Beyond Triple-Negative: High Prevalence of Quadruple-Negative Breast Cancer in African Americans
Abstract
1. Introduction
2. Materials and Methods
3. Results
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- DeSantis, C.E.; Ma, J.; Goding Sauer, A.; Newman, L.A.; Jemal, A. Breast cancer statistics, 2017, racial disparity in mortality by state. CA Cancer J. Clin. 2017, 67, 439–448. [Google Scholar] [CrossRef] [PubMed]
- Lund, M.J.; Trivers, K.F.; Porter, P.L.; Coates, R.J.; Leyland-Jones, B.; Brawley, O.W.; Flagg, E.W.; O’Regan, R.M.; Gabram, S.G.; Eley, J.W. Race and triple negative threats to breast cancer survival: A population-based study in Atlanta, GA. Breast Cancer Res. Treat. 2009, 113, 357–370. [Google Scholar] [CrossRef] [PubMed]
- Lehmann, B.D.; Bauer, J.A.; Chen, X.; Sanders, M.E.; Chakravarthy, A.B.; Shyr, Y.; Pietenpol, J.A. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J. Clin. Investig. 2011, 121, 2750–2767. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Isakoff, S.J.; Mayer, E.L.; He, L.; Traina, T.A.; Carey, L.A.; Krag, K.J.; Rugo, H.S.; Liu, M.C.; Stearns, V.; Come, S.E.; et al. TBCRC009: A Multicenter Phase II Clinical Trial of Platinum Monotherapy with Biomarker Assessment in Metastatic Triple-Negative Breast Cancer. J. Clin. Oncol. 2015, 33, 1902–1909. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Li, Q.; Li, Q.; Zhang, P.; Yuan, P.; Wang, J.; Ma, F.; Luo, Y.; Fan, Y.; Cai, R.; Xu, B. A phase II study of capecitabine plus cisplatin in metastatic triple-negative breast cancer patients pretreated with anthracyclines and taxanes. Cancer Biol. Ther. 2015, 16, 1746–1753. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Min, A.; Im, S.A.; Kim, D.K.; Song, S.H.; Kim, H.J.; Lee, K.H.; Kim, T.Y.; Han, S.W.; Oh, D.Y.; Kim, T.Y.; et al. Histone deacetylase inhibitor, suberoylanilide hydroxamic acid (SAHA), enhances anti-tumor effects of the poly (ADP-ribose) polymerase (PARP) inhibitor olaparib in triple-negative breast cancer cells. Breast Cancer Res. 2015, 17, 33. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Gross, E.; van Tinteren, H.; Li, Z.; Raab, S.; Meul, C.; Avril, S.; Laddach, N.; Aubele, M.; Propping, C.; Gkazepis, A.; et al. Identification of BRCA1-like triple-negative breast cancers by quantitative multiplex-ligation-dependent probe amplification (MLPA) analysis of BRCA1-associated chromosomal regions: A validation study. BMC Cancer 2016, 16, 811. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Gucalp, A.; Traina, T.A. Androgen receptor-positive, triple-negative breast cancer. Cancer 2017, 123, 1686–1688. [Google Scholar] [CrossRef] [PubMed]
- Meligy, B.M.; Tawfik, E.A.; El Khouly, E.A.; Alagizy, H.; Shehata, M.A.; Elkady, N.M. Androgen receptor expression in estrogen receptor-negative breast cancer. Appl. Immunohistochem. Mol. Morphol. 2003, 11, 138–1423. [Google Scholar]
- Ferrari, P.; Scatena, C.; Ghilli, M.; Bargagna, I.; Lorenzini, G.; Nicolini, A. Molecular Mechanisms, Biomarkers and Emerging Therapies for Chemotherapy Resistant TNBC. Int. J. Mol. Sci. 2022, 23, 1665. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Astvatsaturyan, K.; Yue, Y.; Walts, A.E.; Bose, S. Androgen receptor positive triple negative breast cancer: Clinicopathologic, prognostic, and predictive features. PLoS ONE 2018, 13, e0197827. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Rampurwala, M.; Wisinski, K.B.; O’Regan, R. Role of the androgen receptor in triple-negative breast cancer. Clin. Adv. Hematol. Oncol. 2016, 14, 186–193. [Google Scholar] [PubMed] [PubMed Central]
