Journal of Cancer Survivorship

, Volume 5, Issue 4, pp 320–336

Exercise in patients with lymphedema: a systematic review of the contemporary literature

  • Marilyn L. Kwan
  • Joy C. Cohn
  • Jane M. Armer
  • Bob R. Stewart
  • Janice N. Cormier
Reviews

Abstract

Background

Controversy exists regarding the role of exercise in cancer patients with or at risk for lymphedema, particularly breast. We conducted a systematic review of the contemporary literature to distill the weight of the evidence and provide recommendations for exercise and lymphedema care in breast cancer survivors.

Methods

Publications were retrieved from 11 major medical indices for articles published from 2004 to 2010 using search terms for exercise and lymphedema; 1,303 potential articles were selected, of which 659 articles were reviewed by clinical lymphedema experts for inclusion, yielding 35 articles. After applying exclusion criteria, 19 articles were selected for final review. Information on study design/objectives, participants, outcomes, intervention, results, and study strengths and weaknesses was extracted. Study evidence was also rated according to the Oncology Nursing Society Putting Evidence Into Practice® Weight-of-Evidence Classification.

Results

Seven studies were identified addressing resistance exercise, seven studies on aerobic and resistance exercise, and five studies on other exercise modalities. Studies concluded that slowly progressive exercise of varying modalities is not associated with the development or exacerbation of breast cancer-related lymphedema and can be safely pursued with proper supervision. Combined aerobic and resistance exercise appear safe, but confirmation requires larger and more rigorous studies.

Conclusions

Strong evidence is now available on the safety of resistance exercise without an increase in risk of lymphedema for breast cancer patients. Comparable studies are needed for other cancer patients at risk for lymphedema.

Implications for cancer survivors

With reasonable precautions, it is safe for breast cancer survivors to exercise throughout the trajectory of their cancer experience, including during treatment.

Keywords

Lymphedema Breast cancer Exercise Physical activity Systematic review Literature review 

Introduction

Lymphedema is a condition of the lymphatic system caused by a disruption of lymph transport. This perturbation leads to the accumulation of protein-rich fluid, resulting in swelling within the subcutaneous tissues of the affected body part [1, 2]. The condition may be acute or chronic, transient or progressive. If left untreated, it can become permanent and disfiguring. The effects of lymphedema on an individual can lead to functional impairment, social and emotional distress, and poor quality of life [3, 4, 5, 6, 7, 8, 9, 10, 11, 12].

Lymphedema can generally be classified into primary and secondary etiologies [13, 14]. Primary lymphedema is rare with no known acquired causes. It develops from an insufficiency in the structure and/or function of the lymphatic system that is characterized by malfunction of the lymphatic system in keeping up with the lymph load demands of the affected body part [14, 15, 16]. Secondary lymphedema, which is more commonly diagnosed in developed countries, is often caused by the disruption or compression of the lymphatic system resulting from tumors or their treatment. A recognized risk factor for secondary lymphedema is the surgical removal of axillary lymph nodes and/or radiation therapy to the axilla for breast cancer treatment, which can result in swelling of the arm, hand, or adjacent trunk quadrant [17]. Lymphedema can also occur in the head/neck region, trunk, and lower extremities following the treatment of head/neck, gynecologic, and genitourinary malignancies [14, 17, 18].

About 12 million cancer survivors currently reside in the USA [19], and at least 2.5 million are female breast cancer survivors [20]. The incidence of breast cancer-related lymphedema (BCRL) is estimated conservatively to be about 26% at 2 years after surgery [17]. Consequently, the risk-reduction and management of treatment sequelae, such as lymphedema, have grown in importance for breast cancer survivors and their clinicians.

The importance of exercise in cancer prevention and control has emerged over the last 20 years [21, 22, 23]. For individuals with chronic conditions such as cancer, it is recommended that these individuals be as physically active as their abilities and conditions allow and to avoid inactivity [24]. Upper body exercise has historically been discouraged for breast cancer survivors following axillary lymph node dissection and/or radiation [25]. This unsubstantiated recommendation stemmed from the belief that upper body exercise might induce or exacerbate upper extremity lymphedema [26, 27]. Beginning with the 1998 seminal study of dragon boat racing in breast cancer survivors [28, 29], recent studies and reviews, including well-designed randomized controlled trials (RCT), have challenged this belief by demonstrating that there is no association between upper body exercise and the onset or worsening of BCRL [30, 31, 32]. Evidence is also emerging which establishes that exercise, including aquatic physical therapy [33] and weight lifting [34], may not exacerbate lower extremity lymphedema.

Given the controversy regarding the role of exercise in patients with or at risk for lymphedema, we performed a systematic review of the peer-reviewed literature from 2004 to 2010 to distill the weight of the evidence and provide best practice recommendations for exercise and lymphedema care. Findings focus predominantly on BCRL as most of the published literature to date addresses lymphedema in breast cancer survivors.

Methods

This systematic review of 2004–2010 literature on exercise and lymphedema management was jointly commissioned by the American Lymphedema Framework Project (ALFP) and the International Lymphoedema Framework (ILF) to update the ILF Best Practices document, which summarized the literature up until 2003[35]. A systematic review of the literature for articles related to exercise and lymphedema was performed in two phases (Fig. 1). For the first phase, a reference librarian searched 11 major medical indices (PubMed-MEDLINE, CINAHL, Cochrane Library databases (Systematic Reviews and Controlled Trials Register), PapersFirst, ProceedingsFirst, Worldcat, PEDro, National Guidelines Clearing House, ACP Journal Club, and Dare) for articles published from 2004 to 2010 using keywords related to lymphedema (lymphedema, lymphodema, lymphoedema, elephantiasis, swelling, edema, and oedema). Article archives of the authors and reference lists from related articles were also examined through 2010. A total of 5,927 articles were retrieved and 4,624 articles not relevant to lymphedema research were excluded by research associates (screen 1). The remaining 1,303 articles were reviewed by two editors for inclusion (lymphedema related, ≥10 cases) and exclusion (non-refereed articles) criteria, and a total of 644 articles were excluded, thus leaving 659 articles for the exercise review (screen 2). Translation was requested for non-English language articles directly from the relevant authors, and duplicate articles were removed. Articles with no English translation available were excluded.
Fig. 1

Literature review process for exercise and lymphedema systematic review (2004–2010)

For the second phase, keywords for exercise were applied (exercise, physical activity, movement, physical therapy, physiotherapy, strength training, resistance training, and aerobic fitness). A total of 39 articles on exercise were selected and subsequently reviewed by the first and second authors (screen 3). Inclusion criteria for the final review included valid epidemiologic study design or literature review (randomized clinical trial, cohort study, case–control study, meta-analysis, and systematic review); primary or secondary study outcome was lymphedema; and evident classification of exercise exposure into a priori domains of resistance exercise, aerobic and resistance exercise, and physical therapy. A total of 20 studies were excluded for the following reasons: case-series design (n = 5), abstract only (n = 3), exercise was outcome or lymphedema was covariate only (n = 3), general exercise and cancer overview with no lymphedema information (n = 2), aquatic therapy or dance (n = 2), duplicate study (n = 1), and other (n = 4). Any disagreements were resolved by discussion in order to arrive at consensus.

