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Abstract

Worldwide, over 1 million cases of breast cancer are diagnosed each year. In the USA, approximately 185,000 women are newly diagnosed annually. Nearly 90% of newly diagnosed cancer patients in the USA will live for 5 years beyond diagnosis and there are estimated to be 2.4 million breast cancer survivors currently living in the USA. There are unique challenges in meeting the medical needs of these survivors. Persistent impairment and increased medical risks can occur as a result of treatment, including changes to the cardiovascular, pulmonary, endocrine, immune, musculoskeletal, neurological and lymphatic systems. Physical activity can cause positive changes in each of these body systems. However, physiologic impairments and altered risks for cardiopulmonary, bone health, neurosensory and other outcomes among breast cancer survivors can cause confusion regarding the safety of returning to exercise after treatment. In this article, we review the adverse effects of cancer treatments on the body systems affected by and used to perform exercise, the risks of exercise among breast cancer survivors, the effects of exercise on persistent treatment toxicities, whether exercise may prevent recurrence or mortality, as well as providing guidance for exercise testing and prescription among breast cancer survivors.

Keywords

breast neoplasm exercise survivorship

Worldwide, over 1 million cases of breast cancer are diagnosed each year [101]. In the USA, approximately 185,000 women are newly diagnosed with invasive breast cancer each year, and the number of survivors currently totals over 2 million [102]. Substantial improvements in the success of treating breast cancer have resulted in the welcome challenge of identifying and addressing the unique long-term medical and psychological needs of these women. The process of receiving breast cancer treatment necessitates exposure to interventions that can have persistent negative side effects [1]. Regular exercise may be useful to breast cancer survivors for preventing, attenuating or reversing those persistent adverse treatment effects. However, it is important to recognize that some of the persistent adverse effects of curative treatments (e.g., surgery, chemotherapy, radiation, biological treatments and hormonal therapy) may increase the risk posed by exercise and may require altered exercise assessment and/or prescription compared with age-matched peers in order to ensure safety. The purpose of this paper is to review the following:

The persistent adverse effects of cancer treatments on the body systems affected by and used to perform exercise;

The evidence regarding adverse effects of exercise among breast cancer survivors;

The effects of exercise on persistent treatment toxicities;

The evidence regarding whether exercise may prevent recurrence or mortality among breast cancer survivors;

This article will also provide guidance for exercise testing and prescription among breast cancer survivors based on the available evidence. The focus of this review is on the period after surgery, chemotherapy and radiation are complete.

Breast cancer treatments & associated persistent adverse effects

Breast cancer treatments differ by histology, stage and hormone susceptibility of disease. The main categories of treatment include surgery, chemotherapy, radiation therapy, hormone therapy and targeted drugs. Persistent toxicities and negative effects vary by intensity and combination of treatments, as well as by host characteristics, such as age and pre-existing health conditions. In this article, we focus on the effects of common breast cancer treatments on the body systems required for, or affected by, performing exercise, including the cardiovascular, pulmonary, musculoskeletal, neurological, cognitive, immune, lymphatic and endocrine systems.

Surgery

The effects of surgery include scarring, change in sensation and shoulder morbidities [2,3]. Postmastectomy pain syndrome occurs in up to 30% of patients, including patients who undergo lumpectomy and/or axillary dissection [4]. There is also the risk of lymphedema onset, which occurs in 20–30% of survivors [5,6]. Secondary surgeries, such as breast reconstruction or implant procedures, can result in infection, tissue necrosis and seroma [7], as well as numbness, decreased sensitivity in the breast [8] and altered physical function in the region from which tissue is harvested [9]. There is a high likelihood that secondary surgeries will require corrective procedures [10]. Another issue with surgery is the period of inactivity and bed rest that may result in muscle atrophy and loss of physical function. Arm and shoulder problems are among the most commonly reported persistent negative effects of breast cancer surgery [3,11], occurring in 35–58% of survivors.

In addition to breast surgeries, some patients may undergo ovarian ablation or oophorectomy in order to reduce the risk of recurrence of hormone-sensitive cancers. These procedures are performed on pre- or perimenopausal women and have the result of inducing early menopause and its associated effects, such as infertility, bone loss and menopausal symptoms [4].

Chemotherapy

The persistent negative effects of chemotherapy depend upon the specific type and dosage of drugs prescribed, as well as precancer health status. Weight gain is common [12,13], with an average increase of 2.5–5.0 kg [14], although specific types of body composition changes (e.g., total weight, lean body mass and fat mass) may differ by chemotherapeutic agent [15,16]. Treatment with anthracyclines and/or traztusumab (Herceptin®) is associated with cardiotoxicity and autonomic nervous system dysfunction [17]. Several chemotherapeutic agents used to treat breast cancer are associated with pulmonary damage (e.g., cyclophosphamide and paclitaxel) [17]. There is also the potential for chemotherapy-related amenorrhea and/or premature menopause, particularly after treatment with aylkylating agents (e.g., cyclophosphamide) [4]. Taxanes are associated with peripheral sensory and motor neuropathies [4]. It is increasingly being accepted that there are also negative short- and long-term cognitive effects associated with chemotherapy [4].

Radiation

The persistent negative effects of exposure to ionizing radiation for breast cancer include lymphedema onset [18], pulmonary [19] and cardiac toxicities [20], as well as damage to gastrointestinal tissues [4] and sustained immune suppression [21]. The risk of radiation pneumonitis is higher in patients treated with combined or sequential paclitaxel chemotherapy and radiation [22]. Radiation may also contribute to the arm and shoulder morbidities often observed after breast cancer treatment through nerve damage or fibrotic damage to soft and/or contractile tissue [4].

Hormone therapy

In addition to the oophorectomy and ovarian ablation effects on hormones discussed previously in the ‘Surgery’ section, there are multiple hormonal therapies used in the treatment of breast cancer that also have negative persistent effects, including antiestrogens (e.g., tamoxifen) and aromatase inhibitors (e.g., anastrozole).

Tamoxifen

The side effects of tamoxifen are similar to the symptoms of menopause. The most common side effects are hot flashes and vaginal discharge. Premenopausal women may experience irregular menstrual periods. Other symptoms include fatigue, nausea and/or vomiting, vaginal dryness or itching, irritation of the skin around the vagina and skin rash. As with menopause, not all women who take tamoxifen have these symptoms [4]. Since tamoxifen is a selective estrogen-receptor modulator, negative effects on the bones are less severe than those associated with aromatase inhibitors, the other common hormonal therapy used in the treatment of breast cancer.

