Vol.5, No.11, 1866-1871 (2013) Health
http://dx.doi.org/10.4236/health.2013.511251
Electromyographic study of shoulder and
acromioclavicular joint muscles in women who
underwent unilateral breast surgery of the types
mastectomy and quadrantectomy
Antonia Dalla Pria Bankoff1,2, Sonia Regina Jurado2
1Postural Assessment Laboratory, FEF-Unicamp, Campinas, Brazil; dallabankoff@bol.com.br
2Federal University of Mato Grosso do Sul-Campus de Três Lagoas, Três Lagoas, Brazil
Received 10 September 2013; revised 15 October 2013; accepted 26 October 2013
Copyright © 2013 Antonia Dalla Pria Bankoff, Sonia Regina Jurado. This is an open access article distributed under the Creative
Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original
work is properly cited.
ABSTRACT
We studied 20 women with m ea n ag e 5 7.7 years,
being 9 w ith unilateral quadra ntectomy surger y,
1 with surgery type bilateral quadrantectomy
and 10 with unilateral mastectomy surgery. The
average operative time was 9.8 (nine years and
eight months). We studied using surface elec-
tromyography the mean deltoid, upper trape-
zius and latissimus dorsi muscles in order to
check the action potentials of these muscles
when performing a sequence of movements of
these joints. It was used for the study, an Ac-
quisition Data System ADS1000 containing 12
channels. The electromyography (EMG) results
expressed in RMS (Root Mean Square) were
analyzed and compared between the surgical
and nonsurgical side, among the three repeti-
tions of the sequence of movements and be-
tween mastectomy and quadrantectom y for e ac h
muscle. For statistical analysis we used analy-
sis of variance (ANOVA) with a double repetition
factor (p < 0.05) for the EMG results. The results
showed a significant difference (p < 0.05) between
the surgical and non-surgical sides to the mus-
cles studied. There was no significant differ-
ence betw een the three repetitions of sequential
movement s in electromyographic analy sis to the
muscles studied. There was no significant dif-
ference between the types of surgery (mastec-
tomy and quadrantectomy) for the muscles stu-
died.
Keywords: Electromyography; Skeletal Muscle;
Breast Surgery; Quadrantectomy; Mastectomy
1. INTRODUCTION
The breasts are glands and their main function is to
produce milk. They are composed of lobes that divide
into smaller portions; the lobules and ducts that carry
milk produced outwards through the nipple. Like all
other organs of the human body, they are also found in
breast blood vessels that supply blood to the breast, and
lymphatic vessels through which lymph flows. Lymph
is a clear liquid that has a function similar to the blood
to carry nutrients to various parts of the body and col-
lect undesirable substances. The lymphatic vessels are
grouped in what is called lymph nodes, or swollen
lymph nodes. The lymphatic vessels drain into the breast
glands in the armpits (lower arms) in the neck and chest
[1].
Breast cancer occurs when cells of the body begin to
divide and reproduce very quickly and haphazardly.
Most breast cancer affects the cells of the ducts of the
breasts. Therefore, the most common breast cancer is
called ductal carcinoma. It can be in situ, when there is
nothing of the first cell layers of duct or attacker, when
invading the surrounding tissue. Cancers that begin in the
breast lobules are called lobular carcinoma and are less
common than the first. This type of cancer most often
affects both breasts. Carcinoma Inflammatory breast
cancer is rarer and usually presents itself aggressively,
compromising the entire breast, leaving it red, swollen
and hot [1].
As a result of breast cancer treatment, several compli-
cations have been reported, among them, including those
resulted from surgery. The surgical techniques can be
Copyright © 2013 SciRes. OPEN A CCESS
A. D. P. Bankoff, S. R. Jurado / Health 5 (2013) 1866-1871 1867
used for the mastectomy or conservative surgery, which
may be associated with axillary lymphadenectomy (AL)
or sentinel lymph node biopsy [2]. Among the surgical
complications of AL, it is the long thoracic nerve injury [3].
Most injuries of this nerve are partial and transient (neu-
ropraxia), which gradually recover with conservative
treatment [2]. However, when this regression does not
occur in the first six months, the lesion can be considered
complete, with few chances of rehabilitation [4].
