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前列腺癌(prostate cancer,PCa)是全球男性第二常见的恶性肿瘤,国际癌症研究机构统计结果显示,2020年全球有近140万新发PCa病例和37.5万PCa病死病例[1]。由于医疗水平不断进步和疾病早期筛查的普及,PCa患者的病死率也在不断下降[2]。近年来,随着对前列腺特异性膜抗原(prostate-specific membrane antigen,PSMA)的深入研究,经放射性核素标记后的PSMA应用于PET,其在PCa的分期、指导治疗方案和改善患者预后方面发挥着重要作用。
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PSMA是一种Ⅱ型跨膜糖蛋白,其分为三部分,即胞内区、跨膜区和胞外区,胞外区占PSMA蛋白的95%,是小分子和抗体作用的主要位点。PSMA是叶酸合成代谢过程中至关重要的酶,在PCa发生发展过程中起着重要作用,包括微血管形成、增强PCa的雄激素受体的非依赖性等[3]。Chang等[4]的研究结果显示,在结肠癌、乳腺癌和肾癌等实体肿瘤的新生血管中同样存在PSMA表达。PSMA在唾液腺、肾脏和前列腺等正常组织中的表达水平较低。PSMA高表达提示PCa的发生发展,约90%~95%PCa细胞膜上的PSMA过度表达,且其表达水平随PCa去分化程度、去势抵抗性及转移性病灶的增加而升高[5-6],这种独特的生物学特性使其成为PCa诊疗的理想靶点。
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目前,PSMA PET对原发性PCa局部病灶的高检出率已得到证实。Eiber等[7]的研究结果显示,68Ga-PSMA PET/MRI对原发性PCa的检测效能比多参数磁共振成像(multiparameter magnetic resonance imaging, mpMRI)和68Ga-PSMA-11 PET更高,其在检测盆腔转移性淋巴结方面同样具有更高的灵敏度和特异度。PET的高特异度与MRI的精准定位相结合在很大程度上提高了诊断的准确率,PET/MRI联合应用的诊断准确率明显优于mpMRI,可以为医师提供更有价值的病灶代谢相关信息,有助于进行精准的临床分期[8]。Donato等[9]的一项回顾性研究中,58例未经治疗且高度怀疑PCa的患者接受mpMRI和68Ga-PSMA PET/CT检查,以术后组织病理学检查检测出的88个病灶为标准,68Ga-PSMA PET/CT对Gleason评分最高或体积最大的PCa单双侧和多病灶性病变检出的灵敏度均高于mpMRI,并且68Ga-PSMA PET/CT的病灶检出率高于mpMRI。综上,68Ga-PSMA PET/CT在检测原发性PCa方面具有较高的灵敏度和特异度。尽管目前mpMRI仍是临床医师诊断PCa首选的影像方法,但PSMA PET/MRI体现出更高的灵敏度,对初诊的原发性PCa患者价值更大,未来或可替代mpMRI,PSMA PET显像与mpMRI对PCa局部病灶诊断的准确率有待深入研究[10-14]。
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PCa患者转移性病变的及时检出对疾病分期及治疗方式的选择至关重要。常规影像检查检测转移性淋巴结的灵敏度和特异度较低,术前评估PCa患者转移性淋巴结的效能有限。Herlemann等[15]评估了68Ga-PSMA PET/CT对PCa患者术前N分期的准确率,发现68Ga-PSMA PET诊断转移性淋巴结的灵敏度、特异度、阳性预测值、阴性预测值及N分期的准确率均高于CT,68Ga-PSMA PET在PCa患者淋巴结清扫术前提供了更准确的病灶信息。目前已有多项研究结果显示,PSMA PET/MRI和PSMA PET/CT检出转移性淋巴结的准确率更高,可对PCa术前或生化复发的患者进行更准确的N分期,对临床治疗方案的制定具有指导作用[16-19]。
骨转移为PCa最常见的远处转移,全身骨扫描是确诊骨转移瘤的常用检查方法,且随着18F-NaF PET的深入研究,骨转移的检出率逐渐提高。Hofman等[20]的一项多中心、2组随机试验研究结果显示,与常规显像(包括CT和99Tcm−MDP SPECT全身骨扫描)相比,68Ga-PSMA PET/CT对转移性病变的检出灵敏度和特异度均较高。Uprimny等[21]对比分析了68Ga-PSMA PET/CT和18F-NaF PET/CT对骨转移病灶的检出率,结果显示,18F-NaF PET/CT对骨转移病灶的检出率和SUVmax更高,且其肿瘤/本底比值更高。但由于18F-NaF PET/CT对PCa的特异度较低,不能单独应用于PCa的诊断,二者联合可提高骨转移诊断的准确率[22]。
