Persons with spinal cord injury (SCI) are characterized as leading relatively inactive sedentary lives. This population also displays significantly greater incidences of health risk factors such as obesity, dyslipidemia, hypertension, and insulin resistance compared with the general population (7). Related to the increased risk factor incidences and low activity levels, individuals with SCI are far more likely to develop serious medical complications including diabetes and heart disease (8). It is crucial to implement adjustments in the daily behavior of persons with SCI to increase activity levels and reduce health risk factors with the aim of reducing the rates of cardiovascular disease and diabetes and enhancing quality of life.
Persons with SCI face considerable challenges in the performance of important activities of daily living (ADL). The ability to perform ADL, such as body weight transfers and wheelchair propulsion up an incline, requires repeated high-intensity muscular efforts of the upper extremities (20). The intensity of ADL performed by persons with SCI is generally not strenuous enough to maintain or elicit improvements in either cardiorespiratory fitness or muscular strength (20). Therefore, to enhance cardiorespiratory and muscular fitness, and possibly reduce the incidence of medical complications, persons with SCI must participate in structured exercise activities. Unfortunately, individuals with SCI have limited options for exercise, with arm ergometry being one of the most common modes available (25).
Adaptations that occur in response to exercise training are primarily dependent on the intensity and mode of exercise performed (14,15). Endurance training (ET) generally involves the performance of high-repetition low-intensity exercise of large muscle groups for extended periods with a primary objective of enhanced cardiovascular functioning (10,14,15). However, endurance training results in little or no increases in maximal force output of the muscles (14). In contrast, resistance training (RT) is an effective means to increase the maximal force output of the muscles via high-intensity low-repetition exercise (10,14,15). Programs of RT are generally considered to provide minimal, if any, improvements in maximal aerobic capacity; however, research does indicate that some modes of RT can result in significant improvements in cardiorespiratory fitness in individuals with SCI paraplegia (19).
Although many studies have examined the effects of ET on cardiorespiratory fitness in persons with SCI (6,11,16,29,34), few studies have investigated the application of RT in this population (4,6,24). An early study performed by Nilsson et al. (25) examined the effects of a program consisting arm RT and arm cranking designed to enhance walking with crutches and long-leg braces. Results of this combination of RT and ET program included enhanced V˙O2peak, increased dynamic strength, and increased muscular endurance. Cooney and Walker (4) applied a 9-wk program of concentric RT in 10 persons with SCI using hydraulic resistance devices and reported significant increases in V˙O2peak and power output during arm crank testing. Another study indicated that RT with elastic bands reduced upper extremity pain, but muscular strength and cardiovascular outcomes were not reported (5). Thus, the limited studies that have applied RT in persons with SCI have not examined the effects on muscular strength, muscular power, and work capacity (as indicated by V˙O2peak). Moreover, the effects of RT have not been investigated in this population in comparison with the standard exercise modality available, namely, ET arm cranking. Therefore, the purpose of the current study was to compare the training effects of 12 wk of RT with the effects of 12 wk of ET regarding values of V˙O2peak, upper extremity strength, and power output in persons with chronic SCI paraplegia.
METHODS
Eighteen individuals (12 males and 6 females) with complete motor paraplegia (T6-T10) volunteered to serve as subjects for this investigation. Injury level and degree of completeness were determined from a motor and sensory physical examination before study inclusion, using the International Standards for Neurological Classification of Spinal Injury (2). Subjects were apparently healthy and were not taking any medications that would affect the results of this study. All testing procedures were verbally explained in detail, and subjects signed written informed consent documents approved by the Institutional Medical Sciences Subcommittee for the Protection of Human Subjects.
Study design.
All research subjects participated in a series of testing sessions before and after a 12-wk training period. The assessment battery included a graded exercise test (GXT) to determine aerobic capacity, dynamic strength testing, and arm Wingate testing to assess upper extremity power output. Subjects were matched into pairs by gender, age, and body mass and were then randomly assigned, by pairs, into either an RT or an ET group. Descriptive characteristics of the subjects assigned to the two study groups are shown in Table 1. All subjects were scheduled for three training sessions weekly during a 12-wk study period.