Aromatase inhibitors

A recently completed study by the advocacy organization Breast Cancer Action reported that the side effects associated with taking aromatase inhibitors include hot flashes, bone pain, feeling tired, muscle pain, insomnia, weight gain, mental fuzziness, increased sweating, anxiety, hair thinning, depression, swelling of the arms/legs, osteoporosis, dizziness, constipation, headache, shortness of breath, high blood pressure, cough, sinusitis, influenza-like symptoms, nausea and stomach pain [103]. The most common symptoms reported are arthralgias (muscle pain) and hot flashes, which have been reported to occur in 35% of women taking aromatase inhibitors [23].

Physical function changes with breast cancer

There are two large cohort studies that have observed there to be a subset of breast cancer survivors who experience a loss of functional mobility (a key element of functional status) and a reduced ability to live independently, as compared with women who have never had a cancer diagnosis [24,25]. The finding is sustained even 5 years after diagnosis. Although the majority of breast cancer survivors recover sufficient functional mobility to function independently, it is hypothesized that cancer treatment may alter the aging trajectory towards loss of independence in a manner that could be amenable to exercise rehabilitation [26].

Summary

Breast cancer patients undergo surgery, and many receive radiation plus chemotherapy and are also prescribed hormonal therapies. The changes resulting from these treatments include increased risks of cardiovascular outcomes, pulmonary toxicities, altered shoulder, arm and torso musculoskeletal structure and function, decreased bone density, overall deconditioning, motor and sensory neuropathies, weight gain and immune suppression. There is also an increased risk for lymphedema and other arm and shoulder problems. All of these outcomes are amenable to intervention. These persistent negative effects may occur individually or synergistically and may alter one's ability to exercise, as well as altering the safety of exercise. They may also alter the usefulness of exercise, since exercise may be helpful to restore function and rehabilitate damaged body systems. An analogous situation may be cardiac rehabilitation after repair of a damaged heart, or specific exercises for patients with back pain. As with the cardiac rehabilitation and back pain examples, exercise has been demonstrated to be able to gradually increase the capacity of damaged body systems so that they can withstand the stress of common daily activities without resulting in further injury to the system. In the following two sections, we review the available evidence that exercise is safe, given the physiologic changes caused by breast cancer treatment, followed by a review of the available evidence that exercise improves the body systems impacted by cancer treatment.

Risks of adverse effects of exercise among breast cancer survivors

The effects of exercise training on outcomes in post-treatment breast cancer survivors has been the topic of 38 randomized controlled trials (Table 1). Publications from 16 of these trials include comments on the adverse effects of exercise. This section reviews the available evidence regarding the adverse effects of physical activity among breast cancer survivors.

Table 1.

Summary of 38 randomized controlled exercise intervention trials in breast cancer survivors.

