endosergЭндокринная хирургияEndocrine Surgery2306-35132310-3965Типография «Печатных дел Мастер»10.14341/serg12825endoserg-12825Research ArticleОригинальное исследованиеOriginal studyМРТ без контрастного усиления — высокоточный метод визуализации инсулиномыMRI without contrast enhancement is a highly accurate method of imaging insulinomahttps://orcid.org/0000-0002-8771-8300ЮкинаМ. Ю.YukinaM. Yu.

Юкина Марина Юрьевна - к.м.н.

117292, Москва, ул. Дмитрия Ульянова, д. 11; Researcher ID: P-5181-2015; Scopus Author ID: 57109367700

Marina Yu. Yukina - MD, PhD.

117292, Москва, ул. Дмитрия Ульянова, д. 11; Researcher ID: P-5181-2015; Scopus Author ID: 57109367700

yukina.ERC@yandex.ruhttps://orcid.org/0000-0002-8520-8702ТрошинаЕ. А.TroshinaE. A.

Трошина Екатерина Анатольевна - д.м.н., профессор.

Москва

Ekaterina A. Troshina - MD, PhD, Professor.

Moscow

troshina.ekaterina@endocrincentr.ruhttps://orcid.org/0000-0001-6876-3336НуралиеваН. Ф.NuralievaN. F.

Нуралиева Нурана Фейзуллаевна - к.м.н.

Москва

Nurana F. Nuralieva - MD, PhD.

Moscow

nuralieva.nurana@endocrincentr.ruhttps://orcid.org/0000-0001-7965-9454ТарбаеваН. В.TarbaevaN. V.

Тарбаева Наталья Викторовна - к.м.н.

Москва

Natalya V. Tarbaeva - MD, PhD.

Moscow

Tarbaeva.Natalya@endocrincentr.ruhttps://orcid.org/0000-0002-6733-0958РеброваО. В.RebrovaO. Yu.

Реброва Ольга Юрьевна - д.м.н.

Москва

Olga Yu. Rebrova - MD, PhD.

Moscow

rebrova.olga@endocrincentr.ruhttps://orcid.org/0000-0002-9717-9742МокрышеваН. Г.MokryshevaN. G.

Мокрышева Наталья Георгиевна - д.м.н., профессор.

Москва

Natalia G. Mokrysheva - MD, PhD, Professor.

Moscow

mokrisheva.natalia@endocrincentr.ruГосударственный научный центр Российской Федерации Федеральное государственное бюджетное учреждение «Национальный медицинский исследовательский центр эндокринологии»РоссияEndocrinology Research CentreRussian FederationГосударственный научный центр Российской Федерации Федеральное государственное бюджетное учреждение «Национальный медицинский исследовательский центр эндокринологии»; Федеральное государственное автономное образовательное учреждение высшего образования «Российский национальный исследовательский медицинский университет имени Н.И. Пирогова» Министерства здравоохранения Российской ФедерацииРоссияEndocrinology Research Centre; Pirogov Russian National Research Medical UniversityRussian Federation2024091220241832435Copyright © Юкина М.Ю., Трошина Е.А., Нуралиева Н.Ф., Тарбаева Н.В., Реброва О.В., Мокрышева Н.Г., 20242024Юкина М.Ю., Трошина Е.А., Нуралиева Н.Ф., Тарбаева Н.В., Реброва О.В., Мокрышева Н.Г.Yukina M.Y., Troshina E.A., Nuralieva N.F., Tarbaeva N.V., Rebrova O.Y., Mokrysheva N.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.surg-endojournals.ru/jour/article/view/12825ОБОСНОВАНИЕ

ОБОСНОВАНИЕ. Согласно литературным источникам, имеются противоречивые результаты относительно диагностической точности магнитно-резонансной томографии (МРТ) без контрастного усиления (к/у) при инсулиноме, а исследования, которые анализируют факторы, влияющие на получение ложноотрицательных результатов, не описаны. ЦЕЛЬ. Оценка операционных характеристик МРТ без к/у при визуализации инсулиномы.

МАТЕРИАЛЫ И МЕТОДЫ

МАТЕРИАЛЫ И МЕТОДЫ. Пациентам с подозрением на недиабетическую гипогликемию (НДГ) выполнены визуализирующие исследования органов брюшной полости и забрюшинного пространства: МРТ без к/у (индексный тест) и КТ с к/у (референсный тест первого ряда). В качестве референсного теста второго ряда применялось ультразвуковое исследование, третьего ряда — артериально-стимулированный венозный забор крови. Диагноз НДГ и инсулиномы устанавливался на основании выявления гиперинсулинемической гипогликемии в ходе лабораторного обследования и подтверждения наличия опухоли поджелудочной железы.