;)
TABLE 1: Characteristics of subjects in the resistance training (RT) group and the endurance training (ET) group.
Testing protocols.
The upper extremity GXT were performed to determine peak metabolic responses to arm cranking exercise using a discontinuous, multistage, progressive protocol with a Monark 881 Rehab Trainer arm ergometer (Monark, Varberg, Sweden). The subjects performed the GXT while seated in their own wheelchairs situated such that their elbows were slightly flexed (<10°) at the point of furthest arm extension. The ergometer was equipped with a metronome that assisted the subjects in maintaining the assigned cranking pace of 50 rpm for the duration of the test. The initial 3-min stage was performed at a power output of 30 W with the power output increased by 10 W per the subsequent 3-min stage. Oxygen consumption was continuously monitored via open circuit spirometry (Vmax 229 System; SensorMedics, Loma Linda, CA) and HR was collected during the final 20 s of each stage via a 12-lead EKG (Cardiosoft; SensorMedics, Yorba Linda, CA). Immediately after each stage, the subjects were asked to indicate the level of exertion on a 6- to 20-point RPE scale (3). Termination points for the GXT were in accordance with the Guidelines of Graded Exercise Testing and Prescription (5th ed.) (1).
Upper extremity dynamic strength was assessed in all subjects before and after the 12-wk training period. The strength testing was performed on the same system used in the RT program, Hammer Strength MTS equipment (Hammer Strength, Franklin, IL). The resistance levels were progressively increased during the strength tests until the subjects were able to complete at least three but no more than eight repetitions with good technique and control. The 1RM values were then calculated using the Mayhew regression equation (23).
Upper extremity power was assessed via arm Wingate anaerobic testing (WAnT). A Monark 834E leg cycle ergometer (Monark) was adapted for arm cranking (18). SMI OptoSensor 2000 (Sports Medicine Industries, Inc., St. Cloud, MN) was used to determine values of anaerobic power including peak power (Ppeak), the highest greatest power output measured during any 5-s period of the WAnT, and mean power (Pmean), the average power output during the 30-s trial. After a 3-min unloaded warm-up period, subjects were directed to increase their pedaling cadence to their maximal unloaded pace. A resistance load equivalent to 3.5% of body mass was then applied and the subject was then directed to crank as rapidly as possible for the 30-s period. This protocol has been shown to provide the optimal levels of power output and to allow reliable measurement of anaerobic power when testing upper extremities in persons with paraplegia (17).
Training protocols.
All subjects participated in three training sessions per week during the 12-wk study period, typically on a Monday, Wednesday, and Friday basis. The subjects assigned to the ET group performed 30 min of arm cranking exercise using a Saratoga arm crank device during each session (Rand-Scot, Inc, Fort Collins, CO). Subjects in this group were directed to exercise at an effort level that produced HR levels equivalent to 70% to 85% of the HRpeak values determined during the pretraining GXT. During the ET sessions, subjects were provided with a HR band monitor and wristwatch receiver unit to guide the exercise intensity (Polar Electro, Inc, Lake Success, NY). The subjects assigned to the RT group performed three sets of 10 repetitions on each of six Hammer Strength MTS exercise stations including horizontal press, horizontal row, overhead press, overhead pull, seated dips, and arm curls. These stations had been slightly modified to allow direct wheelchair access. Exercise intensity (weights used) for the RT group was based on function of the 1RM assessments, i.e., as percentages of peak strength values for each exercise movement as measured before the study and during the last session of the fourth and eight weeks of training. Resistance levels were set in three 4-wk training cycles, where the training weights assigned gradually increased in a weekly fashion during the 4-wk periods and were equivalent to 60%, 65%, 70%, and 70% of the 1RM for each training movement.
Statistics.
Outcome variables were compared between groups (RT and ET) and across time (before and after training) using two-way ANOVA for repeated measures. Results were expressed as mean ± SD. Statistical significance was accepted at the P < 0.05 level.
