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CAR NK-клетки и возможность их использования для лечения гематологических новообразований
Грибкова И.В. CAR NK-клетки и возможность их использования для лечения гематологических новообразований. Современная Онкология. 2022;24(3):331–335.
DOI: 10.26442/18151434.2022.3.201699
© ООО «КОНСИЛИУМ МЕДИКУМ», 2022 г.
DOI: 10.26442/18151434.2022.3.201699
© ООО «КОНСИЛИУМ МЕДИКУМ», 2022 г.
________________________________________________
Gribkova IV. CAR NK-сells for the treatment of hematological malignancies: A review. Journal of Modern Oncology. 2022;24(3):331–335. DOI: 10.26442/18151434.2022.3.201699
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Аннотация
Гематологические злокачественные новообразования включают в себя более 100 различных подтипов и составляют около 4,8% от всех опухолевых заболеваний в России. Несмотря на значительные успехи в диагностике и лечении, многие из них связаны с плохим прогнозом. В последние годы клеточная терапия представляется многообещающим подходом к лечению неизлечимых гематологических злокачественных новообразований, показывая поразительные результаты в различных клинических испытаниях. Наиболее изученной и показавшей значимые клинические результаты клеточной терапией является терапия Т-лимфоцитами с химерными антигенными рецепторами (CAR Т-лимфоциты или CAR Т-клетки, от англ. СAR – chimeric antigen receptor). Управление по контролю пищевых продуктов и лекарств в США (Food and Drug Administration) одобрило применение CAR T-клеток для терапии В-клеточных лимфом и В-клеточных острых лимфобластных лейкозов. Однако остаются значительные проблемы, связанные с производством, стоимостью и серьезными побочными эффектами данного метода лечения. Альтернативой применения Т-клеток может стать использование клеток врожденного иммунитета, в частности натуральных киллеров (NK), обладающих высоким противоопухолевым потенциалом. В исследованиях последних лет показана противо- опухолевая эффективность терапии, в которой используются генетически модифицированные натуральные киллеры – CAR NK-клетки. Целью данного обзора является описание и систематизация опыта использования CAR NK-клеток для лечения гематологических новообразований. В обзоре представлены преимущества и недостатки данного метода, а также проблемы, которые еще предстоит решить для его широкого внедрения в клиническую практику.
Ключевые слова: гематологические злокачественные новообразования, CAR NK-клеточная терапия, химерный антигенный рецептор, адоптивная терапия, иммунотерапия
Ключевые слова: гематологические злокачественные новообразования, CAR NK-клеточная терапия, химерный антигенный рецептор, адоптивная терапия, иммунотерапия
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Hematological malignant neoplasms include more than a hundred different subtypes and account for about 4.8% of all neoplastic diseases in Russia. Despite significant advances in diagnosis and treatment, many of them remain incurable. In recent years, cell-based therapy appears to be a promising approach to the treatment of these incurable hematologic malignancies, showing striking results in various clinical trials. The most studied and advanced cell therapy is the therapy with T-lymphocytes modified with chimeric antigen receptors (CAR). However, although the US Food and Drug Administration has approved CAR T cells for the treatment of B-cell lymphoma and acute lymphoblastic leukemia, significant problems remain in terms of production, cost, and serious side effects. An alternative to the use of T cells can be the use of innate immune cells, in particular natural killer cells (NK), which have a high antitumor potential. Recent studies have shown the antitumor efficacy of a therapy that uses genetically modified natural killer cells – CAR NK cells. The purpose of this review was to describe and systematize the experience of using CAR NK cells for the treatment of hematological neoplasms. The review presents the advantages and disadvantages of this method, as well as the problems that still have to be solved for its widespread introduction into clinical practice.
