{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,11,25]],"date-time":"2025-11-25T20:28:16Z","timestamp":1764102496772},"reference-count":25,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2009,9,24]],"date-time":"2009-09-24T00:00:00Z","timestamp":1253750400000},"content-version":"unspecified","delay-in-days":0,"URL":"http:\/\/www.springer.com\/tdm"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["BMC Cancer"],"published-print":{"date-parts":[[2009,12]]},"abstract":"<jats:title>Abstract<\/jats:title>\n          <jats:sec>\n            <jats:title>Background<\/jats:title>\n            <jats:p>It has been reported that triple negative phenotype is characterized by aggressive clinical history in Western breast cancer patients, however its pattern of metastatic spread had never been reported in the Chinese population. Considering racial disparities, we sought to analyze the spread pattern for different sites of first recurrence in Chinese triple negative breast cancers.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Methods<\/jats:title>\n            <jats:p>A retrospective study of 1662 patients was carried out from a large database of breast cancer patients undergoing surgery between January 1, 2000 and March 31, 2004 at the Cancer Hospital, Fudan University, Shanghai, China. Survival curves were generated using the Kaplan-Meier method and annual relapse hazards were estimated by the hazard function.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Results<\/jats:title>\n            <jats:p>We found a statistically significant difference in relapse-free survival (RFS) for locoregional and visceral recurrence (<jats:italic>P<\/jats:italic> = 0.007 and <jats:italic>P<\/jats:italic> = 0.025, respectively) among the triple negative, ERBB2+ and HR+\/ERBB2- subgroups in univariate analysis. In the multivariate Cox proportional hazards regression analysis, RFS for either locoregional or visceral relapse in the triple negative category was inferior to that in HR+\/ERBB2- patients (<jats:italic>P<\/jats:italic> = 0.027 and <jats:italic>P<\/jats:italic> = 0.005, respectively), but comparable to that in ERBB2+ women (both <jats:italic>P<\/jats:italic> &gt; <jats:italic>0.05<\/jats:italic>). Furthermore, the early relapse peak appeared later in the triple negative group than that in the ERBB2+ counterpart for both locoregional and visceral relapse. On the other hand, when compared with triple negative breast cancers, a significantly lower risk of developing bone relapse was discerned for ERBB2+ women (<jats:italic>P<\/jats:italic> = 0.048; HR = 0.384, 95% CI 0.148-0.991), with the borderline significance for HR+\/ERBB2- breast cancers (<jats:italic>P<\/jats:italic> = 0.058; HR = 0.479, 95% CI 0.224-1.025). In terms of bone metastasis, the hazard rate remained higher for the triple negative category than that for the ERBB2+ subtype.<\/jats:p>\n          <\/jats:sec>\n          <jats:sec>\n            <jats:title>Conclusion<\/jats:title>\n            <jats:p>Based on the site-specific spread pattern in different subgroups, the triple negative category of breast cancers in the Chinese population exhibits a different pattern of relapse, which indicates that different organotropism may be due to the different intrinsic subtypes. A better knowledge of the triple negative category is warranted for efficacious systemic regimens to decrease and\/or delay the relapse hazard.<\/jats:p>\n          <\/jats:sec>","DOI":"10.1186\/1471-2407-9-342","type":"journal-article","created":{"date-parts":[[2009,9,24]],"date-time":"2009-09-24T18:15:06Z","timestamp":1253816106000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":27,"title":["Site-specific relapse pattern of the triple negative tumors in Chinese breast cancer patients"],"prefix":"10.1186","volume":"9","author":[{"given":"Yanping","family":"Lin","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Wenjin","family":"Yin","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Tingting","family":"Yan","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Liheng","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Genhong","family":"Di","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiong","family":"Wu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhenzhou","family":"Shen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Zhimin","family":"Shao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jinsong","family":"Lu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2009,9,24]]},"reference":[{"issue":"14","key":"1676_CR1","doi-asserted-by":"publisher","first-page":"8418","DOI":"10.1073\/pnas.0932692100","volume":"100","author":"T Sorlie","year":"2003","unstructured":"Sorlie T, Tibshirani R, Parker J, Hastie T, Marron JS, Nobel A, Deng S, Johnsen H, Pesich R, Geisler S, et al: Repeated observation of breast tumor subtypes in independent gene expression data sets. Proc Natl Acad Sci USA. 2003, 100 (14): 8418-8423. 