DOI QR코드

DOI QR Code

Clinical Application and Limitations of Myeloma Response Assessment and Diagnosis System (MY-RADS)

골수종 반응평가와 진단체계의 임상적용 및 제한점

  • Dong Kyun Kim (Department of Radiology, Seoul St. Mary's Hospital, and, College of Medicine, The Catholic University of Korea) ;
  • Sung-Soo Park (Department of Hematology, Seoul St. Mary's Hospital, and, College of Medicine, The Catholic University of Korea) ;
  • Joon-Yong Jung (Department of Radiology, Seoul St. Mary's Hospital, and, College of Medicine, The Catholic University of Korea)
  • 김동균 (가톨릭대학교 의과대학 서울성모병원 영상의학과) ;
  • 박성수 (가톨릭대학교 의과대학 서울성모병원 혈액내과) ;
  • 정준용 (가톨릭대학교 의과대학 서울성모병원 영상의학과)
  • Received : 2022.11.13
  • Accepted : 2023.01.16
  • Published : 2023.01.01

Abstract

Multiple myeloma, which is a proliferative disease of plasma cells that originate from a single clone, is the second most common hematologic malignancy following non-Hodgkin lymphoma. In the past, its diagnosis was made based on clinical findings (so-called "CRAB") and a skeletal survey using radiographs. However, since the implementation of the International Myeloma Working Group's revised guideline regarding the radiologic diagnosis of multiple myeloma, whole-body (WB) MRI has emerged to play a central role in the early diagnosis of multiple myeloma. Diffusion-weighted imaging and fat quantification using Dixon methods enable treatment response assessment by MRI. In keeping with the trend, a multi-institutional and multidisciplinary consensus for standardized image acquisition and reporting known as the Myeloma Response Assessment and Diagnostic System (MY-RADS) has recently been proposed. This review aims to describe the clinical application of WB-MRI based on MY-RADS in multiple myeloma, discuss its limitations, and suggest future directions for improvement.

다발성 골수종(multiple myeloma)은 단일 클론에서 기원한 형질세포의 증식성 질환으로 비호지킨림프종에 이어 두 번째로 흔한 악성 혈액종양질환이다. 과거에는 'CRAB'이라는 임상 소견과 일반 촬영을 통한 골격계 조사(skeletal survey)에 의존하여 진단하였으나, 최근 International Myeloma Working Group의 개정된 가이드라인에 영상의학적 진단기준이 새로 제시되었다. 이에 병변의 조기 발견이 가능한 전신자기공명영상(whole-body MRI; 이하 WB MRI)의 임상적 유용성이 강조되고 있다. 또한 WB-MRI의 확산강조영상(diffusion-weighted image)과 딕슨 기법을 이용한 지방함량 정량화(fat quantification) 영상을 이용한 정확한 치료반응 평가가 가능하다. 이러한 추세에 따라 표준화된 영상 획득 및 보고를 위한 다기관, 다학제적 컨센서스인 Myeloma Response Assessment and Diagnosis System (이하 MY-RADS)가 발표되었다. 본 종설은 다발성 골수종의 전신자기공명영상 및 MY-RADS의 임상 적용에 대하여 최신 지견을 중심으로 종합적 기술하고자 한다. 이에 더하여 한계점과 추후 개선 방향에 대해서도 고찰하고자 한다.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (2019R1C1C1007122).