Keywords: hematological malignancies, CAR NK-cell therapy, chimeric antigen receptor, adoptive therapy, immunotherapy
Полный текст
Список литературы
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8. Lee HR, Baek KH. Role of natural killer cells for immunotherapy in chronic myeloid leukemia (Review). Oncol Rep. 2019;41:2625-35. DOI:10.3892/or.2019.7059
9. Van Acker HH, Versteven M, Lichtenegger FS, et al. Dendritic Cell-Based Immunotherapy of Acute Myeloid Leukemia. J Clin Med. 2019;8:579. DOI:10.3390/jcm8050579
10. Song W, Zhang M. Use of CAR-T cell therapy, PD-1 blockade, and their combination for the treatment of hematological malignancies. Clin Immunol. 2020;214:108382. DOI:10.1016/j.clim.2020.108382
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12. Грибкова И.В., Завьялов А.А. CAR Т-клетки для лечения хронического лимфоцитарного лейкоза. Клиническая онкогематология. 2021;14(2):225-30 [Gribkova IV, Zavyalov AA. CAR T-cells for the treatment of chronic lymphocytic leukemia. Klinicheskaia onkogematologiia. 2021;14(2):225-30 (in Russian)]. DOI:10.21320/2500-2139-2021-14-2-225-230
13. Боробова Е.А., Жеравин А.А. Натуральные киллеры в иммунотерапии онкологических заболеваний. Сибирский онкологический журнал. 2018;17(6):97‑104 [Borobova EA, Zheravin AA. Natural killer cels in immunotherapy for cancer. Sibirskij onkologicheskij zhurnal. 2018;17(6):97-104 (in Russian)]. DOI:10.21294/1814-4861-2018-17-6-97-104
14. Hu Y, Tian Zh, Zhang C. Chimeric antigen receptor (CAR)-transduced natural killer cells in tumor immunotherapy. Acta Pharmacologica Sinica. 2018;39:167‑76. DOI:10.1038/aps.2017.125
15. Orange JS. Natural killer cell deficiency. J Allergy Clin Immunol. 2013;132:515‑25. DOI:10.1016/j.jaci.2013.07.020
16. Xie G, Dong H, Liang Y, et al. CAR-NK cells: A promising cellular immunotherapy for cancer. EBioMedicine. 2020;59:102975. DOI:10.1016/j.ebiom.2020.102975
17. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9(5):495-502. DOI:10.1038/ni1581
18. Hofland T, Eldering E, Kater AP, Tonino SH. Engaging Cytotoxic T and NK Cells for Immunotherapy in Chronic Lymphocytic Leukemia. Int J Mol Sci. 2019;20(17):4315. DOI:10.3390/ijms20174315
19. Wang W, Erbe AK, Hank JA, et al. NK cell-mediated antibodydependent cellular cytotoxicity in cancer immunotherapy. Front Immunol 2015;6:368. DOI:10.3389/fimmu.2015.00368
20. Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331(6013):44-9. DOI:10.1126/science.1198687
21. Zhang C, Hu Y, Shi C. Targeting Natural Killer Cells for Tumor Immunotherapy. Front Immunol. 2020;11:60. DOI:10.3389/fimmu.2020.00060
22. Sun C, Sun HY, Xiao WH, et al. Natural killer cell dysfunction in hepatocellular carcinoma and NK cell-based immunotherapy. Acta Pharmacol Sin. 2015;36:1191‑9. DOI:10.1038/aps.2015.41
23. Habif G, Crinier A, Andre P, et al. Targeting natural killer cells in solid tumors. Cell Mol Immunol. 2019;16:415-22. DOI:10.1038/s41423-019-0224-2
24. Bi J, Tian Z. NK Cell exhaustion. Front Immunol. 2017;8:760. DOI:10.3389/fimmu.2017.00760
25. Wang W, Jiang J, Wu C. CAR-NK for tumor immunotherapy: Clinical transformation and future prospects. Cancer Lett. 2020;472:175-80. DOI:10.1016/j.canlet.2019.11.033
26. Wang L, Dou M, Ma Q, et al. Chimeric antigen receptor (CAR)-modified NK cells against cancer: Opportunities and challenges. Int Immunopharmacol. 2019;74:105695. DOI:10.1016/j.intimp.2019.105695
27. Rotolo R, Leuci V, Donini C, et al. CAR-Based Strategies beyond T Lymphocytes: Integrative Opportunities for Cancer Adoptive Immunotherapy. Int J Mol Sci. 2019;20:2839. DOI:10.3390/ijms20112839
28. Boissel L, Betancur M, Wels WS, et al. Transfection with mRNA for CD19 specific huchimeric antigen receptor restores NK cell mediated killing of CLL cells. Leuk Res. 2009;33:1255-9. DOI:10.1016/j.leukres.2008.11.024
29. Romee R, Schneider SE, Leong JW, et al. Cytokine activation induces human memory-like NK cells. Blood. 2012;120:4751-60. DOI:10.1182/blood-2012-04-419283
30. Acharya UH, Dhawale T, Yun S, et al. Management of cytokine release syndrome and neurotoxicity in chimeric antigen receptor (CAR) T cell therapy. Expert Rev Hematol. 2019;12:195-205. DOI:10.1080/17474086.2019.1585238
31. Bryceson YT, March ME, Ljunggren HG, Long EO. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol Rev. 2006;214:73‑91.
