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Мультипараметрическая магнитно-резонансная томография в дифференциальной диагностике эпителиальных опухолей яичников
Мультипараметрическая магнитно-резонансная томография в дифференциальной диагностике эпителиальных опухолей яичников
Носова Ю.В., Солопова А.Е., Хабас Г.Н. Мультипараметрическая магнитно-резонансная томография в дифференциальной диагностике эпителиальных опухолей яичников. Гинекология. 2020; 22 (6): 27–31. DOI: 10.26442/20795696.2020.6.200519
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Аннотация
Проведен систематический анализ исследований, опубликованных в последние 10 лет и посвященных использованию функциональных методик магнитно-резонансной томографии (МРТ) в ранней и дифференциальной диагностике эпителиальных опухолей яичников, с использованием актуальных данных: базы данных SCOPUS, подборки ведущих научных монографий SCOPUS, pubmed.org, elibrary.ru (с расширенным доступом к полнотекстовым ресурсам), ресурсов NCCN, ECR, ESUR, ACR. Дифференциальная диагностика опухолей яичников имеет решающее значение для выбора последующего алгоритма обследования и лечения пациента. В последние годы исследователи выдвинули гипотезу о том, что применение функциональных методик наряду с базовым протоколом МРТ органов малого таза позволяет улучшить диагностические показатели в характеристике новообразований яичников с «пограничным риском злокачественности». Нами обобщен и проанализирован опыт ведущих мировых центров, занимающихся вопросами внедрения новых методик МРТ и изучения их диагностических возможностей.
Ключевые слова: рак яичников, эпителиальные опухоли яичников, онкология, дифференциальная диагностика, мультипараметрическая магнитно-резонансная томография, диффузионно-взвешенная магнитно-резонансная томография, магнитно-резонансная томография с динамическим контрастным усилением, временная кривая интенсивности сигнала.
Key words: ovarian tumors, dynamic contrast-enhanced magnetic resonance imaging, differential diagnosis, magnetic resonance imaging with diffusion analysis, apparent diffusion coefficient, TIC-curves.
Ключевые слова: рак яичников, эпителиальные опухоли яичников, онкология, дифференциальная диагностика, мультипараметрическая магнитно-резонансная томография, диффузионно-взвешенная магнитно-резонансная томография, магнитно-резонансная томография с динамическим контрастным усилением, временная кривая интенсивности сигнала.
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Key words: ovarian tumors, dynamic contrast-enhanced magnetic resonance imaging, differential diagnosis, magnetic resonance imaging with diffusion analysis, apparent diffusion coefficient, TIC-curves.
Полный текст
Список литературы
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[Makarov O.V., Borisenko S.A. Prophylaxis, diagnosis, treatment of ovarian cancer. Med J Russ Feder. 1996; 3: 36–40 (in Russian).]
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[Gasparov A.S., Zhordania K.I., Payanidi Y.G., Dubinskaya E.D. Oncogynecologycal aspects of adnexal masses. Ann Russ Acad Med Sci. 2013; 68 (8): 9–13 (in Russian).]
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14. Van Calster, Van Hoorde K, Valentin L et al. Evaluating the risk of ovarian cancer before surgery using the ADNEX model to differentiate between benign, borderline, early and advanced stage invasive, and secondary metastatic tumours: prospective multicentre diagnostic study. BMJ 2014; 349: g5920. DOI: 10.1136/bmj.g5920
15. Andreotti RF, Timmerman D, Benacerraf BR et al. Ovarian-Adnexal Reporting Lexicon for Ultrasound: A White Paper of the ACR Ovarian-Adnexal Reporting and Data System Committee. J Am Coll Radiol 2018; 15 (10): 1415–29. DOI: 10.1016/j.jacr.2018.07.004
16. Pereira PN, Sarian LO, Yoshida A et al. Accuracy of the ADNEX MR scoring system based on a simplified MRI protocol for the assessment of adnexal masses. Diagn Interv Radiol 2018; 24: 63–71.
17. Солопова А.Е., Макацария А.Д., Сдвижков А.М., Терновой С.К. Магнитно-резонансная томография в дифференциальной диагностике образований яичника. Возможности количественной мультипараметрической оценки. Акушерство и гинекология. 2017; 2: 80–85. DOI: 10.18565/aig.2017.2.80-5
[Solopova AE, Makatsaria AD, Sdvizhkov AM, Ternovoy SK. Magnetic resonance imaging in the differential diagnosis of ovarian masses: Capabilities of quantitative multiparametric evaluation. Obstetrics and Gynecology. 2017; 2: 80–5. DOI: 10.18565/aig.2017.2.80-5 (in Russian).]
18. Kwee TC, Takahara T, Ochiai R et al. Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potentional applications in oncology. Eur Radiol 2008; 18: 1937–52.
19. Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR 2007; 188 (6): 1622–35.
20. Figueiras RG, Goh V, Padhani AR et al. The role of functional imaging in colorectal cancer. AJR 2010; 195 (1): 54–66.
21. Mohaghegh P, Rockall A. Imaging strategy for early ovarian cancer: characterization of adnexal masses with conventional and advanced imaging techniques. Radiographics 2012; 32 (6): 1751–73. DOI: 10.1148/rg.326125520
22. Zhao SH, Qiang JW, Zhang GF et al. Diffusion-weighted MRimaging for differentiating borderline from malignant epithelial tumors of the ovary: pathological correlation. Eur Radiol 2014; 24 (9): 2292–9. DOI: 10.1007/s00330– 014–3236–4
23. Li W, Chu C, Cui Y et al. Diffusion-weighted MRI: a useful technique to discriminate benign versus malignant ovarian surface epithelial tumors with solid and cystic components. Abdom Imaging 2012; 37: 897–903.
