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   复旦学报(医学版)  2020, Vol. 47 Issue (6): 882-887      DOI: 10.3969/j.issn.1672-8467.2020.06.013
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卵巢性索间质肿瘤的临床及超声表现分析
陆蓓蕾1 , 黄备建1,2 , 漆玖玲1 , 樊韵玲1 , 王文平1,2     
1. 复旦大学附属中山医院超声科 上海 200032;
2. 上海市影像医学研究所 上海 200032
摘要目的 探索卵巢常见类型性索间质肿瘤的超声特点及其与临床表现的相关性,并分析误诊原因。方法 收集2010年至2019年复旦大学附属中山医院经阴道及/或经腹部超声检查并经手术病理证实的71例卵巢性索间质肿瘤患者。卵泡膜纤维瘤、卵泡膜细胞瘤及纤维瘤属于卵巢纤维-卵泡膜瘤组(ovarian thecoma-fibroma groups,OTFG),共64例;成人颗粒细胞瘤(adult granular cell tumor,AGCT)共7例。收集患者卵巢肿块的最大径线、回声、形态、边界、后方回声是否衰减、彩色多普勒血流成像(color Doppler flow imaging,CDFI)信号等信息;比较不同大小肿瘤之间盆腔积液、CA125及肿瘤囊性成分是否具有差异;分析超声成像诊断符合率及误诊情况。结果 OTFG多纵横比 < 1(89.1%),AGCT多为不规则形或分叶状(100%);OTFG以实质低回声为主(73.4%),AGCT常表现为囊实混合型(100%);68.8%OTFG病灶伴回声衰减,AGCT均不伴回声衰减;所有病灶边界清晰;OTFG病灶CDFI多表现为无或少量彩色血流信号,血流信号以周边多见(60.9%),AGCT则CDFI以3、4级彩色血流多见(100%)。不同大小肿瘤之间囊性成分、CA125及盆腔积液差异有统计学意义(χ2=7.407、16.080和21.540;P=0.025、< 0.001和 < 0.001)。实性及实性为主型病变诊断符合率高于囊实性及囊性为主型。结论 OTFG与AGCT在超声表现上有一定差异,可通过声像图特征对两组疾病进行鉴别诊断。
关键词卵巢    性索间质肿瘤    卵巢纤维-卵泡膜瘤组(OTFG)    成人颗粒细胞瘤(AGCT)    超声    
Clinical and sonographic features of ovarian sex cord stromal tumors
LU Bei-lei1 , HUANG Bei-jian1,2 , QI Jiu-ling1 , FAN Yun-ling1 , WANG Wen-ping1,2     
1. Department of Ultrasound, Zhongshan Hospital, Fudan University, Shanghai 200032, China;
2. Shanghai Institute of Imaging Medicine, Shanghai 200032, China
Abstract: Objective To explore the sonographic characteristics of common ovarian sex cord stromal tumors and their correlation with clinical manifestations, and to analyze the causes of misdiagnosis. Methods Ultrasound data of 71 patients with ovarian sex cord stromal cell tumors who underwent transvaginal ultrasonography and confirmed by surgery and pathology from 2010 to 2019 in Department of Ultrasound, Zhongshan Hospital were enrolled in our study.Sixty-four cases of thecal fibroma, thecal cell tumor and fibroma were belong to ovarian thecoma-fibroma groups (OTFG), and 7 cases of adult granular cell tumor (AGCT).Ultrasound features including maximum diameter, echo, boundary, attenuation of posterior echo, color Doppler flow imaging (CDFI) were collected.The cystic components, pelvic fluid and CA125 were compared among different size.The coincidence rate and misdiagnosis of ultrasound imaging were analyzed. Results The longitudinal and transverse ratio of the most of OTFG were less than 1 (89.1%), and most of AGCT were irregular or lobulated (100%).OTFG were predominantly hypoechoic (73.4%), and AGCT were often mixed with cystic solids (100%).68.8% of OTFG lesions were accompanied by echo attenuation, while AGCT were not.All lesions were well-defined.CDFI of OTFG lesions showed no or a small amount of color blood flow signal, and most of the blood flow signals were peripheral (60.9%).In AGCT, CDFI was more common in grade 3 and 4 (100%).Different size of ovarian sex cord-stromal tumors masses were different in cystic components, pelvic fluid and CA125 (χ2=7.407, 16.080, 21.540;P=0.025, < 0.001, < 0.001).The coincidence rate of diagnosis of solid and solid predominant lesions was higher than that of cystic solid and cystic predominant lesions. Conclusion Ultrasound diagnosis of ovarian sex cord stromal tumors has some characteristic features, which can be used to differentiate the two groups of diseases.
Key words: ovary    sex cord stromal tumor    ovarian thecoma-fibroma groups (OTFG)    adult granulosa cell tumor (AGCT)    ultrasound    