РЕЗУЛЬТАТЫ

РЕЗУЛЬТАТЫ. Включено 125 пациентов с инсулиномой и 55 пациентов с прочими причинами НДГ. Чувствительность МРТ без к/у в диагностике инсулиномы составила 94%, 95% ДИ [89%; 98%], специфичность — 98%, 95% ДИ [90%; 100%], прогностическая ценность положительного результата — 99%, 95% ДИ [95%; 100%], прогностическая ценность отрицательного результата — 87%, 95% ДИ [76%; 94%]. Индекс Kappa согласия с заключительным диагнозом составил 0,886 (95% ДИ [0,814; 0,958]), что соответствует отличному согласию, с КТ — 0,750 (95% ДИ [0,651; 0,850]), что соответствует существенному согласию.

При сравнительном анализе томографических и патоморфологических характеристик инсулиномы, в случаях с расхождением результатов при применении МРТ без к/у и КТ с к/у, значимых отличий по структуре, форме, особенностям контуров, локализации и степени злокачественности опухоли, а также структуре окружающей ее паренхимы не выявлено.

В представленной выборке инсулинома имеет медиану размера 14–15 мм, медиану оптической плотности в нативную фазу КТ 42–44 ед.Н, гиперинтенсивность на Т2-взвешенных изображениях МРТ в 89%, 95% ДИ [78%; 95%] случаев и низкую степень злокачественности Grade 1 в 70%, 95% ДИ [56%; 81%] случаев.

ЗАКЛЮЧЕНИЕ

ЗАКЛЮЧЕНИЕ. КТ с к/у и МРТ без к/у характеризуются существенным согласием в диагностике инсулиномы. В связи с этим, а также ввиду отсутствия лучевой нагрузки и строгой необходимости введения контрастных веществ, МРТ без к/у может быть рекомендована в качестве метода первого ряда наравне с абдоминальным УЗИ и КТ с к/у для выявления инсулиномы.

BACKGROUND

BACKGROUND: According to the literature, there are contradictory results regarding the diagnostic accuracy of magnetic resonance imaging (MRI) without contrast enhancement (CE) in insulinoma, and studies that analyze the factors influencing the obtaining of false negative results have not been described.

AIM

AIM: Evaluation of the operational characteristics of MRI imaging of insulinoma without CE.

MATERIALS AND METHODS

MATERIALS AND METHODS: Imaging studies of the abdominal cavity and retroperitoneal space were performed in patients with suspected nondiabetic hypoglycemia (NDH): MRI without CE (index test) and CT with CE (first row reference test). Ultrasound examination was used as a reference test of the second row, and arteriostimulated venous blood sampling was used in the third row. The diagnosis of NDH and insulinoma was established based on the detection of hyperinsulinemic hypoglycemia during laboratory examination and confirmation of the presence of a pancreatic tumor.

RESULTS

RESULTS: 125 patients with insulinoma and 55 patients with other causes of NDH were included. The sensitivity of MRI without CE in the diagnosis of insulinoma was 94%, 95% CI [89%; 98%], specificity — 98%, 95% CI [90%; 100%], prognostic value of a positive result — 99%, 95% CI [95%; 100%], prognostic value of a negative result is 87%, 95% CI [76%; 94%]. The Kappa index of agreement with the final diagnosis was 0.886 (95% CI [0.814; 0.958]), which corresponds to excellent agreement, with CT — 0.750 (95% CI [0.651; 0.850]), which corresponds to significant agreement.

In a comparative analysis of the tomographic and pathomorphological characteristics of insulinoma, in cases with divergent results when using MRI without CE and CT with CE, significant differences in structure, shape, contour features, localization and degree of malignancy of the tumor, as well as the structure of its surrounding parenchyma were not revealed.

In the presented sample, the insulinoma has a median size of 14–15 mm with the median optical density in the native phase of CT 42–44 units.H, hyperintensivity on T2-weighted MRI images in 89%, 95% CI [78%; 95%] cases and low Grade 1 malignancy in 70%, 95% CI [56%; 81%] cases.

CONCLUSION

CONCLUSION: CT with CE and MRI without CE are characterized by significant agreement in the diagnosis of insulinoma. In this regard, as well as due to the lack of radiation exposure and the strict need for contrast agents, MRI without CE can be recommended as a first-line method on a par with abdominal ultrasound and CT with CE to detect insulinoma.