RESULTS
Statistical analyses revealed significant effects of both modes of training (RT and ET) in the physiological responses to peak GXT. Peak physiological responses to GXT are displayed in Table 2. There were statistically significant increases in V˙O2peak in both groups after training (P < 0.05). The RT and ET groups displayed 15.1% and 11.8% increases in V˙O2peak, respectively, with no significant differences observed between groups. Peak values of minute ventilation (V˙E) and HR reached during GXT were not significantly altered with training. Moreover, RPE responses at the point of peak physiological effort were not significantly affected by training.
TABLE 2: Peak responses to graded exercise testing in persons with paraplegia before and after participation in either 12 wk of resistance training (RT) or 12 wk of endurance training (ET).
Table 3 presents the pretraining and posttraining values of power output determined during WAnT. After 12 wk of training, both study groups (ET and RT) displayed significant increases in Ppeak and Pmean (P < 0.05). Mean power increased 8% and 5% for the RT and ET groups, respectively, with no statistically significant differences apparent between groups. Whereas RT and ET both produced significant enhancement of Ppeak (P < 0.05), the RT produced significantly greater gains (15.6%) compared with ET (2.6%).
TABLE 3: Results of upper extremity Wingate anaerobic power testing in persons with paraplegia before and after participation in either 12 wk of resistance training (RT) or 12 wk of endurance training (ET).
Values of upper extremity dynamic strength determined before and after participation in RT or ET are shown in Table 4. The RT group displayed significantly increased strength values for all the exercise maneuvers (P < 0.01). The strength gains of the RT group varied from 34% to 55% for the six exercise maneuvers. In contrast, the ET group did not display increases in muscular strength for any of the six exercises after 12 wk of training.
TABLE 4: Results of isotonic strength testing in persons with paraplegia before and after participation in either 12 wk of resistance training (RT) or 12 wk of endurance training (ET).
DISCUSSION
The results of this study demonstrate that participation in RT can produce significant increases in work capacity, apparently through enhancements of muscular strength and anaerobic power in persons with SCI. The improvements in strength and power after RT are not unexpected. Previous strength training studies in the SCI population have reported the expected significant increases in muscular strength and endurance (4,13,19,25). However, the improvements in V˙O2peak after RT are quite considerable as they tend to refute the laws of the specificity of training. The average increase in V˙O2peak achieved by the RT group (13.1%) in the current study was greater than the cardiorespiratory enhancements previously reported after most programs of low-intensity long-duration ET (6,11,25,29,34).
Resistance training has been shown to improve anaerobic power through adaptations in both the central nervous system and the peripheral muscle system (22). Central neurological adaptations that may result from RT include improved motor unit activation and synchronization, improved force development, and improved reflex activity (21,22,30). Peripheral adaptations of the muscular system that may occur as a result of RT include increased activity of anaerobic enzymes and increased muscle fiber cross-sectional area (21,22). In contrast, RT is generally not associated with increases in capillary density, which suggests that oxygen diffusion and delivery in the working musculature remains at pretraining values. Research has indicated that improvements in endurance performance after RT are likely due to neural adaptations (27).
In marked contrast to RT, long-term ET significantly increases capillary and mitochondrial density, oxidative enzyme activity, and intramuscular substrate stores while concomitantly reducing the activity of the glycolytic enzymes (9,14). Similar to RT, long-term ET alters the size and ratio of Type II muscle fibers. Research has found that the cross-section area of the Type II fibers decrease while the ratio of Type IIa to Type IIb increase after ET, reflecting a muscle fiber transformation in the trained musculature (31). In addition, ET changes the contractile properties of the trained musculature as it reduces the maximum shortening velocity of the Type II muscle fibers and reduces the maximal tension that can be developed in all muscle fiber types (33). Collectively, the alterations in muscle fiber size, ratio, and contractile properties reduce the peak force-generating capability of the trained musculature. Therefore, the muscular adaptations that occur after long-term ET facilitate aerobic processes. It is important to note that these studies were performed in persons without disability and generally examined lower extremity functioning. However, it seems reasonable to consider the findings of these studies to persons with SCI when their training uses neurologically intact musculature above the level of the spinal lesion.
