Comprehensive Physiology Wiley Online Library

Exercise Training in Cancer Control and Treatment

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ABSTRACT

Exercise training is playing an increasing role in cancer care, as accumulating evidence demonstrates that exercise may prevent cancer, control disease progression, interact with anti‐cancer therapies, and improve physical functioning and psychosocial outcomes. In this overview article, we present the current state of the field of exercise oncology, which currently comprises of nearly 700 unique exercise intervention trials with more than 50,000 cancer patients. First, we summarize the range of these interventions with regard to diagnoses, clinical setting, timing, and type of intervention. Next, we provide a detailed discussion of the 292 trials, which have delivered structured exercise programs, outlining the impact of exercise training on cancer‐specific, physiological, and psychosocial outcomes in the light of the challenges and physiological limitations cancer patients may experience. In summary, the safety and feasibility of exercise training is firmly established across the cancer continuum, and a wide range of beneficial effects on psychosocial and physiological outcomes are well documented. Many of these beneficial effects are linked to the general health‐promoting properties of exercise. However, it is becoming increasing evident that exercise training can have direct effects on cancer and its treatment. This calls for future exercise oncology initiatives, which aim to target cancer‐specific outcomes, and which are integrated into the concurrent cancer trajectory. Here, the field must bridge extensive knowledge of integrative exercise physiology with clinical oncology and cancer biology to provide a basis of individualized targeted approaches, which may place exercise training as an integrated component of standard cancer care. © 2019 American Physiological Society. Compr Physiol 9:165‐205, 2019.

