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Journal of Clinical Medicine logoLink to Journal of Clinical Medicine
. 2021 Apr 1;10(7):1432. doi: 10.3390/jcm10071432

Evaluation of Late Postural Complications in Breast Cancer Patients Undergoing Breast-Conserving Therapy in Relation to the Type of Axillary Intervention-Cross-Sectional Study

Iwona Głowacka-Mrotek 1,*, Magdalena Tarkowska 2, Lukasz Leksowski 1, Tomasz Nowikiewicz 3,4, Wojciech Zegarski 3
Editors: Rossana Berardi, Maria Lina Tornesello
PMCID: PMC8036801  PMID: 33916060

Abstract

Purpose: The aim of the study was to evaluate posture in patients undergoing breast-conserving therapy (BCT) in relation to the type of surgical intervention to the axilla. Methods: The study was conducted on patients who had undergone breast-conserving surgical treatment for breast cancer 5–6 years earlier. In 54 patients, BCT+ALND (axillary lymph node dissection) was performed, while 63 patients were subjected to BCT+SLND (sentinel lymph node dissection). The control group consisted of 54 females. The study was conducted using digital postural assessment. Results: No statistically significant differences were observed with respect to the parameters between the BCT+SLNB and BCT+ALND groups (p > 0.05). However, the differences were highly significant between the CG (control group) and the studied groups (BCT+ALND, BCT+SLNB) for the following parameters: BETA angle of thoracolumbar spine inclination (p = 0.002), GAMMA angle of thoracic spine inclination (p = 0.0044), TKA (thoracic kyphosis angle) (p < 0.0001) and shoulder level inclination (p = 0.0004). The BCT+ALND patients were characterized by higher dependency of raised shoulder (p = 0.0028) and inferior angle of the scapula (p = 0.00018) on the operated side compared to BCT+SLNB patients. Conclusions: Postural imbalance occurs independent of the type of axillary intervention. Disturbances within the upper torso (abnormal position of shoulders and inferior angles of scapulae) are more pronounced in patients after ALND.

Keywords: breast-conservingtherapy, body posture, axillary lymph node dissection, sentinel lymph node dissection

1. Introduction

In oncology, efforts are made to minimize adverse sequelae while maintaining oncological radicality, and in spite of that, late complications are still observed in breast cancer patients subjected to breast-conserving therapy [1,2]. The type of surgical intervention to the axilla also plays an important role. Depending on the initial staging of the disease, sentinel lymph node biopsy (SLNB) or axillary lymph node dissection (ALND) may be performed. Randomized clinical trials and meta-analyses showed significantly higher rate of late complications in the case of ALND [3,4]. At the same time, it was established that BCT+SLNB is not free of adverse sequelae. In patients undergoing BCT+SLNB, a limited motion range of the shoulder, lymphedema and hypoesthesia are observed [5].

In the literature, there are studies evaluating posture; however, most of them refer to breast cancer patients undergoing mastectomy. Research shows that this type of intervention is associated with deepened thoracic kyphosis, flattened lumbar lordosis, unequal shoulder level on both sides, and foot deformation [6,7,8]. Other studies suggest a beneficial effect of concurrent breast reconstruction on posture [9,10]. There are only single reports on the effect of breast-conserving therapy on posture in breast cancer patients [11,12]. Previous studies have demonstrated that, when compared to patients treated with BCT approach, women who underwent mastectomy were more often observed to present the following posture abnormalities: greater trunk inclination angle, more prominent scapular and shoulder asymmetry, greater forward trunk inclination, more prominent scapular asymmetry, greater pelvic tilt angle, significant disproportion in the prominence of both inferior scapular angles. Previous research in this field has also confirmed that problems in the arm and shoulder, including lymphedema, have a significantly higher incidence after mastectomy, in comparison to BCT [13].

There is a lack of evidence regarding the effect of axillary intervention (ALND or SLND) on patient’s posture.

The aim of the study was to evaluate the long-term effect of treatment on posture in breast cancer patients receiving breast-conserving therapy depending on the type of axillary intervention.

2. Materials and Methods

2.1. Study Design

A cross-sectional study was conducted between January 2018 and March 2019 on patients who had undergone breast-conserving surgical treatment for breast cancer 5–6 years earlier, based on the acceptance of the Bioethics Committee of Collegium Medicum in Bydgoszcz (KB 8/2018). Informed consent was obtained from all individual participants included in the study. The study design was as follows: medical records were subjected to preliminary analysis against the inclusion and exclusion criteria, then the patients undergoing BCT surgery between January 2012 and December 2012 were contacted by phone in order to invite them for a voluntary and free-of-charge postural assessment. Women from the control group were recruited from local senior clubs. Study protocol was developed by researchers. The study variables such as age, disease stage, type of adjuvant treatment, disease stage, number of lymph nodes removed were collected from the patient’s medical record. During the process of qualification for adjuvant therapy, treatment was provided according to generally accepted guidelines regarding breast cancer [14,15]. Radical 3D radiotherapy was planned and administered to all patients who underwent BCT (radiotherapy with 6 MeV X-rays was applied to the entire breast with margin and adjusted to anatomical structures—a total dose of 50 Gy was administered in 25 fractions). An additional 10 Gy of radiation (boost dose) were applied to the primary tumor bed, including a 1–2 cm tissue margin.

If metastatic changes were identified in at least 4 axillary lymph nodes (or an extra capsular infiltration of metastatic changes was present—irrespective of the number of involved lymph nodes), the area treated with radiation also included lymph node regions (axilla region and medial portion of the supraclavicular region).

We decided to examine women 5 years after surgery to see the long-time effect on posture.

The inclusion criteria contained:

  • -

    informed consent for participation in the study;

  • -

    5 years since surgery.