DOI:10.1111/j.1600-065X.2006.00457.x
32. Olson JA, Leveson-Gower DB, Gill S, et al. NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects. Blood. 2010;115:4293-301. DOI:10.1182/blood-2009-05-222190
33. Oberschmidt O, Kloess S, Koehl U. Redirected Primary Human Chimeric Antigen Receptor Natural Killer Cells as an “off-the-Shelf Immunotherapy” for Improvement in Cancer Treatment. Front Immunol. 2017;8:654. DOI:10.3389/fimmu.2017.00654
34. MacKay M, Afshinnekoo E, Rub J, et al. The therapeutic landscape for cells engineered with chimeric antigen receptors. Nat Biotechnol. 2020;38(2):233-44.
DOI:10.1038/s41587-019-0329-2
35. Tang X, Yang L, Li Z, et al. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am J Cancer Res. 2018;8(6):1083-9.
36. Liu E, Marin D, Banerjee P, et al. Use of CAR-Transduced Natural Killer Cells in CD19-Positive Lymphoid Tumors. N Engl J Med. 2020;382(6):545-53. DOI:10.1056/NEJMoa1910607
37. Liu E, Tong Y, Dotti G, et al. Cord blood NK cells engineered to express IL-15 and a CD19-targeted CAR show long-term persistence and potent antitumor activity. Leukemia. 2018;32(2):520-31. DOI:10.1038/leu.2017.226
38. Li Y, Hermanson DL, Moriarity BS, Kaufman DS. Human iPSC-Derived Natural Killer Cells Engineered with Chimeric Antigen Receptors Enhance Anti-tumor Activity. Cell Stem Cell. 2018;23(2):181-92.e5. DOI:10.1016/j.stem.2018.06.002
39. Pfefferle A, Huntington ND. You Have Got a Fast CAR: Chimeric Antigen Receptor NK Cells in Cancer Therapy. Cancers. 2020;12:706. DOI:10.3390/cancers12030706
40. Quintarelli C, Sivori S, Caruso S, et al. Efficacy of third-party chimeric antigen receptor modified peripheral blood natural killer cells for adoptive cell therapy of B-cell precursor acute lymphoblastic leukemia. Leukemia. 2020;34(4):1102‑15. DOI:10.1038/s41375-019-0613-7
41. van Ostaijen-ten Dam MM, Prins HJ, Boerman GH, et al. Preparation of Cytokine-activated NK Cells for Use in Adoptive Cell Therapy in Cancer Patients: Protocol Optimization and Therapeutic Potential. J Immunother. 2016;39(2):90-100. DOI:10.1097/CJI.0000000000000110
42. Domogala A, Madrigal JA, Saudemont A. Cryopreservation has no effect on function of natural killer cells differentiated in vitro from umbilical cord blood CD34(+) cells. Cytotherapy. 2016;18(6):754-9. DOI:10.1016/j.jcyt.2016.02.008
43. Shah NN, Baird K, Delbrook CP, et al. Acute GVHD in patients receiving IL-15/4-1BBL activated NK cells following T-cell-depleted stem cell transplantation. Blood. 2015;125(5):784-92. DOI:10.1182/blood-2014-07-592881
2. DeSantis CE, Miller KD, Dale W, et al. Cancer statistics for adults aged 85 years and older, 2019. CA Cancer J Clin. 2019;69:452-67. DOI:10.3322/caac.21577
3. Oostindie SC, van der Horst HJ, Kil LP, et al. DuoHexaBody-CD37((R)), a novel biparatopic CD37 antibody with enhanced Fc-mediated hexamerization as a potential therapy for B-cell malignancies. Blood Cancer J. 2020;10(3):30. DOI:10.1038/s41408-020-0292-7
4. Bonello F, D’Agostino M, Moscvin M, et al. CD38 as an immunotherapeutic target in multiple myeloma. Expert Opin Biol Ther. 2018;18:1209-21. DOI:10.1080/14712598.2018.1544240
5. Salles G, Barrett M, Foa R, et al. Rituximab in B-Cell Hematologic Malignancies: A Review of 20 Years of Clinical Experience. Adv Ther. 2017;34:2232-73.
