Breast Cancer DOI 10.1007/s12282-014-0570-y
ORIGINAL ARTICLE
Short-term outcomes of immediate breast reconstruction using an implant or tissue expander after mastectomy in breast cancer patients Se Won Kim • Hae Kyung Lee • Sun Mi Kang • Tae Ho Kang • Chan Seok Yoon Seung Sang Ko • Min Hee Hur • Sung Soo Kang • Chul Hwan Seul • Ja Sung Gu
•
Received: 18 April 2014 / Accepted: 23 September 2014 Ó The Japanese Breast Cancer Society 2014
Abstract Background Mastectomy is an optional surgical management of breast cancer, but it can cause significant adverse reactions. Breast reconstruction is a concern in post-mastectomy recovery. We assessed the oncologic safety and patient satisfaction following immediate breast reconstruction using an implant or tissue expander. Methods We retrospectively reviewed all patients who underwent reconstruction with an implant or tissue expander immediately after mastectomy. Seventy-seven patients underwent breast reconstruction at a general hospital breast cancer center from January 2008 to December 2010. Fourteen patients were excluded due to loss at follow-up, so 63 patients were included in this study. Questionnaires were sent to all patients to assess patient satisfaction. Results Mean age was 44.1 years (range 29–64). After a median follow-up period of 22.4 months, there was 1 case of locoregional recurrence, 1 case of distant metastasis, and an overall breast cancer-specific survival of 100 %. Overall rate of major complications, such as nipple areolar complex (NAC) necrosis and implant removal, was 11.1 % (7
patients). Of the 10 patients who had NAC necrosis, 6 patients improved after observation and 4 patients had NAC excision. Three patients had their implant removed due to severe infection, leakage, and dissatisfaction, respectively. There were 32 cases of total mastectomy (TM), 12 cases of skin-sparing mastectomy (SSM), and 19 cases of NAC-sparing mastectomy (NSM). According to the questionnaire, 84.1 % were satisfied with the general operational result and 77.8 % with the cosmetic result. Of the 31 patients who received conservative surgery, 87.1 % were satisfied with the general result and 83.9 % with the cosmetic result. Conclusions Immediate breast reconstruction using an implant after mastectomy was technically feasible and oncologically safe. In addition, the reconstruction resulted in a relatively high rate of patient satisfaction. Further long-term studies are warranted to confirm these findings. Keywords Breast cancer Mastectomy Immediate breast reconstruction Implant Tissue expander
Introduction S. W. Kim H. K. Lee (&) S. M. Kang T. H. Kang C. S. Yoon S. S. Ko M. H. Hur S. S. Kang Department of General Surgery, Catholic Kwandong University College of Medicine, Cheil General Hospital, 1-19 Mukjeong-dong, Jung-gu, Seoul 100-380, Korea e-mail: [email protected] C. H. Seul JW Plastic Surgery, Seoul, Korea J. S. Gu Department of Nursing, Graduate School of Kyung Hee University, Seoul, Korea
In breast cancer patients, the purpose of post-mastectomy breast reconstruction is to recreate a balanced, symmetrical, and natural appearance for both breasts that fulfills the patient’s expectations. The method and timing of breast reconstruction vary, and the outcome depends on the patient’s personal preferences, physical characteristics, and the oncologic safety. Recently, immediate breast reconstruction (IBR) has become an accepted procedure in breast cancer patients. The feasibility of this procedure is largely attributed to the improvement in operational skill, which involves
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conservation of the skin envelope or even the nipple–areola complex (NAC). Since Toth and Lappert introduced the skin-sparing mastectomy (SSM) in 1991 [1], IBR has improved cosmetic results [2–4]. More recently, nipple sparing mastectomy (NSM) has been proposed in select cases and provides an additional option for IBR. Because IBR has become a common practice and has proven medical and psychosocial benefits, the current goal is to produce cosmetically satisfying results that are consistent with oncologic safety requirements [5, 6]. In the present study, we studied the technical feasibility, oncologic safety, cosmetic outcome, and patient satisfaction following IBR using an implant or a tissue expander after mastectomy in Korean women with breast cancer.
Patients and methods Seventy-seven patients underwent breast reconstructions with a permanent implant or tissue expander immediately after mastectomy at Cheil General Hospital breast cancer center from January 2008 to December 2010. During the period, total 300 cases of surgery for breast cancer were performed. Total mastectomy consisted 54 % (321/600). Fourteen patients were excluded from the study because of the lack of follow-up visits; therefore, 63 patients were included in this study. The medical records of these patients were reviewed retrospectively. Mastectomies were performed by five different surgeons and all reconstructions were performed by one plastic surgeon. In principle, immediate reconstruction is recommended for early-stage breast cancer patients who need mastectomy but the final decision is made by the patient preference. In this study, some patients who clinically considered as early breast cancer, later upgraded to advanced stage by the final pathological results were included. To assess the oncologic safety of the procedure, all patients received periodic postoperative follow-up assessments such as physical examinations, breast ultrasonograms, whole body bone scans, and positron-emission tomography-computed tomography (PET-CT) scans to detect locoregional recurrence (LRR) or distant metastasis of primary cancer. The mean follow-up period was 22.4 months (range 6–45). To evaluate satisfaction, a questionnaire consisting of 9 questions was sent to all patients. Questions 1 through 5 assessed general operation satisfaction, and questions 6 through 9 assessed cosmetic satisfaction. A Likert 5-point scale was used for each question (except question 3, which used a visual analog scale that indicated patient satisfaction on a scale of 1–10), with possible answers ranging from ‘‘very satisfied’’ (1) to ‘‘very dissatisfied’’
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Table 1 The questionnaire Items on general satisfaction of surgery If you can choose again, do you want to have breast reconstruction? If you can choose again, do you choose the same type of breast reconstruction? Do you satisfied with the general result of reconstruction? Do you recommend the type of breast reconstruction that you had to your friends? Do you receive sufficient information about your reconstruction options before the operation? Items on cosmetic satisfaction of surgery Do you feel that the size and shape of your breasts are the same? Do you think that the nipple–areola complex reconstruction was appropriate? Do you feel that your reconstructed breast feel soft to touch? Do you feel unnatural when you put on clothes?
