How to differentiate uterine leiomyosarcoma from leiomyoma with imaging
如何通过影像学鉴别子宫平滑肌肉瘤和平滑肌瘤

a Department of Radiology, McGill University Health Centre, 1001 Decarie boulevard, H4A 3J1 Montreal, QC, Canada
一个放射科，麦吉尔大学健康中心，1001 Decarie 大道，H4A 3J1 蒙特利尔，魁北克，加拿大

b Inserm, U1194, Department of Radiology, Montpellier Cancer Institute, University of Montpellier, 34295 Montpellier, France
b Inserm，U1194，放射科，蒙彼利埃癌症研究所，蒙彼利埃大学，法国 34295 蒙彼利埃

c Université de Paris, Descartes-Paris 5, 75006 Paris, France

d Department of Radiology, Hôpital Européen Georges Pompidou, Assistance
d 放射科，欧洲乔治·蓬皮杜医院，援助

Publique-Hôpitaux de Paris, 75015 Paris, France

e Department of Radiology A, Hôpital Cochin, Assistance Publique-Hôpitaux de Paris, 75014 Paris, France

Department of Radiology, Cambridge University Hospitals, NHS Foundation Trust, CB2 OQQ Cambridge, United Kingdom
剑桥大学医院放射科，NHS 基金会信托，CB2 OQQ 剑桥，英国

Leiomyosarcoma; 平滑肌肉瘤;

Leiomyoma; 平滑肌瘤;

Differentiation;

Magnetic resonance imaging (MRI);
磁共振成像（MRI）;

Uterine tumor 子宫肿瘤

MRI features that may allow distinction between leiomyomas and leiomyosarcomas according to the most recent evidence in the literature. The potential contribution of texture analysis is also discussed. In order to help guide-imaging diagnosis, we provide an MRI-based diagnostic algorithm which takes into account morphological and functional features, both individually and in combination, in an attempt to optimize radiologic differentiation of leiomyomas from leiomyosarcomas.
MRI 特征可能根据文献中最新证据区分平滑肌瘤和平滑肌肉瘤。还讨论了纹理分析的潜在贡献。为了帮助指导影像诊断，我们提供了一种基于 MRI 的诊断算法，该算法考虑了形态和功能特征，无论是单独还是组合，试图优化从平滑肌瘤到平滑肌肉瘤的放射学区分。

© 2019 Société française de radiologie. Published by Elsevier Masson SAS. All rights reserved.

Uterine leiomyomas, sometimes incorrectly colloquially referred to as uterine fibroids, are the most frequently encountered benign myomatous tumors of the uterus, being observed in up to of reproductive-age women and of perimenopausal women [1-6]. In addition, these benign tumors may become symptomatic in of patients and subsequently produce pelvic pain, subfertility or abnormal uterine bleeding, requiring gynecologic hospitalization in about of affected women [2].
子宫平滑肌瘤，有时在口头上错误地称为子宫肌瘤，是子宫中最常见的良性肌瘤肿瘤，可在生育年龄妇女中观察到 ，在围绝经期妇女中观察到 [1-6]。此外，这些良性肿瘤可能在 的患者中出现症状，并随后产生盆腔疼痛、生育困难或异常子宫出血，约 的患者需要妇科住院治疗 [2]。

On the malignant spectrum, uterine sarcomas tend to occur in an older patient population when compared to leiomyomas, and only account for of all uterine malig nancies [7]. They often present with the same symptoms as leiomyomas and thus cannot reliably be distinguished clinically [8-10]. Leiomyosarcomas (LMSs) are the most common uterine sarcomas, with an estimated annual incidence of per women, followed by endometrial stromal sarcomas with an annual incidence of /million per women .
在恶性谱中，子宫肉瘤往往发生在年龄较大的患者群体中，与平滑肌瘤相比，仅占所有子宫恶性肿瘤的 [7]。它们通常表现出与平滑肌瘤相同的症状，因此在临床上无法可靠地区分 [8-10]。平滑肌肉瘤（LMSs）是最常见的子宫肉瘤，估计每年发病率为 ，其次是子宫内膜间质肉瘤，每年发病率为 /百万女性 。

Given that leiomyomas may currently be managed with minimally invasive treatment, it is particularly important to distinguish them preoperatively from confounding malignant entities such as LMSs. This is aimed to avoid inadvertent dissemination by laparoscopic morcellation or delaying diagnosis with conservative management such as uterine artery embolization [3,15-17]. The misdiagnosis of a LMS for a benign leiomyoma could result in treatment delays and greater morbidity, given its poor prognosis and high propensity to locally recur and metastasize [3,18-20].
鉴于目前可以通过微创治疗来管理平滑肌瘤，因此在术前将其与混淆的恶性实体如 LMSs 区分开来尤为重要。这旨在避免腹腔镜碎片化手术或延误诊断，采用保守治疗如子宫动脉栓塞术等导致意外传播[3,15-17]。将 LMS 误诊为良性平滑肌瘤可能导致治疗延误和更严重的疾病，因为其预后不良且具有局部复发和转移的高倾向[3,18-20]。

On the basis of the FIGO 2009 classification, up to of LMSs are diagnosed as stage I and only up to are diagnosed as stage IV (Table 1) [21-24]. Therefore, the imaging characteristics of the primary lesion, rather than secondary signs of malignancy, will ultimately help in differential diagnosis and drive treatment stratification. While relatively rare, uterine LMSs carry a poor prognosis even when confined to the uterus, as they are responsible for a quarter of the deaths from uterine malignancies, with 5 -year survival rates ranging from . Additionally, LMSs also have a rate of recurrence, with up to occurring in the lungs and up to in the pelvis [10,19,20,26].
根据 FIGO 2009 分类，高达 的 LMS 被诊断为 I 期，只有高达 的 LMS 被诊断为 IV 期（表 1）[21-24]。因此，原发病灶的影像特征，而不是恶性的继发征象，最终将有助于鉴别诊断并推动治疗分层。虽然相对罕见，子宫 LMS 即使局限于子宫，也带来不良预后，因为它们导致子宫恶性肿瘤死亡的四分之一，5 年生存率范围为 。此外，LMS 还有 的复发率，高达 发生在肺部，高达 发生在盆腔[10,19,20,26]。

Considering this challenging clinical context and recent advances in magnetic resonance imaging (MRI), multiple attempts have been made to define imaging characteristics for the preoperative differentiation of uterine leiomyomas from LMSs. Although certain imaging features such as
考虑到这种具有挑战性的临床背景和磁共振成像（MRI）的最新进展，已经进行了多次尝试来定义用于术前区分子宫平滑肌瘤和 LMS 的成像特征。尽管某些成像特征如
Table 1 FIGO staging for uterine LMS (2009).
表 1 FIGO 分期子宫平滑肌肉瘤（2009 年）。

Adapted from Prat et al. [91].
改编自 Prat 等人[91]。

ill-defined margins, increased signal intensity on T1- and T2-weighted images, hemorrhage, central necrosis, specific diffusion-weighted imaging (DWI) characteristics and texture analysis histogram metrics have shown promising results, the literature still alludes to equivocal levels of consistency and agreement [3,4,21,22,27-34].
边缘不清晰，T1-和 T2 加权图像信号强度增加，出血，中心坏死，特定扩散加权成像（DWI）特征和纹理分析直方图指标显示出有希望的结果，文献仍然提到一致性和协议水平存在模棱两可的情况[3,4,21,22,27-34]。

Through this review, we aim to identify and summarize the main imaging features and their efficacy in differentiating uterine leiomyomas from LMSs. A particular emphasis will be placed on the different MRI characteristics of both entities along with their outputs derived from DWI and texture analysis, recent state of the art advances .
通过这项审查，我们旨在确定和总结子宫平滑肌瘤与 LMS 之间的主要成像特征及其区分效果。我们将特别强调两种实体的不同 MRI 特征以及它们从 DWI 和纹理分析中得出的结果，以及最新的技术进展 。

While differentiating uterine leiomyomas from LMSs on imaging may be challenging, the two neoplasms have separate origins and distinct chromosomal rearrangements, very few of which share enough transcriptional overlap to hypothesize a definite common origin .
尽管在影像学上区分子宫平滑肌瘤和 LMS 可能具有挑战性，但这两种肿瘤具有不同的起源和明显的染色体重排，其中很少有足够的转录重叠来推测明确的共同起源 。

Uterine leiomyomas are benign monoclonal tumors enriched in extracellular matrix, with large amounts of collagen types I-III and disorganized fibril arrangements. They arise from the smooth muscle cells of the myometrium . The precise etiology of these tumors remains unclear, but studies have established that factors such as congenitally elevated estrogen receptors in the myometrium, hormonal changes, response to ischemic injury during menses and intrinsic myometrial abnormalities may play a role in initiating causative genetic mutations [2].
子宫平滑肌瘤是富含细胞外基质的良性单克隆肿瘤，具有大量的胶原类型 I-III 和无序的纤维排列。它们起源于子宫肌层的平滑肌细胞 。这些肿瘤的确切病因尚不清楚，但研究已经确定，子宫肌层中的先天性雌激素受体升高、激素变化、月经期间对缺血损伤的反应以及内在子宫肌层异常可能在引发致病基因突变方面发挥作用[2]。

