Upper Limb Rehabilitation Following Spinal Cord Injury

Danielle Rice PhD (c) Pavlina Faltynek P MSc McIntyre A MSc RN Swati Mehta PhD Brianne Foulon HBA Robert Teasell MD FRCPC

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Key Points

Neuromuscular stimulation-assisted exercise following a SCI is effective in improving muscle strength, preventing injury and increasing independence in all phases of rehabilitation.

Augmented feedback does not improve motor function of the upper extremity in SCI rehabilitation patients.

Intrathecal baclofen may be an effective intervention for upper extremity hypertonia of spinal cord origin.

Restorative therapy interventions need to be associated with meaningful change in functional motor performance and incorporate technology that is available in the clinic and at home.

The use of concomitant auricular and electrical acupuncture therapies when implemented early in acute spinal cord injured persons may contribute to neurologic and functional recoveries in spinal cord injured individuals with AIS A and B.

There is clinical and intuitive support for the use of splinting for the prevention of joint problems and promotion of function for the tetraplegic hand; however, there is very little research evidence to validate its overall effectiveness.

Shoulder exercise and stretching protocol reduces post SCI shoulder pain intensity.

Acupuncture and Trager therapy may reduce post-SCI upper limb pain.

Prevention of upper limb injury and subsequent pain is critical.

Reconstructive surgery appears to improve pinch, grip and elbow extension functions that improve both ADL performance and quality of life in tetraplegia.

Nerve transfer surgery to restore hand and upper limb function in the person with tetraplegia is emerging as another surgical alternative. This review has been prepared based on the scientific and professional information available in 2013. The SCIRE information (print, CD or web site www.scireproject.com) is provided for informational and educational purposes only. If you have or suspect youThe have usea health of problem, neuroprostheses you should consult yourappears health care to provider. have Thea positive SCIRE editors, impact contributors on andpinch supporting and partnersgrip shall strength not be liable and for anyADL damages, functions claims, liabilities, in C5 -costsC6 orcomplete obligations arising tetraplegia, from the use however,or misuse of thi s material.

Riceacce D, Faltynekss to P, the McIntyre devices A, Mehta, are S, Foulonlimited BL, andTeasell continue RW. (2016). Upperto be Limb expensive Rehabilitation in Following use. Spinal Cord Injury. In Eng JJ, Teasell RW, Miller WC, Wolfe DL, Townson AF, Hsieh JTC, Connolly SJ, Noonan VK, Loh E, McIntyre A, editors.The Spinal IST -C12ord neuroprosthesis,Injury Rehabilitation Evidence. a second Version 6.0: generation, p 1-121. myoelectrically controlled www.scireproject.comimplantable device appears to have a positive effect on pinch and grasp functions which result in increased independence with activities of daily living.

Table of Contents

Abbreviations ...... i 1.0 Introduction ...... 1 2.0 Acute Phase of Rehabilitation ...... 4 2.1 Exercise and Strengthening ...... 6 3.0 Augmented Feedback on Motor Functions ...... 12 4.0 Pharmacological Interventions ...... 16 5.0 Restorative Strategies ...... 17 5.1 Plasticity of Motor Systems ...... 19 5.2 Complementary Alternative Therapies ...... 29 5.3 Splinting ...... 32 6.0 Subacute Phase of Rehabilitation ...... 35 6.1 Shoulder Injuries ...... 40 6.2 Elbow, Wrist and Hand Injuries ...... 44 7.0 Reconstructive Surgery and Tendon Transfer ...... 46 7.1 Hand ...... 46 7.1.1 Pinch ...... 48 7.1.2 Pinch and Grasp (Key-Pinch and Hook Grip) ...... 51 7.2 Elbow Extension ...... 56 7.2.1 Posterior Deltoid to Triceps ...... 56 7.2.2 Biceps to Triceps...... 59 7.3 Multiple Reconstructions ...... 61 8.0 Nerve Transfers ...... 69 Advantages over Tendon Transfers ...... 69 Potential Drawbacks of Nerve Transfers ...... 70 Assessment and Surgical Timing ...... 70 9.0 Neuroprostheses ...... 74 Reported Benefits of Neuroprosthesis Use ...... 75 Clinical Results of Neuroprosthesis Use...... 75 Challenges in Neuroprosthesis Use and Reasons for Not Using Neuroprosthesis ...... 76 9.1 Surface or Percutaneous Neuroprosthesis Systems ...... 80 9.1.1 Freehand System...... 80 9.1.2 NESS H200 (formerly HandMaster-NMS-1) ...... 88 9.1.3 Bionic Glove ...... 89 9.1.4 ETHZ-ParaCare System ...... 91 9.1.5 Stimulus Router System ...... 92 9.1.6 Exo-Glove ...... 92 9.1.7 NEC-FES System ...... 94 9.1.8 Rebersek and Vodovik (1973) Neuroprosthesis ...... 94 This review has been prepared based on the scientific and professional information available in 2013. The SCIRE information (print, CD or web site www.scireproject.com) is provided for informational and educational purposes only. If you have or suspect you have a health problem, you should consult your health care provider. The SCIRE editors, contributors and supporting partners shall not be liable for any damages, claims, liabilities, costs or obligations arising from the use or misuse of this material.

Rice D, Faltynek P, McIntyre A, Mehta, S, Foulon BL, Teasell RW. (2016). Upper Limb Rehabilitation Following Spinal Cord Injury. In Eng JJ, Teasell RW, Miller WC, Wolfe DL, Townson AF, Hsieh JTC, Connolly SJ, Noonan VK, Loh E, McIntyre A, editors. Spinal Cord Injury Rehabilitation Evidence. Version 6.0: p 1-121. www.scireproject.com

9.1.9 Belgrade Grasping-Reaching System ...... 95 9.3 Myoelectrically Controlled Neuroprostheses ...... 95 10.0 Brain Interface Neuroprostheses ...... 97 11.0 Virtual Reality ...... 98 12.0 Summary...... 99 References ...... 105

This review has been prepared based on the scientific and professional information available in 2013. The SCIRE information (print, CD or web site www.scireproject.com) is provided for informational and educational purposes only. If you have or suspect you have a health problem, you should consult your health care provider. The SCIRE editors, contributors and supporting partners shall not be liable for any damages, claims, liabilities, costs or obligations arising from the use or misuse of this material.

Abbreviations

AbINT Activity based Intervention ADL Activities of Daily Living AIS ASIA Impairment Scale AP Action Potential APB Abductor Pollicis Brevis BGS Belgrade Grasping-Reaching System BR Brachioradialis CAM Complementary Alternative Therapies CHART Craig Handicapped Assessment and Reporting Tools CNS Central Nervous System COPM Canadian Occupational Performance Measure CPG Central Pattern Generators CSF Cerebrospinal Fluid Cu- Cutaneous CWRU Case Western Reserve University ECRB Extensor Capri Radialis Brevis ECRL Extensor Capri Radialis Longus EDM Extensor Digiti Minimi EMG Electromyography FCR Flexor Carpi Radialis FDP Flexor Digitorum Profundus FES Functional Electrical Stimulation FEV-1 Forced Expiratory Flow FIM Functional Independence Measure fMRI Functional Magnetic Resonance Imaging FNS Functional Neurostimulation FPL Flexor Pollicis Longus FVC Forced Vital Capacity GRT Grasp and Release Test HHD Handheld Dynamometry IST-12 Implanted Stimulator-Telemeter MeCFES Myoelectrically Controlled Functional Electrical Stimulation MP Massed Practice MRCS Medical Research Council Scale MRI Magnetic Resonance Imaging NMS Neuromuscular Stimulation NP Neuroprothesis NRS Numeric Rating Scale O- Ocular OT Occupational Therapy PC Performance Corrected PD Posterior third of the deltoid PET Positron Emission Topography PO Power Output PT Physiotherapy PT Pronator Teres PVA Paralyzed Veterans of America QIF Quadriplegic Index Function REL Rehabilitation Engineering Laboratory Hand Function Test

ROM Range of Motion rTMS Repetitive Transcranial Magnetic Stimulation SCI Spinal Cord Injury SCIM Spinal Cord Independence Measure SEM Standard Error of Mean SRS Stimulator Router System SS Somatosensory Peripheral Nerve Stimulation VRS Verbal Rating Scale WUSPI Wheelchair Users Shoulder Pain Index

Upper Limb Rehabilitation Following Spinal Cord Injury

1.0 Introduction Raineteau and Schwab (2001) defined a spinal cord injury (SCI) as a lesion within the spinal cord that results in the disruption of nerve fibre bundles that convey ascending sensory and descending motor information. A SCI at the cervical level results in tetraplegia, the loss of hand and upper limb function with impairment or loss of motor and/or sensory function. In incomplete spinal cord injuries, some neural transmission can still pass through the spinal cord, but it is often fragmentary or distorted which leads to additional neurological complications such as chronic pain or spasticity. Tetraplegia results in impairment of function in the arms, as well as in the trunk, legs, and pelvic organs. It is estimated that cervical SCI accounts for approximately 50% of all people living with SCI (Steeves et al., 2007). The loss of upper limb function, especially the use of the hands is one of the most significant and devastating losses an individual can experience. The use of the upper extremities is critical in completing basic activities of daily living (ADL) such as self-feeding, dressing, bathing, and toileting. Mobility needs such as transfers from surface to surface, transitional movements such as rolling, bridging and sit to lying down, crutch walking and wheeled mobility are also completed using one’s arms (Snoek et al. 2004). The level at which the injury or lesion occurs and the completeness of the lesion (incomplete or complete) indicate the level of independence of the person (Ditunno 1999).

The Paralyzed Veterans of America (PVA) have published a clinical practice guideline, “Outcomes Following Traumatic Spinal Cord Injury: Clinical Practice Guidelines for Health Care Professionals,” that outlines the expected skills and outcomes that a person is expected to acquire and achieve at each significant level of injury (Consortium for Spinal Cord Medicine 1999). As medical care of the spinal cord injured person has improved, life expectancy now approaches the rest of the population. Secondary complications from SCI and aging are ongoing challenges and include pain, contractures and upper limb musculoskeletal injuries (Sipski & Richards 2006). Elderly patients with SCI also have greater activity-related deficits than younger patients with SCI (Wirz et al., 2015).

Hanson and Franklin (1976) compared sexual function to three other impairments in patients with SCI; approximately 76% of the subjects gave the highest priority to upper extremity function. Snoek et al. (2004) surveyed the needs of patients with SCI and found a high impact and high priority for improvement in hand function in those with tetraplegia comparable to that for bladder and bowel dysfunction. A study by Anderson (2004) found similar results in which 48.7% of persons with tetraplegia (3.3% of persons with paraplegia) reported that regaining arm and hand function would most improve their quality of life. These findings did not differ by gender or number of years post SCI which suggests that recovering even partial arm and hand function may have a significant impact on the independence of many spinal cord individuals (Anderson et al., 2004).

Given the above, the initial care, management, rehabilitation, and prevention of injuries in the upper limb of those with tetraplegia are of great importance in maximizing and maintaining independence. Management of the tetraplegic upper limb tends to be eclectic involving traditional rehabilitation interventions of task directed training in which clients perform many repetitions of movements relevant to ADL, use of orthosis (splints and adaptive devices), and upper extremity surgery. Bryden et al. (2005) proposed a similar hierarchy of upper extremity functional restoration for individuals with tetraplegia including the provision of conservative treatment methods followed by surgical restoration using residual motor functions and increasing or augmenting voluntary functions with functional electrical stimulation (FES) for maximal upper limb function. The management and care of the upper limb can relate to the phase of upper limb rehabilitation, which has been divided into three phases, including the: acute, subacute, and reconstructive phase (Murphy and Chuinard 1998). The aims of the first two phases of rehabilitation are to prevent complications, to achieve optimal functioning within the limits of the neurological deficit, and to create optimal conditions for the reconstructive phase (Bedbrook 1981; Curtin 1994; Harvey 1996; Keith & Lacey 1991). In the latter phase, various surgical options and FES are available to improve positioning and stabilization of the arm as well as key and palmar grasp function (Johnstone et al., 1988; Peckham et al., 2001; Snoek et al., 2000; Triolo et al., 1996; Waters et al., 1996). The clinical practice guidelines by the Consortium for Spinal Cord Medicine (2005) emphasize the prevention of upper limb injuries among individuals with tetraplegia to maintain independence.

There is no consensus regarding the management of the tetraplegic upper limb, this may be due to the variations in muscle function after a SCI (Thomas et al., 2014). Understanding the diversity of a SCI is important in ensuring that therapy is tailored to each individual and that feedback is elicited from patient’s regarding their perceptions of the usefulness of specific interventions (Thomas et al., 2014). Hummel et al. (2005), Snoek et al. (2005) and the Consortium for Spinal Cord Medicine (2005) provide excellent recommendations as a starting point for the management of the tetraplegic upper limb.

There is agreement that restoration of hand function is an important goal in rehabilitation. It is also worth noting that there are few upper extremity tests that accurately evaluate upper limb function in this population (van Tuijl et al., 2002). Curtin (1994) and Krajnik and Bridle (1992) noted a great inconsistency in evaluation and documentation of the tetraplegic upper limb between therapists. The initial upper- extremity motor score (UEMS) in combination with ulnar compound motor action potentials (CMAP) is one set of measures that can serve as early predictors of ADL outcomes and sensorimotor deficit after injury (Wirz et al., 2015).

Several studies have explored increased hand function as a result of reconstructive surgery and/or neuroprosthesis. Although these, and many other treatment options exist, and can improve the overall functioning and functional independence of the person with tetraplegia, suitable candidates for reconstructive surgery or FES

interventions often do not accept the treatment that is offered (Snoek et al., 2004). According to Moberg (1975), over 60% of the persons with tetraplegia could benefit from reconstructive surgery and it continues to be widely advocated (Snoek et al., 2004). Curtin et al. (2005) reported in their study that reconstructive surgery is underutilized in this population reporting that fewer than 10% of persons with tetraplegia undergo surgical reconstruction. Reconstructive surgeries such as muscle/tendon transpositions of the intact arm or hand muscles are designed to substitute for lost motor function (van Tuijl et al., 2002). Despite this, controversy still exists among clinicians as to whether to perform reconstructive surgeries.

The main focus in rehabilitation of the spinal cord injured person is compensation of functional loss and using those parts of the sensorimotor system, which are still intact (van Tuijl et al., 2002). Research findings regarding neuroplasticity and neurological recovery of the spinal cord also include current rehabilitation practices that focus on strategies to restore function lost after SCI as significant recovery of function is observed after incomplete and even complete SCI (Beekhuizen 2005; Bradbury et al., 2002; Buchuli & Schwab 2005; Curt et al., 2008; Kirshblum et al., 2004; Marino et al., 1999; Waters et al., 1994). There is emerging evidence demonstrating and highlighting the importance of understanding the motor control strategies that the central nervous system (CNS) uses to govern hand movements in abled individuals. This information may be useful in guiding the rehabilitation process after cervical SCI and ensuring that the exercises performed for the hand and upper limb are effective for restoring functional ability (Backus 2010). The literature reporting on the presence of muscle synergies that involve a motor control paradigm is being actively investigated (Bizzi et al., 2008; Cheung et al., 2005; d’Avella et al., 2003; Overduin et al., 2008).

This body of research puts forth the theory that there is a modular approach to motor control, where the CNS activates predefined combinations of muscles, rather than explicitly controlling individual muscles (Zariffa et al., 2012a). This could have implications in neurorehabilitation treatment implementation where there is explicit retraining of muscle synergies that are known to be useful in the able-bodied population. It is that functional performance might be improved across a broad range of tasks (Zariffa et al., 2012a). To date most of the muscle synergy studies have explored the arm with a limited number of studied investigating the existence of muscle synergies in the hand (Zariffa et al., 2012a). Zarriffa et al. (2012a) investigated if there are any synergies present in able-bodied individuals while using different types of hand grips relevant to ADLs such as pulp to pulp pinch, cylindrical grasp and lateral key pinch and attempted to determine whether the presence or absence of these synergies after SCI is correlated with functional abilities. There were several time-invariant synergies that occur consistently in a substantial proportion of able-bodied subjects, and in the SCI population there was evidence that similar synergies existed but in different proportions. No clear relationship was found between the functional abilities of subjects with SCI and those subject deviations from able-bodied synergy patterns. Further, Zariffa et al. (2012a) found that the most common synergy in the able-bodied population was EDC and EIP for finger extension and FDS and FCU for wrist flexion used to position the hand during grasping activities. In SCI, the most common synergy was FCR and ECR

for stabilizing the wrist and DII and TEMG for independent thumb movement (Latash et al., 2010; Santello et al., 1998; Weiss et al., 2004). Further research and investigation is required to determine how this information can be transferred into the treatment of the hand and upper limb of the SCI injured person for improving functional task performance.

2.0 Acute Phase of Rehabilitation

Rehabilitation and management of the person with a SCI requires an interdisciplinary team approach during the acute phase of rehabilitation. The level and classification of the injury is determined and the goals of maintaining range of motion (ROM), improving strength, managing tone, spasticity, and the prevention of secondary complications to achieve the person’s maximum functional ability for independent transfers, ADL and mobility are developed (Drolet et al., 1999; Haisma et al., 2006; Sipski & Richards 2006). Clinicians must be knowledgeable about the change in physical capacity based on level of injury as a prerequisite to developing optimal rehabilitation programs and for setting realistic individual rehabilitation goals.

Table 1 Acute Phase of Rehabilitation Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Intervention Group (IG; n=12): 1. In wheel chair set-up, no significant Mean age: 33.2±14.3 yr; Gender: males=9, interaction, between-subject females=3; Level of injury: paraplegia=12, differences, or within subject tetraplegia=0; AIS level: A=6, B=1, C=3, differences were found between study D=1, Not rated=1. groups (p>0.05). Standard Care Group (SCG; n=25): Mean 2. Although differences were not age: 40.8±16.4 yr; Gender: males=19, significant, the percentage of IG females=6; Level of injury: paraplegia=22, participants within the guideline tetraplegia=3; Severity of Injury: AIS A=14, recommendation increased by 25% ASI B=3, AIS C=5, AIS D=1, N/R=2. while the percentage of SCG Intervention: All participants were participants within the guideline independent manual wheelchair (MWC) recommendation decreased by 5%. users. The intervention group was strictly 3. No significant differences were found Rice et al. 2014 educated on the Paralyzed Veterans of between groups in wheelchair selection USA America’s Clinical Practice Guidelines (p>0.05); however, 100% of the IG RCT (CPG) for Preservation of Upper Limb participants had an ultralight MWC at PEDro=8 Function by a physical therapist and an 6mon and 1 yr compared with 68.8% (6 N=93 occupational therapist in an inpatient mon) and 77.8% (1Y) of the SCG rehabilitation facility. The standard of care participants. group received standard therapy services. 4. IG propelled with a significantly lower Outcome Measures: Comparison of push frequency than the SCG on tile wheelchair setup, selection, propulsion (p<0.02) and on a ramp (p<0.03) but biomechanics, Numeric Rating Scale not carpet (p=0.10). (NRS), Wheelchair Users 5. No significant differences were found Shoulder Pain Index (WUSPI), and between NRS or WUSPI scores in the Satisfaction With Life Scale (SFWL), Craig IG and SCG (p>0.05). Handicap Assessment and Reporting 6. A simple main effect trend (p=0.07) Technique (CHART) scores. found that the IG had an increase in the CHART physical subsection scores between 6-mon and 1 yr and an increase in the occupational subsection

Author Year Country Research Design Methods Outcome Score Total Sample Size scores between 6 mon and 1 yr (p=0.07).

Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Discussion

Rice et al. (2014) tested the efficacy of providing education of the PVA Clinical Practice Guidelines for Preservation of Upper Limb Function among manual wheelchair users. This RCT compared education to standard care among individuals with new SCI and found that receiving education resulted in better wheelchair skills including improved push frequency and length.

Rice et al. (2014) recommended further research in this area to:

• Determine if differences in propulsion skills result in decreased pain and improved quality of life. • Determine if improvements are maintained over the long-term.

Conclusions

There is level 1b evidence (from one randomized controlled trial; Rice et al., 2014) that education improves wheelchair skills after 1- year post discharge.

Providing education to manual wheelchair users is effective in improving the push frequency and push length while using a wheelchair.

2.1 Exercise and Strengthening In the acute phase of rehabilitation, the person with a SCI has a reduced physical capacity because of muscle weakness, loss of autonomic control below the level of injury, reduced activity, and subsequent changes in metabolic and vascular function (Haisma et al., 2006). The inability to reach one’s maximum potential can result in an increased risk of medical and secondary complications and has been correlated to a reduced level of functioning and quality of life. One of the important goals of rehabilitation is to reverse the debilitative cycle of reduced physical capacity that leads to decreased activity and functioning (Haisma et al., 2006). With shorter length of stay in hospital, individuals with a SCI have fewer in hospital rehabilitation opportunities.

There are very few evidence-based analyses of the effectiveness of specific exercise therapies (Sipski & Richards 2006). Most research has only focused on one component of physical capacity (e.g., peak oxygen uptake [VO2 peak], or muscle strength, or respiratory function).

Many physical factors have been associated with optimal functional independence post- SCI and muscle strength is identified as an important contributor to functional independence (Drolet et al., 1999). Studies by Noreau et al. (1993), Marciello et al. (1995) and Durand et al. (1996) all noted a correlation between the level of the lesion, performance in functional abilities in relationship to peak oxygen intake, and level of muscle strength. These associations were significant in individuals with tetraplegia especially in areas of sitting balance, spasticity of the lower limb, hand-grip strength, wrist extensor strength, and global upper extremity strength. These functional areas have also been related to Functional Independence Measure (FIM) motor and self-care scores. It was also identified that upper extremity strength must be adequate to support the body weight during transfers and lower limb strength for walking. Optimal recovery of muscle strength following a SCI is an essential objective of functional rehabilitation of individuals with a SCI (Drolet et al., 1999).

Changes in motor function observed six months after an injury may be partially explained by collateral sprouting within the spinal cord (Mange et al., 1990). Changes

between two and eight months may be related to peripheral nerve sprouting and muscle fiber hypertrophy after partial denervation (Mange et al., 1990; Yang et al., 1990). Natural muscle strength recovery may occur up to two years’ post injury, with the recovery rate being more important for the first six months as measured by manual muscle testing (Ditunno et al., 1992; Mange et al., 1992; Waters et al., 1993). Muscle strength gains have been attributed to two different mechanisms in healthy subjects. In healthy subjects, short-term gains (two-four weeks) might be explained by improved capacity to recruit motor units (neural adaptation), and gains observed after four weeks have been attributed to morphological changes within the contractile tissue inducing muscle fiber hypertrophy (Sale 1988). Additional studies regarding cardiovascular and exercise interventions are discussed in the Cardiovascular chapter and Physical Activity chapter.

Table 2 Exercise and Strengthening Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 19-65 yr; Level of 1. Overall 11 in the EX group (exercise injury: C4-L1; Severity of injury: AIS A-D; adherence 82.5%) and 13 in the Time since injury: 1-24 yr. control group completed the study. Intervention: Experimental group (EX) 2. No differences were noted between participated in progressive exercise the two groups at baseline. training twice weekly for nine mo-each 3. Following training, EX group had session offered on alternative days lasing significant increases in sub maximal Hicks et al., 2003 90-120 min. arm ergometry power output (81%; Canada Outcome Measures: Perceived stress p<0.05) and significant increases in RCT scale, Muscle strength, Depression, upper body muscle strength (19- PEDro=5 Physical self-concept pain, Perceived 34%; p<0.05). NInitial=34; NFinal=11 health, Quality of Life (QoL). 4. EX group reported less pain, stress and depression after training + scored higher than CON in indices of satisfaction with physical function, level of perceived health + overall quality of life (p<0.05). Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Author Year Country Research Design Methods Outcome Score Total Sample Size

Population: Age: 18-45 yr; Gender: 1. No significant difference was found males=31, females=3; Level of injury: at the four-week evaluation between tetraplegia; Mean time since injury: 3 yr. Groups 1 and 2 (p=0.22) or between Intervention: Subjects randomly Groups 2 and 3 (p=0.07). assigned to one of three groups: Group 1 2. Subjects in Group 1 had a higher Needham-Shrophire et – received 8 wk of neuromuscular proportion of muscles improving one al., 1997 stimulation (NMS) assisted arm ergometry or more muscle grades after four USA exercise; Group 2 – received 4 wk of weeks of NMS cycling compared RCT NMS assisted exercise, then 4 wk of with Group 3 (p<0.003). PEDro=8 voluntary arm crank exercise; Group 3 3. Following the second four weeks of NInitial=43; NFinal=32 (control group) – voluntary exercise for 8 training, a significant difference was wk without the application on NMS. found between Groups 1 and 3 Outcome Measures: Manual muscle (p<0.0005) and between Groups 2 test. and 3 (p<0.03). 4. No statistical difference was found between Groups 1 and 2 (p=0.15). Population: SCI population (n=23): Mean 1. Significant effect of group (p=0.001) age: 51.9±11.8 yr; Gender: males=21, but not task (p=0.21) or interaction females=2; Level of injury: C2-C8=23; (p=0.19) on FDI mean rectified EMG Severity of Injury: AIS-A=2, AIS-B=1, AIS- activity. C-D=2. 2. EMG activity increased in SCI Age matched controls (n=20): Mean age: patients taking baclofen (SCIBac) 45±16.2 yr; Gender: males=8, (p=0.001) and patients who never Bunday et al. 2014 females=12. took baclofen (SCINo-Bac) (p=0.01) USA Intervention: Participants performed compared with controls; no Prospective Controlled tasks requiring precision grip and index significance between patient groups Trial finger abduction while noninvasive cortical (p=0.95). N=43 and cervicomedullary stimulation allowed 3. Both SCI and control groups motor evoked potentials (MEPs). The maintained similar EMG activity in activity in intracortical and subcortical the FDI muscle during precision grip pathways were examined. and index finger abduction (p=0.21). Outcome Measures: EMG activity, F- 4. During index finger abduction, wave amplitude and persistence, controls (p=0.01), SCIBac (p<0.001) Suppression of voluntary EMG by and SCINo-Bac (p=0.04) more EMG subthreshold TMS (svEMG). activity in FDI compared to APB at

Author Year Country Research Design Methods Outcome Score Total Sample Size all Transcranial magnetic stimulation (TMS) intensities. 5. Significant decrease in MEP size in controls (p<0.001) and SCIBac (p=0.001) during precision grip compared with index finger abduction. 6. At increasing stimulus intensities, MEP sizes in control subjects were significantly larger than SCINo-Bac and SCIBac (p<0.001). 7. FDI cervicomedullary MEPs decreased during precision grip compared with index finger abduction in controls (p<0.01) and SCIBac (p<0.01) but not SCINo-Bac (p=0.57). 8. No effect of task, group or their interaction on F-wave amplitude or F-wave persistence (p>0.05). 9. Significant effect of task (p<0.001), but not group (p=0.39) or their interaction (p=0.20) on svEMG. 10. Significant decrease in svEMG area during precision grip compared with index finger abduction in controls (p=0.03), SCIBac (p=0.02) and SCINo-Bac (p=0.02). Population: Mean age: 40 yr; Gender: 1. Age was related to the PO peak and males=140, females=46; Level of Injury: handheld dynamometry (HHD) paraplegia, tetraplegia; Severity of injury: score (p<0.05), the older the subject complete=125, incomplete=61; Mean time the more improvement in either of since injury: 105 d. these measures was significantly Intervention: Assessments were taken at less than it was in younger subjects. four time points: start of inpatient 2. Men had greater PO peak, VO2 peak rehabilitation; three months later; and HHD score than women did discharge and at one year after (p<0.05), thus improvement in men Haisma et al., 2006 discharge. was greater than women. Netherlands Outcome Measures: Power output (PO) 3. In tetraplegia subjects the PO peak, Prospective cohort peak, VO2 peak, strength of upper VO2 peak, muscle strength and % of NInitial=186; NFinal=42 extremity, respiratory function. forced vital capacity (FVC) was lower (p<0.05) than it was in paraplegia subjects, but tetraplegia subjects improved more in muscle strength and % of forced expiratory flow (FEV1). 4. Those with a complete lesion had greater HHD score and lower % of FVC than those with incomplete lesions (p<0.05). Population: Mean age: 29.5 yr; Gender: 1. Strength values at admittance were males=27, females=4; Level of injury: inversely repeated to strengthen Drolet et al., 1999 paraplegia=18, tetraplegia=13; Severity of changes during rehab (Pearson Canada injury: AIS A-D; Mean time since injury: 2 correlation coefficients ranging from Pre-post mo; Mean length of stay: 4.5 mo. -0.47 (p=0.001 shoulder flexors) to - NInitial=40; NFinal=31 Intervention: Rehab included 0.73 (p<0.001 shoulder adductors). physiotherapy (PT), occupational therapy

Author Year Country Research Design Methods Outcome Score Total Sample Size (OT) and physical conditioning. There 2. For those with paraplegia the range were four 1 hr sessions of each was from -0.48 (p=0.049 shoulder intervention. abductors to -0.72 (p=0.001 elbow Outcome Measures: Mean muscle flexors) compared to those with strength, Muscle strength changes. tetraplegia, the correlation coefficients ranged from -0.28 (p=0.345 elbow extensors) to -0.68 (p=0.010 shoulder adductors). 3. Patterns of change in muscle strength from admittance to the 15 mo follow up differed between the paraplegia group and the tetraplegia group. Differences in strength have been observed for: elbow flexors (p=0.001) and shoulder extensors (p=0.04). Population: Age: 18-45 yr; Gender: 1. All subjects showed improvement in males=10, females=1; Level of injury: C4- one or more of their manual muscle C7; Time since injury: >1 yr. scores with the most dramatic Intervention: Testing of hybrid device, occurring in the tricep muscle group Cameron et al., 1998 eight weeks of Neuromuscular Stimulation (average increase 1.1±0.2 for L USA (NMS) assisted exercise with training triceps, 0.7±0.1 for R). Case Series sessions three times per week. Results show NMS in combination N=11 Outcome Measures: Manual muscle with resistive exercise can be used test. safely and assists in the strengthening of voluntary contractions.