(5). For each question, the authors defined satisfied patients as those answering 1, 2 or 3 and dissatisfied patients as those answering 4 or 5. Overall general satisfaction for each patient was defined as having a ‘‘satisfied’’ result on four or five of the five questions, and overall cosmetic satisfaction as having a ‘‘satisfied’’ result on three or four of the four questions (Table 1). Mastectomy included three types of surgery such as total mastectomy, skin-sparing mastectomy or nipple–areolacomplex-sparing mastectomy. SSM was indicated in patients with ductal carcinomas in situ (DCIS), in early breast cancers, and in carefully selected advanced cancers [7]. NSM was frequently selected in patients with carcinomas that do not involve the NAC, which was determined by preoperative radiologic examinations and intraoperative pathology confirmation by frozen section [8]. During the study period, autologous tissue reconstruction was not available in our hospital. All reconstruction was performed using expanders or implants. We used an expander for those who needed to expand the size of breast, such as most of TM, SSM or some NSM patients, an expander was initially used and then replaced by inserting the implant. Impalnts were preferably used by one step for most of whom were indicated for NAC preservation mastectomy. However, if patients wanted more extension with future contralateral augmentation at that time, expanders could be inserted first. In patients with SSM or TM, the NAC was reconstructed in the second stage to optimize the symmetry. Complications included severe infection that led to implant removal and NAC necrosis that required the sacrifice of the preserved NAC. This study was approved by institutional review board.
Breast Cancer Fig. 1 Flowchart of postoperative management of breast reconstruction. 42-yearold woman who had invasive ductal carcinoma on her left breast, was performed total mastectomy and immediate breast reconstruction with tissue expander. She already had bilateral breast augmentation with saline implant a few years ago. To balance the symmetry, saline implant was removed and inframammary fold was elevated on right breast. Tissue expander on left side was removed and inframammary fold was recreated. Afterward, nipple reconstruction and tattooing were completed
Fig. 2 Photographs of preoperative and postoperative findings. 35-year-old woman who had invasive ductal carcinoma on her left breast, was performed NAC-sparing total mastectomy and immediate breast reconstruction with tissue expander. After several months, tissue expander was replaced with permanent implant, and breast augmentation was performed on the contralateral breast to balance the symmetry (upper: preoperative/lower: postoperative)
Results The mean age of the patients was 44.1 years old (range 29–64). There were 16 cases of DCIS, 18 cases of stage I, 21 cases of stage II, and 8 cases of stage III. Thirty-two patients received a total mastectomy and 12 patients had SSM. For these patients, the reconstruction was completed with a tissue expander and a delayed nipple reconstruction (Fig. 1). Nineteen patients had NSM and an immediate permanent implant insertion (Fig. 2). As for the type of prosthesis, 23 patients (36.5 %) obtained a permanent implant and 40 patients (63.5 %) got a tissue expander. Of these 40 patients, 36 later replaced their expander with a
permanent implant. Of the 44 patients who did not have NAC preservation, 28 of them completed NAC reconstruction. Thirty-nine patients had postoperative chemotherapy, 44 patients had endocrine therapy, and 31 patients received both therapies (Table 2). After a mean follow-up period of 22.4 months (range 6–45) there was one case of locoregional recurrence and one case of distant metastasis. The locoregional recurrence case was a 49-year-old woman who had undergone NSM for invasive ductal carcinoma developed ipsilateral axillary recurrence. Her initial pathology reports indicated the tumor was invasive ductal carcinoma 1.6 cm in sized, and the sentinel lymph nodes were negative for metastases. The
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Breast Cancer Table 2 Clinicopathological characteristics of patients
Table 3 Outcome of reconstruction
No. (%) Mean age (range)
44.1 years (29–64)
Mean follow-up periods (range)
22.4 months (6–45)
Cancer stage Ductal carcinoma in situ
16 (25.4)
No. (%) Technical outcome Success
56/63 (88.9)
Failure
7/63 (11.1)
Total
63 (100.0)
I
18 (28.6)
II
21 (33.3)
Nipple–areola complex necrosis
III
8 (12.7)
Removal of prosthesis
3/63 (4.8)
Total
63 (100.0)
Total
7/63 (11.1)
Type of surgery
Major complications 4/63 (6.3)
Oncologic outcome
Total mastectomy
32 (50.8)
Locoregional recurrence
1/63 (1.6)
Skin-sparing mastectomy Nipple–areola-complex-sparing mastectomy
12 (19.0) 19 (30.2)
Distant metastasis Total
1/63 (1.6) 2/63 (3.2)
Total
63 (100.0)
Adjuvant treatment Chemotherapy
39 (60.9)
Endocrine therapy
44 (69.8)
Radiotherapy
Table 4 The results of the questionnaire Classification
General satisfaction
Cosmetic satisfaction
53/63 (84.1 %)
49/63 (77.8 %)
(?)
