Aerobic exercise requires sufficient ventilation to provide oxygen to working muscles (22). In most able-bodied individuals, ventilatory capacity is more than adequate to meet metabolic demands for all exercise intensities (10,22). However, some highly trained individuals demonstrate a mismatch between the increased ability of the skeletal muscle to consume oxygen and ventilatory capacity (13). By contrast, those with a spinal cord injury (SCI) are unlikely to demonstrate a mismatch even after training because of significant skeletal muscle denervation, which reduces O2 demand dramatically. Even in high-level injuries, the limitation to total oxygen consumption during exercise is skeletal muscle mass, despite significant respiratory muscle denervation. This is due to the proportional denervation of both skeletal and pulmonary muscles such that the respiratory system still has ample capacity to cope with the demands of arms-only exercise, even after training (27).
To augment aerobic capacity for persons with SCI, functional electrical stimulation (FES) of the legs has been combined with voluntary upper body exercise to create a hybrid FES exercise to allow engagement of more muscle mass (16,21,37). In addition, this exercise creates a leg muscle pump in synchrony with the upper body work, potentially aiding cardiac output in response to exercise (5). Moreover, arms-only exercise in SCI can be limited by the inability to vasconstrict in the nonactive legs (31), whereas hybrid FES exercise obviates the need for this vasoconstriction (30). The normally “wasted” blood flow to the legs serves a purpose to allow for increased oxygen consumption (6,7,29). In fact, regular FES training can result in a reduction in the normally strong inverse relationship between injury level and peak aerobic capacity (28). Our previous work showed that FES-row training (FES-RT) in individuals with low-level injuries effectively improved aerobic capacity to the point that it was no longer related to injury level (28). However, for individuals with injuries above T3, respiratory capacity is much more compromised and is proportional to the injury level (4,34). Hence, the increase in ventilatory requirements with FES training could result in an imbalance between ventilatory capacity and greater whole body skeletal muscle demand after FES-RT.
We hypothesized that peak ventilation would be a key factor in determining the aerobic capacity that could be achieved with FES-RT for individuals with injuries above T3. We assessed oxygen consumption and ventilation during FES-rowing exercise in 12 volunteers with spinal cord injuries at T2 and above before and after 6 months of FES-RT and investigated the relationship between aerobic capacity, peak ventilation, and injury level. In addition, we determined oxygen uptake efficiency slope (OUES), an objective and reproducible measure of cardiopulmonary reserve (1,18), to examine the integrated function of the cardiovascular, pulmonary, and musculoskeletal systems during exercise.
Twelve individuals (one female) with incomplete and complete SCI at T2 and above participated in this study. The mean age was 33.3 ± 3.8 yr (22–60), and the mean BMI was 23.5 ± 1.1 kg·m−2 (18.1–29.7). Time since injury ranged from 0.33 to 33 yr and averaged 8.3 ± 3.3 yr. Three individuals were older than 35 yr, six had BMI in the category of overweight, and eight had a time since injury less than 10 yr. None of the subjects smoked, had a history of any cardiovascular or pulmonary disease, or were taking cardioactive medications. Each subject gave written informed consent as approved by the Institutional Review Board at Spaulding Rehabilitation Hospital. Before the study, all participants completed a healthy history and were classified by an experienced physician according to the American Spinal Injury Association impairment scale.
