超声造影在脑胶质瘤切除术术中的应用价值

doi:10.3877/cma.j.issn.1672-6448.2023.07.015

目的

评估超声造影在脑胶质瘤切除术术中的应用价值。

方法

选取2020年9月至2021年7月于哈尔滨医科大学附属第一医院神经外科行脑胶质瘤切除术的27例患者（术前MRI诊断为脑胶质瘤），所有患者术中均行二维超声及超声造影检查，以术后病理作为诊断金标准，明确脑胶质瘤病理类型。采用随机区组设计方差分析比较高级别脑胶质瘤的肿瘤组织、正常脑组织和供血动脉超声造影参数［开始强化时间（TTS）、达峰时间（TTP）、峰值强度（API）］的差异，组间多重比较采用Tukey HSD检验；采用配对t检验比较低级别脑胶质瘤的肿瘤组织和正常脑组织超声造影参数的差异。

结果

27例脑胶质瘤患者中，根据术后病理回报，其中高级别脑胶质瘤16例，低级别脑胶质瘤11例。在高级别脑胶质瘤中，肿瘤组织的TTS为（30.94±2.11）s、TTP为（45.04±2.74）s、API为（79.56±7.35）dB；主要供血动脉的TTS为（28.88±1.54）s、TTP为（43.04±2.85）s、API为（134.27±14.57）dB；正常脑组织的TTS为（35.88±2.16）s、TTP为（46.41±2.75）s、API为（48.02±4.79）dB；高级别脑胶质瘤肿瘤组织的TTS、TTP低于正常脑组织、高于主要供血动脉，API高于正常脑组织、低于主要供血动脉，差异均具有统计学意义（P均＜0.001）。在低级别脑胶质瘤中，肿瘤组织的TTS为（23.62±1.90）s、TTP为（35.66±2.38）s、API为（103.67±7.32）dB；正常脑组织的TTS为（27.97±2.23）s、TTP为（44.11±4.68）s、API为（67.27±11.59）dB；低级别脑胶质瘤肿瘤组织的TTS、TTP低于正常脑组织，API高于正常脑组织，差异均具有统计学意义（t=-14.80、-7.41、8.67，P均＜0.001）。

结论

术中超声造影可为脑胶质瘤定位及切除范围的确定提供帮助，可最大限度提高肿瘤切除范围。

关键词: 脑胶质瘤, 超声, 超声造影, 时间-强度曲线

Objective

To investigate the application value of intraoperative contrast-enhanced ultrasound (CEUS) in surgical resection of glioma.

Methods

A total of 27 patients who underwent glioma resection at Neurosurgery Department of the First Affiliated Hospital of Harbin Medical University from September 2020 to July 2021 (diagnosed as having glioma by MRI before surgery) were selected. All patients underwent intraoperative two-dimensional ultrasound and CEUS. Postoperative pathology was used as the diagnostic gold standard to define the pathological type of glioma. Random block design analysis of variance was used to compare CEUS parameters between tumor tissue, normal brain tissue, and the blood supplying arteries of high-grade glioma. Tukey HSD test was used for multiple comparisons among groups. Paired t test was used for comparison of CEUS parameters between the normal brain tissue and tumor tissue of low-grade glioma.

Results

Among the 27 patients with glioma, 16 had high-grade glioma and 11 had low-grade glioma according to postoperative pathology. In high-grade glioma, the time to start (TTS), time to peak (TTP), and absolute peak intensity (API) were (30.94±2.11) s, (45.04±2.74) s, and (79.56±7.35) dB, respectively. The TTS, TTP, and API of the main supplying arteries were (28.88±1.54) s, (43.04±2.85) s, and (134.27±14.57) dB, respectively. The TTS, TTP, and API of normal brain tissue were (35.88±2.16) s, (46.41±2.75) s, and (48.02±4.79) dB, respectively. The TTS and TTP of high-grade glioma tumor tissue were significantly lower than those of normal brain tissue and higher than those of the main supplying arteries, and the API was significantly higher than that of normal brain tissue and lower than that of the main supplying arteries (P＜0.001). In low-grade glioma, the TTS, TTP, and API were (23.62±1.90) s, (35.66±2.38) s, and (103.67±7.32) dB, respectively. The TTS, TTP, and API of normal brain tissue were (27.97±2.23) s, (44.11±4.68) s, and (67.27±11.59) dB, respectively. The TTS and TTP of low-grade glioma tumor tissue were significantly lower than those of normal brain tissue, while the API of low-grade glioma tumor tissue was significantly higher than that of normal brain tissue (t=-14.80, -7.41, and 8.67, respectively, P＜0.001 for all).

Conclusion

Intraoperative CEUS can contribute to the localization of glioma and the determination of the extent of resection (EOR), thus providing valuable information for surgeons, maximizing the EOR of the tumor, and prolonging the survival of patients.

