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Original article
Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors Ronzi a,b, B. Perrouin-Verbe b, O. Hamel c, R. Gross b,*
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Q1 Y.
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Q2 a Centre re´gional de re´e´ducation et de re´adaptation fonctionnelles Les Capucins, rue des Capucins, Angers, France b
Service de me´decine physique et de re´adaptation neurologique, centre hospitalier universitaire de Nantes, 85, rue Saint-Jacques, 44093 Nantes cedex 1, France c Service de neurotraumatologie, centre hospitalier universitaire de Nantes, place Alexis-Ricordeau, 44093 Nantes cedex 1, France
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A R T I C L E I N F O
A B S T R A C T
Article history: Received 16 October 2016 Accepted 25 September 2017
Objectives: To specify outcomes and identify prognostic factors of neurologic and functional recovery in patients with an acute traumatic spinal cord injury (SCI) associated with cervical spinal canal stenosis (SCS), without spinal instability. Methods: A retrospective study was conducted using data from a Regional Department for SCI rehabilitation in France. A description of the population characteristics, clinical data and neurological and functional outcomes of all patients treated for acute SCI due to cervical trauma associated with SCS was performed. A statistical analysis provided insights into the prognostic factors associated with the outcomes. Results: Sixty-three patients (mean age 60.1 years) were hospitalized for traumatic SCI with SCS and without instability between January 2000 and December 2012. Falls were the most frequent cause of trauma (77.8%). At admission, most patients had an American Spinal Injury Association Impairment Scale (AIS) grade of C (43.3%) or D (41.7%) and the most frequent neurological levels of injury were C4 (35.7%) and C5 (28.6%). Clinical syndromes were frequently identified (78.6%), with the most frequent being the Brown-Sequard plus syndrome (BSPS) (30.9%), followed by central cord syndrome (CCS, 23.8%). Almost 80% of survivors returned to the community, 60% were able to walk and 75% recovered complete voluntary control of bladder function. Identified prognostic factors of favourable functional outcomes were higher AIS at admission, age under 60 years and presence of BSPS or CCS. Conclusion: Traumatic SCI, associated with SCS results mostly in incomplete injuries, can cause various syndromes and is associated with favourable functional outcomes.
C 2017 Elsevier Masson SAS. All rights reserved.
Keywords: Spinal cord injury Cervical spinal canal stenosis Cord syndromes Tetraplegia Functional outcome
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1. Introduction
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Cervical spondylosis affects up to 50% of persons over 40 years of age [1]. It often causes spinal canal stenosis (SCS), leading to neck pain, cervical radiculopathy and cervical myelopathy [1]. Subjects with cervical spondylosis have a higher risk of spinal cord lesions since the cord cannot move freely within the spinal canal, thus mild cervical trauma can cause devastating spinal cord
Abbreviations: ACS, anterior cord syndrome; AIS, ASIA Impairment Scale; ASIA, American Spinal Injury Association; BSPS, Brown-Sequard plus syndrome; CCS, central cord syndrome; MRI, magnetic resonance imaging; NLI, neurological level of injury; SCI, spinal cord injury; SCS, spinal canal stenosis; TDM, tomodensitometry. * Corresponding author. E-mail address: [email protected] (R. Gross).
injuries [2]. The anatomical features of such injuries usually include haematoma, oedema and myelomalacia, mostly affecting the central part of the spinal cord [3]. Schneider and Cherry provided the classical description of the symptoms that occur following cervical spinal cord injury (SCI) on an already compressed spinal cord [3]: weakness mostly affecting the upper limbs and various impairments of the lower limbs, including loss of bladder and bowel function. This clinical condition is today referred to as ‘traumatic central cord syndrome’ (CCS) and criteria for its diagnosis have recently been precisely defined [4]. Despite the generally older age of patients with CCS [5], this syndrome is associated with more favourable functional outcomes than other SCI-related syndromes [5–7]. CCS and traumatic SCI with CCS are frequently confused, probably because of the initial statement by Schneider and Cherry
http://dx.doi.org/10.1016/j.rehab.2017.09.003 C 2017 Elsevier Masson SAS. All rights reserved. 1877-0657/
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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that CCS affects older patients with cervical spondylosis [3]. However, various situations may arise in subjects with acute SCI and concomitant cervical spondylosis [8]. Although this condition was first described more than 50 years ago, data relating to sociodemographic characteristics, clinical signs and symptoms and outcomes are lacking [8,9]. Such knowledge would help to determine appropriate management for this condition. One retrospective study investigated the clinical features and prognostic factors of CCS, however this was in a subset of patients who underwent surgical decompression [10]. The aims of this study were therefore:
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to describe the clinical features at the time of admission in patients with acute traumatic SCI associated with cervical CCS, without spinal instability; to identify outcomes and prognostic factors of neurologic and functional recovery in these patients.
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2. Methods
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2.1. Patients
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A retrospective analysis of all patients referred to our SCI centre was conducted. This centre includes an acute care Neurotrauma unit and a Physical and Rehabilitation Medicine (PRM) department. All cases, admitted between the 1st of January 2000 and the 31st of December 2012, were reviewed. The inclusion criteria were:
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trauma to the cervical spinal cord with neurological impairment in the acute phase; no unstable spinal lesion, verified by computed tomography (CT) and magnetic resonance images (MRI) using the criteria defined by White and Panjabi [11] (all patients systematically underwent CT and MRI). Any patients with fracture, dislocation, disc lesion or vertebral sprain that was at risk of displacement or compromising the spinal canal were excluded. This choice is in accordance with many previous studies [9,10,12]: patients with radiological features of spinal instability were excluded because in many centres, including ours, these patients undergo immediate surgery to treat the cause of instability and reduce cord compression. Besides, it is not possible to differentiate between neurological involvement due to spinal stenosis and cord oedema and that due to acute cord compression by bony or disc elements; presence of cervical spinal canal stenosis. Cervical spinal canal stenosis was confirmed by the ‘Pavlov’ ratio on CT images [13]. A ratio < 0.8 at any level between C3 and C7 was considered as stenosis, with or without evidence of spondylosis.
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All patients who met these three criteria were considered, whether they underwent surgery during the initial stages or not and regardless of corticosteroid administration.
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2.2. Data collection
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All applicable institutional and governmental regulations concerning the ethical use of human volunteers were followed during the course of this research. This study conformed to the Helsinki Declaration of 1975, revised in 2013 and was approved by our institutional ethics board. Data were collected retrospectively, during the year 2015. The two-year delay between the end of the inclusion period and the beginning of data collection was necessary in order to obtain discharge data for all patients.
Two time points were considered:
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admission to the acute care unit; discharge from the PRM department.