Karagiannis等[23]研究发现,18F-PSMA PET/CT对局部或转移性疾病的检出改变了约60%患者的放疗计划。 Calais等[24]也发现,行68Ga-PSMA PET/CT后,16.5%~37.0%的患者的放疗范围更加精准。这两项研究的结果都证明了PSMA PET/CT对转移性病变的检出可以指导治疗计划,这表明PSMA PET/CT对PCa患者的初始分期及复发后再分期的准确率更高,可提供更多相关功能和代谢信息,在诊断和治疗中发挥关键作用,可及时调整治疗策略,改善患者预后,目前还需要进一步评估PSMA PET/CT与PCa患者总生存期的关系。
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部分PCa患者初次治疗后仍会出现生化复发,表现为PCa根治术后前列腺特异性抗原(prostate-specific antigen, PSA)水平持续升高。PSA水平升高无法区分局部或全身性疾病复发,其诊断主要依赖影像检查。传统影像检查对复发性PCa的定位具有局限性,特别是对于PSA水平较低的患者[25]。Mingels等[26]回顾性研究18F-PSMA-1007 PET/CT对复发性PCa患者诊断的准确率,结果显示,对于不同水平的PSA患者,18F-PSMA-1007 PET/CT检测生化复发性病灶的灵敏度均较高,总体阳性率为91%,且其诊断局部复发和盆腔淋巴结转移的准确率较高。Beheshti等[27]对135例PSA水平<1 ng/ml的复发性PCa患者行68Ga-PSMA PET/CT多时相动态研究结果显示,结合68Ga-PSMA PET/CT动态和延迟显像,26%的患者能提高病变检出率,这表明多时相显像可以提供更多的信息,有利于早期发现PCa复发,为患者提供挽救性治疗的机会,对PCa的精准治疗具有重要意义。目前复发性PCa病灶的检出仍较困难,PSMA PET/CT在这一方面具有极大的优势,通过分子靶向显像剂与病灶结合可尽早监测疾病进展,使患者生存期得到明显延长,从而改善患者预后[28-29]。
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影像组学可从医学影像图像中提取高通量定量参数并获得对疾病诊断更具意义的数据,进一步探究病变的异质性。PSMA PET与影像组学相结合可精准评估PCa的侵袭性,目前已独立应用于低-中危和高危PCa的鉴别诊断[30-31]。Papp等[32]的研究纳入52例在治疗前行PSMA PET/MRI检查的原发性PCa患者,他们将影像组学特征与机器学习相结合,评估其在鉴别低、高危PCa和预测治疗后生化复发的效能,结果显示,基于机器学习的模型比传统PET参数的诊断准确率更高,这表明在PCa患者术前风险分层和预后预测中,PSMA PET影像组学具有重要的临床意义。Solari等[33]评估了PSMA PET联合mpMRI影像组学对PCa患者术后Gleason评分的预测效能,结果表明,单模态和双模态模型均具有良好的预测效能,预测效能最好的模型为PET+表观扩散系数影像组学,表明PSMA PET和表观扩散系数影像组学具有互补价值。目前,PSMA PET影像组学在原发性PCa诊断中的应用价值已得到证实,其在PCa转移性病变、生化复发的预测和预测预后方面具有一定价值,但相关研究的样本量较少,仍需要更大规模的研究以确定可以应用于临床的标准化方案。
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中国PCa研究协作组推荐PSA水平>10 ng/ml、直肠指检发现前列腺可疑结节及影像检查发现可疑病灶的患者进行前列腺活体组织病理学检查,最常用的方法是经直肠超声引导活体组织病理学检查(transrectal ultrasound-guided biopsy,TRUS-GB)[34]。然而,TRUS-GB会高估惰性PCa并低估侵袭性PCa,PCa患者术前风险分层的准确率<50%[35]。一项荟萃分析结果显示,以组织病理学检查结果为“金标准”,68Ga-PSMA-11 PET/CT在临床可疑PCa患者中首次检出PCa的阴性似然比为0.05,这表明68Ga-PSMA-11 PET/CT显像结果阴性可排除疑似PCa患者,避免不必要的活体组织病理学检查[36]。Zhang等[37]对120例PCa患者进行分组研究,PSMA组阳性患者经臀行靶向活体组织病理学检查(targeted biopsy,TB),结果显示,PSMA PET/CT引导下的TB(简称PSMA-TB)对PCa的检出率明显高于TRUS-GB,且PSMA-TB在低PSA水平(<20.0 ng/ml)患者中的检出率更高,与TRUS-GB组患者相比,PSMA-TB组均未观察到血尿、尿潴留或盆腔感染等并发症。Liu等[38]的前瞻性研究结果也证明,相较于系统活体组织病理学检查,PSMA-TB对PCa的检出率更高。Qiu等[39]比较了mpMRI-TB、PSMA-TB及TRUS-GB对PCa的检出率,结果显示,PSMA-TB对PCa的检出率明显高于TRUS-GB和mpMRI-TB。综上所述,PSMA PET-TB对PCa检查部位的定位更精确,同时还能评估PCa患者的全身情况,其检出率高及不良事件发生率低等优点使其成为一种极具潜力的TB方法。