инсулиномакомпьютерная томографиямагнитно-резонансная томографияinsulinomacomputed tomographymagnetic resonance imagingИсследование выполнено при поддержке гранта Министерства науки и высшего образования Российской Федерации (соглашение №075-15-2022-310 от 20.04.2022)ReferencesZhao K, Patel N, Kulkarni K, et al. Essentials of insulinoma localization with selective arterial calcium stimulation and hepatic venous sampling. Journal of Clinical Medicine. 2020;9(10):1–14. doi: https://doi.org/10.3390/jcm9103091Zhao K, Patel N, Kulkarni K, et al. Essentials of insulinoma localization with selective arterial calcium stimulation and hepatic venous sampling. Journal of Clinical Medicine. 2020;9(10):1–14. doi: https://doi.org/10.3390/jcm9103091Fu J, Zhang J, Wang Y, et al. Comparison of angio-CT versus multidetector CT in the detection and location for insulinomas. Clinical Radiology. 2020;75(10):796.e11-796.e16. doi: https://doi.org/10.1016/j.crad.2020.05.012Fu J, Zhang J, Wang Y, et al. Comparison of angio-CT versus multidetector CT in the detection and location for insulinomas. Clinical Radiology. 2020;75(10):796.e11-796.e16. doi: https://doi.org/10.1016/j.crad.2020.05.012An L, Li W, Yao KC, et al. Assessment of contrast-enhanced ultrasonography in diagnosis and preoperative localization of insulinoma. Eur J Radiol. 2011;80(3):675-680. doi: https://doi.org/10.1016/j.ejrad.2010.09.014An L, Li W, Yao KC, et al. Assessment of contrast-enhanced ultrasonography in diagnosis and preoperative localization of insulinoma. Eur J Radiol. 2011;80(3):675-680. doi: https://doi.org/10.1016/j.ejrad.2010.09.014McAuley G, Delaney H, Colville J, et al. Multimodality preoperative imaging of pancreatic insulinomas. Clin Radiol. 2005;60(10):1039-1050. doi: https://doi.org/10.1016/j.crad.2005.06.005McAuley G, Delaney H, Colville J, et al. Multimodality preoperative imaging of pancreatic insulinomas. Clin Radiol. 2005;60(10):1039-1050. doi: https://doi.org/10.1016/j.crad.2005.06.005Mehrabi A, Fischer L, Hafezi M, et al. A systematic review of localization, surgical treatment options, and outcome of insulinoma. Pancreas. 2014. doi: https://doi.org/10.1097/MPA.0000000000000110Mehrabi A, Fischer L, Hafezi M, et al. A systematic review of localization, surgical treatment options, and outcome of insulinoma. Pancreas. 2014. doi: https://doi.org/10.1097/MPA.0000000000000110Zhu L, Xue H, Sun H, et al. Insulinoma detection with MDCT: Is there a role for whole-pancreas perfusion? American Journal of Roentgenology. 2017;208(2):306–314. doi: https://doi.org/10.2214/AJR.16.16351Zhu L, Xue H, Sun H, et al. Insulinoma detection with MDCT: Is there a role for whole-pancreas perfusion? American Journal of Roentgenology. 2017;208(2):306–314. doi: https://doi.org/10.2214/AJR.16.16351Lin XZ, Wu ZY, Tao R, et al. Dual energy spectral CT imaging of insulinoma Value in preoperative diagnosis compared with conventional multi-detector CT. European Journal of Radiology. 2012;81(10):2487–2494. doi: https://doi.org/10.1016/j.ejrad.2011.10.028Lin XZ, Wu ZY, Tao R, et al. Dual energy spectral CT imaging of insulinoma Value in preoperative diagnosis compared with conventional multi-detector CT. European Journal of Radiology. 2012;81(10):2487–2494. doi: https://doi.org/10.1016/j.ejrad.2011.10.028Song P, Yan JY, Wang Y, Li X. Value of multi-detector computed tomography during intra-arterial infusion of contrast medium for locating insulinomas. Journal of International Medical Research. 2020;48(3). doi: https://doi.org/10.1177/0300060519889432Song P, Yan JY, Wang Y, Li X. Value of multi-detector computed tomography during intra-arterial infusion of contrast medium for locating insulinomas. Journal of International Medical Research. 