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Exercise Tolerance in Children With Early Onset Scoliosis: Growing Rod Treatment “Graduates”
Spine Deformity 4 (2016) 413e419 www.spine-deformity.org
Exercise Tolerance in Children With Early Onset Scoliosis: Growing Rod Treatment ‘‘Graduates’’ Kelly A. Jeans, MS*, Charles E. Johnston, MD, Wilshaw R. Stevens, Jr, BS, Dong-Phuong Tran, MS Texas Scottish Rite Hospital for Children, Dallas, TX 75219, USA Received 3 March 2016; revised 27 June 2016; accepted 29 June 2016
Abstract Study Design: Prospectively enrolled early-onset scoliosis (EOS) patients undergoing growing rod treatment, who have had no surgery for O1 year and/or have received definitive fusion (growing rod ‘‘graduates’’). Objectives: To assess oxygen consumption during exercise and determine if a diminished conventional pulmonary function test (PFT) correlates with metabolic, pulmonary, and cardiovascular measures during exercise. Summary of Background Data: Based on clinical impression and sequential PFT values, EOS patients who have undergone extensive treatment are thought to have limited capacity during exercise. The use of PFTs in this population has been a primary outcome measure of respiratory capacity; however, PFTs are dependent on effort, and thus subjective. This led us to find a new assessment of outcome, to better understand their pulmonary capacity. Methods: Patients underwent oxygen consumption (VO2) testing while walking at self-selected speed over-ground and during a graded exercise test. Maximal VO2 was predicted in those who completed the test to 85% of maximal heart rate (HR). Statistical analysis included Mann-Whitney U test and Spearman correlation coefficient (a 5 0.05). Results: 12 patients participated. Over-ground walking showed that EOS graduates chose to walk at the same speed, but at a higher VO2 Cost (0.28 mL/kg/m) than controls (0.22 mL/kg/m; p ! .001). Treadmill exercise testing showed 9 of 12 subjects able to complete the 85% of predicted maximum protocol. The EOS group had lower VO2 during the final stage (27.9 mL/kg/min) compared to controls (34.2 mL/kg/ min; p 5 .021); however, their heart rate reached the same values. Subjects completing the protocol had lower predicted VO2 max (38.5 mL/kg/min) compared with controls (45.0 mL/kg/min), but this was not significant. Conclusions: Although PFT data suggest clinically relevant pulmonary compromise in EOS patients, the current study shows that these children are able to keep up with their peers in daily activities and also have the capacity to exercise. Level of Evidence: Level II, therapeutic Ó 2016 Scoliosis Research Society. All rights reserved. Keywords: EOS; Scoliosis; Graded exercise test; VO2 maximum; PFT
Introduction Children with early-onset scoliosis (EOS) can have varying levels of physical impairment associated with their scoliosis. Depending on the severity of spine and chest wall Author disclosures: KAJ (none); CEJ (personal fees from Medtronic, personal fees from Wolters Kluwer, outside the submitted work); WRS (none); D-PT (none). There are no outside funding sources for this study. All funding was provided by the Texas Scottish Rite Research Fund. *Corresponding author. 2222 Welborn St, Dallas, TX 75219, USA. Tel.: (214) 559-7581; fax: (214) 559-7884. E-mail address: [email protected] (K.A. Jeans).
deformity, standard pulmonary function testing can show moderate to severe compromise. Definitive spine fusion in the very young child is associated with poor pulmonary function [1] probably because of thoracic growth inhibition [2-4]. Karol et al. have reported that almost half the children studied showed 50% impairment in predicted forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1) following early fusion [3]. In the attempt to avoid iatrogenic thoracic insufficiency syndrome, orthopedic surgeons have moved away from fusing the spine in the very young child and have turned to increasing growth potential in the thoracic region by delaying definitive fusion with various methods of ‘‘growth-friendly’’
2212-134X/$ - see front matter Ó 2016 Scoliosis Research Society. All rights reserved. http://dx.doi.org/10.1016/j.jspd.2016.06.002
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surgical treatment. However, functional outcomes of patients completing a growth-friendly protocol (eg, growing rod or VEPTR instrumentation of the spine and/or chest wall) have to this point been unavailable. The distraction-based growing rod method has been shown to be effective, although most outcome measures in the EOS population have been limited to reports on surgical outcomes [5-11], including correction in the sagittal and coronal plane, final growth achieved, number of lengthenings, revision and complication rates, and pulmonary function testing (PFT) [1,3,4,12,13]. In patients treated with a ‘‘growth-friendly’’ approach, absolute pulmonary function values have been shown to improve following lengthening whereas the percent predicted values were unchanged [13]. Growing rod treatment also has significant surgical complication rates, which increase with each return to the operating room [9,10,14]. There is a significant relationship between the number of lengthenings and psychosocial pathology (aggression, rule breaking, and conduct) in patients who undergo growing rod treatment [15]. With each planned surgical procedure, play, social interactions and participation in sports or community activities may be decreased, and the long-term effect on such an adapted lifestyle is unknown in the EOS population. Predicted PFT values have been the standard used to assess a child’s pulmonary potential, but pulmonary function testing can be unreliable when assessed in the young child [12]. It seems intuitive, however, that children with impairment measured by PFT would have poor exercise capacity and be limited in their ability to participate in activities with cardiovascular demand. The purpose of this study was to assess metabolic function during a graded exercise test, designed to slowly increase the cardiovascular and pulmonary demand with incremental increases in load while the participant is walking. We wished to determine if diminished pulmonary function correlates with diminished oxygen consumption and other measures during exercise.
