Breast Cancer Related Lymphedema and Resistance.36

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 10

BRIEF REVIEW

BREAST CANCER–RELATED LYMPHEDEMA AND


RESISTANCE EXERCISE: A SYSTEMATIC REVIEW
NICOLE L. NELSON
Clinical and Applied Movement Sciences, Brooks College of Health, University of North Florida, Jacksonville, Florida

ABSTRACT INTRODUCTION

B
Downloaded from http://journals.lww.com/nsca-jscr by BhDMf5ePHKav1zEoum1tQfN4a+kJLhEZgbsIHo4XMi0hCywCX1AWnYQp/IlQrHD3i3D0OdRyi7TvSFl4Cf3VC1y0abggQZXdgGj2MwlZLeI= on 01/30/2022

Nelson, NL. Breast cancer–related lymphedema and resis- reast cancer is the most common cancer type
tance exercise: a systematic review. J Strength Cond Res among women in the United States and is the
30(9): 2656–2665, 2016—Breast cancer–related lymphe- second leading cause of cancer death (26).
dema (BCRL) is characterized by the accumulation of fluid Approximately 1 in every 8 women will develop
in the interstitial tissues in the arm, shoulder, neck, or torso
breast cancer at some time during her lifetime. Improvements
in early detection, diagnosis, and treatment have improved
and attributed to the damage of lymph nodes during breast
the 5-year relative survival rate to above 80% (5). Despite the
cancer treatments involving radiation and axillary node dis-
tremendous enhancement of current breast cancer care, sur-
section. Resistance exercise training (RET) has recently
vivors are at risk for several treatment complications, perhaps
shown promise in the management of BCRL. The aims of the most concerning being breast cancer–related lymphede-
this review were twofold: (a) To summarize the results of ma (BCRL). Breast cancer–related lymphedema is a chronic
recent randomized controlled trials (RCTs) investigating the and progressive issue characterized by the accumulation of
effect of resistance exercise in those with, or at risk for, fluid in the interstitial tissues in the arm, shoulder, neck, or
BCRL. (b) To determine whether breast cancer survivors torso. This accumulation is attributed to the disruption of the
can perform RET at sufficient intensities to elicit gains in lymphatic pathways from surgical resection and, or radiation
strength without causing BCRL flare-up or incidence. A of lymphatic vessels or nodes during breast cancer treatment
search was performed on the electronic databases (20). Breast cancer–related lymphedema most commonly de-
PubMed, MEDLINE, SPORT Discus, and Science Direct, velops within 3 years of treatment; however, there are studies
up to July 10, 2015, using the following keywords: breast in which this condition is reported to develop up to 20 years
cancer–related lymphedema, strength training, resistance
after treatment (21). Reported incidence of lymphedema
among breast cancer survivors varies and is believed to be
training, systematic review, and breast cancer. Manual
dependent on the type of treatment received (e.g., axillary
searches of references were also conducted for additional
lymph node dissection vs. sentinel lymph node biopsy); how-
relevant studies. A total of 6 RCTs, involving 805 breast
ever, recent estimates indicate that more than 1 in 5 breast
cancer survivors, met the inclusion criteria and corre- cancer survivors will develop BCRL (9). The associated
sponded to the aims of this review. The methodological swelling may range from mild to disabling and is associated
quality of included RCTs was good, with a mean score with feelings of discomfort, heaviness, and weakness in the
6.8 on the 10-point PEDro scale. The results of this review arm, pain, and an increased risk for infection (20). These
indicate that breast cancer survivors can perform RET at symptoms further impair functional and self-care abilities of
high-enough intensities to elicit strength gains without trig- the individuals, causing significant psychological distress and
gering changes to lymphedema status. There is strong evi- reduced quality of life (QOL).
dence indicating that RET produces significant gains in Common clinical advice emphasizes protection of the
muscular strength without provoking BCRL. affected arm in an effort to reduce the risk of overstressing
a compromised lymphatic system. Although these recom-
KEY WORDS strength training, resistance training mendations are judicious, this advice may lead to physical
activity (PA) avoidance and declines in strength of the
affected limb. Over time, fears of exacerbation may lead to
low self-efficacy, reduced QOL, deconditioning, and obesity.
To compound matters, overweight and obesity, and a sed-
Address correspondence to Nicole L. Nelson, nicole.nelson@unf.edu. entary lifestyle, are known risk factors for development and
30(9)/2656–2665 of BCRL progression (13–15).
Journal of Strength and Conditioning Research Although there is no cure for BCRL, decongestive therapy
Ó 2016 National Strength and Conditioning Association is considered the gold standard for the management of BCRL
the TM

