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Breast Cancer Research and Treatment

https://doi.org/10.1007/s10549-018-4725-y

REVIEW

Effects of physical exercise on breast cancer‑related secondary


lymphedema: a systematic review
F. T. Baumann1 · A. Reike1 · V. Reimer1 · M. Schumann2 · M. Hallek1 · D. R. Taaffe3,4,5 · R. U. Newton3,4,6,7 ·
D. A. Galvao3,4,5

Received: 15 February 2018 / Accepted: 16 February 2018


© Springer Science+Business Media, LLC, part of Springer Nature 2018

Abstract
Purpose  The aim of this systematic review is to assess the effect of different types of exercise on breast cancer-related
lymphedema (BCRL) in order to elucidate the role of exercise in this patient group.
Methods  A systematic data search was performed using PubMed (December 2016). The review is focused on the rehabilita-
tive aspect of BCRL and undertaken according to the PRISMA statement with Levels of Evidence (LoE) assessed.
Results  11 randomized controlled trials (9 with LoE 1a and 2 with LoE 1b) that included 458 women with breast cancer in
aftercare were included. The different types of exercise consisted of aqua lymph training, swimming, resistance exercise,
yoga, aerobic, and gravity-resistive exercise. Four of the studies measured a significant reduction in BCRL status based on
arm volume and seven studies reported significant subjective improvements. No study showed adverse effects of exercise
on BCRL.
Conclusion  The evidence indicates that exercise can improve subjective and objective parameters in BCRL patients, with
dynamic, moderate, and high-frequency exercise appearing to provide the most positive effects.

Keywords  Breast cancer · Oncology · Exercise · Physical activity · Lymphedema

Introduction

According to recent statistics, breast cancer is most com-


mon cancer in women worldwide [1]. In the United States,
in 2016 the number of new cases of female breast carci-
* F. T. Baumann noma and melanoma in situ was estimated to be 120.000
freerk.baumann@uk‑koeln.de
[1]. Although there have been substantial improvements in
1
Department I of Internal Medicine, Center of Integrated early detection, diagnosis, treatment, and reduction of com-
Oncology Köln Bonn, University Hospital of Cologne, plications, side effects of the cancer itself and also its treat-
Cologne, Germany ment remain [2]. These may include fatigue, weakness, loss
2
Department of Molecular and Cellular Sport, Medicine, of muscle extensibility, limited shoulder range of motion,
Institute of Cardiovascular Research and Sport Medicine, upper-body pain, pulmonary complications, neuropathy,
German Sport University Cologne, Cologne, Germany
decreases in lean mass and concomitant increases in fat
3
Exercise Medicine Research Institute, Edith Cowan mass, and BCRL [3].
University, Joondalup, WA, Australia
BCRL is one of the most common side effects of the can-
4
School of Medical and Health Sciences, Edith Cowan cer itself or its treatments. The BCRL arises as a result of
University, Joondalup, WA, Australia
fluid accumulation in the interstitial tissue due to damage of
5
School of Human Movement and Nutrition Sciences, The the lymphatic system, induced by surgery and/or radiation,
University of Queensland, Brisbane, QLD, Australia
or tumor-induced neo-lymphangiogenesis [4]. The majority
6
Institute of Human Performance, The University of Hong of women undergoing axillary intervention develop swell-
Kong, Hong Kong, Hong Kong
ing within 2 years [5]. The development of BCRL is further
7
University of Queensland Centre for Clinical Research, increased by risk factors such as obesity, axillary lymph
University of Queensland, Brisbane, QLD, Australia

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Breast Cancer Research and Treatment

node dissection, extensive surgery, and radiotherapy to the A number of studies have been published that have inves-
regional lymph nodes [4]. In the literature, the occurrence of tigated the effect of exercise on BCRL and, as a result, the
BCRL is typically reported to vary from 2 to 81% [6], while effects of resistance exercise on BCRL have already been
the prevalence has also been reported to be as high as 94% extensively reviewed [11–13]. However, to the best of our
in women following breast cancer treatment [7]. This large knowledge, previous reviews have not incorporated other
variance is attributed to differences not only in the thera- modes of exercise, such as aerobic training or water-based
peutic treatment and measurement techniques, but also the activities such as aqua aerobics and swimming. As the type
definition of BCRL used. Even though the 5-year survival of exercise and the training mode may actually determine
rate of breast cancer improved over past 40 years, to date the adherence to regular physical exercise training and out-
still more than one in five women that survive breast cancer comes derived, the purpose of this review was to examine
will develop BCRL [5]. the effects of the various types of exercise in women with
Patients with BCRL typically suffer from a swollen upper BCRL. As such, we are aiming to provide a comprehensive
limb, with concomitant feelings of weakness, heaviness, dis- exercise-based treatment advice for breast cancer survivors
comfort, and pain. Furthermore, there is an increased risk suffering from BCRL.
of infection and a chronic, progressive course of disease,
leading to psychosocial distress and impaired quality of life
(QoL) [5]. Treatment of BCRL typically consists of a mul- Methods
timodal therapy approach, including complex decongestive
medicine, physiotherapy, and skin care [8]. Although pre- A systematic PubMed search was conducted in December
vious studies have indicated numerous positive benefits of 2016, and studies were considered from 2001. Key words
exercise in breast cancer treatment such as improvements searched included ‘breast cancer-related lymphedema OR
in physical performance, body composition, and quality of lymphoedema’ AND ‘training OR exercise.’ Further terms
life along with an acute and chronic reduction in fatigue [9]. used were ‘breast cancer,’ ‘prevention,’ ‘physical activity,’
The lack of clinical recommendation for exercise programs ‘physical exercise,’ ‘physical fitness,’ ‘exercise program,’
along with the symptoms of BCRL often leads to insecurity ‘exercise intervention,’ ‘moving therapy,’ ‘sports therapy,’
of patients and physical activity avoidance. The resulting ‘sport,’ ‘endurance,’ ‘aerobic training,’ ‘resistance training,’
vicious cycle in which sedentary subjects tend to increase ‘strength training,’ and ‘strength.’
body mass, leads to an undesired progression of the dis- Included studies focused on women of all ages and
ease because overweight and obesity are considered as risk nationalities that were undergoing BCRL. The inclusion
factors for the development of lymphedema. Therefore, the and exclusion criteria for selected articles are outlined in
American Cancer Society recommends that primary care Table 1. The intervention had to involve a form of physical
clinicians should counsel survivors on how to prevent or activity for women who are already suffering from BCRL.
reduce the risk of BCRL, including weight loss for those Studies that had a preventive approach or that included both
who are overweight or obese and the role of an individual women with BCRL and women that are at risk for BCRL
tailored exercise program [10]. were excluded. In addition, studies that were not published