24. Katayama M, Masui T, Kobayashi S et al. Diffusion-weighted echo planar imaging of ovarian tumors: is it useful to measure apparent diffusion coefficients? J Comput Assist Tomogr 2002; 26: 250–6.
25. Thomassin-Naggara I, Darai E, Cuenod CA et al. Contribution of diffusion-weighted MR imaging for predicting benignity of complex adnexal masses. Eur Radiol 2009; 19: 1544–52.
26. Kim HJ, Lee SY, Shin YR et al. The value of diffusion-weighted imaging in the differential diagnosis of ovarian lesions: a meta-analysis. PLoS One 2016; 11: e0149465.
27. Zhang P, Cui Y, Li W et al. Diagnostic accuracy of diffusion-weighted imaging with conventional MR imaging for differentiating complex solid and cystic ovarian tumors at 1.5 T. World J Surg Oncol 2012; 10: 237.
28. Ren J, Huan Y, Wang H et al. Dynamic contrast-enhanced MRI of benign prostatic hyperplasia and prostatic carcinoma: correlation with angiogenesis. Clin Radiol 2008; 63: 153–9. DOI: 10.1016/j.crad.2007.07.023
29. Ho VB, Allen SF, Hood MN, Choyke PL. Renal masses: quantitative assessment of enhancement with dynamic MR imaging. Radiology 2002; 224: 695–700. DOI: 10.1148/radiol.2243011048
30. Koo HR, Cho N, Song IC et al. Correlation of perfusion parameters on dynamic contrast-enhanced MRI with prognostic factors and subtypes of breast cancers. J Magn Reson Imaging 2012; 36: 145–51. DOI: 10.1002/jmri.23635
31. Tofts PS, Berkowitz B, Schnall MD. Quantitative analysis of dynamic Gd-DTPA enhancement in breast tumors using a permeability model. Magn Reson Med. 1995; 33: 564–568. DOI: 10.1002/mrm.1910330416
32. Paweletz N, Knierim M. Tumor-related angiogenesis. Crit Rev Oncol Hematol 1989; 9: 197–242. DOI: 10.1016/S1040-8428(89)80002-2
33. Thomassin-Naggara I, Bazot M, Daraï E et al. Epithelial ovarian tumors: value of dynamic contrast-enhanced MR imaging and correlation with tumor angiogenesis. Radiology 2008; 248: 148–59. DOI: 10.1148/radiol.2481071120
34. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multi-phase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22: 880–90. DOI: 10.1007/s00330-011-2331-z
35. Li HM, Qiang JW, Ma FH, Zhao SH. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4. DOI: 10.1186/s13048-017-0302-y
36. Thomassin-Naggara I, Balvay D, Aubert E et al. Quantitative dynamic contrast-enhanced MR imaging analysis of complex adnexal masses: a preliminary study. Eur Radiol 2012; 22: 738–45. DOI: 10.1007/s00330-011-2329-6
37. Forstner R, Thomassin-Naggara I, Cunha TM et al. ESUR recommendations for MR imaging of the sonographically indeterminate adnexal mass: an update. Eur Radiol 2017; 27: 2248–57. DOI: 10.1007/s00330-016-4600-3
38. Thomassin-Naggara I, Daraï E, Cuenod CA et al. Dynamic contrast-enhanced magnetic resonance imaging: a useful tool for characterizing ovarian epithelial tumors. J Magn Reson Imaging 2008; 28 (1): 111–20. DOI: 10.1002/jmri.21377
39. Li X, Hu LJ, Zhu LM et al. The clinical value of dynamic contrast-enhanced MRI in differential diagnosis of malignant and benign ovarian lesions. Tumor Biol 2015; 36 (7): 5515–22. DOI: 10.1007/s13277-015-3219-3
40. Dilks P, Narayanan P, Reznek R et al. Can quantitative dynamic contrast-enhanced MRI independently characterize an ovarian mass? Eur Radiol 2010; 20 (9): 2176–83. DOI: 10.1007/s00330-010-1795-6
41. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multiphase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22 (4): 880–90. DOI: 10.1007/s00330-011-2331-z
42. Mansour SM, Saraya S, EI-Faissal Y. Semi-quantitative contrast-enhanced MR analysis of indeterminate ovarian tumors: when to say malignancy? Br J Radiol 2015; 88 (1053): 20150099. DOI: 10.1259/bjr.20150099
43. Li HM, Qiang JW, Ma FH et al. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4.
44. Emad-Eldin S, Grace MN, Wahba MH et al. The diagnostic potential of diffusion weighted and dynamic contrast enhanced MR imaging in the characterization of complex ovarian lesions. Egypt J Radiol Nucl Med 2018; 49: 884–91.
45. Farhood Saremi. Perfusion imaging in clinical practice. 2015.
46. Carter JS, Koopmeiners JS, Kuehn-Hajder JE et al. Quantitative multiparametric MRI of ovarian cancer. J Magn Reson Imaging 2013; 38 (6): 1501–9.
47. Li H, Feng F, Qiang J et al. Quantitative dynamic contrast-enhanced MR imaging for differentiating benign, borderline, and malignant ovarian tumors. Abdom Radiol 2018; 43: 3132–41. DOI: 10.1007/s00261-018-1569-1
2. Makarov O.V., Borisenko S.A. Prophylaxis, diagnosis, treatment of ovarian cancer. Med J Russ Feder. 1996; 3: 36–40 (in Russian).
