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 Table of Contents  
ORIGINAL ARTICLE
Year : 2020  |  Volume : 16  |  Issue : 6  |  Page : 1287-1293

Male breast cancer: Outcome with adjuvant treatment


1 Department of Radiation Oncology, Regional Cancer Centre, Postgraduate Institute of Medical Education and Research, Chandigarh, India
2 Department of Radiation Oncology, M.M. Institute of Medical Sciences and Research, Ambala, Haryana, India
3 CMC, General Surgery, Sector-17, Chandigarh, India
4 Department of General Surgery, PGIMER, Chandigarh, India
5 Department of Radiation Oncology, PGIMER, Chandigarh, India

Date of Submission21-Nov-2016
Date of Decision15-Aug-2017
Date of Acceptance24-Feb-2018
Date of Web Publication24-Oct-2018

Correspondence Address:
Budhi Singh Yadav
Department of Radiation Oncology, Regional Cancer Centre, Postgraduate Institute of Medical Education and Research, Chandigarh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jcrt.JCRT_1305_16

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 > Abstract 


Introduction: Male breast cancer (MBC) incidence is <1%, but it is increasing. MBC incidence increases with age. There are no randomized trials on MBC because of low number of patients seen in any institution and hence its management is derived from breast cancer (BC) in women. In this study, we analyzed outcome in MBC patients with adjuvant treatment.
Materials and Methods: From 1991 to 2014, 81 men with BC were retrospectively analyzed for demographic, clinicopathological, and treatment outcomes. Disease-free survival (DFS) was defined as time duration from diagnosis to first recurrence. Overall survival (OS) was defined as time duration from pathologic diagnosis to death or last follow-up with any death defined as an event. DFS and OS were estimated using Kaplan–Meier method and compared between patients receiving and not receiving adjuvant treatment using log-rank test.
Results: The median age was 57 years (range 30–86 years). Right, left, and bilateral BCs were seen in 41 (51%), 38 (47%), and 2 (2%) men, respectively. The mean duration of symptoms was 25 months (range 1–240 months). Comorbidity and family history was present in 31 (38%) and 3 (4%) men, respectively. The mean tumor size was 5 cm × 5 cm (range, 1 cm × 1 cm to 10 cm × 10 cm). Nipple was involved in 46 (57%) men. Early, locally advanced, and metastatic disease were seen in ??30 (37%), 34 (42%), and 17 (21%) men, respectively. Majority (71, 88%) of men had invasive ductal carcinoma histology. In radically treated 64 men, neoadjuvant chemotherapy was given to 12 (19%) patients (fluorouracil, adriamycin, and cyclophosphamide [FAC] to 9 and FAC + taxanes to 3), with CR in 4 (33.3%) and partial response (PR) in 8 (66.7%) patients. Mastectomy was done in 55 (86%) and wide local excision in 9 (14%) men. Margins and nodes were positive in 17 (27%) and 38 (59%) men, respectively. Estrogen receptor, PR, and human epidermal growth factor receptor 2/neu positive were seen in 27 (42%), 17 (26.5%), and 2 (3%) patients, respectively. Adjuvant hypofractionated radiotherapy, chemotherapy, and tamoxifen were received by 51 (80%), 35 (55%), and 45 (70%) men, respectively. Median follow-up was 60 months (range 4–278 months). Locoregional recurrence occurred in 8 (12.5%) and distant metastasis in 22 (34%) men, respectively. DFS and OS at 10 years were 42% and 53%, respectively. DFS and OS were significantly better in men with adjuvant radiation (54% vs. 24%, P = 0.007 and 57% vs. 35%, P = 0.022, respectively) and hormonal therapy (57% vs. 14.5%, P = 0.004 and 62% vs. 39%, P = 0.045, respectively). Chemotherapy had no impact on DFS and OS.
Conclusion: Adjuvant hypofractionated radiotherapy and hormonal therapy significantly improved DFS and OS in MBC patients. Chemotherapy had no impact on DFS and OS.