Discussion

Five of the six studies presented address the long-term change of upper limb strength after the spinal cord injured person has returned to community living. Needham- Shophire et al. (1997) and Cameron et al. (1998) found that Neuromuscular stimulation (NMS)-assisted exercise ergometry alone and in combination with exercise was effective for strengthening of the upper limb for SCI injured individuals well after injury.

Hicks et al. (2003) demonstrated all study participants had progressive increases in muscle strength in each of the muscle groups tested and that the change scores were significant from the control group except for the left anterior deltoid. Study participants self-reported decreases in stress, pain, depression, enhanced physical self-concept and overall quality of life.

Drolet et al. (1999) conducted one of the first longitudinal studies published in muscle strength changes in individuals with SCI during rehabilitation. Significant improvement of muscle strength during rehabilitation for individuals with both paraplegia and tetraplegia was noted and were maintained three-months post discharge for the tetraplegia group in the four muscle groups (elbow flexors and extensors and shoulder flexors and extensors) and then began to plateau. One year later elbow flexors showed

significant improvement in both paraplegia and tetraplegia groups and shoulder extension showed significant gains only on individuals with paraplegia. Large variability was noted indicating the recovery of strength may be influenced by a variety of individual factors such as level and severity of injury, associated health conditions, age, gender, motivation and physical condition before SCI.

Haisma et al. (2006) found positive changes in the different components of physical capacity both during and after inpatient rehabilitation. SCI subjects continued to improve highlighting the importance of regularly assessing the physical capacity of people with SCI after discharge. It is important to create conditions (education, exercise facilities) that facilitate further improvements (Haisma et al., 2006).

Bunday et al. (2014) tested the involvement of subcortical pathways while SCI subject’s completed measures of precision grip. Authors of this study concluded that precision grip involves premotoneuronal subcortical mechanisms and that the pathways that are impacted after SCI are restored by long-term use of baclofen.

Haisma et al. (2006) and Sipski and Richards (2006) recommended further research in this area: • Further research is needed to document benefits of exercise interventions post- SCI including optimal methods for strengthening muscles, merits of endurance versus strength training, ROM, gait, ADL, and transfer training. • Due to impact of body composition, age, concomitant medical problems and our limited knowledge of recovery post SCI, research needs to be performed through well-designed multicentre trials. • Longitudinal studies are needed to gain more insight into the changes that occur after inpatient rehabilitation and the factors which influence these changes. • Exercise and strengthening of the upper limb in both the acute and subacute phase of rehabilitation are important in promoting independence and prevention of injury.

Conclusions

There is level 2 evidence (from one randomized controlled trial; Hicks et al., 2003) that physical capacity continues to improve after 1- year post discharge, and is correlated to a decrease in stress, pain, and depression.

There is level 1b evidence (from one randomized controlled trial; Needham- Shrophire et al., 1997) that neuromuscular stimulation-assisted exercise improves muscle strength over conventional therapy.

There is level 4 evidence (from one case series study; Cameron et al., 1998) that neuromuscular stimulation-assisted ergometry alone and in conjunction with voluntary arm crank exercise was an effective strengthening intervention for chronically injured individuals.

There is level 4 evidence (from one pre-post study; Drolet et al., 1999) that overall muscle strength continues to improve up to 15 months’ post hospital discharge for both persons with tetraplegia and paraplegia despite large variability in patients.

There is level 5 evidence (from one observational study; Bunday et al., 2014) that the control of precision grip involves premotoneuronal subcortical mechanisms, which are lacking after SCI.

Neuromuscular stimulation-assisted exercise following a SCI is effective in improving muscle strength, preventing injury and increasing independence in all phases of rehabilitation, particularly in the first 12 months. Additionally, these positive physical outcomes are correlated to positive emotional states, such as an increase in perceived independence and a decrease in depression, anxiety, and pain.

3.0 Augmented Feedback on Motor Functions

Several studies have addressed the use of augmented feedback, such as biofeedback, with spinal cord injured populations. Van Dijik et al. (2005) conducted a systematic review of RCTs on the effect of augmented feedback on motor function of the affected upper extremity in rehabilitation patients. Much of the information about augmented feedback comes from the motor learning literature where it has been noted that feedback combined with practice is a potent variable for affecting motor skill learning (Newell 1991; Schmidt & Lee 1999). There are two types of performance-related information or feedback. The first type of feedback, task intrinsic or inherent feedback, is sensory-perceptual information and is a natural part of performing a skill. The second type of feedback is augmented feedback or information-based extrinsic or artificial feedback. Augmented feedback refers to enhancing task intrinsic feedback with an external source (Magill 2001; Schmidt & Lee 1999), such as a therapist or device (biofeedback or timer) (van Dijik et al., 2005). It has been suggested that augmented feedback may have practical implications for rehabilitation therapy since re-acquisition of motor skills is an important part of functional motor recovery (Jarus 1994; Jarus & Ratzon 2005; Kilduski & Rice 2003; Winstein 1991).

The ability to use intrinsic feedback to guide performance is impaired in patients with cognitive and perceptual deficits (Flinn & Radomski 2002). In persons who are compromised by neurological sensory impairments, augmented feedback is important (Sabari 2001).

Table 3 Augmented Feedback on Motor Functions Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 25-70 yr; Level of injury: 1. A great deal of variance between tetraplegia; Severity of injury: AIS A-D, incomplete; participants in most measures due to Time Since Injury: 15-243 day; Chronicity: low numbers of subjects, no significant Popovic et al., acute/subacute. differences was found between the 2006 Intervention: The control group received Control and Intervention groups. Canada conventional Occupational Therapy; Intervention RCT group received Functional Electrical Therapy and PEDro=6 conventional Occupational Therapy. N=21 Outcome Measures: Functional Independence Measure (FIM), Spinal Cord Independence Measure (SCIM), Rehabilitation Engineering Laboratory Hand Function Test (REL Test), Consumer Perceptions. Population: Mean age: 39 yr; Gender: males=40, 1. Comparison of Groups (Increment or females=5; Level of injury: C4-C6; Severity of injury: Decrement or No Change): no complete, incomplete. relationship between treatment group Intervention: Extremities were randomly assigned to and observed change; no treatment one of four treatment groups: 1. conventional produced a significantly higher Kohlmeyer et al., strengthening; 2. electrical stimulation; 3. proportion of individuals that improved 1996 biofeedback and electrical stimulation; 4. relative to the proportion showing no USA biofeedback. Participation ranged from five to six change or a decrement; no change RCT weeks post SCI. between treatment groups. PEDro=10 Outcome Measures: Manual muscle test, Activities 2. Influence of Initial Muscle Grade: a NInitial=60; of Daily Living (ADL) performance. correlation between the initial muscle NFinal=45 grade and increment in muscle grade was seen at the end of treatment; poorer initial muscle grades, more likely to see a larger increment in muscle grade as a result of treatment. Population: Age: 18-35 yr; Gender: males=24, 1. Scores after training indicated no females=4; Level of injury: C5-C7; Time since injury: significant differences for the muscle ≥1 yr. test score and functional activities score Intervention: Both groups received 45 min of between groups. aggressive exercise therapy three times per week for 2. Analysis of the repeated measures 12 weeks along with 30 min of neuromuscular factor showed a significant change for stimulation (NMS) to assist with upper extremity the manual muscle test and functional muscle strength. Experimental group also received activities score (p<0.05). Klose et al., 1993 12 wk of 30 min EMG biofeedback 3x/wk. USA Outcome Measures: Manual muscle test, Functional RCT activities score. PEDro=5 Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- NInitial=31; and post-intervention data. NFinal=28

Klose et al., 1990 Population: Age: 18-45 yr; Level of injury: C4-C6; 1. No statistically significant differences USA Severity of injury: incomplete; Time since injury: ≥1 were noted between the groups. RCT yr. PEDro=3

Author Year Country Research Design Methods Outcome Score Total Sample Size NInitial=43; Intervention: All received three days/wk of therapy 2. Differences were noted for the repeated NFinal=39 in two consecutive eight-week treatment blocks. measures of mobility, self-care, and the Treatment blocks were as follows; Group 1: left arm muscle test scores (p<0.05). Biofeedback followed by supervised physical therapy 3. The repeated measures factor was exercise Group 2: Biofeedback followed by statistically significant in all of the neuromuscular stimulation (NMS); Group 3: NMS analyses looking at measures of followed by physical therapy exercise; Group 4: 16 physical function (p<0.01) but not in wks physical therapy exercise. those that compared EMG values. Outcome Measures: Manual muscle test (biceps, triceps, wrist flexors, wrist extensors), Self-care measures looking at feeding, hygiene and dressing, Mobility measure and a muscle electrical activity were also measured. Population: Mean Age: 28 yr; Gender: males=3, 1. Overall grasp success rates varied females=0; Level of Injury: C2=1, C5=2; Severity of between 62 and 64% with success rate Injury: AIS A=2, AIS B=1, Unspecified=2. significantly better than chance for each Intervention: Patients with complete hand paralysis patient (p<0.001). participated in a virtual hand grasping task. The 2. Although grasp success rates improved virtual stop-motion hand was projected onto a screen after breaks between trials, the success and was controlled by the patient’s sensorimotor rate was not significantly different when rhythms (SMRs). The SMRs were utilised via compared to trials before breaks magnetoencephalography. Patients were asked to (p=0.22). grasp or rest the virtual hand and were required to 3. Success rates were also significantly hold the position for a set time depending on difficulty greater than chance during grasp-only level of the trial. Patients were also asked to attempt and rest-only trials (both p<0.001). Foldes et al. 2015 grasping and resting their own paralysed hand during 4. Two patients demonstrated a significant USA each virtual hand trial. The intervention consisted of increase in their ability to modulate their Post Test 200 trials (75% grasp, 25% rest) in a pseudorandom SMRs by 14.9pp and 15.0pp (both N=3 order with a 1min break after every 20 trials. Trials p<0.05) from baseline to post-treatment. were also broken down into segments of 50 trials for The remaining patient did not exhibit any analysis purposes. Assessments were performed at significant improvement in modulating baseline and during each trial through to post- SMRs. treatment. 5. ANOVA analyses revealed a significant Outcome Measures: Grasp success rate, SMR interaction between patient and session- modulation, time to successful grasp. segment (p<0.001) and a significant main effect of session-segment (p<0.001). 6. Patients took an average of 1.96sec to complete a successful grasp, indicating that grasping using SMRs had been learnt quickly. Population: Age: 17-63 yr; Gender: males=81, 1. T-test analysis of the differences before females=19; Level of injury: C2-C6; Time since and after initial biofeedback treatment injury: 1-29.7 yr. was done. An increase of 19.21% of Intervention: Electromyography (EMG) biofeedback normal EMG scores for right triceps and treatment sessions. increase of 19.59% of normal EMG Outcome Measures: EMG scores. scores from the left triceps from one Brucker & biofeedback treatment session were Bulaeva 1996 found, significant (p<0.001). USA 2. T-test analysis of the difference from Pre-post before initial biofeedback treatments to N=100 after additional treatments, increase in percentage of normal EMG scores of 41.55% right triceps and 38.31% left triceps, significant (p<0.001). Increases in percentage of normal EMG scores after initial biofeedback treatment to

Author Year Country Research Design Methods Outcome Score Total Sample Size after additional biofeedback treatment 22.3% right triceps and 18.72% for left triceps, significant (p<0.001). 3. Correlation coefficient for manual muscle test score and EMG pretest before initial treatment was r=0.569 for right triceps and r=0.437 for left triceps, significant (p<0.001). 4. Increases in percentage of normal EMG before, after, and after additional treatments was significant in right and left triceps regardless of initial manual muscle test.

Discussion

Four of the six included studies concluded that there was no evidence for the effectiveness of augmented feedback to improve arm function in rehabilitation. These four studies are the only RCTs to date that have test augmented feedback for arm rehabilitation post SCI.

One study by Brucker et al. (1996) tested biofeedback treatment among 100 participants and found an increase in normal EMG scores in the right and left triceps, however, this sample did not include a control group. A more recent study with just three participants applied magnetoencephalography based neurofeedback and authors concluded that neurofeedback training may have the potential to be used for motor rehabilitation (Foldes et al., 2015). Given the small sample sizes within each of the six included studies, conducting additional RCTs with larger samples is necessary to gain a more conclusive understanding of the impact of augmented feedback in upper limb rehabilitation.

In a systematic review, van Dijik et al. (2005) recommended the following be considered in future research in this area: • future studies should focus on content, form, and timing of the augmented feedback to clarify its importance in rehabilitation. • studies should recognize the difference between performance and learning effects concerning reacquisition of motor skills by re-examining the study population after a follow up period.

Conclusion

There is level 1a evidence (from two randomized controlled trials; Kohlmeyer et al., 1996; Popovic et al., 2006) that augmented feedback is not effective in improving upper limb function in tetraplegia.

There is level 2 evidence (from two randomized control trials; Klose et al., 1990; Klose et al., 1993) that the addition of biofeedback does not improve patient scores in rehabilitation more than physical exercise alone.

There is level 4 evidence (from one pre-post test; Bruker and Bulaeva, 1996) that EMG biofeedback sessions can significantly improve normal EMG muscle test scores of both triceps.

There is level 4 evidence (from one post-test; Foldes et al., 2015) that patients with complete hand paralysis can learn to significantly modulate their sensory motor rythyms using a virtual hand task over time.

Augmented feedback does not improve motor function of the upper extremity in SCI rehabilitation patients. However, biofeedback has been shown to positively effect normal EMG muscle scores in both triceps. Patients may be ale to learn to regulate their sensory motor rhythms in their upper extremities using virtual tasks like hand-grasping.

4.0 Pharmacological Interventions

Cervical injuries of the spinal cord frequently lead to hypertonia characterized by disabling spasticity and dystonia involving the upper and lower limb. Spasticity has been defined by Lance (1980) as “a velocity exaggerated increase in the tonic stretch reflexes (muscle tone) resulting from hyperactivity of the stretch reflex.” The EU-SPASM Thematic Network or Consortium (Support Network for the Assembly of Database for Spasticity Measurement) has presented an updated definition of spasticity that reflects recent research findings and current clinical interpretations. Spasticity has been re- defined as “disordered sensori-motor control, resulting from an upper motor neurone lesion, presenting as intermittent or sustained involuntary activation of muscles” (Pandyan et al., 2005).

The management of severe cases of hypertonia can be challenging as it can be refractory to oral medications. Many studies have shown that intrathecal delivery of baclofen has been effective for refractory hypertonia in the lower extremity. Baclofen, 4- amino-3 (p-chlorophenyl) butyric acid works by binding to the inhibitory presynaptic GABA-B receptors in the spinal cord (Meythaler et al., 1999). Intrathecal delivery of the drug facilitates achievement of therapeutic levels in the cerebral spinal fluid (CSF) while minimizing systemic side effects (drowsiness, confusion). Burns and Meythaler (2001) is the only study published which deals with hypertonia involving the upper extremity post- SCI. Further discussion regarding the management of hypertonia can be found in the spasticity chapter.

Table 4 Pharmacological Interventions Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 25-64 yr; Level of 1. Significant decline in UE hypertonia injury: C4-C7; Severity of injury: AIS A-D; during 12 mo follow up period. Time since injury: 1.2-24 yr. 2. Average baseline Ashworth score Intervention: Intrathecal baclofen. was 2.4±1.1 compared to 1.8±1.0 at Outcome Measures: Ashworth Scale, 12 mo (p<0.0001). Spasm Frequency Scale, Reflex Scale. 3. The average spasm score decreased from 2.3±1.6 to 0.5±0.9, not significant at p=0.2503 (Friedman test). 4. The difference was significant (p=0.0012 Wilcoxon signed rank Burns & Meythaler 2001 test). UE reflexes, average baseline USA reflex score was 2.3±0.2 compared Case Series to 0.9±0.2 at 12 mo (p<0.0001 N=14 Friedman). 5. Dosage requirements increased during the 12-mo follow-up period, statistically significant (p<0.0001, Friedman). 6. Statistically significant declines in upper extremity spasm scores (1.8 points, p=0.012), reflex scores (1.4 points, p<0.0001) and Ashworth scores (0.6 points, p<0.0001) for the 1-yr follow-up period.

Discussion

Burns and Meythaler (2001) showed a statistically significant decrease in Ashworth (tone) and reflex scores in upper extremity hypertonia due to pathology at the level of the spinal cord.

Conclusion

There is level 4 evidence (from one case series study; Burns & Meythaler 2001) that intrathecal baclofen may be an effective treatment for upper extremity hypertonia of spinal cord origin.

Intrathecal baclofen may be an effective intervention for upper extremity hypertonia of spinal cord origin.

5.0 Restorative Strategies Neuroplasticity at the site of injury post SCI can mediate functional recovery (Kakulas 2004). Motor imagery (MI) can stimulate activity-dependent neuroplasticity (Grangeon et al., 2012). Specifically, MI has been shown to stimulate cerebral reorganization and

improve motor functioning in patients with stroke and Parkinson’s disease (Page et al., 2009; Sun et al., 2013). Two studies authored by one group of researchers tested the use of MI in improving motor learning post SCI.

Table 5 Restorative Strategies Author Year Country Research Design Methods Outcome Score Total Sample Size Population: SCI participants (n=6); Age: 1. Mean KVIQ visual and kinesthetic 18-55 yr; Level of injury: C6/C7=6. subscores, as well as KVIQ total Intervention: SCI participants received scores were comparable in both motor imagery (MI) training imbedded groups (p=0.52). within traditional physiotherapy for 5 wk 2. Data from the mental chronometry (3x/wk) to investigate effect of MI training task showed significant correlation on Tenodesis prehension (TP). This was between MI and PP durations at the compared to a healthy control group (HP) whole-group level (p<0.001). performing physical practice (PP)-based 3. No significant difference between MI Di Rienzo et al. 2014b training. and PP durations (p=0.66). France Outcome Measures: 4. A higher MV during the pre-test 3 as Pre-Post Magnetoencephalography (MEG) compared to the pre-test 2 in HP N=12 measurements, Kinesthetic and Visual (p<0.05); in the SCI group, MV during Imagery Questionnaire (KVIQ), Movement the post-test 1 was significantly lower Time (MT), Movement Variability (MV). than during each of the pre-tests (all p<0.01). 5. Lower MT and MV in HP compared to SCI subjects, for each experimental session (all p<0.01). 6. There was no MV difference between post-test 1 and 2 in SCI participants (p>0.05). Population: SCI participants (n=4): Mean 1. No statistically significant differences age: 27.5 yr; Gender: males=2, females=2; between groups on KVIQ scores or Severity of Injury: AIS C6=4; Mean time sub-scores (all p>0.05). since injury: 14.5 mo. 2. MT were greater in SCI participants Intervention: SCI participants had motor during the first pretest compared to the imagery (MI) training imbedded within third pretests of the design (p<0.01) but traditional physiotherapy for 5 additional wk not in HC (p>0.05). (3x/wk) to investigate effect of MI training 3. In SCI participants, post-test MV was on Tenodesis prehension (TP), compared superior to the median pretest value to healthy control group (HC) performing (p<0.05), but not in HC (p>0.05). Di Rienzo et al. 2015 physical practice (PP)-based training. 4. The total number of SAM sources France Outcome Measures: elicited during MI was similar in HC and Pre-Post Magnetoencephalography (MEG) SCI groups across experimental N=8 measurements, Motor performance data, sessions (p=0.89). Kinesthetic and Visual Imagery 5. Post-test values showing cortical Questionnaire (KVIQ), Movement Time recruitment (SAM sources) were (MT), Movement Variability (MV), Synthetic significantly higher than those recorded aperture magnetometry (SAM). during the pretests in the SCI group (p<0.01) but not in HC (p>0.05). 6. MV was statistically predicted by the number of SAM rouces activated during MI in the SCI group (p<0.001) but not in HC (p=0.32).

Discussion

Di Rienzo et al. (2014b, 2015) conducted two small studies and applied the same methodology involving SCI participants receiving MI and traditional physiotherapy compared to healthy controls performing physical practice. These studies resulted in mixed findings, however, SCI participants’ movement time and variability generally improved after MI.

Conclusion

There is level 4 evidence (from two pre-post studies; Di Rienzo et al., 2014b, 2015) that MI treatment incorporated into physiotherapy for individuals with SCI may help to improve prehensile tenodesis performance.

Motor imagery may be an effective intervention for improving prehensile tenodesis performance in persons with SCI.

5.1 Plasticity of Motor Systems It has been reported that 55% of all spinal cord injured persons are classified as having complete injuries. Magnetic resonance imaging (MRI) and histopathology indicates that approximately 65% of the traumatic injuries initially classified as ‘neurologically complete’ (absence of sensory and motor function in lowest sacral segment) show some tissue and axonal sparing across the lesion (Bunge et al., 1997). It is now accepted that the CNS is capable of substantial reorganization, especially in incomplete SCI because cortical, subcortical and much of the local spinal cord circuitry remains largely intact and still partially interconnected by unlesioned fibres (Raineteau & Schwab 2001). Information may still pass through the level of the lesion on spared fiber tracts, but the information may be fragmented or distorted (Beekhuizen & Field-Fote 2005). Functional recovery can occur for several years after injury in incomplete SCI, with the degree of recovery dependent upon the reorganization of circuits that have been spared by the lesion (Green et al., 1999). Cortical reorganization occurs after SCI with evidence that the sensorimotor cortex may play a role in the recovery of function in individuals with SCI (Green et al., 1999). Results of neuroimaging and neurophysiological techniques (functional magnetic resonance imaging (fMRI), transcranial magnetic stimulation (TMS) and positron emission tomography (PET) demonstrate that changes occur in the cortex following damage to the spinal cord with expansion of cortical areas corresponding to muscles spared after SCI into the cortical areas previously associated with control of muscle reinnervated at spinal cord levels below the level of the lesion (Bruehlmeier et al., 1998; Cohen et al., 1991; Levy et al., 1990; Raineteau & Schwab 2001).

In SCI, reorganization might occur at two levels; in pre-existing circuits by modifications of synaptic strength (synaptic plasticity) or by new circuits through sprouting or anatomical reorganization, including growth of axonal branches and dendrites (anatomical plasticity) (Raineteau & Schwab 2001). Laboratory work is currently explaining and researching cortical reorganization, cortical plasticity, sub-cortical plasticity, plasticity at the red nucleus, plasticity and spontaneous adaptation of the central pattern generators and plasticity of unlesioned descending pathways. The strengthening and weakening of synapses, axonal and dendritic sprouting can occur at different levels of motor system in response to spinal cord lesions, in the cortex, the brainstem, and the spinal descending pathways and in the intraspinal circuits. All interact with each other; therefore, it is difficult to interpret functional recovery processes. A SCI interrupts distinct descending fibre populations; the overall complexity of an incomplete SCI resides first in the organization of descending spinal tracts. Most of the descending systems terminate on spinal interneurons, but some direct excitatory or inhibitory connections to motor neurons also exist. Different tracts are involved in specific functions. For example, lesions of the cortical and rubrospinal systems lead to more severe and longer lasting deficits for movement of the distal extremities and lesions of the reticulo and vestibulospinal systems affect movements of proximal and axial muscles. Functional outcomes of given spinal cord lesions therefore depend on the type of fibres that are interrupted (Raineteau & Schwab 2001).

Functional reorganization is based on two mechanisms; synaptic plasticity in pre- existing circuits and sprouting and anatomical reorganization that leads to the formation of new circuits. The study of animal models provides further understanding of rehabilitation treatments and development of new therapeutic approaches for people with SCI (Raineteau & Schwab 2001).

Traditional approaches to improving arm and hand function in persons with tetraplegia generally use compensatory strategies to have the muscles that are intact substitute for the lost function of the weakened or paralyzed muscles and management of musculoskeletal complications as described in the Guidelines for Clinical Practice for the Consortium for Spinal Cord Medicine Clinical Practice Guidelines supported by the PVA 2005 (Backus 2010).

Based on the neuroplasticity research, there is a belief that there are similarities between incomplete tetraplegia after SCI and hemiplegia after stroke as incomplete tetraplegia often have altered and inappropriate sensory input and motor output and not simply the loss of sensory or motor function (Backus 2010). Persons with hemiplegia who have altered (but not absent) sensory perception and paresis (but not complete paralysis) demonstrate disordered motor control in the ULs which include the ability to balance agonist and antagonist muscles (Chae et al., 2002; Levin et al., 2000), strength imbalances (Lum et al., 2002), disruptions in initiation and cessation of movement (Chae et al., 2002) and inappropriate muscle activation (Kamper et al., 2001). Persons with tetraplegia, much like hemiplegia experience the inability to effectively activate and deactivate (relax) muscles at appropriate time and extent. The difficulty is seen in being able to control the strength or force output during movement and the altered timing and

control of movement at a joint or across multiple joints. Based on this, it is thought that ISCI closely resembles hemiplegia (Backus 2010).

There are several principles underlying the facilitation of neural plasticity and functional recovery such as intense activity, repeated practice, attention and somatosensory augmentation concurrent with movement practice. The interventions usually combine intense, repetitive and often rhythmical input to CNS below the level of injury. These principles are the basis for constraint induced movement therapy approach and activity based intervention (ABint) (i.e., treadmill training, FES approach, constraint-induced therapy). The goal of ABint is to facilitate long term changes in spinal and cortical circuits and improve overall function after neural injury or disease. Until the past decade, studies researching the use and effectiveness of ABint for improving function and potentially neural activity in arm and hand in persons with tetraplegia have been scarce in the upper limb literature (Backus 2010). The research studying the use of massed practice (MP) and/or somatosensory peripheral nerve stimulation (SS) have demonstrated potential for both neural and functional improvements in persons with tetraplegia (Beekhuizen & Field-Fote 2005; Beekhuizen & Field-Fote 2008; Hoffman & Field-Fote 2007).

Seven studies were found that tested the use of MP, SS, transcranial direct current stimulation (tDCS), transcutaneous electrical nerve stimulation (TENS), vibration therapy, and repetitive transcranial magnetic stimulation (rTMS) in changing the cortex.