The long thoracic nerve injury results in decreased
strength or paralysis of the serratus anterior muscle,
leading to destabilization of the shoulder girdle on the
prominence of the medial border of the scapu la and infe-
rior angle of rotation of the middle line, featuring a
winged scapula [5]. In addition to the specific lesion of
the long thoracic nerve, muscle changes are also seen as
morbidity related to the muscles in the sho ulder joint and
scapular stabilization and, we can cite, in addition to the
serratus anterior muscle, others such as the upper trape-
zius and deltoid medium [6].
After the AL in the treatment of breast cancer, the
prevalence of scapular winging has varied 1.5% - 12.6%
[7] and the incidence of 8% to 30% [8]. In a cross-sec-
tional study conducted in Rio de Janeiro, the prevalence
of 6.3% in women with seven to 287 months elapsed
after the AL was observed. In an incidence study with
599 women who underwent AL, we observed the pres-
ence of winged scapula in 69.5% of patients evaluated in
the immediate postoperative period [9].
The efficacy of physiotherapists, as well as the recov-
ery of normal movement in cases of neuropraxia may be
accompanied by physical examination. However, it is
believed that the use of objective methods such as sur-
face electromyography, for example, will provide more
reliable results on the evolution of the clinical status of
patients [10]. The EMG is defined as a non-invasive ex-
perimental technique, which consists of the development,
registration and analysis of myoelectric signals [11]. The
myoelectric activity through the electromyographic sig-
nal, based on the action potential of the plasma mem-
brane of muscle fibers, results from the process of de-
polarization and repolarization [4]. The root mean square
electromyographic signal (RMS) is one of the parameters
used to measure muscle electrical activity and indicates
changes in firing frequency and range of muscle activity,
so that the higher the value—and, consequently, the
range is greater—the greater the muscle electrical activ-
ity [12].
Decreased Range of Shoulder Motion
Range of motion (ROM) is the complete movement
possible of a segment being maintained by periodic
mov eme n t o f the me mbe r [ 1 3]. S ome fa ct o rs may le ad to
impairment of ROM. Among them we emphasize the
surgical aggression and inactivity or immobilization of
the limb. In case of realization of the radical mastectomy,
the pectoralis major and minor are removed, resulting in
a decrease in strength and upper limb function involved.
The same occurs when the nerve of Bell is temporarily
traumatized during axillary dissection, resulting in weak-
ness of the serratus anterior muscle, disrupting the move-
ment of the scapula and shoulder abduction on the af-
fected side [14,15]. Re-education of upper limb girdle
is a basic need in the patient undergoing surgery for
breast cancer, whatever the surgical technique is. Its
main objective is to restore limb functio n as soon as pos-
sible [16].
2. MATERIALS AND METHODS
We studied the middle deltoid, upper trapezius and
latissimus dorsi by surface electromyography in order to
check the action potentials of these muscles in women
affected by breast surgeries types unilateral mastectomy
and quadrantectomy
3. POPULATION
We studied 20 women with a mean age 57.7 years;
being 9 with unilateral quadrantectomy surgery, 1 with
bilateral quadrantectomy surgery and 10 with unilateral
radical mastectomy surgery. The average operative time
was 9.8 (nine years and eight months). The electromy-
ographic study was conducted with women who under-
went this surgery in a period longer than six months of
surgeries and that performed all sessions of physical
therapy after the surgery recommended by the physician
and the SUS after surgery being a total of 12 sessions.
4. Method
4.1. Instruments
It was used in the study, a data acquisition system
ADS1000 12-channel of analog input for simple signs,
50 × gain, 1 - 1000 Hz band (1), 12 differential analog
input channels, gains 1×, 100×, 300× and 600× select-
able in factory, 0 - 1000 Hz band (2), high-pass filter
with cutoff frequencies selectable in software options: 1
Hz, 2 Hz, 5 Hz, 10 Hz, 20 Hz, 50 Hz or without filter;
Low Pass Filter with upper cutoff frequencies selectable
software for the options: 100 Hz, 200 Hz, 300 Hz, 500
Hz, 1000 Hz or without filter; Filters “Notch” operated
by software in the options: 60 Hz, 120 Hz, 180 Hz and
240 Hz and 2 optically isolated digital inputs, 2 digital
outputs optically isolated acquired by FAPESP Process
No. 2010/08923-2.