The remaining 19 studies met the inclusion criteria for this review (screen 4) and were categorized into the a priori domains of (1) resistance exercise only (n = 7); (2) aerobic and resistance exercise combined (n = 7); and (3) other exercise, primarily physical therapy (n = 5). Each article was summarized by one author and reviewed by the other author to ensure appropriate and accurate representation of the material. Information was abstracted on study design/objectives, participants, outcomes, intervention, results, and study strengths and weaknesses. The two authors rated the totality of the evidence in the three exercise domains using the research grading system from the Oncology Nursing Society (ONS) Putting Evidence into Practice® (PEP) classification (Table 1) [36]. The final PEP rating (recommended for practice, likely to be effective, benefits balanced with harms, effectiveness not established, effectiveness unlikely, and not recommended for practice) was agreed upon by consensus among all authors. This PEP rating system was chosen due to its high reliability and accessibility for evidence-based practice guidelines when compared with other published rating methods [37].
Table 1

Putting Evidence into Practice® (PEP) Weight-of-Evidence Classification Schema

Weight-of-evidence category

Description

Examples

Recommended for practice

Effectiveness is demonstrated by strong evidence from rigorously designed studies, meta-analyses, or systematic reviews. Expected benefit exceeds expected harms

At least two multisite, well-conducted, randomized, controlled trials (RCTs) with at least 100 subjects

Panel of expert recommendation derived from explicit literature search strategy; includes thorough analysis, quality rating, and synthesis of evidence

Likely to be effective

Effectiveness has been demonstrated by supportive evidence from a single rigorously conducted controlled trial, consistent supportive evidence from well-designed controlled trials using small samples, or guidelines developed from evidence and supported by expert opinion.

One well-conducted RCT with fewer than 100 patients or at one or more study sites

Guidelines developed by consensus or expert opinion without synthesis or quality rating

Benefits balanced with harms

Clinicians and patients should weight the beneficial and harmful effects according to individual circumstances and priorities

RCTs, meta-analyses, or systematic reviews with documented adverse effects in certain populations

Effectiveness not established

Data currently are insufficient or are of inadequate quality.

Well-conducted case control study or poorly controlled RCT

Conflicting evidence or statistically insignificant results

Effectiveness unlikely

Lack of effectiveness is less well established than those listed under not recommended for practice

Single RCT with at least 100 subjects that showed no benefit

No benefit and unacceptable toxicities found in observational or experimental studies

Not recommended for practice

Ineffectiveness or harm is clearly demonstrated, or cost or burden exceeds potential benefits

No benefit or excess costs or burden from at least two multisite, well-conducted RCTs with at least 100 subjects

Discouraged by expert recommendation derived from explicit literature search strategy; includes thorough analysis, quality rating, and synthesis of evidence

Based on information from Mitchell and Friese [36]

Summary of selected studies

Resistance exercise studies (Table 2)

Table 2

Summary of lymphedema resistance exercise studies (2004–2010); overall recommendation: likely to be effective

Author (year)

Study design/objectives

Participants

Outcomes

Intervention

Results

Study strengths

Study weaknesses

Schmitz (2009) [38]

RCT to examine the effect of twice-weekly progressive weight lifting

141 breast cancer survivors with stable LE

(1) Change in arm and hand swelling as measured by water displacement

Studying group (n = 71): twice-weekly (90 min) supervised weight lifting for 13 weeks followed by twice-weekly unsupervised exercise for 39 weeks

130 women completed follow-up at 1 year

Largest study to date to examine weight lifting in breast cancer survivors with LE

Evaluations for LE exacerbations not completed by a single therapist

(2) Incidence of exacerbations of LE, number and severity of LE symptoms, muscle strength.

Control group (n = 70): no change in exercise level

Proportion of women with ≥5% increase in swelling similar between groups

Long follow-up

Some participants might have disclosed their randomization during evaluations for perceived exacerbations

Weight-lifting group had improvement in self-reported severity of LE symptoms, upper and lower body strength, and a lower incidence of LE exacerbations

Weight-lifting protocol with no upper limit on resistance level

No serious adverse events reported

Intervention delivered in community centers

Included diverse population 1 to 15 years post-treatment

Schmitz (2010) [41]

RCT to examine the effect (safety) of twice-weekly progressive weight lifting

154 breast cancer survivors at risk for BCRL

(1) Change in arm and hand swelling as measured by water displacement

Study group (n = 71): twice-weekly (90 min) supervised weight lifting for 13 weeks followed by twice-weekly unsupervised exercise for 39 weeks

134 women completed follow-up at 1 year

Largest study to date to examine weight lifting in breast cancer survivors

Marginal significance of a treatment effect on lean mass

(2) Clinician-defined BCRL based on the Common Toxicity Criteria version 3.0 criteria including interlimb differences, changes in tissue tone or texture, and symptoms

Control group (n = 70): no change in exercise level

Proportion of women who had incident BCRL onset was 11% in the intervention group and 17% in the control group

Long follow-up

Among women who had ≥5 nodes removed, incident BCRL onset was 7% in intervention group and 22% in the control group

Weight-lifting protocol with no upper limit on resistance level

Clinician-defined BCRL occurred in 1 woman in the intervention group and 3 women in the control group

Intervention delivered in community centers

Included diverse population 1 to 15 years post-treatment

Ahmed (2006) [42]

RCT to examine the effects of weight training on the incidence and symptoms of LE

45 breast cancer survivors (4–36 months status post-axillary node dissection)