10 (15.8)
(-)
53 (84.2)
Total
63 (100.0)
Type of surgery
Total
Conventional surgery
patient was diagnosed with ipsilateral axillary recurrence 29 months after the operation and had additional axillary dissection that included the level I and II area. According to pathology reports, there was only one metastatic lymph node among sixteen lymph nodes after this additional operation. A 45-year-old woman who had undergone a MRM for invasive ductal carcinoma stage T2N2M0 developed distant metastasis in the cervical spine 13 months after the initial mastectomy. Radiotherapy was given on the chest wall and spine, after which a capsular contracture developed. The patient eventually decided to remove the implant because of cosmetic dissatisfaction and discomfort. There were no cancer-related deaths among the patients, and thus the breast cancer-specific survival rate was 100 %. Two major complications which included an expander removal or NAC necrosis developed in 11.1 % (7 patients). Three patients removed their implant due to a severe Methicillin-resistant Staphylococcus Aureus infection, implant leakage, and subjective dissatisfaction, respectively. (Table 3) All three were the cases of tissue expander. Among them, one patient who received the radiation therapy wanted to remove the expander with the reason of dissatisfaction. The other two patients did not receive the radiation therapy. NAC survival was the concern for NSM only. Six of the 10 patients who developed NAC necrosis improved after observation and the remaining four
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Total mastectomy
26/32 (81.3 %)
24/32 (75 %)
Conservative surgery
27/31 (87.1 %)
26/31 (83.9 %)
Skin-sparing mastectomy
10/12 (83.3 %)
10/12 (83.3 %)
Nipple–areola-complexsparing mastectomy
17/19 (89.5 %)
16/19 (84.2 %)
Nipple areola complex reconstruction (?)
24/28 (85.7 %)
23/28 (82.1 %)
(-)
12/16 (75.0 %)
10/16 (62.5 %)
Adjuvant radiotherapy (?)
8/10 (80.0 %)
6/10 (60.0 %)
(-)
45/53 (84.9 %)
43/53 (81.1 %)
underwent NAC excision. All 10 cases of necrosis of NAC were not related to radiation therapy. Instead, the more injury to microcirculation for nipple made the more necrosis. Based on the questionnaire, 53 patients (84.1 %) were satisfied with general operational result and 49 patients (77.8 %) were satisfied with the cosmetic result. The 27 patients who received conservative surgery, especially patients who underwent NSM, tended to be more satisfied with the general and cosmetic results than patients who underwent conventional surgery. The 28 patients who received NAC reconstruction were more satisfied with general and cosmetic results (85.7 and 82.1 %, respectively) than patients who did not have it (75.0 and 62.5 % satisfaction with the general and cosmetic results, respectively). Postoperative radiotherapy was associated with
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relatively low satisfaction in the general and cosmetic operation results (Table 4).
Discussion IBR after mastectomy is an oncologically safe and effective procedure for achieving a satisfactory breast shape [9– 11]. Taylor et al. [12] states that IBR does not adversely affect the disease-free state or overall survival, nor does it significantly delay the detection of recurrent disease or delivery of adjuvant therapy. Cocquyt et al. [13] reports that the cosmetic outcome is better for patients with IBR than for those with breast-conserving surgery (BCS). Moreover, Ueda et al. [14] reports that compared to BCS, SSM and NAC-sparing SSM with IBR result in a similar objective cosmetic outcome, patient satisfaction, and a satisfactory body image from the mastectomy. SSM may achieve a superior cosmetic outcome compared to conventional mastectomy in patients for whom mastectomy is inevitable [14]. For a woman with small breasts, SSM with IBR may be an optimal alternative to breast preservation because the cosmetic outcome for BCS is best when the tumor is small relative to the size of the whole breast. While SSM has its limitations in patients with early breast cancer and DCIS, the indications and roles for SSM remain unclear in more advanced stages [15]. Therefore, the treatment for the patient should be selected carefully when considering SSM and IBR. The NAC is a cosmetically essential part of the female breast, and the cosmetic outcome after breast reconstruction is substantially influenced by the quality of the NAC reconstruction. However, a natural-looking NAC is difficult to reconstitute due to its particular color, structure, and texture [16]. In this study, patients who had their NAC preserved were more satisfied with the cosmetic result compared to patients who had NAC reconstruction. However, NAC preservation is controversial in breast cancer treatment because it may increase the risk of local recurrence. Because the NAC has a high probability of containing occult tumor cells, NAC resection is commonly included in all conventional mastectomies.1 Nevertheless, Simmons et al. [17] demonstrates in a retrospective study of 217 mastectomy patients that this risk is overestimated and in many patients, resection of the NAC may be an overtreatment. In this study, the patients did not show any recurrence originating from the preserved NAC, even though the tumors were located centrally or close to the NAC.
1
The locoregional recurrence case was a 49-year-old woman who had undergone NSM for invasive ductal carcinoma developed ipsilateral axillary recurrence
Occasionally, the preserved NAC may be threatened due to impaired microcirculatory blood flow, and surgeons must decide whether to preserve or sacrifice the NAC [18]. In this study, 10 patients were suspected to have NAC necrosis, and six of these improved after observation. Several other studies have shown that patients with a preserved NAC who have temporary color changes and suspected necrosis show improvements in their condition after conservative treatment. In the case of suspected NAC necrosis, a careful choice is necessary for proper NAC management. A drawback of immediate reconstruction is the risk of skin necrosis and associated implant loss. Skin necrosis is often the main complication of SSM because the resection of a large amount of glandular tissue inevitably leaves an extremely thin skin envelope [19, 20]. Skin necrosis may lead to muscle or implant exposure and thus implant loss. The human acellular dermal matrix cushions and supports the breast implant by providing an additional soft tissue layer at the lower pole of the breast, which reinforces the overlying skin. Consequently, the use of human acellular dermal matrix may help to minimize the rate of skin breakdown and implant loss, which is often the main pitfall of immediate implant reconstructions. Salzberg et al. [21] reported a low (3.9 %) rate of overall complications, including infection, skin necrosis, implant loss, hematoma, and capsular contracture. This low complication rate suggests that introducing a subsidiary material such as this matrix gradually reduces postoperative complications. In addition, a surgeon’s experience in performing IBR may also contribute to the likelihood of postoperative complications. In our study, the major complications occurred during the early stage of the observation period. Oncologic issues concerning the diagnosis and treatment of LRR have been the primary consideration in deciding the appropriate timing for reconstruction [22]. According to some studies, reconstruction may mask local recurrence and thus may be a concern of patients considering IBR [23, 24]. A retrospective analysis of 203 consecutive patients during long-term follow-up by Sandelin et al. [25] found that 13 patients (6.4 %) developed an LRR and 7 of these patients were still alive. Thus, IBR does not impair oncological outcome even in women with LRR. Even if the patient has an LRR, survival depends more on systemic disease than local recurrence [26, 27]. Although the mean follow-up period was relatively short in our study, the reconstruction did not negatively affect the recurrence rate nor did it interfere with the detection and treatment of the recurrences in any of our patients. We observed only one case of LRR, which was a postoperative axillary recurrence combined with putative false-negative sentinel lymph nodes at the time of mastectomy. Therefore, IBR can likely be offered without the fear of concealing a recurrence or influencing the oncologic outcome.
