Article Data

  • Views 808
  • Dowloads 151

Original Research

Open Access

Characteristics and prognosis of young breast cancer patients with low expression of estrogen receptor

  • Shuaibing Wang1
  • Yang Li2,3,4
  • Xiuheng Qi1
  • Hong Liu2,3,4,*,

1Hebei Petrochina Central Hospital, 065000 Langfang, Hebei, Chin

2Tianjin Medical University Cancer Institute and Hospital, National Clinical Research Center for Cancer, 300060 Tianjin, China

3Tianjin Key Laboratory of Cancer Prevention and Therapy, 300060 Tianjin, China

4Tianjin’s Clinical Research Center for Cancer, 300060 Tianjin, China

DOI: 10.22514/ejgo.2023.022 Vol.44,Issue 2,April 2023 pp.50-57

Submitted: 23 June 2022 Accepted: 22 September 2022

Published: 15 April 2023

*Corresponding Author(s): Hong Liu E-mail:


To evaluate the clinical characteristics and prognosis of young breast cancer patients with an ER of 1%–10%. Breast cancer patients aged ≤35 years old were selected and classified into three groups, ER-negative group, ER-low positive group (ER positivity: 1%–10%) and ER-high positive group (ER positivity: ≥10%), to compare their clinicopathological characteristics and prognosis. Of the 1387 patients assessed, 30.4% were ER-negative, 4.3% were ER-low positive, and 65.3% were ER-high positive. There was no difference in age, Tumor Node Metastasis (TNM) stage, histological type, adjuvant chemotherapy and adjuvant radiation therapy among the three groups (p > 0.05). A higher histological grade and greater Human Epidermal Growth Factor Receptor-2 (HER-2) positivity were observed in the ER-low positive group than in the ER-high positive group (p < 0.001). The number of patients with Progesterone Receptor (PR) negative in the ER-low positive group was between the other two groups. The recurrence rate of breast cancer in the ER-low positive group was 27.1%, which was similar to that of the ER-negative group (28%; p > 0.05) but higher than the ER-high positive group (21.4%; p = 0.03). After a median follow-up of 74 months, the ER-high positive group had the longest Disease Free Survival (DFS) compared with the ER-negative group (p < 0.0001) and ER-low positive group (p < 0.05), while there was no significant difference in DFS between the latter two groups (p = 0.73). Similarly, the ER-high positive group had the longest Overall Survival (OS) than the ER-negative group (p < 0.0001) and the ER-low positive group (p < 0.05), while there was no statistical difference in OS between the latter two groups (p = 0.77). After endocrine therapy, no improvement in DFS (p = 0.71) and OS (p = 0.54) was observed in the ER-low positive group. In young breast cancer patients, the clinicopathological characteristics of the ER-low positive group were different from the ER-high positive group but were more similar to the ER-negative group. The DFS and OS were shorter than the ER-high group, and despite receiving endocrine therapy, DFS and OS of the ER-low positive group were not significantly prolonged.


Breast cancer; Young age; Estrogen receptor; Low positive; Survival

Cite and Share

Shuaibing Wang,Yang Li,Xiuheng Qi,Hong Liu. Characteristics and prognosis of young breast cancer patients with low expression of estrogen receptor. European Journal of Gynaecological Oncology. 2023. 44(2);50-57.


[1] Han JG, Jiang YD, Zhang CH, Pang D, Zhang M, Wang YB, et al. Clinicopathologic characteristics and prognosis of young patients with breast cancer. Breast. 2011; 20: 370–372.

[2] Fredholm H, Eaker S, Frisell J, Holmberg L, Fredriksson I, Lindman H. Breast cancer in young women: poor survival despite intensive treatment. PLoS One. 2009; 4: e7695.

[3] Yi M, Huo L, Koenig KB, Mittendorf EA, Meric-Bernstam F, Kuerer HM, et al. Which threshold for ER positivity? A retrospective study based on 9639 patients. Annals of Oncology. 2014; 25: 1004–1011.

[4] Fidler MM, Gupta S, Soerjomataram I, Ferlay J, Steliarova-Foucher E, Bray F. Cancer incidence and mortality among young adults aged 20–39 years worldwide in 2012: a population-based study. The Lancet Oncology. 2017; 18: 1579–1589.

