Abstract
BACKGROUND
Although peak oxygen uptake (VO2peak) is considered the most useful index of functional capacity, it’s difficult to interpret the results of cardiopulmonary exercise testing (CPET) in individuals with spinal cord injury (SCI). In fact, VO2peak is usually normalized for total body weight, but body composition in persons with SCI largely varies depending on physical activity and time since injury, with a progressive loss of fat-free mass (FFM). This can lead to a misinterpretation of the cardiopulmonary fitness in this population.
AIM
Our study proposes a methodology of evaluation, based on bioelectrical impedance analysis (BIA), which could provide more individualized and accurate data in sportsmen with SCI.
DESIGN
Case-control study.
POPULATION
Ambulatory patients at the Sports Medicine Unit of the IRCCS A. Gemelli University Polyclinic Foundation, Rome, Italy.
METHODS
Comparison of data derived from BIA, echocardiography and CPET between 10 male sportsmen with complete, high SCI (group T) and 10 able-bodied controls (group C).
RESULTS
Mean VO2peak, weight-normalized VO2peak, fat-free mass (FFM)-normalized VO2peak and body cellular mass (BCM)-normalized values were significantly lower in group T. At the same heart rate (on average the 55% of the maximal theoretical for age), mean of absolute VO2, weight-normalized VO2 and FFM-normalized VO2 were still significantly lower in group T. Considering the BCM-normalized VO2, the group T showed greater values than controls, 39.4±7.8 vs. 31.1±8.5 mL/kg/min.
CONCLUSIONS
Body composition is a crucial factor for properly interpreting a CPET in individuals with SCI. In particular, normalization of VO2peak values for the BCM seems the most reliable tool to assess the real functional capacity in this population.
CLINICAL REHABILITATION IMPACT
A more accurate definition of the aerobic power and functional capacity of people with SCI can improve the monitoring of rehabilitations protocols and physical exercise in this population.
Key words: Oxygen consumption, Para-athletes, Wheelchair, Exercise test
Peak oxygen uptake (VO2peak) is considered one of the best indexes of aerobic fitness and functional capacity. In persons who have suffered a spinal cord injury (SCI), it assumes an even greater relevance, being related to cardiovascular risk,1, 2 to the ability to perform daily activities and ultimately to the quality of life.3
Although some authors have tried to provide standards of normality4 or to create predictive equations,5 it is difficult to interpret the results of cardiopulmonary exercise testing (CPET) in individuals with SCI, for different reasons. First, the small number of studies available, often conducted with different methodologies and on small case series. Second, the heterogeneity of the population, ranging from people with low/incomplete spinal lesions and low impairment to others with high/complete lesions and poor residual functional capacity. Furthermore, VO2peak is usually normalized for body weight, being expressed in milliliters per minute per kilogram (mL/min/kg), but body composition in persons with SCI largely varies depending on physical activity, time since injury, with a progressive loss of fat-free mass (FFM),6, 7 etc.
Given that VO2peak is negatively correlated with total body fat percentage and positively with FFM,8-10 it is clear that the criteria of normalization utilized for able-bodied people have an intrinsic limit.
Moreover, the CPET provides, beyond the VO2peak, many parameters which can help in identifying cardiac and/or respiratory diseases,11, 12 but the above-mentioned problems often make difficult for physicians to interpret such parameters in individuals with SCI and to understand what can be considered “normal” or “abnormal.”
The bioelectrical impedance analysis (BIA) might be of help in this context. Through an instrument (the bio-impedance meter) that is very simple to use and inexpensive, it is possible to determine the resistance to flow of a current through the body, providing estimates of body water from which body fat (fat-mass), FFM and body active cellular mass (BCM) can be calculated using equations. Everything that is “not fat” is defined FFM. The FFM includes the extra-cellular mass (ECM) and the body active cellular mass (BCM). The ECM represents the metabolically inactive parts of the body components including bone, minerals and blood plasma, while the BCM includes muscle tissue, organs, red blood cells and tissue cells. In other words, the BCM is the metabolically active cell mass involved in O2 consumption, CO2 production and energy expenditure. In able-bodied individuals, BCM tends to decrease with age and it depends on sex, as well as the FFM, but it is less influenced by race than the FFM.13-15 In subjects with SCI, the severity of the lesion and the time elapsed by it must be added, factors that cause further reduction in bone density and muscle atrophy in variable and different percentages between 25% and 50%.16
The aim of this study is to try to remove or reduce the confounding factors in assessing the cardio-respiratory profile of adult individuals with complete, high SCI (C4-C7), physically active and with no overt cardiac and/or respiratory diseases. Doing that, we try to provide a yardstick against the parameters considered normal in able-bodied subjects and we propose a methodology for evaluating individuals with SCI which could be useful to assess the real functional capacity in this population.
