Abstract
Cancer-related fatigue (CRF) occurs in up to 90% of patients receiving cancer treatment and in 30–40% of cancer survivors. In this chapter, we describe the instruments that have been developed to identify CRF. Although the measurement of CRF is not standardized, clinicians are encouraged to incorporate CRF assessment in clinical practice. We also summarize the ongoing research demonstrating the association of inflammatory cytokines and CRF as well as other proposed mechanisms. We also suggest that exercise and psychological interventions, which have consistently demonstrated benefits in treating CRF, be utilized in the initial management of CRF. Finally, we summarize guidelines proposed by the American Society of Clinical Oncology, National Comprehensive Cancer Network, and Pan-Canadian Clinical Practice Guidelines for clinicians and health professionals in the screening, assessment, and treatment of CRF.
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1 Definition of Cancer-Related Fatigue
Cancer-related fatigue (CRF) is a distressing, persistent, and subjective sense of physical, emotional, and/or cognitive tiredness or exhaustion related to cancer or cancer treatment that is not proportional to recent activity and interferes with usual functioning [1, 2]. CRF is different from common physical or mental tiredness in that CRF is not relieved by sleep or rest, whereas general fatigue (i.e., physical or mental tiredness) is a transient inability to maintain optimal performance that is relieved by rest [3]. CRF negatively interferes with patients’ ability to complete their cancer treatments and their ability to complete activities of daily living, and it reduces quality of life [3].
2 Prevalence of Cancer-Related Fatigue
CRF can occur as a consequence of the cancer itself [4] or cancer treatment. It is the most commonly reported [5] and also the most distressing [6] side effect of cancer treatments including chemotherapy [7,8,9], radiation therapy [4, 10], or selected biologic modifiers [11]. As many as 40% of patients with cancer report CRF at the initial time of diagnosis [4], and the majority of patients experience CRF during the course of their treatment. Up to 90% [4, 10] of patients with a variety of cancer subtypes undergoing radiation therapy and up to 80% [7, 8] of those receiving chemotherapy experience CRF. While CRF will resolve for some survivors after completion of treatments, there are still approximately 30–40% of cancer survivors reported to have persistent CRF up to 10 years posttreatment [1, 3, 12,13,14,15,16,17,18,19,20,21,22]. In survivors of Hodgkin lymphoma, CRF has been shown to have a major impact on treatment outcomes and social reintegration [23].
3 Measurement of Cancer-Related Fatigue
Self-report assessment tools , also referred to as patient-reported outcome tools, are the most commonly used, reliable, and valid methods for both clinical and research measurement of CRF. There are many patient-reported instruments that can quantify CRF. A systematic review of 1453 published studies evaluating CRF instruments in patients with cancer and survivors [24] identified 37 studies and 40 instruments. The instruments were classified as three unidimensional and 37 multidimensional. These instruments vary by CRF dimensions, number of items, rating scales, types of cancer population studied, and psychometric properties. The validity and reliability were evaluated by internal consistency, test-retest reliability, and convergent validity. Of these 40 instruments, five instruments including:
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1.
Brief Fatigue Inventory (BFI) [25]
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2.
Cancer Fatigue Scale (CFS) [26]
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3.
Chinese CFS (C-CFS)
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4.
Functional Assessment of Cancer Therapy-Fatigue (FACT-F) [27], and
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5.
Multidimensional Fatigue Symptom Inventory-Short Form (MFSI-SF) [28]
have been optimally tested for validity and reliability with an internal consistency of 0.9 by Cronbach α coefficient and a concurrent validity ≥0.45 by Pearson correlation [24]. The type and the stage of cancer may affect CRF. Most of the CRF instruments were used in mixed cancer populations, and only a number of them used a homogenous cancer patient population, including the BFI [25], FACT-F [27], Fatigue Functional Impact Scale [29], MFSI-SF [28], Piper Fatigue Scale [30], Visual Analogue Scale (VAS) [31], and Wu Cancer Fatigue Scale [32].
Although the measurement of CRF is not universally standardized, some instruments are more commonly used than others, as listed in Table 8.1. The authors of a systematic review review suggest use of a simple unidimensional measure that includes a rating of severity (such as the FACT-F and VAS) as an initial step for identifying the presence of CRF among survivors. If CRF is present, a multidimensional instrument can be considered to further identify the most problematic domain(s) of CRF. Oncologists and clinicians then can prescribe the optimal treatment specifically targeting the problematic domains for patients at early stages of cancer and survivors who have completed primary treatments but are still receiving hormone therapies or biologics. The authors of the systematic review recommended using BFI to evaluate CRF in patients with advanced cancer undergoing palliative treatment given the short length of the questionnaire (fewer than 10 items) and its optimal psychometric properties [24]. In addition, BFI is sensitive when measuring change of CRF over time. The three items related to fatigue included in the European Organization for Research and Treatment of Cancer Quality-of-Life Questionnaire Core 30 [33] have also been used among patients with advanced cancer [24] and validated with good test-retest reliability [34].