2656 Journal of Strength and Conditioning Research

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
the TM

Journal of Strength and Conditioning Research | www.nsca.com

and is performed by trained lymphedema therapists. Decon- Data Extraction


gestive therapy often involves manual lymphatic drainage The following data were extracted: authors, year of publi-
followed by compression bandaging to control arm volume cation, description of the resistance training protocol used in
(9). Compression garments are occasionally used as a long- the intervention (volume, intensity, frequency, length of the
term management method of BCRL; however, compliance trial), strength measures and outcomes, change in lymphe-
is often an issue, as these garments are considered uncomfort- dema status, description of the comparison group, assess-
able and difficult for the patients to put on by themselves (17). ment times, study results, and conclusions of the authors.
Recent evidence indicates that resistance exercise training
Methodological Quality and Strength of Evidence
(RET) can be an effective management strategy for BCRL not
The methodological quality of studies within this systematic
only by improving functional capacity but also by improving
review was assessed using the PEDro scale (25). The scale
lymph flow through the pumping effect stimulated by
has been shown to have good levels of validity and reliability
muscular contraction (10,11). Additionally, maintaining or
(18). The PEDro scale evaluates the risk of bias and statisti-
augmenting muscular strength and improving body composi-
cal reporting of RCTs and comprises 11 items: 8 items relat-
tion may offset some of the deleterious effects of cancer treat-
ing to methodological quality (e.g., random allocation,
ment (e.g., frailty, reduced bone mineral density, fatigue) (4,12).
concealed allocation, etc) and 2 items relating to statistical
The primary objective of this review was to explore the
reporting (e.g., between-group comparisons, and point esti-
evidence regarding the efficacy of resistance exercise among
mates and variability). An eligibility criterion relating to
those with or at risk for BCRL. Specifically, this review
external validity is the first item and is not considered part
aimed to answer the question, “Can women who are at risk
of the total score. The total PEDro score ranges from 0 to 10
for, or currently have, BCRL increase muscular strength
points, with a score 6 or greater considered of high quality
without increasing BCRL incidence or symptoms?”
(HQ), RCTs receiving less than 6 were considered of low
quality (LQ).
METHODS The overall strength of evidence was assessed against
This review was aligned to the PRISMA (preferred reporting a modified version of the grading system presented by van
items for systematic reviews and meta-analyses) statement Tulder et al. (27). Strong evidence was based on results
(19). PRISMA includes a 27-item checklist that focuses on derived from a minimum of 2 HQ studies. Moderate evi-
ensuring a transparent and complete reporting of health care dence was based on results derived from 1 HQ study and
interventions. at least 1 LQ study. Limited evidence included results from
multiple LQ studies or from 1 HQ study. Very limited evi-
Search Strategy
dence included results from 1 LQ study.
The records of 4 electronic databases were searched from
their inception until July 10, 2015. The databases examined Lymphedema Status and Outcome Measures
included PubMed, MEDLINE, SPORT Discus, and Science Lymphedema status at baseline varied among the trials
Direct. A manual search of references was also performed to included in this review. Similarly, measures of lymphedema
identify additional relevant studies. Key words searched status and muscular strength varied. Table 1 presents the
included resistance training, strength training, and breast BCRL status at baseline and the strength and lymphedema
cancer–related lymphedema. measures used in each trial.
Eligibility Criteria
Studies evaluating the effects of resistance training were included RESULTS
in this review based on the following criteria: (a) participant Quality
studies involving breast cancer survivors with, or at risk for The methodological quality and reporting of the included
BCRL, with no limitations on participant age, or nationality; (b) trials is presented in Table 2. The total PEDro score ranged
intervention research in which resistance training was used as from 4 to 8. Five trials were considered to be of HQ and to
the sole intervention, or as part of the intervention; (c) control have a low risk of bias (6,7,16,23,24), whereas 1 was consid-
research in which there was a comparison group involving RET ered of LQ (1). Each of the included RCTs satisfied the items
of another intensity or another mode of exercise, or a nonexer- concerning random allocation, baseline comparability,
cising control; (d) outcome-research in which strength out- between-group comparisons, and point estimates and vari-
comes and changes in lymphedema status were reported; (e) ability. The items that were least frequently satisfied included
study design–published randomized controlled trials (RCTs). blinded participants and blinded therapists.
Studies were excluded if they were not reported in English.
Description of Studies
Review Process The initial search yielded 669 potential articles. Once dupli-
All retrieved studies were cross-referenced and duplicate studies cates were removed, 267 abstracts were screened. Among
were deleted. Relevant titles were highlighted, with abstracts these, 26 full articles were retrieved and reviewed. Of these
and full texts reviewed for inclusion by 1 reviewer (N.N.). articles, 6 met the inclusion criteria (1,6,7,16,23,24). Figure 1

