Abstract
Background:
Although breast-conserving surgery is one of the standard treatments for breast cancer, few studies have assessed its recent implementation in China. We aimed to clarify the current real-world status of breast-conserving surgery in China.
Methods:
This cross-sectional survey relied on data collected by the Chinese Society of Breast Surgery (CSBrS) to examine patients who underwent this surgery between January 2018 and December 2018. The survey was conducted using a uniform electronic questionnaire to collect information, including clinical and pathological data on these patients.
Results:
Overall, 4459 breast-conserving surgeries were performed in 34 member units of CSBrS, accounting for 14.6% of all breast cancer surgeries performed in these units during the study period. In patients who underwent breast-conserving surgery with information on tumor size available, more than half (61.2%) of the tumors were smaller than 2 cm in diameter, and only 87 (3.2%) tumors were larger than 4 cm in diameter. Among patients who underwent breast-conserving surgeries, 457 (10.2%) patients received neoadjuvant therapy before the surgery. Among patients with a reported margin width, 34 (2.0%) patients had a margin of ≤2 mm, and 1530 (88.2%) of them had a margin of >5 mm.
Conclusions:
This study demonstrated the rates of breast-conserving surgery in member units of the CSBrS, and introduced the characteristics and surgical margins of patients who underwent this surgery. This information helps describe the real-world status of breast-conserving surgery in China.
Trial registration
chictr.org.cn, ChiCTR1900026841; http://www.chictr.org.cn/showproj.aspx?proj=42783
Keywords: Breast cancer, Breast-conserving surgery, Multi-center research, Real-world study
Introduction
After several clinical studies confirmed the efficacy of breast-conserving surgery,[1,2] the National Institutes of Health recommended it as an appropriate treatment method for early-stage breast cancer in 1991.[3] Early randomized clinical trials using large sample sizes found that breast-conserving surgery yielded comparable survival rates and better cosmetic outcomes compared to radical surgery.[1,4] A recent study showed that early-stage breast cancer patients who underwent breast-conserving surgery plus radiotherapy had a better 10-year overall and relative survival than those who underwent a mastectomy.[5] Due to its excellent clinical and cosmetic outcomes, breast-conserving surgery has been accepted as one of the standard treatments for early-stage breast cancer over the past 30 years.
Currently, several academic organizations in China actively promote breast-conserving surgery and have successively established relevant guidelines.[6,7] Some hospitals in South China, such as the Sun Yat-sen Memorial Hospital, had a breast-conserving surgery rate of more than 50%, which was close to the rate observed in developed countries.[8] However, the overall rate of breast-conserving surgery in China was still low.[9,10] Treatment-related decisions can be influenced by multiple factors, including clinician preferences, concerns about recurrence, and additional treatment requirements. The “no ink on tumor” or negative margin guideline may also affect the implementation of breast-conserving surgery.[11] However, in recent years, few studies have examined the characteristics of patients who underwent breast-conserving surgeries in China. The Chinese Society of Breast Surgery (CSBrS) conducted a multi-center cross-sectional survey of breast-conserving surgeries based on the member units. Using data from this survey, we aimed to clarify the current real-world status of breast-conserving surgery in a Chinese population and to provide a reference for the formulation of relevant strategies.
Methods
Ethical approval
The study was performed in accordance with the Declaration of Helsinki and was approved by the Ethics Committee of the Second Hospital of Shandong University (No. KYLL-2019 (KJ) P-0082). As this was a retrospective study and all data analyses were performed anonymously, the need for informed consent from patients was waived.
