Archives of Physical Medicine and Rehabilitation journal homepage: www.archives-pmr.org Archives of Physical Medicine and Rehabilitation 2014;95:642-8

ORIGINAL ARTICLE

Survival in Persons With Traumatic Spinal Cord Injury Receiving Structured Follow-Up in South India Apurba Barman, MD,a,c Devika Shanmugasundaram, MSc,b Rohit Bhide, DNB (PMR),a Anand Viswanathan, MD,a Henry Prakash Magimairaj, MD,a Guru Nagarajan, PhD,a Elango Arumugam, MA (SW),a George Tharion, DNB (PMR),a Raji Thomas, MDa From the aDepartment of Physical Medicine and Rehabilitation, Christian Medical College, Vellore; bDepartment of Biostatistics, Christian Medical College, Vellore, Tamil Nadu; and cDepartment of Physical Medicine and Rehabilitation, All India Institute of Medical Sciences, Bhubaneswar; India.

Abstract Objective: To assess the survival in persons with traumatic spinal cord injury (SCI) receiving structured follow-up in South India. Design: Retrospective study. Setting: Rehabilitation center. Participants: Persons with traumatic SCI (NZ490) residing within a 100-km radius of the institute who were managed and regularly followed up by the rehabilitation center between the years 1981 and 2011. Interventions: Not applicable. Main Outcome Measures: Survival rates and mortality risk factors. Measures were estimated using the product limit (Kaplan-Meier) method and the Cox model. Results: The survival rate after SCI was 86% after 5 years, 71% after 15 years, and 58% after 25 years. Survival of persons with complete high cervical injury is substantially low compared with other levels of SCI. Level of injury and extent of lesion (Frankel classification and/or American Spinal Injury Association Impairment Scale) play a significant role in predicting survival of this population. Conclusions: Survival rates of regularly followed-up persons with SCI from this study show promising results, though survival rates are lesser when compared with studies from developed countries. Better understanding of the predictors, causes of deaths, comprehensive rehabilitation, community integration, and regular follow-up could possibly assist in improving survival rates. Archives of Physical Medicine and Rehabilitation 2014;95:642-8 ª 2014 by the American Congress of Rehabilitation Medicine

Survival analysis is vital for any longstanding disabilities in order to assess survival at the individual and population level.1 There are many studies on spinal cord injury (SCI) survival analysis, mostly from countries with advanced SCI care systems. SCI survival analysis is essential to understand the prognostic factors and to assess and compare treatment achievements. It can significantly impact future survival rates by improving treatment and rehabilitation options. Similarly, it can also influence policy making and utilization of available resources.1 SCI has significant impact on an individual’s life in terms of physical impairment and related psychosocial issues.2 Data about No commercial party having a direct financial interest in the results of the research supporting this article has conferred or will confer a benefit on the authors or on any organization with which the authors are associated.

survival and life expectancy help in understanding the effects of SCI, not only for the individual but also for families, community, and society. Persons with SCI and their family members often have wrong assumptions and negative thoughts regarding life expectancy in persons with SCI. It is therefore important for clinicians to provide accurate evidence-based information and enable a more informed understanding of how to cope and live with spinal injuries. Research about survival after SCI in developed countries has shown that life expectancy of persons with SCI is lower than that of the general population, though it has improved greatly in the last few decades.3 Data on survival of the SCI population from developing countries are scarce because of the lack of proper SCI death registration systems and inadequate clinical follow-up. In

0003-9993/14/$36 - see front matter ª 2014 by the American Congress of Rehabilitation Medicine http://dx.doi.org/10.1016/j.apmr.2013.11.003

Survival after traumatic SCI India, there is no registry collecting data on persons with SCI at either the national or state level. The purpose of the present study was to determine the survival rates and mortality risk factors in persons with traumatic spinal cord injury (TSCI) who were registered with our hospital, underwent rehabilitation, and are undergoing follow-up in our center. The risk factors considered were age, sex, cause, level, and neurologic completeness of injury. It is assumed that survival of the SCI population will be less in India compared with developed countries because of inadequate rehabilitation facilities and the absence of protocol for management of SCI. Problems such as lack of knowledge about SCI and poor social support further complicate this issue. To our knowledge, this is the first study on survival analysis of persons with posttraumatic SCI in India.