The exclusion criteria included:

  • -

    patients with conversion to breast amputation or an extended intervention to the axilla;

  • -

    diagnosed with: neurological (Parkinson’s disease, peripheral neuropathy), musculoskeletal (inflammation, scoliosis) or rheumatoid disorders;

  • -

    with a history of trauma prior to or during the course of study;

  • -

    bilateral intervention;

  • -

    patients diagnosed with cancer metastases over the course of the study;

  • -

    undergoing breast reconstruction within the studied period;

  • -

    patients with lymphoedema of the limb on the operated side.

The physical examination was carried out according to the protocol below:

  1. Height measurement

  2. Weight measurement on clinical scales without shoes

Based on the height and weight, the body mass index (BMI) was calculated for each patient.

  • 3.
    Photogrammetric evaluation, i.e., digital evaluation of posture (DEP). The physical basis of this method is the Moire phenomenon [16]. The evaluation by the Moire method was conducted in the following manner:
    • -
      specific anthropometric points were marked on the patient’s back (cervical spinal processes, posterior superior iliac spines, inferior angles of scapulae). The patient would stay freely in an upright position, feet apart, arms resting along the waist, head pointing forward. On the screen, the patient’s back down to the intergluteal cleft was displayed, bra having been removed and underwear not pressing buttocks.
    • -
      a preview was launched, the room was darkened and the lighting was turned on. The device was placed at the appropriate height so that the center of the back was displayed at the center of the screen. The camera obtained a series of pictures. From all the photographs, the one with optimal position of the pelvis was chosen.
    • -
      the selected picture was evaluated using digital software. The measured values were collected in an Excel spreadsheet.

Photogrammetric study enables to evaluate about 60 postural parameters. For statistical analysis, the parameters describing posture in sagittal and coronary planes were used.

Sagittal plane parameters:

  • -

    ALPHA–lumbosacral spine angle

  • -

    BETA–thoracolumbar spine angle

  • -

    GAMMA–thoracic spine angle

  • -

    LLA–lumbar lordosis angle

  • -

    TKA–thoracic kyphosis angle

  • -

    TBA torso bend angle. This parameter describes anterior or posterior bend of the torso based on the analysis of the line connecting spinal processes C7 to S1. Its value is positive for posterior bend and negative for anterior bend.

Coronary plane parameters (TTA, PTA, SLA, SL, SP, VP)

  • -

    TTA–torso tilt angle. It describes lateral tilt of the torso to the left or right based on the analysis of the line connecting spinal processes C7 to S1. Its value is positive for right tilt and negative for left tilt.

  • -

    PTA–pelvic tilt angle. It refers to the position of the posterior superior iliac spines. Positive values refer to right spina above the left spina, while negative values describe the opposite situation. Its numerical value corresponds with the difference in height between both iliac spines expressed in millimeters.

  • -

    SLA–shoulder level angle. It describes left and right shoulder. Its value is expressed in degrees; positive values describe the situation when the right shoulder is above the left shoulder, while negative value denotes left shoulder being higher. The value in millimeters expresses the difference in shoulder level on both sides.

  • -

    SL–scapula level. It describes the difference in inferior angle level of the scapulae, expressed in degrees; if the left scapula is raised, the value is negative, otherwise it is positive.

  • -

    SP–scapula protrusion. It characterizes shoulder blade protrusion from the spine in millimeters.

  • -

    VP–vertebra position. It describes the displacement of spinal processes from the midline in millimeters; positive for right displacement, negative for left displacement.

2.2. Statistical Analysis

Statistical analysis was performed using PQStat statistical package, version v. 1.6.4.122 (PQStat, Poznań, Poland). Age, height, weight and difference between groups were analyzed using Kruskal–Wallis and post hoc Dunn’s tests. The advancement of the disease and type of adjuvant therapy in different groups was analyzed using the Chi-squared test. The number of removed lymph nodes and metastatic lymph nodes were analyzed using Mann–Whitney U test. The postural parameters irrespective of the operated side were analyzed using Kruskal–Wallis and post hoc Dunn’s tests. The postural parameters dependent on the operated side were compared using the Chi-squared test. The correlation between the operated side and body posture was investigated with Mental–Haenszel stratified analysis. The probability level of p < 0.05 was considered significant, while the level of p < 0.01 was assumed to be highly significant.

3. Results

3.1. Group Characteristics

A total of 472 breast-conserving surgeries were performed in the Department of Breast Cancer and Reconstructive Surgery, Oncology Center in Bydgoszcz between January 2012 and December 2012. We have made an attempt to establish contact with 472 patients (one patient remained anonymous). The inclusion criteria were met by 117 females, 54 with BCT+ALND and 63 with BCT+SLNB. The control group consisted of 54 women of similar age, who agreed to participate in the study. The studied group consisted of 117 women, 63 of whom underwent BCT+SLNB, while 54 women underwent BCT+ALND. The control group consisted of 54 individuals. Scheme describing patient exclusion from the study are shown in Figure 1.

Figure 1.

Figure 1

Study scheme describing patient exclusion from the study. BCT+SLNB: breast-conserving therapy+sentinel lymph node biopsy, BCT+ALND: breast-conserving therapy+axillary lymph node dissection.

No statistically significant differences were found between the groups with regard to body weight, height, operated side. Statistically significant differences were noted as to the staging of the disease, number of resected lymph nodes, number of the involved lymph nodes and type of adjuvant treatment.

Detailed clinical and socio-demographics data are shown in Table 1.

Table 1.

Sociodemographic and clinical data in studied group.