DOI:10.1007/s12325-017-0612-x
6. Mori Y, Choi I, Yoshimoto G, et al. Phase I/II study of bortezomib, lenalidomide, and dexamethasone treatment for relapsed and refractory multiple myeloma. Int J Hematol. 2020;111:673-80. DOI:10.1007/s12185-020-02833-w
7. Fathi E, Farahzadi R, Sheervalilou R, et al. A general view of CD33(+) leukemic stem cells and CAR-T cells as interesting targets in acute myeloblatsic leukemia therapy. Blood Res. 2020;55:10-6. DOI:10.5045/br.2020.55.1.10
8. Lee HR, Baek KH. Role of natural killer cells for immunotherapy in chronic myeloid leukemia (Review). Oncol Rep. 2019;41:2625-35. DOI:10.3892/or.2019.7059
9. Van Acker HH, Versteven M, Lichtenegger FS, et al. Dendritic Cell-Based Immunotherapy of Acute Myeloid Leukemia. J Clin Med. 2019;8:579. DOI:10.3390/jcm8050579
10. Song W, Zhang M. Use of CAR-T cell therapy, PD-1 blockade, and their combination for the treatment of hematological malignancies. Clin Immunol. 2020;214:108382. DOI:10.1016/j.clim.2020.108382
11. Грибкова И.В., Завьялов А.А. Терапия Т-лимфоцитами с химерным антигенным рецептором (CAR) В-клеточной неходжкинской лимфомы: возможности и проблемы. Вопросы онкологии. 2021;67(3):350-60 [Gribkova IV, Zavyalov AA. Chimeric antigen receptor T-cell therapy for B-cell non-Hodgkin lymphoma: opportunities and challenges. Voprosy onkologii. 2021;67(3):350-60 (in Russian)]. DOI:10.37469/0507-3758-2021-67-3-350-360
12. Грибкова И.В., Завьялов А.А. CAR Т-клетки для лечения хронического лимфоцитарного лейкоза. Клиническая онкогематология. 2021;14(2):225-30 [Gribkova IV, Zavyalov AA. CAR T-cells for the treatment of chronic lymphocytic leukemia. Klinicheskaia onkogematologiia. 2021;14(2):225-30 (in Russian)]. DOI:10.21320/2500-2139-2021-14-2-225-230
13. Боробова Е.А., Жеравин А.А. Натуральные киллеры в иммунотерапии онкологических заболеваний. Сибирский онкологический журнал. 2018;17(6):97‑104 [Borobova EA, Zheravin AA. Natural killer cels in immunotherapy for cancer. Sibirskij onkologicheskij zhurnal. 2018;17(6):97-104 (in Russian)]. DOI:10.21294/1814-4861-2018-17-6-97-104
14. Hu Y, Tian Zh, Zhang C. Chimeric antigen receptor (CAR)-transduced natural killer cells in tumor immunotherapy. Acta Pharmacologica Sinica. 2018;39:167‑76. DOI:10.1038/aps.2017.125
15. Orange JS. Natural killer cell deficiency. J Allergy Clin Immunol. 2013;132:515‑25. DOI:10.1016/j.jaci.2013.07.020
16. Xie G, Dong H, Liang Y, et al. CAR-NK cells: A promising cellular immunotherapy for cancer. EBioMedicine. 2020;59:102975. DOI:10.1016/j.ebiom.2020.102975
17. Lanier LL. Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol. 2008;9(5):495-502. DOI:10.1038/ni1581
18. Hofland T, Eldering E, Kater AP, Tonino SH. Engaging Cytotoxic T and NK Cells for Immunotherapy in Chronic Lymphocytic Leukemia. Int J Mol Sci. 2019;20(17):4315. DOI:10.3390/ijms20174315