3. Gasparov A.S., Zhordania K.I., Payanidi Y.G., Dubinskaya E.D. Oncogynecologycal aspects of adnexal masses. Ann Russ Acad Med Sci. 2013; 68 (8): 9–13 (in Russian).
4. Jayson GC, Kohn EC, Kitchener HC, Ledermann JA. Ovarian cancer. Lancet 2014; 384: 1376–88.
5. Chien J, Poole E. Ovarian cancer prevention, screening and early detection: report from the 11th Biennial Ovarian Cancer Research Symposium. Int J Gynecol Cancer 2018; 27: S20–2.
6. Institute of Medicine, Committee on the State of the Science in Ovarian Cancer Research, Board on Health Care Services et al. Ovarian Cancers: Evolving Paradigms in Research and Care. Washington (DC): National Academies Press (US), 2016.
7. Buys SS, Partridge E, Black A et al. Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial. JAMA 2011; 305 (22): 2295–303. DOI: 10.1001/jama.2011.766
8. Gilbert L, Basso O, Sampalis J et al. Assessment of symptomatic women for early diagnosis of ovarian cancer: results from the prospective DOvE pilot project. Lancet Oncol 2012; 13 (3): 285–91. DOI: 10.1016/S1470-2045(11)70333-3
9. Menon U, Gentry-Maharaj A, Hallett R et al. Sensitivity and specificity of multimodal and ultrasound screening for ovarian cancer, and stage distribution of detected cancers: results of the prevalence screen of the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS). Lancet Oncol 2009; 10 (4): 327–40. DOI: 10.1016/S1470-2045(09)70026-9
10. Mohaghegh P, Rockall AG. Imaging strategy for early ovarian cancer: characterization of adnexal masses with conventional and advanced imaging techniques. Radiographics 2012; 32 (6): 1751–73. DOI: 10.1148/rg.326125520
11. Thomassin-Naggara I, Cuenod CA, Darai E et al. Dynamic contrast- enhanced MR imaging of ovarian neoplasms: current status and future perspectives. Magn Reson Imaging Clin N Am 2008; 16 (4): 661–72. DOI: 10.1016/j.mric.2008.07.012
12. Anthoulakis C, Nikoloudis N, Pelvic MRI. As the “gold standard” in the subsequent evaluation of ultrasound-indeterminate adnexal lesions: a systematic review. Gynecol Oncol 2014; 132: 661–8.
13. Timmerman D, Ameye L, Fischerova D et al. Simple ultrasound rules to distinguish between benign and malignant adnexal masses before surgery: prospective validation by IOTA group. BMJ 2010; 341: c6839.
14. Van Calster, Van Hoorde K, Valentin L et al. Evaluating the risk of ovarian cancer before surgery using the ADNEX model to differentiate between benign, borderline, early and advanced stage invasive, and secondary metastatic tumours: prospective multicentre diagnostic study. BMJ 2014; 349: g5920. DOI: 10.1136/bmj.g5920
15. Andreotti RF, Timmerman D, Benacerraf BR et al. Ovarian-Adnexal Reporting Lexicon for Ultrasound: A White Paper of the ACR Ovarian-Adnexal Reporting and Data System Committee. J Am Coll Radiol 2018; 15 (10): 1415–29. DOI: 10.1016/j.jacr.2018.07.004
16. Pereira PN, Sarian LO, Yoshida A et al. Accuracy of the ADNEX MR scoring system based on a simplified MRI protocol for the assessment of adnexal masses. Diagn Interv Radiol 2018; 24: 63–71.
17. Solopova AE, Makatsaria AD, Sdvizhkov AM, Ternovoy SK. Magnetic resonance imaging in the differential diagnosis of ovarian masses: Capabilities of quantitative multiparametric evaluation. Obstetrics and Gynecology. 2017; 2: 80–5. DOI: 10.18565/aig.2017.2.80-5 (in Russian).
18. Kwee TC, Takahara T, Ochiai R et al. Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potentional applications in oncology. Eur Radiol 2008; 18: 1937–52.
19. Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR 2007; 188 (6): 1622–35.
20. Figueiras RG, Goh V, Padhani AR et al. The role of functional imaging in colorectal cancer. AJR 2010; 195 (1): 54–66.
21. Mohaghegh P, Rockall A. Imaging strategy for early ovarian cancer: characterization of adnexal masses with conventional and advanced imaging techniques. Radiographics 2012; 32 (6): 1751–73. DOI: 10.1148/rg.326125520
22. Zhao SH, Qiang JW, Zhang GF et al. Diffusion-weighted MRimaging for differentiating borderline from malignant epithelial tumors of the ovary: pathological correlation. Eur Radiol 2014; 24 (9): 2292–9. DOI: 10.1007/s00330– 014–3236–4
23. Li W, Chu C, Cui Y et al. Diffusion-weighted MRI: a useful technique to discriminate benign versus malignant ovarian surface epithelial tumors with solid and cystic components. Abdom Imaging 2012; 37: 897–903.
24. Katayama M, Masui T, Kobayashi S et al. Diffusion-weighted echo planar imaging of ovarian tumors: is it useful to measure apparent diffusion coefficients? J Comput Assist Tomogr 2002; 26: 250–6.
25. Thomassin-Naggara I, Darai E, Cuenod CA et al. Contribution of diffusion-weighted MR imaging for predicting benignity of complex adnexal masses. Eur Radiol 2009; 19: 1544–52.