[5] Hariharan N, Rao TS, Naidu CK, Raju KVVN, Rajappa S, Ayyagari S, et al. The Impact of stage and molecular subtypes on survival outcomes in young women with breast cancer. Journal of Adolescent and Young Adult Oncology. 2019; 8: 628–634.

[6] Fu J, Zhong C, Wu L, Li D, Xu T, Jiang T, et al. Young patients with hormone receptor-positive breast cancer have a higher long-term risk of breast cancer specific death. Journal of Breast Cancer. 2019; 22: 96–108.

[7] Martínez MT, Oltra SS, Peña-Chilet M, Alonso E, Hernando C, Burgues O, et al. Breast cancer in very young patients in a spanish cohort: age as an independent bad prognostic indicator. Breast Cancer. 2019; 13: 1–10.

[8] Fleming G, Francis PA, Láng I, Ciruelos EM, Bellet M, Bonnefoi HR, et al. Randomized comparison of adjuvant tamoxifen (T) plus ovarian function suppression (OFS) versus tamoxifen in premenopausal women with hormone receptor-positive (HR+) early breast cancer (BC): Update of the SOFT trial. San Antonio Breast Cancer Symposium: San Antonio, TX, USA. 2017.

[9] Pagani O, Regan MM, Fleming GF, Walley BA, Colleoni M, Láng I, et al. Randomized comparison of adjuvant aromatase inhibitor exemestane (E) plus ovarian function suppression (OFS) vs tamoxifen (T) plus OFS in premenopausal women with hormone receptor positive (HR+) early breast cancer (BC): update of the combined TEXT and SOFT trials. San Antonio Breast Cancer Symposium: San Antonio, TX, USA. 2017.

[10] Dellapasqua S, Gray KP, Munzone E, Rubino D, Gianni L, Johansson H, et al. Neoadjuvant degarelix versus triptorelin in premenopausal patients who receive letrozole for locally advanced endocrine-responsive breast cancer: a randomized phase II trial. Journal of Clinical Oncology. 2019; 37: 386–395.

[11] Hammond MEH, Hayes DF, Wolff AC, Mangu PB, Temin S. American society of clinical oncology/college of american pathologists guideline recommendations for immunohistochemical testing of estrogen and progesterone receptors in breast cancer. Journal of Oncology Practice. 2010; 6: 195–197.

[12] Harvey JM, Clark GM, Osborne CK, Allred DC. Estrogen receptor status by immunohistochemistry is superior to the ligand-binding assay for predicting response to adjuvant endocrine therapy in breast cancer. Journal of Clinical Oncology. 1999; 17: 1474–1481.

[13] Morgan DAL, Refalo NA, Cheung KL. Strength of ER-positivity in relation to survival in ER-positive breast cancer treated by adjuvant tamoxifen as sole systemic therapy. The Breast. 2011; 20: 215–219.

[14] Landmann A, Farrugia DJ, Zhu L, Diego EJ, Johnson RR, Soran A, et al. Low estrogen receptor (ER)-positive breast cancer and neoadjuvant systemic chemotherapy: is response similar to typical ER-positive or ER-negative disease? American Journal of Clinical Pathology. 2018; 150: 34–42.

[15] Shoemaker ML, White MC, Wu M, Weir HK, Romieu I. Differences in breast cancer incidence among young women aged 20–49 years by stage and tumor characteristics, age, race, and ethnicity, 2004–2013. Breast Cancer Research and Treatment. 2018; 169: 595–606.

[16] Ruggeri M, Pagan E, Bagnardi V, Bianco N, Gallerani E, Buser K, et al. Fertility concerns, preservation strategies and quality of life in young women with breast cancer: baseline results from an ongoing prospective cohort study in selected European centers. The Breast. 2019; 47: 85–92.

[17] Chen HL, Zhou MQ, Tian W, Meng KX, He HF. Effect of age on breast cancer patient prognoses: a population-based study using the SEER 18 database. PLoS One. 2016; 11: e0165409.

