Breast cancer in Tanzanian, black American, and white American women: An assessment of prognostic and predictive features, including tumor infiltrating lymphocytes

English version

Autoři: Alex Mremi ^aff001; Gloria Broadwater ^aff002; Kahima Jackson ^aff003; Patrick Amsi ^aff001; Cosmas Mbulwa ^aff003; Terry Hyslop ^aff002; Cecilia Ong ^aff004; Allison Hall ^aff005
Působiště autorů: Department of Pathology, Kilimanjaro Christian Medical University College, Moshi, Tanzania ^aff001; Department of Biostatistics and Bioinformatics, Duke University Medical Center, Durham, North Carolina, United States of America ^aff002; Department of Pathology, Bugando Medical Centre, Mwanza, Tanzania ^aff003; Department of Surgery, Duke University Medical Center, Durham, North Carolina, United States of America ^aff004; Department of Pathology, Duke University Medical Center, Durham, North Carolina, United States of America ^aff005
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0224760

Souhrn

Introduction

Breast cancer is a major cause of morbidity and mortality for women in Sub-Saharan Africa and for black American women. There is evidence that the pathologic characteristics of breast cancers in both African women and black American women may differ from their counterparts of European ancestry. However, despite the great burden of disease, data on pathologic features of breast carcinoma in Sub-Saharan Africa is limited and often contradictory. This lack of information makes it difficult to prioritize resource use in efforts to improve breast cancer outcomes in the region.

Methods

We examined consecutive cases of breast cancer in Tanzanian women (n = 83), black American women (n = 120), and white American women (n = 120). Each case was assessed for tumor type, grade, mitotic count, ER and HER2 status, and tumor infiltrating lymphocyte involvement.

Results

The Tanzanian subjects were younger and had higher stage tumors than the subjects in either American group. Breast cancers in the Tanzanian and black American groups were more likely to be high grade (p = 0.008), to have a high mitotic rate (p<0.0001), and to be ER-negative (p<0.001) than the tumors in the white American group. Higher levels of tumor infiltrating lymphocyte involvement were seen among Tanzanian and black American subjects compared to white American subjects (p = 0.0001). Among all subjects, tumor infiltrating lymphocyte levels were higher in tumors with a high mitotic rate. Among Tanzanian and black American subjects, tumor infiltrating lymphocyte levels were higher in ER-negative tumors. These findings have implications for treatment priorities for breast cancer in Tanzania and other Sub-Saharan African countries.

Klíčová slova:

Europe – Africa – Oncology – Biomarkers – Cancer chemotherapy – Carcinomas – Breast cancer – Tumor-infiltrating lymphocytes

Zdroje

1. 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(6):394–424. Epub 2018/09/13. doi: 10.3322/caac.21492 30207593.

2. Wabinga HR, Nambooze S, Amulen PM, Okello C, Mbus L, Parkin DM. Trends in the incidence of cancer in Kampala, Uganda 1991–2010. Int J Cancer. 2014;135(2):432–9. doi: 10.1002/ijc.28661 24615279.

3. Chokunonga E, Borok MZ, Chirenje ZM, Nyakabau AM, Parkin DM. Trends in the incidence of cancer in the black population of Harare, Zimbabwe 1991–2010. Int J Cancer. 2013;133(3):721–9. doi: 10.1002/ijc.28063 23364833.

4. Howlader N, Noone AM, Krapcho M, Miller D, Brest A, Yu M, et al. SEER Cancer Statistics Review, 1975–2016 Bethesda, MD: National Cancer Institute; [cited 2019 May 20, 2019]. Available from: https://seer.cancer.gov/csr/1975_2016.

5. DeSantis CE, Fedewa SA, Goding Sauer A, Kramer JL, Smith RA, Jemal A. Breast cancer statistics, 2015: Convergence of incidence rates between black and white women. CA Cancer J Clin. 2016;66(1):31–42. Epub 2015/10/30. doi: 10.3322/caac.21320 26513636.