2020;48(3). doi: https://doi.org/10.1177/0300060519889432Yang Y, Shi J, Zhu J. Diagnostic performance of noninvasive imaging modalities for localization of insulinoma: A meta-analysis. European Journal of Radiology. 2021;145. doi: https://doi.org/10.1016/j.ejrad.2021.110016Yang Y, Shi J, Zhu J. Diagnostic performance of noninvasive imaging modalities for localization of insulinoma: A meta-analysis. European Journal of Radiology. 2021;145. doi: https://doi.org/10.1016/j.ejrad.2021.110016Antwi K, Fani M, Heye T, et al. Comparison of glucagon-like peptide-1 receptor (GLP-1R) PET/CT, SPECT/CT and 3T MRI for the localisation of occult insulinomas: evaluation of diagnostic accuracy in a prospective crossover imaging study. European Journal of Nuclear Medicine and Molecular Imaging. 2018;45(13):2318–2327. doi: https://doi.org/10.1007/s00259-018-4101-5Antwi K, Fani M, Heye T, et al. Comparison of glucagon-like peptide-1 receptor (GLP-1R) PET/CT, SPECT/CT and 3T MRI for the localisation of occult insulinomas: evaluation of diagnostic accuracy in a prospective crossover imaging study. European Journal of Nuclear Medicine and Molecular Imaging. 2018;45(13):2318–2327. doi: https://doi.org/10.1007/s00259-018-4101-5Hasanov R, Samadov E, Bayramov N, et al. Surgical management of insulinomas at the Azerbaijan medical university: A retrospective study of 21 cases over a 10-year period. Turkish Journal of Medical Sciences. 2020;50(5):1262–1269. doi: https://doi.org/10.3906/sag-2001-150Hasanov R, Samadov E, Bayramov N, et al. Surgical management of insulinomas at the Azerbaijan medical university: A retrospective study of 21 cases over a 10-year period. Turkish Journal of Medical Sciences. 2020;50(5):1262–1269. doi: https://doi.org/10.3906/sag-2001-150Daneshvar K, Grenacher L, Mehrabi A, et al. Preoperative tumor studies using MRI or CT in patients with clinically suspected insulinoma. Pancreatology. 2011;11(5):487–495. doi: https://doi.org/10.1159/000330208Daneshvar K, Grenacher L, Mehrabi A, et al. Preoperative tumor studies using MRI or CT in patients with clinically suspected insulinoma. Pancreatology. 2011;11(5):487–495. doi: https://doi.org/10.1159/000330208Owen NJ, Sohaib SAA, Peppercorn PD, et al. MRI of pancreatic neuroendocrine tumours. Br J Radiol. 2001;74(886):968-973. doi: https://doi.org/10.1259/bjr.74.886.740968Owen NJ, Sohaib SAA, Peppercorn PD, et al. MRI of pancreatic neuroendocrine tumours. Br J Radiol. 2001;74(886):968-973. doi: https://doi.org/10.1259/bjr.74.886.740968Thoeni RF, Mueller-Lisse UG, Chan R, Do NK, Shyn PB. Detection of Small, Functional Islet Cell Tumors in the Pancreas: Selection of MR Imaging Sequences for Optimal Sensitivity. Radiology. 2000;214(2):483-490. doi: https://doi.org/10.1148/radiology.214.2.r00fe32483Thoeni RF, Mueller-Lisse UG, Chan R, Do NK, Shyn PB. Detection of Small, Functional Islet Cell Tumors in the Pancreas: Selection of MR Imaging Sequences for Optimal Sensitivity. Radiology. 2000;214(2):483-490. doi: https://doi.org/10.1148/radiology.214.2.r00fe32483He M, Xu J, Sun Z, et al. Prospective Comparison of Reduced Field-of-View (rFOV) and Full FOV (fFOV) Diffusion-Weighted Imaging (DWI) in the Assessment of Insulinoma: Image Quality and Lesion Detection. Acad Radiol. 2020;27(11):1572-1579. doi: https://doi.org/10.1016/j.acra.2019.11.019He M, Xu J, Sun Z, et al. Prospective Comparison of Reduced Field-of-View (rFOV) and Full FOV (fFOV) Diffusion-Weighted Imaging (DWI) in the Assessment of Insulinoma: Image Quality and Lesion Detection. Acad Radiol. 2020;27(11):1572-1579. doi: https://doi.org/10.1016/j.acra.2019.11.019Zhu L, Xue H, Sun Z, et al. Prospective comparison of biphasic contrast‐enhanced CT, volume perfusion CT, and 3 Tesla MRI with diffusion‐weighted imaging for insulinoma detection. J Magn Reson Imaging. 