- Bianchini, G.; Balko, J.M.; Mayer, I.A.; Sanders, M.E.; Gianni, L. Triple-negative breast cancer: Challenges and opportunities of a heterogeneous disease. Nat. Rev. Clin. Oncol. 2016, 13, 674–690. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Narayanan, R.; Dalton, J.T. Androgen Receptor: A Complex Therapeutic Target for Breast Cancer. Cancers 2016, 8, 108. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Gerratana, L.; Basile, D.; Buono, G.; De Placido, S.; Giuliano, M.; Minichillo, S.; Coinu, A.; Martorana, F.; De Santo, I.; Del Mastro, L.; et al. Androgen receptor in triple negative breast cancer: A potential target for the targetless subtype. Cancer Treat. Rev. 2018, 68, 102–110. [Google Scholar] [CrossRef] [PubMed]
- You, C.P.; Leung, M.H.; Tsang, W.C.; Khoo, U.S.; Tsoi, H. Androgen Receptor as an Emerging Feasible Biomarker for Breast Cancer. Biomolecules 2022, 12, 72. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Tsutsumi, Y. Apocrine carcinoma as triple-negative breast cancer: Novel definition of apocrine-type carcinoma as estrogen/progesterone receptor-negative and androgen receptor-positive invasive ductal carcinoma. Jpn. J. Clin. Oncol. 2012, 42, 375–386. [Google Scholar] [CrossRef] [PubMed]
- Barton, V.N.; D’Amato, N.C.; Gordon, M.A.; Christenson, J.L.; Elias, A.; Richer, J.K. Androgen Receptor Biology in Triple Negative Breast Cancer: A Case for Classification as AR+ or Quadruple Negative Disease. Horm. Cancer 2015, 6, 206–213. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Hon, J.D.; Singh, B.; Sahin, A.; Du, G.; Wang, J.; Wang, V.Y.; Deng, F.M.; Zhang, D.Y.; Monaco, M.E.; Lee, P. Breast cancer molecular subtypes: From TNBC to QNBC. Am. J. Cancer Res. 2016, 6, 1864–1872. [Google Scholar] [PubMed] [PubMed Central]
- Huang, M.; Wu, J.; Ling, R.; Li, N. Quadruple negative breast cancer. Breast Cancer 2020, 27, 527–533. [Google Scholar] [CrossRef] [PubMed]
- Haruna, M.; Daramola, A.O.; Awolola, N.A.; Badr, N.M.; Banjo, A.A.F.; Shaaban, A. Clinicopathological features and androgen receptor expression in triple negative breast cancer at Lagos, Nigeria. Ecancermedicalscience 2022, 16, 1452. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Jinna, N.; Jovanovic-Talisman, T.; LaBarge, M.; Natarajan, R.; Kittles, R.; Sistrunk, C.; Rida, P.; Seewaldt, V.L. Racial Disparity in Quadruple Negative Breast Cancer: Aggressive Biology and Potential Therapeutic Targeting and Prevention. Cancers 2022, 14, 4484. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Davis, M.; Tripathi, S.; Hughley, R.; He, Q.; Bae, S.; Karanam, B.; Martini, R.; Newman, L.; Colomb, W.; Grizzle, W.; et al. AR negative triple negative or “quadruple negative” breast cancers in African American women have an enriched basal and immune signature. PLoS ONE 2018, 13, e0196909. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Christenson, J.L.; Trepel, J.B.; Ali, H.Y.; Lee, S.; Eisner, J.R.; Baskin-Bey, E.S.; Elias, A.D.; Richer, J.K. Harnessing a Different Dependency: How to Identify and Target Androgen Receptor-Positive versus Quadruple-Negative Breast Cancer. Horm. Cancer 2018, 9, 82–94. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Mohammed, A.A.; Elsayed, F.M.; Algazar, M.; Rashed, H.E.; Anter, A.H. Neoadjuvant Chemotherapy in Triple Negative Breast Cancer: Correlation between Androgen Receptor Expression and Pathological Response. Asian Pac. J. Cancer Prev. 2020, 21, 563–568. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Azim, H.A.; Shohdy, K.S.; Elghazawy, H.; Salib, M.M.; Almeldin, D.; Kassem, L. Programmed death-ligand 1 (PD-L1) expression predicts response to neoadjuvant chemotherapy in triple-negative breast cancer: A systematic review and meta-analysis. Biomarkers 2022, 27, 764–772. [Google Scholar] [CrossRef] [PubMed]
- Riaz, N.; Idress, R.; Habib, S.; Lalani, E.N. Lack of Androgen Receptor Expression Selects for Basal-like Phenotype and Is a Predictor of Poor Clinical Outcome in Non-Metastatic Triple Negative Breast Cancer. Front. Oncol. 2020, 10, 1083. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Ricks-Santi, L.J.; Fredenburg, K.; Rajaei, M.; Esnakula, A.; Naab, T.; McDonald, J.T.; Kanaan, Y. Characterization of GATA3 and Mammaglobin in breast tumors from African American Women. Arch. Microbiol. Immunol. 2023, 7, 18–28. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Beyene, D.; Naab, T.; Apprey, V.; Ricks-Santi, L.; Esnakula, A.; Qasim, M.; George, M., Jr.; Minoza, K.G.; Copeland, R.L., Jr.; Broome, C.; et al. Cyclin A2 and Ki-67 proliferation markers could be used to identify tumors with poor prognosis in African American women with breast cancer. J. Cancer Biol. 2023, 4, 3–16. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Khan, F.; Ricks-Santi, L.J.; Zafar, R.; Kanaan, Y.; Naab, T. Expression of p27 and c-Myc by immunohistochemistry in breast ductal cancers in African American women. Ann. Diagn. Pathol. 2018, 34, 170–174. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Khan, F.; Esnakula, A.; Ricks-Santi, L.J.; Zafar, R.; Kanaan, Y.; Naab, T. Loss of PTEN in high grade advanced stage triple negative breast ductal cancers in African American women. Pathol. Res. Pract. 2018, 214, 673–678. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Esnakula, A.K.; Ricks-Santi, L.; Kwagyan, J.; Kanaan, Y.M.; DeWitty, R.L.; Wilson, L.L.; Gold, B.; Frederick, W.A.; Naab, T.J. Strong association of fascin expression with triple negative breast cancer and basal-like phenotype in African-American women. J. Clin. Pathol. 2014, 67, 153–160. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Maqbool, M.; Bekele, F.; Fekadu, G. Treatment Strategies Against Triple-Negative Breast Cancer: An Updated Review. Breast Cancer Targets Ther. 2022, 14, 15–24. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Mandapati, A.; Lukong, K.E. Triple negative breast cancer: Approved treatment options and their mechanisms of action. J. Cancer Res. Clin. Oncol. 2023, 149, 3701–3719. [Google Scholar] [CrossRef] [PubMed] [PubMed Central]
- Bhattarai, S.; Sugita, B.M.; Bortoletto, S.M.; Fonseca, A.S.; Cavalli, L.R.; Aneja, R. QNBC Is Associated with High Genomic Instability Characterized by Copy Number Alterations and miRNA Deregulation. Int. J. Mol. Sci. 2021, 22, 11548. [Google Scholar] [CrossRef] [PubMed]
