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Prostate Specific Membrane Antigen PET/MRI for the Management of Prostate Cancer: Current Status and Future Directions
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摘要: 前列腺癌(prostate cancer, PCa)是常见的老年男性恶性肿瘤，并是其主要致死原因之一。前列腺特异性膜抗原(prostate specific membrane antigen, PSMA)是一种PCa组织特异性高表达的跨膜蛋白，这使得PSMA成为PCa良好的特异性分子影像靶点。目前，PSMA PET/CT在PCa诊断、分期等方面的价值已被广泛认可。随着PET/MRI逐步进入临床，PSMA PET与MRI两种诊断PCa的重要影像学方法的有机结合成为可能。本文就PSMA PET/MRI在PCa中的应用现状与前景进行阐述，以期为临床诊疗提供借鉴。Abstract: Prostate cancer (PCa) is one of the most common malignancies and one major leading cause of mortality from cancers in old men. Due to its specific overexpression in PCa cells, the prostate specific membrane antigen (PSMA) has become an ideal molecular imaging target for PCa.Currently, the value of PSMA PET/CT in the diagnosis and staging of PCa has been widely accepted. With the clinical application of simultaneous PET/MRI, it enables the possibility of combination of PSMA PET and MRI for the management of PCa. Here we present this review on the current status and future direction of the application of PSMA PET/MRI in the management of PCa.
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Keywords:
- prostate cancer /
- prostate specific membrane antigen /
- PET/MRI
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前列腺癌(prostate cancer, PCa)是欧美老年男性最常见的恶性肿瘤，并是其主要致死原因之一[1-2]。2018年全球恶性肿瘤统计报告显示，PCa世标发病率与死亡率分别为29.3/10万和7.6/10万[3]。我国PCa的世标发病率和死亡率分别为6.47/10万和2.65/10万，与欧美发达国家相比，处于相对较低水平[4]。但近年来，随着我国人口老龄化进程加快，PCa诊疗水平提高以及人们生活方式的改变，我国PCa的发病率亦呈明显上升趋势[4-6]。流行病学数据显示，我国PCa发病率平均每年上升约11.5%[6]。PCa已成为国民公共卫生需要重点关注的疾病之一。鉴于PCa生物学行为(惰性、侵袭性、致死性)差异大，因此个体化诊疗至关重要[7]。其中，PCa的精准影像学评估是实现个体化治疗的基石，亦是目前本领域的研究热点之一。多参数MRI(multi-parameter MRI, mpMRI)对PCa的诊断具有重要价值，是目前诊断PCa最常用的影像学方法，但存在特异度较低等局限性[8]。随着对前列腺特异性膜抗原(prostate specific membrane antigen, PSMA)研究的深入，发现PSMA这一跨膜蛋白特异性表达于前列腺上皮细胞，并于PCa组织中高表达，这使得PSMA成为PCa良好的特异性分子影像靶点[9]。目前，PSMA PET/CT在PCa诊断、分期、复发病灶探查等方面的重要价值已被广泛认可[10-12]，其已成为与mpMRI具有重要互补价值的检查手段。基于前期良好的临床试验结果，美国食品药品监督管理局已于2020年12月1日正式批准68Ga-PSMA-11用于PCa的临床诊断。随着PET/MRI技术的成熟以及临床应用的开展，PSMA PET与MRI两种评估PCa的重要影像学方法的有机结合成为可能。2013年Afshar-Oromieh等[13]首次将PSMA PET/MRI应用于PCa的临床评估。PSMA PET/MRI同机采集可一站式获得PSMA PET图像及mpMRI图像，实现结构、功能和分子影像在空间和时间上的最佳配准，提供代谢和功能的综合信息[14]，并在一次检查中充分联合PSMA PET分子影像与MRI高软组织分辨率及多参数成像的优势，为PCa的影像学评估提供更多信息。
