Cardiovascular Training in Spinal Cord Injury

Original Editor - Naomi O'Reilly

Top Contributors - Naomi O'Reilly and Kim Jackson  

Introduction

Cardiovascular training involves the use of oxygen to meet the energy demands of the body’s muscles during exercise. It is associated with longer duration exercise during a given session of training, often at a consistent pace. Regular cardiovascular training has been shown to improve cardiovascular function, aerobic capacity and exercise tolerance in individuals with a spinal cord injury, often resulting in improved independence in activities of daily living.

Definition

According to the Oxford Dictionary of Sport Science and Medicine, cardiovascular fitness is the "ability of the heart and blood vessels to supply nutrients and oxygen to tissues, including muscle, during sustained exercise".[1]

Assessment of Cardiovascular Fitness

Assessment of cardiovascular fitness is essential for physiotherapists to directly determine training or conditioning intensities required to elicit improvements in cardiovascular and cardiometabolic health. Gold standard laboratory-based assessment with ergometer i.e. arm crank, wheelchair treadmill is becoming more commonplace, particularly within competitive sport, although these results alone do not represent the full picture. Pushing proficiency, sport-specific skills, wheelchair propulsion technique, and individual adaptations to their wheelchair in order to develop appropriate exercise programs and monitor the response to training it is important to first assess cardiovascular fitness under reproducible test situations, ensuring factors such as the type of ergometer, constraints used, position of individual are standardised. Precautions should also be followed when conducting cardiovascular assessments as strenuous exercise can lead to a cardiovascular event.

Prior to completing any maximal exercise testing a detailed medical and surgical history is required to identify indications for an exercise test and determine any underlying conditions eg, cardiovascular, pulmonary, musculoskeletal, or neurological dysfunction or the presence of diabetes, hypertension or heart block requiring a pacemaker, anaemia, thyroid dysfunction, obesity, deformity, vertigo, or impaired cognitive function. It is also important to be aware of any medications that can influence the test procedures and the response to the exercise.[2][3]

Peak Oxygen Consumption Tests

The Peak Oxygen Consumption (VO2 Peak) test, equivalent to the VO2 Max test in able-bodied individuals, measures the maximal capacity of the body to deliver oxygen from the lungs to the mitochondria of exercising muscles by expired gas collection and is the most accurate way to assess cardiovascular fitness in spinal cord injury. The terminology is used to reflect the lower maximal rate of oxygen consumption with arm exercises v leg exercises due to both lower demand for oxygen from smaller muscle groups and the circulatory implication of arm exercise.[4]

In individuals with a spinal cord injury, the VO2 Peak Test is typically performed using an arm cycle ergometer, but can also be completed with manual wheelchair propulsion or handcycle on an ergometer or treadmill with gradually increasing exercise intensities until exhaustion. Rest periods of 20 - 30 seconds are at times provided for between each increment. Starting points for arm ergometry vary depending on the level of spinal cord injury and level of fitness. Power output can be adjusted by changing the cranking velocity and / or externally applied resistance. For example; [4]

  • Paraplegia; Start at 30 Watts and increase by 10 - 15 Watts every 2 minutes. Maximal power output is likely to be between 50 - 100 Watts.
  • Tetraplegia; Start at 5 Watts and increase by 2.5 - 10 Watts every 2 minutes. Maximal power output is likely to be between 10 - 50 Watts.

While the VO2 Peak is the gold standard method for assessing exercise response for an individual with a spinal cord injury, it is rarely used in spinal cord injury units due to the complex nature of the test.

Submaximal Exercise Tests

Submaximal exercise tests, typically involve measuring the responses to standardized physical activities that are typically encountered in everyday life and are more commonly used in individuals with a spinal cord injury to evaluate the adaptation of the oxygen transport system to exercise below maximal intensity, so that main energy system used is aerobic.[1] While portable expired gases analysis systems can be utilised and are often used in high-performance paralympic sport, heart rate measurement is more commonly used in spinal injury rehabilitation units. Use of heart rate measurements does not allow estimation of VO2 Peak, but is used as a means to monitor the response of individuals with a spinal cord injury to training, with improvements in cardiovascular fitness indicated by decreased heart rate at the same power output with training or improvements in individual's perception of exertion with the Borg Exertion Scale.[4][3]