10.1073\/pnas.0932692100.","journal-title":"Proc Natl Acad Sci USA"},{"key":"1676_CR2","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/S1470-2045(07)70074-8","volume":"8","author":"S Cleator","year":"2007","unstructured":"Cleator S, Heller W, Coombes RC: Triple-negative breast cancer: therapeutic options. Lancet Oncol. 2007, 8: 235-244. 10.1016\/S1470-2045(07)70074-8.","journal-title":"Lancet Oncol"},{"issue":"21","key":"1676_CR3","doi-asserted-by":"publisher","first-page":"2492","DOI":"10.1001\/jama.295.21.2492","volume":"295","author":"LA Carey","year":"2006","unstructured":"Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, Karaca G, Troester MA, Tse CK, Edmiston S, et al: Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006, 295 (21): 2492-2502. 10.1001\/jama.295.21.2492.","journal-title":"JAMA"},{"issue":"2","key":"1676_CR4","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1007\/s10549-008-0096-0","volume":"115","author":"WJ Yin","year":"2009","unstructured":"Yin WJ, Lu JS, Di GH, Lin YP, Zhou LH, Liu GY, Wu J, Shen KW, Han QX, Shen ZZ, et al: Clinicopathological features of the triple-negative tumors in Chinese breast cancer patients. Breast Cancer Res Treat. 2009, 115 (2): 325-333. 10.1007\/s10549-008-0096-0.","journal-title":"Breast Cancer Res Treat"},{"issue":"Suppl 2","key":"1676_CR5","doi-asserted-by":"publisher","first-page":"S72","DOI":"10.1016\/j.breast.2007.07.017","volume":"16","author":"J Kurebayashi","year":"2007","unstructured":"Kurebayashi J, Moriya T, Ishida T, Hirakawa H, Kurosumi M, Akiyama F, Kinoshita T, Takei H, Takahashi K, Ikeda M, et al: The prevalence of intrinsic subtypes and prognosis in breast cancer patients of different races. Breast. 2007, 16 (Suppl 2): S72-77. 10.1016\/j.breast.2007.07.017.","journal-title":"Breast"},{"key":"1676_CR6","volume-title":"American Society of Clinical Oncology Annual Meeting: 5-8 June 2004; New Orleans, Louisiana, USA","author":"OI Olopade","year":"2004","unstructured":"Olopade OI, Ikpatt FO, Dignam JJ, Khramtsov A, Tetriakova M, Grushko T, Fackenthal J, Nanda R, Ndoma-Egba R, CM P: \"Intrinsic Gene Expression\" subtypes correlated with grade and morphometric parameters reveal a high proportion of aggressive basal-like tumors among black women of African ancestry. American Society of Clinical Oncology Annual Meeting: 5-8 June 2004; New Orleans, Louisiana, USA. 2004"},{"key":"1676_CR7","first-page":"2329","volume":"15","author":"LA Carey","year":"2004","unstructured":"Carey LA, Dees EC, Sawyer L, Gatti L, Moore DT, Collichio F, Ollila DW, Sartor CI, Graham ML, CM P: The triple negative paradox: primary tumor chemosensitivity of breast cancer subtypes. Clin Cancer Res. 2004, 15: 2329-2334.","journal-title":"Clin Cancer Res"},{"issue":"16","key":"1676_CR8","doi-asserted-by":"publisher","first-page":"5367","DOI":"10.1158\/1078-0432.CCR-04-0220","volume":"10","author":"TO Nielsen","year":"2004","unstructured":"Nielsen TO, Hsu FD, Jensen K, Cheang M, Karaca G, Hu Z, Hernandez-Boussard T, Livasy C, Cowan D, Dressler L, et al: Immunohistochemical and clinical characterization of the basal-like subtype of invasive breast carcinoma. Clin Cancer Res. 2004, 10 (16): 5367-5374. 10.1158\/1078-0432.CCR-04-0220.","journal-title":"Clin Cancer Res"},{"issue":"19","key":"1676_CR9","doi-asserted-by":"publisher","first-page":"10869","DOI":"10.1073\/pnas.191367098","volume":"98","author":"T Sorlie","year":"2001","unstructured":"Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, Rijn van de M, Jeffrey SS, et al: Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA. 2001, 98 (19): 10869-10874. 