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Correlation and prognosis evaluation of 18F-FDG PET/CT imaging findings with high-risk cytogenetic abnormalities in newly diagnosed multiple myeloma patients

  • 1.

    Department of Nuclear Medicine, Shantou Central Hospital, Shantou 515031, China

  • 2.

    Department of Hematology, Shantou Central Hospital, Shantou 515031, China

  • Corresponding author: Zhaohua Huang, sthzh093@163.com
  • Received Date: 2021-02-25
  • Objective To investigate the correlation between 18F-fluorodeoxyglucose (FDG) PET/CT imaging findings and high-risk cytogenetic abnormalities (HRCA) in patients newly diagnosed with multiple myeloma (MM), and the value of both combined applications in evaluating the prognosis of patients with MM. Methods The clinical and imaging data of 44 patients with MM diagnosed by bone marrow histopathology and laboratory examination and who underwent 18F-FDG PET/CT imaging before treatment in Shantou Central Hospital from June 2016 to November 2020 were retrospectively analyzed, including 23 males and 21 females, aged 38–91 (61.1±9.6) years old. Patients were divided into the HRCA group and the non-HRCA group according to the result of fluorescence in situ hybridization. Patients were divided into stage Ⅰ+Ⅱ group and stage Ⅲ group according to the Revised-International Staging System (R-ISS) issued by the International Myeloma Working Group. Patients were divided into two groups, a standard-risk group, and a high-risk group according to the Mayo Stratification of Myeloma and Risk-adapted Therapy (mSMART) 3.0 risk stratification criteria. Through the analysis of the 18F-FDG PET/CT imaging data, patients were divided into ≤3 groups and >3 groups according to the number of focal lesions (FLs), divided into ≤4.2 groups and >4.2 groups according to maximum standardized uptake value (SUVmax), divided into extramedullary disease (EMD) group and non-EMD group according to the presence of EMD lesions, respectively. Gather data on progression-free survival (PFS) and overall survival (OS) begins from the first follow-up. Imaging findings with clinical features, HRCA, and prognostic stages were compared using the χ2 test. The independent risk factors of HRCA and stages were analyzed using the multivariate logistic regression analysis. The differences between PFS and OS among the groups were compared using the Kaplan-Meier method and Log-rank test. The independent risk factors of PFS and OS were analyzed using the Cox proportional hazards regression model. Results FLs≤3 or >3 varied among groups of R-ISS, mSMART 3.0, and HRCA (χ2=4.919, 8.472, 8.167; all P<0.05). EMD or non-EMD varied among groups of mSMART 3.0 and HRCA (χ2=4.061, 6.808; both P<0.05). FLs>3 were independent risk factors for HRCA, R-ISS, and mSMART 3.0 (OR=10.952, 5.000, 10.714; 95%CI: 1.195–100.393, 1.127–22.181, 2.269–50.598; all P<0.05). PFS and OS varied among groups of EMD and HRCA (PFS: χ2=8.572, 9.023; both P<0.01 and OS: χ2=6.030, 4.877; both P<0.05). EMD was an independent poor prognosis factor for both PFS and OS (OR=4.466, 6.520; 95%CI: 1.084–18.396, 1.174–36.211; both P<0.05). HRCA was an independent poor prognosis factor for PFS (OR=8.458, 