Oncological Safety, Surgical Outcome, and Patient Satisfaction of Oncoplastic Breast-Conserving Surgery With Contralateral Balancing Reduction Mammoplasty

Abstract

Introduction:

Oncoplastic breast-conserving surgery (OBCS) is considered a cornerstone in the management of locally invasive breast cancer. We evaluated patient-reported outcomes of OBCS with contralateral balancing breast reduction mammoplasty and reviewed its oncologic outcomes and complications.

Methods:

This is mixed method study design using retrospective chart review and prospective cohort study. Patient demographics were reviewed. Outcome measures included clinicopathologic characteristics, complications, margin status, local recurrence, tumor histopathologies, duration of follow-up, patient satisfaction, self-esteem, event-related stress, and quality of life.

Results:

A total of 48 patients were included in this study. Complete excision with negative margins was obtained in 42 (87.5%) patients, positive margins in 6 (12.5%) patients, all who had re-excision with repeat lumpectomy. Thirteen patients developed minor complications, defined as being managed as an outpatient. No patients developed major complications requiring inpatient admission. These complications did not delay commencement of chemotherapy or radiotherapy. Postsurgery BREAST-Q^TM26 scores demonstrated no statistical difference in satisfaction with breasts, nipples, and sexual well-being. There was high satisfaction with overall outcome with average score of 80.8%. For the Rosenberg self-esteem scale, the results were similar for 3- and 12-month post-operative indicating maintenance of normal self-esteem post-operatively. The Impact of Events Scale showed statistically significant difference at 12-month post-operative (25.1) when compared with preoperative scores indicating that patients had lower event-related stress. There was no significant change in Hospital Anxiety and Depression Scale.

Conclusion:

Our study has shown that the patient who undergo OBCS have high patient-reported outcomes with acceptable oncologic outcomes and complication rates.

Introduction

Breast reconstruction and the preservation of breast appearance post breast cancer treatment correlates with better psychosocial outcomes. ^{1 -4} Breast-conserving therapy (BCT), which includes wide local excision of the tumor (or lumpectomy) followed by irradiation, has become a standard of care in the management of early-stage invasive breast cancer. ^4,5 An important secondary goal is a satisfactory cosmetic outcome as this is associated with both patient satisfaction and improved quality of life. ^6,7 Multiple long-term randomized controlled trials have shown survival following BCT to be equivalent to that of mastectomy. ^{8 -11} Although the standard lumpectomy using breast-conserving techniques may result in very minor asymmetry, they can also result in large defects that leave the breast distorted. Current literature reports incidence of unfavorable aesthetic results following BCT to affect up to 40% of patients and has shown to affect patients’ psychosocial and quality of life. ^4,5,12,13 Oncoplastic breast conservation surgery (OBCS) is a type of BCT, which involves combining the latest plastic surgery techniques with breast surgical oncology. When a large lumpectomy is required, the remaining tissue is sculpted to realign the nipple and areola and restore a natural appearance to the breast shape. The contralateral breast is also modified to create symmetry. ^{14 -16} There are 3 ways this can be achieved, through simple reduction, rearrangement of internal breast parenchymal tissue or replacing by using local or distant flap to reconstruct the defect. Studies in Europe and Asian countries have demonstrated many benefits to immediate oncoplastic reconstruction including single surgery, surgery completion prior to radiation, which decreases the risk of wound healing problems, immediate symmetry of breast after lumpectomy, and relief of symptoms of macromastia. ^{6,17 -24} Despite these benefits there are limited data on outcomes of oncoplastic reconstruction in North America. ^4,25 The goal of our study was to review patient-reported outcomes of OBCS with contralateral balancing breast reduction mammoplasty, complications, oncologic outcomes, and patient satisfaction.

Methods

This was a mixed method study using retrospective chart review and a prospective cohort study. The study population involved patients 18 years of age or older, who underwent OBCS and contralateral balancing breast reduction mammoplasty with a multidisciplinary approach at the Ottawa Hospital during the period of September 2014 to December 2017. Data collection included retrospective chart review from September 2015 to October 2016. Patients were recruited onward and data and outcome measures were collected prospectively. Approval from the Ottawa Health Science Network Research Ethics Board was obtained.

