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Влияние внутреннего подтипа на эффективность терапии ингибиторами CDK4/6 при распространенном HR+/HER2- раке молочной железы
Гречухина К.С., Филоненко Д.А., Сухова М.В., Жукова Л.Г. Влияние внутреннего подтипа на эффективность терапии ингибиторами CDK4/6 при распространенном HR+/HER2- раке молочной железы. Современная Онкология. 2024;26(2):182–189. DOI: 10.26442/18151434.2024.2.202748
© ООО «КОНСИЛИУМ МЕДИКУМ», 2024 г.
© ООО «КОНСИЛИУМ МЕДИКУМ», 2024 г.
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Grechukhina KS, Filonenko DA, Sukhova MV, Zhukova LG. Effect of internal subtype on the efficacy of CDK4/6 inhibitor therapy in advanced HR+/HER2- breast cancer: A review. Journal of Modern Oncology.
2024;26(2):182–189. DOI: 10.26442/18151434.2024.2.202748
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Аннотация
В настоящее время в рутинной клинической практике используют классификацию рака молочной железы (РМЖ) по иммуногистохимическим фенотипам. Однако генетический профиль опухоли не всегда соответствует патоморфологическому, что может значимо влиять на прогноз и предсказывать эффективность терапии при РМЖ. В статье рассмотрена эффективность эндокринотерапии в зависимости от внутреннего подтипа РМЖ, а также представлены данные об эффективности ингибиторов CDK4/6 в данных подгруппах. Показано, что в процессе метастазирования опухоль приобретает более агрессивный подтип (например, переходит из люминального в HER2-E или базальноподобный), что может быть остановлено при применении терапии ингибиторами CDK4/6, при назначении которых внутренний подтип переходит в более благоприятную группу.
Ключевые слова: ингибиторы CDK4/6, рибоциклиб, HR+/HER2-, распространенный рак молочной железы, молекулярные подтипы, гетерогенность опухолей
Ключевые слова: ингибиторы CDK4/6, рибоциклиб, HR+/HER2-, распространенный рак молочной железы, молекулярные подтипы, гетерогенность опухолей
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The classification of breast cancer (BC) by immunohistochemical phenotypes is widely used in routine clinical practice. However, the genetic profile of the tumor does not always correspond to the pathomorphological one, which can significantly affect the prognosis and predict the effectiveness of therapy in BC. This literature review examines the effectiveness of endocrine therapy depending on the internal subtype of BC, and also presents data on the effectiveness of CDK4/6 inhibitors in these subgroups. It has been shown that during metastasis, the tumor acquires a more aggressive subtype (for example, it switches from luminal to HER2-E or basal-like), which can be stopped when using CDK4/6 inhibitors: the change of the internal subtype passes into a more favorable group.
Keywords: CDK4/6 inhibitors, ribociclib, HR+/HER2-, advanced breast cancer, molecular subtypes, tumor heterogeneity
Полный текст
Список литературы
1. Russnes HG, Lingjærde OC, Børresen-Dale AL, Caldas C. Breast Cancer Molecular Stratification: From Intrinsic Subtypes to Integrative Clusters. Am J Pathol. 2017;187(10):2152-62. DOI:10.1016/j.ajpath.2017.04.022
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2019;37(14):1169-78. DOI:10.1200/JCO.18.00925
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21. Perez EA, Romond EH, Suman VJ, et al. Trastuzumab plus adjuvant chemotherapy for human epidermal growth factor receptor 2-positive breast cancer: planned joint analysis of overall survival from NSABP B-31 and NCCTG N9831. J Clin Oncol. 2014;32(33):3744-52. DOI:10.1200/JCO.2014.55.5730