2017;46(6):1648-1655. doi: https://doi.org/10.1002/jmri.25709Zhu L, Xue H, Sun Z, et al. Prospective comparison of biphasic contrast‐enhanced CT, volume perfusion CT, and 3 Tesla MRI with diffusion‐weighted imaging for insulinoma detection. J Magn Reson Imaging. 2017;46(6):1648-1655. doi: https://doi.org/10.1002/jmri.25709Jyotsna VP, Pal S, Kandasamy D, et al. Evolving management of insulinoma: Experience at a tertiary care centre. Indian Journal of Medical Research. 2016;144:771–777. doi: https://doi.org/10.4103/ijmr.IJMR_1477_14Jyotsna VP, Pal S, Kandasamy D, et al. Evolving management of insulinoma: Experience at a tertiary care centre. Indian Journal of Medical Research. 2016;144:771–777. doi: https://doi.org/10.4103/ijmr.IJMR_1477_14Krieger AG, Smirnov AV, Berelavichus SV, et al. Organic hyperinsulinism: radiological diagnostics and surgical treatment. Khirurgiia (Mosk). 2016;(6):14-29. doi: https://doi.org/10.17116/hirurgia2016614-22Krieger AG, Smirnov AV, Berelavichus SV, et al. Organic hyperinsulinism: radiological diagnostics and surgical treatment. Khirurgiia (Mosk). 2016;(6):14-29. doi: https://doi.org/10.17116/hirurgia2016614-22Andreassen M, Ilett E, Wiese D, et al. Surgical Management, Preoperative Tumor Localization, and Histopathology of 80 Patients Operated on for Insulinoma. J Clin Endocrinol Metab. 2019;104(12):6129-6138. doi: https://doi.org/10.1210/jc.2019-01204Andreassen M, Ilett E, Wiese D, et al. Surgical Management, Preoperative Tumor Localization, and Histopathology of 80 Patients Operated on for Insulinoma. J Clin Endocrinol Metab. 2019;104(12):6129-6138. doi: https://doi.org/10.1210/jc.2019-01204Angeli E, Vanzulli A, Castrucci M, et al. Value of abdominal sonography and MR imaging at 0.5 T in preoperative detection of pancreatic insulinoma: a comparison with dynamic CT and angiography. Abdom Imaging. 1997;22(3):295-303. doi: https://doi.org/10.1007/s002619900193Angeli E, Vanzulli A, Castrucci M, et al. Value of abdominal sonography and MR imaging at 0.5 T in preoperative detection of pancreatic insulinoma: a comparison with dynamic CT and angiography. Abdom Imaging. 1997;22(3):295-303. doi: https://doi.org/10.1007/s002619900193Shi Z, Li X, You R, et al. Homogenously isoattenuating insulinoma on biphasic contrast-enhanced computed tomography: Little benefits of diffusion-weighted imaging for lesion detection. Oncol Lett. 2018;16(3):3117-3125. doi: https://doi.org/10.3892/ol.2018.9037Shi Z, Li X, You R, et al. Homogenously isoattenuating insulinoma on biphasic contrast-enhanced computed tomography: Little benefits of diffusion-weighted imaging for lesion detection. Oncol Lett. 2018;16(3):3117-3125. doi: https://doi.org/10.3892/ol.2018.9037Anaye A, Mathieu A, Closset J, et al. Successful preoperative localization of a small pancreatic insulinoma by diffusion-weighted MRI. JOP. 2009;10(5):528-31Anaye A, Mathieu A, Closset J, et al. Successful preoperative localization of a small pancreatic insulinoma by diffusion-weighted MRI. JOP. 2009;10(5):528-31Cryer PE, Axelrod L, Grossman AB, et al. Evaluation and management of adult hypoglycemic disorders: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2009;94(3):709-28. doi: https://doi.org/10.1210/jc.2008-1410Cryer PE, Axelrod L, Grossman AB, et al. Evaluation and management of adult hypoglycemic disorders: an Endocrine Society Clinical Practice Guideline. J Clin Endocrinol Metab. 2009;94(3):709-28. doi: https://doi.org/10.1210/jc.2008-1410Нейроэндокринные опухоли. Клинические рекомендации. 2020 г. Available from: https://cr.minzdrav.gov.ru/recomend/610_1Nejroendokrinnye opuholi. Klinicheskie rekomendacii. 