ojrdrtОнкологический журнал: лучевая диагностика, лучевая терапияJournal of oncology: diagnostic radiology and radiotherapy2587-75932713-167XНЕКОММЕРЧЕСКОЕ ПАРТНЕРСТВО «ОБЩЕСТВО ИНТЕРВЕНЦИОННЫХ ОНКОРАДИОЛОГОВ»10.37174/2587-7593-2025-8-3-52-63ojrdrt-466Research ArticleЛУЧЕВАЯ ДИАГНОСТИКАDIAGNOSTIC RADIOLOGYРоль КТ и МРТ в оценке степени злокачественности нейроэндокринных опухолей поджелудочной железыThe role of CT and MRI in assessing the degree of malignancy of neuroendocrine tumors of the pancreashttps://orcid.org/0009-0005-2532-1956БелозерскихА. М.BelozerskikhA. M.

Анастасия Михайловна Белозерских 

115478, Москва, Каширское шоссе, 24 

Anastasiya M. Belozerskikh 

24 Kashirskoye Shosse, Moscow, 115478 

nastiabelozerka@mail.ruhttps://orcid.org/0000-0003-1779-003XМедведеваБ. М.MedvedevaB. M.

115478, Москва, Каширское шоссе, 24 

24 Kashirskoye Shosse, Moscow, 115478 

https://orcid.org/0000-0002-1295-4106ЛаптеваМ. Г.LaptevaM. G.

115478, Москва, Каширское шоссе, 24 

24 Kashirskoye Shosse, Moscow, 115478 

https://orcid.org/0000-0002-5548-1724МарковичА. А.MarkovichA. A.

115478, Москва, Каширское шоссе, 24 

24 Kashirskoye Shosse, Moscow, 115478 

https://orcid.org/0000-0001-8893-1894АбгарянМ. Г.AbgaryanM. G.

115478, Москва, Каширское шоссе, 24 

24 Kashirskoye Shosse, Moscow, 115478 

Национальный медицинский исследовательский центр онкологии им. Н. Н. Блохина Минздрава РоссииРоссияN.N. Blokhin National Medical Research Center of OncologyRussian Federation202523092025835263Copyright © Белозерских А.М., Медведева Б.М., Лаптева М.Г., Маркович А.А., Абгарян М.Г., 20252025Белозерских А.М., Медведева Б.М., Лаптева М.Г., Маркович А.А., Абгарян М.Г.Belozerskikh A.M., Medvedeva B.M., Lapteva M.G., Markovich A.A., Abgaryan M.G.Данная работа распространяется под лицензией Creative Commons Attribution 4.0.This work is licensed under a Creative Commons Attribution 4.0 License.https://www.oncoradjournal.ru/jour/article/view/466

Цель: Оценка диагностической значимости КТ и МРТ в определении степени злокачественности нейроэндокринных новообразований поджелудочной железы.Материалы и методы: В исследование включены 89 пациентов с нейроэндокринными опухолями (НЭО) поджелудочной железы. Диагноз устанавливался на основании морфологического исследования после выполненного хирургического вмешательства или биопсии опухоли. 54 пациента прошли КТ с контрастированием, 71 — МРТ с контрастированием. По данным КТ и МРТ оценивали размеры, форму, структуру и признаки некроза опухолей, а также измеряли количественные показатели плотности при КТ и интенсивности сигнала (ИС) при МРТ в опухолевой ткани в различных фазах контрастирования, вычисляли абсолютный и относительный проценты вымывания МР-контрастного средства (МРКС). Дополнительно по данным КТ определялось наличие кальцинатов в НЭО, по данным МРТ — ИС на Т2-взвешенных изображениях (ВИ), на диффузионновзвешенных изображениях (ДВИ) с b-фактором 50, 400 и 800с/мм2, на ИКД-картах измерялось значение измеряемого коэффициента диффузии (ИКД) на ИКД-картах.Результаты: При анализе данных КТ и МРТ выявлено, что размер опухоли не зависит от степени злокачественности и не коррелирует с индексом Ki-67. Количество узлов статистически значимо различалось: множественные поражения чаще встречались при Grade 1, а солитарные — при Grade 2. Форма и контуры опухолей также зависели от степени злокачественности: при Grade 1 преобладали овальные или округлые опухоли с четкими контурами, при Grade 3 — неправильной формы с нечеткими контурами, что сопровождалось более высоким уровнем Ki-67. Накопление контрастного препарата снижалось с увеличением степени злокачественности, особенно в артериальной и венозной фазах по данным КТ, при этом наблюдалась обратная связь с индексом Ki-67. Вымывание контрастного препарата по КТ было значительно ниже при Grade 3. По МРТ значимых различий в ИС и значении ИКД не выявлено, за исключением умеренной обратной связи ИС на T1 FS с Ki-67. Накопление и вымывание МРКС имели обратную корреляцию с Ki-67.Заключение: КТ и МРТ могут быть использованы в оценке степени злокачественности НЭО ПЖ, что улучшает предоперационную стратификацию риска. Наиболее надежные визуализируемые маркеры агрессивности включают нечеткие контуры, неправильную форму, гиповаскулярность, выраженный некроз, слабый или отрицательный процент вымывания КС и снижение ИС на T1 FS.