Patient demographics included age, body mass index (BMI), course of disease, past medical history, type of procedure, and reduction technique. Outcome measures included clinicopathologic characteristics, complications, margin status, local recurrence, tumor histopathologies, duration of follow-up, patient satisfaction, self-esteem, event-related stress, and quality of life.

Patient-reported outcomes and satisfaction were collected using questionnaires, which were given preoperatively, then at 3-month and 12-month post-operatively. The questionnaires included BREAST-Q^TM, ²⁶ Rosenburg Self-Esteem Scale, ²⁷ Impact of Events Scale (IES), ²⁸ and Hospital Anxiety and Depression Scale (HADS). ²⁹

A total scale score of BREAST-Q^TM was calculated through the QScore software, ranging from 0 to 100, with a higher score meaning better quality of life or higher satisfaction. Rosenburg Self-Esteem Scale was measured using a 10-item scale that measures global self-worth by measuring both positive and negative feelings about the self. All items are answered using a 4-point Likert scale format ranging from strongly agree to strongly disagree, a score less than 15 may indicate problematic low self-esteem. The IES is rated on a 5-point scale ranging from 0 (“not at all”) to 4 (“often”). The IES scale consists of 15 items, 7 of which measure intrusive symptoms (intrusive thoughts, nightmares, intrusive feelings, and imagery), 8 avoidance symptoms (numbing of responsiveness, avoidance of feelings, situations, ideas), and combined, provide a total subjective stress score. The scale is intended to be helpful in detecting the effect of the most severe impact events, and those that can leave patients having post-traumatic stress disorder. Cutoff point of above 26 is considered moderate or severe impact. The HADS is a 14-item scale, 7 of the items relate to anxiety and 7 relate to depression. Each item on the questionnaire is scored from 0 to 3 and this means that a person can score between 0 and 21 for either anxiety or depression.

Statistical Analysis

We characterized the sample using descriptive statistics. Outcome measures at 3 different time points (preoperative, 3 months post-operative and 12 months post-operative) were compared using 1-way analysis of variance with repeated measures and paired sample t test for 2 different time points (3-month and 12-month post-operative). Significance level was set at P < .05. Data were expressed as mean and standard deviation for the entire sample.

Results

During October 2014 to December 2017, a total of 48 patients underwent OBCS and contralateral balancing reduction mammoplasty. The mean age was 56 (range, 36-83years), with a BMI 29.11 kg/m ² (range, 19.6-42.3 kg/m ² ), over a mean follow-up of 72.5 weeks (range, 1-260 weeks; Table 1). Complete excision with negative margins was obtained in 42 (87.5%) patients, positive margins in 6 (12.5%) patients, all who had re-excision with repeat lumpectomy. No patients had local recurrence. The most common tumor histopathologies were invasive ductal carcinoma 28 (58.3%), followed by ductal carcinoma in situ (DCIS) 8 (16.6%), and invasive lobular carcinoma 6 (12.5%).

Table 1.

Demographic and Clinical Characteristics.

Variables	No. of patients (%)
Patients	48 (100)
Age, year
Mean	56
Range	36-83
BMI, kg/m 2
Average	29.11
Range	19.6-42.3
Margin status
Positive	6 (12.5)
Negative	42 (87.5)
Smokers	5 (10.41)
Comorbidities
Hypertension	10 (20.83)
Asthma	3 (6.28)
Thyroid disease (hypo/hyperthyroidism,  goiter)	6 (12.50)
Hypercholesterolemia	5 (10.41)
Obesity	15 (31.25)
Diabetes mellitus	2 (4.16)
Stage
I	3 (6.28)
II	17 (35.4)
III	18 (37.5)
IV	2 (4.16)
I and II	1 (2.08)
II and III	1 (2.08)
NA	4 (8.33)
Tumor histopathologies
Invasive ductal carcinoma	28 (58.33)
DCIS	8 (16.66)
Invasive lobular carcinoma	6 (12.50)
Invasive mammary carcinoma	3 (6.25)
Benign phyllodes tumor	1 (2.08)
Intraductal papilloma	1 (2.08)
Pleomorphic LCIS	1 (2.08)
Local recurrence	0
Lumpectomy size—documented	27 (56.25)
Mean	426 g
Range	50-1090 g
Lumpectomy size—NA	21 (43.75)
Reduction size
Mean	472 g
Range	50.7-1500 g

Abbreviations: BMI, body mass index; DCIS, ductal carcinoma in situ; LCIS, lobular carcinoma in situ; NA, not available.

