Traumatic spinal cord injury in the elderly: predictors for mortality and functional outcomes

Introduction

Background

Traumatic spinal cord injury (tSCI) is a significant cause of morbidity and mortality in Australia, with an estimated incidence of 8.6 per million population aged over 15 (1). The proportion of the population aged 65 years and older is predicted to rise from 16% in 2020 to 20% by 2066, and with an ageing population, the incidence of tSCI in the elderly is likewise increasing (2). It is forecasted that by 2032 approximately 40% of tSCIs will involve patients 60 years or older (3). Beck et al. found the incidence of tSCI in the elderly is rising even after adjusting for population increase (4). The primary insult is commonly a consequence of high-energy trauma from motor vehicle crashes in the young or low-energy falls in the elderly population (1). Pathophysiological hallmarks of this irreversible primary injury include local haemorrhage, oedema, and ischemia that progresses and initiates the secondary phase (5). Subsequent to this, secondary injury refers to the self-propagating response that causes further tissue loss and dysfunction, beginning shortly following the initial insult and lasting weeks to months (6). The mechanisms governing this process are complex, incompletely understood, and include spinal shock, vascular dysfunction, ischemia, membrane compromise, ionic dysregulation, and neurotransmitter accumulation (7). Survivors of tSCI have worse long-term mortality. Middleton et al. (8) reported in their study of tSCI in New South Wales residents from 1955–2006 that tetraplegic patients who survived the first year had double the subsequent mortality rate of the general population, with a standardized mortality rate (SMR) of 2.2, and for paraplegic survivors, an SMR of 1.6. This demographic presents a unique set of challenges to clinicians, where the benefit of intervention and hospital management is often compounded by an increased rate of medial comorbidities and frailty, and by extension increased risk of morbidity and mortality.

Rationale and knowledge gap

Preceding research has established age as a major predictor of in-hospital mortality in tSCI (4,9), and the severity of the neurological deficit as important predictors of long-term survival and functional status (8,10). However, there is a paucity in the current literature regarding the predictors for mortality and functional outcomes in elderly tSCI, and in particular in an Australian cohort. This cohort commonly presents following low-impact trauma, and their unique physiological and injury profile means their clinical courses can be unpredictable, with significant social, physical, and economic implications at play. As such, there is an urgent need to establish predictors for morbidity and mortality in this subset of patients.

Objective

We aim to present and define the clinical course of tSCI in the elderly Australian cohort (aged 65 years and over) and identify risk factors and predictors for mortality to enhance understanding and guide decision-making in this devastating and costly disease. We present this article in accordance with the STROBE reporting checklist (11) (available at https://jss.amegroups.com/article/view/10.21037/jss-24-138/rc).

Methods

A review of the prospectively maintained Victorian State Trauma Registry (12) (VSTR) database was performed to identify patients who sustained a tSCI between 2007 and 2021 and were managed at the Victorian Spinal Cord Injury Service at Austin Health, the bi-state referral centre for tSCI. The population-based VSTR collects data for all patients hospitalised in Victoria who meet any of the following criteria: (I) death after injury; (II) all patients admitted to an intensive care unit or high-dependency area for more than 24 hours or mechanically ventilated after admission; (III) an Injury Severity Score (ISS) greater than 12 [calculated with the Abbreviated Injury Scale (AIS) 2005 (13)]; and (IV) urgent surgery for intracranial, intrathoracic or intraabdominal injury, or fixation of pelvic or spinal fractures. Ethical approval for this process was approved by the Victorian State Trauma Outcomes Registry and Monitoring Group (VSTORM) (12). The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Austin Health Human Research Ethics Committee (No. EC00204; approval No. 89769) and deemed exempt from requiring informed consent from participants due to the retrospective nature of the study.

Definitions and data collection

We defined the elderly as any patient aged 65 years and over. tSCI was defined as an injury to the spinal cord with an AIS score of 4 or more, ensuring complete population coverage (given the VSTR inclusion criterion of an ISS exceeding 12). Cases of cauda equina and nerve root injury were excluded. Consistent with AIS codes, tSCIs were classified as complete or incomplete injuries in the cervical (subclassified: C3 or above, C4 or below), thoracic, or lumbar spine. AIS coding data was supplemented with information regarding the neurological level of the injury and the type of incomplete cervical tSCI (central cord syndrome, or other incomplete cervical injury) derived from the International Classification of Diseases, tenth revision Australian modification (ICD-10-AM) coding (14). Isolated tSCI was defined as the absence of injuries with an AIS score greater than one in any other body region. Demographic and treatment data were all extracted from the database, with incomplete data obtained from patient medical records where available. Patients were excluded if 6-month follow-up data was unavailable or incomplete within the database. Exposure variables of interest collected included age and sex, ISS, whether spinal surgery was performed, Charlson Comorbidity Index (CCI) (15), neurological level of injury, completeness of neurological injury, intensive care admission, and mechanical ventilation.