Variable BCT+ALND
(n = 54)
BCT+SLND
(n = 63)
CG
(n = 54)
Kruskal–Wallis Test
/Chi^2/
Mann–Whitney’s U-Test
Dunn’s PostHoc Test
Age S.D. = 60.04
Me = 61
S.D. = 60.67
Me = 62
S.D. = 59.76
Me = 62
p = 0.9877 1 vs. 2 p = 1.0000
1 vs. 3 p = 1.0000
2 vs. 3 p = 1.0000
Body weight S.D = 69.57
Me = 66
S.D. = 72.94
Me = 73
S.D. = 74.37
Me = 72
p = 0.1179 1 vs. 2 p = 0.2626
1 vs. 3 p = 0.1748
2 vs. 3 p = 1.0000
Height S.D. = 1.64
Me = 1.64
S.D. = 1.63
Me = 1.64
S.D. = 1.62
Me = 1.61
p = 0.1382 1 vs. 2 p = 1.0000
1 vs. 3 p = 0.1571
2 vs. 3 p = 0.5346
Operated side p = 0.1929
R 21 (38.89%) 33 (52.38%)
L 33 (61.11%) 30 (47.62%)
Clinical stage p = 0.0098
I A 30 (55.56%) 50 (79.35%)
II A 21 (38.89%) 13 (20.65%)
II B 3 (5.56%) 0 (0.0%)
Number
of dissected nodes
S.D. = 15.74
Me = 14.00
S.D. = 2.48
Me = 3
p < 0.0001
Number
of affected nodes
S.D. = 2.35
Me = 2
S.D. = 0.03
Me = 0
p < 0.0001
Suplementary treatment
CHTH, RTG
RTG
45(81.48%)
9 (16.67%)
61 (96.83%)
1 (3.17%)
p < 0.0001

n—number of patients, S.D.—standard deviation, Me—median, BMI—body mass index, L—left. R—right, BCT+SLNB—breast-conserving therapy+sentinel lymph node biopsy, BCT+ALND—breast-conserving therapy+axillary lymph node dissection, CG—control group, ER—estrogen receptor, PR—progesterone receptor, HER2—human epidermal growth factor receptor 2, RTH—radiotherapy, CHTH—chemotherapy, p—calculated probability value.

3.2. Analysis of Postural Parameters in Studied Groups (BCT+ALND, BCT+SLNB, CG).

The following parameters were compared: ALPHA, BETA, GAMMA, TKA, LLA, PTA (mm), SLA (mm), SP (mm). No statistically significant differences between the BCT+SLNB and BCT+ALND groups were found (p > 0.05). However, between the control and studied groups (BCT-SLND and BCT+ALND), highly statistically significant differences were observed with respect to the following parameters:

  • -

    difference in BETA between the control and BCT+SLNB group was statistically significant (p = 0.002);

  • -

    difference in GAMMA between the control and BCT+ALND group was highly statistically significant (p = 0.0044);

  • -

    difference in TKA between CG vs. BCT+ALND, and between CG vs. BCT+ALND was highly statistically significant (p < 0.0001);

  • -

    difference in SLA between CG vs. BCT+ALND, and between CG vs. BCT+ALND was highly statistically significant (p = 0.0001) (Table 2).

Table 2.

Analysis of ALPHA, BETA, GAMMA, TKA, LLA, PTA (mm), SLA (mm) and SP (mm) in studied groups (BCT+ALND, BCT+SLNB, CG).

Postural Parameters BCT+ALND
(n = 54)
BCT+SLND
(n = 63)
CG
(n = 54)
Kruskal–Wallis Test Dunn’s PostHoc Test
ALPHA S.D. = 13.22
Me = 13.25
S.D. = 11.14
Me = 12
S.D. = 12.29
Me = 12.4
p = 0.1568 1 vs. 2 p = 0.1630
1 vs. 3 p = 0.8636
2 vs. 3 p = 1.0000
BETA S.D. = 11.23
Me = 10.6
S.D. = 12.40
Me = 12.3
S.D. = 8.98
Me = 9.1
p = 0.002 1 vs. 2 p = 0.7587
1 vs. 3 p = 0.0796
2 vs. 3 p = 0.0015
GAMMA S.D. = 13.53
Me = 13.65
S.D. = 13.31
Me = 12.3
S.D. = 11.18
Me = 11.3
p = 0.0044 1 vs. 2 p = 1.0000
1 vs. 3 p = 0.0047
2 vs. 3 p = 0.0547
TKA S.D. = 151.75
Me = 154.85
S.D. = 154.29
Me = 154.8
S.D. = 159.85
Me = 160
p < 0.0001 1 vs. 2 p = 1.0000
1 vs. 3 p = 0.0001
2 vs. 3 p = 0.0001
LLA S.D. = 155.55
Me = 155.95
S.D. = 156.46
Me = 158.1
S.D. = 158.74
Me = 158
p = 0.1212 1 vs. 2 p = 0.8961
1 vs. 3 p = 0.1200
2 vs. 3 p = 0.8524
PTA S.D. = 0.99
Me = 0
S.D. = 1.59
Me = 0
S.D. = 1.09
Me = 0
p = 0.4869 1 vs. 2 p = 0.8792
1 vs. 3 p = 0.8847
2 vs. 3 p = 1.0000
SLA S.D. = 6.03
Me = 5.8
S.D. = 5.76
Me = 5.8
S.D. = 4.15
Me = 2.9
p = 0.0004 1 vs. 2 p = 1.0000
1 vs. 3 p = 0.0008
2 vs. 3 p = 0.0040
SP S.D. = 7.34
Me = 7.15
S.D. = 5.90
Me = 5.1
S.D. = 3.84
Me = 3.1
p = 0.0002 1 vs. 2 p = 0.1280
1 vs. 3 p = 0.0001
2 vs. 3 p = 0.0825

M—arithmetic mean. Me—median, BCT+SLND—breast-conserving therapy+sentinel lymph node biopsy, BCT+ALND—breast-conserving therapy+axillary lymph node dissection, CG—control group, n—number of patients, S.D.—standard deviation, Me—median, ALPHA—lumbosacral spine angle, BETA—thoracolumbar spine angle, GAMMA—thoracic spine angle, TKA—thoracic kyphosis angle, LLA—lumbar lordosis angle, PTA—pelvic tilt angle, SLA—shoulder level angle, SL—scapula level, mm—millimeters. ALPHA, BETA, GAMMA, TKA, LLA parameters are expressed in degrees, PTA, SLA, SP are expressed in millimeters, p—calculated probability value.