VOLUME 30 | NUMBER 9 | SEPTEMBER 2016 | 2657

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
2658

BCRL and Resistance Exercise


Journal of Strength and Conditioning Research
the

TABLE 1. Lymphedema status, outcome measures, and use of compression garments.*

Objective
Lymphedema lymphedema Use of compression garment
Study status at baseline measures Muscular strength/endurance measures during RET

Ahmed et al. (1) Thirteen had BCRL AC (cm) Strength Those with BCRL were
at baseline encouraged to wear CG
during RET
1RM bench press and leg press
Cormie et al. (6) Met criteria for BIS Strength 25% wore a CG
BCRL
Affected AV (ml)  Grip strength affected arm
Interlimb AV  1RM chest press, seated row and leg press
difference (%)
TM

Affected AC (cm) Endurance


Interlimb AC  Max reps 70% 1RM chest press, seated row, and leg
difference (%) press
Courneya et al. (7) At risk for BCRL Interlimb WV Strength NR
difference (%)
 8RM horizontal bench press and leg extension
Kilbreath et al. (16) At risk for BCRL BIS Strength hand-held dynamometer. Measures taken while NR
seated with shoulder flexed to 908 and elbow extended
Affected AC (cm)  Forward flexion
Interlimb AC  Abduction
difference (%)
 Horizontal flexion
 Horizontal extension
Schmitz et al. (24) Met criteria for Interlimb WV Strength Required to wear CG during
BCRL difference (%) RET
 1RM bench press and leg press
Schmitz et al. (23) At risk for BCRL Interlimb WV Strength Required to wear CG during
difference (%) RET
 1RM bench press and leg press

*RET = resistance exercise training; BCRL = breast cancer–related lymphedema; AC = arm circumference; 1RM = 1 repetition maximum; CG = compression garment; BIS =
bioimpedance spectroscopy; AV = arm volume; reps = repetitions; WV = water volume; NR = not reported.

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
the TM

Journal of Strength and Conditioning Research | www.nsca.com

TABLE 2. Methodological quality and reporting of eligible studies (n = 6).*

PEDro scale itemsz

Study PEDro score (0–10)† 1 2 3 4 5 6 7 8 9 10 11

Ahmed et al. (1) 4 Y Y N Y N N N N N Y Y


Cormie et al. (6) 7 Y Y Y Y N N N Y Y Y Y
Courneya et al. (7) 7 Y Y Y Y N N N Y Y Y Y
Kilbreath et al. (16) 8 Y Y Y Y N N Y Y Y Y Y
Schmitz et al. (23) 7 Y Y Y Y N N Y Y N Y Y
Schmitz et al. (24) 8 Y Y Y Y N N Y Y Y Y Y

*Y = yes; N = no.
†Scores of 6 or greater considered of high quality, scores of less than 6 considered of low quality.
zPEDro scale items: (a) eligibility criteria and source of participants; (b) random allocation; (c) concealed allocation; (d) baseline
comparability; (e) blinded subjects; (f) blinded therapists; (g) blind assessors; (h) adequate follow-up; (i) intention-to-treat; (j) between-
group comparisons; (k) point estimates and variability.

depicts a summary of the selection process. The primary rea- The 6 included trials were published between 2006 and
sons for exclusion were as follows: the intervention did not 2013 and included 805 breast cancer survivors who either
involve a form resistance exercise, the study did not report had BCRL at the start of the trial or were considered to be at
muscular strength or endurance outcomes, and the study did risk for developing BCRL. The interventions involved RET
not report lymphedema measures. alone, or RET was used in conjunction with stretching. The
per-study sample sizes ranged
from 46 to 242 participants.
The majority of the trials
involved intervention partici-
pants performing RET 2 days
per week. The lengths of the
interventions involving super-
vised RET ranged from 8
weeks to 17 weeks. Four studies
performed follow-up assess-
ments, at either 6 months or 1
year after intervention
(7,16,23,24). Table 3 presents
an account of muscular
strength/endurance outcomes
and changes to lymphedema
status.
Comparisons
Among the 6 investigations
included, 1 trial compared the
effects of low-intensity upper-
body (beginning with no weight
or very light weight) RET along
with flexibility training with
a nonexercising control group
(16). Two trials compared the
effects of moderate (55–70%
1RM) to high intensity (75–
Figure 1. Flow diagram of selection process using PRISMA Guidelines. 85% 1RM) RET against either
an aerobic exercise group or