To be able to perform functional movements for rowing, subjects underwent preliminary FES strength training before FES-RT. Pairs of electrodes placed over the motor points of the right and left quadriceps and hamstring muscles were attached to the four-channel electrical stimulator (Odstock, Salisbury, United Kingdom). Stimulation parameters were set at a 1-s contraction with a 6-s rest for alternating muscles with an electrically stimulated knee extension followed by knee flexion. The intensity of stimulation to the quadriceps was increased to a level producing full knee extension; if full extension was not produced, the stimulation intensity was increased up to maximal (110 mA). Subjects trained three times weekly and only advanced to FES-RT when 30 min of full knee extension was achieved (2–12 wk of strength training). Subsequently, subjects underwent FES-RT three times weekly. A detailed explanation of the FES-rowing device has been described previously (29). Basically, an existing rower (Concept, Morrisville, VT) with a seating system for stability was used with an electrical stimulator (Odstock). The stimulator was connected to a button on the handle of the rower, allowing the exercising individual to synchronize the voluntarily controlled upper body with the FES-controlled legs to produce a rowing stroke. Participants began with short intervals of FES-RT interspersed with rest intervals and/or arms-only rowing depending on fitness level and the response to the FES, for a training session of 30 min. Each individual was expected to engage in three sessions per week for 6 months with the goal of reaching an exercise intensity of 75%–85% of HRpeak for a continuous 30 min. Training data were monitored on a weekly basis.
Aerobic capacity testing
Once individuals were able to perform more than 10 min of continuous FES rowing, the first graded exercise test was performed. This test was repeated after 6 months of training. Before the test, subjects refrained from food for 2 h, from caffeine and alcohol for 24 h, and from vigorous physical activity for 48 h. The FES-rowing protocol was individualized to the fitness level of each individual with work progression specific to each subject. In general, work output increased every 1 to 2 min until volitional exhaustion with a total testing time between 8 and 12 min. Online computer-assisted open circuit spirometry (ParvoMedics, Sandy, UT) was used to determine O2 consumption (V˙O2), CO2 production, and RER. Expired O2 and CO2 gas fractions were measured with a paramagnetic O2 and infrared CO2 analyzers. Ventilation (V˙E) was measured via a Hans Rudolph 3813 pneumotachograph. Tidal volume (V T) was obtained by integration of the flow signal. An HR monitor (Suunto, Vantaa, Finland) was used throughout the test. To determine whether maximal exercise capacity was reached, at least three of the following criteria had to be met: 1) an RER value of 1.1 or higher, 2) a plateau in V˙O2 despite increasing workload, 3) 85% of age-predicted maximal HR (220 − age), 4) a subjective RPE with a Borg scale of 17 or higher, and 5) a precipitous decline in power >20 W during maximal leg stimulation. Because there are no explicit HRpeak parameters for those with higher-level injuries, we used the standard approach to exercise testing of 220 − age. In fact, only those with SCI at level T2 achieved this HRpeak.
Data and statistical analysis
Values for peak aerobic capacity (V˙O2peak), peak ventilation (V˙Epeak), peak tidal volume (V Tpeak), peak breathing frequency (BFpeak), RERpeak, and HRpeak were derived from the highest average 30-s value obtained during the exercise test, usually the final 30 s or within the final workload. In addition, breath-by-breath V˙O2 and V˙E were averaged for 10-s periods to derive the OUES for each individual. This measure has been established in healthy subjects (2,17), children (3), and adult patients with cardiac or other metabolic diseases (11,32,33). OUES was calculated as follows: V˙O2 = OUESlog10V˙E + constant. OUES represents the rate of increases in V˙O2 in relation to increasing V˙E. Thus, a steeper slope indicates greater oxygen uptake for any given amount of ventilation during exercise. To determine the effect of 6 months of FES-RT, a paired Student t-test was used to compare pre- and posttraining values. Relations among injury level, V˙Epeak, V Tpeak, and V˙O2peak were determined via linear regressions. The injury score was derived from the injury level (C4–5, C5–6, C6–7, C7–8, and T2–10) and did not account for grade of injury. Rowing sessions per week across training months were analyzed by a one-way repeated-measures ANOVA. A two-way repeated-measures ANOVA was used to assess the effects of 6 months of FES-RT on the tidal volume and breathing frequency responses to the graded maximal exercise test as a function of relative exercise intensity (%V˙O2peak). Significance was set at P < 0.05. All results are presented as mean ± SEM.
