Российский биотерапевтический журнал. 2024; 23: 22-29
Влияние спонтанной регрессии опухоли на прогрессию меланомы
Титов К. С., Сорокина М. В., Паклина О. В., Киселевский М. В., Лебедев С. С., Лунина А. В.
https://doi.org/10.17650/1726-9784-2024-23-4-22-29Аннотация
Введение. Меланома кожи (МК) – злокачественная неэпителиальная опухоль из трансформированных меланоцитов с преимущественной локализацией на коже (более 90 % случаев). Согласно статистике за 2021 г., в России МК составила 1,82 % всех злокачественных новообразований взрослого населения и 12,65 % всех опухолей кожи. Отмечается неуклонный и ежегодный рост заболеваемости МК во всем мире, особенно в странах с населением преимущественно европеоидной расы. В России за последние 10 лет смертность от МК увеличилась на 17,6 %. МК – гетерогенная опухоль с высоким метастатическим потенциалом, вследствие чего, помимо стандартных клинических и патоморфологических прогностических факторов, выявление дополнительных факторов прогрессии и неблагоприятного прогноза заболевания остается актуальной и не решенной до конца проблемой современной онкологии.
Цель исследования – определить роль спонтанной регрессии опухоли при возникновении прогрессии МК на основе анализа данных литературы и их систематизации.
Результаты. Представленный обзор литературы отражает различные мировые данные исследователей о роли спонтанной регрессии МК при прогрессировании. Спонтанная регрессия МК представляет собой иммунологический процесс, при котором наблюдается исчезновение опухолевых клеток, что приводит к разделению опухоли на отдельные островки с промежуточными участками неопухолевой ткани. Механизм возникновения спонтанной регрессии первичной МК, как и ее прогностическая значимость, недостаточно понятен и изучен. Большинство исследователей в первую очередь связывают возникновение спонтанной регрессии меланомы с иммунным ответом, так как во всех случаях регрессии отмечалась лимфоцитарная инфильтрация опухоли. Наличие лимфоидной инфильтрации, а также количественное и качественное соотношение ее клеток имеют значение в развитии опухолевого процесса, влияют на эффективность иммунотерапии и являются в большей степени фактором благоприятного прогноза для пациента.
Заключение. Прогностическая роль спонтанной регрессии меланомы до сих пор остается нерешенным и спорным вопросом. Интересно то, что ряд исследований демонстрируют следующее: регрессия есть независимый предиктор прогрессирования МК.
Список литературы
1. Каприн А.Д., Старинский В.В., Шахзадова А.О., Лисичникова И.В. Злокачественные новообразования в России в 2022 году (заболеваемость и смертность). М.: МНИОИ им. П.А. Герцена – филиал ФГБУ «НМИЦ радиологии» Минздрава России, 2023. 275 с.