Purpose: Assessment of the diagnostic value of CT and MRI in determining the malignancy grade of pancreatic neuroendocrine tumors (NETs).Materials and methods: The study included 89 patients with pancreatic NETs. The diagnosis was established based on morphological examination after surgery or tumor biopsy. 54 patients underwent CT with contrast agent, 71 patients underwent MRI with MR contrast agent (MRCA). Based on CT and MRI data, the size, shape, structure, and signs of tumor necrosis were assessed, and quantitative indicators of density on CT and signal intensity on MRI in tumor tissue in different contrast phases were measured, and the absolute and relative percentages of contrast agent washout were calculated. Additionally, the presence of calcifications in NETs was determined using CT data, IS on T2-weighted images (WI), on diffusion-weighted images (DWI) with a b-factor of 50, 400 and 800 s/mm2 was determined using MRI data, and the value of the apparent diffusion coefficient (ADC) was measured on ADC-maps.Results: The analysis of CT and MRI data revealed that the tumor size did not depend on the degree of malignancy and did not correlate with the Ki-67 index. The number of nodes statistically significantly differed: multiple lesions were more common in Grade 1, and solitary ones in Grade 2. The shape and contours of the tumors also depended on the degree of malignancy: oval or round tumors with clear contours prevailed in Grade 1, while irregularly shaped tumors with unclear contours prevailed in Grade 3, which was accompanied by a higher Ki-67 level. Contrast agent accumulation decreased with increasing malignancy degree, especially in the arterial and venous phases according to CT data, while an inverse relationship with the Ki-67 index was observed. Contrast agent washout according to CT was significantly lower in Grade 3. No significant differences in contrast agent washout and ADC values were found in MRI, with the exception of a moderate inverse relationship between MRCA accumulation on T1-WI FS and Ki-67. MRCA accumulation and washout were inversely correlated with Ki-67.Conclusion: CT and MRI can be used to assess the grade of pancreatic NETs, improving preoperative risk stratification. The most reliable imaging markers of aggressiveness include poor margins, irregular shape, hypovascularity, severe necrosis, poor or negative washout, and decreased SI on T1-WI FS.