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Symmetrical size, shape, and balance of both NAC are important factors when analyzing cosmetic results of breast reconstruction [14]. Because patient satisfaction is related to her expectations and motive for having a reconstruction, the concordant shape and symmetry of the breasts should be the ultimate concerns of the surgeons. The physical comfort and the mobility of the reconstructed breast also determine patient satisfaction. Postoperative radiation therapy after IBR with an implant or tissue expander may have a significantly negative effect on the quality of the reconstruction. Radiation can take away the symmetry, volume, and projection obtained initially at the time of the reconstruction. It is also associated with high complication rates, the most common being capsular contracture. However, the indications for post-mastectomy chest wall irradiation are broadening [28], and whether the patients will require radiation therapy is difficult to predict. Therefore, careful selection of patients for implant use in breast reconstruction should be implemented while considering the oncological need for radiation therapy. In addition, the quality of the cosmetic outcome may be reduced if they receive radiation therapy. Commonly, lower quality cosmetic results are observed when the radiation therapy is administered shortly after the reconstructive procedure [29], suggesting that the negative effects of irradiation may be minimized with appropriate timing of irradiation delivery. Our results suggest delaying breast reconstruction for those patients likely to need radiation therapy and offering implant-assisted immediate reconstruction only for those who, after informed consideration, refuse other options. The ideal time to measure cosmetic outcomes of breast reconstruction is also unclear. The follow-up period in our study was relatively short, and some evidence suggests that cosmetic satisfaction with breast reconstruction decreases as time progresses, especially for expander/implant surgery [30]. Therefore, a longer period of follow-up is needed in future studies to accurately assess satisfaction. In conclusion, immediate breast reconstruction after mastectomy using an implant or tissue expander is oncologically safe and cosmetically acceptable for the majority of patients. Preservation of the skin envelope and NAC may improve esthetic results with minimal complications. However, the oncologic safety of this technique is still a major concern and larger studies are necessary and in progress. Close collaboration between breast surgeons and plastic surgeons is mandatory to thoroughly plan the therapies and the surgical approaches to optimize disease treatment while considering the reconstructive needs. Conflict of interest of interest.
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The authors declare that they have no conflict
References 1. Toth BA, Lappert P. Modified skin incision for mastectomy: the need for plastic surgical input in preoperative planning. Plast Reconstr Surg. 1991;87:1048–53. 2. Newman LA, Kuerer HM, Hunt KK, Kroll SS, Ames FC, Ross MI, et al. Presentation, treatment, and outcome of local recurrence after skin-sparing mastectomy and immediate breast reconstruction. Ann Surg Oncol. 1998;5:620–6. 3. Fersis N, Hoenig A, Relakis K, Pinis S, Wallwiener D. Skinsparing mastectomy and immediate breast reconstruction: incidence of recurrence in patients with invasive breast cancer. Breast. 2004;13:488–93. 4. Margulies AG, Hochberg J, Kepple J, Henry-Tillman RS, Westbrook K, Klimberg S. Total skin-sparing mastectomy without preservation of the nipple–areola complex. Am J Surg. 2005;190:920–6. 5. Fisher B, Bryant J, Wolmark N, Mamounas E, Brown A, Fisher ER, et al. Effect of preoperative chemotherapy on the outcome of women with breast cancer. J Clin Oncol. 1998;16:2672–85. 6. Malata CM, McIntosh SA, Purushotham AD. Immediate breast reconstruction after mastectomy for cancer. Br J Surg. 2000;87:1455–72. 7. Protocollo di diagnosi e trattamento del carcinoma mammario FONCaM. Firenze: Edizione OIC; 2001. 8. Documento di consenso sulla Nipple Sparing Mastectomy. In: Attualita’ in Seno-logia, n.59. Darwin Editore Roma; Gennaio/ Aprile 2010. 9. Cordeiro PG, Mccarthy CM. A single surgeon’s 12-year experience with tissue expander/implant breast reconstruction: part II. An analysis of long-term complications, aesthetic outcomes, and patient satisfaction. Plast Reconstr Surg. 2006;118(4):832–9. 10. Spear SL, Pellettiere CV. Immediate breast reconstruction in two stages using textured, integrated-valve tissue expanders and breast implants. Plast Reconstr Surg. 2004;113:2098–103. 11. Spear SL, Spittler CJ. Breast reconstruction with implants and expanders. Plast Reconstr Surg. 2001;107:177–87. 12. Taylor C, Horgan K, Dodwell D. Oncological aspects of breast reconstruction. Breast. 2005;14:118–30. 13. Cocquyt VF, Blondeel PN, Depypere HT, Van de Sijpe KA, Daems KK, Monstrey SJ, et al. Better cosmetic results and comparable quality of life after skin-sparing mastectomy and immediate autologous breast reconstruction compared to breast conservation treatment. Br J Plast Surg. 2003;56:462–70. 14. Ueda S, Tamaki Y, Yano K, Okishiro N, Yanagisawa T, Imasato M, et al. Cosmetic outcome and patient satisfaction after skinsparing mastectomy for breast cancer with immediate reconstruction of the breast. Surgery. 2008;143:414–25. 15. Foster RD, Esserman LJ, Anthony JP, Hwang ES, Do H. Skin sparing mastectomy and immediate breast reconstruction: a prospective cohort study for the treatment of advanced stages of breast carcinoma. Ann Surg Oncol. 2002;9:462–6. 16. Wirth R, Banic A, Erni D. Aesthetic outcome and oncological safety of nipple–areola complex replantation after mastectomy and immediate breast reconstruction. J Plast Reconstr surg. 2010;63:1490–4. 17. Simmons RM, Brennan M, Christos P, King V, Osborne M. Analysis of nipple/areolar involvement with mastectomy: can the areola be preserved? Ann Surg Oncol. 2002;9:165–8. 18. Hudson DA, Skoll PJ. Single-stage, autologous breast restoration. Plast Reconstr Surg. 2001;108:1163–71. 19. Carlson GW, Losken A, Moore B, Thornton J, Elliott M, Bolitho G, et al. Results of the immediate breast reconstruction after skinsparing mastectomy. Ann Plast Surg. 2001;46:222–8.