2020 (In Russ.)] Available from: https://cr.minzdrav.gov.ru/recomend/610_1Ponzi E, Maiorana A, Lepri FR, et al. Persistent Hypoglycemia in Children: Targeted Gene Panel Improves the Diagnosis of Hypoglycemia Due to Inborn Errors of Metabolism. J Pediatr. 2018;202:272-8. doi: https://doi.org/10.1016/j.jpeds.2018.06.050Ponzi E, Maiorana A, Lepri FR, et al. Persistent Hypoglycemia in Children: Targeted Gene Panel Improves the Diagnosis of Hypoglycemia Due to Inborn Errors of Metabolism. J Pediatr. 2018;202:272-8. doi: https://doi.org/10.1016/j.jpeds.2018.06.050Cavalcanti MS, Gönen M, Klimstra DS. The ENETS/WHO grading system for neuroendocrine neoplasms of the gastroenteropancreatic system: a review of the current state, limitations and proposals for modifications. Int J Endocr Oncol. 2016;3(3):203-219. doi: https://doi.org/10.2217/ije-2016-0006Cavalcanti MS, Gönen M, Klimstra DS. The ENETS/WHO grading system for neuroendocrine neoplasms of the gastroenteropancreatic system: a review of the current state, limitations and proposals for modifications. Int J Endocr Oncol. 2016;3(3):203-219. doi: https://doi.org/10.2217/ije-2016-0006Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1):159-174. doi: https://doi.org/10.2307/2529310.Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics. 1977;33(1):159-174. doi: https://doi.org/10.2307/2529310.Егоров А.В., Мусаев Г.Х., Фоминых Е.В., Кондрашин С.А., Парнова В.А., и др. Эволюция алгоритма топической диагностики гормонально-активных нейроэндокринных опухолей поджелудочной железы // Анналы хирургической гепатологии. 2016. — Т. 21. — №1. — С. 21-27. doi: https://doi.org/10.16931/1995-5464.2016121-27Egorov AV, Musaev GKh, Fominykh EV, Kondrashin SA, Parnova VA, et al. Evolution of topical diagnostic algorithm for pancreatic hormoneproducing neuroendocrine tumors. Annaly khirurgicheskoy gepatologii = Annals of HPB Surgery. 2016;21(1):21-27. (In Russ.) doi: https://doi.org/10.16931/1995-5464.2016121-27Fu J, Liu F, Yuan K, et al. The Value of Hybrid Angio-CT in Preoperative Detection and Localization of Insulinomas: A Single-Center Retrospective Study. Cardiovasc Intervent Radiol. 2018;41(4):633-638. doi: https://doi.org/10.1007/s00270-017-1847-2Fu J, Liu F, Yuan K, et al. The Value of Hybrid Angio-CT in Preoperative Detection and Localization of Insulinomas: A Single-Center Retrospective Study. Cardiovasc Intervent Radiol. 2018;41(4):633-638. doi: https://doi.org/10.1007/s00270-017-1847-2Druce MR, Muthuppalaniappan VM, O’Leary B, et al. Diagnosis and localisation of insulinoma: the value of modern magnetic resonance imaging in conjunction with calcium stimulation catheterization. Eur J Endocrinol. 2010;162(5):971-8. doi: https://doi.org/10.1530/EJE-10-0056Druce MR, Muthuppalaniappan VM, O’Leary B, et al. Diagnosis and localisation of insulinoma: the value of modern magnetic resonance imaging in conjunction with calcium stimulation catheterization. Eur J Endocrinol. 2010;162(5):971-8. doi: https://doi.org/10.1530/EJE-10-0056Crippa S, Zerbi A, Boninsegna L, et al. Surgical management of insulinomas: shortand long-term outcomes after enucleations and pancreatic resections. Arch Surg. 2012;147(3):261-6. doi: https://doi.org/10.1001/archsurg.2011.1843Crippa S, Zerbi A, Boninsegna L, et al. Surgical management of insulinomas: shortand long-term outcomes after enucleations and pancreatic resections. Arch Surg. 2012;147(3):261-6. doi: https://doi.org/10.1001/archsurg.2011.1843Хацимова Л.С., Каронова Т.Л., Цой У.А., Яневская Л.Г., Гринева Е.Н. Инсулинома: диагностические подходы и врачебная тактика // Проблемы эндокринологии. — 2017. — Т. 63. — №4. — С. 212—218. doi: https://doi.org/10.14341/probl2017634212-218Khacimova LS, Karonova TL, Tsoy UA, Ianevskaia LG, Grineva EN. Insulinoma: diagnostic features and treatment management. Problems of Endocrinology. 