Neurological Surgery, University of Miami, Miller School of Medicine, 1095 NW 14th Ter, R-48, Miami, FL 33136.
Supported by the Miami Project to Cure Paralysis. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/ are associated. PII: S0003-9993(06)01520-6 doi:10.1016/j.apmr.2006.11.012 © 2007 American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation. Published by Elsevier Inc. All rights reserved. | |
|
FULL TEXT
01520-6/journalimage?img=PIIS0003999306015206.gr1.lrg.gif&fig=fig1&kwhquery=&issn=0003-9993&ishighres=false&allhighres=false&free=yes','journalimage');)
01520-6/journalimage?img=PIIS0003999306015206.gr2.lrg.gif&fig=fig2&kwhquery=&issn=0003-9993&ishighres=false&allhighres=false&free=yes','journalimage');)
01520-6/journalimage?img=PIIS0003999306015206.gr3.lrg.gif&fig=fig3&kwhquery=&issn=0003-9993&ishighres=false&allhighres=false&free=yes','journalimage');)