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The nipple sparing mastectomy: a 5-year experience at the European Institute of Oncology of Milan

Background

Under certain conditions, the nipple sparing mastectomy can be proposed for the treatment of breast cancer when the mastectomy remains indicated. The nipple areola complex (NAC) preservation improves the quality of life, reducing the feeling of mutilation. The main argument against the procedure is the lack of radical resection of the retroareolar ductal system. A novel radiosurgical treatment combining subcutaneous mastectomy with intraoperative radiotherapy is proposed.

Methods

Seven hundred and seventy-three nipple sparing mastectomies have been performed since March 2002, for invasive carcinoma in 63% and for in situ carcinoma in 37%. Clinical complications, aesthetic results, and oncological and psychological results were recorded.

Results

The NAC necrosed totally in 26 cases (3.3%) and partially in 49 cases (6.3%), and was removed in 36 cases (4.6%). Thirteen infections (1.6%) were observed and 32 (4.14%) prostheses removed. The median rating of the patients for global cosmetic results on a 0 (worst) to 10 (excellent) scale was 8. The surgeon in charge of the follow-up has given the same rating. A radio dystrophy was observed on the areola in 5.1% of the patients. The sensitivity of the NAC recovered slowly and partially in only 30% of the cases. Twelve local recurrences (1.5%) occurred in an average follow-up period of 18 months (range 1–61 months). Most recurrences were located far from the nipple areola site, outside the radiated field. Two recurrences were Paget disease associated with an in situ carcinoma. Overall, we observed 23 metastases and three deaths. Sixty-eight per cent of patients were satisfied with their reconstructed breast and 97% were satisfied with having preserved the NAC.

Introduction

Conservative treatment is now well accepted for a majority of breast cancers and is performed in around 70–80% of cases [1]. However, mastectomy remains indicated in at least 20% of patients. An important improvement resulted from the skin-sparing mastectomy technique, validated by several publications [2–11]. The preservation of the skin envelope has favoured the quality of the breast reconstruction, and breast reconstructive surgery has made important progress, providing more natural shape. However, despite the reconstruction, patients often deplore a feeling of mutilation. The nipple areola complex (NAC) appears an identity mark of the breast [12]. Several authors have evaluated the risk of nipple areola involvement and investigated the possibility of nipple areola preservation [13–18]. Focusing on such risk, and the possible cancer recurrence in the breast tissue preserved beneath the NAC for the blood supply, we proposed to combine the subcutaneous mastectomy technique with intraoperative radiotherapy with electrons (ELIOT), previously trialled in breast-conserving treatment [19]. The preliminary results of the 'nipple sparing mastectomy' (NSM) were published in 2003 [20]. Today, we report the results of 773 NSMs performed at the European Institute of Oncology.

Materials and methods

From March 2002 to March 2007, 898 patients were invited to undergo a NSM. The inclusion criteria were primary tumours located at least 1 cm outside the areola margins, an absence of nipple retraction or bloody discharge, and an absence of retro areola micro-calcifications. Multifocality was not a cause for exclusion, provided that all the tumour sites were distant from the areola. Invasive as well as in situ carcinomas were included. Patients were excluded at the time of the operation when the frozen examination of the retro areola tissue had been positive for carcinoma: in these cases, ELIOT was not delivered and the NAC was removed. Among the 898 cases, 98 were excluded, mainly because of the positive extemporaneous examination and in several cases because of the poor blood supply requiring the NAC removal. Fifty-one candidates were excluded because no radiotherapy was delivered, most often when the blood supply was poor and the risk of necrosis very high. Finally, 749 patients underwent a NSM, among whom 24 had a bilateral NSM.

The mean patient age was 46 years (range 20–73 years). Seventy-five per cent of the patients have a mean follow-up of 18 months (range 1–61 months).

The surgical technique has already been described [20]. Breast reconstruction was achieved with a definitive prosthesis in 689 cases (89%) and with an expander in 185 (24%). Only six patients underwent a reconstruction with an autologous transverse rectus abdominis myocutaneous and one with an autologous Latissimus dorsi.

Once the glandular tissue has been removed and the frozen section of the retro areola tissue proved free of cancer, ELIOT was performed on the NAC area. The ELIOT technique has already been described [21–24]. In our technique, 16 Gy were delivered on the NAC in one shot with lead and aluminium disk protection of the pectoralis muscle and thoracic wall (see Figure 1). However, in 145 cases, the same radiotherapy was postponed to the following day, due to technical problems with the machine in the operating room.

Sensitivity, colour, radio dystrophy, position and symmetry, and global evaluation by the surgeon and the patient, were rated according to a scale (0–10), 10 indicating the best results. (The results were rated poor when rated from 0 to 3, fair from 5 to 6 and good or excellent from 7 to 10.)

Local recurrences, distant metastases and death were also recorded. A psychological study was conducted concomitantly. A detailed questionnaire was sent to the patients 1 year after the operation to evaluate the degree of satisfaction. The statistic analysis of psychological results was performed with the chi-square test and exact Fisher test.