4.2. Procedures and Data Acquisition
All research subjects; dressed on ly a brassiere, in itially,
Copyright © 2013 SciRes. OPEN A CCESS
A. D. P. Bankoff, S. R. Jurado / Health 5 (2013) 1866-1871
1868
it was performed the posterior superior asepsis of the
thorax and upper arm, thus preparing the sites for elec-
trode placement, avoiding any interference in the acqui-
sition of electromyographic signals.
Surface electrodes with electric-conductive gel were
fixed on the skin in the respectiv e muscles. For the latis-
simus dorsi muscle in the lower back and side of the
chest, deltoid medium in the ventral portion of the upper
trapezius. We analyzed the muscle action potentials bi-
laterally, regardless of the side where the surgery took
place (right or left). Each research subject underwent 3
proposed sequences of moves.
The study was conducted at the Laboratory of Elec-
tromyography and Biomechanics of Posture, School of
Physical Education—Unicamp. For each procedure be-
fore starting data acquisition, the subject was asked three
times to conduct the activities of sequential movements
of the shoulder joint, thus avoiding some sort of error
during execution.
All subjects in the study signed an informed consent
for participation in the research. The project was ap-
proved by the Ethics Committee of Unicamp under No.
984/2010.
5. MOVEMENTS REVIEWED
Hyper-flexion and extension of the arm, arm abduc-
tion and adduction, extension and flexion of the arm
horizontal, internal and external rotation of the arm, lift-
ing and lowering the shoulder.
6. RESULTS
In our work we studied the electrical potential of mus-
cle cells in skeletal muscles acting on the shoulder joint
of women who underwent breast surgeries due to breast
cancer. When women perform these types of surgeries
(mastectomy and quandrantectomia) are removed com-
pletely or partially muscles around th e shoulder joint, for
example muscles pectoralis major and minor and other
muscles. Then, using electromyography to measure the
action potentials of the latissimus dorsi, upper trapezius
and middle deltoid in women who have these types of
surgeries. What is electromyography? When we speak of
electromyography signals, we talk about “Generation of
Action Potential”. Therefore, an action potential is an
electrical control type all or nothing produced by the cell
in response to the impulse received. The signals are
action potentials generated b y an electric control between
neurons and muscle fibers. This means both neurons as
muscle fibers can generate action potentials, in other
words, the impulses received by the neuron, which are
the basis for the generation of the action potential. In this
sense, it is much easier to understand the relationsh ip be-
tween the action potential and electromy ography signals.
The trapezius muscle shown in Figure 1 had the low-
est average RMS values of EMG signals on the type of
mastectomy surgery, although the figures presented by
the type quadrantectomy hand surgery were not as im-
pressive. When we look at this graph the surgical side
considering both types of surgery, we found that the val-
ues are lower. With the results, it is quite evident that
both types of surgery compromise the kinesiology of the
trapezius muscle in relation to the joints studied. One of
the complaints of women is the difficulty of raising the
shoulder of the hand surgery to perform daily tasks and
also complain that the non-surgical side does not offer
force necessary to accomplish necessary task on a daily
basis.
Figure 2 shows the results of latissimus dorsi muscle.
One can check, on th e latter, that the lowest RMS values
through the acquisition of electromyography signals are
30
25
20
15
10
5
0
ANOVA-Analysis of Varian ce
N
SM SM NSQ SQ NS S
Avera
g
e 26.8 18.96 29.7 24.23 27.85 21.3
Variance 11.75 2.03 18.46 16.32 19.24 14.31
Figure 1. Income statement in RMS (Root Mean Square) on
the electromyography evaluation in women mastectomized and
quadrantectomized on the Trapezius muscle. Non-Surgical Mas-
tectomy (NSM), Sur gical Maste ctomy (SM), Non-Sur gical Qua-
drantectomy (NSQ), Surgical Quadrantectomy (SQ), Non-Sur-
gical (NS) and Surgical (S).
