The association between cancer location and lymph node metastasis in early stage of breast cancer_CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY

Authors：

ZHANG Yuanxin ,  LI Hongjiang , DU Zhenggui

Department of Breast Surgery, West China Hospital, Sichuan University, Chengdu 610041, P. R. China;

Corresponding author：

LI Hongjiang, Email: lihongjiang@sohu.com

Keywords：

breast cancer; tumor location; tumor anatomy level location; lymph node metastasis; review

DOI：

10.7507/1007-9424.201807062

Video：

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Objective To summarize the relation between tumor location and lymph node metastasis in early stage of breast cancer, which is aimed at providing a more individualized treatment for breast cancer patients. Method The literatures about breast cancer location and lymph node metastasis in recent years were extracted, through the literatures study we made a thematic review of the relation between them. Results There were two main classification methods for the location of breast tumors at present: tumor in the different quadrants and tumor to skin distance. In the quadrant classification method, the tumor in the upper inner quadrant (UIQ) had the lowest lymph node metastasis rate, while the lower inner quadrant (LIQ) tumor recurrence-free survival rate and overall survival rate were significantly lower than other quadrants. When measuring tumor to skin distance, the closer the tumor was to the skin, the more likely lymph node metastasis occurred. In combination with the distribution, histology, and anatomical differences of lymphatic and lymphatic networks, our study group proposed to classify tumors according to different anatomical levels of the breast, thus the anatomic location of the tumor was divided into four types: constricted in the gland, break the anterior gland, break the posterior gland, and break both anterior and posterior gland. Conclusions Regardless of the way the location is classified, the location of breast tumors is closely related to lymphatic and lymph node metastasis. The new classification according to the distribution of tumors at different anatomical levels of the breast accords with the law of lymphatic metastasis is scientific and reasonable. Therefore, during clinical practices, we recommend to use the new method to classify tumor location, and we should consider the differences in the location of the patients’ tumor to assess the status of axillary lymph node, which may provide a more individualized treatment for breast cancer patients.

Citation： ZHANG Yuanxin, LI Hongjiang, DU Zhenggui. The association between cancer location and lymph node metastasis in early stage of breast cancer. CHINESE JOURNAL OF BASES AND CLINICS IN GENERAL SURGERY, 2019, 26(2): 247-252. doi: 10.7507/1007-9424.201807062 Copy