19. Wang W, Erbe AK, Hank JA, et al. NK cell-mediated antibodydependent cellular cytotoxicity in cancer immunotherapy. Front Immunol 2015;6:368. DOI:10.3389/fimmu.2015.00368
20. Vivier E, Raulet DH, Moretta A, et al. Innate or adaptive immunity? The example of natural killer cells. Science. 2011;331(6013):44-9. DOI:10.1126/science.1198687
21. Zhang C, Hu Y, Shi C. Targeting Natural Killer Cells for Tumor Immunotherapy. Front Immunol. 2020;11:60. DOI:10.3389/fimmu.2020.00060
22. Sun C, Sun HY, Xiao WH, et al. Natural killer cell dysfunction in hepatocellular carcinoma and NK cell-based immunotherapy. Acta Pharmacol Sin. 2015;36:1191‑9. DOI:10.1038/aps.2015.41
23. Habif G, Crinier A, Andre P, et al. Targeting natural killer cells in solid tumors. Cell Mol Immunol. 2019;16:415-22. DOI:10.1038/s41423-019-0224-2
24. Bi J, Tian Z. NK Cell exhaustion. Front Immunol. 2017;8:760. DOI:10.3389/fimmu.2017.00760
25. Wang W, Jiang J, Wu C. CAR-NK for tumor immunotherapy: Clinical transformation and future prospects. Cancer Lett. 2020;472:175-80. DOI:10.1016/j.canlet.2019.11.033
26. Wang L, Dou M, Ma Q, et al. Chimeric antigen receptor (CAR)-modified NK cells against cancer: Opportunities and challenges. Int Immunopharmacol. 2019;74:105695. DOI:10.1016/j.intimp.2019.105695
27. Rotolo R, Leuci V, Donini C, et al. CAR-Based Strategies beyond T Lymphocytes: Integrative Opportunities for Cancer Adoptive Immunotherapy. Int J Mol Sci. 2019;20:2839. DOI:10.3390/ijms20112839
28. Boissel L, Betancur M, Wels WS, et al. Transfection with mRNA for CD19 specific huchimeric antigen receptor restores NK cell mediated killing of CLL cells. Leuk Res. 2009;33:1255-9. DOI:10.1016/j.leukres.2008.11.024
29. Romee R, Schneider SE, Leong JW, et al. Cytokine activation induces human memory-like NK cells. Blood. 2012;120:4751-60. DOI:10.1182/blood-2012-04-419283
30. Acharya UH, Dhawale T, Yun S, et al. Management of cytokine release syndrome and neurotoxicity in chimeric antigen receptor (CAR) T cell therapy. Expert Rev Hematol. 2019;12:195-205. DOI:10.1080/17474086.2019.1585238
31. Bryceson YT, March ME, Ljunggren HG, Long EO. Activation, coactivation, and costimulation of resting human natural killer cells. Immunol Rev. 2006;214:73‑91.
DOI:10.1111/j.1600-065X.2006.00457.x
32. Olson JA, Leveson-Gower DB, Gill S, et al. NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects. Blood. 2010;115:4293-301. DOI:10.1182/blood-2009-05-222190
33. Oberschmidt O, Kloess S, Koehl U. Redirected Primary Human Chimeric Antigen Receptor Natural Killer Cells as an “off-the-Shelf Immunotherapy” for Improvement in Cancer Treatment. Front Immunol. 2017;8:654. DOI:10.3389/fimmu.2017.00654
34. MacKay M, Afshinnekoo E, Rub J, et al. The therapeutic landscape for cells engineered with chimeric antigen receptors. Nat Biotechnol. 2020;38(2):233-44.
