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Received: 17 June 2017 | Accepted: 21 July 2017

DOI: 10.1002/jso.24800

RESEARCH ARTICLE

Changes in shoulder muscle activity pattern on surface


electromyography after breast cancer surgery

Eun Joo Yang MD, PhD1 | YoungOk Kwon PhD2

1 Department of Rehabilitation Medicine,


Seoul National University Bundang Hospital, Background and Objectives: Alterations in muscle activation and restricted shoulder
Seoul National University College of
mobility, which are common in breast cancer patients, have been found to affect
Medicine, Seongnam, Korea
2 Division
of Business Administration, upper limb function. The purpose of this study was to determine muscle activity
Sookmyung Women’s University, Seoul, Korea patterns, and to compare the prevalence of abnormal patterns among the type of

Correspondence
breast surgery.
YoungOk Kwon, Associate Professor, Division Methods: In total, 274 breast cancer patients were recruited after surgery. Type of
of Business Administration, Sookmyung
Women’s University, Address: Cheongpa-ro
breast surgery was divided into mastectomy without reconstruction (Mastectomy),
47-gil 100, Yongsan-gu, Seoul, Korea. reconstruction with tissue expander/implant (TEI), latissimus dorsi (LD) flap, or
Email: yokwon@sm.ac.kr
transverse rectus abdominis flap (TRAM). Activities of shoulder muscles were
Funding information measured using surface electromyography. Experimental analysis was conducted
National Research Foundation of Korea,
Grant number: 2014R1A1A2055384
using a Gaussian filter smoothing method with regression.
Results: Patients demonstrated different patterns of muscle activation, such as normal,
lower muscle electrical activity, and tightness. After adjusting for BMI and breast
surgery, the odds of lower muscle electrical activity and tightness in the TRAM are
40.2% and 38.4% less than in the Mastectomy only group. The prevalence of abnormal
patterns was significantly greater in the ALND than SLNB in all except TRAM.
Conclusions: Alterations in muscle activity patterns differed by breast surgery and
reconstruction type. For breast cancer patients with ALND, TRAM may be the best
choice for maintaining upper limb function.

KEYWORDS
breast cancer, reconstruction, shoulder muscle, surface electromyography

1 | INTRODUCTION achieve a smooth scapulohumeral rhythm. The contributions made by


various muscles to shoulder motion have been studied using various
The possibility of shoulder morbidity following treatment for breast approaches, including assessment of muscle activation by electromy-
cancer is well known. Patient reports of arm morbidity include pain, ography (EMG) during arm motion.6 However, shoulder muscle
1
weakness, tightness, and reduced functional capacity. Evaluations of activation in breast cancer patients depends on both clinical and
altered shoulder movements in breast cancer patients have taken the patient variables, such as the use of chemotherapy, type of breast
form of clinical observations and goniometric measures of the surgery, time since surgery, and current physiotherapy, exercise, and
glenohumeral range of movement2,3 or assessments of shoulder pain statuses.7 To date, shoulder morbidity has been described
4,5
kinematics and muscle function. Elevation of the arm is a function of according to knowledge of how muscle activation and force
both glenohumeral movement and scapulothoracic movement and production contribute to shoulder kinematics in patients with breast
timed interaction between these two groups of muscle is essential to cancer.

116 | © 2017 Wiley Periodicals, Inc. wileyonlinelibrary.com/journal/jso J Surg Oncol. 2018;117:116–123.