95%CI: 1.671–42.812, P<0.05). By the end of follow-up, patients without EMD and HRCA or only one of them had not reached median PFS and median OS; median PFS for patients with both EMD and HRCA was 11 months (χ2=20.903, P<0.001) and median OS were 17 months (χ2=10.656, P<0.01). Conclusion There is a significant correlation between 18F-FDG PET/CT imaging findings and HRCA in patients newly diagnosed with MM, and the combination of both has a certain predictive value for the prognosis of patients with MM.
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    [8] Patriarca F, Carobolante F, Zamagni E, et al. The role of positron emission tomography with 18F-fluorodeoxyglucose integrated with computed tomography in the evaluation of patients with multiple myeloma undergoing allogeneic stem cell transplantation[J]. Biol Blood Marrow Transplant, 2015, 21(6): 1068−1073. DOI: 10.1016/j.bbmt.2015.03.001.
    [9] Russell SJ, Rajkumar SV. Multiple myeloma and the road to personalised medicine[J]. Lancet Oncol, 2011, 12(7): 617−619. DOI: 10.1016/S1470-2045(11)70143-7.
    [10] 林志畑, 林晓平, 黄朝华. 18F-FDG PET/CT在初诊多发性骨髓瘤患者分期的临床应用[J]. 中山大学学报: 医学科学版, 2016, 37(6): 919−924. DOI: 10.13471/j.cnki.j.sun.yat-sen.univ(med.sci).2016.0127.Lin ZT, Lin XP, Huang CH. Role of 18F-FDG PET/CT in newly diagnosed multiple myeloma[J]. J Sun Yat-sen Univ (Med Sci), 2016, 37(6): 919−924. DOI: 10.13471/j.cnki.j.sun.yat-sen.univ(med.sci).2016.0127.
    [11] 邸丽娟, 张建华, 王荣福, 等. 18F-FDG PET/CT可用于多发性骨髓瘤临床分期及病灶代谢活性评价[J]. 中华核医学与分子影像杂志, 2017, 37(1): 35−38. DOI: 10.3760/cma.j.issn.2095-2848.2017.01.009.Di LJ, Zhang JH, Wang RF, et al. 18F-FDG PET/CT in staging and metabolic activity assessment of multiple myeloma[J]. Chin J Nucl Med Mol Imaging, 2017, 37(1): 35−38. DOI: 10.3760/cma.j.issn.2095-2848.2017.01.009.
    [12] Park S, Lee SJ, Chang WJ, et al. Positive correlation between baseline PET or PET/CT findings and clinical parameters in multiple myeloma patients[J]. Acta Haematol, 2014, 131(4): 193−199. DOI: 10.1159/000354839.
    [13] Abe Y, Narita K, Kobayashi H, et al. Medullary abnormalities in appendicular skeletons detected with 18F-FDG PET/CT predict an unfavorable prognosis in newly diagnosed multiple myeloma patients with high-risk factors[J]. Am J Roentgenol, 2019, 213(4): 918−924. DOI: 10.2214/AJR.19.21283.
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    [15] Rajan AM, Rajkumar SV. Interpretation of cytogenetic results in multiple myeloma for clinical practice[J/OL]. Blood Cancer J, 2015, 5(10): e365[2021-02-24]. https://www.nature.com/articles/bcj201592. DOI: 10.1038/bcj.2015.92.
    [16] Moreau P, Attal M, Caillot D, et al. Prospective evaluation of magnetic resonance imaging and 18F-fluorodeoxyglucose positron emission tomography-computed tomography at diagnosis and before maintenance therapy in symptomatic patients with multiple myeloma included in the IFM/DFCI 2009 trial: results of the IMAJEM study[J]. J Clin Oncol, 2017, 35(25): 2911−2918. DOI: 10.1200/JCO.2017.72.2975.
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Correlation and prognosis evaluation of 18F-FDG PET/CT imaging findings with high-risk cytogenetic abnormalities in newly diagnosed multiple myeloma patients