Performed in a similar way to the VO2 Peak test with a different set of protocols and terminated prior to exhaustion. There are numerous submaximal protocols from which to choose, many of which have been developed to meet the needs of individuals with various functional limitations and impairments, including spinal cord injury. A commonly used protocol for individuals with a spinal cord injury includes 3 x 7 Minute Exercise Bouts of exercise at 40%, 60% and 80% of predicted maximal exercise capacity.[4]

  • Paraplegia with High Level of Fitness; 7 mins each at 40 Watts, 60 Watts and 80 Watts
  • Tetraplegia; 7 mins each at 20 Watts, 30 Watts and 40 Watts

Production of a sufficient level of exercise stress without physiologic or biomechanical strain is the key goal of submaximal testing. Factors that we believe should be considered in selecting the appropriate test include the person's primary and secondary pathologies and how these pathologies physically affect the person's daily life. Other factors include cognitive status, age, weight, nutritional status, mobility, use of walking aids or orthotic or prosthetic devices, independence, work situation, home situation, and the person's needs and wants. 

Submaximal exercise testing overcomes many of the limitations of maximal exercise testing, appears to have greater applicability to physiotherapists in their role as clinical exercise specialists compared with maximal exercise testing, and are much easier to implement within a spinal injury unit and rehabilitation setting.[3] There is new evidence to suggest that in cervical level spinal cord injury peak heart rate and blood lactate concentration attained during maximal incremental laboratory-based wheelchair exercise on a treadmill were below those attained during maximal field-based exercise testing in highly trained wheelchair rugby athletes, suggesting that incremental exercise testing in the laboratory does not elicit true peak cardiometabolic responses in highly-trained wheelchair rugby athletes with a cervical spinal cord injury and field exercise tests may give a better indication of maximal performance.[6]

Field Exercise Tests

A field exercise test is usually a measurement of a physiological function produced, while an athlete is performing in a simulated sport situation. While often thought not to be as reliable as lab-based tests, they are considered to have more validity as a result of greater specificity. A range of options can be used for field testing including;
Time Based; Measurements of distance travelled over a set period of time e.g. 12 min push standardised test
Distance Based; Measurements of time taken to complete certain distance e.g. Time for 1km

Implications for Rehab

  • Use of regular cardiovascular capacity testing during spinal cord injury rehabilitation allows us to monitor the impact of rehabilitation interventions on an individual level,
  • Incremental arm ergometry with small increments per stage is the most relevant means of assessment for peak cardiovascular capacity for individuals with a spinal cord injury,
  • Use of the submaximal wheelchair ergometer test is preferable to use for the assessment of daily life functioning,
  • Systematic reporting on test termination, peak outcomes criteria and adverse events is key to enhance comparability of results. [2]

Response to Cardiovascular Fitness Training

Response to cardiovascular fitness training is significantly influenced by the type of spinal cord injury including neurological level, level of completeness and extent of the injury. Those with an incomplete level of injury, particularly those who can ambulate and have some lower limb use during exercise, respond to exercise in a similar way to able-bodied individuals. While those with a complete cervical level injury or upper thoracic level injury have a significantly different response as a result of reliance on upper limb exercise, lower limb paralysis and most importantly loss of supraspinal sympathetic nervous control, which adversely affect cardiac output and arterio-venous oxygen; the two components of VO2 Peak.[4][7]

The Fick Principle summarises the relationship between cardiac output, arterio-venous oxygen difference and VO2 Peak;
VO2 Peak = Cardiac Output (Q) x (a-vO2 Difference) [4]
Key determinants of Heart Rate, Stroke Volume and Aterio-Venous Oxygen Difference
Heart Rate Stroke Volume Arterio-Venous Oxygen Difference
Sympathetic Nervous System

Parasympathtetic Nervous System

Circulating Noradrenalin

Intrinsic Heart Rhythm

Venous Return

After-Load

Contractility

Blood Volume

Size of Exercising Muscle Mass

Ability of Muscles to Extract Oxygen

  • Capillarisation
  • Number Mithochonria
  • Blood Flow through Exercising Muscle
  • Oxidative Enzyme Activity

Cardiac Output

Cardiac Output (Q) is defined as the amount of blood pumped by the left ventricle of the heart per minute. It is expressed as litres/minute.
Cardiac Output (Q) = Heart Rate (HR) x Stroke Volume (SV)

Heart Rate

Heart rate is determined by the balance between sympathetic control to the heart via T1 - T4 nerve roots that increase heart rate and parasympathetic control via the vagal nerve which decrease heart rate. The heart will beat at between 70 - 80 beats per min, the intrinsic firing rate of the sinoatrial node in the heart, without input from either the sympathetic or parasympathetic systems.