(1) Swelling measured using arm circumference (baseline and 6 months)

Study group (n = 23): twice-weekly exercise with fitness trainers for 6 months

Over 6 months, group mean changes in circumference <2 cm

80% adherence

LE measures were secondary outcomes

(2) Self-reported diagnosis and symptoms

Control group (n = 22): no exercise program

At 6 months, 2/16 in study group and 1/16 in control group reported onset of LE

Validated surveys used for LE diagnosis and symptoms

No repeated measures during intervention

At 6 months, 3/23 in control group and 0 in study group reported an increase in LE symptoms

Inadequate capture of transient changes in LE

Sagen (2009) [43]

RCT to evaluate the development of arm LE

204 women with early stage breast cancer status post-axillary node dissection

(1) Difference in volume between the affected and control arms (baseline, 3, 6, and 24 months)

Study group (n = 104): no activity restrictions (NAR) with supervised moderate progressive resistance exercise training 2–3 times a week

Changes in arm volume did not differ significantly: 3 months. LE increased from 5% in the NAR group and 7% in the AR 24 months. LE 13% in both groups

Long-term follow-up

52 dropouts at 24 months

(2) Visual analogue scales (VAS) used to record pain and the sensation of heaviness during physical activity

Control group (n = 100): activity restriction (AR) with standard information to avoid heavy physical activities, usual care physical therapy program weekly for 6 months

Adherence 83% in study group and 89% in control group

(3) Questionnaire recorded upper-limb physical activity, which included intensity, duration, and frequency of activities

Supervised programs

VAS ratings for the affected limb during physical activity significantly higher at 3 and 6 months, but no difference at 24 months

Initial assessments performed before surgery

2 participants developed adhesive capsulitis with immobilization and 1 patient supraspinatus tendinopathy

Objective criteria for defining LE—volume difference >200 ml

Activity level documented in questionnaire

Irdesel (2007) [45]

RCT to test the effect of exercise and compression garments versus exercise alone

19 patients with BCRL

(1) Limb volume calculated from circumferential measurements (before treatment and during 2nd week and 1st,, 3rd, and 6th month)

Study group (n = 10): exercise program consisting of upper extremity range of motion exercises and light resistive exercises 3×/day and prescribed a compression garment (40 mmHg)

For both groups, most measurements did not differ from baseline

Repeated measures and long-term follow-up

Small study

(2) Shoulder range of motion

Control group (n = 9): same exercise program, no compression

For study group, significant improvements in distal measurements (2nd week and 3rd and 6th month)

Exercise program not supervised

(3) Symptoms potentially related to LE such as pain and tender points

For control group, proximal circumference measurements showed significant improvement in only the 1st month

Kilbreath (2006) [44]

RCT to examine the efficacy of resistance and stretching exercise

22 early breast cancer patients 4 to 5 weeks post-surgery

(1) Arm circumference with measures 4–5 weeks after surgery and 8-weeks after intervention

Study group (n = 14): daily exercises aimed at increasing shoulder range of motion and strength (supervised by a physiotherapist 1×/week)

After 8 weeks, a greater proportion of women in the control group had an limb difference ≥2 cm, compared with study group (p = 0.03)

Homogeneity of sample

Small sample size

(2) Range of motion of shoulder and strength

Control group (n = 8): no exercise or additional care

No significant differences for strength and range of motion scores

Early introduction of exercise

Lack of blinding

(3) QOL assessed using Euro QOL-QLQ-C30

Weekly checks and reiteration of exercise protocol

Short-term follow-up only

Sander (2008) [46]

Case crossover series to examine the effectiveness of upper extremity resistive exercise program (6 upper extremity resistive exercises using free weights)

14 breast cancer survivors diagnosed with stage I or II disease at least 6 months post-treatment with no LE history

(1) Arm volume calculated using arm measurements; taken every 1–2 weeks for 15 weeks

Study group 1 (n = 5): exercises 2×/week and 1 repetition maximum (RM)

For both groups, significant increase in the calculated 1 RM for all of the 6 exercises observed

Multiple longitudinal measurements

Small sample size

(2) QOL assessed using the RAND 36-Item Health Survey 1.0 and Functional Assessment of Therapy-Breast (FACT-B)

Study group 2 (n = 5): exercises 3×/week and 1 RM

No changes in arm volume

A-B-A design with each subject serving as own control

(3) Self-report of arm differences

Significant changes in 4 subscales of quality of life

No a priori hypothesis to initiate Group 2 intervention

Lack of randomization and blinding

Level of evidence: likely to be effective

The physical activity and lymphedema (PAL) trial [38, 39] is the largest RCT to date with the longest follow-up to evaluate the impact of weight lifting on lymphedema outcomes in 141 breast cancer survivors previously diagnosed with BCRL [40]. One group of 71 women was randomly assigned to the twice-weekly weight-lifting program with no upper limit on weight progression while the other group of 70 women was assigned to the control group and asked not to change their exercise level during the study. All participants in the weight-lifting group were required to wear a compression garment for the arm and hand while weight lifting. The main outcome was change in arm and hand swelling at 1 year, as measured by an absolute increase of 5% or more by water displacement of the affected and unaffected limbs. Other outcomes included incident exacerbations of lymphedema, amount and severity of lymphedema symptoms, and muscle strength. Compared with the control group, weight lifting did not significantly affect the severity of BCRL, and the regimen decreased the number and severity of arm and hand symptoms, increased muscular strength, and reduced the incidence of lymphedema exacerbations as assessed by a lymphedema specialist. Adherence was high at 85%. Of note, the intervention was delivered in community fitness centers in anticipation of possibly disseminating the weight-lifting program if found to be effective.

A follow-up equivalence study from the PAL trial was published on the impact of the weight-lifting program compared to no exercise on BCRL risk in 154 randomized breast cancer survivors from 1 to 5 years post-breast cancer surgery (including lymph node removal) and no clinical signs of BCRL [41]. Similar to the previous study, incident BCRL was identified by an interlimb difference of 5% or more by water displacement at 1 year follow-up. Progressive weight lifting did not increase the incidence of BCRL: 11% (8/72) in the weight-lifting group and 17% (13/75) in the control group experienced incident BCRL onset (p equivalence = 0.04) while among women with ≥5 lymph nodes removed, 7% (3/45) in the intervention group and 22% (11/49) in the control group had incident BCRL onset (p equivalence = 0.003). Therefore, this study supports the safety of weight lifting in women with breast cancer and suggests that weight lifting will not increase BCRL risk.

