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Disability and Rehabilitation, 2008; 30(15): 1098 1105

RESEARCH PAPER

Decreased muscle strength following management of breast cancer

C. R. MERCHANT1, T. CHAPMAN1, S. L. KILBREATH1, K. M. REFSHAUGE1 & K. KRUPA2


1
Discipline of Physiotherapy, University of Sydney, and 2Breast and Endocrine Surgery Unit, Concord Hospital, Sydney,
New South Wales, Australia
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Accepted May 2007

Abstract
Purpose. To assess whether muscle strength, power and endurance at the affected shoulder were reduced in women
treated for breast cancer. Secondly, we assessed whether muscle performance was explained by management or other
symptoms.
Methods. Participants were 40 women (mean + SD: 56.7 + 11.6 yr) who had completed all treatments for breast cancer at
least 6 m previously. We measured dynamic concentric strength at one repetition maximum (1RM), endurance at 90%1RM,
and power through a range of 40 100% 1RM for shoulder protractors, extensors and retractors. Strength and endurance,
but not power, were measured for shoulder flexors. Additionally, maximal grip strength, passive shoulder range of motion
For personal use only.

and arm circumference were measured. Self-reported symptoms were recorded using a questionnaire.
Results. Shoulder protractors ( p 0.011), retractors ( p 0.007), and extensors (p 0.009), but not flexors, were signi-
ficantly weaker on the affected side compared to the unaffected side. Muscle power and endurance at the shoulder and grip
strength were not impaired. Inter-limb differences in muscle strength were not explained by the surgical and medical
management of the cancer. Self-reported weakness correlated poorly with our measures of muscle strength.
Conclusions. Long-term weakness occurs about the shoulder secondary to treatment for breast cancer. Strategies to prevent
weakness need to be considered.

Keywords: Shoulder, grip, strength, range of motion

see 8;2,9]. The prevalence of these symptoms at


Introduction
6 months or later following surgery is high: *25% of
In recent years, rates of survival from breast cancer women develop lymphedema; up to 18% have
have increased mainly due to early detection [1]; weakness; 420% have stiffness; and 40% have pain
however, as current management of breast cancer is in the axilla and/or chest wall [3,9,10]. Most of these
invasive, aggressive and liable to leave women with problems are present within 3 months of surgery and
long-term shoulder morbidity, the number of women have not resolved up to 2 years after surgery [9,11].
living with the after-effects of breast cancer mana- These symptoms have generally been attributed to
gement is increasing. It is not uncommon for surgery involving the axilla and to radiotherapy
women to report shoulder and upper limb problems [10,12 16].
years after surgery, particularly when the surgery in- The extent to which muscle strength at the
cluded axillary node dissection [2 4]. Interestingly, affected shoulder has been impaired has not been
womens self-reported impairments are often more investigated to date although women report weak-
severe than the measured changes would infer ness as a long-term problem. Grip strength has been
[5 7]. used as an indication of strength of the upper limb,
The chronic shoulder and arm problems identified even though surgery is in the region of the shoulder
by women after treatment for breast cancer include [2,17]. The aim of this descriptive study was,
weakness, arm and breast swelling (lymphedema), therefore, to determine the extent to which muscle
shoulder stiffness, pain, and numbness [for review, strength, power and endurance were impaired in

Correspondence: Dr Sharon L. Kilbreath, School of Physiotherapy, Faculty of Health Science, University of Sydney, PO Box 170, Lidcombe NSW 1825,
Australia. Tel: 61 2 9351 9272. Fax: 61 2 93519601. E-mail: s.kilbreath@usyd.edu.au
ISSN 0963-8288 print/ISSN 1464-5165 online 2008 Informa UK Ltd.
DOI: 10.1080/09638280701478512
Decreased muscle strength following management of breast cancer 1099

women treated for breast cancer, and whether inter- Table I. Participant characteristics and medical management.
limb strength was explained by the surgical and Mastectomy Wide Local
medical management. As loss of shoulder range and (n 16) Excision (n 24)
swelling are commonly reported and can impact on
shoulder strength, we also assessed range of motion Age (yr; mean + SD) 55.3 + 12.0 57.7 + 11.5
Time since surgery 27.7 + 21.4 29.3 + 21.0
at the shoulder and arm circumference.
(months; mean + SD)
Dominant side affected (n) 11 15