Author (year)	Sample size†	Intervention length	Exercise mode	Exercise dose (frequency, intensity and duration)‡	Outcomes§	Ref.
Basen-Engquist et al. (2006)	60	6 months	Lifestyle intervention	Tailored to stage of readiness	Physical function, fitness§, flexibility, QOL§, physical activity behavior, pain§, body composition and lymphedema (arm circumferences)	[36]
Bennett et al. (2007)	56	6 months	Lifestyle intervention	Goal of 30 min moderate intensity most days	Kcals/week, aerobic fitness, physical and mental health status and fatigue	[45]
Berglund et al. (1994)	160	4 weeks	Strength, flexibility	Once weekly	Strength, fatigue, body image§, pain§, QOL, anxiety, depression and psychosocial outcomes	[59]
Burnham et al. (2002)	15	10 weeks	Aerobic	Thrice weekly, moderate intensity, increased to 32 min per session by week 10	Fitness§, flexibility§, QOL§, body composition§, vigor/vitality§, depression and anxiety§	[42]
Cho et al. (2006)	55	10 weeks	Lifestyle intervention, aerobic, stretching	Twice weekly, 90 min per session	Range of motion-flexion, extension§, abduction§, external rotation§, internal rotation§, psychosocial adjustment§ and QOL§	[68]
Courneya et al. (2003); Fairey et al. (2005)	53	15 weeks	Aerobic	Thrice weekly, moderate intensity, 35 min per session	Fitness, fatigue, QOL and body composition	[29,71]
Courneya et al. (2003)	44	10 weeks	Aerobic	3-5 times weekly, 65–75% maximum heart rate, 20–30 min per session	Flexibility, fatigue§ QOL§ and body composition§	[40]
Culos-Reed et al. (2006)	38	7 weeks	Yoga	75 min session	Emotional functioning§ QOL§ dyspnea§ diarrhea§ finances§ gastrointestinal, emotional irritability, cognitive disorganization, tension§ depression, concentration, total mood disturbance, weight§ blood pressure, hand grip§ distance walked§ sit and reach§ heart rate and perceived exertion§	[83]
Daley et al. (2007)	108	8 weeks	Aerobic	Thrice weekly, moderate intensity, 50 min per session	Fitness§ fatigue, QOL§ body composition, physical function§ depression§ and body image	[46]
Demark-Wahnefried et al. (2006)	104	6 months	Aerobic	Five times weekly, moderate intensity, 30 min session	Physical activity behavior, QOL, body composition, physical function and depression	[58]
Demark-Wahnefried et al. (2007)	306	10 months	Aerobic	Five times weekly, moderate intensity, 30 min per session	Physical activity behavior§ QOL and body composition§	[54]
Dimeo et al. (1997)	17	7 weeks	Aerobic	Five times weekly, intensity progressed from moderate to vigorous, session duration progressed from 15 to 30 min	Fitness§ and hemoglobin§	[28]
Djuric et al. (2002)	48	12 months	Aerobic	Most days of the week, moderate intensity 30–45 min per session	Body weight§	[52]
Fillion et al. (2008)	87	4 weeks	Lifestyle intervention, walking training, stress management	Tailored by physical condition and personal goal, 2.5 h per weekly session	Active coping, distraction, instrumental, passive coping, palliative, emotional preoccupation, perceived impact, mastery, stressors, fatigue§, energy level§, physical QOL§, mental QOL, maximal oxygen consumption and psychological distress	[49]
Hayes et al. (2009)	32	12 weeks	Aerobic, strength	3-4 times weekly, intensity and duration progressed over 12 weeks	Lymphedema	[30]
Herrero et al. (2006)	16	8 weeks	Aerobic, strength	Thrice weekly, 90 min per session, moderate to vigorous intensity	Fitness§ strength§ QOL§ body composition§ and physical function§	[37]
Irwin et al. (2009)	75	6 months	Aerobic	150 min per week, moderate intensity	Physical activity behavior§ QOL, body composition§ IGF-1§ IGF binding protein-3§ and bone mineral density§	[51]
Kilgour et al. (2008)	27	11 days	Shoulder stretches	Daily, light intensity, 15–30 min per session	Shoulder range of motion§ strength, arm circumferences and pain	[35]
Ligibel et al. (2008)	101	16 weeks	Aerobic, strength	90 min weekly aerobic activity, twice weekly strength training	Body composition, insulin and glucose	[57]
Matthews et al. (2007)	36	12 weeks	Lifestyle intervention, walking training	3-5 times weekly, moderate intensity, 20–40 min per session	Total activity MET h/week, counts per min§ steps per day§ moderate walking min/day, inactive time percentage, light intensity time percentage, moderate to vigorous time percentage, body mass, fat-free mass, fat mass and body fat percentage	[56]
McKenzie et al. (2003)	14	8 weeks	Aerobic, strength, flexibility upper body only	Thrice weekly, moderate intensity	Lymphedema (arm volume), QOL and pain	[32]
Mefferd et al. (2007)	85	16 weeks	Aerobic, strength	1 h daily, moderate intensity, 2–3 times weekly strength training	Physical activity behavior, body composition§ and blood lipids§	[55]
Milne et al. (2008)	58	12 weeks	Aerobic, strength	Thrice weekly, 30–45 min per session	General and breast cancer-specific QOL§ physical§ social, emotional and functional well-being§ fatigue§ and anxiety§	[62]
Moadel et al. (2007)	128	12 weeks	Yoga	Once weekly, 1.5 h per session	QOL, physical, social, emotional and functional well-being, fatigue, spiritual well-being, anxiety, irritability and confusion	[65]
Morey et al. (2009)	289	12 months	Aerobic, strength	15 min strength training 3–4 times weekly, 30 min aerobic exercise daily	Functional status§ health behavior changes§ QOL§ body weight§ and BMI§	[50]
Mustian et al. (2006)	21	12 weeks	Tai chi chuan	Thrice weekly, light intensity, 60 min per session	Strength§ and flexibility§	[48]
Nieman et al. (1995)	16	8 weeks	Aerobic, strength	Thrice weekly, 60 min per session, moderate intensity	Fitness§ and immune parameters	[41]
Nikander et al. (2007)	28	12 weeks	Aerobic	Thrice weekly, moderate intensity, 30–40 min per session	Weight, BMI, eight-figure running§ jumping force, jumping power§ leg extension force, elbow extension force and 2 km walk time	[47]
Pinto et al. (2003)	24	12 weeks	Aerobic, strength	Thrice weekly, moderate intensity, 50 min per session	Fitness§ fatigue, depression and body image§	[60]
Pinto et al. (2005)	86	12 weeks	Aerobic	Five times weekly, moderate intensity, 30 min per session	Fitness§ physical activity behavior§ fatigue§ body composition, vigor/vitality§ and body image§	[43]
Sandel et al. (2005)	38	12 weeks	Dance	1-2 times weekly, 60 min per session	QOL§ physical and mental health status, body image, shoulder range of motion and arm circumference	[34]
Schmitz et al. (2005); Ahmed et al. (2006),	86	6 months	Strength	Twice weekly, 60–90 min per session	Strength§ QOL§ body composition§ lymphedema, IGF-1, IGF-II§ and IGF binding proteins	[31,53]
Schmitz et al. (2009)	141	12 months	Strength	Twice weekly, 90 min per session	Bench press§ leg press§ weight, BMI, % body fat, fat mass, lean mass, Kcals intake, MET h/week, change in lymphedema symptoms and change in lymphedema symptom severity§	[33]
Segar et al. (1998)	24	10 weeks	Lifestyle, aerobic	Four times weekly, moderate intensity, 30 min per session	Depression§ anxiety and self-esteem	[67]
Sprod et al. (2005)	12	8 weeks	Aerobic, strength	Twice weekly, moderate intensity, 20 min per session	Muscular endurance§	[69]
Thorsen et al. (2005)	80	14 weeks	Aerobic, strength or flexibility – at discretion of participant	Tqice weekly, moderate to vigorous intensity, 30 min per session	Fitness§ fatigue, QOL, depression§ anxiety§ and mental distress	[44]
Vallance et al. (2007)	377	12 weeks	Aerobic	30 min, five times weekly	Physical activity level§ and QOL§	[61]

†

Sample sizes reflect the number of breast cancer survivors. Some studies also included other diagnoses.

‡

If frequency, intensity or duration of session is not provided in this column, then that detail was not provided in the published work.

Outcomes that were significantly affected by the exercise intervention.

MET: Metabolic unit; QOL: Quality of life.

A theme across many of the comments on adverse events was fear of harm from exercise during or soon after the end of treatment, when patients may be anemic, have reduced blood cell counts and a fear of exacerbation of the unexplained weight loss in the advanced cancer patient suffering from cachexia. However, with few exceptions, exercise of multiple levels of intensity (e.g., light to vigorous) and modes (e.g., aerobic, stretching or resistive) were well-tolerated by participants during and post-treatment. However, there is room for caution in prescribing exercise to survivors. The inverted J-shaped association of exercise training with immune outcomes is well described [27] and was commented on by multiple authors as a reason to avoid high-intensity exercise in cancer survivors, particularly during the period that is close to the end of active treatment, when immune function may already be compromised. Some authors suggest that anemia is a contraindication to the prescription of exercise during active treatment. However, Dimeo et al. did not exclude anemic patients from prescribed exercise, and observed no adverse effects of a 6-week vigorous aerobic exercise intervention immediately upon hospital discharge after high-dose chemotherapy and autologous peripheral stem cell transplantation [28]. One argument against using anemia as a contraindication for exercise was that aerobic exercise increases hemoglobin and hematocrit levels in healthy volunteers [28].

Another common issue raised by the reviewed papers was the risk for lymphedema. With the exception of a small number of patients in two studies [29,30], aerobic, lifestyle and upper body resistive exercise was tolerated by breast cancer survivors with no adverse effect on the development or exacerbation of lymphedema. Courneya et al. reported a higher rate of lymphedema in the physical activity group than the comparison group [29]. The authors noted that two of the three participants who developed lymphedema had undergone axillary irradiation, a strong risk factor for lymphedema. The authors commented that it was not clear whether the onset of lymphedema was due to the physical activity. Hayes et al. noted that, among 16 post-treatment breast cancer survivors, one woman with lymphedema and who attended 50% of all exercise sessions had significant worsening of lymphedema throughout the entire 13 weeks of supervised group exercise intervention [30]. This participant was subsequently diagnosed with a breast cancer recurrence within 6 months. It is unclear whether the intervention was the cause of the lymphedema worsening.