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Figure 1. Figure 1. Historic overview of exercise intervention studies in cancer patients. Here, the time course of the number of published exercise intervention studies in cancer patients is presented. Seminal clinical exercise intervention trials are highlighted in black at the time of publication. Other important contributions to the field are inserted in blue, including the first publication of exercise guidelines in cancer patients, the first epidemiological evidence for a protective effect of exercise on relapse and mortality in cancer patients, and the first major review to summarize the role of exercise‐dependent regulation of systemic cancer risk factors.
Figure 2. Figure 2. Flowchart of the screening process for exercise intervention studies. The figure provides an overview of the screening process for exercise intervention studies. Presented first is the total number of PubMed indexed studies (n = 9616) identified using our search string. The total number of studies were screened on title and abstract for studies utilizing exercise and physical activity interventions, which resulted in 679 studies. Next, we differentiated between studies applying structured exercise interventions and physical activity interventions. Exercise interventions were defined as structured, planned, and repetitive interventions aiming to maintain or improve physical fitness. Thus, studies, which did not provide a description of the exercise protocol, were excluded. Furthermore, we excluded studies applying multimodal interventions (e.g., combined exercise and diet interventions), counseling‐based physical activity studies, holistic training including yoga or tai chi and other preference‐based interventions. Based on these inclusion criteria, 292 unique exercise intervention studies were identified. For both exercise training intervention studies (n = 292), and the excluded studies (n = 387), we determined the number of specific intervention arms evaluated (note: the number of intervention arms do not add up to the total number of studies as some studies included more than one intervention arm).
Figure 3. Figure 3. Overview of exercise intervention studies across the cancer trajectory. The figure illustrates the number of exercise intervention trials performed according to diagnosis. Further, trials are subcategorized by timing relative to primary treatments. We distinguish between four overall clinical settings: (i) exercise interventions prescribed before surgery as preoperative optimization, (ii) exercise interventions prescribed during systemic adjuvant therapies for patients treated with curative intend, (iii) exercise interventions prescribed after completion of curative and/or adjuvant therapy, and (iv) exercise interventions prescribed for patients with metastatic cancer with or without concurrent palliative treatment. aFor studies in prostate cancer, systemic/adjuvant treatment includes radiotherapy and androgen deprivation therapy without surgery in patient with local or locally advanced stage disease.bFor blood cancers, adjuvant/systemic treatment includes high dose chemotherapy prior to or during inpatient chemotherapy after allogenic stem cell transplantation in the vast majority of studies.
Figure 4. Figure 4. Summary of the outcomes measured in exercise‐oncology trials. Here, we present an overview of the number of different outcomes reported in the 292 unique exercise intervention studies, which examined the effects of structured exercise programs identified in our PubMed search. Overall, we divide these outcomes into four different categories: (i) cancer‐specific outcomes, that is, survival, disease progression, regulation of tumor markers, and treatment tolerability; (ii) secondary prevention outcomes, that is, cardiotoxicities, body weight, body composition, sex hormone levels, insulin levels, and immune function; (iii) exercise‐specific physiological outcomes, that is, cardiopulmonary fitness and muscle function; and (iv) psychosocial outcomes, that is, health‐related quality of life (HRQoL), depression, and cancer‐related fatigue.
Figure 5. Figure 5. Factors linking exercise training to cancer survival. The association between exercise behavior and cancer prognosis is well established, and this protective role is likely mediated by a wide range of exercise‐dependent responses. Here, we outline three interrelated modes‐of‐action, through which exercise training may directly or indirectly influence the prognostic outlook following a cancer diagnosis. Exercise training may influence the risk of clinical disease progression, evaluated by disease‐free survival or surrogate tumor markers, by imposing direct antiproliferative actions on residual tumor cells. In addition, exercise training may interact with the impact of standard treatment in different settings including preoperative optimization, improvement of treatment tolerability and/or enhancement of antineoplastic efficacy. Finally, exercise training can play a critical role in secondary prevention of acute‐ and late‐occurring detrimental health‐effects associated with cancer and its’ treatments, including protection from cardiotoxicity, weight gain, metabolic disturbances, and dysregulation of systemic cancer risk factors.
Figure 6. Figure 6. Mechanisms involved in exercise‐dependent control of tumor growth. Evidence from preclinical studies indicates that exercise can reduce tumor growth and inhibit metastasis through various mechanistic pathways. Exercise is associated with an acute mobilization and redistribution of cytotoxic immune cells, Natural Killer (NK)‐Cells to malignant tumors. Exercise is also associated with the release of antioncogenic myokines from contracting muscles. Finally, exercise‐derived increase in epinephrine is shown to activate the ‘Hippo Tumor Suppressor’ signaling pathway in tumor cells, which in particular has been found to inhibit the formation of new malignant tumors associated with the metastatic process.
Figure 7. Figure 7. Exercise‐dependent regulation of the Hippo signaling pathway. The Hippo signaling pathway is involved in basal processes like cellular growth, differentiation, and apoptosis, and is particularly recognized for its role in tissue development. The Hippo signaling pathway comprise of the oncoproteins Yap and Taz, which in the activated state, will translocate to the nucleus and induce transcription of factors involved in cell proliferation, antiapoptosis, and metastasis. However, upon phosphorylation by Lats1/2, Yap, and Taz are retained in the cytosol and degraded. This inactivation and degradation of Yap and Taz will reduce the rate of tumor metastasis. The Hippo signaling pathway has been shown to be dysregulated in several types of cancer, including breast cancer, where activation of the oncoproteins YAP/TAZ have been associated with a poor prognosis. Exercise can regulate the Hippo signaling pathway, as exercise‐induced epinephrine can induce phosphorylation and degradation of Yap and Taz, and this has in mice been shown to reduce tumor formation by 50%.
Figure 8. Figure 8. Exercise‐dependent regulation of immune cells. Several studies have reported that patients allocated to exercise training were either more likely to receive their planned dosage of chemotherapy or reported fewer toxicities compared with usual care controls. This observation has coincided with maintenance of the patients’ immune cells population, that is, the patient experienced lower incidence of neutropenia, trombopenia, and lymphopenia, which are principle causes of chemotherapy dose reduction and/or postponement. During exercise, immune cells are acutely mobilized to the circulation through adrenergic signaling and shear stress on the vascular bed induced by the increased blood flow during exercise. The most responsive immune cells are NK cells and monocytes, followed by T cells and to a lesser extent B cells. Once mobilized, the immune cells will be distributed to the peripheral tissue to survey for malignant transformed or virus infected cells. This exercise‐mediated mobilization and redistribution of immune cells will provide yet unidentified signals to the bone marrow to initiate the production of new immune cells, which are released to the circulation and stored in the spleen and lymph nodes. This exercise‐mediated feedback loop to the bone marrow may explain why cancer patients can maintain their immune cell population despite receiving bone marrow suppressive anti‐cancer treatment.
Figure 9. Figure 9. Drug compartmentalization in untrained and trained individuals. Systemic treatments with chemotherapy or immunotherapy are associated with toxicities and organ damage in a dose‐dependent manner. Importantly, systemic treatments are administered by anthropometrics, that is, body mass or body surface area, which do not take into account the relative composition of fat and fat‐free mass. Since cancer drugs is distributed in metabolically active tissues only, it has been proposed that obesity alone, and in particular in combination with low muscle mass, known as sarcopenic obesity, is associated with higher risk of toxicity induced dose reduction. This figure illustrates the hypothetical distribution of the same absolute dosage, administered to two individuals with the same body mass/surface area, but different distribution of fat and muscle, as often observed in untrained (high fat mass, low muscle mass) and training individuals (low fat mass, high muscle mass). The “relative” dose encountered in thus metabolically (fat free) active tissue is thus higher in the untrained, relative to the trained individual, who are distributing the same dose to a larger fat‐free mass.
Figure 10. Figure 10. Exercise‐mediated enhancement of anti‐cancer therapy efficacy. Data from clinical trials and preclinical experiments suggest that exercise training may enhance the antineoplastic efficacy of traditional cancer treatments including radiotherapy, chemotherapy, and immunotherapy. The principle candidate mechanism responsible for this synergistic effect is increased vascularization leading to improved intratumoral blood perfusion. Such increase in blood perfusion by exercise training has been demonstrated in murine studies, where acute exercise directly can blood perfusion, while long‐term training has been associated with increased vascularization, normalization of capillary perfusion and reduction in tumor hypoxia. Together, this can improve the anti‐cancer efficacy by (i) increasing the delivery capacity of drugs, for example, chemotherapy to the interior of the tumor, (ii) improving oxygenation of the interior of the tumor, which is required for the generation of reactive oxidative species (ROS) in radiotherapy, and (iii) increasing intratumoral immune cell infiltration, which are required for removal of dead cells after cytotoxic treatment, as well as for interaction with immunotherapy.
Figure 11. Figure 11. Conceptual model of the possible interaction between exercise training and cancer treatment. In pharmacology, the therapeutic window is determined by the dosage range interval from the “median effective dose” (ED50), defined as the dose achieving a positive response in 50% of the patients, and the “median toxic dose” (TD50) defined as the dose resulting in toxicity (here arbitrarily defined) in 50% of the patients. The lower limit of this therapeutic window is therefore determined by the antineoplastic potency of the treatment, that is, the more potent the agent, the higher tumor response to the same absolute dose. The upper limit of the window is, on the other hand, determined by the drug toxicity profile, that is, the adverse cytotoxic reactions in nontargeted tissues (e.g., the lungs, kidneys or bone marrow). Through direct and indirect mechanisms, exercise training may widen the therapeutic window. Exercise‐induced improvement in blood perfusion, and thus improved drug delivery, less intratumoral hypoxia and higher invasion of cytotoxic immune cells, potentially shirts the treatment efficacy curve to the left eliciting a higher tumor response to the same dose or similar response at a lower dose. In parallel, exercise‐dependent improvements in treatment toxicity profile by protection against immunosuppression and improved drug compartmentalization (distribution of the toxic agents a to larger mass of metabolic active tissue) may shift the toxicity curve to the right, thus improving treatment tolerability by lower toxicity profile to the same absolute dose or allowing for similar toxicity profile to a higher dose. In concert, this interaction between exercise training and standard therapies can have profound impact on patient management in both adjuvant and palliative settings, but requires full integration of the exercise intervention within standard oncology therapeutic framework regarding prescription, delivery, and evaluation.
Figure 12. Figure 12. Exercise‐dependent regulation of cardiopulmonary fitness (VO2peak) in cancer patients. VO2peak is determined as the maximum capacity to deliver oxygen to the working muscles, and requires integration of multiple steps known as the oxygen cascade. Here, we outline the various limiting steps in oxygen cascade in cancer patient with regard to the training‐time required for exercise‐dependent adaptation, as well as cancer‐specific pathophysiological impairments in the response potential. The first step involves the oxygen saturation of the blood as a result of pulmonary diffusion capacity from the atmospheric air in the lungs to the blood in the alveoli. This step is extremely rarely a limiting factor for maximum oxygen uptake, but may be significantly hampered in the event of thoracic surgery. The next step involves the capacity to distribute oxygenated blood to the metabolic active tissues. The maximum cardiac output (liters of blood per minute) is determined by the maximum heart rate and the stroke volume of the heart, of which only stroke volume is considered trainable healthy subjects. Cardiac output is a well‐established limiting factor of cardiopulmonary fitness in sedentary and recreationally active humans, and constitutes a robust exercise adaptation within days to weeks of commencing an aerobic exercise program. However, various cancer drugs and/or irradiation to closely situated tumors (e.g., thoracic or mammary irradiation) can cause cardiotoxicity in the form of various limiting symptoms including cardiomyopathy, inhibiting the capacity to improve stroke volume. Another key determinant of cardiac output is the total blood volume (in liters), which consists of total plasma volume and red blood cell volume. Integrative physiology research has shown a close correlation between changes in blood volume, especially red blood cell volume, with changes in VO2peak, and elegant phlebotomy experiments have found that exercise‐induced improvements in VO2peak is abolished when the increase in blood volume is normalized to pretraining levels. Exercise‐induced regulation of blood volume in cancer patients has to our knowledge never been examined and may to some extend explain the lack of robust increases in VO2peak, as normally observed in healthy individuals. Indeed, a number of treatment‐related pathophysiological changes may impact, and reduce, particularly red cell blood volume by bone marrow toxicity and/or dehydration due to nephrotoxicity. Finally, extraction of oxygen from the capillaries to the muscle cells and mitochondrial metabolic turnover rate comprise the last steps of the oxygen cascade. The capillary density, that is, “the cross sectional muscle area supply by one capillary” as well as oxidative enzymes are key regulators of intramuscular oxygen utilization, and while these are rarely considered limiting factors for VO2peak, as they show robust adaptations to exercise in healthy individuals. In patients with cancer, few studies have examined muscular toxicities, but a number of common symptoms, for example, muscular pain from taxanes, which is considered a result of serious muscular inflammation may be so severe, at least in the acute treatment phase, that they significantly limit maximum aerobic exercise performance irrespective of the oxygen delivery capacity.
Figure 13. Figure 13. Regulation of muscle function in cancer patients. Overall maximum contractile muscle strength is determined by anatomical features especially the cross‐sectional area (mass) and pennation angle, and a neural component, that is, recruitment and synchronization of motor‐units. The vast majority of resistance training trials performed in cancer patients have found a significant increase in contractile strength, whereas changes in muscle architecture, which have mostly been evaluated by whole‐body and appendicular lean mass, have yielded ambiguous results especially in studies performed during active treatment. One explanation for this apparent lack of muscular adaptation may stem from the relative short duration of most exercise interventions (from 4 to 16 weeks), and the possible counteracting impact of cytotoxic or antiandrogenic treatments, which may impair protein synthesis and/or enhance protein degradation signal in skeletal muscle. Although, this limited or inhibited hypertrophic exercise‐response may discourage the clinical application of resistance training in cancer patients, it is important to acknowledge the almost unanimous improvements in muscle strength, irrespective of changes in muscle mass, are reported in almost every exercise intervention studies in cancer patients, including advance stage lung cancer patients and patients treated for head and neck cancer, who are subject to massive muscle wasting due to nutritional deficits.
Figure 14. Figure 14. Exercise reduce depression through regulation of kynurenine metabolism. Exercise training has consistently been shown to reduce symptoms of depression in cancer patients. Recently, a mechanism to explain how exercise can regulate symptoms of depression at the molecular level was proposed involving regulation of the Kynurenine degradation products. Degradation of Kynurenine follows one of two possible pathways: Kynurenine is either converted to nicotinamide adenine dinucleotide (NAD) or anthranilic acid through kynurenine 3‐monooxygenase (KMO); or converted to kynurenic acid by kynurenine aminotransferases (KATs). The Kyn‐NAD pathway is induced by inflammation, which might occur secondary to chemotherapy in muscles of cancer patients. This transformation leads to production of quinolinic acid, a potent NMDA receptor agonist leading to excitotoxicity in the central nervous system. Kynurenic acid, on the other hand, is neuroprotective, acting as an antagonist of the NDMA‐receptor and thereby counteracting the neurotoxic effects of quinolinic acid. Moreover, kynurenic acid cannot cross the blood‐brain‐barrier, so the conversion of kynurenine to kynurenic acid in the periphery can reduce accumulation of kynurenine in central nervous system. The imbalance between these neuroprotective and neurotoxic metabolites has been proposed to be critical for development of symptoms of depression.
Figure 15. Figure 15. The exercise continuum for cancer patients. Exercise training interventions are often divided into distinct categories, typically described as resistance training using weights or fitness machines, and aerobic training using, for example, treadmills and stationary bikes, based on basic exercise physiology outlining that different exercise stimuli elicit different responses to different organ systems. However, all exercise interventions essentially consist of voluntary muscular contractions performed in a manner determined by a continuous relationship between (A) the external load and/or internal energy turnover rate, and (B) the duration of the active work period. Here, we have exemplified five modes of exercise training on the (duration‐intensity) continuum with regard to the duration of active work period and the corresponding relative load/intensity, as well as the required work‐to‐rest time frame‐ratio, and the main physiological stimulus and response. This ranges from maximum muscle force‐generation performed against high external loads for just a few seconds known as “power training” to very light repetitive contractions performed for up to several hours as endurance training. Naturally, targeted exercise prescriptions stimulate different organ systems with different effectiveness and thus can be applied if specific adaptations are warranted, but it is important to emphasize that all physical exercise interventions involve physiological challenges of the entire continuum. By proper application of the principles of training, this internal feature can be utilized advantageously, when prescribing exercise training for patients with cancer. Most importantly, it provides a unique opportunity for individualization of an exercise program according to patient preferences and/or limitations, and the recognition of the individual's physical capacity, for example, for elderly, frail patients a structured walking intervention can comprise a relatively high‐intensity exercise stressing both the oxygen cascade and neuromuscular components. This view of exercise training may also take into consideration training periodization as certain activities may be unfavorable during certain periods in the cancer trajectory. For example, patients who are seriously symptom‐burdened during cytotoxic treatment phases may be precluded from performing exercise with highly elevated heart rate and blood pressure associated with high‐intensity exercise, but may tolerate lower intensity for a longer duration. Or they may contrarily prefer short‐term, high‐load activity with high‐intensity interval training (HIIT) or heavy resistance training, which can be concluded in short sessions. Abbreviations: RM, repetition maximum; MVC, maximum voluntary contraction; RFD, rate of force development; ATP, adenosine triphosphate.