60
50
40
30
20
10
0
ANOVA- A nalys is of Var ia nce
N
SM SM NSQ SQ NS S
Avera
g
e 55.66 37.43 55.43 41.53 55.48 36.81
Variance 13.26 18.32 28.18 17.01 34.99 17.1
Figure 2. Income statement in RMS (Root Mean Square) for
electromyography evaluation in women mastectomized and
quadrantectomized on the latissimus dorsi muscle. Non-Surgi-
cal Mastectomy (NSM), Surgical Mastectomy (SM), Non-Sur-
gical Quadrantectomy (NSQ), Surgical Quadrantectomy (SQ),
Non-Surgical (NS)and Surgical (S).
Copyright © 2013 SciRes. OPEN A CCESS
A. D. P. Bankoff, S. R. Jurado / Health 5 (2013) 1866-1871 1869
scored on the type of surgery and hand surgery Mastec-
tomy both types of surgery. The results presented aimed
to be a muscle that suffer the consequences in their kine-
siology types of breast surgeries. It seemed to us to be
more engaged in radical mastectomy surgery, but in the
quadrantectomy surgery was also weakened in relation to
the achievement of the sequence of movements for the
shoulder joint. In the adduction movement women dem-
onstrated great difficulty in approaching the body side
arm with surgery. It is the primary motor adduction, ex-
tension and hyperextension of the shoulder joint, helping
also in the horizontal extens ion and internal rotation . It is
a muscle that works in many movements of the shoulder
joint and also interferes with the body posture tak ing into
account its origin from the ilium, through the lumbar,
thoracic, and its insertion to the humerus at the back. As
a result, it may change the biomechanical relationship
between shoulder and pelvis, causing misalignment be-
tween the sacrum and the ilium bones bilaterally, asym-
metrically tilting the pelvis, or pulling your shoulders
down causing drooping shoulders. For women with mas-
tectomy and quadrantectomy surgery the inability can
cause postural problems [17].
Figure 3 shows the results of the Middle Deltoid mus-
cle, which showed low values in RMS through the ac-
quisition of electromyography signals. Considering its
kinesiology as a whole performs the abduction of the arm,
specifically the middle portion. Part clavicular and ac-
romial portions of adjacent flex the arm, the spinal and
adjacent parts of the acromial portions extend arm. The
ventral portion rotates the arm medially and laterally
dorsal portio n.
Considering the kinesics trapezius muscle rotates the
scapula, raising the acromial extremity in abduction and
full flexion of the arm. The top acting alone elevates the
40
30
20
10
0
ANOVA-Ana lysis of Variance
N
SM SM NSQ SQ NS S
Avera
g
e 36.23 27.73 38.16 30.2 35.86 29.76
Variance 31.08 7.16 16.83 2.00 28.49 11.91
Figure 3. St atement of the results in RMS (Root Mean Square)
on the electromyography evaluation in women mastectomized
and quadrantectomized on the Middle Deltoid muscle. Non-
Surgical Mastectomy (NSM), Surgical Mastectomy (SM), Non-
Surgical Quadrantectomy (NSQ), Surgical Quadrantectomy (SQ),
Non-Surgical (NS)and Surgical (S).
scapula cranially, elevating the shoulder, then it has an
important participation from the shoulder joint. It is im-
portant to note that when all portions of the trapezius
contract simultaneously, they act more on the upper por-
tion than on the lower por tion of the scapu la. It should be
noted the effect of posture, the action of the trapezius
muscle. When the shoulder is the most high, or when a
weight is supported on the shoulders, with the individual
standing, the second portion is contracted vigorously and,
third, little or nothing [17].
One of the difficulties of women with breast surgeries
types of mastectomy and quadrantectomy is the realize-
tion of abduction movement of the arm because the mus-
cles that control the movements of the shoulder joint to
be affected by surgery. It showed electromyographic
signal after 45 degrees of abduction of the arm, stopping
soon after, because most could not reach the 90 degrees
of amplitude. If we look in depth at Figure 3 we see that
the values shown for the mastectomy surgery side, quad-
rantectomy surgery side and surgical side with both types
of surgery, the difference found between the values is
very small. This leads us to believe that the middle del-
toid muscle kinesiology suffer consequences with both
types of surg ery.