Body mass did not change from pre- to posttraining periods, averaging 72.5 ± 3.89 versus 73.3 ± 4.19 kg. Compliance to the 6-month training program averaged 1.8 ± 0.2 rowing sessions per week, which corresponded to 59% of planned rowing sessions. There was no significant change in rowing sessions per week across training months (F = 0.13, P = 0.99). Although subjects were all encouraged to attend three sessions per week, this population, in particular, is subject to several secondary health complications, as well as transportation issues that gave rise to cancellations during the training period. Training intensity progressed, on average, to 86% of HRpeak (ranging from 76% to 94%) by the end of 6 months, but this increase in intensity was not consistent across all subjects (7 of 12). Figure 1 shows one subject’s training performance on a weekly basis for 6 months. This subject was consistent in FES-RT (83% planned training session attended) and demonstrated a 34% relative increase in aerobic capacity from 16.2 to 21.7 mL·kg−1·min−1.
For all participants, V˙O2peak increased on average by 12% with 6 months of FES-RT, from 15.3 ± 1.5 to 17.1 ± 1.6 mL·kg−1·min−1 (P = 0.02; Fig. 2). This was accompanied by a 28% increase in peak wattage (34.6 ± 4.4 vs 44.4 ± 5.7 W, P < 0.01). The average V˙Epeak did tend to be higher after FES-RT (37.5+ 4.4 vs 40.7 + 3.0 L·min−1, P = 0.09), but an increase was demonstrated in only seven individuals. This modest increase in V˙Epeak result from slight increases in V Tpeak (1.23 ± 0.1 vs 1.28 ± 0.12 L, P = 0.18) and BFpeak (38.4 ± 2.6 vs 40.0 ± 1.5 min−1, P = 0.20). There were no significant differences between pre- and posttraining RERpeak and HRpeak. The magnitude of the increases in V˙O2peak was not related to exercise compliance (P = 0.72).
Before FES-RT, there was a close relationship between injury level and V˙O2peak (y = 0.17x − 0.15, adjusted R 2 = 0.70, P = 0.0004; Fig. 3). In addition, there was a significant relationship between injury level and V˙Epeak (y = 3.85x + 8.97, adjusted R 2 = 0.48, P = 0.0076). Although these relations remained after the 6 months of FES-RT, they were somewhat weaker (injury level and V˙O2peak: y = 0.17x − 0.03, adjusted R 2 = 0.55, P = 0.0035; injury level and V˙Epeak: y = 4.26x + 9.14, adjusted R 2 = 0.43, P = 0.0126). By contrast, 6 months of FES-RT markedly enhanced the relationship between V˙O2peak and V˙Epeak (Fig. 4). Before training, the relationship of V˙O2peak to V˙Epeak was similar to its relation to injury level (y = 0.03x − 0.03, adjusted R 2 = 0.62, P = 0.0014; Fig. 4). However, after training, the relationship of V˙O2peak to V˙Epeak became almost completely linearized (V˙O2peak to V˙Epeak: y = 0.03x − 0.12, adjusted R 2 = 0.84, P < 0.0001). Underscoring the importance of ventilation in determining the V˙O2peak after training was its relationship to V Tpeak. Before FES-RT, V˙O2peak and V˙Tpeak were modestly related (y = 0.616x + 0.33, adjusted R 2 = 0.34, P = 0.03). However, after training, the explained variance doubled such that ∼75% of V˙O2peak across these individuals could be predicted by V Tpeak (y = 0.79x + 0.21, adjusted R 2 = 0.74, P = 0.0002). A likelihood ratio test between the regression models for all four variables showed that the pre- and post-FES-RT regressions were significantly different (chi-squared < 0.01). The breathing pattern during the graded exercise tests before and after FES-RT is presented in Figure 5. As expected, both V T and BF increased with exercise intensity (P < 0.05), and the magnitude of response was unchanged after FES-RT (P ≥ 0.15).