2017;63(4):212-218. (In Russ.) doi: https://doi.org/10.14341/probl2017634212-218Nikfarjam M, Warshaw AL, Axelrod L, et al. Improved contemporary surgical management of insulinomas: a 25-year experience at the Massachusetts General Hospital. Ann Surg. 2008;247(1):165-72. doi: https://doi.org/10.1097/SLA.0b013e31815792edNikfarjam M, Warshaw AL, Axelrod L, et al. Improved contemporary surgical management of insulinomas: a 25-year experience at the Massachusetts General Hospital. Ann Surg. 2008;247(1):165-72. doi: https://doi.org/10.1097/SLA.0b013e31815792edInan N, Arslan A, Akansel G, et al. Unusual magnetic resonance image of an insulinoma with extensive desmoplastic reaction. JOP. 2008;9(1):61-6Inan N, Arslan A, Akansel G, et al. Unusual magnetic resonance image of an insulinoma with extensive desmoplastic reaction. JOP. 2008;9(1):61-6Afonso PD, Duarte S, Barata MJ, Camacho R. A type of pancreatic islet cell tumor: Insulinoma. A case report. 2007. doi: https://doi.org/10.1594/EURORAD/CASE.6144Afonso PD, Duarte S, Barata MJ, Camacho R. A type of pancreatic islet cell tumor: Insulinoma. A case report. 2007. doi: https://doi.org/10.1594/EURORAD/CASE.6144Sundin A, Arnold R, Baudin E, et al. ENETS Consensus Guidelines for the Standards of Care in Neuroendocrine Tumors: Radiological, Nuclear Medicine and Hybrid Imaging. In: Neuroendocrinology. 2017. doi: https://doi.org/10.1159/000471879Sundin A, Arnold R, Baudin E, et al. ENETS Consensus Guidelines for the Standards of Care in Neuroendocrine Tumors: Radiological, Nuclear Medicine and Hybrid Imaging. In: Neuroendocrinology. 2017. doi: https://doi.org/10.1159/000471879Khanna L, Prasad SR, Sunnapwar A, et al. Pancreatic Neuroendocrine Neoplasms: 2020 Update on Pathologic and Imaging Findings and Classification. Radiographics. 2020;40(5):1240-1262. doi: https://doi.org/10.1148/rg.2020200025Khanna L, Prasad SR, Sunnapwar A, et al. Pancreatic Neuroendocrine Neoplasms: 2020 Update on Pathologic and Imaging Findings and Classification. Radiographics. 2020;40(5):1240-1262. doi: https://doi.org/10.1148/rg.2020200025AlJadir S. Insulinoma: Literature’s Review (2). Endocrinol Int J. 2015. doi: https://doi.org/10.15406/emij.2015.02.00031AlJadir S. Insulinoma: Literature’s Review (2). Endocrinol Int J. 2015. doi: https://doi.org/10.15406/emij.2015.02.00031Sumarac-Dumanovic M, Micic D, Krstic M, et al. Pitfalls in diagnosing a small cystic insulinoma: a case report. J Med Case Rep. 2007:1:181. doi: https://doi.org/10.1186/1752-1947-1-181Sumarac-Dumanovic M, Micic D, Krstic M, et al. Pitfalls in diagnosing a small cystic insulinoma: a case report. J Med Case Rep. 2007:1:181. doi: https://doi.org/10.1186/1752-1947-1-181Tamagno G, Maffei P, Pasquali C, et al. Clinical and diagnostic aspects of cystic insulinoma. Scand J Gastroenterol. 2005;40(12):1497-501. doi: https://doi.org/10.1080/00365520510024160Tamagno G, Maffei P, Pasquali C, et al. Clinical and diagnostic aspects of cystic insulinoma. Scand J Gastroenterol. 2005;40(12):1497-501. doi: https://doi.org/10.1080/00365520510024160Kou HW, Yu MC, Chong SW, Hsu HY, Chou HH, et al. Successful Localization and Resection of Small Pancreatic Cystic Insulinoma Using Intraoperative Near-Infrared Fluorescence Imaging: A Case Report and Literature Review. Pancreas. 2020;49(10):1388-1392. doi: https://doi.org/10.1097/MPA.0000000000001678Kou HW, Yu MC, Chong SW, Hsu HY, Chou HH, et al. Successful Localization and Resection of Small Pancreatic Cystic Insulinoma Using Intraoperative Near-Infrared Fluorescence Imaging: A Case Report and Literature Review. Pancreas. 