Methods The Christian Medical College and Hospital is a tertiary care, university teaching hospital in South India. This is a major referral center for rehabilitation from hospitals throughout the country. The rehabilitation center, which is a part of the hospital, has had 83 beds since 2004 (previously it had 35 beds) and is a specialized rehabilitation facility for individuals with SCI and acquired brain injuries. More than 2000 persons with SCI have been rehabilitated in our center over last 30 years. These persons were referred from the neurosurgery and orthopedics department of our institute and from other hospitals. Among these, 537 persons with TSCI were residing within a 100-km radius of the rehabilitation center. Of these, 490 persons with TSCI who were treated between 1981 and 2011 and received regular follow-up in our center were included in the study. This number does not include persons with SCI who were rehabilitated in other surrounding hospitals and centers. There is no central registry for persons with SCI that could account for the total number of persons with SCI in the 100-km radius. The remaining 47 persons had been lost to follow-up because they were shifted elsewhere; they were excluded from the analysis. The intervention at the rehabilitation center included functional mobility, bowel and bladder management, sexual rehabilitation, caregiver training, and vocational training. Follow-up visits stressed the screening of bowel-bladder, evaluations of new-onset complications, assessment of functional status, and community reintegration of the person. Persons with SCI are followed up once annually in the outpatient department, during a home visit by the community liaison team, or during the annual follow-up program (Rehab Mela). Home visits by the community liaison team were started regularly in 1990; Rehab Mela was started in 1994. Before 1990, persons with SCI were followed up in the outpatient department. The community liaison team consists of a physician, social worker, physical therapist, occupational therapist, orthotist, psychological counselor, and rehabilitation nurse. The community liaison team kept an up-to-date record of any new-onset medical, physical, functional, social, vocational, and environmental issues. Demographic and clinical data (eg, age at injury, cause of trauma, level and severity of injury) were collected by reviewing patient’s hospital medical records. Mortality data were obtained

List of abbreviations: AIS IQR SCI TSCI

American Spinal Injury Association Impairment Scale interquartile range spinal cord injury traumatic spinal cord injury

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643 from hospital and home visit records maintained by social workers of the rehabilitation center. This study was approved by the institutional ethics review board.

Data collection The community liaison team reported date of death to the social workers in the course of their routine follow-up. The social workers later entered it into the SCI records. All persons were followed-up until death or until April 30, 2011. All persons under regular follow-up of our team of social workers, and not reported as deceased, were alive on April 30, 2011. Data were analyzed by the statistical analysis software SPSS version 17 for Windows.a Survival rates were estimated using the product limit (Kaplan-Meier) method, and differences between subgroups (sex, age at injury, SCI level, severity of neurologic deficit, and year of injury) were analyzed by log-rank test. The Cox proportional hazard model was used to determine the probability of mortality (hazard) in the presence of specific risk factors and to create survival curves for various combinations of age and level of injury. Neurologic examination was performed at the time of admission with Frankel classification4 till the year 2001 and with the International Standards for Neurological Classification of Spinal Cord Injury from 2001 onward.5,6 Neurologic level of injury was defined as the most caudal segment of the spinal cord with normative sensory and motor function on both sides of the body. In this study, levels of injury were categorized as high cervical (C1-4), low cervical (C5-8), high thoracic (T1-6), low thoracic (T7-12), and lumbosacral (L1-S5). Severity of neurologic deficit was based on either the Frankel classification or the American Spinal Injury Association Impairment Scale (AIS) and divided into 4 groups: grades A, B, C, and D.

Results Demographic and clinical data Records of 490 persons with TSCI were studied. The median age (interquartile range [IQR]) at injury was 31 (IQR, 23e40) years (range, 7e70y). The number of admissions was 59 in the first decade (1981e1990), 212 during the 1990s, and 219 during the 2000s. The median interval from the date of injury till admission to the rehabilitation center was 69 (IQR, 9e240) days. Table 1 shows causes of trauma, and table 2 shows the distribution of persons with SCI in different subgroups. In the high cervical group (C1-4), all persons (nZ47) sustained C4-level injury. Table 3 shows the distribution of persons with complete (Frankel/AIS grade A) and incomplete (Frankel/ AIS grade BeD) SCI in various subgroups. In our study, none of the injured persons were ventilator dependent.