Materials and methods
Study design
We conducted a case-control study in the Sports Medicine Unit of the IRCCS A. Gemelli University Polyclinic Foundation in Rome, Italy.
Participants
The study population consisted of 10 male wheelchair rugby players with complete SCI (group T) between level C4 and C7 (AIS Grade A).17 Ten healthy, sedentary individuals matched for the age served as controls (group C).
The inclusion criteria were: 1) male sex; 2) age between 20 and 40; 3) not being affected by conditions able to influence the oxygen consumption or the body composition estimation (beyond the SCI), in particular systolic or diastolic disfunction of the left ventricle, hypertension, coronary artery disease, myopathies, hematological disease like anemia, dehydration.
Data sources and variables
The study protocol included:
anthropometric measurements and bioelectrical impedance analysis (BIA; Akern Bodygram Plus, Akern SRL, Pontassieve, Florence, Italy) with analysis of FM, FFM, relative FFM (percentage of the whole body mass), BCM. The BIA was performed placing four gel electrodes on the dorsal surfaces of the right hand and foot, with a test frequency of 50 kHz;
two-dimensional echocardiography (Toshiba Artida SSH-880 CV, Toshiba Medical Systems, Inc. Tustin, CA, USA);
CPET with an arm-crank ergometer (ERGOLINE Ergoselect 400 and K5 metabolimeter, Cosmed SRL, Rome, IT), using an incremental exercise protocol of 15 watt (W) every 2 minutes.
In individuals of group T, height was obtained through the sum of the measurements of the individual body segments (length of the head from the vertex to the chin, length of the neck from the chin to the suprasternal point, length of the thorax from the suprasternal point to the pubic symphysis, length of the inferior limb from the antero-superior iliac spine to the internal malleolar point, distance from the malleolar point inside the heel). Weight was measured using a platform scale Seca 635 (Seca Inc., CA, USA), initially measuring the weight of the patient sitting in a wheelchair and subsequently subtracting the weight of the wheelchair only.
Echocardiographic measurement of left atrial size (LA), left ventricular end-diastolic diameter (LVDD), interventricular septum end-diastolic thickness (IVSd) and posterior wall end-diastolic thickness (PWd) were performed in parasternal long-axis view; the ejection fraction (EF) was calculated in 4 chambers view using the Simpson’s single plane algorithm; left ventricular mass (LVM) was calculated using the Teichholz’s formula; the diameter of the inferior vena cava (IVC) was measured from the subcostal view. For verifying the absence of diastolic disfunction, the mitral E/A ratio was measured in the 4-chambers view.18
Statistical analysis
We compared the two groups with regard to:
anthropometric measures;
left ventricle size, wall thickness, mass and function;
resting and maximum heart rate (HR) reached during the CPET, arterial blood pressure (BP) and workload (WL) reached, peak oxygen uptake (VO2peak), weight-normalized VO2peak, FFM-normalized VO2peak, BCM-normalized VO2peak, peak oxygen pulse (VO2/HR), VE/VCO2 slope, resting and peak CO2 end-tidal pressure (PETCO2), oxygen uptake efficiency slope (OUES) and oxygen consumption/WL (VO2/Watt) slope. Predicted values of VO2peak were obtained using Wasserman’s formula.12, 19, 20
Finally, in group T, we analyzed the correlation between time since injury (in months) and echocardiographic and cardiopulmonary parameters.
Continuous variables are presented as mean (SD) or median (IQR), depending on the shape of the distribution curve. Student’s t-test or the Wilcoxon signed-rank test were performed to evaluate differences between the two groups. Pearson’s test was utilized for the correlations’ analysis. A P value <0.05 was considered to indicate statistical significance. All computations were carried out by SPSS v. 22.0 (SPSS Inc., Chicago, IL, USA).