22. Perez EA, Ballman KV, Mashadi-Hossein A, et al. Intrinsic Subtype and Therapeutic Response Among HER2-Positive Breaty st Tumors from the NCCTG (Alliance) N9831 Trial. J Natl Cancer Inst. 2017;109(2). DOI:10.1093/jnci/djw207
23. Prat A, Parker JS, Fan C, et al. Concordance among gene expression-based predictors for ER-positive breast cancer treated with adjuvant tamoxifen. Ann Oncol. 2012;23(11):2866-73. DOI:10.1093/annonc/mds080
24. Lesurf R, Griffith OL, Griffith M, et al. Genomic characterization of HER2-positive breast cancer and response to neoadjuvant trastuzumab and chemotherapy-results from the ACOSOG Z1041 (Alliance) trial. Ann Oncol. 2017;28(5):1070-7. DOI:10.1093/annonc/mdx048
25. Prat A, Cheang MC, Galván P, et al. Prognostic Value of Intrinsic Subtypes in Hormone Receptor-Positive Metastatic Breast Cancer Treated With Letrozole With or Without Lapatinib. JAMA Oncol. 2016;2(10):1287-94. DOI:10.1001/jamaoncol.2016.0922
26. Prat A, Brase JC, Cheng Y, et al. Everolimus plus Exemestane for Hormone Receptor-Positive Advanced Breast Cancer: A PAM50 Intrinsic Subtype Analysis of BOLERO-2. Oncologist. 2019;24(7):893-900. DOI:10.1634/theoncologist.2018-0407
27. Ellis MJ, Suman VJ, Hoog J, et al. Randomized phase II neoadjuvant comparison between letrozole, anastrozole, and exemestane for postmenopausal women with estrogen receptor-rich stage 2 to 3 breast cancer: clinical and biomarker outcomes and predictive value of the baseline PAM50-based intrinsic subtype-ACOSOG Z1031. J Clin Oncol. 2011;29(17):2342-9. DOI:10.1200/JCO.2010.31.6950
28. Brasó-Maristany F, Palafox M, Monserrat L, et al. 16P Understanding the biologic determinants of ribociclib efficacy in breast cancer. Ann Oncol.
2021;32:21-36. DOI:10.1016/j.annonc.2021.03.030
29. Portman N, Alexandrou S, Carson E, et al. Overcoming CDK4/6 inhibitor resistance in ER-positive breast cancer. Endocr Relat Cancer. 2019;26(1):R15-30. DOI:10.1530/ERC-18-0317
30. Feng Y, Spezia M, Huang S, et al. Breast cancer development and progression: Risk factors, cancer stem cells, signaling pathways, genomics, and molecular pathogenesis. Genes Dis. 2018;5(2):77-106. DOI:10.1016/j.gendis.2018.05.001
31. Witkiewicz AK, Cox D, Knudsen ES. CDK4/6 inhibition provides a potent adjunct to Her2-targeted therapies in preclinical breast cancer models. Genes Cancer. 2014;5(7-8):261-72. DOI:10.18632/genesandcancer.24
32. Piezzo M, Cocco S, Caputo R, et al. Targeting Cell Cycle in Breast Cancer: CDK4/6 Inhibitors. Int J Mol Sci. 2020;21(18). DOI:10.3390/ijms21186479
33. Zhang J, Bu X, Wang H, et al. Cyclin D-CDK4 kinase destabilizes PD-L1 via cullin 3-SPOP to control cancer immune surveillance. Nature.
2018;553(7686):91-5. DOI:10.1038/nature25015
34. Laphanuwat P, Jirawatnotai S. Immunomodulatory Roles of Cell Cycle Regulators. Front Cell Dev Biol. 2019;7:23. DOI:10.3389/fcell.2019.00023
35. Chaikovsky AC, Sage J. Beyond the Cell Cycle: Enhancing the Immune Surveillance of Tumors Via CDK4/6 Inhibition. Mol Cancer Res. 2018;16(10):1454-7.
DOI:10.1158/1541-7786.MCR-18-0201
36. Finn R, Liu Y, Martin M, et al. Abstract P2-09-10: Comprehensive gene expression biomarker analysis of CDK 4/6 and endocrine pathways from the PALOMA-2 study. Cancer Res. 2018;78:P2-09-10. DOI:10.1158/1538-7445.SABCS17-P2-09-10
37. Carey L, Solovieff N, Andre F, O’Shaughnessy J. GS2-00. Correlative analysis of overall survival by intrinsic subtype across the MONALEESA-2, -3, and -7 studies of ribociclib + endocrine therapy in patients with HR+/HER2- advanced breast cancer. San Antonio Breast Cancer Symposium. San Antonio, Texas. 2021.