Outcome Out of 490 persons, 357 were alive at the end of the follow-up period. The 5-year survival rate was 86%, and the 25-year survival rate was 58% (table 4). A significant difference was found in the mean survival of higher neurologic levels and severity of neurologic impairment (see table 2). Figures 1 through 4 show the Kaplan-Meier survival curves of the study population.

644 Table 1

A. Barman et al Causes of trauma in SCI (NZ490)

Modes of Trauma

Table 3 n

Falls Falls from tree Fall into well Fall from electric post Fall from roof top/terrace/workplace Motor vehicle collision Others*

%

140 94 38 37 113 68

28.57 19.18 7.76 7.55 23.06 13.88

* Other modes of trauma include work-related injury/fall of heavy objects/stabbing/sports-related injury/attempted suicide/fire arm injury.

Mean survival of SCI injuries among subcategories has been shown in table 3. Among complete injuries (Frankel/ AIS grade A), survival was lowest in high cervical injuries (C1-C4),8 years, where as in incomplete injuries (Frankel/ AIS grade BeD), survival was lowest in low cervical injuries (C5-C8), 16 years, followed by high cervical injuries. Within the group of persons with paraplegic injuries (T1-S5), persons with complete high thoracic injuries (T1-6) had lower survival and a higher mortality rate (see table 3). In univariate assessment (table 5), survival differences reached statistical significance for mode of trauma, neurologic level, and extent of lesion (Frankel/AIS grade). Survival difference did not reach statistical significance in men and with advanced age. From the multivariate results (see table 5), which control for other variables in the analysis, the following patterns were evident: subjects with high cervical tetraplegia (C1-4) had 3.9 times the risk of death compared with L1-S5 subjects; and subjects with complete SCI lesions had 23 times the risk of death and subjects with Frankel/AIS grade B lesions had 20 times the risk of death compared with those with incomplete (Frankel/AIS grade D) lesions.

Table 2

Distribution and survival of cases in SCI subgroups

Injury Subgroups Age (y) 20 20e30 30e40 40e50 >50 Sex Male Female Neurologic level C1-4 C5-8 T1-6 T7-12 L1-S5 AIS grade A B C D

Distribution and survival of cases in SCI subgroups

n

Mean Survival (y)

SE

P

69 174 132 83 32

25.20 21.86 19.68 20.64 18.11

1.26 0.99 0.89 1.33 1.79

.368

439 51

21.69 22.27

0.65 1.43

.359

47 76 59 208 100

17.10 19.89 19.94 21.45 24.66

2.03 1.26 1.66 0.84 1.45

.002

275 78 87 50

19.97 19.26 25.04 28.44

0.81 1.71 0.98 0.55

.000

Abbreviation: ASIA, American Spinal Injury Association.

Injury Subgroup

Cases

No. of Deaths (%)

Mean Survival (y)

SE

C1-4 (grade A) C1-4 (grades B and C) C5-8 (grade A) C5-8 (grades B and C) T1-6 (grade A) T1-6 (grades B and C) T7-12 (grade A) T7-12 (grades B and C) L1-S5 (grade A) L1-S5 (grades B and C) T1-S5 (grade A) T1-S5 (grades B and C) C1-S5 (grade D)

16 23 29 35 42 14 141 55 47 38 230 107 50

11 7 9 13 18 4 44 11 14 1 76 16 1

8.31 18.65 19.70 16.21 18.08 19.57 20.41 20.87 19.72 27.50 20.47 24.71 28.44

1.82 3.03 2.00 1.88 2.05 2.27 1.03 1.36 1.62 1.77 0.87 1.28 0.55

(68.75) (30.43) (31.03) (37.14) (42.86) (28.57) (31.21) (20.00) (29.79) (2.63) (33.04) (14.95) (2.00)