The Weight Training for Breast Cancer Survivors study is another RCT that examined the effects of weight training on the incidence and symptoms of lymphedema in 45 breast cancer survivors who were up to 36 months postadjuvant therapy and had axillary lymph node dissection [42]. Women in the intervention group (n = 23) met twice-weekly for weight training sessions over 6 months while women in the control group (n = 22) were told not to change their exercise level during the study. Women with BCRL were not required to wear a compression sleeve during exercise, unless specified by their clinician. Lymphedema onset was measured by a ≥2-cm difference in arm circumference of the affected and unaffected arms, along with self-report of symptoms and clinical diagnosis. No significant change in difference of arm circumferences (p = 0.40), nor self-reported incidence of BCRL (p = 0.22), was found between the two groups. Adherence to the intervention was high (80%). Study limitations were BCRL being a secondary outcome and a few randomly selected cases having BCRL at baseline.

A large RCT of 204 early stage breast cancer patients who had breast surgery including axillary node dissection evaluated the impact of an intervention of two rehabilitation programs, one of no activity restrictions in daily living combined with a moderate resistance exercise program and the other of activity restrictions combined with a usual care program [43]. The no activity restrictions group followed a supervised physical therapy program at an outpatient clinic that emphasized moderate progressive resistance exercise training two to three times per week. The activity restrictions group was told to avoid heavy or strenuous physical activities and participated in the usual care physical therapy program. Arm volume increased significantly over time in both groups in both the affected and unaffected arms (p < 0.001). A study limitation was 25% loss-to-follow-up at 2 years.

Two small RCTs with limited follow-up were conducted to assess the effects of light resistance exercises on BCRL risk [44] and BCRL treatment [45]. Kilbreath et al. recruited 22 breast cancer patients within 4 to 5 weeks post-surgery and randomized them into an exercise group (n = 14) and control group (n = 8) with no blinding [44]. The 8-week exercise program consisted of daily stretches with a Theraband targeted towards increasing shoulder range of motion and shoulder strength. Primary outcomes included difference in arm circumference and self-report of symptoms. Fewer women in the exercise group had interlimb differences of ≥2 cm and in general reported fewer arm and breast symptoms. Irdesel et al. recruited 19 breast cancer survivors diagnosed with BCRL and randomized them into an exercise group (n = 9) and exercise with compression garment group (n = 10) [45]. The non-supervised 6-month exercise program consisted of upper extremity range of motion exercises and light resistive exercises three times a day, with ten repetitions each time. The second group participated in the same exercise program and was also prescribed a compression garment. Primary outcomes were difference in arm circumference, shoulder range of motion, and self-report of symptoms measured at multiple time points over 6 months. Almost all measures were improved in the group who exercised with a compression garment compared with the group who did not wear a garment.

A small study of 14 breast cancer survivors diagnosed with early stage breast cancer who had no history of lymphedema tested the effectiveness of an exercise program consisting of upper extremity resistive exercises using free weights [46]. Two exercise regimens which differed by frequency of exercise (twice vs. three times weekly) were tested in the same group of women. Outcomes were arm volume calculated from arm measurements of both arms and quality of life as measured by validated survey instruments. No significant changes in arm volume were observed, and quality of life measures improved. Study limitations were its small sample size and each case serving as her control.

Aerobic and resistance exercise studies (Table 3)

Table 3

Summary of lymphedema resistance and aerobic exercise studies (2004–2010); overall recommendation: benefits balanced with harms

Author (year)

Study design and objectives

Participants

Outcomes

Intervention

Results

Study strengths

Study weaknesses

Courneya (2007) [47]

Prospective, 3-armed, RCT to examine the effects of aerobic and resistance exercise

242 breast cancer patients receiving adjuvant chemotherapy

(1) QOL and fatigue assessed by FACT-Anemia scale

Study group 1 (n = 78): aerobic exercise training (AET) 3×/week on cycle ergometer, treadmill, or elliptical beginning at 60% of their vo2max for weeks 1–6, progression to 70% weeks 7–12, and 80% beyond week 12; duration at 15 min progressing to 45 min at week 18

No difference between groups in QOL, fatigue, depression, or anxiety

Multicenter recruitment

LE assessed as secondary outcome

(2) Fatigue, psychosocial functioning, physical fitness, and body composition

Study group 2 (n = 82): resistance exercise training (RET) 3×/week—2 sets of 8–12 repetitions of 9 different exercises at 60–70% of 1 repetition maximum (RM); resistance increased by 10% after completing at least 12 repetitions

AET improved self-esteem (p = 0.015), preserved aerobic fitness (p = 0.006), and maintained body fat levels (p = 0.076)

Moderate sample size

70.2% adherence rate

(3) Chemotherapy completion rate

Study group 3 (n = 82): usual care (UC) not to start exercise program

RET improved self-esteem (p = 0.018), muscular strength (p < 0.001), lean body mass (p = 0.015), and chemotherapy completion rate (p = 0.033)

Validated assessment measures

Low recruitment rate

(4) LE assessed using water displacement, measures taken at baseline (1 to 2 weeks after starting chemotherapy), middle of chemotherapy, 3–4 weeks and 6 months after chemotherapy

Repeated measures

Study sample homogeneous with respect to race and education

First study to report strength gains during chemotherapy

Exercise did not result in LE or adverse events

Focus on body composition change

Bicego (2006) [48]

Literature review to assess the effects of aerobic exercise and upper extremity resistance training for women with or at risk for BCRL

6 studies of 177 women (14 w/either pre-existing LE or LE developed during the study) and 2 studies of 45 women with pre-existing LE

Evaluation of study design (2 RCTs), Sackett level of evidence (5 low evidence), and methodological quality

Not applicable

Aerobic exercise and upper extremity resistance training neither initiated nor exacerbated LE

Review of the physiologic rationale for the effect of exercise and compression in at-risk limbs

No tabular summary of study quality, design, interventions, and outcomes

More research required with large sample size, rigorous design, and better outcome measures of LE

Suggestions on improved measurement techniques to assess change in lymphatic function

Cheema (2008) [25]

Systematic review of clinical studies that prescribed progressive resistance training (PRT)

10 clinical trials (4 uncontrolled trials, 1 controlled, and 5 RCTs)