- Di Leone, A.; Fragomeni, S.M.; Scardina, L.; Ionta, L.; Mule, A.; Magno, S.; Terribile, D.; Masetti, R.; Franceschini, G. Androgen receptor expression and outcome of neoadjuvant chemotherapy in triple-negative breast cancer. Eur. Rev. Med. Pharmacol. Sci. 2021, 25, 1910–1915. [Google Scholar] [PubMed]
- Xu, M.; Yuan, Y.; Yan, P.; Jiang, J.; Ma, P.; Niu, X.; Ma, S.; Cai, H.; Yang, K. Prognostic Significance of Androgen Receptor Expression in Triple Negative Breast Cancer: A Systematic Review and Meta-Analysis. Clin. Breast Cancer 2020, 20, e385–e396. [Google Scholar] [CrossRef] [PubMed]
- Naimi, A.; Soltan, M.; Amjadi, E.; Goli, P.; Kefayat, A. Androgen Receptor Expression and Its Correlation with Clinicopathological Parameters in Iranian Patients with Triple Negative Breast Cancer. Iran. J. Pathol. 2020, 15, 239–244. [Google Scholar] [CrossRef] [PubMed]
- Zuo, T.; Wilson, P.; Cicek, A.F.; Harigopal, M. Androgen receptor expression is a favorable prognostic factor in triple-negative breast cancers. Hum. Pathol. 2018, 80, 239–245. [Google Scholar] [CrossRef]
- Sunar, V.; Dogan, H.T.; Sarici, F.; Ates, O.; Akin, S.; Baspinar, B.; Aksoy, S.; Altundag, K. Association between androgen receptor status and prognosis in triple negative breast cancer. J. BUON 2018, 23, 1325–1330. [Google Scholar]
- Asano, Y.; Kashiwagi, S.; Goto, W.; Tanaka, S.; Morisaki, T.; Takashima, T.; Noda, S.; Onoda, N.; Ohsawa, M.; Hirakawa, K.; et al. Expression and Clinical Significance of Androgen Receptor in Triple-Negative Breast Cancer. Cancers 2017, 9, 4. [Google Scholar] [CrossRef] [PubMed]
- Maeda, T.; Nakanishi, Y.; Hirotani, Y.; Fuchinoue, F.; Enomoto, K.; Sakurai, K.; Amano, S.; Nemoto, N. Immunohistochemical co-expression status of cytokeratin 5/6, androgen receptor, and p53 as prognostic factors of adjuvant chemotherapy for triple negative breast cancer. Med. Mol. Morphol. 2016, 49, 11–21. [Google Scholar] [CrossRef] [PubMed]
- Choi, J.E.; Kang, S.H.; Lee, S.J.; Bae, Y.K. Androgen receptor expression predicts decreased survival in early stage triple-negative breast cancer. Ann. Surg. Oncol. 2015, 22, 82–89. [Google Scholar] [CrossRef] [PubMed]
- Pistelli, M.; Caramanti, M.; Biscotti, T.; Santinelli, A.; Pagliacci, A.; De Lisa, M.; Ballatore, Z.; Ridolfi, F.; Maccaroni, E.; Bracci, R.; et al. Androgen receptor expression in early triple-negative breast cancer: Clinical significance and prognostic associations. Cancers 2014, 6, 1351–1362. [Google Scholar] [CrossRef] [PubMed]
- Tang, D.; Xu, S.; Zhang, Q.; Zhao, W. The expression and clinical significance of the androgen receptor and E-cadherin in triple-negative breast cancer. Med. Oncol. 2012, 29, 526–533. [Google Scholar] [CrossRef] [PubMed]
- He, J.; Peng, R.; Yuan, Z.; Wang, S.; Peng, J.; Lin, G.; Jiang, X.; Qin, T. Prognostic value of androgen receptor expression in operable triple-negative breast cancer: A retrospective analysis based on a tissue microarray. Med. Oncol. 2012, 29, 406–410. [Google Scholar] [CrossRef] [PubMed]
- Loibl, S.; Muller, B.M.; von Minckwitz, G.; Schwabe, M.; Roller, M.; Darb-Esfahani, S.; Ataseven, B.; du Bois, A.; Fissler-Eckhoff, A.; Gerber, B.; et al. Androgen receptor expression in primary breast cancer and its predictive and prognostic value in patients treated with neoadjuvant chemotherapy. Breast Cancer Res. Treat. 2011, 130, 477–487. [Google Scholar] [CrossRef]