Both training study groups, RT and ET, presented similar improvements in work capacity, as indicated by V˙O2peak, as a result of participation in very different exercise strategies. The subjects in the RT group also presented significant enhancement of upper extremity muscular strength and power. The dissimilar training effects of the two modes of training regarding strength and power suggest that although the cardiorespiratory responses are similar in magnitude, they likely result from two very different sets of physiological adaptations. It seems evident that arm ET would enhance cardiorespiratory function by improvements in cardiovascular, muscular, and metabolic responses to exercise (12). However, the sources of the cardiorespiratory benefits of upper extremity RT are less obvious. It has been shown that central factors such as cardiorespiratory fatigue are generally not the reason individuals reach voluntary exhaustion during peak arm ergometry but rather peripheral factors that actually regulates UE exercise capacity (28). The general reason cited for test termination during arm GXT is local muscle fatigue, commonly in the triceps muscles. Enhanced muscle function in the upper extremities may allow greater levels of power output to be reached (more exercise test stages) thereby requiring greater levels of oxygen uptake to supply the needed energy stores to the muscles under stress. Thus, the increased values of V˙O2peak after RT in this study are likely, to a great extent, a function of improved upper extremity force generation related to neurological and anaerobic metabolism adaptations. The lack of significant increases in V˙Epeak after either RT or ET suggests that the observed increases in work capacity were due to adaptations other than increased peak respiratory flow. The findings of the present study are supported by the work of Miles et al. (24) who reported significant increases of V˙O2peak (26%) in a group of wheelchair athletes after an endurance training program. Those athletes did not display increases in lung volume measures indicating to those authors that other physiological mechanisms were responsible for the increases in work capacity.
The findings of the present investigation must be considered regarding the subject population, the training interventions, and the testing protocols. The subjects in this study were persons with motor complete SCI paraplegia (T6-T10) which may, to some degree, limit the ability to generalize to other populations. For example, the decreased ability to stabilize the lower body during the upper extremity GXT may affect the testing outcomes. Exercise with the upper body, in general, is known to differ in many regards from lower extremity training. Sawka (32) discussed the unique physiological responses to upper extremity exercise, outlining several factors that might have contributed to the unexpected findings of the present study. First, the GXT in the present study were performed using a discontinuous protocol, which is the common approach with arm cranking testing to obtain electrocardiography measurements without the electrical discharge associated with intense muscular efforts. Discontinuous protocols may lessen local muscle fatigue (the primary reason for arm crank test termination) thereby affecting peak performance. Sawka (32) suggested that the low efficiency of muscle contraction during arm cranking may indicate a greater role of fast-twitch muscle fiber with potentially earlier recruitment of those fibers during upper extremity exercise. Finally, total peripheral resistance is greater for arm exercise requiring a greater percentage of maximal muscle tension in smaller muscles to overcome compression of the peripheral vasculature.
A direct association between upper extremity strength and peak oxygen uptake in persons with paraplegia is not unsupported. Zoeller et al. (35) examined the potential relationships among measures of upper extremity isokinetic strength, values of V˙O2peak and lactate threshold as established with arm ergometry testing, and endurance performance. Their study indicated that muscular strength is directly associated with aerobic capacity in persons with paraplegia. It was suggested that greater values of muscular strength could possibly allow greater levels of cardiorespiratory stress as a result of enhanced resistance to local muscle fatigue. The present investigation did in fact examine that suggestion, finding that RT can provide increased work capacity in addition to the expected enhancements of muscular strength and power.
The significant changes in V˙O2peak after both RT and ET in this study might suggest that a sole training strategy designed to provide the physiological adaptations of the two exercise approaches may provide even greater benefits. However, simultaneously participation in both RT and ET has been shown to limit increases in muscular strength in persons without disability (10,14,15). A novel form of RT, circuit resistance training (CRT), has been shown by these researchers to provide dramatically greater improvements in V˙O2peak (26%) than either RT or ET in persons with paraplegia (19). This form of training combines a series of paired RT stations with exercise intervals using standard ET equipment, at a rapid pace of movement but with minimal resistance levels. In addition, CRT has been shown to not only stimulate anaerobic metabolism but to also provide continual cardiorespiratory stress throughout each training session (19). However, controlled randomized studies must be performed to allow comparison of the exercise benefits among CRT, RT, and ET.
