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Home » Cardiovascular Training in Spinal Cord Injury

Cardiovascular Training in Spinal Cord Injury

Introduction

Cardiovascular training involves the use of oxygen to meet the energy demands of the body’s muscles during exercise. It has to do with longer duration workouts performed at a consistent pace during a given session. Regular cardiovascular training has been shown to improve Cardiovascular function Aerobic capacity and exercise tolerance in patients with spinal cord injury often improve independence in activities of daily living.

Definition

According to the Oxford Dictionary of Sports Science and Medicine, cardiovascular fitness refers to the ability of the heart and blood vessels to deliver nutrients and oxygen to tissues, including muscles, during sustained exercise. [1]

Assessment of Cardiovascular Fitness

Cardiovascular fitness assessment is essential to determine the intensity of training or conditioning required to improve cardiovascular and cardiovascular health in a trained individual. The gold standard based on laboratory testing (i.e. a ergometer arm crank wheelchair treadmill) is becoming especially common in competitive sports. But the results of these experiments alone do not give us a complete picture. It is paramount to first evaluate cardiovascular dynamics under reproducible test conditions with instrumental standard limits applied and experimental position. Because strenuous exercise can cause a cardiovascular event physical therapists should consider caution during the assessment.

Before completing any ultimate exercise test, a physiotherapist should obtain a detailed medical and surgical history to identify indications for exercise testing and determine status any underlying. These include: cardiovascular pulmonary artery disease and bone or muscle dysfunction the presence of diabetes mellitus hypertension cardiac arrest requiring pacemaker anemia thyroid dysfunction obesity deformity vertigo or impaired cognitive function. It is also important to be aware of any medications that may influence testing protocols and responses to the exercises.[2][3]

Peak Oxygen Consumption Tests

The Peak Oxygen Consumption (VO2 Peak) test, which is equivalent to the VO2 Max test in non-disabled individuals, measures the maximum ability of the body to transfer oxygen from the lungs to the mitochondria of exercising muscles via air on an outdated collection. It is the most accurate method of cardiovascular examination fitness in spinal cord injury. This definition reflects the maximum oxygen consumption during hand exercises compared to leg exercises. By lower oxygen demand from small groups of muscles and blood flow indicating arm exercises.[4]

VO2 Peak Test Test conditions for individuals with spinal cord injury:

  • Performed on an ergometer or treadmill using an arm cycle ergometer manual wheelchair propulsion handwheel.
  • Exercise intensity is gradually increased until exhaustion.
  • The starting point for an arm ergometer varies with the degree of spinal cord injury and fitness level.
  • Power output can be adjusted by varying the actuation speed and/or externally applied resistance. E.g
VO2 peak test example:[4]
  • Individual with paraplegia: Start at 30 Watts and increase by 10 – 15 Watts every 2 minutes. The peak power output is likely to be between 50 – 100 Watts.

  • Individual with tetraplegia: Start at 5 Watts and increase 2.5 – 10 Watts every 2 minutes. The peak power output is likely to be between 10 – 50 Watts.

Although VO2 Peak is the gold standard method for assessing motor response in SCI patients, it is rarely used in SCI units due to the complexity of the test.

[5]

Submaximal Exercise Tests

Submaximal exercise testing is often used to measure responses to standardized daily physical activity in patients with spinal cord injury. They assess the adaptation of the oxygen delivery system to submaximal intensity exercise so that the primary energy system used is Aerobic.[1]

Examples of submaximal exercise tests are:

  • An obsolete portable gas analysis system for use in high-performance Paralympic sports
  • Use of heart rate measurements in spinal cord injury centers

But the use of heart rate measurement does not allow the monitor to estimate VO2 Peak. It helps to monitor the response of individuals with spinal cord injury to training. Improvements in cardiovascular fitness are indicated by decreases in heart rate at the same intensity as training or improvement of an individual’s perception of exertion using the Borg Physical Activity Scale.[4][3]

There are many submaximal protocols to choose from many of which meet the needs of individuals with functional limitations and disorders including spinal cord injury. Common protocols for individuals with spinal cord injury include 3 x 7 Minute Exercise Bouts of exercise at 40% 60% and 80% of the predicted maximum exercise intensity.[4]Exercise is measured by continuously performing a graded arm crank protocol. Suggested programs for individuals with disabilities and tetraplegia who are very healthy are as follows:

  • Highly fit paraplegic; 7 minutes at 40W, 7 minutes at 60W, 7 minutes at 80W.

  • Quadriplegic; 7 minutes at 20W, 7 minutes at 30W, 7 minutes at 40W.