Outcome assessment

A primary outcome of death at 6 months was defined. Secondary outcomes were collated for Extended Glasgow Outcome Score (GOS-E) (16) at 6 months to determine functional status, length of stay in hospital which confers economic implications, and discharge disposition.

Statistical analysis

All statistical analyses were performed using Stata version 14.2 (17). Complete case analysis was performed in preference over multiple imputations to handle missing data in line with research methodology guidelines (18). A full model approach to multivariate analysis was used as all predictors were considered clinically important factors. To assess the primary outcome of death at 6 months, a multivariate logistic regression model was performed with the binary outcome being whether the patient was deceased at the 6-month follow-up. This was repeated with age categorized as less than or greater than 75 to establish a threshold age effect. A multivariate ordinal logistic regression was performed with the GOS-E; a likelihood ratio test of proportionality of odds was conducted and rejected (P=0.12). A logistic regression was performed to assess whether a patient resided at home (with or without support) at 6 months. To assess the length of stay as an outcome, a Poisson regression was conducted with a robust variance estimator.

Results

Patient characteristics

Of 171 patients within the registry, a total of 169 elderly patients with tSCI were eligible for analysis, and 168 had sufficient follow-up at 6 months. Those ineligible for analysis had insufficient demographic information or did not meet inclusion criteria. The mean age was 73.5 years [standard deviation (SD) 6.6] and the median age was 72 years with a range from 65 to 94. Demographic and treatment data is summarised in Tables 1-6. Of the 162 patients with a determinable CCI, 46.2% (n=78) of patients had a CCI of 0, 31.4% (n=53) with 1, and 22.4% (n=34) with 2 or greater. Most injuries were subaxial involving C4 and caudal (n=81, 47.9%). Furthermore, 26.6% were classified as complete (Table 2). The overwhelming majority of injuries (75.4%) were secondary to low-velocity falls, with 52.7% from a height of less than 1 m and 23.1% from more than 1 m. The median ISS was 25 with a range from 16 to 75. The mean length of stay was 41.9 days and the median was 25.8 days. Of this cohort, 35.5% (n=60) received ventilation whilst an inpatient, with the median ventilation time being 91 days for those who received ventilation, and 78.3% (n=47) of such patients remaining ventilated upon discharge from acute care. It was found that 50.3% (n=85) required intensive care admission, and 67.5% (n=114) underwent a spinal operation, including those received before transfer from a referring hospital.

Outcomes

Primary outcome

At 6 months, 19.6% (n=33) of patients were dead, whether from spinal cord injury or otherwise. Twenty-two patients passed away in hospital or following transfer to a palliative care unit and out of these, 17 had adequate documentation to determine the cause of death. Eight patients (47%) died from respiratory failure or pneumonia, 2 (11.8%) from sepsis, 1 (5.9%) from congestive cardiac failure, and 1 (5.9%) from vertebral artery dissection. Of five patients who had medical care withdrawn, 5 (29.4%) were due to irreversible medical deterioration or injuries deemed nonsurvivable at the time of diagnosis, and 2 (11.8%) were cervical tSCI patients palliated on the patient’s wishes. On multivariate logistic regression (Table 7), the likelihood of death at 6 months was significantly associated with increasing age [odds ratio (OR) 1.22 per year increase in age; 95% confidence interval (CI): 1.09–1.36; P=0.001], ISS (OR 1.11 per unit ISS; 95% CI: 1.05–1.18; P=0.001), and complete spinal cord injury (OR 7.96 compared with incomplete; 95% CI: 1.61–39.4; P=0.01). The first logistic regression model achieved a pseudo-R squared of 0.382. Other variables assessed including the neurological level of injury, having a spinal operation, intensive care admission, ventilation, and CCI of 1 or greater did not reach significance in association with death at 6 months. However, lower cervical and thoracic spinal cord injuries demonstrated a lower OR in comparison to high cervical injuries. A second logistic regression performed with age dichotomized as less than 75 and 75 years or older was performed with the otherwise same factors in the previous model. Death at 6 months was similarly significantly associated with the 75 years or older group, with OR 6.4 (95% CI: 1.68–24.8; P=0.007).

Secondary outcomes

Extended Glasgow Outcome Scale

In an ordinal logistic regression analysis (Table 8), increasing age (OR 0.938; 95% CI: 0.883–0.998), ISS (OR 0.927; 95% CI: 0.892–0.964), and complete spinal cord injury (OR 0.357; 95% CI: 0.134–0.951) were associated with poorer Glasgow outcome scale extended scores at the 6-month mark. The neurological level of injury, a spinal operation, sex, intensive care admission, increasing CCI, and ventilation were not significantly associated with worsening scores.