卵巢性索间质肿瘤是卵巢肿瘤中较为少见的类型,占所有卵巢肿瘤的5%~10%,卵泡膜纤维瘤、卵泡膜细胞瘤、纤维瘤同属于卵巢纤维-卵泡膜瘤组(ovarian thecoma-fibroma groups,OTFG),OTFG是最常见的性索间质细胞瘤,其次是成人颗粒细胞瘤(adult granular cell tumor,AGCT)[1-2]。卵巢性索间质肿瘤起源于卵巢性索间质,因其不同组织学类型而表现多样,部分类型之间影像学表现可能会相互重叠,与其他来源性肿瘤较易混淆。卵巢性索间质肿瘤中只有小部分患者糖类抗原125(carbohydrate antigen 125,CA125)升高[3],临床缺乏特异性肿瘤标记物,影像学检查是主要诊断方法。经阴道超声是附件区肿块首选的检查方法,可用于判断肿块来源及性质,既往文献显示OTFG表现为附件区实质性肿块伴有后方回声衰减,AGCT表现多样,尚无统一的诊断标准。本研究通过分析不同种类性索间质肿瘤的临床表现及超声特征,不同大小肿瘤对于囊性成分、盆腔积液和CA125的影响,探索此种类型肿瘤诊断与鉴别诊断的思路,以增加术前诊断的准确性。

资料和方法

一般资料  回顾性分析2010年至2019年复旦大学附属中山医院行阴道及/或经腹检查并经手术病理证实的71例卵巢性索间质肿瘤患者,其中卵泡膜纤维瘤患者35例,卵泡膜细胞瘤21例,纤维瘤8例,颗粒细胞瘤7例。术前收集患者一般资料、CA125、CA199、甲胎蛋白(alpha fetoprotein,AFP)及人附睾蛋白4(human epididymisprotein4,HE4)等肿瘤标志物检测,正常参考值范围分别为 < 35 U/mL、< 37 U/mL、< 20 ng/mL及 < 150 pmol/L。

仪器和方法  使用GE E10、Philips IU22和Aloka 4000等超声诊断仪,所有患者均经阴道超声检查,使用阴道探头(频率5~9 MHz)及/或经腹探头(频率2~5 MHz)观察子宫、双附件及盆腔,测量肿块大小、回声、形状、边界、后方回声、彩色多普勒超声及积液等情况。依据国际卵巢肿瘤分析组织(International Ovarian Tumor Analysis,IOTA)彩色多普勒成像(color Doppler flow imaging,CDFI)分级标准[4],将肿块分为4级:1级,无彩色血流信号;2级,少量彩色血流信号;3级,中等程度彩色血流信号;4级,丰富彩色血流信号。依据声像图特征,将肿块回声分为4类:1类,完全实性(图 1~2);2类,实性伴囊性区(实性成分 > 2/3,图 3A);3类,囊实混合性肿块(实性成分1/3~2/3,图 3B3C);4类,囊性为主(实性成分 < 1/3,图 4[5]。当患者同时有多枚肿块时,取最大的一枚作为观察目标。