Breast Cancer 20. Woerdeman LA, Hage JJ, Smeulders MJ, Rutgers EJ, van der Horst CM. Skin-sparing mastectomy and immediate breast reconstruction by use of implants: an assessment of risk factors for complications and cancer control in 120 patients. Plast Reconstr Surg. 2006;118:321–30. 21. Salzberg C, Ashikari A, Koch RM, Chabner-Thompson E. An 8-year experience of direct-to-implant immediate breast reconstruction using human acellular dermal matrix (Alloderm). Plast Reconstr Surg. 2011;127:514. 22. Deucker-Zertuche M, Robles-Vidal C. A 7 year experience with immediate breast reconstruction after skin sparing mastectomy for cancer. EJSO. 2007;33:140–6. 23. Kroll S, Ames F, Singltary ES, Schusterman MA. The oncologic aspects of skin preservation at mastectomy when combined with immediate reconstruction of the breast. Surg Gynecol Obstet. 1991;172:17–20. 24. Rajan TP, Webster DJT, Mansel RE, Hughes LE. Is immediate post mastectomy reconstruction safe in the long-term? Eur J Surg Oncol. 1993;19:372–5.
25. Sandelin K, Wickman M, Billgren A. Oncological outcome after immediate breast reconstruction for invasive breast cancer: a long-term study. Breast. 2004;13:210–8. 26. Kroll SS, Ames F, Singletary SE. The oncologic risks of skin preservation at mastectomy when combined with immediate reconstruction of the breast. Surg Gynecol Obstet. 1991;172:17–20. 27. Ziegler LD, Kroll SS. Primary breast cancer after prophylactic mastectomy. Am J Clin Oncol. 1991;14:451–4. 28. Overgaard M, Hansen PS, Overgaard J, Rose C, Andersson M, Bach F, et al. Postoperative radiotherapy in high-risk premenopausal women with breast cancer who receive adjuvant chemotherapy. N Engl J Med. 1997;337:956–62. 29. Jackson WB, Goldson AL, Staud C. Postoperative irradiation following immediate breast reconstruction using a temporary tissue expander. J Natl Med Assoc. 1994;86:538–42. 30. Colakoglu S, Khansa I, Curtis MS, Yueh JH, Ogunleye A, Haewyon C, et al. Impact of complications on patient satisfaction in breast reconstruction. Plast Reconstr Surg. 2011;127:1428–36.
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ORIGINAL ARTICLE
Short-term outcomes of immediate breast reconstruction using an implant or tissue expander after mastectomy in breast cancer patients Se Won Kim • Hae Kyung Lee • Sun Mi Kang • Tae Ho Kang • Chan Seok Yoon Seung Sang Ko • Min Hee Hur • Sung Soo Kang • Chul Hwan Seul • Ja Sung Gu
•
Received: 18 April 2014 / Accepted: 23 September 2014 Ó The Japanese Breast Cancer Society 2014
Abstract Background Mastectomy is an optional surgical management of breast cancer, but it can cause significant adverse reactions. Breast reconstruction is a concern in post-mastectomy recovery. We assessed the oncologic safety and patient satisfaction following immediate breast reconstruction using an implant or tissue expander. Methods We retrospectively reviewed all patients who underwent reconstruction with an implant or tissue expander immediately after mastectomy. Seventy-seven patients underwent breast reconstruction at a general hospital breast cancer center from January 2008 to December 2010. Fourteen patients were excluded due to loss at follow-up, so 63 patients were included in this study. Questionnaires were sent to all patients to assess patient satisfaction. Results Mean age was 44.1 years (range 29–64). After a median follow-up period of 22.4 months, there was 1 case of locoregional recurrence, 1 case of distant metastasis, and an overall breast cancer-specific survival of 100 %. Overall rate of major complications, such as nipple areolar complex (NAC) necrosis and implant removal, was 11.1 % (7
patients). Of the 10 patients who had NAC necrosis, 6 patients improved after observation and 4 patients had NAC excision. Three patients had their implant removed due to severe infection, leakage, and dissatisfaction, respectively. There were 32 cases of total mastectomy (TM), 12 cases of skin-sparing mastectomy (SSM), and 19 cases of NAC-sparing mastectomy (NSM). According to the questionnaire, 84.1 % were satisfied with the general operational result and 77.8 % with the cosmetic result. Of the 31 patients who received conservative surgery, 87.1 % were satisfied with the general result and 83.9 % with the cosmetic result. Conclusions Immediate breast reconstruction using an implant after mastectomy was technically feasible and oncologically safe. In addition, the reconstruction resulted in a relatively high rate of patient satisfaction. Further long-term studies are warranted to confirm these findings. Keywords Breast cancer Mastectomy Immediate breast reconstruction Implant Tissue expander
Introduction S. W. Kim H. K. Lee (&) S. M. Kang T. H. Kang C. S. Yoon S. S. Ko M. H. Hur S. S. Kang Department of General Surgery, Catholic Kwandong University College of Medicine, Cheil General Hospital, 1-19 Mukjeong-dong, Jung-gu, Seoul 100-380, Korea e-mail: [email protected] C. H. Seul JW Plastic Surgery, Seoul, Korea J. S. Gu Department of Nursing, Graduate School of Kyung Hee University, Seoul, Korea
In breast cancer patients, the purpose of post-mastectomy breast reconstruction is to recreate a balanced, symmetrical, and natural appearance for both breasts that fulfills the patient’s expectations. The method and timing of breast reconstruction vary, and the outcome depends on the patient’s personal preferences, physical characteristics, and the oncologic safety. Recently, immediate breast reconstruction (IBR) has become an accepted procedure in breast cancer patients. The feasibility of this procedure is largely attributed to the improvement in operational skill, which involves
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conservation of the skin envelope or even the nipple–areola complex (NAC). Since Toth and Lappert introduced the skin-sparing mastectomy (SSM) in 1991 [1], IBR has improved cosmetic results [2–4]. More recently, nipple sparing mastectomy (NSM) has been proposed in select cases and provides an additional option for IBR. Because IBR has become a common practice and has proven medical and psychosocial benefits, the current goal is to produce cosmetically satisfying results that are consistent with oncologic safety requirements [5, 6]. In the present study, we studied the technical feasibility, oncologic safety, cosmetic outcome, and patient satisfaction following IBR using an implant or a tissue expander after mastectomy in Korean women with breast cancer.