    Corresponding author: Zhaohua Huang, sthzh093@163.com
  • 1. Department of Nuclear Medicine, Shantou Central Hospital, Shantou 515031, China
  • 2. Department of Hematology, Shantou Central Hospital, Shantou 515031, China
  • Received Date: 2021-02-25
  • Available Online: 2022-04-25

Abstract:  Objective To investigate the correlation between 18F-fluorodeoxyglucose (FDG) PET/CT imaging findings and high-risk cytogenetic abnormalities (HRCA) in patients newly diagnosed with multiple myeloma (MM), and the value of both combined applications in evaluating the prognosis of patients with MM. Methods The clinical and imaging data of 44 patients with MM diagnosed by bone marrow histopathology and laboratory examination and who underwent 18F-FDG PET/CT imaging before treatment in Shantou Central Hospital from June 2016 to November 2020 were retrospectively analyzed, including 23 males and 21 females, aged 38–91 (61.1±9.6) years old. Patients were divided into the HRCA group and the non-HRCA group according to the result of fluorescence in situ hybridization. Patients were divided into stage Ⅰ+Ⅱ group and stage Ⅲ group according to the Revised-International Staging System (R-ISS) issued by the International Myeloma Working Group. Patients were divided into two groups, a standard-risk group, and a high-risk group according to the Mayo Stratification of Myeloma and Risk-adapted Therapy (mSMART) 3.0 risk stratification criteria. Through the analysis of the 18F-FDG PET/CT imaging data, patients were divided into ≤3 groups and >3 groups according to the number of focal lesions (FLs), divided into ≤4.2 groups and >4.2 groups according to maximum standardized uptake value (SUVmax), divided into extramedullary disease (EMD) group and non-EMD group according to the presence of EMD lesions, respectively. Gather data on progression-free survival (PFS) and overall survival (OS) begins from the first follow-up. Imaging findings with clinical features, HRCA, and prognostic stages were compared using the χ2 test. The independent risk factors of HRCA and stages were analyzed using the multivariate logistic regression analysis. The differences between PFS and OS among the groups were compared using the Kaplan-Meier method and Log-rank test. The independent risk factors of PFS and OS were analyzed using the Cox proportional hazards regression model. Results FLs≤3 or >3 varied among groups of R-ISS, mSMART 3.0, and HRCA (χ2=4.919, 8.472, 8.167; all P<0.05). EMD or non-EMD varied among groups of mSMART 3.0 and HRCA (χ2=4.061, 6.808; both P<0.05). FLs>3 were independent risk factors for HRCA, R-ISS, and mSMART 3.0 (OR=10.952, 5.000, 10.714; 95%CI: 1.195–100.393, 1.127–22.181, 2.269–50.598; all P<0.05). PFS and OS varied among groups of EMD and HRCA (PFS: χ2=8.572, 9.023; both P<0.01 and OS: χ2=6.030, 4.877; both P<0.05). EMD was an independent poor prognosis factor for both PFS and OS (OR=4.466, 6.520; 95%CI: 1.084–18.396, 1.174–36.211; both P<0.05). HRCA was an independent poor prognosis factor for PFS (OR=8.458, 95%CI: 1.671–42.812, P<0.05). By the end of follow-up, patients without EMD and HRCA or only one of them had not reached median PFS and median OS; median PFS for patients with both EMD and HRCA was 11 months (χ2=20.903, P<0.001) and median OS were 17 months (χ2=10.656, P<0.01). Conclusion There is a significant correlation between 18F-FDG PET/CT imaging findings and HRCA in patients newly diagnosed with MM, and the combination of both has a certain predictive value for the prognosis of patients with MM.

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  • 多发性骨髓瘤（multiple myeloma，MM）是一种浆细胞增殖异常的恶性疾病，约占血液系统恶性肿瘤的10%[1]。MM患者的临床特征及预后差异很大，建立精准的预后评估体系是制定个性化治疗方案和改善预后的关键。

    高危细胞遗传学异常（high-risk cytogenetic abnormalities，HRCA）是MM分期的重要指标，与其临床特征具有一定的相关性[2]。近年来，18F-FDG PET/CT作为一种将解剖结构和功能显像相结合的影像学检查方法，已被国际骨髓瘤工作组推荐应用于初诊MM患者的预后评估[3]，但目前关于MM患者的18F-FDG PET/CT影像学表现与HRCA相关性的研究较少。本研究旨在分析MM的18F-FDG PET/CT影像学表现与HRCA的相关性，并初步探讨18F-FDG PET/CT影像学表现与HRCA联合应用在MM患者预后评估中的价值。

    • 1.   资料与方法

      1.1.   一般资料

    • 回顾性分析2016年6月至2020年11月于汕头市中心医院确诊为MM的44例患者的临床资料和影像学资料，其中男性23例、女性21例，年龄38~91（61.1±9.6）岁。纳入标准：经骨髓组织病理学检查结果、实验室检查结果确诊为MM的患者。排除标准：患有其他恶性肿瘤或严重的心脏、肝、肺、肾等疾病的患者。所有患者均于检查前签署了知情同意书。本研究符合《赫尔辛基宣言》的原则。

      以荧光原位杂交（FISH）检测结果确定是否存在t（4; 14）、t（14; 16）、t（14; 20）、17p−、1q+和p53突变，作为有无HRCA的分组标准。按照国际骨髓瘤工作组发布的修订版国际分期系统（Revised-International Staging System，R-ISS）的分期标准[4]和Mayo骨髓瘤分层级风险调整治疗（Mayo Stratification of Myeloma and Risk-Adapted Therapy，mSMART）3.0危险度分层标准[5]对患者进行分组。