VOLUME 30 | NUMBER 9 | SEPTEMBER 2016 | 2659

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
2660

BCRL and Resistance Exercise


TABLE 3. Key data for randomized controlled trials.*

Length of trial
Journal of Strength and Conditioning Research

Study and and assessment


the

participants Intervention Control points Key outcomes Authors’ conclusions

Ahmed et al. (1), RET, n = 23 No exercise First 3 mo Strength: significant differences in 6 mo 2 d wk21 RET did not
n = 46, mean supervised leg press and bench press in favor increase incidence, AC, or
age 52 y of the RET gp (p , 0.001) symptoms of BCRL compared
with controls
2 d wk21 9 UBE + LBE n = 23 3–6 mo BCRL: no reported increases in
unsupervised BCRL symptoms in RET gp. Three
reported flare-ups in the control gp
UBE begin with no weight AP: 6 mo
or 1/2 lb wrist wts
If no symptoms progress at
the next session by the
smallest increment
LBE MVC 8–10 rep
TM

After first 2–3 W increase


from 2 sets to 3 sets
Cormie et al. (6), (i) High load RET, n = 22 No exercise 3 mo Strength: both RET gps had Women with BCRL can lift heavy
n = 6, mean significantly greater gains in weights without fear of BCRL
age = 57.2 y strength (1RM chest press, seated exacerbation
row, leg press) and endurance
(chest press, seated row, leg
press) compared with the control
gp
2 d wk21 8 UBE + LBE n = 19 AP: 3 mo BCRL: no btwn-gp differences for
any swelling measure
1–4 sets 6–10 reps 75–
85% 1RM
(ii) Low load RET, n = 21
2 d wk21 8 UBE + LBE
15–20 reps 55–65% 1RM
Progress by 5–10% if able
to perform more reps than
the specified reps

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
Corneya et al. (7), RET, n = 82 Control gp (1): 17 wk Strength: RET was superior to usual AET and RET improved self-
n = 242, mean n = 78 care for improving bench press and esteem, physical fitness, body
age = 49.2 y leg extension (p , 0.001 for both composition, and chemotherapy
comparisons) completion rate without causing
BCRL or significant adverse
events
3 d wk21 9 UBE + LBE 3 d wk21 AET AP: 17 wk BCRL: RET did not cause BCRL
2 sets 8–12 reps 60–70% Intensity: 60%
1RM V_ O2max for
first 6 W
70% V_ O2max
6–12 wk
Progress by 10% when 80% V_ O2max
reps .12 beyond 12
wk
Duration:
15 min first 3
W, increase
by 5 min
every 3 wk
Control gp (2):
n = 82
Usual care
Kilbreath et al. RET + stretching, n = 81 No exercise 8 wk Strength: significant increase in RET did not precipitate BCRL
(16), n = 160, shoulder abduction strength in RET
mean age = gp at 8 wk compared with the

Journal of Strength and Conditioning Research


53.5 y control group

the
1 wk supervised + HP 4 n = 79 AP: 8 wk and 6 No significant btwn-gp differences at
UBE mo 6 mo
Begin with 1–1.5 kg BCRL: no btwn-gp differences
2 sets 8–15 reps
VOLUME 30 | NUMBER 9 | SEPTEMBER 2016 |

Progress based on RPE =


15
(continued on next page)

TM
| www.nsca.com
2661

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
2662

BCRL and Resistance Exercise


Schmitz et al. (24), RET, n = 71 No exercise 13 wk Strength: RET gp had greater Slowly progressed RET had no
n = 141, mean supervised + significantly greater increases in significant effect on limb
age = 57 y 39 wk 1RM bench press and leg press (p swelling and resulted in
Journal of Strength and Conditioning Research