26. Kim HJ, Lee SY, Shin YR et al. The value of diffusion-weighted imaging in the differential diagnosis of ovarian lesions: a meta-analysis. PLoS One 2016; 11: e0149465.
27. Zhang P, Cui Y, Li W et al. Diagnostic accuracy of diffusion-weighted imaging with conventional MR imaging for differentiating complex solid and cystic ovarian tumors at 1.5 T. World J Surg Oncol 2012; 10: 237.
28. Ren J, Huan Y, Wang H et al. Dynamic contrast-enhanced MRI of benign prostatic hyperplasia and prostatic carcinoma: correlation with angiogenesis. Clin Radiol 2008; 63: 153–9. DOI: 10.1016/j.crad.2007.07.023
29. Ho VB, Allen SF, Hood MN, Choyke PL. Renal masses: quantitative assessment of enhancement with dynamic MR imaging. Radiology 2002; 224: 695–700. DOI: 10.1148/radiol.2243011048
30. Koo HR, Cho N, Song IC et al. Correlation of perfusion parameters on dynamic contrast-enhanced MRI with prognostic factors and subtypes of breast cancers. J Magn Reson Imaging 2012; 36: 145–51. DOI: 10.1002/jmri.23635
31. Tofts PS, Berkowitz B, Schnall MD. Quantitative analysis of dynamic Gd-DTPA enhancement in breast tumors using a permeability model. Magn Reson Med. 1995; 33: 564–568. DOI: 10.1002/mrm.1910330416
32. Paweletz N, Knierim M. Tumor-related angiogenesis. Crit Rev Oncol Hematol 1989; 9: 197–242. DOI: 10.1016/S1040-8428(89)80002-2
33. Thomassin-Naggara I, Bazot M, Daraï E et al. Epithelial ovarian tumors: value of dynamic contrast-enhanced MR imaging and correlation with tumor angiogenesis. Radiology 2008; 248: 148–59. DOI: 10.1148/radiol.2481071120
34. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multi-phase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22: 880–90. DOI: 10.1007/s00330-011-2331-z
35. Li HM, Qiang JW, Ma FH, Zhao SH. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4. DOI: 10.1186/s13048-017-0302-y
36. Thomassin-Naggara I, Balvay D, Aubert E et al. Quantitative dynamic contrast-enhanced MR imaging analysis of complex adnexal masses: a preliminary study. Eur Radiol 2012; 22: 738–45. DOI: 10.1007/s00330-011-2329-6
37. Forstner R, Thomassin-Naggara I, Cunha TM et al. ESUR recommendations for MR imaging of the sonographically indeterminate adnexal mass: an update. Eur Radiol 2017; 27: 2248–57. DOI: 10.1007/s00330-016-4600-3
38. Thomassin-Naggara I, Daraï E, Cuenod CA et al. Dynamic contrast-enhanced magnetic resonance imaging: a useful tool for characterizing ovarian epithelial tumors. J Magn Reson Imaging 2008; 28 (1): 111–20. DOI: 10.1002/jmri.21377
39. Li X, Hu LJ, Zhu LM et al. The clinical value of dynamic contrast-enhanced MRI in differential diagnosis of malignant and benign ovarian lesions. Tumor Biol 2015; 36 (7): 5515–22. DOI: 10.1007/s13277-015-3219-3
40. Dilks P, Narayanan P, Reznek R et al. Can quantitative dynamic contrast-enhanced MRI independently characterize an ovarian mass? Eur Radiol 2010; 20 (9): 2176–83. DOI: 10.1007/s00330-010-1795-6
41. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multiphase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22 (4): 880–90. DOI: 10.1007/s00330-011-2331-z
42. Mansour SM, Saraya S, EI-Faissal Y. Semi-quantitative contrast-enhanced MR analysis of indeterminate ovarian tumors: when to say malignancy? Br J Radiol 2015; 88 (1053): 20150099. DOI: 10.1259/bjr.20150099
43. Li HM, Qiang JW, Ma FH et al. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4.
44. Emad-Eldin S, Grace MN, Wahba MH et al. The diagnostic potential of diffusion weighted and dynamic contrast enhanced MR imaging in the characterization of complex ovarian lesions. Egypt J Radiol Nucl Med 2018; 49: 884–91.
45. Farhood Saremi. Perfusion imaging in clinical practice. 2015.
46. Carter JS, Koopmeiners JS, Kuehn-Hajder JE et al. Quantitative multiparametric MRI of ovarian cancer. J Magn Reson Imaging 2013; 38 (6): 1501–9.
47. Li H, Feng F, Qiang J et al. Quantitative dynamic contrast-enhanced MR imaging for differentiating benign, borderline, and malignant ovarian tumors. Abdom Radiol 2018; 43: 3132–41. DOI: 10.1007/s00261-018-1569-1
2. Макаров О.В., Борисенко С.А. Профилактика, диагностика, лечение рака яичников. Российский медицинский журнал. 1996; 3: 36–40.
[Makarov O.V., Borisenko S.A. Prophylaxis, diagnosis, treatment of ovarian cancer. Med J Russ Feder. 1996; 3: 36–40 (in Russian).]
3. Гаспаров А.С., Жорданиа К.И., Паяниди Ю.Г., Дубинская Е.Д. Онкогинекологические аспекты кистозных образований яичников. Вестн. РАМН. 2013; 8 (68): 9–13.
[Gasparov A.S., Zhordania K.I., Payanidi Y.G., Dubinskaya E.D. Oncogynecologycal aspects of adnexal masses. Ann Russ Acad Med Sci. 2013; 68 (8): 9–13 (in Russian).]