Discussion Overall survival rates from this study are lower than those of corresponding large-scale studies in Western countries.7-10 In this study, 63% persons were alive with sufficient follow-up after 20 years of injury. Studies1,3,11-16 from countries with advanced SCI care systems show survival rates ranging from 69% to 86% after 20 years of injury. Among these, Yeo et al11 (Australia) reported separate survival rates for persons with tetraplegia (76%) and paraplegia (80%) at 20 years. Median survival of persons with TSCI has been variable in different studies. Catz1 (Israel), Lidal12 (Norway), and colleagues showed that the median survival of persons with TSCI was 36.5 years and 27 years, respectively. Similarly, based on level of injury, Lhe´ritier17 (France), Hagen18 (Norway), and colleagues reported the median survival for persons with tetraplegia as 35.6 and 6.8 years, respectively. Other published studies1,2,19,20 have shown that age has a significant impact on survival in the SCI population. Mortality risk increases with higher age at injury, especially in TSCI. A higher hazard ratio was observed with increased age but did not demonstrate statistically significant negative association of survival with age. One possible explanation could be that younger persons had more severe injury and older persons who availed rehabilitative services had lower level and less severe injury. Further investigation is warranted to find the association between age and survival after trauma. We did not find any statistically significant association between sex and survival after TSCI. Catz,1 Claridge,21 Furlan,22 Pollard,23 and colleagues failed to demonstrate significant association between survival of men and women; however, Griffin,9 Frankel,19 DeVivo,24 and colleagues found significant longer survival rates Table 4

Survival rates at various periods after injury (NZ490)

Duration Since Injury (y)

Survival Rate (%)

SE

5 10 15 20 25

86.11 76.76 70.66 63.06 57.75

1.58 2.00 2.37 3.26 4.86

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Survival after traumatic SCI

645

Fig 1 Kaplan-Meier survival curves of the study population (NZ490). 25

among women. Sipski et al reported better neurologic and functional recovery after TSCI in women. Further research is required to demonstrate the association between sex and survival after SCI. Severity of SCI depends on the mode and impact of injury. In this study, we noticed that SCI as a result of falls from height and other modes of trauma (stabbing, attempted suicide, and sportsrelated injury) had higher death rates compared with motor vehicle collisions. However, further postemortem-based studies on the type of injuries and mechanisms involved would be valuable to construe whether it’s a mere coincidence that the nonmotor vehicle collision group had a lower survival rate. Level of injury was an important predictor of survival in our SCI population. The findings were consistent with previous studies.1,2,5,19 High cervical injury (C1-4) had the poorest survival, irrespective of age.26 In our study population, none of the persons in the high cervical injury group had cervical level C1-C3. Among those with complete high cervical injuries (Frankel/AIS grade A), which included only C4 level injury (nZ16), 3 persons died within the first year. At the end of 5 years, 8 (73%) persons

Fig 2

Kaplan-Meier survival curve according to level of injury.

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Fig 3

Kaplan-Meier survival curve according to Frankel/AIS grade.

expired. Only 1 person with complete C4 tetraplegia whose injury occurred at age 38 years survived >10 years. However, these data need to be interpreted cautiously. These findings may not be an actual representation of the overall SCI population because the persons who expired in an acute setting and ventilator-dependent high cervical injuries did not form part of the study population. These data represent only a limited number of persons with SCI who survived the acute insult. Survival was better in lower cervical injuries than high level injuries, as expected. Among persons with complete C5-8 injury (Frankel/AIS grade A, nZ29), 24 persons (83%) survived at least 5 years. We also observed that 1 person (C5-8) with Frankel/AIS grade A impairment survived 23.6 years, which suggests that a well-rehabilitated, motivated individual with complete tetraplegia can achieve a better survival rate. Severity of neurologic injury was found to be an important predictor of survival in TSCI.2,19,24,26 Findings from this study also showed longer survival in populations with better Frankel/AIS grades (or milder SCI). However, this was not observed by Samsa,27 Catz,1 and colleagues, who failed to demonstrate statistically significant association between survival and severity of neurologic

Fig 4 Kaplan-Meier survival curve according to injury level in Frankel/AIS grade A.