Study population
This study relied on data collected by CSBrS to investigate patients who underwent breast-conserving surgeries from January 2018 to December 2018. All patients included in the study were (a) women, (b) breast cancer patients from member hospitals of CSBrS, and (c) diagnosed with breast cancer pathologically and had undergone breast-conserving surgery. The exclusion criteria were: (a) occurrence of distant metastases before surgery, (b) inflammatory breast cancer, and (c) male breast cancer. The survey was conducted using a uniform, electronic questionnaire, which included questions regarding the general conditions and clinical-pathological data of the patients. The clinical-pathological data included information on the tumor location (side and quadrant), tumor size, neoadjuvant therapy, mode of lymph node surgery, pathological type, molecular subtype, and margin width. Data were obtained through the electronic medical record system of each hospital. The molecular subtypes including luminal A, luminal B, human epidermal growth factor receptor 2 (HER2)+, and triple-negative breast cancer were based on the expression of the estrogen receptor, progesterone receptor, HER2, and Ki-67 according to the European Society for Medical Oncology 2015 Primary Breast Cancer Clinical Practice Guidelines.[12] All investigators received uniform training from the CSBrS. Data collection was completed by June 31, 2019.
Statistical analysis
After the collection of data, the logic was checked, and outliers were removed. The general information on the clinical and pathological data from patients undergoing breast-conserving surgeries was evaluated. The areas of hospitals covered in this study were divided into seven regions: Northeast China, North China, East China, South China, Central China, Northwest China, and Southwest China according to the registering regions of the National Central Cancer Registry of China.[13] Data were presented as numbers and percentages. SPSS version 20.0 software (IBM, Armonk, NY, USA) was used for statistical analyses.
Results
Rates of breast-conserving surgery
Questionnaires were sent to 40 member units of the CSBrS, and 34 of them responded by providing the required data. According to the responses, a total of 30,494 breast cancer patients underwent surgery from January 2018 to December 2018, and 4459 (14.6%) of those had breast-conserving surgeries. Hospitals in South China reported the highest rate of breast-conserving surgery (47.1%), while those in Northeast China reported a rate of only 8.9% [Table 1].
Table 1.
Rates of breast-conserving surgery by geographic regions.
| Region | Breast-conserving surgery, n | Surgeries of breast cancer, n | Breast-conserving rate (%) |
| Northeast China | 540 | 6052 | 8.9 |
| North China | 872 | 3743 | 23.3 |
| East China | 1122 | 8019 | 14.0 |
| South China | 631 | 1341 | 47.1 |
| Central China | 592 | 4145 | 14.3 |
| Northwest China | 241 | 2213 | 10.9 |
| Southwest China | 461 | 4981 | 9.3 |
| Total | 4459 | 30,494 | 14.6 |
Characteristics of patients
The mean age of patients who underwent breast-conserving surgery was 48.7 ± 11.2 years. While 855 (19.8%) patients were <40 years of age, only 100 (2.3%) of them were over 75 years of age. The proportion of premenopausal and postmenopausal patients was 58.2% and 41.8%, respectively. The tumor was located on the left side in 1863 (51.5%) patients, and in the lateral upper quadrant in 1387 (49.4%) patients. Among the patients, 139 (5.3%) reported a family history of breast cancer, and 197 (7.9%) had a family history of malignant tumors [Table 2].
Table 2.
Characteristics of patients who underwent breast-conserving surgery.
| Characteristics | Breast-conserving surgery, n (%) |
| Age (years) | 4319 |
| <40 | 855 (19.8) |
| 40–49 | 1662 (38.5) |
| 50–65 | 1481 (34.4) |
| 66–75 | 221 (5.1) |
| >75 | 100 (2.3) |
| Menstrual status | 3535 |
| Premenopausal | 2056 (58.2) |
