325

NeuroRehabilitation 35 (2014) 325–340 DOI:10.3233/NRE-141124 IOS Press

Spinal cord injury rehabilitation: Which way forward? Mohammad Karimia,∗ , Abdul Hafidz Haji Omarb,c and Francis Fatoyec a Rehabilitation

Faculty of Isfahan University of Medical Sciences, Isfahan, Iran of Sports Innovation and Technology, University Technology of Malaysia, Kuala Lumpur, Malaysia c Department of Health Professions, Manchester Metropolitan University, Manchester, UK b Centre

Abstract. BACKGROUND: Spinal cord injury (SCI), damage to spinal cord, influences the ability of the subjects to stand and walk. Moreover, they have some problems such as osteoporosis, muscle spasm, joint contracture and bowel and bladder function. These subjects use various orthoses and undergo different rehabilitation programmes to restore their ability. It is controversial whether use of aforementioned methods improves the physiological health of SCI individuals and improves their ability to ambulate or not. Therefore, the aim of this review was to investigate the effectiveness of assistive devices to restore their physiological health and their functional ability in patients with SCI. METHOD: A search was done in some databases such as Medline, Embasco, and ISI Web of sciences between 1960 and 2013. The quality of studies was assessed using the Down and Black tool. RESULTS: Two hundred articles were found based on the selected key words. Sixty papers were selected for final analysis, of which 35 and 45 focused on benefits of standing and walking, performance of SCI during standing and walking with various systems, respectively. CONCLUSION: Although there was lots of variation between the studies based on the number of subjects, level of lesion, type of lesion and time post injury, it can be concluded that use of various orthoses neither improve the abilities of subjects to stand and walk nor improve their physiological health. It may be concluded that the use of other methods of exercise may have more physiological benefits for SCI subjects. Keyword: Spinal cord injury, physiological health, walking ability, orthosis, hybrid, functional electrical stimulation, robotic

1. Introduction Spinal cord injury (SCI) is a damage or trauma to spinal cord resulting to loss of function, mobility and sensation depends on the levels and types of injury (Stolov & Clowers, 1981; Wyndaele & Wyndaele, 2006). The incidence of SCI in varies among different countries. It varies from 12.7 in France to 59 new cases per million, each year in the United State of America (Chen et al., 1997; Karacan et al., 2000; ∗ Address for correspondence: Mohammad Karimi, Rehabilitation Faculty of Isfahan University of Medical Sciences, Isfahan, Iran. Tel.: +98 3137922021; Fax: +98 3136687270; E-mail: [email protected].

Karamehmetoglu et al., 1995; Maharaj, 1996; O’Connor, 2005; Subbarao, Klopfstein, & Turpin, 1995; Surkin, Gilbert, Harkey, Sniezek, & Currier, 2000; Wyndaele & Wyndaele, 2006). It has been estimated that more than 230000 and 400000 SCI cases are living in the USA and UK, respectively (NSCISC, 2001; Wyndaele & Wyndaele, 2006). Individuals with SCI may have difficulty in standing and walking depending on the level of injury. These individuals also use various types of assistive devices (orthosis) and wheelchairs to ambulate from a place to place (Somers, 1992). However, paralysis whether partial or complete may lead to development of complications in other parts of body. Some compli-

1053-8135/14/$27.50 © 2014 – IOS Press and the authors. All rights reserved

326

M. Karimi et al. / Spinal cord Injury Rehabilitation

cations such as, reduce bone mineral density (BMD) (long bone fracture), respiratory, gastrointestinal and cardiovascular, skin breakdown, musculoskeletal and psychological problems are the main disorders association with SCI injury (NSCISC, 2001; Somers, 1992). Various types of methods have being used to restore functional ability of the subject to stand and walk and to decrease the complication with SCI (Somers, 1992). Some orthoses such as ankle foot orthosis (AFO), knee ankle foot orthosis (KAFO), hip knee ankle foot orthosis (HKAFO), have been designed to stabilize paralyzed joints and to improve the ability of individuals with SCI to stand and walk (American Academy of Orthopaedic Surgeons, 1985; Kent, 1992; Merkel, Miller, Westbrook, & Merritt, 1984). Hip guidance orthosis (HGO) (Major, Stallard, & Rose, 1981; Stallard, 2000), Louisiana State University reciprocal gait orthosis (LSU-RGO) (Douglas, Larson, D’ Ambrosia, & McCall, 1983), Advanced RGO (ARGO) (Jefferson & Whittle, 1990), medial linkage orthosis (MLO)(Middleton, Fisher, Davis, & Smith, 1998), Moroong (MMLO) (Middleton et al., 1998) are some sophisticated orthoses designed for SCI. The ability of these subjects based on energy expenditure during walking, stability during standing and walking speed is not comparable with normal subject (Jefferson & Whittle, 1990; Karimi, 2011a, 2012b; Merkel et al., 1984). Functional electrical stimulation (FES),which is the application of external electrical stimulation to paralysed muscles to restore their function has been used for patients with SCI (Kralj & Bajd, 1989). In the first application of FES for paraplegic subjects, transcutaneous electrodes were used to stimulate quadriceps and gluteus muscles in standing and walking (Stallard & Major, 1995). However, early onset of muscles fatigue, limited walking speed and problems with donning and doffing the electrodes are some important issues associated with the use of FES for SCI individuals (Mirbagheri, Ladouceur, Barbeau, & Kearney, 2002; Stallard & Major, 1995). Hybrid orthosis, which is a combination of mechanical orthosis and FES, is the other approach used in this regard. Various combination of FES with HGO, KAFO, ARGO have been reported in the literature (Baardman et al., 2002a; Baardman et al., 2002b; Ferguson, Polando, Kobetic, Triolo, & Marsolais, 1999; Hirokawa, Solomonow, Baratta, & D’Ambrosia, 1996; Stallard & Major, 1995). There are two main approaches with this method including hybrid system based on the available orthoses and hybrid system based on the new design of the orthoses (Karimi, Sedigh,

& Fatoye, 2012; Karimi, 2011a). Although various approaches have been used in hybrid systems to restore the functional ability in patients with SCI, however, the results were not successful (Maurizio Ferrarin & Pedotti, 1994; Karimi et al., 2012; Karimi, 2012a). The external powered systems employ various kinds of power source including pneumatic, hydraulic and electrical powers (Karimi et al., 2012). These orthoses can be divided into the system used for walking and standing and those designed for therapeutic purposes (Colombo, Wirz, & Dietz, 2001b; Ohta et al., 2007; Tefertiller, Pharo, Evans, & Winchester, 2011; Wessels, Lucas, Eriks, & de Groot, 2010). The concept of hybrid exoskeletons (used for walking), introduced in 1978 and was not reported until 1989. They are categorized based on exoskeleton joint actuation principle employed such as breaking or clutching and active joint actuators (DelAma et al., 2012). Driven gait orthosis is a system develops by Hocama AG Medical Engineering in Staefa at rehabilitation center Para Care of the University hospital Balgrist in Zurich, which stimulate the motions of the leg and pelvic while subjects walking on a treadmill (Colombo, Wirz, & Dietz, 2001a). There are two main reasons to use several of the aforementioned systems for paraplegic subjects. The first reason is to restore the ability of the subjects to stand and walk. It means that SCI individuals use these devises to ambulate from a place to place. The second reason is for therapeutic benefits (Karimi et al., 2012; Karimi, 2011a). It has been mentioned that decreasing decubitus ulcers, osteoporosis, joint deformities, especially hip joint flexion and adduction deformities, improving the performance of cardiovascular and digestive systems, are the main benefits associated with the use of orthosis (American Academy of Orthopaedic Surgeons, 1985; Douglas et al., 1983; Karimi, 2011a). To date, it is unknown whether the use of the aforementioned systems restores functional ability of the subjects or not. In addition, the main benefits of the using these orthoses and using these approaches have not been well documented. It is currently uncertain if there are any other approaches that can be used to achieve the mentioned benefits. Understanding the benefits associated with the use of orthoses in patients with SCI may highlight the best approach in rehabilitation for these individuals. Therefore, the aim of this review was to determine the benefits of using various rehabilitation approaches for SCI individuals based on the available literature.

M. Karimi et al. / Spinal cord Injury Rehabilitation

2. Method An electronic search was done in databases of PubMed, Embase, and ISI web of knowledge to extract the data related to the year 1960–2013. The following keywords were used for the search: spinal cord injury and paraplegia in combination with, rehabilitation, walking, standing, robotic orthosis, orthosis, mechanical orthosis, powered orthosis, exoskeleton, functional electrical stimulation and hybrid orthosis. In the first step the title and abstracts of each study was evaluated by the first author based on whether the title and abstract addressed the research question of interest or not. The quality of all the relevant papers extracted was assessed using the Down and Black checklist. This tool consists of 28 questions divided into four categories including, reporting, external validity, internal validity (bias), internal validity (confounding). This tool ranges from 0 to 28, which the higher score indicating higher methodological quality (Downs & Black, 1998). The collected papers were categorized based on the benefits of walking and standing with orthosis, ability to do other types of exercise and interventions, the performance of SCI while standing and walking with mechanical, hybrid, and external powers orthosis. The results of some research done on normal subjects walking with an orthosis was also provided to high light the best performance which can be achieved by use of orthosis. It is mentioned that the best performance which can be enhanced during walking of SCI individuals will be the performance of normal subjects when walking and standing with an orthosis (Karimi, Spence, Nicol, & Solomonidis, 2010).