4 Possible Mechanisms Associated with Cancer-Related Fatigue
A number of mechanisms associated with the development of CRF have been proposed in recent decades. Some of these include (1) anemia, (2) circadian rhythm disruption, (3) stress and cytokine dysregulation, (4) psychological distress, (5) pain and neuroimmunologic changes, (6) cardiovascular and physical dysfunction, and (7) energy, nutritional deficits, and imbalance [42,43,44]. Of these potential mechanisms, cytokine dysregulation has been the most studied to date. Research has shown that cancer may activate pro-inflammatory cytokines, such as interleukin-6 (IL-6), and markers of inflammation, such as C-reactive protein (CRP), resulting in the development of CRF prior to cancer treatment initiation [45,46,47,48,49,50]. In addition, cancer treatments continue to prolong activation of pro-inflammatory cytokines during treatment [45, 51] and after treatment completion [43].
The use of radiation therapy and chemotherapy is also associated with increased inflammation (e.g., CRP, IL-1 receptor antagonist, IL-6). Patients with breast and prostate cancer have been shown to have elevated levels of CRP and IL-1 receptor antagonist [52]. In another sample of 53 patients with breast cancer receiving chemotherapy, serum IL-6 was found to be increased after treatment [53]. These inflammatory markers are positively associated with increased self-reported CRF [47, 50, 53,54,55,56,57,58,59,60,61,62]. Clevenger et al. [47] showed that in 136 women with ovarian cancer, higher levels of plasma IL-6 was associated with greater CRF prior to surgery. Pertl et al. [50] also reported a positive association of plasma CRP levels and self-reported CRF in 61 patients with breast cancer prior to initiation of chemotherapy. In 103 breast cancer survivors, elevated plasma soluble tumor necrosis factor receptor type II (sTNFRII), which is a downstream marker of TNF activity, was associated with persistence of CRF one month after treatment [58]. Breast cancer survivors who received chemotherapy had higher levels of CRF and sTNFRII level compared to those who did not receive chemotherapy. Other studies also reported the positive associations of CRF with CRP [56, 60, 61], IL-6 [62], and IL-1 receptor antagonist [60] in long-term cancer survivors who received any modality of treatment. In addition, cancer survivors with persistent CRF showed increased expression of genes encoding pro-inflammatory cytokines [57, 59]. However, the association of CRF and inflammation markers is not consistent. CRP and IL-1 receptor antagonist were not found in association with CRF in women newly diagnosed with breast cancer [48] or shortly after primary treatment [58]. Also, IL-6 was not correlated with CRF in breast cancer patients prior to chemotherapy [50].
The dysregulation of pro-inflammatory cytokines may influence CRF directly or indirectly. Disruption can occur via the hypothalamic-pituitary-adrenal axis (HPA axis), autonomic nervous system, and circadian rhythm modulation. The HPA axis controls the secretion of cortisol during stress. Bower et al. [63] reported that breast cancer survivors without CRF responded to stress with an increased cortisol level, while those with CRF demonstrated a blunted cortisol response to stress.Circulating cortisol concentration also changes throughout the day based on the circadian rhythm [64]. In a healthy adult, the blood level of cortisol quickly increases after awakening and reaches a peak level 30 min after waking up. This is followed by a decline throughout the day, and the level reaches its minimum at night during sleep [64,65,66].
However, a disrupted circadian rhythm was observed in patients with cancer irrespective of stage or treatment. The disrupted circadian rhythm may be associated with the occurrence of CRF [64, 67, 68]. Studies have shown that patients with cancer and persistent CRF had an altered diurnal cortisol slope and elevated evening cortisol levels during adjuvant therapy [69] and after cancer treatment [70].CRF is also associated with elevated norepinephrine and lower heart rate variability in breast cancer survivors at least two to three months posttreatment [71, 72]. However, these findings are not conclusive, and more studies are warranted to fully understand the relationship between the autonomic nervous system and CRF.
5 Treatment of Cancer-Related Fatigue
Many randomized clinical trials have attempted to treat CRF using interventions such as exercise, psychological therapies, mind-body approaches, pharmacological interventions, and others [43]. In a recent meta-analysis of 113 randomized clinical trials using exercise, psychological, the combination of exercise and psychological, or pharmacological interventions to treat CRF in adult cancer patients and survivors, Mustian et al. [73] demonstrated that exercise, psychological, and the combination of exercise and psychological interventions reduced CRF during and after treatment, whereas pharmacological interventions alone did not reduce CRF. We elaborate on different interventions in the following sections.