Results

NAC total necrosis was observed in 26 cases out of 773 NSMs (3.3%). Partial necrosis was observed in 49 cases (6.3%). The NAC was removed in 36 cases (4.6%). The definitive histology of the 773 NSMs was invasive carcinoma in 63% and in situ carcinoma in 37%. In 53 cases (6%), the definitive histology of the retro areola tissue returned positive for carcinoma (invasive in 35 cases and in situ in 18 cases). Thirteen infections (1.6%) were observed in the immediate postoperative period; 32 prostheses were removed (4.1%). A capsulotomy has been required in 137 cases (17.7%).

Cosmetic results and sequelea were evaluated by the surgeon in charge of the follow-up according to the scale previously mentioned. The average evaluation of the sensitivity of the areola and the periareolar area was 2/10. Thirty per cent of the patients recovered some kind of sensitivity in several months. The colour of the areola was judged 8/10. The radio dystrophy was absent in most cases: 9/10. A radio dystrophy such as telangiectasia has been observed in 5.1% of the cases. The symmetry of the breasts was evaluated well in most cases: 7/10. The global result was rated by the patient as 8/10 and also as 8/10 by the surgeon (see cases 1–3, Figures 2, 3, 4).

Figure 1
figure 1

(a) The sterile collimator of the LINAC. (b) The gauze over the areola allows a more homogeneous distribution of the dose to the nipple and the areola. (c) Protective lead and aluminum disks. (d) Pectoralis major muscle.

Figure 2
figure 2

Case 1. (a) Preoperative drawing and result. (b) and (c) Final result with contralateral augmentation.

Figure 3
figure 3

Case 2. (a) Right NSM. (b) Breast reconstruction with TRAM flap.

Figure 4
figure 4

case 3. (a) Left nipple sparing mastectomy, right prophylactic mastectomy. (b) Bilateral reconstruction with prosthesis.

Cancer results

Despite the frozen section performed underneath the NAC to eliminate the cases with positive results, the final histology of the retro areola tissue was positive in 53 (6.8%) cases, among which 35 were invasive carcinomas (66%). However, the NAC has been preserved in most cases when the final examination returned positive, taking into account the intraoperative radiotherapy to avoid recurrences. The secondary removal was due to local necrosis. Twelve local recurrences were observed. Two were located on the NAC and the 10 others at a distance from the radiated area, usually in the same area of the tumour location. Both recurrences on the NAC were a DCIS associated with a Paget disease on the nipple. No recurrence on the NAC was observed in the group of patients with persistent positive histology.

Twenty-three cases of distant metastases and three deaths were observed in our series.

The psychological study was completed for 159 patients who had at least 1 year follow-up and who answered our questionnaire. Ninety-seven per cent of the patients interviewed declare being very satisfied with the appearance of the breast after the NSM. No patient regretted having undergone reconstructive surgery, and 91.5% agreed with the mutilation being decreased by having preserved the NAC. Similarly, 93% of women responded that conserving the nipple aided in facing illness, and only 1.6% expressed a total dissatisfaction.

Discussion

Our study on 773 skin-sparing mastectomies performed at the European Institute of Oncology confirms the feasibility of the procedure, with a majority of good results after the preservation of the NAC. However, a partial or total NAC necrosis due to insufficient blood supply was observed in 9.7% of the cases. Moreover, 6.6% of the final retro areola histology return positive while it was observed negative at the frozen section. Such results could be improved with a better selection of the NSM, if we cancel the cases requiring an extensive retro areola tissue removal and if we change the surgical indications of the reconstruction in cases of large breast, more often using autologous tissue reconstruction. Concerning the retro areola free margins, we should verify with more accuracy the clinical proximity between the tumour and the NAC.

A partial or global return of the NAC sensitivity was present in only 30% of the patients. As expected, the return is incomplete and takes months to happen [25]. The risk of radio dystrophy is low with such intraoperative radiotherapy at the level of 16 Gy. Seven per cent of the patients had a severe or moderate radio dystrophy, but a mild pigmentation was observed in around one-third of the women with at least 1 year follow-up.

Two in situ local recurrences were observed on the preserved NAC, which is reassuring although the median follow-up is only 18 months. A longer follow-up is required to prove the efficacy of the intraoperative radiotherapy. The dose of ELIOT chosen to reduce the recurrence risk could be questioned [20–24]. The single application of 16 Gy corresponds to the classic fractioned radiotherapy of 45 Gy for tumour cells and of 70–80 Gy for late responding normal tissue. This dose should be sufficient to sterilise more than 90% of the residual cancer cells, and to obtain an acceptable risk (less than 5%) of severe late complications (necrosis). However, the percentage of patients with positive persistent carcinoma behind the NAC in our series justifies ELIOT, although other authors advocate the possibility of NAC preservation without ELIOT [13, 26–29].

Finally, the primary goal of the NSM is the psychological improvement of patients requiring a mastectomy. The preliminary results of the questionnaire report a high level of satisfaction and confirm the psychological importance of NAC conservation.

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Petit, J., Veronesi, U., Orecchia, R. et al. The nipple sparing mastectomy: a 5-year experience at the European Institute of Oncology of Milan. Breast Cancer Res 9 (Suppl 1), S10 (2007). https://doi.org/10.1186/bcr1693

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