monitor (Polar, Kempele, Finland). The participants were required to abstain from eating for at least 2 hours before testing. During the testing protocol, talking was discouraged and hand signals were used for communication between the examiner and the participant. Patients were instructed that if they were having serious problems, they were to vocalize the problem immediately. Oxygen consumption testing consisted of a 5-minute seated rest, followed by a 10-minute warmup while walking at a self-selected speed. Following the warmup, the participant underwent a submaximal graded exercise test (GXT) on a treadmill (Fig. 1). The treadmill protocol included three-minute stages, where each load was increased incrementally by speed and incline. Once the patient was walking at a brisk pace (selected by the individual), load was increased with incline, increasing 3% at each stage until 85% 5% of age-predicted maximum heart rate was achieved. At each stage, the participant was asked to rate their perceived exertion (RPE) on the widely used Borg scale from 6 to 20 [16]. Variables assessed (Fig. 2) for rest and over-ground walking included breathing frequency (breaths/min; Rf), tidal volume (L; VT), ventilation (L/min; VE), rate of oxygen consumption (mL/kg/min; VO2 Rate), heart rate (beats/min; HR), and the respiratory exchange ratio (R; VCO2/VO2). Oxygen cost (mL/kg/m; VO2 Cost) was calculated for over-ground walking by taking the VO2 Rate divided by walking speed (m/min; velocity). The aforementioned measures,
Materials and Methods Children with EOS who were more than 3 years from application of a growth-friendly construct and had undergone definitive fusion or were at least 1 year from the last lengthening, were invited to participate in this prospective IRB approved study (IRB approval no.: 062004-059). Participants were excluded if they underwent a lengthening procedure less than one year from the time of testing or if they were uncooperative with the testing protocol. PFTs were conducted by a pulmonary function technician and measures included absolute and percent predicted values for FVC and FEV1. Metabolic testing protocol Metabolic testing was conducted using a Cosmed K4b2 portable telemetry unit (Rome, Italy) with a heart rate
Fig. 1. A patient with EOS completing the graded exercise testing protocol.
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Results
Fig. 2. Abbreviations and definitions.
perceived exertion, and the final stage treadmill load (speed and incline) were also assessed for the GXT. In participants who reached 85% 5% of their maximum predicted heart rate (220-age; HRmax), VO2 max was predicted using the linear relationship between HR and VO2 Rate [17]. The control group consisted of 20 age-matched children. Statistical analysis was conducted using SAS, version 9.4 (SAS Institute, Cary, NC). Group means were compared using a Mann-Whitney U test, and correlations between PFT variables and metabolic data were assessed with a Spearman correlation coefficient (a 5 0.05). Power analysis comparing patients with PFTs less than or greater than 50% predicted value indicated 18 patients in each group were required for valid statistical comparison.
Sixteen children with EOS agreed to participate in this study. Four patients were excludeddone for not being able to perform the testing protocol and three for being less than 1 year from their last lengthening. Primary diagnoses for the 12 study patients included 6 congenital, 2 syndromic, 3 infantile idiopathic, and 1 neuromuscular. The age at index surgery was on average 5.3 years (range 1.3e8.3 years), and the average follow-up time from the initial surgery was 7.1 years (range 3.7e10.4 years). On the day of testing, the average duration since the last procedure was 2.3 years (range 1.0e3.6 years). Nine patients had undergone fusion, and three were being observed having completed lengthening protocol. PFT measures, including absolute (abs) and percent predicted (%) values for FVC and FEV1, and number of surgeries (including index, lengthening, revisions, and unplanned returns) can be found in Table 1. In this patient cohort, 7/12 patients had percent predicted PFT values less than or equal to 50%. There was no difference between the age of the control subjects (12.8 years; range 9.1e16.5) and the EOS patients (12.4 years; range 9e16.5) (p 5 .876). Height and weight of the EOS group were 1.43 0.19 m and 37.5 13.4 kg, respectively, compared to controls’ 1.57 0.17 m and 51.8 21.9 kg (p O .05). At rest, compared to controls, the EOS group had significantly lower VT (0.35 0.17 L vs. 0.77 0.38 L, p 5 .001) and VE (7.6 2.5 L/min vs. 11.5 2.5 L/min, p ! .001). No differences were found between EOS and controls for resting HR (93 15 bpm and 87 14 bpm, respectively; p 5 .381) or VO2 Rate (6.3 2.1 mL/kg/min and 5.7 1.2 mL/kg/min, respectively; p 5 .573). Results from over-ground walking at self-selected speed can be found in Table 2. Respiratory measures showed a
Table 1 Demographics for the EOS group. Subject Gender Age, years Diagnosis
1 2 3 4 5 6 7 8 9 10 11 12
M F F F M M M F F F F M Mean SD
9.0 10.0 12.8 12.0 13.1 10.8 15.1 11.6 13.7 12.4 12.1 16.5 12.4 2.1
Congenital Congenital Congenital Congenital Congenital- VATER Congenital- VATER Dubowitz Syndrome IIS IIS IIS Marfan Neuromuscular
Age at initial Last surgery, Procedures, nb FVC FEV1 surgery, years yearsa Absolute % Predicted Absolute % Predicted 1.3 2.1 5.2 8.3 2.7 4.1 6.3 7.4 8.1 4.8 6.3 6.8 5.3 2.3
1.7 1.0 3.3 1.4 3.6 2.5 2.8 1.1 1.9 2.5 1.9 3.5 2.3 0.9
14 12 7 5 9 12 9 5 5 12 5 6 8.4 3.4
0.48 0.83 2.04 1.34 0.81 0.53 0.99 1.56 1.17 1.17 1.07 1.13 1.09 0.43
34% 66% 63% 71% 37% 23% 59% 55% 39% 46% 36% 23% 46% 17%
0.40 0.82 1.77 1.12 0.63 0.34 0.99 1.47 1.34 1.09 2.59 0.64 1.10 0.64
31% 70% 62% 68% 33% 17% 52% 62% 39% 50% 72% 15% 48% 20%
EOS, early-onset scoliosis; FEV1, forced expiratory volume in 1 second; FVC, forced vital capacity; IIS, infantile idiopathic scoliosis; SD, standard deviation. a Years since last surgery was performed. b Number of procedures including index surgery, lengthenings, revisions, unplanned returns.