Table 1  Study inclusion and exclusion criteria


Inclusion criteria Exclusion criteria

Diagnosis breast cancer Preventive therapy approach or mixed groups (women that are already
suffering from BCRL combined with women that are at risk for
BCRL)
Diagnosis BCRL Physical therapy
Randomized controlled studies Studies published in 2000 or before
Women
Any kind of exercise
Lymphedema was measured by arm volume and/or arm circumference
Completed primary therapy of Breast Cancer
Selective exercise and exercise + lymph drainage
Number of participants > 10
Supervised and non-supervised (exercise and physical activity)
Published in English

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Breast Cancer Research and Treatment

in English or were not randomized controlled trials were The interventions differed among the studies and com-
excluded. prised several modes of exercise: four studies included
This review focused on outcome measures that presented resistance exercise training (RET) alone [15, 17, 21, 25],
the severity and development of BCRL, based on the vol- two studies included RET combined with aerobic training
ume difference between the operated-on and contralateral [23, 24], two studies included aqua lymph therapy (ALT)
arms. Volume measures could be undertaken by using the and water-based exercise [16, 18], one study included grav-
water displacement method or non-invasive optoelectronic ity-resistive arm exercises [19], one study included Yoga
scanning (perometry), or could be calculated from a series [20], and one study included an exercise and relaxation pro-
of circumferential measurements using a measuring tape gram consisting of Tai Chi, Qigong, and gravity-resistive
[13]. The review was aligned to the preferred reporting arm exercises [22]. The number of training sessions varied
items for systematic reviews and meta-analyses (PRISMA) between one and seven sessions per week. All interventions
process [14]. The search was performed by two independ- were at least initially supervised.
ent reviewers (A.R. and V.R.) and was supervised by one Measurements in all trials were undertaken at baseline
senior reviewer (F.T.B.). In addition, the quality of the 12 and at different times during and after the interventions.
identified publications has been assessed with respect to the Arm volume and arm circumference were assessed in all of
levels of evidence. For this purpose, the American Society the included trials. One or more evaluation methods were
of Clinical Oncology (ASCO) criteria for the assessment of used in the studies: limb circumference measurements were
the evidence (LoE) were used and carried out by A.R. and undertaken in six studies [15–17, 20, 21, 24], bioimpedance
F.T.B. [10]. spectroscopy in five [17, 18, 20, 22, 23], water displacement
Levels of evidence [10]: method in three [16, 24, 25], simple arm volume measure-
I: Meta-analyses of RCTs ments in one [22], perometry in three [18, 19, 23], and dual
IA: RCT of breast cancer survivors X-ray absorptiometry in one study [17]. Detailed informa-
IB: RCT based on cancer survivors across multiple cancer tion concerning the diversity of the different interventions
sites is presented in Table 3.
IC: RCT not based on cancer survivors but on general The risk of bias was assessed for each study as per the
population experiencing a specific long-term or late effect guidelines of the Cochrane handbook [14] (Table 3). All
(e.g., managing menopausal symptoms, sexual dysfunction, included studies had a controlled randomized study design
etc.) and included women with pre-existing BCRL. Of the 11
IIA: Non-RCTs based on breast cancer survivors studies, only two had both the participants and assessors
IIB: Non-RCTs based on cancer survivors across multiple blinded [19, 20], seven trials mentioned blinding of the
sites assessor [15–18, 22, 23, 25], and two studies did not men-
IIC: Non-RCTs not based on cancer survivors but on tion any blinding [21, 24]. Eight studies were ranked with
general population experiencing a specific long-term or late LoE 1a and two with LoE 1b (Table 2).
effect Three studies showed excellent adherence and did not
III: Case–control study or prospective cohort study record any dropouts [17, 19, 21]. Hayes et al. reported miss-
0: Expert opinion ing data for two of their thirty-two participants; however,
they indicated that there was no difference in data analy-
sis with or without the missing data [23]. McClure et al.
reported ‘good adherence’ of the control group and ‘excel-
Results lent adherence’ of the intervention group and did not record
any dropouts [22]. Schmitz et  al. excluded two women
A total of 822 studies were identified and were filtered by because of a second primary or recurrent cancer and nine
“clinical trial,” “English language,” and “female.” Follow- women because of missing follow-up [25]. Three studies
ing this, 733 studies were excluded and 89 were selected described dropouts but did not explain the reasons [16, 18,
for abstract- or full-text-analysis (Fig. 1). From these, 11 20] and McKenzie et al. [24] and Bok et al. [15] did not refer
articles were included in this systematic review that com- to the adherence rate.
prised a total number of 458 patients (Table 2). The studies In regard to the use of compression garments, the National
were published between 2003 and 2016 and the study sample Lymphedema (NLN) Network Medical Advisory Committee
sizes ranged from 14 to 141 patients. All women included in recommends the use of compression garments for people suf-
the trials had been diagnosed with BCRL at study entry and fering from lymphedema, especially for women with BCRL
had completed the primary therapy for breast cancer. The [14]. This advice was considered in seven of the 11 studies [15,
average age of the women was 56.8 years, and the interven- 16, 19–21, 24, 25]. In three studies, the participants were free
tion period ranged from 8 weeks up to 1 year. to choose whether to wear a compression garment during the