(1) Physiological, functional, and psychological outcomes

Not applicable

No exacerbation of LE

Tabular summary of study quality, design, interventions, and outcomes

None

538 breast cancer patients

(2) Study quality assessed using the Delphi for RCTs, non-RCTs, and uncontrolled trials

Breast cancer patients after surgery can receive health-related benefits from PRT

More research required with well-designed RCTs with standardized reporting of interventions and adverse events

De Backer (2009) [49]

Systematic review of the effects of resistance training programs

24 studies (10 RCTs, 4 controlled clinical trials, and 10 uncontrolled trials) of 586 (54%) breast cancer, 196 (13%) prostate cancer, and 428 (25%) with others

Evaluation of study design and methodological quality using 10 defined criteria

Not applicable

Most studies included combination of resistance and aerobic training

Tabular summary display of study quality, design, interventions, and outcomes

None

3 studies focused on LE in breast cancer patients - none found an increase in LE after training

Tabulated exercise intensity

Cardiopulmonary and muscle function improved with training, but no effects found for body composition, endocrine and immune function, and hematological variables

Reviewed studies in patients with various malignancies

Poage (2008) [50]

Literature review of the effective interventions for the treatment of secondary LE

218 articles (1997–2007)

(1) Evidence-based review of clinical practice guidelines, systematic reviews, and research studies

Not applicable

Interventions recommended: complete decongestive therapy (CDT), compression bandaging, and infection treatment with antibiotics

Systematic literature review with a clinical focus

None

(2) Studies categorized according to Oncology Nursing Society Weight of the Evidence classification system

Interventions likely to be effective: maintain optimal body weight and manual lymph drainage (MLD)

Developed evidence tables

Interventions of benefits balanced with harms: exercise, prophylactic antibiotics for recurrent infections, and surgery

Interventions of effectiveness is not established: compression garments, hyperbaric oxygen, low-level laser therapy, nanocrystalline silver dressing on lymphatic ulcers, pneumatic compression pump, and simple lymphatic drainage

Interventions not recommended for practice: drug therapy (diuretics and benzopyrenes)

Hayes (2009) [51]

RCT, single-blind trial to evaluate the effect of a supervised, mixed-type exercise program

32 women with LE after breast cancer

LE status assessed by bioimpedance spectroscopy and perometry—measures taken at baseline, immediately post-intervention, and at 12-week follow-up

Study group (n = 16): participated in 12-week mixed-type exercise program, including aerobic and resistance exercise; choice of whether or not to wear a compression garment during the exercise sessions

No changes in mean volume measures over time observed for either group

Repeated measures with the same assessor who was blinded to study group

Small sample size

Control group (n = 16): taught to continue habitual activities

2 women in the study group no longer had evidence of LE

70% adherence

Response bias most likely present with more active, educated, affluent women in study

38% lacked measurable LE at baseline

No assessment of compression use during exercise

Portela (2008) [52]

3-arm RCT to explore the feasibility of exercise program

44 breast cancer survivors who had received breast surgical treatment within the past 5 years (only 34 completed the study)

(1) Functional evaluation measured using the disabilities of the arm, Shoulder, and Hand (DASH) questionnaire

Study group 1: Gym-exercise group and home-exercise group met with physical therapists for training in their assigned exercise program. Both groups performed 2 resistance training session and 3 aerobic training sessions per week for 26 weeks

Decrease in self-reported disability in gym and home groups, but not in control

1 physical therapist blinded to group assignment

Small sample size

(2) Shoulder range of motion examined through goniometry

Study group 2: Gym-exercise group met with the staff once a week, whereas the home-exercise group met with the staff once a week for the first 3 weeks and then met once a month

Increase in flexion range of motion in gym, but not in home or control groups

2 intervention groups (gym exercise and home exercise)

10 participants did not complete the study

(3) Exercise tolerance assessed by a 12-min walk test

Control group: received usual care provided by their physicians

No differences in shoulder abduction in any group

 

Low adherence rate (47% for aerobic exercise and 63% for strengthening exercise in the gym-exercise group; 71% for aerobic exercise and 86% for strengthening exercise in the home-exercise group)

(4) Handgrip strength examined using a hand-held dynamometer

Increase in external rotation in gym and home groups but not in control

(5) QOL—Spanish version FACT-B

Increase in the 12-minute walk test only in home group but not in gym and control group

(6) Development of LE—volumetric edema gauge

No significant effects in BMI, handgrip strength, and QOL among 3 groups

For the endurance training, all achieved the 30-minute duration at the set intensity

Adverse effects in exercise programs included high blood pressure, severe headache, hypoglycemia

Level of evidence: benefits balanced with harms

The Supervised Trial of Aerobic Versus Resistance Training was a multicenter RCT in Canada of 242 breast cancer patients initiating adjuvant chemotherapy randomly assigned to usual care (n = 82), supervised resistance exercise (n = 82), or supervised aerobic exercise (n = 78) for the duration of their chemotherapy (median = 17 weeks) [47]. Lymphedema was a secondary outcome and measured by water displacement while the primary outcomes were cancer-specific quality of life and fatigue. Neither the resistance exercise training nor the aerobic exercise training triggered the onset of lymphedema. One study limitation was a low adherence rate of 70.2%.

Four literature reviews have been conducted on the safety of aerobic and/or upper resistance exercise in breast cancer survivors, with a secondary focus on BCRL [25, 48, 49, 50]. Two of these reviews focused primarily on resistance exercise, yet in the context of the review, the authors evaluated trials that examined a combination regimen of resistance and aerobic exercise [25, 49]. All reviews concluded that breast cancer patients can derive health-related and clinical benefits from various exercise programs and that exercise neither initiated nor exacerbated BCRL symptoms [48, 50]. Methodological limitations in study design and sample size were acknowledged. The reviews also called for more robustly designed RCTs of targeted exercise regimens with long-term follow-up during breast cancer treatment to rigorously test the effects of aerobic exercise and upper resistance exercise in breast cancer survivors.

A small pilot RCT of 32 breast cancer survivors with lymphedema were randomized into an exercise intervention group (n = 16) and control group of usual care (n = 16) [51]. The exercise program was 20 group sessions of a supervised, 12-week mixed-type exercise program, including aerobic and resistance exercise, and use of a compression sleeve was left up to the participant’s discretion. Lymphedema was assessed by bioimpedance spectroscopy (impedance ratio between limbs) and perometry (volume differences between limbs) at baseline, immediately after each exercise session, and at 12-week follow-up. No change in mean ratio and volume measures were observed over time. Study limitations were 38% of the participants lacking measurable evidence of BCRL at baseline and a low adherence rate of 70%.