38. Prat A, Chaudhury A, Solovieff N, et al. Abstract GS1-04: Correlative biomarker analysis of intrinsic subtypes and efficacy across the MONALEESA Phase III studies. San Antonio Breast Cancer Symposium. San Antonio, Texas. 2020.
39. Jacobson A. Ribociclib Improves Overall Survival in HR+/HER2- Metastatic Breast Cancer Across Common Genomic and Clinical Subtypes. Oncologist. 2022;27(Suppl. 1):S11-2. DOI:10.1093/oncolo/oyac010
40. Martínez OS, Tolosa P, Sánchez De Torre A, et al. 23P CDK4/6 inhibition and endocrine therapy (ET) in the HER2-enriched subtype (HER2-E) in hormone receptor-positive/HER2-negative (HR+/HER2-) advanced breast cancer (ABC): a retrospective analysis of real-world data. Ann Oncol. 2021;32:21-36. DOI:10.1016/j.annonc.2021.03.037
41. Pascual T, Stover DG, Thuerigen A, et al. 272TiP HARMONIA SOLTI-2101 / AFT-58: A head-to-head phase III study comparing ribociclib (RIB) and palbociclib (PAL) in patients (pts) with hormone receptor-positive/HER2-negative/HER2-enriched (HR+/HER2-/HER2-E) advanced breast cancer (ABC). Ann Oncol. 2022;33:S662. DOI:10.1016/j.annonc.2022.07.1856
42. Jørgensen CLT, Larsson AM, Forsare C, et al. PAM50 Intrinsic Subtype Profiles in Primary and Metastatic Breast Cancer Show a Significant Shift toward More Aggressive Subtypes with Prognostic Implications. Cancers (Basel). 2021;13(7). DOI:10.3390/cancers13071592
43. Prat A, Saura C, Pascual T, et al. Ribociclib plus letrozole versus chemotherapy for postmenopausal women with hormone receptor-positive, HER2-negative, luminal B breast cancer (CORALLEEN): an open-label, multicentre, randomised, phase 2 trial. Lancet Oncol. 2020;21(1):33-43. DOI:10.1016/S1470-2045(19)30786-7
2. Cejalvo JM, Pascual T, Fernández-Martínez A, et al. Clinical implications of the non-luminal intrinsic subtypes in hormone receptor-positive breast cancer. Cancer Treat Rev. 2018;67:63-70. DOI:10.1016/j.ctrv.2018.04.015
3. Prat A, Chaudhury A, Solovieff N, et al. Correlative Biomarker Analysis of Intrinsic Subtypes and Efficacy Across the MONALEESA Phase III Studies. J Clin Oncol. 2021;39(13):1458-67. DOI:10.1200/JCO.20.02977
4. Parker JS, Mullins M, Cheang MC, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009;27(8):1160-7. DOI:10.1200/JCO.2008.18.1370
5. Paquet ER, Hallett MT. Absolute assignment of breast cancer intrinsic molecular subtype. J Natl Cancer Inst. 2015;107(1):357. DOI:10.1093/jnci/dju357
6. Turner NC, Liu Y, Zhu Z, et al. Cyclin E1 Expression and Palbociclib Efficacy in Previously Treated Hormone Receptor-Positive Metastatic Breast Cancer. J Clin Oncol.
2019;37(14):1169-78. DOI:10.1200/JCO.18.00925
7. Finn RS, Liu Y, Zhu Z, et al. Biomarker Analyses of Response to Cyclin-Dependent Kinase 4/6 Inhibition and Endocrine Therapy in Women with Treatment-Naïve Metastatic Breast Cancer. Clin Cancer Res. 2020;26(1):110-21. DOI:10.1158/1078-0432.CCR-19-0751