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The endpoint evaluation was performed at discharge since data at other time points (for instance, 6 months post-injury) were not available for all patients. Moreover, it is common practice to report data at discharge in epidemiological studies of patients with SCI [6,14,15]. All patients underwent standard neurological assessment. The neurological examination was performed according to the International Standards for Neurological Classification of Spinal Cord Injury [16]. The American Spinal Injury Association (ASIA) Impairment Scale (AIS), the neurological level of injury (NLI) and the presence of a clinical syndrome were evaluated. Clinical syndromes included central cord syndrome (CCS), Brown-Sequard plus syndrome (BSPS), transverse syndrome, anterior cord syndrome (ACS) and posterior cord syndrome. CCS was defined according to the criteria by the EM-SCI study group [4]: disproportionately more motor impairment of the upper than lower extremities, with a difference of at least 10 motor score points between the upper and lower extremities. BSPS was defined according to the description by Roth et al. [17]: asymmetric paresis with more marked hypoalgesia on the less paretic side. Transverse syndrome was considered as complete SCI. ACS was defined as loss of motor function and pain/temperature sensation at and below the injury level, with preservation of light touch and joint position sense [16]. PCS was defined as isolated loss of proprioception and vibration sense below the level of injury [6]. Data regarding function, including ambulatory status and lower urinary tract function on discharge and discharge mode were collected from the medical files. Level of ambulation was defined as the mode of locomotion for distances over 10 m (without gait aid, with gait aid, manual or electric wheelchair). Lower urinary tract function included bladder-emptying method (voluntary control, self-intermittent catheterization, hetero-catheterization, indwelling catheter or reflex micturition). Discharge mode included return home with or without any personal assistance for activities of daily living or hospital/institution care.
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2.3. Data analysis and prognostic factors
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For qualitative variables, data are provided as numbers and percentages. For quantitative variables, data are presented as means and/or medians and standard deviations. To search for explanatory factors relating to progression or stability of the AIS grade between admission and discharge (neurological prognosis), Fisher exact tests were performed with improvements in grade (yes/no) on one side and potential explanatory factors of improvement on the other side. The potential explanatory factors were:
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age ( 60 or < 60); cause of SCI; surgery (yes/no); the type of clinical syndrome caused by the SCI.
Three categories of clinical syndrome were considered to determine prognostic factors (BSPS, CCS and no, or other, identified syndrome) in order to have approximately similar numbers in each group. Then, in order to search for explanatory factors of functional outcome, Fisher exact tests were performed with patients with or without favourable outcomes on one side and potential explanatory factors of outcomes on the other side. Three outcomes were assessed:
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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discharge mode; ambulation mode; bladder function.
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The potential explanatory factors for functional outcomes were the same as for neurological prognosis. SPSS software was used for data analysis with the significance level set at P = 0.05.
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Q3 3. Results
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3.1. Sociodemographic data and neurological status at admission
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Sixty-three patients were included in the study. Fifty were male (79.4%). Mean age was 60.1 years (S.D. = 14.8; range = 30–88 years) Fig. 1. Falls were the main cause of trauma (49 patients, 77.8%), followed by motor vehicle crashes (7 patients, 11.1%) sports injuries (6 patients, 9.5%) and acts of violence (1 patient, 1.6%). AIS was established at admission for 60 out of the 63 patients and NLI and clinical syndrome were determined for 42 patients (see Fig. 2 for results). Associated drowsiness prevented these data being obtained in the other patients. Forty-six out of 63 patients (73%) underwent cervical spine surgery. The time between trauma and surgery ranged from 0 to 430 days (mean: 62.7 94.7 days, median: 14.5 days). Surgery was independent of age and AIS grade. All patients who were operated underwent decompressive laminectomy (posterior approach). No patients were administered corticosteroids (Figs. 1 and 2).
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3.2. Neurological status at discharge
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Three patients died in the acute care phase because of respiratory complications. Three patients were lost to follow-up because of transfer to another rehabilitation centre. Therefore, a complete neurological and functional assessment at discharge was obtained for 57 patients. The mean length of stay (time from admission to discharge) for these 57 patients was 267.7 days and the median was 140 days (range: 8–2561). The very long stay of 2561 days was due a patient with AIS A SCI at C3 for whom a care institution could not be found. Table 1 shows the change in AIS grade between admission and discharge for the 57 patients. AIS grade improved by at least one point between admission and discharge for thirty-five patients (61.4%) and remained unchanged for 22 patients (38.6%). Age, cause, surgery and clinical syndrome were not significantly associated with improvement in AIS grade. Table 2 shows the change in NLI between admission and discharge for the 42 patients who had a complete assessment at both admission and discharge.
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3.3. Functional status at discharge and prognostic factors
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Data regarding discharge mode, ambulation status at discharge and bladder function could be obtained for 57 patients. Table 3 displays the complete results for functional outcomes and associated prognostic factors (Table 3).
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Fig. 1. Flow-chart of patients included with SCI with underlying spinal canal stenosis without instability. AIS: ASIA impairment scale; NLI: neurological level of injury.
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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Fig. 2. Neurological data of the patients at admission. A: ASIA impairment scale (AIS); B: neurological level of injury. C: distribution of clinical syndromes in the 42 patents with a complete neurological examination; ACS: anterior cord syndrome; CCS: central cord syndrome; BSPS: Brown-Sequard plus syndrome.
Table 1
Q4 Change in ASIA impairment scale (AIS) grade between admission and discharge for the 57 patients with AIS scores at both time points.
Table 2 Change in neurological level of injury (NLI) between admission and discharge for the 42 patients with a complete assessment at both time points.
AIS at discharge
AIS at admission A B C D Total
NLI at discharge
A
B
C
D
E
Total
1 – – – 1
– 1 – – 1
2 3 4 – 9
– 1 19 16 36
– – 2 8 10
3 5 25 24 57
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4. Discussion
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This study reviewed all consecutive cases of acute SCI caused by trauma to the cervical spinal cord with associated spinal canal stenosis and no spinal instability, over a 12-year period. The majority of patients had incomplete lesions with AIS grades of C or D and NLI at C4 and C5. A clinical syndrome could be identified in more than 75% of cases, with BSPS and CCS being the most frequent. Overall, outcomes were positive regarding discharge mode, ambulatory status and bladder function. Age under 60 years, higher AIS grades at admission and the presence of CCS or BSPS were identified as favourable prognostic factors.