Methods Medical management (n)


Axillary surgery
Participants None 0 3
Sentinel node biopsy 5 3
Forty women who had undergone unilateral surgery Axillary lymph node biopsy 11 18
for breast cancer and whose treatment had been
Adjuvant treatment
completed for at least 6 months volunteered to parti- Radiotherapy 1 16
cipate. Participants responded to recruitment letters
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Chemotherapy 4 0
mailed out from either the local breast cancer sur- Both 5 7
geon associated with the study or through the Encore None 6 1
online support program run through the YWCA. To Hormone therapy 10 11
(Tamoxifen)
be included, participants were required to be female,
have undergone surgery for unilateral breast cancer, Symptoms (n)
and had their last intervention at least 6 months Swelling 4 2 cm{ 3 4
previously. Potential participants were excluded from Loss of range* 6 11
the study if they had undergone bilateral surgery, {
2 cm difference present between affected and unaffected limbs
experienced unstable hypertension or had a history of 10 cm above and/or below the elbow; *108 difference present
stroke, cardiac conditions, or had any upper limb between affected and unaffected limbs for forward flexion or
For personal use only.

morbidity of the non-surgical side. abduction range.


Participants were aged between 37 and 81 years
(mean + SD: 57 + 12 yr). All had undergone uni-
lateral surgery for breast cancer and had completed Muscle strength, power and endurance. The unilateral
their treatment for cancer between 9 and 106 months concentric strength of shoulder protractors, retrac-
previously (29 + 21 m). Sixteen women (40%) had tors and extensors was measured as the one repetition
undergone a mastectomy and 24 women (60%) a maximum (1RM) using Keiser pneumatic-resistance
wide local excision (WLE). Surgery was performed machines for biaxial chest press, shoulder retractors
to the breast on the same side as hand dominance in and latisimuss dorsi pull down1. The Hur Push
26 women (65%). Treatments and symptoms are Up machine2 was used to measure 1RM for the
summarized in Table I. shoulder flexors.
Ethics approval was received from the Human We used a standardized protocol for determining
Research Ethics Committee of The University of 1RM which involved familiarization with the equip-
Sydney and all participants gave informed consent ment, and verbal encouragement. For all tests, parti-
before data collection. cipants were seated with legs supported. For a lift to
be considered successful, it had to be completed
through full range with no compensatory movement.
Protocol
To identify 1RM accurately, the examiner pro-
Participants attended the research laboratory for one gressively increased the resistance until the partici-
test session lasting 2 hours. Both the affected and pant was unable to complete more than 1 repetition.
unaffected sides were tested. Muscle strength was To identify the 1RM required approximately 8
measured before power and endurance because the progressions.
1RM results were used as the basis for testing power Maximal grip strength was measured using a com-
and endurance. A recovery period of 10 15 min puterized dynamometer3. The participant was seated
between muscle tests ensured that there was suffi- with the forearm in neutral and the elbow at 908.
cient recovery time before commencing the next test. They squeezed the hand grip as hard as they could,
The protocols used for strength, power and endur- and the best of 3 attempts was used for analysis.
ance have been previously reported [18,19] and are The peak force, velocity and power achievable
based on the American College of Sports Medicine during a single explosive contraction for shoulder
Guidelines [20]; protocols for strength and power extensors, retractors and protractors were deter-
are reliable [21]. The order in which the muscle mined on the Keiser pneumatic-resistance training
groups were tested was randomized. equipment. The Hur Push Up used for measurement
1100 C. R. Merchant et al.