Normally during exercise in able-bodied individuals heart rate increases as a result of reduced vagal nerve activity and increased activity of the sympathetic nervous system, with maximal heart rates between 200 - 220bpm possible. [4]

In spinal cord injury lesions between T1 - T4 there is a partial loss of Supraspinal Sympathetic Control to the heart, with increases in heart rate occurring primarily as a result of the withdrawal of excitatory input from the vagal nerve, resulting in lower maximal heart rates of between 110 - 130. [4][7]

In spinal cord injury lesions T1 and above there is a complete loss of Supraspinal Sympathetic Control to the heart, with increases in heart rate occurring primarily as a result of the withdrawal of excitatory input from the vagal nerve. As a result in many individuals with tetraplegia they are unable to increase their heart rate beyond the natural rhythm of the heart, and as such, heart rate may not be considered the best indicator of training in tetraplegia.[7]

Stroke Volume

Stroke volume is the volume of blood ejected at each stroke of the heart during systole, with typical stroke volume in able-bodied individuals 70ml at rest increasing to a maximum of 120 ml during strenuous exercise. Typically stroke volume increases during exercise in able-bodied individuals as an adaption to cardiovascular training.

In spinal cord injury maximal stroke volume, and as a result cardiac output, are decreased due to loss of supraspinal sympathtic control below the level of the injury and use of the upper limb alone during exercise. Both these factors have a negative effect on venous return as a reult of venous pooling with reduced return of oxygen from the lower limbs and reduced intra-thoracic muscle pumps, and contractility, meaning less blood returning to the heart with each beat.[4]

Aterio-Venous Oxygen Difference

The arteriovenous oxygen difference is a measure of the amount of oxygen taken up from the blood by the tissues. Cardiac output and arteriovenous oxygen difference are the determinants of overall oxygen uptake. During exercise blood flow increases to the tissues; haemoglobin dissociates quicker and easier. This results in a greater arteriovenous oxygen difference during exercise. In trained athletes, the arteriovenous oxygen difference is greater as a result of the tissues becoming more efficient in oxygen uptake with aerobic training.[8]

Size Exercising Muscle Mass

The size of the exercising muscle mass is the most important determinant of the arteriovenous oxygen difference. This can be seen in able bodied athletes where the VO2 Max with upper limb exercise is approximately 70% of their VO2 Max when exercising with the lower limbs, which occurs as a result of reduced opportunity, need and ability to extract and utilize the oxygen with upper limb exercise. [4]

In spinal cord injury individuals with tetraplegia and partial paralysis in the upper limb have a smaller active muscle mass than those individuals with paraplegia, similarily those with an incomplete injury have a larger active muscle mass than those with a complete injury at the same neurolgical level. Cardiovascular training has the ability to increase the arteriovenous oxygen difference through muscle hypertrophy, resulting in increased muscle mass.[4]

Ability Muscle to Extract Oxygen

Oxygen extraction from the exercising muscle is the other key determinant of arteriovenous oxygen difference, which is determined by factors including some and type of muscle fibres, density of capillaries, regulation of blood flow, the size and number of mitochondria and type of metabolism, which tend to be relatively unaffected by spinal cord injury, although the loss of supraspinal sympathetic control can impact the ability of the body to redirect blood from non-essential organs to exercising muscles. Vasoconstrction in the non-essential organs occurs as a result of sympathetic activity during exercise in able bodied individuals, increasing blood flow to the exercising muscles and when this does not adequatley occur in individuals with a spinal cord injury it can result in exercise induced hypotension.[4][7]

Increased ability of the exercising muscles to extract oxygen, and therfore play a key role in increased VO2 Peak, is one of the key benefits from cardiovascular training in individuals with a spinal cord injury, both tetraplegia and paraplegia, which delays the onset of muscle fatigue and increases maximal exercise capacity.[4]

Exercise Prescription

Several national and international organisations e.g. American College of Sports Medicine provide clinicians and allied health professionals with guidelines on how to screen, assess, and, when appropriate, prescribe exercise for tdifferent population groups. A group led by Dr. Kathleen Martin Ginis at the University of British Columbia and Dr. Victoria Goosey-Tolfrey at Loughborough University, UK have recently developed international guidelines on exercise after spinal cord injury which provide minimum thresholds for improving cardiorespiratory fitness and muscle strength and for improving cardiometabolic health, which should be considered when prescribing cardiovascular exercise for individuals with a spinal cord injury, which you can read more about here.