646 Table 5

A. Barman et al Case description and univariate and multivariate assessment of hazard ratios using Cox proportional hazards regression Univariate Results

Variable Age (y) 20 20e30 30e40 40e50 >50 Sex Female Male Mode of trauma MVC Fall Others Neurologic level L1-S5 C1-4 C5-8 T1-6 T7-12 AIS grade D A B C

Cases

Deaths

HR

95% CI

Multivariate Results HR

95% CI

69 174 132 83 32

12 49 36 26 10

1.00 1.68 1.60 1.88 2.11

Referent 0.89e3.16 0.83e3.08 0.95e3.72 0.91e4.89

1.00 1.77 1.40 1.69 2.14

Referent 0.93e3.35 0.72e2.72 0.84e3.40 0.91e5.03

51 439

12 121

1.00 1.32

Referent 0.73e2.38

1.00 1.13

Referent 0.62e2.07

113 309 68

20 85 28

1.00 1.62 2.80

Referent 1.00e2.64 1.58e4.98

1.00 1.92 2.83

Referent 1.16e3.18 1.56e5.15

100 47 76 59 208

15 18 22 22 56

1.00 3.58 2.20 2.71 1.81

Referent 1.80e7.11 1.14e4.24 1.41e5.22 1.02e3.20

1.00 3.90 2.02 2.06 1.39

Referent 1.87e8.15 1.01e4.05 1.05e4.02 0.78e2.47

50 275 78 87

1 96 28 8

1.00 21.50 23.71 5.03

Referent 3.00e154.25 3.22e174.33 0.63e40.21

1.00 23.31 20.15 4.85

Referent 3.23e168.15 2.73e148.91 0.60e38.90

Abbreviations: ASIA, American Spinal Injury Association; CI, confidence interval; HR, hazard ratio; MVC, motor vehicle collisions.

injury. Mesard et al7 found such an association only when the level of injury was cervical or high thoracic. In our study, there was a definite difference in mean survival between persons with SCI with motor complete (Frankel/AIS grades A and B) and incomplete (Frankel/AIS grades C and D) injuries. All persons with motor recovery showed better survival rates. DeVivo et al28 documented significant difference in survival between nonfunctional (Frankel grade C) and functional (Frankel grade D) persons. However, Frankel/AIS grades may improve over time and can result in underestimation of the effect of actual SCI severity on mortality. Strauss et al5 noticed a 7 year difference in life expectancy between complete (AIS grade A) and incomplete (AIS grades B and C) high tetraplegia (C1-3). In our study population, a difference of 10 years was observed between survival of complete and incomplete (AIS grades B and C) high tetraplegia (C1-4). However, this was not seen in the low cervical injuries group (C58). In fact, the mean survival of incomplete low cervical injury (Frankel/AIS grades B and C) was 3 years less when compared with complete injury (Frankel/AIS grade A). This finding did not corroborate with findings from previous studies and clinical experience. Further evaluation is warranted to see the association of survival between persons with complete and incomplete lower level tetraplegia. Though we did not observe any significant difference in the mean survival of persons with complete (Frankel/AIS grade A, nZ183, 19y) and incomplete (Frankel/AIS grades B and C, nZ69, 20y) thoracic level (T1-12) injury, there was an 8-year difference (Frankel/AIS grade A vs Frankel/AIS grades B and C) in the lumbosacral (L1-S5) level of injury. Our study showed that among persons with complete (Frankel/AIS grade A) paraplegia (T1-S5,

nZ230), 110 (48%) persons survived at least 10 years. Persons with incomplete (Frankel/AIS grades B and C) paraplegia had 4 years more mean survival than complete (Frankel/AIS grade A) injury. This was not observed by Strauss et al,5 who did not find any difference between complete and incomplete injury among persons with paraplegia. We did not observe a significant difference between complete (AIS grade A) low tetraplegia (C5-8) and complete (AIS grade A) paraplegia (T1-S5). In the United Kingdom SCI data, similar findings have been reported by Coll et al.10 Our study did not account for most of the admitted persons with SCI because 60% to 70% of the persons with SCI rehabilitated at our center are referred from the northeastern part of the country, which is approximately 2000-km away from our center. We do admit and rehabilitate all persons with SCI with significant neurologic deficits regardless of the state/province. Regular home visits for persons who come from distant states/provinces is not possible for either our team and the patients. The regular structured follow-up with home visits and the Rehab Mela have been instrumental in educating and empowering persons with SCI and their families. This has positively influenced their survival in the community. Survival data from other studies when compared with our study should be assessed cautiously, considering the differences in methodology, study design, and analytical methods, which can affect outcomes. Survival expectancy after injury depends on several factors, such as initial management, family support, comorbidities, complications, and existing health care support services. Ronen et al29 pointed out that other risk factors, such as quality of medical care and social attitudes, nutritional status, and socioeconomic factors, affect the survival of persons with SCI. www.archives-pmr.org