References

  1. Siegel RL, Miller KD, Jemal A. Cancer statistics, 2015. CA Cancer J Clin 2015;65:5-29 
  2. Rollig C, Knop S, Bornhauser M. Multiple myeloma. Lancet 2015;385:2197-2208 
  3. International Myeloma Working Group. Criteria for the classification of monoclonal gammopathies, multiple myeloma and related disorders: a report of the international myeloma working group. Br J Haematol 2003;121:749-757 
  4. Mead GP, Carr-Smith HD, Drayson MT, Morgan GJ, Child JA, Bradwell AR. Serum free light chains for monitoring multiple myeloma. Br J Haematol 2004;126:348-354 
  5. Kyle RA, Remstein ED, Therneau TM, Dispenzieri A, Kurtin PJ, Hodnefield JM, et al. Clinical course and prognosis of smoldering (asymptomatic) multiple myeloma. N Engl J Med 2007;356:2582-2590 
  6. Cowan AJ, Green DJ, Kwok M, Lee S, Coffey DG, Holmberg LA, et al. Diagnosis and management of multiple myeloma: a review. JAMA 2022;327:464-477 
  7. Terpos E, Zamagni E, Lentzsch S, Drake MT, Garcia-Sanz R, Abildgaard N, et al. Treatment of multiple myeloma-related bone disease: recommendations from the bone working group of the international myeloma working group. Lancet Oncol 2021;22:e119-e130 
  8. Rajkumar SV, Dimopoulos MA, Palumbo A, Blade J, Merlini G, Mateos MV, et al. International myeloma working group updated criteria for the diagnosis of multiple myeloma. Lancet Oncol 2014;15:e538-e548 
  9. Kastritis E, Moulopoulos LA, Terpos E, Koutoulidis V, Dimopoulos MA. The prognostic importance of the presence of more than one focal lesion in spine MRI of patients with asymptomatic (smoldering) multiple myeloma. Leukemia 2014;28:2402-2403 
  10. Larsen JT, Kumar SK, Dispenzieri A, Kyle RA, Katzmann JA, Rajkumar SV. Serum free light chain ratio as a biomarker for high-risk smoldering multiple myeloma. Leukemia 2013;27:941-946 
  11. Ghanem N, Lohrmann C, Engelhardt M, Pache G, Uhl M, Saueressig U, et al. Whole-body MRI in the detection of bone marrow infiltration in patients with plasma cell neoplasms in comparison to the radiological skeletal survey. Eur Radiol 2006;16:1005-1014 
  12. Edelstyn GA, Gillespie PJ, Grebbell FS. The radiological demonstration of osseous metastases. Experimental observations. Clin Radiol 1967;18:158-162 
  13. Hillengass J, Fechtner K, Weber MA, Bauerle T, Ayyaz S, Heiss C, et al. Prognostic significance of focal lesions in whole-body magnetic resonance imaging in patients with asymptomatic multiple myeloma. J Clin Oncol 2010;28:1606-1610 
  14. Moulopoulos LA, Dimopoulos MA, Kastritis E, Christoulas D, Gkotzamanidou M, Roussou M, et al. Diffuse pattern of bone marrow involvement on magnetic resonance imaging is associated with high risk cytogenetics and poor outcome in newly diagnosed, symptomatic patients with multiple myeloma: a single center experience on 228 patients. Am J Hematol 2012;87:861-864 
  15. D'Anastasi M, Notohamiprodjo M, Schmidt GP, Durr HR, Reiser MF, Baur-Melnyk A. Tumor load in patients with multiple myeloma: β2-microglobulin levels versus whole-body MRI. AJR Am J Roentgenol 2014;203:854-862 
  16. Herget GW, Wasch R, Klein L, Schmal H, Terpos E, Engelhardt M. Prevention of bone disease and early detection of impending fractures in multiple myeloma patients can reduce morbidity and mortality: the necessity of interdisciplinary state-of-the-art treatment. Haematologica 2020;105:859-861 
  17. Lecouvet FE, Malghem J, Michaux L, Michaux JL, Lehmann F, Maldague BE, et al. Vertebral compression fractures in multiple myeloma. Part II. Assessment of fracture risk with MR imaging of spinal bone marrow. Radiology 1997;204:201-205 
  18. Blackledge MD, Collins DJ, Tunariu N, Orton MR, Padhani AR, Leach MO, et al. Assessment of treatment response by total tumor volume and global apparent diffusion coefficient using diffusion-weighted MRI in patients with metastatic bone disease: a feasibility study. PLoS One 2014;9:e91779 
  19. Pawlyn C, Fowkes L, Otero S, Jones JR, Boyd KD, Davies FE, et al. Whole-body diffusion-weighted MRI: a new gold standard for assessing disease burden in patients with multiple myeloma? Leukemia 2016;30:1446-1448 
  20. Winfield JM, Poillucci G, Blackledge MD, Collins DJ, Shah V, Tunariu N, et al. Apparent diffusion coefficient of vertebral haemangiomas allows differentiation from malignant focal deposits in whole-body diffusion-weighted MRI. Eur Radiol 2018;28:1687-1691 