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4.1. Precise definition of the condition investigated and epidemiologic data
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The purpose of this study was to specifically investigate the initial condition, outcomes and prognostic factors of patients with acute, traumatic SCI within a stenotic cervical spinal canal, without spinal instability. This particular condition was chosen because it is clinically relevant [12,18,19]. Recent epidemiological data in the
NLI at admission C1 C3 C4 C5 C6 C7 C8 Total
C1
C3
C4
C5
C6
C7
C8
Total
– – – – – – – 0
– 2 2 2 1 – – 7
– 1 3 1 – – – 5
– 2 9 4 1 – – 16
– – 1 3 2 – – 6
– 3 – 2 1 1 – 7
– – – – – 1 – 1
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field of SCI have focused on the aging population, incomplete injuries and an increased proportion of falls as the cause of trauma [20]. Thus, there has been an increase in attention on SCS. To date, the only studies describing neurological data and outcomes of patients with SCS, included patients who underwent surgical decompression [10], or involved small samples from several SCI centres [9]. In the present study, which provided a global analysis of this clinical condition, the single-centre design allowed for a homogenous sample, which was, moreover, relatively large since the study covered a period of 12 years. The mean and median age of the patients in the present study was about 60 years. This is in line with previous studies and confirms that patients with spinal stenosis who have a SCI (age at injury about 60 years) are older than the overall SCI population (age at injury 35 to 40 years [20]). Falls were the greatest cause of trauma in the present study, representing more than 75% of cases. This rate is higher than reports in previous studies [21]. This could be due to the fact that all patients in this study had canal stenosis, making them vulnerable to SCI from minor trauma such as a fall. It
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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Table 3 Prognostic factors of independence (discharge home with or without a carer), ambulatory status (independent walking with or without crutches) and bladder function at discharge. Predictive factor Age (n = 57) < 60 years (n = 29) 60 years (28) AIS at admission (n = 57) A (n = 3) B (n = 5) C (n = 25) D (n = 24) Surgery (n = 57) Yes (n = 43) No (n = 14) Delay of surgery (n = 43) 14 days (n = 22) 15 days (n = 21) Clinical Syndrome (n = 42) BSPS (n = 13) CCS (n = 10) Other (n = 19)
Patients discharged home [n (%)]
Fisher’s exact test
Independent walkers at discharge [n (n (%)]
P < 0.001 29 (100%) 17 (60.7%)
20 (69%) 9 (32.1%)
(33.3%) (60%) (72%) (100%)
P = 0.765
P=1
P = 0.728 33 (77.3%) 10 (71.4%)
P = 0.033 8 (36.4%) 15 (71.4%)
P = 0.507 9 (69.2%) 9 (90%) 15 (78.9%)
P < 0.001 0 1 (20%) 16 (64%) 24 (100%)
22 (51.2%) 8 (57.1%)
19 (86.4%) 19 (90.5%)
P = 0.141
P < 0.001
P=1
P = 0.6988 17 (86.4%) 18 (85.7%)
P = 0.038 3 (23.1%) 8 (80%) 8 (42.1%)
Fisher’s exact test
24 (82.3%) 18 (64.3%)
0 1 (20%) 8 (32%) 19 (79.1%)
21 (48.8%) 7 (50%)
Patients with voluntary bladder control at discharge [n (%)]
P = 0.008
P = 0.001 1 3 18 24
Fisher’s exact test
P = 0.013 10 (76.9%) 9 (90%) 3 (15.8%)
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is also likely that some patients with SCS had pre-existing cervical myelopathy, increasing their risk of falls.
SCI and the consequences (type/clinical presentation) must not be confused.
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4.2. Clinical profiles of patients
4.3. Neurological and functional outcomes and associated prognostic factors
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Not surprisingly, the majority of patients included had incomplete lesions with AIS grades C and D and the most frequent NLI were C4 and C5. All previous studies of acute SCI with SCS, starting with the pioneering study by Schneider and Cherry [3], reported mostly incomplete motor lesions, today classified as AIS C or D. The NLI has been less extensively investigated. Interestingly, the distribution of levels in the present study does not differ from the overall distribution among patients with SCI [15]. It may be that the mid-cervical spine is particularly vulnerable to injury, explaining that it is the most frequent site of SCI. Alternatively, the distribution of NLI could follow the topography of spondylosisrelated degeneration, known to be most prevalent between C3 and C6 [10]. The outstanding feature of the sample in the present study was the high rate of clinical syndromes and the fact that CCS was not the most frequent. A previous study in 839 patients with SCI found that only 20.9% had a clinical syndrome [6], while this rate reached 78.6% in the present study. Such a discrepancy could be attributed several factors. First, the syndromes included differed. The study by McKinley et al. [6], included patients with posterior cord syndrome, cauda equina syndrome and conus medullaris syndrome and the transverse syndrome was only included in the present study. Second, the definitions of CCS differed, since we used the criteria proposed recently by the EMSCI study group [4]. Finally, the present study only covered cervical SCI. Since most cervical lesions are incomplete, there is a higher probability of occurrence of a clinical syndrome than for lesions in other parts of the spine. BSPS (30.9%) was a little more frequent than CCS (23.8%) in the present sample of posttraumatic SCI with underlying SCS. In previous studies, the most frequent syndrome was found to be CCS, accounting for about 50% [6] or even 70% [9,22] of syndromes. However, as mentioned above, the diagnostic criteria for CCS used in the present study has been recently revised, possibly explaining the lower rate found here. Nonetheless, the present study reports several syndromes, not only the classical CCS, relating to SCI with underlying cervical spinal canal stenosis. This emphasizes that the cause/mechanism of the
The outcomes of the patients included were fair. The mortality rate was lower than 5%. Almost two thirds experienced an improvement of at least one grade on the AIS between admission and discharge, which is a markedly higher rate than for the general SCI population [15]. More than 80% of patients had an AIS grade of D or E at discharge. Acute CCS associated with traumatic cervical SCI is known to have a favourable prognosis overall [3,5,9]. Our data confirm that regardless of the syndrome, patients with incomplete cervical SCI associated with SCS have a high potential for improvement of AIS grade and reach the D or E grade. It is thus important to provide appropriate acute-care treatment and to determine relevant goals and rehabilitation strategies in this population. The functional outcomes were favourable. Almost 80% of survivors returned to the community, 60% could walk and 75% recovered complete voluntary control of bladder function. The prognostic factors identified for positive functional outcomes were a less severe AIS grade at admission, age under 60 and the presence of CCS or BSPS. Age and AIS at admission are well established as prognostic factors in SCI [8,9,14,15]. However, caution must be taken when considering the type of clinical syndrome as a predictive factor because BSPS and CCS are very often associated with AIS grades C or D and it could be that they stood out as prognostic factors only because they were associated with more severe AIS grades at admission. Future studies with larger samples might allow other statistical analyses that account for such confounding factors to be carried out. There was no difference in outcomes between patients who underwent surgery and those who did not. The benefits of surgery in patients with SCI and cervical SCS is a matter of debate since, as stated by Schneider et al. and Schneider and Cherry, recovery can occur spontaneously in this condition [2,3]. More recently, the meta-analysis by La Rosa et al. suggested outcomes may be improved when early decompression is performed in case of incomplete SCI. In 2010, a consensus of experts provided recommendations concerning this issue [19]. They stated that early (within 24 hours) surgery is
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Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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indicated in patients with AIS grade C with obvious spinal compression in the absence of unstable lesions, while they recommended observation in the acute phase for patients with AIS grade D. In the present study, surgical decompression was not a prognostic factor of neurological improvement or of favourable functional outcomes. However, the time between trauma and surgery, when performed, was extremely variable (ranging from 0 to 430 days). The present results showed a higher rate of independent walking at discharge following delayed ( 15 days) than early ( 14 days) surgery. The reasons behind the decision to carry out early surgical decompression are diverse (neurological worsening, absence of neurological improvement associated with persistent spinal compression on MRI, evidence of severe spinal canal stenosis and cord oedema, extension of the pathological signal on MRI etc.) Therefore, in the present study early surgery may have been performed in a subset of patients who were not improving, which could explain why it was associated with a less favourable outcome. Uncertainty thus persists regarding the riskbenefit ratio of surgical decompression and the optimal timing for surgery. We hope the results of the recently designed COSMIC trial, comparing early surgical management to conservative treatment in incomplete cervical SCI without spinal instability will give answers to this key-issue [12]. As canal stenosis is the main pathophysiological factor in this type of SCI, we hypothesise that early decompression would improve outcomes for patients with this condition. To verify this hypothesis, we have recently begun a randomized controlled trial, comparing early (within 48 hours) vs. delayed (at 15 days posttrauma) surgery in this population.