There is a fear of overusing the arm in physical activity among cancer survivors, and this is particularly noted in the qualitative results reported by Hayes et al. [30]. The women in this study were so concerned about whether the exercise they were performing was harmful to them that interim measures were needed in order to allay their fears [30]. These participants also reported that they felt that doing the exercise in a supervised setting was vital to reducing their fear of overuse, injury and lymphedema onset or worsening [30]. Unfortunately, the fear of lymphedema leads many women to adopt lifestyle choices that decondition the arm, which may place the arm at a greater risk than gradually and progressively increasing the strength and endurance of the arm after surgery. There are now seven published studies that have examined the safety of upper body exercise among women with risk and at risk for lymphedema [30 –36]. In each of these studies, the benefits of upper body exercise far exceeded the risks.

Lymphedema is only one of a multitude of arm and shoulder problems experienced by breast cancer survivors. The safety of upper body activity among the 35–58% of women with some arm or shoulder problem secondary to breast cancer treatment [3,11] is poorly studied. In one of the few studies on this topic, Kilgour et al. reported that four of the 16 treatment group women had to stop the home-based shoulder rehabilitation program prescribed during the first 3 weeks after surgery owing to pain in the shoulder joint or swelling in the axillary region [35]. Research is required in order to provide knowledge regarding what level of supervision is needed, what timing after surgery is the safest and what modes, intensity, frequency and duration of activity is most effective for returning women to their best possible arm and shoulder function.

Another issue related to upper body exercise is the safety of the various exercise assessments that might be used to determine upper body strength. There is little doubt that a timed push-up test would be inappropriate for a woman with arm and shoulder problems secondary to breast cancer, whether the problem is lymphedema or something musculoskeletal or neurological in nature. Herrero et al. excluded breast cancer survivors with lymphedema for fear of the negative effects of one-repetition maximum testing among this at-risk population [37]. Ahmed et al., Schmitz et al. and Schwartz et al. included breast cancer survivors with and without lymphedema in one-repetition maximum testing with no reported adverse events [31,33,38]. From this evidence, it appears that symptom-limited one-repetition maximum testing for the upper body is safe for breast cancer survivors. It is also possible that handgrip dynamometry, manual muscle testing and implementing the various resistive modes and arm/shoulder evaluations possible with isokinetic dynamometry could further contribute to the safe and reliable modalities available for measuring functional loss among breast cancer survivors.

The collection of adverse events data is typically accomplished by self-report in these studies. This may be problematic; for example, Mock et al. commented that self-reported data collection of the worsening of side effects leaves open the possibility that survivors with more extreme side effects brought on by exercising may not have felt well enough to complete data collection at the end of the study [39]. This highlights the importance of minimizing loss to follow-up in these studies.

In summary, the results of completed randomized controlled trials of exercise in breast cancer survivors support the safety of cardiorespiratory exercise, strength training and flexibility activities. Fear of exercising during anemia appears to be greater than is warrented by the actual risk. Similarly, fear of lymphedema onset or worsening with exercise is greater than is warranted, given the documented safety of upper body exercise in multiple studies. One area yet to be studied in depth is the safety of upper body exercise among women with nonlymphedema-related arm and shoulder morbidity secondary to breast cancer treatment.

Effects of exercise training on the persistent negative effects of breast cancer treatment

As noted previously, the effects of exercise training on outcomes in post-treatment breast cancer survivors has been the topic of 38 randomized controlled trials. Results from these studies are reviewed in the following sections.

Aerobic fitness

Timed distance tests and maximal oxygen consumption have been evaluated in physical activity interventions for breast cancer survivors post-treatment in order to determine improvements in aerobic fitness [28,29,36,37,40 –49]. All studies have observed improvements in aerobic fitness; however, the difference between the treatment and control groups have not been consistently significant; for example, Basen-Engquist et al., Nieman et al. and Pinto et al. found significant improvements in timed distance walked tests (e.g., 6-min walk and 1-mile walk) [36,41,43], while Nikander et al. and Mustian et al. did not find a significant improvement [47,48]. There are multiple possible reasons for these contradictory findings; for example, the Mustian intervention focused on tai chi chuan, a lower-intensity activity not specifically focused on aerobic fitness gains [48]. The Nikander intervention was only supervised once weekly; perhaps the participants reduced their intensity to below threshold required to observe a training effect in the nonsupervised twice-weekly home sessions [47].

Physical function

Only two studies have objectively measured changes in physical function as a result of a physical activity intervention. The Basen-Engquist et al. lifestyle intervention [36] and the Herrero et al. combined aerobic and resistance interventions [37] assessed the sit-to-stand maneuver. They reported a significant improvement in the intervention group as compared with the control group. In addition, the recently published Reach Out to Enhance Wellness (RENEW) study indicates that a nutrition and exercise intervention improves self-reported physical function among cancer survivors, including breast cancer survivors [50].

Strength

Resistance- and aerobic-based physical activity trials for post-treatment breast cancer survivors have assessed changes in both upper and lower body strength. The evidence is consistently positive for improvements in strength. The twice-weekly strength training interventions for breast cancer survivors reported by Ahmed et al. and Schmitz et al. observed significant differences in improvement between the intervention and control groups in both upper and lower body measures of strength [31,33].

Body composition

Changes in body weight, BMI, fat mass, lean mass, body fat percentage and waist circumference have been assess in randomized controlled physical activity interventions for breast cancer survivors post-treatment [29,36,37,40,42,43,46 –48,50 –58]. Aerobic training, resistance training, the combination of aerobic and resistance training, as well as tai chi chuan, have all been demonstrated to be beneficial, although not for all variables.

Fatigue

Multiple randomized controlled physical activity interventions of various exercise modalities have examined fatigue outcomes in breast cancer survivors post-treatment [28,29,42 –46,49,59 –62]. There have also been literature reviews and metaanalyses focusing on activity-based interventions for cancer-related fatigue [63,64]. Findings favor the intervention groups in the majority of studies; however, the heterogeneity of studies prevents the drawing of firm conclusions as to the specific magnitude of the intervention effect. Some researchers have observed that aerobic exercise interventions at frequencies of both three and five times per week result in positive, significant improvements in fatigue [40,43]; however, those results have not been observed consistently in interventions of a similar design and frequency [29,46,60]. One study has evaluated the impact of yoga on fatigue; the results were not significant [65].

Lymphedema

Ahmed et al. demonstrated that twice-weekly weight training does not increase lymphedema-related symptoms [31]. The recently completed Physical Activity and Lymphedema Trial demonstrated that slowly progressive resistance training is protective against lymphedema flare-ups among women with lymphedema [33]. A behavioral physical activity intervention by Basen-Engquist et al. found no difference between the intervention and control group in arm circumference, suggesting that the intervention did not increase the risk for lymphedema [36]. In a home-based shoulder flexibility and stretching intervention for women postradical mastectomy and axillary node dissection, no evidence of lymphedema (as measured by forearm circumference) was observed [35]. Combined aerobic and resistance interventions produce similar results. Mckenzie and Kalda found no changes in arm circumference or volume after 8 weeks of upper body resistance and aerobic training [32]. Hayes et al. found no group changes in bioimpedence spectroscopy or perometry measures of lymphedema during their intervention study [30]. The Lebed method dance program has also been found to be safe with regard to lymphedema risk [34].