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Table 2 Metabolic data collected during self-selected over-ground walking. Variable
Rf VT VE VO2 Rate VO2 Cost R HR Velocity
Units
breaths/min L L/min mL/kg/min mL/kg/m VCO2/VO2 bpm m/min
EOS (n 5 12)
Control (n 5 20)
p
Mean
SD
Mean
SD
41.1 0.61 22.8 20.5 0.28 0.90 129 73.9
12.0 0.33 10.9 5.4 0.04 0.07 20 14.0
27.7 1.13 26.7 18.2 0.22 0.82 119 79.5
7.9 0.57 6.6 3.3 0.03 0.08 16 6.6
.002 .001 .106 .340 !.001 .009 .192 .076
EOS, early-onset scoliosis; HR, heart rate; R, respiratory exchange quotient; Rf, breathing frequency; VT, tidal volume; VE, ventilation; VO2 Rate, rate of oxygen consumption; VO2 Cost, oxygen cost. Statistical significance, p ! .05.
48% increase in respiratory rate (p 5 .002) and a 54% reduction in tidal volume (p 5 .001) in the EOS patients compared to controls. The EOS group walked slightly slower and had a slightly higher HR and VO2 Rate than controls; however, these differences were not significant. When VO2 Cost was calculated (VO2 Rate/velocity), the EOS group walked with a significantly higher oxygen cost (p ! .001), and the respiratory exchange quotient (R; VCO2/VO2) was also significantly higher compared to controls (p 5 .009). Following the 10-minute warm-up during over-ground walking, each participant underwent a GXT. The goal was to have the participant reach 85% 5% of their age predicted heart rate maximum as the criteria used to predict VO2 max. Each participant was encouraged to continue as far into the test as they could. If the criteria were not met, VO2 max was not predicted. Of the 12 EOS participants, 9 were able to reach this goal. Two participants elected to stop testing at 55% and 63% of their age-predicted maximum. Both patients reported their perceived exertion to be 19 of 20 and 20 of 20, indicating they had reached their capacity. (It should be noted that the use of the Borg Scale has been reported to be variable in children [18-20], and the current results should be interpreted with this in mind.) One patient refused increased treadmill walking speed (selected 42.9 m/min) and reached the maximum incline increment of the treadmill before his heart rate reached the target goal. The final stage of the GXT protocol is reported in Table 3. Respiration during the final stage of the GXT showed that the EOS patients had a greater respiratory rate (p 5 .003), whereas VT and VE were significantly lower than controls (p ! .05). The EOS group self-selected a slower treadmill walking speed (75.1 13.4 m/min) than controls (96.6 8.1 m/min, p ! .001) to reach a similar percent HRmax (p 5 .360). VO2 Rate was also lower than controls’ (p 5 .021); however, R was greater in the EOS patients (p 5 .008), indicating they were closer to their VO2 max during the final stage, then controls [21].
Table 3 Metabolic data collected during treadmill walking for the final stage of a graded exercise test. EOS (n 5 12)
Variable
Unit
Rf VT VE VO2 Rate R HR Percent HRmax Velocity Incline
breaths/min 50.9 10.3 37.5 10.3 .003 L 0.74 0.40 1.52 0.66 .001 L/min 34.6 13.4 50.6 12.2 .003 mL/kg/min 27.9 7.3 34.3 6.4 .021 1.00 0.11 0.89 0.08 .008 VCO2/VO2 bpm 161 23 174 5 .134 % 78% 11% 84% 2% .360 m/min 75.1 13.4 96.6 8.1 !.001 % 12% 4% 13% 4% .300
Mean
SD
Control (n 5 20) Mean
p SD
EOS, early-onset scoliosis; HRmax, maximal heart rate; R, respiratory exchange quotient; Rf, breathing frequency; VT, tidal volume; VE, ventilation; VO2 Rate, rate of oxygen consumption. Statistical significance, p ! .05.
For the nine EOS patients who reached 85% 5% of the age-predicted HRmax during the final stage, VO2 max was predicted. Using the linear relationship between VO2 Rate and HR, VO2 max was predicted to be on average 38.5 10.3 mL/kg/min in the EOS group and 45.0 9.5 mL/kg/min in the control group, which was not significantly different (p 5 .151). The standard deviation in the EOS group emphasizes the variability of this prediction within the group. The VO2 Rate during over-ground walking as a percentage of the predicted VO2 max showed that during typical ambulation, the EOS group used 56.3% 14.4% of their predicted VO2 max, whereas the control group was only using 41.1% 7.1% of their VO2 potential (p 5 .004) (Fig. 3). EOS with PFTs <50% and O50% predicted Because EOS patients with PFTs of <50% predicted at maturity are predicted to have significant respiratory
Fig. 3. Results of VO2 Rate during over-ground walking as a percentage of predicted VO2 max.
K.A. Jeans et al. / Spine Deformity 4 (2016) 413e419 Table 4 Metabolic data collected during the final stage of a graded exercise test: EOS comparison with FVC cut off of <50% and O50% predicted. Variable
Units
FVC% of < 50% (n 5 7)
FVC% of O 50% (n 5 5)
Mean
SD
Mean
SD
Rf VT VE VO2 Rate R HR Percent HRmax Velocity Incline
breaths/min L L/min mL/kg/min VCO2/VO2 bpm % m/min %
50.2 0.67 30.0 24.8 1.00 158 76% 72.4 11%
12.6 0.39 12.5 6.6 0.11 26 13% 16.1 4%
51.9 0.83 40.9 32.2 1.01 165 79% 83.2 12%
7.4 0.43 18.1 6.3 0.12 18 9% 8.1 3%
p
.999 .417 .194 .194 .999 .296 .931 .206 .552
EOS, early-onset scoliosis; FVC, forced vital capacity; HRmax, maximal heart rate; R, respiratory exchange quotient; Rf, breathing frequency; VT, tidal volume; VE, ventilation; VO2 Rate, rate of oxygen consumption. Statistical significance, p ! .05.