3.3. Analysis of Correlations between Groups (BCT+ALND, BCT+SLNB) and Parameters (TBA, TTA, PTA, SLA, SL, VP) in Relation to the Operated Side (Left or Right).

Next, the correlation between the operated side and the change in selected postural parameters (TBA, TTA, PTA, SLA, SL, VP) was evaluated. For the sake of the analysis, patients from the BCT+SLND and BCT+ALND groups were merged into one group. Then, the parameters were analyzed according to the operated side (left or right). No statistically significant differences in TBA and PTA were found (p > 0.05). However, statistically significant difference was observed for TTA (p = 0.0264). Highly statistically significant differences were observed for the following parameters: SLA (p < 0.0001), SL (p = 0.0010), and SP (p < 0.0001), indicating that those parameters depend on side of surgery (Table 3).

Table 3.

Analysis of TBA, TTA, PTA, SLA, SL and VP in studied groups; analysis of correlations between groups and parameters in relation to the operated side (left or right).

Postural Parameters L R chi^2 Test
TBA Front 30 (55.56%) 34 (53.97%) p = 0.9762
Back 23 (42.59%) 28 (44.44%)
Zero 1 (1.85%) 1 (1.59%)
TTA Left 36 (66.67%) 28 (44.44%) p = 0.0264
Right 18 (33.33%) 32 (50.79%)
Zero 0 (0.00%) 3 (4.76%)
PTA Left 18 (33.33%) 15 (23.81%) p = 0.3811
Right 4 (7.41%) 3 (4.76%)
Zero 32 (59.26%) 45 (71.43%)
SLA Left 36 (66.67%) 7 (11.11%) p < 0.0001
Right 18 (33.33%) 56 (88.89%)
Zero 0 (0.00%) 0 (0.00%)
SL Left 30 (55.56%) 16 (25.40%) p = 0.0010
Right 8 (14.81%) 26 (41.27%)
Zero 16 (29.63%) 21 (33.33%)
VP Minus 39 (72.22%) 6 (9.52%) p < 0.0001
Plus 15 (27.78%) 57 (90.48%)
Zero 0 (0.00%) 0 (0.00%)

M—arithmetic mean, Me—median, BCT+SLND—breast-conserving therapy+sentinel lymph node biopsy. BCT+ALND breast-conserving therapy +axillary lymph node dissection. L—left. R—right. CG—control group. TBA—torso bend angle. TTA—torso tilt angle. PTA—pelvic tilt angle. SLA—shoulder level angle. SL—scapula level. VP—vertebra position. TBA, TTA, PTA, SLA, SL parameters are expressed in degrees. VP parameter is expressed in millimeters. p—calculated probability value.

Postural parameters dependent on the operated side (TBA, TTA, PTA, SLA, UL, UK) were also evaluated with respect to the BCT+ALND and BCT+SLNB groups. Highly statistically significant differences in SLA (p = 0.0028) and SL (p = 0.0018) were observed depending on the operated side. The patients from the BCT+ALND group were characterized by a raised shoulder position and lowered angle of the scapula on the operated breast side compared to patients from the BCT+SLNB group (Table 4).

Table 4.

Analysis of side-dependent (left or right) parameters in BCT+ALND and BCT+SLNB groups; correlations between groups (BCT+ALND vs. BCT+SLNB).

Postural Parameters BCT+ALNB BCT+SLNB Homogeneity
L P L P
TBA Front 13 (61.95%) 17 (51.51%) 17 (53.12%) 17 (58.62%) 0.3986
Back 8 (38.05%) 16 (48.49%) 15 (46.88%) 12 (41.38%)
TTA Left 16 (76.19%) 16 (53.33%) 20 (60.61%) 12 (40.00%) 0.8121
Right 5 (23.81%) 14 (46.67%) 13 (39.39%) 18 (60.00%)
PTA Left 7 (87.50%) 8 (72.73%) 11 (78.57%) 7 (100%) 0.1229
Right 1 (12.50%) 3 (27.27%) 3 (21.43%) 0 (0%)
SLA Left 18 (85.71%) 1 (3.03%) 18 (54.55%) 6 (20.00%) 0.0028
Right 3 (14.29%) 32 (96.97%) 15 (45.45%) 24 (80.00%)
SL Left 16 (84.21%) 5 (17.86%) 14 (73.68%) 11 (78.57%) 0.0018
right 3 (15.79%) 23 (82.14%) 5 (26.32%) 3 (21.43%)
VP Minus 16 (76.19%) 1 (3.03%) 23 (69.70%) 5 (16.67%) 0.0800
Plus 5 (23.81%) 32 (96.97%) 10 (30.30%) 25 (83.33%)

M—arithmetic mean, Me—median, BCT+SLND—breast-conserving therapy+sentinel lymph node biopsy, BCT+ALND—breast-conserving therapy+axillary lymph node dissection, L—left, R—right, CG—control group, ALPHA—lumbosacral inclination angle, BETA—thoracolumbar inclination angle, GAMMA—thoracic inclination angle, TBA—torso bend angle, TTA—torso tilt angle, PTA—pelvic tilt angle, SLA—shoulder level angle, SL—scapula level, VP—vertebra position, TBA, TTA, PTA, SLA, SL, VP parameters are expressed in degrees, p—calculated probability value.

4. Discussion

In this study, we examined the relationship between postural imbalance in breast cancer patients undergoing BCT depending on type of axillary intervention (ALND vs. SLNB). Our study is the first observation study evaluating long-term effects on posture in breast cancer patients depending on type of axillary intervention. The validity of the study is raised by inclusion of control group. The increased life expectancy of women diagnosed with breast cancer suggests that many of these women may be living with the sequelae of treatment [17], which is why we decided to check the long-term effect on posture among women operated with BCT.

