Pediatric-Onset Rehabilitation

Cardiovascular Health and Fitness

Accumulating evidence supports the important role of pediatric cardiovascular (CVS) health in CVS health throughout life (Umer et al. 2017; Urbina et al. 2019; Wright et al. 2001). The accumulation of behavioral and clinical risk factors that will later influence adult CVS health could be substantially accentuated in children with SCI/D-related paralysis, because, as shown in previous studies, different measures of physical performance, like strength, walking speed, and balance, can act as markers of current and future health in adults (Cooper et al. 2011). Growing and living with paralysis can influence numerous factors that, in turn, could impact lifelong CVS and metabolic health: 1) biological factors: inflammation, gut microbiome, levels of total cholesterol, blood pressure, and fasting glucose; 2) behavioral factors: activity/exercise level, diet and healthy weight/BMI, smoking (including marijuana), sleep, social isolation/bullying, participation, electronic media usage; and 3) economic factors: socioeconomic status, access to care, transition to adult care.

It is suspected that individuals with childhood-onset SCI/D paralysis may fair worse as it pertains to CVS health lifelong. As CVS disease is number one cause of morbidity and mortality in adults living with chronic paralysis (Whiteneck et al. 1992) and the prevalence rate of symptomatic CVS disease is higher in individuals with paralysis than in able body individuals (Myers et al. 2007). While there is no concrete evidence that individuals with childhood-onset paralysis have higher CVS morbidity and mortality than those with adult-onset of paralysis, they do have a 31% increase in the annual odds of dying compared with persons injured at older ages (Shavelle et al. 2007). Thus, assessing and improving CVS fitness in children with paralysis appears quite essential amidst the confluence of multiple inter-relating biological, interpersonal, and behavioral features of this life stage.

Evidence to guide optimal care is quite limited in pediatric medicine and even more so in the relatively small field of SCI/D-related paralysis.

This section reviews evidence examining the following CVS factors:

  1. Body composition (as assessed by Dual X-ray Absorptiometry), specifically total lean mass, fat mass, percentage body fat, and BMC/BMD
  2. Anthropometric measures, like weight, height, and BMI
  3. Measures of metabolic efficiency meant to assess metabolic syndrome likelihood, like fasting lipids, fasting glucose, insulin resistance, resting metabolic rate
  4. Measures of cardio-respiratory function: resting heart rate, VO2
  5. Measures of functional performance, like muscle strength, power output, forced vital capacity

Author, Year

Country

Study Design

Sample Size

 Population

Intervention

Outcome Measure

Results
(Johnston, Smith, et al., 2009)

USA

RCT

N=30

PEDro=5

 Population: Original RCT (n=30): Age: 9.7±2.5; Gender: males=17, females=13; Injury etiology: Traumatic SCI=26, Transverse Myelitis=2, Chemotherapy=1, Ischemia=1; Level of Injury: cervical=11, thoracic=19; Severity of Injury: AIS A=22, B=6, C=2.

Intervention: Subjects were randomized to one of three groups: 1) Functional Electrical Stimulation Cycling [FESC; n=10] (50 rpm while seated in wheelchair, pulse duration=150 ls, frequency=33 Hz, amplitude max 140 mA, increased automatically to generate sufficient force to maintain the cadence); 2) passive cycling [PC; n=10] (50 rpm), or 3) non-cycling with 20 min daily surface electrical stimulation [ES; n=10] to lower extremity muscles. Sessions were conducted for 1 hr/day, 3 days/wk for 6 mo.

Outcome Measures: Heart rate (HR), oxygen consumption (VO2/kg) under four conditions (pre-exercise, warm-up, activity to fatigue, recovery), Forced Vital Capacity (FVC), Lipid Profile (i.e., high density lipoprotein [HDL], low density lipoprotein [LDL], cholesterol, triglycerides).

 1.         There were no significant differences between groups in VO2/kg, HR, FVC or any of the lipids between baseline and the 6 mo follow-up.
(Johnston, Smith, et al., 2008b)

USA

RCT*

N=4

*Subjects were a subset from the larger RCT by (Johnston, Smith, et al., 2009)

 Population: Case 1: 7 yr, female, T4-T6, ASIA A SCI at 2 yr of age; Case 2: 9 yr, female, C7, ASIA A SCI at 4 yr of age; Case 3: 7 yr, male, T3, ASIA A SCI at 3 yr of age; Case 4: 11 yr, male, C7, ASIA A SCI at 3 yr of age.