Keywords: Chemotherapy, male breast cancer, radiotherapy, surgery


How to cite this article:
Yadav BS, Sharma SC, Singh R, Dahiya D, Ghoshal S. Male breast cancer: Outcome with adjuvant treatment. J Can Res Ther 2020;16:1287-93

How to cite this URL:
Yadav BS, Sharma SC, Singh R, Dahiya D, Ghoshal S. Male breast cancer: Outcome with adjuvant treatment. J Can Res Ther [serial online] 2020 [cited 2021 Nov 27];16:1287-93. Available from: https://www.cancerjournal.net/text.asp?2020/16/6/1287/243480




 > Introduction Top


Male breast cancer (MBC) incidence is <1% and 0.1% of all malignancies, but it is increasing.[1] MBC incidence increases with age; the median age at diagnosis is 67 years compared to 57 years in women. The risk factors for MBC includes genetic disorders such as BRCA2 and BRCA1 mutations; family history of breast cancer (BC) and Klinefelter's syndrome; chronic liver and testicular diseases; and lifestyle-related factors such as obesity, alcohol intake, and ethnicity.[2],[3],[4] There are no randomized trials because of low number of patients seen in any institution, and retrospective series are also very few. MBC management is derived from BC in women. Initial studies have suggested that MBC had worse prognosis as compared to female BC.[5],[6],[7] The lack of breast tissue in male poses difficulty in achieving adequate margins even in small tumors. However, in India, patients present in advanced stage and this poses a challenge to achieve negative margin. Hence, there are definitely indications for adjuvant treatment in these patients.

Postmastectomy radiotherapy (PMRT) indications in men treated for BC; the guidelines followed are same as for women with BC. PMRT appears to reduce locoregional recurrence (LRR) in MBC; however, the influence on survival is unknown.[8],[9],[10],[11] Few studies have reported benefit with PMRT in MBC patients.[12],[13],[14],[15] Many retrospective studies have evaluated the role of adjuvant hormonal therapy, and these studies have revealed that most MBC patients can benefit from adjuvant tamoxifen in terms of recurrence and survival.[16],[17],[18],[19],[20] Although chemotherapy has been used to treat high-risk MBC patients, data supporting it are lacking. Some data also suggested that adjuvant and systemic treatment in MBC should be as in women with BC.,[16],[17],[18],[21] In this study, we analyzed outcome in MBC patients with adjuvant treatment.


 > Materials and Methods Top


From 1991 to 2013, 81 men with BC were retrospectively analyzed for patient-related characteristics such as age, comorbidity, family history, pathological stage/tumor size, histology, grade, extracapsular extension, lymphovascular invasion, estrogen/progesterone, human epidermal growth factor receptor 2 (HER-2) status, and treatment-related factors such as radiotherapy, chemotherapy, and hormonal therapy [Table 1]. All parameters were entered into a computerized database.
Table 1: Patient characteristics

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PMRT was delivered to patients with T3 tumor, close/positive margins, and positive nodes. Standard two tangential opposed fields were used to irradiate Chest wall (CW). Hypofractionated radiotherapy, 35 Gy was delivered in 15 fractions over 3 weeks to CW. Dose was prescribed at the midpoint of the central axis. Bolus was used on alternate days in patients with negative margins and daily in patients with positive margins. For supraclavicular fossa, dose delivered was 40 Gy/15#/3 weeks with a single-incident field. Radiation therapy was delivered using60Co machine.

Tamoxifen was given to ER/PR-positive patients for 5 years. Patients were followed up at regular intervals: every 3 monthly till 1 year, 4 monthly till 3 years, 6 monthly till 5 years, and yearly thereafter. Further tests were done only if they had symptoms or evidence of recurrent or metastatic disease.

Treatment outcomes analyzed were LRR, disease-free survival (DFS), and overall survival (OS). LRR was defined as any recurrence in the skin or soft tissue over CW or a recurrence in the regional lymphatic sites (axilla, internal mammary nodes, infraclavicular, and supraclavicular). DFS was defined as time duration from surgery to the first recurrence. OS was defined as time duration from pathologic diagnosis to death or last follow-up with any death defined as an event. DFS and OS were estimated using Kaplan–Meier method and compared between patients receiving and not receiving adjuvant treatment using log-rank test. All statistical tests were two tailed, and the differences were considered statistically significant if P < 0.05. Statistical analysis was performed using Statistical Package for the Social Science software version 18.0 (Chicago, IL, USA).


 > Results Top


The median age was 57 years (range 30–86 years). Right, left, and bilateral BCs were seen in 41 (51%), 38 (47%), and 2 (2%) men, respectively. The mean duration of symptoms was 25 months (range 1–240 months). Comorbidity and family history were present in 31 (38%) and 3 (4%) men, respectively. The mean tumor size was 5 cm × 5 cm (range, 1 cm × 1 cm to 10 cm × 10 cm). Nipple was involved in 46 (57%) men. Early, locally advanced, and metastatic disease were seen in 30 (37%), 34 (42%), and 17 (21%) patients, respectively. Majority (71, 88%) of patients had invasive ductal carcinoma histology. Among 17 patients with metastatic disease, 14 men received chemotherapy, 6 became operable, and 4 also received radiotherapy and tamoxifen. Other 8 patients received palliative radiotherapy and hormonal therapy. Rest out of 5 patients, 3 received hormonal therapy, 1 chemotherapy and hormonal therapy and 2 with poor general condition were given only supportive care.