3. Results In the first step 200 papers were found. Based on the mentioned criteria, 60 papers were used for final analysis, of which 20 focused on the benefits of standing and walking with orthoses, 18 on the performance of subjects walking with mechanical orthosis, 4 on FES, 10 on hybrid orthosis and 4 on external powered orthosis. Moreover, there were 4 papers focused on the performance of normal subjects while walking with orthosis. The quality of the papers based on the Down and Black checklist is summarized in Table 1. The effect of SCI on BMD of spine and lower extremity bones is shown in Table 2. As can be seen from this table, the results of various studies confirmed that the

327

Table 1 The number and quality of the studies on SCI rehabilitation Studies Physiological health Mechanical orthosis Hybrid orthoses FES External powered orthoses Orthosis on normal subjects

Number

Quality (out of 28)

20 18 10 4 4 4

20 15 14 16 13 16

BMD decreased significantly follow SCI. Table 3 represents the effect of walking and standing on BMD. There were 12 papers on the effect of FES on the BMD of the long bone. Based on the results of these studies it is controversial weather using FES influences BMD or not (Table 4). In Table 5, the outputs of 10 papers regarding the effects of using FES and orthosis on muscle spasm are summarized. Tables 6 and 7 show the stability of SCI subjects in static and dynamic conditions. In Tables 8 and 9 the walking performance of SCI with different levels of spinal lesion and with various orthoses are summarized. As can be seen from these tables, walking speed of SCI subjects varied between 1.68 and 59.9 m/min. There were a few studies reported the force applied on the crutch during walking. The energy consumption of the subjects walking with different orthoses is shown in Table 10. The energy consumption of SCI subjects based on Physiological cost index (PCI) varied between 0.95 to 11.5 beats/m. In contrast, the PCI of normal subjects walking with orthosis was between 0.61 and 0.7 beats/min (Table 11). 4. Discussion Although lots of research studies have been done on rehabilitation of SCI, the quality of most of the studies are poor, Table 1. The number of subject was too limited and also level of lesion differed significantly between the studies. The time of post injury, kind of lesion (complete or incomplete), time of involvement in the studies varied amongst the studies. Various kinds of methods have been used to enable patients with SCI to stand and walk and to improve their physiological health. These subjects use different orthoses and wheelchair to ambulate from a place to place. However, there is another point of view which is the use of orthosis and other assistive devices to influence the general health of SCI, to decrease bone osteoporosis, to improve cardiovascular and digestive functions and to decrease urinary tract infection (Karimi

T4-T5 C4-T12

80 myelomeningocle 46 complete and incomplete SCI

(Rosenstein, Greene, Herrington, & Blum, 1987) Sabo et al., 24, 25

C7-L1

Lesion level

8 complete SCI

Number

(S. F. Biering, Bohr, & Schaadt, 1990)

References

1–26 years

–

41 months

Time post injury

Methods

BMD of distal radius and tibia was measured. BMD of proximal and distal femur was measured.

BMD of proximal tibia and lumbar spine was evaluated after 41 months of injury.

Procedure

Table 2 The bone mineral density (BMD) of subjects with spinal cord injury (SCI)

BMD remained unchanged in lumbar spine, but decreased to 50 to 70 % at proximal of tibia. The effect of ambulatory is less important than that of neurological status. BMD does not depend on lesion level and ambulatory status. Every effort should be done to prevent incomplete injury to complete.

Results

328 M. Karimi et al. / Spinal cord Injury Rehabilitation

C8-T12

21

2.2 years

–

2–25 years

19 years 1 year

Time post injury

Methods

The subjects were asked to stand one hour per day, five times per week and for 12 to 24 months. The subjects were trained to walk with RGO hybrid orthosis. They were trained between 3–14 months (2 sessions, three times a week). BMD was measured in lumbar spine and femoral neck.

BMD of lumbar spine, femoral neck and shaft and proximal tibia was evaluated.

The subjects stud 144 days per 135 days. BMD of femur was measured one year after walking with KAFO.

Procedure

BMD = Bone Mineral Density, KAFO = Knee Ankle Foot Orthosis, RGO = Reciprocal Gait Orthosis.

–

54

(Alekna, Tamulaitiene, Sinevicius, & Juocevicius, 2008) (Thoumie et al., 1995)

C6-L4

– –

Lesion level

26 complete SCI

6 53

Number

(S. Biering, Bohr, & Schaadt, 1988)

(Kunkel et al., 1993) (Goemaere, Van Laere, De Neve, & Kaufman, 1994)

References

Table 3 The effect of walking and standing on BMD in SCI subjects

No change seen in bone mineral density.

Standing did not modify BMD in any sites. A significant change was seen on proximal part of femur. Mechanical loading influences on prevention of bone mass. BMD of femoral neck and shaft of femur decreased by 25%. BMD of Proximal part of tibia decreased by more than 50%. Using KAFO did not influence BMD. Leg BMD reduced by 19.6% in standing group and 24% in none standing group.

Results

M. Karimi et al. / Spinal cord Injury Rehabilitation 329

–

15

24 20 6 9

12

(Lai et al., 2010)

(Sloan et al., 1994)

(Leeds et al., 1990)

(Bloomfield, Mysiw, & Jackson, 1996)

(Needham-Shropshire et al., 1997)

–

C5-T7

–

–

–

–

4 complete

(Shields & Dudley-Javoroski, 2007) (S.C. Chen et al., 2005)

C5-T5

14

(Belanger, Stein, Wheeler, Gordon, & Leduc, 2000)

C5-T10

C5-T10

12 complete and incomplete 37

(Hangartner et al., 1994)

T1-T12

6 complete

(Needham-Shropshire et al., 1997) (Rodgers et al., 1991)

C6-T4

Lesion level

10

Number

(Mohr et al., 1997)

References

9.7

6

–

1–4

0.12–0.6

–

2

–

0.1–22.4

0.6–17

3.8

–

Time post injury

FES cycling done for 3 months followed by 3 months no exercise Combination of FES cycling and physical exercise was used. FES cycling was used to improve the BMD of proximal of femur FES cycling was used to improve the BMD of leg bones. The BMD was measured at lumbar spine, femoral neck, distal of femur and proximal part of tibia FES was used to stimulate quadriceps, hamstring and gluteus muscles. The BMD of lumbar and proximal of femur was measured.

FES cycling done for 6 months followed by 6 months no exercise

FES stimulation of soleus

FES stimulation of quadriceps

FES used to stimulate knee extensor

FES used to move lower limb joints

FES used to move lower limb joints

Cycling

Intervention

Methods

–

–

–

–

–

–

0.5

1

–

–

–

0.5

Duration per day

–

–

3

–

–

–

5

5

3

3

–

3

Times per week

Procedure

–

9

6

6–12

3

6

11

8

1–4

12

–

12

Duration (month)

No change in BMD of lower limb bone but a positive trend was seen in the upper spine.

No statistically significant difference was seen after 6 months of training. BMD was increased at lumbar spine. The change of BMD of femoral neck, distal of femur and proximal part of tibia was not significant.

BMD of distal femur and proximal of tibia increased but decreased again. BMD of femoral neck decreased progressively. BMD decrease rate decreased in distal part of femur. BMD did not restore.

BMD measurements revealed a potentially positive effect of FES exercise for rehabilitation of SCI patients. After training the BMD of proximal of tibia and distal of femur improved by 30%. Osteoporosis partly reserved by regular FES. No change to BMD of tibia.

No change in BMD

BMD remained unchanged in lumbar spine, but increased by 10% in proximal part of tibia. BMD remained unchanged.

Results

Table 4 The effect of using functional electrical stimulation (FES) and FES cycling on bone mineral density (BMD) of subjects with spinal cord injury (SCI)

330 M. Karimi et al. / Spinal cord Injury Rehabilitation

1

1

6

4

25

70

6

20

99

152

(Spadone et al., 2003)

(Granat et al., 1993)

(Mirbagheri et al., 2002)

(Middleton et al., 1997b)

(Solomonow et al., 1997)

(Kunkel et al., 1993)

(Ben et al., 2005)

(Dunn et al., 1998)

(Eng et al., 2001)

Number

(Spadone et al., 2003)

References

–

–

–

–

C6-C7

C5-T12

–

C3-L1

T5-T6

T5-T6

Lesion level

Methods

Standing frame

Standing frame

Tilt table

Standing frame

RGO with FES

Walk about

FES

AFO or KAFO with FES

ARGO with FES

ARGO

Type of orthosis

A 17 items questionnaire was sent to participants

The subjects with recent injury were recruited in this study. They were asked to stand on a tilt table for 30 minutes, 3 times and for 12 weeks. The subjects used the device 1 to 6 times per week.