morbidity [22] and an overall poor prognosis [3], we compared patients with severe pulmonary compromise (FVC <50% predicted; n 5 7) to those with mild or moderate compromise (FVC O50% predicted; n 5 5). In this comparison (Table 4), self-selected over-ground walking speed trended slower in EOS patients with FVC <50% predicted (66.3 9.5 m/min) compared to those EOS patients with FVC O50% predicted (84.4 12.8 m/ min; p 5 .051). The relationship between PFT measures and oxygen consumption testing To determine if PFT measures predicted metabolic outcomes, cross-correlations were run between FVC/ FEV1% predicted and all metabolic measures. FVC% predicted was shown to be positively correlated to both overground walking velocity (r 5 0.655; p 5 .021) and to treadmill walking velocity during the GXT (r 5 0.670; p 5 .017). FVC% predicted also showed a moderate but significant relationship to the patient’s perceived exertion rating during the final stage (r 5 0.583; p 5 .047). PFT variables were not shown to be significantly predictive of respiratory or metabolic measures collected during overground walking or during the GXT in the EOS population. Discussion Early definitive spinal fusion in very young patients with EOS is generally avoided because of the detrimental impact fusion has on thoracic growth potential, which has been shown to be associated with diminished pulmonary capacity [3]. Use of growth-friendly techniques that maximize growth potential through periodic lengthenings while stabilizing the scoliosis is now standard in patients with EOS. Outcome measures following growing rod treatment have been limited to clinical outcomes measures, PFT and
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patient reported surveys. A known limitation to PFT reliability in a young child is that they are heavily dependent on effort [12]. One way to address this limitation is to measure metabolic capacity during an activity. More than half the participants in this cohort have <50% predicted pulmonary function and might be expected to have limitations participating in ‘‘daily activities’’ [23]. Depending on the patient population, what constitutes ‘‘daily activities’’ can be very different. In senior adults, this may include getting out of bed and walking to the bathroom in the morning. For children, daily activities may include recess and physical education in school or, in the very young child, the ability to go to the playground. As the prognosis for patients recruited in this study was suspected to be poor because of impaired PFTs determined during treatment, we were uncertain if these patients would be able to complete the testing protocol. Three patients were in fact unable to complete the GXT. Two of the patients were the youngest in the cohort, suggesting an agerelated motivation issue. All three had undergone the greatest number of surgeries (minimum 11). One activity of daily living is self-selected walking speed. During over-ground walking, EOS patients may have a greater respiratory rate because of a smaller lung volume than their peers, but they chose to keep up with their peers (reflected by their walking speed) by increasing their oxygen cost. When asked to complete a GXT on a treadmill, all patients agreed to participate, with 9 of 12 able to complete the protocol. Pulmonary measures showed an increased respiratory rate and decreased total volume and ventilation compared to controls. VO2 Rate was lower at the final stage of the test, whereas the respiratory exchange ratio was significantly higher compared to agematched controls, indicating patients nearing their VO2 max. When looking specifically at the perceived exertion rating [16] during the final stage, 5 of 12 patients rated the last stage between 18 and 20 of a possible 20, that is, maximal exertion. Because of the variability within this small group of EOS patients, detecting significant differences in predicted VO2 max would have required at least 18 subjects (power analysis). At the time of the review, these 12 patients represented our cohort of growing rod ‘‘graduates,’’ and though small, this series shows strong clinical significance. Compared with published normative data (cooper Institute, Dallas, TX), our EOS patients fell in the ‘‘Fair to Good’’ range as a group [24]. PFTs were shown to be predictors of walking speed both over-ground and during the GXT but were not correlated to metabolic measures. These data allow assessment of metabolic capacity estimating patients’ cardiovascular and pulmonary potential to participate with their peers. These data, however, do not actually identify what activities are actually being pursued. Future work is underway assessing daily activity through wearable monitors that track activity time and steps taken. Because PFTs may be poor predictors of metabolic
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function, the relationship between metabolic cost and actual measured activity need further investigation. Expert consensus is that children should spend at least 60 minutes at moderate to vigorous physical activity a day for positive health benefit [25]. Because participation in organized sports may be unfeasible in some children with EOS, time spent on the playground may be an important substitute for organized sports [26]. Both physical and psychosocial interactions are important to foster in young children [27], but it may be especially important in the EOS population who can benefit physically from activity and participation. Metabolic testing in the form of VO2 Rates and Cost during treadmill exercise has provided new insight into the metabolic capacity in patients with EOS following growthfriendly treatment. Physical exercise and activity have been shown to positively impact both physical and mental health in school-age children [25,28]. Despite the perception of poor functional outcome in children with impaired pulmonary function as measured by traditional PFT’s, it is clear that these children have more in reserve than previously thought. We conclude that clinical emphasis on participation in physical activity both during and following the course of growth-friendly treatment in patients with EOS is not contraindicated from a respiratory perspective, because 9 of 12 graduates in this small cohort were able to keep up with their peer group and were able to exercise, albeit at a slightly slower speed and with increased oxygen cost. Future longitudinal studies should reveal the clinical importance of these metabolic findings. 3-5 Key points 1. EOS patients completing growth-friendly treatment walk at the same speed as controls but with higher VO2 cost. 2. Seventy-five percent of EOS ‘‘graduates’’ are able to complete a submaximal graded exercise test to achieve 85% of their maximum predicted heart rate. 3. VO2 maximum is not significantly different in patients with EOS than in controls. 4. Despite a perception of poor functional outcomes in patients with <50% predicted pulmonary function tests, these patients have better exercise tolerance and respiratory reserve than previously thought.