Grade II and III disease were the most common, 17 (35.4%) and 18 (37.5%), respectively. A total of 43 patients were administered adjuvant radiation, 35 patients were administered hormonal therapy and 24 patients were administered adjuvant chemotherapy (Table 2). Patients began chemotherapy mean of 49.7 days following their surgery (range, 34-72 days). Four (8.3%) patients had reported delays in commencement of chemotherapy. This was due to patient choice or uncertainty about proceeding with chemotherapy in 3 patients and only one patient had delay due to surgical complication with bilateral breast cellulitis. Patients started radiotherapy mean of 114.1 days following surgery (range, 34-231 days). Patients who received chemotherapy began their radiation generally one month following last cycle of chemotherapy. No patients had reported delay in radiation due to surgical complications. Two patients had delays in commencement of radiation due to patient choice and genetic testing.

Table 2.

Summary of Therapy.

Therapy	No. of patients
Neoadjuvant chemotherapy	8
Adjuvant chemotherapy	24
Neoadjuvant radiation	0
Adjuvant radiation	43
Hormonal therapy	35

The mean lumpectomy size weighed 426 g and reduction size weighed 472 g with largest size, respectively, weighing 1090 g and 1500 g. Figure 1 demonstrated a large lumpectomy oncoplastic reconstruction. Most common pedicles for nipple areolar complex were superior medial pedicle (35.4%) and inferior pedicle (35.4%) on oncoplastic side and superior medial pedicle on the contralateral side (68.2%).

Figure 1.

Large lumpectomy with oncoplastic reconstruction.

Thirteen patients developed minor complications, defined as being managed as an outpatient. No patients developed major complications requiring inpatient admission. Of the minor complications, 7 (14.5%) were wound infections treated with outpatient antibiotics. Some of these were diagnosed by ED physician or family physician and a smaller number were diagnosed by primary surgeon. Five (10.4%) patients developed seroma that was aspirated as outpatient, and 6 (12.5%) had minor wound dehiscence that were treated with dressings and healed by secondary intention. These complications were immediate post-operative stage. Only one patient had delay in commencement of chemotherapy due to surgical complication, and no patients had delay in their radiation due to these minor complications.

Patient-reported outcomes and satisfaction questionnaires were given to 18 patients. At 3-month post-operative, 18 patients had returned their questionnaires which is a response rate of 100%. At 12-month post-operatively, 16 patients returned their questionnaires, a response rate of 83.8%. Our results for BREAST-Q^TM26 demonstrate no statistical significant difference in satisfaction with breasts, nipples, and sexual well-being (P = .522). Similarly, there was no statistically significant difference in physical well-being of the chest and psychosocial well-being (P = .117). There was high satisfaction with overall outcome with average score of 80.8%. Women also reported satisfaction with care with average scores of 82.7% for surgeon, 93.7% for medical staff, and 99.4% for office staff (Table 3). Figure 2 demonstrated preoperative and post-operative photos of a patient 6 months following completion of radiotherapy.

Table 3.

BREAST-Q Questionnaire Scores Mean (Standard Deviation).