1.	Harlow SP, Krag DN, Julian TB, et al. Prerandomization surgical training for the national surgical adjuvant breast and bowel project (NSABP) B-32 trial: a randomized phase Ⅲ clinical trial to compare sentinel node resection to conventional axillary dissection in clinically node-negative breast cancer. Ann Surg, 2005, 241(1): 48-54.
2.	Galimberti V, Cole BF, Zurrida S, et al. Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial. Lancet Oncol, 2013, 14(4): 297-305.
3.	Caudle AS, Hunt KK, Tucker SL, et al. American College of Surgeons Oncology Group (ACOSOG) Z0011: impact on surgeon practice patterns. Ann Surg Oncol, 2012, 19(10): 3144-3151.
4.	Donker M, van Tienhoven G, Straver ME, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol, 2014, 15(12): 1303-1310.
5.	Eom YH, Kim EJ, Chae BJ, et al. The distance between breast cancer and the skin is associated with axillary nodal metastasis. J Surg Oncol, 2015, 111(7): 824-828.
6.	Manca G, Tardelli E, Rubello D, et al. Sentinel lymph node biopsy in breast cancer: a technical and clinical appraisal. Nucl Med Commun, 2016, 37(6): 570-576.
7.	Zhang L, Huang Y, Yang C, et al. Application of a carbon nanoparticle suspension for sentinel lymph node mapping in patients with early breast cancer: a retrospective cohort study. World J Surg Oncol, 2018, 16(1): 112.
8.	Kim GR, Choi JS, Han BK, et al. Preoperative axillary US in early-stage breast cancer: potential to prevent unnecessary axillary lymph node dissection. Radiology, 2018, 288(1): 55-63.
9.	Gentilini O, Veronesi U. Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: Sentinel node vs Observation after axillary UltraSouND). Breast, 2012, 21(5): 678-681.
10.	Huang TW, Kuo KN, Chen KH, et al. Recommendation for axillary lymph node dissection in women with early breast cancer and sentinel node metastasis: a systematic review and meta-analysis of randomized controlled trials using the GRADE system. Int J Surg, 2016, 34: 73-80.
11.	Torre LA, Islami F, Siegel RL, et al. Global cancer in women: burden and trends. Cancer Epidemiol Biomarkers Prev, 2017, 26(4): 444-457.
12.	Zheng A, Duan W, Zhang L, et al. How great is current curative expenditure and catastrophic health expenditure among patients with cancer in China? A research based on " System of Health Account 2011”. Cancer Med, 2018, 7(8): 4036-4043.
13.	Skinner KA, Silberman H, Sposto R, et al. Palpable breast cancers are inherently different from nonpalpable breast cancers. Ann Surg Oncol, 2001, 8(9): 705-710.
14.	Shayan R, Inder R, Karnezis T, et al. Tumor location and nature of lymphatic vessels are key determinants of cancer metastasis. Clin Exp Metastasis, 2013, 30(3): 345-356.
15.	Ryan T. The ageing of the blood supply and the lymphatic drainage of the skin. Micron, 2004, 35(3): 161-171.
16.	Moore JE Jr, Bertram CD. Lymphatic system flows. Annu Rev Fluid Mech, 2018, 50: 459-482.
17.	Dawood S, Merajver SD, Viens P, et al. International expert panel on inflammatory breast cancer: consensus statement for standardized diagnosis and treatment. Ann Oncol, 2011, 22(3): 515-523.
18.	Redig AJ, McAllister SS. Breast cancer as a systemic disease: a view of metastasis. J Intern Med, 2013, 274(2): 113-126.
19.	王静文, 唐建武, 赵君怡. VEGFC/D-VEGFR3/NRP2 轴通路相关分子在肿瘤及其淋巴道转移时的变化与意义. 现代肿瘤医学, 2016, 24(17): 2808-2811.
20.	Deng Y, Zhang X, Simons M. Molecular controls of lymphatic VEGFR3 signaling. Arterioscler Thromb Vasc Biol, 2015, 35(2): 421-429.
21.	Pepper MS, Skobe M. Lymphatic endothelium: morphological, molecular and functional properties. J Cell Biol, 2003, 163(2): 209-213.
22.	Smith KJ, Jones PF, Burke DA, et al. Lymphatic vessel distribution in the mucosa and submucosa and potential implications for T1 colorectal tumors. Dis Colon Rectum, 2011, 54(1): 35-40.
23.	Eccles SA, Welch DR. Metastasis: recent discoveries and novel treatment strategies. Lancet, 2007, 369(9574): 1742-1757.
24.	He Y, Rajantie I, Pajusola K, et al. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res, 2005, 65(11): 4739-4746.
25.	Karpanen T, Egeblad M, Karkkainen MJ, et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res, 2001, 61(5): 1786-1790.
26.	Cunningham JE, Jurj AL, Oman L, et al. Is risk of axillary lymph node metastasis associated with proximity of breast cancer to the skin. Breast Cancer Res Treat, 2006, 100(3): 319-328.
27.	Bae MS, Shin SU, Song SE, et al. Association between US features of primary tumor and axillary lymph node metastasis in patients with clinical T1-T2N0 breast cancer. Acta Radiol, 2018, 59(4): 402-408.