2. Потекаев Н.Н., Титов К.С., Маркин А.А., Кашурников А.Ю. Эпидемиология меланомы кожи в Российской Федерации и в городе Москве за 10 лет (2008–2018 гг.). Клиническая дерматология и венерология 2020;19(6):810–6. DOI: 10.17116/klinderma202019061810
3. Эркенова Ф.Д., Пузин С.Н. Статистика меланомы в России и странах Европы. Медико-социальная экспертиза и реабилитация 2020;23(1):44–52. DOI: 10.17816/MSER34259
4. van den Berg J.H., Heemskerk B., van Rooij N. et al. Tumor infiltrating lymphocytes (TIL) therapy in metastatic melanoma: boosting of neoantigen-specific T cell reactivity and long-term follow-up. J Immunother Cancer 2020;8(2):e000848. DOI: 10.1136/jitc-2020-000848
5. Mulder E.E.A.P., Dwarkasing J.T., Tempel D. et al. Validation of a clinicopathological and gene expression profile model for sentinel lymph node metastasis in primary cutaneous melanoma. Br J Dermatol 2021;184(5):944–51. DOI: 10.1111/bjd.19499
6. Khosravi H., Akabane A.L., Alloo A. et al. Metastatic melanoma with spontaneous complete regression of a thick primary lesion. JAAD Case Rep 2016;2(6):439–41. DOI: 10.1016/j.jdcr.2016.09.011
7. Shah S., Al-Omari A., Cook K.W. et al. What do cancer-specific T cells ‘see’? Discov Immunol 2022;2(1):kyac011. DOI: 10.1093/discim/kyac011
8. Motofei I.G. Melanoma and autoimmunity: spontaneous regressions as a possible model for new therapeutic approaches. Melanoma Res 2019;29(3):231–6. DOI: 10.1097/CMR.0000000000000573
9. Larkin J., Chiarion-Sileni V., Gonzales R. et al. Five-year survival with combined nivolumab and ipilimumab in advance melanoma. N Engl J Med 2019;381(16):1535–46. DOI: 10.1056/NEJMoa1910836
10. Pan C., Shang J., Jiang H. et al. Transcriptome analysis reveals the molecular immunological characteristics of lesions in patients with halo nevi when compared to stable vitiligo, normal nevocytic nevi and cutaneous melanoma. J Inflamm Res 2021;14:4111–24. DOI: 10.2147/JIR.S321672
11. Aung P.P., Nagarajan P., Prieto V.G. Regression in primary cutaneous melanoma: etiopathogenesis and clinical significance. Lab Investig 2017;97(6):657–68. DOI: 10.1038/labinvest.2017.8
12. Osella-Abate S., Conti L., Annaratone L. et al. Phenotypic characterisation of immune cells associated with histological regression in cutaneous melanoma. Pathology 2019;51(5):487–93. DOI: 10.1016/j.pathol.2019.04.001
13. Blanc F., Bertho N., Piton G. et al. Deciphering the immune reaction leading to spontaneous melanoma regression: initial role of MHCII+ CD163– macrophages. Cancer Immunol Immunother 2023;72(11):3507–21. DOI: 10.1007/s00262-023-03503-6
14. Gauthier L., Morel A., Anceriz N. et al. Multifunctional natural killer cell engagers targeting NKp46 trigger protective tumor immunity. Cell 2019;177(7):1701–13. DOI: 10.1016/j.cell.2019.04.041
15. Rahimi A., Malakoutikhah Z., Rahimmanesh I. et al. The nexus of natural killer cells and melanoma tumor microenvironment: crosstalk, chemotherapeutic potential, and innovative NK cell-based therapeutic strategies. Cancer Cell Int 2023;23(1):312. DOI: 10.1186/s12935-023-03134-y
16. Nakai Y., Ueki A., Yamanaka K. Progressive vitiligo induced by recurrent melanoma. Clin Case Rep 2022;10(1):e05290. DOI: 10.1002/ccr3.5290
17. Paolino G., Pampena R., Di Ciaccio S.M. et al. Thin amelanotic and hypomelanotic melanoma: clinicopathological and dermoscopic features. Medicina (Kaunas) 2024;60(8):1239. DOI: 10.3390/medicina60081239
18. Ribero S., Moscarella E., Ferrara G. et al. Regression in cutaneous melanoma: a comprehensive review from diagnosis to prognosis. J Eur Acad Dermatol Venereol 2016;30(12):2030–7. DOI: 10.1111/jdv.13815
19. Cartron A.M., Aldana P.C., Khachemoune A. Reporting regression in primary cutaneous melanoma. Part 1: history, histological criteria and pathogenesis. Clin Exp Dermatol 2021;46(1):28–33. DOI: 10.1111/ced.14328
20. Conde E., Casares N., Mancheño U. et al. FOXP3 expression diversifies the metabolic capacity and enhances the efficacy of CD8 T cells in adoptive immunotherapy of melanoma. Mol Ther 2023;31(1):48–65. DOI: 10.1016/j.ymthe.2022.08.017
21. Maibach F., Sadozai H., Seyed Jafari S.M. et al. Tumorinfiltrating lymphocytes and their prognostic value in cutaneous melanoma. Front Immunol 2020;11:2105. DOI: 10.3389/fimmu.2020.02105
22. Camisaschi C., Vallacchi V., Castelli C. et al. Immune cells in the melanoma microenvironment hold information for prediction of the risk of recurrence and response to treatment. Expert Rev Mol Diagn 2014;14(6):643–6. DOI: 10.1586/14737159.2014.928206
23. Taylor R.C., Patel A., Panageas K.S. et al. Tumor-infiltrating lymphocytes predict sentinel lymph node positivity in patients with cutaneous melanoma. J Clin Oncol 2007;25(7):869–75. DOI: 10.1200/JCO.2006.08.9755
24. Жулай Г.А., Олейник Е.К. Регуляторные Т-лимфоциты CD4+CD25+FoxP3+. Перспективы применения в иммунотерапии. Труды Карельского научного центра Российской академии наук 2012;2:3–17.