5.1 Exercise
Over a dozen systematic reviews and meta-analyses have been conducted to assess the effect of exercise on CRF in adult patients [74,75,76,77,78,79,80,81,82,83,84,85,86], children, and adolescents with cancer [87,88,89] during and after cancer treatment. Overall, supervised aerobic and/or the combination of aerobic and resistance exercise with or without stretching have been found to be effective in reducing CRF , particularly in the domains of general and physical fatigue [76]. The positive impact of exercise on CRF was shown in adult patients with cancer during [75, 76, 82, 85] and after treatment [77, 78, 82, 84]. Given that multiple studies demonstrated the benefits of exercise, the American College of Sports Medicine (ACSM) recommends that patients with cancer and cancer survivors start low and increase to 150 min weekly of moderate intensity or 75 min of vigorous intensity aerobic exercise accompanied by 20–30 min of strength training across all the major muscle groups two to three times with daily stretching [90]. Despite this recommendation, an estimated 70% of cancer survivors do not meet the standard established by the ACSM physical activity guideline [91].
The appropriate exercise mode, intensity, frequency, and duration need to be carefully considered, and an individualized exercise prescription is strongly recommended when discussing exercise with cancer populations. Mustian et al. [92] suggested that exercise prescriptions for cancer patients and survivors should be individualized and tailored based on the individual’s health status, disease trajectory, previous and/or current treatment, symptom burden, current fitness level, past and present exercise participation, and individual preferences to ensure that the exercise is safe and effective. This is illustrated by Tian et al. [77] who reported that supervised aerobic exercise for 50 min/session, two sessions/week for eight weeks, had a moderate effect on CRF, while the same exercise only had a small effect on CRF when it was performed using shorter sessions occurring more frequently: 20–30 min/session, three sessions/week. Clinicians should also consider barriers that cancer patients face in completing exercise and should consider the use of new technologies in improving and tracking exercise adherence [93]. In children and adolescents with cancer, the effects of exercise on CRF are not consistent and are likely due to the lack of rigorous studies [87, 88].
5.2 Psychosocial Therapy
Some meta-analyses have demonstrated that psychosocial therapy has small to moderate effect sizes on CRF reduction relative to a control [73, 94,95,96]. For example, three randomized controlled trials of psychosocial interventions in patients with breast cancer undergoing chemotherapy or radiation therapy who received a three-session individualized CRF education and support program showed improvement in CRF compared to controls [97,98,99]. These benefits were also seen in the posttreatment period. One of the largest trials, The Moving Beyond Cancer Trial, with 418 breast cancer patients who recently (≤ 6 weeks) completed surgery, showed that a 23-min psychoeducational video, which addresses reentry challenges in physical health, emotional well-being, interpersonal relations, and life perspectives, significantly improved CRF six months after the intervention compared to the control group [100].
5.3 Mind-Body Approaches
In recent years, mind-body approaches such as yoga, acupuncture, and meditation have been commonly studied in adult cancer populations for management of CRF [101,102,103,104,105,106,107,108,109,110,111,112,113,114,115,116]. Some studies evaluated the effects of yoga on CRF in patients with cancer receiving chemotherapy or radiotherapy [105, 108, 109, 111, 113, 114]; others investigated the efficacy of yoga on CRF in cancer survivors after the completion of cancer treatment [101,102,103,104, 106, 107, 109,110,111,112, 115, 116]. Eight studies showed that yoga significantly reduced CRF at the end or months after the intervention has been completed compared to the control group, which was usual cancer care [101, 104, 106, 115, 116] or a health education intervention [102, 103, 114]. However, six studies did not find a group difference for the effects of the mind-body intervention on CRF [108,109,110,111,112,113]. These studies are heterogeneous in terms of the type, duration, intensity, frequency, and length of the yoga intervention. Taken together, studies that showed benefits of yoga on CRF reduction suggest that gentle yoga performed in 60- to 120-min sessions, at low to moderate intensity, one to three times per week over a period of four to 12 weeks, may improve CRF in patients with cancer and survivors [117].
In another two studies that evaluated the effect of acupuncture on CRF in 429 patients with a variety of cancer subtypes, authors found patients who received acupuncture had significantly improved CRF compared to patients in the usual care group [118, 119]. However, when acupuncture was compared to sham acupuncture, no difference in CRF was noted [120]. While a number of systematic reviews of acupuncture and its effect on CRF have been conducted [120,121,122,123,125], results are inconsistent. More rigorous randomized control trials are needed.