Ethics standard
The whole study was conducted according the GCP, the Helsinki’s declaration and the “Standards for Ethics in Sport and Exercise Science Research”. The study design was approved from the Ethics Committee of our Institution (study protocol no. 6549/18), and written consent was obtained from participants.
Results
Characteristics of the study population and comparation between the two groups are summarized in Table I.
Table I. —Details of the population’s characteristics and comparation between participants with SCI (T) and controls (C).
| Parameters | Group T | Group C | P value | 95% CI |
|---|---|---|---|---|
| N. subjects | 10 | 10 | ||
| Age (years) | 34±4 | 34±4 | - | - |
| Weight (kg) | 75.5±10.0 | 71.6±8.9 | 0.40 | -13.2; 5.5 |
| Height (cm) | 178.9±5.2 | 174.3±7.2 | 0.12 | -10.5; 1.3 |
| BMI | 23.6±3.9 | 23.5±2.1 | 0.93 | -3.1; 2.9 |
| BSA Dubois (m2) | 1.93±0.12 | 1.86±0.14 | 0.23 | -0.20; 0.05 |
| Time since injury (months) | 176±70 | - | ||
| Arm-crank ergometer exercise testing | ||||
| Resting Heart Rate (bpm) | 54±6 | 75±11 | <0.01* | 12; 29 |
| Peak Heart Rate (bpm) | 102±9 | 177±10 | <0.01* | 66; 84 |
| % of the theor. | 55±6 | 95±5 | <0.01* | 35; 44 |
| Max workload (W) | 43.5±8.5 | 114.0±21.2 | <0.01* | 55.3; 85.7 |
| Peak arterial SBP (mmHg) | 128±14 | 158±22 | <0.01* | 14; 48 |
| Peak arterial DBP (mmHg) | 65±5 | 80±8 | <0.01* | 9; 22 |
| Echocardiography | ||||
| LA (mm) | 34.2±2.9 | 33.7±3.1 | 0.76 | -2.4; 3.2 |
| LA ind (mm/m2) | 17.5±1.7 | 18.4±1.5 | 0.20 | -0.6; 2.4 |
| LVDD (mm) | 52.9±2.9 | 49.9±4.1 | 0.05 | -6.8; -0.2 |
| LVDD ind (mm/m2) | 27.4±1.7 | 26.6±1.5 | 0.27 | -2.3; 0.7 |
| LVSD (mm) | 32.4±2.3 | 29.5±3.6 | 0.05 | -5.8; 0.1 |
| IVSd (mm) | 8.3±0.9 | 8.2±0.6 | 0.68 | -0.9; 0.6 |
| PWd (mm) | 8.1±0.9 | 7.9±0.7 | 0.50 | -1.0; 0.5 |
| LVM (g) | 126.6±20.4 | 117.4±33.8 | 0.64 | -35.8; 17.4 |
| LVM ind (g/m2) | 65.4±8.8 | 62.8±14.9 | 0.64 | -14.2; 9.1 |
| EF (%) | 60.3±3.7 | 59.6±2.9 | 0.47 | -3.8; 2.4 |
| IVC (mm) | 17.3±4.0 | 22.4±4.1 | <0.05* | 1.3; 9.0 |
| IVC ind (mm/m2) | 9.0±2.1 | 12.1±2.2 | <0.01* | 1.1; 5.1 |
| Bio-impedentiometry | ||||
| Fat mass (kg) | 25.0±6.2 | 18.1±4.8 | <0.05* | -12.3; -1.7 |
| Fat-free mass (kg) | 56.1±5.3 | 58.6±5.0 | 0.3 | -2.3; 7.3 |
| % of FFM | 75.0±6.2 | 82.1±4.8 | <0.05* | 1.8; 12.3 |
| Body cellular mass (kg) | 22.9±2.4 | 35.4±3.3 | <0.01* | 9.8; 15.2 |
| Cardiopulmonary testing | ||||
| VO2peak (mL/min) | 889±134 | 2016±300 | <0.01* | 901; 1351 |
| VO2peak /kg (mL/min/kg) | 12.1±2.8 | 28.3±3.7 | <0.01* | 13.2; 19.3 |
| % of the theor. | 31±7 | 70±9 | <0.01* | -46; -31 |
| VO2peak /FFM (mL/min/kg) | 12.0±1.7 | 24.1±5.8 | <0.01* | 7.8; 16.3 |
| VO2peak /BCM (mL/min/kg) | 39.4±7.8 | 55.8±10.1 | <0.05* | 7.9; 24.9 |
| VO255 (mL/min) | 889±134 | 1087±257 | <0.05* | 1; 395 |
| VO255 /kg (mL/min/kg) | 12.1±2.8 | 15.4±4.4 | 0.06 | -0.15; 6.8 |
| VO255 /FFM (mL/min/kg) | 12.0±1.7 | 18.7±5.1 | <0.05* | -1.1; 6.7 |