      • 1.2.   影像学检查

    • 所有患者均于治疗前行18F-FDG PET/CT显像。显像剂为18F-FDG，购自北京原子高科股份有限公司，放射化学纯度>95%，使用美国GE公司Discovery Elite PET/CT仪进行显像。所有患者均于检查前空腹6 h以上，将血糖水平控制在10 mmol/L以下。患者平静状态下经静脉注射18F-FDG，剂量为3.7 MBq/kg，并静卧休息60 min。排空膀胱后行18F-FDG PET/CT显像，扫描范围自颅顶至双大腿中段。先进行CT平扫，参数：管电压120 kV、管电流自动调节、矩阵512×512、层厚3.3 mm、间隔3.27 mm。随后进行PET扫描，采用三维数据采集模式，1.5 min/床位、重建层厚3.75 mm。扫描完成后采用CT平扫数据对PET图像进行衰减校正，PET图像采用有序子集最大期望值+飞行时间技术+点扩展函数技术迭代法重建后获得PET/CT融合图像。

      • 1.3.   图像分析

    • 所有图像均由1位具有5年以上工作经验的核医学科主治医师阅片，由1位具有10年以上工作经验的主任医师审核，意见有分歧时，由第3位具有10年以上工作经验的主任医师阅片后统一意见。将骨骼内除关节部位外高于骨髓背景摄取的高代谢病灶（不论是否伴有相应部位骨质破坏）中最大径>1.0 cm且SUVmax≥2.5或最大径在0.5~1.0 cm且SUVmax≥1.5的溶骨性病灶定义为局灶病变（focal lesions，FLs）[6-7]。FLs经其他影像学检查或临床随访确认，并根据其个数（≤3或>3）进行分组。参考既往相关研究普遍采用的分组方法[7-8]，以FLs的SUVmax≤4.2或>4.2进行分组。将与骨不相关的FLs定义为髓外病变（extramedullary disease，EMD），并以有无EMD进行分组。

      • 1.4.   随访方法

    • 通过病历资料和电话随访患者的生存情况，随访终止时间为2020年12月，时间1~51（21.7±13.5）个月。无进展生存（progression-free survival，PFS）期为疾病确诊至疾病进展、复发或随访终止的时间。总生存（overall survival，OS）期为疾病确诊至患者病死或随访终止的时间。

      • 1.5.   统计学分析

    • 应用SPSS 22.0软件进行统计学分析。计数资料以个数或百分数表示，采用χ2检验比较MM患者的18F-FDG PET/CT影像学表现与临床特征、HRCA和分期等差异；采用多因素Logistic回归分析MM患者HRCA、R-ISS分期和mSMART 3.0分期的独立危险因素。采用Kaplan-Merier和Log-rank检验比较组间PFS期和OS期的差异。将FLs个数、SUVmax、有无EMD、有无HRCA纳入Cox比例风险回归模型，分析PFS期和OS期的独立预后不良因素。P<0.05为差异有统计学意义。

    2.   结果

      2.1.   一般资料

    • 44例MM患者的临床特征：年龄<65岁26例、≥65岁18例；无HRCA 25例、有HRCA 19例；R-ISS分期Ⅰ期+Ⅱ期21例、Ⅲ期23例；mSMART 3.0分期标危组16例、高危组28例。18F-FDG PET/CT影像学表现：FLs个数≤3共12例（典型病例的18F-FDG PET/CT显像结果见图1）、>3共32例；SUVmax≤4.2共11例、>4.2共33例；无EMD 共32例、有EMD共12例（图2）。随访结果：44例MM患者均无失访，其中11例出现疾病进展或复发，6例病死。

      Figure 1.  18F-FDG PET/CT images of a patient (male, 80 years old) with multiple myeloma

      Figure 2.  18F-FDG PET/CT images of a patient (male, 57 years old) with multiple myeloma

      • 2.2.   18F-FDG PET/CT影像学表现与HRCA及分期的相关性分析

    • 由表1可知，FLs个数≤3或>3在有无HRCA分组、不同R-ISS分期和不同mSMART 3.0分期间的差异均有统计学意义（均P<0.05）；有无EMD在不同mSMART 3.0分期和有无HRCA分组间的差异均有统计学意义（均P<0.05）；SUVmax≤4.2或>4.2在分期和有无HRCA分组间的差异均无统计学意义（均P>0.05）。