Patients and methods Seventy-seven patients underwent breast reconstructions with a permanent implant or tissue expander immediately after mastectomy at Cheil General Hospital breast cancer center from January 2008 to December 2010. During the period, total 300 cases of surgery for breast cancer were performed. Total mastectomy consisted 54 % (321/600). Fourteen patients were excluded from the study because of the lack of follow-up visits; therefore, 63 patients were included in this study. The medical records of these patients were reviewed retrospectively. Mastectomies were performed by five different surgeons and all reconstructions were performed by one plastic surgeon. In principle, immediate reconstruction is recommended for early-stage breast cancer patients who need mastectomy but the final decision is made by the patient preference. In this study, some patients who clinically considered as early breast cancer, later upgraded to advanced stage by the final pathological results were included. To assess the oncologic safety of the procedure, all patients received periodic postoperative follow-up assessments such as physical examinations, breast ultrasonograms, whole body bone scans, and positron-emission tomography-computed tomography (PET-CT) scans to detect locoregional recurrence (LRR) or distant metastasis of primary cancer. The mean follow-up period was 22.4 months (range 6–45). To evaluate satisfaction, a questionnaire consisting of 9 questions was sent to all patients. Questions 1 through 5 assessed general operation satisfaction, and questions 6 through 9 assessed cosmetic satisfaction. A Likert 5-point scale was used for each question (except question 3, which used a visual analog scale that indicated patient satisfaction on a scale of 1–10), with possible answers ranging from ‘‘very satisfied’’ (1) to ‘‘very dissatisfied’’
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Table 1 The questionnaire Items on general satisfaction of surgery If you can choose again, do you want to have breast reconstruction? If you can choose again, do you choose the same type of breast reconstruction? Do you satisfied with the general result of reconstruction? Do you recommend the type of breast reconstruction that you had to your friends? Do you receive sufficient information about your reconstruction options before the operation? Items on cosmetic satisfaction of surgery Do you feel that the size and shape of your breasts are the same? Do you think that the nipple–areola complex reconstruction was appropriate? Do you feel that your reconstructed breast feel soft to touch? Do you feel unnatural when you put on clothes?
(5). For each question, the authors defined satisfied patients as those answering 1, 2 or 3 and dissatisfied patients as those answering 4 or 5. Overall general satisfaction for each patient was defined as having a ‘‘satisfied’’ result on four or five of the five questions, and overall cosmetic satisfaction as having a ‘‘satisfied’’ result on three or four of the four questions (Table 1). Mastectomy included three types of surgery such as total mastectomy, skin-sparing mastectomy or nipple–areolacomplex-sparing mastectomy. SSM was indicated in patients with ductal carcinomas in situ (DCIS), in early breast cancers, and in carefully selected advanced cancers [7]. NSM was frequently selected in patients with carcinomas that do not involve the NAC, which was determined by preoperative radiologic examinations and intraoperative pathology confirmation by frozen section [8]. During the study period, autologous tissue reconstruction was not available in our hospital. All reconstruction was performed using expanders or implants. We used an expander for those who needed to expand the size of breast, such as most of TM, SSM or some NSM patients, an expander was initially used and then replaced by inserting the implant. Impalnts were preferably used by one step for most of whom were indicated for NAC preservation mastectomy. However, if patients wanted more extension with future contralateral augmentation at that time, expanders could be inserted first. In patients with SSM or TM, the NAC was reconstructed in the second stage to optimize the symmetry. Complications included severe infection that led to implant removal and NAC necrosis that required the sacrifice of the preserved NAC. This study was approved by institutional review board.