| Postmenopausal | 1479 (41.8) |
| Number of births | 3049 |
| 0 | 173 (5.7) |
| 1–2 | 2684 (88.0) |
| ≥3 | 192 (6.3) |
| Family history of breast cancer | 2641 |
| No | 2502 (94.7) |
| Yes | 139 (5.3) |
| Family history of malignant tumors | 2481 |
| No | 2284 (92.1) |
| Yes | 197 (7.9) |
| Tumor side | 3616 |
| Left | 1863 (51.5) |
| Right | 1733 (47.9) |
| Bilateral | 20 (0.6) |
| Tumor quadrant | 2806 |
| Lateral upper quadrant | 1387 (49.4) |
| Lateral lower quadrant | 603 (21.5) |
| Interior upper quadrant | 503 (17.9) |
| Interior lower quadrant | 264 (9.4) |
| Areola area | 49 (1.7) |
| Tumor size | 2754 |
| ≤1 cm | 349 (12.7) |
| 1 cm < size ≤ 2 cm | 1335 (48.5) |
| 2 cm < size ≤ 3 cm | 806 (29.3) |
| 3 cm < size ≤ 4 cm | 177 (6.4) |
| >4 cm | 87 (3.2) |
| Neoadjuvant therapy | 4459 |
| No | 4002 (89.8) |
| Yes | 457 (10.2) |
| Axillary surgery | 3632 |
| SLNB | 2932 (80.7) |
| ALND | 700 (19.3) |
| Number of metastatic nodes | 2969 |
| 0 | 2284 (76.9) |
| 1–3 | 526 (17.7) |
| 4–9 | 116 (3.9) |
| ≥10 | 43 (1.4) |
| Pathological type | 3957 |
| IDC | 2523 (63.8) |
| ILC | 100 (2.5) |
| DCIS | 436 (11.0) |
| LCIS | 32 (0.8) |
| Other subtypes | 866 (21.9) |
| Molecular subtype | 3768 |
| Luminal A | 875 (23.2) |
| Luminal B | 2186 (58.0) |
| HER2+ | 229 (6.1) |
| TNBC | 478 (12.7) |
SLNB: Sentinel lymph node biopsy; ALND: Axillary lymph node dissection; IDC: Invasive ductal carcinoma; ILC: Invasive lobular carcinoma; DCIS: Ductal carcinoma in situ; LCIS: Lobular carcinoma in situ; HER2: Human epidermal growth factor receptor 2; TNBC: Triple-negative breast cancer.
In patients who reported information regarding tumor size (n = 2754), 1684 (61.2%) of the tumors were smaller than 2 cm in diameter, and only 87 (3.2%) patients had tumors larger than 4 cm in diameter. Among these patients, 457 (10.2%) patients received neoadjuvant therapy before surgery, 2932 (80.7%) patients underwent sentinel lymph node biopsy, and 2284 (76.9%) patients had negative axillary lymph nodes. In terms of pathological type, invasive ductal carcinomas (IDCs) accounted for 63.8% of the tumors, while ductal carcinomas in situ (DCIS) accounted for 11.0% of the tumors [Table 2].
Surgical margins of patients
Among patients who reported information regarding surgical margins (n = 3119), 227 (7.3%) of them had positive margins at the first time and underwent extended excision until the margins were negative. Among patients who reported the margin width (n = 1734), 34 (2.0%) of them had a margin ≤2 mm, and 1530 (88.2%) had a margin of >5 mm. Among patients with a margin of ≤2 mm, 21 (1.9%) had IDCs, and 1 (0.7%) had DCIS [Table 3].
Table 3.
Information on surgical margins in patients who underwent breast-conserving surgery.
| Characteristics | Breast-conserving surgery, n (%) | IDC, n (%) | DCIS, n (%) |
| Positive residual tumor margin for the first time, n = 3119 | |||
| No | 2892 (92.7) | 1436 (92.3) | 305 (90.8) |
| Yes | 227 (7.3) | 120 (7.7) | 31 (9.2) |
| Margin width, n = 1734 | |||
| ≤1 mm | 7 (0.4) | 2 (0.2) | 1 (0.7) |
| 1 mm < width ≤ 2 mm | 27 (1.6) | 19 (1.7) | 0 (0) |
| 2 mm < width ≤ 5 mm | 170 (9.8) | 77 (6.8) | 14 (10.3) |
| >5 mm | 1530 (88.2) | 1027 (91.3) | 121 (89.0) |
IDC: Invasive ductal carcinoma; DCIS: Ductal carcinoma in situ.
Discussion
Breast-conserving surgery has been accepted as a standard treatment for early-stage breast cancer.[14] It is used to treat more than 50% of patients with early breast cancer in western countries.[15,16] The present study found that the rate of breast-conserving surgeries in member units of the CSBrS was 14.6%. Although the rate had increased since 2008 (11.88%) based on a multi-center study in China,[9] our findings suggest that this rate should continue to increase further. This surgery was reported at a rate of 8.9% in Northeast China and 47.1% in South China, illustrating regional differences in the acceptance of breast-conserving surgery by doctors and patients.