Table 6 Plasticity of Motor Systems Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Mean age: 38 yr; Gender: 1. Intervention groups differed significantly in hand males=22, females=2; Level of injury: function (p<0.001). All intervention groups had a tetraplegia; Severity of injury: AIS C=11, significant improvement in their hand function D=13; Mean time since injury: 67 mo; (MP, p<0.01; SS, p<0.05; MP+SS, p<0.001), as Chronicity=chronic. compared to the control group. The MP+SS Beekhuizen & Intervention: One of four conditions two hr group improved more than the MP and SS group Field-Fote 2008 per day, 5 days/wk: 1) Massed practice alone (p<0.01). USA training (MP); 2) Somatosensory peripheral 2. MP+SS and SS groups significantly improved RCT nerve stimulation (SS); 3) MP +SS combined; motor function scores when compared to the PEDro=5 4) No intervention (control). control group (p<0.001, p<0.05, respectively). NInitial=24; NFinal=18 Outcome Measures: Jebson-Taylor Hand MP+SS improved more than MP and SS alone Function Test, Wolf Motor Function Test, Key (p<0.01). pinch force, Monofilament testing, Motor 3. MP+SS and SS groups also significantly evoked potential thresholds. improved pinch grip forces (p<0.01). MP+SS was the only group to have a significant sensory function improvement (p=0.01). Population: Age: 22-63 yr; Gender: 1. Pinch grip scores: differences were noted in the males=9, females=1; Level of injury: C5-C7; MP+SS group (Z=-2.023, p<0.05) only. Beekhuizen & Severity of injury: AIS C=4, D=6; Time since 2. The MP+SS group also showed greater increase Field-Fote 2005 injury: 12-154 mo. in pinch grip strength than the MP group (U=2.0, USA Intervention: Subjects participated in two p<0.05). RCT hours of massed practice (MP) therapy five 3. Upper extremity Functional tests: the Pre/post PEDro=8 times per week for three weeks or Wolf Motor Function Test timed scores in the N=10 MP+median nerve somatosensory MP+SS group showed a difference (Z=-2.023, stimulation (SS). Massed practice (MP)

Author Year Country Research Design Methods Outcome Score Total Sample Size training focused on continuous repetitions of p<0.05). No statistical differences were noted for the following: gross upper extremity the MP group. movement, grip, and grip with rotation, pinch 4. Timed test scores between the two groups were and pinch with rotation. Tasks in each block also found to be statistically different (U=1.0, were performed for 25 min before moving to p<0.05). the next category. 5. Jebsen test scores: pre-and post-test scores Outcome Measures: Maximal pinch grip were different for the MP+SS group (Z=-2.023, force, Wolf motor function test timed task p<0.05). The MP+SS group showed greater scores, Jebson hand function test scores, improvement than the MP group (U=3.0, Stimulus intensity required to elicit motor p<0.05). threshold response in muscles, Motor evoked Cortical Excitability: No significant differences potentials amplitude. were noted between the two groups. Population: Mean Age: 43.7 yr; Gender: 1. Results on the 9HPT improved significantly from males=21, females=3; Injury etiology: Motor baseline to post treatment after patients received Vehicle Accident=17, Diving=2, Non- TENS (p=0.003) and tDCS (p=0.05) with traumatic=1, Unspecified=4; Severity of improvements maintained from baseline to 30 Injury: AIS C=9, AIS D=11, Unspecified=4; min post treatment (p<0.001 and p=0.003 Level of Injury: C4=1, C5=4, C6=10, C7=5. respectively). Intervention: Patients received three types 2. Vibration therapy did not significantly change of stimulation in a randomized order; from baseline to post treatment or 30 min post transcranial direct current stimulation (tDCS), treatment. transcutaneous electrical nerve stimulation 3. Pinch strength significantly improved from (TENS), and vibration therapy. Both TNS and baseline to post treatment after vibration therapy vibration therapy was performed on the volar only (p=0.03). At 30 min post treatment, patients aspect of the wrist. tDCS was performed on demonstrated improved pinch strength after both the primary left/right motor area and on the vibration therapy (p=0.03) and tDCS (p=0.005) contralateral supraorbital area. During each compared to baseline. condition, the patients engaged in functional 4. Visuomotor tracking did not improve from task practice. The intervention was provided baseline to post treatment for any of the once for each condition with a 1 wk break conditions. Only tDCS improved from baseline to Gomes-Osman & between each. Assessments were conducted 30 min post treatment (p=0.05). Field-Fote 2015 at baseline, post-treatment and at 30 min 5. Corticomotor excitability improved significantly USA post treatment. from baseline to post treatment after TENS Crossover RCT Outcome Measures: Nine-hole Peg Test (p=0.003) only but at 30 min post treatment, only N=24 (9HPT), pinch strength, Corticomotor vibration therapy demonstrated a significant excitability/motor-evoked potentials, improvement compared to baseline (p=0.006). Visuomotor tracking task. Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Author Year Country Research Design Methods Outcome Score Total Sample Size

Population: SCI Group (n=11): Mean Age: 1. Improvements in JTT scores revealed large effect 46.7 yr; Gender: males=10, females=1; sizes for the rTMS condition (0.85) while the Severity of Injury: AIS C=5, AIS D=6. sham-rTMS condition yielded a smaller effect Healthy Group (n=10): Mean Age: 33.7 yr; size (0.42). Although both conditions Gender: males=6, females=4. demonstrated an improvement in time to Intervention: Patients and healthy complete the JTT but no significant differences volunteers were randomized to receive were reported (p=0.4). repetitive transcranial magnetic stimulation 2. Differences between the trained hand and non- (rTMS) or sham-rTMS to the corticomotor trained hand approached statistical significance region that controlled the weaker hand in time to complete the JTT (p=0.06). Gomes-Osman & (trained hand). After 1 wk of treatment, the 3. No significant differences were found for grasp Field-Fote 2014 two groups were crossed over for an strength and pinch strength between the two USA additional week. Both groups were asked to conditions from baseline to post treatment RCT complete the Nine-hole Peg Test (9HPT) although the rTMS condition produced a larger PEDro=6 during each rTMS/sham-rTMS session and effect size in grasp strength on the trained hand N=21 on days in between. The patients completed (0.67) compared to the sham-rTMS condition three sessions of each condition. (0.39). Assessments were completed at baseline 4. Performance on the 9HPT improved significantly, and at post treatment for each condition. regardless of condition, for the SCI group and the Outcome Measures: Jebsen-Taylor Hand healthy group during the first six days of Function Test (JTT), pinch strength, grasp treatment (p<0.0006 and p=0.05 respectively). strength, Nine-hole Peg Test (9HPT), motor 5. Resting and active MT did not differ significantly threshold (MT). between rTMS and sham-rTMS for both the SCI group and the healthy group at post treatment. Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Author Year Country Research Design Methods Outcome Score Total Sample Size

Population: Experimental Group (n=11): 1. A significant Time x Group interaction was Mean Age: N/R; Gender: males=7, reported for JTHF scores with the experimental females=4; Level of Injury: C3=2, C4=3, group improving significantly from baseline to C5=1, C6=3, C7=2; Severity of Injury: AIS post treatment on the JTHF compared to the B=1, AIS C=4, AIS D=6. control group (p=0.03). Control Group (n=13): Mean Age: N/R; 2. A significant improvement in JTHF scores were Gender: males=10, females=3; Level of found after the control group received the Injury: C4=2, C5=2, C6=5, C7=4; Severity of interventions (p=0.01) when comparing baseline Injury: AIS A=2, AIS B=3, AIS C=5, AIS D=3. to post treatment. However, the correlation Intervention: Patients were randomly between initial scores and the amount of change assigned to either an experimental group or a was not significant (p=0.19) indicating the control group then further divided into four improvement may have been due to chance. conditions, Unimanual Somatosensory 3. After analysing all four conditions, only a Stimulation (Uni-SS), Bimanual SS (Bi-SS), significant effect of Time was found (p=0.0006) Unimanual Functional Electrical Stimulation indicating that regardless of intervention, patients (Uni-FES) and Bimanual FES (Bi-FES). For all demonstrated improvement on JTHF scores patients who received SS, electrodes were from baseline to post treatment. placed over median nerve in the wrist. FES 4. No significant difference in JTHF scores were Hoffman & Field- electrodes were also placed on the median found between FES and SS from baseline to post Fote 2013 nerve in the wrist but FES was only triggered treatment (p=0.46). USA when muscle activation exceeded the 5. No significant difference in JTHF scores were RCT threshold value. During each session, found between bimanual and unimanual activities PEDro=4 patients completed a set of activities (either from baseline to post treatment (p=0.57). N=24 unimanually or bimanually) including 6. A significant Time x Group interaction was grasping, grasping and rotation, pinching, reported for Corticomotor activity with the pinch with rotation, and finger isolation. experimental group demonstrating an increase in Control patients received the interventions Corticomotor map area whilst the control group after an initial delayed control period. The did not demonstrate any changes (p=0.03). interventions were provided 2hr/day, 5day/wk 7. A significantly greater amount of change from for a total of 3 wk. Assessments were baseline to post treatment was found for patients conducted at baseline and at post treatment. in both bimanual conditions on the CAHAI Outcome Measures: Jebsen Taylor compared to patients in the unimanual Hand Function Test (JTHF), Corticomotor conditions (p=0.03). activity, Chedoke Arm and Hand Activity Inventory (CAHAI). Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Author Year Country Research Design Methods Outcome Score Total Sample Size

Population: Tetraplegic group (n=16): Mean 1. Three-way interaction between number of drifts, age: 45.9±14.5 yr; Gender: males=10, group and stimulation-type and body part was females=6; Mean Spinal Cord Independence significant (p=0.02). Measure-III (SCIM-3): 33.4±16.8; Level of 2. Tetraplegic group showed significantly greater injury: AIS A=8, AIS B=8; Severity of Injury: values in IRQ than ICQ responses in hand- C4-C6; Mean time since injury: 13.3±10.9 yr. synchronous (p=0.0001), hand-asychronous Paraplegic group (n=16): Mean age: (p=0.026), and face-synchronous conditions 50.0±13.2 yr; Gender: males=12, females=4; (p=0.024). Scandola et al. Level of injury: AIS A=14, AIS B=2; Severity 3. In paraplegic group significant values found in 2014 of Injury: T1-L4; Mean time since injury: IRQ over ICQ responses in hand-synchronous Italy 18.5±12.4 yr. (p<0.0001) and hand-asychronous (p=0.0002); Post Test Healthy controls (n=16): Mean age: whereas in healthy group only found significance N=48 43.1±16.9 yr; Gender: males=8, females=8. in hand-synchronous condition (p<0.0001). Intervention: Induction of the Rubber Hand 4. No statistically significant correlations were Illusion (RHI) through synchronous found between drifts or questionnaire responses multisensory visuo-tactile bodily stimulation and the TAS, the BFI-10, the SCIM-3 and the (cheek and rubber hand vertically aligned NLI. with real hand) to determine the correlation with plastic remapping. Outcome Measures: 6-item questionnaire; Illusion Related Questions (IRQ), Illusion

Author Year Country Research Design Methods Outcome Score Total Sample Size Control Questions (ICQ), Big-Five Inventory (BFI-10), Tellegen Absorption Scale (TAS). Population: Unimanual group (n=6): Mean 1. JTHFT scores improved significantly for both age: 42 yr; Gender: males=5, females=1; groups (p=0.01), and both groups completed Level of Injury: C5=1, C3=1, C4=4, Severity tasks in a shorter period of time. There were no of Injury: B=1, C=4, D=1. significant differences on this test between Bimanual group (n=7): Mean age; 34.7 yr; groups. Gender: males=5, females=2; Level of Injury: 2. CAHAI scores were significantly negatively C5=3, C6=4; Severity of Injury: AIS B=3, AIS correlated with JTHFT scores (p=0.02) indicating C=4. that increased scores on the CAHAI were Intervention: Participants were randomly correlated to faster completion times of the assigned to receive either unimanual or JTHFT. CAHAI scores improved significantly for bimanual massed practice in conjunction with both groups (p=0.02), but there were no SS for 2 hours a day for 5 days a week, over significant differences between groups. a three-week period. 3. SWMT scores improved significantly for both Outcome Measures: Jebsen Taylor Hand groups (p=0.004), there were no significant Function Test duration (JTHFT), Chedoke differences between groups over time. McMaster Hand Activity Inventory (CAHAI), 4. There were no significant changes in pinch grip Semmes-Weinstein Monofilament Test between groups, or over time. (SWMT), Pinch-grip strength (lbs), 5. Post-intervention there was a mean increase in Corticomotor map area, Resting corticomotor cortical map area (p=0.05), indicating a trend Hoffman and Field- threshold. towards enlargement of cortical map. There were Fote, 2010 no significant changes in cortical map area USA between groups. RCT 6. There were no significant differences between PEDro=5 groups or overtime in resting corticomotor N=11 threshold. Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Population: Group 1 (n=10): Mean Age: 1. There was no statistically significant difference 33.2±6.1 yr; Gender: males=8, females=2; between the 3 groups in age, sex, duration of Handedness: Rt=9, Lt=1; Level of injury: illness, ASIA scale, handedness and level of Nasser et al. 2014 C5=5, C6=4, C7=1; Severity of Injury: AIS injury (p>0.05). Eqypt C=4, AIS D=6; Mean time since injury: 2. There was a highly significant increase in post- Pre-Post 21.8±19.1 yr. Group 2 (n=10): Mean Age: treatment ASIA motor score in group I and group N=25 38.7±12.1 yr; Gender: males=8, females=2; II (p<0.001) but not group III (p>0.05). Handedness: Rt=8, Lt=2; Level of injury: 3. Comparison between pre and post-treatment C5=5, C6=4, C7=1; Severity of Injury: AIS scores in light touch and pinprick values showed a significant increase in both post -treatment in

Author Year Country Research Design Methods Outcome Score Total Sample Size C=3, AIS D=7; Mean time since injury: group II (p<0.05); but not in group I and III 24.1±22.1 yr. (p>0.05). Group 3 (n=5): Mean Age: 33.4±7.1 yr; 4. Pinch grip force showed a significant increase Gender: males=3, females=2; Handedness: after treatment in group II (p<0.001) and group I Rt=4, Lt=1; Level of injury: C5=2, C6=2, (p<0.05) but not in Group III (p>0.05). C7=1; Severity of Injury: AIS C=2, AIS D=3; 5. Comparison between pre and post-treatment Mean time since injury: 18.0±12.2 yr. WMFT timed scores showed significant decrease Intervention: Group I: 10 patients received in group I and group II (p<0.05) but not in group massed practice (MP) training. Group II: 10 III (p>0.05). patients received somatosensory (SS) with 6. There was no significant difference between massed practice. Group III: 5 patients groups on JTHFT timed scores (p>0.05). received traditional rehabilitation program. 7. There was a significant decrease in group I and Outcome Measures: Maximal grip force, group II in JTHFT score post-treatment compared Wolf Motor Function Test (WMFT) timed to pre-treatment value (p<0.05). score, Jebsen–Taylor hand function test score (JTHFT). Population: Age: 41-54 yr; Gender: 1. No difference between patients when looking at males=3, females=1; Level of injury: C5=4; the assessments done after baseline and after Severity of injury: AIS D=4; Time since injury: sham intervention. 1.25-8 yr. 2. The level of intracortical inhibition was reduced Intervention: Five days of sham repetitive to 37.5±8.0% of pre-treatment levels during the Belci et al., 2004 transcranial magnetic stimulation (rTMS) week of therapeutic treatment (p<0.05) and UK followed by five days of therapeutic returned to 90.2±15% of pre-treatment levels Pre-post stimulation (rTMS). during the follow-up period. N=4 Outcome Measures: ASIA Impairment 3. This was linked to improvements in clinical Scale (AIS), Nine Hole Peg Board. measures of both motor and pinprick of 4-10% during treatment week. (p<0.05). 4. Subjects also improved perceptual threshold to electrical stimulation of the skin and peg board test scores (p<0.05).

Discussion

Beekhuisen and Field-Fote (2005) suggested that MP or constraint-induced therapy promotes cortical reorganization that may be an effective rehabilitative tool for improving strength and function in individuals with cervical SCI. Improvement may be further enhanced by the addition of somatosensory stimulation. Beekhuisen and Field-Fote (2008) showed that the use of MP with somatosensory peripheral nerve stimulation (SS) and the use of SS only showed significant improvements in upper extremity function and pinch strength when compared to the results demonstrated by the control group. The study also showed that use of MP and SS together had a significant change in sensory scores and the MP with SS and MP groups only showed greater change in threshold measures of cortical excitability when compared to the control group results. These findings were supported in a more recent study (Nasser et al., 2014), however, Nasser et al (2014) also found that the combination of MP and SS resulted in a greater improvement than MP alone (Nasser et al., 2014). The mechanism of how SS and FES improves hand functioning has also been studied (Hoffman & Field-Fote, 2013). In unimanual and bimanual SS and FES conditions only a significant effect of time was found, regardless of intervention, with each condition resulting in improvements of hand functioning.

Multisensory visuo-tactile bodily stimulation has also been tested and illusory ownership over the hand was found to be more likely to occur in the presence of upper spinal levels (Scandola et al, 2014). Belci et al. (2004) observed clinical changes consistent with the concept that reduced corticospinal inhibition can facilitate functional recovery. Recovery involved increased AIS sensory and motor scores, improved response to cutaneous electrical stimulation over the thenar muscles and possibly improved hand/finger function. This preliminary study demonstrated rTMS treatment in patients with chronic stable incomplete SCI can produce reductions in corticospinal inhibition detectable using electrophysiological techniques. A more recent RCT found that rTMS resulted in improvements in hand functioning but not grasp strength or motor threshold (Gomes-Osman & Field-Fote, 2014).

One study tested the use of transcutaneous electrical nerve stimulation (TENS), transcranial direct current stimulation (tDCS), and vibration therapy (Gomes-Osman & Field-Fote, 2015). Authors concluded that TENS, tDCS, and vibration therapy resulted in significant improvements in hand functioning when combined with functional task practice.

For restorative strategies to be feasible for use in everyday clinical practice it is important that the interventions be available in the clinic and at home (Beekhuizen & Field-Fote 2005).

Conclusion

There is level 1a evidence (from three randomized controlled trials; Bekkhuizen & Field-Fote 2005, 2008; Hoffman & Field-Fote 2013) that showed that massed practice (repetitive activity) and somatosensory stimulation (median nerve stimulation) demonstrated significant improvement in upper extremity function, grip and pinch strength required for functional activity use.

There is level 1b evidence (from one randomized control trial; Gomes-Osman & Field-Fote, 2014) that showed that rTMs treatment in individuals with chronic stable SCI may produce reductions in corticospinal inhibition that resulted in clinical and functional changes for several weeks after treatment.

There is level 2 evidence (from two randomized controlled trials; Gomes-Osman & Field-Fote, 2015; Hoffman and Field-fote, 2010) that showed that tDCS, TENS, vibration therapy and repetitive massed practice resulted in significant improvements in upper extremity function and pinch strength.

There is level 4 evidence (from one post-test study; Scandola et al., 2014) that showed that the induction of the rubber hand illusion through synchronous multisensory visuo-tactile bodily stimulation resulted in ownership of the hand.

There is level 4 evidence (from one pre-post study; Belci et al., 2004) that showed therapeutic TMS can lower intracortical inhibition, which is linked to better clinical motor scores.

There is level 4 evidence (from one pre-post study; Nasser et al., 2014) that showed massed practice and somatosensory stimulation significantly improved motor function and pinch grip strength compared to traditional rehabilitation programs over time.

Afferent inputs in the form of sensory stimulation associated with repetitive movement and peripheral nerve stimulation may induce beneficial cortical neuroplasticity required for improvement in upper extremity function. Repetitive activity combined with somatosensory stimulation can significantly increase the functionality of upper extremities, potentially improving the over all quality of life for patients. Restorative therapy interventions need to be associated with meaningful change in functional motor performance and incorporate technology that is available in the clinic and at home.

5.2 Complementary Alternative Therapies Acupuncture is an ancient Chinese therapy practiced for more than 2500 years to cure disease and relieve pain (Lee & Liao 1990). There are 361 identified acupoints that have been formed into a network of 14 channels called the meridians. Acupuncture therapy has been shown to be effective in improving functional outcomes in hemiplegic stroke patients and in SCI patients with paraplegia (Cheng et al., 1998). In electrical acupuncture therapy, electrical stimulation is provided directly to the acupoint areas. It has been speculated that acupuncture therapy through the correct acupoints and meridians in the acute SCI episode assists in minimizing of posttraumatic cord shrinkage and sparing of the ventral horn neurons (Politis & Korchinski 1990; Ran et al., 1992; Tsay 1974; Wu 1990).

Table 7 Complementary Alternative Therapies Author Year Country Research Methods Design Outcome

Score Total Sample Size Population: Age: 28-69 yr; Gender: males=18, 1. There was a significant effect of time for females=6; Time since injury: 5-33 yr; Length both treatments on performance corrected of shoulder pain: 4 mo -22 yr. (PC)-WUSPI (Acupuncture p<0.001 and Intervention: Subjects received either Trager p=0.001). acupuncture treatments (sessions lasted 20-30 2. Overall a reduction of the PC-WUSPI could min) or Trager Psychophysical Integration - be seen when looking at the data from the sessions lasted approx 45 min. Consisted of beginning of treatment to the end for both both table work and Mentastic exercises groups (p<0.05) (easy, natural movement sequences to 3. There was a significant effect of time for enhance relaxation and decrease pain during both acupuncture and Trager groups for table work). average pain & most severe pain (p<0.01, p<0.001 respectively), for the least severe Dyson-Hudson Outcome Measures: Intake questionnaire pain the acupuncture group showed a et al., 2001 (demographics and medical history), Weekly significant reduction (p<0.01) compared to USA log, Wheelchair users shoulder pain index the Trager group. RCT (WUSPI), Numeric rating scale (NRS), Verbal 4. Verbal response scores- there was a PEDro=7 rating scale (VRS), Range of Motion (ROM). statistically significant treatment effect for N=21 both groups (p=0.001). Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Population: Mean age: 35 yr; Gender: 1. Acupuncture group - sensory, motor + FIM scores males=80, females=20; Level of injury: improved significantly day of D/C + one yr after paraplegia=63, tetraplegia=37; Severity of injury (p<0.05). Control group - only motor score injury: AIS A-B; Chronicity: acute. significant improvement at 1yr post injury F/U Intervention: Acupuncture was administered p=0.023. Wong et al., to the treatment group via 4 x 5 cm adhesive 2. Comparison of AIS + FIM scores of both groups 2003 surface electrodes at the acupoints of bilateral not at admission; D/C + one yr post significant Taiwan Hou Has (S13) and Shen Mo (B62). Frequency improvement AIS + FIM in acupuncture versus RCT was set at 75 hz with a pulse duration of 200 control p<0.05. PEDro=5 usec and the magnitude of stimulation was set 3. More patients in acupuncture group improved to N=100 at 10 mV. Sessions were 30 min, 5x/wk. AIS grade B + C or better at D/C + one-yr post Outcome Measures: ASIA Impairment Scale p<0.05. (AIS) (sensory + motor), Functional Independence Measure (FIM). Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Author Year Country Research Methods Design Outcome

Score Total Sample Size

Discussion

With acupuncture, thin metal needles are inserted into specific body sites and slowly twisted manually or stimulated electrically. The uncomfortable pain sensation or de qi, a prerequisite for effective acupuncture therapy, is induced by needle manipulation (Wong et al., 2003).

The RCT by Wong et al. (2003) studied the use of electrical acupuncture therapy through adhesive surface electrodes and concomitant auricular acupuncture therapy in improving the neurologic or functional recovery in acute traumatic SCI patients. This study demonstrated significant improvements in the acupuncture group on the day of discharge from hospital and one year after injury. The control group (auricular acupuncture) had significant improvement in only one outcome one-year post-injury follow up. The acupuncture group revealed significant improvement in all AIS and FIM scores when compared to the control group. An inherent bias may have been present as the reviewer who assessed the participants was not blinded to the group assignment.

Conclusion

There is level 2 evidence (from one randomized controlled trial; Wong et al., 2003) that showed that the use of concomitant auricular and electrical acupuncture therapy may improve the neurological and functional recovery of acute spinal cord injured individuals.

5.3 Splinting Splinting of the upper extremity in the management of tetraplegia is a well-accepted therapy intervention and has been an accepted practice for many years in the management of SCI especially in the acute phase of injury for the prevention of contractures and for joint protection (Curtin 1994; Krajnik & Bridle 1992). The therapeutic goals of splinting are the immobilization, protection and support of the joints of the wrist and hand, prevention of joint malalignment, prevention and reduction of soft tissue shortening and contractures, prevention of soft tissue overstretch, counteracting hypertrophic scars, support of weak muscles, improvement of function and pain relief (Curtin 1994; Krajnik & Bridle 1992; Paternostro-Sluga & Stieger 2004). It has been shown that elbow flexion contractures greater than 25 degrees have significant impact on the independence with the spinal cord injured person especially in the ability to transfer and complete depression lift for pressure relief (Bryden et al., 2004; Dalyan et al., 1998; Grover et al., 1996). The most common static hand splints for patients with tetraplegia are the resting pan or paddle splints, wrist extension splints (Futuro-type splint, long opponens splint and dorsal cock-up splint and spiral splint), short hand splints and tenodesis splints (Curtin 1994). Splints are also used to position the elbow in extension as flexion contractures of this joint are very common due to lack of triceps innervation and the effects of increased tone and spasticity (Bryden et al., 2004; Grover et al., 1996).

Table 8 Splinting of the Hand Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: N/R; Gender: N/R; Injury 1. After 12 wk, control thumbs carpometacarpal etiology: SCI=23, Stroke=14, ABI=7; Mean angle mean change was 45-47°. time since injury: 4 yr. Experimental thumbs carpometacarpal angle Intervention: Experimental group: thumbs mean change was 45-47°. The mean splinted into a stretched, abducted position, difference between these two groups was 1°. Harvey et al., 2006 every night (average eight hours), for 12 wk. 2. Twenty-two experimental subjects wanted to Australia Control group: no intervention. With the continue with the splinting regime and 20 RCT bilateral thumb group, splinting was applied to experimental subjects said their thumb web PEDro=8 one thumb and no splinting to the other (own space extensibility was increased by the NInitial=44; NFinal=43 control). With unilateral thumb, subjects were splinting. divided into experimental and control. 3. The intra-class correlation coefficient Outcome Measure: Palmar abduction of between carpometacarpal angle of the carpometacarpal joint, Subjective attitudes of control and unaffected thumbs, before and effectiveness and convenience of splinting. after treatment, was 0.87.

Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 18-42 yr; Gender: 1. No significant differences were noted males=12, females=1; Time since injury: 6–8 between the two groups-all subjects wk. demonstrated improvement in hand function Intervention: Experimental group was given and pinch strength. long or short orthosis to be worn at night 2. At eight wks the 13 subjects showed (eight hours) as soon as the subject could improvement in their performance on the tolerate it. checkers subtest (p<0.01), simulated feeding Outcome Measure: Pinch strength, subtest (p<0.01), and the large light object Functional activity use, Jebsen-Taylor Hand subtest (p<0.01). Function (JTHF). 3. At the 12-wk marker, improvement could be seen on the card subtest (p<0.05). 4. An increase in pinch strength was noted at eight wks for all subjects (p<0.05) and at 12 DiPasquale-Lehnerz wk nine remaining subjects (p<0.05). 1994 USA RCT Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- PEDro=4 and post-intervention data. NInitial=13; NFinal=9

Discussion

Even though splinting and orthotic fabrication is an accepted practice, there is minimal research on the effectiveness of this intervention (DiPasquale-Lehnerz 1994; Krajnik & Bridle 1992), although there are numerous anecdotal descriptions of orthotic devices and rationales for orthotic intervention (DiPasquale-Lehnerz 1994). Curtin (1994) and Krajnik and Bridle (1992) also found formal assessments were often not done due to; a lack of time and staff shortages; inconsistent documentation; absence of standardized tests available for spinal cord injured patients; limited funding to purchase equipment; and/or patient declined to participate in formal assessments due to boredom and frustration. Krajnik and Bridle (1992) noted that therapists considered observation of the patient when involved in a functional activity as the most informative assessment although this was not an objective means of documenting a patient’s status and progress. There appears to be a variety of splints made for similar purposes because there is little research as to what splint is best for the level and stage of SCI (Krajnik & Bridle 1992). It was noted by Harvey et al., (2006) that the use of splints is also viewed as a major inconvenience to both the client and therapist and the overall effect of the splint needs to be substantial in order to justify the inconvenience and discomfort.

Harvey et al., (2006) also reported that clients were initially agreeable to wear splints at the beginning of their treatment, but by the end of treatment they were less compliant.

In Paternostro-Sluga and Stieger’s (2004) review, the therapeutic aims of splinting and the choice of splint depend on the disease and the individual functional problem resulting from the impairment. These authors also concluded that there is insufficient evidence from clinical trials on splinting strategies in SCI patients.

Harvey et al. (2006) noted that twelve weeks of nightly stretch does not reduce thumb web-space contractures in people with a neurological condition (stroke, acquired brain injury, SCI). Even with careful monitoring of the fit of the splint for the thumb joint, it was unclear if the splint was able to produce enough torque to the thumb joint for a sufficient stretch. The study also raised questions concerning if the length of time wearing the splint was enough, if the time spent wearing the splint was accurately reported by the client, and if there is a difference in outcomes when considering the type of neurological condition being splinted.

DiPasquale-Lehnerz (1994) noted that there was no significant improvement in hand function as it related to passive ROM, strength of prehension or coordination in subjects with C6 tetraplegia who wore a thumb opponens orthosis during sleep as compared to those subjects with C6 tetraplegia who did not wear such an orthosis. The study did show over time a significant improvement of hand function especially pinch strength, and functional use (e.g., turning cards, and picking up small objects) for those wearing the splint.

There are several published surveys that address the use of splints in the spinal cord population with the majority of splints being functional use splints (i.e., feeding splint, writing splint, typing splint or an application for an assistive device) (Garber & Gregoria 1990; Krajnik & Bridle 1992). Research using larger study sizes, objective measures, and studying the type of neurological condition being splinted is needed to determine the effectiveness in contracture reduction.

Conclusion

There is level 2 evidence (from one randomized controlled trial; DiPasquale- Lehnerz 1994) that wearing a thumb opponens splint will improve pinch strength and functional use of the hand.

There is level 1b evidence (from one randomized controlled trial; Harvey et al., 2006) that 12 weeks of nightly stretch with a thumb splint did not reduce thumb web-space contractures in persons with a neurological condition (i.e., stroke, ABI, SCI).

6.0 Subacute Phase of Rehabilitation A spinal cord injured individual is forced to rely on their upper extremities for their weight bearing activities such as transfers, mobility needs, and ADLs using limbs that were designed to place hands in space (Consortium for Spinal Cord Medicine 2005; Dalyan et al., 1999; Dyson-Hudson & Kirshblum 2004). Repeated use of the upper limb for weight bearing activities such as manual wheelchair propulsion, transfers, raised ischial pressure reliefs (weight shifts), and reaching from a seated position in the wheelchair in environments designed for nondisabled individuals places a great deal of stress on the bones, joints, and soft tissues of the shoulder complex. The structures of the upper limb are therefore at significant risk for overuse and subsequent injury (Dyson-Hudson & Kirshblum 2004). Pain in the early post injury period is typically due to increased demands on anatomically weakened muscles or muscle weakness induced because of deconditioning.

Upper limb pain is known to interfere with a wide range of functional activities, transfers, ambulation, pressure relief, and self-care (Curtis et al., 1995a, Dalyan et al., 1999); many individuals report alteration/cessation of activities critical to functional independence (Pentland & Twomey 1994; Sie et al., 1992). Shoulder pain may be functionally and economically equivalent to a higher level of lesion (Salisbury et al., 2003). Dalyan et al. (1999) reported that of individuals with upper limb pain, 26% needed additional help with functional activities and 28% reported limitations of independence. Subbarao et al. (1994) and Gerhart et al. (1993) found that individuals with SCI reported that their dependence in personal care assistance fluctuated with upper limb pain and was a major reason for functional decline. The Consortium for Spinal Cord Medicine (2005) has written clinical practice guidelines “Preservation of Upper Limb Function Following Spinal Cord Injury: A Clinical Practice Guideline for Health Care Professionals,” to address upper limb problems. Recent studies have also started to explore factors that relate to upper extremity pain (Barbetta et al., 2016).

In the subacute phase of rehabilitation, the strategies that were initiated during the acute phase of rehabilitation are continued (Field-Fote, 2009). Adjustments may be made to the approaches to rehabilitation, however, working towards the therapeutic goals to help persons with SCI achieve optimal functioning continues. Exercises to strengthen the upper limb during this phase of rehabilitation can include progressive increases to the resistance of weight to improve muscle strength (Field-Fote, 2009). Hand grasping and opening are also a focus of this phase of rehabilitation.

Table 9 Subacute Phase of Rehabilitation Author Year Country Research Design Methods Outcome Score Total Sample Size Population: SCI population (n=8): Mean 1. Maximum hand opening was reduced age: 37±4.4 yr; Gender: males=7, in SCI participants as compared to females=1; Level of injury: AIS C4-C7=1, controls (p=0.002). AIS C5=1, AIS C5-C7=6; Mean time since 2. No correlation between maximum injury: 10.9 yr. voluntary hand opening and hand Healthy controls (n=8): Mean age: 26.6±2.4 function with BBT (p=0.934) and JTHF yr; Gender: males=6, females=2. (p=0.701). Intervention: Measured hand kinematics 3. SCI participants had greater EMG and surface electromyography from seven activity in AD (anterior deltoid) muscles of the hand and wrist during (p=0.018), TRI (triceps brachii) attempts at maximum hand opening as well (p=0.009), FCU (flexor carpi ulnaris as reaching for four balls of different (p=0.020), and FDS (flexor digitorum diameters. superficialis) (p=0.051) as compared Outcome Measures: Hand kinematics, to AB group. Surface electromyography (EMG) of wrist 4. Co-activation ratios at wrist and hand and hand muscles, Peak aperture, Box- were reduced for the SCI group and-Blocks Test (BBT), Jebsen-Taylor compared to the control group (wrist: Hand Function (JTHF). p=0.030, hand: p=0.006). Stahl et al. 2015 5. Peak aperture for balls B, C, and D USA was larger in the AB group than the Post-Test SCI group (all p≤0.042), while peak N=16 aperture for the smallest ball A was not different (p=0.163). 6. AB participants utilized less of their aperture range compared to the SCI group (p=0.035). 7. There was no difference in number of muscle coordination patterns (p=0.227) as both groups required three patterns to sufficiently account for >90% of EMG data variance. 8. For the SCI group, the wrist flexion muscle coordination pattern (p=0.002) increased activation as the ball size increased. 9. The wrist extension muscle coordination pattern also showed a nonsignificant trend to increase activation as ball size increased (p>0.05).

Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Mean age: 34.0 yr; Gender: 1. Prevalence of musculoskeletal UE males=446, females=118; Mean BMI: pain was 27.7% (CI 95%, 24.0–31.4). 22.4±4.8 kgm2; Level of injury: C1-5=32, 2. In groups with and without pain, age C6-1=189, T2-6=146, T7-S5=197; Severity (p=0.185), BMI (p=0.312) and mobility of injury: AIS A=317, AIS B=85, AIS C=48, aid (p=0.101) showed no statistically AIS D=54; Mean time since injury: 5.0 yr. significant difference. Intervention: No intervention. 3. Gender (p=0.007), time of injury Retrospective charts were reviewed (p<0.001), level (p<0.001) and analyze impact of demographic (gender, completeness of injury (p=0.039), and age, body mass index (BMI)) and injury locomotion (p<0.001) were based variables (level of injury, severity of significantly different between pain injury, time of injury, type of mobility, and no pain groups. locomotion aid) on occurrence of 4. Women are twice as likely to musculoskeletal pain. experience UE pain as men (95% CI, Outcome Measures: Musculoskeletal 1.3-3.4). pain. 5. Individuals aged ≥41 yr are twice as Barbetta et al. 2016 likely to have pain as are patients Brazil <24.7 yr of age (95% CI, 0.3-0.9). Case Series 6. Individuals with injury that has lasted N=564 <1 yr have a greater risk of pain than individuals in other quartiles; the former are two times more likely to experience UE pain than are individuals with 1.1–2.8 yr of injury (95% CI, 0.2-0.7) and three times more likely than individuals with 2.9– 6.8 (95% CI, 0.2-0.5) and 6.9+yr of injury (95% CI, 0.2-0.6). 7. The individuals exclusively using wheelchairs for locomotion had twice the risk of pain than did those in the ‘wheelchair+orthostatism’ (95% CI, 0.3-0.8) and ‘wheelchair+walking exercise’ groups (95% CI, 0.3-1.0). 8. There was no difference in a comparison with the ambulators.

Discussion

Opening the hand to grasp for objects is often compromised after cervical SCI. Stahl etl al. (2015) hypothesized that persons with SCI demonstrate neuromuscular coordination strategies, allowing object-specific hand aperture scaling while reaching. This was tested with different sized objects and authors concluded that motor planning for aperture modulation is preserved despite the limitations on hand opening capacity and muscle co-activity (Stahl et al., 2015).

The increased use of the upper extremity has been associated with a higher occurrence of musculoskeletal pain among SCI injured individuals (Boninger et al., 2005). A retrospective chart review considered factors that are associated with musculoskeletal pain. This study found that women, tetraplegia, being over 41 years of age, exclusively

using a wheelchair for locomotion, and being less than one-year post-injury were significantly related to the presence of musculoskeletal pain (Barbetta et al., 2016).

The following are the identified risk factors for the development of musculoskeletal pain (Barbetta et al. 2016): • Gender - women. • Compleness of injury- tetraplegia. • Time of injury- persons less than one-year post-injury. • Age – being over 41 years of age. • Locomotion – exlusively using a wheelchair.

Psychological interventions among non-SCI individuals with chronic pain are popular and it has been suggested that selected approaches may be useful for those with SCI (Consortium for Spinal Cord Medicine 2005). Cognitive-behavioural strategies have been found to produce changes in pain experience, increase positive cognitive coping and appraisal skills, and reduce pain behaviours (Morley et al., 1999). Cognitive- behavioural strategies have also been suggested to be beneficial among SCI injured individuals (Heutink et al., 2013).

As identified in the Consortium for Spinal Cord Medicine (2005) document, modification of task performance based on ergonomic analysis has been shown to reduce the incidence of upper limb pain and cumulative trauma disorders of the upper limb in various work settings (Carson 1994; Chatterjee 1992; Hoyt 1984; McKenzie et al., 1985). It is suggested that these same interventions can be used to prevent pain and injury in SCI. Although the number of studies linking activities of individual with SCI to injury may be small, the ergonomics literature provides a strong basis for evidence- based practice. Rice et al. (2013) studied the impact of a strict education protocol in the implementation of the clinical practice guideline “Preservation of Upper Limb Function Following Spinal Cord Injury” addressing the impact of an education protocol on transfer skills and wheelchair propulsion. The study demonstrated a positive effect on the importance of proper education in improving the quality of transfers and better wheelchair propulsion biomechanics as key elements in reducing the risk of shoulder injury and pain (Rice et al., 2013).

The Consortium for Spinal Cord Medicine (2005) Clinical Practice Guideline Preservation of Upper Limb Function published a series of recommendations regarding the upper limb. First, both the spinal cord injured person and the clinician need to be educated about the prevalence of upper limb pain and injury and the potential impact of pain and possible means of prevention. Additionally, patients should have their function, ergonomics, equiptment and level of pain assessed at each perodic review. At this time other potential risk factors can also be addressed, such as changes in medical status, new medical problems, and changes in weight. Lastly, general housekeeping measures which can benefit the patient were identified as reducing the number of non-level transfers per day, assessing work related activities and re-evaluating their current exercise program.

The Consortium for Spinal Cord Medicine (2005), Sipski and Richards (2006), Campbell and Koris (1996), Dalyan et al. (1999), and Nichols et al. (1979), identified the following as important areas of further research in the upper limb: • Research to validate and support the adoption of a standardized classification scheme with accompanying diagnostic procedures and criteria. • Determine the best methods to treat existing painful shoulder lesions and prevent others so that these individuals are as pain free and independent as possible. • Further study is needed to elucidate the mechanisms of pain in this group and to establish why some patients who have pain early in rehabilitation continue to have pain at discharge and others do not. • Multicentre RCT of intervention are also needed to reduce the severity and impact of different subtypes of SCI pain. • Possible links between pain during rehabilitation and pain in long-term SCI. • Detailed investigation of the biomechanics of activities commonly performed by people with tetraplegia to enhance understanding of the stresses placed on the shoulder and the mechanical causes of shoulder pain. • Causes of shoulder pain in the acutely injured individual compared to the chronic spinal cord injured person. • Implementation of upper limb pain prevention and management programs for persons with SCI- acute and ongoing patient education about basic biomechanical principles on avoiding impingement and overuse. • Managing the early signs of strain and overuse and knowledge of several alternative techniques of ADL. • Education and training in endurance and balanced strengthening of muscles acting around the shoulder and optimizing posture to achieve a normal alignment of shoulder, head, and the spine are critical for avoidance of injuries. • Ergonomically designed environmental changes and wheelchair, home and work modifications. • Further clinical and biomechanical research to improve the preventative measures and treatment methods of upper limb pain in SCI persons in order for them to maintain optimal functional status.

Conclusion

There is level 4 evidence (from one post-test study; Stahl et al., 2015) that among persons with chronic SCI motor planning for aperture modulation is preserved.

There is level 4 evidence (from one case series; Barbetta et al., 2016) that the presence of musculoskeletal pain is not necessarily related to lifestyle factors (such as BMI and mobility aid) but more of a function of other demographic factors (such as gender, age, and level of injury).

Preliminary reseach suggests that persons with SCI may preserve the ability to scale peak hand aperture with ball size objects while reaching, which may be due to distinct muscle coordination patterns including increased co-activity of flexors and extensors at the wrist.

hypertonia of spinal cord origin.

6.1 Shoulder Injuries Upper limb pain and injury are highly prevalent in people with SCI and consequences are significant. The Consortium for Spinal Cord Medicine (2005) and Dyson-Hudson and Kirshblum (2004) reported through surveys and cross-sectional studies that shoulder pain in chronic spinal cord injured persons are common in both paraplegia and tetraplegia. The incidence of shoulder pain in acute tetraplegia (less than six months post injury) has been reported to range from 51%-78% (Salisbury et al., 2003). In the acute phase after SCI, shoulder pain is reported in approximately 75% of patients (Silfverskiold & Waters 1991; Wanring & Maynard 1991), and 33%-63% of patients in the chronic phase (greater than 6 months) experience shoulder pain (Nepomuceno et al., 1979; Sie et al., 1992; Silfverskiold & Waters 1991). Curtis et al. (1995a), Nichols et al. (1979) and Pentland and Twomey (1991) reported in cross sectional studies that 60- 100% of long-term wheelchair users experience shoulder pain. Subbardo et al. (1994) and Sie et al. (1992) reported that shoulder pain is still prevalent in individuals 15-20 years’ post injury. Pain experienced above the injury level during the first three to six months after injury is different than the pain experienced one year or more after injury (Apple 2001). Pain above the level of injury in chronically injured person assumes the character of overuse syndromes (Apple 2001). Injury involving the shoulder, elbow, wrist, and hand are seen at an earlier age in spinal cord injured individuals than in the general population because of the stresses of weight bearing and mobility that are added to the normal use of the upper limb (Pentland & Twomney 1994). Individuals who are older at the time of injury may experience functional changes earlier than people who are injured at a younger age (Thompson 1999), this results in difficulty determining whether shoulder pain is a function of duration of SCI or simply a part of the normal aging process (Neer & Welsh 1977).

The range in prevalence of shoulder pain is likely a reflection of the heterogeneity of participant populations between the studies with respect to duration of injury, age, neurologic level and severity of injury, as well as body mass index. Small sample size, selection bias, and variations in participant populations across the different studies make it difficult to assess the true prevalence of shoulder pain in individuals with shoulder pain (Pentland & Twomey 1991).

Nichols et al. (1979) was one of the first groups to report an association between chronic SCI and shoulder pain coining the term “wheelchair user’s shoulder”. Due to the prevalence of shoulder pain, Curtis et al. (1995b) developed a Wheelchair Users’ Shoulder Pain Index (WUSPI) that measures the severity of pain for 14 functional activities.

Table 10 Shoulder Injury Intervention Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 19-65 yr; Level of injury: C4- 1. EX group reported less pain, stress and L1; Severity of injury: AIS A-D; Time since depression after training + scored higher injury: 1-24 yr. than CON in indices of satisfaction with Intervention: Experimental group participated physical function, level of perceived health + in a progressive exercise training 2x/wk for overall quality of life (p<0.05). nine mo-each session offered on alternative 2. Following training, EX group had significant days lasting 90-120 min. Control group were increases in sub maximal arm ergometry offered educational sessions bimonthly power output (81%; p<0.05) and significant (exercise physiology for SCI osteoporosis, post increases in upper body muscle strength SCI relaxation methods). (19-34%; p<0.05). Outcome Measures: Perceived stress scale, Muscle strength, Depression, Physical self- concept pain, Perceived health, Quality of Life (QOL). Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Hicks et al., 2003 Canada RCT PEDro=5 NInitial=32; NFinal=24

Population: Age: 28-69 yr; Gender: males=18, 1. There was a significant effect of time for females=6; Time since injury: 5-33 yr; Length both treatments on performance corrected of shoulder pain: 4 mo-22 yr. (PC)-WUSPI (Acupuncture p<0.001 and Intervention: Subjects received either Trager p=0.001). acupuncture treatments (sessions lasted 20-30 2. Overall a reduction of the PC-WUSPI could min) or Trager Psychophysical Integration - be seen when looking at the data from the Dyson-Hudson et al., sessions lasted approx 45 min. Consisted of beginning of treatment to the end for both 2001 both table work and Mentastic exercises groups (p<0.05) USA (easy, natural movement sequences to 3. There was a significant effect of time for RCT enhance relaxation and decrease pain during both acupuncture and Trager groups for PEDro=7 table work). average pain & most severe pain (p<0.01, N=21 Outcome Measures: Weekly log, Wheelchair p<0.001 respectively), for the least severe users shoulder pain index (WUSPI), Numeric pain the acupuncture group showed a rating scale (NRS), Verbal rating scale (VRS), significant reduction (p<0.01) compared to Range of Motion (ROM). the Trager group.

Author Year Country Research Design Methods Outcome Score Total Sample Size 4. Verbal response scores- there was a statistically significant treatment effect for both groups (p=0.001). Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- and post-intervention data.

Population: Mean age: 35 yr; Gender: 1. There were no significant differences males=35, females=7; Level of injury: cervical- between control and experimental group in lumbar; Mean duration of wheelchair use: 24 age, yr of wheelchair use or activity levels. yr. 2. When looking at the effect of exercise of Intervention: Both groups completed the intervention on performance corrected (PC) Wheelchair Users Shoulder Pain Index WUSPI, a two factor repeated measures (WUSPI) every two mo for six mo. The ANOVA showed a significant effect of time experimental group attended a 60 min only (p=0.048). educational session where they were instructed in five shoulder exercises. Curtis et al., 1999 Outcome Measures: Wheelchair User's USA Shoulder Pain Index (WUSPI), Visual Analog RCT Scale (VAS). PEDro=5 Effect Sizes: Forest plot of standardized mean differences (SMD±95%C.I.) as calculated from pre- N=42 and post-intervention data.

Discussion

Outcome studies of surgical treatment in SCI also very limited. Two small studies report the outcome of rotator cuff repair – one showing relatively poor results (Goldstein et al., 1997) and another study showing relatively good outcomes (Robinson et al., 1993). Both studies recommend non-surgical approaches prior to surgical intervention. One RCT found that supervised exercise produced results similar to arthroscopic surgery for patients with impingement syndrome (Brox et al., 1993), however; this study did not include SCI patients.

Exercise has been shown to reduce pain in a RCT in which subtypes of pain were not reported (Hicks et al., 2003). Two studies found an association between restricted ROM and pain, reduced activity and/or injury (Ballinger et al., 2000; Waring & Maynard 1991). RCT’s incorporating stretching into an exercise program for individuals who use manual wheelchairs found stretching exercises were associated with decreased reported shoulder pain intensity (Curtis et al., 1999; Hick et al., 2003).

One RCT demonstrated that acupuncture was no more effective than Trager Treatment in the treatment of shoulder pain (Dyson-Hudson et al., 2001). There are several studies that address the use of complementary or alternative medicine (CAM) with the spinal cord population, which is used at similar rates to the general population. It was reported that the most common reason CAM was used, was for dissatisfaction with conventional medicine for treatment of chronic pain (Nayak et al., 2001). The only CAM technique evaluated in the SCI population is acupuncture although studies do not provide conclusive evidence of effectiveness (Dyson-Hudson et al., 2001; Nayak et al., 2001; Rapson et al., 2003).

The following are the many identified risk factors for the development of injury and pain in the shoulder: • The shoulder is the most common joint above the level of injury where pain complaints are reported with persons with paralysis (tetraplegia or paraplegia) (Apple 2001). • The shoulder is not well designed to handle the higher intra-articular pressures required for both weight bearing and mobility (Apple 2001). • Partial innervation and impaired balance of shoulder, scapular and thoracolumbar muscles place individuals with tetraplegia at a higher risk for developing shoulder pain especially during weight-bearing upper limb activities such as wheelchair propulsion, transfers, and pressure reliefs. • Due to differences in trunk postural control, differences may also occur between individuals with high paraplegia (T2-T7) and low paraplegia (T8-T12). • Individuals with C1-C4 motor levels of injury are also at risk for shoulder pain. • SCI severity also may be associated with shoulder pain (Dyson-Hudson & Kirshblum 2004). • Lack of use of immobilization of the shoulder girdle muscles can limit their active joint movement and lead to muscle shortening and shoulder capsule tightness. • The development of pain is associated with decreased shoulder ROM. • Weakness and paralysis in these muscles can lead to increased reliance on the trapezius, which can result in overuse and pain in this muscle. • Shoulder pain can occur from nerve root injury or radicular pain with dysesthesias or phantom sensations. • People of certain age groups, those with higher cervical lesions, and those with shorter lengths of bed rest may be at a greater risk. • Gender may be associated with shoulder pain in individuals with SCI (Pentland & Twomey 1991). • Body mass index (BMI) also may play a role in shoulder injuries in manual wheelchair using individuals with SCI because it directly relates to the amount of

physical strain experienced during ADLs in these individuals (Boninger et al., 2001; Jensen et al., 1996). • Shoulder pain is more common in individuals with tetraplegia and complete injuries and in women and duration of injury, older age, and higher BMI all may be risk factors for developing shoulder pain and/or abnormalities in persons with SCI (Dyson-Hudson & Kirshblum 2004).

Conclusions

There is level 1b evidence (from two randomized controlled trials; Hicks et al., 2003; Curtis et al., 1999) that a shoulder exercise and stretching protocol reduces the intensity of shoulder pain post SCI.

There is level 1b evidence (from one randomized controlled trial; Dyson-Hudson et al. 2001) that general acupuncture is no more effective than Trager therapy in reducing post-SCI upper limb pain.

Shoulder exercise and stretching protocol reduces post SCI shoulder pain intensity. Acupuncture and Trager therapy may reduce post-SCI upper limb pain. Prevention of upper limb injury and subsequent pain is critical.

6.2 Elbow, Wrist and Hand Injuries

The prevalence of elbow pain and injury has been reported to be between 5-16% (Consortium for Spinal Cord Medicine 2005). Sie et al. (1992) found that pain localized in the elbow region in persons with tetraplegia and paraplegia was present in approximately 15% of SCI injured individuals, while a study by Dalyan et al. (1999) found that up to 35% of participants in their study complained of elbow pain.

The prevalence of carpal tunnel syndrome is reported to be between 40-66% (Consortium for Spinal Cord Medicine 2005). There are four studies that found an association between length of time since injury and prevalence of carpal tunnel syndrome (Aljure et al., 1985; Gellman et al., 1988; Schroer et al., 1996; Sie et al., 1992). Some studies also found median nerve damage without clinical symptoms.

Table 11 Elbow, Wrist and Hand Injuries Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Paraplegic group (PG; n=56): 1. PG experienced significantly more Mean age: 53.0±9.0 yr; Gender: males=44, pain in wrist (p=0.004) and females=12; Level of lesion: thoracic=50, trapeziometacarpal joint (p=0.08) CTS lumbar=6; Mean time since injury: 34.7±6.8 symptoms reported more often than yr; AB (p=0.02). Able-bodied group (AB): Mean age: 52±10 2. CTS was diagnosed by clinical and yr; Gender: males=44, females=12. neurophysiological examination Intervention: No intervention. Compared significantly more often in the PG functional and structural changes in hand, (p<0.05 for both). particularly carpal tunnel syndrome (CTS) 3. Mean DML differed significantly in wheelchair dependent paraplegic vs between the groups (p<0.001). healthy subjects. 4. There was no significant difference in Outcome Measures: Current pain, CTS CTS between dominant and non- symptoms, German version of the disability dominant hands in PG, but was for AB of the arm, Shoulder and hand (p=0.01). questionnaire, Phalen’s Test, Tiel’s sign at 5. Women did not present with CTS more carpel tunnel, Distal motor latency (DML) often than men in the PG. measurement, Magnetic Resonance 6. The relative risk of developing Imaging (MRI). symptoms of CTS was increased 25- fold in the PG over AB (95% CI: 8–81). Akbar et al. 2014 7. There was no correlation between the Germany prevalence of CTS and the duration of Observational SCI. N=112 8. Hand function according to the mean disability of the arm, shoulder and hand score was significantly worse in PG than AB (p<0.001). 9. Significantly higher incidences of trapeziometacarpal, radiocarpal and midcarpal osteoarthritis, pathological changes in triangular fibrocartilage complex of right hand in PG right hand (p<0.05 for all). 10. Significantly more flexor tendon sheath and thickening of flexor retinaculum in PG left hand (p<0.05 for both). 11. Relative risk for PG to develop wrist osteoarthritis increased 3.7 times (95% CI: 1–11) on right side, increased 2.8 times (95% CI: 1–9) on left side; developing trapeziometacarpal osteoarthritis on right side increased 4 times (95% CI: 1–16) and left side by 2.5 times (95% CI:0.6–10).

Discussion

The most significant activities causing pain in the wrist and hand are reported to be propelling a wheelchair and doing transfers (Subbarao et al., 1994). Individuals with paraplegia report much higher rates of carpel tunnel syndrome and pain, compared to able-bodied individuals (Akbar et al., 2014). Management of established upper limb pain

is very difficult and thus prevention is critical. Evidence-based best practice standards have not been established for the medical, rehabilitative, or surgical treatment of upper limb injuries in people with SCI. In addition, there is little consensus among health-care providers on the best treatment practices for upper limb injuries in the general population. In general, musculoskeletal upper limb injuries in the SCI population are managed in a similar fashion as the unimpaired population.

Conclusion

There is level 5 evidence (from one observational study; Akbar et al., 2014) that people with paraplegia are significantly more likely to develop bilateral carpel tunnel syndrome.

Clinicians should be mindful of the risk factors that could influence the development of musculoskeletal pain and consider rehabilitation options accordingly.

7.0 Reconstructive Surgery and Tendon Transfer

Reconstructive surgery is one option when trying to improve the function of the hand and upper limb in persons with tetraplegia. Functionally, the benefit of reconstructive surgery may be evident through improved ability to write, complete catheterizations, dress, self-feed, drive, lift objects, button, propel the wheelchair, catch objects overhead, turn in bed, and swim, which are only some of the activities that can become possible after surgery (Rabischong et al., 1993). Surgery has been reported to improve quality of life for those people who had little or no upper limb function (Freehafer et al., 1984). Despite the potential benefits, the option to receive reconstructive surgery in persons with SCI is often declined. This decision is influenced by a temporal element including hope for a cure or recovery from SCI (Dunn et al., 2013). It has been recommended that persons with SCI be offered upper limb surgery multiple times throughout their lives to consider changes in perspective. Flexibility of the timing for surgery and the type of rehabilitation offered may also help to increase the uptake of surgery (Dunn et al., 2013).

7.1 Hand The loss of upper limb function especially the use of the hand is one of the most significant and devastating losses an individual can experience. Tetraplegia is responsible for many problems in daily living, especially related to the preservation of independence for the individual with tetraplegia (Welraeds et al., 2003). A study by Hanson and Franklin (1976) showed recovery of hand function was preferred to that of the bladder, bowel or even sexual function among persons with tetraplegia. In a survey of tetraplegia patients, 75% responded that hand function was very important for their independence in ADL and to increase their quality of life (Snoek et al., 2004). In another study conducted in the United States with a sample of individuals with tetraplegia, 42% of the individuals viewed upper limb as the function they wanted restored first and 44%

of the surveyed individuals reported an interest in receiving upper extremity reconstructive surgery (Wagner et al., 2007).

Despite the many reported studies of hand reconstructive surgery, it is not common practice in many spinal units. Internationally, many barriers for SCI injured individuals exist which results in an underutilization of reconstructure survey (Fox et al., 2015). The efficacy of surgery to improve hand function still remains controversial (Forner-Cordero et al., 2003). Guttmann (1976), McSweeney (1969) and Bedbrook (1969) believed that only a small percentage of persons with tetraplegia (5%) benefit from hand surgery because they re-adjust the function of their arm and hands if properly rehabilitated, while other authors have estimated that 75% of persons with tetraplegia can benefit from hand surgery (Moberg 1975). A review of epidemiologic data from 1988 to 2000 in the USA found that only seven percent of appropriate surgical candidates actually received surgery (Curtin et al. 2005). In a study completed by Wuolle et al. (2003), individuals with tetraplegia who received upper extremity surgery were surveyed and 70% of the individuals were satisfied with their results and 68% reported improvement in ADLs. These statistics are consistent with physician estimates of 75% of client’s being satisfied, suggesting that both the client and medical professional often view reconstructive surgery as being beneficial and satisfying (Wagner et al., 2007). Reason for underutilization of reconstructive surgery for those with tetraplegia have been identified as; lack of clarity in the literature about the value of reconstructive procedures, lack of access to centres that perform reconstructive surgeries, lack of qualified and experienced hand surgeons and physiatrists who have an interest in this area of surgery and negative physician bias toward reconstructive surgery (Curtin et al., 2005; Squitieri and Chung 2008).

Reconstructive surgery and tendon transfers are generally performed following an identifiable pattern based on the level of injury and results depend on the patient’s residual motor and sensory function as identified in each group (Freehafer et al., 1984). In 1978, the International Classification for Surgery of the Hand in Tetraplegia was developed and has since been modified. The classification takes into account the residual motor strength below the elbow, considering that only the muscles graded four or five according to the Medical Research Council Scale are adequate for muscle transfer, as well as the sensibility in thumb and index. The sensibility was evaluated by the two-point discrimination test in the thumb and the index. If it is lower than 10mm the classification belongs to the group Cutaneous (Cu-) and if it is higher than 10mm and the patient needs visual help it is classified in the group Ocular (O-).

Table 12 Modified International Classification for Surgery of the Hand in Tetraplegia (McDowell et al., 1986) Sensory Motor O- Cu- Total 0 Weak or absent Brachioradialis (BR) ≤ grade 3 - - - 1 BR (≥ grade 4) 2 1 3 2* BR, ECRL - 1 1 3* BR, ECRL, ECRB 1 1 2 4* BR, ECRL, ECRB, PT 3 4 7 5* BR, ECRL, ECRB, PT, FCR - 4 4

Sensory Motor O- Cu- Total 6* BR, ECRL, ECRB, PT, FCR, Finger Extensors - - - 7* BR, ECRL, ECRB, PT, FCR, Finger Extensors, Thumb Extensors - 1 1 BR, ECRL, ECRB, PT, FCR, Finger Extensors, Thumb Extensors, 8* 1 - 1 Finger Flexors 9* Lacks intrinsics only - 1 1 Total 7 13 20

Candidates for reconstructive surgery are carefully selected and are followed by a rehabilitation team that includes an orthopedic surgeon, rehabilitation physiatrist, and therapist over a significant period of time. The identified criteria for selection are as follows: at least one-year post-injury, completed a comprehensive rehabilitation program, neurologically stable, and psychologically adjusted to their injury. The measure of outcomes following reconstructive surgery continues to be debated in the literature. Many of the reported studies on surgical outcomes are older, are case series evaluations, and have subjective outcomes based on reported client satisfaction. In addition, there is little consensus in the literature on the assessment instruments and tools to be used in this population as their reliability, validity and responsiveness have not been adequately evaluated. The methodology appears to be a major failing of the various scales and the absence of clear conceptual models forming the basis of their scales. Also, the scales or instruments may lack sensitivity and overlook the small but meaningful functional gains made by those with tetraplegia after functional surgery (Fattal 2004). Many authors state that comparing the post-surgical condition is the best way to evaluate results (Freehafer et al., 1984). There have been several articles published that discuss the use of the ICF conceptual framework as a way to interpret hand function outcomes following tendon transfer surgery for tetraplegia (Bryden et al., 2005; Sinnott et al., 2004).

The reconstructions of upper limb to obtain functions of pinch and grasp often require multiple procedure and are also individualized to each person. The reconstructions performed are also dependent on what motor muscles/tendons are present and strong enough for transfer (Kozin 2002). Dunn et al. (2012) completed a study that addressed client’s decision-making process for reconstructive upper limb surgery and it was found that that a client’s decision to have surgery were underpinned by 6 core influences. These influences were the overall outcome of surgery, the client’s current goals and priorities in their life, the hope that their overall QOL would be improved, a stable home environment, available social supports and assistance for assisting with increased care needs post-surgery and access to information on surgery. It was also found that these factors were individualized to each person and change with time.

7.1.1 Pinch

The most commonly performed surgeries for reconstructive pinch are: • Key-Pinch Grip – Brachioradialis to Extensor Carpi Radialis Longus, Flexor Pollicis Longus split tenodesis. The IP joint of the thumb may need to be stabilized to prevent excessive IP flexion.

• Key-Pinch Grip with or without Hook Grip – Brachioradialis to Flexor Pollicis Longus with or without Flexor Digitorum Profundus tenodesis or Brachioradialis to Extensor Carpi Radialis Longus. • Key-Pinch Grip and Hook Grip – Brachioradialis or Pronator Teres to Flexor Pollicis Longus and Brachioradialist or Extensor Carpi Radialis Longus to Flexor Digitorum Profundus.

Additional procedures to increase thumb pinch and thumb opposition may also be completed.

Table 13 Reconstructive Surgery – Pinch Studies Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 8-58 yr; Gender: 1. All patients had preoperative grip males=103, females=30; Level of injury: strength of zero. At an average tetraplegia; Follow-up time: 3-24 mo. follow-up period of 31 mo, the Intervention: Extrinsic hand average final grip strength was 69N reconstruction with intrinsic balancing (7kg) and the ADL improvement procedures versus extrinsic score averaged 35.5. reconstructions without intrinsic balancing 2. Patients who underwent an intrinsic procedures. procedure had a statistically Outcome Measures: Pre-and post- stronger grip (72N) than patients operative assessments of grip strength who did not undergo an intrinsic (on the second position of the Jamar procedure (p=0.026). dynamometer), Activities of Daily Living 3. Ocular group: Five patients with an (ADL). intrinsic procedure had a statistically stronger grip than patients without an intrinsic procedure (p=0.028). 4. With the exception of Ocular group 7, in which eight patients did not undergo an intrinsic procedure due to their ability to balance tension McCarthy et al., 1997 between the extensors and flexors, USA all other Ocular groups with an Pre-post intrinsic reconstruction showed N=135 stronger grip than patients without an intrinsic reconstruction. 5. ADL improvements scores were higher but not statistically significant for those with intrinsic rebalancing versus those without rebalancing. 6. There was significant difference between the hands treated by FDS lasso and those treated by intrinsic tenodesis when patients were stratified by Ocular level. 7. There was also no significant difference in grip strength results between the FDS lasso versus the intrinsic tenodesis procedures when stratified by both Ocular level and type of extrinsic reconstruction, both surgical techniques were effective in improving strength and ADL.

Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 16-29 yr; Gender: 1. All patients reported a significant males=14, females=4; Level of injury: C5- increase in independent hand C6; Time since injury: 16 mo-13 yr; Mean function in relation to ADLs, no follow-up time: 3.5 yr. patient reported hand function was Intervention: Carpal-metacarpal fusion worse after surgery. House et al. 1992 was performed; along with extensor 2. Technique provided a reliable and USA pollicis longus tenodesis and motor reproducible key pinch. Case Series transfer to flexor pollicis longus. 3. All patients had significant N=18 Outcome measures: Function of the improvement in functional ADLs and hand, subjective pain scale, Level of highly satisfied with results of satisfaction with surgery and surgery. rehabilitation, Activities of Daily Living (ADL). Population: Age: 20-47 yr; Gender: 1. Release of the BR and suture to the males=13, females=2; Time since injury: FPL. In 16/17 hands, fixation of the 8 mo-18 yr; Follow-up time: 8-48 mo. IP joint of the thumb was obtained Intervention: Surgery. with a Moberg screw. 11/17 patients Outcome Measures: Pinch strength, lacked active thumb extension had Activities of Daily Living (ADL) reports, tenodesis of the thumb extensors to Brachioradialis (BR), Flexor Pollicis the MCP to prevent excessive Longus (FPL), Flexor Digitorum flexion of the MCP joint. Profundus (FDP), Extensor Capri Radialis 2. FPL and EPB were secured to the Longus (ECRL), Extensor Pollicis Brevis dorsum of the MC. 6/11 patients did (EPB). not require tenodesis had sufficient strength in the FPL to extend the thumb. 3. Two of six EIP was transferred to FPL for active extension. 4. Satisfactory finger flexion present in 10 hands. In seven hands: intertendinous suture of all FDP tendons in four patients who had active flexion in the ulnar profundi of Waters et al., 1985 small and ring finger, but could not USA flex index finger. Case Series 5. Transfer of PT to all FDP tendons in N=15 two patients; transfer of ECRL to all FDP tendons in one patient; transfer of FCU to all FDP tendons in one patient. 6. Preoperative lateral pinch ranged from 0-0.15 lbs, post-operative lateral pinch ranged from 2.2-4 (depending on elbow and wrist position). 7. Residual motor function in triceps (fair plus) (11 patients) and pinch strength; lateral pinch 5.1 lbs, strength fair or less (6patients) 2.0 lbs pinch. 8. 87% (13/15) reported significant improvement; four patients wanted stronger pinch. 9. 80% (12/15) could name four ADL activities that they were able to perform. 10. 13% (2/15) were dissatisfied.

Author Year Country Research Design Methods Outcome Score Total Sample Size 11. 20% (3/15) reported discomfort tip of thumb.

Table 14 Summary of Pinch Studies Author N Intervention Main Outcome(s) Extrinsic reconstruction with Intrinsic +ve grip strength with intrinsic McCarthy et al., Balancing versus without Intrinsic balancing 135 patients 1997 Balancing =ADL and functional use (183 procedures) FDS Lasso versus Intrinsic Tenodesis =grip strength for Intrinsic Balancing =ADL and functional use CMC fusion +ve pinch strength EPL tenodesis +ve ADL and functional use 18 patients House et al., 1992 BR 0r ECRL or ECRI to FPL (21 procedures) As indicated: stabilization of thumb IP joint and Zancolli Lasso procedure +ve lateral pinch strength in all BR to FPL (lateral pinch) with thumb test positions IP joint stabilization (16 hands) +ve ADL functions Waters et al., 1985 15 patients 11 patients also had EPL tenodesis +ve direct correlation between (17 procedures) and EPB to metacarpal joint; 2/17 pinch strength and amount of patients EIP to EPL procedure residual triceps and wrist extensor strength

Conclusion

There is level 4 evidence (from two case series studies; House et al., 1992; Waters et al., 1985) that metacarpal fusion can increase pinch strength as well as improve the over all ability to complete daily living tasks.

There is level 4 evidence (from one pre-post study; McCarthy et al., 1997) that the addition of intrinsic balancing procedures to extrinsic hand reconstruction can improve pinch strength and the ability to perform daily living tasks compared to extrinsic hand reconstruction alone.

Increasing pinch strength and the ability to execute daily living tasks is achieveable through a variety of surgical interventions such as metacarpal fusion or stabilization.

7.1.2 Pinch and Grasp (Key-Pinch and Hook Grip)

The most commonly performed surgeries to obtain key-pinch and hook grip are:

Wrist Extension – If the person does not have adequate wrist extension, Brachioradialis (BR) to Extensor Carpi Radialis Brevis (ECRB) is performed prior to any surgery for pinch reconstruction.

Key-Pinch and Hook Grip – Extensor Carpi Radialis Longus (ECRL) to Flexor Digitorum Profundus (FDP). This is a synergistic transfer in which dorsiflexion of the wrist potentiates the effects of the transfer. The amplitude of excursion provides strong flexion of the fingers into the palm. Brachioradialis (BR) is also transferred to Flexor Pollicis Longus (FPL).

The aim of these transfers is to provide mass finger flexion for grasp and independent thumb flexion for key-pinch against the side of the middle phalanx of the index finger. Adjustment of tension in these transfers is also completed (Lamb & Chan 1983).

Table 15 Reconstructive Surgery: Pinch and Grip Studies Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 20-62 yr; Level of 1. Strength: key-pinch strength injury: C4-C7; Time since injury: 15-239 average of 17.2 kPa (5-50 kPa); mo. grasp strength average 18.8 kPa (3- Intervention: Surgical reconstruction. 45 kPa). Forner-Cordero et al., Outcome Measures: Increased hand 2. No relation found between the ADL 2003 movement and strength, Activities of test and the key pinch strength Spain Daily Living (ADL), Patient's satisfaction, (p=0.7976) or grasp strength Retrospective Follow-up Fulfillment of patient's expectations, (p=0.6948). NInitial=15; NFinal=14 Surgical complications. 3. Modification of ADL questionnaire; excellent (3) 21.4%; good (7) 50.0%; fair (2) 14.3 %; poor (2) 14.3%. Scores ranged from 54-122 points. Population: Age: 21-57 yr; Gender: 1. Operative interventions on the males=21, females=3; Time since injury: tetraplegic hand brings gains in Meiners et al., 2002 9-59 mo. cylindrical and lateral grip and Germany Methodology: Surgery. improvement in ADL. Case Series Outcome Measures: Activities of Daily 2. Subjective acceptance is high. NInitial=24; NFinal=22 Living (ADL) questionnaire, Satisfaction 3. Complication rate is high. Survey, Key grip, Lateral force grip. 4. Long duration of treatment. Population: Level of injury: C5-6; Time 1. All reported they would have surgery since injury: ≥1 yr. again. Intervention: Surgery. 2. Key pinch strength in non-op limbs Lo et al., 1998 Outcome Measures: Not specified. was 1.0±1.3 kg, in surgically treated Canada arms it was 1.2±1.1 kg. Case Series 3. Minnesota rate of manipulation: non- N=9 operative limbs were 1.50±0.25 sec, post-operative limbs was 2 min 56 secs±1 min 56 sec. Population: Age: 9-58 yr; Level of injury: 1. No statistical results reported-eight tetraplegia. patients interviewed, five completed Intervention: Surgery. questionnaires. Failla et al., 1990 Outcome Measures: Key pinch, Grip 2. Conclusion-transfer of USA strength, Activities of Daily Living (ADL). brachioradialis tendon provides key Case Series pinch and grip of sufficient quality to N=8 improve the ADLs in patients with loss of flexion of the thumb and fingers. Gansel et al., 1990 Population: Age: 20-47 yr. 1. No statistical analysis reported USA Intervention: Surgery. 2. Passive range of motion (ROM) of the Case Series Outcome Measures: Not specified. elbow and wrist remained unchanged N=19 post-surgery. Functional active flexion

Author Year Country Research Design Methods Outcome Score Total Sample Size of the fingers was gained in 10/11 subjects. 3. Improved performance of Activities of Daily Living (ADL) was reported. Rieser & Waters 1986 Population: Mean age: 23.6 yr; Mean 1. Self-assessment questionnaire USA time since injury: 6.2 yr. results indicated: power decreased Case Series Intervention: Surgery. since surgery in all patients. N=23 Outcome Measures: Not specified. Population: Age: 19-60 yr; Gender: 1. Seven extremities had had post males=17, females=7; Level of injury: deltoid to triceps transfer before group III=3(normal shoulder control, opponensplasty; 24 patients, 11 elbow flexion, radial wrist extensors), (46%) had bilateral opponensplasty. group IV=11 (same as group III with 2. Thirty-five opponensplasties were functioning FCR, PT & triceps, weak done. 22 flexor tendon transfers fingers), group V=7 (intrinsic hand muscle were done for voluntary grasp and paralysis), group VI=4 (incomplete then opponensplasty. paralysis); Time since injury: 1-17 yr; 3. Fourteen patients (22 extremities) Follow-up time: 1-17 yr. evaluated. Intervention: Surgery. 4. Subjects reported that they would Outcome Measures: Not specified. have the operation again (95% of the extremities) and had improved Kelly et al., 1985 function (91%). USA 5. One patient reported that function Case Series was unchanged; one was N=24 dissatisfied. Overall value of key pinch 35 extremities was 1.47±1.29 kg (mean± SD). 6. Grasp measured in 20 extremities; 2.81±2.89 kg (mean±SD) (range trace to 10kg). 7. Palmar pinch; 9 of 20 extremities (45%) achieved palmar pinch (1.04±1.02 kg; mean±SD) (range 0.20-3.0 kg). Palmar pinch achieved in 17% of the extremities in group III, 71% in group IV, and 33% in group V. Population: Age: 16-36 yr; Time since 1. 6/8 subjects were evaluated. injury: 4 mo-18 yr. Subjects indicated they were Colyer & Kappelman Intervention: Surgery. pleased with the surgery. 1981 Outcome measures: Not specified. 2. Hand function tests indicated an USA improvement (16-49% Case Series improvement). N=8 3. 5/6 subjects showed key grip strength remained constant. Population: Mean Age: 38.8 yr; Gender: 1. The patients’ responses revealed males=10, females=1; Level of Injury: three phases of recovery; initiating C4=1, C5=2, C6=6, C7=1, Unspecified=1. activity training, establishing hand Intervention: Patients who underwent control in daily life, and challenging Wangdell et al. 2014 hand surgery between February 2009 to dependence. Sweden March 2011 participated in an interview in 2. During phase one, patients reported Observational order to discuss the individual experiencing mood swings (both N=11 experiences of regained hand control positive and negative) such as after grip reconstruction. Interviews were fascination, eagerness and fear, conducted at 12 mo post-surgery at the encouragement from rehabilitation patients’ home clinic. A grounded theory staff, and practicing their hand control in real life situations with beneficial

Author Year Country Research Design Methods Outcome Score Total Sample Size approach was adopted for analyzing the results keeping them motivated. interviews. Patients transitioned into phase 2 Outcome Measures: Qualitative after gaining confidence and belief in analysis, Patient interviews. trying new activities. 3. At phase 2, establishing hand control in daily life, patients reported diverse learning strategies with some patients using trial and error whilst others planned their activities ahead of time but patients consistently approached one task at a time. Patients also reported that new abilities and tasks required time and effort. 4. External factors in phase 2 were also reported that home environments for practicing activities was more beneficial than a clinic and that positive feedback maintained high motivation levels. A theme emerged in that patients transitioned to phase 3 after developing confidence and self-efficacy in hand control. 5. At phase 3, patients reported the use of celebrations to promote motivation and self-affirmation, changing habits and roles to improve awareness, trusting and using their new skills to become more independent, adapting their physical environment to accommodate their new skills, and that social peers had to allow the patients to use their new skills. 6. After phase 3, a theme emerged of higher independence with patients stating several examples of autonomy. Population: Mean Age: 38.8 yr; Gender: 1. The patients’ responses revealed males=10, females=1; Level of Injury: three key areas that enhanced C4=1, C5=2, C6=6, C7=1, Unspecified=1. recovery; physical, psychological, Intervention: Patients who underwent and self-efficacy. hand surgery between February 2009 to 2. Self-efficacy was considered an March 2011 participated in an interview in important element in developing order to discuss the individual independence, especially when experiences of regained hand control gripping and grasping objects. Self- Wangdell et al. 2013 after grip reconstruction. Interviews were efficacy was also revealed to be a Sweden conducted at least 7-17 mo post-surgery. motivator for further improvements Observational Outcome Measures: Qualitative and learning new skills. N=11 analysis, Patient interviews. 3. Ability to perform more activities such as making food, picking up objects, opening/closing doors were among the practical aspects that enhanced independence. Participating in social activities (e.g. eating at a restaurant, sports/games, shopping), increasing levels of activity and decreasing dependence on assistance, and

Author Year Country Research Design Methods Outcome Score Total Sample Size being less restricted by physical environments (i.e. improvising in environments not suited to their needs) were common themes for increasing independence. 4. Psychological aspects that enhanced independence post-surgery included being able to regain privacy and perform self-care tasks alone, and developing a sense of manageability in controlling their own actions which both increased feelings of self- esteem and a decrease in “psychologically bad days”. Further patients reported a sense of identity and a sense of equality (e.g.at work, as a caregiver to children, etc).

Table 16 Summary Pinch and Grip Studies Author N Intervention Main Outcome(s) 15 patients PD to Triceps +ve key-pinch strength (20 limbs) BR to ECRB +ve grip strength Tenodesis of FPL =ADL and functional use APL to CMC joint or arthrodesis of +ve patient satisfaction Forner-Cordero et CMC joint -ve patient expectation al., 2003 BR or ECRL or PT to EDC and EPL or tenodesis of extensor tendons BR or ECRL or ECRB to FPL PT or ECRL or BR to FDP 22 patients FCR to FDP +ve lateral and cylindrical (23 hands) ECRL to FDP grip Meiners et al., 2002 +ve satisfaction with surgery +ve ADL and functional use 8 patients ERCL to FDP and BR to FPL +ve satisfaction with surgery (12 procedures) +ve key-pinch and grip Lo et al., 1998 strength +ve ADL functional use 8 patients BR to FDP or FPL +ve key-pinch and grip Failla et al., 1990 (9 hands) BR or ECRL to FPL strength +ve ADL and functional use 11 patients 11/11 PT to FDP +ve finger flexion Gansel et al., 1990 10/11 BR to FPL +ve key-pinch strength 1/11 BR to FDS +ve ADL functional use 9 patients Tenodesis of FPL, thumb IP joint -ve result, bowstringing of (10 procedures) stabilization FPL across MP joint Rieser & Waters 6/9 MP joint tenodesis of extensor -ve grasp and lateral pinch 1986 tendons of thumb strength 2/9 BR to wrist extensor 7/9 tenodesis of EPL and EPB 24 patients 7/24 also had PD to Triceps +ve satisfaction with surgery (57 procedures) Opponensplasty- FDS to APB Flexor +ve ADL functional use tendon transfers: BR (also used PT, +ve key-pinch, palmar pinch Kelly et al., 1985 FCR, ECRL, FCU, PL) to FDP; 22/35 and grip strength Flexor tendon transfer BR to FDP (also used PT, FCR, ECRL)

Author N Intervention Main Outcome(s) 6 patients FPL tenodesis +ve improved pinch strength Colyer & (8 hands) 2 also had ECRL to FDP -ve finger flexion Kappleman 1981 +ve ADL and functional use

Conclusion

There is level 3 evidence (from one retrospectrive study; Forner-Cordero et al., 2003) that the outcomes of pinch and grasp reconstructive surgeries overall improve the individuals’ hand function and meet individual expectations.

Hand reconstructive surgery includes a variety of diverse proceedures that allows patients to have improved hand function which results in generally high satisfaction rates with surgical outcomes.

7.2 Elbow Extension 7.2.1 Posterior Deltoid to Triceps

The most commonly performed surgery for elbow extension is using the posterior third of the deltoid (PD) to motor the triceps. This converts the transferred portion of the deltoid into a two-joint muscle but causes no functional loss at the shoulder (Moberg 1975).

Table 17 Reconstructive Surgery – Elbow Extension Studies (Posterior Deltoid to Triceps) Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Mean age: 27 yr; Gender: 1. Straight Arm Raising-statistically males=11, females=5. significant decrease in maximal Intervention: Surgery. Control group shoulder abduction (mean 57 SEM members sat on a chair, while those with 12 before, 14 SEM 6 after surgery). tetraplegia sat in a wheelchair. All were 2. Shoulder flexion increased after Remy-Neris et al., 2003 asked to perform two movements; a deltoid-to-triceps transfer by 42% France straight arm lateral and maximal raising (mean 113 SEM 11), remained Pre-post and return. significantly lower (121 SEM 12) N=16 Outcome Measures: Straight Arm than control group (p<0.0001). Raising, Hand-to-nape-of-neck 3. Hand-to-nape-of-neck-movement-no movement. significant improvements were noted after surgery. 4. Peaks of shoulder and elbow flexion speed are almost normal, indicating

Author Year Country Research Design Methods Outcome Score Total Sample Size the importance of restoring elbow extension torque for improving the whole kinematic picture of the upper limb. Population: Age: 23-38 yr; Time since 1. Both groups scored identically on injury: 5-16 yr. the FIM. Dunkerley et al., 2000 Intervention: Surgery. 2. No significant differences in mobility UK Outcome Measures: Questionnaire, were noted (p=0.256, and p=0.432). Case-Control Functional independence measure (FIM), Questionnaire was answered only NInitial=15; NFinal=11 10m push, Figure of 8 push. by the treatment group; clients gave positive response to the questions. Population: Mean age: 33.6 yr; Level of 1. The muscle was tested at six injury: C6; Time since injury: 28-173 mo. different lengths (130º, 110º, 90º, Intervention: The arm and forearm were 70º, 45º and 0º of elbow flexion) with locked in position and a force transducer the shoulder abducted at 90. was used to assess the torque output 2. When compared, the absolute isometrically. The muscle was tested at 6 values (dimension of torque) were different lengths with the shoulder significantly different between abducted at 900. groups (0.000010.1). Post-Test of Injury: AIS A=3, AIS B=1, AIS C=1. 2. For % of type 3 sub-movements, N=10 Control group (n=5): Mean age: 38±7 yr; there was a significant for direction Gender: males=5, females=0. (p<0.05), indicating that both groups

Author Year Country Research Design Methods Outcome Score Total Sample Size Intervention: Aiming movements were made more type 3 sub-movement performed in two directions (20 cm away corrections when aiming away than or toward), with or without vision with a toward the body. ball transfer unit by both SCI patients and 3. A significant effect was shown in age-matched neurotypical controls. Trials direction for movement time (p<0.05) that contained a sub-movement phase and a condition × direction × group (i.e., discontinuity in velocity, acceleration interaction for both movement time or jerk) were identified. (p<0.01) and peak velocity (p<0.05). Outcome Measures: Kinematic 4. Peak acceleration indicated variables, Frequency and distribution significance for group and direction (velocity, acceleration or jerk (p<0.02). discontinuity), Amplitude and duration of 5. Primary movement amplitude was sub-movements. greater when aiming away from than toward the body (p<0.05); this difference was somewhat larger in the vision than no vision condition (p<0.05). 6. Amplitude revealed significance of group, with tetraplegics making larger corrections than controls (p<0.05). 7. No significant for duration of corrective sub-movements between groups (p=0.08). 8. Magnitude of spatial variability at peak velocity in sub-movement trials showed significance in group (p<0.05) as well as condition x direction x group interaction (p<0.05). 9. Both groups made a greater percentage of functional than non- functional corrections when aiming toward, irrespective of vision (p<0.01).

Table 18 Summary Elbow Extension (Posterior Deltoid to Triceps) Author N Intervention Main Outcome(s) 5 pt PD to triceps + ve straight arm raise Remy-Neris et al., 2003 17 limbs +ve speed of movement 5 elbows, 6 PD to triceps =surgical/control gr: FIM (adapted) 13 controls items =surgical/control gr: W/C propulsion Dunkerley 2000 8m&10 m push +ve elbow function indicated on questionnaire Gr 1- 8 pt PD to triceps Initial tension pt transfer at time of 11 elbows surgery is important for torque output Rabischong et al., 1993 Gr 2-control 9 R + ve ADL and functional use hand (female) 10 pt PD to triceps +ve satisfaction with surgery Lacey et al., 1986 16 procedures +ve ADL and functional use 18 pt PD to triceps +ve elbow extension strength Raczka et al., 1984 19 transfers +ve ADL and functional use = submovement % Robinson +ve amplitude for paraplegic +ve functional corrections

Conclusion

There is level 2 evidence (from one prospective control trial; Rabischong et al., 1993) that surgery can increase rotation in the elbow and the relationship with peak torque.

There is level 3 evidence (from one case-control; Dunkerley et al., 2000) that PD to triceps surgical intervention can have limited/similar results to controls when examining functional outcome.

There is level 4 evidence (from two case series; Lacey et al., 1986 and Raczka et al., 1984) that PD to tricep surgery can have a positive effect on functional use as well as result in positive patient satisfaction with surgery.

There is level 4 evidence (from one pre-post study; Remy-Neris et al., 2003) that restoring elbow extension is important for over all upper limb kinematics, however surgical interventions can have limited results.

PD to tricep surgery generally leads to positive satisfaction with surgical outcomes, improves motor function, and the ability to perform daily living tasks.

7.2.2 Biceps to Triceps A biceps to triceps transfer can be used to create elbow extension in patients who have active supinator and brachialis muscles to provide for the lost functions of the transferred biceps (Kuz et al., 1999).

Table 19 Reconstructive Surgery – Elbow Extension Studies (Biceps to Triceps Transfer) Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Gender: males=7, 1. After surgery, elbow extension females=2; Level of injury: tetraplegic; muscle strength was improved in ICSHT: 0-4; Tendon transfer for elbow bicep and deltoid groups (p<0.001). extension: deltoids n=8, biceps n=8. 2. No significant increase in elbow Intervention: Surgery. extension muscle strength was Outcome Measures: Muscle strength, found following surgery. Mulcahey et al., 2003 Flexion torque, Modified University of 3. Seven of eight bicep-to-triceps USA Minnesota Tendon Transfer Functional procedures had clinical RCT Improvement Questionnaire, Canadian improvements in antigravity muscle PEDro=6 Occupational Performance Measure strength, in comparison with one of N=9 (COPM), eight deltoid transfers completed. Activities of Daily Living (ADL). 4. No significant difference between the groups was found for elbow flexion torque (47% reduction in torque after two yr versus baseline). 5. Following surgery, 48/63 elbow extension ADL did not improve in

Author Year Country Research Design Methods Outcome Score Total Sample Size subjects and there was no alteration in the remaining 15/63. 6. Performance and satisfaction with personal goals improved post- surgery as well.

Population: Mean age: 17.3 yr; Level of 1. Manual muscle testing for elbow injury: C5=10, C6=29, C7=1. extension revealed a statistically Intervention: Surgery for a biceps to significant increase in preoperative to triceps tendon transfer (36 left, 32 right). postoperative muscle strength Outcome Measures: Manual muscle (p<0.001). testing, Canadian Occupational 2. 42/68 arms able to extend completely Performance Measure (COPM). against gravity (manual muscle testing 3/5 or greater). 3. 9/68 arms had mild extension lag against gravity (manual muscle Kozin et al., 2010 testing of 3/5). USA 4. 75% (51/68) arms were able to Case Series function overhead. NInitial=45; NFinal=40 5. 17/68 arms were less than 3/5 (lack of strength attributed to a postoperative complication). 6. Improvement in one goal on the COPM was observed by each patient. 7. COPM total mean score statistically increased from 2.6 to 5.6 and from 1.8 to 5.7 for performance (p<0.001) and satisfaction (p<0.001), respectively. Population: Level of injury: tetraplegia. 1. No statistical results reported. Intervention: Surgery. 2. Subjects indicated they were Kuz et al., 1999 Outcome Measures: Not specified. satisfied with the surgery. USA 3. Activities that required precision Case Series hand placement had improved. N=3 4. Elimination of the need for some adaptive aids was possible post- surgery.

Table 20 Summary Reconstructive Surgery - Elbow Extension Studies (Biceps to Triceps Transfer) Author N Intervention Main Outcome 40 patients Biceps to Triceps +ve elbow extension strength 36 left; 32 +ve reaching overhead right elbow Improvement in one goal on Canadian Kozin et al., 2010 surgeries Occupational Performance Measure (COPM) for each patient Statistically significant improvement in performance and satisfaction scores on COPM 9 patients Biceps to Triceps +ve elbow extension from either surgery Mulcahey et al., 2003 16 elbows

Posterior Deltoid to +ve improvement in ADL skill (both Triceps surgeries) +ve antigravity strength (biceps to triceps > posterior deltoid to triceps) 3 patients Biceps to Triceps +ve elbow extension 4 elbows +ve functional improvements through Kuz et al., 1999 ability to place the hand in space +ve satisfaction with surgery

Conclusion

There is level 2 evidence (from one RCT; Mulcahey et al., 2003) that biceps to triceps surgery can increase elbow extension strength, reaching, and overall performance improvement.

There is level 4 evidence (from two case series; Kozin et al., 2010; Kuz et al., 1999) that elbow extension surgery improves elbow extension and overall functionality of the joint.

Elbow extension surgery has strong positive outcomes and should be considered as a viable option for those with limited extension which impacts daily living.

7.3 Multiple Reconstructions The following studies report results from multiple procedures to reconstruct the upper limb.

Table 21 Reconstructive Surgery – Multiple Reconstructions Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age range: 19-70 yr; Type of 1. Active thumb-index opening SCI: traumatic=12, non-traumatic=3; increased significantly from 2.5 (SEM Level of injury: tetraplegia=15, 1.0) cm before surgery to 9.0 (SEM paraplegia=0; Mean time since injury: 0.8) cm after surgery. 54.2±42.8 mo; International classification 2. Nine patients without previous active of patients’ upper extremities: OCu4- opening of the first web space OCu8. recovered a mean thumb-index Intervention: All patients had their opening of 9.1 (SEM 1.7) cm; this Friden et al., 2012a extensor digiti minimi (EDM) tendon distance increased an average of 2.9 Sweden transferred to the abductor pollicis brevis (SEM 0.8) cm in six patients who had Pre-post (APB) through the interosseous active thumb-index distance of 6.3 N=15 membrane, in addition to ≥3.2 procedures (SEM 1.6 cm) before surgery. to restore key pinch. 3. 14/15 patients were able to direct and Outcome Measures: Maximum distance coordinate key pinch and perform between the thumb and index finger tips tasks using restored APB function during active or passive opening of the including five patients whose EDM hand, Maximum angle of palmar strength was rated as grade 3 before abduction, grip and key pinch strength, the transfer. Active finger range of motion (ROM).

Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Treatment group (n=6): 9. Post-operative active pronation was Mean age: 32.2±4.9 yr; Gender: males=4, significantly greater in the dorsal females=2. transfer group in comparison to the Control group (n=6): Mean age: 31.2±5.0 palmar group (149±6° and 75±3°, yr; Gender: males=4, females=2. respectively). Friden et al., 2012b Intervention: Individuals in the treatment 10. Pinch strength was similar between Sweden group had a brachioradialis (BR) to Flexor both groups (1.28±0.16 kg and Case Control pollicis longus (FPL) transfer dorsal to 1.20±0.21 kg), respectively. N=12 radius through the interosseous 11. It is feasible to reconstruct lateral key membrane whereas the control group pinch and forearm pronation received traditional palmar BR to FPL. simultaneously using only the BR Outcome Measures: Lateral key pinch, muscle. Pronation range of motion (ROM). Population: Mean age: 42.9 yr; Mean 1. Elbow Extension: bilateral surgery time since injury: 20.5 yr; Mean time since 9/11 subjects; Hook Grip; 17 right surgery: 15.1 yr; Handedness: right=22, hands (av. Grip 46.2 mm Hg in left=24; Level of Injury: 01: 6 hands; 02: t3 1991; improved slightly, not hands; 03: 5 hands; 0Cu2: 2 hands; statistical significant (p=0.30)) Left 0Cu3: 6 hands; 0Cu4: 17 hands; 0Cu5: 8 hand: 15 hands: significant increase hands; 0Cu6: 1 hand; tetraplegia. (p<0.001), av. 28.7 mmHg to 53.2 Intervention: Surgery. mmHg; no statistical significance Outcome Measures: Lamb and Chan between right and left hook grip as questionnaire with additional 10 Burwood measured by SGM and DA in 2001 questions, Swanson sphygmomanometer (p=0.93 and p=0.97). (SGM) (hook grip), Preston Pinch Meter 2. Key Pinch: av. key pinch 20 right (key pinch), Quadriplegic index of thumbs in 1991 25.8 N and Function (QIF), Digital Analyzer (DA) (key decreased in time to av. 13.9 N and grip pinch). (significant decrease p<0.001); average pinch strength 18 left thumbs decreased from 17.7-8.8 N (significant decrease p<0.001). Average pinch strength measured by DA, increase in key pinch when Rothwell et al., 2003 compared to 1991, significant for New Zealand both right (p=0.01) and left (p=0.01) Case Series thumbs. NInitial=29; NFinal=24 3. Active Transfer versus Tenodeses: hook grip: active transfers 2x strength of tenodeses in 1991 (p=0.05) and 2001 (p=0.03). Pinch grip: similar to 1991 data (p<0.001), 2001 data does not follow trend. 2001 DA data did not reach significance (p=0.06). 4. Longitudinal Comparison: hook grip strength 25 hands with active transfers significant increase 42.1- 60.2 mm Hg (p<0.001) and pinch grip increase from 24.0-38.4 N in 31 thumbs that had active transfers using 2001 DA data (p=0.03). Hook strength obtained from a tenodesis in seven hands did not weaken over time (p=0.05) but pinch strength in 7 thumbs significantly increased (p<0.001) using 2001 DA data.