The relationship between V˙O2 and logV˙E from one typical case is shown in Figure 6. The relationship shifted upward with an increased slope from pre- to posttraining periods. Thus, after FES-RT, this subject had a larger increase in V˙O2 for a given increase in V˙E. For all 12 subjects, the average OUES was higher after 6 months of FES-RT (1.24 ± 0.11 vs 1.38 ± 0.12, P < 0.05). Hence, FES-RT improved the efficiency of oxygen uptake in these individuals with SCI.
Consistent with prior research (8,28,34), we found that both peak aerobic capacity and ventilatory capacity were related to injury level. Higher-level injuries cause greater skeletal muscle denervation, resulting in lower peak aerobic capacities. One might surmise that the accompanying pulmonary muscle denervation contributes to this lower capacity (4). However, previous work suggests that even well-trained individuals with cervical spinal cord injuries rarely demonstrate ventilatory constraint during high-intensity arms-only exercise (27). Nonetheless, arms-only exercise engages a small muscle mass, and in those with SCI, the amount of denervated skeletal muscle and denervated pulmonary muscle would be directly proportional. Hence, it might be difficult to create a mismatch between even highly trained skeletal muscle and pulmonary capacity. We found that hybrid FES exercise, which effectively trains both innervated upper body and denervated leg skeletal muscles, results in the restricted ventilatory capacity becoming a key limitation to aerobic capacity.
Individuals with SCI have significantly lower peak aerobic capacity and peak ventilation than the able-bodied (18,34,36). Moreover, peak aerobic capacity decreases as injury level moves up the spinal cord (4,28). Thus, active muscle mass has a profound effect on aerobic capacity and is a significant challenge to achieve high-level exercise in the SCI population. Hybrid FES exercise can overcome the limitations of limited muscle mass (20,35) and results in higher peak aerobic capacity than arms-only or FES legs-only exercise (6,7,15,37). Our previous work demonstrated an almost 30% greater peak aerobic capacity with FES-rowing exercise as compared with arms-only rowing (29). Regular training with FES-rowing will increase aerobic capacity (12,16), but adequate ventilation is critical to provide sufficient oxygen to working muscles during aerobic exercise. Those with SCI above T7 have the greatest functional reduction in respiratory capacity (14,25). Hence, for individuals with high-level injuries, the greater muscle mass engaged during hybrid FES exercise as compared with arms-only exercise could potentially tax ventilatory ability. In fact, before training, we did find a strong relationship between peak aerobic capacity and peak ventilation. However, peak ventilation contributed less than injury level to the prediction of peak aerobic capacity so that injury level might be considered to play a more important role in limiting peak aerobic capacity. Our previous work reported FES-RT in those with injuries at T3 and below improved not only aerobic capacity but also ventilatory capacity (28). In these individuals, ventilatory capacity appeared to be sufficient for the exercise demand, and aerobic capacity was no longer related to injury level after training. However, the current work shows that those with higher-level injuries and greater pulmonary denervation demonstrate a strikingly different response to training. The relationship of aerobic capacity to injury level remained and the relative role of peak ventilation in determining aerobic capacity increased. Moreover, after 6 months of FES-RT, the relationship between aerobic capacity and peak tidal volume was markedly stronger; hence, it contributed more to the prediction of aerobic capacity. Thus, the inability to sufficiently increase tidal volume limited peak ventilation and hence restricted the increase in aerobic capacity. This suggests that the improvements in muscle metabolism and cardiovascular function and potentially greater active muscle mass after FES-RT outstrips the ability of the pulmonary musculature to generate higher levels of ventilation. This might be considered as analogous to highly trained elite athletes. During maximal exercise, highly trained elite athletes can reach the mechanical limits of the lung and respiratory muscles for producing alveolar ventilation (13). Similarly, in these FES–row trained individuals, the pulmonary system may not be able to meet the demands of muscular exercise and hence limit further training induced increases in aerobic capacity. In the able-bodied, the pattern of increasing ventilation is an initial increase in both tidal volume and breathing frequency, followed by a plateau in tidal volume, and further increases in breathing frequency (24). Our data showed linear increases in both tidal volume and breathing frequency throughout graded maximal exercise testing in those with high-level SCI. Hence, these individuals do not reach the mechanical limit for tidal volume during exercise, suggesting that respiratory insufficiency limits exercise.