We examined our groups with the photogrammetric method. In our study, we used photogrammetric evaluation with Moire phenomenon. This method is based on Moire conturography observed in the optics. When a light ray falls upon an uneven surface, the light is reflected in different directions. This image is then registered by a camera and analyzed with the use of a dedicated computer program. The Moire phenomenon is a result of interaction between two periodic structures [18,19]. It has been widely used in a number of studies evaluating posture in children and adults [20,21].An important advantage of this method is that photogrammetric evaluation is a non-invasive test which can be repeated many times without putting patient’s health at risk [22,23].This technique has also been used in previous studies to evaluate the posture of women treated for breast cancer [7,8,11,12].

The main advantages of this approach are that they allow for an evaluation of the body using the same image [24,25].

The lack of statistically significant differences between the groups proves that breast surgery has a greater impact on posture compared to axillary intervention itself [17]. The study showed that BCT+SLNB is associated with a lower rate of late complications.

The analysis of the side-dependent parameters proved that patients tend to tilt towards the operated side (TTA), raise shoulder on the operated side (SLA), inferior angle of the scapula tends to be raised on the operated side, and also the maximal lateral deviation of spinal processes can be observed on the operated side (VP). Additionally, the comparison of the side-dependent parameters showed that BCT+ALND patients raised their shoulder and inferior angle of the scapula significantly more often on the operated side.

The study showed that in BCT patients, thoracic kyphosis was more advanced, as expressed by increased GAMMA and BETA angles and a decreased TKA. The differences were obvious when compared to the control group.

The reason behind deepening kyphosis is both surgery and adjuvant treatment. As a result, the patients start to lead a more sedentary lifestyle, causing weakening of torso muscles and bone deformities [26]. Abnormal curvature of the spine results in a diminished ability to transfer the load and poor amortization [27]. Other studies suggest that, in breast cancer patients, physical activity is limited and the percentage of muscle tissue is lower and it causes the body postural changes [28,29].Another reason for increased kyphosis in patients after BCT may be the fact that these patients suffered from breast tissue defect. Patients who undergo BCT do not receive breast prostheses, which may further affect the development of deformations within the spine, especially in patients with large breasts and significant tissue defects. The studies conducted by Findikcioglu et al. revealed statistically significant differences in the angles of thoracic kyphosis and lumbar lordosis observed in patients after mastectomy with breast cup A and D [30].

Another factor which could influence postural imbalance may be post-operative radiotherapy. Previous research demonstrated that patients who received radiotherapy also reported greater problems with shoulder mobility and higher incidence of lymphedema or sensory disorders [31]. These aspects may lead to the development of postural disorders, adopting involuntary posture or forward bending of the trunk [32,33]. A similar effect can occur in patients for whom radiotherapy was applied to the breast and axillary fossa. The majority of patients included in our study received radiotherapy.

Post-operative radiotherapy, as well as the presence of scar within the breast and axillary fossa, may cause the retraction of cervical muscles and spasms in the trapezium and scalene muscles. Moreover, scars left after surgical treatment or radiation therapy result in the reduction of elastic properties and fibrosis of the skin [34].

Limited physical activity and fatigue are the main causes of weakening of muscles responsible for maintaining posture [35,36].The results were significantly worse in patients after axillary lymph node resection compared to the control group with respect to the following parameters: GAMMA, TKA, SLA (in mm) and SP (in mm).

It has been found that BCT+ALND patients showed stronger association of the operated side and higher position of the shoulder and scapula compared to BCT+SLNB patients. It can be explained by the fact that physical activity in BCT+ALND patients within the upper girdle is limited compared to patients without axillary lymphadenectomy [37]. Limited motion range of the shoulder girdle affects BCT patients regardless of the type of surgical intervention. On the operated side, the upper extremity is characterized by limited movement and motion range as well as muscle weakness, which leads to biomechanical changes and asymmetry between left and right side [38,39].

In our study, a statistically significant correlation between the operated side and torso tilting was observed. The patients tended to tilt to the operated side and raise the shoulder and inferior angle of the scapula on the operated side. Raised shoulder and scapula, lateral inclination towards the operated side—those are typical symptoms of so-called “half-woman complex”. Our study confirmed that it affects not only patients after radical surgery, but those who underwentto breast-conserving therapy as well [40,41].

Postural imbalance stems from both biomechanics and psychological disturbances. BCT patients require psychological support, which can help improve posture and has been emphasized by other authors [42]. It can be concluded that non-usage of breast prosthetics filling the tissue defect negatively influences posture after breast-conserving treatment. Depending on the breast size, the difference in load can be substantial [30,43]. However, not only surgical treatment affects posture. Other authors highlight the impact of hormonal therapy on bone density [44,45,46].

An important strength of this study is the evaluation of posture in women operated on due to breast cancer, which not only includes the type of surgical intervention in the axillary fossa, but also examines the control group. In our study, all patients from the experimental group received treatment in the same facility, which ensured reliability of medical data (the stage of clinical advancement of neoplastic disease, the types of complementary therapies, the number of removed lymph nodes and the type of surgical procedure). In our study, also the control group was carefully selected.

Our study, despite being the first report evaluating the influence of axillary intervention on posture, has several limitations. Despite adequate selection of patients to each group, our research is not a prospective study; evaluating the initial posture of patients before surgical procedure could provide a valuable insight to this research. Results from our study are creating a hypothesis for a prospective study in the future. Also, other confounding factors were not included, such as level of physical activity and participation in rehabilitation programs. Another limitation of our study is the fact that we have not analyzed the relation between postural changes and post-operative radiotherapy in the axillary fossa region in the group of patients who were operated on with the BCT+SLNB approach.

Lastly, there was no comparison according to hand dominance and the postural changes.