Subjects were asked to stand 144 times per 135 weeks.

The subjected were asked to walk with walk about orthosis and were followed up regularly for two months. The subjects were asked to walk with hybrid RGO for average of 14 weeks (3 hours per week). The spasticity of quadriceps was evaluated after this time.

The effect of 19 months FES assisted walking on ankle mobility was evaluated.

The effects of FES on muscle conditioning, spasticity and bone density were evaluated after a period of walking with ARGO orthosis. The effects of FES on muscle conditioning, spasticity and bone density were evaluated after a period of walking with HARGO. The effect of ambulation with hybrid orthosis on quadriceps spasticity was evaluated.

Procedure

Table 5 The effect of standing and walking on muscles spasm

There was a favorite response by some participants on effect of standing device on bowel regularity and leg spasm. 30% reported they were engaged for prolong standing for average 40 minutes per cession, 3 to 4 times per week. Favour responses were obtained on the effect of orthosis on reflex response.

The results of spasticity analysis showed a reduction in spasticity of quadriceps which extended for at least 24 hours after the use of FES Reflex stiffness decreased by 53% following FES assisted walking. The finding of this research showed that FES assisted walking may have a therapeutic effect and help to reduce abnormal joint stiffness. Maintaince of joint mobility and psychological benefits were the most important outcomes of walkabout usage 33 subjects participated in the survey. Twenty (61%) of them reported a significant reduction in spasm that lasted for 1 and up to 3 days. 2 patients (6%) reported a short term reduction, 3 reported (9%) a slight reduction in spasticity and 5 (15%) reported no change. No important difference was reported between initial and final score of joints range of motion Use of tilt table for 12 weeks had a small effect on ankle mobility.

No change in spasticity

No change in spasticity

Results

M. Karimi et al. / Spinal cord Injury Rehabilitation 331

332

M. Karimi et al. / Spinal cord Injury Rehabilitation Table 6 The stability performance of paraplegic subjects during quiet standing

References

(M. T. Karimi, Amiri et al., 2013) (M. T. Karimi, Amiri et al., 2013) (Baardman et al., 1997) (Baardman et al., 1997) (Middleton et al., 1999) (Middleton et al., 1999)

Methods Number

Lesion level

Type of orthosis

5 5 9 9 9 9

T11-L1 T11-L1 T4-T12 T4-T12 T5-T12 T5-T12

KAFO MTK-RGO ARGO NARGO Linked AFO KAFO

Results COP excursion in AP (mm) 67 17 35.22 37.93 1.75 2.07

COP excursion in ML (mm) 42.7 22.6 41.72 34.94 1.11 1.09

Velocity in AP

Velocity in ML

30.2 7.36 – – – –

31.23 21.02 – – – –

Crutch force (N/BW) 0.12 0 43 59.3 – –

Table 7 The stability performance of paraplegic subjects during doing hand tasks References

(M. T. Karimi, Amiri et al., 2013) (M. T. Karimi, Amiri et al., 2013) (Baardman et al., 1997) (Baardman et al., 1997) (Middleton et al., 1999) (Middleton et al., 1999)

Methods Number

Lesion level

Type of orthosis

5 5 9 9 9 9

T11-L1 T11-L1 T4-T12 T4-T12 T5-T12 T5-T12

KAFO MTK-RGO ARGO NARGO Linked KAFO KAFO

et al., 2012). Although, various methods have being used to enable the SCI subjects to stand and walk, most of them withdrew from being involved in rehabilitation programs (Hawran & Biering, 1996; Karimi et al., 2012; Melis, Torres-Moreno, Barbeau, & Lemaire, 1999; Whittle et al., 1991). It is not clear which kinds of rehabilitation method has more physiological benefits to the patients and also dose the use of designed orthotic devices improve the abilities of the SCI subjects or not. There is no doubt that paraplegic subject use robotic device to ambulate or do different exercise to improve their health. One of the main reasons to use the aforementioned rehabilitation programme is to decrease bone osteoporosis (Karimi et al., 2012). It has been shown that few years after SCI individual with this injury experience a rapid 20%–80% decrease in BMD of long bones. Trabecular and cortical bone loss in tibia was 0/4 to 8% and 1/7% to 32/7%, respectively, Table 2. It has also been shown that excessive immobility of SCI individuals was the most significant factor in determination of bone in trabecular (Hangartner, Rodgers, Glaser, & Barre, 1994). As it can be seen from Tables 2–4 there are 20 studies that focused on bone osteoporosis and influence of rehabilitation programme on improving bone mineral density. Although there are lots of variations between the participants in the research studies in relation to the sample sizes, type of injury, duration of exercise or walking, level of injury and time post injury it is difficult to con-

Results COP excursion COP excursion Velocity Velocity Crutch in AP (mm) in ML (mm) in AP in ML force (N/BW) 87.22 74.2 – – 4.78 5.35

50.17 43 – – 4.94 4.4

71.8 67.2 – – – –

54.28 46.6 – – – –

0.26 0.07 0.22 0.26 – –

clude that walking with orthosis BMD. There were 12 studies that evaluated the effects of other methods of rehabilitation such as functional electrical stimulation, cycling and rowing, using FES and hybrid orthosis, and robotic rehabilitation on BMD of paraplegic subjects. However, in most of these studies no improvement was reported in functional ability of individuals with SCI (Chen et al., 2005; Lai et al., 2010; Leeds, Klose, Ganz, Serafini, & Green, 1990; Mohr et al., 1997; Rodgers et al., 1991; Shields & Dudley-Javoroski, 2007; Sloan, Bremner, Byrne, Day, & Scull, 1994). Based on Mechanostat theory (developed by Harold Frost), the local deformation from the mechanical loading stimulates bone cells and results in bone adaption (Frost, 1987, 2003; Robling, Castillo, & Turner, 2006). It means that bone responses to the loads applied on it. However, two important factors needs to be considered in this regard, these include the magnitude of applied loads and duration of applied load. Based on the results of various research studies the loads applied on body and orthosis is mostly transmitted by body (long bone) and also the role of orthosis to transmit the moments is negligible (Karimi, 2011, 2012; Karimi, Esrafilian, Esrafilian, Sadigh, & Amiri, 2013). Therefore, the time and duration of the applied load are more important. In most of the studies presented in Tables 2–4, the subjects participated in a rehabilitation programme for a short period of time. Therefore, it can be concluded that the time of involvement in a rehabili-

M. Karimi et al. / Spinal cord Injury Rehabilitation

333

Table 8 The walking performance of SCI subjects with various orthoses References

Methods Number Lesion level

Results Type of orthosis

(Merkel et al., 1984) (Merkel et al., 1984)

8 8

C7-T12 C7-T12

(Ijzerman, Baardman, Holweg et al., 1997) (Thoumie, Perrouin-Verbe et al., 1995) (Kawashima, Sone, Nakazawa, Akai, & Yano, 2003) (Baardman et al., 2002b) (Baardman et al., 2002b) (Baardman et al., 2002a) (Baardman et al., 2002a) (Thoumie, Le Claire et al., 1995) (Thoumie, Le Claire et al., 1995) (Thoumie, Le Claire et al., 1995) (Sykes, Campbell, Powell, Ross, & Edwards, 1996) (Sykes et al., 1996) (Thoumie, Perrouin-Verbe et al., 1995) (Thoumie, Perrouin-Verbe et al., 1995) (Shimada et al., 2006)

5

T4-T12

KAFO KAFOwith stiff ankle ARGO

21

–

4

COP excursion COP excursion Velocity Velocity Crutch in AP (mm) in ML (mm) in AP in ML force (N/BW) 8.8–17.5 6.3–15.3

– –

– –

– –

– –

14.4

32

0.89

–

0.33–0.43

RGO

12.6

33.61

0.72

–

–

T8-T12

WBC

19.88

44

–

–

–

1 1 2 2 21 21 21 5

T12 T12 T4-T8 T4-T8 C8-T12 C8-T12 C8-T12 C2-T6

ARGO HARGO ARGO HARGO RGO FES HRGO RGO

12 10.8 10.8–13.2 10.8–12 23.9 6.2 25.2 8–24

28.8 13.4 13.4–15.3 14.5–14.8 39 20 42 –

0.84 0.79 0.79–0.86 0.76–0.8 0.61 0.31 0.59 –

– – – – – – – –

– – – – – – – –

5 26

C2-T6 T4-T12

HRGO RGO

8.4–27 12.6

– 34.5

– 0.72

– –

– –

26

T4-T12

HRGO

12

33.6

0.72

–

–

2

T8-T12

9.3–17.9

–

–

–

–

(Shimada et al., 2006)

