Introduction

Death and dying is the final phase in the human condition but the definition of “dying” is not singular, either legally or medically; for this article, we will consider “end of life” and “dying” to be up to the last few months of life and “imminently dying” as the last few days of life.

Achieving a “good death” is a collaborative process and one that is unique to everyone. What may be important to one person may not be important to another. Studies on this topic are revelatory: people want to be as symptom-free as possible, remain as functional and clear-thinking as possible, and contribute to those around them [1,2,3]. To this end, the rehabilitation team is well-poised to provide important contributions to meet this goal.

Serious illnesses have different trajectories of functional decline, thereby requiring different resources at different times. Rehabilitation can be subcategorized into preventative rehabilitation (also known colloquially as “prehab,” where the goal is to mitigate potential functional declines in those with serious illness), restorative rehabilitation (typically what we think about; where the goal is to try to get back to a pre-illness or pretreatment state when no significant long-term decline is anticipated), supportive rehabilitation (where the goal is to maximize function in those with serious illness after the disease or treatment causes permanent morbidity), and palliative rehabilitation. Palliative rehabilitation is defined as “the process of helping a person with a progressive, often terminal illness reach their physical, psychological, and social potential consistent with physiological and environmental limitations and life preferences [5]” and is the predominant context of this article.

People approaching the end of life can deal with different sources of distress, including physical and psychosocial distress, that affects their quality of life and personhood. Physical symptoms such as pain, fatigue, and insomnia, as well as symptoms of depression and anxiety can limit function and independence — leading causes of patients asking for physician-assisted suicide [4]. Rehabilitation services (e.g., physical and occupational therapy and speech-language pathology) are often thought to be for those who have suffered an acute illness and need restorative therapy to regain lost function(s). This is an incomplete understanding, however, as the role of rehabilitation specialists is broader and includes treating pain and disabling conditions and providing care to the whole person, regardless of their life expectancy.

Symptoms Towards End-of-Life

Pain

Pain at the end of life is a complex process that affects all aspects of a person’s life. It occurs in up to half of those with cancer, and 80% of those with advanced cancer can have moderate to severe pain [6]. Pain can be debilitating and significantly affect the quality of life of the dying cancer patient. Physical pain — as opposed to psychological, social, and spiritual pain — can be categorized as neuropathic (e.g., cord compression), visceral (e.g., organ sheath distension, acute obstruction, or perforation), or somatic (e.g., direct bone invasion or pathologic fracture) depending on the etiology. Pain can be directly related to the cancer or can be due to cancer treatments (e.g., oral mucositis after radiation therapy, post-operative wound pain, or chemotherapy-induced peripheral neuropathy). Evaluation includes a thorough history and physical exam, including careful examination of painful sites and overlooked skin breakdown. The history should also include a comprehensive review of systems as comorbid symptoms/conditions can contribute to pain (e.g., anxiety and pain can certainly make the other feel more intense). Asking about pain characteristics can help clinicians define the type of pain and choose appropriate interventions.

Bone pain from metastases is the most common source of cancer-related pain [7]. Bone pain is often incidental, affected by movement and positioning. It is correlated with increased psychologic distress, reduced function, and decreased quality of life [9]. Unfortunately, there is not a clear association between size, location, and number of bone metastases and pain. The rehabilitation team can play a crucial role in maximizing quality of life in the dying patient. Physical and occupational therapists can help maximize functional ability, decrease sequelae such as falls, and improve quality of life [7, 8]. Physical therapists can educate patients and caregivers on safe lifting techniques and the importance of body mechanics, as well as help with assistive devices to offload at-risk areas, to help prevent further pathologic fractures. Massage, heat, TENS, and acupuncture are among physical modalities that can also be helpful in treating somatic pain under the guidance of a rehabilitation specialist [10]. Physiatrists can consider several different medications for bone pain. Bone pain can be managed with NSAIDs, opioids, osteoclast inhibitors, and glucocorticoids depending on severity and expected prognosis, though none of these agents are without side effects. Consideration can be given to long-acting opioids for baseline pain and short-acting opioids for breakthrough pain. Long-acting formulations include oral and transdermal (e.g., fentanyl) while short-acting include oral, IV, IM, subQ, and transmucosal. Typical side effects can include sleepiness, nausea, and constipation, and clinicians should monitor for adverse cognitive effects like hallucinations or confusion and respiratory depression.

Neuropathic pain is present in up to 40% of patients and also contributes to significant pain [11]. This pain is often described as burning, tingling, shooting, or electric-like. While we have medications for these “positive” symptoms, medications for the “negative” symptom of numbness are lacking. Neuropathic pain can occur due to several pathologies; some examples include malignant compression causing radiculopathies and plexopathies, chemotherapy-induced peripheral neuropathies, and leptomeningeal disease.