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Breast Cancer Research and Treatment

Fig. 1  PRiSMA-flow chart
Records idenfied through PubMed
(search date December 2016)

Idenficaon
Records found: 822

Screening
Records excluded:
Records screened: 89
733

Full-text arcles
Full-text arcles
Eligibility

assessed for eligibility:


excluded: 8
19
Included

Studies included in the


analysis: 11

exercise session or not [17, 22, 23]. McClure et al. included Discussion
the adherence to compression garments as a covariate in their
analysis and mentioned that participants that were most com- To the best of our knowledge, this is the first systematic
pliant with it did not show the largest improvement in the bio- review that has considered the effect of different types of
impedance analysis [22]. Further, in the study by Johansson physical exercise (aqua lymph training, swimming, resist-
et al. the use of water was regarded as compression [18]. ance exercise, yoga, aerobic, gravity-resistive exercise)
The outcome data of the 11 studies can be summarized as on women suffering from BCRL. Within the 11 included
follows: four of the studies measured a significant reduction studies, we found four studies [15, 19, 21, 22] that meas-
in BCRL status based on arm volume [15, 19, 21, 22] and six ured a significant reduction in lymphedema status based
studies reported significant subjective improvements [16, 17, on upper limb volume. Furthermore, six studies reported
21, 22, 24, 25]. No study showed adverse effects of exercise objective improvements in subcutaneous fat and muscle
on BCRL.

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Table 2  Summary of the included studies
Authors/year Design Experimental intervention Control activity Outcomes Level of
evidence

Bok et al. [15] N = 32 Progressive resistance exercise Conventional therapy Limb circumference: ↓ in IG from t1 1a
Stage of breast cancer was not men- Daily session, repeated twice per day, 5 days a week for 1 h a day to t2 (p < 0.05)
tioned five times: manual lymphatic drainage, non-elas- Subcutaneous thickness of the arm:
Duration: 8 weeks Dumbbell fly, triceps extension, one tic bandage compression therapy, ↓ in IG from t1 to t2 in distal part
Included on average 17.5 months after arm bent-over row, biceps curl, and skin care (p = 0.02) and in proximal part
treatment dumbbell side raise, and lifting the (p = 0.016)
Mean age = 49 years. arms forward using a 0.5-kg dumb- Muscle thickness of the arm: ↑
Breast Cancer Research and Treatment

All received axillary lymph node dis- bell. Every week, the number of in IG in distal part from t0 to t2
section with mastectomy repetitions was increased by 5 (p = 0.037). ↑ in IG in proximal part
BMI: IG, 22.6; CG, 24.9 Conventional therapy from t1 to t2 (p = 0.025)
5 days a week for 1 h a day, Measuring point: t1 = 4 weeks,
manual lymphatic drainage, non-elas- t2 = 8 weeks
tic bandage compression therapy,
and skin care
Letellier et al. [16] N = 25 Supervised Aqua Lymph training in Non-supervised home land-based Lymphedema-Volume: Ø significant 1a
Stage I–II breast cancer 31° Celsius warm water exercise treatment effect in CG and IG
Duration: 12 weeks Weekly session, 1 h 30 min daily Grip strength: ↑ CG and IG from t0-t1
Included > 3 months after radiation/ Non-supervised home land-based Home land-based exercise program (p = 0.008)
chemotherapy or > 6 months after exercise from DVD. Exercise program con- Pain: present pain intensity score CG
surgery Delivered by DVD: self-massage and sists of three parts: (1) self-massage versus IG ↓ t1 (p = 0.04)
Mean age = 55 years exercises for range of motion, cor- and exercises for range of motion Arm disability (disability of arm,
Axillary node dissection (number of rective exercises, and strengthening (2) corrective exercises shoulder and hand): ↓ IG from t0 to
patients): IG: 12; CG: 9 exercises for 30 min daily (3) strengthening exercises t1 (p = 0.016)
BMI: IG, 25.7; CG, 26 QoL: ↑ IG from t0 to t1 (p = 0.021)
Measuring point: t1: 12 weeks