6. Sankaranarayanan R, Swaminathan R, Brenner H, Chen K, Chia KS, Chen JG, et al. Cancer survival in Africa, Asia, and Central America: a population-based study. Lancet Oncol. 2010;11(2):165–73. doi: 10.1016/S1470-2045(09)70335-3 20005175.

7. DeSantis CE, Ma J, Goding Sauer A, Newman LA, Jemal A. Breast cancer statistics, 2017, racial disparity in mortality by state. CA Cancer J Clin. 2017;67(6):439–48. Epub 2017/10/04. doi: 10.3322/caac.21412 28972651.

8. Jedy-Agba E, McCormack V, Adebamowo C, Dos-Santos-Silva I. Stage at diagnosis of breast cancer in sub-Saharan Africa: a systematic review and meta-analysis. Lancet Glob Health. 2016;4(12):e923–e35. Epub 2016/11/20. doi: 10.1016/S2214-109X(16)30259-5 27855871; PubMed Central PMCID: PMC5708541.

9. DeSantis CE, Siegel RL, Sauer AG, Miller KD, Fedewa SA, Alcaraz KI, et al. Cancer statistics for African Americans, 2016: Progress and opportunities in reducing racial disparities. CA Cancer J Clin. 2016;66(4):290–308. Epub 2016/02/26. doi: 10.3322/caac.21340 26910411.

10. Sail K, Franzini L, Lairson D, Du X. Differences in treatment and survival among African-American and Caucasian women with early stage operable breast cancer. Ethn Health. 2012;17(3):309–23. Epub 2011/11/10. doi: 10.1080/13557858.2011.628011 22066691.

11. 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(5):713–9. Epub 2008/12/24. doi: 10.1200/JCO.2008.17.9234 19103731.

12. Amadori D, Serra P, Bravaccini S, Farolfi A, Puccetti M, Carretta E, et al. Differences in biological features of breast cancer between Caucasian (Italian) and African (Tanzanian) populations. Breast Cancer Res Treat. 2014;145(1):177–83. doi: 10.1007/s10549-014-2903-0 24658893.

13. Rambau P, Masalu N, Jackson K, Chalya P, Serra P, Bravaccini S. Triple negative breast cancer in a poor resource setting in North-Western Tanzania: a preliminary study of 52 patients. BMC Res Notes. 2014;7:399. doi: 10.1186/1756-0500-7-399 24964871; PubMed Central PMCID: PMC4081017.

14. Joko-Fru WY, Miranda-Filho A, Soerjomataram I, Egue M, Akele-Akpo MT, N'da G, et al. Breast cancer survival in sub-Saharan Africa by age, stage at diagnosis and Human Development Index (HDI): A population-based registry study. Int J Cancer. 2019. Epub 2019/05/16. doi: 10.1002/ijc.32406 31087650.

15. Sawe RT, Kerper M, Badve S, Li J, Sandoval-Cooper M, Xie J, et al. Aggressive breast cancer in western Kenya has early onset, high proliferation, and immune cell infiltration. BMC Cancer. 2016;16:204. Epub 2016/03/12. doi: 10.1186/s12885-016-2204-6 26964534; PubMed Central PMCID: PMC4787041.

16. Eng A, McCormack V, dos-Santos-Silva I. Receptor-defined subtypes of breast cancer in indigenous populations in Africa: a systematic review and meta-analysis. PLoS Med. 2014;11(9):e1001720. Epub 2014/09/10. doi: 10.1371/journal.pmed.1001720 25202974; PubMed Central PMCID: PMC4159229.

17. Jiagge E, Jibril AS, Chitale D, Bensenhaver JM, Awuah B, Hoenerhoff M, et al. Comparative Analysis of Breast Cancer Phenotypes in African American, White American, and West Versus East African patients: Correlation Between African Ancestry and Triple-Negative Breast Cancer. Ann Surg Oncol. 2016;23(12):3843–9. Epub 2016/07/30. doi: 10.1245/s10434-016-5420-z 27469125.

18. Carey LA, Perou CM, Livasy CA, Dressler LG, Cowan D, Conway K, et al. Race, breast cancer subtypes, and survival in the Carolina Breast Cancer Study. JAMA. 2006;295(21):2492–502. Epub 2006/06/08. doi: 10.1001/jama.295.21.2492 16757721.