Only three previous longitudinal studies have explored the effects of FES-RT, reporting increases in aerobic capacity from 8% to 11% (19,28,37). However, there appears to have been only one subject with high-level injury in these studies, and no separate data were reported. Our current results are the first to show a comparable increase in aerobic capacity in 12 individuals with injuries at T2 and above after 6 months of FES-RT (∼12%). In fact, 5 of our 12 subjects showed a >20% increase in peak aerobic capacity. Although participants achieved high training intensity by the end of 6 months, compliance ranged widely and averaged only <60% of sessions. We did not find a close relationship between compliance and the increase in aerobic capacity, which may simply reflect variances in the degree of atrophy and fatigability of the denervated muscles (23). Nonetheless, our current work suggests that FES-RT provides a form of regular aerobic exercise that circumvents the compromised innervation of skeletal muscle mass in those with high-level injuries.
We used OUES as a composite value for the efficiency of the cardiopulmonary system to provide sufficient oxygenated blood to active muscle to perform exercise. In essence, it reflects the integrated function and health of the pulmonary, cardiovascular, and skeletal muscle systems during aerobic exercise (11,23). Before training, the OUES in this group of spinal cord–injured individuals was 61% less than that observed in able-bodied individuals of similar age (9,26). This is likely due to the lesser and untrained skeletal muscle mass, although pulmonary and cardiovascular limitations could also have played a role. After training, there was an 11% increase; however, the increase was as great as 58%, and five individuals showed a >22% increase. Interestingly, the change in OUES with FES-RT was unrelated to the change in peak ventilation (adjusted R 2 = 0.09, P = 0.20) yet strongly related to the change in peak aerobic capacity (adjusted R 2 = 0.72, P < 0.05). Thus, the change in OUES with FES-RT may mainly be due to cardiovascular and skeletal muscle adaptations.
Our subjects included both tetraplegic and paraplegic individuals, and because they can demonstrate quantitatively different exercise responses, they could be considered as different groups. However, we were focused on compromised respiratory capacity. With injuries at T2 and above, vital capacity can be less than 30% of normal respiratory function, and as the injury level moves down from T4 and below, vital capacity improves greatly. Therefore, we studied individuals with injuries at T2 and above to provide a range of respiratory impairment. If we only examine the 10 subjects with cervical SCI, our findings remain. Although the sample size was small, it was sufficient to answer our primary hypothesis. Future measurements of arterial oxyhemoglobin saturation during exercise could provide a direct indicator of effective pulmonary gas exchange and determine the extent of inadequate ventilation during intense exercise.
In conclusion, we found that 6 months of FES-RT increased aerobic capacity with only a modest increase in ventilatory capacity in those with SCI at T2 and above. However, we found that this increased aerobic capacity resulted in trained individuals who appeared to be at their ventilatory constraint for maximal exercise. Hence, improvements of cardiopulmonary reserve appear to be derived from cardiovascular and skeletal muscle adaptations and not from any improvement in ventilatory capacity. This suggests that aerobic adaptations in response to high-intensity FES-RT in those with high-level injuries are limited by the amount of pulmonary muscle denervation. If this ventilatory limitation could be overcome, high-level injuries may experience greater improvements in aerobic capacity with hybrid FES exercise training.
This study was funded by the National Institutes of Health (grant no. R01HL117037). No commercial company or manufacturer has any professional relationship with any of the authors involved in this work, and the results of this work will not confer any commercial benefit upon the authors involved. The results of the present study do not constitute endorsement by the American College of Sports Medicine.
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