      因素例数（%）FLs个数≤3或>3SUVmax≤4.2或>4.2无或有EMD
      χ2值P值χ2值P值χ2值P值
      性别 0.243 0.622 0.759 0.384 0.744 0.388
      　男 23（52.3）
      　女 21（47.7）
      年龄 1.200 0.273 1.128 0.479 0.001 1.000
      　<65岁 26（59.1）
      　≥65岁 18（40.9）
      HRCA 8.167 0.004 0.001 1.000 6.808 0.009
      　无 25（56.8）
      　有 19（43.2）
      R-ISS分期 4.919 0.027 0.030 0.862 3.416 0.065
      　Ⅰ期+Ⅱ期 21（47.7）
      　Ⅲ期 23（52.3）
      mSMART 3.0分期 8.472 0.004 0.131 0.717 4.061 0.044
      　标危 16（36.4）
      　高危 28（63.6）
      注：FDG为氟脱氧葡萄糖；PET为正电子发射断层显像术；CT为计算机体层摄影术；HRCA为高危细胞遗传学异常；FLs为局灶病变；SUVmax为最大标准化摄取值；EMD为髓外病变；R-ISS为修订版国际分期系统；mSMART为Mayo骨髓瘤分层级风险调整治疗

      Table 1.  Comparison of 18F-FDG PET/CT imaging findings with clinical features, high-risk cytogenetic abnormalities and stages in 44 patients newly diagnosed with multiple myeloma

      由表2可知，FLs个数>3是HRCA、R-ISS分期和mSMART 3.0分期的独立危险因素（均P<0.05）。EMD不是HRCA、R-ISS分期和mSMART 3.0分期的独立危险因素（均P>0.05）。SUVmax>4.2不是HRCA、R-ISS分期和mSMART 3.0分期的独立危险因素（χ2=0.042~1.357，均P>0.05）。

      因素局灶病变个数>3有髓外病变
      OR值95%CIP值OR值95%CIP值
      HRCA 10.952 1.195~100.393 0.034 4.900 0.981~24.483 0.053
      R-ISS分期 5.000 1.127~22.181 0.034 2.805 0.592~13.300 0.194
      mSMART 3.0分期 10.714 2.269~50.598 0.003 7.184 0.653~79.021 0.107
      注：HRCA为高危细胞遗传学异常；R-ISS为修订版国际分期系统；mSMART为Mayo骨髓瘤分层级风险调整治疗；CI 为置信区间

      Table 2.  Analysis of independent risk factors affecting high-risk cytogenetic abnormalities and staging in 44 patients newly diagnosed with multiple myeloma

      • 2.3.   预后评估

    • Log-rank检验结果显示，有无EMD和有无HRCA组间在PFS期和OS期的差异均有统计学意义（均P<0.05，图3）。

      Figure 3.  Kaplan-Merier survival curves of 44 patients newly diagnosed with multiple myeloma

      Cox比例风险模型多因素分析结果显示，EMD是PFS期和OS期的独立预后不良因素；HRCA是PFS期的独立预后不良因素（均P<0.05，表3）。

      因素无进展生存期 总生存期
      OR值95%CIP值OR值95%CIP值
      髓外病变 4.466 1.084~18.396 0.038 6.520 1.174~36.211 0.032
      高危细胞遗传学异常 8.458 1.671~42.812 0.010 − − 0.155
      注： CI 为置信区间；−表示无此项数据

      Table 3.  Analysis of Cox proportional hazards model multiple factors affecting the prognosis of 44 patients newly diagnosed with multiple myeloma

      至随访结束，无EMD且无HRCA或仅存在两者之一的患者均未达到中位PFS期和中位OS期，同时存在EMD和HRCA患者的中位PFS期为11个月（P<0.001），中位OS期为17个月（P=0.005），同时存在EMD和HRCA的患者预后较无EMD且无HRCA或仅存在两者之一的患者预后差（图3）。