YANG AND KWON | 117

Pectoralis tightness, the most common form of upper limb The study protocol was approved by the institutional review board
8
dysfunction at up to 6 months after breast surgery, can alter scapular of the authors’ institution. All participants provided written informed
kinematics.9 The scapula provides a foundational base of support for consent. The trial was conducted in accordance with the Declaration of
coordinated, functional shoulder movements.10 Alterations in scapular Helsinki.15
muscle activation, which are common in breast cancer patients, may
affect upper limb function differently according to treatment and
2.2 | Surface electromyography (SEMG)
patient factors. Previous research demonstrated an association
between dysfunction and more aggressive mastectomy procedures.11 SEMG signals were acquired using a four-channel EMG Nicolet EDX
There are strong associations between shoulder movement deviations, instrument (Natus Medical, Inc, San Carlos, CA). SEMG recordings
muscle control, patient-reported pain, chemotherapy, and radiother- were done for each muscle using small disposable electrodes (Ag/AgCl
apy.12,13 In one study, fear of lymphedema and disuse of the affected discs, 10 mm in diameter; CareFusion, San Diego, CA) in a bipolar
arm contributed significantly to a difference in muscle strength configuration. The sites of electrode placement were prepared by
between the affected and unaffected shoulders of patients.14 Pain abrading the skin with fine sandpaper and cleansing the area with 70%
7
serves to increase muscle activation and is likely to limit movement. isopropyl alcohol. Excess hair was shaved off as necessary. Bipolar
Along with the key clinical variables of age, affected side, dominant surface electrodes were placed on the skin overlying the scapular and
hand, degree of arm elevation, treatment protocol, time since surgery, shoulder muscles, and reference electrodes were placed on the
chemotherapy status, and degree of shoulder pain, the extent of ipsilateral clavicle of the test extremity. The anatomic placement of
pectoralis tightness should also be considered. electrodes was parallel to the fiber direction of each muscle, as follows:
Changes in force transfer of part of the pectoralis major (PM) upper trapezius (UT) electrodes were placed at half the distance
muscle after breast reconstruction could reduce the contribution between the spine (C7 vertebra) and acromion process over the muscle
to overall force and movement. Fear of lymphedema may further belly. Deltoid (D) electrodes were placed over the most prominent
weaken the affected arm due to reduced muscle activity. Previous portion of the middle D. Pectoralis (P) electrodes were placed below
studies have reported the prevalence rates of impaired range of the clavicle and above the breast and nipple. Bilateral EMG measure-
motion (ROM; 2-51%) and decreased strength (17-33%) after ments of the shoulder muscles were taken for each patient. The
breast cancer surgery.3,8 Factors that contribute to muscle activity of each muscle was recorded in microvolts (μV) for 1 ms during
weakness and tightness, such as the type of breast cancer arm abduction. At each time point, four EMG measures were obtained
treatment, should be identified. With so many treatment options (one for each of the four muscles), to allow for the possibility of
available, both the type of breast surgery, such as breast multiple correlations. The incremental data obtained at different time
conservation and mastectomy, and the type of reconstruction, points in each muscle can also be regarded as “repeated measures.” In
such as implant-based procedures and flap-based techniques, summary, four responses (one each for each shoulder and each
should be considered. Weighing the relative risks and benefits of movement) were generated and correlated.
each type of operation can prove challenging.
In this study, we compared the shoulder kinematics and spatial
2.3 | Shoulder range of motion
pattern of muscle activation associated with various breast cancer
treatments. The hypothesis of our study was that alterations in the Shoulder ROM was measured in abduction in the affected upper limb
normal motion of the shoulder may be associated with scapular using a goniometer, based on our clinical experience with patients in
positioning, as well as movement-related pain and lower muscle a seated position.8 Movement-related pain was assessed using an
electrical activity. The purpose of this study was to compare shoulder 11-point numerical rating scale (NRS).16,17 Clinically meaningful
muscle activity in the affected and unaffected shoulder, and to explore restriction in ROM was >10°, according to the definition of Thomas-
the impact of type of breast and lymph node surgery, and shoulder Maclean et al.18
contracture, on the observed deviation. In the absence of definitive diagnostic criteria, to rule out
pectoralis tightness or establish the degree of limitation in movement
after breast cancer surgery, pectoralis tightness was defined as the
2 | M ATERIA LS AN D METH ODS
presence of a limitation in forward flexion >10°, with no limitation in
external rotation, and a limitation in horizontal abduction of >10°,
2.1 | Subjects
based on our clinical experience.19
Between July 2013 and March 2016, 274 women with breast cancer Clinical variables included the affected side, degree of arm
underwent breast surgery at the authors’ institution. Patients who had elevation, type of surgery, type of reconstruction, time since surgery
bilateral or recurrent breast cancer, a history of previous cancer, or (3, 6, and 24 months), age (years), and body mass index (BMI). The
who needed palliative surgery or a contralateral breast operation for breast surgery group included patients who receive mastectomy
benign disease were excluded. Patients who complained of pain on without reconstruction (Mastectomy group) and patients who
shoulder movement, or had a previous history of upper limb received underwent breast reconstruction using a transverse rectus
dysfunction, were also excluded. abdominis (TRAM) flap (TRAM group)20 and latissimus dorsi (LD) flap
118 | YANG AND KWON