, 0.001 for both comparisons)


the

unsupervised decreased incidence of


exacerbations of BCRL,
reduced symptoms, and
increased strength
2 d wk21 9 UBE + LBE n = 70 AP: 1 y BCRL: increase of 5% or more in
interlimb volume difference was
prespecified as a lymphedema
exacerbation. The proportion of
women experiencing an
exacerbation was 11% in the RET
and 12% in the control gp (p = 1.0)
Over first 5 wk increase
from 2 to 3 sets
UBE beginning with no wt
or 1 lb
LBE MVC 8–10 reps
TM

Progress by smallest
increment if able to
perform 10 reps for 2
consecutive sessions
Schmitz et al. (23), RET, n = 72 No exercise 13 wk Strength: RET gp showed Slowly progressed RET
n = 154, mean supervised + significantly greater increases in compared with no exercise did
age = 55 y 39 wk 1RM bench press (p , 0.001) and not result in increased
unsupervised leg press (p = 0.02) compared with incidence of BCRL
the control gp
2 d wk21 9 UBE + LBE n = 75 AP: 1 y BCRL: incident BCRL onset
prespecified as an increase in
interlimb volume difference of 5%
or more. The proportion of women
experiencing BCRL onset was
11% in the RET gp and 17% in the
control gp (p = 0.04)
3 sets 10 reps
UBE begin with no wt or 1 lb
LBE MVC 8–10 reps
Progress by smallest
possible increment after
completing 3 sets of 10 for
2 consecutive sessions

*RET = resistance training; gp = group; AC = arm circumference; BCRL = breast cancer–related lymphedema; UBE = upper-body exercises; LBE = lower-body exercises; wts =
weights; AP = assessment point; MVC = maximal voluntary contraction; reps = repetitions; 1RM = 1 repetition maximum; btwn = between; AET = aerobic training; HP = home
program; RPE = rating of perceived exertion.

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
the TM

Journal of Strength and Conditioning Research | www.nsca.com

a nonexercising control group (6,7). Three trials compared the proper progression for this population should involve
effects of progressive RET involving intervention participants participants lifting weight with proper technique for the
beginning the trial with low-intensity upper-body and prescribed number of repetitions, with the intention of
moderate-intensity lower-body resistance against nonexercis- increasing the load by small increments (5–10%) when the
ing controls (1,23,24). The conclusion statements are based on participant can successfully lift the weight with relative ease
the aforementioned adapted version of van Tulder’s classifica- for the prescribed number of repetitions.
tion system and range from limited evidence to strong With respect to frequency, optimal training frequency
evidence. likely depends on the current fitness level of the breast
cancer survivor. However, participants performing 2 to 3
Comparison 1: Low-Intensity Upper-Body RET + Flexibility. RET sessions per week on nonconsecutive days demon-
There is limited evidence (1 HQ trial; 160 participants) that strated statistically significant improvements in strength
low-intensity shoulder RET and flexibility exercise elicits compared with control subjects (1,6,7,23,24).
significantly greater strength gains in shoulder flexion and There were significant variances for the training variables
abduction with no change to lymphedema status when of intensity and volume among the included trials, and future
compared with no exercise (16). RCTs are needed to fully elucidate the optimal RET dose for
breast cancer survivors who are at risk for, or currently have,
Comparison 2: Moderate-to-High Intensity RET vs. Aerobic BCRL. It should be noted, however, that none of the
Exercise or No Exercise. There is strong evidence (2 HQ included trials reported an association between RET and
trials; 304 participants) that moderate-to-high intensity RET BCRL incidence or symptoms regardless of the RET