    3.   讨论

    • MM是一种高度异质性疾病，患者的预后受宿主、肿瘤负荷、HRCA和治疗反应等多种因素影响而差异很大[9]，影像学方法是在临床分期基础上进一步提高预后评估准确性的重要手段。既往18F-FDG PET/CT影像学表现与MM分期的相关性研究主要涉及DS（Durie Salmon）分期和R-ISS分期[10-11]。美国梅奥诊所于2018年基于HRCA研究而更新的mSMART 3.0发布时间较短，其与影像学表现的相关性研究未见报道[5]。同时，目前HRCA与影像学表现的相关性研究较少且结论不一[12-13]，亦未见其与影像学方法联合应用于MM患者预后评估的研究。在本研究中，我们分析了18F-FDG PET/CT影像学表现与初诊MM患者的HRCA和分期的相关性，并初步探讨18F-FDG PET/CT的影像学表现和HRCA联合应用于MM患者预后评估中的价值。

      本研究中，多因素分析结果显示，FLs个数>3是HRCA的独立危险因素，与Park等[12]和Abe等[13]的研究结果相似。但与Moon等[14]的研究结果不一致，可能与对HRCA的定义不同有关，本研究采用mSMART 3.0定义的t（4; 14）、t（14; 16）、t（14; 20）、17p−、1q+和p53突变为HRCA，而Moon等[14]则未将p53突变和1q+纳入HRCA的研究。p53突变和1q+往往为二次打击的遗传学异常，出现于疾病的进展、复发或终末期[15]，其患者预后相对较差，因此我们认为本研究对HRCA的定义更符合临床实际。

      本研究中，多因素分析结果显示，FLs个数>3与R-ISS分期具有相关性，这与Park等[12]的研究结果存在差异，可能与研究中R-ISS分期的分组方式不同有关，其研究采用Ⅰ、Ⅱ~Ⅲ期进行分组，而本研究因样本分布原因采用Ⅰ~Ⅱ、Ⅲ期进行分组，后期我们仍需通过增加样本量并采用多种分组方式进一步研究。本研究通过多因素分析结果显示，FLs个数>3为mSMART 3.0分期的独立危险因素，首次揭示了18F-FDG PET/CT影像学表现与mSMART 3.0分期具有一定的相关性。

      本研究中，多因素分析结果显示，存在EMD是PFS期和OS期的独立预后不良因素，与Bartel等[6]和Moreau等[16]的研究结果相似。但Bartel等[6]认为，FLs个数>3是患者PFS期和OS期的独立预后不良因素，其结果与本研究不一致。本研究结果FLs个数>3组中，虽然中位PFS期和中位OS期相较于FLs个数≤3组短，但差异无统计学意义，分析原因可能与样本数量和后期治疗方案有关。本研究结果中SUVmax≤4.2或>4.2对PFS期和OS期无明显影响，而Zamagni等[7]的研究结果表明，SUVmax>4.2是PFS期和OS期的独立预后不良因素，Patriarca等[8]的研究结果则表明SUVmax>4.2与OS期相关而与PFS期无关，本研究结果与其他研究结果不一致的原因可能与本研究样本量相对较少且未排除病理性骨折等影响SUVmax的因素有关。

      既往有研究者认为，影像学联合β2-微球蛋白（β2-MG）、乳酸脱氢酶（LDH）等实验室检查指标对MM的预后评估有较好的应用价值[17]，本研究中生存分析结果显示，同时存在EMD和HRCA 2种危险因素的患者中位PFS期和中位OS期相较于不存在此2种危险因素或仅存在此2种危险因素其中之一的患者均短，其生存预期相对较差，这提示影像学联合HRCA对MM的预后评估亦具有一定的应用价值。

      本研究存在一些局限性，包括样本量较少、未考虑不同类型的HRCA对预后可能产生的影响，仍需通过增加样本量、对不同类型的HRCA进行分组等方法来进一步研究论证。

      总之，初诊MM患者的18F-FDG PET/CT影像学表现与HRCA及与HRCA相关的分期（R-ISS分期和mSMART 3.0分期）均存在相关性，存在EMD是MM患者的独立预后不良因素，EMD联合HRCA对MM患者的预后评估有一定的应用价值。

      利益冲突　所有作者声明无利益冲突

      作者贡献声明　林志畑负责命题的设计、数据的分析、论文的撰写；蔡宋浩、黄锦桂负责数据的收集与分析；黄朝华负责命题的设计、论文的审阅

Reference (17)

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