Research has shown that individuals with SCI lead relatively sedentary lives, which is responsible for the poor fitness levels and increased risk of cardiovascular disease in these individuals (8). For example, one quarter of individuals with SCI paraplegia are unable to successfully perform most of their ADL because of inadequate cardiorespiratory fitness (18,26). Common ADL such as body weight transfers and wheelchair propulsion over uneven surfaces or up inclines require high-intensity short-duration muscular efforts (17). Therefore, it is obvious that greater emphasis needs to be placed on developing muscular strength and power in this population because this will improve their ability to complete ADL. More importantly, however, are the several major risk factors commonly observed in individuals with SCI that have been shown to increase the rate of developing cardiovascular disease, which includes dyslipidemia, hypertension, insulin resistance, and an increase in percent body fat. Therefore, strength, power, and cardiorespiratory fitness are vital for this population. This study is significant because it demonstrates that RT provides important benefits in cardiorespiratory fitness, muscular strength, and muscular power. Therefore, it seems that individuals with SCI may benefit from a single mode of exercise training (RT) because it provides not only muscular strength and power benefits but also cardiorespiratory benefits.
CONCLUSION
Although the American College of Sports Medicine recommends that individuals should include resistance training in their exercise program, limited studies have examined the effectiveness of resistance training to improve work capacity, particularly in the population with SCI. The findings of the present study indicate that chronic survivors of SCI paraplegia can safely and significantly improve their upper extremity work capacity, strength, and power output through the participation in short-term RT.
Funding was not provided by any governmental agency or foundation for the performance of this study. The results of the present study do not constitute any endorsement by the ACSM.
The author acknowledges Edward T. Mahoney and Bradley M. Johnson for their assistance with the training interventions and testing procedures.
REFERENCES
1. American College of Sports Medicine.
Guidelines for Exercise Testing and Prescription. 6th ed. Baltimore (MD): Lippincott, Williams & Wilkins; 2006. p. 106.
2. American Spinal Injury Association.
International Standards for Neurological Classification of Spinal Cord Injury, Revised. Chicago (IL): American Spinal Injury Association; 2002. p. 1-17.
3. Borg GAV.
Borg's Perceived Exertion and Pain Scale. Champaign (IL): Human Kinetics; 1998. p. 54-62.
4. Cooney MM, Walker JB. Hydraulic resistance exercise benefits cardiovascular fitness of spinal cord injured.
Med Sci Sport Exerc. 1986;18(5):522-5.
5. Curtis KA, Drysdale GA, Lanza RD, et al. Shoulder pain in wheelchair users with tetraplagia and paraplegia.
Arch Phys Med Rehabil. 1999;80:453-7.
6. Davis GM, Kofsky PR, Kelsey JC, Shephard RJ. Cardiorespiratory fitness and muscular strength of wheelchair users.
Can Med Assoc J. 1981;125(12):1317-23.
7. DeVivo ML, Black KL, Stover SL. Causes of death during the first 12 years after spinal cord injury.
Arch Phys Med Rehabil. 1993;74:248-54.
8. DeVivo MJ, Schechuk RM, Stover SL, Black KL, Go BK. A cross-sectional study of the relationship between age and current health status for persons with spinal cord injuries.
Paraplegia. 1992;30:820-7.
9. Dudley GA, Djamil R. Incompatibility of endurance- and strength-training modes of exercise.
J Appl Physiol. 1985;59(5):1446-51.
10. Dudley GA, Fleck SJ. Strength and endurance training; are they mutually exclusive.
Sports Med. 1987;4:79-85.
11. Franklin BA. Exercise testing, training and arm ergometry.
Sports Med. 1985;2:100-19.
12. Green H, Jones S, Ball-Burnett ME, Smith D, Livesey J, Farrance BW. Early muscular and metabolic adaptations to prolonged exercise training in humans.
J Appl Physiol. 1991;70:2032-8.
13. Hicks AL, Martin KA, Ditor DS, et al. Long-term exercise training in persons with spinal cord injury: effects on strength, arm ergometry performance and psychological well-being.
Spinal Cord. 2003;41(1):34-43.
