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https://doi.org/10.1007/s00701-020-04701-2
Abstract
Background Traumatic spinal cord injuries (TSCI) are associated with uncertainty regarding the prognosis of func-
tional recovery. The aim of the present study was to evaluate the potential of early clinical variables to predict the
degree of functional independence assessed by Spinal Cord Independence Measure III (SCIM-III) up to 1 year after
injury.
Methods Prospectively collected data from 143 SCI patients treated in Western Denmark during 2012–2019 were retrospectively
analysed. Data analysis involved univariate methods and multivariable linear regression modelling total SCIM-III scores against
age, gender, body mass index (BMI), comorbidity, American Spinal Injury Association (ASIA) Impairment Scale (AIS) grades
A–B and C–D, ASIA Motor Score (AMS), timing of surgical treatment and occurrence of medical complications. Statistical
significance was set at p < .05.
Results Univariate analyses indicated that variables significantly associated with decreased functional independence included
increased age (p = .023), increased BMI (p = .012), pre-existing comorbidity (p = .001), AIS grades A–B (p < .001), decreased
AMS (p < .001) and occurrence of medical complications (p < .001). However, in the multivariable regression model were pre-
existing comorbidity (p = .010), AIS grades A–B (p < .001), low AMS (p < .001) and late surgical treatment (p = .018) significant
predictors of decreased functional independence 1 year after injury.
Conclusion TSCI patients with greatest potential for functional recovery up to 1 year after injury seem to be patients that
immediately after trauma present with few or no comorbidities, who sustain motor-incomplete injuries and undergo early
decompressive surgery.
Coef Coefficient rehabilitation process, e.g. body mass index (BMI), burden of
ISNCSCI International Standards for Neurological pre-existing comorbidities, timing of surgical treatment and
Classification of Spinal Cord Injury occurrence of medical complications during the acute hospi-
IQR Interquartile range talization [18, 19, 30]. In order to address this knowledge gap,
R2 Adjusted R-square the objective of the present study was to evaluate the potential
SCIM-III Spinal Cord Independence Measure III of early clinical variables to predict total SCIM-III score up to
TSCI Traumatic spinal cord injury 1 year following TSCI.
24 h, and neurological evaluation performed in accordance Table 2 Description of outcomes and predictor variables
with ISNCSCI. The neurological evaluation covered AIS, Description
AMS and ALT. AIS was defined as grade A (no sensory or
motor function preserved in the sacral segments), grade B Outcome variables
(sensory function preserved, but no motor function preserved SCIM-III Continuous 0–100
below the neurological level), grade C (motor function pre- Predictor variables
served in less than half of key muscles below the neurological Age Continuous Years
level having a muscle grade ≥ 3) and grade D (motor function Gender Binary Male
preserved in at least half (or more) of key muscles below the Female
neurological level having a muscle grade ≥ 3). AIS was BMI Continuous kg/m2
grouped into motor-complete (AIS grades A–B) and motor- Pre-existing comorbidity Binary Yes
incomplete (AIS grades C–D); AMS was defined as a total No
score between 0 and 100 assessing ten key muscles bilaterally, AIS grade Binary Motor complete
ranging from paralysis (0) to active movement against full Motor incomplete
resistance (5); ALT was defined as a total score of 112 ASIA Motor Score Continuous 0–100
assessing 28 dermatomes bilaterally as absent, altered or nor- Timing of surgical treatment Binary ≤24 h
mal. Acute care hospitalization–related information included >24 h
days of hospitalization and occurrence of medical complica- Medical complications Binary Yes
tions (pneumonia, urinary tract infection and pressure ulcer). No
Inpatient rehabilitation information included SCIM-III regis-
tered approximately 12 months after injury. Supported by the ASIA, American Spinal Injury Association; AIS, American Spinal Injury
literature, 6-month follow-up SCIM-III scores were used, if Association Impairment Scale; BMI, body mass index; SCIM-III, Spinal
Cord Independent Measure III
the 12-month follow-up SCIM-III scores were unavailable [6,
27]. The SCIM-III score comprised three scales: self-care (6
items with a total sub-score of 0–20), respiration and sphincter timing of surgical treatment and occurrence of medical com-
management (4 items with a total sub-score of 0–40), mobility plications (Table 2). The associations were expressed as coef-
and transfers (9 items with a total sub-score of 0–40). The sum ficients, 95% confidence intervals (CI) and p values. The ad-
of all sub-scores generates a total SCIM-III score ranging from justed R-squared (R2) value was used to evaluate the regres-
0 to 100, reflecting complete dependence and complete inde- sion model’s goodness-of-fit. Lack of fit was indicated by
pendence, respectively. p > .05. Stata/IC 16.0 (StataCorp LP, College Station, TX)
was used for all statistical tests and results were considered
Statistical analyses statistically significant at p < .05.