Acknowledgments The authors thank Anna McClung for her help with this study and for the financial support of the Texas Scottish Rite Hospital Research Fund. References [1] Goldberg CJ, Gillic I, Connaughton O, et al. Respiratory function and cosmesis at maturity in infantile-onset scoliosis. Spine (Phila Pa 1976) 2003;28:2397e406.
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Exercise Tolerance in Children With Early Onset Scoliosis: Growing Rod Treatment ‘‘Graduates’’ Kelly A. Jeans, MS*, Charles E. Johnston, MD, Wilshaw R. Stevens, Jr, BS, Dong-Phuong Tran, MS Texas Scottish Rite Hospital for Children, Dallas, TX 75219, USA Received 3 March 2016; revised 27 June 2016; accepted 29 June 2016
Abstract Study Design: Prospectively enrolled early-onset scoliosis (EOS) patients undergoing growing rod treatment, who have had no surgery for O1 year and/or have received definitive fusion (growing rod ‘‘graduates’’). Objectives: To assess oxygen consumption during exercise and determine if a diminished conventional pulmonary function test (PFT) correlates with metabolic, pulmonary, and cardiovascular measures during exercise. Summary of Background Data: Based on clinical impression and sequential PFT values, EOS patients who have undergone extensive treatment are thought to have limited capacity during exercise. The use of PFTs in this population has been a primary outcome measure of respiratory capacity; however, PFTs are dependent on effort, and thus subjective. This led us to find a new assessment of outcome, to better understand their pulmonary capacity. Methods: Patients underwent oxygen consumption (VO2) testing while walking at self-selected speed over-ground and during a graded exercise test. Maximal VO2 was predicted in those who completed the test to 85% of maximal heart rate (HR). Statistical analysis included Mann-Whitney U test and Spearman correlation coefficient (a 5 0.05). Results: 12 patients participated. Over-ground walking showed that EOS graduates chose to walk at the same speed, but at a higher VO2 Cost (0.28 mL/kg/m) than controls (0.22 mL/kg/m; p ! .001). Treadmill exercise testing showed 9 of 12 subjects able to complete the 85% of predicted maximum protocol. The EOS group had lower VO2 during the final stage (27.9 mL/kg/min) compared to controls (34.2 mL/kg/ min; p 5 .021); however, their heart rate reached the same values. Subjects completing the protocol had lower predicted VO2 max (38.5 mL/kg/min) compared with controls (45.0 mL/kg/min), but this was not significant. Conclusions: Although PFT data suggest clinically relevant pulmonary compromise in EOS patients, the current study shows that these children are able to keep up with their peers in daily activities and also have the capacity to exercise. Level of Evidence: Level II, therapeutic Ó 2016 Scoliosis Research Society. All rights reserved. Keywords: EOS; Scoliosis; Graded exercise test; VO2 maximum; PFT
Introduction Children with early-onset scoliosis (EOS) can have varying levels of physical impairment associated with their scoliosis. Depending on the severity of spine and chest wall Author disclosures: KAJ (none); CEJ (personal fees from Medtronic, personal fees from Wolters Kluwer, outside the submitted work); WRS (none); D-PT (none). There are no outside funding sources for this study. All funding was provided by the Texas Scottish Rite Research Fund. *Corresponding author. 2222 Welborn St, Dallas, TX 75219, USA. Tel.: (214) 559-7581; fax: (214) 559-7884. E-mail address: [email protected] (K.A. Jeans).
deformity, standard pulmonary function testing can show moderate to severe compromise. Definitive spine fusion in the very young child is associated with poor pulmonary function [1] probably because of thoracic growth inhibition [2-4]. Karol et al. have reported that almost half the children studied showed 50% impairment in predicted forced vital capacity (FVC) and forced expiratory volume in 1 second (FEV1) following early fusion [3]. In the attempt to avoid iatrogenic thoracic insufficiency syndrome, orthopedic surgeons have moved away from fusing the spine in the very young child and have turned to increasing growth potential in the thoracic region by delaying definitive fusion with various methods of ‘‘growth-friendly’’
2212-134X/$ - see front matter Ó 2016 Scoliosis Research Society. All rights reserved. http://dx.doi.org/10.1016/j.jspd.2016.06.002
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surgical treatment. However, functional outcomes of patients completing a growth-friendly protocol (eg, growing rod or VEPTR instrumentation of the spine and/or chest wall) have to this point been unavailable. The distraction-based growing rod method has been shown to be effective, although most outcome measures in the EOS population have been limited to reports on surgical outcomes [5-11], including correction in the sagittal and coronal plane, final growth achieved, number of lengthenings, revision and complication rates, and pulmonary function testing (PFT) [1,3,4,12,13]. In patients treated with a ‘‘growth-friendly’’ approach, absolute pulmonary function values have been shown to improve following lengthening whereas the percent predicted values were unchanged [13]. Growing rod treatment also has significant surgical complication rates, which increase with each return to the operating room [9,10,14]. There is a significant relationship between the number of lengthenings and psychosocial pathology (aggression, rule breaking, and conduct) in patients who undergo growing rod treatment [15]. With each planned surgical procedure, play, social interactions and participation in sports or community activities may be decreased, and the long-term effect on such an adapted lifestyle is unknown in the EOS population. Predicted PFT values have been the standard used to assess a child’s pulmonary potential, but pulmonary function testing can be unreliable when assessed in the young child [12]. It seems intuitive, however, that children with impairment measured by PFT would have poor exercise capacity and be limited in their ability to participate in activities with cardiovascular demand. The purpose of this study was to assess metabolic function during a graded exercise test, designed to slowly increase the cardiovascular and pulmonary demand with incremental increases in load while the participant is walking. We wished to determine if diminished pulmonary function correlates with diminished oxygen consumption and other measures during exercise.