4. Jayson GC, Kohn EC, Kitchener HC, Ledermann JA. Ovarian cancer. Lancet 2014; 384: 1376–88.
5. Chien J, Poole E. Ovarian cancer prevention, screening and early detection: report from the 11th Biennial Ovarian Cancer Research Symposium. Int J Gynecol Cancer 2018; 27: S20–2.
6. Institute of Medicine, Committee on the State of the Science in Ovarian Cancer Research, Board on Health Care Services et al. Ovarian Cancers: Evolving Paradigms in Research and Care. Washington (DC): National Academies Press (US), 2016.
7. Buys SS, Partridge E, Black A et al. Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial. JAMA 2011; 305 (22): 2295–303. DOI: 10.1001/jama.2011.766
8. Gilbert L, Basso O, Sampalis J et al. Assessment of symptomatic women for early diagnosis of ovarian cancer: results from the prospective DOvE pilot project. Lancet Oncol 2012; 13 (3): 285–91. DOI: 10.1016/S1470-2045(11)70333-3
9. Menon U, Gentry-Maharaj A, Hallett R et al. Sensitivity and specificity of multimodal and ultrasound screening for ovarian cancer, and stage distribution of detected cancers: results of the prevalence screen of the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS). Lancet Oncol 2009; 10 (4): 327–40. DOI: 10.1016/S1470-2045(09)70026-9
10. Mohaghegh P, Rockall AG. Imaging strategy for early ovarian cancer: characterization of adnexal masses with conventional and advanced imaging techniques. Radiographics 2012; 32 (6): 1751–73. DOI: 10.1148/rg.326125520
11. Thomassin-Naggara I, Cuenod CA, Darai E et al. Dynamic contrast- enhanced MR imaging of ovarian neoplasms: current status and future perspectives. Magn Reson Imaging Clin N Am 2008; 16 (4): 661–72. DOI: 10.1016/j.mric.2008.07.012
12. Anthoulakis C, Nikoloudis N, Pelvic MRI. As the “gold standard” in the subsequent evaluation of ultrasound-indeterminate adnexal lesions: a systematic review. Gynecol Oncol 2014; 132: 661–8.
13. Timmerman D, Ameye L, Fischerova D et al. Simple ultrasound rules to distinguish between benign and malignant adnexal masses before surgery: prospective validation by IOTA group. BMJ 2010; 341: c6839.
14. Van Calster, Van Hoorde K, Valentin L et al. Evaluating the risk of ovarian cancer before surgery using the ADNEX model to differentiate between benign, borderline, early and advanced stage invasive, and secondary metastatic tumours: prospective multicentre diagnostic study. BMJ 2014; 349: g5920. DOI: 10.1136/bmj.g5920
15. Andreotti RF, Timmerman D, Benacerraf BR et al. Ovarian-Adnexal Reporting Lexicon for Ultrasound: A White Paper of the ACR Ovarian-Adnexal Reporting and Data System Committee. J Am Coll Radiol 2018; 15 (10): 1415–29. DOI: 10.1016/j.jacr.2018.07.004
16. Pereira PN, Sarian LO, Yoshida A et al. Accuracy of the ADNEX MR scoring system based on a simplified MRI protocol for the assessment of adnexal masses. Diagn Interv Radiol 2018; 24: 63–71.
17. Солопова А.Е., Макацария А.Д., Сдвижков А.М., Терновой С.К. Магнитно-резонансная томография в дифференциальной диагностике образований яичника. Возможности количественной мультипараметрической оценки. Акушерство и гинекология. 2017; 2: 80–85. DOI: 10.18565/aig.2017.2.80-5
[Solopova AE, Makatsaria AD, Sdvizhkov AM, Ternovoy SK. Magnetic resonance imaging in the differential diagnosis of ovarian masses: Capabilities of quantitative multiparametric evaluation. Obstetrics and Gynecology. 2017; 2: 80–5. DOI: 10.18565/aig.2017.2.80-5 (in Russian).]
18. Kwee TC, Takahara T, Ochiai R et al. Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potentional applications in oncology. Eur Radiol 2008; 18: 1937–52.
19. Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR 2007; 188 (6): 1622–35.
20. Figueiras RG, Goh V, Padhani AR et al. The role of functional imaging in colorectal cancer. AJR 2010; 195 (1): 54–66.
21. Mohaghegh P, Rockall A. Imaging strategy for early ovarian cancer: characterization of adnexal masses with conventional and advanced imaging techniques. Radiographics 2012; 32 (6): 1751–73. DOI: 10.1148/rg.326125520
22. Zhao SH, Qiang JW, Zhang GF et al. Diffusion-weighted MRimaging for differentiating borderline from malignant epithelial tumors of the ovary: pathological correlation. Eur Radiol 2014; 24 (9): 2292–9. DOI: 10.1007/s00330– 014–3236–4
23. Li W, Chu C, Cui Y et al. Diffusion-weighted MRI: a useful technique to discriminate benign versus malignant ovarian surface epithelial tumors with solid and cystic components. Abdom Imaging 2012; 37: 897–903.
24. Katayama M, Masui T, Kobayashi S et al. Diffusion-weighted echo planar imaging of ovarian tumors: is it useful to measure apparent diffusion coefficients? J Comput Assist Tomogr 2002; 26: 250–6.
25. Thomassin-Naggara I, Darai E, Cuenod CA et al. Contribution of diffusion-weighted MR imaging for predicting benignity of complex adnexal masses. Eur Radiol 2009; 19: 1544–52.