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4.4. Limitations
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Due to the retrospective nature of this study, no strong conclusions can be made regarding the relationship between the patient’s history and clinical status and outcomes. Another limitation is that although the proportion of patients who were lost to follow-up was reasonable (approximately 10%: 6 out of 63), one third of the patients had an incomplete neurological evaluation at admission, preventing attribution of a precise NLI or AIS grade. ASIA motor and sensory scores were not included in the study because of missing data and uncertainties regarding their reporting. The statistical associations between potential explanatory factors and neurological or functional outcomes may have been affected by these missing data. Some limitations cannot be avoided, such as drowsiness that prevents precise evaluation in the acute phase, even in prospective studies. Other evaluations would be useful in this population, such as the functional independence measure. The present study focused on the outcomes that are the easiest to assess in a retrospective study. However, our team is currently joining the European Multicenter Study on Human Spinal Cord Injury (EM-SCI; www. emsci.org) and we hope that this will improve the exhaustiveness and homogeneity of follow-up for patients with SCI in the future. Moreover, the more systematic approach will help provide complete, multidimensional data with outcomes in the domains of impairments, activity limitations, participation restrictions and quality of life.
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5. Conclusion
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Traumatic SCI associated with cervical spinal canal stenosis with no spinal instability was caused by falls in 75% of cases. It resulted mostly in incomplete injuries of AIS grade C or D and NLI C4 or C5. Various syndromes occurred, with a slightly higher frequency of BSPS than CCS. Patients with this condition had overall favourable outcomes regarding bladder function, ambula-
tory capacity and independence. A less severe AIS grade at admission, age under 60 years and the presence of BSPS or CCS were associated with more positive outcomes. Further prospective studies and exhaustive data collection are essential to provide strong recommendations regarding indications and timing of decompressive surgery in these patients.
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Funding
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This study received no funding. Disclosure of interest The authors declare that they have no competing interest.
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References
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[1] Rao RD, Currier BL, Albert TJ, Bono CM, Marawar SV, Poelstra KA, et al. Degenerative cervical spondylosis: clinical syndromes, pathogenesis and management. J Bone Jt Surg 2007;89:1360–78. [2] Schneider RC, Thompson JM, Bebin J. The syndrome of acute central cervical spinal cord injury. J Neurol Neurosurg Psychiatry 1958;21:216–27. [3] Schneider R, Cherry GHP. The syndrome of acute central cervical spinal cord injury: with special reference to the mechanisms involved in hyperextension injuries of cervical spine. J Neurosurg 1954;11:546–77. [4] Middendorp JJ, Van, Pouw MH, Hayes KC, Williams R, Chhabra HS, et al. Diagnostic criteria of traumatic central cord syndrome. Part 2: a questionnaire survey among spine specialists. Spinal Cord 2010;48:657–63. [5] Aito S, Andrea MD, Werhagen L, Farsetti L, Cappelli S, Bandini B, et al. Neurological and functional outcome in traumatic central cord syndrome. Spinal Cord 2007;45:292–7. [6] Mckinley W, Santos K, Meade M, Brooke K. Incidence and outcomes of spinal cord injury clinical syndromes. J Spinal Cord Med 2007;30:215–24. [7] Roth EJ, Lawler M, Yarkony G. Traumatic central cord syndrome: clinical features and functional outcomes. Arch Phys Med Rehabil 1990;71:18–23. [8] Harrop JS, Sharan A, Ratliff J. Central cord injury: pathophysiology, management and outcomes. Spine J 2006;6:S198–206. [9] Waters RL, Adkins RH, Sie IH, Yakura JS. Motor recovery following spinal cord injury associated with cervical spondylosis: a collaborative study. Spinal Cord 1996;34:711–5. [10] Aarabi B, Alexander M, Mirvis SE, Shanmuganathan K, Chesler D, Maulucci C, et al. Predictors of outcome in acute traumatic central cord syndrome due to spinal stenosis. J Neurosurg Spine 2011;14:122–30. [11] White A, Panjabi M. The problem of clinical instability in the human spine: a systematic approach. Clin Biomech spine. Baltimore, New York: Lippincott, Philadelphia; 1990. p. 277–378. [12] Bartels RHM, Hosman AJF, van de Meent H, Hofmeijer J, Vos PE, Slooff WB, et al. Design of COSMIC: a randomized, multicentre controlled trial comparing conservative or early surgical management of incomplete cervical cord syndrome without spinal instability. BMC Musculoskelet Disord 2013;14:52. [13] Pavlov H, Torg J, Robie B, Jahre C. Cervical spinal stenosis: determination with vertebral body ratio method. Radiology 1987;164:771–5. [14] Kirshblum SC, O’Connor KC. Predicting neurologic recovery in traumatic cervical spinal cord injury. Arch Phys Med Rehabil 1998;79:1456–66. [15] Marino RJ, Ditunno JF, Donovan WH, Maynard F. Neurologic recovery after traumatic spinal cord injury: data from the model spinal cord injury systems. Arch Phys Med Rehabil 1999;80:1391–6. [16] Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves D, Jha A, et al. International standards for neurological classification of spinal cord injury (revised 2011). J Spinal Cord Med 2011;34:535–46. [17] Roth EJ, Park T, Pang T, Markony TM, Lee MY. Traumatic cervical brownsequard and brown-sequard-plus syndromes: the spectrum of presentations and outcomes. Paraplegia 1991;29:582–9. [18] La Rosa G, Conti A, Cardali S, Cacciola F, Tomasello F. Does early decompression improve neurological outcome of spinal cord injured patients? Appraisal of the literature using a meta-analytical approach. Spinal Cord 2004;42:503–12. [19] Lenehan B, Fisher C, Vaccaro A, Fehlings M, Aarabi B, Dvorak M. The urgency of surgical decompression in acute central cord injuries with spondylosis and without instability. Spine (Phila Pa 1976) 2010;1:S180–6. [20] Devivo MJ, Chen Y. Trends in new injuries, prevalent cases and aging with spinal cord injury. Arch Phys Med Rehabil 2011;92:332–8. [21] Kato H, Kimura A, Sasaki R, Kaneko N, Takeda M, Hagiwara A, et al. Cervical spinal cord injury without bony injury: a multicenter retrospective study of emergency and critical care centers in Japan. J Trauma-Injury Infect Crit Care 2008;65:373–9. [22] Lamothe G, Muller F, Vital JM, Goossens D, Barat M. Evolution of spinal cord injuries due to cervical canal stenosis without radiographic evidence of trauma (SCIWORET): a prospective study. Ann Phys Rehabil Med 2011;54:213–24.
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Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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Available online at
ScienceDirect www.sciencedirect.com
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Original article
Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors Ronzi a,b, B. Perrouin-Verbe b, O. Hamel c, R. Gross b,*
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Q1 Y.