elicits significantly greater gains in strength without the risk protocol used. Additionally, all 6 investigations reported
of increased lymphedema symptoms when compared with improvements in strength, regardless of training volume or
no exercise (6,7). Furthermore, there is limited evidence (1 intensity. Interestingly, Courneya et al. (7) reported that
HQ trial; 62 participants) that moderate-to-high intensity moderate-intensity RET adherence was associated with in-
RET is superior for improving upper- and lower-body creases in lean body mass (r = 0.25; p = 0.037). Moreover,
strength, without provoking BCRL, when compared with the changes in lean body mass were associated with im-
moderate-intensity aerobic exercise (7). provements in QOL (r = 0.19; p = 0.022), self-esteem (r =
0.19; p = 0.022), and depression (r = 20.19; p = 0.019).
Comparison 3: Low-Intensity Upper-Body and Moderate-
Three trials in this review indicated that, after receiving
Intensity Lower-Body RET. There is strong evidence (2 HQ
initial instruction, participants performing unsupervised RET
and 1 LQ trials; 341 participants) that lower-intensity upper-
experienced no increases in lymphedema status and dem-
body RET, combined with moderate-intensity lower-body
onstrated significant strength improvements (1,23,24). From
RET, produces no significant increase in the risk for BCRL
a cost perspective, this may increase exercise adherence.
measures, and elicits significantly greater upper- and lower-
Additionally, once the constraints of maintaining a fixed
body strength when compared with no exercise (1,23,24).
schedule are removed, participants are free to exercise at
Adverse Effects their convenience. To this end, once breast cancer survivors
No major adverse effects were reported in any of the 6 trials have undergone thorough instruction of exercise technique
included. by a fitness professional, they should be encouraged to per-
form this mode of exercise on their own.
DISCUSSION It is worth noting that the National Lymphedema (NLN)
This systematic review is the first to explicitly investigate Network Medical Advisory Committee recommends use of
whether women who have, or are at risk for, BCRL can compression garments during exercise, particularly among
perform resistance training at sufficient intensities to breast cancer survivors who have lymphedema (8). Among
improve muscular strength without increasing BCRL symp- trials reporting on the use of compression garments in this
toms or incidence of BCRL. Six studies were considered review, 2 investigations required participants to wear com-
eligible, and based on the PEDro score, 5 were considered of pression garments during RET (23,24), whereas 1 trial gave
HQ and 1 of LQ. Despite widespread misconceptions that participants the choice of wearing compression garments,
breast cancer survivors should avoid upper-body exercise, whereby 25% opted to wear them (6). Interestingly, in the
there is no evidence to suggest that RET increases the trial not requiring garments, no changes to lymphedema
incidence or is associated with BCRL exacerbations. More- status were reported among participants not wearing the
over, there is strong evidence that resistance training has compression garments. Accordingly, future trials should
favorable effects in women who are at risk for, or currently investigate the necessity of garments, as these are often re-
have, BCRL. ported to be restrictive and uncomfortable during exercise.
Preliminarily RET recommendations regarding the prin- Although tremendous advances have been made regard-
ciples of progression, frequency, intensity, and volume can ing our understanding of resistance training and BCRL,
be gained from this systematic review. First, it seems that there are some notable research gaps and challenges that