Figure 1. Historic overview of exercise intervention studies in cancer patients. Here, the time course of the number of published exercise intervention studies in cancer patients is presented. Seminal clinical exercise intervention trials are highlighted in black at the time of publication. Other important contributions to the field are inserted in blue, including the first publication of exercise guidelines in cancer patients, the first epidemiological evidence for a protective effect of exercise on relapse and mortality in cancer patients, and the first major review to summarize the role of exercise‐dependent regulation of systemic cancer risk factors.


Figure 2. Flowchart of the screening process for exercise intervention studies. The figure provides an overview of the screening process for exercise intervention studies. Presented first is the total number of PubMed indexed studies (n = 9616) identified using our search string. The total number of studies were screened on title and abstract for studies utilizing exercise and physical activity interventions, which resulted in 679 studies. Next, we differentiated between studies applying structured exercise interventions and physical activity interventions. Exercise interventions were defined as structured, planned, and repetitive interventions aiming to maintain or improve physical fitness. Thus, studies, which did not provide a description of the exercise protocol, were excluded. Furthermore, we excluded studies applying multimodal interventions (e.g., combined exercise and diet interventions), counseling‐based physical activity studies, holistic training including yoga or tai chi and other preference‐based interventions. Based on these inclusion criteria, 292 unique exercise intervention studies were identified. For both exercise training intervention studies (n = 292), and the excluded studies (n = 387), we determined the number of specific intervention arms evaluated (note: the number of intervention arms do not add up to the total number of studies as some studies included more than one intervention arm).


Figure 3. Overview of exercise intervention studies across the cancer trajectory. The figure illustrates the number of exercise intervention trials performed according to diagnosis. Further, trials are subcategorized by timing relative to primary treatments. We distinguish between four overall clinical settings: (i) exercise interventions prescribed before surgery as preoperative optimization, (ii) exercise interventions prescribed during systemic adjuvant therapies for patients treated with curative intend, (iii) exercise interventions prescribed after completion of curative and/or adjuvant therapy, and (iv) exercise interventions prescribed for patients with metastatic cancer with or without concurrent palliative treatment. aFor studies in prostate cancer, systemic/adjuvant treatment includes radiotherapy and androgen deprivation therapy without surgery in patient with local or locally advanced stage disease.bFor blood cancers, adjuvant/systemic treatment includes high dose chemotherapy prior to or during inpatient chemotherapy after allogenic stem cell transplantation in the vast majority of studies.