Quality of life

Multiple quality of life (QOL) outcomes have been assessed in numerous physical activity interventions for breast cancer survivors post-treatment. There are definite trends toward improvements in QOL when taking part in physical activity interventions. However, the majority of studies have not found a statistically significant difference in outcome scores between the intervention and control groups. The Breast Cancer Subscale of the Functional Assessment of Cancer Therapy-Breast (BCS FACT-B) is the only QOL outcome demonstrating consistent and statistically significant positive improvement [66].

Other psychosocial outcomes

Other psychosocial outcomes examined in physical activity interventions for breast cancer survivors include body image, self-esteem, mood state, depression and anxiety. Evidence suggests that all of these variables are improved by physical activity interventions; however, the difference in improvement between the treatment and control groups is not always significant. The outcome demonstrate improvement in the highest proportion of studies with significant findings is depression, with a third of studies observing a significant improvement for the treatment versus control group [44,46,67].

Symptoms/side effects & pain

There is also evidence that exercise has positive effects on persistent symptoms and pain after breast cancer treatment [33,35,59].

Shoulder function

The Lebed method did not improve the range of shoulder motion in breast cancer survivors [34], but a twice-weekly 10-week stretching program did result in improvements [68]. A pole walking program resulted in significantly improved muscular endurance in the shoulders of breast cancer survivors [69].

Bone health

To date, there is only one published study that has examined the effects of an exercise intervention on bone health in breast cancer survivors. The Yale Exercise and Survivorship (YES) trial observed a significant improvement in bone mineral density from dual-energy x-ray absorptiometry scans after a 12-month intervention [51].

Immune function

Two randomized controlled trials have examined the effects of exercise training on immune parameters after breast cancer treatment.

Nieman et al. did not find that exercise training resulted in significant increases in natural killer (NK) cells or NK-cell cytotoxic activity after 8 weeks of training [70]. Fairey et al. observed significant improvements in NK-cell cytotoxic activity after 15 weeks of thrice-weekly aerobic exercise [71]. No significant changes were observed for intervention impact on C-reactive protein.

Effects of physical activity on breast cancer recurrence & mortality

Evidence is emerging that physical activity may play a preventative role in breast cancer recurrence and survival. There are multiple hypothesized mechanisms for this process [72], including the relationship between deconditioning and body weight gain. Lack of physical activity has been found to be related to weight gain in breast cancer survivors [12]. Weight gain has also been observed to be a commonly experienced adverse effect during treatment [12,15] and in the years that follow [73]. Being overweight at diagnosis and experiencing weight gain following treatment has been found to be associated with poorer survival [74]. Physical activity before and after breast cancer diagnosis has been found to be associated with a decreased risk of recurrence and or death from breast cancer [25,75,76].

Guidance for exercise testing & prescription in breast cancer survivors

It appears that moderate-intensity exercise is well-tolerated by breast cancer survivors, and that there are numerous outcomes that are improved by exercise training in this population. However, given the potential for the carryover of cardiac, pulmonary, neurologic and musculoskeletal toxicities from the post-treatment period, it would be prudent to individualize the exercise prescription for breast cancer survivors according to each woman's particular abilities, limitations, cancer treatment history and pre-existing medical conditions. Exercise testing assists with refining exercise prescriptions by clarifying the current physiologic capacity and allows for the tracking of progress as women regain and improve physical fitness after treatment is completed. Guidelines for exercise testing and prescription have been published by the American College of Sports Medicine (ACSM) [77]. These guidelines are designed to maximize the ability to exercise while concurrently maximizing the safety of exercise testing. There may need to be revisions to the guidance provided for both exercise testing and exercise prescription based on the physiologic changes that could occur in cancer survivors simply as a result of the treatments or owing to the effects of cancer treatments interacting with pre-existing medical conditions. For example, if a woman with diabetes prior to breast cancer treatment then experiences peripheral neuropathy in her feet owing to treatment with taxanes, she will require specific guidance in order to ensure that her exercise program also includes a plan to frequently review the integrity of the skin on her feet, since she may not experience foot problems with the same sensitivity anymore. In the following two sections, we present a proposed approach to altered exercise testing and prescription guidelines that are specific to breast cancer survivors who have completed surgery, radiation and/or chemotherapy.

Exercise testing guidance for breast cancer survivors

Appropriate allowance for recovery from surgery, as well as recovery of hematologic and immunoco-logic parameters altered by chemotherapy and radiation, should guide the timing of exercise testing after treatment. The specific amount of time allowed for recovery after a patient's treatment is completed will vary between survivors according to a given woman's prediagnosis fitness and health status, and should be guided by symptom response and medical parameters; for example, no exercise testing or exercise sessions should occur during fever, ataxia or extreme fatigue. Low physical functional status may or may not be a contraindication for testing, but will alter the choice of testing modality and the appropriate level of medical supervision. If a woman develops an irregular increase in pulse or respiratory rates with minimal exertion, a sharp pain in her bones or joints, disorientation, confusion, dizziness, lightheadedness, blurred vision or fainting during exercise, she should stop exercising immediately.

For women who are able to complete standard exercise testing, the purpose of exercise testing after breast cancer treatment is to establish baseline cardiorespiratory function, strength, flexibility and balance, in order to inform a personalized exercise prescription. For women who are not able to complete standard exercise testing owing to low physical functional status, the goal is to establish self-reported and objective physical functional status, in order to inform the recommendations for rehabilitative exercise programming, potentially within the setting of a medical clinic. Breast cancer survivors under 50 years of age who have been treated with chemotherapy and/or radiation should be considered to be in the same exercise testing risk category as women over 50 years of age according to the ACSM guidelines for exercise testing [77], owing to the risk of cardiopulmonary toxicities after radiation and/or chemotherapy. As noted previously, cardiotoxicities (e.g., arrythmias, cardiomyopathies, left ventricular dysfunction or congestive heart failure) that impact on endurance may result from treatment with anthracyclines and/or traztusumab [17]. The incidence of cardiotoxicity in breast cancer survivors varies and is influenced by cumulative doses of chemotherapy, age, radiation therapy, pre-existing cardiac risk factors and concomitant chemotherapy [78]. Furthermore, fitness professionals should screen for common persistent symptoms and toxicities from treatment – including those noted previously in this article – prior to testing, and appropriately alter exercise test timing, mode and intensity according to the responses from these screenings; for example, if chronic fatigue is an issue, the testing should be scheduled during the time of day when the individual feels most well-rested. It should be noted that the types of cardiac screening tests that would be most useful for assessing cardiotoxicity brought on by prior chemotherapy treatment can neither be carried out nor interpreted by fitness professionals and must be conducted by a physician.