7. STATISTICAL RESULTS ABSTRACT
For statistical analysis we used analysis of variance
(ANOVA) with a double repetition factor (p < 0.05) for
the EMG results. The results showed significant differ-
ence (p < 0.05) between the surgical and nonsurgical
sides for all muscles studied. There was no significant
variation between the three sets of repetitions for all
muscles studied. There was no significant difference be-
tween the types of surgery (mastectomy and quadran-
tectomy) for the trapezius, latissimus dorsi and Middle
Deltoid.
8. DISCUSSION
When I discussed the project and drafted the literature
impressing me, the placements of some authors say that
the recovery was long overdue. The long thoracic nerve i n-
jury results in decreased strength or paralysis of the ser-
ratus anterior muscle, leading to destabilization of the
shoulder girdle on the prominence of the medial border
of the scapula and inferior angle of rotation of the middle
line, featuring a winged scapula [5]. [6] describes that in
addition to the specific lesion of the long thoracic nerve,
muscle changes are also seen as morbidity related to the
muscles in the shoulder joint and scapular stabilization
and can cite, in addition to the serratus anterior muscle,
others such as the upper trapeziu s and middle deltoid [4 ].
Reports that when this regression does not occur in the
first six months, the lesion can be considered complete,
Copyright © 2013 SciRes. OPEN A CCESS
A. D. P. Bankoff, S. R. Jurado / Health 5 (2013) 1866-1871
1870
with few chances of rehabilitation.
Considering the kinesiology of the muscles studied in
relation to the shoulder joint and acromioclavicular
which act in many of the movements of these joints, it
was evident that the types of mastectomy and quadran-
tectomy surgeries impair the quality of surgical hand
movements specifically, however, the non-surgical side
also suffers from some kind of commitment in the per-
formance of movements and also in relation to body
posture due to overload [1,18].
In our results electromyographic and Middle Deltoid
muscle Trapezius had lower RMS values representing
the action potentials of muscles in the sequence of move-
ments performed, specifically the surgical side confirm-
ing the findings of [6]. An observation, however, not
assessed by this project is that these types of surgeries
and more the problem of the disease also affect the next
non-surgical, body posture, body balance, muscle stre ng th
and more emotional, mainly because they feel fear and
pain on movement. They complain much of the limita-
tions on range of motion of these joints, especially for
performing everyday tasks.
9. CONCLUSIONS
Based on the results we believe we can draw the fol-
lowing conclusions regarding the three parts of our ex-
perimental work:
There was a sign ifican t d iffere nce be tween su rgic al an d
nonsurgical sides (p < 0.05) for the muscles studied;
There was no significant difference between the three
replicates during analysis of electromyography to the
muscles studied;
There was no significant difference between the types
of surgery (mastectomy and quadrantectomy) (p <
0.05) for the muscles studied.
REFERENCES
[1] Bankoff, A.D.P. (2012) Electromyographic study of
shoulder and acromioclavicular joint muscles in women
who underwent unilateral breast surgery of the types
mastectomy and quadrantectomy. Sport Inspiring a Lear-
ning Legacy, Routledge Online Studies, Glasgow, 2, 79-
142.
[2] Langer, I., Guller, U., Berclaz, G., Koechli, O.R., Schaer,
G., Fehr, M.K., et al. (2007) Morbidity of sentinel lymph
node biopsy (SLN) alone versus SLN and completion
axillary lymph node dissection after breast cancer surgery:
A prospective Swiss multicenter study on 659 patients.
Annals of Surgery, 245, 452-461.
http://dx.doi.org/10.1097/01.sla.0000245472.47748.ec
[3] Freitas Júnior, R., Ribeiro, L.F.J., Taia, L., Kajita, D., Fer-
nandes, M.V. and Quiroz, G.S. (2001) Linfedema em pa-
cientes submetidas à mastectomia radical modificada. Re-
vista Brasileira de Ginecologia e Obstetrícia, 23, 205-
208.
http://dx.doi.org/10.1590/S0100-72032001000400002
[4] Campbell, W.W. (2008) Evaluation and management of
peripheral nerve injury. Clinical Neurophysiology, 11 9,
1951-1965. http://dx.doi.org/10.1016/j.clinph.200 8.03.018
[5] Schmitz, C., Sodian, R., Witt, T.N., Juchem, G., Lang, N.,
Bruegger, C., et al. (2009) Winged scapula after aortic
valve replacement. The Annals of Thoracic Surgery, 87,
1277-1279.
