Volume 42 Issue 5
Oct.  2018
Article Contents


The application and progress of PET/CT and MRI in multiple myeloma

  • Multiple myeloma (MM) is a malignant B-cell neoplasm, primarily involving the bone marrow, and some may have extramedullary involvement. Imaging examination is an indispensable tool for comprehensive assessment of MM X-ray and CT have lower lesion detection rate, poor quantitative ability. PET/CT and MRI have great value in the assessment of MM, especially the application of 18F-FDG and other novel molecular probes, whole-body diffusion weighted imaging (DWI), dynamic contrast-enhanced (DCE) MRI and water-fat separation. The author will review the application and progress of PET/CT and MRI in MM.
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    [9] Fonti R, Larobina M, Del Vecchio S, et al. Metabolic tumor volume assessed by 18F-FDG PET/CT for the prediction of outcome in patients with multiple myeloma[J]. J Nucl Med, 2012, 53 (12):1829-1835. DOI:10.2967/jnumed.112.106500.
    [10] Bladé J, de Larrea CF, Rosiñol L. Extramedullary involvement in multiple myeloma[J]. Haematologica, 2012, 97 (11):1618-1619. DOI:10.3324/haematol.2012.078519.
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    [16] Okasaki M, Kubota K, Minamimoto R, et al. Comparison of 11C-4'-thiothymidine, 11C-methionine, and 18F-FDG PET/CT for the detection of active lesions of multiple myeloma[J]. Ann Nucl Med, 2015, 29 (3):224-232. DOI:10.1007/s12149-014-0931-9.
    [17] Lapa C, Knop S, Schreder M, et al. 11C-Methionine-PET in Multiple Myeloma:Correlation with Clinical Parameters and Bone Marrow Involvement[J]. Theranostics, 2016, 6 (2):254-261. DOI:10.7150/thno.13921.
    [18] Lin C, Ho CL, Ng SH, et al. 11C-acetate as a new biomarker for PET/CT in patients with multiple myeloma:initial staging and postinduction response assessment[J]. Eur J Nucl Med Mol Imaging, 2014, 41 (1):41-49. DOI:10.1007/s00259-013-2520-x.
    [19] Ho CL, Chen S, Leung YL, et al. 11C-acetate PET/CT for metabolic characterization of multiple myeloma:a comparative study with 18F-FDG PET/CT[J]. J Nucl Med, 2014, 55 (5):749-752. DOI:10.2967/jnumed.113.131169.
    [20] Nanni C, Zamagni E, Cavo M, et al. 11C-choline vs. 18F-FDG PET/CT in assessing bone involvement in patients with multiple myeloma[J/OL]. World J Surg Oncol, 2007, 5: 68[2018-02-21]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1913918. DOI: 10.1186/1477-7819-5-68.
    [21] Philipp-Abbrederis K, Herrmann K, Knop S, et al. In vivo molecular imaging of chemokine receptor CXCR4 expression in patients with advanced multiple myeloma[J]. EMBO Mol Med, 2015, 7 (4):477-487. DOI:10.15252/emmm.201404698.
    [22] Lapa C, Schreder M, Schirbel A, et al.[68Ga]Pentixafor-PET/CT for imaging of chemokine receptor CXCR4 expression in multiple myeloma-Comparison to[18F]FDG and laboratory values[J/OL]. Theranostics, 2017, 7 (1): 205-212[2018-02-21]. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5196897. DOI: 10.7150/thno.16576.
    [23] Dimopoulos MA, Hillengass J, Usmani S, et al. Role of magnetic resonance imaging in the management of patients with multiple myeloma:a consensus statement[J]. J Clin Oncol, 2015, 33 (6):657-664. DOI:10.1200/JCO.2014.57.9961.
    [24] Baur-Melnyk A, Buhmann S, Becker C, et al. Whole-body MRI versus whole-body MDCT for staging of multiple myeloma[J]. AJR Am J Roentgenol, 2008, 190 (4):1097-1104. DOI:10.2214/AJR.07.2635.
    [25] Mai EK, Hielscher T, Kloth JK, et al. Association between magnetic resonance imaging patterns and baseline disease features in multiple myeloma:analyzing surrogates of tumour mass and biology[J]. Eur Radiol, 2016, 26 (11):3939-3948. DOI:10.1007/s00330-015-4195-0.
    [26] Moulopoulos LA, Dimopoulos MA, Kastritis E, 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[J]. Am J Hematol, 2012, 87 (9):861-864. DOI:10.1002/ajh.23258.