Uterine LMSs are a member of the uterine sarcoma category, rare malignant tumors of mesenchymal origin [10,20]. LMSs typically arise de novo given their considerable chromosomal differences in comparison to leiomyomas, although malignant transformation of leiomyoma to LMS has been reported [2,35]. Uterine LMSs are diagnosed on histology based on hypercellularity, severe nuclear atypia and high mitotic rate (greater than 15 mitotic figures per 10 high power fields); however, this is not always clear-cut and a differential diagnosis may need to be entertained [10,36-38]. Potential diagnostic challenges arise due to the existence of epithelioid and myxoid LMS. These are rare, but often aggressive variants with mild atypia, low mitotic rate and frequent absence of necrosis [39,40]. In addition, smooth muscle uterine neoplasms can present only select suspicious histologic features without meeting the full histologic diagnostic criteria of a LMS. In these equivocal cases, they are classified as smooth muscle tumors of uncertain malignant potential (STUMP), which are generally thought to have a favorable prognosis [41].
子宫平滑肌肉瘤（LMS）是子宫肉瘤类别的一员，是一种罕见的起源于间叶组织的恶性肿瘤[10,20]。LMS 通常是 de novo 形成的，因为与平滑肌瘤相比，它们在染色体上有明显的差异，尽管有报道称平滑肌瘤恶变为 LMS[2,35]。根据组织学诊断，子宫 LMS 的诊断基于细胞增生、严重的核异型和高有丝分裂率（每 10 个高倍视野大于 15 个有丝分裂图像）；然而，这并不总是明确的，可能需要进行鉴别诊断[10,36-38]。由于上皮样和黏液样 LMS 的存在，可能会出现潜在的诊断挑战。这些类型罕见，但通常具有轻度异型、低有丝分裂率和频繁缺乏坏死[39,40]。此外，平滑肌子宫肿瘤可能仅表现出部分可疑的组织学特征，而不符合 LMS 的完整组织学诊断标准。在这些模棱两可的情况下，它们被分类为具有不确定恶性潜力的平滑肌肿瘤（STUMP），通常被认为具有良好的预后[41]。

Hyperactivation of the PI3K/AKT/mTOR pathway, which controls cell proliferation and survival through regulation of gene transcription and protein synthesis has been thought to play a role in the pathogenesis of LMS, with many of them demonstrating phosphorylation of AKT and mTOR [42,43]. Currently there are very scarce clinical reports on targeted treatments for uterine LMS patients although there have been accounts of promising preclinical responses by acting on the pathway through the combination of mTOR pathway inhibitors with aurora kinase A inhibitors, MDM2 inhibitors or histone deacetylase inhibitors [43].
超活化 PI3K/AKT/mTOR 途径，通过调控基因转录和蛋白质合成控制细胞增殖和存活，被认为在 LMS 的发病机制中起作用，其中许多表现出 AKT 和 mTOR 的磷酸化[42,43]。目前对子宫 LMS 患者的靶向治疗的临床报告非常稀缺，尽管有关通过联合 mTOR 途径抑制剂与极化激酶 A 抑制剂、MDM2 抑制剂或组蛋白去乙酰化酶抑制剂作用于 途径的前临床反应的报道[43]。

While there are currently no reliable clinical markers for LMS diagnosis, recent genetic advances have also confirmed frequent alterations in TP53, RB1, -thalassemia/mental retardation syndrome X-linked (ATRX), and mediator complex subunit 12 (MED12). MED12 in particular, may be helpful for the diagnosis of LMS derived from leiomyoma, which while very rare, tend to have a favorable prognosis [44]. A few overexpressed genes at the primary lesion site (osteocrin, neuroligin 4 X , SLITRK4, TSPAN7) are also being investigated [44].
目前尚无可靠的临床标记用于 LMS 诊断，最近的遗传进展也确认了 TP53、RB1、 -地中海贫血/智力迟钝综合征 X 连锁(ATRX)和介质复合物亚单位 12(MED12)的频繁改变。特别是 MED12 可能有助于从平滑肌瘤衍生的 LMS 的诊断，尽管这种情况非常罕见，但往往有良好的预后[44]。一些在原发病变部位过度表达的基因(骨钙蛋白、神经连接素 4X、SLITRK4、TSPAN7)也正在研究中[44]。

Leiomyomas and LMSs have a very similar clinical presentation, although the mean age at presentation for LMSs (45 years and greater) is usually higher than for leiomyomas (under 45 years). Women with these conditions can present with clinical symptoms such as profuse menstrual bleeding, pelvic discomfort, infertility, increased urinary frequency or incontinence, constipation and dyspareunia [45-47]. Therefore, early distinction of LMS from a benign uterine leiomyoma can prove challenging clinically [24]. While not specific for uterine leiomyomas, cancer antigen 125 (CA125) is elevated in the presence of large ( ) or degenerated subserosal leiomyomas [48,49]. On the other hand, there is no general consensus on the utility of CA125 in the diagnosis of LMS. Juang et al. have found significantly higher preoperative serum CA125 values in patients with LMS than in those with leiomyomas; whereas Menczer at al. found in a series of 17 patients that CA125 was not immunohistochemically expressed in any of their LMS pathologic specimens . This raises the possibility that CA125 may sometimes increase due to nonspecific irritation of epithelial surfaces caused by tumor cells [51].
Leiomyomas 和 LMSs 具有非常相似的临床表现，尽管 LMSs（45 岁及以上）的平均发病年龄通常高于 leiomyomas（45 岁以下）。患有这些疾病的妇女可能出现临床症状，如月经过多出血、盆腔不适、不孕、尿频增多或失禁、便秘和性交疼痛。因此，早期将 LMS 与良性子宫平滑肌瘤区分开在临床上可能具有挑战性。虽然 CA125 对子宫平滑肌瘤不具有特异性，但在存在大型或变性的浆膜下子宫平滑肌瘤时 CA125 升高。另一方面，关于 CA125 在 LMS 诊断中的实用性尚无一致意见。Juang 等发现术前血清 CA125 值在 LMS 患者中显著高于 leiomyomas 患者；而 Menczer 等在一系列 17 名患者中发现 CA125 在他们的 LMS 病理标本中没有免疫组化表达。这引发了 CA125 有时可能由于肿瘤细胞引起上皮表面的非特异性刺激而增加的可能性。

Non-invasive diagnostic imaging has been extensively evaluated to differentiate uterine LMSs from leiomyomas given the important differences in their prognosis and management. Along with standard morphologic imaging tools, including transabdominal ultrasound (TAUS) or transvaginal ultrasound (TVUS), MRI and computed tomography (CT), functional and quantitative techniques, such as diffusion, positron emission tomography/CT (PET/CT) and texture analysis (TA) can also play a role in the initial diagnosis, staging and post treatment evaluation. Moreover, quantitative imaging analysis is now being increasingly used for preoperative prognostic stratification.
非侵入性诊断成像已广泛评估，以区分子宫 LMS 和平滑肌瘤，鉴于它们在预后和治疗方面的重要差异。除了标准形态学成像工具，包括经腹超声（TAUS）或经阴道超声（TVUS）、MRI 和计算机断层扫描（CT）外，功能性和定量技术，如扩散、正电子发射断层扫描/CT（PET/CT）和纹理分析（TA）也可以在初步诊断、分期和治疗后评估中发挥作用。此外，定量成像分析现在越来越多地用于术前预后分层。

Ultrasound is usually the first imaging modality employed for the detection of uterine myometrial pathology. TVUS is generally preferred as it allows for better evaluation of patients with a retroverted uterus, inadequate bladder distension, significant bowel gas or obese patients. TAUS, however, is superior for assessment of large and fundal leiomyomas [52]. Transvaginal grayscale and color Doppler ultrasound remain easily accessible, radiation free and cost effective for assessment and follow-up of benign uterine leiomyomas. On ultrasound, leiomyomas typically appear as well-defined hypoechoic masses, with possible calcifications resulting in acoustic shadowing. However, it has a limited role in the accurate diagnosis of LMS [2,21,31,52]. Ultrasound is inherently limited by a low depth of penetration and inter-operator variability. Moreover, uterine LMSs and leiomyomas can both demonstrate similar heterogeneous echogenicity and central necrosis, especially in cases of atypical benign lesions [2,52,53]. Although not always reliable, increased vascularity on color Doppler ultrasound can sometimes favor malignancy, especially when combined with a large size and degenerative cystic changes. This combination of findings increases the sensitivity to and positive predictive value to [52,54,55]. Additionally, leiomyomas have a statistically significant lower mean arteriolar resistance index [SD]) in comparison to mixed mesodermal tumors ( [SD]), although no significant difference was found when comparing the same variable between leiomyomas and LMSs [53].
超声波通常是用于检测子宫肌瘤病变的首选成像模式。TVUS 通常被优先选择，因为它可以更好地评估子宫后屈、膀胱充盈不足、肠道气体明显或肥胖患者。然而，TAUS 对于大型和宫底子宫肌瘤的评估更为优越。经阴道灰度和彩色多普勒超声仍然是易于获取、无辐射且经济有效的评估和随访良性子宫肌瘤的方法。在超声上，子宫肌瘤通常呈现为界定清晰的低回声肿块，可能出现钙化导致声影。然而，在 LMS 的准确诊断中起到的作用有限。超声受限于穿透深度低和操作者间的可变性。此外，子宫 LMS 和子宫肌瘤都可能表现出类似的异质性回声和中央坏死，特别是在非典型良性病变的情况下。 尽管彩色多普勒超声在某些情况下并不总是可靠，但增加的血管化在某些情况下有利于恶性肿瘤，特别是当结合大尺寸和变性囊性变化时。这些发现的组合增加了对 的敏感性和对 的阳性预测值[52,54,55]。此外，与混合中胚层肿瘤（ [SD]）相比，平滑肌瘤的平均动脉阻力指数 [SD]明显较低，尽管在比较同一变量时，平滑肌瘤和 LMS 之间没有发现显著差异[53]。