2

T8-T12

12.8–18.2

–

–

–

–

(Greene & Granat, 2003) (Greene & Granat, 2003) (Goldfarb, Korkowski, Harrold, & Durfee, 2003b) (Arazpour, Ahmadi Bani et al., 2012) (Arazpour, Ahmadi Bani et al., 2012) (Arazpour, Ahmadi Bani et al., 2012) (Arazpour, Ahmadi Bani et al., 2012) (Arazpour, Chitsazan et al., 2012) (Arazpour, Chitsazan et al., 2012) (Shields & Dudley-Javoroski, 2007) (Shields & Dudley-Javoroski, 2007) (Shields & Dudley-Javoroski, 2007) (Esrafilian, Karimi, Amiri, & Sedigh, 2012) (Esrafilian et al., 2012)

2 2 4

T6 T6 T6-T8

HMLO with hinge HMLO with sling HKAFO HFKO CBO

7.2–7.8 7.2–8.4 1.68–5.52

– – –

0.58–0.82 0.65–0.8 –

– – –

– – –

4 4 4 4 1 1 1 1 1 3

T6-T12 T6-T12 T6-T12 T6-T12 T8 T8 T9 T9 T9 T12-L1

PIRGO (A) PIRGO (B) PIRGO (C) PIRGO (D) PIRGO IRGO IRGO FNS HNP MTK-RGO

22 21.6 24 18 21 14.4 7.2 25.8 8.4 18.95

53.9 53.8 49.6 51.2 48 37 36 60 34 43.2

0.82 0.81 0.88 0.7 0.88 0.76 0.62 0.84 0.72 0.63

– – – – – – – – – –

– – – – – – – – – –

3

T12-L1

KAFO

18.3

45.5

0.7

–

–

tation programme might have been too long to influence the BMD. During activities of daily living, we stand for a long period of time and walk for a long distance. In contrast, in most of the mentioned studies the subjects stood and walked for a short period of time. As the time of involvement of the patient’s dose not comparable with normal standing and walking, it cannot influence BMD significantly. Some portion of body weight applied on bone decreased by use of BWTT (FieldFote, Lindley, & Sherman, 2005; Moreh, Meiner, Neeb,

Hiller, & Schwartz, 2009; Wernig, Muller, Nanassy, & Cagol, 1995), therefore this type of rehabilitation programme may not be as effective as other methods. Other reasons to use mechanical orthoses, hybrid orthoses or other therapeutic approaches are to reduce muscle spasm, to decrease joint contracture, and to improve bowel and bladder functions, Table 5 (Douglas et al., 1983; Dunn et al., 1998; Eng et al., 2001; Granat, Ferguson, Andrews, & Delargy, 1993; Middleton et al., 1997a; Ogilvie, Bowker, & Rowley, 1993;

334

M. Karimi et al. / Spinal cord Injury Rehabilitation Table 9 The walking performance of paraplegic subjects

References

Method Number

(Noreau et al., 1995) (Slavens, Frantz, Sturm, & Harris, 2007) (Slavens et al., 2007) (Jefferson & Whittle, 1990) (Jefferson & Whittle, 1990) (Jefferson & Whittle, 1990) (Kent, 1992)

Results

Lesion level

Type of orthosis

COP excursion in AP (mm)

COP excursion in ML (mm)

Velocity in AP

Velocity in ML

Crutch force (N/BW)

9 5

L3-L4

KAFO HKAFO

41.7–59.9 33.l4

67–79 75.43

1.15–1.23 0.86

– –

– 0.556–0.572

5 1 1 1 29

L3-L4 T5 T5 T5 T2-L5

RGO RGO ARGO HGO VRSO

23.4 18 18.6 18 26

67.12 35 37 37

0.66 1.02 0.99 0.98

– – – – –

0.447–0.451 – – – –

KAFO = Knee Ankle Foot Orthosis, HKAFO = Hip Knee Ankle Foot orthosis, RGO = Reciprocal Gait orthosis, ARGO = Advanced Reciprocal Gait Orthosis, HGO = Hip Guidance Orthosis, VRSO = Vanili Rizzoli Stabilizing orthosis, N = Newton, BW = Body Weight. Table 10 The energy consumption of SCI during walking with various orthoses References

Method Number Lesion level

(Waters & Lunsford, 1985) (Huang, Kuhlemeier, Moore, & Fine, 1979) (A. V. Nene & Patrick, 1989) (Cuddeford et al., 1997) (Cuddeford et al., 1997) (Cerny et al., 1980) (Waters & Lunsford, 1985) (Merkel et al., 1984) (Kawashima et al., 2003) (Ijzerman, Baardman, Hermens et al., 1997) (Stallard & Major, 1995) (Stallard & Major, 1995) (Ijzerman, Baardman, Hermens et al., 1997) (Middleton et al., 1998) (Middleton et al., 1998) (Yano, Kaneko, Nakazawa, Yamamoto, & Bettoh, 1997) (Yano et al., 1997) (Baardman et al., 2002a) (Baardman et al., 2002a) (Sykes et al., 1996) (Sykes et al., 1996) (Merati, Sarchi, Ferrarin, Pedotti, & Veicsteinas, 2000) (Merati et al., 2000) (Beillot, Le Claire, & Thoumie, 1996) (Beillot et al., 1996) (Phillips & Hendershot, 1991) (Phillips & Hendershot, 1991) (A.V. Nene, 1989; A. V. Nene & Patrick, 1989) (A.V. Nene, 1989; A. V. Nene & Patrick, 1989) (Goldfarb, Korkowski, Harrold, & Durfee, 2003a) (Goldfarb et al., 2003a) (Shields & Dudley-Javoroski, 2007) (Shields & Dudley-Javoroski, 2007) (Shields & Dudley-Javoroski, 2007) (Esrafilian et al., 2012) (Esrafilian et al., 2012)

Results Type of orthosis Energy cost () Energy consumption PCI (beats/m)

25 8 10 26 26 3 10 8 4 6 3 3 6 1 1 1

T1-T12 T4-T12 T4-T9 T12-L4 T12-L4 T11-L2 T1-T9 C7-T12 T8-T12 T4-T12 T8-L1 T8-L1 T4-T12 C6 incomplete C6 T7

KAFO KAFO HGO RGO HKAFO KAFO KAFO KAFO WBC ARGO HGO Parawalker ARGO Walk about MMLO WBC

15.3 – 16 16.92 11.28 20.69 15.46 63.95 119.5 – – – – – – –

288.8 234.12 186 239.1 441 446.8 303 – – 355.6 – – – 275 245 –

– – – – – – – – – – 0.95–1.65 0.8–1.26 5.4 11.5 11.5 1.9

1 2 2 5 5 6

T7 T4-T12 T4-T12 C2-T6 C2-T6 T3-T11

HGO ARGO HARGO RGO HRGO RGO

– 17.4 15.88

– – –

13.8

–

3.9 – – 1.44–3.44 1.72–3.32 –

4 24 24 8 8 3

C7-T10 T2-T12 T2-T12 C7 C7 T5-T7

HRGO RGO HRGO RGO HRGO HGO

17.2 – – – – 10.1–12.72

– – – – – –

– 1 1.14 1 1.15 –

3

T5-T7

HHGO

9.3–11.8

–

–

4

T6-T8

HCBO

–

378–462

1–16.7

4 5 5 5 3 3

T6-T8 T6-T12 T6-T12 T6-T12 T12-L1 T12-L1

CBO HKAFO IRGO PIRGO MTK-RGO KAFO

– – – – – –

463–613 – – – – –

2.1–18.9 1.97 1.93 0.92 2.26 2.9

M. Karimi et al. / Spinal cord Injury Rehabilitation

335

Table 11 The performance of normal subjects with RGO (IRGO and MTK-RGO) orthoses Reference

Method Number Type of orthosis

(M. T. Karimi, 2011b) (M. T. Karimi, 2011b) (M. T. Karimi, 2011b) (Yang et al., 1996)

Results of gait analysis

Energy consumption

Stability analysis

Stride Cadence Velocity Foot force Crutch force length (m) (steps/min) (m/min) (N/BW) (N/BW)

PCI (beats/m)

COP COP excursion excursion in AP (mm) in ML (mm)