VOLUME 30 | NUMBER 9 | SEPTEMBER 2016 | 2663

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
BCRL and Resistance Exercise

BCRL researchers face. First, current evidence is lacking  Initiate RET at a low level of intensity and use a conser-
regarding the programming variables of order, exercise vative model of progression.
selection, and rest periods. Second, to reduce the risk of  Be cognizant of early signs of potential injury or symp-
musculoskeletal injury in this population, future study should tom flare-up (e.g., increased muscle soreness, excessive
investigate the utility of including exercises that consider fatigue, redness, or heaviness in the involved arm, bone,
endurance, strength, range of motion (ROM), and function and joint pain).
of specific areas that may be affected by breast cancer  Select exercises that are appropriate for the breast can-
treatments (e.g., rotator cuff muscles (3), core function, cer survivor’s training experience and consider ROM
respiratory diaphragm muscles). Third, factors such as restrictions that may result from surgery and/or radia-
obesity, age, nutrition, and level of deconditioning are tion therapy.
variables known to influence exercise-related outcomes in  Set realistic training goals.
apparently healthy and at-risk populations. These factors  Prescribe RET based on current fitness level and desires
have not been fully explored within the context of BCRL; of the participant.
whereby subgroup analysis may reveal specific associations  All individuals with BCRL or those who are at risk for
that might influence exercise prescription. Fourth, the BCRL should have medical approval before beginning
psychosocial variables that may influence participation in any exercise, particularly in the presence of cardiovas-
PA and exercise (e.g., fear avoidance, coping strategies) are cular, pulmonary, or metabolic disease.
not fully understood in this population and are worthy of Practitioners and researchers must be aware that the
further study. Fifth, ACSM guidelines recommend a combi- aforementioned recommendations are derived from the
nation of aerobic and resistance training for individuals with limited available evidence. To better understand the effects
cancer as each confers unique health benefits (2). To date, of RET among breast cancer survivors with, or at risk for
there is a paucity of data regarding the combined effects of BCRL, further research is necessary. Specific areas of
RET and aerobic conditioning among those with or at risk investigation should include the influence of biopsychosocial
for BCRL. Finally, to strengthen the evidence regarding the factors (fear avoidance, age, obesity, and overweight) known
effects of exercise in this population, universally accepted to influence RET outcomes in other populations and
BCRL diagnostic criteria, measurement methods, and termi- determining optimal training dose, rest periods, and exercise
nology must be established. selection.
This review is not without limitations. First, there was
only 1 reviewer who performed the literature search and REFERENCES
handled data extraction; as such, bias is an inherent 1. Ahmed, RL, Thomas, W, Yee, D, and Schmitz, KH. Randomized
limitation. Second, this review included a relatively small controlled trial of weight training and lymphedema in breast cancer
survivors. J Clin Oncol 24: 2765–2772, 2006.
number of investigations (n = 6) trials. Third, there was
2. American College of Sports Medicine. ACSM’s Guidelines for
significant heterogeneity of training volume and exercise Exercise Testing and Prescription. Baltimore, MD: Lippincott Williams
selection, and strength outcomes (i.e., 1RM bench press & Wilkins, 2014.
and leg press, shoulder abduction and flexion, weight lifted 3. Brown, JC, Troxel, AB, and Schmitz, KH. Safety of weightlifting
at final session compared with beginning of the study), among women with or at risk for breast cancer-related
lymphedema: Musculoskeletal injuries and health care use in
which limits the pooling of data and the robustness of con- a weightlifting rehabilitation trial. Oncologist 17: 1120–1128, 2012.
clusions. Finally, RCTs that were not reported in English 4. Cameron, D, Douglas, S, Brown, J, and Anderson, R. Bone mineral
were not considered for this review; as such, studies relevant density loss during adjuvant chemotherapy in pre-menopausal
to this topic may have been missed. For these reasons, cau- women with early breast cancer: Is it dependent on oestrogen
deficiency? Breast Cancer Res Treat 23: 805–814, 2010.
tion must be used when interpreting the results of this sys-
tematic review. 5. Coleman, MP, Quaresma, M, Berrino, F, Lutz, J, De Angelis, R,
Capocaccia, R, Baili, P, Rachet, B, Gatta, G, Hakulinen, T,
Micheli, A, Sant, M, Weir, HK, Elwood, JM, Tsukuma, H,
PRACTICAL APPLICATIONS Koifman, S, E Silva, GA, Francisci, S, Santaquilani, M, Verdecchia, A,
Based on the findings of this review, a few preliminarily Storm, HH, and Young, JL. Fast track—Articles: Cancer survival in
five continents: A worldwide population-based study (CONCORD).
recommendations can be made regarding RET among those Lancet Oncol 9: 730–756, 2008.
with or at risk for BRCL. It seems that 2 to 3 days of 6. Cormie, P, Pumpa, K, Galvao, DA, Turner, E, Spry, N, Saunders, C,
progressive RET, performed on nonconsecutive days, is an Zissiadis, Y, and Newton, RU. Is it safe and efficacious for women
effective method to develop strength without risk of with lymphedema secondary to breast cancer to lift heavy weights
during exercise: A randomised controlled trial [with consumer
incidence or exacerbation of lymphedema among breast summary]. J Cancer Survivorship 7: 413–424, 2013.
cancer survivors. In this review, all 6 studies reported on the 7. Courneya, KS, Segal, RJ, Mackey, JR, Gelmon, K, Reid, RD,
safety of RET, with no evidence of serious adverse effects Friedenreich, CM, Ladha, AB, Proulx, C, Vallance, JKH, Lane, K,
associated with this mode of training. Notwithstanding, Yasui, Y, and McKenzie, DC. Effects of aerobic and resistance
exercise in breast cancer patients receiving adjuvant chemotherapy:
there are a few safeguards that practitioners should be made A multicenter randomized controlled trial. J Clin Oncol 25: 4396–
aware of before initiating RET: 4404, 2007.
the TM