http://dx.doi.org/10.1016/j.athoracsur.2008.08.050
[6] Shamley, D.R., Srinanaganathan, R., Weatherall, R., Osk-
rochi, R., Watson, M., Ostlere, S., et al. (2007) Changes
in shoulder muscle size and activity following treatment
for breast cancer. Breast Cancer Research and Treatment,
106, 19-27. http://dx.doi.org/10.1007/s10549-006-9466-7
[7] Sahin, F., Yilmaz, F., Esit, N., Aysal, F. and Kuran, B.
(2007) Compressive neurophaty of long thoracic nerve
and accessory nerve secondary to heavy load bearing. A
case report. Europa Medicophysica, 43, 71-74.
[8] Paim, C.R., de Paula Lima, E.D., Fu, M.R., de Paula
Lima, A. and Cassali, G.D. (2008) Post lymphadenectomy
complications and quality of life among breast cancer pa-
tients in Brazil. Cancer Nursing, 31, 302-309.
http://dx.doi.org/10.1097/01.NCC.0000305747.49205.b1
[9] Bergmann, A., Mattos, I.E., Koifman, R.J., Ribeiro, M.J.
P., Nogueira, E.A., Oliveira, A.C.G., et al. (2005) In-
cidência de complicações no pós-operatório imediato:
Análise descritiva de 599 mulheres submetidas a linfad-
enectomia axilar no câncer de mama. Congresso Bra-
sileiro de Mastologia, Rio de Janeiro, 146-329.
[10] Wolf, S.L., Butler, A.J., Alberts, J.L. and Kim, M.W. (2005)
Contemporary linkage s between EMG, kinetics and str oke
rehabilitation. Journal of Electromyography & Kinesiol-
ogy, 15, 229-239.
http://dx.doi.org/10.1016/j.jelekin.2005.01.002
[11] Hermens, H.J., Freriks, B., Disselhorst-Klug, C. and Rau,
G. (2000) Development of recommendations for SEMG
sensors and sensor placement procedures. Journal of Elec -
tromyography & Kinesiology, 10, 361-374.
http://dx.doi.org/10.1016/S1050-6411(00)00027-4
[12] Goodman, B.E. (2008) Channels active in the excitability
of nerves and skeletal muscles across the neuromuscular
junction: Basic function and pathophysiology. Advances
in Physiology Education, 32, 127-135.
http://dx.doi.org/10.1152/advan.00091.2007
[13] Kisner, C. and Colby, L.A. (1998) Exercícios terapêuticos:
Fundamentos e técnicas. Manole, São Paulo, 56-95.
[14] Box, R.C., Reul-Hirche, H.M., Bullock-Saxton, J.E. and
Furnival, C.M. (2002) Physiotherapy after breast cancer
surgery: Results of a randomized controlled study to mi-
nimiselymphoedema. Breast Cancer Research and Treat-
ment, 75, 51-64.
http://dx.doi.org/10.1023/A:1016591121762
[15] Camargo, M.C. and Marx, A.G. (2000) Reabilitação física
no câncer de mama. Editora Roca, São Paulo, 79-93.
[16] Nagel, P.H., Bruggink, E.D., Wobbes, T. and Strobbe, L.J.
(2003) Arm morbidity after complete axillary lymph node
dissection for breast cancer. Acta Chirurgica Belgica, 103,
Copyright © 2013 SciRes. OPEN A CCESS
A. D. P. Bankoff, S. R. Jurado / Health 5 (2013) 1866-1871
Copyright © 2013 SciRes. OPEN ACCESS
1871
212-216.
[17] Bankoff, A.D.P. (2007) Morfologia e cinesiologia apli-
cada ao movimento humano. Editora Guanabara Koogan,
Rio de Janeiro, 143-157.
[18] Seghers, J. and Spaepen, A. (2004) Muscle fatigue of the
elbow flexor muscles during two intermittent exercise
protocols with equal mean muscle loading. Clinical Bio-
mechanics, 19, 24-30.
http://dx.doi.org/10.1016/j.clinbiomech.2003.08.003