(LD group),21,22 and subpectoral prosthetic reconstruction with a undergo reconstruction procedures. The average age of the cohort
23
tissue expander/implant (TEI group). was 50.6 ± 0.31 years and the average BMI was 23.3 ± 0.12 kg/m2.
Clinical characteristics of breast cancer patients are summarized in
Table 1.
2.4 | Pattern analysis of EMG data At months 3, 6, and 24 (M3, M6, and M24, respectively), 11.6%,

Analysis was conducted after Gaussian filter smoothing to eliminate 5.8%, and 17.2% of the patients showed reported normal patterns of
noise. Linear regression modeling was done to analyze trends. First, muscle activation. Lower muscle electrical activity patterns were seen
using data from the EMG analysis, we constructed a polynomial in 9.1% of patients at M3, 3.3% at M6, and 12.9% at M24. Tightness
regression model that fitted the data. Second, we converted negative patterns were seen in 12.0%, 10.1%, and 17.8% of the patients at M3,

values to positive values to make the model fit better. Finally, we M6, and M24, respectively (see Figure 1). Comparisons of the
applied a Gaussian filter to remove outliers. As shown in Supplemen- prevalence of the different muscle activation patterns such as normal,
tary Online Resource S1, the difference between the left and right tightness, and lower muscle electrical activity between the breast

sides was analyzed by computing the ratio (%) between the area under surgeries and between the axillary surgeries are illustrated at all time
the curve (AUC; red) and the AUC (black) of the unaffected side. points in Figure 2. The prevalence of lower muscle electrical activity
Significant outliers (above 120%; 64 of 1041 data points) were were significantly greater in the ALND group compared with the SLNB

identified and removed. Then, the averages of the ratios were group at 3 months after surgery in patients without reconstruction
compared between the different conditions, that is, surgery type, (41.0% vs 6.3% at 3 months, P < 0.001), but by 6 months, no significant
muscle, activity, and time since surgery. The lowest quintile of each difference was observed between groups. In the patients with LD flap,
muscle ratio was classified as lower muscle electrical activity. the prevalence of lower muscle electrical activity were significantly
According to the combination of lower muscle electrical activity greater in the ALND group at 6 months (50.0% vs 0% at 6 months,
patterns, shoulder muscle activation patterns were reclassified into P < 0.001). The prevalence of tightness was significantly greater in the
normal (no D or UT lower muscle electrical activity), lower muscle ALND group in compared with the SLNB group in patients without

electrical activity (D and/or UT lower electrical activity, and P lower reconstruction (58.3% vs 30.0% at 6 months, P < 0.001), patients with
muscle electrical activity without pectoralis tightness [as defined by TEI (50.0% vs 37.5% at 3 months, P < 0.001), and LD flap (66.6% vs
the ROM]), and tightness groups (D and/or UT lower muscle electrical 33.3% at 3 months, P < 0.001; 100% vs 62.5% at 6 months, P < 0.001).