1. PSMA PET/MRI的优势
当前，mpMRI凭借良好的软组织分辨率及多参数成像的优势，已成为PCa患者局部分期的首选影像学方式[15]。mpMRI包括T2加权、弥散加权以及动态增强MRI，基于上述序列已形成前列腺影像及报告数据系统(prostate imaging and reporting and data system，PI-RADS)，以便更加客观地评估病灶。随机对照试验结果显示[16-17]，mpMRI可提升临床显著癌的检出率，减少不必要的活检。对于原发性PCa，因研究人群或采集技术不一，mpMRI的诊断灵敏度和特异度差异较大，分别为22%~85%和50%~99%[7]。一项纳入14项研究共1785例患者的Meta分析显示，mpMRI诊断PCa的灵敏度和特异度分别为78%和79%[18]。mpMRI评估前列腺包膜外侵犯(extracap-sular extension, ECE)和精囊腺侵犯(seminal vesicle invasion, SVI)的灵敏度分别为39%和33%，特异度分别为56%和95%[19]。可见，尽管mpMRI诊断PCa已有长足发展，但远非完美。因此，需要探索更多方法或靶点用于评估PCa。
研究显示，超过90%的原发性PCa高表达PSMA[20]，PSMA PET/CT在原发性PCa诊断分期中的高灵敏度、高特异度已被证实。Eiber等[21]发现68Ga-PSMA-11 PET/CT诊断PCa的灵敏度和特异度分别为64%和94%。另有研究报道病灶最大标准摄取值(maximum standardized uptake value，SUVmax) 与其恶性程度呈正相关[22]。此外，Liu等[12]的研究显示，68Ga- PSMA-617 PET / CT的半定量分析指标还可预测PCa的风险分层和转移风险。
PSMA PET/MRI可实现PSMA PET与mpMRI的优势整合，一站式获得PSMA PET和mpMRI图像，为PCa的评估提供更为全面的信息。
2. PSMA PET/MRI在原发性PCa评估中的应用
2.1 局部分期
Eiber等[21]首次报道了68Ga-PSMA-11 PET/MRI可进一步提升对原发性PCa诊断的准确性，该研究纳入53例中高危PCa患者，发现PSMA PET/MRI的病灶检出率明显高于单独PSMA PET或mpMRI(98% 比92% 比66%)，且诊断效能明显升高[曲线下面积(area under the curve, AUC)：0.88比0.83比0.73]，这种提升原因在于PSMA PET较高的特异性以及PSMA PET与mpMRI二者联用敏感性提高。Wang等[23]的Meta分析纳入了6项研究(257例患者，1278个病灶)，结果显示68Ga-PSMA PET/MRI诊断原发性PCa的灵敏度为83%，特异度为81%。此外，PSMA PET/MRI中PSMA PET的高特异性对于mpMRI中PI-RADS 3分这类模棱两可的病变的诊断具有重要价值。Al-Bayati等[24]分析了22例PCa患者的41个病灶，发现mpMRI中模棱两可的病灶的比率(36.6%, 15/41)明显高于PSMA PET(4/41)和PSMA PET/MRI(14.6%，6/41);对于mpMRI模棱两可的病灶，PSMA PET的结果更多倾向于恶性，7个被PSMA PET评为恶性病变的PI-RADS 3分病灶，随后病理学确认均为恶性，可见PSMA PET/MRI能够更好地诊断PI-RADS 3分这类具有挑战性的病变[25]。我国学者Chen等[26]对54例患者的90个病灶进行逐个分析，亦发现PSMA PET/MRI对PI-RADS 3分病灶重分类诊断为临床显著癌具有明显作用(重分类改善指标为66.7%, P＜0.01)。
ECE和SVI会影响PCa临床治疗决策并与复发风险增加相关，因而亦是局部分期中需要重点评估的内容。一项对40例患者的比较研究显示，相较于mpMRI，68Ga-PSMA-11 PET/MRI可显著提高诊断ECE(47%比28%)和SVI(50%比35%)的灵敏度[27]。Grubmüller等[28]的研究显示，68Ga-PSMA-11 PET/MRI诊断ECE的准确度为79%，诊断SVI的准确度为94%。另一方面，PSMA PET/MRI中的mpMRI对于PSMA假阳性或PSMA阴性病灶的诊断具有重要补充价值。约10%的原发性PCa不表达PSMA[21, 29]，因此无法通过PSMA PET检出，这些病灶通常分化较差，可被mpMRI检出。在Domachevsky等[30]的研究中，12个(7.6%)病灶未显示出PSMA摄取，但在mpMRI上被评为PI-RADS≥4分。可见，PSMA PET/MRI可实现对病灶进行精准分期，T分期的准确度可达82.5%[28]。