of the shoulder flexors did not have the capability to Arm swelling. Participants were seated with the arm
measure power. Participants were asked to perform a flexed to 908 and resting on a Perspex sheet marked
single repetition as rapidly as possible while main- with a 10610 cm grid. The circumference of the
taining good form. To identify peak power, which is arm was measured 10 cm above and below the
the product of the force and the velocity of muscle medial epicondyle using a soft narrow tape mea-
shortening [22], it is necessary to assess power across sure [23] and the grid lines to guide the location of
a range of resistances. The resistance was sequen- the tape measure. Reliability of measures of arm
tially increased to 40, 60, 80 and 100% of parti- circumference has been previously reported [24].
cipants previously determined 1RM. If the power at
100% 1RM was higher than at 80% 1RM, the load Self-reported arm symptoms. McCredie et al.s [3]
was increased by 10% increments until the power questionnaire regarding long-term arm symptoms
dropped below peak. This would be required if, for was used. Participants were asked if they had
example, the participants maximal effort had acti- experienced shoulder stiffness, or pain, numbness,
vated less than 100% of the motor units during or swelling in the arm after the first 6 months post
testing of 1RM. Peak power in watts (W), the surgery, or if they currently experienced these
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percentage of 1RM at which it occurred and the symptoms. In addition to the impairments listed
velocity (cm/s) were recorded. above, we also asked about muscle weakness. They
For measurement of muscle endurance, the were then asked whether the severity of their sym-
position and settings were the same as those used ptoms affected their activities of daily living (ADL).
for 1RM testing. The resistance was set at 90% of They responded with yes/no to indicate the occur-
participants previously determined 1RM for each rence of these symptoms and marked a 4-point
machine. Participants performed as many repetitions Likert scale (with descriptors not at all, only a
as possible at this load using a continuous slow pace little, quite a lot and a great deal) to assess the
until failure. The test was concluded when the lift severity of effect on performance of ADL.
could not be completed through the full range and
For personal use only.

without compensatory strategies. The number of


Data analysis
successful repetitions was recorded.
Descriptive statistics were used to summarize
participants characteristics and performance on
Range of motion
the measures of strength, power, endurance, range
Forward flexion, horizontal extension and external of motion, arm swelling and self-reported arm
rotation were measured passively at the shoulder of symptoms.
both the affected and non-affected sides, and abduc- To determine differences between arms, a 2-way
tion at the shoulder was measured actively. To repeated measures analysis of variance (ANOVA)
accommodate for preconditioning of soft tissue, each was performed for each variable of strength, power
movement was measured 3 times with each position and endurance. The within subject factors were
held for 3 s and a 10 s rest was given between each side (affected or unaffected) and muscle group
measurement. An inclinometer4 was used to mea- (shoulder protractors, retractors, extensors). For
sure the maximum displacement. measures of strength and endurance, muscle group
For measurement of passive range of movements, also included shoulder flexors. If significant effects
participants were positioned in supine with their were identified for side, each muscle group was
knees flexed; gravity provided the standardized force. analysed separately post hoc, using repeated mea-
Active abduction range at the shoulder joint was sures analysis of variance with the within-subject
measured with participants seated adjacent to the factor being side (affected, unaffected). The inter-
plinth. The plinth was adjusted in height to ensure limb difference in grip strength and arm swelling was
that the arm was held in 908 abduction and the assessed with paired t-tests.
forearm in neutral. To restrict movement predomi- We used Pearsons moment-product correlation
nantly to the glenohumeral joint and thereby avoid coefficient (r) to correlate our measurement of
compensatory shoulder elevation, movement of the strength of the affected arm, as well as the absolute
scapula was resisted by applying a downward difference between the affected and unaffected arm,
pressure over the clavicle. Participants were in- with perceived severity of weakness, and the extent
structed to lift the arm as high as they could. The to which weakness was perceived to affect ADL.
angle between the horizontal and the arm was Stepwise regression was used to determine the con-
recorded. This method is reliable (ICC(2,1) 0.81, tribution of type of surgery and adjuvant therapies
95% CI, 0.67 0.90), determined in our laboratory to interlimb differences of muscle strength. The
with a group of women (n 40) tested one week relationship of related symptoms to change in
apart. muscle strength was also investigated. A difference
Decreased muscle strength following management of breast cancer 1101

of 2 cm between the affected and unaffected arm


was defined as swelling. A loss of 10 deg in
forward flexion or abduction was determined as a
clinically worthwhile reduction in range [11]. The
significance level was set at p 5 0.05. Data are
presented as mean + SD. All statistical analyses were
performed using a statistical software package
(SPSS, version 11.0, SPSS headquarters, Chicago,
Illinois, USA).