Survival after traumatic SCI An observational cohort study from Nepal30 comprising 37 persons with SCI with a mean follow-up duration of 1 to 2 years found that 24% (nZ9) of persons had expired, of whom 35% were wheelchair users. The only other SCI survival analysis from a developing country (Bangladesh), which was published by Razzak et al,31 showed a mean survival rate of 10 years to be a mere 16%. The mean survival rates of SCI at 10 years (77%), 20 years (63%), and 25 years (58%) found in our study are significantly higher, considering the fact that the 2 studies were done from similar social settings where health care and rehabilitation are still mostly self-financed. Though survival rates are not comparable with the rates reported in developed countries, survival in our follow-up population is still reasonably good for a developing country. This could probably be because the holistic spinal injury rehabilitation program from the acute phase up to the stages of vocational rehabilitation and community reintegration has a major impact on the overall survival. Subsequent follow-up communications and evaluations done by the social work liaison team and the monthly random home visits made by the rehabilitation team in the follow-up area may be another major factor. The annual follow-up gathering for persons with SCI (Rehab Mela) is a 3-day residential program organized by the rehabilitation center primarily for persons with SCI who were rehabilitated in our center and residing in our geographic follow-up area. Nearly 200 persons with SCI attend the Rehab Mela every year. Similar but smaller gatherings (mini melas), which are regularly organized in the community, help in peer interaction and support groups. These are a few factors that could possibly have contributed to better survival rates reported in this study. To our knowledge, at present, there is no comprehensive centralized SCI database in India; similar survival analysis information collated from other spine injury rehabilitation centers in India, not just from tertiary care hospitals, would provide better representative data. This could form the basis for policy decisions and interventions aimed at achieving improved survival rates after SCI.

Study limitations There are several limitations of the present study. The data reported here come from a subset of discharged persons with SCI from 1 center. Because this study is retrospective, it does not include data from an acute care setting. The other important limitation is that our study is not population based. It only captures data from persons who received comprehensive inpatient rehabilitation services in our center and organized follow-up. Also, the subjects were from a small catchment area and a specific geographic region, and it may be inappropriate to generalize the results to a national level. The demographics of our population are, however, quite similar to other Indian SCI studies with a predominance of young men being injured and the most common mechanism of injury being fall from height.32,33 Between 1981 and 1990, 59 persons were treated and followed-up in our center. This is very low compared with later years. There is a possibility that a few persons were lost to follow-up because of their death or the unavailability of follow-up records. Another limitation is that our study does not include information on other factors such as smoking history, associated injuries, or other major medical comorbidities that might be of prognostic importance in determining overall survival.

Scope for further study There is a definite need for further research to enhance our understanding of low survival rates and to guide intervention www.archives-pmr.org

647 strategies and government policies to promote greater longevity. Assessment of risks, health status, quality of life, community integration, environment, and economic factors along with psychological well-being in the survival of an SCI population needs to be explored.

Conclusions A structured follow-up program of rehabilitated persons can positively impact survival of SCI even in a low-resource setting. Survival analysis of follow-up in persons with SCI in India shows promising results. Neurologic level and completeness of injury are independent predictors of survival after SCI. Survival of complete higher tetraplegia is substantially low compared with other SCI populations. Better understanding of the predictors, causes of deaths, comprehensive rehabilitation, community integration, and regular follow-up could possibly assist in improvement of survival rates.

Supplier a. SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

Keywords Rehabilitation; Spinal cord injuries; Survival

Corresponding author Apurba Barman, MD, Department of PM&R, All India Institute of Medical Sciences, Bhubaneswar, India 751019. E-mail address: [email protected].

Acknowledgment We thank Suranjan Bhattacharji, MS (Ortho), DNB(PMR), for his continuous encouragement, guidance during the data analysis, and valuable suggestions in shaping the manuscript.

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Survival in persons with traumatic spinal cord injury receiving structured follow-up in South India.

To assess the survival in persons with traumatic spinal cord injury (SCI) receiving structured follow-up in South India...
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