Intervention: Subset of patients randomized to one of two groups:

1) Functional Electrical Stimulation Cycling [FESC] at 50 rpm while seated in wheelchair (pulse duration (150 ls) and frequency (33 Hz) were fixed; current amplitude (max 140 mA) increased automatically to generate sufficient

force to maintain the cadence), or 2) Passive cycling at 50 rpm. Sessions were conducted for 1 hr, 3 times/wk for 6 mo.

Outcome Measures: Bone

mineral density (BMD) using Dual Energy X-ray Absorptiometry (DEXA) of the left femoral neck, distal femur, and proximal tibia; left quadriceps muscle volume using magnetic resonance imaging (MRI); electrically stimulated strength of the left quadriceps using a dynamometer; spasticity of the quadriceps and hamstrings muscles using Ashworth scale scores; fasting lipid profile via high density lipoprotein (HDL) and low-density lipoprotein (LDL); heart rate (HR); and oxygen consumption (VO2/kg).

 Case 1: FESC

1.         Improvements in BMD at the femoral neck, distal femur, and proximal tibia; quadriceps muscle volume; stimulated strength of the quadriceps muscles; HDL cholesterol; resting HR; peak VO2/kg; and peak HR; however, cholesterol, LDL, and triglyceride levels and the cholesterol/HDL ratio increased compared to baseline.

2.        No changes in Ashworth scores, but parents reported decreased spasticity and looser muscles.

Case 2: FESC

3.        Improvements in BMD at the femoral neck, distal femur, and proximal tibia; quadriceps muscle volume; stimulated quadriceps muscle strength; and hamstring muscle spasticity; however, cholesterol, LDL, HDL, and triglyceride levels and the cholesterol/HDL ratio worsened as compared to baseline.

4.        The parents reported bigger, firmer muscles; decreased bowel program completion times; increased appetite; and increased spasticity that did not require medical intervention.

Case 3: PC

5.        Improvements in femoral neck BMD, hamstring spasticity, and triglyceride levels.

6.        Distal femur and proximal tibia BMD and stimulated quadriceps strength were lower as compared to baseline, and LDL levels and the cholesterol/HDL ratio were elevated.

7.        Parents reported decreased bowel accidents and new sensation in his knees and stomach.

Case 4: PC

8.        Improvements in BMD at the femoral neck, distal femur, and proximal tibia; quadriceps muscle volume; stimulated quadriceps strength; hamstring spasticity; cholesterol; LDL cholesterol; resting HR; and peak VO2/kg.

9.        HDL cholesterol decreased as compared to baseline but the cholesterol/HDL ratio was unchanged.

10.      Parents reported decreased spasticity, looser muscles, increased energy, decreased lower extremity swelling, and increased appetite.
(Johnston, Smith, Betz, et al., 2008)

USA

Observational

N=29

*Subjects were a subset from the larger RCT by (Johnston, Smith, et al., 2009)

 Population: Age: 9.7±2.5 yr; Gender: males=17, females=12; Injury etiology: Traumatic SCI=24, Transverse Myelitis=1, Other=4; Level of Injury: C8/C9=9, T1-4=9, T5-11=11.

Intervention: Upper extremity, tabletop ergonomic testing.
Outcome Measures: Heart rate (HR), and oxygen consumption (VO2/kg) under four conditions (pre-exercise, warm-up, activity to fatigue, recovery), peak power output (PO) (Wpeak/kg).

 1.         For all subjects, the following peak values were obtained:

·          HR=149.9±31.6 beats per minute

·          VO2=14.0±7.9 mL/kg

·          PO=1.1±0.7 W/kg

2.        Differences were seen between the three injury groupings (C8-9, T1-4, T5-11):

·          HR peak (p=0.013)

·          VO2peak/kg (p=0.041)

·          PO (p=0.001)

3.        Differences were noted between the C8-9 group and the T5-11 group for HR peak (p=0.010), VO2 peak (p=0.038), and PO peak (p=0.001).
(Nelson et al., 2007)

USA

Observational

N=114

(N=20 SCI)

 Population: SCI Group (n=20): Age: 16.9±3.0 yr; Gender: males=11, females=9; Time since injury: 4.8±4.0. Spina Bifida (SB) Group (n=34): Age: 16.3±2.5 yr; Gender: males=18, females=16; Time since injury: 16.3±2.5. Control (CTRL) Group (n=60): Age: 16.2±2.5 yr; Gender: males=27, females=33.

Intervention: None. Anthropometric testing.

Outcome Measures: Height, weight, waist circumference, percentage of trunk fat by Dual X-ray Absorptiometry, blood pressure, body mass index, fasting serum samples (glucose, insulin, triglycerides, total cholesterol, high density lipoprotein (HDL), low density lipoprotein (LDL); metabolic syndrome.