Results
Strength, endurance and power
Overall, the affected side was significantly weaker
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than the unaffected side (Side: F 12.378;


p 0.001). Analysis of each muscle test revealed
that the affected side was significantly weaker than
the unaffected side for shoulder extensors (F 7.61,
p 0.009), protractors (F 7.04, p 0.011) and
retractors (F 8.241, p 0.007) but not for shoulder
flexors (F 3.24, p 0.080) or for grip strength
(F 0.003, p 0.957) (Figure 1). The affected
movements were 10% weaker than the unaffected
ones in approximately 25% of participants, and
For personal use only.

20% weaker in 5 11 participants (12.5 27.5%),


with shoulder retractors least affected and flexors the
most affected. The difference in 1RM was
8.8 + 20.0 N for shoulder extensors, 6.4 + 15.3 N
for shoulder protractors, 7.2 + 15.4 N for shoulder
retractors, 9.7 + 33.2 N for shoulder flexors and
0.4 + 43.2 N for grip strength. Absolute values for
strength are shown in Table II.
Unlike measures of muscle strength, the endur-
ance of the affected arm was not consistently poorer
than the unaffected arm (F 2.668; p 0.112).
However, an interaction was identified between
muscle groups tested and the side tested
(F 3.601; p 0.03) indicating that performance
varied across muscle groups and between sides.
Figure 1. Differences in strength and range of motion
Thus, each muscle group was analyzed separately.
(mean + SD) between the unaffected and affected arm. 1RM
No significant difference was identified between the differences are shown for the shoulder extensors, flexors,
number of repetitions performed by the affected and protractors and retractors, and for grip strength. Differences in
unaffected sides for shoulder protractors, retractors shoulder forward flexion, horizontal extension, external rotation
or flexors; however, the participants were able to and abduction range of motion are shown. The dotted lines
indicate that the affected arm is equal to the unaffected arm in
perform significantly more repetitions with the
terms of strength (A) or range (B). *Indicates significant difference
affected side than the unaffected side for shoulder between limbs.
extensors (Table II).
Overall, power was significantly less in the affected
arm (F 5.07, p 0.03) than the unaffected arm. unaffected sides. For example, the velocity at which
Analysis of each muscle group separately revealed peak power was achieved for shoulder protraction
that protractors were significantly less powerful on was 92.9 + 27.1 cm/s for the affected side and
the affected side (F 8.94, p 0.005), but the 93.2 + 27.4 cm/s for the unaffected side and the
extensors (p 0.08) and retractors were not percentage of force at which peak power was
(p 0.834) (Table II). There was no significant achieved for this muscle group was 71 + 12% 1RM
difference in the %1RM or the velocity at which for the affected side and 71 + 13% 1RM for the
maximum power was achieved between affected and unaffected side.
1102 C. R. Merchant et al.

Table II. Muscle strength, power, and endurance for the Table III. Self-reported symptoms.
affected and unaffected shoulder and muscle strength for grip
(mean + SD). Present in the past Present now

Percentage Yes No Yes No Effect on ADL*


difference
Muscle 19 21 15 25 Not at all: 23
(affected/
weakness Little bit: 12
Affected Unaffected unaffected)
A lot: 5
Strength (n) Muscle 17 23 10 30 Not at all: 24
Extensors* 113.2 + 30.2 122.0 + 27.4 93.2 + 16.3 stiffness Little bit: 10
Protractors* 108.4 + 32.5 115.0 + 28.9 93.3 + 14.0 A lot: 6
Retractors* 145.0 + 39.7 152.1 + 34.4 94.8 + 10.7
Flexors 113.8 + 52.0 123.6 + 49.0 92.2 + 26.9 Pain 26 14 16 24 Not at all: 18
Grip 254.0 + 72.6 254.0 + 60.8 99.6 + 16.5 Little bit: 18
A lot: 4
Power (watts)
Extensors 88.3 + 40.4 97.1 + 38.6 93.0 + 51.6 Swelling 21 19 18 22 Not at all: 23
Little bit: 11
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Protractors* 71.2 + 28.4 78.2 + 28.7 98.0 + 42.3


Retractors 117.9 + 51.1 118.7 + 53.9 109.7 + 69.0 A lot: 6

Endurance (repetitions) Numbness 24 16 22 18 Not at all: 25


Extensors* 12 + 5 10 + 5 Little bit: 12
Protractors 10 + 4 11 + 3 A lot: 3
Retractors 12 + 4 12 + 5
*ADL, activities of daily living.
Flexors 5+3 4+4

*Inter limb comparison significant (p 5 0.05).

weakness was poorly correlated with our measure-


ment of shoulder strength (r 0.26 0.41).
For personal use only.