monitor (Polar, Kempele, Finland). The participants were required to abstain from eating for at least 2 hours before testing. During the testing protocol, talking was discouraged and hand signals were used for communication between the examiner and the participant. Patients were instructed that if they were having serious problems, they were to vocalize the problem immediately. Oxygen consumption testing consisted of a 5-minute seated rest, followed by a 10-minute warmup while walking at a self-selected speed. Following the warmup, the participant underwent a submaximal graded exercise test (GXT) on a treadmill (Fig. 1). The treadmill protocol included three-minute stages, where each load was increased incrementally by speed and incline. Once the patient was walking at a brisk pace (selected by the individual), load was increased with incline, increasing 3% at each stage until 85% 5% of age-predicted maximum heart rate was achieved. At each stage, the participant was asked to rate their perceived exertion (RPE) on the widely used Borg scale from 6 to 20 [16]. Variables assessed (Fig. 2) for rest and over-ground walking included breathing frequency (breaths/min; Rf), tidal volume (L; VT), ventilation (L/min; VE), rate of oxygen consumption (mL/kg/min; VO2 Rate), heart rate (beats/min; HR), and the respiratory exchange ratio (R; VCO2/VO2). Oxygen cost (mL/kg/m; VO2 Cost) was calculated for over-ground walking by taking the VO2 Rate divided by walking speed (m/min; velocity). The aforementioned measures,
Materials and Methods Children with EOS who were more than 3 years from application of a growth-friendly construct and had undergone definitive fusion or were at least 1 year from the last lengthening, were invited to participate in this prospective IRB approved study (IRB approval no.: 062004-059). Participants were excluded if they underwent a lengthening procedure less than one year from the time of testing or if they were uncooperative with the testing protocol. PFTs were conducted by a pulmonary function technician and measures included absolute and percent predicted values for FVC and FEV1. Metabolic testing protocol Metabolic testing was conducted using a Cosmed K4b2 portable telemetry unit (Rome, Italy) with a heart rate
Fig. 1. A patient with EOS completing the graded exercise testing protocol.
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Results
Fig. 2. Abbreviations and definitions.
perceived exertion, and the final stage treadmill load (speed and incline) were also assessed for the GXT. In participants who reached 85% 5% of their maximum predicted heart rate (220-age; HRmax), VO2 max was predicted using the linear relationship between HR and VO2 Rate [17]. The control group consisted of 20 age-matched children. Statistical analysis was conducted using SAS, version 9.4 (SAS Institute, Cary, NC). Group means were compared using a Mann-Whitney U test, and correlations between PFT variables and metabolic data were assessed with a Spearman correlation coefficient (a 5 0.05). Power analysis comparing patients with PFTs less than or greater than 50% predicted value indicated 18 patients in each group were required for valid statistical comparison.
Sixteen children with EOS agreed to participate in this study. Four patients were excludeddone for not being able to perform the testing protocol and three for being less than 1 year from their last lengthening. Primary diagnoses for the 12 study patients included 6 congenital, 2 syndromic, 3 infantile idiopathic, and 1 neuromuscular. The age at index surgery was on average 5.3 years (range 1.3e8.3 years), and the average follow-up time from the initial surgery was 7.1 years (range 3.7e10.4 years). On the day of testing, the average duration since the last procedure was 2.3 years (range 1.0e3.6 years). Nine patients had undergone fusion, and three were being observed having completed lengthening protocol. PFT measures, including absolute (abs) and percent predicted (%) values for FVC and FEV1, and number of surgeries (including index, lengthening, revisions, and unplanned returns) can be found in Table 1. In this patient cohort, 7/12 patients had percent predicted PFT values less than or equal to 50%. There was no difference between the age of the control subjects (12.8 years; range 9.1e16.5) and the EOS patients (12.4 years; range 9e16.5) (p 5 .876). Height and weight of the EOS group were 1.43 0.19 m and 37.5 13.4 kg, respectively, compared to controls’ 1.57 0.17 m and 51.8 21.9 kg (p O .05). At rest, compared to controls, the EOS group had significantly lower VT (0.35 0.17 L vs. 0.77 0.38 L, p 5 .001) and VE (7.6 2.5 L/min vs. 11.5 2.5 L/min, p ! .001). No differences were found between EOS and controls for resting HR (93 15 bpm and 87 14 bpm, respectively; p 5 .381) or VO2 Rate (6.3 2.1 mL/kg/min and 5.7 1.2 mL/kg/min, respectively; p 5 .573). Results from over-ground walking at self-selected speed can be found in Table 2. Respiratory measures showed a
Table 1 Demographics for the EOS group. Subject Gender Age, years Diagnosis
1 2 3 4 5 6 7 8 9 10 11 12
M F F F M M M F F F F M Mean SD
9.0 10.0 12.8 12.0 13.1 10.8 15.1 11.6 13.7 12.4 12.1 16.5 12.4 2.1
Congenital Congenital Congenital Congenital Congenital- VATER Congenital- VATER Dubowitz Syndrome IIS IIS IIS Marfan Neuromuscular
Age at initial Last surgery, Procedures, nb FVC FEV1 surgery, years yearsa Absolute % Predicted Absolute % Predicted 1.3 2.1 5.2 8.3 2.7 4.1 6.3 7.4 8.1 4.8 6.3 6.8 5.3 2.3
1.7 1.0 3.3 1.4 3.6 2.5 2.8 1.1 1.9 2.5 1.9 3.5 2.3 0.9
14 12 7 5 9 12 9 5 5 12 5 6 8.4 3.4
0.48 0.83 2.04 1.34 0.81 0.53 0.99 1.56 1.17 1.17 1.07 1.13 1.09 0.43
34% 66% 63% 71% 37% 23% 59% 55% 39% 46% 36% 23% 46% 17%
0.40 0.82 1.77 1.12 0.63 0.34 0.99 1.47 1.34 1.09 2.59 0.64 1.10 0.64
31% 70% 62% 68% 33% 17% 52% 62% 39% 50% 72% 15% 48% 20%
EOS, early-onset scoliosis; FEV1, forced expiratory volume in 1 second; FVC, forced vital capacity; IIS, infantile idiopathic scoliosis; SD, standard deviation. a Years since last surgery was performed. b Number of procedures including index surgery, lengthenings, revisions, unplanned returns.