Items	Preoperative score	Post- operative 3-month score	Post- operative 12-month score
Satisfaction with breasts	50.4 (18.4)	66.4 (25.7)	71.4 (19.4)
Satisfaction with outcome		78.4 (19.5)	80.8 (18.6)
Psychosocial well-being	70.1 (18.0)	82.2 (20.1)	76.2 (18.3)
Physical well-being: Chest	74.1 (12.2)	71.3 (15.6)	67.2 (20.8)
Sexual well-being	47.9 (28.8)	63.8 (27.9)	55.5 (27.6)a
Satisfaction with nipples		75.9 (35.2)	80.0 (23.3)
Satisfaction with information		73.1 (18.4)	73.9 (17.5)
Satisfaction with surgeon		82.9 (20.2)	82.7 (21.3)
Satisfaction with medical staff		91.5 (17.5)	93.7 (14.9)
Satisfaction with office staff		97.4 (11.1)	99.4 (2.3)

^a P < .05.

Figure 2.

Oncoplastic reconstruction with contralateral reduction mammaplasty preoperative (above) and 6 months post radiation (below).

For the Rosenberg Self-Esteem ²⁷ Scale, the results were similar for 3- and 12- months post-operative, with an average score of 25.3 and 25.4, respectively; indicating normal and maintenance of self-esteem post-operatively (P > .05; Table 4). The IES ²⁸ showed statistically significant difference at 3 and 12 months post-operative when compared with preoperative scores, preoperative (41.7) versus 3-month post-operative (27.2) and 12-month post-operative (25.1); P < .003. The results indicate that patients had lower event-related stress (Table 4). There was no statistically significant change in HADS (P > .05; Table 4).

Table 4.

Patient-Reported Outcomes.

Outcome measures	Mean (SD)
Rosenberg Self-Esteem Scale
Post-operative 3-month	25.3 (2.4)
Post-operative 12-month	25.4 (1.8)
Impact of Events Scale
Preoperative	41.7 (16.2)
Post-operative 3-month	27.2 (15.0)
Post-operative 12-month	25.1 (18.7)a
Hospital Anxiety and Depression Scale
Preoperative	27.8 (5.14)
Post-operative 3-month	30.2 (8.7)
Post-operative 12-month	29.8 (6.8)

Abbreviation: SD, standard deviation.

^a P < .05.

Discussion

Breast-conserving therapy is considered a cornerstone in the management of locally invasive breast cancer, aiming to create a breast with a natural shape and symmetry. The patient experience is crucial; key indicators such as patient satisfaction and quality of life have become important outcomes for evaluating the success of OBCS.

In our study, OBCS demonstrated oncological safety comparable to the literature, good patient satisfaction, and psychosocial outcomes post-operatively. Complete excision with negative margins was obtained in 42 (87.5%) patients, positive margins in 6 (12.5%) patients, all who had re-excision with repeat lumpectomy. Breast-conserving therapy has become a standard of care in the management of early-stage invasive breast cancer. Women in our study had lower grade disease with grade II and III disease most common, 17 (35.4%) and 18 (37.5%), respectively. Patients who undergo OBCS generally have day surgery with low rates of complications. Thirteen patients developed minor complications, defined as being managed as an outpatient. No patients developed major complications requiring inpatient admission. Patients avoid the risk of associated with prosthesis or longer recovery with autologous free flap reconstruction.

At our institute, patients are referred to radiation and medical oncology immediately following breast-conserving surgery. Patients who are candidates and elect to proceed with chemotherapy begin this followed by radiation therapy approximately one month after the completion of their chemotherapy. Patients in our study began chemotherapy mean of 49.7 days and radiotherapy a mean of 114.1 days following their surgery. Four (8.3%) patients had reported delays in commencement of chemotherapy. This was due to patient choice or uncertainty about proceeding with chemotherapy in 3 patients and only one patient had delay due to surgical complication with bilateral breast cellulitis. No patients had reported delay in radiation due to surgical complications. Two patients had delays in commencement of radiation due to patient choice and genetic testing.

Cancer Care Ontario reports that the optimal sequencing of chemotherapy and radiotherapy is unknown. ³⁰ They report that it is reasonable to start radiotherapy after the completion of chemotherapy, or concurrently if anthracycline-containing regimens are not used. ³⁰ At our institute, women begin with chemotherapy and proceed with radiation generally one month following their last cycle of chemotherapy. Cancer Care Ontario also recommends women with early stage (stage I and II) breast cancer who have undergone breast-conserving surgery should be offered post-operative breast irradiation and begin this as soon as possible following wound healing. ³⁰ They suggest it be reasonable to start breast irradiation within 12 weeks of definitive surgery, but that the safe interval between surgery and the start of radiotherapy is unknown. ³⁰ The mean time from surgery to radiation was slightly greater than 12 weeks in our study which can be explained by the sequencing of chemotherapy completion prior to initiation of radiation.