8. Burstein MD, Tsimelzon A, Poage GM, et al. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res.
2015;21(7):1688-98. DOI:10.1158/1078-0432.CCR-14-0432
9. Badve S, Dabbs DJ, Schnitt SJ, et al. Basal-like and triple-negative breast cancers: a critical review with an emphasis on the implications for pathologists and oncologists. Mod Pathol. 2011;24(2):157-67. DOI:10.1038/modpathol.2010.200
10. Cancer Genome Atlas Network. Comprehensive molecular portraits of human breast tumours. Nature. 2012;490(7418):61-70. DOI:10.1038/nature11412
11. Cejalvo JM, Martínez de Dueñas E, Galván P, et al. Intrinsic Subtypes and Gene Expression Profiles in Primary and Metastatic Breast Cancer. Cancer Res. 2017;77(9):2213-21. DOI:10.1158/0008-5472.CAN-16-2717
12. Godoy-Ortiz A, Sanchez-Muñoz A, Chica Parrado MR, et al. Deciphering HER2 Breast Cancer Disease: Biological and Clinical Implications. Front Oncol. 2019;9:1124. DOI:10.3389/fonc.2019.01124
13. Prat A, Carey LA, Adamo B, et al. Molecular features and survival outcomes of the intrinsic subtypes within HER2-positive breast cancer. J Natl Cancer Inst. 2014;106(8). DOI:10.1093/jnci/dju152
14. Ferrari A, Vincent-Salomon A, Pivot X, et al. A whole-genome sequence and transcriptome perspective on HER2-positive breast cancers. Nat Commun. 2016;7:12222. DOI:10.1038/ncomms12222
15. Slamon DJ, Clark GM, Wong SG, et al. Human breast cancer: correlation of relapse and survival with amplification of the HER-2/neu oncogene. Science. 1987;235(4785):177-82. DOI:10.1126/science.3798106
16. Baselga J. Why the epidermal growth factor receptor? The rationale for cancer therapy. Oncologist. 2002;7(Suppl. 4):2-8. DOI:10.1634/theoncologist.7-suppl_4-2
17. Polyak K. Heterogeneity in breast cancer. J Clin Invest. 2011;121(10):3786-8. DOI:10.1172/JCI60534
18. Kim HK, Park KH, Kim Y, et al. Discordance of the PAM50 Intrinsic Subtypes Compared with Immunohistochemistry-Based Surrogate in Breast Cancer Patients: Potential Implication of Genomic Alterations of Discordance. Cancer Res Treat. 2019;51(2):737-47. DOI:10.4143/crt.2018.342
19. Cheang MC, Martin M, Nielsen TO, et al. Defining breast cancer intrinsic subtypes by quantitative receptor expression. Oncologist.
2015;20(5):474-82. DOI:10.1634/theoncologist.2014-0372
20. Perez EA, Romond EH, Suman VJ, et al. Four-year follow-up of trastuzumab plus adjuvant chemotherapy for operable human epidermal growth factor receptor 2-positive breast cancer: joint analysis of data from NCCTG N9831 and NSABP B-31. J Clin Oncol. 2011;29(25):3366-73. DOI:10.1200/JCO.2011.35.0868
21. Perez EA, Romond EH, Suman VJ, et al. Trastuzumab plus adjuvant chemotherapy for human epidermal growth factor receptor 2-positive breast cancer: planned joint analysis of overall survival from NSABP B-31 and NCCTG N9831. J Clin Oncol. 2014;32(33):3744-52. DOI:10.1200/JCO.2014.55.5730
22. Perez EA, Ballman KV, Mashadi-Hossein A, et al. Intrinsic Subtype and Therapeutic Response Among HER2-Positive Breaty st Tumors from the NCCTG (Alliance) N9831 Trial. J Natl Cancer Inst. 2017;109(2). DOI:10.1093/jnci/djw207
23. Prat A, Parker JS, Fan C, et al. Concordance among gene expression-based predictors for ER-positive breast cancer treated with adjuvant tamoxifen. Ann Oncol. 2012;23(11):2866-73. DOI:10.1093/annonc/mds080
24. Lesurf R, Griffith OL, Griffith M, et al. Genomic characterization of HER2-positive breast cancer and response to neoadjuvant trastuzumab and chemotherapy-results from the ACOSOG Z1041 (Alliance) trial. Ann Oncol. 2017;28(5):1070-7. DOI:10.1093/annonc/mdx048
25. Prat A, Cheang MC, Galván P, et al. Prognostic Value of Intrinsic Subtypes in Hormone Receptor-Positive Metastatic Breast Cancer Treated With Letrozole With or Without Lapatinib. JAMA Oncol. 2016;2(10):1287-94. DOI:10.1001/jamaoncol.2016.0922
26. Prat A, Brase JC, Cheng Y, et al. Everolimus plus Exemestane for Hormone Receptor-Positive Advanced Breast Cancer: A PAM50 Intrinsic Subtype Analysis of BOLERO-2. Oncologist. 2019;24(7):893-900. DOI:10.1634/theoncologist.2018-0407
27. Ellis MJ, Suman VJ, Hoog J, et al. Randomized phase II neoadjuvant comparison between letrozole, anastrozole, and exemestane for postmenopausal women with estrogen receptor-rich stage 2 to 3 breast cancer: clinical and biomarker outcomes and predictive value of the baseline PAM50-based intrinsic subtype-ACOSOG Z1031. J Clin Oncol. 2011;29(17):2342-9. DOI:10.1200/JCO.2010.31.6950
28. Brasó-Maristany F, Palafox M, Monserrat L, et al. 16P Understanding the biologic determinants of ribociclib efficacy in breast cancer. Ann Oncol.