The types of exercise tests that might be useful include evaluation of cardiopulmonary endurance (e.g., a 6-min walk test) [79]; musculoskeletal strength (e.g., one-repetition maximum testing) [80]; flexibility (e.g., range of motion assessments) [77]; and balance (e.g., ability to stand on one leg) [81]. Balance may be altered owing to neuropathies after treatment with taxanes or general deconditioning. Physicians should be ready to provide assistance and additional time for navigating exercise equipment and facilities. The types and intensity of exercise assessments will also need to vary according to the precancer fitness level of a specific survivor.

For the most part, exercise testing should focus on functional testing, rather than the types of exercise testing that might be used to test performance in elite athletes, since this will better reflect the level of ability and goals of most breast cancer survivors. It is expected that breast cancer survivors will be deconditioned after finishing treatment. Therefore, the intensity of testing activities should initially be conservative. For strength testing, we previously noted that multiple studies have included breast cancer survivors with and without lymphedema in one-repetition maximum testing with no reported adverse events [31,33,38]. Therefore, it appears that this is a test that can be used in this population. Any testing, including strength testing, should be symptom limited. Given the high incidence of arm and shoulder morbidity in the breast cancer survivor population, push-up tests (which are commonly used to assess muscle strength and endurance) should be avoided.

Exercise prescription guidance for breast cancer survivors

Each breast cancer survivor will have her own goals that she wants to achieve from an exercise program. Common goals will probably include regaining and improving physical function, aerobic capacity, strength and flexibility, in order to improve body image, body composition, physical fitness and to reduce the risk of recurrence.

There are published guidelines for the mode, frequency, intensity and duration of exercise recommended for improving and maintaining health [104]. In order to discuss how this guidance needs to be altered for the breast cancer survivor, it is necessary to establish what those guidelines are. Box 1 presents the recently published guidelines for physical activity for all Americans and for adults over 65 years of age from the US Department of Health and Human Services (DHHS). In addition, the American Cancer Society (ACS) has published some very general guidance that cancer survivors who have completed treatment should follow physical activity guidelines for the general public to the extent that their health allows [82]. However, to be more specific, the available evidence from completed randomized controlled trials in breast cancer survivors indicates that no alterations to the US DHHS guidelines for aerobic exercise for the general population are needed for breast cancer survivors who have completed treatment. In addition, the US DHHS physical activity guidelines do not mention flexibility activities, but guidance from the ACS and results from the published randomized controlled trials suggest that flexibility exercises would probably be helpful to breast cancer survivors in assisting with the return of full shoulder and arm mobility after breast cancer treatment [82].

The key concern with strength training for breast cancer survivors has been the risk of lymphedema onset or exacerbation. Results of multiple trials indicate that this risk aversion is unwarranted [30 –36]. One of these studies even included women with interlimb differences greater than 40%, indicating that there may be no upper limit in lymphedema severity for this type of exercise [33]. However, it seems prudent to avoid upper body exercise, such as strength training, during an active flare-up that requires therapist-delivered treatment or a bout of cellulitic infection requiring antibiotics. Strength training can be started during active treatment and continue beyond the end of treatment without fear that this will result in the development or worsening of lymphedema. Most studies of strength training in breast cancer survivors start with 8 or more weeks of twice-weekly supervised training in order to ensure that participants learn the proper biomechanics and how to progress their training over time. Upper body strength training should be started with low resistance (the lightest possible resistance for a given exercise [e.g., 1 kg dumbbells or the ‘top plate’ on a machine]) and should also progress slowly (e.g., progress from 0.5 kg or by ‘half-plates’ after several sessions). Survivors should be taught to pay close attention to symptom responses and to reduce resistance if the affected side of the body starts to feel heavy, tired, full or achy. Women with lymphedema should wear a well-fitting compression garment during strength training. The majority of the protocols reviewed employed strength training two-or three-times weekly; therefore, this appears to be a safe frequency in this population. Finally, after instances of the inevitable breaks from exercise that occur owing to life events (e.g., vacations, family care and work), survivors should be instructed to begin again in terms of resistance level and to rebuild resistance slowly, to avoid injury or inflammatory responses that may overwhelm an already compromised lymphatic system. An example of an inflammatory response would be a hot, red area on the arm, indicating that there is some acute inflammatory reaction occurring in the affected area, particularly if accompanied by a fever. This could be indicative of a cellulitic infection requiring immediate antibiotic treatment [105].

Although there is no need for altering aerobic training guidelines for this population and only minor adaptations to strength training, there is a need for additional monitoring for cardiovascular and pulmonary late-effects among survivors treated with radiation and/or chemotherapy. These issues do not require testing prior to starting an exercise program. However, fitness professionals and survivors should be taught to pay closer attention to cardiac and pulmonary symptoms in breast cancer survivors compared with the average woman, particularly among younger breast cancer survivors, in whom cardiac or pulmonary symptoms might be inappropriately discounted. Examples of parameters that it might be useful to monitor more closely in this population include the frequency and severity of arrhythmias, dyspnea and angina. We are unaware of any published observations of any effects on blood pressure response to exercise in breast cancer survivors.

Box 1.

US Federal Guidelines for physical activity for adults and older adults.

For all individuals, some activity is better than none. Physical activity is safe for almost everyone, and the health benefits of physical activity far outweigh the risks.

People without diagnosed chronic conditions (e.g., diabetes, heart disease or osteoarthritis) and who do not have symptoms (e.g., chest pain or pressure, dizziness or joint pain) do not need to consult with a healthcare provider concerning physical activity.

Adults (18–64 years of age)

Adults should do 2 h and 30 min a week of moderate-intensity aerobic physical activity, or 1 h and 15 min (75 min) a week of vigorous-intensity aerobic physical activity or an equivalent combination of moderate- and vigorous-intensity aerobic physical activity. Aerobic activity should be performed in episodes of at least 10 min, preferably spread throughout the week.

Additional health benefits are provided by increasing to 5 h (300 min) a week of moderate-intensity aerobic physical activity, 2 h and 30 min a week of vigorous-intensity physical activity or an equivalent combination of both.

Adults should also perform muscle-strengthening activities that involve all major muscle groups, performed on 2 or more days per week.

Older adults (65 years of age and older)

Older adults should follow the adult guidelines.