19. Morris GJ, Naidu S, Topham AK, Guiles F, Xu Y, McCue P, et al. Differences in breast carcinoma characteristics in newly diagnosed African-American and Caucasian patients: a single-institution compilation compared with the National Cancer Institute's Surveillance, Epidemiology, and End Results database. Cancer. 2007;110(4):876–84. doi: 10.1002/cncr.22836 17620276.

20. Denkert C, von Minckwitz G, Brase JC, Sinn BV, Gade S, Kronenwett R, et al. Tumor-infiltrating lymphocytes and response to neoadjuvant chemotherapy with or without carboplatin in human epidermal growth factor receptor 2-positive and triple-negative primary breast cancers. J Clin Oncol. 2015;33(9):983–91. doi: 10.1200/JCO.2014.58.1967 25534375.

21. Loi S, Sirtaine N, Piette F, Salgado R, Viale G, Van Eenoo F, et al. Prognostic and predictive value of tumor-infiltrating lymphocytes in a phase III randomized adjuvant breast cancer trial in node-positive breast cancer comparing the addition of docetaxel to doxorubicin with doxorubicin-based chemotherapy: BIG 02–98. J Clin Oncol. 2013;31(7):860–7. doi: 10.1200/JCO.2011.41.0902 23341518.

22. West NR, Milne K, Truong PT, Macpherson N, Nelson BH, Watson PH. Tumor-infiltrating lymphocytes predict response to anthracycline-based chemotherapy in estrogen receptor-negative breast cancer. Breast Cancer Res. 2011;13(6):R126. doi: 10.1186/bcr3072 22151962; PubMed Central PMCID: PMC3326568.

23. Denkert C, von Minckwitz G, Darb-Esfahani S, Lederer B, Heppner BI, Weber KE, et al. Tumour-infiltrating lymphocytes and prognosis in different subtypes of breast cancer: a pooled analysis of 3771 patients treated with neoadjuvant therapy. Lancet Oncol. 2018;19(1):40–50. Epub 2017/12/14. doi: 10.1016/S1470-2045(17)30904-X 29233559.

24. Elston CW, Ellis IO. Pathological prognostic factors in breast cancer. I. The value of histological grade in breast cancer: experience from a large study with long-term follow-up. Histopathology. 1991;19(5):403–10. Epub 1991/11/01. doi: 10.1111/j.1365-2559.1991.tb00229.x 1757079.

25. Salgado R, Denkert C, Demaria S, Sirtaine N, Klauschen F, Pruneri G, et al. The evaluation of tumor-infiltrating lymphocytes (TILs) in breast cancer: recommendations by an International TILs Working Group 2014. Ann Oncol. 2015;26(2):259–71. doi: 10.1093/annonc/mdu450 25214542.

26. Stuart-Harris R, Caldas C, Pinder SE, Pharoah P. Proliferation markers and survival in early breast cancer: a systematic review and meta-analysis of 85 studies in 32,825 patients. Breast. 2008;17(4):323–34. Epub 2008/05/06. doi: 10.1016/j.breast.2008.02.002 18455396.

27. Vincent-Salomon A, Rousseau A, Jouve M, Beuzeboc P, Sigal-Zafrani B, Freneaux P, et al. Proliferation markers predictive of the pathological response and disease outcome of patients with breast carcinomas treated by anthracycline-based preoperative chemotherapy. Eur J Cancer. 2004;40(10):1502–8. Epub 2004/06/16. doi: 10.1016/j.ejca.2004.03.014 15196533.

28. Chibon F, de Mascarel I, Sierankowski G, Brouste V, Bonnefoi H, Debled M, et al. Prediction of HER2 gene status in Her2 2+ invasive breast cancer: a study of 108 cases comparing ASCO/CAP and FDA recommendations. Mod Pathol. 2009;22(3):403–9. Epub 2008/12/09. doi: 10.1038/modpathol.2008.195 19060846.