Another small pilot RCT tested the feasibility of implementing a mixed aerobic and resistance exercise intervention by assigning 44 women previously diagnosed with breast cancer who had surgery to one of three groups: gym exercise, home exercise, and non-exercise [52]. Both exercise groups were initially trained by physical therapists and then participated in two resistance training sessions and three aerobic training sessions per week for 26 weeks. A volumetric edema gauge was used to monitor the onset of BCRL. Overall, the side effects were minimal in both exercise groups after participating in the study, although study limitations included a high proportion of dropouts (n = 10) and low adherence rates of 47% for aerobic exercise and 63% for strengthening exercise in the gym-exercise group, and 71% for aerobic exercise and 86% for strengthening exercise in the home-exercise group.

Other exercise studies (Table 4)

Table 4

Summary of other lymphedema exercise studies (2004–2010); overall recommendation: effectiveness not established

Author (year)

Study design/objectives

Participants

Outcomes

Intervention

Results

Study strengths

Study weaknesses

Torres Lacomba (2010) [57]

RCT to examine the effectiveness of early physiotherapy

120 breast cancer patients after axillary lymph node dissection

>2 cm increase in arm circumference compared to non-affected arm

Study group (n = 60): treated by a physiotherapist with a program of manual lymph drainage, massage of scar tissue, and shoulder exercises; educational instruction about risk and prevention of lymphedema

116 women completed 1 year follow-up

Treatment allocation was blinded

Assessment of arm circumference change not completed by single physiotherapist

Control group (n = 60): received educational instructional only

Secondary lymphedema was more likely to be diagnosed in the control group compared with the study group (HR = 0.26; 95% CI, 0.09, 0.79)

Randomized groups of moderate size

Only 1 measure of BCRL prone to measurement error

Long follow-up

Kilgour (2008) [53]

RCT to examine the effectiveness of a self-administered, home-based exercise (HBE) rehabilitation program

27 breast cancer patients after axillary node dissection

(1) Shoulder range of motion, strength, and grip strength

Study group (n = 16): followed an 11-day HBE rehabilitation program of shoulder flexibility, stretching exercises described on videotape, 2 sets/day at 10–15 min/set

Study group showed greater increase in shoulder flexion range of motion (p = 0.003) and abduction range of 2motion (p = 0.036)

All assessments conducted by a single certified athletic therapist

Small sample size

(2) Forearm circumferences on both arms measured before surgery and at 3 and 14 days post-surgery

Control group (n = 11): usual and standard information, including information about diet, skin care, and a brochure—“Exercise Guide after Breast Surgery”

No significant differences in shoulder strength

Presurgical assessment of limb circumference

No long-term follow-up

(3) Diaries to monitor medication use, pain ratings, and ratings of perceived exertion during intervention period.

Increases in external rotation (p = 0.036) and grip strength (p = 0.001) in both groups

∼50% of women did not complete the exercise video intervention

Significant decrease in forearm circumferences over time (p < 0.001) in both groups

Beurskens (2007) [55]

RCT to examine the efficacy of physiotherapy on shoulder function, pain and QOL

30 breast cancer patients after axillary lymph node dissection

(1) Pain in shoulder/arm using visual analogue scale

Study group (n = 15): physiotherapy (advice and arm and shoulder exercises) 2 weeks after surgery, 1–2×/weekly for the first 3 weeks, and 1×/week total number of treatments, 9. Home exercises for 10 min/day for 3 months

After 3 and 6 months, study group showed improvement in shoulder mobility and had less pain

Researcher blinded to treatment allocation

Small sample

(2) Shoulder mobility using a digital inclinometer

Control group (n = 15): leaflet containing advice and exercises for the first week after surgery

No change in handgrip strength and arm volume between the groups

Homogeneity of sample

LE a secondary outcome

(3) Shoulder disabilities during daily activities (Disabilities of the Arm, Shoulder and Hand [DASH] questionnaire)

10 patients study group reported improvement in participation in social activities and less avoidance of heavy household work

Patients in study group had physiotherapy done in a private practice of their choice (n = 15), no observations of compliance

(4) LE—water displacement

Improvement of shoulder mobility and shoulder/arm disabilities in the study group

Duration of exercise treatment varied from 1 to 3 months

(5) Grip strength -hand-held dynamometer

Only general details of physiotherapy intervention provided

(6) QOL—sickness impact profile-short questionnaire

de Rezende (2006) [56]

RCT to compare 2 physiotherapy schemes, directed or free, on shoulder function and lymphatic disturbance

60 breast cancer patients after axillary node dissection

Shoulder movements measured with a universal full-circle manual goniometer

Study group 1 (n = 30): directed group performed physiotherapy with a regimen of 19 exercises

Directed group 1 with better flexion, adduction, and external rotational movements of the shoulder

Details of physiotherapy interventions provided

Small sample size

Daily wound fluid production noted before and after the drains removed

Study group 2 (n = 30): free group performed exercises following the biomechanical physiological movements of the shoulder

No significant difference in lymphatic disturbance between 2 groups

Very early exercise intervention (24 h post-op)

No information on blinding

Measurements of arm circumferences performed with a universal tape measure

3 exercises day #1 after surgery in both groups. At 48 h after surgery, exercises performed in 40-min sessions, 3×/week for 42 days

Incidence of seromas not significantly different between the 2 groups

Lack of long-term follow-up

Few limb measurements—size changes closer to the elbow could have been missed

Moseley (2005) [54]

Case series with a comparison group to examine changes in LE

38 women with unilateral secondary LE related to breast cancer treatment

(1) Arm volume measured by bioimpedance and perometry

Study group (n = 38): 5 exercises combined with deep breathing followed by 1-min rest, 5 × 5 cycles of exercise and breathing over the 10-min period (25 exercises in total)

After 10 min exercise, median reduction in arm volume of 52 ml. (p = 0.004). Reduction sustained at 30 min (p = 0.006), but fluid gradually returned, and by 60 min, the median volume returned to baseline. At 1 month, volume reduced 9%