25. Zhou Z., Xu J., Liu S. et al. Infiltrating treg reprogramming in the tumor immune microenvironment and its optimization for immunotherapy. Biomark Res 2024;12(1):97. DOI: 10.1186/s40364-024-00630-9
26. Бережная Н.М. Роль клеток системы иммунитета в микроокружении опухоли. Клетки и цитокины – участники воспаления. Онкология 2009;11(1):6–17.
27. Gerber A.L., Münst A., Schlapbach C. et al. High expression of FOXP3 in primary melanoma is associated with tumour progression. Br J Dermatol 2014;170(1):103–9. DOI: 10.1111/bjd.12641
28. Knol A.C., Nguyen J.M., Quéreux G. et al. Prognostic value of tumor-infiltrating Foxp3+ T-cell subpopulations in metastatic melanoma. Exp Dermatol 2011;20(5):430–4. DOI: 10.1111/j.1600-0625.2011.01260
29. Fujii H., Arakawa A., Kitoh A. et al. Perturbations of both nonregulatory and regulatory FOXP3+ T cells in patients with malignant melanoma. J Dermatol 2011;164(5):1052–60. DOI: 10.1111/j.1365-2133.2010.10199
30. Morrison S.L., Han G., Elenwa F. et al.; Sentinel Lymph Node Working Group. Is the presence of tumor-infiltrating lymphocytes predictive of outcomes in patients with melanoma? Cancer 2022;128(7):1418–28. DOI: 10.1002/cncr.34013
31. Grigore L.E., Ungureanu L., Bejinariu N. et al. Complete regression of primary melanoma associated with nevi involution under BRAF inhibitors: A case report and review of the literature. Oncol Lett 2019;17(5):4176–82. DOI: 10.3892/ol.2018.9738
32. Сергеев Ю.Ю., Мордовцева В.В. Меланома кожи с явлениями регресса: описание клинического случая и обзор литературы. Клиническая дерматология и венерология 2017;16(5):36–41. DOI: 10.17116/klinderma201716536-41
33. Kocsis A., Karsko L., Kurgyis Z. et al. Is it necessary to perform sentinel lymph node biopsy in thin melanoma? A retrospective single center analysis. Pathol Oncol Res 2020;26(3):1861–8. DOI: 10.1007/s12253-019-00769-z
34. Vargas G.M., Shafique N., Xu X., Karakousis G. Tumorinfiltrating lymphocytes as a prognostic and predictive factor for melanoma. Expert Rev Mol Diagn 2024;24(4):299–310. DOI: 10.1080/14737159.2024.2312102
35. Bastian B.C. Hypothesis: a role for telomere crisis in spontaneous regression of melanoma. Arch Dermatol 2003;139(5):667–8. DOI: 10.1001/archderm.139.5.667
36. Cartron A.M., Aldana P.C., Khachemoune A. Reporting regression in primary cutaneous melanoma. Part 2: prognosis, evaluation and management. Clin Exp Dermatol 2020;45(7):818–23. DOI: 10.1111/ced.14329
37. Morris K.T., Busam K.J., Bero S. et al. Primary cutaneous melanoma with regression does not require a lower threshold for sentinel lymph node biopsy. Ann Surg Oncol 2008;15(1):316–22. DOI: 10.1245/s10434-007-9675-2
38. Rubinstein J.C., Han G., Jackson L. et al. Regression in thin melanoma is associated with nodal recurrence after a negative sentinel node biopsy. Cancer Med 2016;5(10):2832–40. DOI: 10.1002/cam4.922
39. Aivazian K., Ahmed T., El Sharouni M.A. et al. Correction to: Histological regression in melanoma: impact on sentinel lymph node status and survival. Mod Pathol 2021;34(11):2091. DOI: 10.1038/s41379-021-00878-8