26. Kim HJ, Lee SY, Shin YR et al. The value of diffusion-weighted imaging in the differential diagnosis of ovarian lesions: a meta-analysis. PLoS One 2016; 11: e0149465.
27. Zhang P, Cui Y, Li W et al. Diagnostic accuracy of diffusion-weighted imaging with conventional MR imaging for differentiating complex solid and cystic ovarian tumors at 1.5 T. World J Surg Oncol 2012; 10: 237.
28. Ren J, Huan Y, Wang H et al. Dynamic contrast-enhanced MRI of benign prostatic hyperplasia and prostatic carcinoma: correlation with angiogenesis. Clin Radiol 2008; 63: 153–9. DOI: 10.1016/j.crad.2007.07.023
29. Ho VB, Allen SF, Hood MN, Choyke PL. Renal masses: quantitative assessment of enhancement with dynamic MR imaging. Radiology 2002; 224: 695–700. DOI: 10.1148/radiol.2243011048
30. Koo HR, Cho N, Song IC et al. Correlation of perfusion parameters on dynamic contrast-enhanced MRI with prognostic factors and subtypes of breast cancers. J Magn Reson Imaging 2012; 36: 145–51. DOI: 10.1002/jmri.23635
31. Tofts PS, Berkowitz B, Schnall MD. Quantitative analysis of dynamic Gd-DTPA enhancement in breast tumors using a permeability model. Magn Reson Med. 1995; 33: 564–568. DOI: 10.1002/mrm.1910330416
32. Paweletz N, Knierim M. Tumor-related angiogenesis. Crit Rev Oncol Hematol 1989; 9: 197–242. DOI: 10.1016/S1040-8428(89)80002-2
33. Thomassin-Naggara I, Bazot M, Daraï E et al. Epithelial ovarian tumors: value of dynamic contrast-enhanced MR imaging and correlation with tumor angiogenesis. Radiology 2008; 248: 148–59. DOI: 10.1148/radiol.2481071120
34. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multi-phase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22: 880–90. DOI: 10.1007/s00330-011-2331-z
35. Li HM, Qiang JW, Ma FH, Zhao SH. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4. DOI: 10.1186/s13048-017-0302-y
36. Thomassin-Naggara I, Balvay D, Aubert E et al. Quantitative dynamic contrast-enhanced MR imaging analysis of complex adnexal masses: a preliminary study. Eur Radiol 2012; 22: 738–45. DOI: 10.1007/s00330-011-2329-6
37. Forstner R, Thomassin-Naggara I, Cunha TM et al. ESUR recommendations for MR imaging of the sonographically indeterminate adnexal mass: an update. Eur Radiol 2017; 27: 2248–57. DOI: 10.1007/s00330-016-4600-3
38. Thomassin-Naggara I, Daraï E, Cuenod CA et al. Dynamic contrast-enhanced magnetic resonance imaging: a useful tool for characterizing ovarian epithelial tumors. J Magn Reson Imaging 2008; 28 (1): 111–20. DOI: 10.1002/jmri.21377
39. Li X, Hu LJ, Zhu LM et al. The clinical value of dynamic contrast-enhanced MRI in differential diagnosis of malignant and benign ovarian lesions. Tumor Biol 2015; 36 (7): 5515–22. DOI: 10.1007/s13277-015-3219-3
40. Dilks P, Narayanan P, Reznek R et al. Can quantitative dynamic contrast-enhanced MRI independently characterize an ovarian mass? Eur Radiol 2010; 20 (9): 2176–83. DOI: 10.1007/s00330-010-1795-6
41. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multiphase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22 (4): 880–90. DOI: 10.1007/s00330-011-2331-z
42. Mansour SM, Saraya S, EI-Faissal Y. Semi-quantitative contrast-enhanced MR analysis of indeterminate ovarian tumors: when to say malignancy? Br J Radiol 2015; 88 (1053): 20150099. DOI: 10.1259/bjr.20150099
43. Li HM, Qiang JW, Ma FH et al. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4.
44. Emad-Eldin S, Grace MN, Wahba MH et al. The diagnostic potential of diffusion weighted and dynamic contrast enhanced MR imaging in the characterization of complex ovarian lesions. Egypt J Radiol Nucl Med 2018; 49: 884–91.
45. Farhood Saremi. Perfusion imaging in clinical practice. 2015.
46. Carter JS, Koopmeiners JS, Kuehn-Hajder JE et al. Quantitative multiparametric MRI of ovarian cancer. J Magn Reson Imaging 2013; 38 (6): 1501–9.
47. Li H, Feng F, Qiang J et al. Quantitative dynamic contrast-enhanced MR imaging for differentiating benign, borderline, and malignant ovarian tumors. Abdom Radiol 2018; 43: 3132–41. DOI: 10.1007/s00261-018-1569-1
________________________________________________
2. Makarov O.V., Borisenko S.A. Prophylaxis, diagnosis, treatment of ovarian cancer. Med J Russ Feder. 1996; 3: 36–40 (in Russian).
3. Gasparov A.S., Zhordania K.I., Payanidi Y.G., Dubinskaya E.D. Oncogynecologycal aspects of adnexal masses. Ann Russ Acad Med Sci. 2013; 68 (8): 9–13 (in Russian).
4. Jayson GC, Kohn EC, Kitchener HC, Ledermann JA. Ovarian cancer. Lancet 2014; 384: 1376–88.
5. Chien J, Poole E. Ovarian cancer prevention, screening and early detection: report from the 11th Biennial Ovarian Cancer Research Symposium. Int J Gynecol Cancer 2018; 27: S20–2.