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晚期PCa患者常用的治疗手段为雄激素剥夺疗法,但其长期使用会导致患者的耐药性增强,治疗效果下降[40]。目前,以PSMA为基础的PCa治疗已经取得较大进展并有望实现PCa的精准治疗。RLT是目前应用较广泛的靶向治疗方法,常用于RLT的放射性核素包括177Lu、131I和90Y等。Sartor等[41]对831例转移性去势抵抗性PCa (metastatic castration-resistant prostate cancer,mCRPC)患者随机分组,结果显示,177Lu-PSMA-617治疗组患者的无进展生存期和总生存期较对照组均显著延长,这表明177Lu-PSMA-617可有效治疗mCRPC。Satapathy等[42]的一项前瞻性研究比较了177Lu-PSMA-617和多西紫杉醇治疗对初诊mCRPC患者的疗效和安全性,PSA水平较基线下降>50%的患者中,分别有60%和40%在177Lu-PSMA-617组和多西紫杉醇组,因此与多西紫杉醇相比,177Lu-PSMA-617的治疗效果更好,安全性更高,且患者生活质量得到明显改善。一项前瞻性Ⅱ期单中心研究使用177Lu-PSMA-617对患者进行治疗,结果显示,57%的患者PSA水平下降>50%,在治疗过程中患者的认知功能、失眠和疼痛等症状均得到改善,这表明177Lu-PSMA-617可能具有抗肿瘤活性[43]。随着对mCRPC患者治疗方法的深入研究,以PSMA为基础的靶向治疗方法得到不断改进,相较于传统治疗手段,177Lu-PSMA-617治疗具有独特优势,但由于mCRPC患者的耐药性,RLT的治疗效果仍未达到预期,需对RLT进行大样本量研究,为mCRPC患者提供有效的治疗方法。
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放射性核素标记的PSMA作为一种特异性较强的分子探针,近年来受到广泛关注,PSMA PET为PCa患者的诊疗带来了新希望。相较于传统的影像检查,PSMA PET在原发性PCa病灶检出、临床分期、生化复发检出及预后评估等方面均有较好的临床价值。PSMA PET联合影像组学作为前沿的影像技术,在PCa的临床应用方面有很广阔的前景,可以通过制定标准模型使其在PCa诊断及预后评估方面更规范化。目前晚期PCa患者的治疗方法有限,基于PSMA的RLT在这一方面有很大的价值和潜力,或许可以寻找更具特异性的靶点进行精准治疗,延长患者生存期或改善患者生活质量,通过PSMA PET预测其治疗效果,实现PCa患者的精准诊疗一体化。相信随着PSMA PET的深入研究,PCa患者的诊疗方案会更加个体化。
利益冲突 所有作者声明无利益冲突
作者贡献声明 刘珊负责综述的撰写;吕哲昊、付鹏负责综述的修改与审阅;赵长久负责综述的审阅与最终版本的修订
前列腺特异性膜抗原PET在前列腺癌诊疗中的研究进展
Research progress of prostate specific membrane antigen PET in prostate cancer diagnosis and treatment
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摘要: 前列腺癌(PCa)是男性最常见的泌尿系统肿瘤。前列腺特异性膜抗原(PSMA)在PCa中的表达具有特异性。放射性核素标记的 PSMA PET在PCa的早期诊断、分期和治疗中具有独特优势。笔者就PSMA PET在PCa诊疗中的最新研究进展进行综述。
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关键词:
- 前列腺肿瘤 /
- 正电子发射断层显像术 /
- 前列腺特异性膜抗原
Abstract: Prostate cancer (PCa) is the most common urinary tumor in men. Prostate specific membrane antigen (PSMA) is specific in PCa expression. Radionuclide labeled PSMA PET has unique advantages in early diagnosis, staging and treatment of PCa. This paper reviews the latest research progress of PSMA PET in the diagnosis and treatment of PCa. -
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