The rate of breast-conserving surgeries is reported to be low in some low- and middle-income countries due to the advanced stage at diagnosis.[17,18] In recent years, with advances in screening technology and health awareness, the detection of early breast cancer in China has increased.[19] However, the rate of detection is still low compared to that in developed countries,[20,21] which was an important factor limiting the implementation of breast-conserving surgery in China. Neoadjuvant therapy is an important strategy to improve the rate of breast-conserving surgery, and its safety was confirmed in the TBCRC017 study.[22] The NSABP B18 study demonstrated comparable long-term survival rates in patients who underwent neoadjuvant chemotherapy followed by breast-conserving surgery when compared to those who underwent early breast-conserving surgery.[23] This study also showed that only 10.2% of Chinese patients underwent breast-conserving surgery after neoadjuvant therapy, which was lower than the proportion reported in developed countries.[23,24] Patients play a vital role in the choice of surgery for breast cancer, and nearly 80% of them were directly or indirectly involved in choosing the surgical approach.[25] Concerns regarding the risk of recurrence and the effects of post-operative radiation therapy made patients more likely to choose mastectomy over breast-conserving surgery.[25] A questionnaire survey investigated 1264 patients with early-stage breast cancer in China and found that only 7.3% of them anticipated undergoing breast-conserving surgery.[26] This was primarily due to an insufficient understanding of the safety of breast-conserving surgery, and concerns about local recurrence after the surgery. In such cases, recommendations from doctors were particularly important.
A negative surgical margin is an indicator of successful breast-conserving surgery. Studies have confirmed that positive margins following breast-conserving surgery increase the risk of local recurrence requiring re-operation.[27] This, in turn, may result in poor cosmetic appearance and increased complications and financial burden.[27] However, among patients with negative margins, a wider margin did not reduce the local recurrence rate.[28] In 2014, the Society of Surgical Oncology and American Society for Radiation Oncology recommended the “no ink on tumor” guideline to be the standard for negative margins in breast-conserving surgery.[29] The overall re-excision rates declined significantly after the adoption of this guideline.[30] In the present study, the incidence of a close margin (≤1 mm) was 0.4%, which was lower than that reported by the Memorial Sloan Kettering Cancer Center.[30] The incidence of cases with margins >5 mm was 88.2%, which was comparable to that reported in a study from Denmark (93%).[28] These findings indicate that the majority of Chinese patients who underwent breast-conserving surgery had a margin of >5 mm. The rate of initial positive margins was 7.3% in this study, which was lower than that observed in developed countries.[29] This indicates that Chinese doctors were relatively conservative with margins during breast-conserving surgeries and that a wide range of glands was removed. Currently, in China, the margins for breast-conserving surgeries are determined based on the intraoperative frozen pathology. Moreover, these surgeries require longer intra-operative waiting periods and; therefore, add to the workload of breast surgeons and pathologists. At the same time, the overall follow-up rate for breast cancer in China is low. Therefore, without timely regular re-examinations, relapse after a breast-conserving surgery might not be detected until the terminal stage. These factors limit the extensive use of breast-conserving surgery in the absence of sufficient human resources and advanced medical technology.
The present study has some limitations that require consideration. First, the hospitals enrolled in this study were all members of the CSBrS. All of them were third-grade hospitals, providing relatively high-quality health care services. The overall rate of breast-conserving surgeries performed in the included hospitals was 14.6%, which may be possibly higher than the nationwide rate. Second, this study only collected the general, clinical, and pathological data from patients who underwent breast-conserving surgery. We could not analyze differences in the rates of breast-conserving surgeries in different patients. Finally, considerable data were missing for some variables. Tumor size and margin width were reported for only 2754 (61.8%) and 1734 (38.9%) cases, respectively, which might affect the results of this study.
In conclusion, this study demonstrated the rates of breast-conserving surgery in member units of the CSBrS and introduced the characteristics and surgical margins of patients who underwent this surgery. It was helpful to understand the real-world status of breast-conserving surgery in China. The attitude of doctors and patients towards breast-conserving surgery was conservative in some hospitals. Efforts to improve the expertise of breast surgeons are required to standardize the breast-conserving surgery procedure and increase its implementation in China.