| VO255 /BCM (mL/min/kg) | 39.4±7.8 | 31.1±8.5 | <0.05* | -15.9; -0.6 |
| VE/VCO2 slope | 26.2±6.6 | 25.9±4.4 | 0.89 | -5.6; 4.9 |
| PETCO2 at baseline (mmHg) | 34.2±4.4 | 35.0±2.7 | 0.63 | -2.6; 4.3 |
| PETCO2 peak (mmHg) | 40.1±3.7 | 40.1±4.3 | 1 | -3.8; 3.8 |
| OUES | 1072±380 | 1913±355 | <0.01* | 495; 1186 |
| VO2/HR peak (mL/bpm) | 8.6±1.5 | 12.2±2.3 | <0.05* | 1.7; 5.4 |
| VO2/W slope (mL/min/W) | 10.6±4.2 | 14.3±1.7 | <0.05* | 0.6; 6.8 |
BMI: Body Mass Index; BSA: body surface area; SBP: systolic blood pressure; DBP: diastolic blood pressure; LA: left atrium; ind: indexed for BSA; LVDD: left ventricle diastolic diameter; LVSD: left ventricle systolic diameter; IVSd: inter-ventricular septum diastolic thickness; PWd: posterior wall diastolic thickness; LVM: left ventricle mass; EF: ejection fraction; IVC: inferior vena cava; OUES: oxygen uptake efficiency slope; HR: heart rate. *Statistically significant difference. 95% CI refers to the differences between the means of the two groups.
Mean age was 34±4 years. Details of the subjects included in group T are provided in Supplementary Digital Material 1 (Supplementary Table I and II).
None of the anthropometric parameters showed significant differences between the two groups.
Mean time since injury (TSI) was 176±70 months (min. 83, max. 248 months).
Body composition
Absolute FM was significantly higher in group T, 25.0±6.2 vs. 18.1±4.8 kg, while absolute FFM was similar, 56.1±5.3 vs. 58.6±5.0 kg. Relative FFM was significantly lower in individuals of group T, 75.0±6.2% vs. 82.1±4.8%, as well as the BCM, 22.9±2.4 vs. 35.4±3.3 kg.
Echocardiography
No statistically significant differences were found between the two groups as regard echocardiographic left atrial size, left ventricular size, wall thickness, mass and function, both in absolute and BSA-indexed values (details in Table I). As expected, participants with SCI had smaller inferior vena cava’s size than controls, both in absolute and BSA-indexed values, 17.3±4.0 vs. 22.4±4.1 mm and 9.0±2.1 vs. 12.1±2.2 mm, respectively.
CPET
Mean resting HR was significantly lower in group T, 54±6 vs. 75±11 bpm, as well as the maximum HR reached during the exercise testing, 102±9 vs. 177±10 bpm, corresponding on average to the 55±6% and the 95±5% of the predicted values for participants’ age (P<0.01). Maximum WL sustained at the arm-crank ergometer was significantly lower in group T, 43.5±8.5 vs. 114.0±21.2 watts, as well as arterial systolic and diastolic BP at peak exercise, which were respectively 128±14 vs. 158±22 mmHg and 65±5 vs. 80±8 mmHg.
Mean VO2peak value was significantly lower in group T, 889±134 vs. 2016±300 mL/min, as well as the weight-normalized VO2peak (VO2/kg), 12.1±2.8 vs. 28.3±3.7 mL/min/kg (Figure 1A, B), corresponding on average to the 31±7% and 70±9% (P<0.01) of the predicted values for age according the Wasserman’s formula.15
Figure 1.