28.	Ansari B, Morton MJ, Adamczyk DL, et al. Distance of breast cancer from the skin and nipple impacts axillary nodal metastases. Ann Surg Oncol, 2011, 18(11): 3174-3180.
29.	Siotos C, McColl M, Psoter K, et al. Tumor site and breast cancer prognosis. Clin Breast Cancer, 2018, 18(5): e1045-e1052.
30.	Sohn VY, Arthurs ZM, Sebesta JA, et al. Primary tumor location impacts breast cancer survival. Am J Surg, 2008, 195(5): 641-644.
31.	Chan S, Chen JH, Li S, et al. Evaluation of the association between quantitative mammographic density and breast cancer occurred in different quadrants. BMC Cancer, 2017, 17(1): 274.
32.	Bevilacqua J, Cody H 3rd, MacDonald KA, et al. A prospective validated model for predicting axillary node metastases based on 2,000 sentinel node procedures: the role of tumour location. Eur J Surg Oncol, 2002, 28(5): 490-500.
33.	Wu S, Zhou J, Ren Y, et al. Tumor location is a prognostic factor for survival of Chinese women with T1-2N0M0 breast cancer. Int J Surg, 2014, 12(5): 394-398.
34.	Colleoni M, Zahrieh D, Gelber RD, et al. Site of primary tumor has a prognostic role in operable breast cancer: the international breast cancer study group experience. J Clin Oncol, 2005, 23(7): 1390-1400.
35.	Lim ST, Choi JE, Kim SJ, et al. Prognostic implication of the tumor location according to molecular subtypes in axillary lymph node-positive invasive ductal cancer in a Korean population. Breast Cancer Res Treat, 2016, 156(3): 473-483.
36.	Sarp S, Fioretta G, Verkooijen HM, et al. Tumor location of the lower-inner quadrant is associated with an impaired survival for women with early-stage breast cancer. Ann Surg Oncol, 2007, 14(3): 1031-1039.
37.	Shahar KH, Buchholz TA, Delpassand E, et al. Lower and central tumor location correlates with lymphoscintigraphy drainage to the internal mammary lymph nodes in breast carcinoma. Cancer, 2005, 103(7): 1323-1329.
38.	Veronesi U, Marubini E, Mariani L, et al. The dissection of internal mammary nodes does not improve the survival of breast cancer patients. 30-year results of a randomised trial. Eur J Cancer, 1999, 35(9): 1320-1325.
39.	Jayasinghe UW, Boyages J. Tumour location is not an independent prognostic factor for survival following a diagnosis of breast cancer. Breast, 2009, 18(1): 41-46.
40.	Lewis EI, Ozonoff A, Nguyen CP, et al. Breast cancer close to the nipple: does this increase the risk of nodal metastasis at diagnosis. Can Assoc Radiol J, 2011, 62(3): 209-214.
41.	Braverman IM, Keh A, Goldminz D. Correlation of laser Doppler wave patterns with underlying microvascular anatomy. J Invest Dermatol, 1990, 95(3): 283-286.
42.	Nimboriboonporn A, Chuthapisith S. Nipple-areola complex reconstruction. Gland Surg, 2014, 3(1): 35-42.
43.	Hauben DJ, Adler N, Silfen R, et al. Breast-areola-nipple proportion. Ann Plast Surg, 2003, 50(5): 510-513.
44.	Thomassin-Naggara I, Tardivon A, Chopier J. Standardized diagnosis and reporting of breast cancer. Diagn Interv Imaging, 2014, 95(7-8): 759-766.
45.	Irshad A, Leddy R, Pisano E, et al. Assessing the role of ultrasound in predicting the biological behavior of breast cancer. AJR Am J Roentgenol, 2013, 200(2): 284-290.
46.	Gundry KR. Breast ultrasound: indications and findings. Clin Obstet Gynecol, 2016, 59(2): 380-393.
47.	Caan BJ, Cespedes Feliciano EM, Prado CM, et al. Association of muscle and adiposity measured by computed tomography with survival in patients with nonmetastatic breast cancer. JAMA Oncol, 2018, 4(6): 798-804.
48.	Iwase T, Sangai T, Nagashima T, et al. Impact of body fat distribution on neoadjuvant chemotherapy outcomes in advanced breast cancer patients. Cancer Med, 2016, 5(1): 41-48.
49.	Greenlee H, Unger JM, LeBlanc M, et al. Association between body mass index and cancer survival in a pooled analysis of 22 clinical trials. Cancer Epidemiol Biomarkers Prev, 2017, 26(1): 21-29.
50.	Ali MA, Czene K, Eriksson L, et al. Breast tissue organisation and its association with breast cancer risk. Breast Cancer Res, 2017, 19(1): 103.
51.	Chen YW, Lai YC, Hsu CC, et al. Value of nodal drainage patterns and tumor location from lymphoscintigraphic mapping in detecting axillary sentinel lymph node status in breast cancer: experience at Kaohsiung Medical University Hospital. Kaohsiung J Med Sci, 2005, 21(6): 251-257.
52.	Kroman N, Wohlfahrt J, Mouridsen HT, et al. Influence of tumor location on breast cancer prognosis. Int J Cancer, 2003, 105(4): 542-545.
53.	Grobmyer SR, Djohan R. Comments on " Primary tumor location predicts the site of local relapse after nipple-areola complex (NAC) sparing mastectomy” by Cont et al. Breast Cancer Res Treat, 2017. Breast Cancer Res Treat, 2017, 166(1): 323-324.