  21. Dong H, Huang W, Ji X, Huang L, Zou D, Hao M, et al. Prediction of early treatment response in multiple myeloma using MY-RADS total burden score, ADC, and fat fraction from whole-body MRI: impact of anemia on predictive performance. AJR Am J Roentgenol 2022;218:310-319 
  22. Jo A, Jung JY, Lee SY, Lee SE, Park H, Lee SE, et al. Prognosis prediction in initially diagnosed multiple myeloma patients using intravoxel incoherent motion-diffusion weighted imaging and multiecho dixon imaging. J Magn Reson Imaging 2021;53:491-501 
  23. Messiou C, Hillengass J, Delorme S, Lecouvet FE, Moulopoulos LA, Collins DJ, et al. Guidelines for acquisition, interpretation, and reporting of whole-body MRI in myeloma: myeloma response assessment and diagnosis system (MY-RADS). Radiology 2019;291:5-13 
  24. Barnes A, Alonzi R, Blackledge M, Charles-Edwards G, Collins DJ, Cook G, et al. UK quantitative WB-DWI technical workgroup: consensus meeting recommendations on optimisation, quality control, processing and analysis of quantitative whole-body diffusion-weighted imaging for cancer. Br J Radiol 2018;91:20170577 
  25. Padhani AR, van Ree K, Collins DJ, D'Sa S, Makris A. Assessing the relation between bone marrow signal intensity and apparent diffusion coefficient in diffusion-weighted MRI. AJR Am J Roentgenol 2013;200:163-170 
  26. Perez-Lopez R, Nava Rodrigues D, Figueiredo I, Mateo J, Collins DJ, Koh DM, et al. Multiparametric magnetic resonance imaging of prostate cancer bone disease: correlation with bone biopsy histological and molecular features. Invest Radiol 2018;53:96-102 
  27. Lecouvet FE. Whole-body MR imaging: musculoskeletal applications. Radiology 2016;279:345-365 
  28. Koh DM, Blackledge M, Padhani AR, Takahara T, Kwee TC, Leach MO, et al. Whole-body diffusion-weighted MRI: tips, tricks, and pitfalls. AJR Am J Roentgenol 2012;199:252-262 
  29. Anagnostopoulos A, Hamilos G, Zorzou MP, Grigoraki V, Anagnostou D, Dimopoulos MA. Discordant response or progression in patients with myeloma treated with thalidomide-based regimens. Leuk Lymphoma 2004;45:113-116 
  30. Zamagni E, Tacchetti P, Cavo M. Imaging in multiple myeloma: how? when? Blood 2019;133:644-651 
  31. Lin C, Luciani A, Belhadj K, Deux JF, Kuhnowski F, Maatouk M, et al. Multiple myeloma treatment response assessment with whole-body dynamic contrast-enhanced MR imaging. Radiology 2010;254:521-531 
  32. Hillengass J, Usmani S, Rajkumar SV, Durie BGM, Mateos MV, Lonial S, et al. International myeloma working group consensus recommendations on imaging in monoclonal plasma cell disorders. Lancet Oncol 2019;20:e302-e312 
  33. Park HY, Kim KW, Yoon MA, Lee MH, Chae EJ, Lee JH, et al. Role of whole-body MRI for treatment response assessment in multiple myeloma: comparison between clinical response and imaging response. Cancer Imaging 2020;20:14 
  34. Derlin T, Peldschus K, Munster S, Bannas P, Herrmann J, Stubig T, et al. Comparative diagnostic performance of 18F-FDG PET/CT versus whole-body MRI for determination of remission status in multiple myeloma after stem cell transplantation. Eur Radiol 2013;23:570-578 
  35. Baik JS, Jung JY, Jee WH, Chun CW, Kim SK, Shin SH, et al. Differentiation of focal indeterminate marrow abnormalities with multiparametric MRI. J Magn Reson Imaging 2017;46:49-60 
  36. Sung MS, Lee GK, Kang HS, Kwon ST, Park JG, Suh JS, et al. Sacrococcygeal chordoma: MR imaging in 30 patients. Skeletal Radiol 2005;34:87-94 
  37. Moulopoulos LA, Varma DG, Dimopoulos MA, Leeds NE, Kim EE, Johnston DA, et al. Multiple myeloma: spinal MR imaging in patients with untreated newly diagnosed disease. Radiology 1992;185:833-840 
  38. Stabler A, Baur A, Bartl R, Munker R, Lamerz R, Reiser MF. Contrast enhancement and quantitative signal analysis in MR imaging of multiple myeloma: assessment of focal and diffuse growth patterns in marrow correlated with biopsies and survival rates. AJR Am J Roentgenol 1996;167:1029-1036 
  39. Lee SY, Kim HJ, Shin YR, Park HJ, Lee YG, Oh SJ. Prognostic significance of focal lesions and diffuse infiltration on MRI for multiple myeloma: a meta-analysis. Eur Radiol 2017;27:2333-2347 