5.4 Pharmacological Interventions
There have been over 14 randomized trials examining pharmacological interventions, but the evidence supporting their ability to treat CRF among cancer survivors is limited [73]. Existing studies showed mixed findings, often did not use rigorous trial designs, and included only small sample sizes [126]. Modafinil and methylphenidate were most commonly studied. In a randomized controlled trial of 631 patients with mixed cancer types undergoing chemotherapy, only those with severe CRF (score ≥ 7 on the scale of 0–10 in the BFI item 3 “What is your worst level of CRF during the past week?”) benefited from modafinil [127]. In contrast, another randomized controlled trial of 208 patients with non-small cell lung cancer showed that patients who received modafinil demonstrated no improvement in CRF [128]. For methylphenidate, a meta-analysis of five studies [129] suggested possible benefits in three studies [129,130,132] where CRF was evaluated by Functional Assessment for Chronic Illness Therapy-Fatigue (FACIT-F) but not in the other two studies [133, 134] where CRF was measured by BFI. In addition, methylphenidate may be associated with vertigo, anxiety, anorexia, and nausea [129]. Given the limited evidence, most guidelines from professional societies recommend using pharmacologic interventions after ruling out other causes of fatigue or if behavioral interventions have failed.
6 Clinical Practice Guidelines for Cancer-Related Fatigue
The American Society of Clinical Oncology, National Comprehensive Cancer Network, and Pan-Canadian Clinical Practice Guidelines for clinicians and health professionals are summarized in Table 8.2. Each of these guidelines includes recommendations on screening, comprehensive and focused assessment, and treatment options.
6.1 Screening
All healthcare providers should routinely screen for the presence of CRF at the time of initial diagnosis and on subsequent visits, including after the completion of primary treatment. Screening should be performed and documented using a quantitative or semiquantitative , valid, and reliable tool (see Table 8.1) to assess CRF (e.g., asking patients “How would you rate your fatigue on a sale of 0–10 over the past seven days?” from 0 to 10 as 0 = no fatigue and 10 = worse fatigue or using a rating of mild, moderate, or severe).
6.2 Comprehensive and Focused Assessment
History and physical examination , including fatigue history (onset, pattern, duration, changes over time), disease status (progression, recurrence), medication/supplement usage and side effects, social support, and economic status should be incorporated during these visits. Laboratory evaluation, such as complete blood count with differential and comprehensive metabolic panel, should be considered depending on the presence, onset, and severity of CRF as well as the presence of concurrent symptoms such as anemia. Other potential treatable contributing factors including pain, emotional distress, sleep disruption, impaired functional status, medications, nutritional deficits, and comorbidities should also be assessed.
7 Treatment Options
All patients and/or their caregivers should be educated and counseled on the occurrence of CRF. Contributing factors that are identified should be treated accordingly. Non-pharmacological interventions such as exercise, psychosocial therapy, and mind-body approaches could be considered. The evidence for pharmacological interventions is limited and should be used judiciously.
8 Future Directions
As described above, much progress has been made in our understanding of CRF in the past decade. There is now a greater awareness and recognition that CRF is a major concern among cancer patients and survivors and that it is a multidimentional problem. The development of reliable and valid methods to measure CRF have facilitated better communication between healthcare teams and also allowed longitudinal monitoring of CRF. Knowledge in this area has also facilitated the selection of endpoints for clinical trials evaluating interventions targeting CRF. Published clinical trials in CRF have provided us a better understanding of the available options for managing CRF, specifically exercise, psychosocial therapy, and mind-body approaches. With increasing availability of well-conducted studies, multiple clinical practice guidelines have been created for the management of CRF. Lastly, we have an improved understanding of the biobehavioral mechanisms associated with the development of CRF.
Despite the progress, many research gaps exist in the area of CRF. The negative impact of CRF on other outcomes such as healthcare utilization, cost, and survivorship needs to be studied. Although studies have consistently demonstrated the benefits of exercise in CRF, the dose and intensity of exercise remain unclear. Given the multidimentional nature of CRF, a one-size-fits-all approach is likely not sufficient. Combinations of various strategies such as exercise and various psychological or biobehavioral interventions need to be further investigated. With an increasing emphasis of personalized medicine in oncology, it is crucial for us to understand the biobehavioral mechanisms associated with CRF in order to develop individualized interventions for patients and to know for whom and when specific treatments for CRF can be best prescribed. Finally, we need to disseminate the clinical practice guidelines into clinical settings in order to identify patients with CRF and implement these interventions for patients with cancer.
In conclusion, CRF is a common and debilitating toxicity for cancer patients and survivors and can persist for many years after treatment. Many instruments exist for measuring CRF and may be incorporated in the routine assessment of CRF. Exercise and psychological interventions have consistently demonstrated benefits in treating CRF and should be incorporated in the care of cancer patients and survivors.
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Mustian, K.M., Lin, PJ., Loh, K.P., Kleckner, I.R. (2018). Fatigue. In: Feuerstein, M., Nekhlyudov, L. (eds) Handbook of Cancer Survivorship. Springer, Cham. https://doi.org/10.1007/978-3-319-77432-9_8
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