- Bhattarai, S.; Saini, G.; Gogineni, K.; Aneja, R. Quadruple-negative breast cancer: Novel implications for a new disease. Breast Cancer Res. 2020, 22, 127. [Google Scholar] [CrossRef] [PubMed]
- Angajala, A.; Mothershed, E.; Davis, M.B.; Tripathi, S.; He, Q.; Bedi, D.; Dean-Colomb, W.; Yates, C. Quadruple Negative Breast Cancers (QNBC) Demonstrate Subtype Consistency among Primary and Recurrent or Metastatic Breast Cancer. Transl. Oncol. 2019, 12, 493–501. [Google Scholar] [CrossRef]
- Safarpour, D.; Pakneshan, S.; Tavassoli, F.A. Androgen receptor (AR) expression in 400 breast carcinomas: Is routine AR assessment justified? Am. J. Cancer Res. 2014, 4, 353–368. [Google Scholar]
- McGhan, L.J.; McCullough, A.E.; Protheroe, C.A.; Dueck, A.C.; Lee, J.J.; Nunez-Nateras, R.; Castle, E.P.; Gray, R.J.; Wasif, N.; Goetz, M.P.; et al. Androgen receptor-positive triple negative breast cancer: A unique breast cancer subtype. Ann. Surg. Oncol. 2014, 21, 361–367. [Google Scholar] [CrossRef] [PubMed]
- Mrklic, I.; Pogorelic, Z.; Capkun, V.; Tomic, S. Expression of androgen receptors in triple negative breast carcinomas. Acta Histochem. 2013, 115, 344–348. [Google Scholar] [CrossRef] [PubMed]
- Choi, Y.L.; Oh, E.; Park, S.; Kim, Y.; Park, Y.H.; Song, K.; Cho, E.Y.; Hong, Y.C.; Choi, J.S.; Lee, J.E.; et al. Triple-negative, basal-like, and quintuple-negative breast cancers: Better prediction model for survival. BMC Cancer 2010, 10, 507. [Google Scholar] [CrossRef] [PubMed]
Markers | Antibodies | Clone | Dilution | Source | Expression |
---|---|---|---|---|---|
Estrogen Receptor | Rabbit monoclonal | SP-1 | 1:100 | Dako | Nuclear |
Progesterone Receptor | Mouse monoclonal | PgR636 | 1:500 | Dako | Nuclear |
Human Epidermal Growth Factor Receptor 2 | Rabbit polyclonal | e-erb-2 | 1:200 | Dako | Membranous |
Cytokeratin 5 | Mouse monoclonal | XM26 | 1:150 | VWR | Cytoplasmic |
Ki-67 | Mouse monoclonal | MIB-1 | 1:100 | Dako | Nuclear |
Vimentin | Mouse monoclonal | V9 | 1:100 | Dako | Cytoplasmic |
Fascin | Mouse monoclonal | 55k-2 | 1:500 | Cell Marque Corp | Cytoplasmic |
GATA3 | Mouse monoclonal | L50–823 | 1:500 | Biocare Medical | Nuclear |
Mammaglobin | Mouse monoclonal | 304–1A5 | 1:200 | Dako | Cytoplasmic |
Androgen Receptor | Mouse monoclonal | Clone AR441 | 1:100 | Agilent | Nuclear |
Characteristic | Frequency (%) n = 190 |
---|---|
Age, years | |
<50 | 54 (28.4) |
≥50 | 136 (71.6) |
ER status | |
Positive | 109 (57.4) |
Negative | 81 42.6) |
PR status | |
Positive | 91 (47.9) |
Negative | 99 (52.1) |
Subtype a | |
Luminal A | 83 (43.7) |
Luminal B | 27 (14.2) |
HER2+ | 18 (9.5) |
Triple-negative | 62 (32.6) |
Pathologic stage | |
Stage I | 59 (31.1) |
Stage II | 79 (41.6) |
Stage III | 40 (21.1) |
Stage IV | 12 (6.3) |
Grade | |
Grade 1 | 9 (4.7) |
Grade 2 | 54 (28.4) |
Grade 3 | 127 (66.8) |
Recurrence | |
None | 128 (67.4) |
Loco-regional | 10 (5.3) |
Distant | 20 (10.5) |
Never disease-free | 17 (8.9) |
Unknown | 15 (7.9) |
Luminal A (%) | Luminal B (%) | HER2+ (%) | TNBC (%) | QNBC (%) | p-Value | |||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
n = 83 | n = 14 | n = 18 | n = 43 | n = 14 | ||||||||
Stage | 0.378 | |||||||||||