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Q2 a Centre re´gional de re´e´ducation et de re´adaptation fonctionnelles Les Capucins, rue des Capucins, Angers, France b
Service de me´decine physique et de re´adaptation neurologique, centre hospitalier universitaire de Nantes, 85, rue Saint-Jacques, 44093 Nantes cedex 1, France c Service de neurotraumatologie, centre hospitalier universitaire de Nantes, place Alexis-Ricordeau, 44093 Nantes cedex 1, France
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A R T I C L E I N F O
A B S T R A C T
Article history: Received 16 October 2016 Accepted 25 September 2017
Objectives: To specify outcomes and identify prognostic factors of neurologic and functional recovery in patients with an acute traumatic spinal cord injury (SCI) associated with cervical spinal canal stenosis (SCS), without spinal instability. Methods: A retrospective study was conducted using data from a Regional Department for SCI rehabilitation in France. A description of the population characteristics, clinical data and neurological and functional outcomes of all patients treated for acute SCI due to cervical trauma associated with SCS was performed. A statistical analysis provided insights into the prognostic factors associated with the outcomes. Results: Sixty-three patients (mean age 60.1 years) were hospitalized for traumatic SCI with SCS and without instability between January 2000 and December 2012. Falls were the most frequent cause of trauma (77.8%). At admission, most patients had an American Spinal Injury Association Impairment Scale (AIS) grade of C (43.3%) or D (41.7%) and the most frequent neurological levels of injury were C4 (35.7%) and C5 (28.6%). Clinical syndromes were frequently identified (78.6%), with the most frequent being the Brown-Sequard plus syndrome (BSPS) (30.9%), followed by central cord syndrome (CCS, 23.8%). Almost 80% of survivors returned to the community, 60% were able to walk and 75% recovered complete voluntary control of bladder function. Identified prognostic factors of favourable functional outcomes were higher AIS at admission, age under 60 years and presence of BSPS or CCS. Conclusion: Traumatic SCI, associated with SCS results mostly in incomplete injuries, can cause various syndromes and is associated with favourable functional outcomes.
C 2017 Elsevier Masson SAS. All rights reserved.
Keywords: Spinal cord injury Cervical spinal canal stenosis Cord syndromes Tetraplegia Functional outcome
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1. Introduction
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Cervical spondylosis affects up to 50% of persons over 40 years of age [1]. It often causes spinal canal stenosis (SCS), leading to neck pain, cervical radiculopathy and cervical myelopathy [1]. Subjects with cervical spondylosis have a higher risk of spinal cord lesions since the cord cannot move freely within the spinal canal, thus mild cervical trauma can cause devastating spinal cord
Abbreviations: ACS, anterior cord syndrome; AIS, ASIA Impairment Scale; ASIA, American Spinal Injury Association; BSPS, Brown-Sequard plus syndrome; CCS, central cord syndrome; MRI, magnetic resonance imaging; NLI, neurological level of injury; SCI, spinal cord injury; SCS, spinal canal stenosis; TDM, tomodensitometry. * Corresponding author. E-mail address: [email protected] (R. Gross).
injuries [2]. The anatomical features of such injuries usually include haematoma, oedema and myelomalacia, mostly affecting the central part of the spinal cord [3]. Schneider and Cherry provided the classical description of the symptoms that occur following cervical spinal cord injury (SCI) on an already compressed spinal cord [3]: weakness mostly affecting the upper limbs and various impairments of the lower limbs, including loss of bladder and bowel function. This clinical condition is today referred to as ‘traumatic central cord syndrome’ (CCS) and criteria for its diagnosis have recently been precisely defined [4]. Despite the generally older age of patients with CCS [5], this syndrome is associated with more favourable functional outcomes than other SCI-related syndromes [5–7]. CCS and traumatic SCI with CCS are frequently confused, probably because of the initial statement by Schneider and Cherry
http://dx.doi.org/10.1016/j.rehab.2017.09.003 C 2017 Elsevier Masson SAS. All rights reserved. 1877-0657/
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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that CCS affects older patients with cervical spondylosis [3]. However, various situations may arise in subjects with acute SCI and concomitant cervical spondylosis [8]. Although this condition was first described more than 50 years ago, data relating to sociodemographic characteristics, clinical signs and symptoms and outcomes are lacking [8,9]. Such knowledge would help to determine appropriate management for this condition. One retrospective study investigated the clinical features and prognostic factors of CCS, however this was in a subset of patients who underwent surgical decompression [10]. The aims of this study were therefore:
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to describe the clinical features at the time of admission in patients with acute traumatic SCI associated with cervical CCS, without spinal instability; to identify outcomes and prognostic factors of neurologic and functional recovery in these patients.
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2. Methods
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2.1. Patients
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A retrospective analysis of all patients referred to our SCI centre was conducted. This centre includes an acute care Neurotrauma unit and a Physical and Rehabilitation Medicine (PRM) department. All cases, admitted between the 1st of January 2000 and the 31st of December 2012, were reviewed. The inclusion criteria were:
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trauma to the cervical spinal cord with neurological impairment in the acute phase; no unstable spinal lesion, verified by computed tomography (CT) and magnetic resonance images (MRI) using the criteria defined by White and Panjabi [11] (all patients systematically underwent CT and MRI). Any patients with fracture, dislocation, disc lesion or vertebral sprain that was at risk of displacement or compromising the spinal canal were excluded. This choice is in accordance with many previous studies [9,10,12]: patients with radiological features of spinal instability were excluded because in many centres, including ours, these patients undergo immediate surgery to treat the cause of instability and reduce cord compression. Besides, it is not possible to differentiate between neurological involvement due to spinal stenosis and cord oedema and that due to acute cord compression by bony or disc elements; presence of cervical spinal canal stenosis. Cervical spinal canal stenosis was confirmed by the ‘Pavlov’ ratio on CT images [13]. A ratio < 0.8 at any level between C3 and C7 was considered as stenosis, with or without evidence of spondylosis.
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All patients who met these three criteria were considered, whether they underwent surgery during the initial stages or not and regardless of corticosteroid administration.
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2.2. Data collection
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All applicable institutional and governmental regulations concerning the ethical use of human volunteers were followed during the course of this research. This study conformed to the Helsinki Declaration of 1975, revised in 2013 and was approved by our institutional ethics board. Data were collected retrospectively, during the year 2015. The two-year delay between the end of the inclusion period and the beginning of data collection was necessary in order to obtain discharge data for all patients.
Two time points were considered:
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admission to the acute care unit; discharge from the PRM department.
