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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 5  |  Issue : 1  |  Page : 27-32

Exploring the value of neuro-oncological rehabilitation within a neurorehabilitation setting


1 Department of Neurorehabilitation, PDRU, Queen Elizabeth University Hospital, Glasgow, United Kingdom
2 Department of Neurorehabilitation, Astley Ainslie Hospital, Edinburgh, United Kingdom

Date of Submission03-Nov-2021
Date of Decision12-Dec-2021
Date of Acceptance13-Dec-2021
Date of Web Publication29-Jan-2022

Correspondence Address:
Dr. Teng Cheng Khoo
PDRU, Queen Elizabeth University Hospital, 1345 Govan Road, Glasgow G51 4TF
United Kingdom
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jisprm.JISPRM-000152

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  Abstract 


Background: Cancer rehabilitation is gaining recognition in response to treatment advances, with more survivors living with functional impairments. This study aims to describe the outcomes from neuro-oncological rehabilitation within an inpatient neurorehabilitation setting, focusing on patients with malignancy. Subjects and Methods: A review of neuro-oncological admissions from 2009 to 2017 was performed comparing length of stay (LOS), changes in United Kingdom Functional Independence Measure + Functional Assessment Measure (UK FIM + FAM) scores, discharge outcome, and survival between patients with benign and malignant diagnoses. Results: One hundred and twenty patients were included (40% with malignancy). Eighteen percent required transfer back to acute setting due to cancer- or treatment-related complications. Having malignancy was associated with a higher rate of acute transfer (34% vs. 7%, x2 = 13.8, P < 0.01). LOS was not significantly different between the two groups (median difference: 5 days, 95% confidence interval [CI]: −8–18, P = 0.187). While UK FIM + FAM change was significantly lower in the malignant group, the corresponding lower UK FIM + FAM efficiency was not (mean difference: 16, 95% CI: 1–31, P = 0.043 and 0.18, −0.42–0.05, P = 0.114, respectively). The median survival in the malignant group was 3.2 months (95% CI: 2.0–8.4), with survival up to 40.4 months. Conclusion: While patient outcomes with benign and malignant diagnoses were similar, the UK FIM + FAM does not capture the full benefit of rehabilitation. Given that patients with malignancy have limited survival, quality of life measures and goal attainment scaling may be more appropriate. Effective and efficient inpatient neuro-oncological rehabilitation in malignancy is deliverable, but collaboration with both oncology and palliative care services is crucial.

Keywords: Cancer, functional outcomes, neuro-oncology, rehabilitation, United Kingdom Functional Independence Measure + Functional Assessment Measure


How to cite this article:
Khoo TC, FitzGerald A. Exploring the value of neuro-oncological rehabilitation within a neurorehabilitation setting. J Int Soc Phys Rehabil Med 2022;5:27-32

How to cite this URL:
Khoo TC, FitzGerald A. Exploring the value of neuro-oncological rehabilitation within a neurorehabilitation setting. J Int Soc Phys Rehabil Med [serial online] 2022 [cited 2022 May 22];5:27-32. Available from: https://www.jisprm.org/text.asp?2022/5/1/27/336879




  Introduction Top


Recognition of the benefit of cancer rehabilitation is increasing as improved survival associated with treatment advances leads to increased prevalence of survivors with neurological or functional impairments. Traditionally low referral rates to rehabilitation services from oncology have increased in response to recognized benefit, even in patients with malignant brain tumors.[1],[2],[3] Cancer rehabilitation provision remains variable both inter- and intranationally.[4],[5],[6],[7] This can be due to a number of factors, including health-care funding structures, rehabilitation service provider perceptions about cancer prognosis or their ability to manage metastatic or chemotherapy-related complications, or limited awareness among cancer service providers about potential benefit of rehabilitation.[5],[8],[9]

Defining cancer rehabilitation is compromised by the diversity of rehabilitation needs specific to cancer histology, site, paraneoplastic manifestations, and/or treatment complications that triggered the rehabilitation need. A Canadian consensus statement highlights the need to clearly define what cancer rehabilitation is and to develop personalized interventions tailored to the individual patient.[10]