5. Conclusions

In our study, we demonstrated a lack of any statistically significant impact of type of axillary intervention (ALND vs. SLNB) on postural imbalance in breast cancer patients subjected to breast-conserving therapy (BCT). Our study showed that body posture in BCT patients was different from that of healthy women. It was manifested by deepened thoracic kyphosis, unequal shoulder levels, scapula protrusion. The abnormalities were more pronounced in patients after axillary lymphadenectomy.

Acknowledgments

We wish to thank the patients and professional personnel in the Department of Surgical Oncology, Oncology Centre, Bydgoszcz, Poland, for their assistance in this study.

Author Contributions

Conceptualization, I.G.-M.; data curation, M.T., L.L.; formal analysis, M.T. and I.G.-M.; investigation, I.G.-M. and T.N.; methodology, I.G.-M.; project administration, I.G.-M.; resources, I.G.-M. and M.T.; software, T.N., L.L.; supervision, T.N., W.Z.; validation I.G.-M.; visualization, T.N.; writing—original draft, I.G.-M.; writing—review and editing, I.G.-M., M.T., T.N. and W.Z. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

The project was approved by the Bioethics Committee of Collegium Medicum in Bydgoszcz (KB 8/2018). All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed Consent Statement

Informed consent was obtained from all individuals/participants included in the study.

Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on responsible request.

Conflicts of Interest

The authors declare no conflict of interest.