In radically treated 64 men, neoadjuvant chemotherapy with fluorouracil, adriamycin, and cyclophosphamide (FAC) (5-FU: 600 mg/m2, adriamycin: 50 mg/m2, and cyclophosphamide: 600 mg/m2) and FAC + taxanes regimen was given to 9 (14%) and 3 (5%) patients, respectively. Complete response (CR) and partial response (PR) were seen in 4 (33.3%) and 8 (66.7%) patients, respectively. Mastectomy was done in 55 (86%) and wide local excision in 9 (14%) men. Margin was positive in 17 (27%) patients. Nodes were positive in 38 (59%) men [Table 1]. ER, PR, and Her2neu positive were seen in 27 (42%), 17 (26.5%), and 2 (3%) patients, respectively. Adjuvant hypofractionated radiotherapy, chemotherapy, and tamoxifen were received by 51 (80%), 35 (55%), and 45 (70%) men, respectively. Chemotherapy regimens used were cyclophosphamide, methotrexate, and fluorouracil (cyclophosphamide: 600 mg/m2, methotrexate: 40 mg/m2, and 5-FU: 600 mg/m2) in 9 (25%), FAC in 16 (46%), and anthracyclines and taxanes in 8 (23%) patients. Only 2 (6%) patients received platinum-based chemotherapy.

Median follow-up was 60 months (range 4–278 months). For the entire cohort, LRR occurred in 8 (12.5%) and distant metastasis in 22 (34%) men. The LRR was 8% (4/51) with PMRT as compared to 31.7% (4/13) without PMRT [Table 2]. PMRT reduced LRR in all groups irrespective of stage, margins, and nodal status. It reduced LRR in low- as well as high-risk patients [Table 2]. For the entire cohort, the median DFS was 43 months, and the 5- and 10-year survival rates were 58% and 42%, respectively. The median OS was 60 months, and the 5- and 10-year survival rates were 69% and 52%, respectively. DFS at 10 years [Figure 1] was 54% and 24% with and without PMRT (P = 0.007), respectively. OS at 10 years [Figure 2] was significantly better in men with PMRT (57%) as compared to 35% in without PMRT (P = 0.022). Hormonal therapy also significantly improved DFS [Figure 3] and OS [Figure 4] at 10 years (57% vs. 14.5%, P = 0.004 and 62% vs. 39%, P = 0.045, respectively). Chemotherapy had no impact on DFS and OS. DFS [Figure 5] at 10 years with and without chemotherapy was 44% and 60%, respectively (P = 0.60). OS [Figure 6] at 10 years with and without chemotherapy was 46% and 68%, respectively (P = 0.33). There was no DFS or OS benefit with neoadjuvant chemotherapy. DFS at 10 years with and without neoadjuvant chemotherapy was 62% and 57%, respectively (P = 0.66). Similarly, OS at 10 years with and without neoadjuvant chemotherapy was 64% and 59%, respectively (P = 0.77).
Table 2: Pattern of recurrence

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Figure 1: Disease-free survival with radiotherapy

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Figure 2: Overall survival with radiotherapy

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Figure 3: Disease-free survival with tamoxifen

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Figure 4: Overall survival with tamoxifen

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Figure 5: Disease-free survival with chemotherapy

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Only 1 (1%) patient developed second malignancy in the contralateral breast after 8 years of follow-up.


 > Discussion Top


In this study of MBC, patients were 10 years younger than those reported from the Western literature. The median age in the present study was 57 years (range 30–86 years) as compared to 67 years reported from the West.[4] The patients in the present study presented late (mean symptom duration 25 months) and also had more advanced disease (mean tumor size 5 cm) as compared to Western patients that is why majority of patients (80%) were given adjuvant radiation. Most of the patients presented to our institute at advanced stage because of lack of awareness of the disease, ignorance, taking alternative treatment (desi medicine and ayurvedic treatment), and long distance for the treatment. Apart from it, there are logistic problems such as male attitude of “I am fine” and seek medical help once the disease becomes advanced and interferes with quality of life of the patient.