Antidepressants in the serotonin and norepinephrine reuptake inhibitors (SNRI) class (e.g., duloxetine) and anticonvulsants (e.g., gabapentin) are considered first-line treatment options for neuropathic pain per National Comprehensive Cancer Network (NCCN) guidelines. Common side effects of these agents include dizziness, drowsiness, fatigue, and nausea [12]. When the above agents are not enough, consideration can be given to short-and long-acting opioids. Consideration can also be given to steroids when the neuropathic pain is caused by nerve compression.

Lymphedema is a common delayed effect of cancer treatment and can be another source of pain in the dying cancer patient. It is often present as unilateral, non-pitting edema. The history and examination should rule out other causes of edema, including deep venous thrombosis and infection. Prevalence varies by disease: around 20% in breast cancer and between 31 and 36% in ovarian, endometrial, and colorectal cancer [13, 14]. Compression of lymph nodes or lymphatic channels by direct mass effect/obstruction; disruption of the lymphatic system after lymph node dissection; and infiltration of lymphatic vessels can contribute to painful lymphadenopathy. Treatment goals include not only pain relief but also preserving skin integrity and improving function. Though lacking in a strong evidence base, anecdotal reports suggest that individual patients may experience benefits such as reduced discomfort and improved quality of life from manual lymphatic drainage. Complete decongestive therapy (CDT) is considered the “gold standard” for lymphedema management. It consists of two phases, the intensive and the maintenance, though if prognosis is limited, perhaps the first phase is the most critical. Interventions in this phase include skin and wound care, exercise (which, again, may be limited in this specific population), manual lymphatic drainage, and compression bandages. CDT can achieve limb volume reductions of 50–70% [15]. There are limited medical options, but a clinician can consider furosemide if there is concurrent generalized edema. Surgical options are unlikely to be considered in this population.

Fatigue

Fatigue is one of the most common symptoms affecting patients with cancer with recent studies demonstrating a prevalence of 43% [16]. It is even more common in those having active treatment affecting virtually everyone undergoing chemotherapy/radiation [17]. Cancer-related fatigue is differentiated from regular fatigue in that it is not alleviated by rest, is not proportional to activity level, and is particularly severe. Severity may be such that patients are frequently unable to participate in regular work and social activities. As disease progresses towards end of life, fatigue can often reach a point as to interfere with activities of daily living and patients may have difficulties with transfers and ambulation. While increasing fatigue is expected in the dying patient, rehabilitation interventions can to some degree slow and alleviate the process.

Cancer-related fatigue is almost always multimodal. Evaluation for progressive fatigue should occur on a regular basis and should be comprehensive. The NCCN has an excellent framework for assessing treatable factors of fatigue which include pain, emotional distress, anemia, sleep disturbance, nutritional deficits, physical activity, and comorbidities [18]. Furthermore, it is believed that polypharmacy is common in patients with cancer, particularly among the elderly [19]. Opioids, muscle relaxants, gabapentinoids, benzodiazepines, and anti-emetics are all commonly used in this population and may likely be contributing to fatigue. It is critical to assess what dose, how often, and at what time of day such medications and others are being used.

Once treatable factors have been identified, actions should be taken to ameliorate each specific one. Anemic patients, even those on hospice, may receive transfusions if it is treating symptoms. Patients in emotional distress may be referred to clinical social work, spiritual care services, support groups, and psychotherapy. Particular attention should be given to sleep duration and quality. Underlying reasons for difficulty in sleeping such as pain or anxiety should be treated and for those with primary insomnia, cognitive behavioral therapy, and pharmacotherapy per American Academy of Sleep Medicine guidelines may be useful [20, 21]. When available, consultation with clinical nutritionists may be helpful to ensure adequate calorie, protein, and fluid intake and is also recommended by the NCCN. After review of potentially sedating medications, discontinuation of those of minimal or unclear benefit, and dose reduction or changing the time of day when taken if possible can also reduce fatigue.

Finally, the role of physical activity and exercise cannot be overstated. Numerous systematic reviews have demonstrated the positive impact of exercise on cancer-related fatigue across variable patient populations [22,23,24,25]. This ample evidence backs guidelines from multiple organizations including the American Cancer Society, the NCCN, and the American College of Sports Medicine which generally recommend 150 min of moderate intensity aerobic activity per week with 2–3 days per week of resistance training [18, 26, 27]. For patients with lower baseline levels of activity, multiple comorbidities and those with advanced disease, this level of exercise likely will not be feasible. In such cases, patients should be advised to do whichever amount of exercise they are able to and are comfortable doing within their goals of care as even light levels of exercises have been found to be beneficial [28]. As adherence rates are believed to be higher with supervised vs unsupervised programs, personal trainers and group exercise classes may be encouraged for patients who are well resourced and in those without concern for injury. For patients in whom financial toxicity or injury is of concern, skilled therapies including home or outpatient physical and occupational therapy may be considered. It is beyond the scope of this article to discuss all safety indications when clearing advanced cancer patients for exercises, but factors for consideration can be found within the NCCN survivorship guidelines [29]. Physiatrists may also have insights and be of unique benefit in discussing exercise considerations and precautions in medically complex patients.