Stepwise regression of medical interventions


Other impairments
(type of primary and axillary surgery, and occurrence
Overall, range of motion was impaired on the of radiotherapy and chemotherapy) did not explain
affected side (F 10.01; p 0.003). Analysis of each the difference in absolute muscle strength between
movement direction separately revealed that forward the two limbs. Stepwise regression of loss of 108
flexion (F 20.66, p 0.000), horizontal flexion range in forward flexion or abduction and swelling of
(F 12.33, p 0.001), external rotation (F 6.15, the limb was also conducted to determine whether
p 0.02) and abduction (F 12.71, p 0.001) were these other symptoms contributed to the between-
all significantly restricted on the affected side limb differences in shoulder strength. Decreased
(Figure 1). A difference of 108 between limbs for forward flexion significantly contributed to de-
abduction or forward flexion was experienced by 17 creased shoulder flexor strength (p 0.001) whereas
participants, of whom 5 experienced a loss 108 in decreased abduction significantly contributed to
both directions (Table I). decreased shoulder extensor strength ( p 0.045).
Overall, arm circumference was significantly great- Swelling did not contribute to loss of muscle
er on the affected side than the unaffected side strength.
(F 5.45, p 0.025). Analysis of each measurement
revealed that the affected arm was significantly bigger
Discussion
than the unaffected arm 10 cm below the elbow
(F 4.39, p 0.043) but not above the elbow This study shows that muscle strength about the
(F 3.89, p 0.06). A clinical diagnosis of lymphe- shoulder persists even years following surgery for
dema is based on a difference of 2 cm between breast cancer. However, the loss in strength for most
limbs [6,25,26]; seven women (17.5%) met this women was minimal. Whilst there was statistically
criterion (Table I). significant loss of muscle strength, the ability to
Analysis of self-reported symptoms revealed that activate the muscles, as evidenced by the lack of
31 (77.5%) women experienced at least one symp- significant difference between the affected and un-
tom. Nine women reported no current symptoms, affected side in tests of endurance and power, was
seven reported one symptom, nine reported two not overall significantly impaired. Loss of overhead
symptoms, seven reported three symptoms, five range 108, i.e., shoulder flexion and abduction,
reported four symptoms, and three women reported significantly contributed to loss of strength of
having all five symptoms (Table III). Of particular shoulder flexors and extensors.
note, 15 women reported that their affected arm was Because of our broad selection criteria, i.e.,
currently weak. However, self- reported shoulder surgery for breast cancer, it was not possible to
Decreased muscle strength following management of breast cancer 1103

determine from the current sample what aspects better than the unaffected side, albeit at an absolute
of the treatment contributed to the impairment. lower torque.
Given the relatively small cohort in this study, this Shoulder strength may not be addressed after
finding is not surprising. Further research, in a breast cancer surgery out of concern that measure-
larger sample, is now required to determine ment of strength and performance of resistance
whether particular interventions are associated with exercises may cause lymphedema [11,32]. However,
weakness. there is preliminary evidence to challenge the belief
Muscle weakness among the women in our study that resistance training early following surgery for
was not of the same magnitude as that reported by breast cancer leads to lymphedema [33]. In our pilot
Nikkanen et al. [27]. They showed a reduction in randomized controlled trial, 22 women who had
strength of 25% in women treated for breast cancer undergone surgery for breast cancer, including
up to 8 years after surgery [27]. Notably, the surgical axillary surgery, were randomized to either usual
and adjuvant treatment received by their cohort was care or to an exercise intervention group. The
more extensive. For example, 66 (87%) women had exercise comprised resistance training using thera-
undergone a Halsted mastectomy in which the entire band plus prolonged stretching commencing 4 weeks
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breast, chest muscles and all lymph nodes found in following surgery. No swelling, measured by arm
the axilla were removed, and a further 10 (13%) had circumference, occurred within the 8 weeks of
undergone a mastectomy with axillary exploration. training [33]. Furthermore, recent studies of
All participants received radiotherapy. Changes in moderate to high intensity resistance training in
surgical and medical management may explain, in women months to years following surgery for breast
part, why women typically present with only mild cancer has shown that resistance training neither
muscle weakness. In the current study, only 16 caused nor exacerbated lymphoedema [28,34 36].
(40%) women had undergone a mastectomy; of Thus, as shoulder weakness is a persisting problem
these women, none had their chest muscles removed, years following surgery, consideration should be
11 underwent axillary dissection, and only one had given to prescribing resistance training exercises for
For personal use only.