6. Institute of Medicine, Committee on the State of the Science in Ovarian Cancer Research, Board on Health Care Services et al. Ovarian Cancers: Evolving Paradigms in Research and Care. Washington (DC): National Academies Press (US), 2016.
7. Buys SS, Partridge E, Black A et al. Effect of screening on ovarian cancer mortality: the Prostate, Lung, Colorectal and Ovarian (PLCO) Cancer Screening Randomized Controlled Trial. JAMA 2011; 305 (22): 2295–303. DOI: 10.1001/jama.2011.766
8. Gilbert L, Basso O, Sampalis J et al. Assessment of symptomatic women for early diagnosis of ovarian cancer: results from the prospective DOvE pilot project. Lancet Oncol 2012; 13 (3): 285–91. DOI: 10.1016/S1470-2045(11)70333-3
9. Menon U, Gentry-Maharaj A, Hallett R et al. Sensitivity and specificity of multimodal and ultrasound screening for ovarian cancer, and stage distribution of detected cancers: results of the prevalence screen of the UK Collaborative Trial of Ovarian Cancer Screening (UKCTOCS). Lancet Oncol 2009; 10 (4): 327–40. DOI: 10.1016/S1470-2045(09)70026-9
10. Mohaghegh P, Rockall AG. Imaging strategy for early ovarian cancer: characterization of adnexal masses with conventional and advanced imaging techniques. Radiographics 2012; 32 (6): 1751–73. DOI: 10.1148/rg.326125520
11. Thomassin-Naggara I, Cuenod CA, Darai E et al. Dynamic contrast- enhanced MR imaging of ovarian neoplasms: current status and future perspectives. Magn Reson Imaging Clin N Am 2008; 16 (4): 661–72. DOI: 10.1016/j.mric.2008.07.012
12. Anthoulakis C, Nikoloudis N, Pelvic MRI. As the “gold standard” in the subsequent evaluation of ultrasound-indeterminate adnexal lesions: a systematic review. Gynecol Oncol 2014; 132: 661–8.
13. Timmerman D, Ameye L, Fischerova D et al. Simple ultrasound rules to distinguish between benign and malignant adnexal masses before surgery: prospective validation by IOTA group. BMJ 2010; 341: c6839.
14. Van Calster, Van Hoorde K, Valentin L et al. Evaluating the risk of ovarian cancer before surgery using the ADNEX model to differentiate between benign, borderline, early and advanced stage invasive, and secondary metastatic tumours: prospective multicentre diagnostic study. BMJ 2014; 349: g5920. DOI: 10.1136/bmj.g5920
15. Andreotti RF, Timmerman D, Benacerraf BR et al. Ovarian-Adnexal Reporting Lexicon for Ultrasound: A White Paper of the ACR Ovarian-Adnexal Reporting and Data System Committee. J Am Coll Radiol 2018; 15 (10): 1415–29. DOI: 10.1016/j.jacr.2018.07.004
16. Pereira PN, Sarian LO, Yoshida A et al. Accuracy of the ADNEX MR scoring system based on a simplified MRI protocol for the assessment of adnexal masses. Diagn Interv Radiol 2018; 24: 63–71.
17. Solopova AE, Makatsaria AD, Sdvizhkov AM, Ternovoy SK. Magnetic resonance imaging in the differential diagnosis of ovarian masses: Capabilities of quantitative multiparametric evaluation. Obstetrics and Gynecology. 2017; 2: 80–5. DOI: 10.18565/aig.2017.2.80-5 (in Russian).
18. Kwee TC, Takahara T, Ochiai R et al. Diffusion-weighted whole-body imaging with background body signal suppression (DWIBS): features and potentional applications in oncology. Eur Radiol 2008; 18: 1937–52.
19. Koh DM, Collins DJ. Diffusion-weighted MRI in the body: applications and challenges in oncology. AJR 2007; 188 (6): 1622–35.
20. Figueiras RG, Goh V, Padhani AR et al. The role of functional imaging in colorectal cancer. AJR 2010; 195 (1): 54–66.
21. Mohaghegh P, Rockall A. Imaging strategy for early ovarian cancer: characterization of adnexal masses with conventional and advanced imaging techniques. Radiographics 2012; 32 (6): 1751–73. DOI: 10.1148/rg.326125520
22. Zhao SH, Qiang JW, Zhang GF et al. Diffusion-weighted MRimaging for differentiating borderline from malignant epithelial tumors of the ovary: pathological correlation. Eur Radiol 2014; 24 (9): 2292–9. DOI: 10.1007/s00330– 014–3236–4
23. Li W, Chu C, Cui Y et al. Diffusion-weighted MRI: a useful technique to discriminate benign versus malignant ovarian surface epithelial tumors with solid and cystic components. Abdom Imaging 2012; 37: 897–903.
24. Katayama M, Masui T, Kobayashi S et al. Diffusion-weighted echo planar imaging of ovarian tumors: is it useful to measure apparent diffusion coefficients? J Comput Assist Tomogr 2002; 26: 250–6.
25. Thomassin-Naggara I, Darai E, Cuenod CA et al. Contribution of diffusion-weighted MR imaging for predicting benignity of complex adnexal masses. Eur Radiol 2009; 19: 1544–52.
26. Kim HJ, Lee SY, Shin YR et al. The value of diffusion-weighted imaging in the differential diagnosis of ovarian lesions: a meta-analysis. PLoS One 2016; 11: e0149465.