1. Harlow SP, Krag DN, Julian TB, et al. Prerandomization surgical training for the national surgical adjuvant breast and bowel project (NSABP) B-32 trial: a randomized phase Ⅲ clinical trial to compare sentinel node resection to conventional axillary dissection in clinically node-negative breast cancer. Ann Surg, 2005, 241(1): 48-54.
2. Galimberti V, Cole BF, Zurrida S, et al. Axillary dissection versus no axillary dissection in patients with sentinel-node micrometastases (IBCSG 23-01): a phase 3 randomised controlled trial. Lancet Oncol, 2013, 14(4): 297-305.
3. Caudle AS, Hunt KK, Tucker SL, et al. American College of Surgeons Oncology Group (ACOSOG) Z0011: impact on surgeon practice patterns. Ann Surg Oncol, 2012, 19(10): 3144-3151.
4. Donker M, van Tienhoven G, Straver ME, et al. Radiotherapy or surgery of the axilla after a positive sentinel node in breast cancer (EORTC 10981-22023 AMAROS): a randomised, multicentre, open-label, phase 3 non-inferiority trial. Lancet Oncol, 2014, 15(12): 1303-1310.
5. Eom YH, Kim EJ, Chae BJ, et al. The distance between breast cancer and the skin is associated with axillary nodal metastasis. J Surg Oncol, 2015, 111(7): 824-828.
6. Manca G, Tardelli E, Rubello D, et al. Sentinel lymph node biopsy in breast cancer: a technical and clinical appraisal. Nucl Med Commun, 2016, 37(6): 570-576.
7. Zhang L, Huang Y, Yang C, et al. Application of a carbon nanoparticle suspension for sentinel lymph node mapping in patients with early breast cancer: a retrospective cohort study. World J Surg Oncol, 2018, 16(1): 112.
8. Kim GR, Choi JS, Han BK, et al. Preoperative axillary US in early-stage breast cancer: potential to prevent unnecessary axillary lymph node dissection. Radiology, 2018, 288(1): 55-63.
9. Gentilini O, Veronesi U. Abandoning sentinel lymph node biopsy in early breast cancer? A new trial in progress at the European Institute of Oncology of Milan (SOUND: Sentinel node vs Observation after axillary UltraSouND). Breast, 2012, 21(5): 678-681.
10. Huang TW, Kuo KN, Chen KH, et al. Recommendation for axillary lymph node dissection in women with early breast cancer and sentinel node metastasis: a systematic review and meta-analysis of randomized controlled trials using the GRADE system. Int J Surg, 2016, 34: 73-80.
11. Torre LA, Islami F, Siegel RL, et al. Global cancer in women: burden and trends. Cancer Epidemiol Biomarkers Prev, 2017, 26(4): 444-457.
12. Zheng A, Duan W, Zhang L, et al. How great is current curative expenditure and catastrophic health expenditure among patients with cancer in China? A research based on " System of Health Account 2011”. Cancer Med, 2018, 7(8): 4036-4043.
13. Skinner KA, Silberman H, Sposto R, et al. Palpable breast cancers are inherently different from nonpalpable breast cancers. Ann Surg Oncol, 2001, 8(9): 705-710.
14. Shayan R, Inder R, Karnezis T, et al. Tumor location and nature of lymphatic vessels are key determinants of cancer metastasis. Clin Exp Metastasis, 2013, 30(3): 345-356.
15. Ryan T. The ageing of the blood supply and the lymphatic drainage of the skin. Micron, 2004, 35(3): 161-171.
16. Moore JE Jr, Bertram CD. Lymphatic system flows. Annu Rev Fluid Mech, 2018, 50: 459-482.