Author Year Country Research Design Methods Outcome Score Total Sample Size 5. Questionnaire results; Lamb and Chan activity measure: showed perceived improvement of functional activities significantly lower in 2001 (p<0.001). QIF scores of current functional independence was significantly better (p=0.004). 6. Additional Burwood questionnaire showed levels of satisfaction, perceived expectation, gratification and opportunity enhancement were maintained over time (p=0.281). Population: Mean age: 37 yr; Level of 1. No statistical analysis provided- injury: C5-C8; Time since injury: 7-356 gestural ability improved in more mo. than 80% of the patients and Intervention: Upper limb surgery. functional gain was important in Welraeds et al., 2003 Outcome measures: Functional testing. more than half. Belgium 2. 43 procedures; Atypical procedures Case Series (2) good: 2; Moberg procedures (18) N=25 good: 17; poor: 1; Deltoid/triceps (12) good: 7; fair 3; poor 2; Additional procedures (11) good: 7; fair: 3; poor: 1. Population: Level of injury: C5-C8. 1. Oponens transfers were done 180 Intervention: Surgical reconstruction. times; transfers for finger flexion-161 Freehafer 1998 Outcome Measures: Not specified. times; posterior deltoid transfers-59 USA times; transfers for wrist extension- Case Series 17 times. N=285 2. 13 out of 285 stated that they were no better, and no patient said they were worse. Population: Mean age: 27 yr; Gender: 1. Subjective Assessment: obtained for males=51, females=6; Level of Injury: 86% of the patients, av. Follow up of 00:4; 01: 6; 02: 4; 03: 6; 0X: 3; Cu3: 6; Cu 37 mo (range 5-86 mo); 70% 4: 24; Cu 5: 10; Cu 6: 3; Cu X: 3; reported good or excellent results; tetraplegia. 22% fair; 8% poor. Intervention: Surgery. 2. Simultaneous surgery for key-grip Outcome Measures: Activities of Daily and hook grip strength: 96% good or Mohammed et al., 1992 Living (ADL), Preston Pinch Meter, Hook- excellent results. New Zealand grip strength, Elbow extension. 3. Objective Results: over 70% of Case Series patients, av. follow up of 32 mo; Key N=57 Pinch 52/68 cases (76%); av. strength was 2.1 kg. Hook grip measured in 42/58 cases (72%), thumb included av. strength was 42 mmHg; thumb excluded 29 mmHg. 4. Elbow extension measured in 71% of patients, obtained grade 3 or 4 strength. Population: Age: 26-70 yr; Gender: 1. Elbow Extension: 30 elbows in 23 males=36, females=7; Level of Injury: 0:1 patients; (23/30 with free tendon Ejeskar & Dahllof 1988 9 pts; 0:2 2 pts; 0Cu:1 4 pts; 0Cu:2 13 graft;7/30 Castro-Sierra and Lopez- Sweden pts; 0Cu:3 9 pts; 0Cu:4 5 pts; 0Cu:6 1 pt. Pita method); 5/23 with free tendon Case Series Re-examined 1-14 yr after the last graft 1/23 full ext.; 8/23 lack ext. N=43 operation. against gravity of max. 60; 10/23 Intervention: Surgery. lack even more ext.; 6/7 ext. deficit greater than 60.

Author Year Country Research Design Methods Outcome Score Total Sample Size Outcome Measures: Activities of Daily 2. Key Grip: 50 hands/40 patients; Living (ADL), Elbow extension, Key grip Strength 0-3.5 kg (av. 0.7 kg); 15 pinch, Finger flexion. cases had minimum of 1.0 kg. 3. Finger Flexion: 14 hand/13 patients (ECRL to profundi II-V); grip 0-0.27 kP (av. 0.13 kP); 5/14 minimum strength 1.0 kg. 4. Four patients reported no improvement (1 severe spasticity, 2 BR muscle transferred to wrist; 1 operation on weaker hand); 4/43 could not state how much they had improved, 35/43 average improved capacity to perform 23/55 ADL tasks; 3/43 patients a functional deterioration. Population: Age: 15-61 yr; Level of 1. 142 transfers were performed on 68 injury: tetraplegia; Time since injury: 1-17 subjects. Freehafer et al., 1984 yr. 2. No upper limbs were made worse. USA Intervention: Surgical reconstruction. 3. Four remained unimproved, all Case Series Outcome Measures: Comparison of the others that had tendon transfers N=68 post-surgical with the pre-surgical improved. condition. Population: Mean age: 29 yr; Gender: 1. Elbow Function: 10/16 elbows (10 males=38, females=3; Level of injury: patients): full extension; 2/16 elbows tetraplegia; Severity of injury: complete. 20-degree flexion contracture; 4/16 Intervention: Surgery. 15 degrees of extension lag. All 10 Outcome Measures: Elbow strength, patients considered the procedure Hand function (assessment checklist beneficial. developed), Activities of daily living (ADL). 2. Hand Function: 48 hands (assessed only 27 patients). 5 rated as excellent; 28 rated good; 11 rated as fair; 4 graded as poor. No patient had any impairment of hand function after operation. Lamb & Chan 1983 3. ADL: 29 patients assessed. No one UK considered their functional capability Case Series deteriorated after operation. Most N=41 significant improvement in basic activities such as washing, eating and using the toilet, hold glasses and cups, wash limbs and brush hair, turn on taps, improve bladder compression, insertion of suppositories, change from complete reliance on other for self- care, more mobile, 7 able to drive a car. Improvement in UL function facilitated development of personal interests. Population: Level of injury: OCu 1,2,3. 1. No statistically significant findings Intervention: Reconstruction of key grip reported. Hentz et al., 1983 and active elbow extension. 2. Subjective client reports. USA Outcome Measures: Interview and/or Case Series questionnaire (self-care, communication, NInitial=30; NFinal=23 mobility), Objective measurements - pre + post op strength, Range of motion (ROM)

Author Year Country Research Design Methods Outcome Score Total Sample Size of wrist + elbow extension, Strength of key pinch, Range of passive wrist flexion + functional testing. Population: Median Age: 48 yr; Gender: 1. The mean percentage for positive males=33, females=7; Level of Injury: responses (strongly agree/agree) C4=7, C5=14, C6=12, C7=6, C8=1; was 76% for general satisfaction and Severity of Injury: AIS A=25, AIS B=9, AIS 84% for life impact. C=3, AIS D=3. 2. Appearance of the patients’ hand(s) Intervention: Patients completed a was scored relatively lower with only questionnaire on general satisfaction, 28% reporting an improvement in independence, activities of daily living appearance post-surgery and 49% (ADL), appearance, reliability of the were unsatisfied. surgery, postoperative therapy, and life 3. Positive responses were reported in impact since undergoing upper extremity 73% of patients for improvements in surgery post-SCI. Patients were also ADL with 85% reporting that ADL had asked to write a list of activities that they become easier and 58% reporting performed better/worse and if they that activities could be performed needed fewer aids post-surgery. A total of faster after surgery. Gregersen et al. 2015 102 surgical procedures had been 4. Patients who had received surgery Denmark performed including pinch/thumb between the yr 1991-2008 reported Post Test stabilization (n=46), elbow extension greater levels of general satisfaction N=40 posterior deltoid to triceps (n=20), hand and ADL than patients who had grasp/finger flexion (n=14), wrist received surgery between the yr extension (n=7), Zancolli (n=7), freehand 1973-1990 (both p<0.001). (n=3), and miscellaneous (n=5). 5. When comparing patients who had Assessments were conducted at post- elbow extension or pinch/thumb treatment. surgery as the only procedure, Outcome Measures: Custom satisfaction patients who had received elbow survey. extension surgery reported significantly greater levels of satisfaction regarding ADL (p=0.027) and independence (p<0.001). 6. Patients reported that eat and drinking, grasping and coordination, dressing/undressing, stretching, and using tools were easier after surgery. Population: Mean Age: 53 yr; Gender: 1. Only patients who had undergone a males=18, females=1; Level of Injury: left-side tenodesis reported a C5=3, C6=9, C7=7. significant improvement in key pinch Intervention: Patients who had received strength (p=0.04) from the previous tendon transfers between 1982-1991 follow-up (2001) to current follow-up were followed up as part of a longitudinal (2012). study. Surgical procedures included 2. No significant differences were brachioradialis (BR) to flexor pollicis reported between patients who had Dunn et al. 2014 longus (FPL; n=27, 31%), extensor carpi undergone active transfer or New Zealand radialis longus (ECRL) to flexor digitorum tenodesis at current follow-up. Cohort profundus (FDP; n=20, 23%), elbow 3. The active transfer patients declined N=19 extension (n=18, 21%), BR to FDP (n=7, by 8% (left side) and 5% (right side), 8%), FPL tenodesis (n=6, 7%), pronator but left and right side tenodesis grip teres (PT) to FPL (n=4, 5%), and FDP strength increased by 70% and 32%, tenodesis (n=4, 5%). Assessments were respectively (both p<0.05) from conducted 11yr after previous follow-up. previous follow-up to current follow- Outcome Measures: Lamb & Chan up. questionnaire (LCQ), Key pinch strength, 4. Although the majority of the items on Grip strength, Type of wheelchair used. the LCQ were unchanged from the previous follow-up to current follow-

Author Year Country Research Design Methods Outcome Score Total Sample Size up, three items were found to have worsened with 10 patients reporting a decline in their ability to propel their wheelchair up and down a slope, and the ability to propel their wheelchair on a level surface. 5. Further, 7 patients reported a decline in the ability to raise themselves from their seat on the LCQ. Population: Mean Age: 49 yr; Gender: 1. Key pinch strength had improved males=4, females=7; Injury etiology: significantly with means increasing Thrombosis=3, Spinal haemorrhage=2, from 0kg at pre-treatment to 1.6kg at Tumour=2, Syringomyelia=1, Guillain- 12m post treatment (p<0.05). Barre Syndrome=1, Unspecified=2. 2. Grip strength had improved Intervention: Data was collected and significantly with means increasing analysed from patient records who had from 0kg at pre-treatment to 3.2kg at completed evaluations prior to and after 12m post treatment (p<0.05). tendon transfer surgery. Surgical 3. Maximal distance between the thumb procedures included active key pinch by and index finger had improved brachioradialis-to-flexor pollicis longus significantly with means increasing (FPL) transfer (n=10), distal thumb from 2.1cm at pre-treatment to 6.4cm Friden et al. 2014 tenodesis (n=10), extensor carpi radialis at 12m post treatment (p<0.05). Sweden longus-to-flexor digitorum profundus 2-4 4. Anti-gravity elbow extension was Case Series transfer (n=8), intrinsic balancing using restored in one patient. N=11 either House or Zancolli plasty (n=6), activation of thumb abduction by extensor digiti minimi-to-abductor pollicis brevis transfer in (n=3), carpometacarpal joint of thumb, arthrodesis (n=3), posterior deltoid-to-triceps transfer (n=1), passive key pinch by FPL tenodesis to the radius (n=1). Assessments were conducted at pre-treatment and at 12 mo post treatment. Outcome Measures: Key pinch strength, Grip strength, Maximal distance between the thumb and index finger, Anti-gravity elbow extension.

Table 22 Summary Multiple Reconstructions Author N Intervention Main Outcome(s) Friden et al., 2012a 15 patients EDM to APB +ve key-pinch and grip strength Friden et al., 2012b 12 patients BR to FPL +ve pinch strength BR to FPL or BR and +ve key-pinch and hook grip 24 patients tenodesis FPL +ve ADL and functional use Rothwell et al., 2003 (48 reconstructions) ECRL to FDP PD to Triceps PD to Triceps +ve elbow extension 25 patients Welraeds et al., 2003 ECRL to FDS +ve key grip and grasp (43 procedures) BR to FDS +ve ADL and functional use Opponens transfer: 180 Review of surgical procedures and 285 patients times recommendations. Freehafer 1998 (417 transfers) Transfers to finger flexors: 161 times

Author N Intervention Main Outcome(s) PD to Triceps: 59 times Transfers for wrist extension: 17 times PD to Triceps + hook grip strength Key-Pinch: BR or PT to +ve ADL and functional use 57 patients ECRL; FPL tenodesis Mohammed et al., 1992 (97 transfers) and IP stabilization Hook Grip: BR or ECRL to FDP PD to Triceps -ve elbow extension 43 patients Tenodesis FPL, thumb +ve key-grip and finger flexion Ejeskar & Dahllof 1988 (94 transfers) IP joint stabilization +ve ADL and functional use ECRL to Profundus iv Variation of all +ve key-pinch and grip strength 68 patients Freehafer et al., 1984 procedures +ve elbow extension (142 transfers) +ve ADL and functional use PD to Triceps +ve elbow extension and function Biceps to Triceps -ve elbow extension (biceps to Hand Grip: ECRL to triceps) FDP +ve hook grip and key pinch and BR to FPL ADL and functional use 41 patients Key-Pinch: FPL Lamb & Chan 1983 (57 reconstructions) tenodesis or FPL tenodesis plus ECRL to FDP Other: EPB to ECU, FCR to FDS, APB to EDM PD to Triceps or Biceps +ve satisfaction with surgery to Triceps +ve pinch and grip strength 30 patients Hentz et al., 1983 FPL tenodesis (40 limbs) BR to ECRB EPL and EPB tenodesis Pinch/Thumb +ve satisfaction with surgery stabilzatoin +ve life impact 40 patients Deltoid to tricep +ve ability for perform ADL Gregersen et al., 2015 (102 procedures) Hand grasp Wrist extension Freehand BR to FPL +ve improvement in pinch strength ECRL to FDP for left sided tenodesis BR to FDP = outcome for active transfer vs FPL tenodesis 19 patients FDP -ve decline for active transfer Dunn et al., 2014 (89 procedures) patients +ve increase in grip strength for tenodesis -ve decline for functionality and use of wheelchair FPL transfer +ve pinch strength Distal thumb tenodesis +ve grip strength Extensor carpi radialis +ve increase in max thumb to longus-to-flexor finger distance digitorum profundus Anti-gravity elbow extension was 11 patients transfer restored in one patient Friden et al. 2014 (42 procedures) Intrinsic balancing Activation of thumb abduction Arthrodesis Deltoid to triceps transfer

Discussion

In reviewing the identified studies, the operative interventions on the tetraplegic hand and upper limb bring definite gains in pinch force, cylindrical grasp, and the ability to reach above shoulder height that result in an improvement in ADL function and quality of life for the individual with tetraplegia. Despite the low level of evidence, the subjective acceptance among patients who have had reconstructive surgery is high (Gregersen et al., 2015). One of the reported downsides of surgery is the high complication rate (infection, torn attachments) and the extended period of time post-surgery for rehabilitation and increased need for personal care (Meiners et al., 2002).

Many SCI centres do not offer or have access to reconstructive surgery or neuroprothesis interventions. It is also debated whether surgery or the use of neuroprostheses is beneficial to the client as new movement strategies have to be relearned to perform ADL (van Tuijl et al., 2002), however, surgeries occurring more recently have been associated with greater satisfaction and ability to perform ADLs (Gregersen et al., 2015).

Conclusion

There is level 4 evidence (from one pre-post study; Friden et al., 2012a) that multiple reconstructions can improve key-pinch andgrip strength.

There is level 3 evidence (from one case-control study; Friden et al., 2012b) that patients who had multiple stage BR to FPL through the interosseous membrane had significantly greater active pronation, while other measures remained similar.

There is level 4 evidence (from nine case series; Rothwell et al., 2003; Welraeds et al., 2003; Freehafer, 1998; Mohammed et al., 1992; Ejeskar and Dahllof 1988; Freehafer et al., 1984; Lamb and Chan, 1983; Hentz et al., 1983; Friden et al., 2014) that multiple reconstructive surgery over all increases motor function as well as the ability to perform daily living tasks.

There is level 4 evidence (from one post-test; Gregersen et al., 2015) that a variety of reconstructive surgeries can be used to improve overall elbow function and strength.

There is level 2 evidence (from one cohort study; Dunn et al., 2004) that active transfer procedures may have little benefit over tenodesis procedures as the rate of decline post-surgery is greater and other functional outcomes are equal.

Multiple concurrent reconstructive surgery appears to improve pinch, grip, and elbow extension functions that improve both ADL performance and quality of life in tetraplegia. However, active transfer seems to be the least successful of these procedures.

8.0 Nerve Transfers

Recently, the surgical procedure of nerve transfers is evolving as an alternative procedure to tendon transfers for improving the functional ability of the hand and upper limb post SCI (Keith & Peljovich 2012). A nerve transfer involves the repair of distal denervated nerve element by using a proximal foreign nerve as the donor of neurons and their axons to re-innervate the distal targets (Addas & Midha 2009; Brown et al., 2012; Midha 2004). The transfer involves sacrificing the function of a lesser valued donor nerve to revive function in the recipient nerve and muscles, which is considered functionally more critical than the donor nerve (Senjaya & Midha 2013).

Nerve transfers have traditionally been performed for brachial plexus injuries. More recently, the development of brachialis to the anterior interosseous nerve transfer for SCI has been applied (Hawasli et al., 2015).

Senjaya and Midha (2013) and Midha (2004) described the fundamental principles, advantages and potential drawbacks of nerve transfers when compared to tendon transfers in a review article. They state that the recipient nerve should be repaired as close as possible to the target muscle to ensure the shortest amount of time for re- innervation in an attempt to minimize distal denervation and motor end plate changes. Furthermore, that the donor nerve should be from a muscle whose function is expendable or has redundant innervtion and that the nerve repair should be performed directly without intervening grafts. It is highly recommended that a donor muscle with pure motor fibers be used to maximize the muscle fiber re-innervation, while also ensuring the donor nerve should have a large number of motor axons and be a reasonable size match to the recipient nerve. Lastly, to facilitate motor re-education, a donor nerve that has a function synergistic to the muscle reconstructed should be used because cortical re-adaptation is the physiological basis of functional recovery. Clinicians should also be mindful that motor re-education improves functional recovery post operatively.

Advantages over Tendon Transfers

Nerve transfers have many advantages over tendon transfers. Tendon transfers require significantly more dissection and extended post-operative limb immobilization while the tendon heals (Brown 2012). There is also less surgical scarring in common areas of the hand where tendons overlap anatomically, thus fewer chances of restricted motion (Keith & Peljovich 2012). Reconstruction of finger flexion and extension must be done in separate phases, owing to conflicting positions for postoperative immobilizations (Revol et al., 2002) which may be problematic for some who are highly dependent on others for care to be incapable of performing most basic ADL for quite some time (Bertelli et al., 2011; Brown 2012; Hentz 2002). Also, tenotomy may cause detrimental effects on muscle function owing to the fact that reduced specific force is developed (Guelinekx et al., 1998). In general nerve transfers take a shorter period of less restrictive immobilization probably with less pain, minimal loss of donor muscle function (Brown 2012). Reconstruction of finger flexion and extension can be done at the same time-

tension-insertion balance of the muscle tendon unit is preserved because there is no disruption to the insertion or attachment of the muscle in question-maintaining line of pull and excursion and avoiding scar induced restrictions of movement (Brown 2012). Nerve transfers compared to tendon transfers, offer a greater functional gain for a given transfer (Brown 2011; Brown 2012; Brown et al., 2012). The transferred axon, which originally provided re-innervation to a single muscle can re-innervate multiple motor fibers, with motor re-education and central plasticity, it is possible to activate multiple functions independently by the same nerve that initially controls only a single function (Brown 2011; Brown 2012; Midha 2004). Lastly, nerve transfers can be accomplished without appreciable loss of function from the donor muscle group because nerve transfers can be performed with only a portion of the donor nerve, not entirely denervating the muscle associated with the donor nerve (Brown 2011; Brown 2012).

Although the partial denervation results in a reduced number of axons to the original muscle, the residual motor axons sprout within the muscle and innervate orphaned muscle fibers to enlarge the motor unit. Each motor axon can increase innervation five times the number of muscle fibers that it originally served (Gordon et al., 1993). This phenomenon is called adoption (Brunelli & Brunelli 1983) and in time, the donor muscle may regain its original strength.

Potential Drawbacks of Nerve Transfers

There are also a few potential drawbacks of nerve transfers (Senjaya & Midha 2013). When the donor nerve and its pertinent muscle sacrificed are of suboptimal function to begin with (MRC 3 or 4), nerve transfer many significantly downgrade its intended function. An entirely denervated muscle, as a result of its nerve being donated is no longer suitable for muscle transfer donor. Central motor re-education is needed to achieve functional recovery-this re-education can be challenging for patients, especially for nerve transfers from non-synergistic nerves.

Assessment and Surgical Timing

Prior to considering surgery, a detailed and careful assessment must be completed. Coulet et al. (2002) recommended assessing the following; the extent of LMN injury and mapping muscles to identify functionality. The extent of LMN injury at the injured metamere should be assessed and each key muscle group evaluated to determine the following; type of motor neuron injury (LMN, UMN) by evaluating tone, trophic status, deep tendon reflex, joint ROM and deformities and electrodiagnostic studied are beneficial to determine extent of SCI. After a careful and complete evaltuation of the LMN injury, mapping the relevant muscles should be conducted to categorize muscles in one of three ways; functional muscles (innervated by supralesional segments), paralyzed and denervated muscles (innervated by injured metamere with damage to LMN), and paralyzed but innervated muscles (innervated by infralesional segment, with preserved LMN).

The next assessment to be made is to decide what primary function to restore. Kozin (2002) recommended the following priority: 1) restoration of elbow extension; 2) pinch restoration for hand function; and 3) grasp and release function.

Nerve transfers should be performed after a re-innervation window, to allow adequate waiting time to ensure optimal spontaneous recovery has been achieved for lesional level myotomes. Bertelli et al. (2011) recommended waiting at least six months. Re- innervation of muscle innervated by infralesional segment is not time-dependent and can performed years after injury (Bertelli et al., 2011).

Table 23 Nerve Transfers Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Mean Age: 32.9 yr; Gender: 1. Functional gains were reported from males=7, females=1. 6mos onwards according to patient Intervention: Data was collected on self-reports which included increased patients who had received nerve transfer grasp strength (n=2), an increased use surgery and had been followed-up over a of their hand for feeding (n=2), an period of 12 mo. 20 surgeries were increase in wrist stability (n=1), and performed which included Brachialis (BR) improvement in pinch activities (n=1). to the anterior interosseous nerve (AIN; 2. Three patients reported no changes or n=7), BR to the flexor carpi radialis (FCR; improvements since surgery. n=3), deltoid-to-triceps (n=3, 15%), BR to 3. All patients achieved grades of 1-3 on Fox et al. 2015a the AIN/flexor digitorum superficialis (FDS; the MRC indicating a trace of USA n=1), BR to the FDS/FCR (n=1), BR to the contraction, active movement with Case Series AIN/FCR (n=1, BR to extensor carpi gravity eliminated, and active N=9 radialis (n=1), supinator to extensor carpi movement against gravity respectively. ulnaris (n=1), supinator to posterior 4. Complications post-surgery included interosseous nerve (n=1), and exploratory paresthesias of the thumb (n=3), surgery (n=1). Assessments were urinary tract infection with sepsis (n=1), conducted every 3 mos until 12 mos post- and seroma (n=1). surgery. Outcome Measures: Functional gain self- reports by patients, Medical Research Council elbow flexion grade (MRC), Complications post-surgery. Population: Mean Age: 28 yr; Gender: 1. Histomorphometric analysis revealed males=6, females=1; Level of Injury: C4=2, excellent functioning of the transferred C5=2, C6=3; Severity of Injury: AIS A=4, nerves. AIS B=2, AIS C=1. 2. One patient experienced a reduced Intervention: Patients receiving nerve fiber density, heterogeneity of fibers, transfer surgery completed assessments and imperfect architecture of the nerve and self-reports, and were prospectively cell after histomorphometric analysis, Fox et al. 2015b followed-up over a minimum of 12 mo. however, this patient was found to USA Nerve tissue was also collected during have low motor neuron involvement at Cohort surgery. Surgeries included Brachialis (BR) the time of surgery. N=7 to the anterior interosseous nerve (AIN; 3. No patients experienced a decline in n=7), BR to the flexor carpi radialis (FCR; postoperative functioning compared to n=5), BR to the flexor digitorum baseline functioning according to MRC superficialis (FDS; n=3), supinator to scores. extensor carpi ulnaris (ECU; n=1), 4. One patient who underwent deltoid-to- supinator to posterior interosseous nerve triceps transfer experienced (PIN; n=1), deltoid-to-triceps (n=1), and postoperative weakness of the deltoid exploratory surgery (n=1). Assessments (MRC grade 4) but eventually subsided

Author Year Country Research Design Methods Outcome Score Total Sample Size were conducted at baseline and at 2,4 and and strength returned to baseline levels 12 wk post-surgery. (MRC grade 5). Outcome Measures: Medical Research 5. Functional gains as according to Council elbow flexion grade (MRC), patient self-reports included an Histomorphometric analysis, Complications improvement in grasp strength (n=2), post-surgery, Functional gains reported by greater wrist stability (n=1), an patients. improvement in pinch activity (n=1), and greater use of their hand for activities such as feeding and using a cell phone (n=1). 6. Two patients did not report any changes in functioning from presurgery to post-surgery. 7. Four patients experienced minor complications including paresthesia of the thumb (n=2), hypesthesia of the thumb (n=1), and a seroma which required drainage (n=1). 8. Two patients experienced major complications including urosepsis (n=1) and a urinary tract infection (n=1). Population: Mean age: 26 yr; Gender: 1. At time of final postoperative males=6, females=1; Level of injury: assessment, elbow extension scored complete C-6=7; Mean ASIA motor score: BMRC Grade M4 and under full 15.8±3.9; Mean time since injury: 7 yr. voluntary control in 11 upper limbs Intervention: 27 recipient nerves. Elbow, (UL) and in 2 UL within same patient, thumb and finger extension reconstruction elbow extension scored Grade M3. via nerve transfer was performed on 2. A BMRC Grade M4 for full thumb patients with midcervical spinal cord extension with wrist in neutral was injuries on average 7 mo post injury and observed in 8 UL and 4 hands had outcomes were reported. thumb extension that scored M3. Bertelli et al. 2015 Outcome Measures: British Medical 3. Full metacarpal extension scoring M4 Brazil Research Council scale (BMRC). was demonstrated in 12 hands. Post-Test 4. Finger extension scoring M3 with only N=7 partial range of motion at the metacarpal phalangeal joint was observed in the remaining 1 limb. 5. All patients improved at self- transferring and controlling their wheelchairs. 6. After surgery, all patients extended their thumb and fingers without restriction, no decreased function at donor sites and no patient lost abduction strength or shoulder range.

Discussion

Restoration of elbow extension function is an integral part of upper extremity reconstruction because recovery of this improves elbow stability, the ability to perform pressure relief maneuvers, push a manual wheelchair, reach for items and objects above shoulder height and the ability to complete functional transfers such as bed, toilet, tub and car transfers. To date there has been one case report (Brown et al., 2011)

and one cadaver study (Bertelli et al., 2011) on nerve transfer for elbow extension function.

The primary goal of reconstruction in hands of a person with tetraplegia is the restoration of the ability to create a pinch using the thumb and lateral side of the index finger, for example when holding a key (Bertelli et al., 2012). To date there has been four published case reports (Bertelli et al., 2012; Mackinnon et al., 2012; Brown 2011; Hsiao et al., 2009) on nerve transfer for pinch and grip.

Finger extension is required for object acquisition (grasp) and object release (let go) (Kozin 2002). To date there have been three case reports (Brown 2011; Bertelli et al., 2010; Palazzi et al., 2006) and one cadaver study (Bertelli et al., 2009) on nerve transfer for thumb and finger extension.

Case studies and feasibility trial have comprised the studies that have applied brachialis to the anterior interosseous nerve transfer for SCI. These studies support the feasibility and safety of these nerve transfers, yet, perioperative complications were present for some patients (Fox et al., 2015b). Continued research on the transfer of the brachialis to the anterior interosseous nerve for the treatment of tetraplegia after a cervical SCI with larger samples will be beneficial to determine the potential for improving hand function while also considering the consequences of this surgery (Hawasli et al., 2015). Future research should also investigate the optimal timing for surgeries and the combination of traditional treatment options and nerve transfers (Fox et al., 2015a).

Conclusion

There are only a few published studies on nerve transfer surgery for restoring hand and upper limb function after a SCI and based on the published literature, nerve transfer surgery is emerging as another surgical alternative.

There is level 4 evidence (from one case series; Fox et al., 2015a) that nerve transfer surgery can increase functionality and grasp strength in some patients, however not all patients have successful surgical outcomes.

There is level 2 evidence (from one cohort study; Fox et al., 2015b) that the risk of negative outcomes, such as postoperative decline compared to baseline, for nerve transfer surgery are low.

There is level 4 evidence (from one post-test study; Bertelli et al., 2015) that nerve transfer surgery can increase motor hand function without compromising donor site fuction in patients with midcervical spinal cord injuries.

With greater satisfaction and lower risks reported since 1990, nerve transfer surgery to restore hand and upper limb function in persons with tetraplegia is emerging as another viable surgical alternative.

9.0 Neuroprostheses

A neuroprostheses for grasping is a device designed to improve or restore the grasping, holding, and reaching functions in individuals with stroke and SCI (Baker et al., 1993; Cornwall & Hausman 2004). The neuroprostheses applies FES of the motor branches of the peripheral nerve in which paralyzed muscles are electrically stimulated to produce muscle contraction, replacing the electrical signals coming from the brain through the injured spinal cord (Shimada et al. 1996; Handa 1997; Hincapie et al., 2008). The FES uses bursts of short electrical pulses (pulse widths 0-250 mSec and pulse amplitude 0- 150 mA) to generate muscle contraction by stimulating motoneurons or reflex pathways. The key element for achieving synergistic activity of muscles that results with reaching and grasping is the appropriate sequencing of bursts of electrical pulses. For continuous contraction of the arm and hand muscles (tetranization), a FES system has to deliver at least 16 stimulation pulses per second to elicit action potentials (AP) in the motor nerve, causing the corresponding muscles to contract. FES enables the patients with high SCI to reconstruct grasp movements such as palmar and lateral grasps of the upper extremity (Shimada et al., 2003). The palmar grasp is used to hold bigger and heavier objects such as cans and bottles and the lateral grasp is used to hold smaller and thinner objects such as keys, paper and CDs (Popovic et al., 2002). It has been reported to be useful in improving ADL functions (Popovic et al., 2001a; Shimada et al., 1996). FES is also applied to generate elbow extension by stimulating the triceps brachii in combination with voluntary biceps contraction used to augment reaching (Grill & Peckham 1998; Popovic et al., 1998). Elbow and shoulder FES systems have not been developed into practical clinical devices but may be an area of future research. The next generation of neuroprosthetic systems are currently being developed with the goal of integrating fully implantable multi-channel stimulators and feedback sensors with adaptive control systems (Grahn et al., 2014).