Acknowledgements
The authors would like to acknowledgement the member units of CSBrS for data collection: Sun Yat-Sen Memorial Hospital, Henan Cancer Hospital, Jiangsu Province Hospital, The Fifth Medical Center of Chinese PLA General Hospital, The Second Affiliated Hospital of Zhejiang University School of Medicine, Peking University People's Hospital, Yunnan Cancer Hospital, Xijing Hospital, The First Affiliated hospital of Zhejiang University School of Medicine, The First Bethune Hospital of Jilin University, Peking University First Hospital, The First Hospital Affiliated to AMU (Southwest Hospital), Zhongshan Hospital Affiliated to Fudan University, Fujian Medical University Union Hospital, The Second Affiliated Hospital of Harbin Medical University, Inner Mongolia Autonomous Region People's Hospital, Affiliated Wudang Hospital of Guizhou Medical University, Xiangya Hospital Central South University, Shengjing Hospital of China Medical University, The Second Hospital of Dalian University, The Fourth Hospital of Hebei Medical University, Beijing Friendship Hospital Capital Medical University, The First Affiliated Hospital of China Medical University, Obstetrics and Gynecology Hospital of Fudan University, Sichuan Provincial People's Hospital, Xuan Wu Hospital affiliated to Capital Medical University, Lanzhou University Second Hospital, The Second Affiliated Hospital of Nanchang University, Beijing Chaoyang Hospital of Capital Medical University, Tangshan People's Hospital, Jilin Cancer Hospital, Qilu Hospital of Shandong University.
Funding
This work was supported by grants from the National Key Research and Development Program of China (Nos. 2016YFC0901300 and 2016YFC0901302).
Conflicts of interest
None.
Footnotes
How to cite this article: Yu LX, Shi P, Tian XS, Yu ZG, Chinese Society of Breast Surgery. A multi-center investigation of breast-conserving surgery based on data from the Chinese Society of Breast Surgery (CSBrS-005). Chin Med J 2020;133:2660–2664. doi: 10.1097/CM9.0000000000001152
References
- 1.Fisher B, Redmond C, Fisher ER, Bauer M, Wolmark N, Wickerham DL, et al. Ten-year results of a randomized clinical trial comparing radical mastectomy and total mastectomy with or without radiation. N Engl J Med 1985; 312:674–681. doi: 10.1056/NEJM198503143121102. [DOI] [PubMed] [Google Scholar]
- 2.Veronesi U, Saccozzi R, Del Vecchio M, Banfi A, Clemente C, De Lena M, et al. Comparing radical mastectomy with quadrantectomy, axillary dissection, and radiotherapy in patients with small cancers of the breast. N Engl J Med 1981; 305:6–11. doi: 10.1056/NEJM198107023050102. [DOI] [PubMed] [Google Scholar]
- 3.NIH Consensus Conference Treatment of early-stage breast cancer. JAMA 1991; 265:391–395. doi: 10.1001/jama.1991.03460030097037. [PubMed] [Google Scholar]
- 4.Veronesi U, Cascinelli N, Mariani L, Greco M, Saccozzi R, Luini A, et al. Twenty-year follow-up of a randomized study comparing breast-conserving surgery with radical mastectomy for early breast cancer. N Engl J Med 2002; 347:1227–1232. doi: 10.1056/NEJMoa020989. [DOI] [PubMed] [Google Scholar]
- 5.van Maaren MC, de Munck L, de Bock GH, Jobsen JJ, van Dalen T, Linn SC, et al. 10 year survival after breast-conserving surgery plus radiotherapy compared with mastectomy in early breast cancer in the Netherlands: a population-based study. Lancet Oncol 2016; 17:1158–1170. doi: 10.1016/S1470-2045(16)30067-5. [DOI] [PubMed] [Google Scholar]