If this is not possible owing to limiting chronic conditions, older adults should be as physically active as their abilities allow.

Older adults should avoid inactivity.

Older adults should do exercises that maintain or improve balance if they are at risk of falling.

Adults with disabilities

Adults with disabilities should follow the adult guidelines.

If this is not possible, adults with disabilities should be as physically active as their abilities allow.

Adults with disabilities should avoid inactivity.

Data from [103].

There are many other forms of exercise that are of interest to breast cancer survivors beyond cardiovascular exercise, strength training or stretching; for example, there are over 125 dragon boat racing teams around the world that are made up solely of breast cancer survivors [106]. This activity, which can be described as synchronized rowing in a large, skinny canoe with between 20 and 30 rowers, appears to be safe for survivors, given that over 2000 survivors have participated to date. However, rigorous empirical testing of this form of exercise remains to be completed. There are no studies into the risks or benefits of specific sport activities for breast cancer survivors; however, there is plenty of anecdotal evidence that women who were active in a particular sport prior to breast cancer treatment can return to the activity after treatment. Empirical testing of this issue remains to be completed.

Finally, there are three popular forms of exercise in US women that require particular attention: Pilates, yoga, and ‘Curves’. There have been two randomized controlled trials of the safety and efficacy of yoga for breast cancer survivors who have completed treatment [65,83].

These studies indicate that yoga is safe and may be useful for improving QOL and other outcomes, but more rigorous testing in a large, long-term randomized trial is still needed. Finally, there have been no randomized controlled trials to assess the safety or efficacy of the activities performed at the commercial fitness centers known as ‘Curves’ or for Pilates. Given the popularity of these activities and that both activities include elements of strength training, it is important that the safety of Curves and Pilates be tested prior to concluding that they are safe for survivors with risk and at risk for lymphedema (e.g., women who have had lymph nodes removed and/or treated with radiation to the axilla) and other arm and shoulder problems.

Summary

To summarize, the persistent negative effects of breast cancer treatment result in altered risks associated with and an altered need for exercise testing and training. The results of 38 randomized controlled trials in this population indicate that exercise is well-tolerated, despite commonly experienced toxicities that alter the body systems that are needed for and impacted by exercise training. There is evidence that exercise after breast cancer treatment can improve aerobic fitness, strength, flexibility, physical function, shoulder function, QOL and symptoms and side effects, while also reducing fatigue and pain.

There is also ample evidence that upper body exercise is safe for women with risk and at risk for lymphedema.

There are persistent negative effects of breast cancer treatment that should be acknowledged in developing an appropriate exercise assessment and prescription for breast cancer survivors. However, for the most part, breast cancer survivors should follow the same physical activity guidelines recommended for the health of adults or older adults, including regular cardiovascular exercise, strengthening exercises and activities that improve flexibility and balance. Regular performance of these activities will probably improve the experience of survivorship, both medically and psychologically.

Research gaps

Despite the fact that there have been 38 randomized controlled trials of exercise intervention in breast cancer survivors who have completed treatment, multiple questions remain unanswered; for example, it is generally accepted that precancer weight and fitness status are important considerations in determining what activities are safe and appropriate after cancer treatment. However, our knowledge of the interaction of precancer fitness with safe and effective exercise prescriptions lacks specificity. Research regarding safe methods to facilitate a return to competitive athletic activities is needed.

Research on the effects of exercise training on numerous frequently experienced persistent negative effects of treatment is scant or nonexistent, including shoulder function, pain, objective physical functional status, menopausal symptoms, bone health, neuropathies and cognitive effects, as well as cardiac and pulmonary toxicities. It should also be noted that few studies have targeted ethnic minority breast cancer survivors. Many physical activity interventions for cancer survivors that aim to improve physiological and psychological outcomes do not target participants on a needs-based approach. Participants are rarely recruited for physical activity intervention studies based on their need for improvement in the given outcome of interest (e.g., low fatigue level, poor QOL or low physical function). Rather, a ‘come one, come all’ approach is often used. It could be argued that because of this approach, interventions may actually only be testing feasibility and not true efficacy or effectiveness of intervention effects.

Finally, there is a need for the research community to agree on standardized outcome measures and methods of intervention assessment.

The current variability in outcome measures across studies hampers the ability to draw firm conclusions regarding the effects of exercise.

Future perspective

At present, the field of exercise and cancer survivorship is a beehive of emergent activity. There are webinars, books and certification programs emerging to train fitness professionals in how to work with cancer survivors (including offerings from the ACSM). There is a partnership between the Lance Armstrong Foundation (LAF) and the National YMCA called ‘LiveSTRONG at the YMCA’ that is working to make the YMCA the destination of choice for cancer survivors interested in fitness activities and to be sure that the YMCA staff are ready to meet the unique needs of cancer survivors. There are LAF-funded Cancer Survivorship Centers of Excellence in eight cities across the USA that are trying to find ways to promote the health and well-being of cancer survivors, including wellness offerings. The ACS has published general guidelines regarding physical activity for cancer survivors [82]. However, in June 2009, the ACSM convened a roundtable of research experts of exercise and cancer survivorship to develop the first official ACSM position on exercise for cancer survivors, which will be much more specific than the prior ACS guidelines. Publication of these guidelines (expected in 2010) is intended to give patients, health professionals and fitness professionals more focused guidance on safe and effective exercise testing and prescription for cancer survivors. Publications of exercise trials in cancer survivors have received tremendous press recently, including articles in the ‘Science Times’ section of the New York Times newspaper associated with one New England Journal of Medicine paper [34,107]. Independent cancer exercise programs are emerging in many large US cities, led by a vanguard of fitness and healthcare professionals who see that the well-documented physiologic benefits of exercise training are well suited to assisting cancer survivors with preventing, attenuating or recovering from the negative persistent effects of cancer. Efforts are underway at multiple comprehensive cancer centers across the USA to find ways of translating the results of the evidence-based exercise research reviewed in this article into providing better and more consistent physical therapy for breast cancer patients so that they are better able to participate in exercise after their treatment is completed. This groundswell of activity creates the potential for a larger, more organized effort to make exercise programming for rehabilitation after breast cancer treatment part of the standard of care in all cancer treatment centers. Whether this will happen depends largely on the following:

Additional research to further demonstrate the safety and efficacy of exercise training among cancer survivors;

The ability to demonstrate that such efforts will save money by reducing healthcare costs among the growing population of cancer survivors;

The ability to convince medical, surgical and radiation oncologists, as well as physical therapists who work with cancer survivors, that exercise is both safe and effective for addressing the needs of their patients;

Building the capacity in the fitness industry and/or within physical therapy clinics to provide exercise programming that is safe and effective for the growing population of cancer survivors.