поджелудочная железанейроэндокринные опухолиМРТКТpancreasneuroendocrine tumorsMRICTReferencesКоханенко НЮ, Моргошия ТШ. Нейроэндокринные опухоли поджелудочной железы: этиология, патогенез, диагностика, современные аспекты лечения. Анналы хирургической гепатологии. 2018;23(2):100-10. https://doi.org/10.16931/1995-5464.20182100-110.Kokhanenko NYu, Morgoshiya TSh. Neuroendocrine tumors of the pancreas: etio-pathogenesis, diagnosis, current treatment. Annals of HPB Surgery. 2018;23(2):100-110. (In Russ.). https://doi.org/10.16931/1995-5464.20182100-110.Oberg K. Pancreatic endocrine tumors. Semin Oncol. 2010 Dec;37(6):594-618. https://doi.org/10.1053/j.seminoncol.2010.10.014.Oberg K. Pancreatic endocrine tumors. Semin Oncol. 2010 Dec;37(6):594-618. https://doi.org/10.1053/j.seminoncol.2010.10.014.Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9(1):61-72. https://doi.org/10.1016/S1470-2045(07)70410-2.Modlin IM, Oberg K, Chung DC, et al. Gastroenteropancreatic neuroendocrine tumours. Lancet Oncol. 2008;9(1):61-72. https://doi.org/10.1016/S1470-2045(07)70410-2.Dasari A, Shen C, Halperin D, et al. Trends in the Incidence, Prevalence, and Survival Outcomes in Patients With Neuroendocrine Tumors in the United States. JAMA Oncol. 2017;3(10):1335-42. https://doi.org/10.1001/jamaoncol.2017.0589Dasari A, Shen C, Halperin D, et al. Trends in the Incidence, Prevalence, and Survival Outcomes in Patients With Neuroendocrine Tumors in the United States. JAMA Oncol. 2017;3(10):1335-42. https://doi.org/10.1001/jamaoncol.2017.0589Fraenkel M, Kim M, Faggiano A, et al. NETwork. Incidence of gastroenteropancreatic neuroendocrine tumours: a systematic review of the literature. Endocr Relat Cancer. 2014;21(3):R153-63. https://doi.org/10.1530/ERC-13-0125.Fraenkel M, Kim M, Faggiano A, et al. NETwork. Incidence of gastroenteropancreatic neuroendocrine tumours: a systematic review of the literature. Endocr Relat Cancer. 2014;21(3):R153-63. https://doi.org/10.1530/ERC-13-0125.Rossi RE, Massironi S. The Increasing Incidence of Neuroendocrine Neoplasms Worldwide: Current Knowledge and Open Issues. J Clin Med. 2022;11:3794. https://doi.org/10.3390/jcm11133794.Rossi RE, Massironi S. The Increasing Incidence of Neuroendocrine Neoplasms Worldwide: Current Knowledge and Open Issues. J Clin Med. 2022;11:3794. https://doi.org/10.3390/jcm11133794.Pavel M, Öberg K, Falconi M, et al. ESMO Guidelines Committee. Electronic address: clinicalguidelines@esmo.org. Gastroenteropancreatic neuroendocrine neoplasms: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31(7):844-60. https://doi.org/10.1016/j.annonc.2020.03.304.Pavel M, Öberg K, Falconi M, et al. ESMO Guidelines Committee. Electronic address: clinicalguidelines@esmo.org. Gastroenteropancreatic neuroendocrine neoplasms: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2020;31(7):844-60. https://doi.org/10.1016/j.annonc.2020.03.304.Nagtegaal ID, Odze RD, Klimstra D, et al. WHO Classification of Tumours Editorial Board. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182-8. https://doi.org/10.1111/his.13975.Nagtegaal ID, Odze RD, Klimstra D, et al. WHO Classification of Tumours Editorial Board. The 2019 WHO classification of tumours of the digestive system. Histopathology. 2020;76(2):182-8. https://doi.org/10.1111/his.13975.La Rosa S. Diagnostic, Prognostic, and Predictive Role of Ki67 Proliferative Index in Neuroendocrine and Endocrine Neoplasms: Past, Present, and Future. Endocr Pathol. 