Safe and effective exercise prescription requires careful consideration for the target individual's health status, baseline fitness, goals and exercise preferences. When considering exercise prescription in an individual with a spinal cord injury you should also consider their neurolgical level of injury, and the implications it may have the type of exercise available and the modifcations required to support their participation including trunk stability and balance, and use of strapping, gripping aids and assistive devices.[7] The FITT Principle (Frequency, Intensity, Time and Type) should be used to develop, guide and monitor cardiovascular training to ensure an effective exercise program, and the initials F, I, T, T, stand for: Frequency, Intensity, Time and Type.] For those only starting to participate in cardiovascular training, start with smaller amounts of exercise and gradually increase the duration, frequency and intensity.

FITT Principle [7]
F I T
F Frequency How Often to Train 3 - 5 Days per Week
I Intensity How Hard to Train 50 - 80% Peak Herat Rate

Can use Borg Scale to monitor

T Time of Exercise How Long to Train 20 - 60 minutes
T Type of Exercise What Exercise Continuous Training

Varied Pace Training

Interval Training

Frequency

In line with the new Spinal Cord Injury Exercise Guidelines to improve cardiorespiratory fitness, adults with a spinal cord injury should engage in at least;
Aerobic Exercise 2 times per week for Cardiorespiratory Fitness
Aerobic Exercise 3 times per week for Cardiometabolic Health
For those not already exercising, start with a lower frequency and gradually increase the frequency as a progression towards meeting the guidelines, recognising that exercise below the recommended levels may or may not bring small changes in cardiorespiratory fitness.[9]

Intensity

This is an extremely important aspect of the FITT Principle and is probably the hardest factor to monitor, particulalry in individuals with a spinal cord injury. In able bodied individuals heart rate is the most commonly used method to gauge the intensity of cardiorespiratory exercise, but this is less reliable for individuals with a spinal cord injury who have loss of supraspinal sympathetic control.[4][7][10]

Subjective measures of aerobic intensity such as Rating of Percieved Exerction Scales are suggested to be the most appropraite method to use in a clinical setting to monitor training intensity, although currently there is a lack of moderate or high-quality evidence for a strong clinical recommendation for their use. However there is some emerging evidence to suggest use of the overall RPE 6-20 Scale and current recommendations state that “Overall RPE 6-20 can tentatively be used to assess and form the basis for regulating upper-body exercise at a moderate to vigorous intensity in adults with chronic spinal cord injury who have high fitness levels, have been familiarized with the measure and areprompted with the scale during exercise" [10]

In line with the new Spinal Cord Injury Exercise Guidelines to improve cardiorespiratory fitness, adults with a spinal cord injury should engage in at least;
Moderate to Vigorous Intensity Aerobic Exercise for Cardiorespiratory Fitness and Cardiometabolic Health
For those not already exercising, start with a lower intensity and gradually increase the intensity as a progression towards meeting the guidelines, recognising that exercise below the recommended levels may or may not bring small changes in cardiorespiratory fitness.[9]

Time

In line with the new Spinal Cord Injury Exercise Guidelines to improve cardiorespiratory fitness, adults with a spinal cord injury should engage in at least;
20 Mins of Aerobic Exercise for Cardiorespiratory Fitness
30 Min of Aerobic Exercise for Cardiometabolic Health
For those not already exercising, start with smaller amounts of time and gradually increase the time as a progression towards meeting the guidelines, recognising that exercise below the recommended levels may or may not bring small changes in cardiorespiratory fitness.[9]