3

Normal walking

1.66

3

HGO

1.1

3

MTK-RGO

3

IRGO

105

88.8

1.18

0

0.21

30.72

17.7

50.12

33.6

1

0.18

0.7

28.1

10.7

1.03

57.6

35.64

1

0.163

0.61

11.5

8.1

–

–

–

0.68

–

–

Solomonow et al., 1989; Spadone et al., 2003). Unfortunately, there are limited research studies evaluating the importance of these parameters while subjects walk with orthosis or use other methods. There are only a few studies that have shown that SCI individuals mentioned that walking with an orthosis, decreases the number of bowel and bladder infection (Dunn et al., 1998; Ogilvie et al., 1993), however, no clinical finding support their claims. Based on the studies presented in the literature it is difficult to conclude that walking and standing have any effects on performance of digestive, bladder and cardiovascular systems. However, there are noticeable numbers of studies in the literature that show that using exercise, FES has a significant effect on improving the performance of the cardiovascular system (Ditor et al., 2005; Thoumie, Le Claire et al., 1995; Thoumie, Perrouin-Verbe et al., 1995). Although it has been mentioned that standing and walking influences digestive system function, there is no evidence to support it. From the above mentioned studies it can be concluded that there is not enough evidence to show the benefits of standing and walking on physiological health of SCI as was expected (Karimi et al., 2012). However, the effect of manual therapy and other exercise on performance of some systems such as cardiovascular is supported. Therefore, it can be concluded that use of other methods of rehabilitation may be more effective and affordable for SCI subjects to improve their general health. Another reason which may be considered regarding use of various assistive devices is to enable the subjects to stand and walk. The performance of individuals with SCI while standing with orthosis is shown in Tables 6 and 7. As it can be seen from these Tables the stability of the subjects mostly evaluated in a static posture and for a short period of time (Baardman et al., 1997; Karimi,

28

–

Esrafilian et al., 2013; Middleton, Sinclair, Smith, & Davis, 1999). The subjects stand on the force plate for a minute in a quite standing posture. However, most of us stand for a long period of time, when we are talking with some bodies or waiting in a line. Unfortunately, SCI subjects need to use upper limb and crutch or walker to stabilize their body in a quiet static posture (Baardman et al., 1997; Karimi, Esrafilian et al., 2013). Therefore, they do not have a dynamic stability which they need when doing hand tasks. Regarding the mobility of SCI subjects, while they are using various methods already mentioned, there is no difference between the ability of the subjects while using the aforementioned systems. Different kinds of mechanical orthoses have been designed so far to improve the performance of the subjects during walking. Based on literature the performance of the subjects can be measured by considering the walking speed, magnitude of energy consumption during walking and by measuring the force applied on the upper limb during walking (especially in SCI subjects). In comparison with walking performance of normal subjects, individuals with SCI had a significant difficulty walking (Karimi, 2012b), Tables 8 and 9. Moreover, their energy consumption was between 2 and 11 times more than normal walking, Table 10. The force applied on upper limb differed between 25% and 70% of body weight (Ferrarin, Pedotti, & Boccardi, 1993; Major et al., 1981; Noreau, Richards, Comeau, & Tardif, 1995), which increases the incidence of some pathology such as shoulder pain, wrist pain and carpal tunnel syndrome (Dalyan, Cardenas, & Gerard, 1999; Subbarao et al., 1995). As there was a big gap between walking performance of SCI individuals and healthy subjects it was conducted that the difference may be related to lack of motion of knee joint, lack of motion

336

M. Karimi et al. / Spinal cord Injury Rehabilitation

of knee and ankle joint, and or lack of motion of pelvic joint. These problems were considered in designed hybrid orthoses (Baardman et al., 2002a; Baardman et al., 2002b; Ferguson et al., 1999; Gharooni, Heller, & Tokhi, 2001; Greene & Granat, 2003; Kagaya et al., 1996; Shimada et al., 2006). Incorporating knee flexion or ankle motion not only did not improve the walking performance of the SCI subjects, but also did not decrease the loads applied on upper limb through crutches. Hybrid orthosis incorporates combination of muscle activation with functional electrical stimulation and mechanical orthosis. As can be seen from Table 4, there is neither any significant improvement in walking abilities of SCI individuals nor energy consumption. Moreover, these subjects explain some problems in putting the electrodes in their appropriate locations and also infection of electrodes locations (Granat et al., 1993; Stallard & Major, 1995). External powered orthosis is the other approach used to influence the abilities of subjects to stand or walk. Some sources of power such as pneumatic, hydraulic and electrical actuators have been used to produce and control the motions of the knee and hip joints during walking (Colombo et al., 2001a; Field-Fote et al., 2005; Ohta et al., 2007; Tefertiller et al., 2011; Wirz, Bastiaenen, de Bie, & Dietz, 2011). However, no difference has been seen between mechanical and external powered orthoses (Karimi, 2012b). There are also a few studies on normal subjects when walking with orthosis with the same style as that of paraplegic subjects (Karimi et al., 2010; Karimi, Amiri, Esrafilian, Sedigh, & Fatoye, 2013; Yang, Condie, Granat, Paul, & Rowley, 1996). The normal subjects walked with RGO orthosis with a speed which was less than that of normal walking. Moreover, their energy consumption increased by three times, Table 11. Therefore, it can be conducted that external powered orthoses were not as successful as expected to restore functional ability of subjects with SCI. As the function of normal subjects decreased while walking with RGO orthosis it can also be conducted that lack of power in SCI is not the only important parameter. Regarding FES system, it did not influence the performance of SCI subjects as was expected (Karimi, 2012a). Based on some research, the energy consumption of subjects walking with FES is more than that of mechanical orthosis (Karimi, 2012a). There is another approach in this regard including use of exoskeleton based orthoses. Although some sophisticated mechanisms have been used in their designs but no improvements have been seen in performance of

SCI subjects. The performance of normal subjects while standing and walking with an orthosis is a benchmark to represent the best ability of paraplegic subjects which can be achieved. From the above mentioned it can be concluded that it is may not be possible to use various kind of assistive devices instead of wheelchair. It should be emphasized that most individuals with SCI would prefer to not use any orthoses (Karimi, 2011a, 2012b) due to the following problems: High energy demand, dependency to don and doff orthosis, lack of mechanical reliability, and the style of walking with the orthosis which is abnormal. There is a big difference between the ability of SCI subjects while walking with orthoses or ambulate with wheelchair (Cerny, Waters, Hislop, & Perry, 1980). Moreover, most of research studies showed that SCI individuals ambulate with wheelchair with the same speed as that of normal walking, fewer forces are applied on their upper limb and their energy consumption is the same as that during walking (Waters & Lunsford, 1985). Therefore, it can be conducted that using various orthoses is not successful to fulfill the needs of patients in standing and walking. There are lots of problems with available studies on SCI subject’s rehabilitation, such as limited number of subjects, short period of involvement of the subjects, differences between the studies in relation to the level of lesion of SCI participants and time post injury. However, as the results is nearly the same and represents a big difference between the walking ability of SCI and normal subjects, it can be conducted that using various orthoses is neither successful to provide physiological health nor improve the ability of SCI while walking. Other methods of rehabilitation such as FES, cycling, rowing or robotic rehabilitation seems to be more successful to provide physiological benefits for SCI subjects. Moreover, they are not as costly as using orthosis. It cannot be recommended to use orthoses instead of wheelchair. If it is a goal there will be a long way to go. It seems that lack of dynamic stability during walking, use of crutch or walker and inappropriate style of walking are some reasons that can influence the design of new orthoses for individuals with SCI. 5. Conclusion Although various systems have been used to improve the performance of subjects with SCI to stand and walk and to improve their physiological health, none of them are successful. Therefore, instead of using various sys-

M. Karimi et al. / Spinal cord Injury Rehabilitation

tems to enable the subjects to ambulate, other methods of rehabilitation should be used. It seems that inappropriate style of walking and using crutch and walkers are the problems which need to be emphasized in this regards. References Alekna, V., Tamulaitiene, M., Sinevicius, T., & Juocevicius, A. (2008). Effect of weight-bearing activities on bone mineral density in spinal cord injured patients during the period of the first two years. Spinal Cord, 46(1362-4393 (Print)), 727-732. American Academy of Orthopaedic Surgeons. (1985). Atlas of orthotics (2nd. ed., Vol. 10, pp. 199-237). St. Louis, Mo.: Mosby. Arazpour, M., Ahmadi Bani, M., Vahab Kashani, R., Tabatabai Ghomshe, F., Mousavi, M. E., & Hutchins, S. W. (2012). Effect of powered gait orthosis on walking in individuals with paraplegia. Prosthet Orthot Int, 37(4), 261-7. Arazpour, M., Chitsazan, A., Hutchins, S. W., Mousavi, M. E., Takamjani, E. E., Ghomshe, F. T., et al. (2012). Evaluation of a novel powered gait orthosis for walking by a spinal cord injury patient. Prosthet Orthot Int, 36(2), 239-246. Baardman, G., IJzerman, M. J., Hermens, H. J., Veltink, P. H., Boom, G., & Zilvold, G. (2002a). Knee flexion during the swing phase of orthotic gait: Influence on kinematics, kinetics and energy consumption in two paraplegic cases. Saudi Journal of Disability and Rehabilitation, 8, 20-32. Baardman, G., Ijzerman, M. J., Hermens, H. J., Veltink, P. H., Boom, H. B., & Zilvold, G. (1997). The influence of the reciprocal hip joint link in the Advanced Reciprocating Gait Orthosis on standing performance in paraplegia. Prosthetics and Orthotics International, 21(0309-3646 (Print)), 210-221. Baardman, G., IJzerman, M. J., Hermens, H. J., Veltink, P. H., Boom, H. B. K., & Zilvold, G. (2002b). Augmentation of the knee flexion during the swing phase of orthotic gait in paraplegia by means of functional electrical stimulation. Saudi Journal of Disability and Rehabilitation, 8(2), 73-81. Beillot, J. F., Le Claire, C., & Thoumie, P. (1996). Energy consumption of paraplegic locomotion using reciprocal gait orthosis. European journal of applied physiology and occupational physiology, 73, 376-381. Belanger, M., Stein, R. B., Wheeler, G. D., Gordon, T., & Leduc, B. (2000). Electrical stimulation: Can it increase muscle strength and reverse osteopenia in spinal cord injured individuals? Arch Phys Med Rehabil, 81(8), 1090-1098. Ben, M., Harvey, L., Denis, S., Glinsky, J., Goehl, G., Chee, S., et al. (2005). Does 12 weeks of regular standing prevent loss of ankle mobility and bone mineral density in people with recent spinal cord injuries? Aust J Physiother, 51(4), 251-256. Biering, S., Bohr, H., & Schaadt, O. (1988). Bone mineral content of the lumbar spine and lower extremities years after spinal cord lesion. Paraplegia, 26(0031-1758 (Print)), 293-301. Biering, S. F., Bohr, H. H., & Schaadt, O. P. (1990). Longitudinal study of bone mineral content in the lumbar spine, the forearm and the lower extremities after spinal cord injury. European Journal of Clinical Investigation, 20(3), 330-335. Bloomfield, S. A., Mysiw, W. J., & Jackson, R. D. (1996). Bone mass and endocrine adaptations to training in spinal cord injured individuals. Bone, 19(1), 61-68.