There is little doubt that the additional research on the safety and efficacy of exercise for the major outcomes yet to be studied will occur in the next 5–10 years, including the outcomes noted previously in this article. However, this research will only translate into substantive changes in the standard of care if evidence regarding cost–effectiveness becomes available.

If such evidence can be provided, this may drive an effort to build the capacity for exercise programs in the fitness industry and/or physical therapy clinics. The other major challenge to altering the standard of care for breast cancer survivors is finding ways to convince clinicians who treat cancer that exercise is safe and effective for their patients. This might be a catch-22 situation with regard to building the capacity for the programs, in that it may require clinicians to be convinced to build the referral base for these programs, yet the clinicians might not be convinced until they see the local capacity to deliver the programs safely and effectively. The opportunity exists, with the current groundswell of activity in the arena of cancer survivorship and exercise, to substantially alter the experience of the 2.4 million breast cancer survivors alive in the USA today.

Executive summary

Persistent negative effects observed after breast cancer treatments

Negative effects following different types of surgery include:

– Breast surgery: post-mastectomy pain syndrome, scarring, change in sensation, shoulder impairment, lymphedema, sensory or motor neuropathies, altered physical function of arm and/or shoulder and deconditioning.

– Oophrectomy/ovarian ablation: premature menopause, bone loss, vasomotor symptoms and weight gain.

Negative effects after chemotherapy include weight gain, cardiotoxicity, pulmonary tissue damage, autonomic nervous system dysfunction, peripheral sensory and motor neuropathies, cognitive changes and fatigue.

Negative effects after radiation include lymphedema, pulmonary and cardiac toxicities, sustained immune suppression, nerve damage, arm and shoulder morbidities and fatigue.

Negative effects after hormonal therapy include vasomotor symptoms, bone loss, cognitive changes and weight gain.

Physical function changes following cancer treatment may alter the aging trajectory towards the loss of the ability to live independently.

Risk of adverse effects of exercise among breast cancer survivors who have completed surgery, radiation & chemotherapy

Fear of exercise in women with anemia is often greater than is warranted, although the risks of vigorous exercise among immuneimpaired individuals are acknowledged.

Fear of lymphedema from exercise may be greater than is warranted, given the consistent evidence of a lack of increased onset or worsening of lymphedema in randomized controlled exercise interventions. However, caution is urged with regard to doing too much exercise too soon. Advice regarding increasing upper body exercise gradually and following guidance for protecting an arm that is at risk is acknowledged.

Not enough data exist regarding the risk of exercise on the 35–58% of women with arm and shoulder problems to draw many conclusions.

Symptoms that are limited to one-repetition maximum testing have been observed to be safe.

Adverse events data from research studies are flawed since they rely on self-report from participants, and those with the most severe side effects are likely to drop out of exercise studies, so their side effects may never be recorded.

Effects of exercise on persistent negative effects of cancer treatment

There is evidence from randomized controlled trials that exercise training improves aerobic fitness, physical function, strength, body composition, fatigue, quality of life, other psychosocial outcomes, other symptoms/side effects and pain, shoulder function, bone health, immune function and lymphedema symptoms.

There are seven completed randomized controlled trials that have assessed the safety of upper body exercise among breast cancer survivors with risk or at risk for lymphedema. Each of these trials demonstrates the safety of upper body exercise for this population.

Effects of exercise on breast cancer recurrence & mortality

There are multiple observational studies that have reported inverse associations of physical activity before and after breast cancer diagnosis, as well as the risk for recurrence or death from breast cancer.

Guidance for exercise testing in breast cancer survivors

The American College of Sports Medicine (ACSM) provides guidance for safe and effective exercise testing.

Revisions to the ACSM guidelines are warranted for breast cancer survivors, including revisions to the timing of exercise after treatment, which should allow for hematologic and immune recovery. No testing during fever, ataxia or extreme fatigue should be carried out. Testing staff should screen for common persistent effects and alter testing accordingly.

Types of testing that would be useful include cardiorespiratory endurance, musculoskeletal strength and endurance, flexibility and balance testing.

Guidance for exercise prescription in breast cancer survivors

Prescription should fit the goals of the woman.

Guidelines for physical activity for all healthy Americans should be followed, with a few alterations (e.g., women with lymphedema should wear a well-fitting compression garment while doing strength training).

Exercises to improve balance should be performed if the patient is at risk of falling.

Flexibility exercises may be warranted in order to regain a full range of motion after treatment.

Research gaps

We know little about the return to competitive athletic activities after cancer.

We know little about the interaction of precancer fitness and the safety and effectiveness of exercise programs after cancer.

Very little research has focused on a multitude of frequently experienced persistent effects of breast cancer, including shoulder function, pain, objective physical functional status, menopausal symptoms, bone health, neuropathies, cognitive effects or cardiac or pulmonary toxicities.

Few studies have focused on ethnic minority breast cancer survivors.

Studies should focus on recruiting those who need the intervention (e.g., if the intervention is designed to help with fatigue, the participants recruited should have experienced fatigue).

There is a need for standardizing outcomes and methods in this research arena.

Future perspective

There is a groundswell of activity in the field of exercise and cancer survivorship

This groundswell creates an opportunity to alter the standard of care to include exercise as rehabilitation for breast cancer survivors.

There is a need to build a capacity in the fitness industry and/or within physical therapy clinics for the provision of exercise programming that is safe and effective for the growing population of cancer survivors.

Footnotes

The authors have no relevant affiliations or financial involvement with any organization or entity with a financial interest in or financial conflict with the subject matter or materials discussed in the manuscript. This includes employment, consultancies, honoraria, stock ownership or options, expert testimony, grants or patents received or pending, or royalties.

No writing assistance was utilized in the production of this manuscript.

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Risks and Benefits of Physical Activity among Breast Cancer Survivors who have Completed Treatment

Abstract

Keywords

Breast cancer treatments & associated persistent adverse effects

Surgery

Chemotherapy

Radiation

Hormone therapy

Tamoxifen

Aromatase inhibitors

Physical function changes with breast cancer

Summary

Risks of adverse effects of exercise among breast cancer survivors

Effects of exercise training on the persistent negative effects of breast cancer treatment

Aerobic fitness

Physical function

Strength

Body composition

Fatigue

Lymphedema

Quality of life

Other psychosocial outcomes

Symptoms/side effects & pain

Shoulder function

Bone health

Immune function

Effects of physical activity on breast cancer recurrence & mortality

Guidance for exercise testing & prescription in breast cancer survivors

Exercise testing guidance for breast cancer survivors

Exercise prescription guidance for breast cancer survivors

Summary

Research gaps

Future perspective

Footnotes

References