The history of familial cancer was in 4% patients in the present study. This could be because of geographical variation. In a study by Ahmed et al. from Nigeria, familial risk was 2.5%.[22]

There are not much data from India, especially on the risk of familial cancer in MBC, might be our patients have less familial risk. In a study from Bengaluru,[23] it was reported to be 15.4%. Gogia et al. reported 10% risk of familial cancer from Delhi.[24] In another study from Delhi by Sundriyal et al., of 18 patients, none had familial cancer.[25] Other studies from India have not reported familial risk.

Other reasons could be under reporting in the history, but its chances are less as there is standard format for noting history and it includes family history as one of the components.

It was seen that PMRT significantly improved DFS and OS in these patients. The benefit of PMRT was irrespective of tumor stage, margin, and lymph nodal status [Table 2]. In a study from Canada by Yu et al., they reported a trend toward improving LRR with PMRT in patients with high-risk features (node positive, advanced stage, and =2 mm or unknown surgical margin). However, the same study did not show a benefit in OS for patients receiving PMRT.[11] The median follow-up in that study was only 46 months. Our study had a longer median follow-up of 60 months. In the present study, LRR rate without radiotherapy ranged from 14% to 25% in low-risk patients and from 25% to 50% in high-risk patients. LRR rate with PMRT was 8% (range 3.5%–13%). Hence, PMRT reduced LRR to 1/3rd in low-risk patients and 1/4th in high-risk patients [Table 2]. In the present study also, LRR in high-risk patients was consistence with other studies in the literature [Table 3]. In contrast to other studies reported in the literature [Table 4], LRR rate without PMRT was higher in the present study.[7],[15],[31],[34] This may be attributed to larger tumor size and advanced stage of presentation in our patients. In a study by Chakravarthy and Kim, local recurrence was 3.5% in Stage I/II patients.[7] Cutuli et al. in their study with a median follow-up of 74 months demonstrated local recurrence of 4.7% with PMRT and 11.5% without PMRT. Local recurrence rate was 6.4% among patients with T1 and T2 tumors.[15] Similarly, Yu et al. reported a LRR from 6.9% to 10.3% in low-risk patients without PMRT and 17%–20% in high-risk patients.[11] In contrast in a study by Hultborn et al., patients with tumor sizes 5 cm, or metastasis with perinodal growth, had approximately a 30% recurrence rate on the chest wall.[26]
Table 3: Characteristics of patients with local recurrence as first failure

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Table 4: PMRT studies with LRR reported in literature

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It is a routine practice in our institute to give PMRT to majority of MBC patients because of advanced stage at presentation, the lack of breast tissue in male patients, and the concern of adequate surgical margin even in small tumors, that is why only 13 patients did not receive PMRT. Limited prospective studies with limited patient number are available to evaluate the value of PMRT in MBC. Further, there are few data in the literature demonstrating the benefit of PMRT in MBC.[12],[13] The LRR rate in the present study with PMRT was 7.4%. LRR reported in the literature ranged from 2% to 68% (median, 13%). The 5-year local recurrence-free survival (LRFS) in the present study was 63% which is comparable to those reported in the literature where it ranged from 55% to 69% (median, 66%).[8],[10],[11],[12],[13],[14],[15],[19],[27],[28],[29],[30],[31],[32] Erlichman et al. revealed that the addition of radiation decreases the incidence of local recurrence in MBC. Among 89 patients evaluated retrospectively, 57 patients had PMRT. The LRFS rate was better in patients receiving PMRT compared to patients receiving surgery alone (P = 0.038). However, there was no difference in survival (P = 0.72).[12]

All our patients were treated on60Co with hypofractionated radiotherapy. None of the patients in the present study received boost to the scar. Although radiation was frequently used in many series, there is a wide variation in radiation source, dose, and techniques. The wide range of local recurrence rates in PMRT reported in various studies may reflect the inconsistent use of PMRT. Our results are consistent with other studies that MBC patients who received PMRT have better LRFS rate compared with patients who received surgery alone.[11],[15],[29],[30],[31] In a recent study from Turkey by Selcukbiricik et al., they reported 5-year LRR of 11.3% with PMRT in 86 MBC patients.[33] Similarly, a decade back, Perkins et al. had reported LRR of 18% in 142 patients who received PMRT.[14] In a study by Cutuli et al. from 20 French institutions of 489 patients, LRR rate varied significantly between irradiated an nonirradiated patients (7.3% vs. 13%, respectively).[34] However, Erlichman et al. had reported higher relapse rates with PMRT compared to other studies.[12]

Only 11 patients (FAC in 9 and anthracyclines and taxanes in 2) received neoadjuvant chemotherapy. There was no DFS or OS benefit with neoadjuvant chemotherapy. DFS at 10 years with and without neoadjuvant chemotherapy was 62% and 57%, respectively (P = 0.66). Similarly, OS at 10 years with and without neoadjuvant chemotherapy was 64% and 59%, respectively (P = 0.77).