2021;32:21-36. DOI:10.1016/j.annonc.2021.03.030
29. Portman N, Alexandrou S, Carson E, et al. Overcoming CDK4/6 inhibitor resistance in ER-positive breast cancer. Endocr Relat Cancer. 2019;26(1):R15-30. DOI:10.1530/ERC-18-0317
30. Feng Y, Spezia M, Huang S, et al. Breast cancer development and progression: Risk factors, cancer stem cells, signaling pathways, genomics, and molecular pathogenesis. Genes Dis. 2018;5(2):77-106. DOI:10.1016/j.gendis.2018.05.001
31. Witkiewicz AK, Cox D, Knudsen ES. CDK4/6 inhibition provides a potent adjunct to Her2-targeted therapies in preclinical breast cancer models. Genes Cancer. 2014;5(7-8):261-72. DOI:10.18632/genesandcancer.24
32. Piezzo M, Cocco S, Caputo R, et al. Targeting Cell Cycle in Breast Cancer: CDK4/6 Inhibitors. Int J Mol Sci. 2020;21(18). DOI:10.3390/ijms21186479
33. Zhang J, Bu X, Wang H, et al. Cyclin D-CDK4 kinase destabilizes PD-L1 via cullin 3-SPOP to control cancer immune surveillance. Nature.
2018;553(7686):91-5. DOI:10.1038/nature25015
34. Laphanuwat P, Jirawatnotai S. Immunomodulatory Roles of Cell Cycle Regulators. Front Cell Dev Biol. 2019;7:23. DOI:10.3389/fcell.2019.00023
35. Chaikovsky AC, Sage J. Beyond the Cell Cycle: Enhancing the Immune Surveillance of Tumors Via CDK4/6 Inhibition. Mol Cancer Res. 2018;16(10):1454-7.
DOI:10.1158/1541-7786.MCR-18-0201
36. Finn R, Liu Y, Martin M, et al. Abstract P2-09-10: Comprehensive gene expression biomarker analysis of CDK 4/6 and endocrine pathways from the PALOMA-2 study. Cancer Res. 2018;78:P2-09-10. DOI:10.1158/1538-7445.SABCS17-P2-09-10
37. Carey L, Solovieff N, Andre F, O’Shaughnessy J. GS2-00. Correlative analysis of overall survival by intrinsic subtype across the MONALEESA-2, -3, and -7 studies of ribociclib + endocrine therapy in patients with HR+/HER2- advanced breast cancer. San Antonio Breast Cancer Symposium. San Antonio, Texas. 2021.
38. Prat A, Chaudhury A, Solovieff N, et al. Abstract GS1-04: Correlative biomarker analysis of intrinsic subtypes and efficacy across the MONALEESA Phase III studies. San Antonio Breast Cancer Symposium. San Antonio, Texas. 2020.