- 6.Chinese Association of Breast Surgery A consensus statement on the breast-conserving surgery of early-stage breast cancer (2019) (in Chinese). Chin J Surg 2019; 57:81–84. doi: 10.3760/cma.j.issn.0529-5815.2019.02.001. [DOI] [PubMed] [Google Scholar]
- 7.National Health Commission of the People's Republic of China Chinese guidelines for diagnosis and treatment of breast cancer 2018 (English version). Chin J Cancer Res 2019; 31:259–277. doi: 10.21147/j.issn.1000-9604.2019.02.02. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Chen K, Pan Z, Zhu L, Hu T, Peng M, Jia W, et al. Comparison of breast-conserving surgery and mastectomy in early breast cancer using observational data revisited: a propensity score-matched analysis. Sci China Life Sci 2018; 61:1528–1536. doi: 10.1007/s11427-018-9396-x. [DOI] [PubMed] [Google Scholar]
- 9.Zhang BL, Sivasubramaniam PG, Zhang Q, Wang J, Zhang B, Gao JD, et al. Trends in radical surgical treatment methods for breast malignancies in China: a multicenter 10-year retrospective study. Oncologist 2015; 20:1036–1043. doi: 10.1634/theoncologist.2014-0281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Guo R, Si J, Xue J, Su Y, Mo M, Yang B, et al. Changing patterns and survival improvements of young breast cancer in China and SEER database, 1999-2017. Chin J Cancer Res 2019; 31:653–662. doi: 10.21147/j.issn.1000-9604.2019.04.09. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Kantor O, Pesce C, Kopkash K, Barrera E, Winchester DJ, Kuchta K, et al. Impact of the Society of Surgical Oncology-American Society for Radiation Oncology margin guidelines on breast-conserving surgery and mastectomy trends. J Am Coll Surg 2019; 229:104–114. doi: 10.1016/j.jamcollsurg.2019.02.051. [DOI] [PubMed] [Google Scholar]
- 12.Senkus E, Kyriakides S, Ohno S, Penault-Llorca F, Poortmans P, Rutgers E, et al. Primary breast cancer: ESMO clinical practice guidelines for diagnosis, treatment and follow-up. Ann Oncol 2015; 26: Suppl 5: v8–v30. doi: 10.1093/annonc/mdv298. [DOI] [PubMed] [Google Scholar]
- 13.Chen W, Zheng R, Baade PD, Zhang S, Zeng H, Bray F, et al. Cancer statistics in China, 2015. CA Cancer J Clin 2016; 66:115–132. doi: 10.3322/caac.21338. [DOI] [PubMed] [Google Scholar]
- 14.Liu Q, Liu Y, Xu L, Duan X, Li T, Qin N, et al. Multicenter prospective study of magnetic resonance imaging prior to breast-conserving surgery for breast cancer. Chin Med J 2014; 127:2401–2406. doi: 10.3760/cma.j.issn.0366-6999.20132508. [PubMed] [Google Scholar]
- 15.Freedman RA, He Y, Winer EP, Keating NL. Trends in racial and age disparities in definitive local therapy of early-stage breast cancer. J Clin Oncol 2009; 27:713–719. doi: 10.1200/JCO.2008.17.9234. [DOI] [PubMed] [Google Scholar]
- 16.Garcia-Etienne CA, Tomatis M, Heil J, Friedrichs K, Kreienberg R, Denk A, et al. Mastectomy trends for early-stage breast cancer: a report from the EUSOMA multi-institutional European database. Eur J Cancer 2012; 48:1947–1956. doi: 10.1016/j.ejca.2012.03.008. [DOI] [PubMed] [Google Scholar]
- 17.Ferlay J, Colombet M, Soerjomataram I, Mathers C, Parkin DM, Pineros M, et al. Estimating the global cancer incidence and mortality in 2018: GLOBOCAN sources and methods. Int J Cancer 2019; 144:1941–1953. doi: 10.1002/ijc.31937. [DOI] [PubMed] [Google Scholar]
- 18.Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A. Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 2018; 68:394–424. doi: 10.3322/caac.21492. [DOI] [PubMed] [Google Scholar]