    [27] Bartel TB, Haessler J, Brown TL, et al. F18-fluorodeoxyglucose positron emission tomography in the context of other imaging techniques and prognostic factors in multiple myeloma[J]. Blood, 2009, 114 (10):2068-2076. DOI:10.1182/blood-2009-03-213280.
    [28] Mai EK, Hielscher T, Kloth JK, et al. A magnetic resonance imaging-based prognostic scoring system to predict outcome in transplant-eligible patients with multiple myeloma[J]. Haematologica, 2015, 100 (6):818-825. DOI:10.3324/haematol.2015.124115.
    [29] Giles SL, DeSouza NM, Collins DJ, et al. Assessing myeloma bone disease with whole-body diffusion-weighted imaging:comparison with x-ray skeletal survey by region and relationship with laboratory estimates of disease burden[J]. Clin Radiol, 2015, 70 (6):614-621. DOI:10.1016/j.crad.2015.02.013.
    [30] Pawlyn C, Fowkes L, Otero S, et al. Whole-body diffusion-weighted MRI:a new gold standard for assessing disease burden in patients with multiple myeloma?[J]. Leukemia, 2016, 30 (6):1446-1448. DOI:10.1038/leu.2015.338.
    [31] Horger M, Weisel K, Horger W, et al. Whole-body diffusion-weighted MRI with apparent diffusion coefficient mapping for early response monitoring in multiple myeloma:preliminary results[J]. AJR Am J Roentgenol, 2011, 196 (6):W790-795. DOI:10.2214/AJR.10.5979.
    [32] Lacognata C, Crimì F, Guolo A, et al. Diffusion-weighted whole-body MRI for evaluation of early response in multiple myeloma[J]. Clin Radiol, 2017, 72 (10):850-857. DOI:10.1016/j.crad.2017.05. 004.
    [33] Messiou C, Kaiser M. Whole body diffusion weighted MRI-a new view of myeloma[J]. Br J Haematol, 2015, 171 (1):29-37. DOI:10.1111/bjh.13509.
    [34] Koh DM, Blackledge M, Padhani AR, et al. Whole-body diffusion-weighted MRI:tips, tricks, and pitfalls[J]. AJR Am J Roentgenol, 2012, 199 (2):252-262. DOI:10.2214/AJR.11.7866.
    [35] Merz M, Ritsch J, Kunz C, et al. Dynamic Contrast-Enhanced Magnetic Resonance Imaging for Assessment of Antiangiogenic Treatment Effects in Multiple Myeloma[J/OL]. Clin Cancer Res, 2015, 21 (1): 106-112[2018-02-21]. http://clincancerres.aacrjournals.org/content/21/1/106.long. DOI: 10.1158/1078-0432.CCR-14-1029.
    [36] Merz M, Moehler TM, Ritsch J, et al. Prognostic significance of increased bone marrow microcirculation in newly diagnosed multiple myeloma:results of a prospective DCE-MRI study[J]. Eur Radiol, 2016, 26 (5):1404-1411. DOI:10.1007/s00330-015-3928-4.
    [37] Lin C, Luciani A, Belhadj K, et al. Multiple myeloma treatment response assessment with whole-body dynamic contrast-enhanced MR imaging[J]. Radiology, 2010, 254 (2):521-531. DOI:10.1148/radiol.09090629.
    [38] Takasu M, Tani C, Sakoda Y, et al. Iterative decomposition of water and fat with echo asymmetry and least-squares estimation (IDEAL) imaging of multiple myeloma:initial clinical efficiency results[J].Eur Radiol, 2012, 22 (5):1114-1121. DOI:10.1007/s00330-011-2351-8.
    [39] Takasu M, Kaichi Y, Tani C, et al. Iterative Decomposition of Water and Fat with Echo Asymmetry and Least-Squares Estimation (IDEAL) Magnetic Resonance Imagingas a Biomarker for Symptomatic Multiple Myeloma[J/OL]. PLoS One, 2015, 10 (2): e116842[2018-02-21]. http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0116842. DOI: 10.1371/journal.pone.0116842.
    [40] Latifoltojar A, Hall-Craggs M, Rabin N, et al. Whole body magnetic resonance imaging in newly diagnosed multiple myeloma:early changes in lesional signal fat fraction predict disease response[J]. Br J Haematol, 2017, 176 (2):222-233. DOI:10.1111/bjh.14401.
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    [43] Shah SN, Oldan JD. PET/MR Imaging of Multiple Myeloma[J]. Magn Reson Imaging Clin N Am, 2017, 25 (2):351-365. DOI:10.1016/j.mric.2017.01.003.
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The application and progress of PET/CT and MRI in multiple myeloma