13

Table 2  (continued)
Authors/year Design Experimental intervention Control activity Outcomes Level of
evidence

13
Cormie et al. [17] N = 62 Supervised Resistance exercise Usual care Extent of swelling: Ø significant 1b
Stage I–III breast cancer 2 times a week for 1 h with warm-up, treatment effect in CG and both IG
Duration: 3 months 6 upper-body and 2 lower-body exer- groups
Included with histological cises, and stretching Severity of symptoms: Ø significant
result > 1 year ago High-load group (22): 75–85% of 1 treatment effect in CG and both IG
Mean age = 57 years RM, 6–10 repetition groups
Number of lymph nodes removed Low-load group (21): 55–65% of 1 Physical function:
(mean ± SD): High-load group: RM, 15–20 repetitions Ø significant treatment effect in CG
15.3 ± 7.2 and both IGs in ROM. Maximal
Low-load group: 14.3 ± 4.6 muscle strength ↑ in both IG from
CG: 17.2 ± 9.4 t0 to t1 (p < 0.001), chest press ↑ in
BMI: both IG from t0 to t1 (p = 0.001),
High-load group, 30.8 ± 6.5 seated row ↑ in low-load IG from t0
Low-load group, 30.4 ± 5.7 to t1 (p = 0.001), shoulder flexion
CG, 28.2 ± 6.0 ↑ in low-load IG from t0 to t1
(p = 0.011).
QoL: physical function ↑ in low-load
IG from t0 to t1 (p = 0.040).
Measuring point: t1: 3 months
Johansson et al. [18] N = 29 Non-supervised Aqua aero- Maintain physical activity as under- LE status: Ø significant treatment 1a
Stage of breast cancer is not men- bics + swimming taken before the study effect in CG and IG
tioned 3 times a week. 30 min. 6 exercises. Shoulder range of motion (ROM):
Duration: 8 weeks 10 repetitions abduction + external rotation Ø
Included on average 10 years after Swimming + performing shoulder significant treatment effect in CG
surgery and with pre-existing exercises and IG. Flexion CG vs. IG ↑ t2
LE > 6 months (p < 0.001)
Mean age = 63 years Measuring points before (t1) and
Number of lymph nodes removed immediately after intervention (t2)
(Median per group):
IG: 5 (11-19); CG: 17 (13-20)
BMI: IG: 30; CG: 30.1
Breast Cancer Research and Treatment
Table 2  (continued)
Authors/year Design Experimental intervention Control activity Outcomes Level of
evidence

Jeffs et al. [19] N = 23 Non-supervised gravity-resistive Continue their usual daily activities Excess limb volume: 1a
Stage of breast cancer is not men- isotonic arm exercises absolute volume: Ø significant treat-
tioned Daily session for 10–15 min. ment effect in CG and IG
Duration: 6 months 3 exercises incorporate deep breathing relative volume %: ↓ in CG
Mean age = 65 years to stimulate the lymphatics, and (p = 0.041) and IG (p = 0.05) from
Sentinel node biopsy (number of 4 gravity-resistive arm exercises t0-t2. CG vs. IG ↓ t4. Ø significant
patients): IG: 1; CG: 0) follow to stimulate venous and treatment effect CG versus IG t4
Axillary node dissection: IG: 7; lymphatic return. Finally, the first Arm function: Ø significant treatment
Breast Cancer Research and Treatment

CG:11 3 exercises are repeated in reverse effect in CG and IG


Sentinel node biopsy and axillary order Shoulder ROM: Ø significant treat-
node dissection (mean per group): ment effect in CG and IG
IG: 3; CG: 1 QoL: Ø significant treatment effect in
BMI: IG: 30.95; CG: 27.43 CG and IG
Measuring points: t1: 1 month. t2:
3 months. t3 6 months
Loudon et al. [20] N = 28 Supervised yoga Usual care Volume of lymphedema: Ø significant 1b
Stage I–III breast cancer Satyananda yoga: gentle repetitions treatment effect in CG and IG
Duration: 8 weeks of physical movements followed Extra cellular fluid: Ø significant
Included > 3 months after treatment by rest. Weekly teacher-led class, treatment effect in CG and IG
Mean age = 58 90 min, plus daily non-supervised Tissue induration: Ø significant treat-
Number of lymph nodes removed session delivered by DVD, 40 min ment effect in CG and IG
(mean ± SD): IG: 14.3 ± 2.3 Degree of sensations, pain, fatigue
CG: 11.2 ± 2.7 and their limiting effects: Ø signifi-
BMI: IG: 29.1 ± 4.6; CG: 25.1 ± 4.5 cant treatment effects in CG and IG
QoL: Ø significant treatment effect in
CG and IG
Measuring points: t1, 1 month; t2,
2 months; t3, 3 months

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Table 2  (continued)
Authors/year Design Experimental intervention Control activity Outcomes Level of
evidence