17. Dawood S, Merajver SD, Viens P, et al. International expert panel on inflammatory breast cancer: consensus statement for standardized diagnosis and treatment. Ann Oncol, 2011, 22(3): 515-523.
18. Redig AJ, McAllister SS. Breast cancer as a systemic disease: a view of metastasis. J Intern Med, 2013, 274(2): 113-126.
19. 王静文, 唐建武, 赵君怡. VEGFC/D-VEGFR3/NRP2 轴通路相关分子在肿瘤及其淋巴道转移时的变化与意义. 现代肿瘤医学, 2016, 24(17): 2808-2811.
20. Deng Y, Zhang X, Simons M. Molecular controls of lymphatic VEGFR3 signaling. Arterioscler Thromb Vasc Biol, 2015, 35(2): 421-429.
21. Pepper MS, Skobe M. Lymphatic endothelium: morphological, molecular and functional properties. J Cell Biol, 2003, 163(2): 209-213.
22. Smith KJ, Jones PF, Burke DA, et al. Lymphatic vessel distribution in the mucosa and submucosa and potential implications for T1 colorectal tumors. Dis Colon Rectum, 2011, 54(1): 35-40.
23. Eccles SA, Welch DR. Metastasis: recent discoveries and novel treatment strategies. Lancet, 2007, 369(9574): 1742-1757.
24. He Y, Rajantie I, Pajusola K, et al. Vascular endothelial cell growth factor receptor 3-mediated activation of lymphatic endothelium is crucial for tumor cell entry and spread via lymphatic vessels. Cancer Res, 2005, 65(11): 4739-4746.
25. Karpanen T, Egeblad M, Karkkainen MJ, et al. Vascular endothelial growth factor C promotes tumor lymphangiogenesis and intralymphatic tumor growth. Cancer Res, 2001, 61(5): 1786-1790.
26. Cunningham JE, Jurj AL, Oman L, et al. Is risk of axillary lymph node metastasis associated with proximity of breast cancer to the skin. Breast Cancer Res Treat, 2006, 100(3): 319-328.
27. Bae MS, Shin SU, Song SE, et al. Association between US features of primary tumor and axillary lymph node metastasis in patients with clinical T1-T2N0 breast cancer. Acta Radiol, 2018, 59(4): 402-408.
28. Ansari B, Morton MJ, Adamczyk DL, et al. Distance of breast cancer from the skin and nipple impacts axillary nodal metastases. Ann Surg Oncol, 2011, 18(11): 3174-3180.
29. Siotos C, McColl M, Psoter K, et al. Tumor site and breast cancer prognosis. Clin Breast Cancer, 2018, 18(5): e1045-e1052.
30. Sohn VY, Arthurs ZM, Sebesta JA, et al. Primary tumor location impacts breast cancer survival. Am J Surg, 2008, 195(5): 641-644.
31. Chan S, Chen JH, Li S, et al. Evaluation of the association between quantitative mammographic density and breast cancer occurred in different quadrants. BMC Cancer, 2017, 17(1): 274.
32. Bevilacqua J, Cody H 3rd, MacDonald KA, et al. A prospective validated model for predicting axillary node metastases based on 2,000 sentinel node procedures: the role of tumour location. Eur J Surg Oncol, 2002, 28(5): 490-500.
33. Wu S, Zhou J, Ren Y, et al. Tumor location is a prognostic factor for survival of Chinese women with T1-2N0M0 breast cancer. Int J Surg, 2014, 12(5): 394-398.
34. Colleoni M, Zahrieh D, Gelber RD, et al. Site of primary tumor has a prognostic role in operable breast cancer: the international breast cancer study group experience. J Clin Oncol, 2005, 23(7): 1390-1400.
35. Lim ST, Choi JE, Kim SJ, et al. Prognostic implication of the tumor location according to molecular subtypes in axillary lymph node-positive invasive ductal cancer in a Korean population. Breast Cancer Res Treat, 2016, 156(3): 473-483.
36. Sarp S, Fioretta G, Verkooijen HM, et al. Tumor location of the lower-inner quadrant is associated with an impaired survival for women with early-stage breast cancer. Ann Surg Oncol, 2007, 14(3): 1031-1039.