Type

While it may seem restrictive initially, there are a wide range of exercise types available to individuals with a spinal cord injury including wheelchair propulsion (daily wheelchair or racing wheelchair), handcycling / handcycle ergometer, nordic skier, rowing, swimming, seated aerobics, and wheelchair sports including wheelchair basketball, wheelchair rugby, wheelchair tennis. [4][7] The appropriate type of exercise will be dependant on the needs of the individual and whetherpower output needs to be monitored. Ergometers provide the means to monitor exercise, improve overall cardiovascular fitness and exercise capacity but the benefits may not be transferrable to wheelchair propulsion, particulalry during early rehabilitation post injury where the individual may be significantly deconditioned.Individual motivation and adherance to a cardiovascular training programme is key, and variety in the training programme can be useful to improve adherance. Cardiovascular traiing programs should balance frequency, intensity, and duration for maximum effectiveness and safety.

Upper Limb Training

Upper limb training can incorporate a wide choice of exercise activities including hand crank ergometry, handcycling, nordic ski, rowing, swimming etc.and can be adapted to the needs of the individual. A SCIRE Review outlined the following significant evidence that individuals witha spinal cord injury can improve their cardiovascular fitness and physical work capacity through aerobic upper limb exercise training. [11]

  • Level 1b evidence that vigorous intensity (70% - 80% HR Reserve) exercise leads to greater improvements in aerobic capacity than moderate intensity (50 - 60% HR Reserve) exercise.[12] 
  • Level 1b and Level 2 evidence that moderate intensity aerobic arm training, performed 20-60 min/day, three days/week for at least 6-8 weeks, is effective in improving aerobic capacity and exercise tolerance of individiuals with a spinal cord injury. [13] 
  • Level 2 evidence that hand cranking against a workload corresponding to 60% of WMax, performed 3-5 hours/day for one year, increases WMax and VO2 Max.[14] 
  • Level 2 evidence that hand cycling exercise increases the power output, oxygen consumption, and muscle strength in individuals with paraplegia, but not tetraplegia during active rehabilitation.[15]
  • Level 4 evidence that hand cycling increases power output and oxygen consumption in individuals with tetraplegia, although further research is warranted.[16]
  • Level 4 evidence that hand cycling interval training program increases peak power output and peak VO2 in individuals with paraplegia and tetraplegia.[17]
  • Level 5 evidence that aortic pulse wave velocity is significantly lower in hand cyclists with a spinal cord injury compared to sedentary individuals with a spinal cord injury.[18]

Treadmill Training

Treadmill training is often used more commonly during the rehabilitation phase following a spinal cord injury and in individuals with a incomplete spinal cord injury. In the SCIRE Review they show the following growing list of evidence for body weight supported treadmill training (BWSTT) to improve indicators of cardiovascular health in individuals with complete and incomplete spinal cord injury. [11]

  • Level 1a evidence that cardiac autonomic balance improves in persons with tetraplegia and paraplegia with BWSTT. [19] 
  • Level 2 evidence that standing and stepping exercises with BWSTT can increase VO2 and heart rate levels in individuals with spinal cord injury.[20]
  • Level 2 evidence that gait training with neuromuscular electrical stimulation can increase metabolic and cardiorespiratory responses in individuals with complete tetraplegia.[21]
  • Level 4 evidence that arterial compliance is improved with BWSTT in individuals with motor-complete spinal cord injury.[22]
  • Level 4 evidence of decreased walking exercise heart rate following 8 weeks of underwater treadmill training.[23] 
  • Multiple Level 4 evidence that BWSTT increases peak oxygen uptake and heart rate, and decreases the dynamic oxygen cost for individuals with spinal cord injury.[24][25] 

Functional Electrical Stimulation

There is evidence that use of Functional Electrical Stimulation training may improve muscular endurance, oxidative metabolism, exercise tolerance, and cardiovascular fitness. [11]

  • Level 1b evidence handcycling has beneficial effects on metabolic syndrome components, inflammatory status and visceral adiposity. [26]
  • Level 4 evidence that FES assisted arm-crank exercise increases peak power output, and may increase oxygen uptake. [27]
  • Level 4 evidence that decreased platelet aggregation and blood coagulation occurs following FES leg cycle ergometry in individuals with a spinal cord injury. [28] 
  • Multiple Level 4 evidence that exercise cardiac function is improved with FES training in individuals with a spinal cord injury. [29][30][31]
  • Multiple Level 4 evidence that a minimum of three days per week FES training for two months may be effective for improving musculoskeletal fitness, the oxidative potential of muscle, exercise tolerance, and cardiovascular fitness. [32][33][34][35][36][37][38][39]
  • Level 5 evidence that metabolic rate, heart rate, and ventilation levels are higher during hybrid cycling than during hand cycling.[40]