Table 2 Standard pelvic MRI protocol for leiomyoma/leiomyosarcoma imaging.
表 2 针对平滑肌瘤/平滑肌肉瘤成像的标准盆腔 MRI 方案。

T1-weighted sequence in the axial plane
在轴面上的 T1 加权序列

T1-weighted fat-saturated sequence in the axial plane
在轴面上的 T1 加权脂肪饱和序列

T2-weighted sequence in the axial plane
在轴面上的 T2 加权序列

T2-weighted sequence in the sagittal plane
T2-weighted 序列在矢状面

T2-weighted sequence in the axial oblique plane
在轴斜面上的 T2 加权序列

DWI (b1000) with corresponding ADC map
DWI（b1000）与相应的 ADC 图

Dynamic contrast-enhanced sequence in plane best depicting the morphology of the lesion
动态增强序列在平面上最能描绘病变的形态

CT plays a limited role in the initial diagnosis and local staging of myometrial lesions. CT is excellent for demonstrating calcifications; they are often found in leiomyomas but may also be present in LMSs [56]. CT can also be useful in the initial evaluation of patients presenting with acute abdominal pain, especially those with torsed subserosal leiomyomas, which can then undergo hemorrhagic necrosis and confound the diagnosis . In women with LMS, CT is primarily used for staging purposes and to exclude distant recurrence post therapy (LMS tends to metastasize to the lungs and liver) [59]. CT is also optimal for visualizing the postoperative pelvic anatomy, allowing for proper evaluation of surgical complications including bowel obstruction or injury, ureteral or bladder injuries and urinary fistulas [60].
CT 在子宫肌层病变的初步诊断和局部分期中起有限作用。CT 在显示钙化方面表现出色；它们通常在平滑肌瘤中发现，但也可能存在于 LMSs 中[56]。CT 在评估急性腹痛患者时也很有用，特别是那些患有扭曲的子宫浆膜下平滑肌瘤的患者，这些病变可能随后发生出血性坏死并使诊断复杂 。对于患有 LMS 的女性，CT 主要用于分期目的，并排除治疗后的远端复发（LMS 倾向于转移至肺部和肝脏）[59]。CT 还是观察术后盆腔解剖学的最佳选择，可允许对手术并发症进行适当评估，包括肠梗阻或损伤、输尿管或膀胱损伤和尿瘘[60]。

Despite equivocal levels of agreement over the diagnostic accuracy of individual features, MRI remains the preferred imaging modality for in-depth evaluation of myomatous uterine tumors and for delineation of local spread of malignant disease .
尽管对于个别特征的诊断准确性存在不一致的看法，MRI 仍然是深入评估子宫肌瘤性肿瘤和恶性疾病局部扩散的首选成像模式 。

According to the European Society of Urogenital Radiology (ESUR) guidelines, MRI of the pelvis should be performed following a period of fasting ( 3 to 6 hours) and with a moderately distended urinary bladder to achieve optimal visualization of the pelvis. The administration of an antiperistaltic agent is also recommended in order to optimize image quality. While specific scheduling according to patient's menstrual cycle is not indicated, clinical information relat ing to the specifics of the patient's menstrual cycle and hormonal status should however be documented. As per the ESUR guidelines, the current standard MRI protocol for the pelvis includes: axial T1-weighted imaging, with fat saturation sequence in the presence of high signal/fat containing lesions; sagittal and axial T2-weighted imaging, with at least two orthogonal oblique planes of the uterus. Diffusionweighted imaging (DWI) and dynamic contrast-enhanced (DCE) imaging should always be included when assessing an indeterminate myometrial mass (Table 2) [63]. Signal intensity characteristics of myometrial lesions on T1-weighted sequences are defined in comparison to the fatty bone marrow in the pubic symphysis, while on T2-weighted sequences they are defined in comparison to the outer myometrium. Finally, signal intensity on DWI is defined in comparison to the endometrium: high signal represents equal or higher signal than the endometrium .
根据欧洲泌尿生殖放射学会（ESUR）的指南，盆腔 MRI 应在禁食（3 至 6 小时）后进行，并且要有适度充盈的膀胱以实现对盆腔的最佳可视化。为了优化图像质量，还建议使用抗蠕动药物。虽然根据患者的月经周期进行具体安排并非必要，但应记录与患者月经周期和激素状态相关的临床信息。根据 ESUR 指南，盆腔的当前标准 MRI 方案包括：轴向 T1 加权成像，存在高信号/脂肪含量病变时应使用脂肪饱和序列；矢状和轴向 T2 加权成像，子宫至少应有两个正交斜面。评估不确定的子宫肌层肿块时，应始终包括扩散加权成像（DWI）和动态增强（DCE）成像（表 2）[63]。 信号强度特征在 T1 加权序列中与耻骨联合处的脂肪骨髓相比定义了子宫肌病变，而在 T2 加权序列中与外部子宫肌相比定义了它们。最后，在 DWI 上的信号强度与子宫内膜相比：高信号代表与子宫内膜相等或更高的信号 。

On MRI, typical uterine leiomyomas present as welldelineated masses of variable size that may be solitary or multifocal, with low signal intensities on T1- and T2weighted images; this is mainly due to their increased proportion of smooth muscle content . They range in size from 10 mm to 20 cm , taking into account that most available imaging techniques cannot accurately help characterize lesions smaller than . Currently, leiomyomas are classified according to the International Federation of Obstetrics and Gynecology (FIGO) classification, mainly based on their location relative to the uterus [5,67]. Leiomyomas generally tend to demonstrate low apparent diffusion coefficient (ADC) values, but in the presence of cystic or myxomatous degeneration, could potentially demonstrate higher ADC values than LMSs [34]. Enhancement characteristics of leiomyomas are variable, with highly cellular leiomyomas often demonstrating marked early contrast enhancement. On the other hand, degenerated leiomyomas tend to show faint or irregular enhancement [64]. As a unifying feature however, nontreated leiomyomas usually lack areas of central contrast non-enhancement (necrosis) [29,64].
在 MRI 上，典型的子宫平滑肌瘤呈现为大小不等的明显分界的肿块，可能是单发或多发，T1-和 T2 加权图像上信号强度低；这主要是由于它们平滑肌含量增加的比例 。它们的大小范围从 10 毫米到 20 厘米，考虑到大多数可用的成像技术无法准确帮助表征小于 的病变。目前，根据国际妇产科联合会（FIGO）分类，平滑肌瘤主要根据其相对于子宫的位置进行分类[5,67]。平滑肌瘤通常倾向于显示低表观扩散系数（ADC）值，但在囊性或黏液样变性存在时，可能显示比 LMS 更高的 ADC 值[34]。平滑肌瘤的增强特征是多变的，高细胞密度的平滑肌瘤通常表现出明显的早期对比增强。另一方面，退变的平滑肌瘤倾向于显示微弱或不规则的增强[64]。然而，作为一个统一特征，未经治疗的平滑肌瘤通常缺乏中心对比度不增强区域（坏死）[29,64]。

By comparison, LMSs usually present as solitary heterogeneous and poorly demarcated masses [34]. While their size can be variable, LMSs have been found to be associated with a worse prognosis [68]. Their appearance on T1-weighted images is variable. They may show low or intermediate signal intensity like leiomyomas, but frequently demonstrate areas of high signal intensity on T1weighted images, corresponding to hemorrhage or necrosis, therefore favouring malignancy [64]. LMSs show intermediate to high signal on T2-weighted images along with low ADC values, ranging from to ; despite partial overlap, reported LMS ADC values can be lower relative to degenerated leiomyomas to [SD] . After intravenous administration of gadolinium-based contrast agents, they tend to enhance early and heterogeneously, often demonstrating non-enhancing areas of central necrosis [9,29].
相比之下，LMSs 通常呈现为孤立的异质性和边界不清晰的肿块[34]。虽然它们的大小可能是可变的，但已发现与较差的预后有关[68]。它们在 T1 加权图像上的出现是多变的。它们可能显示出低或中间信号强度，如平滑肌瘤，但在 T1 加权图像上经常显示出高信号强度的区域，对应于出血或坏死，因此有利于恶性[64]。LMSs 在 T2 加权图像上显示出中等到高信号，以及低 ADC 值，范围从 到 ；尽管部分重叠，报道的 LMS ADC 值相对于退变的平滑肌瘤 到 [SD] 可能较低。经铼基造影剂静脉注射后，它们往往早期和不均匀地增强，通常显示出中心坏死的非增强区域[9,29]。