13
Kim et al. [21] N = 40 Supervised CDPT (complete decon- CDPT for 8 weeks (2 weeks super- Arm volume: CG versus IG ↓ t1 1a
Stage of breast cancer is not men- gestive physiotherapy; manual vised. 6 weeks non-supervised) (p < 0.05). Ø significant treatment
tioned lymphatic drainage, compression 5 times a week. Warm-up: movement effect in volume reduction of the
Duration 8 weeks therapy and remedial exercise) for of large joints. 20–30 repetitions at distal and total arms in CG and IG
Inclusion criteria are not mentioned 2 weeks a moderate pace; movement of the QoL: ↑ physical functioning,
Mean age = 50 years 5 times a week. Warm-up: movement shoulder girdle: patients experience body pain, and mental health in
Lymph node invasion (number of of large joints. 20–30 repetitions at muscle contraction and relaxation of IG (p < 0.05) t0–t1; ↑ physical
patients): IG: 15; a moderate pace; movement of the the shoulder; decongestive exercise: functioning, body pain, and mental
CG: 18 shoulder girdle: patients experience exercising the muscle chain. 15–30 health in CG (p < 0.05) t0–t1. CG
BMI: IG: 25.09 ± 2.99 muscle contraction and relaxation of repetitions. sitting or standing; and versus IG ↑ in role physical and
CG: 24.93 ± 2.67 the shoulder; decongestive exercise: stretching: stretching parts of the general health (p < 0.05) t1
exercising the muscle chain. 15–30 pectoralis and trapezius muscles Measuring point: t1: 8 weeks
repetitions, sitting or standing; and
stretching: stretching parts of the
pectoralis and trapezius muscles
RE for 8 weeks
5 times a week for 15 min. Patients
performed 2 supervised sets of
10 repetitions of each exercise for
2 weeks followed by 2 sets of 10
unsupervised repetitions of each
exercise for 6 weeks. A 0.5-kg
dumbbell was used for the first
2 weeks and a 1-kg dumbbell was
used for the next 6 weeks. Sets
included seated row, bench press,
latissimus dorsi pull-down, 1-arm
bent-over row, triceps extension, and
biceps curl
Breast Cancer Research and Treatment
Table 2  (continued)
Authors/year Design Experimental intervention Control activity Outcomes Level of
evidence

McClure et al. [22] N = 32 Supervised 10 biweekly, 1-h sessions Continue with medical instructions Arm volume: Ø significant treatment 1a
Stage of breast cancer is not men- for 5 weeks: relaxation techniques, from medical team effect in CG and IG
tioned including hands-on practice in deep BIS: ↑ in IG t0–t3 (p = 0.049)
Duration: 4 months diaphragmatic breathing (DDB), Effect of Compression Adherence on
Included approx. 73 months after progressive muscle relaxation, Bioimpedance Measures: Ø signifi-
diagnosis and facial massage followed by a cant treatment effect in CG and IG
Mean age = 59 years 3-month self-monitored non-super- ROM: ↑ in IG t0-t3 (p = 0.034)
Number of lymph nodes removed vised home program period Weight loss: ↓ in IG t0–t3 (p = 0.038)
Breast Cancer Research and Treatment

(Mean ± SD): +17 min daily by DVD (Flow-Video, Mood: ↑ in IG t0-t2 (p = 0.03) and


IG: 18.2 ± 7.3 From Lymphedema onto Wellness t0-t3 (p = 0.017)
CG: 13.4 ± 6.3 (Gravity-resistive arm flexibility QoL: ↑ in IG in norm-based physical
BMI: IG: 29.8 ± 1.6; CG: 33.7 ± 2.3 exercises, DDB, progressive muscle function t0–t3 (p = 0.02). ↑ in IG in
relaxation, Qigong, and Tai Chi general health t0–t3 (p = 0.03). ↑ in
elements) IG in vitality t0–t2 (p = 0.05)
The FLOW exercises and DDB follow Measuring points: t1, 2.5 weeks; t2,
a proximal to distal sequence as 5 weeks; t3, 12 weeks
in manual lymphatic drainage and
are designed to encourage flow in
alternate lymphatic pathways
Hayes et al. [23] N = 32 Supervised aerobic + resistance Continue usual activities Lymphedema status: Ø significant 1a
Stage of breast cancer is not men- exercise treatment effect in CG and IG
tioned Week 1–2: aerobic low to moderate Bioimpedance spectroscopy: Ø
Duration: 12 weeks intensity significant treatment effect in CG
Included > 6 months after treatment Week 3–4: aerobic + water-based RE. and IG
Mean age = 55 years moderate intensity Perometry: Ø significant treatment
All lymph nodes removed: 10 Week 5–8: aerobic + water-based and effect in CG and IG
1 + lymph nodes removed (unsure free-weight RE, moderate intensity Measuring points:
how many): 22 Week 9–12: Aerobic + machine- before (t1) and immediately after
BMI: not mentioned weight RE, moderate to high intervention (t2) for 12 weeks
intensity
Week 1–4: 3 times per week.
20–30 min
Week 5–8: 4 times per week.
30–45 min
Week 9–12: at least 4 times per week.
45+ min

13

Table 2  (continued)
Authors/year Design Experimental intervention Control activity Outcomes Level of
evidence