 1.         There was a significant difference in body weight between SB and CTRL, with SB weighing 14.6% less than CTRL (p<0.001) but no significant difference between SCI and CTRL or between SB and SCI.

2.        Percent total body fat and trunk fat was significantly different between each group, with SB averaging 6.3% more trunk fat than SCI and 11.5% more trunk fat than CTRL (among all 3 groups, p<0.001; SB versus SCI and SB versus CTRL, p=0.004).

3.        Obese SCI had been injured almost twice as long as nonobese SCI subjects (p<0.001).

4.        BMI z-scores were 0.7 higher in SB than CTRL and 1.36 higher in SB than SCI (p<0.001 for both).

5.        There were no significant differences in systolic BP z-scores; serum LDL, triglyceride, or cholesterol concentrations, or glucose between groups.

6.        Serum HDL concentrations lower in SCI.

7.        There was no significant difference in glucose between SCI and CTRL groups.

8.        A total of 5.9% of SB and 5.0% of SCI subjects had no components of metabolic syndrome.

9.        A total of 32.4% of SB and 35.0% of SCI subjects had 1 risk factor.

10.      A total of 61.8% of SB and 60.0% of SCI subjects had 2 risk factors of metabolic syndrome.

11.       In total, 32% of SB subjects and 55 .0% of SCI subjects met the criteria for metabolic syndrome (3+ criteria).

12.      There was a strong association between diagnostic group (SCI, SB, and CTRL) and presence of metabolic syndrome.
(Widman et al., 2007)

USA

Observational

N=115

(N=19 SCI)

 Population: SCI Group (n=19): Age: 16.0±3.2 yr; Gender: males=10, females=9; Level of injury: T4-6=10, T7-11=6, L1-5=3. Severity of injury: AIS A=13, AIS B=3, AIS C=1, AIS D=2. Height: males=158.0±15.4 cm, females=162.4±11.9 cm; Weight: males=65.8±23.6 kg, females=66.3±22.8 kg. Injury etiology: SCI (n=19), Spina Bifida (SB, n=37), Normal Weight Controls (CTRL, n=34), Overweight Controls (OW, n=25).

Intervention: Upper extremity, tabletop ergonomic testing.

Outcome Measures: Body Mass Index (BMI), shoulder and elbow strength, heart rate (HR), and oxygen consumption (VO2/kg), power output (PO).

 1.     For both males and females, the CTRL group was significantly lighter than the OW, SB, and SCI groups.

2.     The male and female SB and OW groups had significantly higher BMI than CTRL.

3.     Percent body fat of OW, SB, and SCI groups was significantly higher CTRL group.

4.     There was no significant difference in any of the peak strength values between the SB and SCI groups for either gender.

5.     Both the male and female CTRL groups had significantly greater shoulder extension strength values than the OW, SB, and SCI groups of the same gender.

6.     Within each gender, the SB and SCI groups had significantly lower VO2 peak values at rest than the CTRL and OW groups did.

7.     Accounting for body mass, the SB, SCI, and OW groups had significantly lower VO2 peak/kg than the CTRL group.

8.     For the males, the CTRL and OW groups reached similar max PO (86±4.4 W and 93±8.5 W, respectively), while both the SB and SCI groups reached exhaustion at significantly lower levels (62±4.9 W and 60±6.6 W, respectively) than either the CTRL or OW subjects; females showed similar relationships.

9.     All of the groups reached similar peak HR but the male and female SB groups had significantly higher resting HR than the CTRL group of the same gender.

13.      Mean resting HR for female SCI groups was also higher than the CTRL and OW groups.
(Liusuwan et al., 2004)

USA

Observational

N=54

(N=27 SCI)

 Population: SCI Group (n=27): Age: 10-21 yr, Gender: males=18, females, 9. Time since injury: 1-3 yr; Severity of injury: complete=3, incomplete=24, paraplegia=23, tetraplegia=4, AIS A=18, AIS B=2, AIS C=4, AIS D=3.

Able-Bodied Controls (CTRL, n=27): Age and sex matched to SCI group.

Intervention: None. Anthropometric Testing.

Outcome Measures: Height, weight, Lean Tissue Mass (LTM), % Body Fat, Bone Mineral Content (BMC), Body Mass Index (BMI), body composition, Resting Metabolic Rate (RMR)

 1.     There was no difference in height between the SCI and control groups.

2.     The weight of the SCI group was 14.5% lower than the weight of the able-bodied control group (p<0.005).

3.     The BMI of the SCI group was 1 0.8% less than the control group (p<0 .007).

4.     The SCI group had significantly lower mean LTM than CTRL group (p<0.001) and higher percent body fat (p<0.02) despite their reduced BMI (p<0.010.