activity with normal P, and pectoralis tightness [as defined by the No significant difference was observed between the ALND and SLNB
ROM]). group in TRAM flap group.
Table 2 shows the results of univariate and multivariate analyses
of shoulder activation patterns (normal, lower muscle electrical
2.5 | Statistical analysis activity, tightness). In univariate analyses, lower muscle electrical
activity (vs normal) was positively associated with BMI (odds ratio
We used a mixed multinominal logistic regression model to test for
[OR] = 1.115, 95% confidence interval [CI] = 1.061-1.172; P < 0.001)
associations between the factors and muscle activity pattern (normal,
and negatively associated with axillary surgery (sentinel lymph node
lower muscle electrical activity, tightness): The factors were as follows:
biopsy [SLNB] vs axillary lymph node dissection [ALND], OR = 0.676,
(1) follow-up characteristics: follow-up time; (2) personal factors: age,
95%CI = 0.466-0.980; P = 0.039) and reconstruction surgery (TRAM vs
dominant hand, BMI; (3) treatment characteristics: breast surgery such
no reconstruction, OR = 0.346, 95%CI = 0.160-0.751; P = 0.007).
as Mastectomy, TRAM, LD, TEI group, and axillary surgery such as
Variables with a P value >0.05 were removed from multivariate
axillary lymph node dissection (ALND) and sentinel lymph node biopsy
stepwise regression analyses (forward selection), whereas those with a
(SLNB); and (4) functional factors: pain limited ROM. Before the
P value >0.1 were eliminated. Results of the multivariate multinomial
analyses, normalized EMG data were evaluated for outliers and
logistic regression for the lower muscle electrical activity muscle
sphericity using the Kolmogorov-Smirnov test.
activation pattern (vs normal) showed that after adjusting for BMI and
The velocities of the trajectories were computed by numerical
breast surgery, the odds of lower muscle electrical activity in the TRAM
differentiation after smoothing (bidirectional second-order Butter-
group are 47.3% less than in the Mastectomy group (TRAM vs no
worth low-pass filter at 8 Hz). When a significant effect was observed,
reconstruction, OR = 0.475, 95% CI = 0.161-0.624; P = 0.017).
Bonferroni adjustment was performed for pair-wise comparisons. In all
Tightness was analyzed in a similar way and results also revealed
tests, P values <0.05 were considered to indicate statistical
negative association with TRAM flap reconstruction. In univariate
significance.
analyses, tightness (vs normal) was positively associated with time
since surgery (M6 vs M3, OR = 1.696, 95%CI = 1.079-2.667;
3 | RE SULTS P = 0.022), side of operation (left vs right, OR = 1.414,
95%CI = 1.028-1.945; P = 0.033), and negatively associated with
Data from 274 patients were included in the analysis. The reconstruction surgery (TRAM vs no reconstruction, OR = 0.402,
reconstructions included 38 implant procedures (13.8%), 18 LD flaps 95%CI = 0.210-0.768; P = 0.006). Results of the multivariable multi-
(6.5%), and 18 TRAM flaps (6.5%). In total, 200 patients did not nomial regression for the tightness muscle activation pattern (vs
YANG AND KWON | 119

TABLE 1 Clinical characteristics of breast cancer patients


Without reconstruction (n = 200) TEI (n = 38) LD flap (n = 18) TRAM flap (n = 18)
Age (y) 52.07 ± 0.36 47.68 ± 0.60 45.27 ± 0.94 46.56 ± 1.12
(51.35-52.78) (46.50-46.85) (43.42-47.14) (44.37-48.74)
BMI 23.60 ± 0.26 22.75 ± 0.51 23.10 ± 1.19 21.99 ± 0.56
(23.08-24.12) (21.75-23.75) (21.05-25.16) (20.88-23.09)
Side
Rt 105 14 9 15
Lt 95 24 9 3
Time after surgery
3 months 56 12 12 9
6 months 35 9 4 5
24 months 109 17 2 4
Axillary surgery
ALND 141 7 6 9
SLNB 59 31 12 8
EMG ratio 21.79 ± 1.03 23.31 ± 2.79 28.87 ± 6.28 27.64 ± 6.40
(19.76-23.83) (17.81-28.81) (16.50-41.25) (15.04-40.24)
Shoulder muscle activation pattern
Normal 64 14 7 10
Weakness 56 7 3 3
Tightness 80 17 8 5

BMI, body mass index; Rt, right; Lt, left; ALND, axillary lymph node dissection; SLNB, sentinel lymph node biopsy; EMG, electromyography TEI, tissue
expander/implant; LD, latissimus dorsi; TRAM, transverse rectus abdominis.
Data are means ± standard error (95%CI).