Footnotes

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

  • 1.Del Bianco P., Zavagno G., Burelli P., Scalco G., Barutta L., Carraro P., Pietrarota P., Meneghini G., Morbin T., Tacchetti G., et al. Morbidity comparison of sentinel lymph node biopsy versus conventional axillary lymph node dissection for breast cancer patients: Results of the sentinella–GIVOM Italian randomised clinical trial. Eur. J. Surg. Oncol. (EJSO) 2008;34:508–513. doi: 10.1016/j.ejso.2007.05.017. [DOI] [PubMed] [Google Scholar]
  • 2.Kootstra J.J., Msc J.E.H.M.H.-W., Rietman J.S., De Vries J., Baas P.C., Geertzen J.H.B., Hoekstra H.J. A Longitudinal Comparison of Arm Morbidity in Stage I–II Breast Cancer Patients Treated with Sentinel Lymph Node Biopsy, Sentinel Lymph Node Biopsy Followed by Completion Lymph Node Dissection, or Axillary Lymph Node Dissection. Ann. Surg. Oncol. 2010;17:2384–2394. doi: 10.1245/s10434-010-0981-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Fleissig A., Fallowfield L.J., Langridge C.I., Johnson L., Newcombe R.G., Dixon J.M., Kissin M., Mansel R.E. Post-operative arm morbidity and quality of life. Results of the ALMANAC randomised trial comparing sentinel node biopsy with standard axillary treatment in the management of patients with early breast cancer. Breast Cancer Res. Treat. 2005;95:279–293. doi: 10.1007/s10549-005-9025-7. [DOI] [PubMed] [Google Scholar]
  • 4.Giuliano A.E., Haigh P.I., Brennan M.B., Hansen N.M., Kelley M.C., Ye W., Glass E.C., Turner R.R. Prospective Observational Study of Sentinel Lymphadenectomy Without Further Axillary Dissection in Patients With Sentinel Node–Negative Breast Cancer. J. Clin. Oncol. 2000;18:2553–2559. doi: 10.1200/JCO.2000.18.13.2553. [DOI] [PubMed] [Google Scholar]
  • 5.Kozak D., Głowacka-Mrotek I., Nowikiewicz T., Siedlecki Z., Hagner W., Sowa M., Zegarski W. Analysis of Undesirable Sequelae of Sentinel Node Surgery in Breast Cancer Patients—A Prospective Cohort Study. Pathol. Oncol. Res. 2017;24:891–897. doi: 10.1007/s12253-017-0306-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Głowacka-Mrotek I., Sowa M., Siedlecki Z., Nowikiewicz T., Hagner W., Zegarski W. Evaluation of changes to foot shape in females 5 years after mastectomy: A case–control study. Breast Cancer Res. Treat. 2017;163:287–294. doi: 10.1007/s10549-017-4183-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Malicka I., Barczyk K., Hanuszkiewicz J., Skolimowska B., Woźniewski M. Body posture of women after breast cancer treatment. Ortop. Traumatol. Rehabil. 2010;12:353–361. [PubMed] [Google Scholar]
  • 8.Bak M., Rostkowska E. The influence of using breast prosthesis during the night on the changes of body posture among woman after mastectomy. Fizjoterapia. 2000;8:11–15. [Google Scholar]
  • 9.Ciesla S., Polom K. The effect of immediate breast reconstruction with Becker-25 prosthesis on the preservation of proper body posture in patients after mastectomy. Eur. J. Surg. Oncol. (EJSO) 2010;36:625–631. doi: 10.1016/j.ejso.2010.05.005. [DOI] [PubMed] [Google Scholar]
  • 10.Peres A.C.A.M., Latorre M.D.R.D.D.O., Maesaka J.Y., Filassi J.R., Baracat E.C., Ferreira E.A.G. Body Posture After Mastectomy: Comparison Between Immediate Breast Reconstruction Versus Mastectomy Alone. Physiother. Res. Int. 2017;22:e1642. doi: 10.1002/pri.1642. [DOI] [PubMed] [Google Scholar]
  • 11.Głowacka I., Nowikiewicz T., Siedlecki Z., Hagner W., Nowacka K., Zegarski W. The Assessment of the Magnitude of Frontal Plane Postural Changes in Breast Cancer Patients After Breast-Conserving Therapy or Mastectomy—Follow-up Results 1 Year After the Surgical Procedure. Pathol. Oncol. Res. 2016;22:203–208. doi: 10.1007/s12253-015-9995-7. [DOI] [PubMed] [Google Scholar]
  • 12.Głowacka I., Nowikiewicz T., Hagner W., Nowacka K., Sowa M., Zegarski W. Sagittal Plane Postural Changes in Female Patients with Breast Cancer after Different Surgical Techniques. Breast J. 2017;23:109–111. doi: 10.1111/tbj.12697. [DOI] [PubMed] [Google Scholar]
  • 13.Nesvold I.-L., Dahl A.A., Løkkevik E., Mengshoel A.M., Fosså S.D. Arm and shoulder morbidity in breast cancer patients after breast-conserving therapy versus mastectomy. Acta Oncol. 2008;47:835–842. doi: 10.1080/02841860801961257. [DOI] [PubMed] [Google Scholar]
  • 14.Coates A.S., Winer E.P., Goldhirsch A., Gelber R.D., Gnant M., Piccart-Gebhart M., Thürlimann B., Senn H.-J., André F., Baselga J., et al. Tailoring therapies—improving the management of early breast cancer: St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2015. Ann. Oncol. 2015;26:1533–1546. doi: 10.1093/annonc/mdv221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Goldhirsch A., Wood W.C., Coates A.S., Gelber R.D., Thürlimann B., Senn H.-J., Panel Members Strategies for subtypes—dealing with the diversity of breast cancer: Highlights of the St Gallen International Expert Consensus on the Primary Therapy of Early Breast Cancer 2011. Ann. Oncol. 2011;22:1736–1747. doi: 10.1093/annonc/mdr304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Wong H.-K., Balasubramaniam P., Rajan U., Chng S.-Y. Direct spinal curvature digitization in scoliosis screening e a comparative study with Moire conturography. J. Spinal Disord. 1997;10:185–192. doi: 10.1097/00002517-199706000-00001. [DOI] [PubMed] [Google Scholar]
  • 17.Rangel J., Perez C.S., Oliveira R., Guirro E.C. Effects of Breast Cancer Treatment on Posture: A Current Review. Int. J. Phys. Ther. Rehabil. 2019;5:152. doi: 10.15344/2455-7498/2019/152. [DOI] [Google Scholar]
  • 18.Rossler T., Hrabovsky M., Pochmon M. Moiré methods for measurement of displacement andtopography. Czechoslov. J. Phys. 2006;56:101–124. doi: 10.1007/s10582-006-0073-y. [DOI] [Google Scholar]
  • 19.Wenzel K., Antal A., Molnar J., Tóth B., Tamás P. New optical equipment in 3 surfacemeasuring. J. Autom. Mob. Robot. Intell. Syst. 2009;3:29–32. [Google Scholar]
  • 20.Balla P., Manhertz G., Antal A. Diagnostic moiré image evaluation in spinal deformities. Opt. Appl. 2016;46:375–385. [Google Scholar]
  • 21.Gaál Z., Antal Á., Tamás P. Scoliosis testing features on the basis of electronically generatedmoiré patterns. Biomech. Hung. 2010;3:84–92. [Google Scholar]
  • 22.Karachalios T., Sofianos J., Roidis N., Sapkas G., Korres D., Nikolopoulos K. Ten-year follow-up evaluation of a school screening program for scoliosis. Is the forward-bending test an accurate diagnostic criterion for the screening of scoliosis? Spine. 1999;24:2318–2324. doi: 10.1097/00007632-199911150-00006. [DOI] [PubMed] [Google Scholar]
  • 23.Meadows D.M., Johnson W.O., Allen J.B. Generation of Surface Contours by Moiré Patterns. Appl. Opt. 1970;9:942–947. doi: 10.1364/AO.9.000942. [DOI] [PubMed] [Google Scholar]