5.     There was a significant reduction in the BMC in the SCI group compared with the controls (p<0 .007).

4.        The SCI group had lower RMR than the CTRL group (p<0.001) but there was no difference in RMR when adjusted for LTM.

Discussion

Seven papers related to CVS health in children with SCI/D-related paralysis were identified. Of the seven, four were observational studies, consisting of anthropometric measurements in cohorts of children that included those with traumatic and non-traumatic paralysis, specifically spina bifida (Liusuwan et al. 2007; Nelson et al. 2007; Widman et al. 2007); Liusuwan et al. (2007) and Widman et al. (2007) also included age and sex-matched able-bodied controls and obese able-bodied cohorts. (Liusuwan et al. 2004) compared SCI with age and sex-matched able-bodied controls.

Three of the papers described findings from the same randomized controlled study of 30 children with traumatic and nontraumatic SCI undergoing either FES-assisted lower extremity ergometry, passive lower extremity cycling, or no cycling electrical stimulation (Johnston, Smith, Betz, et al. 2008; Johnston, Smith, et al. 2009; Johnston, Smith, et al. 2008b).

Children with SCI were found to have higher fat mass and fat %, lower total lean mass, lower BMI, and higher rate of metabolic syndrome. Calculated BMI was found to underestimate body fat in children with SCI. Resting metabolic rate and energy consumption was found to be similar with controls when adjusted for muscle mass. Obesity was not consistently defined, with cut-off ranging 25-30% in males and 30-35% in females in different cohorts. Metabolic syndrome was more common in children with paralysis. Exercise was not found to significantly affect cardio-vascular or metabolic factors. FES-assisted lower limbs ergometry induced a statistically significant change in measure VO2, especially in the children with less neurologic involvement (lower thoracic and lumbar paralysis), but no significant difference in objective pre-post intervention values was noted. Muscle mass, volume, and strength were found to increase with FES, but exercise’s effect on lipid profile was, at the most, partial, limited, and inconsistent. It does appear that response to exercise in pediatric SCI is influenced by injury level, same as in adults.

The only interventional randomized controlled trial was limited by lack of true controls, as all three arms received some sort of exercise intervention (Johnston, Smith, et al. 2009). In addition, normative data for cardio-metabolic parameters were obtained from able-body children and adults with SCI. What the study did show was good adherence with the exercise protocol when the study is done in a home environment.

It is apparent from all controlled cohorts that, in children with SCI/D-related paralysis, physical inactivity and muscle loss are driving factors in the onset of cardio-metabolic complications. In addition, paralysis onset appears to create enduring vulnerabilities that influence the trajectory of cardiovascular health in this population.

Similar to the adult population (Weil et al. 2002), obesity is more prevalent in children with SCI/D-related paralysis and further studies are needed to assess if this is related to unhealthy diet, decreased physical activity patterns, and compounded by genetic, psychological, health behaviors (cigarette smoking, sleep>7hrs/night, etc.).

According to World Health Organization, children should exercise 60 min at moderate intensity per day with short bouts of anaerobic intensities and perform exercises to strengthen muscles and bones three times a week (World Health Organization 2010). The American College of Sports Medicine launched Exercise in Medicine in 2007, a global initiative designed to make exercise part of standard clinical care for people of all abilities (Medicine. 2021).

We already know that CVS risk factors models underestimate the risk for CVS disease events in adults with SCI (Barton TJ 2021). Assessing the role of inactivity related to pediatric-onset paralysis should be performed in a systematic way. In addition, prospective randomized studies with controls and adequate power are essential. A systematic analysis of the effect of exercise on functional and metabolic parameters that affect CVS health should be devised. Determining normative data for meaningful cardio-metabolic changes in children with paralysis should be undertaken. Looking at sensitive biomarkers of CVS health in the pediatric population, including those with paralysis is paramount. Instituting behavioral changes immediately after paralysis to offset the consequences of immobility should be a priority. Normalizing disability, and eliminating inequality to access to resources and care will require a societal intervention. Using technology to improve adherence to exercise and access to resources should be leveled.

Children with SCI/D paralysis consistently exhibit body composition and metabolic changes that predispose them to poor CVS health

There is no exercise/therapeutic intervention that has been proven to consistently/predictably improve the CVS profile in this population.

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