Macmillan Cancer Support (United Kingdom [UK]) commissioned guidance on prehabilitation in the cancer care pathway based on review of current evidence, although none included patients with neurological cancer or neurological complications.[11] Systemic review suggests that positive physical outcomes arise when prehabilitation is combined with rehabilitation,[12] and that inpatient cancer rehabilitation is generally effective although evidence for the latter is based on heterogenous samples.[13],[14],[15],[16] Evidence relating to neurological rehabilitation related to an oncological diagnosis, especially in malignancy, is less well established.[17],[18],[19],[20] A particular challenge of an inpatient rehabilitation admission for patients with malignancy is in balancing the enhancement of the remaining quality of life (QoL) through goal-oriented rehabilitation, and the reduction of the remaining time to spend with loved ones at home or the distraction from the preparation for end of life.

We describe our experience as an inpatient specialist neurorehabilitation unit serving a catchment of 1,000,000 patients in the South-East of Scotland in rehabilitating patients with neurological impairment arising from primary neurological or nonneurological cancers.


  Subjects and Methods Top


Subjects and setting

All patients with a cancer diagnosis admitted for inpatient neurorehabilitation from 2009 to 2017 were included in this retrospective study. Since 2013, a weekly multidisciplinary team meeting was established to discuss the rehabilitative and discharge planning needs for relevant cancer patients. This multidisciplinary team consists of consultants in rehabilitation medicine and geriatric medicine; oncology ward-based physiotherapist, occupational therapist, nurse specialists, and social worker; with occasional attendance by medical staff from clinical and medical oncology. Inclusion criteria for admission for inpatient rehabilitation require the combination of presence of new neurological deficit, sufficient medical stability to be able to engage in rehabilitation, and identified realistic achievable goals.

Inpatient rehabilitation outcomes

The outcomes assessed were length of stay (LOS), change in UK Functional Independence Measure + Functional Assessment Measure (UK FIM + FAM), discharge outcome, and survival. The UK FIM + FAM is a validated 30-item inpatient global measure of disability and functional independence that is responsive to functional changes in a neurorehabilitation cohort.[21] UK FIM + FAM scores were collected prospectively for each patient on admission and again at the point of discharge, but this was only implemented in 2012.

UK FIM + FAM change is defined as the absolute difference between discharge and admission scores. UK FIM + FAM efficiency is defined as UK FIM + FAM change divided by LOS and represents the absolute change made per day. Discharge outcome is defined as “home,” “acute transfer,” “palliation” (including transfer to hospice or on the ward), “long-term care facility” (including hospital-based complex care facilities and residential homes), and “others.”

Statistical analysis

Patients were categorized by benign versus malignant status, based on tumor grading and/or presence of metastases. Shapiro–Wilk test is used to test for normality of datasets. Mann–Whitney U-test and Student's t-test were used to compare age, LOS, and UK FIM + FAM scores between the two groups. Chi-squared test was used to determine associations between gender and acute transfers between the two groups. The survival rate as of July 25, 2019, was estimated by the Kaplan–Meier method. All data were analyzed using SAS University Edition. P < 0.05 was considered statistically significant.

Ethics approval

Caldicott Guardian approval was granted.


  Results Top


Patient characteristics

One hundred and twenty patients were admitted, of whom 40% had a malignant diagnosis. There was no significant difference in age between the two groups and there was no significant association between gender and a malignant diagnosis (x2 = 2.0, P = 0.157). [Table 1] illustrates the patient characteristics in their diagnostic subgroups. Of the 74 patients with brain-related tumors, 52 were benign (70%), with the most common diagnosis being meningioma (37% of benign brain-related tumors). The majority of malignant brain tumors were glioblastomas (55% of malignant brain-related tumors). Of the 29 patients with spine-related tumors, only 9 were benign (31%), with the majority being ependymomas (22%); the majority of malignant spine tumors were metastatic compression from a primary nonneurological tumor (85%). The “other” group (65% benign) consisted of patients presenting with a wide spectrum of noninvasive, noncompressive cancer-related presentations ranging from deconditioning (e.g., prolonged hospital stay and postchemotherapy), treatment-related complications (e.g., peripheral neuropathy and congestive heart failure), to paraneoplastic syndromes (e.g., peripheral neuropathy and cerebellar degeneration).
Table 1: Patient characteristics

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Discharge outcome and transfers

[Table 1] illustrates the discharge destinations for the patients from the two groups. The two inpatient patient deaths arose from limitations in alternative placement options for palliation in patients whose disease recurred or progressed.