337

Cerny, D., Waters, R., Hislop, H., & Perry, J. (1980). Walking and wheelchair energetics in persons with paraplegia. Physical Therapy, 60(0031-9023 (Print)), 1133-1139. Chen, H. Y., Chen, S. S., Chiu, W. T., Lee, L. S., Hung, C. I., Wang, Y. C., et al. (1997). A nationwide epidemiological study of spinal cord injury in geriatric patients in Taiwan. Neuroepidmiology, 16(5) (0251-5350 (Print)), 241-247. Chen, S. C., Lai, C. H., Chan, W. P., Huang, M. H., Tsai, H. W., & Chen, J. J. (2005). Increases in bone mineral density after functional electrical stimulation cycling exercises in spinal cord injured patients. Disabil Rehabil, 27(22), 1337-1341. Colombo, G., Wirz, M., & Dietz, V. (2001a). Driven gait orthosis for improvement of locomotor training in paraplegic patients. [Case Reports Comparative Study Research Support, Non-U.S. Gov’t]. Spinal Cord, 39(5), 252-255. Colombo, G., Wirz, M., & Dietz, V. (2001b). Driven gait orthosis for improvement of locomotor training in paraplegic patients. Spinal Cord, 39(1362-4393 (Print)), 252-255. Cuddeford, T. J., Freeling, R. P., Thomas, S. S., Aiona, M. D., Rex, D., Sirolli, H., et al. (1997). Energy consumption in children with myelomeningocele: A comparison between reciprocating gait orthosis and hip-knee-ankle-foot orthosis ambulators. Developmental Medicine and Child Neurology, 39(0012-1622 (Print)), 239-242. Dalyan, M., Cardenas, D. D., & Gerard, B. (1999). Upper extremity pain after spinal cord injury. Spinal Cord, 37(1362-4393 (Print)), 191-195. Del-Ama, A. J., Koutsou, A. D., Moreno, J. C., de-los-Reyes, A., GilAgudo, A., & Pons, J. L. (2012). Review of hybrid exoskeletons to restore gait following spinal cord injury. J Rehabil Res Dev, 49(4), 497-514. Ditor, D. S., Macdonald, M. J., Kamath, M. V., Bugaresti, J., Adams, M., McCartney, N., et al. (2005). The effects of body-weight supported treadmill training on cardiovascular regulation in individuals with motor-complete SCI. Spinal Cord, 43(11), 664-673. Douglas, R., Larson, P. F., D’ Ambrosia, R., & McCall, R. E. (1983). The LSU Reciprocal-Gait Orthosis. Orthopedics, 6, 834-839. Downs, S. H., & Black, N. (1998). The feasibility of creating a checklist for the assessment of the methodological quality both of randomised and non-randomised studies of health care interventions. J Epidemiol Community Health, 52(6), 377-384. Dunn, R. B., Walter, J. S., Lucero, Y., Weaver, F., Langbein, E., Fehr, L., et al. (1998). Follow-up assessment of standing mobility device users. Assistive Technology 10(1040-0435 (Print)), 84-93. Eng, J. J., Levins, S. M., Townson, A. F., Mah-Jones, D., Bremner, J., & Huston, G. (2001). Use of prolonged standing for individuals with spinal cord injuries. Physical Therapy, 81(0031-9023 (Print)), 1392-1399. Esrafilian, A., Karimi, M., Amiri, P., & Sedigh, J. (2012). Walking Performance of Subjects with Spinal Cord Injury Using the New MTK Reciprocal Gait Orthosis. Journal of Isfahan Medical School, 30(1), 1-12. Ferguson, K. A., Polando, G., Kobetic, R., Triolo, R. J., & Marsolais, E. B. (1999). Walking with a hybrid orthosis system. Spinal Cord, 37(1362-4393 (Print)), 800-804. Ferrarin, M., & Pedotti, A. (1994). Restoration of walking for paraplegics: Recent advancements and trends. Milano: Edizioni Pro Juventute; Oxford : IOS Press. Ferrarin, M., Pedotti, A., & Boccardi, S. (1993). Biomechanical assessment of paraplegic locomotion with hip guidance orthosis (HGO). Clinical Rehabilitation, 7(4), 303-308

338

M. Karimi et al. / Spinal cord Injury Rehabilitation

Field-Fote, E. C., Lindley, S. D., & Sherman, A. L. (2005). Locomotor training approaches for individuals with spinal cord injury: A preliminary report of walking-related outcomes. [Randomized Controlled Trial Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov’t]. J Neurol Phys Ther, 29(3), 127-137. Frost, H. M. (1987). The mechanostat: A proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner, 2(2), 73-85. Frost, H. M. (2003). Bone’s mechanostat: A 2003 update. Anat Rec A Discov Mol Cell Evol Biol, 275(2), 1081-1101. Gharooni, S., Heller, B., & Tokhi, M. O. (2001). A new hybrid spring brake orthosis for controlling hip and knee flexion in the swing phase. IEEE transactions on neural systems and rehabilitation engineering, 9(1534-4320 (Print)), 106-107. Goemaere, S., Van Laere, M., De Neve, P., & Kaufman, J. M. (1994). Bone mineral status in paraplegic patients who do or do not perform standing. Osteoporosis International, 4(0937-941X (Print)), 138-143. Goldfarb, M., Korkowski, K., Harrold, B., & Durfee, W. (2003a). Preliminary evaluation of a controlled-brake orthosis for FESaided gait. IEEE Trans Neural Syst Rehabil Eng, 11, 241-248. Goldfarb, M., Korkowski, K., Harrold, B., & Durfee, W. (2003b). Preliminary evaluation of a controlled-brake orthosis for FESaided gait. IEEE Trans Neural Syst Rehabil Eng, 11(3), 241-248. Granat, M. H., Ferguson, A. C., Andrews, B. J., & Delargy, M. (1993). The role of functional electrical stimulation in the rehabilitation of patients with incomplete spinal cord injury–observed benefits during gait studies. Paraplegia, 31(4), 207-215. Greene, P. J., & Granat, M. H. (2003). A knee and ankle flexing hybrid orthosis for paraplegic ambulation. Medical Engineering & Physics, 25(1350-4533 (Print)), 539-565. Hangartner, T. N., Rodgers, M. M., Glaser, R. M., & Barre, P. S. (1994). Tibial bone density loss in spinal cord injured patients: Effects of FES exercise. J Rehabil Res Dev, 31(1), 50-61. Hawran, S., & Biering, S. F. (1996). The use of long leg calipers for paraplegic patients: A follow-up study of patients discharged 1973-82. Spinal Cord, 34(1362-4393 (Print)), 666-668. Hirokawa, S., Solomonow, M., Baratta, R., & D’Ambrosia, R. (1996). Energy expenditure and fatiguability in paraplegic ambulation using reciprocating gait orthosis and electric stimulation. Disability and Rehabilitation, 18(3)(0963-8288 (Print)), 115-122. Huang, C. T., Kuhlemeier, K. V., Moore, N. B., & Fine, P. R. (1979). Energy cost of ambulation in paraplegic patients using CraigScott braces. Archives of Physical Medicine and Rehabilitation, 60(12)(0003-9993 (Print)), 595-600. Ijzerman, M. J., Baardman, G., Hermens, H. J., Veltink, P. H., Boom, H. B., & Zilvold, G. (1997). The influence of the reciprocal cable linkage in the advanced reciprocating gait orthosis on paraplegic gait performance. Prosthetics and Orthotics International, 21(0309-3646 (Print)), 52-61. Ijzerman, M. J., Baardman, G., Holweg, G. G. J., Hermens, H. J., Veltink, P. H., Boom, H. B. K., et al. (1997). The influence of frontal alignment in the Advanced Reciprocating Gait Orthosis on energy cost and crutch force requirements during paraplegic gait. Basic and Applied Myology, 7, 123-130. Jefferson, R. J., & Whittle, M. W. (1990). Performance of three walking orthoses for the paralysed: A case study using gait analysis. Prosthetics and Orthotics International, 14(0309-3646 (Print)), 103-110. Kagaya, H., Shimada, Y., Sato, K., Sato, M., Iizuka, K., & IObinata, G. (1996). An electrical knee lock system for functional electrical