Breast Cancer Fig. 1 Flowchart of postoperative management of breast reconstruction. 42-yearold woman who had invasive ductal carcinoma on her left breast, was performed total mastectomy and immediate breast reconstruction with tissue expander. She already had bilateral breast augmentation with saline implant a few years ago. To balance the symmetry, saline implant was removed and inframammary fold was elevated on right breast. Tissue expander on left side was removed and inframammary fold was recreated. Afterward, nipple reconstruction and tattooing were completed
Fig. 2 Photographs of preoperative and postoperative findings. 35-year-old woman who had invasive ductal carcinoma on her left breast, was performed NAC-sparing total mastectomy and immediate breast reconstruction with tissue expander. After several months, tissue expander was replaced with permanent implant, and breast augmentation was performed on the contralateral breast to balance the symmetry (upper: preoperative/lower: postoperative)
Results The mean age of the patients was 44.1 years old (range 29–64). There were 16 cases of DCIS, 18 cases of stage I, 21 cases of stage II, and 8 cases of stage III. Thirty-two patients received a total mastectomy and 12 patients had SSM. For these patients, the reconstruction was completed with a tissue expander and a delayed nipple reconstruction (Fig. 1). Nineteen patients had NSM and an immediate permanent implant insertion (Fig. 2). As for the type of prosthesis, 23 patients (36.5 %) obtained a permanent implant and 40 patients (63.5 %) got a tissue expander. Of these 40 patients, 36 later replaced their expander with a
permanent implant. Of the 44 patients who did not have NAC preservation, 28 of them completed NAC reconstruction. Thirty-nine patients had postoperative chemotherapy, 44 patients had endocrine therapy, and 31 patients received both therapies (Table 2). After a mean follow-up period of 22.4 months (range 6–45) there was one case of locoregional recurrence and one case of distant metastasis. The locoregional recurrence case was a 49-year-old woman who had undergone NSM for invasive ductal carcinoma developed ipsilateral axillary recurrence. Her initial pathology reports indicated the tumor was invasive ductal carcinoma 1.6 cm in sized, and the sentinel lymph nodes were negative for metastases. The
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Breast Cancer Table 2 Clinicopathological characteristics of patients
Table 3 Outcome of reconstruction
No. (%) Mean age (range)
44.1 years (29–64)
Mean follow-up periods (range)
22.4 months (6–45)
Cancer stage Ductal carcinoma in situ
16 (25.4)
No. (%) Technical outcome Success
56/63 (88.9)
Failure
7/63 (11.1)
Total
63 (100.0)
I
18 (28.6)
II
21 (33.3)
Nipple–areola complex necrosis
III
8 (12.7)
Removal of prosthesis
3/63 (4.8)
Total
63 (100.0)
Total
7/63 (11.1)
Type of surgery
Major complications 4/63 (6.3)
Oncologic outcome
Total mastectomy
32 (50.8)
Locoregional recurrence
1/63 (1.6)
Skin-sparing mastectomy Nipple–areola-complex-sparing mastectomy
12 (19.0) 19 (30.2)
Distant metastasis Total
1/63 (1.6) 2/63 (3.2)
Total
63 (100.0)
Adjuvant treatment Chemotherapy
39 (60.9)
Endocrine therapy
44 (69.8)
Radiotherapy
Table 4 The results of the questionnaire Classification
General satisfaction
Cosmetic satisfaction
53/63 (84.1 %)
49/63 (77.8 %)
(?)
10 (15.8)
(-)
53 (84.2)
Total
63 (100.0)
Type of surgery
Total
Conventional surgery
patient was diagnosed with ipsilateral axillary recurrence 29 months after the operation and had additional axillary dissection that included the level I and II area. According to pathology reports, there was only one metastatic lymph node among sixteen lymph nodes after this additional operation. A 45-year-old woman who had undergone a MRM for invasive ductal carcinoma stage T2N2M0 developed distant metastasis in the cervical spine 13 months after the initial mastectomy. Radiotherapy was given on the chest wall and spine, after which a capsular contracture developed. The patient eventually decided to remove the implant because of cosmetic dissatisfaction and discomfort. There were no cancer-related deaths among the patients, and thus the breast cancer-specific survival rate was 100 %. Two major complications which included an expander removal or NAC necrosis developed in 11.1 % (7 patients). Three patients removed their implant due to a severe Methicillin-resistant Staphylococcus Aureus infection, implant leakage, and subjective dissatisfaction, respectively. (Table 3) All three were the cases of tissue expander. Among them, one patient who received the radiation therapy wanted to remove the expander with the reason of dissatisfaction. The other two patients did not receive the radiation therapy. NAC survival was the concern for NSM only. Six of the 10 patients who developed NAC necrosis improved after observation and the remaining four
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Total mastectomy
26/32 (81.3 %)
24/32 (75 %)
Conservative surgery
27/31 (87.1 %)
26/31 (83.9 %)
Skin-sparing mastectomy
10/12 (83.3 %)
10/12 (83.3 %)
Nipple–areola-complexsparing mastectomy
17/19 (89.5 %)
16/19 (84.2 %)
Nipple areola complex reconstruction (?)
24/28 (85.7 %)
23/28 (82.1 %)
(-)
12/16 (75.0 %)
10/16 (62.5 %)
Adjuvant radiotherapy (?)
8/10 (80.0 %)
6/10 (60.0 %)
(-)
45/53 (84.9 %)
43/53 (81.1 %)
underwent NAC excision. All 10 cases of necrosis of NAC were not related to radiation therapy. Instead, the more injury to microcirculation for nipple made the more necrosis. Based on the questionnaire, 53 patients (84.1 %) were satisfied with general operational result and 49 patients (77.8 %) were satisfied with the cosmetic result. The 27 patients who received conservative surgery, especially patients who underwent NSM, tended to be more satisfied with the general and cosmetic results than patients who underwent conventional surgery. The 28 patients who received NAC reconstruction were more satisfied with general and cosmetic results (85.7 and 82.1 %, respectively) than patients who did not have it (75.0 and 62.5 % satisfaction with the general and cosmetic results, respectively). Postoperative radiotherapy was associated with
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relatively low satisfaction in the general and cosmetic operation results (Table 4).