    Corresponding author: Yong He, vincentheyong@163.com
  • Department of Nuclear Medicine, Zhong Nan Hospital of Wuhan University, Wuhan 430071, China

Abstract: Multiple myeloma (MM) is a malignant B-cell neoplasm, primarily involving the bone marrow, and some may have extramedullary involvement. Imaging examination is an indispensable tool for comprehensive assessment of MM X-ray and CT have lower lesion detection rate, poor quantitative ability. PET/CT and MRI have great value in the assessment of MM, especially the application of 18F-FDG and other novel molecular probes, whole-body diffusion weighted imaging (DWI), dynamic contrast-enhanced (DCE) MRI and water-fat separation. The author will review the application and progress of PET/CT and MRI in MM.


  • 多发性骨髓瘤(multiple myeloma,MM)是一种恶性B细胞肿瘤,其主要累及骨髓,部分也可出现髓外浸润[1]。MM的评估除了依赖临床指标外,影像学检查也是不可或缺的手段。X射线与CT对于病灶的检出率低、定量能力差,并且疗效的评估价值有限[2]18F-FDG PET/CT、MRI因其诸多方面的优势,目前均已被推荐应用于MM患者病情的全面评估。近年来,随着分子影像学的发展,多种新型PET分子探针及MRI新技术在MM中的应用也被认为具有较大的价值。本文对PET/CT及MRI在MM中的应用与进展进行综述。

1.   18F-FDG PET/CT在MM中的应用
  • 18F-FDG PET/CT是目前最成熟的分子影像技术之一,能够同时反映病灶的结构与代谢情况。目前,18F-FDG PET/CT在MM的诊断、分期、疗效评估、预后分析以及微小残留病(minimal residual disease,MRD)探测方面均具有一定价值。

  • 1.1.   诊断与分期

  • 18F-FDG PET/CT具有快速、灵敏及全身一次性显像的优势。2006年,18F-FDG PET/CT已被纳入最新的Durie/Salmon PLUS分期系统[3]。在诊断效能方面,Zamagni等[4]研究结果显示,在46%的MM患者中,PET/CT较全身X射线发现更多病灶;在35%的患者中,18F-FDG PET/CT较全脊柱及骨盆MRI发现更多病灶(主要位于MRI的探测视野之外)。另外,有研究对比了18F-FDG PET/CT与全身MRI在MM中的应用价值,其观点认为18F-FDG PET/CT与全身MRI对局灶型病灶的诊断效能相当,但对于弥漫型病灶(特别是浆细胞浸润比例较低的弥漫性病变),18F-FDG PET/CT灵敏度低于全身MRI[5]。除此之外,对于弥散性骨髓增生及微小骨髓浸润病灶,18F-FDG PET/CT仍可分别产生假阳性和假阴性结果[2, 5]

  • 1.2.   疗效评估

  • 18F-FDG PET/CT不同于常规CT及MRI检查,它可通过病灶代谢情况来区分活性病灶与非活性病灶,因此被认为更适用于MM的疗效评估。虽然18F-FDG PET/CT在疗效评估方面也存在一定的假阳性,但其假阳性率明显低于MRI。有研究结果显示,完全缓解的MM患者18F-FDG PET/CT与全身MRI的假阳性率分别为14.3%、61.9%[6]