37. Shahar KH, Buchholz TA, Delpassand E, et al. Lower and central tumor location correlates with lymphoscintigraphy drainage to the internal mammary lymph nodes in breast carcinoma. Cancer, 2005, 103(7): 1323-1329.
38. Veronesi U, Marubini E, Mariani L, et al. The dissection of internal mammary nodes does not improve the survival of breast cancer patients. 30-year results of a randomised trial. Eur J Cancer, 1999, 35(9): 1320-1325.
39. Jayasinghe UW, Boyages J. Tumour location is not an independent prognostic factor for survival following a diagnosis of breast cancer. Breast, 2009, 18(1): 41-46.
40. Lewis EI, Ozonoff A, Nguyen CP, et al. Breast cancer close to the nipple: does this increase the risk of nodal metastasis at diagnosis. Can Assoc Radiol J, 2011, 62(3): 209-214.
41. Braverman IM, Keh A, Goldminz D. Correlation of laser Doppler wave patterns with underlying microvascular anatomy. J Invest Dermatol, 1990, 95(3): 283-286.
42. Nimboriboonporn A, Chuthapisith S. Nipple-areola complex reconstruction. Gland Surg, 2014, 3(1): 35-42.
43. Hauben DJ, Adler N, Silfen R, et al. Breast-areola-nipple proportion. Ann Plast Surg, 2003, 50(5): 510-513.
44. Thomassin-Naggara I, Tardivon A, Chopier J. Standardized diagnosis and reporting of breast cancer. Diagn Interv Imaging, 2014, 95(7-8): 759-766.
45. Irshad A, Leddy R, Pisano E, et al. Assessing the role of ultrasound in predicting the biological behavior of breast cancer. AJR Am J Roentgenol, 2013, 200(2): 284-290.
46. Gundry KR. Breast ultrasound: indications and findings. Clin Obstet Gynecol, 2016, 59(2): 380-393.
47. Caan BJ, Cespedes Feliciano EM, Prado CM, et al. Association of muscle and adiposity measured by computed tomography with survival in patients with nonmetastatic breast cancer. JAMA Oncol, 2018, 4(6): 798-804.
48. Iwase T, Sangai T, Nagashima T, et al. Impact of body fat distribution on neoadjuvant chemotherapy outcomes in advanced breast cancer patients. Cancer Med, 2016, 5(1): 41-48.
49. Greenlee H, Unger JM, LeBlanc M, et al. Association between body mass index and cancer survival in a pooled analysis of 22 clinical trials. Cancer Epidemiol Biomarkers Prev, 2017, 26(1): 21-29.
50. Ali MA, Czene K, Eriksson L, et al. Breast tissue organisation and its association with breast cancer risk. Breast Cancer Res, 2017, 19(1): 103.
51. Chen YW, Lai YC, Hsu CC, et al. Value of nodal drainage patterns and tumor location from lymphoscintigraphic mapping in detecting axillary sentinel lymph node status in breast cancer: experience at Kaohsiung Medical University Hospital. Kaohsiung J Med Sci, 2005, 21(6): 251-257.
52. Kroman N, Wohlfahrt J, Mouridsen HT, et al. Influence of tumor location on breast cancer prognosis. Int J Cancer, 2003, 105(4): 542-545.
53. Grobmyer SR, Djohan R. Comments on " Primary tumor location predicts the site of local relapse after nipple-areola complex (NAC) sparing mastectomy” by Cont et al. Breast Cancer Res Treat, 2017. Breast Cancer Res Treat, 2017, 166(1): 323-324.

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The association between cancer location and lymph node metastasis in early stage of breast cancer

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