There can be marked overlap between certain imaging features, notably increased signal intensity on T1-weighted sequences, which can be seen in both leiomyoma and LMS, but due to different etiologies. Areas of high signal in a myometrial lesion on T1-weighted images may be due to intralesional fat, as seen in benign lipoleiomyomas. They might also represent red degeneration, resulting from hemorrhagic infarction in the context of pregnancy or
在某些成像特征之间可能存在明显的重叠，尤其是 T1 加权序列上的信号强度增加，这在子宫肌瘤和 LMS 中都可以看到，但由于不同的病因。在 T1 加权图像上的子宫肌瘤病变区域可能是由于病变内脂肪引起的，就像良性脂肪子宫肌瘤中所见。它们也可能代表红色变性，是由于怀孕或其他情况下的出血梗死所致。

Figure 1. Role of T1-weighted precontrast sequences in differentiating the presence of intralesional fat and hemorrhagic components. a and b: 79-year-old woman with a well-defined rounded intramural lesion in the uterus, heterogeneously hyperintense on T2-weighted imaging (curved arrow, a) and with extensive fat content, as demonstrated by the T1-weighted in-phase (arrows, b) and T1-weighted fat suppressed precontrast images (arrows, c). A typical small intramural leiomyoma with low signal on T2-weighted imaging is also noted on the right (thin arrow, a). Patient underwent hysterectomy with final diagnosis of benign lipoleiomyoma. d and e: 45 -year-old woman with a large leiomyoma in the anterior portion of the uterine body, showing diffuse low signal intensity on T2-weighted imaging (due to its increased proportion of smooth muscle content). It is also characterized by a focal central component demonstrating intermediate signal on T2-weighted imaging and high signal intensity on T1-weighted fat suppressed imaging, in keeping with intralesional hemorrhage or red degeneration (arrows, d and e). A typical intramural leiomyoma with low signal on T2-weighted imaging (arrowhead, d) is also noted posterior to the endometrium (thin white arrow, d).
图 1. T1 加权预对比序列在区分病灶内脂肪和出血成分存在方面的作用。a 和 b：79 岁女性子宫内有一个界定清晰的圆形病变，T2 加权成像呈不均匀高信号（曲线箭头，a），并且具有广泛的脂肪含量，如 T1 加权同相位所示（箭头，b）和 T1 加权抑制脂肪预对比图像（箭头，c）。右侧还注意到一个典型的小子宫内肌瘤，在 T2 加权成像上信号低（细箭头，a）。患者接受子宫切除术，最终诊断为良性脂肪肌瘤。d 和 e：45 岁女性子宫体前部有一个大的平滑肌瘤，T2 加权成像显示弥漫性低信号强度（由于其平滑肌含量增加）。它还具有一个显示 T2 加权成像中间信号和 T1 加权抑制脂肪成像高信号强度的局部中心成分，符合病灶内出血或红变性（箭头，d 和 e）。 典型的宫内平滑肌瘤在 T2 加权成像上显示低信号（箭头，d），也注意到在子宫内膜后方（细白箭头，d）。

Figure 2. A 46-year-old woman with uterine leiomyoma with myxoid degeneration. a-c: 46-year-old woman with history of breast cancer and previous kidney transplant in the right lower quadrant (arrowhead, a). Axial MR images show the presence of a well-defined intramural uterine lesion in the fundus (thin arrows, ), characterized by heterogeneous signal on T2-weighted imaging mixed low/intermediate to high. A few slightly high signal intensity components are noted on the T1-weighted fat suppressed precontrast sequence (thin arrow, b). The lesion also shows tiny scattered areas of non-enhancement ) (white arrows, c). The lesion has remained stable in size over 3 years of follow-up, along with two other dominant uterine leiomyomas (not shown). A lobulated non-enhancing tubular structure with a few internal septations is also noted in the left anterior pelvis, in keeping with a hydrosalpinx (curved arrows, a and c).
图 2. 一名 46 岁的子宫平滑肌瘤患者出现黏液变性。a-c：46 岁女性，有乳腺癌病史，曾在右下腹接受肾移植手术（箭头，a）。轴位 MR 图像显示子宫底部存在一个明确定位的子宫内病变（细箭头， ），在 T2 加权成像上呈现出异质信号，混合低/中等到高信号。在 T1 加权脂肪抑制预对比序列上也可见一些稍高信号强度的成分（细箭头，b）。该病变还显示出微小散在的非增强区域 ）（白色箭头，c）。该病变在 3 年的随访中保持稳定大小，同时还有另外两个主要的子宫平滑肌瘤（未显示）。在左前盆腔还注意到一个有几个内部隔膜的分叶状非增强管状结构，符合输卵管积水（弯曲箭头，a 和 c）。

oral contraceptives, as usually seen in leiomyomas (Fig. 1) . On the other hand, areas of high signal on T1weighted images in LMS are often due to hemorrhage or necrosis [64]. Ideal assessment of signal characteristics on T1-weighted images should therefore be made with fat-saturated T1-weighted images. Additionally, subtracted contrast-enhanced sequences are critical and will differentiate hemorrhage from enhancing tissues in the setting of high signal areas on unenhanced T1-weighted images [64]. On the basis of these findings, high signal intensity involving nearly the entire lesion would favor leiomyoma; in contrast small heterogenous focal/multifocal areas of increased signal intensity on T1-weighted images may be attributable to focal hemorrhage or necrosis in the context of LMS if other aggressive features are associated.
口服避孕药，通常在子宫肌瘤中可见（图 1） 。另一方面，在平滑肌肉瘤的 T1 加权图像上出现高信号区域通常是由于出血或坏死引起的[64]。因此，对 T1 加权图像上信号特征的理想评估应该使用脂肪饱和的 T1 加权图像进行。此外，减去对比增强序列至关重要，可以区分未增强的 T1 加权图像上高信号区域中的出血和增强组织[64]。根据这些发现，涉及几乎整个病变的高信号强度会有利于子宫肌瘤；相反，在 T1 加权图像上出现小的异质性局灶/多灶增强信号区域可能是与 LMS 相关的局灶性出血或坏死，如果存在其他侵袭性特征。

Cellular atypia and high mitotic rates found in LMS cannot be directly assessed on MR imaging. However, the signal intensity on T2-weighted images, which is an imaging biomarker of tissue cellularity, may help in evaluating these tissue features . Based on this principle, tumors with high cellularity (such as uterine LMS) and areas of necrosis would demonstrate increased signal on T2-weighted images. Despite somewhat conflicting opinions in the literature about the usefulness of simple T2 characteristics in the differentiation of LMS from leiomyoma [62], recent reviews have shown a significantly higher signal on T2-weighted images in LMSs in comparison to benign leiomyomas, which generally demonstrate homogenously low signal on T2-weighted images [3]. However, cystic and myxoid degeneration often show high signal on T2-weighted images, similar to large degenerative leiomyoma [71]. This therefore limits the predictive value of these criteria in individual patients (Fig. 2) and review of other MRI features is critical to aid in diagnosis (Fig. 6) [3,64,66].
细胞异型性和 LMS 中发现的高有丝分裂率不能直接在 MR 成像上评估。然而，T2 加权图像上的信号强度，这是组织细胞密度的成像生物标志物，可能有助于评估这些组织特征 。基于这一原则，具有高细胞密度（如子宫 LMS）和坏死区域的肿瘤将在 T2 加权图像上显示增加的信号。尽管文献中关于简单 T2 特征在区分 LMS 和平滑肌瘤中的有些争议意见[62]，但最近的评论显示 LMS 在 T2 加权图像上的信号明显高于良性平滑肌瘤，后者通常在 T2 加权图像上显示均匀低信号[3]。然而，囊性和黏液变性通常在 T2 加权图像上显示高信号，类似于大的变性平滑肌瘤[71]。因此，这限制了这些标准在个体患者中的预测价值（图 2），并且审查其他 MRI 特征对于诊断至关重要（图 6）[3,64,66]。