90% compliance rate in the group who performed the regime over 1-month period

Small sample size

Comparison group was 28 women who received no intervention

(2) Tissue resistance measured by tonometry

After 1 week, 24 women continued the 10-min exercise regime morning and evening for 1 month

Truncal fluid not reduced significantly at any time point

37% dropouts (n = 14)

(3) McGill QOL Questionnaire

Control group (n = 28): no intervention and had previously been monitored for 1 month

Tonometry reading did not change, except at 1 month for the anterior thorax (p = 0.018)

Lack of blinding

(4) Self-report of pain, heaviness, tightness, pins, and needles, cramping, burning sensations, and perceived arm size

Arm heaviness and tightness decreased after exercise regime (p = 0.05, 0.02, respectively), with reduction in tightness being sustained at 24 h (p = 0.00) and reduction in heaviness at 24 h, 1 week, and 1 month

Limited follow-up of 1 month

Sensations of pins and needles reduced at 24 h and 1 week (p = 0.030)

Level of evidence: effectiveness not established

A pilot RCT was conducted on the effectiveness of a home-based exercise rehabilitation program to regain shoulder mobility after mastectomy and axillary node dissection in 27 breast cancer patients [53]. A total of 16 patients were assigned to the rehabilitation group and 11 were assigned to the usual care group. The rehabilitation group followed an 11-day (two sets per day, 10–15 min per set) home-based rehabilitation program consisting of shoulder flexibility and stretching exercises that were described on videotape. The control and rehabilitation groups both received the usual standard information given to post-operative patients, including information about diet, skin care, and a brochure called “Exercise Guide after Breast Surgery.” Forearm circumferences on both arms were measured before surgery and at 3 and 14 days post-surgery to assess for lymphedema. The home-exercise rehabilitation group had a significant increase in shoulder flexion range of motion compared with the usual care group (p = 0.036), and while there was a significant decrease in forearm circumferences over time in both groups (p < 0.001), no difference between the groups was detected.

Several studies have examined the role of physiotherapy, such as standard arm exercises and deep breathing [54], on the post-surgical recovery after breast cancer surgery [55, 56, 57]. Beurskens et al. indicated that the RCT objective was to test the efficacy of a physical therapy treatment on shoulder function, pain, and quality of life in 30 breast cancer patients, yet the details of the treatment regimen were not specified [55]. de Rezende et al. conducted a RCT of directed- or free-physical therapy exercises on shoulder function and lymphatic disturbance in 60 post-operative breast cancer patients but had a short follow-up period of 42 days [56]. Methodological issues such as small sample size, lack of uniform intervention and intervention supervision, short follow-up, and lymphedema assessed as a secondary outcome were apparent in all studies. While study results generally support the role of physical therapy reducing pain, improving shoulder function, benefiting quality of life, and not exacerbating arm swelling, larger, well-designed RCTs with supervision of the intervention to ensure compliance are still needed. More recently, a 2010 RCT study of a physical therapy program consisting of manual lymph drainage, massage of scar tissue, and progressive active and active-assisted shoulder exercises found that women in the physical therapy group were less likely to develop BCRL compared to women in a comparison group which included only an educational strategy [57]. Yet, since the intervention was a mixed regimen, it is unclear if the shoulder exercises were directly associated with the reduction in BCRL risk.

Discussion

In the past 20 years, research efforts have grown to elucidate the benefits of exercise for cancer survivors. This growth has paralleled the gains made in overall cancer survivorship. Yet even today, many patients continue to believe that it is not safe to exercise due to the risk of lymphedema or other surgical or treatment-related complications. In the current systematic review, we found that the majority of exercise studies continue to address lymphedema risk in the breast cancer population. All studies concluded that there is no adverse effect from safe, slowly progressive exercise of varying modalities on the development or exacerbation of BCRL. However, risk of developing BCRL does persist and is reported to range from 13% at 2 years [43]; 17% at 10–40 months [42]; 30% at 18 months [51]; and 17% at 2–6 years post-diagnosis [41]. Aside from studies in breast cancer patients, the literature is very limited with respect to exercise interventions in other patient populations with or at risk for lymphedema.

Benefits of exercise after cancer diagnosis

Numerous benefits of exercise on cancer survivorship have been reported. The 2010 American College of Sports Medicine (ACSM) Exercise Guidelines for Cancer Survivors state that “some of the psychological and physiological challenges faced by cancer survivors can be prevented, attenuated, treated or rehabilitated through exercise” [30]. These benefits include improved flexibility, reduced fatigue, increased strength, improved body image and quality of life, improved body composition, and decreased anxiety. Furthermore, the ACSM guidelines cite that exercise may be associated with a reduced risk of developing a recurrence or secondary cancer. Two additional literature reviews on exercise during cancer treatment also concluded that exercise offers physiologic and psychological benefits [31, 32]. Therefore, with reasonable precautions, it is safe for individuals to exercise throughout the trajectory of their cancer experience, including during treatment. The benefits to be gained by exercise far outweigh the minimal adverse effects reported.

Exercise for a patient who is at risk for lymphedema or has been previously diagnosed with lymphedema has been controversial until recent years. Clinicians who treat breast cancer patients routinely hear that patients are afraid of exercise due to the increased risk of developing BCRL. However, exercise actually confers many physiologic benefits in a limb at risk for lymphedema, such as activating the musculoskeletal pumping mechanism that increases both venous and lymphatic return [46, 48]. Additionally, it is postulated that upper body exercises may reset the sympathetic drive to lymph vessels and thereby assist in the long-term management of lymphedema [48].

Resistance exercise—likely to be effective

The literature on resistance exercise and BCRL is fairly rigorous with six out of seven reviewed studies being RCTs [40, 41, 42, 43, 44, 45] while one was a case-crossover study [46]. Overall, the studies support that resistance exercise is associated with minimal risk of development or exacerbation of lymphedema in the upper extremity. The current weight of the evidence was rated as “Likely to be Effective”.

The studies introduced resistance exercise at various times post-operatively: 4 weeks [44], 4–6 months [42, 45, 46], minimum 1 year [40], and at an indeterminate time in the first 3 months post-operatively [43]. None of the studies observed any significant increase in the development of BCRL with resistance exercise, thus suggesting that slowly progressive resistance exercise is safe at any time interval following surgery for breast cancer.