2023;34(1):79-97. https://doi.org/10.1007/s12022-023-09755-3.La Rosa S. Diagnostic, Prognostic, and Predictive Role of Ki67 Proliferative Index in Neuroendocrine and Endocrine Neoplasms: Past, Present, and Future. Endocr Pathol. 2023;34(1):79-97. https://doi.org/10.1007/s12022-023-09755-3.Hofland J, Kaltsas G, de Herder WW. Advances in the Diagnosis and Management of Well-Differentiated Neuroendocrine Neoplasms. Endocr Rev. 2020;41(2):371-403. https://doi.org/10.1210/endrev/bnz004.Hofland J, Kaltsas G, de Herder WW. Advances in the Diagnosis and Management of Well-Differentiated Neuroendocrine Neoplasms. Endocr Rev. 2020;41(2):371-403. https://doi.org/10.1210/endrev/bnz004.Melhorn P, Raderer M, Mazal P. et al. NEC versus NET G3—is there a grey zone? Case report of pancreatic NET G3 with rapid disease progression. memo – Magazine of European Medical Oncology. 2024;17:310-4. https://doi.org/10.1007/s12254-024-00976-8.Melhorn P, Raderer M, Mazal P. et al. NEC versus NET G3—is there a grey zone? Case report of pancreatic NET G3 with rapid disease progression. memo – Magazine of European Medical Oncology. 2024;17:310-4. https://doi.org/10.1007/s12254-024-00976-8.Zappi A, Persano I, Galvani L, et al. Chemotherapy in Well Differentiated Neuroendocrine Tumors (NET) G1, G2, and G3: A Narrative Review. J Clin Med. 2023;12:717. https://doi.org/10.3390/jcm12020717.Zappi A, Persano I, Galvani L, et al. Chemotherapy in Well Differentiated Neuroendocrine Tumors (NET) G1, G2, and G3: A Narrative Review. J Clin Med. 2023;12:717. https://doi.org/10.3390/jcm12020717.Тoshima F, Inoue D, Komori T, et al. Is the combination of MR and CT findings useful in determining the tumor grade of pancreatic neuroendocrine tumors? Jpn J Radiol. 2017;35(5):242- 53. https://doi.org/10.1007/s11604-017-0627-x.Тoshima F, Inoue D, Komori T, et al. Is the combination of MR and CT findings useful in determining the tumor grade of pancreatic neuroendocrine tumors? Jpn J Radiol. 2017;35(5):242- 53. https://doi.org/10.1007/s11604-017-0627-x.Chiti G, Grazzini G, Cozzi D, et al. Imaging of Pancreatic Neuroendocrine Neoplasms. Int J Environ Res Public Health. 2021;18(17):8895. https://doi.org/10.3390/ijerph18178895.Chiti G, Grazzini G, Cozzi D, et al. Imaging of Pancreatic Neuroendocrine Neoplasms. Int J Environ Res Public Health. 2021;18(17):8895. https://doi.org/10.3390/ijerph18178895.Azoulay A, Cros J, Vullierme M-P, et al. Morphological imaging and CT histogram analysis to differentiate pancreatic neuroendocrine tumor grade 3 from neuroendocrine carcinoma. Diagnostic and Interventional Imaging, 2020;101(12):821-30. https://doi.org/10.1016/j.diii.2020.06.006Azoulay A, Cros J, Vullierme M-P, et al. Morphological imaging and CT histogram analysis to differentiate pancreatic neuroendocrine tumor grade 3 from neuroendocrine carcinoma. Diagnostic and Interventional Imaging, 2020;101(12):821-30. https://doi.org/10.1016/j.diii.2020.06.006Xie Y, Zhang S, Liu X, et al. Minimal apparent diffusion coefficient in predicting the Ki-67 proliferation index of pancreatic neuroendocrine tumors. Jpn J Radiol. 2022;40:823-30. https://doi.org/10.1007/s11604-022-01262-5Xie Y, Zhang S, Liu X, et al. Minimal apparent diffusion coefficient in predicting the Ki-67 proliferation index of pancreatic neuroendocrine tumors. Jpn J Radiol. 2022;40:823-30. https://doi.org/10.1007/s11604-022-01262-5Wang Y, Chen ZE, Yaghmai V, et al. Diffusion-weighted MR imaging in pancreatic endocrine tumors correlated with histopathologic characteristics. J Magn Reson Imaging. 