morphologic sequences, DWI has also been investigated as an adjunct to aid in the imaging diagnosis of LMSs [34]. Along with its visual qualitative analysis, DWI also allows for the quantitative measurement of the ADC values on the corresponding derived maps. These values vary based on the cellular density as a function of the nucleus-tocytoplasm ratio [72,73]. Ordinary leiomyomas demonstrate low signal on DWI because of their corresponding low signal from hyalinized collagen on T2-weighted images, a so-called "T2 blackout effect" [74]. In a retrospective study of 5 LMSs and 51 leiomyomas, Tamai et al. found that all imaged uterine sarcomas demonstrated high signal intensity using high b -value DWI with corresponding decreased ADC value ( ) in comparison to the myometrium. These findings are potentially attributable to the restricted motion of water molecules resulting from the increased cellularity, as typically found in malignant tumors [34]. However, the same study found that LMSs and highly cellular leiomyomas share overlapping values and , respectively) [34]. In the literature, the reported ADC values for LMSs range from [SD] to , while those for ordinary leiomyomas range from to [SD] . Given the potential overlap between ranges, DWI and ADC alone are often not helpful in differentiating cellular leiomyoma from LMS and combination imaging with signal characteristics on T1- and T2-weighted images remains mandatory (Figs. 3 and 6).
形态学序列，DWI 也被研究作为辅助手段，以帮助 LMSs 的成像诊断[34]。除了其视觉定性分析外，DWI 还允许对相应的派生图上的 ADC 值进行定量测量。这些值根据细胞密度而变化，作为核质比的函数[72,73]。普通平滑肌瘤在 DWI 上表现出低信号，因为在 T2 加权图像上由于透明质酸胶原的低信号，产生所谓的“T2 黑化效应”[74]。在一项回顾性研究中，田麻衣等人发现，所有成像的子宫肉瘤在高 b 值 DWI 上表现出高信号强度，相应地 ADC 值减少（ ），与子宫肌层相比。这些发现可能归因于水分子受限运动，这是恶性肿瘤中通常发现的[34]。然而，同一研究发现，LMSs 和高细胞密度的平滑肌瘤共享重叠的 值 和 ，分别）[34]。 在文献中，报告的 LMS 的 ADC 值范围从 [SD] 到 ，而普通平滑肌瘤的 ADC 值范围从 到 [SD] 。鉴于范围之间的潜在重叠，DWI 和 ADC 单独通常无法帮助区分细胞平滑肌瘤和 LMS，必须使用 T1-和 T2 加权图像上的信号特征的组合成像（图 3 和 6）。

To improve diagnostic accuracy and help address overlapping features, several authors have proposed combining multiple MRI features along with potential decision algorithms. Kaganov et al. have shown that there is a statistically significant relationship between increased signal intensity on T1-weighted images and higher risk of LMS [3]. This accordingly may favor a potential decision tree where presence of intralesional areas with high signal intensity on T1-weighted images would lead to subsequent evaluation of signal characteristics on T2-weighted images [3]. Tanaka et al. in a retrospective study of 9 LMSs and 12 leiomyomas reported
为了提高诊断准确性并帮助解决重叠特征，一些作者提出结合多个 MRI 特征以及潜在的决策算法。Kaganov 等人已经表明，在 T1 加权图像上信号强度增加与 LMS 风险增加之间存在统计学显著关系[3]。因此，这可能有利于一个潜在的决策树，其中在 T1 加权图像上存在高信号强度的病灶区域将导致随后对 T2 加权图像信号特征的评估[3]。在一项回顾性研究中，Tanaka 等人报告了 9 例 LMS 和 12 例平滑肌瘤。

Figure 3. DWI and apparent diffusion coefficient (ADC) maps in leiomyosarcomas, typical and degenerated leiomyomas. a-c: 70-year-old woman with a malignant leiomyosarcoma in the uterine fundus (curved arrows, ). The leiomyosarcoma demonstrates intermediate signal intensity on T2 -weighted imaging, with eccentric necrotic changes (thin arrow, a) and high signal intensity on diffusion-weighted imaging (b). The corresponding calculated apparent diffusion coefficient value is (c). There are also several benign leiomyomas showing low signal on T2-weighted imaging (white arrows, a-c) and on diffusion-weighted imaging (b), with a corresponding ADC value of (c). d-f: 67 year-old woman with a large intramural mass in the posterior uterine body. It shows heterogeneous low signal intensity (curved arrow, d) on T2-weighted imaging in comparison to the outer myometrium (arrow, d ) and no restriction on diffusionweighted imaging (arrowhead, e), which is defined in comparison to the intermediate signal intensity of the adjacent endometrium (thin arrow, e). The corresponding apparent diffusion coefficient value is (f). The patient underwent a total hysterectomy with a final diagnosis of markedly vascular atypical leiomyoma, characterized by extensive hyalinization and recent focal infarction secondary to thrombosis.
图 3. 长度加权成像（DWI）和表观扩散系数（ADC）图在平滑肌肉瘤、典型和变性平滑肌瘤中。a-c：70 岁女性子宫底部恶性平滑肌肉瘤（弯箭头， ）示中等信号强度的 T2 加权成像，伴有偏心性坏死变化（细箭头，a）和高信号强度的 扩散加权成像（b）。相应计算的表观扩散系数值为 （c）。还有几个良性平滑肌瘤在 T2 加权成像上显示低信号（白箭头，a-c）和扩散加权成像上显示低信号（b），相应的 ADC 值为 （c）。d-f：67 岁女性后子宫体内有一个大的肌壁内肿块。与外部子宫肌层（箭头，d）相比，在 T2 加权成像上显示不均匀的低信号强度（弯箭头，d），在 扩散加权成像上没有限制（箭头，e），这是相对于相邻子宫内膜的中等信号强度（细箭头，e）定义的。相应的表观扩散系数值为 （f）。 患者接受了全子宫切除术，最终诊断为明显血管型非典型平滑肌瘤，其特点是广泛的透明质化和最近的局部梗死，继发于血栓形成。

Figure 4. Leiomyosarcoma necrosis and non-enhancement. A 72-year-old woman with multiple leiomyomas and a large mass in the lower ventral uterine segment. The lesion shows internal hemorrhage and necrosis, corresponding to non-enhancing areas with high signal intensity on both T1- and T2-weighted imaging (large arrows, ). The dominant solid components show intermediate signal on T2-weighted imaging and high signal intensity on diffusion-weighted imaging ( ), which correlate to a high level of cellularity; these components also avidly enhance after gadolinium-chelate injection (curved arrows, ). There is an abrupt transitional zone between viable/enhancing cells and areas of necrosis, typical of leiomyosarcoma (thin arrows, c). The mass is confined to the uterus.
图 4.平滑肌肉瘤坏死和非增强。一名 72 岁的女性患有多发性平滑肌瘤和下腹子宫段的大肿块。病变显示内部出血和坏死，对应于 T1-和 T2 加权成像上信号强度高的非增强区域（大箭头， ）。主要的实质成分在 T2 加权成像上显示中等信号，扩散加权成像上显示高信号强度（ ），这与高细胞密度相关；这些成分在注射钆螯合物后也显示强烈增强（弯曲箭头， ）。在活跃/增强细胞和坏死区域之间存在明显的过渡区，这是平滑肌肉瘤的典型特征（细箭头，c）。肿块局限于子宫内部。

that the combination of the three following imaging features achieved a sensitivity in diagnosing LMSs and STUMPs:
三种影像特征的组合在诊断 LMSs 和 STUMPs 时达到了 的敏感度：

Given the very low prevalence of these tumors and therefore inherently high negative predictive value (NPV), specificity is much less important than sensitivity in this particular clinical context. Cornfeld et al., in a study that evaluated 4 LMSs and 17 leiomyomas, were only able to achieve a sensitivity applying these criteria [62]. They reported instead that the presence of ill-defined margins achieved a sensitivity and specificity of and , respectively [62]. Additionally, they also noted that reader gestalt showed sensitivities ranging from to , with a specificity [62]. Given that the readers in their study had extensive pelvic MRI interpretation experience ( 10 and 20 years, respectively), this may indicate that these results cannot be reliably reproduced for less subspecialized readers [62].
鉴于这些肿瘤的患病率非常低，因此固有的高阴性预测值（NPV），在这种特定的临床背景下，特异性远不及敏感性重要得多。Cornfeld 等人在一项评估 4 个 LMS 和 17 个平滑肌瘤的研究中，仅能够在应用这些标准时实现 的敏感性[62]。他们反而报告称，存在不明确边缘的情况实现了 和 的敏感性和特异性，分别[62]。此外，他们还指出，读者的整体印象显示敏感性范围从 到 ，特异性为 [62]。考虑到他们研究中的读者具有丰富的盆腔 MRI 解释经验（分别为 10 年和 20 年），这可能表明这些结果对于较少专业化的读者来说无法可靠地再现[62]。
While rapid growth, usually defined as an increase in size of the uterus by 6 gestational weeks over 1 year, has been thought to favor a LMS over a leiomyoma, this is not a reliable finding. Parker at al. have shown in a retrospective study of 371 patients that only of women operated for "rapidly growing" leiomyomas had a final diagnosis of uterine LMS . Thomassin-Naggara et al. developed a multivariate model combining ADC values, signal intensity and characteristics on T2-weighted images to reach an overall accuracy of , for the diagnosis of uterine sarcomas. Their retrospective study was not restricted to LMSs and included 25 malignant mesenchymal uterine tumors and 26 leiomyomas [21]. Their model takes into account the benign fibrous component of ordinary leiomyomas by using their corresponding low signal intensity on T2-weighted images. This is done in combination with the ability of high signal intensity on and corresponding low ADC values to demonstrate high cellularity, thus improving the ability to differentiate malignant tumors from equivocal benign but highly cellular leiomyomas.
尽管快速增长通常被定义为子宫在 1 年内增加 6 个妊娠周的大小，被认为有利于 LMS 而不是平滑肌瘤，但这并不是一个可靠的发现。Parker 等人在对 371 名患者进行的回顾性研究中表明，只有 接受手术治疗的“快速增长”平滑肌瘤的女性最终被诊断为子宫 LMS 。Thomassin-Naggara 等人开发了一个多变量模型，结合 ADC 值、 信号强度和 T2 加权图像上的特征，达到了 的总体准确度，用于诊断子宫肉瘤。他们的回顾性研究并不局限于 LMS，还包括 25 例恶性子宫间叶肿瘤和 26 例平滑肌瘤[21]。他们的模型考虑了普通平滑肌瘤的良性纤维成分，通过使用其在 T2 加权图像上对应的低信号强度来实现。这与高信号强度的能力以及对应的低 ADC 值结合使用，以展示高细胞密度，从而提高了区分恶性肿瘤和模糊的良性但高细胞密度的平滑肌瘤的能力。