Our results for BREAST-Q^TM26 demonstrate no statistically significant difference in satisfaction with breasts, nipples, and sexual well-being. There was also no statistically significant difference in satisfaction with physical well-being of the chest and psychosocial well-being. This is not surprising as women are at the start of their cancer journey and usually undergo radiation and sometimes chemotherapy following their OBCS. There was high satisfaction with overall outcome with average score of 80.8%. Women also reported satisfaction with care with average scores of 82.7% for surgeon, 93.7% for medical staff, and 99.4% for office staff. The Rosenberg Self-Esteem ²⁷ Scores indicated maintenance and normal self-esteem at 3- and 12-month post-operatively. The IES ²⁸ showed statistically significant difference at 3 and 12 months post-operative when compared with preoperative scores. The results indicate that patients had lower event-related stress the farther they were out from surgery.

There is increasing evidence that OBCS offer patients safe and effective oncological outcomes. In a systematic review, the authors revealed overall low local recurrence, distant recurrence, positive margin rate, re-excision rate, and complication rates, thus endorsing the oncologic safety of OBCS in T1 to T2 invasive breast cancer patients. ³¹ Chakravorty et al compared the re-excision and local recurrence rates for OBCS with standard BCS and found that OBCS decreased the rates of both oncological outcomes (2.7%). ²¹ Clough et al found that oncoplastic techniques allow larger resections, and a recurrence rate of 9% was reported. ¹⁴ Kaur et al reported a re-excision rate of 16%, ³² Reitjens et al reported local recurrence rate of 3%, ²² Fitoussi et al reported a local recurrence rate of 6.8%, ³³ and Chauhan et al reported no recurrence rate when compared with standard BCS. ²⁰

Many studies have agreed that oncoplastic reconstruction has improved patient satisfaction, psychosocial well-being, and quality of life. ^5,7,13 A systematic review suggested that patients were satisfied with breast reconstruction regardless of the technique used. ¹ A study in United States reported that OBCS increased in the percentage (from 4% to 15%) between 2007 and 2014 of all breast cancer surgeries performed and accounted for more than 33% of all breast conservation surgeries. ³⁴

The first international consensus conference on standardization of OBCS was recently published in 2017. ³⁵ The experts considered OBCS safe and effective for improving aesthetic outcomes. A slim majority believed that OBCS can be used to reduce the rate of positive margins; however, there was consensus that OBCS may increase risk of complications compared to standard BCS. The experts supported the statement that OBCS procedure should be tailored to each individual patient. ³⁵

Timing of contralateral symmetrizing procedures is variable in the literature. In our study, we performed contralateral symmetrizing simultaneously with the breast reconstruction. Similarly, in one study, it was reported that they performed simultaneous contralateral reduction mastopexy in 67% of OBCS. ¹⁹

North America is behind in adopting oncoplastic breast surgery and in training its surgeons to perform breast reconstruction when compared with Europe. ^3,4,25 Canada has been slow in its clinical uptake of OBCS compared with the rest of the international community. The majority of breast cancer surgery in Ontario is performed by general surgeons in community hospitals (70%). General surgeons with no identified subspecialty perform 69% of breast cancer operations followed by subspecialty breast surgeons and surgical oncologists. A cross-sectional survey of Ontario general surgeons examined the use of oncoplastic techniques in BCS and concluded that lack of training and access to plastic surgeons were considered significant barriers to the adoption of oncoplastic techniques. ⁴

Conclusion

Our study has shown that the patient who undergo OBCS have high patient-reported outcomes with acceptable oncologic outcomes and complication rates. This is safe, well-tolerated and provides good cosmetic outcomes to be performed with contralateral balancing breast reduction mammoplasty.