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The endpoint evaluation was performed at discharge since data at other time points (for instance, 6 months post-injury) were not available for all patients. Moreover, it is common practice to report data at discharge in epidemiological studies of patients with SCI [6,14,15]. All patients underwent standard neurological assessment. The neurological examination was performed according to the International Standards for Neurological Classification of Spinal Cord Injury [16]. The American Spinal Injury Association (ASIA) Impairment Scale (AIS), the neurological level of injury (NLI) and the presence of a clinical syndrome were evaluated. Clinical syndromes included central cord syndrome (CCS), Brown-Sequard plus syndrome (BSPS), transverse syndrome, anterior cord syndrome (ACS) and posterior cord syndrome. CCS was defined according to the criteria by the EM-SCI study group [4]: disproportionately more motor impairment of the upper than lower extremities, with a difference of at least 10 motor score points between the upper and lower extremities. BSPS was defined according to the description by Roth et al. [17]: asymmetric paresis with more marked hypoalgesia on the less paretic side. Transverse syndrome was considered as complete SCI. ACS was defined as loss of motor function and pain/temperature sensation at and below the injury level, with preservation of light touch and joint position sense [16]. PCS was defined as isolated loss of proprioception and vibration sense below the level of injury [6]. Data regarding function, including ambulatory status and lower urinary tract function on discharge and discharge mode were collected from the medical files. Level of ambulation was defined as the mode of locomotion for distances over 10 m (without gait aid, with gait aid, manual or electric wheelchair). Lower urinary tract function included bladder-emptying method (voluntary control, self-intermittent catheterization, hetero-catheterization, indwelling catheter or reflex micturition). Discharge mode included return home with or without any personal assistance for activities of daily living or hospital/institution care.
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2.3. Data analysis and prognostic factors
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For qualitative variables, data are provided as numbers and percentages. For quantitative variables, data are presented as means and/or medians and standard deviations. To search for explanatory factors relating to progression or stability of the AIS grade between admission and discharge (neurological prognosis), Fisher exact tests were performed with improvements in grade (yes/no) on one side and potential explanatory factors of improvement on the other side. The potential explanatory factors were:
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age ( 60 or < 60); cause of SCI; surgery (yes/no); the type of clinical syndrome caused by the SCI.
Three categories of clinical syndrome were considered to determine prognostic factors (BSPS, CCS and no, or other, identified syndrome) in order to have approximately similar numbers in each group. Then, in order to search for explanatory factors of functional outcome, Fisher exact tests were performed with patients with or without favourable outcomes on one side and potential explanatory factors of outcomes on the other side. Three outcomes were assessed:
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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discharge mode; ambulation mode; bladder function.
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The potential explanatory factors for functional outcomes were the same as for neurological prognosis. SPSS software was used for data analysis with the significance level set at P = 0.05.
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Q3 3. Results
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3.1. Sociodemographic data and neurological status at admission
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Sixty-three patients were included in the study. Fifty were male (79.4%). Mean age was 60.1 years (S.D. = 14.8; range = 30–88 years) Fig. 1. Falls were the main cause of trauma (49 patients, 77.8%), followed by motor vehicle crashes (7 patients, 11.1%) sports injuries (6 patients, 9.5%) and acts of violence (1 patient, 1.6%). AIS was established at admission for 60 out of the 63 patients and NLI and clinical syndrome were determined for 42 patients (see Fig. 2 for results). Associated drowsiness prevented these data being obtained in the other patients. Forty-six out of 63 patients (73%) underwent cervical spine surgery. The time between trauma and surgery ranged from 0 to 430 days (mean: 62.7 94.7 days, median: 14.5 days). Surgery was independent of age and AIS grade. All patients who were operated underwent decompressive laminectomy (posterior approach). No patients were administered corticosteroids (Figs. 1 and 2).
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3.2. Neurological status at discharge
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Three patients died in the acute care phase because of respiratory complications. Three patients were lost to follow-up because of transfer to another rehabilitation centre. Therefore, a complete neurological and functional assessment at discharge was obtained for 57 patients. The mean length of stay (time from admission to discharge) for these 57 patients was 267.7 days and the median was 140 days (range: 8–2561). The very long stay of 2561 days was due a patient with AIS A SCI at C3 for whom a care institution could not be found. Table 1 shows the change in AIS grade between admission and discharge for the 57 patients. AIS grade improved by at least one point between admission and discharge for thirty-five patients (61.4%) and remained unchanged for 22 patients (38.6%). Age, cause, surgery and clinical syndrome were not significantly associated with improvement in AIS grade. Table 2 shows the change in NLI between admission and discharge for the 42 patients who had a complete assessment at both admission and discharge.
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3.3. Functional status at discharge and prognostic factors
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Data regarding discharge mode, ambulation status at discharge and bladder function could be obtained for 57 patients. Table 3 displays the complete results for functional outcomes and associated prognostic factors (Table 3).
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Fig. 1. Flow-chart of patients included with SCI with underlying spinal canal stenosis without instability. AIS: ASIA impairment scale; NLI: neurological level of injury.
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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Fig. 2. Neurological data of the patients at admission. A: ASIA impairment scale (AIS); B: neurological level of injury. C: distribution of clinical syndromes in the 42 patents with a complete neurological examination; ACS: anterior cord syndrome; CCS: central cord syndrome; BSPS: Brown-Sequard plus syndrome.
Table 1
Q4 Change in ASIA impairment scale (AIS) grade between admission and discharge for the 57 patients with AIS scores at both time points.
Table 2 Change in neurological level of injury (NLI) between admission and discharge for the 42 patients with a complete assessment at both time points.
AIS at discharge
AIS at admission A B C D Total
NLI at discharge
A
B
C
D
E
Total
1 – – – 1
– 1 – – 1
2 3 4 – 9
– 1 19 16 36
– – 2 8 10
3 5 25 24 57
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4. Discussion
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This study reviewed all consecutive cases of acute SCI caused by trauma to the cervical spinal cord with associated spinal canal stenosis and no spinal instability, over a 12-year period. The majority of patients had incomplete lesions with AIS grades of C or D and NLI at C4 and C5. A clinical syndrome could be identified in more than 75% of cases, with BSPS and CCS being the most frequent. Overall, outcomes were positive regarding discharge mode, ambulatory status and bladder function. Age under 60 years, higher AIS grades at admission and the presence of CCS or BSPS were identified as favourable prognostic factors.