—A) Mean values of peak oxygen uptake (VO2peak); B) weight-normalized VO2peak (VO2/kg); C) FFM-normalized VO2peak (VO2/FFM) and BCM-normalized VO2peak (VO2/BCM) in individuals with SCI (T) vs. controls (C). On the right column (D-F) is reported the comparison between peak values in individuals with SCI vs. values at the 55% of the maximum theoretical heart rate for age of the controls. Wiskers = 95% CI.
FFM-normalized VO2peak (VO2/FFM) was also significantly lower in group T, 12.0±1.7 vs. 24.1±5.8 mL/kg/min, as well as the BCM-normalized values (VO2/BCM), 39.4±7.8 vs. 55.8±10.1 mL/kg/min (Figure 1C).
Peak oxygen pulse (VO2/HR) values were significantly lower in group T, 8.6±1.5 vs. 12.2±2.3 mL/bpm, as well as the OUES values, 1072±380 vs. 1913±355 and the VO2/W slope values, 10.6±4.2 vs. 14.3±1.7 mL/min/W.
Resting and peak PETCO2, as well as the VE/VCO2 slope, showed no significant differences between the two groups, being respectively 34.2±4.4 vs. 35.0±2.7 mmHg, 40.1±3.7 vs. 40.1±4.3 mmHg and 26.2±6.6 vs. 25.9±4.4.
Participants with SCI during exercise reached an average HR of 55% of the maximal theoretical for their age. In order to determine how much this single parameter could have influenced the VO2peak values, we analyzed the VO2 of controls at the 55% of their maximal theoretical HR (VO255%) and then we compared that values with the VO2peak values of the group T. In this case, mean values were still significantly lower in individuals with SCI as regard the absolute VO2, 889±134 vs. 1087±257 mL/min, the weight-normalized VO2, 12.1±2.8 vs. 15.4±4.4 mL/min/kg and the FFM-normalized VO2, 12.0±1.7 vs. 18.7±5.1 mL/kg/min (Figure 1D-F). On the contrary, when we considered the BCM-normalized VO2, individuals with SCI showed significantly greater values than controls, 39.4±7.8 vs. 31.1±8.5 mL/kg/min (Figure 1F).
Finally, no significant correlation was found in Group T between time since injury and all echocardiographic and cardiopulmonary parameters.
Discussion
Our study offers some interesting insights about how to interpret the data derived from a cardio-pulmonary exercise testing (CPET) and from the body composition analysis in individuals with high and complete SCI.
Body composition
As expected, participants with SCI had more FM and less BCM than controls. On the contrary, absolute FFM was lower but not significantly different. This probably because the healthy lifestyle, the work of arms to move the wheelchair and the physical training allowed the individuals with SCI to partially compensate the loss of FFM in the lower limbs with an increase in the upper ones, compatibly with the residual motor function. As a consequence, the FFM of sportsmen with SCI was comparable to a sedentary able-bodied individual of the same age.
Echocardiographic parameters
As regard the left atrial size, left ventricular size, wall thickness, mass and function, both in absolute and BSA-indexed values, there were not significant differences between the two groups (Figure 2), probably for similar reasons. Conversely, as known for a long time,21, 22 the inferior vena cava was significantly smaller in individuals with SCI, due to the reduced venous return from the lower limbs which cannot be compensated in any way.
Figure 2.
—Echocardiographic (A, C) and CPET (B, D) evaluation of a 35-year-old participant with SCI (A, B) and of a 32-year-old control (C, D). Despite the difference in absolute values of peak oxygen uptake (VO2peak) and VO2/W slope, both individuals have normal systolic/diastolic function of the left ventricle.
CPET parameters and body composition
Obviously, participants with SCI had significant inferior global functional capacity compared to able bodied controls, as well as lower values of indexes of cardio-vascular efficiency like the OUES, the oxygen pulse peak (VO2/HRpeak) and the VO2/W Slope.