13
Schmitz et al. [25] N = 141 Partly supervised Resistance exercise No change of exercise level during Lymphedema status: Ø significant 1a
Stage I–III breast cancer 1-year membership at a community study participation treatment effect in CG and IG
Duration: 1 year fitness center. (p = 0.80)
Included 1–15 years after treatment Week 1–13: 90 min, 2 times per week. Improvements in self-reported sever-
Mean age = 57 years Sessions led by certified fitness ity of lymphedema symptoms: CG
Number of lymph nodes removed professionals. Stretching, cardiovas- versus IG ↑ t1 (p = 0.03)
(Mean ± SD): cular warm-up, abdominal and back Upper- and lower-body strength: CG
IG: 15 ± 8; CG: 16 ± 8 exercises, and weight-lifting exer- versus IG ↑ t1 (p = <0.001 for both
BMI: 50 or less cises: upper-body exercises included comparisons)
seated row, chest press, lateral or LE exacerbation: CG versus IG ↑ t1
front raises, bicep curls, and triceps (p = 0.04)
pushdowns. Lower-body exercises Measuring points:
included leg press, back extension, t1: 12 months
leg extension, and leg curl. Weight-
lifting exercises were introduced
with little-to-no resistance, 2–3 sets
with 10 repetitions, then increased
resistance
Week 14–52: unsupervised RE 2
times per week
McKenzie et al. [24] N = 14 Supervised Resistance Exercise: 3 No specific exercise instruction Arm volume: Ø significant treatment 1a
Stage I–II breast cancer times per week, 2–3 sets, for 10 reps. effect in CG and IG
Duration: 8 weeks Exercises: seated row, bench press, Arm circumference: Ø significant
Included > 6 months after primary latissimus dorsi pull-down, one arm treatment effect in CG and IG
therapy bent-over rowing, triceps extension, QoL: ↑ Physical functioning t0–t4
Mean age = 56 years and biceps curl (p = 0.050), general health t0–t4
Number of lymph nodes removed not Supervised aerobic exercise (p = 0.048), and vitality t0–t4
mentioned Warm-up (cycling or walking), (p = 0.023)
BMI: IG: 29.1 ± 6.6 stretching, cool-down period; Measuring points: t1, 2 weeks; t2,
CG: 25.6 ± 3.3 after 2 weeks upper-body aerobic 4 weeks; t3, 6 weeks; t4, 8 weeks
exercise using an arm cycle ergom-
eter was added (under supervision)

CG control group, IG intervention group, ↑ significant increase, ↓ significant decrease, CG versus IG ↑ significantly higher in IG compared to CG, t0 measurement at baseline, QoL quality of
life, ROM range of motion, BIS bioimpedance spectroscopy, reps repetitions, supervised completely supervised, non-supervised partly supervised for at least one time, BMI body mass index
(kg/m2), RM repetition maximum, RE resistance exercise, Ø no significant effect, LE Lymphedema, 1a RCT of breast cancer survivors, 1b RCT based on cancer survivors across multiple sites
[10]
Breast Cancer Research and Treatment
Breast Cancer Research and Treatment

Table 3  Risk of bias summary Study Year Blinding of participants Blinding of outcome Incomplete out-
(performance bias) assessment (detection bias) come data (attrition
bias)

Bok et al. 2016 – + ?


Letellier et al. 2014 – + +
Cormie et al. 2013 – + –
Johansson et al. 2013 – + +
Jeffs et al. 2013 + + –
Loudon et al. 2012 + + +
McClure et al. 2010 – + –
Kim et al. 2010 ? ? –
Hayes et al. 2009 – + –
Schmitz et al. 2009 – + +
McKenzie et al. 2003 ? ? ?

– no, + yes, ? unclear

mass [15], grip strength and arm disability [16], maximum 19, 21, 22]. This was shown by Bok et al. [15] for progres-
strength and shoulder flexion [17, 18], range of motion and sive resistance exercise, by Jeffs et al. [19] for a gravity-
weight loss [22], as well as upper- and lower-body muscle resistive isotonic arm exercise program, by Kim et al. [21]
strength [25]. None of the studies reported adverse events for a manual lymphatic drainage, compression therapy and
during the study period. Moreover, seven studies reported remedial exercise combined with resistance exercise, and
additional improvements in patient reported outcomes, by McClure et al. [22] for gravity-resistive arm flexibility
such as QoL [16, 17, 21], mood and QoL [22], general exercises combined with deep diaphragmatic breathing
health, vitality, and QoL [24], as well as improvements in and progressive muscle relaxation, as well as components
self-reported severity of BCRL status [25]. of Qigong and Tai Chi. It is, however, worthy to note that
As Schmitz et al. noted, historically clinicians advised these studies all included some component of resistance
cancer patients to rest and to avoid activity [25]. However, exercise. Kim et al. [20] concluded that resistance exer-
the roundtable of the American College of Sports Medicine cise could reduce swelling caused by BCRL because of
(ACSM) endorsed exercise during and after cancer treat- increased muscular power and tension, stimulated pump-
ments to be safe and referred to improvements in physical ing of the venous and lymphatic fluids, and stimulation
functioning, QoL, and cancer-related fatigue [26]. In fact, of sympathetic nerves to contract the lymphatic vessels.
this recommendation is similar to the recent guidelines out- In the studies by Jeffs et al. [19] and McClure et al. [22],
lined by the American Cancer Society, stating that main- a combination of gravity-resistance exercises in combi-
taining normal weight through an active and healthy life- nation with breathing practices was utilized. It remains,
style may be one of the key elements in treatment of BCRL thus, questionable if the beneficial effects on BCLR are
[10]. The present review adds to these recommendations by exclusive to resistance exercise or can also be achieved by
suggesting that exercise may indeed be feasible, safe, and a other forms of exercise such as aerobic training or relaxa-
beneficial concomitant therapy for women with BCRL. This tion programs (e.g., Yoga).
is also confirmed by the level of evidence as defined by the Another aspect worthy of note is the training frequency.
American Cancer Society [10], according to which nine out The studies by Bok et al. [15], Jeffs et al. [19], McClure
of 11 studies were ranked with 1a and the remaining two et al. [22], and Kim et al. [21] included nearly daily exercise
studies with 1b. sessions (in the study by Kim et al. only 5 weekly sessions)
Previous reviews summarizing the effects of resistance with a short duration (Bok et al. > 5 repetitions twice a day,
training on BCRL indicated that physical exercise does Jeffs et al. 10–15 min daily, McClure et al. 17 min daily plus
not adversely affect BCRL [11, 13]. This is in line with 2 sessions a week for 60 min, Kim et al. 15 min 5 times a
the results from the present review that found that not week). Daily sessions are also mentioned in the studies by
only resistance exercise but also other types of exercise Letellier et al. [16] and Loudon et al. [20]. It is, thus, likely
do not worsen BCRL and can, thus, be performed safely that training frequency rather than the duration of a single
by breast cancer patients. In fact, four of the 11 studies training session is an important factor to consider when pre-
not only concluded that exercise is not harmful, but that scribing physical exercise programs to breast cancer survi-
it resulted in a significant beneficial treatment effect [15, vors suffering from BCLR.