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4.1. Precise definition of the condition investigated and epidemiologic data
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The purpose of this study was to specifically investigate the initial condition, outcomes and prognostic factors of patients with acute, traumatic SCI within a stenotic cervical spinal canal, without spinal instability. This particular condition was chosen because it is clinically relevant [12,18,19]. Recent epidemiological data in the
NLI at admission C1 C3 C4 C5 C6 C7 C8 Total
C1
C3
C4
C5
C6
C7
C8
Total
– – – – – – – 0
– 2 2 2 1 – – 7
– 1 3 1 – – – 5
– 2 9 4 1 – – 16
– – 1 3 2 – – 6
– 3 – 2 1 1 – 7
– – – – – 1 – 1
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field of SCI have focused on the aging population, incomplete injuries and an increased proportion of falls as the cause of trauma [20]. Thus, there has been an increase in attention on SCS. To date, the only studies describing neurological data and outcomes of patients with SCS, included patients who underwent surgical decompression [10], or involved small samples from several SCI centres [9]. In the present study, which provided a global analysis of this clinical condition, the single-centre design allowed for a homogenous sample, which was, moreover, relatively large since the study covered a period of 12 years. The mean and median age of the patients in the present study was about 60 years. This is in line with previous studies and confirms that patients with spinal stenosis who have a SCI (age at injury about 60 years) are older than the overall SCI population (age at injury 35 to 40 years [20]). Falls were the greatest cause of trauma in the present study, representing more than 75% of cases. This rate is higher than reports in previous studies [21]. This could be due to the fact that all patients in this study had canal stenosis, making them vulnerable to SCI from minor trauma such as a fall. It
Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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Table 3 Prognostic factors of independence (discharge home with or without a carer), ambulatory status (independent walking with or without crutches) and bladder function at discharge. Predictive factor Age (n = 57) < 60 years (n = 29) 60 years (28) AIS at admission (n = 57) A (n = 3) B (n = 5) C (n = 25) D (n = 24) Surgery (n = 57) Yes (n = 43) No (n = 14) Delay of surgery (n = 43) 14 days (n = 22) 15 days (n = 21) Clinical Syndrome (n = 42) BSPS (n = 13) CCS (n = 10) Other (n = 19)
Patients discharged home [n (%)]
Fisher’s exact test
Independent walkers at discharge [n (n (%)]
P < 0.001 29 (100%) 17 (60.7%)
20 (69%) 9 (32.1%)
(33.3%) (60%) (72%) (100%)
P = 0.765
P=1
P = 0.728 33 (77.3%) 10 (71.4%)
P = 0.033 8 (36.4%) 15 (71.4%)
P = 0.507 9 (69.2%) 9 (90%) 15 (78.9%)
P < 0.001 0 1 (20%) 16 (64%) 24 (100%)
22 (51.2%) 8 (57.1%)
19 (86.4%) 19 (90.5%)
P = 0.141
P < 0.001
P=1
P = 0.6988 17 (86.4%) 18 (85.7%)
P = 0.038 3 (23.1%) 8 (80%) 8 (42.1%)
Fisher’s exact test
24 (82.3%) 18 (64.3%)
0 1 (20%) 8 (32%) 19 (79.1%)
21 (48.8%) 7 (50%)
Patients with voluntary bladder control at discharge [n (%)]
P = 0.008
P = 0.001 1 3 18 24
Fisher’s exact test
P = 0.013 10 (76.9%) 9 (90%) 3 (15.8%)
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is also likely that some patients with SCS had pre-existing cervical myelopathy, increasing their risk of falls.
SCI and the consequences (type/clinical presentation) must not be confused.
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4.2. Clinical profiles of patients
4.3. Neurological and functional outcomes and associated prognostic factors
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Not surprisingly, the majority of patients included had incomplete lesions with AIS grades C and D and the most frequent NLI were C4 and C5. All previous studies of acute SCI with SCS, starting with the pioneering study by Schneider and Cherry [3], reported mostly incomplete motor lesions, today classified as AIS C or D. The NLI has been less extensively investigated. Interestingly, the distribution of levels in the present study does not differ from the overall distribution among patients with SCI [15]. It may be that the mid-cervical spine is particularly vulnerable to injury, explaining that it is the most frequent site of SCI. Alternatively, the distribution of NLI could follow the topography of spondylosisrelated degeneration, known to be most prevalent between C3 and C6 [10]. The outstanding feature of the sample in the present study was the high rate of clinical syndromes and the fact that CCS was not the most frequent. A previous study in 839 patients with SCI found that only 20.9% had a clinical syndrome [6], while this rate reached 78.6% in the present study. Such a discrepancy could be attributed several factors. First, the syndromes included differed. The study by McKinley et al. [6], included patients with posterior cord syndrome, cauda equina syndrome and conus medullaris syndrome and the transverse syndrome was only included in the present study. Second, the definitions of CCS differed, since we used the criteria proposed recently by the EMSCI study group [4]. Finally, the present study only covered cervical SCI. Since most cervical lesions are incomplete, there is a higher probability of occurrence of a clinical syndrome than for lesions in other parts of the spine. BSPS (30.9%) was a little more frequent than CCS (23.8%) in the present sample of posttraumatic SCI with underlying SCS. In previous studies, the most frequent syndrome was found to be CCS, accounting for about 50% [6] or even 70% [9,22] of syndromes. However, as mentioned above, the diagnostic criteria for CCS used in the present study has been recently revised, possibly explaining the lower rate found here. Nonetheless, the present study reports several syndromes, not only the classical CCS, relating to SCI with underlying cervical spinal canal stenosis. This emphasizes that the cause/mechanism of the
The outcomes of the patients included were fair. The mortality rate was lower than 5%. Almost two thirds experienced an improvement of at least one grade on the AIS between admission and discharge, which is a markedly higher rate than for the general SCI population [15]. More than 80% of patients had an AIS grade of D or E at discharge. Acute CCS associated with traumatic cervical SCI is known to have a favourable prognosis overall [3,5,9]. Our data confirm that regardless of the syndrome, patients with incomplete cervical SCI associated with SCS have a high potential for improvement of AIS grade and reach the D or E grade. It is thus important to provide appropriate acute-care treatment and to determine relevant goals and rehabilitation strategies in this population. The functional outcomes were favourable. Almost 80% of survivors returned to the community, 60% could walk and 75% recovered complete voluntary control of bladder function. The prognostic factors identified for positive functional outcomes were a less severe AIS grade at admission, age under 60 and the presence of CCS or BSPS. Age and AIS at admission are well established as prognostic factors in SCI [8,9,14,15]. However, caution must be taken when considering the type of clinical syndrome as a predictive factor because BSPS and CCS are very often associated with AIS grades C or D and it could be that they stood out as prognostic factors only because they were associated with more severe AIS grades at admission. Future studies with larger samples might allow other statistical analyses that account for such confounding factors to be carried out. There was no difference in outcomes between patients who underwent surgery and those who did not. The benefits of surgery in patients with SCI and cervical SCS is a matter of debate since, as stated by Schneider et al. and Schneider and Cherry, recovery can occur spontaneously in this condition [2,3]. More recently, the meta-analysis by La Rosa et al. suggested outcomes may be improved when early decompression is performed in case of incomplete SCI. In 2010, a consensus of experts provided recommendations concerning this issue [19]. They stated that early (within 24 hours) surgery is
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Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
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indicated in patients with AIS grade C with obvious spinal compression in the absence of unstable lesions, while they recommended observation in the acute phase for patients with AIS grade D. In the present study, surgical decompression was not a prognostic factor of neurological improvement or of favourable functional outcomes. However, the time between trauma and surgery, when performed, was extremely variable (ranging from 0 to 430 days). The present results showed a higher rate of independent walking at discharge following delayed ( 15 days) than early ( 14 days) surgery. The reasons behind the decision to carry out early surgical decompression are diverse (neurological worsening, absence of neurological improvement associated with persistent spinal compression on MRI, evidence of severe spinal canal stenosis and cord oedema, extension of the pathological signal on MRI etc.) Therefore, in the present study early surgery may have been performed in a subset of patients who were not improving, which could explain why it was associated with a less favourable outcome. Uncertainty thus persists regarding the riskbenefit ratio of surgical decompression and the optimal timing for surgery. We hope the results of the recently designed COSMIC trial, comparing early surgical management to conservative treatment in incomplete cervical SCI without spinal instability will give answers to this key-issue [12]. As canal stenosis is the main pathophysiological factor in this type of SCI, we hypothesise that early decompression would improve outcomes for patients with this condition. To verify this hypothesis, we have recently begun a randomized controlled trial, comparing early (within 48 hours) vs. delayed (at 15 days posttrauma) surgery in this population.