The goal of submaximal testing is to establish a level of athletic activity that does not provide physiological or biomechanical stress to the trainee. Factors to consider when selecting the appropriate test include:

  • Primary and secondary lesions and how they affect people’s daily lives
  • Cognitive status
  • Age
  • Weight
  • Nutritional Status
  • Mobility
  • Use of walking aids
  • Use of orthotic or prosthetic devices
  • Level of Independence
  • Work Situation
  • Home Situation
  • Needs and Wants

Submaximal exercise testing overcomes many of the limitations of maximal exercise testing. They appear to be more suitable for physiotherapists in the role of clinical exercise specialist and are easier to implement in spinal injury wards and rehabilitation settings. [3]

Emerging evidence also shows that in individuals with severe spinal cord injury, peak heart rate and blood lactate concentrations obtained during laboratory-based maximally incremental wheelchair exercise on a treadmill are lower than those obtained in Trained wheelchair rugby players. This suggests that incremental exercise testing in the laboratory does not elicit a true peak cardiometabolic response in highly trained wheelchair rugby players with severe spinal cord injury. Field exercise tests can better indicate Maximum performance. [6]

Field Exercise Tests

Field exercise testing measures the physiological function of athletes as they perform under simulated athletic situations. It is generally considered less reliable than laboratory-based tests, but they have higher validity due to their higher specificity. Below is the range of options for field testing:

Time-based; measures distance traveled over a set period of time, eg. 12 minutes to push standardized tests

Distance-based; measures the time it takes to complete a certain distance, eg. 1 km time

Implications for Rehab
  • Periodic cardiovascular volume testing during SCI rehabilitation allows physical therapists to monitor the impact of rehabilitation interventions on an individual level.
  • Incremental arm ergometry with small increases in each phase is the best method to assess maximal cardiovascular capacity for individuals with spinal cord injury.
  • the lowest wheelchair ergometer test is ideal for assessing function of daily living.
  • Systematic reporting of test termination peak result criteria and adverse events is key to improving comparability of results. [2]

Response to Cardiovascular Fitness Training

Response to cardiovascular fitness training is influenced by the degree, integrity, and severity of spinal cord injury. Individuals with incomplete injuries, especially those who can ambulate and use their lower extremities during exercise, respond to exercise similar to No one was injured. Individuals with a complete cervical level injury or an upper thoracic level injury respond significantly differently due to paralysis of the lower limbs dependent on upper limb movement and loss of supraspinal sympathetic control. The latter has adverse effects on the heart Output and Arteriovenous Oxygen are the two components of VO2 Peak. [4][7]

The following is the Fick principle summarizing the relationship between cardiac output arteriovenous oxygen difference and VO2 Peak;

VO2 Peak = Cardiac Output (Q) x (a-vO2 Difference) [4]

Key Determinants of Heart Rate Stroke Volume and Arteriovenous Oxygen Difference Heart Rate Stroke Volume Arteriovenous Oxygen Difference Sympathetic Nervous System Parasympathetic Nervous System Circulation Norepinephrine Intrinsic Heart Rhythm Venous Return Contractility Blood Volume Building muscle mass Ability of muscle to extract oxygen Capillarization Number of mitochondria Via training muscle blood flow Oxidative enzyme activity

Cardiac Output

Cardiac output (Q) is defined as the volume of blood pumped by the left ventricle of the heart per minute. It is expressed in liters per minute.

Cardiac output (Q) = heart rate (HR) x stroke volume (SV)

Heart Rate

Heart rate is determined by the balance between sympathetic input to the heart through T1 – T4 nerve fibers that increase heart rate and parasympathetic control through vagal innervation that decreases heart rate. The heart rate will be between 70 – 80 beats per minute. This is the intrinsic firing rate of sinoatrial node in the heart that does not receive input from either the sympathetic or parasympathetic system.

Typically, during exercise in non-disabled individuals, heart rate increases due to decreased vagal activity and increased sympathetic nervous system activity, with a maximum heart rate likely to be between 200 – 220bpm. [4]

In spinal cord injury lesions between T1-T4, supraspinal sympathetic control of the heart is partially lost and heart rate increases primarily due to withdrawal of excitatory input from the vagus nerve. This results in a lower maximum heart rate at 110 – 130.[4][7]

In spinal cord injury lesions of T1 and above, supraspinal sympathetic control of the heart is completely lost. This results in an increase in heart rate due to the withdrawal of excitatory input from the vagus nerve. In people with quadriplegia, the heart rate cannot be increased beyond natural levels The rhythm of the heart. Therefore, heart rate may not be considered the best indicator of training effectiveness in quadriplegic patients. [7]

Stroke Volume

Stroke volume is the amount of blood ejected per cardiac stroke during systole. Typical bladder volumes in non-disabled individuals are 70ml at rest increasing to as much as 120 ml during strenuous exercise as an adjustment for cardiovascular training.