Figure 4. Summary of the outcomes measured in exercise‐oncology trials. Here, we present an overview of the number of different outcomes reported in the 292 unique exercise intervention studies, which examined the effects of structured exercise programs identified in our PubMed search. Overall, we divide these outcomes into four different categories: (i) cancer‐specific outcomes, that is, survival, disease progression, regulation of tumor markers, and treatment tolerability; (ii) secondary prevention outcomes, that is, cardiotoxicities, body weight, body composition, sex hormone levels, insulin levels, and immune function; (iii) exercise‐specific physiological outcomes, that is, cardiopulmonary fitness and muscle function; and (iv) psychosocial outcomes, that is, health‐related quality of life (HRQoL), depression, and cancer‐related fatigue.


Figure 5. Factors linking exercise training to cancer survival. The association between exercise behavior and cancer prognosis is well established, and this protective role is likely mediated by a wide range of exercise‐dependent responses. Here, we outline three interrelated modes‐of‐action, through which exercise training may directly or indirectly influence the prognostic outlook following a cancer diagnosis. Exercise training may influence the risk of clinical disease progression, evaluated by disease‐free survival or surrogate tumor markers, by imposing direct antiproliferative actions on residual tumor cells. In addition, exercise training may interact with the impact of standard treatment in different settings including preoperative optimization, improvement of treatment tolerability and/or enhancement of antineoplastic efficacy. Finally, exercise training can play a critical role in secondary prevention of acute‐ and late‐occurring detrimental health‐effects associated with cancer and its’ treatments, including protection from cardiotoxicity, weight gain, metabolic disturbances, and dysregulation of systemic cancer risk factors.


Figure 6. Mechanisms involved in exercise‐dependent control of tumor growth. Evidence from preclinical studies indicates that exercise can reduce tumor growth and inhibit metastasis through various mechanistic pathways. Exercise is associated with an acute mobilization and redistribution of cytotoxic immune cells, Natural Killer (NK)‐Cells to malignant tumors. Exercise is also associated with the release of antioncogenic myokines from contracting muscles. Finally, exercise‐derived increase in epinephrine is shown to activate the ‘Hippo Tumor Suppressor’ signaling pathway in tumor cells, which in particular has been found to inhibit the formation of new malignant tumors associated with the metastatic process.


Figure 7. Exercise‐dependent regulation of the Hippo signaling pathway. The Hippo signaling pathway is involved in basal processes like cellular growth, differentiation, and apoptosis, and is particularly recognized for its role in tissue development. The Hippo signaling pathway comprise of the oncoproteins Yap and Taz, which in the activated state, will translocate to the nucleus and induce transcription of factors involved in cell proliferation, antiapoptosis, and metastasis. However, upon phosphorylation by Lats1/2, Yap, and Taz are retained in the cytosol and degraded. This inactivation and degradation of Yap and Taz will reduce the rate of tumor metastasis. The Hippo signaling pathway has been shown to be dysregulated in several types of cancer, including breast cancer, where activation of the oncoproteins YAP/TAZ have been associated with a poor prognosis. Exercise can regulate the Hippo signaling pathway, as exercise‐induced epinephrine can induce phosphorylation and degradation of Yap and Taz, and this has in mice been shown to reduce tumor formation by 50%.


Figure 8. Exercise‐dependent regulation of immune cells. Several studies have reported that patients allocated to exercise training were either more likely to receive their planned dosage of chemotherapy or reported fewer toxicities compared with usual care controls. This observation has coincided with maintenance of the patients’ immune cells population, that is, the patient experienced lower incidence of neutropenia, trombopenia, and lymphopenia, which are principle causes of chemotherapy dose reduction and/or postponement. During exercise, immune cells are acutely mobilized to the circulation through adrenergic signaling and shear stress on the vascular bed induced by the increased blood flow during exercise. The most responsive immune cells are NK cells and monocytes, followed by T cells and to a lesser extent B cells. Once mobilized, the immune cells will be distributed to the peripheral tissue to survey for malignant transformed or virus infected cells. This exercise‐mediated mobilization and redistribution of immune cells will provide yet unidentified signals to the bone marrow to initiate the production of new immune cells, which are released to the circulation and stored in the spleen and lymph nodes. This exercise‐mediated feedback loop to the bone marrow may explain why cancer patients can maintain their immune cell population despite receiving bone marrow suppressive anti‐cancer treatment.


Figure 9. Drug compartmentalization in untrained and trained individuals. Systemic treatments with chemotherapy or immunotherapy are associated with toxicities and organ damage in a dose‐dependent manner. Importantly, systemic treatments are administered by anthropometrics, that is, body mass or body surface area, which do not take into account the relative composition of fat and fat‐free mass. Since cancer drugs is distributed in metabolically active tissues only, it has been proposed that obesity alone, and in particular in combination with low muscle mass, known as sarcopenic obesity, is associated with higher risk of toxicity induced dose reduction. This figure illustrates the hypothetical distribution of the same absolute dosage, administered to two individuals with the same body mass/surface area, but different distribution of fat and muscle, as often observed in untrained (high fat mass, low muscle mass) and training individuals (low fat mass, high muscle mass). The “relative” dose encountered in thus metabolically (fat free) active tissue is thus higher in the untrained, relative to the trained individual, who are distributing the same dose to a larger fat‐free mass.


Figure 10. Exercise‐mediated enhancement of anti‐cancer therapy efficacy. Data from clinical trials and preclinical experiments suggest that exercise training may enhance the antineoplastic efficacy of traditional cancer treatments including radiotherapy, chemotherapy, and immunotherapy. The principle candidate mechanism responsible for this synergistic effect is increased vascularization leading to improved intratumoral blood perfusion. Such increase in blood perfusion by exercise training has been demonstrated in murine studies, where acute exercise directly can blood perfusion, while long‐term training has been associated with increased vascularization, normalization of capillary perfusion and reduction in tumor hypoxia. Together, this can improve the anti‐cancer efficacy by (i) increasing the delivery capacity of drugs, for example, chemotherapy to the interior of the tumor, (ii) improving oxygenation of the interior of the tumor, which is required for the generation of reactive oxidative species (ROS) in radiotherapy, and (iii) increasing intratumoral immune cell infiltration, which are required for removal of dead cells after cytotoxic treatment, as well as for interaction with immunotherapy.


Figure 11. Conceptual model of the possible interaction between exercise training and cancer treatment. In pharmacology, the therapeutic window is determined by the dosage range interval from the “median effective dose” (ED50), defined as the dose achieving a positive response in 50% of the patients, and the “median toxic dose” (TD50) defined as the dose resulting in toxicity (here arbitrarily defined) in 50% of the patients. The lower limit of this therapeutic window is therefore determined by the antineoplastic potency of the treatment, that is, the more potent the agent, the higher tumor response to the same absolute dose. The upper limit of the window is, on the other hand, determined by the drug toxicity profile, that is, the adverse cytotoxic reactions in nontargeted tissues (e.g., the lungs, kidneys or bone marrow). Through direct and indirect mechanisms, exercise training may widen the therapeutic window. Exercise‐induced improvement in blood perfusion, and thus improved drug delivery, less intratumoral hypoxia and higher invasion of cytotoxic immune cells, potentially shirts the treatment efficacy curve to the left eliciting a higher tumor response to the same dose or similar response at a lower dose. In parallel, exercise‐dependent improvements in treatment toxicity profile by protection against immunosuppression and improved drug compartmentalization (distribution of the toxic agents a to larger mass of metabolic active tissue) may shift the toxicity curve to the right, thus improving treatment tolerability by lower toxicity profile to the same absolute dose or allowing for similar toxicity profile to a higher dose. In concert, this interaction between exercise training and standard therapies can have profound impact on patient management in both adjuvant and palliative settings, but requires full integration of the exercise intervention within standard oncology therapeutic framework regarding prescription, delivery, and evaluation.