Eighteen percent (18%, 21/120) of the patients were transferred to an acute setting, of whom 76% (16/21) were patients with malignancy. Main reasons for transfers include acute medical deterioration (e.g., sepsis, thromboembolism, and electrolyte disturbances) or disease progression. Having a malignant diagnosis was associated with a higher rate of transfer to an acute setting (34% in malignant group vs. 7% in benign group, x2 = 13.8, P < 0.01). Of those transferred, ten patients died (three – benign), two were discharged to hospice, two to long-term care, and seven to home (two – benign).

Length of stay and United Kingdom Functional Independence Measure + Functional Assessment Measure

Of those in whom UK FIM + FAM is fully documented, admission score was not significantly different between the two groups (mean difference: 8, 95% confidence interval [CI]: −11–27, P = 0.423), although this was trending higher in the malignant group. LOS was also not significantly different (median difference: 5 days, 95% CI: –8–18, P = 0.187). While UK FIM + FAM change was significantly lower in the malignant group, the corresponding lower UK FIM + FAM efficiency was not statistically significant (mean difference: 16, 95% CI: 1–31, P = 0.043 and 0.18, −0.42–0.05, P = 0.114, respectively) [Table 1].

Survival

Eighty-nine percent of the patients with benign diagnosis and 29% of the patients with malignant diagnosis survived 1 year or more beyond discharge. The median survival postdischarge for the malignant group (n = 48, n = 7 still alive) was 3.2 months (95% CI: 2.0–8.4), with survival up to 40.4 months [Figure 1]. Of the 21 patients transferred to an acute setting, 40% (2/5) of the patients with benign diagnosis and 13% (2/16) of the patients with malignant diagnosis survived 1 year or more beyond discharge.
Figure 1: Kaplan–Meier curve for patients with malignancy. Total sample size of 48 in malignant group with 41 observations included in survival analysis (7 observations right-censored). Median survival at 3.2 months (95% confidence interval: 2.0–8.4)

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  Discussion Top


Functional measures and survival

LOS was comparable between patients with benign and malignant diagnoses, with a median of just over 6 weeks in each. In fact, the LOS of these two groups of patients was also similar to that of nonneuro-oncological admissions within the same timeframe, with a median LOS of 53 days (n = 988; data not shown), suggesting that there had been no significant issues with discharge planning. While UK FIM + FAM change was significantly lower in the malignant group, there was no significant difference noted in UK FIM + FAM efficiency. This is to be interpreted with caution due to the small sample sizes for UK FIM + FAM data. A potential confounder was the higher proportion (69%) of malignancy in the spinal group compared with the other groups (31%). As there are fewer UK FIM + FAM parameters in which there is potential for functional recovery in spinal-damaged relative to brain-damaged patients, this can skew the results.

Another important consideration is the recognition that reduced life expectancy requires balancing rehabilitation goals against the need to minimize LOS, leading to a focus on goals that enable early safe discharge rather than maximizing independence. Hence, the UK FIM + FAM and other similar functional measures, which focus on functional gains, are unlikely to fully capture the benefit of inpatient rehabilitation for these patients. Goal attainment scaling may be more appropriate and will be important to evaluate in this context.[22]

It is difficult to compare this study to the other studies of inpatient cancer rehabilitation as different functional outcomes (FIM and Barthel Index) were used and most demonstrated functional improvement as an entire study cohort of patients with a cancer diagnosis, rather than compare functional outcomes between the different subgroups of patients with benign and malignant cancers.[17] Sliwa et al. demonstrated that no significant differences in functional gains were seen in patients with versus without metastatic disease in a retrospective study of 176 patients, although the sample was more heterogeneous rather than being specific to neurological impairment.[23]

It is not surprising that survival at 1 year postdischarge is lower for patients with malignancy (29%). Allowing for this, a median survival following discharge of only 3.2 months casts doubt over the value of rehabilitation admission, this duration being not much longer than the median LOS. This was shorter than previously reported in specific populations of malignant disease (5.9 months in leptomeningeal disease and 4.1 months in metastatic spinal cord compression).[19],[20] These studies calculated median survival from rehabilitation admission although their median LOS was also shorter at under 2 weeks. Possible explanations for the difference include selection bias as a result of variations in thresholds for admission and the heterogeneity of the present study sample, which also included patients with high-grade gliomas.