2011;33(5):1071-9. https://doi.org/10.1002/jmri.22541.Wang Y, Chen ZE, Yaghmai V, et al. Diffusion-weighted MR imaging in pancreatic endocrine tumors correlated with histopathologic characteristics. J Magn Reson Imaging. 2011;33(5):1071-9. https://doi.org/10.1002/jmri.22541.De Robertis R, Cingarlini S, Tinazzi Martini P, et al. Pancreatic neuroendocrine neoplasms: Magnetic resonance imaging features according to grade and stage. World J Gastroenterol. 2017 Jan 14;23(2):275-85. https://doi.org/10.3748/wjg.v23.i2.275.De Robertis R, Cingarlini S, Tinazzi Martini P, et al. Pancreatic neuroendocrine neoplasms: Magnetic resonance imaging features according to grade and stage. World J Gastroenterol. 2017 Jan 14;23(2):275-85. https://doi.org/10.3748/wjg.v23.i2.275.Manfredi R, Bonatti M, Mantovani W, et al. Non-hyperfunctioning neuroendocrine tumours of the pancreas: MR imaging appearance and correlation with their biological behaviour. Eur Radiol. 2013;23:3029-39. https://doi.org/10.1007/s00330-013-2929-4Manfredi R, Bonatti M, Mantovani W, et al. Non-hyperfunctioning neuroendocrine tumours of the pancreas: MR imaging appearance and correlation with their biological behaviour. Eur Radiol. 2013;23:3029-39. https://doi.org/10.1007/s00330-013-2929-4Лозовая ВВ, Малихова ОА, Водолеев АС и др. Эндоскопическая радиочастотная абляция под контролем ультрасонографии как новый метод лечения нейроэндокринных опухолей поджелудочной железы и вариант анальгезии при местно-распространенных формах рака поджелудочной железы. Первый опыт в России. Хирургия и онкология. 2023;13(3):11-20. https://doi.org/10.17650/2949‑5857‑2023‑13‑3‑11‑20Lozovaya VV, Malikhova OA, Vodoleev AS et al. Endoscopic radiofrequency ablation under the control of ultrasonography as a new method of treatment of neuroendocrine pancreatic tumors and analgesia option for locally advanced forms of pancreatic cancer. First experience in Russia. Surgery and oncology. 2023;13(3):11-20. https://doi.org/10.17650/2949‑5857‑2023‑13‑3‑11‑20Falconi M, Eriksson B, Kaltsas G, et al. (2016). ENETS Consensus Guidelines Update for the Management of Patients with Functional Pancreatic Neuroendocrine Tumors and Non-Functional Pancreatic Neuroendocrine Tumors. Neuroendocrinology. 2016;103:153-71. https://doi.org/10.1159/000443171.Falconi M, Eriksson B, Kaltsas G, et al. (2016). ENETS Consensus Guidelines Update for the Management of Patients with Functional Pancreatic Neuroendocrine Tumors and Non-Functional Pancreatic Neuroendocrine Tumors. Neuroendocrinology. 2016;103:153-71. https://doi.org/10.1159/000443171.Yano M, Misra S, Carpenter DH, et al. Pancreatic Neuroendocrine Tumors: Computed Tomography Enhancement, But Not Histological Grade, Correlates With Tumor Aggression. Pancreas. 2017;46(10):1366-72. https://doi.org/10.1097/MPA.0000000000000922.Yano M, Misra S, Carpenter DH, et al. Pancreatic Neuroendocrine Tumors: Computed Tomography Enhancement, But Not Histological Grade, Correlates With Tumor Aggression. Pancreas. 2017;46(10):1366-72. https://doi.org/10.1097/MPA.0000000000000922.d’Assignies G, Couvelard A, Bahrami S, et al. Pancreatic endocrine tumors: tumor blood flow assessed with perfusion CT reflects angiogenesis and correlates with prognostic factors. Radiology. 2009;250(2):407-16. https://doi.org/10.1148/radiol.2501080291.d’Assignies G, Couvelard A, Bahrami S, et al. Pancreatic endocrine tumors: tumor blood flow assessed with perfusion CT reflects angiogenesis and correlates with prognostic factors. Radiology. 2009;250(2):407-16. https://doi.org/10.1148/radiol.2501080291.