2.2 淋巴结分期
淋巴结分期方面，当淋巴结出现形态改变(如肿大)时可通过CT或MRI诊断为淋巴结转移(lymph node metastases, LNM)，但CT和MRI诊断性能欠佳，灵敏度仅为13%~40%[31]。而PSMA PET则可根据示踪剂浓聚进而诊断小至2 mm的无明显形态学改变的LNM[32]。Grubmüller等[28]分析了80例进行前列腺癌根治术及淋巴结清扫术的患者，术前PSMA PET/MRI诊断11例(13.8%)患者存在LNM，随后的病理报告显示16例(20%)患者伴LNM，PSMA PET/MRI诊断的阳性淋巴结的中位大小为8 mm，相较于传统CT或MRI，PSMA PET/MRI的诊断灵敏度提高显著(68.8%)，特异度为100%，阳性预测值(positive predictive value, PPV)为100%，阴性预测值(negative predictive value, NPV)为91.7%，诊断准确度达93%。此外，充分联合PSMA PET和mpMRI的定量指标可显著提高PSMA PET/MRI诊断LNM的准确性，研究显示，单独采用SUVmax作为定量指标诊断LNM的灵敏度和特异度分别为77.8%和76.5%，而单独采用表观弥散系数(apparent diffusion coefficient, ADC)诊断LNM的灵敏度和特异度分别为87.5%和76.5%，二者联用可将诊断灵敏度和特异度分别提高至100%和82.4%[33]。
2.3 远处转移分期
远处转移评估方面，鉴于PCa易伴发骨转移，因此对于中高危PCa患者，术前分期常推荐MRI/CT或骨扫描进行骨病灶分期。一项针对126例患者的比较研究显示，PSMA PET诊断骨转移的灵敏度(98.7%~ 100%比86.7%~89.3%)和特异度(88.2%~100%比60.8%~96.1%)明显高于骨扫描(P＜0.001)[34]。另一项研究报道，PSMA PET检出16%(68/420)的患者存在传统影像手段未检出的远处转移灶[35]。在PSMA PET/CT的基础上，PSMA PET/MRI借助mpMRI多序列成像和良好的分辨率优势，可发现早期无骨质密度改变的骨转移病灶，尤其是当骨转移灶仅表现为轻中度PSMA摄取且无骨质密度改变时，PSMA PET/MRI可明显提高对骨转移灶诊断的准确性[36]。
3. PSMA PET/MRI在PCa靶向穿刺引导中的应用
尽管存在着较高的假阴性率，目前欧洲泌尿外科学会指南仍推荐经直肠超声引导下穿刺作为诊断PCa的标准方案。如果超声引导下穿刺阴性，建议行MRI引导下活检，尽管其对PI-RADS 3~5分的病变特异度较低[37]。研究显示，mpMRI引导靶向活检的癌灶检出率为11%~54%[38]。因此，亟需探索更为精准的穿刺活检方法，以减少不必要的活检次数。一项前瞻性研究探索了68Ga-PSMA-11 PET / MRI引导穿刺活检的诊断性能，该研究共入组42例可疑PCa患者，以切片病理作为参考标准，结果在62%的患者中发现了临床显著性PCa，诊断灵敏度可达96%，特异度为81%，PPV为89%，NPV为93%，准确度为90%，可见，PSMA PET/MRI是一种极具前景的引导活检手段[37]。
4. PSMA PET/MRI在复发性PCa评估中的应用
经过有效的局部治疗后仍有约1/3的局限性PCa患者会出现生化复发(biochemical recurrence, BCR)，表现为前列腺特异性抗原(prostate specific antigen, PSA)升高(≥0.2 μg/L)。BCR患者的PSA升高可能是由于局部复发、远处转移或二者兼有[7]。早期准确识别BCR病灶并尽早给予恰当的治疗，可延长患者的生存期[39]。
众所周知，常规影像学手段检测BCR病灶的灵敏度非常差，尤其当PSA＜10 μg/L时[7]。PSMA PET/CT的出现为BCR患者的影像学评估带来了一场突破性的革新。BCR最常见的是淋巴结复发，包括腹盆部淋巴结(50%~55%)、膈上淋巴结(5.2%)，此外还存在骨转移(35.9%)、局部复发(35.1%)和其他器官转移(5.2%，如肺脏)[40]。正如一些研究所报道，PSMA PET对淋巴结的识别比CT或MRI敏感，甚至可以检出短径＜5 mm的LNM[40-41]。Fendler等[10]回顾了635例BCR患者，发现68Ga-PSMA-11 PET/CT共检出475例(75%)患者的BCR病灶，其中87例患者通过病理验证了PSMA PET的诊断，PPV为0.84；217例患者通过临床综合参考标准验证了PSMA PET的诊断，PPV为0.92；且68Ga-PSMA-11 PET/CT对BCR的检出率随PSA升高而显著提高(PSA＜0.5 μg/L：38%，0.5 μg/L≤PSA＜1.0 μg/L：57%，1.0 μg/L≤PSA＜2.0 μg/L：84%，2.0 μg/L≤PSA＜5.0 μg/L：86%，PSA≥5.0 μg/L：97%，P＜0.001)；与此同时，不同阅片者间可保持较高的可重复性。