2664 Journal of Strength and Conditioning Research

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.
the TM

Journal of Strength and Conditioning Research | www.nsca.com

8. Denlinger, C, Ligibel, J, Are, M, Baker, K, Demark-Wahnefried, W, 17. Lasinski, BB. Complete decongestive therapy for treatment of
Dizon, D, Friedman, D, Goldman, M, Jones, L, King, A, Ku, G, lymphedema. Semin Oncol Nurs 29: 20–27, 2013.
Kvale, E, Langbaum, T, Leonardi-Warren, K, McCabe, M, Melisko, M, 18. Maher, CG, Sherrington, C, Herbert, RD, Moseley, AM, and
Montoya, J, Mooney, K, Morgan, M, Moslehi, J, O’Connor, T, Elkins, M. Reliability of the PEDro scale for rating quality of
Overholser, L, Paskett, E, Peppercorn, J, Raza, M, Rodriguez, M, randomized controlled trials. Phys Ther 83: 713–721, 2003.
Syrjala, K, Urba, S, Wakabayashi, M, Zee, P, McMillian, N, and
Freedman-Cass, D. Survivorship: Healthy lifestyles, version 2.2014. 19. Moher, D, Liberati, A, Tetzlaff, J, and Altman, DG. Preferred
J Natl Compr Canc Netw 12: 1222–1237, 2014. reporting items for systematic reviews and meta-analyses: The
PRISMA statement. Ann Intern Med 151: 264–269, 2009.
9. Ezzo, J. Manual lymphatic drainage for lymphedema following
breast cancer treatment. Cochrane Database Syst Rev 5, 2015. DOI:10. 20. Mortimer, P. The pathophysiology of lymphedema. Cancer 83:
1002/14651858. 2798–2802, 1998.
10. Gashev, A. Physiologic aspects of lymphatic contractile function: 21. Petrek, JA, Senie, RT, Peters, M, and Rosen, PP. Lymphedema in
Current perspectives. Ann NY Acad Sci 979: 178–187, 2002. a cohort of breast carcinoma survivors 20 years after diagnosis.
Cancer 92: 1368–1377, 2001.
11. Goddard, A, Pierce, C, and McLeod, K. Reversal of lower limb edea
by calf muscle pump stimulation. J Cardiopulm Rehabil Prev 28: 174– 22. Powell, KE, Heath, GW, Kresnow, MJ, Sacks, JJ, and
179, 2008. Branche, CM. Injury rates from walking, gardening, weightlifting,
outdoor bicycling, and aerobics. Med Sci Sports Exerc 30: 1246–
12. Greep, N, Giuliano, A, Hansen, N, Taketani, T, Wang, H, and
1249, 1998.
Singer, F. The effects of adjuvant chemotherapy on bone density in
postmenopausal women with early breast cancer. Am J Med 114: 23. Schmitz, KH, Ahmed, RL, Troxel, AB, Cheville, A, Lewis-Grant, L,
653–659, 2003. Smith, R, Bryan, CJ, Williams-Smith, CT, and Chittams, J. Weight
lifting for women at risk for breast cancer-related lymphedema: A
13. Hayes, SC, Janda, M, Cornish, B, Battistutta, D, and Newman, B.
randomized trial. JAMA 304: 2699–2705, 2010.
Lymphoedema following breast cancer: Incidence, risk factors and
effect on upper body function. J Clin Oncol 26: 3536–3542, 2008. 24. Schmitz, KH, Ahmed, RL, Troxel, A, Cheville, A, Smith, R, Lewis-
Grant, L, Bryan, CJ, Williams-Smith, CT, and Greene, QP. Weight
14. Helyer, L, Varnic, M, Le, L, Leong, W, and McReady, D. Obesity is
lifting in women with breast-cancer-related lymphedema. N Engl J
a risk factor for developing postoperative lymphedema in breast
cancer patients. Breast J 16: 48–54, 2010. Med 361: 664–673, 2009.

15. Johansson, K, Ingvar, C, Albertsson, M, and Ekdahl, C. Arm 25. Sherrington, C, Herbert, RD, Maher, CG, and Moseley, AM.
lymphoedema, shoulder mobility and muscle strength after breast cancer PEDro. A database of randomized trials and systematic reviews in
treatment—A prospective 2-year study. Adv Physiother 3: 55–66, 2001. physiotherapy. Man Ther 5: 223–226, 2000.

16. Kilbreath, SL, Refshauge, KM, Beith, JM, Ward, C, Lee, M, 26. Siegel, RL, Miller, KD, and Jemal, A. Cancer statistics, 2015. CA
Simpson, JM, and Hansen, R. Upper limb progressive resistance Cancer J Clin 65: 5–29, 2015.
training and stretching exercises following surgery for early breast 27. van Tulder, M, Furlan, A, Bombardier, C, and Bouter, L. Updated
cancer: A randomized controlled trial. Breast Cancer Res Treat 133: method guidelines for systematic reviews in the cochrane
667–676, 2012. collaboration back review group. Spine 28: 1290–1299, 2003.

VOLUME 30 | NUMBER 9 | SEPTEMBER 2016 | 2665

Copyright © National Strength and Conditioning Association Unauthorized reproduction of this article is prohibited.

You might also like