10.1073\/pnas.191367098.","journal-title":"Proc Natl Acad Sci USA"},{"issue":"9","key":"1676_CR10","doi-asserted-by":"publisher","first-page":"1721","DOI":"10.1002\/cncr.22618","volume":"109","author":"KR Bauer","year":"2007","unstructured":"Bauer KR, Brown M, Cress RD, Parise CA, Caggiano V: Descriptive analysis of estrogen receptor (ER)-negative, progesterone receptor (PR)-negative, and HER2-negative invasive breast cancer, the so-called triple-negative phenotype: a population-based study from the California cancer Registry. Cancer. 2007, 109 (9): 1721-1728. 10.1002\/cncr.22618.","journal-title":"Cancer"},{"issue":"15 Pt 1","key":"1676_CR11","doi-asserted-by":"publisher","first-page":"4429","DOI":"10.1158\/1078-0432.CCR-06-3045","volume":"13","author":"R Dent","year":"2007","unstructured":"Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, Lickley LA, Rawlinson E, Sun P, Narod SA: Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007, 13 (15 Pt 1): 4429-4434. 10.1158\/1078-0432.CCR-06-3045.","journal-title":"Clin Cancer Res"},{"issue":"7","key":"1676_CR12","doi-asserted-by":"publisher","first-page":"729","DOI":"10.1136\/jcp.2005.033043","volume":"59","author":"S Banerjee","year":"2006","unstructured":"Banerjee S, Reis-Filho JS, Ashley S, Steele D, Ashworth A, Lakhani SR, Smith IE: Basal-like breast carcinomas: clinical outcome and response to chemotherapy. J Clin Pathol. 2006, 59 (7): 729-735. 10.1136\/jcp.2005.033043.","journal-title":"J Clin Pathol"},{"issue":"5","key":"1676_CR13","doi-asserted-by":"publisher","first-page":"1533","DOI":"10.1158\/1078-0432.CCR-05-2281","volume":"12","author":"SM Rodriguez-Pinilla","year":"2006","unstructured":"Rodriguez-Pinilla SM, Sarrio D, Honrado E, Hardisson D, Calero F, Benitez J, Palacios J: Prognostic significance of basal-like phenotype and fascin expression in node-negative invasive breast carcinomas. Clin Cancer Res. 2006, 12 (5): 1533-1539. 10.1158\/1078-0432.CCR-05-2281.","journal-title":"Clin Cancer Res"},{"key":"1676_CR14","volume-title":"the 49th American Society for Therapeutic Radiology and Oncology (ASTRO) Annual Meeting: 28 October-1 November 2007; Los Angeles, California, USA","author":"BW Chang","year":"2007","unstructured":"Chang BW, Decker RH, Haffy BG, et al: Incidence of brain metastases in early-stage triple negative breast cancer patients. the 49th American Society for Therapeutic Radiology and Oncology (ASTRO) Annual Meeting: 28 October-1 November 2007; Los Angeles, California, USA. 2007"},{"issue":"36","key":"1676_CR15","doi-asserted-by":"publisher","first-page":"5652","DOI":"10.1200\/JCO.2006.06.5664","volume":"24","author":"BG Haffty","year":"2006","unstructured":"Haffty BG, Yang Q, Reiss M, Kearney T, Higgins SA, Weidhaas J, Harris L, Hait W, Toppmeyer D: Locoregional relapse and distant metastasis in conservatively managed triple negative early-stage breast cancer. J Clin Oncol. 2006, 24 (36): 5652-5657. 10.1200\/JCO.2006.06.5664.","journal-title":"J Clin Oncol"},{"issue":"3","key":"1676_CR16","first-page":"923","volume":"9","author":"H Joensuu","year":"2003","unstructured":"Joensuu H, Isola J, Lundin M, Salminen T, Holli K, Kataja V, Pylkkanen L, Turpeenniemi-Hujanen T, von Smitten K, Lundin J: Amplification of erbB2 and erbB2 expression are superior to estrogen receptor status as risk factors for distant recurrence in pT1N0M0 breast cancer: a nationwide population-based study. Clin Cancer Res. 2003, 9 (3): 923-930.","journal-title":"Clin Cancer Res"},{"issue":"2","key":"1676_CR17","doi-asserted-by":"publisher","first-page":"173","DOI":"10.1007\/s10549-004-1722-0","volume":"89","author":"I Jatoi","year":"2005","unstructured":"Jatoi I, Tsimelzon A, Weiss H, Clark GM, Hilsenbeck SG: Hazard rates of recurrence following diagnosis of primary breast cancer. Breast Cancer Res Treat. 2005, 89 (2): 173-178. 10.1007\/s10549-004-1722-0.","journal-title":"Breast Cancer Res Treat"},{"issue":"2","key":"1676_CR18","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1007\/s10549-006-9242-8","volume":"100","author":"LM McShane","year":"2006","unstructured":"McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM: REporting recommendations for tumor MARKer prognostic studies (REMARK). Breast Cancer Res Treat. 2006, 100 (2): 229-235. 