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Table 2 Metabolic data collected during self-selected over-ground walking. Variable
Rf VT VE VO2 Rate VO2 Cost R HR Velocity
Units
breaths/min L L/min mL/kg/min mL/kg/m VCO2/VO2 bpm m/min
EOS (n 5 12)
Control (n 5 20)
p
Mean
SD
Mean
SD
41.1 0.61 22.8 20.5 0.28 0.90 129 73.9
12.0 0.33 10.9 5.4 0.04 0.07 20 14.0
27.7 1.13 26.7 18.2 0.22 0.82 119 79.5
7.9 0.57 6.6 3.3 0.03 0.08 16 6.6
.002 .001 .106 .340 !.001 .009 .192 .076
EOS, early-onset scoliosis; HR, heart rate; R, respiratory exchange quotient; Rf, breathing frequency; VT, tidal volume; VE, ventilation; VO2 Rate, rate of oxygen consumption; VO2 Cost, oxygen cost. Statistical significance, p ! .05.
48% increase in respiratory rate (p 5 .002) and a 54% reduction in tidal volume (p 5 .001) in the EOS patients compared to controls. The EOS group walked slightly slower and had a slightly higher HR and VO2 Rate than controls; however, these differences were not significant. When VO2 Cost was calculated (VO2 Rate/velocity), the EOS group walked with a significantly higher oxygen cost (p ! .001), and the respiratory exchange quotient (R; VCO2/VO2) was also significantly higher compared to controls (p 5 .009). Following the 10-minute warm-up during over-ground walking, each participant underwent a GXT. The goal was to have the participant reach 85% 5% of their age predicted heart rate maximum as the criteria used to predict VO2 max. Each participant was encouraged to continue as far into the test as they could. If the criteria were not met, VO2 max was not predicted. Of the 12 EOS participants, 9 were able to reach this goal. Two participants elected to stop testing at 55% and 63% of their age-predicted maximum. Both patients reported their perceived exertion to be 19 of 20 and 20 of 20, indicating they had reached their capacity. (It should be noted that the use of the Borg Scale has been reported to be variable in children [18-20], and the current results should be interpreted with this in mind.) One patient refused increased treadmill walking speed (selected 42.9 m/min) and reached the maximum incline increment of the treadmill before his heart rate reached the target goal. The final stage of the GXT protocol is reported in Table 3. Respiration during the final stage of the GXT showed that the EOS patients had a greater respiratory rate (p 5 .003), whereas VT and VE were significantly lower than controls (p ! .05). The EOS group self-selected a slower treadmill walking speed (75.1 13.4 m/min) than controls (96.6 8.1 m/min, p ! .001) to reach a similar percent HRmax (p 5 .360). VO2 Rate was also lower than controls’ (p 5 .021); however, R was greater in the EOS patients (p 5 .008), indicating they were closer to their VO2 max during the final stage, then controls [21].
Table 3 Metabolic data collected during treadmill walking for the final stage of a graded exercise test. EOS (n 5 12)
Variable
Unit
Rf VT VE VO2 Rate R HR Percent HRmax Velocity Incline
breaths/min 50.9 10.3 37.5 10.3 .003 L 0.74 0.40 1.52 0.66 .001 L/min 34.6 13.4 50.6 12.2 .003 mL/kg/min 27.9 7.3 34.3 6.4 .021 1.00 0.11 0.89 0.08 .008 VCO2/VO2 bpm 161 23 174 5 .134 % 78% 11% 84% 2% .360 m/min 75.1 13.4 96.6 8.1 !.001 % 12% 4% 13% 4% .300
Mean
SD
Control (n 5 20) Mean
p SD
EOS, early-onset scoliosis; HRmax, maximal heart rate; R, respiratory exchange quotient; Rf, breathing frequency; VT, tidal volume; VE, ventilation; VO2 Rate, rate of oxygen consumption. Statistical significance, p ! .05.
For the nine EOS patients who reached 85% 5% of the age-predicted HRmax during the final stage, VO2 max was predicted. Using the linear relationship between VO2 Rate and HR, VO2 max was predicted to be on average 38.5 10.3 mL/kg/min in the EOS group and 45.0 9.5 mL/kg/min in the control group, which was not significantly different (p 5 .151). The standard deviation in the EOS group emphasizes the variability of this prediction within the group. The VO2 Rate during over-ground walking as a percentage of the predicted VO2 max showed that during typical ambulation, the EOS group used 56.3% 14.4% of their predicted VO2 max, whereas the control group was only using 41.1% 7.1% of their VO2 potential (p 5 .004) (Fig. 3). EOS with PFTs <50% and O50% predicted Because EOS patients with PFTs of <50% predicted at maturity are predicted to have significant respiratory
Fig. 3. Results of VO2 Rate during over-ground walking as a percentage of predicted VO2 max.
K.A. Jeans et al. / Spine Deformity 4 (2016) 413e419 Table 4 Metabolic data collected during the final stage of a graded exercise test: EOS comparison with FVC cut off of <50% and O50% predicted. Variable
Units
FVC% of < 50% (n 5 7)
FVC% of O 50% (n 5 5)
Mean
SD
Mean
SD
Rf VT VE VO2 Rate R HR Percent HRmax Velocity Incline
breaths/min L L/min mL/kg/min VCO2/VO2 bpm % m/min %
50.2 0.67 30.0 24.8 1.00 158 76% 72.4 11%
12.6 0.39 12.5 6.6 0.11 26 13% 16.1 4%
51.9 0.83 40.9 32.2 1.01 165 79% 83.2 12%
7.4 0.43 18.1 6.3 0.12 18 9% 8.1 3%
p
.999 .417 .194 .194 .999 .296 .931 .206 .552
EOS, early-onset scoliosis; FVC, forced vital capacity; HRmax, maximal heart rate; R, respiratory exchange quotient; Rf, breathing frequency; VT, tidal volume; VE, ventilation; VO2 Rate, rate of oxygen consumption. Statistical significance, p ! .05.