Anxiety and Depression

Prevalence of anxiety and depression in patients with cancer is varied; reports range from approximately 10–14% for anxiety and 5–20% for depression, which exceeds population-estimated prevalence of 7% and 5%, respectively [30,31,32]. It should be noted, however, that these conditions can be difficult to diagnose in this population because (1) somatic symptoms in cancer can overlap with symptoms of depression, (2) people may not directly share symptoms of anxiety and depression, and (3) parts of the dying process may be attributed as “normal” when in fact they are pathologic (e.g., pathologic grief can overlap with symptoms of depression and may be incorrectly considered a normal part of the grieving process). Clinical guidelines suggest that screening should be done at diagnosis and when clinically appropriate, including when changes of care plan are made (e.g., focusing on end-of-life care) [33].

Assessment, therefore, is complex, and clinicians may rely more on psychologic symptoms of anhedonia, feelings of being down/depressed, hopelessness, worthlessness, or guilt over the physical symptoms of depression. The PHQ-4 is a validated, short screening tool that can be used to screen for anxiety or depression, and the GAD-7 and PHQ-9 can be used to measure and monitor the severity of anxiety and depression, respectively, over time [33]. It is, as always, also important to rule out reversible and physiologic causes as well as palliate comorbid symptoms such as pain. Clinicians should have a low threshold for diagnosis, as rapid control of symptoms is important to maximize quality of life, and they should consider prognosis (e.g., days to weeks vs weeks to months) when choosing medications.

Initial management of anxiety with benzodiazepines can provide quick control of anxiety, but patients should be monitored closely for potential side effects or interactions with other medications. Short-acting lorazepam can be dosed frequently and may help with anxiety as well as comorbid nausea; longer-acting clonazepam may be considered for more sustained symptom control. While an evidence base is lacking, clinical experience suggests that gabapentin and trazodone can both be used on a PRN basis as potentially safer rapid-acting medications [34]. For patients with more longstanding anxiety or a mix of anxiety and depression, an SSRI can also be considered. SSRIs or SNRIs and buspirone can be considered as well if patients have a prognosis of months as these medications take a few weeks for effect. Consideration can be given to agents such as olanzapine or quetiapine when benzodiazepines alone are not enough. For patients who have a shorter prognosis (i.e., days to weeks), consideration should be given to psychostimulants (e.g., methylphenidate) as effects may be seen within 24 to 48 h of starting treatment. These agents may also be considered in patients with a longer prognosis who need rapid symptom control.

Loss of Function

Functional impairments are extremely common in patients with cancer with reports of limitations in function within adult-onset cancer survivors of 53% [35]. There are myriad sources of impairments whether pre-existing, secondary to disease or secondary to treatment. In addition to specific impairments, it is also important to consider the patient’s loss of function in the context of activity limitations and participation restrictions which is most often done in the International Classification of Functional Disability and Health from the World Health Organization [36]. In such a framework, it is essential to address not only the physical impairment, such as loss of proprioception from chemotherapy-induced neuropathy, but also the activity limitation of inability to run and the participation restriction of no longer being able to play competitive sports.

Considering the different levels at which patient’s lives can be altered, it is critical to evaluate functional status at regular intervals, particularly following sentinel events including surgery, completion of radiation therapy, occurrence of pathologic fracture, development of neuropathy (most often chemotherapy-induced), hospitalization, allopathic transplant, and cellular therapies such as CAR-T. During an evaluation, the patient’s baseline functional status should be determined as well as the current functional status. For patients with advanced cancer approaching the end of life, counseling and education are vital as certain impairments may be permanent such as weakness secondary to an untreatable brain tumor, whereas others may be at least partially reversible such as in adhesive capsulitis following treatment in breast cancer. Whichever the situation, the clinician must tread the ever-moving line of being realistic with functional prognosis without taking away hope for meaningful recovery.

While progressive disablement until the point of death is certain, some may take this point to argue that rehabilitation at the end stage of life is a futile if not counterintuitive endeavor. However, we remember the words of Dame Cicely Saunders who stated, “The work of all the professional team is to enable the dying person to live until he dies, at his own maximal potential, performing to the limit of his physical and mental capacity with control and independence whenever possible [37].” Multiple studies have shown that in regard to helping patients maximize their physical capacity, rehabilitation can be an effective approach.