  • 1.3.   预后分析

  • 18F-FDG PET/CT的某些参数与MM患者的预后密切相关。Zamagni等[7]认为FDG活性病灶数量>3个或SUVmax>4.2以及髓外病变是无进展生存期(progression free survival,PFS)及总生存期(overall survival,OS)的不良预后因素。Usmani等[8]研究结果显示,对于自体造血干细胞移植治疗后的MM患者,FDG活性病灶数量>3个是OS的独立预后因子。除此之外,肿瘤代谢体积(MTV)与MM的预后也有一定的相关性,Fonti等[9]研究结果显示,肿瘤代谢体积≥42.2和≥76.6分别是MM患者PFS和OS的不良预后因素。

  • 1.4.   MRD

  • 以下多项研究认为18F-FDG PET/CT可作为MRD评估的一种补充手段。一方面,部分MM患者存在髓外病变[10],骨髓穿刺结果只能反映骨髓浆细胞情况而不能反映髓外病变情况,18F-FDG PET/CT则能弥补这一缺陷[11];另一方面,MM患者浆细胞在骨髓的分布并不均匀,有些骨髓穿刺结果提示的完全缓解可能存在一定的假阴性结果,Zamagni等[12]研究结果显示,189例MM患者中有53%显示完全缓解,但其中仍有29%患者显示18F-FDG PET/CT阳性,并且这部分患者较18F-FDG PET/CT阴性患者的PFS和OS均明显缩短。

2.   其他分子探针的PET/CT显像
  • 目前,MM患者PET/CT的显像剂主要是18F-FDG,但其存在一定的局限性。MM具有低度增殖的特性,并不是所有的瘤细胞都过度表达葡萄糖转运体1,所以18F-FDG PET/CT不能区分一些良性病变与低代谢的肿瘤病灶,超过1/3的髓内病灶在18F-FDG PET/CT上表现为阴性[13]。因此,新型的分子探针显得尤为重要。

  • 2.1.   11C-蛋氨酸

  • 11C-蛋氨酸是一种新型的PET显像剂,它的高代谢反映了体内蛋白质的高合成状态[14]。Dankerl等[14]首次将11C-蛋氨酸用于MM患者的PET/CT显像,初步证实了11C-蛋氨酸PET/CT可以用于MM患者的肿瘤负荷评估、分期及活性病灶的探测。Nakamoto等[15]认为11C-蛋氨酸能比18F-FDG探测到更多的MM病灶,特别是18F-FDG显像不确定的病灶。Okasaki等[16]也认为11C-蛋氨酸能更加清晰地显示18F-FDG不确定的病灶。并且其对有活性的MM病灶的灵敏度高,特别是在早期MM的表现更为明显。另外,11C-蛋氨酸还能清晰地显示颅骨的病灶,克服了18F-FDG在颅骨病灶检测上的缺陷。Lapa等[17]认为11C-蛋氨酸在髓外病变检测方面也比18F-FDG更有优势。

  • 2.2.   11C-乙酸盐

  • 骨髓瘤细胞高度表达脂肪酸合成酶,并能通过脂肪酸合成酶来代谢乙酸盐。Lin等[18]研究结果显示,无论是局灶型还是弥漫型病灶,11C-乙酸盐相对于18F-FDG均具有较大的优势。不仅如此,该研究结果还显示,治疗有效的MM患者11C-乙酸盐代谢水平较治疗之前均有所减低(2%~83%),并且治疗后明显缓解的MM患者平均11C-乙酸盐代谢减低程度(66%)比部分缓解的MM患者平均乙酸盐代谢减低程度(34%)降低的更为明显,从而证实了11C-乙酸盐在MM患者疗效评估中的应用价值。Ho等[19]也认为11C-乙酸盐较18F-FDG能够更精确地反映MM代谢特点。

  • 2.3.   11C-胆碱

  • 胆碱是磷脂合成的前体,主要参与磷脂酰胆碱和细胞膜的生物合成。肿瘤细胞的分裂增殖活动旺盛,需要大量的胆碱合成磷脂酰胆碱和细胞膜,胆碱进入肿瘤细胞内,一旦被磷酸化后就无法穿过细胞膜,只能停滞在细胞内,即“化学停滞”,这就是胆碱类显像剂用于肿瘤显像的基本原理。Nanni等[20]11C-胆碱用于MM的PET显像,结果显示11C-胆碱较18F-FDG能发现更多的病灶(37/22)。