10.1007\/s10549-006-9242-8.","journal-title":"Breast Cancer Res Treat"},{"issue":"28","key":"1676_CR19","doi-asserted-by":"publisher","first-page":"7089","DOI":"10.1200\/JCO.2005.08.123","volume":"23","author":"G Gruber","year":"2005","unstructured":"Gruber G, Bonetti M, Nasi ML, Price KN, Castiglione-Gertsch M, Rudenstam CM, Holmberg SB, Lindtner J, Golouh R, Collins J, et al: Prognostic value of extracapsular tumor spread for locoregional control in premenopausal patients with node-positive breast cancer treated with classical cyclophosphamide, methotrexate, and fluorouracil: long-term observations from International Breast Cancer Study Group Trial VI. J Clin Oncol. 2005, 23 (28): 7089-7097. 10.1200\/JCO.2005.08.123.","journal-title":"J Clin Oncol"},{"issue":"1","key":"1676_CR20","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1007\/s10549-007-9756-8","volume":"111","author":"DS Tan","year":"2008","unstructured":"Tan DS, Marchio C, Jones RL, Savage K, Smith IE, Dowsett M, Reis-Filho JS: Triple negative breast cancer: molecular profiling and prognostic impact in adjuvant anthracycline-treated patients. Breast Cancer Res Treat. 2008, 111 (1): 27-44. 10.1007\/s10549-007-9756-8.","journal-title":"Breast Cancer Res Treat"},{"issue":"2","key":"1676_CR21","doi-asserted-by":"publisher","first-page":"423","DOI":"10.1007\/s10549-008-0086-2","volume":"115","author":"R Dent","year":"2009","unstructured":"Dent R, Hanna WM, Trudeau M, Rawlinson E, Sun P, Narod SA: Pattern of metastatic spread in triple-negative breast cancer. Breast Cancer Res Treat. 2009, 115 (2): 423-428. 10.1007\/s10549-008-0086-2.","journal-title":"Breast Cancer Res Treat"},{"issue":"2","key":"1676_CR22","doi-asserted-by":"publisher","first-page":"336","DOI":"10.1038\/bjc.1998.52","volume":"77","author":"RE Coleman","year":"1998","unstructured":"Coleman RE, Smith P, RD R: Clinical course and prognostic factors following bone recurrence from breast cancer. Br J Cancer. 1998, 77 (2): 336-340.","journal-title":"Br J Cancer"},{"issue":"3","key":"1676_CR23","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1023\/A:1006308619659","volume":"59","author":"EF Solomayer","year":"2000","unstructured":"Solomayer EF, Diel IJ, Meyberg GC, Gollan C, G B: Metastatic breast cancer: clinical course, prognosis and therapy related to the first site of metastasis. Breast Cancer Res Treat. 2000, 59 (3): 271-278. 10.1023\/A:1006308619659.","journal-title":"Breast Cancer Res Treat"},{"issue":"5","key":"1676_CR24","doi-asserted-by":"publisher","first-page":"650","DOI":"10.1002\/ijc.2910490504","volume":"49","author":"OP Kallioniemi","year":"1991","unstructured":"Kallioniemi OP, Holli K, Visakorpi T, Koivula T, Helin HH, JJ I: Association of c-erbB-2 protein over-expression with high rate of cell proliferation, increased risk of visceral metastasis and poor long-term survival in breast cancer. Int J Cancer. 1991, 49 (5): 650-655. 10.1002\/ijc.2910490504.","journal-title":"Int J Cancer"},{"issue":"17","key":"1676_CR25","doi-asserted-by":"publisher","first-page":"1254","DOI":"10.1093\/jnci\/dji249","volume":"97","author":"G Arpino","year":"2005","unstructured":"Arpino G, Weiss H, Lee AV, Schiff R, De Placido S, Osborne CK, Elledge RM: Estrogen receptor-positive, progesterone receptor-negative breast cancer: association with growth factor receptor expression and tamoxifen resistance. J Natl Cancer Inst. 2005, 97 (17): 1254-1261.","journal-title":"J Natl Cancer Inst"}],"container-title":["BMC Cancer"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/1471-2407-9-342.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/article\/10.1186\/1471-2407-9-342\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"http:\/\/link.springer.com\/content\/pdf\/10.1186\/1471-2407-9-342","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/1471-2407-9-342.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,9,1]],"date-time":"2021-09-01T02:00:21Z","timestamp":1630461621000},"score":1,"resource":{"primary":{"URL":"https:\/\/bmccancer.biomedcentral.com\/articles\/10.1186\/1471-2407-9-342"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2009,9,24]]},"references-count":25,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2009,12]]}},"alternative-id":["1676"],"URL":"https:\/\/doi.org\/10.1186\/1471-2407-9-342","relation":{},"ISSN":["1471-2407"],"issn-type":[{"value":"1471-2407","type":"electronic"}],"subject":[],"published":{"date-parts":[[2009,9,24]]},"assertion":[{"value":"18 April 2009","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 September 2009","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"24 September 2009","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}}],"article-number":"342"}}