A retrospective analysis assessed the feasibility of physical exercise and physical therapy (PT) in terminally ill cancer patients in an inpatient palliative care ward. They found that physical exercise or physical therapy activities were feasible in over 90% of patients with physical exercises, relaxation therapy, and breathing training being the most applied [38]. Other studies have shown improvements in functional performance including ADL and transfers in hospice settings and palliative care units, and a recent review examining the effects of exercise and nutritional rehabilitation in outpatients with incurable cancer found moderate evidence for improvement in physical endurance [39, 40]. This general approach has been termed “Rehabilitation in Reverse” and utilizes energy conservation techniques with a focus on maintaining mobility in the setting of overall decline [41]. Caregivers also stand to benefit as supported by a case study demonstrating improved confidence in assisting with transfers and a short stay palliative inpatient rehabilitation program allowing debilitated patients to be discharged home safely with caregiver assistance [42, 43].

Existential Distress

The field of rehabilitation medicine is centered on optimizing function and quality of life for those with impairments. Typically this is thought to occur through managing physical symptoms such as pain or fatigue or supporting the recovery of physical impairments that occur through catastrophic injuries such as traumatic brain injuries or spinal cord injuries. But when viewed holistically, at its core, the field of rehabilitation medicine is arguably about preserving the dignity of the individual. Indeed, at the end of life, being at peace ranks only marginally below the desire to ease physical pain [44, 45].

When caring for the dying cancer patient, recognizing the demoralization and the profound existential and spiritual challenges that commonly afflict our patients is paramount. These are core healthcare issues, not optional or ancillary ones. Managing physical pain without recognizing existential pain can result in inadequate outcomes at best and may result in severe mismanagement at worst.

It is critical for rehabilitation medicine providers to have some basic understanding of existential distress in order to provide the most comprehensive end-of-life care. While chaplains, social workers, and other mental health professionals can be instrumental in this care, a basic recognition of the value of addressing existential pain and distress can be within the scope of all clinicians who work with dying patients. The Institute of Medicine report Dying in America also showcased the critical importance of addressing existential and spiritual distress among those with advanced cancer [46].

The first step in mitigating suffering and anguish is to recognize and acknowledge how this may manifest in the patient dying from cancer. According to Mount et al., common themes of suffering and anguish often include these facets:

  1. 1.

    Preoccupation with the future or past

  2. 2.

    Sense of disconnection from self, others, or the world

  3. 3.

    A need to be in control

  4. 4.

    A crisis in meaning (an existential vacuum) or

  5. 5.

    Sense of victimization [47]

While chaplains and spiritual leaders may be best equipped to handle these profound challenges, the rehabilitation professional can play an important role through various strategies. Identifying and supporting expressions of fear and thereby acknowledging fears can be an important first step. One option is to help identify sources of meaning before and during the illness. Once this is better crystallized, this may open the opportunity of creating a life narration (through text, music, video, or audio). The rehabilitation professional can promote the creation of a calm, pleasing atmosphere, as best as possible, which can support an environment that can be conducive to more peace. Manualized reminiscence and legacy projects such as these may provide profound comfort for some [48]. Strategies that focus the patient’s attention to the present moment are important: mindfulness meditation, guided imagery, music therapy, art therapy, and prayer can all zero on the here and now and thereby reduce distress.

More recently, randomized clinical trials have shown that manualizing many of these interventions in a structured format can provide meaningful reductions in spiritual distress. For example, Breitbart and colleagues demonstrated benefits from a structured-, meaning-centered psychotherapy for reducing existential distress among patients with advanced cancer [49]. Asher et al. demonstrated that a multi-faceted 6-week intervention that encompasses mindfulness, logotherapy, cognitive behavioral therapy, and positive psychology significantly improved spiritual well-being, quality of life, depression, and hopelessness [50]. As virtual technologies can make these programs more available broadly, they may offer another therapy that can reduce the suffering of some of our most vulnerable patients.

Conclusion

The dying cancer patient — whether their prognosis is days, weeks, or months — has complex psychosocial, spiritual, and physical needs. Some core elements of a “good death” include symptom control, ability to make decisions, being seen as a person, and being able to contribute to others. The role of the rehabilitation clinician goes beyond functional restoration; rather, it is about preserving individual dignity and personhood. A thorough assessment can reveal physical symptoms such as pain and fatigue as well as symptoms of anxiety, depression, and existential distress. All of these contribute to decreased quality of life and loss of independence, two factors antithetical to having a “good death,” and domains in which rehabilitation clinicians can make important contributions.