Table 3 Descriptive statistics of the study population (n = 9), treatment of concomitant traumatic injuries (n = 4) or
Gender, n (%) medical conditions (n = 4), or organizational problems (n = 2).
Male 112 (78%) The causes were unknown in three cases. During acute care
Female 31 (22%)
hospitalization, medical complications occurred in 67 (47%)
Age in years, median (IQR) 56 (32–67)
patients with highest incidence of urinary tract infections
BMI in kg/m2, median (IQR) 24 (22–27)
(34%). The median length of acute care hospitalization was
21 days (range 3–163 days) until admission to inpatient reha-
Smoking status, n (%)
bilitation. A SCIM-III score was available at 12 months post-
Non-smoker 97 (68%)
injury for 80 (56%) patients and at 6 months post-injury for 63
Smoker 46 (32%)
(44%) patients. When comparing these two groups of patients,
Pre-existing comorbidity, n (%)
there was no significant difference in any of the studied char-
Cardiovascular disease 36 (25%)
acteristics, despite a significantly higher occurrence of pres-
Respiratory disease 12 (8%)
sure ulcer in patients with 12-month follow-up (p = .047). The
Diabetes mellitus 9 (6%)
median total SCIM-III score was 65 (35–93).
Neoplastic disease 2 (1%)
Mechanism of injury, n (%)
Predictors of the degree of functional independence
Transport 62 (43%)
Fall 59 (41%)
Univariate analyses indicated that increased age (p = .023),
Other 11 (8%)
increased BMI (p = .012), pre-existing comorbidity
Sport 10 (7%)
(p = .001), AIS grades A–B (p < .001), decreased AMS
Assault 1 (1%) (p < .001) and occurrence of medical complications
Energy of injury, n (%) (p < .001) were significantly associated with decreased func-
High velocity 116 (81%) tional independence.
Low velocity 27 (19%) Multivariable linear regression was based on patients who
Bony level of injury, n (%) underwent surgical treatment. As data on BMI were missing
Cervical 98 (68%) from four patients, the regression model was based on 129
Thoracic 38 (27%) patients. Four variables were significantly associated with to-
Lumbar 7 (5%) tal SCIM-III score: presence of pre-existing comorbidity
Neurological level of injury, n (%) (p = .010), AIS grades A–B (p < .001), low AMS score
Tetraplegia 99 (69%) (p < .001) and surgical treatment > 24 h post-injury
Paraplegia 44 (31%) (p = .034). Neither age (p = .059), gender (p = .181), BMI
ASIA Impairment Scale grade, n (%) (p = .890) nor occurrence of medical complications
AIS A 55 (38%) (p = .292) was a significant predictor (Table 4). The adjusted
AIS B 16 (11%) R2 of .696 indicated an overall fit of the linear regression
AIS C 37 (26%) model (p < .001), thereby confirming the model fit.
AIS D 35 (25%)
ASIA Motor Score, median (IQR) 49 (20–65)
ASIA Light Touch Sensory Score, median (IQR) 64 (41–94) Discussion
Treatment strategy, n (%)
Surgical treatment 133 (93%) Results from our study indicate that pre-existing comorbidity,
Conservative treatment 10 (7%) AIS grades A–B, low AMS and surgical treatment > 24 h after
Medical complications, n (%)a injury during acute care hospitalization significantly predict
Urinary tract infection 49 (34%) decreased functional independence. These findings broadly
Pneumonia 25 (17%) confirm earlier results [4, 26].