In individuals with spinal cord injury, peak stroke volume and cardiac output are reduced due to loss of suprasspinal sympathetic control below the level of injury and use of only the upper limbs during exercise -because of the correction. These factors harm venous return: venous pooling with reduced return of decreased oxygen supply from the lower limbs and intra-thoracic muscle pumps and contractility meaning less blood is returned to the heart with each beat.[4]

Arteriovenous Oxygen Difference

Differences in tissue oxygenation reflect the amount of oxygen taken up by the tissues from the blood. Cardiac output and the difference in tissue oxygenation are the determinants of total oxygen consumption. During exercise blood flow to the muscles increases; hemoglobin is rapidly dissociated and a increased arteriovenous oxygen concentration. In trained athletes, muscle oxygen contrast increases due to muscle efficiency in oxygen uptake during aerobic training.[8]

Size Exercising Muscle Mass

The size of the exercising muscle is the most important determinant of differences in tissue oxygenation. This can be seen in non-disabled athletes where the VO2 Max of the upper extremities is approximately 70% of their VO2 Max when they exercise their lower limbs. This happens because opportunity requirements and decreased ability to extract and utilize oxygen through upper limb exercise. [4] .

In spinal cord injury, individuals with tetraplegia and partial upper limb paralysis have smaller motor function than those individuals with paraplegia. Similarly, those with complete injury have greater muscle activity than those with complete injury to the same muscle colleague. Cardiovascular training has the ability to increase tissue oxygen contrast by increasing muscle mass with increased muscle weight.[4]

Muscle’s Ability to Extract Oxygen

Oxygen removal from exercising muscle is the other major determinant of differences in muscle oxygenation. Properties include muscle fibers that are density of capillaries regulation of blood flow and determine oxygen extraction mitochondria size and number and metabolism. These features are usually less affected by spinal cord injury although the loss of control over the spine can affect the body’s ability to pump blood from non-vital organs to the exercising muscles influence of. Vasoconstriction in non-vital organs occurs as a result of sympathetic activity during exercise in nondisabled subjects increasing blood flow to the exercising muscles. Failure of this to occur successfully in individuals with spinal cord injury can lead to exercise-induced hypertension.[4][7]

The ability of the exercising muscles to excrete increased oxygen and therefore play an important role in increasing VO2 Peak is one of the major benefits of cardiovascular training in individuals with spinal cord injury (tetraplegia and paraplegia). all) of one because it causes muscle fatigue to begin prolonged and increased the ultimate exercise.[4]

Exercise Prescription

Several national and international organizations (e.g. American Academy of Sports Medicine) provide guidance to clinicians and allied health professionals on how to screen for and when appropriately prescribe exercise for different groups of people. A team led by Dr. Kathleen Martin Ginis at the University of British Columbia and Dr. Victoria Goosey-Tolfrey of Loughborough University UK have recently developed international guidelines for exercise after spinal cord injury that provide minimum requirements for cardiorespiratory fitness improve and improve muscle strength cardiovascular health. These should be considered when prescribing cardiovascular exercises for individuals with spinal cord injury. You can read more about these guidelines here.

Safe and effective exercise prescribing requires careful consideration of an individual’s target health status, baseline fitness goals, and exercise preferences. When considering exercise prescriptions for individuals with spinal cord injuries, physical therapists should consider the following levels Take nerve damage into consideration as it can affect the types of exercise available and any modifications needed to successfully participate in therapy. Such modifications may include: trunk stabilization and balance using strapping and grasping aids and assistive devices. [7] Fett Guidelines (frequency intensity time and type) should be used to develop guidelines and monitor cardiovascular training to ensure an effective exercise program. For those new to cardiovascular training, start with smaller volumes and gradually increase the duration frequency and intensity.