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Breast Cancer Research and Treatment

The findings of the present systematic review demonstrate Funding  No sources of funding were used to assist in the preparation
that physical exercise may improve BCRL state, provided of this manuscript.
that the training program is supervised and individually tai-
lored. To the best of our knowledge, this systematic review is Compliance with ethical standards 
the first to summarize the effects of different types of physi-
Conflict of interest  The authors declare that there is no conflict of in-
cal exercises on BCRL and was produced according to the terest.
guidelines of PRISMA [14]. We believe this paper provides
excellent grounds for supporting guidelines on the role of Ethical approval  The authors declare that the publication has been
exercise in women with BCRL. As the studies summarized prepared in accordance with ethical standards.
in this review were published from 2003 to 2016, the find-
ings are both recent and timely. Nevertheless, when inter-
preting the present findings one should consider possible
limitations. First, the overall number of patients included References
into the selected studies is low (N = 458). Second, among
the studies there were three pilot trials [15, 18, 24] and one 1. http://www.wcrf.org/int/cance​r-facts​-figur​es/data-speci​fic-cance​
feasibility trial [19], contributing to the relatively small rs/breas​t-cance​r-stati​stics​
2. Coleman MP, Quaresma M, Berrino F, Lutz J, De Angelis R,
number of total BCRL patients. Third, the training program Capocaccia R, Baili P, Rachet B, Gatta G, Hakulinen T, Micheli
variables such as volume, frequency, and intensity as well A, Sant M, Weir HK, Elwood JM, Tsukuma H, Koifman S, Silva
as the outcome variables differed substantially among the GA, Francisci S, Santaquilani M, Verdecchia A, Storm HH,
studies. Moreover, as a result of the low number of studies Young JL (2008) Fast track—articles: cancer survival in five
continents: a worldwide population-based study (CONCORD).
available, no standard definition for BCRL was used and the Lancet Oncol 9:730–756
measurement techniques differed among the studies. How- 3. Hayes S, Sipio TD, Rye S, Lopez JA, Saunders C et al (2011)
ever, while this must certainly be considered as a limitation Prevalence and prognostic significance of secondary lymphedema
of the present review, it should be noted that there is a lack following breast cancer. Lymphat Res Biol 9(3):135–141
4. Mortimer P (2013) Arm lymphoedema after breast cancer. Lancet
of definition for BCRL even in medical care, making the Oncol 14:423–442
investigation of treatment methods challenging. 5. DiSipio T, Rye S, Newman B, Hayes S (2013) Incidence of uni-
Based on the present findings, it can be concluded from lateral arm lymphoedema after breast cancer: a systematic review
the current literature that physical exercise is not contrain- and meta-analysis. Lancet Oncol 14:500–515
6. Hayes SC, Janda M, Cornish B, Battistutta D, Newman B (2008)
dicated for women with BCRL. When completed according Lymphedema after breast cancer: incidence, risk factors, and
to the ACSM guidelines for cancer survivors [26], there is effect on upper body function. J Clin Oncol 26(21):3536–3542
no restriction recommended regarding BCRL and any form 7. Armer JM, Stewart BR (2010) Post-breast cancer lymphedema:
of exercise. As such, our findings are in contrast to the early incidence increases from 12 to 30 to 60 months. Lymphology
43:118–127
recommendations by health care professionals to avoid vig- 8. Liebl ME, Preiß S, Pögel S et al (2014) Elastic tape as a thera-
orous or excessive upper-body exercise, including activities peutic intervention in the maintenance phase of complex decon-
of daily living [27]. It should, however, be noted that most gestive therapy (CDT) in lymphedema. Phys Med Rehabil Kuror
of studies investigating the effects of exercise on BCRL have 24:34–41
9. Baumann FT, Bloch W, Weissen A et al (2013) Physical activ-
utilized strength training although our findings also suggest ity in breast cancer patients during medical treatment and in the
that other types of training may induce similar effects. As aftercare: a review. Breast Care 8(5):330–334
resistance training may not always be desired by certain 10. Runowicz CD, Leach CR, Henry NL, Henry KS, Mackey HT,
populations, future studies should primarily focus on other Cowens-Alvarado RL, Cannady RS, Pratt-Chapman ML, Edge
SB, Jacobs LA, Hurria A, Marks LB, LaMonte SJ, Warner E,
modes of exercise when investigating the effects of physical Lyman GH, Ganz PA (2016) American Cancer Society/American
training on BCRL. Moreover, future studies may also focus Society of Clinical Oncology Breast Cancer Survivorship Care
on the possible preventive aspects of physical exercise for Guideline. J Clin Oncol 34(6):611–635
the development of BCRL in breast cancer patients. 11. Keilani M, Hasenoehrl T, Neubauer M, Crevenna R (2016) Resist-
ance exercise and secondary lymphedema in breast cancer survi-
vors—a systematic review. Support Care Cancer 24(4):1907–1916
Acknowledgements  The authors Freerk T. Baumann, Alexandra Reike, 12. Nelson NL (2016) Breast cancer-related lymphedema and
Vanessa Reimer, Moritz Schumann, Michael Hallek, Dennis R. Taaffe, resistance exercise: a systematic review. J Strength Cond Res
Robert U. Newton, and Daniel A. Galvao certify that they have no 29:2656–2665
affiliations with or involvement in any organization or entity with any 13. Paramanandam VS, Roberts D (2014) Weight training is not harm-
financial interest (such as honoraria; educational grants; participation ful for women with breast cancer-related lymphoedema: a system-
in speakers’ bureaus; membership, employment, consultancies, stock atic review. J Physiother 60(3):136–143
ownership, or other equity interest; and expert testimony or patent- 14. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC,
licensing arrangements), or non-financial interest (such as personal Ioannidis JPA et al (2009) The PRISMA statement for report-
or professional relationships, affiliations, knowledge or beliefs) in the ing systematic reviews and meta-analyses of studies that evaluate
subject matter or materials discussed in this manuscript.