Pressure ulcer 15 (10%) Identification of predictors of functional outcome has in-
Length of acute care hospitalization in days, median (IQR) 21 (13–43) creasingly gained interest given the uncertainty regarding
functional recovery. When predicting outcome by clinical var-
ASIA, American Spinal Injury Association; AIS, American Spinal Injury iables, the variables of interest should reflect the acute care
Association Impairment Scale; BMI, body mass index
a
hospitalization, as important decision-making regarding treat-
Complications in total
ment is made during this period. Furthermore, patients and
their relatives request information on what to expect of recov-
between hospitals (n = 11), indication for conservative treat- ery. The SCIM-III score is recommended as the primary out-
ment initially or indication for subacute surgical treatment come measure as it covers the most important aspects of
Acta Neurochir
ASIA, American Spinal Injury Association; AIS, American Spinal Injury Association Impairment Scale; BMI,
body mass index; CI, confidence intervals; Coef, coefficients
*Statistical significance at p < .05
functional recovery, which is the ability to reengage into Our results indicate that presence of pre-existing comorbid-
ADLs independently. Yet, only few studies evaluate function- ity significantly predicts functional recovery. We included
al outcome using the total SCIM-III score [4, 12, 20, 24]. cardiovascular, respiratory and neoplastic diseases and diabe-
However, these studies are based on small sample sizes, rang- tes mellitus, thus some of the most common comorbidities. It
ing from 70 to 88 patients [26]. The preponderance of studies seems reasonable to believe that a higher burden of comorbid-
evaluates functional outcome by FIM, thereby hampering the ities increases the risk of medical complications and prolongs
cross-comparisons between studies [26, 34]. the length of hospitalization, thereby causing a delay in the
We therefore fitted a multivariable regression model based rehabilitation process. This may explain why comorbidity
on 129 patients in order to evaluate predictors of the degree of serves as a predictor of decreased functional outcomes [26].
functional recovery. Our model demonstrated pre-existing co- Additionally, it seems intuitive that older age is correlated
morbidity, AIS grade, AMS and timing of surgical treatment with lower functional outcome as older age is associated with
as significant predictors of functional recovery. Neither age, a higher burden of comorbidities. Earlier studies indicate that
gender, BMI nor occurrence of medical complications was a adolescents have significantly higher total SCIM-III scores
significant predictor. A prior study, however, supports the compared to adults, thereby reflecting a higher degree of func-
finding that AIS grade and AMS are significant predictors of tional independence among adolescents [10]. However, the
total SCIM-III score 1 year after injury [20]. Contrary to our influence of age on functional outcome is debated [10, 20]
study, they included ALT and suggest ALT as the strongest and we did not find age to be a significant predictor in any
outcome predictor. Furthermore, they argue that ALT pro- of our models. This may be attributed to the low frequency of
vides a better understanding of injury severity compared to adolescents in our study population, or the low frequency of
AMS [20]. We argue that AMS provides a better understand- AIS grades B and C as the effect of age increases with injury
ing of recovery as motor function recovery is pivotal for severity [33].
regaining functional independence. As AMS does not consid- Consensus exists regarding the beneficial effect of decom-
er sacral neurological function and sensory function, AIS pressive surgery on functional outcome. Currently, the timing
could provide an even better understanding of functional re- of surgical treatment remains controversial, although evidence
covery compared to AMS. supports early surgical treatment. Studies generally use AIS
Acta Neurochir
grade conversion as a primary outcome measure applying statistically significant predictor of decreased functional out-
different cut-off values of surgical timing, e.g. 6, 8, 12, 24, come [4, 16]. Nonetheless, our results did not find a signifi-
48 or 72 h [8, 12, 14]. A cut-off value of 24 h does, however, cant association between continuous BMI and functional out-
seem most feasible from a clinical perspective. Prior studies come in any of the regression models. These results may re-
have shown a beneficial effect of surgical treatment when flect a low frequency of obesity and overweight in our study
performed within the first 24 h [8, 12, 14, 35]. Supporting population.
these studies, our results indicate that patients who undergo Due to the retrospective study design, some limita-
surgery within the first 24 h obtain a significantly higher de- tions must be addressed. It is, however, important to
gree of functional independence compared to patients under- emphasize that all variables were collected prospectively.