  40. Ricci C, Cova M, Kang YS, Yang A, Rahmouni A, Scott WW Jr, et al. Normal age-related patterns of cellular and fatty bone marrow distribution in the axial skeleton: MR imaging study. Radiology 1990;177:83-88 
  41. Dimopoulos MA, Hillengass J, Usmani S, Zamagni E, Lentzsch S, Davies FE, et al. Role of magnetic resonance imaging in the management of patients with multiple myeloma: a consensus statement. J Clin Oncol 2015;33:657-664 
  42. Rahmouni A, Divine M, Mathieu D, Golli M, Haioun C, Dao T, et al. MR appearance of multiple myeloma of the spine before and after treatment. AJR Am J Roentgenol 1993;160:1053-1057 
  43. Moulopoulos LA, Dimopoulos MA, Alexanian R, Leeds NE, Libshitz HI. Multiple myeloma: MR patterns of response to treatment. Radiology 1994;193:441-446 
  44. Drueke TB, Massy ZA. Beta2-microglobulin. Semin Dial 2009;22:378-380 
  45. Durie BG. The role of anatomic and functional staging in myeloma: description of Durie/Salmon plus staging system. Eur J Cancer 2006;42:1539-1543 
  46. Baur A, Stabler A, Nagel D, Lamerz R, Bartl R, Hiller E, et al. Magnetic resonance imaging as a supplement for the clinical staging system of Durie and Salmon? Cancer 2002;95:1334-1345 
  47. Koutoulidis V, Fontara S, Terpos E, Zagouri F, Matsaridis D, Christoulas D, et al. Quantitative diffusion-weighted imaging of the bone marrow: an adjunct tool for the diagnosis of a diffuse MR imaging pattern in patients with multiple myeloma. Radiology 2017;282:484-493 
  48. Rasche L, Chavan SS, Stephens OW, Patel PH, Tytarenko R, Ashby C, et al. Spatial genomic heterogeneity in multiple myeloma revealed by multi-region sequencing. Nat Commun 2017;8:268 
  49. Blade J, Perales M, Rosinol L, Tuset M, Montoto S, Esteve J, et al. Thalidomide in multiple myeloma: lack of response of soft-tissue plasmacytomas. Br J Haematol 2001;113:422-424 
  50. Rager O, Espinet C, Humm J, Weber W. Mixed response on FDG PET/CT: frequency and prognostic relevance in non-small cell lung cancer (NSCLC). J Nucl Med 2014;55(supplement 1):514 
  51. Hendlisz A, Golfinopoulos V, Garcia C, Covas A, Emonts P, Ameye L, et al. Serial FDG-PET/CT for early outcome prediction in patients with metastatic colorectal cancer undergoing chemotherapy. Ann Oncol 2012;23:1687-1693 
  52. Qiang YW, Chen Y, Stephens O, Brown N, Chen B, Epstein J, et al. Myeloma-derived Dickkopf-1 disrupts Wnt-regulated osteoprotegerin and RANKL production by osteoblasts: a potential mechanism underlying osteolytic bone lesions in multiple myeloma. Blood 2008;112:196-207 
  53. Schmidt GP, Wintersperger B, Graser A, Baur-Melnyk A, Reiser MF, Schoenberg SO. High-resolution whole-body magnetic resonance imaging applications at 1.5 and 3 tesla: a comparative study. Invest Radiol 2007;42:449-459 
  54. Khodarahmi I, Fritz J. The value of 3 tesla field strength for musculoskeletal magnetic resonance imaging. Invest Radiol 2021;56:749-763 
  55. Willinek WA, Gieseke J, Kukuk GM, Nelles M, Konig R, Morakkabati-Spitz N, et al. Dual-source parallel radiofrequency excitation body MR imaging compared with standard MR imaging at 3.0 T: initial clinical experience. Radiology 2010;256:966-975 
  56. Kenkel D, Wurnig MC, Filli L, Ulbrich EJ, Runge VM, Beck T, et al. Whole-body diffusion imaging applying simultaneous multi-slice excitation. Rofo 2016;188:E1 
  57. Taron J, Schraml C, Pfannenberg C, Reimold M, Schwenzer N, Nikolaou K, et al. Simultaneous multislice diffusion-weighted imaging in whole-body positron emission tomography/magnetic resonance imaging for multiparametric examination in oncological patients. Eur Radiol 2018;28:3372-3383 
  58. Moore MM, Iyer RS, Sarwani NI, Sze RW. Artificial intelligence development in pediatric body magnetic resonance imaging: best ideas to adapt from adults. Pediatr Radiol 2022;52:367-373 
  59. Zormpas-Petridis K, Tunariu N, Curcean A, Messiou C, Curcean S, Collins DJ, et al. Accelerating whole-body diffusion-weighted MRI with deep learning-based denoising image filters. Radiol Artif Intell 2021;3:e200279 
  60. Jung W, Kim EH, Ko J, Jeong G, Choi MH. Convolutional neural network-based reconstruction for acceleration of prostate T2 weighted MR imaging: a retro- and prospective study. Br J Radiol 2022;95:20211378