27. Zhang P, Cui Y, Li W et al. Diagnostic accuracy of diffusion-weighted imaging with conventional MR imaging for differentiating complex solid and cystic ovarian tumors at 1.5 T. World J Surg Oncol 2012; 10: 237.
28. Ren J, Huan Y, Wang H et al. Dynamic contrast-enhanced MRI of benign prostatic hyperplasia and prostatic carcinoma: correlation with angiogenesis. Clin Radiol 2008; 63: 153–9. DOI: 10.1016/j.crad.2007.07.023
29. Ho VB, Allen SF, Hood MN, Choyke PL. Renal masses: quantitative assessment of enhancement with dynamic MR imaging. Radiology 2002; 224: 695–700. DOI: 10.1148/radiol.2243011048
30. Koo HR, Cho N, Song IC et al. Correlation of perfusion parameters on dynamic contrast-enhanced MRI with prognostic factors and subtypes of breast cancers. J Magn Reson Imaging 2012; 36: 145–51. DOI: 10.1002/jmri.23635
31. Tofts PS, Berkowitz B, Schnall MD. Quantitative analysis of dynamic Gd-DTPA enhancement in breast tumors using a permeability model. Magn Reson Med. 1995; 33: 564–568. DOI: 10.1002/mrm.1910330416
32. Paweletz N, Knierim M. Tumor-related angiogenesis. Crit Rev Oncol Hematol 1989; 9: 197–242. DOI: 10.1016/S1040-8428(89)80002-2
33. Thomassin-Naggara I, Bazot M, Daraï E et al. Epithelial ovarian tumors: value of dynamic contrast-enhanced MR imaging and correlation with tumor angiogenesis. Radiology 2008; 248: 148–59. DOI: 10.1148/radiol.2481071120
34. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multi-phase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22: 880–90. DOI: 10.1007/s00330-011-2331-z
35. Li HM, Qiang JW, Ma FH, Zhao SH. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4. DOI: 10.1186/s13048-017-0302-y
36. Thomassin-Naggara I, Balvay D, Aubert E et al. Quantitative dynamic contrast-enhanced MR imaging analysis of complex adnexal masses: a preliminary study. Eur Radiol 2012; 22: 738–45. DOI: 10.1007/s00330-011-2329-6
37. Forstner R, Thomassin-Naggara I, Cunha TM et al. ESUR recommendations for MR imaging of the sonographically indeterminate adnexal mass: an update. Eur Radiol 2017; 27: 2248–57. DOI: 10.1007/s00330-016-4600-3
38. Thomassin-Naggara I, Daraï E, Cuenod CA et al. Dynamic contrast-enhanced magnetic resonance imaging: a useful tool for characterizing ovarian epithelial tumors. J Magn Reson Imaging 2008; 28 (1): 111–20. DOI: 10.1002/jmri.21377
39. Li X, Hu LJ, Zhu LM et al. The clinical value of dynamic contrast-enhanced MRI in differential diagnosis of malignant and benign ovarian lesions. Tumor Biol 2015; 36 (7): 5515–22. DOI: 10.1007/s13277-015-3219-3
40. Dilks P, Narayanan P, Reznek R et al. Can quantitative dynamic contrast-enhanced MRI independently characterize an ovarian mass? Eur Radiol 2010; 20 (9): 2176–83. DOI: 10.1007/s00330-010-1795-6
41. Bernardin L, Dilks P, Liyanage S et al. Effectiveness of semi-quantitative multiphase dynamic contrast-enhanced MRI as a predictor of malignancy in complex adnexal masses: radiological and pathological correlation. Eur Radiol 2012; 22 (4): 880–90. DOI: 10.1007/s00330-011-2331-z
42. Mansour SM, Saraya S, EI-Faissal Y. Semi-quantitative contrast-enhanced MR analysis of indeterminate ovarian tumors: when to say malignancy? Br J Radiol 2015; 88 (1053): 20150099. DOI: 10.1259/bjr.20150099
43. Li HM, Qiang JW, Ma FH et al. The value of dynamic contrast-enhanced MRI in characterizing complex ovarian tumors. J Ovarian Res 2017; 10: 4.
44. Emad-Eldin S, Grace MN, Wahba MH et al. The diagnostic potential of diffusion weighted and dynamic contrast enhanced MR imaging in the characterization of complex ovarian lesions. Egypt J Radiol Nucl Med 2018; 49: 884–91.
45. Farhood Saremi. Perfusion imaging in clinical practice. 2015.
46. Carter JS, Koopmeiners JS, Kuehn-Hajder JE et al. Quantitative multiparametric MRI of ovarian cancer. J Magn Reson Imaging 2013; 38 (6): 1501–9.
47. Li H, Feng F, Qiang J et al. Quantitative dynamic contrast-enhanced MR imaging for differentiating benign, borderline, and malignant ovarian tumors. Abdom Radiol 2018; 43: 3132–41. DOI: 10.1007/s00261-018-1569-1
Авторы
Ю.В. Носова*, А.Е. Солопова, Г.Н. Хабас
ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии имени академика В.И. Кулакова» Минздрава России, Москва, Россия
*yu_nosova@oparina4.ru
Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*yu_nosova@oparina4.ru
ФГБУ «Национальный медицинский исследовательский центр акушерства, гинекологии и перинатологии имени академика В.И. Кулакова» Минздрава России, Москва, Россия
*yu_nosova@oparina4.ru
________________________________________________
Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology, Moscow, Russia
*yu_nosova@oparina4.ru
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