40. El Sharouni M., Aivazian K., Witkamp A.J. et al. Association of histologic regression with a favorable outcome in patients with stage 1 and stage 2 cutaneous melanoma. JAMA Dermatol 2021;157(2):166–73. DOI:10.1001/jamadermatol.2020.5032
41. Kaur C., Thomas R.J., Desai N. et al. The correlation of regression in primary melanoma with sentinel lymph node status. J Clin Pathol 2008;61(3):297–300. DOI: 10.1136/jcp.2007.049411
42. Tas F., Erturk K. Presence of histological regression as a prognostic factor in cutaneous melanoma patients. Melanoma Res 2016;26(5):492–6. DOI: 10.1097/CMR.0000000000000277
43. Morrison S., Han G., Elenwa F. et al.; Sentinel Lymph Node Working Group. Is there a relationship between TILs and regression in melanoma? Ann Surg Oncol 2022;29(5):2854–66. DOI: 10.1245/s10434-021-11251-z
Russian Journal of Biotherapy. 2024; 23: 22-29
The effect of spontaneous tumor regression on melanoma progression
Titov K. S., Sorokina M. V., Paklina O. V., Kiselevskiy M. V., Lebedev S. S., Lunina A. V.
https://doi.org/10.17650/1726-9784-2024-23-4-22-29Abstract
Background. Skin melanoma (SM) is a malignant non-epithelial tumor of transformed melanocytes with predominant localization on the skin (more than 90 % of cases). According to statistics for 2021, SM in Russia accounted for 1.82 % of all malignant neoplasms of the adult population and 12.65 % of all skin tumors. There has been a steady and annual increase in the incidence of SM throughout the world, especially in countries with a predominantly Caucasian population. In Russia, over the past 10 years, mortality from SM has increased by 17.6 %. SM is a heterogeneous tumor with a high metastatic potential, because in addition to standard clinical and pathomorphological prognostic factors, the identification of additional factors of progression and unfavorable prognosis of the disease remains an urgent and unresolved problem of modern oncology.
Aim. To determine the role of spontaneous tumor regression in the occurrence of SM progression based on the analysis of literature data and their systematization.
Results. This literature review reflects various global research data on the role of spontaneous regression of SM in progression. Spontaneous regression of SM is an immunological process in which the disappearance of tumor cells is observed, which leads to the division of the tumor into separate islands with intermediate areas of non-tumor tissue. The mechanism of spontaneous regression of primary SM, as well as its prognostic significance, is not well understood and studied. Of course, most researchers primarily associate the occurrence of spontaneous regression of melanoma with an immune response, since lymphocytic infiltration of the tumor was noted in all cases of regression. The presence of lymphoid infiltration, as well as the quantitative and qualitative ratio of its cells, are important in the development of the tumor process, affect the effectiveness of immunotherapy and is to a greater extent a factor in a favorable prognosis.