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4.4. Limitations
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Due to the retrospective nature of this study, no strong conclusions can be made regarding the relationship between the patient’s history and clinical status and outcomes. Another limitation is that although the proportion of patients who were lost to follow-up was reasonable (approximately 10%: 6 out of 63), one third of the patients had an incomplete neurological evaluation at admission, preventing attribution of a precise NLI or AIS grade. ASIA motor and sensory scores were not included in the study because of missing data and uncertainties regarding their reporting. The statistical associations between potential explanatory factors and neurological or functional outcomes may have been affected by these missing data. Some limitations cannot be avoided, such as drowsiness that prevents precise evaluation in the acute phase, even in prospective studies. Other evaluations would be useful in this population, such as the functional independence measure. The present study focused on the outcomes that are the easiest to assess in a retrospective study. However, our team is currently joining the European Multicenter Study on Human Spinal Cord Injury (EM-SCI; www. emsci.org) and we hope that this will improve the exhaustiveness and homogeneity of follow-up for patients with SCI in the future. Moreover, the more systematic approach will help provide complete, multidimensional data with outcomes in the domains of impairments, activity limitations, participation restrictions and quality of life.
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5. Conclusion
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Traumatic SCI associated with cervical spinal canal stenosis with no spinal instability was caused by falls in 75% of cases. It resulted mostly in incomplete injuries of AIS grade C or D and NLI C4 or C5. Various syndromes occurred, with a slightly higher frequency of BSPS than CCS. Patients with this condition had overall favourable outcomes regarding bladder function, ambula-
tory capacity and independence. A less severe AIS grade at admission, age under 60 years and the presence of BSPS or CCS were associated with more positive outcomes. Further prospective studies and exhaustive data collection are essential to provide strong recommendations regarding indications and timing of decompressive surgery in these patients.
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Funding
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This study received no funding. Disclosure of interest The authors declare that they have no competing interest.
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References
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[1] Rao RD, Currier BL, Albert TJ, Bono CM, Marawar SV, Poelstra KA, et al. Degenerative cervical spondylosis: clinical syndromes, pathogenesis and management. J Bone Jt Surg 2007;89:1360–78. [2] Schneider RC, Thompson JM, Bebin J. The syndrome of acute central cervical spinal cord injury. J Neurol Neurosurg Psychiatry 1958;21:216–27. [3] Schneider R, Cherry GHP. The syndrome of acute central cervical spinal cord injury: with special reference to the mechanisms involved in hyperextension injuries of cervical spine. J Neurosurg 1954;11:546–77. [4] Middendorp JJ, Van, Pouw MH, Hayes KC, Williams R, Chhabra HS, et al. Diagnostic criteria of traumatic central cord syndrome. Part 2: a questionnaire survey among spine specialists. Spinal Cord 2010;48:657–63. [5] Aito S, Andrea MD, Werhagen L, Farsetti L, Cappelli S, Bandini B, et al. Neurological and functional outcome in traumatic central cord syndrome. Spinal Cord 2007;45:292–7. [6] Mckinley W, Santos K, Meade M, Brooke K. Incidence and outcomes of spinal cord injury clinical syndromes. J Spinal Cord Med 2007;30:215–24. [7] Roth EJ, Lawler M, Yarkony G. Traumatic central cord syndrome: clinical features and functional outcomes. Arch Phys Med Rehabil 1990;71:18–23. [8] Harrop JS, Sharan A, Ratliff J. Central cord injury: pathophysiology, management and outcomes. Spine J 2006;6:S198–206. [9] Waters RL, Adkins RH, Sie IH, Yakura JS. Motor recovery following spinal cord injury associated with cervical spondylosis: a collaborative study. Spinal Cord 1996;34:711–5. [10] Aarabi B, Alexander M, Mirvis SE, Shanmuganathan K, Chesler D, Maulucci C, et al. Predictors of outcome in acute traumatic central cord syndrome due to spinal stenosis. J Neurosurg Spine 2011;14:122–30. [11] White A, Panjabi M. The problem of clinical instability in the human spine: a systematic approach. Clin Biomech spine. Baltimore, New York: Lippincott, Philadelphia; 1990. p. 277–378. [12] Bartels RHM, Hosman AJF, van de Meent H, Hofmeijer J, Vos PE, Slooff WB, et al. Design of COSMIC: a randomized, multicentre controlled trial comparing conservative or early surgical management of incomplete cervical cord syndrome without spinal instability. BMC Musculoskelet Disord 2013;14:52. [13] Pavlov H, Torg J, Robie B, Jahre C. Cervical spinal stenosis: determination with vertebral body ratio method. Radiology 1987;164:771–5. [14] Kirshblum SC, O’Connor KC. Predicting neurologic recovery in traumatic cervical spinal cord injury. Arch Phys Med Rehabil 1998;79:1456–66. [15] Marino RJ, Ditunno JF, Donovan WH, Maynard F. Neurologic recovery after traumatic spinal cord injury: data from the model spinal cord injury systems. Arch Phys Med Rehabil 1999;80:1391–6. [16] Kirshblum SC, Burns SP, Biering-Sorensen F, Donovan W, Graves D, Jha A, et al. International standards for neurological classification of spinal cord injury (revised 2011). J Spinal Cord Med 2011;34:535–46. [17] Roth EJ, Park T, Pang T, Markony TM, Lee MY. Traumatic cervical brownsequard and brown-sequard-plus syndromes: the spectrum of presentations and outcomes. Paraplegia 1991;29:582–9. [18] La Rosa G, Conti A, Cardali S, Cacciola F, Tomasello F. Does early decompression improve neurological outcome of spinal cord injured patients? Appraisal of the literature using a meta-analytical approach. Spinal Cord 2004;42:503–12. [19] Lenehan B, Fisher C, Vaccaro A, Fehlings M, Aarabi B, Dvorak M. The urgency of surgical decompression in acute central cord injuries with spondylosis and without instability. Spine (Phila Pa 1976) 2010;1:S180–6. [20] Devivo MJ, Chen Y. Trends in new injuries, prevalent cases and aging with spinal cord injury. Arch Phys Med Rehabil 2011;92:332–8. [21] Kato H, Kimura A, Sasaki R, Kaneko N, Takeda M, Hagiwara A, et al. Cervical spinal cord injury without bony injury: a multicenter retrospective study of emergency and critical care centers in Japan. J Trauma-Injury Infect Crit Care 2008;65:373–9. [22] Lamothe G, Muller F, Vital JM, Goossens D, Barat M. Evolution of spinal cord injuries due to cervical canal stenosis without radiographic evidence of trauma (SCIWORET): a prospective study. Ann Phys Rehabil Med 2011;54:213–24.
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Please cite this article in press as: Ronzi Y, et al. Spinal cord injury associated with cervical spinal canal stenosis: Outcomes and prognostic factors (SCI with spinal canal stenosis). Ann Phys Rehabil Med (2017), http://dx.doi.org/10.1016/j.rehab.2017.09.003