In exploring whether inpatient rehabilitation is beneficial given the relative proportion of remaining life spent in hospital, and the limited potential for functional gain, one also needs to consider the added value that focus on rehabilitation provides in enabling patients to accept and adapt to the combined impact of neurological deficit and cancer prognosis. In considering this, one should also question whether this constitutes the most appropriate use of inpatient rehabilitation resources. This concern may be offset to some extent by recognition that in some instances, these patients may otherwise find themselves “trapped” in oncology wards if their neurological impairment limits ability to be discharged to their home environment. While this achieves greater patient benefit in situations where overall LOS is not compromised, it nevertheless creates a separate conundrum in terms of balancing rehabilitation and oncological resources.

This again reiterates the need of taking a goal-centered approach within this patient cohort that carefully balances rehabilitation goals with remaining life expectancy. While standard neurorehabilitation approaches typically focus on maximizing function and reducing dependency, potentially including vocational roles, a palliative rehabilitation approach is more suitable for patients with limited life expectancy. Palliative rehabilitation has been described in the literature as a patient-centered process of symptom management in terminal patients with the key aim of improving QoL within a biopsychosocial framework.[24],[25] A shorter inpatient rehabilitation stay focusing on narrow goals achievable in a short timescale aimed at prolonging QoL, autonomy, and dignity may be warranted, and will validate the need for inpatient rehabilitation even if median survival is measured in a few months.

Psychosocial measures and adjustment

In addition to functional benefit, inpatient cancer rehabilitation has been associated with short-term improvements in QoL and psychological distress.[15],[26],[27] Moreover, Ture et al. further demonstrated that patients who underwent inpatient cancer rehabilitation received significantly better improvements in QoL, physical functioning, mental health, and fatigue when compared to outpatient rehabilitation programs at 3-week follow-up.[26] However, there is currently no data regarding long-term sustained benefit although this may be difficult to collate in patients with poorer prognosis. Our study did not provide any data with regard to this aspect.

An important component for managing psychological distress is the facilitation of patient adjustment which includes the delivery of an accurate prognosis for life expectancy. This can be a challenge for the rehabilitation team and does not always fall within its area of expertise, although it can be argued that discussions on prognosis by rehabilitation physicians in the rehabilitation setting are appropriate. Prognostic discussion should not be confined to just survival and disease recurrence, but also include functional recovery, potential to achieve QoL-related goals and acceptance of loss of functioning where relevant. Patients with cancer-related neurological deficit often find adjustment to dual challenges of cancer prognosis and rehabilitation prognosis to be overwhelming. Although oncologists and rehabilitation physicians are skilled in discussing prognosis relevant to their own disciplines, they are likely to be limited in discussing the wider context. One way to mitigate this issue is by having strong collaborative links between oncology and rehabilitation physicians early on in the patient's cancer journey. This can enable frank discussions about predicted survival, rehabilitation potential, and realistic goals to occur early on, before the relevant oncological treatment where possible. This has the potential to facilitate more realistic patient expectations of both the cancer diagnosis and related functional impairment. This view on interdisciplinary cooperation between oncology and rehabilitation medicine to improve communication and education, and ultimately patient care, was previously highlighted.[28]

Delivering compassionate dignified care is a central tenet of both oncological and palliative care and should also be made a priority for this patient group. Improving the patient and family experience across their journey through the health-care setting lies in the heart of this approach, and the use of emotional touchpoints has been recognized to be a helpful tool in identifying both the positive and negative aspects of the patient's experience in this context.[29] Our service is currently trialing the use of emotional touchpoints for patients with neuro-oncological diagnoses.

Discharge outcome and transfers

The majority of the patients admitted were discharged home (85% in benign and 58% in malignant groups). Eight percent (8%) of the patients with malignancy were either discharged to a hospice or died within our unit as part of a planned palliative approach. This highlights the importance of recognizing overlapping roles of palliative care and rehabilitation services in maximizing patient QoL, and the need for a flexible approach to rehabilitation planning in the event of disease progression.