Resources

Physical Activity Recall Assessment for People with Spinal Cord Injury (PARA-SCI)

Physical Activity Recall Assessment for People with Spinal Cord Injury (PARA-SCI) is a self-report physical activity measure for individuals with spinal cord injury. It aims to measure type, frequency, duration, and intensity of physical activity performed by individuials with a spinal cord injury who use a wheelchair as their primary mode of mobility.

ProACTIVE SCI Toolkit

The ProACTIVE SCI Toolkit, from SCI Action Canada, is designed to help physiotherapists work with individuals with a spinal cord injury to be physically active outside of the clinic. It's a step-by-step resource that uses three overarching strategies including education, referral, and prescription to develop tailored strategies that work for both the physiotherapist and the individual with a spinal crod injury.

Active Living Leaders

Active Living Leaders is comprised of a series of peer-mentor training videos with a goal of helping people who would like to use the latest physical activity knowledge, sport resources, and transformational leadership principles to inform and motivate adults living with a spinal cord injury to lead more active lives.

SCI-U Physical Activity Course for Individuals with Spinal Cord Injury

SCI-U Physical Activity Course is a collection of modularized training sessions.  It includes Modules on Living an Active Life, Ways to Get Fit, Overcoming Barriers and Reaching Your Goal.

SCI Action Canada Knowledge Mobilization Training Series

SCI Action Canada's Knowledge Mobilization Training Series (KMTS) is a collection of modularized training sessions, with the goal of advancing physical activity knowledge and participation among individuals living with spinal cord injury. It includes Modules on the Physical Activity Guidelines and Physical Activity Planning.