received radiotherapy. Lane et al. [28] found no these women.


difference in strength between the affected and We hypothesized that measurement of 1RM for
unaffected upper limb in women (n 16) months various shoulder movements would lead to good
following surgery for breast cancer. correlations between measured and self-reported
The relationship between the tests of muscle strength. However, only weak relationships were
strength and power raises an interesting issue. The found for strength. Comparison of the affected arm
shoulder protractors on the affected side were to the intact arm, rather than to an age-matched
reduced in strength and power, and there was a control group, may have biased the results. The
trend for shoulder extensors to be similarly impaired; majority of activities of daily living are bimanual [33],
however, whilst shoulder retractors were weak and therefore if the women had decreased the use of
compared to the unaffected side, power was not both arms, there may have been a consequent
impaired. Other factors may have contributed to the reduction in the strength of both arms. Another
weakness of the shoulder retractors, in particular, explanation for the lack of correlation may be that we
with no consequent reduction in power. Protocols measured the wrong impairment. In the current
such as the one used in this study rely on voluntary study, we examined participants ability to perform
effort. We do not know to what extent the muscles brief maximal contractions for assessment of 1RM,
were activated. Many factors can impact on effort, the power with which they could activate their
including pain and the intent to protect the limb muscles, and the number of repetitions they could
from maximal exertion. Shoulder retraction stretches perform. We did not examine the quality with
the muscles and tissue across the anterior chest wall. which they performed the task. It may be that the
To assess whether women were protecting their chest participants interpreted poor motor control as
and arm and, in fact, exerting less than maximal weakness.
effort, requires neurophysiological studies in which Grip strength has been measured in previous
their effort is compared to that elicited from an studies [17,26,37] as an indicator of upper limb
evoked contraction [29 31]. strength. We found no difference in grip strength
The finding that endurance was not impaired on between the affected and unaffected limb. As we did
the affected side indicates that while there may not have a control group, it is not known whether
weakness as a consequence of loss in cross-sectional the grip strength of both the affected and un-
area of the muscle, the ability to activate the muscle affected sides was within normal limits or both were
was not impaired. As the majority of women were weaker.
affected on their dominant side, it was not surprising The women in this study used a standardised,
that they could perform the same or even slightly rigorous protocol based on one repetition maximum
1104 C. R. Merchant et al.

(1RM) to determine the extent of shoulder weak- 6. Voogd AC, Ververs JM, Vingerhoets AJ, Roumen RM,
ness. There were no reports of increased arm Coebergh JW, Crommelin MA. Lymphoedema and reduced
shoulder function as indicators of quality of life after axillary
swelling and, anecdotally, one woman spontaneously lymph node dissection for invasive breast cancer. Br J Surg
reported that following the testing her arm swelling 2003;90:76 81.
had decreased. Testing was terminated in one 7. Hayes S, Battistutta D, Newman B, Hayes S, Battistutta D,
instance because the woman developed increasing Newman B. Objective and subjective upper body function
six months following diagnosis of breast cancer. Breast Cancer
pins and needles in a median nerve distribution
Res Treatment 2005;94:1 10.
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there was no prolonged adverse reaction. rehabilitation for women who have been treated for breast
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