DOI:10.1038/s41587-019-0329-2
35. Tang X, Yang L, Li Z, et al. First-in-man clinical trial of CAR NK-92 cells: safety test of CD33-CAR NK-92 cells in patients with relapsed and refractory acute myeloid leukemia. Am J Cancer Res. 2018;8(6):1083-9.
36. Liu E, Marin D, Banerjee P, et al. Use of CAR-Transduced Natural Killer Cells in CD19-Positive Lymphoid Tumors. N Engl J Med. 2020;382(6):545-53. DOI:10.1056/NEJMoa1910607
37. Liu E, Tong Y, Dotti G, et al. Cord blood NK cells engineered to express IL-15 and a CD19-targeted CAR show long-term persistence and potent antitumor activity. Leukemia. 2018;32(2):520-31. DOI:10.1038/leu.2017.226
38. Li Y, Hermanson DL, Moriarity BS, Kaufman DS. Human iPSC-Derived Natural Killer Cells Engineered with Chimeric Antigen Receptors Enhance Anti-tumor Activity. Cell Stem Cell. 2018;23(2):181-92.e5. DOI:10.1016/j.stem.2018.06.002
39. Pfefferle A, Huntington ND. You Have Got a Fast CAR: Chimeric Antigen Receptor NK Cells in Cancer Therapy. Cancers. 2020;12:706. DOI:10.3390/cancers12030706
40. Quintarelli C, Sivori S, Caruso S, et al. Efficacy of third-party chimeric antigen receptor modified peripheral blood natural killer cells for adoptive cell therapy of B-cell precursor acute lymphoblastic leukemia. Leukemia. 2020;34(4):1102‑15. DOI:10.1038/s41375-019-0613-7
41. van Ostaijen-ten Dam MM, Prins HJ, Boerman GH, et al. Preparation of Cytokine-activated NK Cells for Use in Adoptive Cell Therapy in Cancer Patients: Protocol Optimization and Therapeutic Potential. J Immunother. 2016;39(2):90-100. DOI:10.1097/CJI.0000000000000110
42. Domogala A, Madrigal JA, Saudemont A. Cryopreservation has no effect on function of natural killer cells differentiated in vitro from umbilical cord blood CD34(+) cells. Cytotherapy. 2016;18(6):754-9. DOI:10.1016/j.jcyt.2016.02.008
43. Shah NN, Baird K, Delbrook CP, et al. Acute GVHD in patients receiving IL-15/4-1BBL activated NK cells following T-cell-depleted stem cell transplantation. Blood. 2015;125(5):784-92. DOI:10.1182/blood-2014-07-592881
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1. Kaprin AD, Starinskij VV, Petrova GV, et al. Zlokachestvennye novoobrazovaniya v Rossii v 2018 godu (zabolevaemost' i smertnost'). Moscow: MNIOI im. P.A. Gercena – filial FGBU «NMIC radiologii» Minzdrava Rossii, 2019 (in Russian).
2. DeSantis CE, Miller KD, Dale W, et al. Cancer statistics for adults aged 85 years and older, 2019. CA Cancer J Clin. 2019;69:452-67. DOI:10.3322/caac.21577
3. Oostindie SC, van der Horst HJ, Kil LP, et al. DuoHexaBody-CD37((R)), a novel biparatopic CD37 antibody with enhanced Fc-mediated hexamerization as a potential therapy for B-cell malignancies. Blood Cancer J. 2020;10(3):30. DOI:10.1038/s41408-020-0292-7
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Авторы
И.В. Грибкова*
ГБУ города Москвы «Научно-исследовательский институт организации здравоохранения и медицинского менеджмента Департамента здравоохранения города Москвы», Москва, Россия
*igribkova@yandex.ru
ГБУ города Москвы «Научно-исследовательский институт организации здравоохранения и медицинского менеджмента Департамента здравоохранения города Москвы», Москва, Россия
*igribkova@yandex.ru
________________________________________________
Irina V. Gribkova*
Research Institute for Healthcare Organization and Medical Management of Moscow Healthcare Department, Moscow, Russia
*igribkova@yandex.ru
Цель портала OmniDoctor – предоставление профессиональной информации врачам, провизорам и фармацевтам.