More recently, a prospective study of 6 LMSs and 25 leiomyomas showed that the presence of hyperintensity on long -value DWI alone did not improve the differentiation
最近，一项对 6 个 LMS 和 25 个平滑肌瘤的前瞻性研究显示，仅长 值 DWI 上的高信号强度并未改善区分

Figure 5. Necrosis, hemorrhage and solid components of a malignant leiomyosarcoma. A 51-year-old woman with a large uterine mass discovered during an ultrasound (a) performed for excessive vaginal bleeding. Doppler ultrasound shows increased vascularity within the mass (thin arrow, a). Multiparametric MRI (b-d) reveals a single heterogeneous intramural uterine mass with nodular borders. It shows solid, mainly peripheral, enhancing components with areas of tongue-like projections within the right anterior edges of the adjacent myometrium (arrows, b and d). The mass is also characterized by extensive necrotic changes (intermediate/high signal on T2-weighted imaging, low signal on T1-weighted imaging; arrowheads, b and c ) and hemorrhagic components (low signal on T2- and intermediate/high signal on T1-weighted images; curved arrows, b and c). Both the necrotic changes and hemorrhagic components correspond to a central large non-enhancing area within the lesion (arrowhead, d). Biopsy confirmed a leiomyosarcoma of the uterus; at the time of diagnosis, the patient also had multiple liver, renal, lung and spinal metastatic lesions (not shown).
图 5. 恶性平滑肌肉瘤的坏死、出血和实质成分。一名 51 岁的女性在进行超声检查（a）时发现子宫内有一个巨大的肿块，这是因为阴道过度出血。多普勒超声显示肿块内血管增多（细箭头，a）。多参数 MRI（b-d）显示一个单一的异质性子宫内肌肉瘤，有结节状边界。它显示实质性的、主要是周边的增强成分，以及在相邻子宫壁右前缘的舌状突起区域（箭头，b 和 d）内的区域。肿块还表现出广泛的坏死变化（T2 加权成像中的中等/高信号，T1 加权成像中的低信号；箭头，b 和 c）和出血成分（T2 加权成像中的低信号，T1 加权成像中的中等/高信号；弯曲箭头，b 和 c）。坏死变化和出血成分都对应于病变内的一个中央大的非增强区域（箭头，d）。活检证实了子宫平滑肌肉瘤；在诊断时，患者还有多发性肝脏、肾脏、肺部和脊柱转移病灶（未显示）。

between LMSs and benign leiomyomas, only reaching an accuracy and specificity [29]. This study showed that adding an ADC cut-off value determined by posthoc analysis increased the overall accuracy of DWI to [29]. However, the recommended ADC cut-off value for differentiating LMSs from leiomyomas varies between studies depending on whether signal intensities are included in the proposed models [21,33]. In the same study, the addition of contrast-enhanced MRI sequences further improved the diagnostic accuracy to , with a sensitivity of and a specificity of . Also, the addition of contrastenhanced sequences improved reader agreement ( ) in comparison to DWI alone ( ) [29]. The underlying principle behind the usefulness of contrast-enhanced MRI lies in the abrupt transitional zone from viable cells to necrotic cells lacking hyalinized tissue, termed coagulative necrosis (Figs. 4 and 5) [61,76]. Coagulative necrosis, frequently noted in LMSs, presents as an area of central nonenhancement on MRI, as opposed to the scattered areas of non-enhancement that may be encountered in leiomyomas with degeneration due to their inherent interlacing pattern of viable and degenerative cells (Fig. 2) [29]. While a useful predictor of malignancy, the presence of non-enhancing central areas observed on post-contrast images is not infallible and may also be seen in benign leiomyomas with extensive vascular infarction [29,62]. Lakhman et al. have also confirmed the value of a multivariate model for the diagnosis of LMS by combining three or more of the following imaging features: nodular borders, hemorrhage, "T2 dark" signal areas and lack of central enhancement, achieving a sensitivity and specificity of and , respectively [4].
在 LMSs 和良性平滑肌瘤之间，仅达到 准确度和 特异性[29]。这项研究表明，通过后续分析确定的 ADC 截止值 的添加提高了 DWI 的整体准确性至 [29]。然而，根据提出的模型是否包含 信号强度，不同研究对区分 LMSs 和平滑肌瘤的推荐 ADC 截止值有所不同[21,33]。在同一研究中，增加对比增强 MRI 序列进一步提高了诊断准确性至 ，敏感性为 ，特异性为 。此外，与仅 DWI 相比，增加对比增强序列提高了读者一致性（ ）[29]。对比增强 MRI 有用性的基本原理在于从有活力的细胞到缺乏透明组织的坏死细胞之间的突然过渡区，称为凝固性坏死（图 4 和 5）[61,76]。 凝固性坏死，在 LMS 中经常出现，MRI 上呈现为中央非增强区域，与平滑肌瘤由于其固有的活细胞和变性细胞交织模式而可能遇到的散在非增强区域形成对比（图 2）[29]。虽然是恶性的有用预测因素，但在增强后的图像上观察到的非增强中央区域并非绝对可靠，也可能出现在具有广泛血管梗死的良性平滑肌瘤中[29,62]。Lakhman 等人还证实了通过结合以下三个或更多的影像特征进行 LMS 诊断的多元模型的价值：结节状边界、出血、“T2 暗”信号区域和缺乏中央增强，分别实现了 和 的敏感性和特异性[4]。

In the wake of recent computer advancements, TA has also been investigated as an adjunct for the diagnosis of LMS on MRI. TA allows computerized conversion of local variations in image pixel intensities into quantifiable outputs [4]. While TA has been frequently investigated in the diagnosis
在最近的计算机进步之后，TA 也被研究作为 MRI 上 LMS 诊断的辅助手段。TA 允许将图像像素强度的局部变化计算机转换为可量化的输出[4]。虽然 TA 在诊断中经常被调查

Table 3 Summary of landmark MRI studies.
表 3 里程碑 MRI 研究总结。

LMS: leiomyosarcoma; T1WI: T1-weighted images; T2WI: T2-weighted images.
LMS: leiomyosarcoma; T1WI: T1 加权图像; T2WI: T2 加权图像.

of prostate, head and neck and ovarian cancer, very few studies have assessed its usefulness in the diagnosis of LMS [30,77,78]. Lakhman et al. have shown in a retrospective study of 41 patients, that 16/21 extracted texture features were significantly different between 19 LMSs and 22 atypical leiomyomas. In particular, LMSs demonstrated greater overall textural heterogeneity suggested by higher intensity image-based and Gabor edge image-based contrast, lower energy, lower kurtosis and higher standard deviation [4]. It is important to note that the combination of both intensitybased and Gabor edge image-based texture features yielded higher accuracy (75%) in comparison to Gabor edge imagebased features alone (58%) [4]. As a proof of concept, Lakhman et al. only applied TA to T2-weighted images and did not fully assess its value independently from conventionally established MRI features reported in the literature [4,22]. More recently, Gerges et al. have also investigated the utility of TA for the diagnosis of LMS on multiple MRI sequences in a retrospective study with 17 LMSs and 51 leiomyomas [22]. They determined that histogram metrics from TA were most useful on T2-weighted images and least helpful on ADC maps, with the most useful metric derived from the actual signal intensity rather than the metrics of lesion texture [22]. More specifically T2 histogram means below the 50 th percentile achieved an area under the curve (AUC) of up to 0.875 . These results reflect the ability of the metrics to accurately identify lesion subregions with very low signal on T2-weighted images, which is a characteristic that strongly favors a leiomyoma given their higher smooth muscle content versus LMS [22]. Additionally, to confirm what has been previously reported [4,21], Gerges et al. have reiterated that patient age over 44 years, whether as an independent variable or combined with a multivariable model, strongly favored the diagnosis of a LMS [22].
前列腺、头颈和卵巢癌中，很少有研究评估了其在 LMS 诊断中的有用性[30,77,78]。Lakhman 等人在一项回顾性研究中表明，41 名患者中有 16/21 个提取的纹理特征在 19 个 LMS 和 22 个非典型平滑肌瘤之间存在显著差异。特别是，LMS 表现出更大的整体纹理异质性，表现为更高的强度图像和 Gabor 边缘图像对比度，更低的能量，更低的峰度和更高的标准偏差[4]。值得注意的是，基于强度和 Gabor 边缘图像的纹理特征的组合相对于仅使用 Gabor 边缘图像特征（58%）具有更高的准确性（75%）[4]。作为概念验证，Lakhman 等人仅将 TA 应用于 T2 加权图像，并未完全独立评估其价值，而是依赖于文献中报道的传统 MRI 特征[4,22]。最近，Gerges 等人还在一项回顾性研究中调查了 TA 在多个 MRI 序列中用于 LMS 诊断的效用，该研究涉及 17 个 LMS 和 51 个平滑肌瘤[22]。 他们确定了来自 TA 的直方图度量在 T2 加权图像上最有用，在 ADC 图上最无助，最有用的度量来自实际信号强度而不是病变纹理的度量[22]。更具体地说，T2 直方图意味着在 50th 百分位以下的度量达到了高达 0.875 的曲线下面积（AUC）。这些结果反映了这些度量的能力，能够准确识别 T2 加权图像上信号非常低的病变亚区，这是一种非常有利于平滑肌瘤的特征，因为与 LMS 相比，平滑肌瘤具有更高的平滑肌含量[22]。此外，为了确认之前报道的内容[4,21]，Gerges 等人重申，44 岁以上的患者年龄，无论是作为独立变量还是与多变量模型结合，都非常有利于诊断为 LMS[22]。