The motor nerves can be stimulated using surface (transcutaneous), percutananeous or implanted electrodes (Mortimer 1981). Transcutaneous stimulation is performed with self-adhesive or non-adhesive electrodes that are placed on the subject’s skin in the vicinity of the motor point of the muscle that needs to be stimulated (Baker et al., 1993; Mortimer 1981). Percutaneous and fully implanted electrodes are placed close to the entry point of the motor nerve to the muscle which should be stimulated, either epimysial or intramuscular (Cameron et al., 1997; Hoshimiya & Nanda 1989).

Individuals with C5-C7 complete SCI and with no major degree of motoneuron or nerve root damage of the stimulated muscles benefit the most from neuroprosthesis. The use of an implanted FES system can only be applied once the patient reaches stable neurological status, which usually occurs two or more years’ post SCI. The use of surface FES systems can be introduced during the early rehabilitation period, as the patient does not have to be neurologically stable.

Gorman et al. (1997) and Cornwall and Hausman (2004) have presented guidelines for patient selection when considering an implantable neuroprosthesis. Their considerations for selection cover a broad range of factors from physical to

psychosocial and should be considered for patient selection. Anatomical factors are important for the physical stability of the implant, it is recommended that the patient have stable tetraplegia with C5 or C6 motor level with international classification motor scores of zero, one, two or an impairment scale level of A, B, C (AIS). Physiological conditions considered should be the presence of adequate ROM in joints of the shoulder, arm, forearm, wrist and hand for the type of prosthesis. Medically, it is generally recommended that patients be free of overwhelming medical problems. Sufficient motivation to learn and use the prosthesis is also critical, as well as knowing the level of support available from caregivers or family members, so psychosocial factors must also be considered. The individual should exhibit certain indirect needs which would impact the success of the implant, such as sufficient vision, and cognitive ability to incorporate visual feedback and progress in the learning of the prosthesis. Lastly, functional recovery should plateau before the consideration of a neuroprosthesis, which usually occurs at one-year post-injury.

Contraindications to neuroprothesis use include cardiac disease, arrhythmias, pace makers, chronic systemic infections, diabetes, and immune disease.

An important barrier to the use of neuroprothesis is the lack of commercially available devices. Despite the demonstrated effectiveness of neuroprothesis for improving hand function and quality of life only one device is currently available commercially (Venugopalan et al., 2015). Three studies of unique devices have been considered in SCI injured individuals.

Reported Benefits of Neuroprosthesis Use There have been many documented and reported benefits of neuroprosthesis use with the spinal cord injured person. The training required to use the device leads to short and long-term changes within the CNS (Popovic et al., 2002). A neuroprosthesis can be used as a neurorehabilitation system that promotes recovery and better hand function in incomplete SCI and stroke subjects or as a permanent orthotic device for complete cervical lesion SCI subjects to augment the grasp and manipulation functions required for typical ADLs.

Clinical Results of Neuroprosthesis Use There are many reported clinical results of neuroprosthesis use. Some focus on patient outcome and improvement while others focus on the efficacy of a specific model of prosthesis. Currently, clinical trials show improvement in the following areas in stroke and SCI patients; grasping, functional ability of upper extremities, and motor control. FES technology specifically facilitates a comfortable and secure grasp that allows the individual to hold and manipulate various objects. In terms of specific outcomes based on the model of prosthetic used, all except the Bionic Glove were able to facilitate both palmar (power) grasp and lateral (fine) grasp. While the Handmaster-NMS-1, the BGS system, and the ETHZ-ParaCare neuroprostheses have been applied successfully as rehabilitation tools to restore grasping function in SCI individuals instead of being used as permanent orthotic systems. The most widely used and accepted neuroprostheses for grasping are the Freehand System and the Handmaster-NMS-1 and all of the other

neuroprostheses mentioned are mainly used in experimental trials for research purposes. In general, to control the neuroprosthesis, subjects are using either an on-off type of switch or have to apply simple analog sensors to generate desired control commands. A usual time delay of one to two seconds from the time the command is issued to the moment the grasp is executed is common. This restricts the speed that an individual can grasp and release objects and therefore neuroprostheses for grasping can only be used for slower grasping tasks.

Challenges in Neuroprosthesis Use and Reasons for Not Using Neuroprosthesis There are several reported challenges in neuroprosthesis use. There is a general perception within the clinical community that neuroprosthesis technology is not fully matured and the application of its use is labour intensive. Patients and families can also overestimate the results that assistive systems can provide and therefore may not be satisfied with the final outcome. The acceptance of the device depends on the specific needs of the client and their specific expectations and limitations should be considered. The success of implantation can also be complicated by variety of age and lifestyle factors represented in patients with UE paralysis, this can also limit the number of individuals willing to consider neuroprostheses. Clients can also have a series of intrinsic motivations for not pursuing a prosthetic, such as they may be waiting for a cure for their illness, afraid of the technology, poor motication, and an unwillingness to devote considerable attention to the everyday use of it. In order for an individual to consier a prosthesis they must themselves feel comfortable with the technology, and using it in a variety of settings, such as the home and work environment. Other potential barriers to the acceptance of a prosthesis can include technical difficulties, cultural differences, and pre-existing psychological perceptions. Then there are the specific limitations associated with the device itself, some models (FES technology) require intensive maintenance through a skilled technician, there can be inadequate reliability of use (breaking of wires orelectrode failure), implantion often requires additional surgeries, and lastly that extensive training is required to use the device. There is also an ongoing battle in technology to simultaneously make devices more effective (natural motions), yet also less complex and cumbersome. This often results in changes to the overall cosmetics of the device which can deter individuals by increasing the donning and doffing times of these prostheses. Lastly, as neuroprosthesis technology is a relatively new field, data on long-term reliability is not yet available, even simple systems for powered tenodesis grip for individuals with lesions at C6 or lower have not been fully explored in deference to volitional tendon transfer surgery (Popovic et al. 2002; Triolo et al., 1996).

Table 24 Neuroprostheses Author Year Country Research Design Methods Outcome Score Total Sample Size Ferrante et al. 2014 Population: Mean age: 47.9 yr; Gender: 1. Grasping and reaching performance Italy males=11, females=3; Injury etiology: for all patients across all four tasks Post Test SCI=8, Friedreich Ataxia=3, Amyotrophic were rated by three observers with a N=14 Lateral Sclerosis=2, Multiple Sclerosis=1.

Author Year Country Research Design Methods Outcome Score Total Sample Size Intervention: Patients tested the median score of 2 (“completely Multimodal Neuroprosthesis for Daily functional”) on a scale of 0-2. Upper limb Support (MUNDUS) system 2. One patient scored 1 (“acceptable”) on for efficacy and functionality. Four tasks all four tasks and two patients scored a were performed including drinking, mixture of 1 and 2 in grasping and touching the contralateral shoulder, reaching performance. No patients touching the contralateral hand, and scored a 0 (“unacceptable”) at any pressing a button. Each movement was time. performed 10 times with a 30 sec break 3. Patients rated the MUNDUS system between each. Patients with no residual highly on the TSQ-WT with Usability, arm or hand function completed the tasks Benefit, Self-concept, Privacy and via an eye-tracking system or a brain- Quality of Life all scoring computer interface program. approximately 80% or higher but Assessments were conducted during Comfort was not scored as highly with each trial and at post-treatment. a value of approximately 55%. Outcome Measures: Telehealthcare 4. A median value of 85% was reported Satisfaction Questionnaire - Wearable on the SUS indicating a high level of Technology (TSQ-WT), System usability but patients did report a Usability Scale (SUS), Technology dissatisfaction with the encumbrance Acceptance Model (TAM) questionnaire, of the system. Grasping and reaching performance 5. Usefulness was rated highly by ratings. caregivers, therapists and technicians on the TAM but ease of use was rated much lower by caregivers and therapists compared to technicians. 6. Caregivers reported higher levels of computer anxiety on the TAM compared to therapists and technicians. Population: Mean age: 37.1 yr; Gender: 1. Pinch force with the orthosis males=22, females=2; Level of Injury: (7.26±3.48 N) was significantly greater C6-C7; Severity of Injury: AIS A=24; than without the orthosis (0.64±0.42 N) Mean time since injury: 5.6 yr. (p<0.001). Intervention: Patients performed pinch 2. The average transfer efficiency of wrist Kang 2013 and wrist extension movements using a extension with maximum voluntary South Korea wrist-driven flexor hinge orthosis. contraction to pinch force was 37.6%; Observational Outcome Measures: Manual Muscle the efficiency was greater for patients N=24 Test (MMT), Wrist extension angle at with weaker wrist extensor strength maximum voluntary contraction, Pinch (r=0.79). force transfer efficiency of wrist extension 3. Pinch strength was not significantly to pinch force. correlated with the wrist extension angle at maximum voluntary contraction (r=0.07). Population: SCI population (n=11): 1. The non-injured participants had Mean age: 37.5 yr; Level of Injury: C1- significantly faster TTC scores than C4=5, C5-C6=6; Severity of Injury: AIS the SCI participants on completing A=11. Targets 3 and 4 (p>0.05). Non-injured group (n=5): Mean age: 29.8 2. Additionally, high cervical participants Scott & Vare 2015 yr. were found to have significantly slower Australia Intervention: Both the SCI and non- TTC scores than the mid cervical Post Test injured groups completed target matching group (p<0.05). N=16 tasks using a user command controller 3. The high cervical group had triggered by head position to manipulate significantly higher IOE than the a virtual hand representation. Participants middle cervical group and the non- using head movements matched the injured participants for Targets 3 and 4 virtual hand to different targets. There (p<0.05).

Author Year Country Research Design Methods Outcome Score Total Sample Size were 10 targets split between the trials, 4. Non-injured participants had a some of which had different locations or significantly lower POE than those with sizes compared to each other. SCI in completing Targets 3 and 4 Additionally, the speed of the virtual hand (p<0.05). was altered in four speed increments 5. On examination of TTC, IOE and POE progressively throughout the experiment for Targets 5 and 6, no significant with a low of speed 1 (18 on-screen differences were found between SCI units/s) to a high of speed 4 (196 on- and non-injured participants (p>0.05). screen units/s). 6. There was a significant increase in the Outcome Measures: Absolute TTC for Target 8 for SCI participants performance on task matching (time to over non-injured participants (p<0.05). complete (TTC)), Efficacy of completion 7. There was a significant increase in on task matching (integral of the error IOE for Target 7 by SCI participants (IOE)), Ability to issue appropriate when compared to non-injured commands using the virtual hand participants (p<0.05). (percentage of errors (POE)). 8. There was a significant increase in the POE commands for Target 7 and Target 8 for SCI participants compared to controls(p<0.05). 9. Non-injured participants were significantly faster than SCI participants in completing Target 10 (p<0.05), but there was no significant difference between the two groups for Target 9 (p>0.05). 10. For speeds 1, 2, and 3, TTC scores were significantly lower for SCI participants (p<0.05). 11. For IOE scores, non-injured participants had higher scores at speeds 1 and 3 compared to SCI participants (p<0.05). 12. For POE scores, non-injured participants were scored significantly lower than the SCI participants at all four speeds (p<0.05).

Author Year Country Research Design Methods Outcome Score Total Sample Size Method: Comprehensive literature 1. Two studies were scored a III, one search of full-length, peer reviewed study scored a VI, and two studies studies of patients with complete or scored VIII. incomplete cervical SCI, investigating 2. In total, there were 10 different functional electrical stimulation (FES) outcome measures between the five (possibly comparing to other conventional included studies assessing functional Patil et al. therapies) in adult and human studies. outcomes and motor control. 2015 Databases: EMBASE, PsycInfo, PubMed 3. All 5 studies reported improvement, UK and Food, Science and Technology both immediate and follow-up, in motor Review of published abstracts. control and functional ability of upper articles between Level of evidence: Jovell and Navarro- extremity as result of FES or FES with September 2009- Rubio classification: Good (I-II): Meta- conventional therapy. September 2014 analysis of randomized controlled trials N= 5 (RCTs), Large-sample RCTs; Good-to- fair (III-V): Small-sample RCTS, non- randomized controlled prospective trials, non-randomized controlled retrospective trials; Fair (VI-VII): cohort studies, case- control studies; Poor (VIII-IX): non- controlled clinical series; descriptive studies, anecdotes or case reports. Questions/measures/hypothesis: Examine the evidence for FES on motor control and functional ability of the upper limb in spinal cord injured people.

Discussion

The use of neuroprosthesis whether implanted or surface electrodes appear to benefit persons with C5-C7 level tetraplegia. The studies consistently demonstrate improvements in pinch (lateral and palmar), grip strength, and ADL functioning and general satisfaction with the use of the device, although the study subject numbers are relatively small. Ongoing compliancy and use of the devices on a long-term basis continue to be problematic. Reasons for discontinuing the use of the device depend on length of time and the amount of assistance required to don and doff the device, if using the device can provide enough of a difference in overall level of functioning. The studies also consistently report both mechanical/electrode failure and adverse medical complications. Many of the devices are only available in specialized rehabilitation centres where access to rehabilitation engineering is available. In addition, many of the devices continue to be only available in clinical trials. The overall cost to use the device continues to be great when considering factors such as cost of the device, the extensive training period required and staff to support the programme. The next generation of implantable FES devices are being developed at the FES Centre in Cleveland, OHIO and The Shriner’s Hospital, Philadelphia, Pennsylvania. These are internally powered and wirelessly controlled, eliminating an external coil and control unit.

Conclusion

There is level 4 evidence (from two post-tests; Ferrante et al., 2014; Scott and Vare, 2015) that although neuroprosthesis use increases functionality, patients score the device lower when looking at social factors such as comfort, encumbrance, and computer anxiety. Compared to healthy controls, patients with SCI encounter more challenges and slower times to use the device.

There is level 5 evidence (from one observational study; Kang, 2013) that pinch force can be increased with the use of an orthosis, and with greater efficiency.

The use of neuroprostheses appears to have a positive impact on pinch and grip strength and ADL functions in C5-C6 complete tetraplegia, however psychosocial factors continue to represent an obstacle in patient use.

9.1 Surface or Percutaneous Neuroprosthesis Systems There are several existing neuroprostheses and these include implanted FES systems such as the Freehand System and the NEC FESMate System and surface stimulation electrode systems such as the NESS H200 (formerly Handmaster NMS-1), Bionic Glove, ETHZ-ParaCare Neuroprosthesis and systems developed by Rebersek and Vodonik (1973) and Popovic et al. (2000).

9.1.1 Freehand System The Freehand System from Cleveland, OH, USA is an implantable neuroprothesis intended to restore hand function in those with C5 and C6 level tetraplegia. The Freehand system can stimulate eight different muscles in order to produce a useful grip and key pinch in individuals with tetraplegia. The system consists of a surgically implanted receiver/stimulator unit and electrodes with an external controller and power supply/microprocessor. It was first implanted in 1986 (Cornwall & Hausman 2004). The Freehand System has been implanted in more than 250 individuals with C5 and C6 level tetraplegia (Ragnarsson 2008).

The NeuroControl Freehand System consists of an active receiver/stimulator that is placed in the chest wall and has eight leads that come from the receiver/stimulator and pass under the skin to a connector site in the upper arm. At this point they are joined to epimyseal electrode leads that are passed under the skin from the forearm and hand. Power and control signals from the unit are passed through the skin to the receiver/stimulator from a skin-mounted coil. The patient controls the device by movement of the opposite shoulder that uses a skin surface mounted position detector. The lateral grasp is generated by first flexing the fingers to provide opposition, which is followed by thumb flexion. Palmar grasp is generated by first forming the opposition between the thumb and palm, followed by simultaneous flexion of both the thumb and fingers. Stimulating the flexor digitorum superficialis and profundus muscles performs finger flexion and finger extension is obtained by stimulating the extensor communis digitorum. Stimulation of the thumb thenar’s muscle or median nerve produces thumb flexion. Hand opening and closure strength are proportional to the distance moved by

the shoulder. Both palmar and lateral grasps are possible by pressing a button on the shoulder controller. Taylor et al. (2002) and Keith et al. (1996) reported that most clients will require several surgical procedures are needed for each client for optimal use of the device. The most common surgeries performed are brachioradialis to extensor carpi radialis for voluntary wrist extension and posterior deltoid to triceps for elbow extension (Keith et al., 1996; Taylor et al., 2002). The 1st generation of the Freehand System is no longer available from NeuroControl Corporation. There are devices still available on a selective basis in several centres (Cornwall & Hausman 2004; Ragnarsson 2008).

Table 25 Freehand System Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 13-16 yr; Level of 1. No statistical results are reported. injury: tetraplegia; Time since injury: 4-16 2. No perioperative complications wk. reported. Intervention: The following muscles were 3. Subjects began Freehand System implanted with intramuscular electrodes: use between 2-5 days after Extensor digitorum profundus, extensor implantation. pollicis longus, flexor pollicis longus, 4. Muscle Strength-no subject gained adductor pollicis, and opponens pollicis significant strength in any key for each subject. muscle on their freehand limb. Outcome Measures: Muscle Strength- 5. Pinch Force-with Freehand System - Mulcahey et al., 2004 Pinch Force & Hand Function, each subject realized significant USA Performance of Activities of Daily Living improvement in pinch force. Case Series (ADL), Satisfaction with + without the 6. Upper Extremity Capacity-first 11 N=4 Freehand System (Canadian questions - no difference with or Occupational Performance Measure without Freehand-last set of (COPM)), Upper Extremity Capacity, questions Freehand System Quadriplegic Index of Function. improved scores. 7. Quadriplegic Index of Function-all subjects increased their level of independence. 8. Freehand System Open-ended Questions-all subjects would repeat implantation. Population: Level of injury: C5-C6. 1. Variation in elbow moment across Intervention: Epimysial or intramuscular subjects significantly greater than electrodes were implanted on the triceps. the variance within subjects Following surgery standard stimulation (ANOVA p<0.001). exercise regimens were followed. 2. 10/11 elbows tested elbow moment Outcome Measures: Elbow extension generated by triceps stimulation at moments at different elbow positions, different elbow angles, elbow Memberg et al., 2003 Performance in controllable workspace moment weakest with elbow in more USA experiments, Comparison to an extended position (30º flexion) and Case Series alternative method of providing elbow peaked with elbow at 90º flexion, N=22 extension in these individuals (posterior significant ANOVA p<0.001. deltoid to triceps tendon transfer). 3. Elbow moment generated by triceps stimulation at 90º and 120º elbow flexion was significantly greater than elbow moment produced by tendon transfer (ANOVA p<0.05), no difference between elbow extension methods at 30º elbow flexion.

Author Year Country Research Design Methods Outcome Score Total Sample Size 4. Triceps stimulation and posterior deltoid together provided a greater elbow moment than each method separately, difference significant at each elbow position p<0.05, except at 90º. 5. Quantitative workspace assessment done on 5 arms, more successful with triceps stimulation, significant for each subject, chi square p<0.05). 6. Average acquisition time with triceps stimulation less than without stimulation 4/5 arms (3.2-6.4 seconds) and significant in 3/5 arms (unpaired t-test p<0.01) and not for one p=0.076. Population: Mean age: 38.4 yr; Gender: 1. Grasp release test results: increase males=7, females=1; Level of injury: C4- in the types of tasks that subjects C6; Mean time since injury: 10.1 yr. could perform (pre n=1.4) and post Intervention: Assessment of the implantation (n=5.1 p=0.011). Freehand System. 2. One-yr post implantation the types Outcome Measures: Grasp Release of tasks performed was 5.5 p=0.027, Taylor et al., 2002 Test, Grip Strength, Activities of Daily without the system it was 1.2 UK Living (ADL), Sensory ability (static 2 pt (p=0.028). Case Series discrimination). 3. Number of repetitions increased N=9 post implantation from 12.7 to 37.4 (p=0.028) and without the implant post-implantation (20.2, p=0.046). 4. At one-yr number of repetitions was increase to 50.5, p=0.046 with the system and without 24.3, p=0.28. Population: Age: 16-55 yr; Level of 1. 7/9 use Freehand System daily. injury: tetraplegia. 2. Provided an active grip of some Intervention: The patients, using an strength which allowed many external stimulator, built up the muscles functional activities. Hobby et al., 2001 strength in the hand and forearm, to 3. Increase in self-confidence. UK ensure the muscles were in good 4. For over 80% of their selected ADL Pre-post condition at the time of surgery. goals, user preferred to be N=9 Outcome Measures: Grip Strength, independent with their Freehand Activities of Daily Living (ADL). system than use previous method or have activity performed by caregiver. Participants: Age: 16-57 yr; Gender: 1. When the neuroprosthesis was males=42, females=9; Level of injury: C5- activated all participants increased C6; Mean time since injury: 4.6 yr. their pinch force in lateral pinch Intervention: Participants were trained to (p<0.001) and some increased their use the neuroprosthesis and to use it for pinch force in palmar grasp functional activities. Once they were (p<0.001). Peckham et al., 2001 satisfied with their ability to perform daily 2. 98% of participants moved at least USA activities or when they reached a plateau one object with the neuroprosthesis Pre-post in proficiency then rehab was complete. (p<0.001) and 37 improved by NInitial=51; NFinal=50 Outcome Measures: Pinch strength, moving at least three more objects active ROM, Grasp-Release Test, (p<0.001). Activities of Daily Living (ADL) Abilities Disability was reduced in 49 of 50 Test, ADL Assessment Test & user participants as measured by the satisfaction survey. ADL abilities or ADL assessment tools.

Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 31-48 yr; Gender: 1. No statistical results reported males=7, females=1; Level of injury: C4- 2. Completion of personal care was 6; Time since injury=43-430 mo; Follow- provided by outside nursing up time=8-53 mo. agencies. (mean 11.5 hr/day, range Intervention: Interviews- reviewing use of 3-24 hr); four users had additional Neuro Control Freehand System. care from family members (mean Outcome Measures: Amount of Care & 3.4 hr/day, range 2-5 hr); no users The System. claimed that care given by family members had decreased System-donning external components 5-10 min; most users reported no significant problems fitting the external equipment; two users had problems locating the coil; three locating the shoulder Taylor et al., 2001 controller; one had persistent UK problems maintaining the position Pre-Post through the day due to the adhesive NInitial=9; NFinal=8 tape used becoming detached (four reported this as an occasional problem); four users had problems with skin allergy to the tape or double sided adhesive rings; two users reported that the system made transfers more difficult; three users never stopped using the system due to system failure; some problems with equipment reliability; no change in paid caregiver time; six users felt more confident when using the system; seven felt their quality of life had improved. Population: Age: 23-48 yr; Level of 1. No statistical analysis was complete. injury: C5-C6. 2. Passive elbow extension was within Intervention: Participants were implanted normal limits. with an upper extremity neuroprothesis 3. With stimulated triceps subjects including a triceps’ electrode to provide attained full elbow extension; stimulated elbow extension. Participants without it full range was not met. exercised triceps 4-6 hr/session using a Bryden et al., 2000 programmed electrical stimulation USA exercise regimen that includes breaks. Case Series Participants exercised either nightly or N=4 every other night-whatever was best for maintaining an optimal amount of strength. Outcome Measures: Five overhead reaching tasks, Amount of assistance required to complete the task, Survey of home use. Population: Mean age: 29.1 yr; Gender: 1. There was significant improvement males=4, females=2; Level of injury: in lateral pinch and palmar grasp Carroll et al., 2000 tetraplegia; Time since injury: 1.2-11.3 yr. force after rehabilitation with and Australia Intervention: The Freehand System – an without the neuroprothesis. Pre-post implanted multichannel neuroprothesis. 2. Force differences were not found N=6 between presurgery and

Author Year Country Research Design Methods Outcome Score Total Sample Size Outcome Measures: Pinch forces, Grasp rehabilitation without and Release Test (GRT), Activities of neuroprothesis. Daily Living (ADL) Test. 3. With neuroprothesis, subjects could grasp, move and release more items in the 30 sec GRT, as compared to without the neuroprothesis. 4. In 35/48 ADL events, less assistance was used (physically or assistive equipment) with the neuroprosthesis. In 41/48 ADL events, neuroprosthesis use was preferred in all subjects. After study, 5/6 subjects still used neuroprosthesis daily. Population: Age: 13-53 yr; Gender: 1. General Satisfaction: 87% were males=26, females=8; Level of injury: positive agree or strongly agree, tetraplegia; Follow-up time: 1 yr. 97% would recommend Intervention: Implemented with a hand neuroprosthesis to others, 90% neuroprosthesis that provides grasp and were satisfied with neuroprosthesis, release. 90% stated neuroprosthesis was Outcome Measures: Standardized test reliable, 87% would have surgery of grasp and release (GRT), again, 80% felt the neuroprosthesis Measurements of pinch strength and met their expectations, & 77% would range of motion, Satisfaction survey, pay for the neuroprosthesis if they Activities of Daily Living (ADL) survey. had the money. 2. Life Impact: 88% responses were positive for life impact; 90% stated neuroprosthesis improved their quality of life; 87% positive impact on their life (90% reported did not make a negative impact); 83% provided a benefit ADL; 87% responses regarding changes in ADL were positive; 93% participants Wuolle et al., 1999 could perform ADL easier; 93% USA could perform ADL such as painting Case Series and shaving; 90% had increased NInitial=42; NFinal=30 confidence when performing ADL; 83% could perform ADL more normally; 73% could perform ADL faster. 3. Independence: 81% of responses were positive; 87% reported they were able to function more independently; 83% used less adaptive equipment; 87% required less assistance from others; 67% felt more comfortable out in the community alone. 4. Occupation: 57% of responses to occupation questions were positive 5. Appearance: 87% felt their hand appearance was unchanged or improved. 6. Usage: used prosthesis median of 5.5 days/wk - ranged from 15 participants (44%) who donned the

Author Year Country Research Design Methods Outcome Score Total Sample Size neuroprosthesis 7day/wk to five participants (15%) who used it less than one day/wk; 24/34 participants (71%) used it ≥4 day/wk; range of usage C4/C5, C5/C5, C6/C6 levels was the same (0-7 day/wk) C5/C6 group - used it most regularly 4-7 day/wk with most participants 8/10 reporting daily use. 7. Activities: most frequently reported activities included eating, drinking, shaving, brushing teeth, brushing hair, writing, operating a computer, playing games. 8. Quality of Life: 18/34 positive comments; 1/34 responded neutrally; 1/34 responded negatively. 9. Improvements: Additional stimulus channels, an implanted command source, smaller, lighter external control unit - easier to don, improve hand and arm function, make device operable if user is confined to bed. Population: Age: 28-57 yr; Level of 1. Pinch force ranged from 8 to 25N, injury: C5-C6; Severity of injury: complete; with stimulation and greater than Time since injury: 2-9 yr. tenodesis grasp alone. Intervention: Implanted neuroprosthesis. 2. All demonstrated functional grasp Outcome Measures: Grasp force, Grasp- patterns and were able to Kilgore et al., 1997 Release Test, Tests of Activities of Daily manipulate at least three more USA Living (ADL) (functional independence), objects with the neuroprosthesis; Case Series Usage Survey. had increased independence and N=5 were able to use the neuroprosthesis at home on a regular basis; the implanted stimulator proved to be safe and reliable. Population: Age: 16-18 yr; Level of 1. 40 electrodes implanted, 37 injury: C6=5, Time since injury: >1yr. continued to work, all implant Intervention: Surgery. stimulators have functioned without Mulcahey et al., 1997 Outcome Measures: Grasp Release problems with follow up ranging USA Test, Activities of Daily Living (ADL). between 16-25 mo. Pre-post Grasp Release Test-lateral pinch N=5 and palmar grasp forces - Wilcoxon test, FES forces were significantly greater than tenodesis forces for both grasps (p=0.043). Population: Age: 13-19 yr; Gender: 1. FNS versus Tenodesis males=3, females=2; Level of injury: 2. With FNS and tenodesis each case C5=5; Time since injury: 3-72 mo. of improved performance in later Smith et al., 1996 Intervention: FNS versus Tenodesis. sessions was significantly better as USA Outcome Measures: CWRU Hand compared to the initial session. Case Series System (Case Western Reserve (p<0.05). N=5 University), Grasp and Release Test. 3. The average grasp forces with FNS increased; the range was from 8.9N (SD+5.2) to 22.5N (SD+8.6) and the

Author Year Country Research Design Methods Outcome Score Total Sample Size palmar grasp forces increases from 2.1N (SD+2.9) to 11.1N (SD+6.0). Population: Age: 13-19 yr; Gender: 1. No predicted difference between males=5; Level of injury: C5-C6; Time electrodes in intrinsic and extrinsic since injury: 3-72 mo. muscles (p=0.93). Intervention: Intramuscular electrodes 2. Significant differences were were implanted in the upper extremity predicted between exit sites Smith et al., 1994 muscles. (p=0.016) + across muscle groups USA Outcome measures: The Breslow Test. (p=0.047). Case Series 3. Survival likelihoods poorer for N=5 electrodes exiting dorsally. At 90 days after implant survivals probabilities of the finger + thumb extensors + thumb abductors were no significant than that of thumb adductor + flexor muscle groups.

Table 26 Summary Implanted Neuroprostheses (Freehand System and CWRU) Author N Intervention Main Outcome(s) =UE strength +ve ADL: QIF scores Mulcahey et al., 2004 4 Implanted Freehand System +ve Satisfaction: COPM +ve lateral and palmar pinch =UE capacity: UEC 5/11 Implanted Freehand System 6/11 CWRU 6/11 tendon transfer surgery for +ve elbow extension Memberg et al., 2003 10 elbow extension +ve workspace assessment

4 arms triceps electrode 11 triceps electrodes/10 UL +ve Grasp Release Test Taylor et al., 2002 9 Implantation of Freehand System +ve Grip Strength +ve ADL Assessment +ve lateral pinch +ve palmar grasp 51 implanted Implanted Neuroprosthesis and +ve Grasp Release Test Peckham et al., 2001 (50 evaluated) adjunctive surgeries +ve satisfaction =no change in ability and long- term stability and function =no change in level of personal care assistance Taylor et al., 2001 8 Implantation of Freehand System -ve system failure +ve ADL and functional use +ve ADL and functional use (80%) +ve lateral grasp +ve palmar grasp Implanted Freehand System and Hobby et al., 2001 9 +ve 5 finger grasp adjunctive surgeries -ve several electrode failures; stimulator failure; medical complications 7/9 use device daily +ve lateral pinch and palmar Implanted Freehand System and Carroll et al., 2000 6 grasp force adjunctive surgeries +ve GRT scores

Author N Intervention Main Outcome(s) +ve ADL (35/48) activities 5/6 still use the device +ve elbow function (strength, 4 Implantation of Freehand System Bryden et al., 2000 ROM) (5 limbs) with electrode to triceps +ve ADL and functional use +ve satisfaction (87%) +ve life impact (90%) +ve ADL (87%) +ve independence (81%) Implanted Freehand System and Wuolle et al., 1999 34 +ve occupation (74%) 31 had adjunctive surgeries +ve appearance +ve usage (5.5 d/week median) +ve activities +ve QOL +ve pinch force Implanted Neuroprosthesis and +ve grasp strength Kilgore et al., 1997 5 adjunctive surgeries +ve Grasp Release Test +ve ADL and functional use Implanted Freehand System and +ve Grasp Release Test Mulcahey et al., 1997 5 adjunctive surgeries +ve ADL and functional use +ve unilateral grasp and release Smith et al., 1996 5 Implanted Neuroprosthesis abilities with FNS Smith et al., 1994 5 Implanted Neuroprosthesis -ve electrode failure

Discussion

Although Freehand System results in significant positive functional outcomes for individuals with tetraplegia, the unavailability of the device impacts its clinical use greatly. Some devices are still available on a selective basis (Cornwall & Hausman, 2004; Ragnarsson, 2008), however there is no opportunity for standardized clinical use at this time. Additionally, most patients need to undergo multiple surgeries for the implantation of electrodes and other various components of the device in order to gain optimal use of the system. This represents another barrier to the wide spread application of the Freehand System.