Discussion IBR after mastectomy is an oncologically safe and effective procedure for achieving a satisfactory breast shape [9– 11]. Taylor et al. [12] states that IBR does not adversely affect the disease-free state or overall survival, nor does it significantly delay the detection of recurrent disease or delivery of adjuvant therapy. Cocquyt et al. [13] reports that the cosmetic outcome is better for patients with IBR than for those with breast-conserving surgery (BCS). Moreover, Ueda et al. [14] reports that compared to BCS, SSM and NAC-sparing SSM with IBR result in a similar objective cosmetic outcome, patient satisfaction, and a satisfactory body image from the mastectomy. SSM may achieve a superior cosmetic outcome compared to conventional mastectomy in patients for whom mastectomy is inevitable [14]. For a woman with small breasts, SSM with IBR may be an optimal alternative to breast preservation because the cosmetic outcome for BCS is best when the tumor is small relative to the size of the whole breast. While SSM has its limitations in patients with early breast cancer and DCIS, the indications and roles for SSM remain unclear in more advanced stages [15]. Therefore, the treatment for the patient should be selected carefully when considering SSM and IBR. The NAC is a cosmetically essential part of the female breast, and the cosmetic outcome after breast reconstruction is substantially influenced by the quality of the NAC reconstruction. However, a natural-looking NAC is difficult to reconstitute due to its particular color, structure, and texture [16]. In this study, patients who had their NAC preserved were more satisfied with the cosmetic result compared to patients who had NAC reconstruction. However, NAC preservation is controversial in breast cancer treatment because it may increase the risk of local recurrence. Because the NAC has a high probability of containing occult tumor cells, NAC resection is commonly included in all conventional mastectomies.1 Nevertheless, Simmons et al. [17] demonstrates in a retrospective study of 217 mastectomy patients that this risk is overestimated and in many patients, resection of the NAC may be an overtreatment. In this study, the patients did not show any recurrence originating from the preserved NAC, even though the tumors were located centrally or close to the NAC.
1
The locoregional recurrence case was a 49-year-old woman who had undergone NSM for invasive ductal carcinoma developed ipsilateral axillary recurrence
Occasionally, the preserved NAC may be threatened due to impaired microcirculatory blood flow, and surgeons must decide whether to preserve or sacrifice the NAC [18]. In this study, 10 patients were suspected to have NAC necrosis, and six of these improved after observation. Several other studies have shown that patients with a preserved NAC who have temporary color changes and suspected necrosis show improvements in their condition after conservative treatment. In the case of suspected NAC necrosis, a careful choice is necessary for proper NAC management. A drawback of immediate reconstruction is the risk of skin necrosis and associated implant loss. Skin necrosis is often the main complication of SSM because the resection of a large amount of glandular tissue inevitably leaves an extremely thin skin envelope [19, 20]. Skin necrosis may lead to muscle or implant exposure and thus implant loss. The human acellular dermal matrix cushions and supports the breast implant by providing an additional soft tissue layer at the lower pole of the breast, which reinforces the overlying skin. Consequently, the use of human acellular dermal matrix may help to minimize the rate of skin breakdown and implant loss, which is often the main pitfall of immediate implant reconstructions. Salzberg et al. [21] reported a low (3.9 %) rate of overall complications, including infection, skin necrosis, implant loss, hematoma, and capsular contracture. This low complication rate suggests that introducing a subsidiary material such as this matrix gradually reduces postoperative complications. In addition, a surgeon’s experience in performing IBR may also contribute to the likelihood of postoperative complications. In our study, the major complications occurred during the early stage of the observation period. Oncologic issues concerning the diagnosis and treatment of LRR have been the primary consideration in deciding the appropriate timing for reconstruction [22]. According to some studies, reconstruction may mask local recurrence and thus may be a concern of patients considering IBR [23, 24]. A retrospective analysis of 203 consecutive patients during long-term follow-up by Sandelin et al. [25] found that 13 patients (6.4 %) developed an LRR and 7 of these patients were still alive. Thus, IBR does not impair oncological outcome even in women with LRR. Even if the patient has an LRR, survival depends more on systemic disease than local recurrence [26, 27]. Although the mean follow-up period was relatively short in our study, the reconstruction did not negatively affect the recurrence rate nor did it interfere with the detection and treatment of the recurrences in any of our patients. We observed only one case of LRR, which was a postoperative axillary recurrence combined with putative false-negative sentinel lymph nodes at the time of mastectomy. Therefore, IBR can likely be offered without the fear of concealing a recurrence or influencing the oncologic outcome.
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Symmetrical size, shape, and balance of both NAC are important factors when analyzing cosmetic results of breast reconstruction [14]. Because patient satisfaction is related to her expectations and motive for having a reconstruction, the concordant shape and symmetry of the breasts should be the ultimate concerns of the surgeons. The physical comfort and the mobility of the reconstructed breast also determine patient satisfaction. Postoperative radiation therapy after IBR with an implant or tissue expander may have a significantly negative effect on the quality of the reconstruction. Radiation can take away the symmetry, volume, and projection obtained initially at the time of the reconstruction. It is also associated with high complication rates, the most common being capsular contracture. However, the indications for post-mastectomy chest wall irradiation are broadening [28], and whether the patients will require radiation therapy is difficult to predict. Therefore, careful selection of patients for implant use in breast reconstruction should be implemented while considering the oncological need for radiation therapy. In addition, the quality of the cosmetic outcome may be reduced if they receive radiation therapy. Commonly, lower quality cosmetic results are observed when the radiation therapy is administered shortly after the reconstructive procedure [29], suggesting that the negative effects of irradiation may be minimized with appropriate timing of irradiation delivery. Our results suggest delaying breast reconstruction for those patients likely to need radiation therapy and offering implant-assisted immediate reconstruction only for those who, after informed consideration, refuse other options. The ideal time to measure cosmetic outcomes of breast reconstruction is also unclear. The follow-up period in our study was relatively short, and some evidence suggests that cosmetic satisfaction with breast reconstruction decreases as time progresses, especially for expander/implant surgery [30]. Therefore, a longer period of follow-up is needed in future studies to accurately assess satisfaction. In conclusion, immediate breast reconstruction after mastectomy using an implant or tissue expander is oncologically safe and cosmetically acceptable for the majority of patients. Preservation of the skin envelope and NAC may improve esthetic results with minimal complications. However, the oncologic safety of this technique is still a major concern and larger studies are necessary and in progress. Close collaboration between breast surgeons and plastic surgeons is mandatory to thoroughly plan the therapies and the surgical approaches to optimize disease treatment while considering the reconstructive needs. Conflict of interest of interest.
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The authors declare that they have no conflict
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