  • 2.4.   68Ga-Pentixafor

  • 部分MM患者的骨髓瘤细胞会过度表达CXC趋化因子受体4(CXC chemokine receptor 4,CXCR4),从而介导骨髓瘤细胞的生长、播散,这部分患者预后较差。68Ga-Pentixafor是一种对CXCR4具有高亲和力的PET显像探针[21-22]。Philipp-Abbrederis等[21]研究结果显示,68Ga-Pentixafor对于高表达CXCR4的MM患者是一种良好的PET显像剂,可用于指导这部分患者的CXCR4放射免疫治疗。Lapa等[22]认为68Ga-Pentixafor的主要应用价值不在于诊断MM,而在于筛选高表达CXCR4的MM患者,从而指导患者的CXCR4放射免疫治疗及进行预后评估。

3.   MRI在MM中的应用
  • 常规MRI具有良好的软组织分辨率及对比度,能清晰地显示骨髓及周围软组织情况。全身扩散加权成像(diffusion weighted imaging,DWI)、动态增强MRI(dynamic contrast-enhanced,DCE-MRI)及水脂分离等新技术可提供诸多定量指标,并能对MM进行更精确地评估。

  • 3.1.   常规MRI

  • MM在常规MRI上主要表现为5种类型:正常型、局灶型、弥漫型、混合型、“椒盐”型。经典的MM病灶多表现为T1WI低信号,T2WI及T2WI抑脂高信号。在病灶检出方面,全脊柱MRI仍是脊柱检查的“金标准”[23]。全身MRI克服了脊柱MRI范围局限的缺点,其灵敏度明显优于全身低剂量CT[24]。对于弥漫型病灶,全身MRI甚至比18F-FDG PET/CT的灵敏度更高。另外,因其与临床指标良好的相关性,脊柱与骨盆MRI检查也已被纳入最新的Durie/Salmon PLUS分期系统[3]。在预后方面,相关研究认为MRI影像学的表现类型与肿瘤负荷、细胞遗传学、分期、骨髓微循环密切相关,弥漫型MM患者总体预后最差,而“椒盐”型预后相对较好[25-26]。Bartel等[27]认为,局灶型MM患者中,中轴骨MRI病灶数>7个的患者PFS明显缩短。Mai等[28]认为高危MRI评分组(中-重度弥漫浸润或者全身MRI局灶型病灶数>25个或者中轴骨MRI病灶数>7个)的中位PFS及OS均明显缩短。常规MRI有其优势,但仍存在一定的局限性:全脊柱MRI扫描范围局限,而部分MM患者脊柱外甚至髓外存在病变;全身MRI图像采集时间长、花费高、临床实用性有待验证,幽闭恐惧症及体内有金属异物者禁忌,且对肋骨、颅骨病灶诊断的灵敏度较差[2];常规MRI检查难以用于MM的疗效评估,Derlin等[6]报道,因为非活性病灶持续存在,常规MRI在疗效评估方面存在较大假阳性率。

  • 3.2.   全身DWI

  • 全身DWI具有灵敏度高、快速、可定量等优点,在肿瘤负荷和疗效评估等方面均具有重要价值。Giles等[29]认为除颅骨外,全身DWI比X射线的诊断灵敏度高,特别是在肋骨病灶检出方面明显优于X射线及常规MRI检查。Pawlyn等[30]研究结果表明,在弥漫型与多灶型病灶上全身DWI比PET/CT的灵敏度高。全身DWI在MM疗效评估方面的应用一直是研究的热点。Horger等[31]发现治疗有反应组病灶的表观扩散系数值较治疗前明显减低,而治疗无反应组病灶的表观扩散系数值较治疗前变化不大。但Lacognata等[32]认为全身DWI更适用于局灶型病灶的疗效评估,对于弥漫型及“椒盐”型病灶,其应用价值不大。尽管全身DWI灵敏度较高,但解剖细节分辨力低,特异度存在争议,仍需结合常规MRI综合分析病灶性质。另外,全身DWI还会受到集落细胞刺激因子的影响,从而产生假阳性结果[33-34]