FITT Principle[7]FITFF Frequency Train 3 – 5 days a week I Intensity Training Difficulty 50 – 80% Peak Heart Rate can be monitored using Borg Scale T Exercise Time How Long to Train 20 – 60 Minutes T Exercise Type What Exercise Continue to Train Multiple Steps training interval training

Frequency

In line with the new 2017 International Spinal Cord Injury Exercise Guidelines to improve cardiorespiratory fitness, adults with spinal cord injuries should participate as a minimum;

Cardio fitness 2 times a week

3x a week of cardio for cardiometabolic fitness

Those who are not already exercising should start at a lower frequency and gradually increase the frequency as you progress toward the guidelines, recognizing that exercising below recommended levels may or may not result in small changes in cardiorespiratory fitness. [9]

Intensity

This is an extremely important aspect of the FITT principle and it is probably the most difficult factor to monitor, especially in patients with spinal cord injury. Among people without disabilities, heart rate is the most common measure of cardiorespiratory exercise intensity, but it is Reliability is lower in patients with spinal cord injury who have lost supraspinal sympathetic control. [4][7][10]

Subjective measures of aerobic exercise intensity, such as perceived exercise scale ratings, are considered the most appropriate method for monitoring training intensity in a clinical setting. Although there is currently a lack of moderate or high-quality evidence to provide a strong clinical recommendation For their use, there is some emerging evidence suggesting the use of the overall RPE 6-20 scale. Therefore, the current recommendations state, “Overall RPE 6-20 may be used tentatively to assess and form the basis for regulating the upper body of moderate to vigorous intensity exercise in adults.” Chronic spinal cord injuries with a high fitness level are already familiar with the measure and are prompted during exercise. [10]

According to new spinal cord injury exercise guidelines to improve cardiorespiratory fitness, adults with spinal cord injuries should participate in:

Moderate to vigorous-intensity aerobic exercise for cardiorespiratory and cardiometabolic fitness

For those who are not already exercising, start at a lower intensity and gradually increase the intensity to progress toward the guidelines, recognizing that exercising below recommended levels may or may not result in small changes in cardiorespiratory fitness. [9]

Time

Consistent with the new Spinal Cord Injury Exercise Guidelines for improving cardiorespiratory fitness, at a minimum, adults with spinal cord injury should participate;

20 minutes of aerobic exercise for Cardiorespiratory Fitness

30 minutes of aerobic exercise for Cardiometabolic Health

For those who aren’t already exercising, start with smaller sessions and gradually increase the time as a progression to guidelines that are accepted as lower than recommended levels of physical activity can with or without minor changes in cardiorespiratory fitness.

Type

While it may seem limited at first there are many types of exercises available for individuals with spinal cord injuries including wheelchair mobility (everyday wheelchair or wheelchair treadmill ) wrist/wrist ergometer nordic skier rowing swimming seated aerobics and wheelchair included sports including wheelchair basketball wheelchair rugby and wheelchair tennis.[4][7] The appropriate exercise will depend on the needs of the individual and whether the force output needs to be monitored. Ergometers provide ways to monitor exercise to improve both cardiovascular fitness and exercise capacity. However the benefits may not extend to wheelchair racing especially during early rehabilitation after injury where the person’s condition may be more independent. Individual motivation and adherence to a cardiovascular training program are significant and varied during the training process can be useful to improve adherence. Cardiovascular training programs must balance frequency and duration to be most effective and safe.

Upper Limb Training

Surface training can incorporate a wide range of exercise activities including hand crank ergometry handcycling nordic ski rowing swimming and more and can be adapted to suit the needs of the individual. A Spinal Cord Injury Research Evidence (SCIRE) Program review described the following important factors evidence that individuals with spinal cord injury can improve cardiovascular fitness and physical performance capacity through aerobic upper limb exercise training.[11] This page on Certification Grades and Ratings explains what each of these levels means.

  • High-intensity (70% – 80% heart rate reserve) exercise improves aerobic capacity more than moderate-intensity (50 – 60% heart rate reserve) exercise (evidence level 1b). [12]
  • Moderate-intensity aerobic arm training for 20-60 minutes per day, three days per week for at least 6-8 weeks is effective in improving aerobic capacity and exercise tolerance in people with spinal cord injury (level 1b and level 2 evidence). 13]
  • Hand cranking A workload corresponding to 60% of the achievable workload (WMax) performed for 3–5 hours per day for one year increased WMax and VO2 Max (level 2 evidence). [14]
  • Hand cycling increased power output, oxygen consumption and muscle strength in paraplegics but not in tetraplegics during active rehabilitation (level 2 evidence). [15]
  • Although further research is needed (level 4 evidence), hand cycling increases power output and oxygen consumption in tetraplegics. [16]
  • A hand circuit interval training program increases peak power output and peak VO2 in paraplegics and tetraplegics (level 4 evidence). [17]
  • Aortic pulse wave velocity was significantly lower in hand cyclists with SCI compared with sedentary individuals with SCI (evidence level 5). [18]
Treadmill Training