Figure 12. Exercise‐dependent regulation of cardiopulmonary fitness (VO2peak) in cancer patients. VO2peak is determined as the maximum capacity to deliver oxygen to the working muscles, and requires integration of multiple steps known as the oxygen cascade. Here, we outline the various limiting steps in oxygen cascade in cancer patient with regard to the training‐time required for exercise‐dependent adaptation, as well as cancer‐specific pathophysiological impairments in the response potential. The first step involves the oxygen saturation of the blood as a result of pulmonary diffusion capacity from the atmospheric air in the lungs to the blood in the alveoli. This step is extremely rarely a limiting factor for maximum oxygen uptake, but may be significantly hampered in the event of thoracic surgery. The next step involves the capacity to distribute oxygenated blood to the metabolic active tissues. The maximum cardiac output (liters of blood per minute) is determined by the maximum heart rate and the stroke volume of the heart, of which only stroke volume is considered trainable healthy subjects. Cardiac output is a well‐established limiting factor of cardiopulmonary fitness in sedentary and recreationally active humans, and constitutes a robust exercise adaptation within days to weeks of commencing an aerobic exercise program. However, various cancer drugs and/or irradiation to closely situated tumors (e.g., thoracic or mammary irradiation) can cause cardiotoxicity in the form of various limiting symptoms including cardiomyopathy, inhibiting the capacity to improve stroke volume. Another key determinant of cardiac output is the total blood volume (in liters), which consists of total plasma volume and red blood cell volume. Integrative physiology research has shown a close correlation between changes in blood volume, especially red blood cell volume, with changes in VO2peak, and elegant phlebotomy experiments have found that exercise‐induced improvements in VO2peak is abolished when the increase in blood volume is normalized to pretraining levels. Exercise‐induced regulation of blood volume in cancer patients has to our knowledge never been examined and may to some extend explain the lack of robust increases in VO2peak, as normally observed in healthy individuals. Indeed, a number of treatment‐related pathophysiological changes may impact, and reduce, particularly red cell blood volume by bone marrow toxicity and/or dehydration due to nephrotoxicity. Finally, extraction of oxygen from the capillaries to the muscle cells and mitochondrial metabolic turnover rate comprise the last steps of the oxygen cascade. The capillary density, that is, “the cross sectional muscle area supply by one capillary” as well as oxidative enzymes are key regulators of intramuscular oxygen utilization, and while these are rarely considered limiting factors for VO2peak, as they show robust adaptations to exercise in healthy individuals. In patients with cancer, few studies have examined muscular toxicities, but a number of common symptoms, for example, muscular pain from taxanes, which is considered a result of serious muscular inflammation may be so severe, at least in the acute treatment phase, that they significantly limit maximum aerobic exercise performance irrespective of the oxygen delivery capacity.


Figure 13. Regulation of muscle function in cancer patients. Overall maximum contractile muscle strength is determined by anatomical features especially the cross‐sectional area (mass) and pennation angle, and a neural component, that is, recruitment and synchronization of motor‐units. The vast majority of resistance training trials performed in cancer patients have found a significant increase in contractile strength, whereas changes in muscle architecture, which have mostly been evaluated by whole‐body and appendicular lean mass, have yielded ambiguous results especially in studies performed during active treatment. One explanation for this apparent lack of muscular adaptation may stem from the relative short duration of most exercise interventions (from 4 to 16 weeks), and the possible counteracting impact of cytotoxic or antiandrogenic treatments, which may impair protein synthesis and/or enhance protein degradation signal in skeletal muscle. Although, this limited or inhibited hypertrophic exercise‐response may discourage the clinical application of resistance training in cancer patients, it is important to acknowledge the almost unanimous improvements in muscle strength, irrespective of changes in muscle mass, are reported in almost every exercise intervention studies in cancer patients, including advance stage lung cancer patients and patients treated for head and neck cancer, who are subject to massive muscle wasting due to nutritional deficits.


Figure 14. Exercise reduce depression through regulation of kynurenine metabolism. Exercise training has consistently been shown to reduce symptoms of depression in cancer patients. Recently, a mechanism to explain how exercise can regulate symptoms of depression at the molecular level was proposed involving regulation of the Kynurenine degradation products. Degradation of Kynurenine follows one of two possible pathways: Kynurenine is either converted to nicotinamide adenine dinucleotide (NAD) or anthranilic acid through kynurenine 3‐monooxygenase (KMO); or converted to kynurenic acid by kynurenine aminotransferases (KATs). The Kyn‐NAD pathway is induced by inflammation, which might occur secondary to chemotherapy in muscles of cancer patients. This transformation leads to production of quinolinic acid, a potent NMDA receptor agonist leading to excitotoxicity in the central nervous system. Kynurenic acid, on the other hand, is neuroprotective, acting as an antagonist of the NDMA‐receptor and thereby counteracting the neurotoxic effects of quinolinic acid. Moreover, kynurenic acid cannot cross the blood‐brain‐barrier, so the conversion of kynurenine to kynurenic acid in the periphery can reduce accumulation of kynurenine in central nervous system. The imbalance between these neuroprotective and neurotoxic metabolites has been proposed to be critical for development of symptoms of depression.


Figure 15. The exercise continuum for cancer patients. Exercise training interventions are often divided into distinct categories, typically described as resistance training using weights or fitness machines, and aerobic training using, for example, treadmills and stationary bikes, based on basic exercise physiology outlining that different exercise stimuli elicit different responses to different organ systems. However, all exercise interventions essentially consist of voluntary muscular contractions performed in a manner determined by a continuous relationship between (A) the external load and/or internal energy turnover rate, and (B) the duration of the active work period. Here, we have exemplified five modes of exercise training on the (duration‐intensity) continuum with regard to the duration of active work period and the corresponding relative load/intensity, as well as the required work‐to‐rest time frame‐ratio, and the main physiological stimulus and response. This ranges from maximum muscle force‐generation performed against high external loads for just a few seconds known as “power training” to very light repetitive contractions performed for up to several hours as endurance training. Naturally, targeted exercise prescriptions stimulate different organ systems with different effectiveness and thus can be applied if specific adaptations are warranted, but it is important to emphasize that all physical exercise interventions involve physiological challenges of the entire continuum. By proper application of the principles of training, this internal feature can be utilized advantageously, when prescribing exercise training for patients with cancer. Most importantly, it provides a unique opportunity for individualization of an exercise program according to patient preferences and/or limitations, and the recognition of the individual's physical capacity, for example, for elderly, frail patients a structured walking intervention can comprise a relatively high‐intensity exercise stressing both the oxygen cascade and neuromuscular components. This view of exercise training may also take into consideration training periodization as certain activities may be unfavorable during certain periods in the cancer trajectory. For example, patients who are seriously symptom‐burdened during cytotoxic treatment phases may be precluded from performing exercise with highly elevated heart rate and blood pressure associated with high‐intensity exercise, but may tolerate lower intensity for a longer duration. Or they may contrarily prefer short‐term, high‐load activity with high‐intensity interval training (HIIT) or heavy resistance training, which can be concluded in short sessions. Abbreviations: RM, repetition maximum; MVC, maximum voluntary contraction; RFD, rate of force development; ATP, adenosine triphosphate.
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Supplementary material 1: Search strategy

J. F. Christensen, C. Simonsen, P. Hojman. Exercise Training in Cancer Control and Treatment. Compr Physiol 9: 2019, 165-205.