References

  1. 1.0 1.1 Kent M, Kent DM. The Oxford Dictionary of Sports Science and Medicine. New York: Oxford University Press; 2006.
  2. 2.0 2.1 Eerden S, Dekker R, Hettinga FJ. Maximal and submaximal aerobic tests for wheelchair-dependent persons with spinal cord injury: a systematic review to summarize and identify useful applications for clinical rehabilitation. Disability and rehabilitation. 2018 Feb 27;40(5):497-521.
  3. 3.0 3.1 3.2 Noonan V, Dean E. Submaximal exercise testing: clinical application and interpretation. Physical therapy. 2000 Aug 1;80(8):782-807.
  4. 4.00 4.01 4.02 4.03 4.04 4.05 4.06 4.07 4.08 4.09 4.10 4.11 4.12 4.13 4.14 Harvey, Lisa. (2008). Chapter 12: Cardiovascular Fitness Training. In Management of Spinal Cord Injuries: A Guide for Physiotherapists. London: Elsevier
  5. Brad Zdanivsky. VO2Max Testing at UBC. Available from: https://youtu.be/hqbtcjXDxto[last accessed 30/10/17]
  6. West CR, Leicht CA, Goosey-Tolfrey VL, Romer LM. Perspective: does laboratory-based maximal incremental exercise testing elicit maximum physiological responses in highly-trained athletes with cervical spinal cord injury?. Frontiers in physiology. 2016 Jan 14;6:419.
  7. 7.0 7.1 7.2 7.3 7.4 7.5 7.6 7.7 Goosey-Tolfrey, Vicky and Price, Mike. (2010). Chapter 3: Physiology of Wheelchair Sport. In Wheelchair Sport: A Complete Guide for Athletes, Coaches and Teachers. London: Elsevier
  8. Glynn, AJ, Fiddler H. Chapter 1: Introduction to Exercise Physiology in The physiotherapist’s pocket guide to exercise: assessment, prescription and training. Elsevier Health Sciences, 2009. p1 - 11
  9. 9.0 9.1 9.2 Ginis KA, van der Scheer JW, Latimer-Cheung AE, Barrow A, Bourne C, Carruthers P, Bernardi M, Ditor DS, Gaudet S, de Groot S, Hayes KC. Evidence-based Scientific Exercise Guidelines for Adults with Spinal Cord Injury: An Update and a New Guideline. Spinal Cord. 2018 Apr;56(4):308.
  10. 10.0 10.1 Van der Scheer, J. W., Hutchinson, M. J., Paulson, T., Martin Ginis, K. A., & Goosey-Tolfrey, V. L. (2018). Reliability and Validity of Subjective Measures of Aerobic Intensity in Adults With Spinal Cord Injury: A Systematic Review. PM&R, 10(2), 194–207. doi:10.1016/j.pmrj.2017.08.440 
  11. 11.0 11.1 11.2 Warburton DER, Krassioukov A, Sproule S, Eng JJ (2018). Cardiovascular Health and Exercise Following Spinal Cord Injury. In Eng JJ, Teasell RW, Miller WC, Wolfe DL, Townson AF, Hsieh JTC, Connolly SJ, Noonan VK, Loh E, Sproule S, McIntyre A, Querée M, editors. Spinal Cord Injury Rehabilitation Evidence. Version 6.0. Vancouver: p 1- 68.
  12. de Groot PC, Hjeltnes N, Heijboer AC, Stal W, Birkeland K. Effect of training intensity on physical capacity, lipid profile and insulin sensitivity in early rehabilitation of spinal cord injured individuals. Spinal Cord 2003; 41: 673-9.
  13. Davis GM, Shephard RJ, Leenen FH. Cardiac effects of short term arm crank training in paraplegics: echocardiographic evidence. Eur J Appl Physiol Occup Physiol 1987; 56: 90-6.
  14. Milia R, Roberto S, Marongiu E, et al. Improvement in hemodynamic responses to metaboreflex activation after one year of training in spinal cord injured humans. BioMed Research International.2014; 2014: 1-9.
  15. Hjeltnes N, Wallberg-Henriksson H. Improved work capacity but unchanged peak oxygen uptake during primary rehabilitation in tetraplegic patients. Spinal Cord 1998; 36: 691-8.
  16. Valent LJ, Dallmeijer AJ, Houdijk H, Slootman HJ, Post MW, van der Woude LH. Influence of hand cycling on physical capacity in the rehabilitation of persons with a spinal cord injury: a longitudinal cohort study. Arch Phys Med Rehabil 2008; 89: 1016-22.
  17. Nooijen CF, Van Den Brand IL, Ter Horst P, Wynants M, Valent LJ, Stam HJ, Van Den BergEmons,RJ. Feasibility of Handcycle Training during Inpatient Rehabilitation in Persons with Spinal Cord Injury. Arch Phys Med Rehabilitation 2015; 96:1654-57.
  18. Hubli M, Currie KD, West CR, Gee CM, Krassioukov AV. Physical exercise improves arterial stiffness after spinal cord injury. J Spinal Cord Med. 2014; 37:782-85.
  19. Millar PJ, Rakobowchuk M, Adams MM, Hicks AL, McCartney N, MacDonald MJ. Effects of short-term training on heart rate dynamics in individuals with spinal cord injury. Auton Neurosci 2009; 150:116-21
  20. Jeffries EC, Hoffman SM, de Leon R, et al. Energy expenditure and heart rate responses to increased loading in individuals with motor complete spinal cord injury performing body weight-supported exercises. Archives of Physical Medicine & Rehabilitation. 2015; 96:1467-73.