stimulation. Archives of Physical Medicine and Rehabilitation, 77(0003-9993 (Print)), 870-873. Karacan, I., Koyuncu, H., Pekel, O., Sumbuloglu, G., Kirnap, M., Dursun, H., et al. (2000). Traumatic spinal cord injuries in Turkey: A nation-wide epidemiological study. Spinal Cord, 38 (11)(13624393 (Print)), 697-701. Karamehmetoglu, S., Unal, S., Karacan, I., Yilmaz, H., Togay, H. S., Ertekin, M., et al. (1995). Traumatic spinal cord injuries in Istanbul, Turkey. An epidemiological study. Paraplegia, 33(8) (0031-1758 (Print)), 469-471. Karimi, M. (2011). Determination of the Loads Applied on the Anatomy and Orthosis During Ambulation With a New Reciprocal Gait Orthosis. Journal of Medical Device, 5(4), 45-50. Karimi, M. (2012). Can walking with orthosis reduce bone mineral dencity? Australasian Physical & Engineering Sciences in Medicine, 5, 250-255. Karimi, M., Sedigh, J., & Fatoye, F. (2012). Evaluation of gait performance of a participant with Perthes disease while walking with and without a Scottish-Rite orthosis. Prosthet Orthot Int. Karimi, M., Spence, W., Nicol, A., & Solomonidis, E. (2010). How can the performance of the paraplegic patients be improved. Orthop Tech, 5(1), 1-8. Karimi, M. T. (2011a). Evidence-based evaluation of physiological effects of standing and walking in individuals with spinal cord injury. Iran J Med Sci, 36(4), 242-253. Karimi, M. T. (2011b). Influences of Joint Motion Restriction on the Performance of Normal Subjects and Their Implications on Development of Orthosis for Spinal Cord Injured Individuals. Journal of Physical Medicine and Rehabilitation Sciences, 13, 122-131. Karimi, M. T. (2012a). Functional walking ability of paraplegic patients: Comparison of functional electrical stimulation versus mechanical orthoses. Eur J Orthop Surg Traumatol, 23(6), 631638. Karimi, M. T. (2012b). What are the next steps in designing an orthosis for paraplegic subjects? Int J Prev Med, 3(3), 145-159. Karimi, M. T., Amiri, P., Esrafilian, A., Sedigh, J., & Fatoye, F. (2013). Performance of spinal cord injury individuals while standing with the Mohammad Taghi Karimi reciprocal gait orthosis (MTK-RGO). Australas Phys Eng Sci Med, 36(1), 35-42. Karimi, M. T., Esrafilian, O., Esrafilian, A., Sadigh, M. J., & Amiri, P. (2013). Determination of the influence of walking with orthosis on bone osteoporosis in paraplegic subjects based on the loads transmitted through the body. Clin Biomech (Bristol, Avon), 28(3), 325-329. Kawashima, N., Sone, Y., Nakazawa, K., Akai, M., & Yano, H. (2003). Energy expenditure during walking with weight-bearing control (WBC) orthosis in thoracic level of paraplegic patients. Spinal Cord, 41(9) (1362-4393 (Print)), 506-510. Kent, H. O. (1992). Vannini-Rizzoli stabilizing orthosis (boot): Preliminary report on a new ambulatory aid for spinal cord injury. Archives of Physical Medicine and Rehabilitation, 73(0003-9993 (Print)), 302-307. Kralj, A. R., & Bajd, T. (1989). Functional electrical stimulation: Standing and walking after spinal cord injury. Boca Raton, Fla.: CRC Press. Kunkel, C. F., Scremin, A. M., Eisenberg, B., Garcia, J. F., Roberts, S., & Martinez, S. (1993). Effect of “standing” on spasticity, contracture, and osteoporosis in paralyzed males. Archives of Physical Medicine and Rehabilitation, 74(0003-9993 (Print)), 73-78.

M. Karimi et al. / Spinal cord Injury Rehabilitation Lai, C. H., Chang, W. H., Chan, W. P., Peng, C. W., Shen, L. K., Chen, J. J., et al. (2010). Effects of functional electrical stimulation cycling exercise on bone mineral density loss in the early stages of spinal cord injury. J Rehabil Med, 42(2), 150-154. Leeds, E. M., Klose, K. J., Ganz, W., Serafini, A., & Green, B. A. (1990). Bone mineral density after bicycle ergometry training. Arch Phys Med Rehabil, 71(3), 207-209. Maharaj, J. C. (1996). Epidemiology of spinal cord paralysis in Fiji: 1985-1994. Spinal Cord, 34 (9)(1362-4393 (Print)), 549-559. Major, R. E., Stallard, J., & Rose, G. K. (1981). The dynamics of walking using the hip guidance orthosis (hgo) with crutches. Prosthetics and Orthotics International, 7(0309-3646 (Print)), 19-22. Melis, E. H., Torres-Moreno, R., Barbeau, H., & Lemaire, E. D. (1999). Analysis of assisted-gait characteristics in persons with incomplete spinal cord injury. Spinal Cord, 37(1362-4393 (Print)), 430-439. Merati, G., Sarchi, P., Ferrarin, M., Pedotti, A., & Veicsteinas, A. (2000). Paraplegic adaptation to assisted-walking: Energy expenditure during wheelchair versus orthosis use. Spinal Cord, 38(1362-4393 (Print)), 37-44. Merkel, K. D., Miller, N. E., Westbrook, P. R., & Merritt, J. L. (1984). Energy expenditure of paraplegic patients standing and walking with two knee-ankle-foot orthoses. Archives of Physical Medicine and Rehabilitation, 65(0003-9993 (Print)), 121-124. Middleton, J. W., Fisher, W., Davis, G. M., & Smith, R. M. (1998). A medial linkage orthosis to assist ambulation after spinal cord injury. Prosthetics and Orthotics International, 22(0309-3646 (Print)), 258-264. Middleton, J. W., Sinclair, P. J., Smith, R. M., & Davis, G. M. (1999). Postural control during stance in paraplegia: Effects of medially linked versus unlinked knee-ankle-foot orthoses. Archives of Physical Medicine and Rehabilitation, 80(0003-9993 (Print)), 1558-1565. Middleton, J. W., Yeo, J. D., Blanch, L., Vare, V., Peterson, K., & Brigden, K. (1997a). Clinical evaluation of a new orthosis, the ‘walkabout’, for restoration of functional standing and short distance mobility in spinal paralysed individuals. Spinal Cord, 35(1362-4393 (Print)), 574-579. Middleton, J. W., Yeo, J. D., Blanch, L., Vare, V., Peterson, K., & Brigden, K. (1997b). Clinical evaluation of a new orthosis, the ‘walkabout’, for restoration of functional standing and short distance mobility in spinal paralysed individuals. Spinal Cord, 35(9), 574-579. Mirbagheri, M. M., Ladouceur, M., Barbeau, H., & Kearney, R. E. (2002). The effects of long-term FES-assisted walking on intrinsic and reflex dynamic stiffness in spastic spinal-cord-injured subjects. IEEE Trans Neural Syst Rehabil Eng, 10(4), 280-289. Mohr, T., Podenphant, J., Biering-Sorensen, F., Galbo, H., Thamsborg, G., & Kjaer, M. (1997). Increased bone mineral density after prolonged electrically induced cycle training of paralyzed limbs in spinal cord injured man. Calcif Tissue Int, 61(1), 22-25. Moreh, E., Meiner, Z., Neeb, M., Hiller, N., & Schwartz, I. (2009). Spinal decompression sickness presenting as partial BrownSequard syndrome and treated with robotic-assisted body-weight support treadmill training. [Case Reports]. J Rehabil Med, 41(1), 88-89. Needham-Shropshire, B. M., Broton, J. G., Klose, K. J., Lebwohl, N., Guest, R. S., & Jacobs, P. L. (1997). Evaluation of a training program for persons with SCI paraplegia using the Parastep 1