A case of 65-year-old woman with ovarian thecal fibroma (12.0 cm):elliptical inhomogeneous hypoechoic mass with palisade echo attenuation in transabdominal ultrasonography.The surrounding area is accompanied by a small amount of non-echoic areas.CDFI shows peripheral dotted color blood flow signals. 图 1 卵泡膜纤维瘤超声表现 Fig 1 Sonographic features of ovarian thecal fibroma
A case of 57-year-old woman with ovarian fibroma (3.4 cm):elliptical inhomogeneous hypoechoic mass with hyperechoic spots in transvaginal sonography. 图 2 卵巢纤维瘤超声表现 Fig 2 Sonographic features of ovarian fibroma
A:A case of 37-year-old woman with ovarian thecal cell tumor (6.1 cm), elliptical hypoechoic mass with global attenuation in transvaginal sonography.B:A case of 62-year-old woman with ovarian thecal cell tumor (12.0 cm), elliptical cystic solid mass in transvaginal sonography.C:A case of 32-year-old woman with ovarian thecal cell tumor (18.0 cm), irregular mass with mainly cystic echo and clear boundary of cystic area in transabdominal ultrasonography. 图 3 卵泡膜细胞瘤超声表现 Fig 3 Sonographic features of ovarian thecal cell tumor
A case of 66-year-old woman with adult granular cell tumor (12.0 cm):irregular cystic solid mass with rich color blood flow and clear boundary in transabdominal ultrasonography. 图 4 AGCT超声表现 Fig 4 Sonographic features of AGCT

统计学方法  采用SPSS 23.0软件进行统计学分析,符合正态分布的计量资料用x±s表示。计数资料采用百分比表示,采用χ2检验或Fisher确切概率法进行两组或多组比较,检验水准为α=0.05。

结果

患者一般情况及临床表现  OTFG及AGCT均好发于老年女性,平均年龄分别为(64.1±4.7)岁和(50.1±11.8)岁,48例OTFG患者均是绝经后女性(绝经2~35年),4例AGCT是绝经后女性(绝经1~20年)。13例OTFG患者CA125升高(42.70~277.30 U/mL),3例AGCT患者CA125升高(129.70~280.40 U/mL);2例OTFG患者HE4升高(185.8~464.1)pmol/L,1例AGCT患者HE4升高(157.2 pmol/L);CA199升高1例(227.2 U/mL),见于卵泡膜纤维瘤中。在有症状的患者中,腹痛最常见(29.6%,21/71),然后依次是腹部包块(25.3%,18/71)、泌尿道症状(11.3%,8/71)及阴道不规则出血(8.5%,6/71)。

表 1 患者的一般情况及临床表现 Tab 1 Clinical demographics of patients  
[x±s or n (%)]
Item Fibrothecoma Thecoma Fibroma AGCT
Case(n) 35 21 8 7
Age (y) 59.8±13.8 54.3±15.3 59.1±16.5 50.1±11.8
Largest diameter (cm) 5.4±3.4 6.3±3.7 2.9±1.1 10.4±4.4
Menopause 27 (77.1) 15 (71.4) 6 (75.0) 4 (57.1)
Bilateral 3 (8.6) 0 (0) 0 (0) 0 (0)
Elevated CA125 9 (25.7) 2 (9.5) 2 (25.0) 3 (42.9)
Elevated HE4 2 (5.7) 0 (0) 0 (0) 1 (14.3)
Elevated CA199 1 (2.9) 0 (0) 0 (0) 0 (0)
Symptoms
    Pain 12 (34.2) 5 (23.8) 0 (0) 4 (57.1)
    Irregular bleeding 4 (11.4) 0 (0) 0 (0) 2 (28.6)
    Palpable mass 9 (25.7) 6 (28.6) 0 (0) 3 (42.9)
    Urinary symptoms 5 (14.3) 2 (9.5) 0 (0) 1 (14.3)
Comorbidities
    Hysteromyoma 8 (22.9) 6 (28.6) 4 (50.0) 1 (14.3)
    Adenomyosis 2 (5.7) 1 (4.8) 1 (12.5) 0 (0)
    Serous/mucinous adenoma 4 (11.4) 1 (4.8) 2 (25.0) 0 (0)
    Endometrial hyperplasia with canceration 1 (2.9) 0 (0) 0 (0) 1 (14.3)
    Endometrial polyp 1 (2.9) 1 (4.8) 0 (0) 1 (14.3)
Pelvic fluid 20 (57.1) 5 (23.8) 1 (12.5) 6 (85.7)
Hydrothorax 0 (0) 0 (0) 0 (0) 1 (14.3)