Residence at 6 months

In a multivariate logistic regression (Table 9), the probability of patients being at home (with or without additional care) at the 6-month follow-up was significantly negatively associated with increasing age (OR 0.924 per year of age; 95% CI: 0.861–0.992), ISS (OR 0.937; 95% CI: 0.882–0.995), and a CCI of 1 or greater (OR 0.394; 95% CI: 0.178–0.873). Other factors including the level or completeness of spinal cord injury, operation, intensive care admission and ventilation did not reach significance.

Length of stay

In a multivariate Poisson regression (Table 10), a spinal operation (coefficient 0.461, P=0.03) and mechanical ventilation (coefficient 0.487, P=0.03) were significantly associated with increasing length of stay. Other factors such as age, sex, ISS, level of injury or completeness of injury did not reach significance in length of stay.

Discussion

Key findings

tSCIs are potentially devastating neurological injuries that have an incidence of up to 40–80 cases per million population (19). Clinical consequences range from minor injuries appropriate for conservative management to severe neurological sequelae which significantly affect the functional independence of already frail elderly patients (4,5). As highlighted earlier, a study has shown in comparison to the general population that tetraplegic patients suffer from long term mortality rates even after 1 year from the injury (8). Our study provides timely novel evidence regarding negative prognostic factors after sustaining a tSCI.

At present, clinicians are reliant on outdated data such as that by O’Connor who determined there was some prolongation in the 2-month and 1-year survival rates (36% and 27% respectively) of Australian spinal cord injury patients between 1986–1991 and 1992–1997 (20). However, the mortality rate 2 years after the initial injury has not improved over this time (21). The most common causes of death were pneumonia and ischaemic heart disease (22). Our original findings demonstrated that age and ISS at 6 months predict mortality, poorer functional outcome (GOS-E), and reduced chance of returning home. Spinal operations and mechanical ventilation independently predicted increased length of stay but did not affect mortality at 6 months, functional outcomes, nor the likelihood of residing at home at 6 months. While not reaching significance, lower cervical injuries demonstrated a pattern of improved survival and functional status at 6 months over high cervical injuries. Thoracic injuries tended towards comparatively worse outcomes; this may be due to a greater relative proportion of complete spinal cord injuries at the thoracic level. This data enables clinicians to adequately counsel both patients and families as to the expected functional and mortality outcomes.

Historically, the threshold age for which studies define an older age group with worse functional and neurological outcomes has been 65 years of age (23-25). This is consistent with the United Nations’ definition of an elderly patient. When our population was dichotomized into those aged between 65 and 74 years of age or 75 years and older, we observed a large parity in mortality rates at 6 months. This is striking and is consistent with a more contemporary understanding of frailty rather than age being a decisive factor. Indeed, it is important to recognise that frailty, a state of decreased physiological reserve, is a more important and accurate measurement of a patient’s robustness and fitness for surgery than age alone (26-32).

Comparison with similar research

It is well known that increasing age in tSCI is associated with poorer functional recovery (33,34), institutionalization (35), and mortality (4,9,36). Furlan et al. conducted a randomized controlled trial and found greater mortality in individuals aged over 65 years compared to their younger counterparts at 6 weeks, 6 months, and 1 year, but no difference in their motor and sensory outcomes (37). Kawu et al. similarly found age as well as a Glasgow coma scale of less than 9, cervical spine injury, complete neurological injury and Frankel type A injury to be predictors for death at 6 months (36). Similarly, Inglis et al. found in their cohort study of patients aged 65 and over with tSCI that age, comorbidities, neurological injury severity, and ventilation status to be predictors for in-hospital mortality following surgery (38). When age in this group was dichotomized similarly to in our study with a threshold age of 77 years, the odds of death 50 days post-surgery was 6 times that of the younger group (38), and complete neurological injury had a 5 times greater odds of death at 50 days. With respect to functional outcomes, Ariji et al. found age, strength in some key muscles, and two mobility assessments to be predictors for the spinal cord independence measure total score (SCIM-TS) at 6 months (34). Wichmann et al. determined increased age, body mass index (BMI), comorbidity, low American Spinal Injury Association (ASIA) motor score, poor AIS, and late surgical treatment to predict decreased functional independence based on the Spinal Cord Independence Measure III (SCIM-III) 1 year after injury (39). Additionally, Keusen et al. found that age in the spinal cord injury patient predicted inpatient nursing care, independence at discharge, and institutionalization (35).