Listed below is the search terms used to identify PubMed Indexed exercise studies. The search was performed in title and abstract as well as in MeSH terms. All the search terms related to training was combined using the “OR” function. Similarly, the search terms related to cancer was combined using “OR”. Then the full search was perfumed using the AND function combining all identified studies related to training with the studies identified related to cancer. The search was performed in PubMed 22nd of February 2018.

Search terms related to training

  • Exercise[mh]
  • “exercise training”[tiab]
  • “exercise therapy”[tiab]
  • “exercise therapies”[tiab]
  • “exercise intervention”[tiab]
  • “exercise program”[tiab]
  • “exercise programme”[tiab]
  • “physical exercise”[tiab]
  • “physical exercises”[tiab]
  • “training intervention”[tiab]
  • “training interventions”[tiab]
  • “training programme”[tiab]
  • “training program”[tiab]
  • ”resistance training”[tiab]
  • “resistance exercise”[tiab]
  • “resistance exercises”[tiab]
  • “muscle training”[tiab]
  • “strength training”[tiab]
  • “weight training”[tiab]
  • “weight lifting”[tiab]
  • “strengthening program”[tiab]
  • “strengthening programs”[tiab]
  • ”aerobic exercise”[tiab]
  • ”aerobic exercises”[tiab]
  • “aerobic interval training”[tiab]
  • “aerobic training”[tiab]
  • “high-intensity interval training”[tiab]
  • “cardiovascular training”[tiab]
  • “Interval training”[tiab]
  • walking[tiab]
  • walking[mh]
  • Exercise therapy[mh]
  • prehabilitation[tiab]
  • rehabilitation[tiab]
  • Sports[mh]
  • Exercise Movement Techniques[mh]

Search terms related to cancer

 

  • cancer[tiab]
  • neoplasms by site[mh]
  • cancer survivors[mh]
  • “Neoplasms/rehabilitation”[MAJR]

 

Supplementary material 2: Exercise studies in cancer patients

J. F. Christensen, C. Simonsen, P. Hojman. Exercise Training in Cancer Control and Treatment. Compr Physiol 9: 2019, 165-205.

Result of the search for exercise intervention studies in cancer patients. The articles listed below were identified using the search string available in Supplementary material 1.

  1. Adams SC, DeLorey DS, Davenport MH, Stickland MK, Fairey AS, North S, et al. Effects of high-intensity aerobic interval training on cardiovascular disease risk in testicular cancer survivors: A phase 2 randomized controlled trial. Cancer. 2017;123(20):4057-65.
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Teaching Material

J. F. Christensen, C. Simonsen, P. Hojman. Exercise Training in Cancer Control and Treatment. Compr Physiol 9: 2019, 165-205.

Didactic Synopsis

Major Teaching Points:

  • Of the almost 700 exercise intervention studies in cancer patients, the vast majority has been performed in early stage breast cancer
  • Exercise training is safe and feasible across the cancer continuum
  • Exercise training can improve physical functioning and psychosocial outcomes; however, adaptations in physiological outcomes may be hampered be adverse effects of concurrent anti-cancer treatment
  • Exercise training may reduce chemotherapy-induced toxicities and improve treatment completion rates
  • Early evidence indicate that exercise training may delay disease progression and improve survival
  • Preclinical evidence points to rationales for an enhanced efficacy of anti-cancer therapy by exercise training
  • Exercise training in cancer patients represents a continuum of stimuli, which may be adjusted according to the physical limitations cancer patients experience

Didactic Legends

The figures—in a freely downloadable PowerPoint format—can be found on the Images tab along with the formal legends published in the article. The following legends to the same figures are written to be useful for teaching.

Figure 1 Historic overview of exercise intervention studies in cancer patients. Here, the time course of the number of published exercise intervention studies in cancer patients is presented. Seminal clinical exercise intervention trials are highlighted in black at the time of publication. Other important contributions to the field are inserted in blue, including the first publication of exercise guidelines in cancer patients, the first epidemiological evidence for a protective effect of exercise on relapse and mortality in cancer patients, and the first major review to summarize the role of exercise-dependent regulation of systemic cancer risk factors.

Figure 2 Flowchart of the screening process for exercise intervention studies. The figure provides an overview of the screening process for exercise intervention studies. Presented first is the total number of PubMed indexed studies (n = 9616) identified using our search string. The total number of studies were screened on title and abstract for studies utilizing exercise and physical activity interventions, which resulted in 679 studies. Next, we differentiated between studies applying structured exercise interventions and physical activity interventions. Exercise interventions were defined as structured, planned, and repetitive interventions aiming to maintain or improve physical fitness. Thus, studies, which did not provide a description of the exercise protocol were excluded. Furthermore, we excluded studies applying multimodal interventions (e.g., combined exercise and diet interventions), counseling-based physical activity studies, holistic training including yoga or tai chi and other preference-based interventions. Based on these inclusion criteria, 292 unique exercise intervention studies were identified. For both exercise training intervention studies (n = 292), and the excluded studies (n = 387), we determined the number of specific intervention arms evaluated (note: the number of intervention arms do not add up to the total number of studies as some studies included more than one intervention arm).

Figure 3 Overview of exercise intervention studies across the cancer trajectory. The figure illustrates the number of exercise intervention trials performed according to diagnosis. Further, trials are subcategorized by timing relative to primary treatments. We distinguish between four overall clinical settings: (i) exercise interventions prescribed before surgery as preoperative optimization, (ii) exercise interventions prescribed during systemic adjuvant therapies for patients treated with curative intend, (iii) exercise interventions prescribed after completion of curative and/or adjuvant therapy, and (iv) exercise interventions prescribed for patients with metastatic cancer with or without concurrent palliative treatment.

aFor studies in prostate cancer, systemic/adjuvant treatment includes radiotherapy and androgen deprivation therapy without surgery in patient with local or locally advanced stage disease.

bFor blood cancers, adjuvant/systemic treatment includes high dose chemotherapy prior to or during inpatient chemotherapy after allogenic stem cell transplantation in the vast majority of studies.

Figure 4 Summary of the outcomes measured in exercise-oncology trials. Here, we present an overview of the number of different outcomes reported in the 292 unique exercise intervention studies, which examined the effects of structured exercise programs identified in our PubMed search. Overall, we divide these outcomes into four different categories: (i) cancer-specific outcomes, that is, survival, disease progression, regulation of tumor markers, and treatment tolerability; (ii) secondary prevention outcomes, that is, cardiotoxicities, body weight, body composition, sex hormone levels, insulin levels, and immune function; (iii) exercise-specific physiological outcomes, that is, cardiopulmonary fitness and muscle function; and (iv) psychosocial outcomes, that is, health-related quality of life (HRQoL), depression, and cancer-related fatigue.