FIGURE 1 Comparison of muscle activation pattern according to type of breast surgery and time since surgery. Type of breast surgery are
mastectomy without reconstruction (Mastectomy) and with reconstruction by tissue expander/implant (TEI), latissimus dorsi flap (LD), or
transverse rectus abdominis flap (TRAM). SLNB, sentinel lymph node biopsy; ALND, axillary lymph node dissection; P, pectoralis; UT, upper
trapezius; D, deltoid
120 | YANG AND KWON

FIGURE 2 Comparison of muscle activation pattern according to type of breast surgery, type of axillary surgery, and time since surgery.
TEI, tissue expander/implant; LD, latissimus dorsi; TRAM, transverse rectus abdominis; SLNB, sentinel lymph node biopsy; ALND, axillary
lymph node dissection

normal) showed that after adjusting for time since surgery and side of considered, because there are differences in muscle adaptation
operation, the odds of tightness in the TRAM group are 38.4% less according to the type of movement performed and type of surgery
than in the Mastectomy group with the true population effect received.
between 75.5% and 19.5%. (TRAM vs no reconstruction, OR = 0.384, Some types of reconstruction, such as the LD flap, cause
95%CI = 0.195-0.755; P = 0.006). decreased muscle strength compared with controls,25 while other
types of reconstruction, such as those using implants or a mastectomy,
4 | DISCUSSION can cause pectoralis tightness.8,26,27 In a systematic review by Hidding
et al28 done in 2014, patients who underwent immediate breast
Our findings showed that shoulder muscle activation depends on reconstruction showed less impairment of upper extremity function
clinical and treatment variables, and the prevalence of the abnormal compared with those who underwent only a mastectomy. However,
activation patterns, such as lower muscle electrical activity or variables such as the method of reconstruction or mastectomy, and
tightness, varied depending on the type of breast surgery and type ALND and radiotherapy status, were not included in the analysis. In our
of reconstruction. Tightness was common after tissue expander/ study, we compared different muscle activation patterns, such as
implant (TEI), but lower muscle electrical activity was more prevalent lower muscle electrical activity without tightness or tightness. Results
after an LD flap. Different axillary surgeries, such as ALND and SLNB, were also found to be different according to the reconstruction type.
done within the same breast surgery or reconstruction, may affect the Tightness was common after TEI, but the lower muscle electrical
prevalence of abnormal muscle activation patterns, but there was less activity pattern was more prevalent after an LD flap. Moreover, the
of an association with TRAM flaps. type of axillary surgery was significantly associated with the
It has been shown that survival and recurrence rates after breast- prevalence of upper limb dysfunction.
conserving surgery are almost identical to those of patients undergoing Upper limb dysfunction has been assessed previously by using the
total mastectomies and radiation therapy, and that the choice of disabilities of the arm, shoulder, and hand (DASH) question-
treatment should be made only after the patient has been fully naire.25,29,30 Forthomme et al24 found decreased muscle strength
informed by the surgeon of the risks and benefits of each procedure. after an LD flap in a comparison of the isokinetic test results for
With respect to clinical factors, previous work has demonstrated that different shoulder muscles. Oskrochi et al7 investigated shoulder
surgical breast cancer treatment can result in shoulder morbidity,12 muscle activities by SEMG to analyze shoulder complexity in breast
which is an important factor in quality of life. Previous studies reported cancer patients. In our study, shoulder complexity after breast cancer
on the impact of shoulder morbidity according to differences in PM was assessed by both SEMG and measurement of the ROM.
activity associated with different types of breast surgery, such as Pectoralis tightness, which is a clinically important complication
mastectomy and wide local excision, 13
or by comparing isokinetic that causes pain and limits the ROM,9 is one of the most common types
muscle strength test results among the different reconstruction of upper limb dysfunction.8,26,27 Scar tissue formation and anterior
types. 24
However, the complexity of shoulder morbidity should be chest wall tightness31 changed muscle activation patterns more clearly
YANG
AND
KWON