339

ambulation system: Part 3. Lack of effect on bone mineral density. Arch Phys Med Rehabil, 78(8), 799-803. Nene, A. V. (1989). An assessment of the ORLAU Parawalkerelectrical stimulation hybrid orthosis. Paper presented at the International conference of IEEE engineering, Seattle, WA, USA. Nene, A. V., & Patrick, J. H. (1989). Energy cost of paraplegic locomotion with the ORLAU ParaWalker. Paraplegia, 27(0031-1758 (Print)), 5-18. Noreau, L., Richards, C. L., Comeau, F., & Tardif, D. (1995). Biomechanical analysis of swing-through gait in paraplegic and non-disabled individuals. Journal of Biomechanics, 28(6)(00219290 (Print)), 689-700. NSCISC. (2001). Spinal cord injury: Facts and figures at a glance. The journal of spinal cord medicine, 24(3)(1079-0268 (Print)), 212-213. O’Connor, P. J. (2005). Prevalence of spinal cord injury in Australia. Spinal Cord, 43(1)(1362-4393 (Print)), 42-46. Ogilvie, C., Bowker, P., & Rowley, D. I. (1993). The physiological benefits of paraplegic orthotically aided walking. Paraplegia, 31(0031-1758 (Print)), 111-115. Ohta, Y., Yano, H., Suzuki, R., Yoshida, M., Kawashima, N., & Nakazawa, K. (2007). A two-degree-of-freedom motor-powered gait orthosis for spinal cord injury patients. Proceedings of the Institution of Mechanical Engineers, 221(0954-4119 (Print)), 629-639. Phillips, C. A., & Hendershot, D. M. (1991). Functional electrical stimulation and reciprocating gait orthosis for ambulation exercise in a tetraplegic patient: A case study. Paraplegia, 29(0031-1758 (Print)), 268-276. Robling, A. G., Castillo, A. B., & Turner, C. H. (2006). Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng, 8, 455-498. Rodgers, M. M., Glaser, R. M., Figoni, S. F., Hooker, S. P., Ezenwa, B. N., Collins, S. R., et al. (1991). Musculoskeletal responses of spinal cord injured individuals to functional neuromuscular stimulation-induced knee extension exercise training. J Rehabil Res Dev, 28(4), 19-26. Rosenstein, B. D., Greene, W. B., Herrington, R. T., & Blum, A. S. (1987). Bone density in myelomeningocele: The effects of ambulatory status and other factors. Developmental Medicine and Child Neurology, 29(0012-1622 (Print)), 486-494. Shields, R. K., & Dudley-Javoroski, S. (2007). Musculoskeletal adaptations in chronic spinal cord injury: Effects of longterm soleus electrical stimulation training. Neurorehabil Neural Repair, 21(2), 169-179. Shimada, Y., Hatakeyama, K., Minato, T., Matsunaga, T., Sato, M., Chida, S., et al. (2006). Hybrid functional electrical stimulation with medial linkage knee-ankle-foot orthoses in complete paraplegics. The Tohoku Journal of Experimental Medicine, 209(0040-8727 (Print)), 117-123. Slavens, B. A., Frantz, J., Sturm, P. F., & Harris, G. F. (2007). Upper extremity dynamics during Lofstrand crutch-assisted gait in children with myelomeningocele. The Journal of Spinal Cord Medicine, 30(1)(1079-0268 (Print)), 165-171. Sloan, K. E., Bremner, L. A., Byrne, J., Day, R. E., & Scull, E. R. (1994). Musculoskeletal effects of an electrical stimulation induced cycling programme in the spinal injured. Paraplegia, 32(6), 407-415. Solomonow, M., Baratta, R., Hirokawa, S., Rightor, N., Walker, W., Beaudette, P., et al. (1989). The RGO Generation II: Muscle stimulation powered orthosis as a practical walking system for

340

M. Karimi et al. / Spinal cord Injury Rehabilitation

thoracic paraplegics. Orthopedics, 12(0147-7447 (Print)), 13091315. Solomonow, M., Reisin, E., Aguilar, E., Baratta, R. V., Best, R., & D’Ambrosia, R. (1997). Reciprocating gait orthosis powered with electrical muscle stimulation (RGO II). Part II: Medical evaluation of 70 paraplegic patients. Orthopedics, 20(5), 411-418. Somers, M. F. (1992). Spinal cord injury: Functional rehabilitation. Norwalk, Conn.: Appleton & Lange. Spadone, R., Merati, G., Bertocchi, E., Mevio, E., Veicsteinas, A., Pedotti, A., et al. (2003). Energy consumption of locomotion with orthosis versus Parastep-assisted gait: A single case study. Spinal Cord, 41(2), 97-104. Stallard, J. (2000). ORLAU, A brief history- The first 25 years 1975 to 2000: ORLAU Stallard, J., & Major, R. E. (1995). The influence of orthosis stiffness on paraplegic ambulation and its implications for functional electrical stimulation (FES) walking systems. Prosthetics and Orthotics International, 19(0309-3646 (Print)), 108-114. Stolov, W. C., & Clowers, M. R. (1981). Handbook of severe disability: A text for rehabilitation counselors, other vocational practitioners, and allied health professionals (Vol. 4). Washington: U.S. Dept. of Education Rehabilitation Services Administration; for sale by the Supt. of Docs. U.S. Govt. Print. Off. Subbarao, J. V., Klopfstein, J., & Turpin, R. (1995). Prevalence and impact of wrist and shoulder pain in patients with spinal cord injury. The journal of spinal cord medicine, 18(1079-0268 (Print)), 9-13. Surkin, J., Gilbert, B. J., Harkey, H. L., Sniezek, J., & Currier, M. (2000). Spinal cord injury in Mississippi. Findings and evaluation, 1992-1994. Spine, 25(6)(0362-2436 (Print)), 716-721. Sykes, L., Campbell, I. G., Powell, E. S., Ross, E. R., & Edwards, J. (1996). Energy expenditure of walking for adult patients with spinal cord lesions using the reciprocating gait orthosis and functional electrical stimulation. Spinal Cord, 34(11), 659-665. Tefertiller, C., Pharo, B., Evans, N., & Winchester, P. (2011). Efficacy of rehabilitation robotics for walking training in neurological disorders: A review. [Review]. J Rehabil Res Dev, 48(4), 387-416. Thoumie, P., Le Claire, G., Beillot, J., Dassonville, J., Chevalier, T., Perrouin-Verbe, B., et al. (1995). Restoration of functional gait in paraplegic patients with the RGO-II hybrid orthosis.

A multicenter controlled study. II: Physiological evaluation. Paraplegia, 33(11), 654-659. Thoumie, P., Perrouin-Verbe, B., Le Claire, G., Bedoiseau, M., Busnel, M., Cormerais, A., et al. (1995). Restoration of functional gait in paraplegic patients with the RGO-II hybrid orthosis. A multicentre controlled study. I. Clinical evaluation. Paraplegia, 33(11), 647-653. Waters, R. I., & Lunsford, B. R. (1985). Energy cost of paraplegic locomotion. Journal of Bone, Joint and Surgery, 67, 1245-1250. Wernig, A., Muller, S., Nanassy, A., & Cagol, E. (1995). Laufband therapy based on ‘rules of spinal locomotion’ is effective in spinal cord injured persons. Eur J Neurosci, 7(4), 823-829. Wessels, M., Lucas, C., Eriks, I., & de Groot, S. (2010). Body weightsupported gait training for restoration of walking in people with an incomplete spinal cord injury: A systematic review. J Rehabil Med, 42(6), 513-519. Whittle, M. W., Cochrane, G. M., Chase, A. P., Copping, A. V., Jefferson, R. J., Staples, D. J., et al. (1991). A comparative trial of two walking systems for paralysed people. Paraplegia, 29(0031-1758 (Print)), 97-102. Wirz, M., Bastiaenen, C., de Bie, R., & Dietz, V. (2011). Effectiveness of automated locomotor training in patients with acute incomplete spinal cord injury: A randomized controlled multicenter trial. [Multicenter Study Randomized Controlled Trial]. BMC Neurol, 11, 60. Wyndaele, M., & Wyndaele, J. J. (2006). Incidence, prevalence and epidemiology of spinal cord injury: What learns a worldwide literature survey? Spinal cord, 44 (9)(1362-4393 (Print)), 523529. Yang, L., Condie, D. N., Granat, M. H., Paul, J. P., & Rowley, D. I. (1996). Effects of joint motion constraints on the gait of normal subjects and their implications on the further development of hybrid FES orthosis for paraplegic persons. Journal of Biomechanics, 29(2)(0021-9290 (Print)), 217-226. Yano, H., Kaneko, S., Nakazawa, K., Yamamoto, S. I., & Bettoh, A. (1997). A new concept of dynamic orthosis for paraplegia: The weight bearing control (WBC) orthosis. Prosthetics and Orthotics International, 21(0309-3646 (Print)), 222-228.

Copyright of NeuroRehabilitation is the property of IOS Press and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express written permission. However, users may print, download, or email articles for individual use.