Stage I | 27 | 32.5% | 11 | 40.7% | 3 | 16.7% | 15 | 31.9% | 3 | 20.0% | ||
Stage II | 37 | 44.6% | 7 | 25.9% | 6 | 33.3% | 19 | 40.4% | 10 | 66.7% | ||
Stage III | 15 | 18.1% | 7 | 25.9% | 7 | 38.9% | 10 | 21.3% | 1 | 6.7% | ||
Stage IV | 4 | 4.8% | 2 | 7.4% | 2 | 11.1% | 3 | 6.4% | 1 | 6.7% | ||
Grade | <0.001 | |||||||||||
Grade 1 | 5 | 6.0% | 3 | 11.1% | 0 | 0.0% | 0 | 0.0% | 0 | 0.0% | ||
Grade 2 | 39 | 47.0% | 10 | 37.0% | 0 | 0.0% | 4 | 8.5% | 1 | 6.7% | ||
Grade 3 | 39 | 47.0% | 14 | 51.9% | 18 | 100.0% | 43 | 91.5% | 14 | 93.3% | ||
Distant Metastases | 0.242 | |||||||||||
No | 75 | 90.4% | 20 | 74.1% | 14 | 77.8% | 38 | 80.9% | 13 | 86.7% | ||
Yes | 8 | 9.6% | 7 | 25.9% | 4 | 22.2% | 9 | 19.1% | 2 | 13.3% | ||
Lymph Nodes | 0.759 | |||||||||||
No | 43 | 59.7% | 13 | 52.0% | 7 | 43.8% | 24 | 60.0% | 8 | 61.5% | ||
Yes | 29 | 40.3% | 12 | 48.0% | 9 | 56.3% | 16 | 40.0% | 5 | 38.5% | ||
Missing | 11 | 2 | 2 | 7 | 2 | |||||||
Recurrence | 0.425 | |||||||||||
None | 65 | 87.8% | 20 | 74.1% | 13 | 81.3% | 36 | 76.6% | 10 | 76.9% | ||
Yes | 9 | 12.2% | 7 | 25.9% | 3 | 18.8% | 11 | 23.4% | 3 | 23.1% | ||
Missing | 9 | 2 | 0 | 2 |
Subtype/AR Status | Mean (mm) | N | SD | p-Value |
---|---|---|---|---|
Luminal A/AR negative | 32.87 | 15 | 24.40 | <0.001 |
Luminal A/AR positive | 24.47 | 60 | 15.65 | |
Luminal B/AR negative | 22.00 | 6 | 20.00 | |
Luminal B/AR positive | 31.37 | 19 | 21.50 | |
HER2+/AR negative | 64.30 | 10 | 44.91 | |
HER2+/AR positive | 27.88 | 8 | 14.00 | |
Quadruple negative BC | 37.31 | 42 | 29.36 | |
Triplenegative BC | 25.36 | 14 | 13.09 |
Luminal Subtype | TNBC | QNBC | |||||||
---|---|---|---|---|---|---|---|---|---|
Mean | Std Dev | Mean | Std Dev | Mean | Std Dev | F Statistic | ANOVA p-Value | ||
Mammary differentiation/tumor suppressor | GATA3 | 216.82 | 76.84 | 81.15 | 87.99 | 15.74 | 48.05 | 138.71 | <0.001 |
Mammary differentiation/tumor suppressor | Mammaglobin | 98.96 | 110.76 | 58.46 | 101.87 | 46.21 | 63.86 | 5.00 | 0.008 |
Invasiveness/oncogene | Fascin | 11.34 | 39.06 | 97.67 | 113.21 | 178.80 | 101.94 | 99.89 | <0.001 |
EMT marker/oncogene | Vimentin | 12.84 | 57.29 | 64.00 | 105.83 | 117.66 | 104.49 | 30.69 | <0.001 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Oladeru, O.; Rajack, F.; Esnakula, A.; Naab, T.J.; Kanaan, Y.; Ricks-Santi, L. Beyond Triple-Negative: High Prevalence of Quadruple-Negative Breast Cancer in African Americans. Biomedicines 2024, 12, 1522. https://doi.org/10.3390/biomedicines12071522
Oladeru O, Rajack F, Esnakula A, Naab TJ, Kanaan Y, Ricks-Santi L. Beyond Triple-Negative: High Prevalence of Quadruple-Negative Breast Cancer in African Americans. Biomedicines. 2024; 12(7):1522. https://doi.org/10.3390/biomedicines12071522
Chicago/Turabian StyleOladeru, Oluwadamilola, Fareed Rajack, Ashwini Esnakula, Tammey J. Naab, Yasmine Kanaan, and Luisel Ricks-Santi. 2024. "Beyond Triple-Negative: High Prevalence of Quadruple-Negative Breast Cancer in African Americans" Biomedicines 12, no. 7: 1522. https://doi.org/10.3390/biomedicines12071522
APA StyleOladeru, O., Rajack, F., Esnakula, A., Naab, T. J., Kanaan, Y., & Ricks-Santi, L. (2024). Beyond Triple-Negative: High Prevalence of Quadruple-Negative Breast Cancer in African Americans. Biomedicines, 12(7), 1522. https://doi.org/10.3390/biomedicines12071522