morbidity [22] and an overall poor prognosis [3], we compared patients with severe pulmonary compromise (FVC <50% predicted; n 5 7) to those with mild or moderate compromise (FVC O50% predicted; n 5 5). In this comparison (Table 4), self-selected over-ground walking speed trended slower in EOS patients with FVC <50% predicted (66.3 9.5 m/min) compared to those EOS patients with FVC O50% predicted (84.4 12.8 m/ min; p 5 .051). The relationship between PFT measures and oxygen consumption testing To determine if PFT measures predicted metabolic outcomes, cross-correlations were run between FVC/ FEV1% predicted and all metabolic measures. FVC% predicted was shown to be positively correlated to both overground walking velocity (r 5 0.655; p 5 .021) and to treadmill walking velocity during the GXT (r 5 0.670; p 5 .017). FVC% predicted also showed a moderate but significant relationship to the patient’s perceived exertion rating during the final stage (r 5 0.583; p 5 .047). PFT variables were not shown to be significantly predictive of respiratory or metabolic measures collected during overground walking or during the GXT in the EOS population. Discussion Early definitive spinal fusion in very young patients with EOS is generally avoided because of the detrimental impact fusion has on thoracic growth potential, which has been shown to be associated with diminished pulmonary capacity [3]. Use of growth-friendly techniques that maximize growth potential through periodic lengthenings while stabilizing the scoliosis is now standard in patients with EOS. Outcome measures following growing rod treatment have been limited to clinical outcomes measures, PFT and
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patient reported surveys. A known limitation to PFT reliability in a young child is that they are heavily dependent on effort [12]. One way to address this limitation is to measure metabolic capacity during an activity. More than half the participants in this cohort have <50% predicted pulmonary function and might be expected to have limitations participating in ‘‘daily activities’’ [23]. Depending on the patient population, what constitutes ‘‘daily activities’’ can be very different. In senior adults, this may include getting out of bed and walking to the bathroom in the morning. For children, daily activities may include recess and physical education in school or, in the very young child, the ability to go to the playground. As the prognosis for patients recruited in this study was suspected to be poor because of impaired PFTs determined during treatment, we were uncertain if these patients would be able to complete the testing protocol. Three patients were in fact unable to complete the GXT. Two of the patients were the youngest in the cohort, suggesting an agerelated motivation issue. All three had undergone the greatest number of surgeries (minimum 11). One activity of daily living is self-selected walking speed. During over-ground walking, EOS patients may have a greater respiratory rate because of a smaller lung volume than their peers, but they chose to keep up with their peers (reflected by their walking speed) by increasing their oxygen cost. When asked to complete a GXT on a treadmill, all patients agreed to participate, with 9 of 12 able to complete the protocol. Pulmonary measures showed an increased respiratory rate and decreased total volume and ventilation compared to controls. VO2 Rate was lower at the final stage of the test, whereas the respiratory exchange ratio was significantly higher compared to agematched controls, indicating patients nearing their VO2 max. When looking specifically at the perceived exertion rating [16] during the final stage, 5 of 12 patients rated the last stage between 18 and 20 of a possible 20, that is, maximal exertion. Because of the variability within this small group of EOS patients, detecting significant differences in predicted VO2 max would have required at least 18 subjects (power analysis). At the time of the review, these 12 patients represented our cohort of growing rod ‘‘graduates,’’ and though small, this series shows strong clinical significance. Compared with published normative data (cooper Institute, Dallas, TX), our EOS patients fell in the ‘‘Fair to Good’’ range as a group [24]. PFTs were shown to be predictors of walking speed both over-ground and during the GXT but were not correlated to metabolic measures. These data allow assessment of metabolic capacity estimating patients’ cardiovascular and pulmonary potential to participate with their peers. These data, however, do not actually identify what activities are actually being pursued. Future work is underway assessing daily activity through wearable monitors that track activity time and steps taken. Because PFTs may be poor predictors of metabolic
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function, the relationship between metabolic cost and actual measured activity need further investigation. Expert consensus is that children should spend at least 60 minutes at moderate to vigorous physical activity a day for positive health benefit [25]. Because participation in organized sports may be unfeasible in some children with EOS, time spent on the playground may be an important substitute for organized sports [26]. Both physical and psychosocial interactions are important to foster in young children [27], but it may be especially important in the EOS population who can benefit physically from activity and participation. Metabolic testing in the form of VO2 Rates and Cost during treadmill exercise has provided new insight into the metabolic capacity in patients with EOS following growthfriendly treatment. Physical exercise and activity have been shown to positively impact both physical and mental health in school-age children [25,28]. Despite the perception of poor functional outcome in children with impaired pulmonary function as measured by traditional PFT’s, it is clear that these children have more in reserve than previously thought. We conclude that clinical emphasis on participation in physical activity both during and following the course of growth-friendly treatment in patients with EOS is not contraindicated from a respiratory perspective, because 9 of 12 graduates in this small cohort were able to keep up with their peer group and were able to exercise, albeit at a slightly slower speed and with increased oxygen cost. Future longitudinal studies should reveal the clinical importance of these metabolic findings. 3-5 Key points 1. EOS patients completing growth-friendly treatment walk at the same speed as controls but with higher VO2 cost. 2. Seventy-five percent of EOS ‘‘graduates’’ are able to complete a submaximal graded exercise test to achieve 85% of their maximum predicted heart rate. 3. VO2 maximum is not significantly different in patients with EOS than in controls. 4. Despite a perception of poor functional outcomes in patients with <50% predicted pulmonary function tests, these patients have better exercise tolerance and respiratory reserve than previously thought.
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