不同种类性索-间质细胞肿瘤超声特点比较  OTFG多表现为纵横比 < 1(横椭圆形)(89.1%),AGCT多表现为不规则形或分叶状(100%),所有病灶边界清晰。OTFG常伴有后方回声衰减(68.8%),多表现为栅栏状或整体回声衰减,AGCT后方回声无衰减。卵泡膜纤维瘤、卵泡膜细胞瘤及纤维瘤均以实质低回声为主(73.4%),其中以不均质低回声伴颗粒状或条索状高回声多见(70.2%),三者CDFI多表现为无或少量彩色血流信号,血流信号以周边多见(60.9%),卵泡膜细胞瘤较其余两者中等程度彩色血流信号更多见(30%)。AGCT全部表现为囊实混合性或囊性为主性,CDFI血流信号较其他三者更为丰富,以3级及4级彩色血流多见(表 2)。

表 2 不同种类性索间质肿瘤超声表现分析 Tab 2 Ultrasound manifestations of different types of sex cord stromal tumors
Tumor type Case Aspect ratio
< 1[n(%)]
Shadowing
[n(%)]
Echogenicity CDFI
Grade 1 Grade 2 Grade 3 Grade 4 Grade 1 Grade 2 Grade 3 Grade 4
Fibrothecoma 35 32(91.4) 28(80.0) 27 5 2 1 20 14 1 0
Thecoma 21 18(85.7) 11(52.4) 14 1 4 2 10 7 3 0
Fibroma 8 7(87.5) 5(62.5) 6 2 0 0 6 2 0 0
AGCT 7 0(0) 0(0) 0 0 6 1 0 0 4 3
  CDFI:Color Doppler flow imaging; AGCT:Adult granular cell tumor.

肿瘤大小与患者临床表现的关系  不同大小OTFG肿块之间囊性成分、盆腔积液及CA125升高差异有统计学意义(χ2=7.407、16.080和21.540,P=0.025、< 0.001和 < 0.001)(表 3)。

表 3 肿瘤大小与囊性成分、盆腔积液及CA125的关系 Tab 3 Relationship between tumor size and cystic components, ascites and CA125  
[n(%)]
Maximum diameter(cm) Case Mixed cystic-solid and mainly cystic Pelvic fluid Elevated CA125
< 5 31 4(12.9) 7(22.6) 4(12.9)
≤5, < 10 24 8(33.3) 15(62.5) 2(8.3)
≥10 9 5(55.6) 8(88.9) 7(77.8)
χ2 7.407 16.080 21.540
P 0.025 < 0.001 < 0.001

超声成像误诊分析  71例进行超声检查的患者中,实性及实性为主型肿瘤最易误诊为子宫浆膜下及阔韧带肌瘤(10.9%),含有囊性成分或囊性为主的类型最易误诊为囊腺瘤/癌(25%),且其诊断符合率低于实性及实性为主类型(表 4)。

表 4 超声成像诊断的符合率及误诊情况 Tab 4 Coincidence rate and misdiagnosis of ultrasound  
[n(%)]
Tumor feature Case Coincidence rate Specific diagnosis suggested by original ultrasound examiner
Subserosal or broad
ligamentleiomyoma
Cystic adenocarcinoma/
Cystadenoma
Cyst Retroperitoneal
mass
Sarcoma Unknown
Solid or mainly solid 55 46 (83.7) 6(10.9) 0 (0) 0 (0) 2(3.6) 0 (0) 1 (1.8)
Mixed cystic-solid or
mainly cystic
16 8 (50.0) 0 (0) 4 (25.0) 1 (6.3) 0 (0) 1 (6.3) 2 (12.5)
讨论