The aerobic functional capacity of group T participants, evaluated with an arm-crank ergometer and expressed in terms of VO2peak, absolute or weight-normalized, corresponded on average to the 43-44% of the controls (889 vs. 2016 mL/min, 12.1 vs. 28.3 mL/min/kg). These values corresponded on average to the 31% of the theoretical optimal values for the age calculated with the Wasserman’s formula, the most used and widespread, and are similar to the reference values of normality proposed by Janssen et al. for this population.4 The distance between individuals with SCI and able-bodied ones slightly shortened when we normalized the VO2peak for the FFM, while it significantly decreased when we normalized it for the BCM, with the participants with SCI showing a functional capacity on average equal to the 70% of the controls. This is probably because, in SCI people, the FFM could not have the same composition than in able-bodied subjects. In fact, the FFM includes water, proteins, bone minerals, soft tissue minerals and glycogen. At the cellular level, these FFM compartments are organized into BCM, extracellular fluid and extracellular solids.23 In individuals with SCI, for example, especially those with high and complete lesions, the modification over the time of the bone mineral content can influence the composition of the FFM, with an only partial effect on the capacity of oxygen utilization. On the contrary, as well explained by Moore et al.,24 the BCM is a “component of body composition containing the oxygen-exchanging, potassium-rich, glucose-oxidizing, and work-performing tissue.” In other words, whereas FFM is everything that is not body fat, the BCM is the metabolically active tissue.
On these bases, we can say that in people with SCI normalizing the VO2 values for the BCM is probably the best way to assess the cardio-respiratory fitness, reducing as much as possible the confounding factors linked to the peculiar body composition, the time since injury, etc. Moreover, as underlined by various authors, studying the BCM could probably eliminate differences related to sex, adiposity13 and ethnicity.14, 15
Even normalizing the VO2peak for BCM, individuals with SCI showed lower values than able-bodied ones. This difference can be attributable to the lower maximal HR they reached during the CPET, due to the sympathetic impairment secondary to the high and complete spinal lesion. In our study, participants with SCI reached on average the 55% of the maximal predicted HR for age, while able-bodied ones the 95%.
For the same reasons, other VO2-derived parameters like the peak oxygen pulse (VO2/HRpeak) and the VO2/W slope resulted lower than normal in this population. In order to understand the “weight” of this aspect, we compared the VO2peak values of participants with SCI with those of controls at the 55% of their maximal predicted HR for age (VO255). In this case, while a difference was still present for absolute, weight-normalized and FFM-normalized values, if considering the BCM-normalized VO2peak individuals with SCI had higher values than the controls. This finding strengthens our considerations as regard the potential utility of BCM-normalized values as reference and shows what it is the effect of the chronotropic incompetence on the functional capacity of people with high and complete SCI.
From another point of view, we can state that, when functionally evaluating middle-aged, active individuals with high and complete SCI, if we utilize the standard reference values and prediction formulas provided with a common CPET software, a VO2peak value around 25-30% of the theoretical one for the age can still be considered “normal,” as well as a reduced VO2/HRpeak value until 6.5-7 mL/bpm, a reduced OUES until 590-600 and a reduced VO2/W slope until 6-7 mL/min/W.
Limitations of the study
The main limitation of this study is the small number of participants, which makes difficult to generalize some considerations. However, it is very difficult to find sportsmen with high SCI and we believe that our work provides useful ideas and bases for further studies. Another limitation can be the role of the bioelectrical impedance analysis in people with SCI. This investigation is less reliable than the dual-energy X-ray absorptiometry (DXA), often used to study this population. However, our purpose was to suggest a methodology of evaluation as non-expensive, easy and feasible as possible. In our opinion, the BIA can be a better compromise between costs and usefulness.
Conclusions
Body composition might be the most appropriate marker for properly interpreting a CPET in individuals with SCI. In fact, the difference between the weight-normalized VO2peak values in able-bodied individuals and those with SCI it is substantially due to the different body composition and the different maximal heart rate reached during exercise. In particular, normalization of VO2peak values for the BCM seems the most reliable tool to assess the real functional capacity in this population. Given the low cost and the easy feasibility of the bioelectrical impedance analysis, the small numbers available in literature and the potential usefulness in reducing as much as possible the confounding factors, we believe that future functional studies in people with SCI, when possible, should include this kind of examination.
Supplementary Digital Material 1
Supplementary Table I
Details of the participants from group T (part I)
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Associated Data
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Supplementary Materials
Supplementary Table I
Details of the participants from group T (part I)