  • 3.3.   DCE-MRI

  • MM常伴有骨髓微循环的增加,从而表现为更高的骨髓微血管密度。MM患者骨髓微血管密度明显高于冒烟型骨髓瘤患者、意义未定的单克隆丙种球蛋白病患者及正常人。骨髓微循环的增加与MM及冒烟型骨髓瘤患者的不良预后密切相关。局部DCE-MRI是一种反映骨髓微循环的无创检查方法,其主要定量参数包括振幅A(反映微循环容积)和交换率常数Kep(组织间对比剂扩散重新回到血管内的速度常数)[35-36]。Merz等[35]研究结果显示,治疗有效组在治疗前腰椎椎体的A值更低,治疗前后腰椎椎体Kep值降低的更为明显,治疗后Kep值越高OS越短。Merz等[36]认为A值及Kep值不仅可以用于评价患者的预后情况,还与某些脊柱并发症具有相关性,更高的A值常提示低位腰椎新发椎体骨折的可能。Lin等[37]首次将全身DCE-MRI应用于MM,骨髓最大增强百分比和病灶最大增强百分比这两个定量指标可同时用于MM的疗效评估,结果证实通过骨髓最大增强百分比和同步病灶最大增强百分比的定量分析,全身DCE-MRI可以用来评估MM患者的治疗反应。

  • 3.4.   水脂分离技术

  • 近年来,以下研究将水脂分离技术[Dixon或迭代分解水和脂肪的回声不对称与最小二乘法估计技术(iterative decomposition of water and fat with echo asymmetry and least squares estimation,IDEAL)]应用到MM研究中。建立在梯度回波序列上的水脂分离技术能同时获得正相位、反相位、水相、脂相共4组图像,并能定量计算病灶的脂肪信号分数(signal fat fraction,SFF)。有研究结果显示,IDEAL技术能够用于区分症状性与无症状性MM,前者椎体的SFF明显低于后者[38-39]。另有研究者将Dixon技术用于MM的疗效评估,结果显示治疗有反应组患者治疗前后病灶的SFF明显增加,而治疗无反应组患者治疗前后的SFF变化不大,初步证实了Dixon技术在MM的疗效评估中的应用价值[40-41]

4.   PET/MRI
  • PET/MRI是目前最先进的分子影像技术。Sachpekidis等[42]认为PET/MRI与PET/CT对MM局灶型病灶的检测效能相当。Shah等[43]则认为PET/MRI结合了PET与MRI各自的优势,能起到优势互补的作用。MRI对小的骨髓瘤病灶(直径<10 mm)、“椒盐”型及轻度弥漫型病灶的诊断灵敏度更高,PET则能从代谢方面反映病灶活性,两者的完美结合使PET/MRI无论在肿瘤负荷评估还是疗效评估方面均提供了更为精确的信息。目前PET/MRI在MM中的研究甚少,因此,未来需要大样本数据去证实其在MM中的应用价值。

5.   小结与展望
  • 综上所述,18F-FDG PET/CT在MM的诊断、疗效评估、预后及MRD评估等方面均具有一定价值,其主要缺点是对弥漫型病灶的灵敏度低,并且部分病灶在18F-FDG PET/CT上代谢不明显。18F-FDG的这一缺陷未来有望被其他显像剂弥补,如11C-蛋氨酸、11C-乙酸盐、11C-胆碱等。68Ga-Pentixafor还可用于筛选高表达CXCR4的MM患者,从而指导患者的放射免疫治疗。未来迫切需要去研发更有临床应用价值的显像剂。全脊柱MRI是脊柱检查的“金标准”。全身MRI在弥漫型病灶的检测方面更具优势。全身DWI在病灶检出方面,特别是弥漫型病灶及多灶型病灶上具有明显优势,在疗效评估方面也具有一定的价值。DCE-MRI的某些参数与MM的疗效、预后或椎体并发症存在一定相关性。水脂分离技术也可为MM患者疗效评估提供一定的帮助。PET/MRI作为目前最先进的分子影像技术,在肿瘤负荷、疗效评估及预后等方面均被认为具有潜在价值,但其在MM中的研究甚少,因此,未来迫切需要大样本研究去证明其临床应用价值。

Reference (43)



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