  • 24.Singla D., Veqar Z. Methods of postural assessment used for sports persons. J. Clin. Diagn. Res. 2014;8:1–4. doi: 10.7860/JCDR/2014/6836.4266. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Barrett E., McCreesh K., Lewis J. Reliability and validity of non-radiographic methods of thoracic kyphosis measurement: A systematic review. Man. Ther. 2014;19:10–17. doi: 10.1016/j.math.2013.09.003. [DOI] [PubMed] [Google Scholar]
  • 26.Elme A., Utriainen M., Kellokumpu-Lehtinen P., Palva T., Luoto R., Nikander R., Huovinen R., Kautiainen H., Järvenpää S., Penttinen H.M., et al. Obesity and physical inactivity are related to impaired physical health of breast cancer survivors. Anticancer. Res. 2013;33:1595–1602. [PubMed] [Google Scholar]
  • 27.Hanuszkiewicz J., Malicka I., Barczyk-Pawelec K., Woźniewski M. Effects of selected forms of physical activity on body posture in the sagittal plane in women post breast cancer treatment. J. Back Musculoskelet. Rehabil. 2015;28:35–41. doi: 10.3233/BMR-140487. [DOI] [PubMed] [Google Scholar]
  • 28.Cantarero-Villanueva I., Fernández-Lao C., Díaz-Rodríguez L., Cuesta-Vargas A.I., Fernández-De-Las-Peñas C., Piper B.F., Arroyo-Morales M. The Piper Fatigue Scale-Revised: Translation and psychometric evaluation in Spanish-speaking breast cancer survivors. Qual. Life Res. 2014;23:271–276. doi: 10.1007/s11136-013-0434-5. [DOI] [PubMed] [Google Scholar]
  • 29.Harrington S., Padua D., Battaglini C., Michener L.A. Upper extremity strength and range of motion and their relationship to function in breast cancer survivors. Physiother. Theory Pract. 2013;29:513–520. doi: 10.3109/09593985.2012.757683. [DOI] [PubMed] [Google Scholar]
  • 30.Findikcioglu K., Findikcioglu F., Ozmen S., Guclu T. The Impact of Breast Size on the Vertebral Column: A Radiologic Study. Aesthetic Plast. Surg. 2007;31:23–27. doi: 10.1007/s00266-006-0178-5. [DOI] [PubMed] [Google Scholar]
  • 31.Sugden E., Rezvani M., Harrison J., Hughes L. Shoulder movement after the treatment of early stage breast cancer. Clin. Oncol. 1998;10:173–181. doi: 10.1016/S0936-6555(98)80063-0. [DOI] [PubMed] [Google Scholar]
  • 32.Nagel P., Bruggink E., Wobbes T., Strobbe L. Arm morbidity after complete axillary lymph node dissection for breast cancer. Acta Chir. Belg. 2003;103:212–216. doi: 10.1080/00015458.2003.11679409. [DOI] [PubMed] [Google Scholar]
  • 33.Blomquivist L., Stark B., Natacha E., Malm M. Evaluation of arm and shoulder mobility and strenght after modified radical mastectomy and radioterapy. Acta Oncol. 2004;43:280–283. doi: 10.1080/02841860410026170. [DOI] [PubMed] [Google Scholar]
  • 34.Camargo M.C., Marx A.G. Reabilitação Física no Câncer de Mama. Roca; São Paulo, Brazil: 2000. [Google Scholar]
  • 35.Lawrence D.P., Kupelnick B., Miller K., Devine D., Lau J. Evidence Report on the Occurrence, Assessment, and Treatment of Fatigue in Cancer Patients. J. Natl. Cancer Inst. Monogr. 2004;2004:40–50. doi: 10.1093/jncimonographs/lgh027. [DOI] [PubMed] [Google Scholar]
  • 36.Cantarero-Villanueva I., Fernández-Lao C., Cuesta-Vargas A.I., Del Moral-Avila R., Fernández-De-Las-Peñas C., Arroyo-Morales M. The Effectiveness of a Deep Water Aquatic Exercise Program in Cancer-Related Fatigue in Breast Cancer Survivors: A Randomized Controlled Trial. Arch. Phys. Med. Rehabil. 2013;94:221–230. doi: 10.1016/j.apmr.2012.09.008. [DOI] [PubMed] [Google Scholar]
  • 37.Hayes S.C., Johansson K., Stout N.L., Prosnitz R., Armer J.M., Gabram S., Schmitz K.H. Upper-body morbidity after breast cancer: Incidence and evidence for evaluation, prevention, and management within a prospective surveillance model of care. Cancer. 2012;118:2237–2249. doi: 10.1002/cncr.27467. [DOI] [PubMed] [Google Scholar]
  • 38.Balzarini A., Lualdi P., Lucarini C., Ferla S., Galli M., Crivellini M., DeConno F. Biomechanical evaluation of scapular girdle in patients with chronic arm lymphedema. Lymphology. 2006;39:132–140. [PubMed] [Google Scholar]
  • 39.Shamley D., Srinaganathan R., Oskrochi R., Lascurain-Aguirrebeña I., Sugden E. Three-dimensional scapulothoracic motion following treatment for breast cancer. Breast Cancer Res. Treat. 2009;118:315–322. doi: 10.1007/s10549-008-0240-x. [DOI] [PubMed] [Google Scholar]
  • 40.Shi H., Uen Y., Yen L., Culbertson R., Juan C., Hou M. Two-year quality of life after breast cancer surgery: A comparison of three surgical procedures. Eur. J. Surg. Oncol. (EJSO) 2011;37:695–702. doi: 10.1016/j.ejso.2011.05.008. [DOI] [PubMed] [Google Scholar]
  • 41.Phillips S.M., McAuley E. Associations between self-reported post-diagnosis physical activity changes, body weight changes, and psychosocial well-being in breast cancer survivors. Support Care Cancer. 2015;23:159–167. doi: 10.1007/s00520-014-2346-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Tsai H.-Y., Kuo R.N.-C., Chung K.-P. Quality of life of breast cancer survivors following breast-conserving therapy versus mastectomy: A multicenter study in Taiwan. Jpn. J. Clin. Oncol. 2017;47:909–918. doi: 10.1093/jjco/hyx099. [DOI] [PubMed] [Google Scholar]
  • 43.Hojan K., Manikowska F., Molinska-Glura M., Chen P.J.B., Jozwiak M. The impact of an external breast prosthesis on the gait parameters of women after mastectomy. Cancer Nurs. 2014;37:E30–E36. doi: 10.1097/NCC.0b013e3182919576. [DOI] [PubMed] [Google Scholar]
  • 44.Baum M., Budzar A.U., Cuzick J., Forbes J., Houghton J.H., Klijn J.G., Sahmoud T. Anastrozole alone or in combination with tamoxifen versus tamoxifen alone for adjuvanttreatment of postmenopausal women with early breast cancer: First results of the ATAC randomized trial. Lancet. 2002;359:2131–2139. doi: 10.1016/s0140-6736(02)09088-8. [DOI] [PubMed] [Google Scholar]
  • 45.Coleman R.E., Banks L.M., Girgis S.I., Kilburn L.S., Vrdoljak E., Fox J., Cawthorn S.J., Patel A., Snowdon C.F., Hall E., et al. Skeletal effects of exemestane on bone-mineral density, bone biomarkers, and fracture incidence in postmenopausal women with early breast cancer participating in the Intergroup Exemestane Study (IES): A randomised controlled study. Lancet Oncol. 2007;8:119–127. doi: 10.1016/S1470-2045(07)70003-7. [DOI] [PubMed] [Google Scholar]
  • 46.Rabaglio M., Sun Z., Price K.N., Castiglione-Gertsch M., Hawle H., Thürlimann B., Mouridsen H., Campone M., Forbes J.F., Paridaens R.J., et al. Bone fractures among postmenopausal patients with endocrine-responsive early breast cancer treated with 5 years of letrozole or tamoxifen in the BIG 1-98 trial. Ann. Oncol. 2009;20:1489–1498. doi: 10.1093/annonc/mdp033. [DOI] [PMC free article] [PubMed] [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The datasets generated and/or analyzed during the current study are available from the corresponding author on responsible request.


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