TABLE 2 Factors associated with shoulder muscle activation pattern (normal, weakness, tightness): univariate and multivariate logistic regression
Univariate analysis Multivariate analysis

Normal vs weakness Normal vs tightness Normal vs weakness Normal vs tightness

OR 95%CI P OR 95%CI P OR 95%CI P OR 95%CI P


Age 0.995 0.974-1.016 0.653 1.012 0.993-1.030 0.192
BMI 1.115 1.061-1.172 <0.001 1.024 0.977-1.073 0.317 1.103 1.049-1.161 <0.001
Month (M)
M3 1 1 1
M6 0.721 0.411-1.261 0.25 1.696 1.079-2.667 0.022 1.562 0.980-2.490 0.061
M 24 0.964 0.651-1.428 0.857 1.003 0.698-1.443 0.983 0.656 0.415-1.035 0.071
Side
Rt 1 1 1 1
Lt 1.351 0.943- 1.933 0.1 1.414 1.028-1.945 0.033 1.296 0.898-1.871 0.166 1.341 1.114-1.883 0.045
Axillary surgery
ALND 1 1 1
SLNB 0.676 0.466-0.980 0.039 1.007 0.728-1.393 0.964 0.820 0.576-1.169 0.274
Reconstruction
No recon 1 1 1 1
TEI 0.577 0.328-1.014 0.056 0.976 0.622-1.531 0.918 0.667 0.362-1.228 0.194 0.904 0.551-1.481 0.689
LD 0.495 0.220-1.111 0.088 0.919 0.496-1.700 0.788 0.536 0.232-1.235 0.144 0.863 0.448-1.662 0.660
TRAM 0.346 0.160-0.751 0.007 0.402 0.210-0.768 0.006 0.473 0.161-0.624 0.017 0.384 0.195-0.755 0.006

CI, confidence interval; BMI, body mass index; Rt, right; Lt, left, ALND, axillary lymph node dissection; SLNB, sentinel lymph node biopsy; TEI, tissue expander/implant; LD, latissimus dorsi; TRAM, transverse rectus
abdominis.
|
121
122 | YANG AND KWON

at the extremes of ROM, due to a pain due to stretching or tearing of 5 | CONCL US IO NS


32
tight or damaged tissues. In our study, the kinematics of the shoulder
joint and spatial activity of the UT and pectoralis were assessed during Alterations in muscle activity patterns differed by breast surgery and
shoulder exercises with and without pectoralis tightness. Postsurgical reconstruction type. For breast cancer patients with ALND, TRAM may
pain related to skin defects and contractures, as well as depression of be the best choice for maintaining upper limb function.
the shoulder girdle due to shortening of the PM and minor muscles, can
lead to a protective posture in patients undergoing mastectomy
without immediate breast reconstruction. In this study, TRAM and LD ACKNOWLEDGMENTS

flap reconstructions were associated with an improved prognosis, with The authors thank Jiho Park and Kiyoung Jang, PhD students at the
regard to tightened pectoralis muscles, versus mastectomy alone. Department of Computer Science, Yonsei University, Seoul, Korea, for
Even with normal pain-free motion of the arm and shoulder, in the their assistance with data collection. This research was supported by
scapulothoracic, glenohumeral, acromioclavicular, and sternoclavicular Basic Science Research Program through the National Research
joints,33 patients may encounter another issue, namely muscle lower Foundation of Korea (NRF) funded by the Ministry of Education (grant
muscle electrical activity. Some studies suggest that humeral elevation number 2014R1A1A2055384).
of the arm, upward movement on the affected side, and left shoulder
movement will increase the electrical activity of all four muscles
regardless of which side is affected, while treatment with wide local ORCID
excision and chemotherapy is associated with generally decreased
YoungOk Kwon PhD http://orcid.org/0000-0001-9231-0492
electrical activities.7 In our study, implant-based and TRAM flap
reconstruction did not affect shoulder muscle strength. However, the
LD flap, which involves detachment of both the origin and insertion
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