Figure 5 Factors linking exercise training to cancer survival. The association between exercise behavior and cancer prognosis is well-established, and this protective role is likely mediated by a wide range of exercise-dependent responses. Here, we outline three interrelated modes-of-action, through which exercise training may directly or indirectly influence the prognostic outlook following a cancer diagnosis. Exercise training may influence the risk of clinical disease progression, evaluated by disease-free survival or surrogate tumor markers, by imposing direct antiproliferative actions on residual tumor cells. In addition, exercise training may interact with the impact of standard treatment in different settings including preoperative optimization, improvement of treatment tolerability, and/or enhancement of antineoplastic efficacy. Finally, exercise training can play a critical role in secondary prevention of acute- and late-occurring detrimental health effects associated with cancer and its’ treatments, including protection from cardiotoxicity, weight gain, metabolic disturbances and dysregulation of systemic cancer risk factors.

Figure 6 Mechanisms involved in exercise-dependent control of tumor growth. Evidence from preclinical studies indicates that exercise can reduce tumor growth and inhibit metastasis through various mechanistic pathways. Exercise is associated with an acute mobilization and redistribution of cytotoxic immune cells, natural killer (NK) cells to malignant tumors. Exercise is also associated with the release of anti-oncogenic myokines from contracting muscles. Finally, exercise-derived increase in epinephrine is shown to activate the ‘Hippo Tumor Suppressor’ signaling pathway in tumor cells, which in particular has been found to inhibit the formation of new malignant tumors associated with the metastatic process.

Figure 7 Exercise-dependent regulation of the Hippo signaling pathway. The Hippo signaling pathway is involved in basal processes like cellular growth, differentiation, and apoptosis, and is particularly recognized for its role in tissue development. The Hippo signaling pathway comprise of the oncoproteins Yap and Taz, which in the activated state, will translocate to the nucleus and induce transcription of factors involved in cell proliferation, antiapoptosis, and metastasis. However, upon phosphorylation by Lats1/2, Yap, and Taz are retained in the cytosol and degraded. This inactivation and degradation of Yap and Taz will reduce the rate of tumor metastasis. The Hippo signaling pathway has been shown to be dysregulated in several types of cancer, including breast cancer, where activation of the oncoproteins YAP /TAZ have been associated with a poor prognosis. Exercise can regulate the Hippo signaling pathway, as exercise-induced epinephrine can induce phosphorylation and degradation of Yap and Taz, and this has in mice been shown to reduce tumor formation by 50%.

Figure 8 Exercise-dependent regulation of immune cells. Several studies have reported that patients allocated to exercise training were either more likely to receive their planned dosage of chemotherapy or reported fewer toxicities compared with usual care controls. This observation has coincided with maintenance of the patients’ immune cells population, that is, the patient experienced lower incidence of neutropenia, trombopenia, and lymphopenia, which are principle causes of chemotherapy dose reduction and/or postponement. During exercise, immune cells are acutely mobilized to the circulation through adrenergic signaling and shear stress on the vascular bed induced by the increased blood flow during exercise. The most responsive immune cells are NK cells and monocytes, followed by T cells and to a lesser extent B cells. Once mobilized, the immune cells will be distributed to the peripheral tissue to survey for malignant transformed or virus-infected cells. This exercise-mediated mobilization and redistribution of immune cells will provide yet unidentified signals to the bone marrow to initiate the production of new immune cells, which are released to the circulation and stored in the spleen and lymph nodes. This exercise-mediated feedback loop to the bone marrow may explain why cancer patients can maintain their immune cell population despite receiving bone marrow suppressive anti-cancer treatment.

Figure 9 Drug compartmentalization in untrained and trained individuals. Systemic treatments with chemotherapy or immunotherapy are associated with toxicities and organ damage in a dose-dependent manner. Importantly, systemic treatments are administered by anthropometrics, that is, body mass or body surface area, which do not take into account the relative composition of fat and fat-free mass. Since cancer drugs is distributed in metabolically active tissues only, it has been proposed that obesity alone, and in particular in combination with low muscle mass, known as sarcopenic obesity, is associated with higher risk of toxicity induced dose reduction. This figure illustrates the hypothetical distribution of the same absolute dosage, administered to two individuals with the same body mass/surface area, but different distribution of fat and muscle, as often observed in untrained (high fat mass, low muscle mass) and training individuals (low fat mass, high muscle mass). The ‘relative‘ dose encountered in thus metabolically (fat free) active tissue is thus higher in the untrained, relative to the trained individual, who are distributing the same dose to a larger fat-free mass.

Figure 10 Exercise-mediated enhancement of anti-cancer therapy efficacy. Data from clinical trials and pre-clinical experiments suggest that exercise training may enhance the antineoplastic efficacy of traditional cancer treatments including radiotherapy, chemotherapy, and immunotherapy. The principle candidate mechanism responsible for this synergistic effect is increased vascularization leading to improved intratumoral blood perfusion. Such increase in blood perfusion by exercise training has been demonstrated in murine studies, where acute exercise directly can blood perfusion, while long-term training has been associated with increased vascularization, normalization of capillary perfusion and reduction in tumor hypoxia. Together, this can improve the anti-cancer efficacy by (i) increasing the delivery capacity of drugs, for example, chemotherapy to the interior of the tumor, (ii) improving oxygenation of the interior of the tumor, which is required for the generation of reactive oxidative species (ROS) in radiotherapy, and (iii) increasing intratumoral immune cell infiltration, which are required for removal of dead cells after cytotoxic treatment, as well as for interaction with immunotherapy.

Figure 11 Conceptual model of the possible interaction between exercise training and cancer treatment. In pharmacology, the therapeutic window is determined by the dosage range interval from the “median effective dose” (ED50), defined as the dose achieving a positive response in 50% of the patients, and the “median toxic dose” (TD50) defined as the dose resulting in toxicity (here arbitrarily defined) in 50% of the patients. The lower limit of this therapeutic window is therefore determined by the antineoplastic potency of the treatment, that is, the more potent the agent, the higher tumor response to the same absolute dose. The upper limit of the window is, on the other hand, determined by the drug toxicity profile, that is, the adverse cytotoxic reactions in nontargeted tissues (e.g., the lungs, kidneys, or bone marrow). Through direct and indirect mechanisms, exercise training may widen the therapeutic window. Exercise-induced improvement in blood perfusion, and thus improved drug delivery, less intratumoral hypoxia and higher invasion of cytotoxic immune cells, potentially shirts the treatment efficacy curve to the left eliciting a higher tumor response to the same dose or similar response at a lower dose. In parallel, exercise-dependent improvements in treatment toxicity profile by protection against immunosuppression and improved drug compartmentalization (distribution of the toxic agents a to larger mass of metabolic active tissue) may shift the toxicity curve to the right, thus improving treatment tolerability by lower toxicity profile to the same absolute dose or allowing for similar toxicity profile to a higher dose. In concert, this interaction between exercise training and standard therapies can have profound impact on patient management in both adjuvant and palliative settings, but requires full integration of the exercise intervention within standard oncology therapeutic framework regarding prescription, delivery, and evaluation.