An additional 2010 report from the PAL Trial [41] focused on at-risk participants who followed the same resistance exercise protocol without use of compression garments as in the 2009 report of women with BCRL [40]. The onset of BCRL was not significantly different between the groups. Furthermore, in a secondary analysis, exercise appeared to confer a protective effect for those with a history of five or more axillary nodes removed. The two PAL studies provide the strongest evidence to date to support our conclusion that resistance exercise is likely to be effective in reducing the risk of BCRL and not exacerbating BCRL symptoms.

Resistance and aerobic exercises—benefits balanced with harms

The seven studies reviewed for a combined regimen of resistance and aerobic exercises uniformly concluded that this type of intervention did not lead to an increase in incidence of lymphedema. Three of the seven studies were RCTs [47, 51, 52]; only one had a sample size larger than 100 yet suffered from a low adherence rate [47]. The remaining four studies were literature reviews and reported no adverse effects regarding BCRL, yet future studies with rigorous study designs and larger sample sizes were recommended [25, 48, 49, 50]. The current weight of the evidence was rated as “Benefits Balanced with Harms”.

The timing of the interventions varied in the three RCTs, from during chemotherapy [47] and at least 2 [52] and 6 months after the completion of treatment [51]. The exercise regimens followed the established physical activity guidelines [30, 31], and resistance interventions were accomplished with free weights, machines, elastic bands, or water based; aerobic interventions included treadmill, cycle, elliptical, and walking. Exercise regimens combining aerobic and resistance exercise appear safe but require larger and more rigorous studies.

Other exercise studies—effectiveness not established

Five studies, of which four were RCTs [53, 55, 56, 57] and one was a case-series study [54], were identified which assessed the effect of physical therapy programs on shoulder dysfunction after breast cancer treatment [53, 54, 55, 56, 57] and onset of BCRL symptoms [54, 57]. Aside from the 2010 study by Torres Lacomba et al. [57], all reviewed studies had small sample sizes of less than 60 patients, and BCRL was a secondary outcome. Furthermore, the interventions tested were quite varied, thereby inhibiting valid comparison of effects across studies. Therefore, the current weight of the evidence was rated as “Effectiveness not Established”.

The role of compression garments

Of particular interest to clinicians is the question of whether compression is necessary during exercise for patients at risk or with BCRL. Compression can be accomplished through multilayer compression bandaging, as used during combined decongestive therapy to achieve volume reduction, or through the use of elastic compression garments. The National Lymphedema Network Position Paper on Exercise states that “current understanding of the underlying physiology provides strong support for the use of compression garments” [58].

The evidence from this review is less clear, as results of the most recently published RCTs did not use compression garments in all patients, commenting only that some patients wore garments if recommended to do so by their therapists [51] or neglecting to mention compression use at all. Several exercise case studies not included in this review reported that any volume increase was transient in the lymphadematous limb [59, 60, 61]. However, these studies examined the response to only one exercise session. Small volume changes are difficult to assess, thereby making it difficult to predict the risk of a cumulative effect with continuing exercise. Overall, a clear, evidence-based recommendation for use of compression garments cannot be made based on this current review.

Limitations

Our systematic review was limited to English language literature published from 2004 to 2010 in peer-reviewed sources; non-English language papers and gray literature were not included. The ONS PEP research grading system used in this review was developed primarily to guide clinical decision making among nursing professionals, yet its utility is of benefit to all medical professionals and cancer survivors interested in the weight of the evidence concerning exercise and lymphedema.

Summary and recommendations for future research

Studies with larger sample sizes and more rigorous study designs are providing strong evidence for the safety of resistance exercise without an increase in lymphedema risk for breast cancer patients. Specifically, breast cancer survivors at risk for lymphedema can be instructed in an exercise regimen and can safely engage in slowly progressive resistance exercise. Breast cancer survivors with lymphedema can be instructed in an exercise regimen and can safely engage in slowly progressive resistance exercise without exacerbating their current lymphedema. The weight of the evidence for a combined regimen of aerobic and resistance exercise indicates some benefit, but clinicians and patients should weigh the beneficial and harmful effects according to individual circumstances and priorities. Finally, limited evidence to date exists on the effectiveness of other exercise regimens involving physical therapy.

Comparable studies are needed to evaluate safe exercise regimens for other patients at risk for lymphedema, particularly for individuals who are at risk for or have lymphedema in the lower extremities. The role of compression during exercise for at risk and affected individuals remains controversial and requires additional study. The methods of diagnosing and quantifying lymphedema continue to vary across studies, prompting more research to determine precise definitions and clinically accessible and sensitive methodologies for detecting the early onset of lymphedema. With stronger, evidence-based consensus, increased safety during exercise interventions can be effectively pursued. Studies with longer follow-up and varying intervals for introducing exercise interventions after diagnosis will provide information on whether such interventions can reduce the risk of developing lymphedema, as well as document any long-term effects of the interventions. Finally, additional research is critical to assess the most effective and cost-efficient methods to instruct cancer patients on the benefits of exercise. With this knowledge, cancer survivors can be confident and comfortable in engaging in physical activities.

Notes

Acknowledgments

This systematic review of contemporary peer-reviewed exercise and lymphedema literature was jointly commissioned by the ALFP and the International Lymphoedema Framework to evaluate the level of evidence in support of exercise in the management of lymphedema. A summary of these findings will be used to support the revisions of the second edition of the Best Practices document [35]. The objectives of the ALFP are to provide evidence of the best practice of lymphedema care, to assist in establishing guidelines for the management of lymphedema, and to increase awareness of this condition in the USA and worldwide. We acknowledge the reference librarian at the University of Missouri and the staff of the ALFP for their contribution to this systematic review.

Source of support

ALFP staff and reference librarian time were supported by industry donations to the ALFP. All authors donated their time in preparation of this manuscript.

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Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Marilyn L. Kwan
    • 1
  • Joy C. Cohn
    • 2
  • Jane M. Armer
    • 3
  • Bob R. Stewart
    • 4
  • Janice N. Cormier
    • 5
  1. 1.Division of ResearchKaiser PermanenteOaklandUSA
  2. 2.Penn Therapy and Fitness, Good Shepherd Penn PartnersPhiladelphiaUSA
  3. 3.Sinclair School of NursingUniversity of MissouriColumbiaUSA
  4. 4.College of Education, Sinclair School of NursingUniversity of MissouriColumbiaUSA
  5. 5.Department of Surgical OncologyUT MD Anderson Cancer CenterHoustonUSA

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