2020;49(10):1388-1392. doi: https://doi.org/10.1097/MPA.0000000000001678Balci NC, Semelka RC. Radiologic features of cystic, endocrine and other pancreatic neoplasms. Eur J Radiol. 2001;38(2):113-9. doi: https://doi.org/10.1016/s0720-048x(01)00296-0Balci NC, Semelka RC. Radiologic features of cystic, endocrine and other pancreatic neoplasms. Eur J Radiol. 2001;38(2):113-9. doi: https://doi.org/10.1016/s0720-048x(01)00296-0Okabayashi T, Shima Y, Sumiyoshi T, et al. Diagnosis and management of insulinoma. World J Gastroenterol. 2013;19(6):829-37. doi: https://doi.org/10.3748/wjg.v19.i6.829Okabayashi T, Shima Y, Sumiyoshi T, et al. Diagnosis and management of insulinoma. World J Gastroenterol. 2013;19(6):829-37. doi: https://doi.org/10.3748/wjg.v19.i6.829Kann P, Bittinger F, Engelbach M, et al. Endosonography of insulinsecreting and clinically non-functioning neuroendocrine tumors of the pancreas: criteria for benignancy and malignancy. Eur J Med Res. 2001;6(9):385-90Kann P, Bittinger F, Engelbach M, et al. Endosonography of insulinsecreting and clinically non-functioning neuroendocrine tumors of the pancreas: criteria for benignancy and malignancy. Eur J Med Res. 2001;6(9):385-90Noone TC, Hosey J, Firat Z, Semelka RC, et al. Imaging and localization of islet-cell tumours of the pancreas on CT and MRI. Best Pract Res Clin Endocrinol Metab. 2005;19(2):195-211. doi: https://doi.org/10.1016/j.beem.2004.11.013Noone TC, Hosey J, Firat Z, Semelka RC, et al. Imaging and localization of islet-cell tumours of the pancreas on CT and MRI. Best Pract Res Clin Endocrinol Metab. 2005;19(2):195-211. doi: https://doi.org/10.1016/j.beem.2004.11.013Taieb D, Legmann P, Prat F, et al. Topographic diagnosis: respective roles of morphological and functional imaging. Ann Endocrinol (Paris). 2013;74(3):185-190. doi: https://doi.org/10.1016/j.ando.2013.05.008Taieb D, Legmann P, Prat F, et al. Topographic diagnosis: respective roles of morphological and functional imaging. Ann Endocrinol (Paris). 2013;74(3):185-190. doi: https://doi.org/10.1016/j.ando.2013.05.008Ciaravino V, De Robertis R, Tinazzi Martini P, et al. Imaging presentation of pancreatic neuroendocrine neoplasms. Insights Imaging. 2018;9(6):943-953. doi: https://doi.org/10.1007/s13244-018-0658-6Ciaravino V, De Robertis R, Tinazzi Martini P, et al. Imaging presentation of pancreatic neuroendocrine neoplasms. Insights Imaging. 2018;9(6):943-953. doi: https://doi.org/10.1007/s13244-018-0658-6Matondanga S, Suwitaa BM, Budiantoa T, Krisnuhonib E. Atypical CT and MR imaging of insulinoma: A case report. Journal of Clinical and Translational Endocrinology: Case Reports. 2021;19:100075. doi: https://doi.org/10.1016/j.jecr.2020.100075Matondanga S, Suwitaa BM, Budiantoa T, Krisnuhonib E. Atypical CT and MR imaging of insulinoma: A case report. Journal of Clinical and Translational Endocrinology: Case Reports. 2021;19:100075. doi: https://doi.org/10.1016/j.jecr.2020.100075Agrawal N, Kar SS, Singh A, et al. Diffusion-weighted MRI in Localization of Insulinoma. Indian J Endocrinol Metab. 2020;24(2):222-224. doi: https://doi.org/10.4103/ijem.IJEM_636_19Agrawal N, Kar SS, Singh A, et al. Diffusion-weighted MRI in Localization of Insulinoma. Indian J Endocrinol Metab. 2020;24(2):222-224. doi: https://doi.org/10.4103/ijem.IJEM_636_19Soyoye DO, Atolani SA, Adetunji TA, Alatise OI. Insulinoma Presenting as Seizures: Challenges of Managing a Rare Disease in a Resource-challenged Setting. JCEM Case Rep. 2023;2(1):luad162. doi: https://doi.org/10.1210/jcemcr/luad162Soyoye DO, Atolani SA, Adetunji TA, Alatise OI. Insulinoma Presenting as Seizures: Challenges of Managing a Rare Disease in a Resource-challenged Setting. JCEM Case Rep. 2023;2(1):luad162. doi: https://doi.org/10.1210/jcemcr/luad162

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