While the current literature has attempted to clarify the ability of MRI to differentiate LMSs from leiomyomas, most
尽管当前文献已经试图澄清 MRI 区分 LMSs 和平滑肌瘤的能力，但大多数

Table 4 Summary of the main MRI and PET/CT characteristics favoring either leiomyoma or leiomyosarcoma.
表 4 主要 MRI 和 PET/CT 特征总结，有利于子宫肌瘤或平滑肌肉瘤。

T1WI: T1-weighted images; T2WI: T2-weighted images.
T1WI：T1 加权图像；T2WI：T2 加权图像。

studies consist of case reports and retrospective studies, with very few prospective analyses [29]. Another unavoidable limitation common to the literature is undoubtedly the rarity of LMS, which inherently limits the sample size, statistical power and external validity of these findings (Table 3) [62].
研究包括病例报告和回顾性研究，很少有前瞻性分析[29]。文献中另一个不可避免的限制无疑是 LMS 的罕见性，这从根本上限制了样本量、统计能力和这些发现的外部有效性（表 3）[62]。

To summarize, for accurate diagnosis of LMS, the evidence in the current MRI literature seems to favor ill-defined margins, high DWI on b1000 images and low ADC signal along with lack of central contrast enhancement (Table 4) . The presence of corresponding high signal intensity on both T1- and T2-weighted imaging can also favour the diagnosis of LMS through the use of a systematic decision tree [3]. While relatively new in the evaluation of LMS, texture analysis has also shown promising initial results by noting increased texture heterogeneity and low percentile histogram means on T2-weighted sequences for LMS (Table 4) [4,22]. Because the integration of individual imaging features can often prove difficult in the differentiation of LMS from leiomyoma, we have attempted to provide a diagnostic flowchart to help direct radiologists based on the presence of selected salient MRI features (Fig. 6).
总结一下，对于 LMS 的准确诊断，当前 MRI 文献中的证据似乎更倾向于不明确的边缘、b1000 图像上的高 DWI 和低 ADC 信号以及缺乏中央对比增强（表 4） 。在 T1-和 T2 加权成像上出现相应的高信号强度也有助于通过系统决策树支持 LMS 的诊断[3]。虽然在 LMS 评估中相对较新，但纹理分析也显示出有希望的初步结果，通过注意 T2 加权序列上的纹理异质性增加和低百分位直方图均值来支持 LMS 的诊断（表 4）[4,22]。由于个体成像特征的整合通常在区分 LMS 和平滑肌瘤时很难，我们尝试提供一个诊断流程图，以帮助基于选择的显著 MRI 特征的存在来指导放射科医师（图 6）。

While CT alone is not particularly helpful for the differentiation of leiomyomas from LMSs, it has shown utility in combination with 18 F-Fludeoxyglucose (18F-FDG)-PET in the context of indeterminate myometrial lesions on MRI . It is thought that malignant tumors experience upregulation of glucose transporter genes (GLUTs) either due to increase of normal cellular enzymes or synthesis of new transporters after transformation due to oncogenes [81,82]. Based on this hypothesis, greater 18F-FDG uptake of LMS would be expected in comparison to leiomyomas due to their increased metabolic rate and glycolysis. There are few studies on this specific topic, however a study by Umesaki et al. has shown sensitivity of 18 F -FDG PET in the diagnosis of uterine sarcoma vs. leiomyoma with a positive standardized uptake value (SUV) cut-off value of 2.5 [83]. The mean standardized uptake value (SUV) of sarcomas was (SD), with LMS demonstrating elevated SUV values between 3 and 4 [83]. However, only five patients had uterine sarcoma, with only 3 of them having LMS. While 18 F -FDG uptake in leiomyoma is generally low with reported of up to (SD), Chura et al. have
尽管 CT 单独对于鉴别平滑肌瘤和 LMS 并不特别有帮助，但在 MRI 中介于不确定的子宫肌层病变的情况下，结合 18 F-氟脱氧葡萄糖（18F-FDG）PET 显示出一定的实用性 。人们认为，恶性肿瘤经历了葡萄糖转运蛋白基因（GLUTs）的上调，要么是由于正常细胞酶的增加，要么是由于癌基因转化后合成新的转运蛋白[81,82]。基于这一假设，由于其代谢率和糖酵解增加，预计 LMS 的 18F-FDG 摄取量将比平滑肌瘤更高。然而，关于这个具体主题的研究很少，但梅崎等人的一项研究显示了 18 F -FDG PET 在诊断子宫肉瘤与平滑肌瘤时的敏感性 ，其阳性标准摄取值（SUV）截断值为 2.5 [83]。肉瘤的平均标准摄取值（SUV）为 （SD），LMS 显示出 3 至 4 之间的升高 SUV 值[83]。然而，只有五名患者患有子宫肉瘤，其中只有 3 名患有 LMS。尽管平滑肌瘤的 18 F -FDG 摄取通常较低，报道的 最高可达 （SD），Chura 等人已经

Figure 6. Diagnostic algorithm for MRI differentiation of uterine leiomyomas and leiomyosarcomas. The signal intensity of the endometrium is generally the standard of reference against which the diffusion-weighted imaging (DWI) signal intensity (low/intermediate/high) of a uterine lesion is defined. For T2-weighted sequences, the lesion is generally considered hyperintense in comparison to the signal intensity of the outer myometrium. The presence or absence of any extrauterine disease/mass refers to what is covered by the field of view of the pelvic MRI. (ADC: apparent diffusion coefficient; SI: signal intensity).
图 6. MRI 鉴别子宫平滑肌瘤和平滑肌肉瘤的诊断算法。子宫内膜的信号强度通常是扩散加权成像（DWI）信号强度（低/中/高）的参考标准，用于定义子宫病变的信号强度。对于 T2 加权序列，病变通常被认为是高信号强度，与外部子宫肌的信号强度相比。任何子宫外疾病/肿块的存在或缺失指的是盆腔 MRI 视野范围内的内容。（ADC：表观扩散系数；SI：信号强度）。