相较于PSMA PET/CT，PSMA PET/MRI系统具有更高的灵敏性和前列腺床等区域更高的软组织分辨率，对BCR病灶的探查也有所增益，且辐射剂量更低。这种增益一方面表现为在极低PSA水平下检出率的增高[42-44]，另一方面表现为对前列腺床局部复发灶的诊断效能的增加[44-46]。Kranzbühler等[43]重点研究了66例PSA＜0.5 μg/L(中位PSA为0.23 μg/L)的BCR患者，68Ga-PSMA-11 PET/MRI检出了36例(54.5%)患者的病灶，其中0.2 μg/L≤PSA＜0.5 μg/L的检出率为65%，PSA＜0.2 μg/L的检出率为38.5%，高于PSMA PET/CT的病灶检出率[10]。Guberina等[46]分析了93例BCR患者，发现PSMA PET/MRI的灵敏度为98.8%，而PSMA PET/CT的灵敏度为93.2%，且PSMA PET/MRI对局部复发灶的诊断置信度更高(P=0.031)。Wang等[23]的Meta分析总结了7项研究(450例患者)，显示PSMA PET/MRI可准确检测BCR，病灶检出率为76%，对于不同PSA水平(0~0.2 μg/L、0.2~1.0 μg/L、1~2 μg/L、＞2 μg/L) 的检出率依次为38%、67%、74%和95%。
5. PSMA PET/MRI在PCa治疗中的应用
5.1 对治疗决策的影响
mpMRI通过对局部的精准分期已体现出其在指导手术术式选择以及积极监测方面的潜力[47]。PSMA PET/MRI在MRI的基础上联合了PSMA分子影像信息，可为局部和全身分期提供更为全面且精准的信息，并可改变部分患者的临床治疗决策。Abufaraj等[48]的研究发现，PSMA PET/CT(MRI)对BCR患者的LNM具有良好的诊断定位能力，且与病理结果之间的高度相关性为针对性手术干预提供了依据，可避免部分患者盲目进行双侧扩大性淋巴结清扫术。在Fendler等[10]的研究中，31例患者在仅接受PSMA PET引导的局部治疗后即可使PSA下降50%或更多。Grubmüller等[28]采用PSMA PET/MRI对原发性PCa进行术前分期的研究中，28.7%(35/122)的患者由于PSMA PET/MRI所提供的信息进而改变了治疗策略，其中14例(11.5%)患者由于远处LNM及远处转移而接受了化疗，8例(6.5%)患者由于局部T4分期而接受了雄激素剥夺治疗联合放疗，19例(15.6%)患者由于很少的肿瘤负荷而接受了主动监测。
5.2 疗效评估
通常情况下，PCa局部治疗的疗效通过MRI进行评估[49-50]，而系统性治疗则通过CT(尤其是实体瘤反应评估标准)和全身骨扫描进行评估[51-52]。尽管这些方法已被广泛使用，有着良好的可重复性，但仍存在一些局限性，例如，MRI的特异性低，CT对骨病变的灵敏性低等[49, 53]。PSMA PET/CT(MRI)作为一种兼具高灵敏度与特异度的全身检查手段，或将在PCa的疗效评价中起重要作用。Burger等[54]探索了68Ga- PSMA-11 PET/MRI评价高能聚焦超声(high-intensity focused ultrasound，HIFU)治疗局部PCa疗效的价值，HIFU治疗后常对患者进行mpMRI和活检随访疗效，但mpMRI常呈假阴性；该研究发现10例模板活检阳性而mpMRI阴性的患者，PSMA PET/MRI诊断mpMRI阴性复发病灶的灵敏度为55%，特异度为100%，PPV为100%，NPV为85%，提示PSMA PET/MRI可良好地定位HIFU治疗后mpMRI阴性的复发病灶，或可用于评价HIFU的治疗疗效。
6. 小结与展望
PSMA PET为PCa患者影像学评估带来了突破性的革新。PSMA PET/MRI整合了PSMA PET兼具高灵敏性与特异性的核医学分子影像以及MRI精细的解剖图像、良好的软组织分辨率及多参数成像的优势，已在原发性PCa的术前分期、靶向穿刺引导、BCR病灶检出以及治疗决策制订等多个方面发挥出巨大的潜力，对患者的诊疗管理产生了显著影响。随着PET/MRI技术的进步，可能触发PSMA PET/MRI在PCa全程管理方面发挥更大的作用。
作者贡献：李慧负责查阅文献和论文撰写；杨志负责修订和审校论文。利益冲突：所有作者均声明不存在利益冲突 -
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