Chemotherapy was received by 35 (55%) patients in the present study; however, it failed to improve DFS and OS. Median number of chemotherapy cycle received was 4.5. Recurrence rate was significantly less in patients who received both chemotherapy and hormonal therapy as compared to chemotherapy alone. Of 26 patients who received chemotherapy and hormonal therapy, 9 (35%) recurred (1 local and 8 distant). Out of 9 who received chemotherapy only, 7 (78%) recurred (1 local and 6 distant). There was no difference in the comorbidity among patients who received chemotherapy and those who did not. However, in a study by Giordano et al., they reported significant benefit with chemotherapy, 10-year OS was 43% in node-positive patients.[21] The OS in the present study is 44% with chemotherapy which is comparable, but it was worse than without chemotherapy [Figure 6].
Figure 6: Overall survival with chemotherapy

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Our study also demonstrated significant DFS [Figure 3] and OS [Figure 4] benefit with hormonal therapy. It has been reported in literature that 90% of MBCs express ERs and 81% express PRs, as compared to 75% and 66% in female BC, respectively.[4],[21] Tamoxifen for 5 years is the standard therapy in these patients. Several retrospective studies have shown a reduced risk of BC recurrence and death in MBC patients who received tamoxifen.[34],[35],[36] Ribeiro and Swindell in a small study of 39 patients reported that in patients with mastectomy followed by tamoxifen for 1 or 2 years as compared to mastectomy only, 5-year DFS and OS was 56% and 28% and 61% and 41%, respectively.[35] Similarly, Goss et al. also reported a significant benefit in both DFS and OS in their study of 229 MBC patients over 40 years.[36] Patients in these two studies have received tamoxifen for only 1 or 2 years, but for optimal results, it should be given for 5 years. In the present study, patients received tamoxifen for 5 years. There are no data on prolonged use of tamoxifen in MBC, but considering the benefit that it may be given beyond 5 years.

Limitation of our study is being retrospective with small number of patients from a single institute. In 1/3rd of our patients, ER/PR expression was not known still majority (70%) received hormonal therapy. Out of four other studies with limited patient number and follow-up from India,[23],[24],[25],[37] three have reported that ER/PR was expressed in 77%–89% of MBC patients.[24],[25],[37] Hence, giving tamoxifen to 70% of patients in the present study may be justified. However, the three other studies have not reported outcome with PMRT or other adjuvant treatments.[24],[25],[37] Majority of studies on MBC are limited by their retrospective nature and many by small sample size. Hence, it is difficult to analyze the effects of different adjuvant treatment strategies on LRR rates and OS using retrospective material from small numbers of patients. Due to less number of patients, the events may also be less in the subgroups. The strength of our study is largest data set from India on MBC with a good median follow-up of 60 months and all patients treated on cobalt machine with hypofractionated radiotherapy which is being considered now the standard of care in female BC patients.

The recurrence rate in MBC patients in the present study is comparable with the female BC patients we have reported in our previous studies.[38],[39] The available data in the literature[40] also support that patient sex does not seem to be a prognostic factor in local disease recurrence and PMRT had improved DFS and OS in female BC; therefore, it is reasonable to consider PMRT in MBC patients who have high-risk features such as large tumor size, microscopic resection margin involvement, inadequate surgery, and positive axillary lymph nodes and extensive lymphovascular invasion. We also propose here that the risk of LRR in early-stage MBC is high, especially in Indian setup and postmastectomy radiation in early Stages I/II disease may be indicated. Adjuvant hormonal therapy also improves DFS and OS in these patients. However, the role of chemotherapy is still not clear.


 > Conclusion Top


Patients in this study were younger as compared to Western series. LRR rate without radiotherapy ranged from 14% to 25% in low-risk patients and from 25% to 50% in high-risk patients. PMRT reduced LRR rate to 8% in low-risk and to 9% in high-risk men with BC. PMRT and hormonal therapy significantly improved DFS and OS in MBC patients. Chemotherapy had no impact on DFS and OS.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]



 

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