13
Breast Cancer Research and Treatment

health care interventions: explanation and elaboration. PLoS Med 21. Sim YJ, Jeong HJ, Kim GC (2010) Effect of active resistive exer-
6(7):1000100 cise on breast cancer-related lymphedema: a randomized con-
15. Bok SK, Jeon Y, Hwang PS (2016) Ultrasonographic evaluation of trolled trial. Arch Phys Med Rehabil 91(12):1844–1848
the effects of progressive resistive exercise in breast cancer-related 22. McClure MK, McClure RJ, Day R, Brufsky AM (2010) Rand-
lymphedema. Lymphat Res Biol 14(1):18–24 omized controlled trial of the breast cancer recovery program for
16. Letellier ME, Towers A, Shimony A, Tidhar D (2014) Breast women with breast cancer-related lymphedema. Am J Occup Ther
cancer-related lymphedema: a randomized controlled pilot and 64(1):59–72
feasibility study. Am J Phys Med Rehabil 93(9):751–759 23. Hayes SC, Reul-Hirche H, Turner J (2009) Exercise and secondary
17. Cormie P, Pumpa K, Galvao DA, Turner E, Spry N, Saunders lymphedema: safety, potential benefits, and research issues. Med
C, Zissiadis Y, Newton RU (2013) Is it safe and efficacious for Sci Sports Exerc 41(3):483–489
women with lymphedema secondary to breast cancer to lift wights 24. McKenzie DC, Kalda AL (2003) Effect of upper extremity exer-
during exercise: a randomized controlled trial. J Cancer Surviv cise on secondary lymphedema in breast cancer patients: a pilot
7(3):413–424 study. J Clin Oncol 21(3):463–466
18. Johansson K, Hayes S, Speck RM, Schmitz KH (2013) Water- 25. Schmitz KH, Ahmed RL, Troxel A, Cheville A, Smith R, Lewis-
based exercise for patients with chronic arm lymphedema: Grant L, Bryan CJ, Williams-Smith CT, Greene QP (2009) Weight
a randomized controlled pilot trial. Am J Phys Med Rehabil lifting in women with breast-cancer-related lymphedema. N Engl
92(4):312–319 J Med 361:664–673
19. Jeffs E, Wiseman T (2013) Randomised controlled trial to deter- 26. Schmitz KH, Courneya KS, Matthews C, Demark-Wahnefried W,
mine the benefit of daily home-based exercise in addition to self- Galvão DA, Pinto BM, Irwin ML, Wolin KY, Segal RJ, Lucia A,
care in the management of breast cancer-related lymphoedema: a Schneider CM, von Gruenigen VE, Schwartz AL (2010) Ameri-
feasibility study. Support Care Cancer 21(4):1013–1023 can College of Sports Medicine roundtable on exercise guidelines
20. Loudon A, Barnett T, Piller N, Immink MA, Williams AD (2014) for cancer survivors. Med Sci Sports Exerc 42(7):1409–1426
Yoga management of breast cancer-related lymphoedema: a ran- 27. Harris SR, Niesen-Vertommen SL (2000) Challenging the myth
domised controlled pilot-trial. BMC Complement Altern Med of exercise-induced lymphedema following breast cancer: a series
14:214 of case reports. J Surg Oncol 74:95–99

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