Eighteen percent (18%) of all the admitted patients were subsequently transferred to an acute or oncological setting with new medical complications and not re-admitted for rehabilitation; of these, 76% were patients with malignancy. This is similar to that reported in other studies, with acute transfer rates ranging between 11% and 35%.[9],[16],[30],[31],[32],[33] About half of the patients in these studies subsequently died in the acute setting. While Alam et al. reported a significant difference in the rate of acute transfers between cancer- and noncancer-matched controls,[33] our study demonstrated a significant association between malignancy and the rate of acute transfers.

Risk factors that have been implicated as increasing likelihood of transfer to acute settings, include lower functional status, elevated creatinine, reduced albumin, and the presence of indwelling tubes.[31],[32] This suggests the potential to develop a more structured patient selection process for admission to inpatient rehabilitation but creates the ethical dilemma of creating barriers based on the risk of acute transfer alone. Our department did not use these factors as exclusion criteria. The likelihood for any unit planning to develop cancer rehabilitation service is that disease progression will remain an inevitable risk that will be difficult to predict or mitigate.

Only a small number of patients were transferred out of the neurorehabilitation setting for further oncological treatment, such as chemo- or radio-therapy, due to disease progression (n=7). One of the main limitations of delivering neuro-oncological rehabilitation in a separate neurorehabilitation unit is that oncological treatment cannot be delivered within that specific setting due to a lack of specialist knowledge and appropriate facilities. This does not preclude short duration (1–3 days) transfers to oncological wards to enable treatment cycles. However, it may not always be suitable for patients undergoing active oncological treatment to engage with more intensive rehabilitation programs, as treatment-related fatigue, neutropenia, or metabolic derangement may limit ability to engage in meaningful rehabilitation interventions. Intensive rehabilitation may improve overall outcomes if planned around oncological treatment blocks, with the aims of either preconditioning the patient prior to a treatment block, or re-conditioning the patient after, but may be hampered by logistics of coordinating bed availability across two sites.

Limitations

The main limitation of this study is its retrospective design. There is potential for selection bias because only patients deemed to have rehabilitation goals that can be met were admitted, or for referral bias where oncology services under-refer due to a lack of awareness of role or perceived benefit. These biases may have been partly mitigated by the collaborative interdisciplinary approach to patient selection. There may also be self-selection bias based on patient motivation and expectations, which may be associated with unrealistic perceptions about prognosis for cancer cure and/or neurological recovery. However, sometimes these patients may still require an opportunity for inpatient rehabilitation to come to terms with their clinical condition and/or physical limitations that will ultimately help to define the goals of ongoing management for the remainder of their care journey.

The heterogeneity of the study sample is another limiting factor. Patients admitted all had neurological dysfunction but of variable etiology, including both nervous system- and nonnervous system-related tumors. However, this heterogeneity reflects the pragmatism of clinical practice of inpatient specialist neurorehabilitation units in assessing and rehabilitating patients based on individual context and need, rather than by histopathological diagnosis.

While LOS was broadly similar between cancer and noncancer patients, no functional outcome comparisons were made between these two groups in this study. However, a recent meta-analysis suggested that functional gains made by brain tumor patients were similar to noncancer patients.[17] This meta-analysis had a pooled sample size of 994 patients, of which 77% of the patients had malignancy. However, the rehabilitation settings were variable, including a study of 239 patients with terminal cancer receiving physiotherapy in a hospice.[34]


  Conclusion Top


This study demonstrates that neuro-oncological rehabilitation can be effectively delivered within an inpatient neurorehabilitation setting with the appropriate support. While the outcomes for inpatient neuro-oncological rehabilitation of patients with benign and malignant diagnoses were potentially similar, the UK FIM + FAM does not necessarily capture the full benefit of rehabilitation. Further research focusing on goal attainment scaling, QoL, and/or emotional touchpoints may provide greater value in identifying the benefit of delivering such a service, especially in patients with malignancy. Given the limited survival after discharge in malignancy, a collaborative approach with both oncology and palliative care medicine is crucial in the development of an inpatient cancer rehabilitation service.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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