卵巢性索间质肿瘤任何年龄均可发病,但以中老年女性更多见,常为单侧,与本研究一致[1-2]。本研究显示多数患者以体检发现附件区占位就诊,当肿瘤较大时可触及腹部包块,部分患者因异常阴道流血就诊,可能与肿瘤细胞刺激雌激素分泌有关,当绝经妇女阴道出血伴附件区肿块时应警惕此病。值得注意的是,合并同侧或对侧卵巢不同来源病变并不少见,当合并囊性或囊实性卵巢病变时应考虑不同类型病变的可能,如合并囊腺瘤/癌、囊肿及子宫内膜异位囊肿等。

纤维瘤由嵌入在胶原间质中的梭形细胞束螺旋状排列构成,无卵泡膜细胞及上皮成分。卵泡膜细胞瘤体内主要成分是富含脂质成分的圆形或椭圆形细胞,类似于卵泡膜细胞,可能具有激活雌激素的能力,可出现阴道流血,子宫内膜增厚及子宫内膜癌[6]。卵泡膜纤维瘤介于这两种类型之间,表现为类似于卵泡膜细胞出现于片状或巢状排列的梭形细胞背景之下,这种巢状排列的梭形细胞可能与肿瘤后方回声衰减有关[7]。以上3种肿瘤为实性肿块,占卵巢肿瘤的4%~6%,大多数为良性,恶性发生率 < 1%。本研究显示卵泡膜纤维瘤、卵泡膜细胞瘤及纤维瘤以无或少量彩色血流信号为主,彩色血流分布于肿块周边较为常见,卵泡膜细胞瘤的3级血流信号比例高于纤维瘤及卵泡膜纤维瘤,可能与卵泡膜细胞瘤中相对丰富的血管有关,而AGCT的血流信号较丰富,多为3、4级,与既往研究相一致[8-9]。虽然卵泡膜纤维瘤、卵泡膜瘤及纤维瘤以均匀或不均匀实性肿块为主,本研究显示随着肿块的增大,出现囊性病变,出血的可能性随之增大,所有病灶中未观察到钙化。实质性回声多为低回声伴颗粒状或条索状高回声,其次是均匀低回声,可能与肿块内部呈巢状排列的细胞有关。Oh等[10]研究发现46%的纤维瘤可以显示完整或残余的卵巢结构。本研究发现,6例性索间质肿瘤外生于卵巢之外,通过蒂游离于卵巢或位于卵巢表面,此时可以观察到正常卵巢形状,鉴别诊断有一定难度。

颗粒细胞瘤是较少见的卵巢性索间质肿瘤,由围绕在卵泡周围的生殖细胞组成,占卵巢肿瘤的2%~3%,占卵巢恶性肿瘤的5%,颗粒细胞瘤被视为低度恶性肿瘤,是最常见的恶性性索间质肿瘤,分为成人型和幼年型,成人型占95%[11]。肿瘤细胞促雌激素作用,从而出现月经增多、子宫内膜增生、子宫内膜癌及经后出血,本研究显示2例患者有绝经后阴道流血,1例伴有子宫内膜癌。AGCT可发生于任何年龄,峰值发病年龄为50~55岁,发现时往往较大(文献报道平均直径12 cm),通常表现为囊实性,偶见实性或完全囊性[8]。本研究显示所有AGCT均表现为囊实性病变,且血流丰富,可能与本组病例数纳入数目较少有关。