- 19.Fan L, Strasser-Weippl K, Li JJ, St Louis J, Finkelstein DM, Yu KD, et al. Breast cancer in China. Lancet Oncol 2014; 15:e279–e289. doi: 10.1016/S1470-2045(13)70567-9. [DOI] [PubMed] [Google Scholar]
- 20.DeSantis C, Ma J, Bryan L, Jemal A. Breast cancer statistics, 2013. CA Cancer J Clin 2014; 64:52–62. doi: 10.3322/caac.21203. [DOI] [PubMed] [Google Scholar]
- 21.Zheng Y, Zhang M. Disparities of breast cancer burden between China and western countries and its implication (in Chinese). Chin J Surg 2015; 53:905–909. doi: 10.3760/cma.j.issn.0529-5815.2015.12.004. [PubMed] [Google Scholar]
- 22.McGuire KP, Hwang ES, Cantor A, Golshan M, Meric-Bernstam F, Horton JK, et al. Surgical patterns of care in patients with invasive breast cancer treated with neoadjuvant systemic therapy and breast magnetic resonance imaging: results of a secondary analysis of TBCRC 017. Ann Surg Oncol 2015; 22:75–81. doi: 10.1245/s10434-014-3948-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Rastogi P, Anderson SJ, Bear HD, Geyer CE, Kahlenberg MS, Robidoux A, et al. Preoperative chemotherapy: updates of National Surgical Adjuvant Breast and Bowel Project Protocols B-18 and B-27. J Clin Oncol 2008; 26:778–785. doi: 10.1200/JCO.2007.15.0235. [DOI] [PubMed] [Google Scholar]
- 24.Buchholz TA, Lehman CD, Harris JR, Pockaj BA, Khouri N, Hylton NF, et al. Statement of the science concerning locoregional treatments after preoperative chemotherapy for breast cancer: a National Cancer Institute conference. J Clin Oncol 2008; 26:791–797. doi: 10.1200/JCO.2007.15.0326. [DOI] [PubMed] [Google Scholar]
- 25.Katz SJ, Lantz PM, Janz NK, Fagerlin A, Schwartz K, Liu L, et al. Patient involvement in surgery treatment decisions for breast cancer. J Clin Oncol 2005; 23:5526–5533. doi: 10.1200/JCO.2005.06.217. [DOI] [PubMed] [Google Scholar]
- 26.Zhang L, Jiang M, Zhou Y, Du XB, Yao WX, Yan X, et al. Survey on breast cancer patients in China toward breast-conserving surgery. Psychooncology 2012; 21:488–495. doi: 10.1002/pon.1922. [DOI] [PubMed] [Google Scholar]
- 27.Metcalfe LN, Zysk AM, Yemul KS, Jacobs LK, Oker EE, Underwood HR, et al. Beyond the margins-economic costs and complications associated with repeated breast-conserving surgeries. JAMA Surg 2017; 152:1084–1086. doi: 10.1001/jamasurg.2017.2661. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.Bodilsen A, Bjerre K, Offersen BV, Vahl P, Amby N, Dixon JM, et al. Importance of margin width in breast-conserving treatment of early breast cancer. J Surg Oncol 2016; 113:609–615. doi: 10.1002/jso.24224. [DOI] [PubMed] [Google Scholar]
- 29.Moran MS, Schnitt SJ, Giuliano AE, Harris JR, Khan SA, Horton J, et al. Society of Surgical Oncology-American Society for Radiation Oncology consensus guideline on margins for breast-conserving surgery with whole-breast irradiation in stages I and II invasive breast cancer. Int J Radiat Oncol Biol Phys 2014; 88:553–564. doi: 10.1016/j.ijrobp.2013.11.012. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 30.Rosenberger LH, Mamtani A, Fuzesi S, Stempel M, Eaton A, Morrow M, et al. Early adoption of the SSO-ASTRO consensus guidelines on margins for breast-conserving surgery with whole-breast irradiation in stage I and II invasive breast cancer: initial experience from Memorial Sloan Kettering Cancer Center. Ann Surg Oncol 2016; 23:3239–3246. doi: 10.1245/s10434-016-5397-7. [DOI] [PMC free article] [PubMed] [Google Scholar]