Explanations of findings

This study further defines and quantifies the constellation of factors that govern the short-term functional outcomes and mortality rates of older adults with tSCI, and its implications concern the elderly in Australia as well as on a global scale. These findings may assist clinicians in three phases. Our data assists in identifying patients who are likely to have poorer outcomes and in counselling patients particularly regarding functional outcomes, given that a patient’s perceived quality of life is heavily influenced by institutionalization (40) and physical independence (41). Careful assessment and optimal treatment of concurrent injuries are crucial.

Implications and actions needed

Our finding that the greatest predictors for poor functional outcomes are unfortunately non-modifiable implies that on a public health scale, prevention is likely the most effective method of reducing the devastating morbidity of this disease. Our findings demonstrate it is imperative to implement strategies to reduce the incidence of trauma in older adults, particularly mechanical falls which dominate the mechanism of injury in this demographic. Our findings provide short-term survival information for elderly tSCI patients. 19.6% of this cohort passed away within 6 months of the initial injury. In comparison, the historical all-cause mortality rate within a 6-month period for Australians aged 65 years and older was 7.7% [based on the annual mortality rate and assuming a constant mortality rate throughout the year (42)]. Clinicians should recognize those aged 75 years and older as a distinct cohort even amongst the 65 years and older age group given their sixfold greater risk of mortality.

Advancing this knowledge, a validated perioperative risk stratification tool as a representation of frailty beyond age alone must be developed in this population given the average life expectancy in Australia is rising with 75% of those over 65 years of age denying any significant medical comorbidities (43). The modified frailty index in its 11-item and 5-item iterations has been validated in the spinal surgery population and specifically the ultra-elderly population as well. Similarly, the CCI has an association with mortality (15). Moreover, we determined that a higher injury score independently correlated with a lower GOS-E.

Future randomized multi-centre international studies would be beneficial to further delineate exact risk factors and predict morbidity and mortality more accurately. New outcome measures such as the revised Catz-Itzkovich Spinal Cord Independence Measure (SCIM), may be a suitable specific score for independence (44) for future studies. Furthermore, clinicians could also consider risk stratification of patients using perioperative instruments such as the modified frailty index (45). Longer-term follow-up of patients would also be beneficial. Although the majority of motor recovery occurs within the first 3 months, ongoing motor and functional recovery reportedly occurs then plateaus 12–18 months post-injury (46). Indeed, Khorasanizadeh et al. (47) found that studies that examined neurological recovery at 6 months reported a significantly lower neurological recovery rate than long-term (3–5 years) follow-up compared with 12 months, suggesting 12 months to be the minimum time to allow for adequate recovery to be represented. It may therefore be reasonable to allow similar periods for functional recovery and larger studies would benefit from longer follow-up.

Strengths and limitations

There are a number of limitations to this study. In particular, the potential for incomplete data and selection bias in a retrospective review is well recognised. The rate of non-operatively managed patients was higher than anticipated, with age as the main predictor. Specifically, 77.6% of patients under 75 years received an operation, whereas only 50% of patients 75 years or older received an operation, which confers a degree of selection bias in consideration of operative candidates. Furthermore, we were reliant on the depth of data contained within the VSTR database, with in particular tSCI lacking American Spinal Injury Association Impairment Scale (AIS) grading and severity only recorded as complete or incomplete, limiting the depth of the analysis. The database also lacked a typical outcome measure for SCI such as the Functional Independence Measure (FIM), or Spinal Cord Independence Measure (48). We were therefore reliant on GOS-E as a functional outcome measure, which although typically used for traumatic brain injury, also confers important information on functional status and independence which is undoubtedly relevant to the tSCI elderly cohort.

Conclusions

We determined that age, ISS and severity of spinal cord injury are associated with increased morbidity and mortality. In particular, the elderly aged 75 years and older sustained significantly worse outcomes compared to younger patients. Larger prospective randomized multi-centre randomized controlled studies are required to clarify our results which suggest that lower cervical injuries have better outcomes than high cervical injuries, and to identify modifiable risk factors to improve outcomes for patients who sustain devastating traumatic spinal cord injuries.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jss.amegroups.com/article/view/10.21037/jss-24-138/rc

Data Sharing Statement: Available at https://jss.amegroups.com/article/view/10.21037/jss-24-138/dss

Peer Review File: Available at https://jss.amegroups.com/article/view/10.21037/jss-24-138/prf

Funding: None.

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jss.amegroups.com/article/view/10.21037/jss-24-138/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. This study was approved by the Austin Health Human Research Ethics Committee (No. EC00204; approval No. 89769) and deemed exempt from requiring informed consent from participants due to the retrospective nature of the study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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