Груздев ИС, Тихонова ВС, Замятина КА и др. Компьютерная томография в прогнозировании степени дифференцировки гиперваскулярных нейроэндокринных опухолей поджелудочной железы: текстурный анализ и характеристики контрастирования. REJR. 2021;11(4):105-14. https://doi.org/10.21569/2222‑7415‑2021‑11‑4‑105‑114Gruzdev IS, Tikhonova VS, Zamyatina KA, at al. Computed tomography in prediction of hypervascular pancreatic neuroendocrine tumors grade: texture analysis and contrast enhancement features. REJR. 2021; 11(4):105-14. (In Russ.). https://doi.org/10.21569/2222‑7415‑2021‑11‑4‑105‑114Lee L, Ito T, Jensen RT. Imaging of pancreatic neuroendocrine tumors: recent advances, current status, and controversies. Expert Rev Anticancer Ther. 2018;18(9):837-60. https://doi.org/10.1080/14737140.2018.1496822.Lee L, Ito T, Jensen RT. Imaging of pancreatic neuroendocrine tumors: recent advances, current status, and controversies. Expert Rev Anticancer Ther. 2018;18(9):837-60. https://doi.org/10.1080/14737140.2018.1496822.Hu HF, Li Z, Chen K, et al. Multimodality imaging differentiation of pancreatic neuroendocrine tumors and solid pseudopapillary tumors with a nomogram model: A large single-center study. Front Surg. 2022;9:970178. https://doi.org/10.3389/fsurg.2022.970178.Hu HF, Li Z, Chen K, et al. Multimodality imaging differentiation of pancreatic neuroendocrine tumors and solid pseudopapillary tumors with a nomogram model: A large single-center study. Front Surg. 2022;9:970178. https://doi.org/10.3389/fsurg.2022.970178.Mebis W, Snoeckx A, Corthouts B, et al. Correlation Between Apparent Diffusion Coefficient Value on MRI and Histopathologic WHO Grades of Neuroendocrine Tumors. Journal of the Belgian Society of Radiology, 2020;104(1):7. Available at: https://doi.org/10.5334/jbsr.1925.Mebis W, Snoeckx A, Corthouts B, et al. Correlation Between Apparent Diffusion Coefficient Value on MRI and Histopathologic WHO Grades of Neuroendocrine Tumors. Journal of the Belgian Society of Radiology, 2020;104(1):7. Available at: https://doi.org/10.5334/jbsr.1925.Kulali F, Semiz-Oysu A, Demir M, et al. Role of diffusion-weighted MR imaging in predicting the grade of nonfunctional pancreatic neuroendocrine tumors. Diagn Interv Imaging. 2018;99(5):301-9. https://doi.org/10.1016/j.diii.2017.10.012.Kulali F, Semiz-Oysu A, Demir M, et al. Role of diffusion-weighted MR imaging in predicting the grade of nonfunctional pancreatic neuroendocrine tumors. Diagn Interv Imaging. 2018;99(5):301-9. https://doi.org/10.1016/j.diii.2017.10.012.Лаптева МГ, Сергеева ОН, Шориков МО, Долгушин БИ. Возможности МРТ с контрастным усилением в оценке степени дифференцировки метастазов нейроэндокринных опухолей в печени. Диагностическая и интервенционная радиология. 2020;14(1);11-7. https://doi.org/10.25512/DIR.2020.14.1.01.Lapteva MG, Sergeeva ON, Shorikov MО, Dolgushin BI. The role of MRI with contrast enhancement in assessment of differentiation grade of liver metastases of neuroendocrine tumors. Journal Diagnostic & interventional radiology. 2020;14(1);11-7. (In Russ.). https://doi.org/10.25512/DIR.2020.14.1.01.Guo C, Zhuge X, Chen X, et al. Value of diffusion-weighted magnetic resonance imaging in predicting World Health Organization grade in G1/G2 pancreatic neuroendocrine tumors. Oncol Lett. 2017;13(6):4141-6. https://doi.org/10.3892/ol.2017.6029.Guo C, Zhuge X, Chen X, et al. Value of diffusion-weighted magnetic resonance imaging in predicting World Health Organization grade in G1/G2 pancreatic neuroendocrine tumors. Oncol Lett. 2017;13(6):4141-6. https://doi.org/10.3892/ol.2017.6029.

The authors declare that there are no conflicts of interest present.