  21. de Carvalho DC, Martins CL, Cardoso SD, Cliquet A. Improvement of metabolic and cardiorespiratory responses through treadmill gait training with neuromuscular electrical stimulation in quadriplegic subjects. Artif Organs 2006; 30: 56-63.
  22. Ditor DS, Macdonald MJ, Kamath MV, Bugaresti J, Adams M, McCartney N, et al. The effects of body- weight supported treadmill training on cardiovascular regulation in individuals with motor-complete SCI. Spinal Cord 2005; 43: 664-73.
  23. Stevens SL, Morgan DW. Heart Rate Response During Underwater Treadmill Training in Adults with Incomplete Spinal Cord Injury. Topics in Spinal Cord Injury Rehabilitation. 2015; 21:40-8
  24. Jack LP, Allan DB, Hunt KJ. Cardiopulmonary exercise testing during body weight supported treadmill exercise in incomplete spinal cord injury: a feasibility study. Technol Health Care 2009; 17: 13-23.
  25. Soyupek F, Savas S, Ozturk O, Ilgun E, Bircan A, Akkaya A. Effects of body weight supported treadmill training on cardiac and pulmonary functions in the patients with incomplete spinal cord injury. J Back Musculoskelet Rehabil 2009; 22: 213-8.
  26. Bakkum AJT, de Groot S, Stolwijk-Swüste ,JM, van Kuppevelt ,DJ, van der Woude ,LHV., Janssen TWJ. Effects of hybrid cycling versus handcycling on wheelchair-specific fitness and physical activity in people with long-term spinal cord injury: a 16-week randomized controlled trial. Spinal Cord. 2015; 53:395-401
  27. Taylor JA, Picard G, Widrick JJ. Aerobic capacity with hybrid FES rowing in spinal cord injury: comparison with arms-only exercise and preliminary findings with regular training. PMR 2011; 3: 817-24.
  28. Kahn NN, Feldman SP, Bauman WA. Lower-extremity functional electrical stimulation decreases platelet aggregation and blood coagulation in persons with chronic spinal cord injury: a pilot study. J Spinal Cord Med 2010; 33: 150-8.
  29. Hopman MT, Groothuis JT, Flendrie M, Gerrits KH, Houtman S. Increased vascular resistance in paralyzed legs after spinal cord injury is reversible by training. J Appl Physiol 2002; 93: 1966-72.
  30. Gerrits HL, de Haan A, Sargeant AJ, van Langen H, Hopman MT. Peripheral vascular changes after electrically stimulated cycle training in people with spinal cord injury. Arch Phys Med Rehabil 2001; 82: 832-9.
  31. Ragnarsson KT, Pollack S, O'Daniel W, Jr., Edgar R, Petrofsky J, Nash MS. Clinical evaluation of computerized functional electrical stimulation after spinal cord injury: a multicenter pilot study. Arch Phys Med Rehabil 1988; 69: 672-7.
  32. Barstow TJ, Scremin AM, Mutton DL, Kunkel CF, Cagle TG, Whipp BJ. Changes in gas exchange kinetics with training in patients with spinal cord injury. Med Sci Sports Exerc 1996; 28: 1221-8.
  33. Crameri RM, Cooper P, Sinclair PJ, Bryant G, Weston A. Effect of load during electrical stimulation training in spinal cord injury. Muscle Nerve 2004; 29: 104-11.
  34. Zbogar D, Eng JJ, Krassioukov AV, Scott JM, Esch BT, Warburton DE. The effects of functional electrical stimulation leg cycle ergometry training on arterial compliance in individuals with spinal cord injury. Spinal Cord 2008; 46: 722-6.
  35. Griffin L, Decker MJ, Hwang JY, Wang B, Kitchen K, Ding Z, et al. Functional electrical stimulation cycling improves body composition, metabolic and neural factors in persons with spinal cord injury. J Electromyogr Kinesiol 2009; 19: 614-22.
  36. Hjeltnes N, Aksnes AK, Birkeland KI, Johansen J, Lannem A, Wallberg-Henriksson H. Improved body composition after 8 wk of electrically stimulated leg cycling in tetraplegic patients. Am J Physiol 1997; 273: R1072-9.
  37. Faghri PD, Glaser RM, Figoni SF. Functional electrical stimulation leg cycle ergometer exercise:training effects on cardiorespiratory responses of spinal cord injured subjects at rest and during submaximal exercise. Arch Phys Med Rehabil 1992; 73: 1085-93.
  38. Hooker SP, Figoni SF, Rodgers MM, Glaser RM, Mathews T, Suryaprasad AG, et al. Physiologic effects of electrical stimulation leg cycle exercise training in spinal cord injured persons. Arch Phys Med Rehabil 1992; 73: 470-6.
  39. Mohr T, Andersen JL, Biering-Sorensen F, Galbo H, Bangsbo J, Wagner A, et al. Long-term adaptation to electrically induced cycle training in severe spinal cord injured individuals. Spinal Cord 1997;35: 1-16.
  40. Bakkum AJT, de Groot S, Onderwater MQ, de Jong J, Janssen TWJ. Metabolic rate and cardiorespiratory response during hybrid cycling versus handcycling at equal subjective exercise intensity levels in people with spinal cord injury. J Spinal Cord Med 2014; 37:758-64