Conclusion

There is level 4 evidence (from eight case series; Malcahey et al., 2004; Memberg et al., 2003; Taylor et al., 2002; Bryden et al., 2000; Wuolle et al., 1999; Kilgoreet al., 1997; Smith et al., 1994; Smith et al., 1996) that the implanted Freehand System increases grip strength, grasping, ADL and function, and overall indepdence.

There is level 4 evidence (from five pre-post studies; Peckham et al., 2001; Taylor et al., 2001; Hobbey et al., 2001; Carroll et al., 2000; Mulcahey et al., 1997) that the implanted Freehand System results in positive increases in grip strength, grasping and overall independence.

Although the Freehand System improves multiple function parameters as well as overall quality of life and independence, its limited production and implantation represent serious challenges in its clinical application.

9.1.2 NESS H200 (formerly HandMaster-NMS-1) The NESS H200 developed by Nathan et al., and produced by Neuromuscular Electrical Stimulator Systems, Ra’anana, Israel is the only commercially available upper limb surface FES system (Ragnarsson 2008; Venugopalan et al., 2015). It has been FDA approved for use with individuals with stroke and SCI. It is predominantly used as an exercise tool for stroke subjects and is commercially available in a limited number of countries (Popovic et al., 2002). The NESS H200 has three surface stimulation channels used to generate grasping function in tetraplegia and stroke subjects. One channel is used to stimulate extensor digitorum communis muscle at the volar side of the forearm. The second channel stimulates the flexor digitorium superficialis and profundus muscles. The third stimulation channel generates thumb opposition. The system is controlled with a push button that triggers the hand opening and closing functions. The system is easy to don and doff. However, it does have some limitations in its design. The system is limited by the rigid arm splint which does not provide enough flexibility of the electrodes for stimulation of the finger flexors for grasp; it is a stiff orthosis that fixes the wrist joint angle and prevents full supination of the forearm (Popovic et al., 2002).

Table 27 NESS H200 (formerly Handmaster-NMS-1) Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Gender: males=7, 1. All were 100% successful in using females=0; Level of injury: C5-C6; Mean the handmaster in the studied ADL time since injury: 6 mo. and grasp (hold and release) tasks. Intervention: Subjects practiced with the 2. Improvements were noted in Alon & McBride 2003 neuroprothesis daily to regain grasp, hold, strength (0.57±98N to 16.5±4.4N, USA and release ability and to restore selected finger linear motion (0.0cm to Pre-Post functions of 1 of the 2 paralyzed hands. 8.4±3.2cm) and Fugi-Meyer scores N=7 Subjects were observed 2-3x/wk for 3 (p<0.05). wks. Outcome Measures: Activities of Daily Living (ADL) tasks, Hand impairment measures (two grasp and release tests). Population: Age: 20-65 yr; Gender: 1. Six people left the study for various males=8, females=2; Level of injury: C4 to reasons (>50%). Over all the four Snoek et al., 2000 C6; Classification: 3-Cu=3, 1-O=5, 2-O=1, remaining were able to perform Netherlands 0-O=1; Fitted hand: Right n=6, Left n=4. several tasks with the Handmaster Pre-Post Intervention: Training for use of that they were not able to without it NInitial=10; NFinal=4 Handmaster. (i.e., 3/4 were able to put the splint Outcome Measures: Not specified. on independently).

Table 28 Summary NESS H200 (formerly Handmaster-NMS-1) Author N Intervention Main Outcome(s) +ve ADL use Alon & McBride 2003 7 NESS Handmaster +ve Grasp Release Test

Author N Intervention Main Outcome(s) +ve grip strength =finger motion Intial: 10 -ve poor compliance, only 4 completed Snoek et al., 2000 Handmaster Final: 7 the training period

Conclusion

There is level 4 evidence (from two pre-post studies; Alon and McBride, 2003; Snoek et al., 2000) that with sufficient practice using the NESS H200 is a reliable way to regain grasp, hold and relsease abilities in tetraplegic patients.

The NESS H200 represents a reliable non-invasive alternative for individuals with tetraplegia with the goal of regaining some functional grasping abilities.

9.1.3 Bionic Glove Developed by Prochazka and colleagues at the University of Alberta the Bionic Glove improves hand function in people with SCI. This device uses three channels of electrical stimulation to stimulate finger flexors, extensors, and thumb flexors. The control signal comes from a wrist position tranducer mounted in the garment. The actual functioning of the device can be described as greatly augmenting tenodesis (Popovic et al., 2006; Prochazka et al., 1997).

The Bionic Glove is designed to enhance the tenodesis grasp in subjects that have a voluntary control over the wrist (flexion and extension). Stimulates finger flexors and extensors during tenodesis grasp, enhances strength of grasp. The Bionic Glove is available at the University of Alberta, Alberta, Canada and used primarily for clinical evaluation. A modified version of this device will be called Tetron (Popovic et al., 2002).

Overall acceptance rate for long-term use is reported in 30% of potential users. Functions of power grasp and handling of big objects were significantly improved (Popovic et al., 2002). There have been several identified concerns with the device that include damage to the stimulator located on the forearm that is frequently damaged through accidental contact during functional activities and the transducer mechanism is delicate and has to be replaced frequently (Popovic et al., 2001b).

Table 29 Bionic Glove Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Mean age: 26.5 yr; Level of 1. QIF: mean was 19.0±6.5 at the injury: C5-C7; Severity of injury: beginning; at the end 28.4±5.2, Popovic et al., 1999 complete=10, incomplete=12; Length of improvement of 49.5%. Yugoslavia experience with device: ≥6 mo. 2. FIM: 63.8±10.4 at the beginning; Case Series Intervention: Taught how to use the 79.0±8.9 after six mo. When three N=12 device. clients excluded who had 120 points on FIM scores were beginning

Author Year Country Research Design Methods Outcome Score Total Sample Size Outcome Measures: Quadriplegia Index 44.4±13.5 and 64.8±16.6 after six of Function (QIF), Functional mo (increase of 20.4 points/46%). Independence Measure (FIM), Upper 3. Functional task completion: six Extremity Function Test, Goniometric subjects continued to use the Measurements. device. On average, 75% of the functions were performed better after six mo of use. 6/12 (50%) did not continue to use the device. C6- C7 individuals may find the device beneficial enough to use it as an assistive device. 4. Technical improvements, specifically cosmetics, positioning of the electrodes, donning/doffing, should increase the number of regular users. 5. Best candidates are individuals with complete C6-C7 tetraplegia. 6. FIM score between 25-50 (up to 75), QIF between 0-13 (up to 27), are motivated to use it, can demonstrate efficient grasp. Population: Age: 22-42 yr; Gender: 1. Mean peak force of tenodesis grasp males=8, females=1; Level of injury: C6- in the nine subjects increased from C7; Time since injury: 16 mo–22 yr. 2.6 N±3.8 N (passive) to 11.3 N±7.4 Intervention: Use of bionic glove. N (glove active), significant than Prochazka et al., 1997 Outcome Measures: Mean peak force of peak passive force (p=0.0064, t- Canada tenodesis grasp, Qualitative ratings of test), and significant at end of fifth Case Series manual tasks. grasp 6.8 N±4.2 N, p=0.0064, Mann- N=9 Whitney rank sum test. 2. Most manual tasks improved significantly with the use of the glove.

Table 30 Summary Bionic Glove Author N Intervention Main Outcome(s) +ve QIF Popovic et al., 1999 12 Bionic Glove +ve FIM +ve UE Function Test +ve grasp Prochazka et al., 1997 9 Bionic Glove +ve compliance (60%)

Conclusion

There is level 4 evidence (from two case series; Popovic et al., 1999; Prochazka et al., 1997) that the Bionic Glove can provide an increase in upper limb functioning and motor function.

The Bionic Glove can be successfully used in SCI patients who still have voluntary control over the wrist to enhance tenodesis grasp.

9.1.4 ETHZ-ParaCare System The ETHZ-Para Care System was developed collaboratively between ParaCare, the University Hospital Zurich, the Rehabilitation Engineering Group at Swiss Federal Institute of Technology Zurich and Compex SA, Switzerland. The system was designed to improve grasping and walking function in SCI and stroke patients. Surface stimulation FES system is programmable, with four stimulation channels and can be interfaced with any sensor or sensory system. The system provides both palmar and lateral grasps. The device has some reported disadvantages that include a lengthy time to don and doff the device (seven to ten minutes) and it is not commercially available. The next generation of the device will be called the Compex Motion (Popovic et al., 2001; Popovic et al., 2006). The Compex Motion device is currently available in clinical trials with approximately 80 units available. The Compex Motion stimulator was designed to serve as a hardware platform for the development of diverse FES systems that apply transcutaneous (surface) stimulation technology. One of the main advantages in this system is that it is easily programmable (Popovic et al., 2006).

Table 31 ETHZ ParaCare and Compex Motion Systems Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Age: 15-70 yr; Gender: 1. Cervical SCI patients can benefit males=9, females=2; Level of injury: C5- from transcutaneous FES of hand C7; Severity of injury: AIS A-D. muscles during rehabilitation with Intervention: FES was carried out with a respect to muscle strengthening, stationary stimulation system and two facilitation of voluntary muscle portable systems (ETHZ-Paracare FES activity and improvements of ADL Mangold et al., 2005 system, and Complex Motion). functions. Switzerland Outcome Measures: Videos of functional 2. Surface FES system is more flexible Case Series tasks: hand function tests, Self-designed in its application and does not need N=11 functional tests, Follow-up query- surgical procedures. assessment of muscle strength. 3. High flexibility in electrode placement, stimulation programmes, and FES control devices is required in order to adapt the system to individual needs.

Table 32 Summary ETHZ ParaCare and Complex Motion Systems Author N Intervention Main Outcome(s) +ve Training Programme ETHZ-ParaCare FES System +ve Functional exercises in therapy Mangold et al., 2005 11 and Compex Motion =ADL function in rehab centre -ve ADL use at home

Conclusion

There is level 4 evidence (from one case series; Mangold et al., 2005) that the ETHZ-ParaCare System represents a specific niche in flexible neuroprosthesis options as the placement of the electrodes is flexible (non-surgical) and has

shown positive outcomes in rehabilitation and the ability to perform daily living tasks.

The ETHZ-ParaCare System is not yet commercially available and therefore does not represent a current option for the majority of patients with SCI. However, future models should be considered if commericially available.

9.1.5 Stimulus Router System The Stimulus Router System (SRS) is an externally controlled neuroprosthesis that has only one component implanted (passive lead, pick-up terminal) under the skin and the other end (delivery terminal) is tunneled to a target nerve. A surface electrode is placed over the implanted pick-up terminal and a second electrode is placed nearby. Current pulses are passed through the skin between the electrodes. The basic properties of the SRS were explored in two animal experiments (Gan et al., 2007; Gan & Prochazka 2010) which showed that the SRS was reliable as a long term neuroprothesis and was able to selectively activate deep-lying nerves in a graded manner over the full physiological range. A case study of the first implant of the SRS in a person with tetraplegia with bilateral hand paralysis was completed (Gan et al., 2012) which showed initial success of the system.

9.1.6 Exo-Glove

The Exo-Glove is a soft, wearable, lightweight, hand robot that uses soft tendon routing system and an underactuation mechanism (It et al., 2015). The Exo-Glove has been tested among healthy subjects and in one participant suffering from paralysis of the hand secondary to SCI. The use of the glove was reported to have aided in grasping various objects among the individual with SCI (It et al., 2015). Other devices for use among SCI injured individuals that have been tested within larger research studies are presented below.

Table 33 Other Surface or Percutaneous Neuroprosthesis Systems

Author Year Country Score Methods Outcome Research Design Total Sample Size Population: Mean age: 40.5±13.0 yr; 1. No significant change in MAS scores Gender: males=8, females=2; Level of (p=0.371) or ISNCSCI scores injury: C2-C3=3, C4-C7=7; Mean ASIA (p=0.299 for motor, p=0.459 for motor score: 15.8±3.9; Mean time since sensory-light tough, p=0.343 for injury: 3.0±1.1 yr. sensory-pin prick). Intervention: Test effect of assisted 2. Strength test scores increased movement with enhanced sensation significantly for MCP extension (AMES) using vibration to antagonist (p≤0.01) and flexion (p≤0.05) and for muscle to reduce impairments and restore wrist extension (p≤0.001) and flexion Backus et al. 2014 upper limb function in people with (p≤0.01). USA incomplete tetraplegia. Two or three 3. Active motion test scores increased Pre-Post sessions over 9-13 wk per participant. significantly for MCP joints (p≤0.001) N=18 Outcome Measures: Strength and active and wrist (p≤0.001). motion tests on the AMES device, 4. Out of GRT, VLT and CUE scores, International Standards for the only GRT scores were significantly Neurological Classification of SCI improved after training and slightly (ISNCSCI) motor and sensory between posttreatment and 3-mo post examinations, Modified Ashworth Scale treatment (p=0.025). (MAS), grasp and release test (GRT), Van Lieshout Test (VLT), Capabilities of Upper Extremity questionnaire (CUE). Population: Injury Group (n=29): Mean 1. No significant difference between age=37.8±13.3 yr; Injury etiology: spinal scenarios 1 and 2 in room/object cord=23, post-stroke locked in selection, validation times and number syndrome=2, arthrogryposis=1, quadruple of failures for controls and patients amputee=1, cerebral palsy=1, spinal (p>0.05). muscular atrophy=1; Controls (n=34): 2. Statistically significant difference Mean age=32.4±11.2 yr. between scenario 2 and 3 in object Intervention: No intervention. To evaluate selection time for controls and patients the reliability and functional acceptability of (p<0.05) but not for number of object the ‘‘Synthetic Autonomous Majordomo’’ selection failures (p>0.05). (SAM) robotic aid system in a domestic 3. Patients took significantly longer to Coignard et al. 2013 environment using three multi-step select the room and the object than the France scenarios: selection of the room in which controls did (for room selection in Observational the object to be retrieved was located, scenarios 1 and 3 and for object N=63 selection of the object to be retrieved, the selection in all three scenarios) grasping of the object itself and the robot’s (p<0.05). return to the user with the object. 4. No significant patient vs. control Outcome Measures: Selection time (time differences in the number of failures between task’s “start” command and (p>0.05). room/object selection click), Number of 5. Experience of computer use had failures, Qualitative questionnaire. significantly affected speed of task for patients in scenario 3 (p<0.05) and controls in all scenarios (p<0.05). 6. Overall, the robot was found to be acceptable by both patients and control participants.

Population: Mean age: 44.8±16.3 yr; 1. Significant improvements in aim and Gender: males=8, females=2; Level of smoothness (p=0.03). injury: C4-C6=10; Severity of injury: AIS-A 2. No changes in deviation, mean speed, complete=3, AIS-B incomplete=4, AIS-C peak speed and duration of movement incomplete=1, AIS-D incomplete=2; Mean was found. time since injury: 4.7±2.5 yr. 3. No changes in motor strength of Intervention: Chronic tetraplegic SCI trained right arm (p=0.4) or untrained patients participated in a 6-wk wrist-robot left arm (p=0.41). training protocol (1hr/day, 3 times/wk) to 4. No significant changes in MAS of evaluate feasibility, safety and either arm (p>0.05 for both). Cortes et al. 2013 effectiveness on upper limb. 5. No significant changes in pain levels USA Outcome Measures: Motor performance, after training (p=0.99). Pre-Post Corticospinal excitability, Upper extremity 6. There were no changes in any N=10 Motor score (UEMS), Visual Analogue neurophysiological parameters after Scale (VAS), Modified Ashworth Scale the 6-wks of training (p>0.05). (MAS), resting motor threshold (RMT), 7. Strong positive correlation between Motor evoked potential (MEP) amplitude change in smoothness according to and latency at rest, MEP facilitation. the initial spasticity level (R2=0.403); change in aim was positively correlated with initial spasticity in trained arm (R2=0.123) 8. Initial UEMS and MEP amplitude had no correlation with the change on smoothness and aim.

Conclusion

There is level 4 evidence (from two pre-post studies; Backus et al., 2014; Cortes et al., 2013) that the Exo-Glove can be safely used in patients with tetraplegia to significantly improve upper limb effectiveness.

There is level 5 evidence (from one observational study; Coignard et al., 2013) that in a real-world home environment the functionality of the Exo-Glovemay be limited, and that healthy controls still exhibit greater control over the robotic device than those with SCI.

The Exo-Glove is a non-invasive safe option for SCI and tetraplegic patients, although the real-world functionality of it may be limited and can be hard to use based on individual functioning.

9.1.7 NEC-FES System The Sendai FES team in corporation with NEC Inc. 1994 developed the NEC-FES System. The system is to restore both grasping and walking abilities. It is an implanted FES system with 16 stimulation channels. It is used almost exclusively for research purposes and is not available outside Japan.

9.1.8 Rebersek and Vodovik (1973) Neuroprosthesis This is one of the first FES systems developed for grasping three decades ago. The device has three stimulation channels (two stimulation electrodes per channel) that are used to generate the grasping function by stimulating finger flexors and extensors and thumb flexors. The user can control the stimulation intensity via different sensory

interfaces such as EMG sensor, sliding resistor, and pressure sensors. The main reported disadvantages of the system are the long donning and doffing times and the selectivity of stimulation is low. This device is not commercially available (Popovic et al., 2001).

9.1.9 Belgrade Grasping-Reaching System The Belgrade Grasping-Reaching System (BGS) as proposed by Popovic et al. (1998) is a neuroprosthesis device designed for grasping and it also provides a reaching function. The device has four stimulation channels (three for generating grasping function and fourth to stimulate triceps brachii muscle for elbow extension). The grasping function is controlled via a push button that triggers hand opening and closing. The motion of grasp is performed in three phases; prehension that forms the correct aperature of the hand, a relaxation phase that allows the hand to get into good contact with the object and closure of the hand by opposing either the palm and the thumb or side of index finger and thumb. The act of hand release is completed in two stages; opening of the hand and resting. Measuring the subject’s shoulder velocity with a goniometer and then generating a synergistic elbow motion by stimulation of the triceps brachii muscle achieves the reaching function of the upper limb. It is reported that the BGS system requires more time to place electrodes compared to Handmaster system, and it is not commercially available (Popovic et al., 2002).

9.3 Myoelectrically Controlled Neuroprostheses Second generation neuroprosthesis being developed at Case Western Reserve, Cleveland, OH, USA, provides control of grasp, forearm pronation and elbow extension through the use of electromyographic signals generated by voluntary musculature used to control the various functions of the NP. The system consists of an implanted stimulator-telemeter (IST-12), implanted electrodes for stimulation and recording, an external control unit and a transcutaneous inductive link. The EMG signals can be obtained from two independent muscles. The IST-12 is capable of stimulating 12 different muscles. The design feature of the IST-12 enables the size of the implanted components to remain small and provides the opportunity for customized control algorithms and stimulation patterns. The NP functions controlled via EMG signal includes grasp pattern selection (two to four grasp patterns), opening and closing the hand in a proportional manner, turning the system on and off, turning elbow extension on and off, and the ability to lock and unlock the hand so that the grasp can be maintained in a fixed position without the need for continued control input. One EMG channel is used to control grasp opening and closing and is generally placed on the most distal UE muscle under voluntary control, typically the extensor carpi radialis longus (ECRL) and brachioradialis (Br). The second EMG channel is used to provide state or logic commands such as system on/off and selection of grasp pattern. The latter channel is placed on a more proximal muscle such as trapezius and platysma. All of the control signals are derived from ipsilateral muscles, enabling bilateral function to be provided by implementing a second system in the contralateral limb (Kilgore et al., 2008).

Augmentive surgical procedures (arthrodeses, tendon transfers and tendon synchronization using side by side repair) to the hand and arm are often performed at the same time of the implantation to provide improved hand function when the IST-12 is not being used and to further optimize the system with electrically stimulated transfers (Kilgore et al., 2008).

Further research is also being completed on an implantable stimulator and wearable external controller (Micropulse) at the Cleveland FES Centre, Cleveland, USA. The controller, under going benching testing, is worn on the wrist and wirelessly communicates with the implantable stimulator (Wheeler & Peckham 2009).

Table 34 Second Generation Neuroprosthesis: Myoelectrically Controlled Author Year Country Research Design Methods Outcome Score Total Sample Size Population: Mean age: 34.0±9.5 yr; 1. Functional Outcomes: all three Level of injury: C5=1, C6=2. subjects used their NP to perform Intervention: A second generation activities that they could not perform neuroprosthesis system was implanted prior to implantation (post implant into individuals and functional outcomes follow up ranged from 2-4 yr). were evaluated. 2. Body Structures and Function: every Outcome Measures: Grasp and Release subject improved in pinch force Test (GRT), Activities of Daily Living strength; post op pinch force with Abilities (ADLAT), Craig Handicapped the NP was significantly greater than Assessment and Reporting Tool without the NP (paired-sample t-test, (CHART), NP Usage Survey. p=0.038). 3. Activities: every subject was able to Kilgore et al., 2008 double the number of objects USA manipulated in the GRT with NP Pre-post (two subjects completed 6/6 tasks; N=3 one subject 5/6 tasks) 4. ADLAT all three subjects improved in least five activities with one subject in all nine. 5. Participation: all three subjects increased their scores for physical independence, one in the mobility task, one in the social integration scale, one subject a decrease in occupation subscale. 6. Device Usage: 2/3 reported daily usage of the NP; 1/3 used the device 50% of the time.

Discussion

The study by Kilgore et al. (2008) studied the first three individuals to receive a myoelectrically controlled NP (IST-12) designed for hand and arm function. The IST-12 can stimulate 12 different muscles versus the first-generation NP (Freehand System) which only stimulated eight muscles. The additional electrodes provided the user with improved hand function (activation of the intrinsic muscles), wrist extension, improved reach (triceps function) and improved shoulder stability through activation of the shoulder musculature. The IST-12 provided each of the three subjects with significantly

increased pinch force and grasp function which resulted in increased independence with ADL functions. All three study subjects used the device at home on a regular basis. The durability of the implanted components was comparable to long-term results from the first-generation NP, an incidence failure of <2%.

Thorsen et al. (2013) tested the myoelectrically controlled FES (MeCFES). This system consists of an amplifier, a signal processor and single-channel stimulator that allows the user to proportionally control the stimulus intensity to reinforce the tendosis grip in subjects with C6-7 tetraplegia. Participants received occupational therapy with and without the MeCFES. Immediate improvements were found in upper limb functioning with the use of the MeCFES and these improvements were maintained post-treatment (Thorsen et al., 2013).

Finally, there have been initial studies on exoskeleton robots (controlled by electromyographical signals (EMGs) of the user) (Ueda et al., 2010), the five degree of freedom user command controller (Scott & Vare 2013) and the use of robotic training for improving hand and upper limb control (Cortes et al., 2013; Zariffa et al., 2012b; Vanmulken et al., 2015). Feasibility studies suggest that robot–assisted technology may be easy to learn and perform, yet, further research is necessary to determine the potential for improving upper limb functioning, and when rehabilitation using robot- assisted technologies may be most beneficial (Vanmulken et al., 2015).

Conclusion

There is level 4 evidence (from one pre-post study; Kilgore et al., 2008) that the use of the IST-12, a second generation neuroprosthesis, combined with augmented surgical procedures (arthrodesis, tendon transfers and tendon synchronization) improved pinch force, grasp function and the functional abilities of individuals with cervical level spinal cord injuries.

There is level 4 evidence (from one pre-post study; Thorsen et al., 2013) that the use of the MeCFES, a second generation neuroprosthesis, in combination with occupational therapy improved tenodesis grip in people with tetraplegia.

The IST-12 neuroprosthesis, a second generation, myoelectrically controlled implantable device appears to have a positive effect on pinch and grasp functions which result in increased independence with activities of daily living.

The MeCFES neuroprosthesis, a second generation, myoelectrically controlled FES device appears to have a positive effect on tenodesis grip.

10.0 Brain Interface Neuroprostheses

Content coming soon, SCIRE Edition 7, 2018.

11.0 Virtual Reality

Content coming soon, SCIRE Edition 7, 2018.

12.0 Summary

The treatment and management of the upper limb in persons with a SCI can be rewarding yet very challenging. Secondary complications related to repetitive strain injury, pain, and hypertonicity in addition to aging presents numerous challenges for both the injured individual and the clinician. In reviewing the critical evidence of treatment interventions there are fewer studies than may be expected on the effectiveness of traditional interventions such as strengthening, exercise, splinting, and management of hypertonicity. The majority of research for the upper limb has been focused on reconstructive surgery and the use of neuroprosthesis. Advancements in understanding the mechanisms related to SCI has led to restorative treatment interventions especially in the management of the incomplete SCI person.

This chapter outlined the importance in the prevention of upper limb dysfunction and the impact of an injury in one’s overall level of basic independence in the areas of self-care and mobility. Further research and consensus is needed in how we assess and document upper limb function, especially hand function in an effort to establish objective, reliable and measurable outcomes. Other areas for further research have been identified throughout the chapter.

There is level 1b evidence (from one randomized controlled trial; Rice et al., 2014) that education improves wheelchair skills after 1- year post discharge.

There is level 1b evidence (from one randomized controlled trial; Needham- Shrophire et al., 1997) that neuromuscular stimulation-assisted exercise improves muscle strength over conventional therapy.

There is level 5 evidence (from one observational study; Bunday et al., 2014) that the control of precision grip involves premotoneuronal subcortical mechanisms, which are lacking after SCI. There is level 1a evidence (from two randomized controlled trials; Kohlmeyer et al., 1996; Popovic et al., 2006) that augmented feedback is not effective in improving upper limb function in tetraplegia.

There is level 4 evidence (from one pre-post test; Bruker and Bulaeva, 1996) that EMG biofeedback sessions can significantly improve normal EMG muscle test scores of both triceps.

There is level 4 evidence (from one case series study; Burns & Meythaler 2001) that intrathecal baclofen may be an effective treatment for upper extremity hypertonia of spinal cord origin.

There is level 2 evidence (from one randomized controlled trial; Gomes-Osman & Field-Fote, 2015) that showed that tDCS, TENS, and vibration therapy resulted in significant improvements in upper extremity function and pinch strength.

There is level 4 evidence (from one pre-post study; Belci et al., 2004) that showed therapeutic TMS can lower intracortical inhibition, which is linked to better clinical motor scores.

There is level 4 evidence (from one pre-post study; Nasser et al., 2014) that showed massed practice and somatosensory stimulation significantly improved

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motor function and pinch grip strength compared to traditional rehabilitation programs over time.

There is level 2 evidence (from one randomized controlled trial; DiPasquale- Lehnerz 1994) that wearing a thumb opponens splint will improve pinch strength and functional use of the hand.

There is level 4 evidence (from one post-test study; Stahl et al., 2015) that among persons with chronic SCI motor planning for aperture modulation is preserved.

There is level 1b evidence (from one randomized controlled trial; Dyson-Hudson et al. 2001) that general acupuncture is no more effective than Trager therapy in reducing post-SCI upper limb pain.

There is level 5 evidence (from one observational study; Akbar et al., 2014) that people with paraplegia are significantly more likely to develop bilateral carpel tunnel syndrome

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There is level 4 evidence (from seven case studies; Meiners et al., 2002; Lo et al., 1998; Failla et al., 1990; Gansel et al., 1990; Rieser and Waters, 1986; Kelly et al., 1985; Colyer and Kappleman, 1981) that pinch and grasp reconstructive surgeries are effective in increasing motor function, strength, and grip of the hand. Patients are also report high satisfaction with their surgical results. There is level 2 evidence (from one prospective control trial; Rabischong et al., 1993) that surgery can increase rotation in the elbow and the relationship with peak torque.

There is level 3 evidence (from one case-control; Dunkerley et al., 2000) that PD to triceps surgical intervention can have limited/similar results to controls when examining functional outcome.

There is level 2 evidence (from one RCT; Mulcahey et al., 2003) that biceps to triceps surgery can increase elbow extension strength, reaching, and overall performance improvement.

There is level 4 evidence (from two case series; Kozin et al., 2010; Kuz et al., 1999) that elbow extension surgery improves elbow extension and overall functionality of the joint.

There is level 4 evidence (from one pre-post study; Friden et al., 2012a) that multiple reconstructions can improve key-pinch andgrip strength.

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There is level 4 evidence (from one post-test; Gregersen et al., 2015) that a variety of reconstructive surgeries can be used to improve overall elbow function and strength.

There is level 2 evidence (from one cohort study; Fox et al., 2015b) that the risk of negative outcomes, such as postoperative decline compared to baseline, for nerve transfer surgery are low.

There is level 5 evidence (from one observational study; Kang, 2013) that pinch force can be increased with the use of an orthosis, and with greater efficiency

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There is level 4 evidence (from two case series; Popovic et al., 1999; Prochazka et al., 1997) that the Bionic Glove can provide an increase in upper limb functioning and motor function.

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