Figure 7. 18F-FDG PET/CT images and SUV values of a benign leiomyoma and leiomyosarcoma. A 44-year-old woman with malignant phyllodes breast tumor. On the staging PET scan, abnormal FDG uptake was found (SUV 5.4) in a small, exophytic lesion in the uterine fundus (curved arrows, a and b); a partially calcified lesion without any uptake is also noted within the posterior aspect of the uterus (thin arrows a and b ). A dedicated pelvic MRI showed a bulky uterus with multiple leiomyomas, one of which demonstrated typical low signal intensity on T2-weighted imaging (thin arrow, c), corresponding to the partially calcified lesion observed on the 18F-FDG PET/CT scan. A small anterior fundal subserosal exophytic leiomyoma, demonstrating homogeneous post-contrast enhancement and typical low signal intensity on T2-weighted imaging, is also noted and corresponds to the source of radiotracer uptake on PET scan (curved arrows, c and d). The lesion has remained stable on imaging over a period of 4 years, confirming its benign nature.
图 7. 良性平滑肌瘤和平滑肌肉瘤的 18F-FDG PET/CT 图像和 SUV 值。一名 44 岁的患有恶性叶状乳腺肿瘤的女性。在分期 PET 扫描中，发现子宫底部的一个小的外生性病变存在异常的 FDG 摄取（SUV 5.4）（弯箭头，a 和 b）；子宫后方也注意到一个部分钙化的病变没有任何摄取（细箭头 a 和 b）。专用盆腔 MRI 显示子宫肿大伴有多发性平滑肌瘤，其中一枚在 T2 加权成像上显示典型低信号强度（细箭头，c），与 18F-FDG PET/CT 扫描上观察到的部分钙化病变相对应。一个小的前底子宫外生性平滑肌瘤，显示均匀的造影增强和 T2 加权成像上的典型低信号强度，也被注意到，并与 PET 扫描上的放射性示踪剂摄取源相对应（弯箭头，c 和 d）。该病变在 4 年的时间内保持稳定，证实其良性性质。
noted that it can sometimes be elevated in cases of cellular leiomyomas (SUV =9.3) or even in ordinary leiomyomas , if they happen to be particularly vascular, thus leading to false-positive diagnoses (Fig. 7) [84,85]. Overall, no uptake on FDG PET will help out rule out a LMS, but a positive result is not as helpful since it is not necessarily diagnostic for LMS. More recently, Kusonoki et al. have reported that a cut-off SUVmax value was able to exclude leiomyoma with an sensitivity and a specificity ( uterine sarcomas and 19 leiomyomas), thus decreasing the false-positive rate [79]. Additionally, 3'-deoxy-3'-[18 F -flurothymidine ( 18 F -FLT) has also been investigated as an alternative radiotracer in the differentiation of uterine sarcomas from benign leiomyomas, showing better performance in comparison to 18F-FDG in terms of specificity ( 90 vs. ), PPV ( 83.9 vs. ) and accuracy ( 93.3 vs. 80%) [86]. While the number of patients was low with three LMSs and 10 leiomyomas, 18 F -FLT-PET specifically showed low uptake in a leiomyoma that had high uptake on PET, therefore this could potentially be used as a confirmatory adjunct in doubtful lesions [86].
注意到在细胞平滑肌瘤（SUV =9.3）的情况下，代谢活性有时会升高，甚至在普通平滑肌瘤 中，如果它们碰巧特别血管化，从而导致假阳性诊断（图 7）[84,85]。总体而言，FDG PET 上没有摄取将有助于排除 LMS，但阳性结果并不那么有帮助，因为它并不一定是 LMS 的诊断标准。最近，Kusonoki 等人报告说，一个 SUVmax 值的截止值 能够排除具有 敏感性和 特异性的平滑肌瘤（ 子宫肉瘤和 19 个平滑肌瘤），从而降低假阳性率[79]。此外，3'-脱氧-3'-[18 F -氟胸苷（18 F -FLT）也已被研究作为子宫肉瘤与良性平滑肌瘤的区分的替代放射性示踪剂，显示出比 18F-FDG 更好的性能，特异性（90 vs. ），PPV（83.9 vs. ）和准确性（93.3 vs. 80%）[86]。 尽管 3 个 LMS 和 10 个平滑肌瘤患者数量较少，但 18F-FLT-PET 显示了一个在 PET 上摄取高的平滑肌瘤在这方面的摄取量较低，因此这可能作为怀疑病变的确认性辅助手段[86]。

In terms of initial staging, 18F-FDG PET/CT has shown excellent performance with a sensitivity, specificity and accuracy reaching up to 80,100 and , respectively. [87] PET/CT is particularly helpful for detecting peritoneal metastases camouflaged between bowel loops, given its ability to outline their increased metabolic activity in comparison to CT alone, and for detecting distant metastasis (sensitivity up to in some studies) . However, PET/CT appears somewhat limited for local pelvic and para-aortic lymph node staging, with a sensitivity of only , although the number of studies on this specific area is currently limited [80,89]. Finally, 18F-FDG PET/CT has also proven highly useful for discriminating between true disease recurrence both in asymptomatic patients and in those with clinical suspicion of recurrent disease, reaching a sensitivity, specificity, accuracy, PPV and NPV of 87.5-92.9%, and respectively .
在初始分期方面，18F-FDG PET/CT 表现出色，其敏感性、特异性和准确性分别可达 80、100 和 。[87] PET/CT 尤其有助于检测藏匿在肠系膜之间的腹膜转移，因为它能够描绘其相对于仅进行 CT 的增加代谢活性，并且有助于检测远处转移（在某些研究中敏感性可达 ） 。然而， PET/CT 在局部盆腔和盆腔主动脉淋巴结分期方面似乎有些局限，仅具有 的敏感性，尽管目前对这一特定领域的研究数量有限[80,89]。最后，18F-FDG PET/CT 也被证明对于在无症状患者和临床怀疑复发疾病的患者之间区分真实疾病复发非常有用，其敏感性、特异性、准确性、PPV 和 NPV 分别为 87.5-92.9%、 和 。

The value of on preoperative 18 F -FDG PET/CT is a powerful prognostic factor for overall and disease-free survival, outperforming more conventional variables such as FIGO stage or tumor size [91]. Specifically, in a series of 19 patients, Park et al. have ascertained more favorable outcomes for patients with tumors exhibiting . [91].
手术前 18 F-FDG PET/CT 上 的价值是全身和无病存活的强大预后因素，优于更传统的变量，如 FIGO 分期或肿瘤大小 [91]。具体来说，在一系列 19 位患者中，Park 等人确定了表现 的肿瘤患者有更有利的预后结果。 [91]。

LMSs tend to spread systematically from the myometrium through the pelvic blood vessels and lymphatics into the adjacent pelvic organs, abdomen and lungs [59]. Precise staging with the 2009 FIGO classification (Table 1), which is now specific to uterine LMS, should be performed to ensure an optimal management [10,92]. A detailed discussion of the role of imaging in staging LMS is however beyond the scope of this manuscript. However, it is important to note that because of the difficulty in the preoperative diagnosis of LMS, many patients initially undergo surgery for presumed benign leiomyomas detected on US. These patients are typically treated by general gynecologists without advanced imaging evaluation or frozen tissue preservation [93]. As a result, this often leads to incomplete surgical staging and a suboptimal primary surgical resection with poorer patient outcomes [3].

Despite current state of the art advances in the imaging differentiation of LMS from atypical leiomyomas, there remains a certain lack of consensus regarding the individual usefulness of MRI features. Through our review of the current diagnostic imaging literature on the subject, we have attempted to summarize and highlight the principal MRI imaging features felt to aid in favoring a diagnosis of LMS over leiomyoma (Table 3). Because assessing the value of individual imaging features may often prove challenging in the context of obtaining a clear diagnosis, we have also attempted to provide some guidance through the use of a diagnostic algorithm combining multiple imaging features (Fig. 6). Further prospective studies with larger populations of interest, using multivariate models with computed image analysis and machine learning could potentially further improve consensus on the ability of MRI to accurately differentiate LMSs from atypical leiomyomas.
尽管目前在 LMS 与非典型平滑肌瘤的成像鉴别方面取得了最新技术进展，但关于 MRI 特征的个体有用性仍存在一定的共识缺乏。通过我们对当前有关该主题的诊断成像文献的回顾，我们试图总结和强调被认为有助于支持 LMS 诊断而非平滑肌瘤的主要 MRI 成像特征（表 3）。由于评估个体成像特征的价值在获得明确诊断的情况下通常会带来挑战，因此我们还尝试通过结合多个成像特征的诊断算法提供一些指导（图 6）。进一步的前瞻性研究，使用具有计算图像分析和机器学习的多变量模型，可能进一步改善 MRI 准确区分 LMS 与非典型平滑肌瘤的共识，尤其是在更大的感兴趣人群中。

This work did not receive any grant from funding agencies in the public, commercial, or not-for-profit sectors.
这项工作没有从公共、商业或非营利部门的资助机构获得任何资助。

All authors attest that they meet the current International Committee of Medical Journal Editors (ICMJE) criteria for Authorship.
所有作者都证明他们符合当前的国际医学期刊编辑委员会（ICMJE）的作者资格标准。

Simon Sun: conceptualization, methodology, validation formal analysis, investigation, resources, data curation, writing - original draft, writing - review and editing, visualization and project administration.
Simon Sun：概念化，方法论，验证正式分析，调查，资源，数据整理，撰写-原始草稿，撰写-审阅和编辑，可视化和项目管理。

Pietro A Bonaffini: conceptualization, methodology, validation, formal analysis, investigation, resources, data curation, writing - original draft, writing - review and editing and visualization.
Pietro A Bonaffini：概念化，方法论，验证，形式分析，调查，资源，数据整理，撰写-原始草案，撰写-审查和编辑以及可视化。

Stephanie Nougaret: conceptualization, methodology, validation, formal analysis, investigation, data curation, writing - review and editing and supervision.
Stephanie Nougaret：概念化，方法论，验证，形式分析，调查，数据整理，撰写 - 审查和编辑以及监督。

Laure Fournier: conceptualization, methodology, validation, writing - review and editing supervision.
Laure Fournier：概念化，方法论，验证，撰写 - 审查和编辑监督。

Anthony Dohan: conceptualization, methodology, writing - review and editing and supervision.
Anthony Dohan：概念化，方法论，写作 - 审查和编辑以及监督。

Jaron Chong: conceptualization, methodology, writing review and editing and supervision.
Jaron Chong：概念化，方法论，写作审查和编辑以及监督。

Jan Smith: conceptualization, methodology, writing review and editing and supervision.
Jan Smith：概念化，方法论，写作审查和编辑以及监督。

Helen Addley: conceptualization, methodology, writing review and editing and supervision.
Helen Addley：概念化，方法论，写作审查和编辑以及监督。

Caroline Reinhold: conceptualization, methodology, validation, formal analysis, data curation, resources, writing
Caroline Reinhold：概念化，方法论，验证，形式分析，数据整理，资源，写作

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