Figure 12 Exercise-dependent regulation of cardiopulmonary fitness (VO2peak) in cancer patients. VO2peak is determined as the maximum capacity to deliver oxygen to the working muscles, and requires integration of multiple steps known as the oxygen cascade. Here, we outline the various limiting steps in oxygen cascade in cancer patient with regard to the training-time required for exercise-dependent adaptation, as well as cancer-specific pathophysiological impairments in the response potential. The first step involves the oxygen saturation of the blood as a result of pulmonary diffusion capacity from the atmospheric air in the lungs to the blood in the alveoli. This step is extremely rarely a limiting factor for maximum oxygen uptake, but may be significantly hampered in the event of thoracic surgery. The next step involves the capacity to distribute oxygenated blood to the metabolic active tissues. The maximum cardiac output (liters of blood per minute) is determined by the maximum heart rate and the stroke volume of the heart, of which only stroke volume is considered trainable healthy subjects. Cardiac output is a well-established limiting factor of cardiopulmonary fitness in sedentary and recreationally active humans, and constitutes a robust exercise adaptation within days to weeks of commencing an aerobic exercise program. However, various cancer drugs and/or irradiation to closely situated tumors (e.g., thoracic or mammary irradiation) can cause cardiotoxicity in the form of various limiting symptoms including cardiomyopathy, inhibiting the capacity to improve stroke volume. Another key determinant of cardiac output is the total blood volume (in liters), which consists of total plasma volume and red blood cell volume. Integrative physiology research has shown a close correlation between changes in blood volume, especially red blood cell volume, with changes in VO2peak, and elegant phlebotomy-experiments have found that exercise-induced improvements in VO2peak is abolished when the increase in blood volume is normalized to pretraining levels. Exercise-induced regulation of blood volume in cancer patients has to our knowledge never been examined and may to some extend explain the lack of robust increases in VO2peak, as normally observed in healthy individuals. Indeed, a number of treatment-related pathophysiological changes may impact, and reduce, particularly red cell blood volume by bone marrow toxicity and/or dehydration due to nephrotoxicity. Finally, extraction of oxygen from the capillaries to the muscle cells and mitochondrial metabolic turnover rate comprise the last steps of the oxygen cascade. The capillary density, that is, ‘the cross sectional muscle area supply by one capillary’ as well as oxidative enzymes are key regulators of intramuscular oxygen utilization, and while these are rarely considered limiting factors for VO2peak, as they show robust adaptations to exercise in healthy individuals. In patients with cancer, few studies have examined muscular toxicities, but a number of common symptoms, for example, muscular pain from taxanes, which is considered a result of serious muscular inflammation may be so severe, at least in the acute treatment phase, that they significantly limit maximum aerobic exercise performance irrespective of the oxygen delivery capacity.

Figure 13 Regulation of muscle function in cancer patients. Overall maximum contractile muscle strength is determined by anatomical features especially the cross-sectional area (mass) and pennation angle, and a neural component, that is, recruitment and synchronization of motor units. The vast majority of resistance training trials performed in cancer patients have found a significant increase in contractile strength, whereas changes in muscle architecture, which have mostly been evaluated by whole-body and appendicular lean mass, have yielded ambiguous results especially in studies performed during active treatment. One explanation for this apparent lack of muscular adaptation may stem from the relative short duration of most exercise interventions (from 4 to 16 weeks), and the possible counteracting impact of cytotoxic or antiandrogenic treatments, which may impair protein synthesis and/or enhance protein degradation signal in skeletal muscle. Although, this limited or inhibited hypertrophic exercise-response may discourage the clinical application of resistance training in cancer patients, it is important to acknowledge the almost unanimous improvements in muscle strength, irrespective of changes in muscle mass, are reported in almost every exercise intervention studies in cancer patients, including advance stage lung cancer patients and patients treated for head and neck cancer, who are subject to massive muscle wasting due to nutritional deficits.

Figure 14 Exercise reduce depression through regulation of kynurenine metabolism. Exercise training has consistently been shown to reduce symptoms of depression in cancer patients. Recently, a mechanism to explain how exercise can regulate symptoms of depression at the molecular level was proposed involving regulation of the Kynurenine degradation products. Degradation of Kynurenine follows one of two possible pathways: Kynurenine is either converted to nicotinamide adenine dinucleotide (NAD) or anthranilic acid through kynurenine 3-monooxygenase (KMO); or converted to kynurenic acid by kynurenine aminotransferases (KATs). The Kyn-NAD pathway is induced by inflammation, which might occur secondary to chemotherapy in muscles of cancer patients. This transformation leads to production of quinolinic acid, a potent NMDA receptor agonist leading to excitotoxicity in the central nervous system. Kynurenic acid, on the other hand, is neuroprotective, acting as an antagonist of the NDMA-receptor and thereby counteracting the neurotoxic effects of quinolinic acid. Moreover, kynurenic acid cannot cross the blood-brain-barrier, so the conversion of kynurenine to kynurenic acid in the periphery can reduce accumulation of kynurenine in central nervous system. The imbalance between these neuroprotective and neurotoxic metabolites has been proposed to be critical for development of symptoms of depression.

Figure 15 The exercise continuum for cancer patients. Exercise training interventions are often divided into distinct categories, typically described as resistance training using weights or fitness machines, and aerobic training using, that is, treadmills and stationary bikes, based on basic exercise physiology outlining that different exercise stimuli elicit different responses to different organ systems. However, all exercise interventions essentially consist of voluntary muscular contractions performed in a manner determined by a continuous relationship between (a) the external load and/or internal energy turnover rate, and (b) the duration of the active work period. Here, we have exemplified five modes of exercise training on the (duration-intensity) continuum with regard to the duration of active work period and the corresponding relative load/intensity, as well as the required work-to-rest time frame-ratio, and the main physiological stimulus and response. This ranges from maximum muscle force-generation performed against high external loads for just a few seconds known as “power training” to very light repetitive contractions performed for up to several hours as endurance training. Naturally, targeted exercise prescriptions stimulate different organ systems with different effectiveness and thus can be applied if specific adaptations are warranted, but it is important to emphasize that all physical exercise interventions involve physiological of the entire continuum. By proper application of the principles of training, this internal feature of can be utilized advantageously, when prescribing exercise training for patients with cancer. Most importantly, this provides a unique opportunity for individualization of an exercise program according to patient preferences and/or limitations, and the recognition of the individual's physical capacity, for example, for elderly, frail patients a structured walking intervention can comprise a relatively high-intensity exercise stressing both the oxygen cascade and neuromuscular components. This view of exercise training may also take into consideration training periodization as certain activities may be unfavorable during certain periods in the cancer trajectory. For example, patients who are seriously symptom-burdened during cytotoxic treatment phases may be precluded from performing exercise with highly elevated heart rate and blood pressure associated with high intensity exercise, but may tolerate lower intensity for a longer duration. Or they may contrarily prefer short-term, high-load activity with high intensity interval training (HIIT) or heavy resistance training, which can be concluded in short sessions. Abbreviations: RM, repetition maximum; MVC, maximum voluntary contraction; RFD, rate of force development; ATP, adenosine triphosphate.

 


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How to Cite

Jesper Frank Christensen, Casper Simonsen, Pernille Hojman. Exercise Training in Cancer Control and Treatment. Compr Physiol 2018, 9: 165-205. doi: 10.1002/cphy.c180016