Treadmill training is often more commonly used in the rehabilitation phase after SCI and in individuals with incomplete SCI. In a SCIRE review they present the following growing list of evidence that body weight supported treadmill training (BWSTT) improves Cardiovascular health indicators in patients with complete and incomplete spinal cord injuries. [11]

  • There is level 1a evidence that cardiac autonomic balance is improved by BWSTT in quadriplegic and paraplegic patients. [19]
  • There is level 2 evidence that standing and stepping exercises using the BWSTT increase VO2 and heart rate levels in people with spinal cord injuries. [20]
  • Level 2 evidence that gait training with neuromuscular electrical stimulation can increase metabolic and cardiorespiratory responses in individuals with complete tetraplegia.[21]
  • Section 4 evidence that neural compliance is effective in BWSTT in individuals with motor complete spinal cord injury.[22]
  • Level 4 evidence of walking exercise heart rate reduction after 8 weeks of submerged training in a treadmill.[23]
  • Multiple Level 4 evidence that BWSTT increases maximal oxygen uptake and heart rate and reduces active oxygen costs for individuals with spinal cord injury.[24][25]
Functional Electrical Stimulation

There is evidence that training with functional electrical stimulation (FES) improves muscular endurance, oxidative exercise tolerance, and cardiovascular fitness. [11]

  • Level 1b evidence that hand circulation has beneficial effects on metabolic syndrome components inflammatory status and visceral adiposity. [26]
  • Level 4 evidence suggests that FES-assisted arm cranking increases peak power output and may increase oxygen uptake. [27]
  • Level 4 evidence of decreased platelet aggregation and blood clotting following FES leg cycle ergometric testing in patients with spinal cord injury. [28]
  • Multiple levels of level 4 evidence suggest that FES training improves exercise cardiac function in patients with spinal cord injury. [29][30][31]
  • Multiple levels of level 4 evidence suggest that two months of FES training at least three days per week may be effective in improving musculoskeletal fitness, muscular exercise tolerance, and oxidative potential for cardiovascular fitness. [32][33][34][35][36] [37][38][39]
  • Level 5 evidence shows that hybrid bikes have higher metabolic rate, heart rate and ventilation levels than manual bikes. [40]
Resources

Physical Activity Recall Assessment in Patients with Spinal Cord Injury (PARA-SCI)

The Physical Activity Recall Assessment in Patients with Spinal Cord Injury (PARA-SCI) is a self-report measure of physical activity in patients with spinal cord injury. It is designed to measure the type, frequency, duration, and intensity of physical activity performed by people with spinal cord injuries A person whose primary mode of mobility is a wheelchair.

ProACTIVE SCI Toolkit

The ProACTIVE SCI Toolkit from SCI Action Canada is designed to help physical therapists work with spinal cord injury patients to engage in physical activity outside of the clinic. It is a step-by-step resource using three overarching strategies including educational referral and prescribing Develop tailored strategies for physical therapists and people with spinal cord injuries.

Active Living Leaders

Active Living Leaders consists of a series of peer-mentor training videos designed to help inform and motivate adults with spinal cord injuries for those who wish to use the latest physical activity knowledge, sports resources and transformational leadership principles to Live a more active life.

SCI-U Physical Activity Program for Patients with Spinal Cord Injury

The SCI-U Physical Activity Course is a collection of modular training courses. It includes modules on how to live an active lifestyle adapted to overcome obstacles and achieve goals.

SCI Action Canada Knowledge Mobilization Training Series

SCI Action Canada’s Knowledge Mobilization Training Series (KMTS) is a series of modular training courses designed to increase knowledge and participation in physical activity for people with spinal cord injuries. It includes modules on physical activity guidelines and physical activity program.

References

  1. ↑ Jump up to:1.0 1.1 Kent M, Kent DM. The Oxford Dictionary of Sports Science and Medicine. New York: Oxford University Press; 2006.
  2. ↑ Jump up to: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. ↑ Jump up to: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. ↑ Jump up to: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. ↑ Jump up to: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. ↑ Jump up to: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. ↑ Jump up to:10.0 10.1 van der Scheer JW, Hutchinson MJ, Paulson T, Martin Ginis KA, Goosey-Tolfrey VL. Reliability and Validity of Subjective Measures of Aerobic Intensity in Adults With Spinal Cord Injury: A Systematic Review. PM R. 2018 Feb;10(2):194-207.
  11. ↑ Jump up to: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.
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  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
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  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
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  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.
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  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.
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