29. Lee AH, Key HP, Bell JA, Hodi Z, Ellis IO. Breast carcinomas with borderline (2+) HER2 immunohistochemistry: percentage of cells with complete membrane staining for HER2 and the frequency of HER2 amplification. J Clin Pathol. 2011;64(6):490–2. Epub 2011/03/19. doi: 10.1136/jcp.2011.089177 21415056.

30. Huo D, Hu H, Rhie SK, Gamazon ER, Cherniack AD, Liu J, et al. Comparison of Breast Cancer Molecular Features and Survival by African and European Ancestry in The Cancer Genome Atlas. JAMA Oncol. 2017;3(12):1654–62. Epub 2017/05/05. doi: 10.1001/jamaoncol.2017.0595 28472234; PubMed Central PMCID: PMC5671371.

31. Millikan RC, Newman B, Tse CK, Moorman PG, Conway K, Dressler LG, et al. Epidemiology of basal-like breast cancer. Breast Cancer Res Treat. 2008;109(1):123–39. Epub 2007/06/21. doi: 10.1007/s10549-007-9632-6 17578664; PubMed Central PMCID: PMC2443103.

32. Haddad SA, Ruiz-Narvaez EA, Haiman CA, Sucheston-Campbell LE, Bensen JT, Zhu Q, et al. An exome-wide analysis of low frequency and rare variants in relation to risk of breast cancer in African American Women: the AMBER Consortium. Carcinogenesis. 2016;37(9):870–7. Epub 2016/06/09. doi: 10.1093/carcin/bgw067 27267999; PubMed Central PMCID: PMC5008246.

33. Huo D, Feng Y, Haddad S, Zheng Y, Yao S, Han YJ, et al. Genome-wide association studies in women of African ancestry identified 3q26.21 as a novel susceptibility locus for oestrogen receptor negative breast cancer. Hum Mol Genet. 2016;25(21):4835–46. Epub 2017/02/09. doi: 10.1093/hmg/ddw305 28171663; PubMed Central PMCID: PMC5975608.

34. Geronimus AT, Hicken M, Keene D, Bound J. "Weathering" and age patterns of allostatic load scores among blacks and whites in the United States. Am J Public Health. 2006;96(5):826–33. Epub 2005/12/29. doi: 10.2105/AJPH.2004.060749 16380565; PubMed Central PMCID: PMC1470581.

35. Williams DR, Mohammed SA, Shields AE. Understanding and effectively addressing breast cancer in African American women: Unpacking the social context. Cancer. 2016;122(14):2138–49. Epub 2016/03/02. doi: 10.1002/cncr.29935 26930024; PubMed Central PMCID: PMC5588632.

36. Dent R, Trudeau M, Pritchard KI, Hanna WM, Kahn HK, Sawka CA, et al. Triple-negative breast cancer: clinical features and patterns of recurrence. Clin Cancer Res. 2007;13(15 Pt 1):4429–34. Epub 2007/08/03. doi: 10.1158/1078-0432.CCR-06-3045 17671126.

37. McCormack VA, Joffe M, van den Berg E, Broeze N, Silva Idos S, Romieu I, et al. Breast cancer receptor status and stage at diagnosis in over 1,200 consecutive public hospital patients in Soweto, South Africa: a case series. Breast Cancer Res. 2013;15(5):R84. Epub 2013/09/18. doi: 10.1186/bcr3478 24041225; PubMed Central PMCID: PMC3978918.

38. Dobon B, Hassan HY, Laayouni H, Luisi P, Ricano-Ponce I, Zhernakova A, et al. The genetics of East African populations: a Nilo-Saharan component in the African genetic landscape. Sci Rep. 2015;5:9996. Epub 2015/05/29. doi: 10.1038/srep09996 26017457; PubMed Central PMCID: PMC4446898.

39. Killelea BK, Yang VQ, Wang SY, Hayse B, Mougalian S, Horowitz NR, et al. Racial Differences in the Use and Outcome of Neoadjuvant Chemotherapy for Breast Cancer: Results From the National Cancer Data Base. J Clin Oncol. 2015;33(36):4267–76. Epub 2015/11/26. doi: 10.1200/JCO.2015.63.7801 26598753.