本研究显示,不同大小OTFG肿瘤之间有无盆腔积液及CA125升高差异具有统计学意义,肿块越大,肿块内部囊性变的比例越高,盆腔积液及CA125升高的概率越大,与既往研究相一致。腹水的形成可能与肿瘤表面的渗出超过腹膜的吸收能力有关,肿瘤表面积越大,形成腹水的可能性越大[2]。性索间质肿瘤CA125与上皮性肿瘤相比,大多数仅轻度增高,可能与肿瘤刺激腹膜促使CA125增高有关[12]。HE4是预测卵巢癌较为灵敏的指标,多项研究表明HE4与卵巢癌、子宫内膜癌、肺癌、膀胱癌等有关,且诊断卵巢癌的敏感性与特异性均优于CA125,可用于卵巢肿块的鉴别诊断、早期发现卵巢癌、监测对化疗的反应性以及评估卵巢癌的预后[13],肾功能不全的患者也可能引起HE4升高[14]。本研究发现2例OTFG及1例AGCT患者HE4升高,均为轻度升高,这3例患者均不伴有肾功能不全,其中AGCT同时合并子宫内膜癌,引起OTFG患者HE4升高的原因有待于进一步大样本量的研究。

本研究发现实性病灶超声误诊为子宫浆膜下肌瘤或阔韧带肌瘤最为多见,其次是腹膜后肿瘤。OTFG大多发生于绝经期妇女,卵巢萎缩不易显示,实质性肿瘤灰阶图像与浆膜下或阔韧带肌瘤相似,两者均表现为边界清楚、形态规则或稍不规则的实质占位,血流信号可不丰富。检查者缺乏经验、对此类疾病声像图特点认识不够、未仔细观察彩色多普勒血流信号是否来源于子宫等原因可造成误判。囊实性病灶最易误诊为卵巢囊腺癌,其次是卵巢囊腺瘤、卵巢单纯囊肿及肉瘤。囊实性病灶的误诊率明显高于实质性病灶,主要原因可能是各类卵巢肿瘤均可表现为附件区囊实性肿块。本研究中的卵巢囊实性肿块体积相对较大,形态规则或呈分叶状,边界清晰,彩色多普勒血流表现差异大,可观察到1~4级血流,部分合并不同程度的盆腔积液或腹水,部分CA125升高,但这些表现都缺乏特异性。早期卵巢上皮性肿瘤、交界性卵巢肿瘤、转移性卵巢肿瘤与囊实性卵巢性索间质肿瘤在灰阶声像图、彩色多普勒血流及CA125肿瘤指标等方面有重叠和交叉,鉴别诊断困难。对于误诊率较高的囊实性性索间质肿瘤,有望通过超声新技术,如超声造影、三维能量多普勒技术等,探索更多的声像图特征,从而减少误判,增加术前诊断的准确性。

本研究的不足之处在于,部分肿瘤性索间质肿瘤例数较少,有待于进一步扩大样本量综合分析;缺少其他卵巢实性及混合性肿块的对比研究,有待于进一步对比分析,找出更多更具特征性的表现。

附件区椭圆形实质性肿块伴后方衰减,边界清晰,CDFI示无或少量彩色血流信号,血供与子宫无关等提示OTFG的诊断;AGCT超声可表现为不规则形或分叶状囊实性肿块,边界清,具有中等或较丰富彩色血流信号。OTFG与AGCT在超声表现上具有一定差异性,可通过声像图特征对两组疾病鉴别诊断。

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文章信息

陆蓓蕾, 黄备建, 漆玖玲, 樊韵玲, 王文平
LU Bei-lei, HUANG Bei-jian, QI Jiu-ling, FAN Yun-ling, WANG Wen-ping
卵巢性索间质肿瘤的临床及超声表现分析
Clinical and sonographic features of ovarian sex cord stromal tumors
复旦学报医学版, 2020, 47(6): 882-887.
Fudan University Journal of Medical Sciences, 2020, 47(6): 882-887.
Corresponding author
QI Jiu-ling,E-mail:qi.jiuling@zs-hospital.sh.cn.
基金项目
上海市自然科学基金(16ZR1433200)
Foundation item
This work was supported by the Shanghai Municipal Natural Science Foundation (16ZR1433200)

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