going surgery later than 24 h from injury. Surprisingly, the First, the difference in follow-up time may be a limita-
timing of surgery was not significant in the univariate analy- tion, although our comparison analysis showed no signif-
sis. This finding is in accordance with a previous report and is icant difference between groups, despite a higher fre-
probably a result of variable interaction; e.g. the timing of quency of pressure ulcers in patients with 12-month fol-
surgery may be influenced by age and pre-existing comorbid- low-up. Therefore, it seems unlikely that this difference
ities [20]. As elderly patients often have multiple pre-existing had influenced the results of our study. Second, patients
comorbidities, and thereby a higher risk of morbidity and with missing baseline ASIA scores and follow-up SCIM-
mortality, surgeons may be more likely to offer early surgical III scores were excluded. These were patients with per-
treatment to younger patients with few or no pre-existing co- manent address in other regions or countries, patients
morbidities. Still, early surgical treatment should be who had died during the first year after injury and pa-
proceeded if feasible and if the anticipated benefits of surgery tients without neurological deficits necessitating rehabil-
exceed the risks of surgery. itation. None of these patients was admitted to inpatient
In our study population, the causes of surgery later than rehabilitation and evaluated by SCIM-III. Both institu-
24 h from injury were primarily delayed diagnosis, transfer tions involved in this study went from paper medical
between hospitals and indication for conservative treatment or records to electronic medical records during the early
subacute surgical treatment. This emphasizes the need for study period, and ASIA scores and SCIM-III scores were
strategies to determine the likelihood of TSCI in the pre- lost during the period of transition. Third, our study is
hospital setting, so TSCI-directed treatment can be initiated based on patients eligible for inpatient rehabilitation from
immediately, and patients can be transferred to the TSCI- a single institution. This may limit our findings’ gener-
treating hospital without delays. These strategies would be alizability to the total TSCI population. Fourth, other
valuable in TSCI patients presenting with vague symptoms potential predictors of functional recovery exist, e.g. du-
or unknown trauma mechanism. ration of surgery, amount of blood loss, length of hospi-
Individuals having sustained a TSCI are highly susceptible talization (acute care hospitalization, intensive care unit
to infections, particularly pneumonia and urinary tract infec- and inpatient rehabilitation), necessity of intubation and
tions, and likely to develop pressure ulcers. These complica- mechanical ventilation. Despite the importance of these
tions may delay or deteriorate the rehabilitation process and potential predictors, investigation of their predictive val-
thereby decrease functional recovery [19]. The incidence of ue is beyond the scope of this manuscript.
medical complications during the acute care hospitalization
was 47%. Earlier studies report higher incidences [3, 4].
Although we did not find a statistically significant association
between SCIM-III and occurrence of medical complications
Conclusion
in our model, recent studies provide evidence that early oc-
Our results indicate that by evaluating the clinical status and
currence of complications impacts functional outcome nega-
the timing of surgical treatment during acute care hospitaliza-
tively [18, 19]. The relatively narrow spectrum of medical
tion, the clinicians are able to more precisely identify patients
complications may explain why our results were non-signifi-
with greatest recovery potential up to 1 year after injury. These
cant. Considering the different results and the preventable
are patients with few or no comorbidities, motor-incomplete
nature of these complications, early identification and treat-
patients and patients undergoing early decompressive surgery.
ment should be proceeded. Obesity and overweight can re-
duce mobility and leave patients more susceptible to medical
complications. Prior studies have evaluated the influence of Compliance with ethical standards
obesity and overweight on functional outcome reaching a con-
Conflict of interest The authors declare that they have no conflict of
sensus [4, 16, 23, 29, 32]. Studies have employed BMI as a interest.
continuous and dichotomous variable with different cut-off
values. Increased BMI has been demonstrated to be a Ethical approval For this type of study, formal consent is not required.
Acta Neurochir
differences in outcome after traumatic spinal cord injury: analysis spinal cord injury: the results of a prospective Canadian cohort
of a combined, multicenter dataset. Spine J 14(7):1192–1198 study. Spinal Cord 50(11):840–843
34. Wilson JR, Grossman RG, Frankowski RF et al (2012) A clinical 36. Witiw CD, Fehlings MG (2015) Acute spinal cord injury. J Spinal
prediction model for long-term functional outcome after traumatic Discord Tech 28(6):202–210
spinal cord injury based on acute clinical and imaging factors. J
Neurotrauma 29(13):2263–2271
Publisher’s note Springer Nature remains neutral with regard to jurisdic-
35. Wilson JR, Singh A, Craven C, Verrier MC, Drew B, Ahn H, Ford
tional claims in published maps and institutional affiliations.
M, Fehlings MG (2012) Early versus late surgery for traumatic