Conclusion. The prognostic role of spontaneous melanoma regression is still an unresolved and controversial issue. Interestingly, a number of studies demonstrate that regression is an independent predictor of the progression of SM.
References
1. Kaprin A.D., Starinskii V.V., Shakhzadova A.O., Lisichnikova I.V. Zlokachestvennye novoobrazovaniya v Rossii v 2022 godu (zabolevaemost' i smertnost'). M.: MNIOI im. P.A. Gertsena – filial FGBU «NMITs radiologii» Minzdrava Rossii, 2023. 275 s.
2. Potekaev N.N., Titov K.S., Markin A.A., Kashurnikov A.Yu. Epidemiologiya melanomy kozhi v Rossiiskoi Federatsii i v gorode Moskve za 10 let (2008–2018 gg.). Klinicheskaya dermatologiya i venerologiya 2020;19(6):810–6. DOI: 10.17116/klinderma202019061810
3. Erkenova F.D., Puzin S.N. Statistika melanomy v Rossii i stranakh Evropy. Mediko-sotsial'naya ekspertiza i reabilitatsiya 2020;23(1):44–52. DOI: 10.17816/MSER34259
4. van den Berg J.H., Heemskerk B., van Rooij N. et al. Tumor infiltrating lymphocytes (TIL) therapy in metastatic melanoma: boosting of neoantigen-specific T cell reactivity and long-term follow-up. J Immunother Cancer 2020;8(2):e000848. DOI: 10.1136/jitc-2020-000848
5. Mulder E.E.A.P., Dwarkasing J.T., Tempel D. et al. Validation of a clinicopathological and gene expression profile model for sentinel lymph node metastasis in primary cutaneous melanoma. Br J Dermatol 2021;184(5):944–51. DOI: 10.1111/bjd.19499
6. Khosravi H., Akabane A.L., Alloo A. et al. Metastatic melanoma with spontaneous complete regression of a thick primary lesion. JAAD Case Rep 2016;2(6):439–41. DOI: 10.1016/j.jdcr.2016.09.011
7. Shah S., Al-Omari A., Cook K.W. et al. What do cancer-specific T cells ‘see’? Discov Immunol 2022;2(1):kyac011. DOI: 10.1093/discim/kyac011
8. Motofei I.G. Melanoma and autoimmunity: spontaneous regressions as a possible model for new therapeutic approaches. Melanoma Res 2019;29(3):231–6. DOI: 10.1097/CMR.0000000000000573
9. Larkin J., Chiarion-Sileni V., Gonzales R. et al. Five-year survival with combined nivolumab and ipilimumab in advance melanoma. N Engl J Med 2019;381(16):1535–46. DOI: 10.1056/NEJMoa1910836
10. Pan C., Shang J., Jiang H. et al. Transcriptome analysis reveals the molecular immunological characteristics of lesions in patients with halo nevi when compared to stable vitiligo, normal nevocytic nevi and cutaneous melanoma. J Inflamm Res 2021;14:4111–24. DOI: 10.2147/JIR.S321672
11. Aung P.P., Nagarajan P., Prieto V.G. Regression in primary cutaneous melanoma: etiopathogenesis and clinical significance. Lab Investig 2017;97(6):657–68. DOI: 10.1038/labinvest.2017.8
12. Osella-Abate S., Conti L., Annaratone L. et al. Phenotypic characterisation of immune cells associated with histological regression in cutaneous melanoma. Pathology 2019;51(5):487–93. DOI: 10.1016/j.pathol.2019.04.001