14. Hickson RC. Interference of strength development by simultaneously training for strength and endurance.
Eur J Appl Physiol. 1980;45:255-63.
15. Hickson RC, Dvorak BA, Gorostiaga EM, Kurowski TT, Foster C. Potential for strength and endurance training to amplify endurance performance.
J Appl Physiol. 1988;65(5):2285-90.
16. Hooker SP, Wells CL. Effects of low- and moderate-intensity training in spinal cord-injured persons.
Med Sci Sports Exerc. 1989;21(1):18-22.
17. Jacobs PL, Mahoney ET, Johnson BM. Reliability of arm Wingate anaerobic testing in persons with complete paraplegia.
J Spinal Cord Med. 2003;26(3):141-4.
18. Jacobs PL, Nash MS. Exercise recommendations for individuals with spinal cord injury.
Sports Med. 2004;34(11):727-51.
19. Jacobs PL, Nash MS, Rusinowski JW. Circuit training provides cardiorespiratory and strength benefits in persons with paraplegia.
Med Sci Sports Exerc. 2001;33(5):711-7.
20. Janssen TW, van Oers CA, van der Woude LH, Hollander AP. Physical strain in daily life of wheelchair users with spinal cord injuries.
Med Sci Sports Exerc. 1994;26(6):661-70.
21. Jung AP. The impact of resistance training on distance running performance.
Sports Med. 2003;33(7):539-52.
22. Kraemer WJ, Descchenes MR, Fleck SJ. Physiological adaptations to resistance exercise: implications for athletic conditioning.
Sports Med. 1988;6:246-56.
23. Mayhew JL, Ball TE, Bowen JC. Relative muscular endurance performance as a predictor of bench press strength in college men and women.
Sports Med Train Rehabil. 1992;3:195-201.
24. Miles DS, Sawka MN, Wilde SW, Durbin RJ, Gotshall RW, Glaser RM. Pulmonary function changes in wheelchair athletes subsequent to exercise training.
Ergonomics. 1982;25:239-46.
25. Nilsson S, Staff PH, Pruett ED. Physical work capacity and the effect of training on subjects with long-standing paraplegia.
Scan Rehabil Med. 1975;7:51-6.
26. Noreau L, Shephard RJ, Simard C, Pare G, Pomerleau P. Relationship of impairment and functional ability to habitual activity and fitness following spinal cord injury.
Int J Rehabil Res. 1993;16(4):265-75.
27. Paavolainen L, Hakkinen K, Hamalainen I, Nummela A, Rusko H. Explosive-strength training improves 5-km running time by improving running economy and muscle power.
J Appl Physiol. 1999;86(5):1527-33.
28. Phillips WT, Kiratli BJ, Sarkatati M, et al. Effect of spinal cord injury on the heart and cardiovascular fitness.
Curr Probl Cardiol. 1998;23(11):641-716.
29. Pollock ML, Miller HS, Linnerud AC, Laughridge E, Coleman E, Alexander E. Arm pedaling as an endurance training regimen for the disabled.
Arch Phys Med Rehabil. 1974;55(9):418-24.
30. Sale DG. Neural adaptation to resistance training.
Med Sci Sports Exerc. 1988;20(5):S135-45.
31. Saltin B, Gollnick PD. Skeletal muscle adaptability: significance for metabolism and performance. In: Peachey LD, Adrian RH, Geiger SR, editors.
Handbook of Physiology. Bethesda (MD): American Physiological Society; 1983, p. 555-631.
32. Sawka MS. Physiology of upper body exercise.
Exerc Sport Sci Rev. 1986;14:175-211.
33. Tanaka H, Swensen T. Impact of resistance training on endurance performance: a new form of cross training?
Sports Med. 1998;25(3):191-200.
34. Taylor AW, McDonell E, Brassard L. The effects of an arm ergometer training programme on wheelchair subjects.
Paraplegia. 1986;24:105-14.
35. Zoeller RF, Riechman SE, Dabayebeh IM, Goss FL, Robertson RJ, Jacobs PL. Relationship between muscular strength and cardiorespiratory fitness in people with thoracic-level paraplegia.
Arch Phys Med Rehabil. 2005;86(7):1441-6.