[18] Paluch-Shimon S, Cardoso F, Partridge AH, Abulkhair O, Azim HA, Bianchi-Micheli G, et al. ESO-ESMO 4th international consensus guidelines for Breast Cancer in Young Women (BCY4). Annals of Oncology. 2020; 31: 674–696.

[19] Han W, Kang SY; Korean Breast Cancer Society. Relationship between age at diagnosis and outcome of premenopausal breast cancer: age less than 35 years is a reasonable cut-off for defining young age-onset breast cancer. Breast Cancer Research and Treatment. 2010; 119: 193–200.

[20] Francis PA, Pagani O, Fleming GF, Walley BA, Colleoni M, Láng I, et al. Tailoring adjuvant endocrine therapy for premenopausal breast cancer. The New England Journal of Medicine. 2018; 379: 122–137.

[21] Raghav KPS, Hernandez-Aya LF, Lei X, Chavez-MacGregor M, Meric-Bernstam F, Buchholz TA, et al. Impact of low estrogen/progesterone receptor expression on survival outcomes in breast cancers previously classified as triple negative breast cancers. Cancer. 2012; 118: 1498–1506.

[22] Fujii T, Kogawa T, Dong W, Sahin AA, Moulder S, Litton JK, et al. Revisiting the definition of estrogen receptor positivity in ER2-negative primary breast cancer. Annals of Oncology. 2017; 28: 2420–2428.

[23] Deyarmin B, Kane JL, Valente AL, van Laar R, Gallagher C, Shriver CD, et al. Effect of ASCO/CAP guidelines for determining ER status on molecular subtype. Annals of Surgical Oncology. 2013; 20: 87–93.

[24] Plichta JK, Rai U, Tang R, Coopey SB, Buckley JM, Gadd MA, et al. Factors associated with recurrence rates and long-term survival in women diagnosed with breast cancer ages 40 and younger. Annals of Surgical Oncology. 2016; 23: 3212–3220.

[25] American Cancer Society. Breast Cancer Facts & Figures 2015–2016. American Cancer Society, Inc.: Atlanta. 2015.

[26] Goldhirsch A, Glick JH, Gelber RD, Coates AS, Thürlimann B, Senn HJ. Meeting highlights: international expert consensus on the primary therapy of early breast cancer 2005. Annals of Oncology. 2005; 16: 1569–1583.

[27] Prabhu JS, Korlimarla A, Desai K, Alexander A, Raghavan R, Anupama C, et al. A majority of low (1–10%) ER positive breast cancers behave like hormone receptor negative tumors. Journal of Cancer. 2014; 5: 156–165.

Abstracted / indexed in

Science Citation Index Expanded (SciSearch) Created as SCI in 1964, Science Citation Index Expanded now indexes over 9,500 of the world’s most impactful journals across 178 scientific disciplines. More than 53 million records and 1.18 billion cited references date back from 1900 to present.

Biological Abstracts Easily discover critical journal coverage of the life sciences with Biological Abstracts, produced by the Web of Science Group, with topics ranging from botany to microbiology to pharmacology. Including BIOSIS indexing and MeSH terms, specialized indexing in Biological Abstracts helps you to discover more accurate, context-sensitive results.

Google Scholar Google Scholar is a freely accessible web search engine that indexes the full text or metadata of scholarly literature across an array of publishing formats and disciplines.

JournalSeek Genamics JournalSeek is the largest completely categorized database of freely available journal information available on the internet. The database presently contains 39226 titles. Journal information includes the description (aims and scope), journal abbreviation, journal homepage link, subject category and ISSN.

Current Contents - Clinical Medicine Current Contents - Clinical Medicine provides easy access to complete tables of contents, abstracts, bibliographic information and all other significant items in recently published issues from over 1,000 leading journals in clinical medicine.

BIOSIS Previews BIOSIS Previews is an English-language, bibliographic database service, with abstracts and citation indexing. It is part of Clarivate Analytics Web of Science suite. BIOSIS Previews indexes data from 1926 to the present.

Journal Citation Reports/Science Edition Journal Citation Reports/Science Edition aims to evaluate a journal’s value from multiple perspectives including the journal impact factor, descriptive data about a journal’s open access content as well as contributing authors, and provide readers a transparent and publisher-neutral data & statistics information about the journal.

Submission Turnaround Time