13. Blanc F., Bertho N., Piton G. et al. Deciphering the immune reaction leading to spontaneous melanoma regression: initial role of MHCII+ CD163– macrophages. Cancer Immunol Immunother 2023;72(11):3507–21. DOI: 10.1007/s00262-023-03503-6
14. Gauthier L., Morel A., Anceriz N. et al. Multifunctional natural killer cell engagers targeting NKp46 trigger protective tumor immunity. Cell 2019;177(7):1701–13. DOI: 10.1016/j.cell.2019.04.041
15. Rahimi A., Malakoutikhah Z., Rahimmanesh I. et al. The nexus of natural killer cells and melanoma tumor microenvironment: crosstalk, chemotherapeutic potential, and innovative NK cell-based therapeutic strategies. Cancer Cell Int 2023;23(1):312. DOI: 10.1186/s12935-023-03134-y
16. Nakai Y., Ueki A., Yamanaka K. Progressive vitiligo induced by recurrent melanoma. Clin Case Rep 2022;10(1):e05290. DOI: 10.1002/ccr3.5290
17. Paolino G., Pampena R., Di Ciaccio S.M. et al. Thin amelanotic and hypomelanotic melanoma: clinicopathological and dermoscopic features. Medicina (Kaunas) 2024;60(8):1239. DOI: 10.3390/medicina60081239
18. Ribero S., Moscarella E., Ferrara G. et al. Regression in cutaneous melanoma: a comprehensive review from diagnosis to prognosis. J Eur Acad Dermatol Venereol 2016;30(12):2030–7. DOI: 10.1111/jdv.13815
19. Cartron A.M., Aldana P.C., Khachemoune A. Reporting regression in primary cutaneous melanoma. Part 1: history, histological criteria and pathogenesis. Clin Exp Dermatol 2021;46(1):28–33. DOI: 10.1111/ced.14328
20. Conde E., Casares N., Mancheño U. et al. FOXP3 expression diversifies the metabolic capacity and enhances the efficacy of CD8 T cells in adoptive immunotherapy of melanoma. Mol Ther 2023;31(1):48–65. DOI: 10.1016/j.ymthe.2022.08.017
21. Maibach F., Sadozai H., Seyed Jafari S.M. et al. Tumorinfiltrating lymphocytes and their prognostic value in cutaneous melanoma. Front Immunol 2020;11:2105. DOI: 10.3389/fimmu.2020.02105
22. Camisaschi C., Vallacchi V., Castelli C. et al. Immune cells in the melanoma microenvironment hold information for prediction of the risk of recurrence and response to treatment. Expert Rev Mol Diagn 2014;14(6):643–6. DOI: 10.1586/14737159.2014.928206
23. Taylor R.C., Patel A., Panageas K.S. et al. Tumor-infiltrating lymphocytes predict sentinel lymph node positivity in patients with cutaneous melanoma. J Clin Oncol 2007;25(7):869–75. DOI: 10.1200/JCO.2006.08.9755
24. Zhulai G.A., Oleinik E.K. Regulyatornye T-limfotsity CD4+CD25+FoxP3+. Perspektivy primeneniya v immunoterapii. Trudy Karel'skogo nauchnogo tsentra Rossiiskoi akademii nauk 2012;2:3–17.
25. Zhou Z., Xu J., Liu S. et al. Infiltrating treg reprogramming in the tumor immune microenvironment and its optimization for immunotherapy. Biomark Res 2024;12(1):97. DOI: 10.1186/s40364-024-00630-9
26. Berezhnaya N.M. Rol' kletok sistemy immuniteta v mikrookruzhenii opukholi. Kletki i tsitokiny – uchastniki vospaleniya. Onkologiya 2009;11(1):6–17.