39. Jacobson A. Ribociclib Improves Overall Survival in HR+/HER2- Metastatic Breast Cancer Across Common Genomic and Clinical Subtypes. Oncologist. 2022;27(Suppl. 1):S11-2. DOI:10.1093/oncolo/oyac010
40. Martínez OS, Tolosa P, Sánchez De Torre A, et al. 23P CDK4/6 inhibition and endocrine therapy (ET) in the HER2-enriched subtype (HER2-E) in hormone receptor-positive/HER2-negative (HR+/HER2-) advanced breast cancer (ABC): a retrospective analysis of real-world data. Ann Oncol. 2021;32:21-36. DOI:10.1016/j.annonc.2021.03.037
41. Pascual T, Stover DG, Thuerigen A, et al. 272TiP HARMONIA SOLTI-2101 / AFT-58: A head-to-head phase III study comparing ribociclib (RIB) and palbociclib (PAL) in patients (pts) with hormone receptor-positive/HER2-negative/HER2-enriched (HR+/HER2-/HER2-E) advanced breast cancer (ABC). Ann Oncol. 2022;33:S662. DOI:10.1016/j.annonc.2022.07.1856
42. Jørgensen CLT, Larsson AM, Forsare C, et al. PAM50 Intrinsic Subtype Profiles in Primary and Metastatic Breast Cancer Show a Significant Shift toward More Aggressive Subtypes with Prognostic Implications. Cancers (Basel). 2021;13(7). DOI:10.3390/cancers13071592
43. Prat A, Saura C, Pascual T, et al. Ribociclib plus letrozole versus chemotherapy for postmenopausal women with hormone receptor-positive, HER2-negative, luminal B breast cancer (CORALLEEN): an open-label, multicentre, randomised, phase 2 trial. Lancet Oncol. 2020;21(1):33-43. DOI:10.1016/S1470-2045(19)30786-7
________________________________________________
1. Russnes HG, Lingjærde OC, Børresen-Dale AL, Caldas C. Breast Cancer Molecular Stratification: From Intrinsic Subtypes to Integrative Clusters. Am J Pathol. 2017;187(10):2152-62. DOI:10.1016/j.ajpath.2017.04.022
2. Cejalvo JM, Pascual T, Fernández-Martínez A, et al. Clinical implications of the non-luminal intrinsic subtypes in hormone receptor-positive breast cancer. Cancer Treat Rev. 2018;67:63-70. DOI:10.1016/j.ctrv.2018.04.015
3. Prat A, Chaudhury A, Solovieff N, et al. Correlative Biomarker Analysis of Intrinsic Subtypes and Efficacy Across the MONALEESA Phase III Studies. J Clin Oncol. 2021;39(13):1458-67. DOI:10.1200/JCO.20.02977
4. Parker JS, Mullins M, Cheang MC, et al. Supervised risk predictor of breast cancer based on intrinsic subtypes. J Clin Oncol. 2009;27(8):1160-7. DOI:10.1200/JCO.2008.18.1370
5. Paquet ER, Hallett MT. Absolute assignment of breast cancer intrinsic molecular subtype. J Natl Cancer Inst. 2015;107(1):357. DOI:10.1093/jnci/dju357
6. Turner NC, Liu Y, Zhu Z, et al. Cyclin E1 Expression and Palbociclib Efficacy in Previously Treated Hormone Receptor-Positive Metastatic Breast Cancer. J Clin Oncol.
2019;37(14):1169-78. DOI:10.1200/JCO.18.00925
7. Finn RS, Liu Y, Zhu Z, et al. Biomarker Analyses of Response to Cyclin-Dependent Kinase 4/6 Inhibition and Endocrine Therapy in Women with Treatment-Naïve Metastatic Breast Cancer. Clin Cancer Res. 2020;26(1):110-21. DOI:10.1158/1078-0432.CCR-19-0751
8. Burstein MD, Tsimelzon A, Poage GM, et al. Comprehensive genomic analysis identifies novel subtypes and targets of triple-negative breast cancer. Clin Cancer Res.
2015;21(7):1688-98. DOI:10.1158/1078-0432.CCR-14-0432
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Авторы
К.С. Гречухина*, Д.А. Филоненко, М.В. Сухова, Л.Г. Жукова
ГБУЗ «Московский клинический научно-практический центр им. А.С. Логинова» Департамента здравоохранения г. Москвы, Москва, Россия
*dr.grechukhina@gmail.com
ГБУЗ «Московский клинический научно-практический центр им. А.С. Логинова» Департамента здравоохранения г. Москвы, Москва, Россия
*dr.grechukhina@gmail.com
________________________________________________
Katerina S. Grechukhina*, Daria A. Filonenko, Margarita V. Sukhova, Liudmila G. Zhukova
Loginov Moscow Clinical Scientific Center, Moscow, Russia
*dr.grechukhina@gmail.com
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