27. Gerber A.L., Münst A., Schlapbach C. et al. High expression of FOXP3 in primary melanoma is associated with tumour progression. Br J Dermatol 2014;170(1):103–9. DOI: 10.1111/bjd.12641
28. Knol A.C., Nguyen J.M., Quéreux G. et al. Prognostic value of tumor-infiltrating Foxp3+ T-cell subpopulations in metastatic melanoma. Exp Dermatol 2011;20(5):430–4. DOI: 10.1111/j.1600-0625.2011.01260
29. Fujii H., Arakawa A., Kitoh A. et al. Perturbations of both nonregulatory and regulatory FOXP3+ T cells in patients with malignant melanoma. J Dermatol 2011;164(5):1052–60. DOI: 10.1111/j.1365-2133.2010.10199
30. Morrison S.L., Han G., Elenwa F. et al.; Sentinel Lymph Node Working Group. Is the presence of tumor-infiltrating lymphocytes predictive of outcomes in patients with melanoma? Cancer 2022;128(7):1418–28. DOI: 10.1002/cncr.34013
31. Grigore L.E., Ungureanu L., Bejinariu N. et al. Complete regression of primary melanoma associated with nevi involution under BRAF inhibitors: A case report and review of the literature. Oncol Lett 2019;17(5):4176–82. DOI: 10.3892/ol.2018.9738
32. Sergeev Yu.Yu., Mordovtseva V.V. Melanoma kozhi s yavleniyami regressa: opisanie klinicheskogo sluchaya i obzor literatury. Klinicheskaya dermatologiya i venerologiya 2017;16(5):36–41. DOI: 10.17116/klinderma201716536-41
33. Kocsis A., Karsko L., Kurgyis Z. et al. Is it necessary to perform sentinel lymph node biopsy in thin melanoma? A retrospective single center analysis. Pathol Oncol Res 2020;26(3):1861–8. DOI: 10.1007/s12253-019-00769-z
34. Vargas G.M., Shafique N., Xu X., Karakousis G. Tumorinfiltrating lymphocytes as a prognostic and predictive factor for melanoma. Expert Rev Mol Diagn 2024;24(4):299–310. DOI: 10.1080/14737159.2024.2312102
35. Bastian B.C. Hypothesis: a role for telomere crisis in spontaneous regression of melanoma. Arch Dermatol 2003;139(5):667–8. DOI: 10.1001/archderm.139.5.667
36. Cartron A.M., Aldana P.C., Khachemoune A. Reporting regression in primary cutaneous melanoma. Part 2: prognosis, evaluation and management. Clin Exp Dermatol 2020;45(7):818–23. DOI: 10.1111/ced.14329
37. Morris K.T., Busam K.J., Bero S. et al. Primary cutaneous melanoma with regression does not require a lower threshold for sentinel lymph node biopsy. Ann Surg Oncol 2008;15(1):316–22. DOI: 10.1245/s10434-007-9675-2
38. Rubinstein J.C., Han G., Jackson L. et al. Regression in thin melanoma is associated with nodal recurrence after a negative sentinel node biopsy. Cancer Med 2016;5(10):2832–40. DOI: 10.1002/cam4.922
39. Aivazian K., Ahmed T., El Sharouni M.A. et al. Correction to: Histological regression in melanoma: impact on sentinel lymph node status and survival. Mod Pathol 2021;34(11):2091. DOI: 10.1038/s41379-021-00878-8
40. El Sharouni M., Aivazian K., Witkamp A.J. et al. Association of histologic regression with a favorable outcome in patients with stage 1 and stage 2 cutaneous melanoma. JAMA Dermatol 2021;157(2):166–73. DOI:10.1001/jamadermatol.2020.5032
41. Kaur C., Thomas R.J., Desai N. et al. The correlation of regression in primary melanoma with sentinel lymph node status. J Clin Pathol 2008;61(3):297–300. DOI: 10.1136/jcp.2007.049411
42. Tas F., Erturk K. Presence of histological regression as a prognostic factor in cutaneous melanoma patients. Melanoma Res 2016;26(5):492–6. DOI: 10.1097/CMR.0000000000000277
43. Morrison S., Han G., Elenwa F. et al.; Sentinel Lymph Node Working Group. Is there a relationship between TILs and regression in melanoma? Ann Surg Oncol 2022;29(5):2854–66. DOI: 10.1245/s10434-021-11251-z
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