Key words: Brain glioma, Ultrasound, Contrast-enhanced ultrasound, Time-intensity curve

图1 高级别脑胶质瘤术中超声声像图。脑胶质瘤呈稍高于正常脑组织的均质回声，较难与正常脑组织辨别

图2 高级别脑胶质瘤的术中超声造影图像。可见肿瘤组织呈高增强，边界清晰（蓝色箭头），内部可见未增强坏死区（绿色箭头），下方侧脑室（黄色星星）未见强化

图3 脑胶质瘤切除后术中超声及超声造影检查图像。图a：左侧颞枕部及丘脑胶质瘤切除术后，术中超声扫查残腔，可见残腔周边一大小约14.3 mm×11.1 mm的略高回声区（黄色箭头），边界欠清晰，为确认是否为残余肿瘤组织行术中超声造影检查。图b：行术中超声造影后，箭头所指处未见造影剂灌注，考虑该处异常回声并非残余肿瘤组织，后术者探查残腔，证实其为术中止血使用的明胶海绵

图4 高级别脑胶质瘤术中超声及超声造影表现。图a为高级别脑胶质瘤术中超声造影图像，感兴趣区域（ROI）1（红色圆圈）为供血动脉，ROI 2（黄色圆圈）、ROI 3（绿色圆圈）为肿瘤组织，ROI 4（蓝色圆圈）为周围正常脑组织；图b为高级别脑胶质瘤术中二维灰阶超声图像，肿瘤组织与周围正常脑组织分界模糊；图c为高级别脑胶质瘤超声造影时间-强度曲线图像，可见供血动脉显著快进，且呈明显高增强，且2处肿瘤组织ROI的开始强化时间、达峰时间均低于正常脑组织，峰值强度均高于正常脑组织

表1 高级别脑胶质瘤及其供血动脉与正常脑组织间的超声造影时间-强度曲线指标比较（

x ¯

±s）

组别	TTS（s）	TTP（s）	API（dB）
供血动脉	28.88±1.54	43.04±2.85	134.27±14.57
肿瘤组织	30.94±2.11^a	45.04±2.74^a	79.56±7.35^a
正常脑组织	35.88±2.16^bc	46.41±2.75^bc	48.02±4.79^bc
F值	116.87	66.74	678.08
P值	＜0.001	＜0.001	＜0.001

表1 高级别脑胶质瘤及其供血动脉与正常脑组织间的超声造影时间-强度曲线指标比较（

x ¯

±s）

组别	TTS（s）	TTP（s）	API（dB）
供血动脉	28.88±1.54	43.04±2.85	134.27±14.57
肿瘤组织	30.94±2.11^a	45.04±2.74^a	79.56±7.35^a
正常脑组织	35.88±2.16^bc	46.41±2.75^bc	48.02±4.79^bc
F值	116.87	66.74	678.08
P值	＜0.001	＜0.001	＜0.001

表2 低级别脑胶质瘤与正常脑组织间的超声造影时间-强度曲线指标比较（

x ¯

±s）

组别	TTS（s）	TTP（s）	API（dB）
肿瘤组织	23.62±1.90	35.66±2.38	103.67±7.32
正常脑组织	27.97±2.23	44.11±4.68	67.27±11.59
t值	-14.80	-7.41	8.67
P值	＜0.001	＜0.001	＜0.001

表2 低级别脑胶质瘤与正常脑组织间的超声造影时间-强度曲线指标比较（

x ¯

±s）

组别	TTS（s）	TTP（s）	API（dB）
肿瘤组织	23.62±1.90	35.66±2.38	103.67±7.32
正常脑组织	27.97±2.23	44.11±4.68	67.27±11.59
t值	-14.80	-7.41	8.67
P值	＜0.001	＜0.001	＜0.001

图5 低级别脑胶质瘤术中超声表现。图a为低级别脑胶质瘤术中超声造影图像，可见肿瘤组织增强高于周围正常脑组织；图b为低级别脑胶质瘤术中二维灰阶超声图像，红色为感兴趣区域（ROI）1，代表肿瘤组织，黄色为ROI 2，代表正常脑组织；图c为相应的色彩叠加图像；图d为超声造影相应时间-强度曲线，红色ROI 1对应为肿瘤组织，黄色ROI 2对应为正常脑组织，可见肿瘤组织的开始强化时间、达峰时间均低于正常脑组织，峰值强度高于正常脑组织

1	Cheng LG, He W, Zhang HX, et al. Intraoperative contrast enhanced ultrasound evaluates the grade of glioma [J]. Biomed Res Int, 2016, 2016: 2643862.
2	Della Pepa GM, Ius T, La Rocca G, et al. 5-Aminolevulinic acid and contrast-enhanced ultrasound: the combination of the two techniques to optimize the extent of resection in glioblastoma surgery [J]. Neurosurgery, 2020, 86(6): E529-E540.
3	Ritschel K, Pechlivanis I, Winter S. Brain tumor classification on intraoperative contrast-enhanced ultrasound [J]. Int J Comput Assist Radiol Surg, 2015, 10(5): 531-540.
4	Prada F, Mattei L, Del Bene M, et al. Intraoperative cerebral glioma characterization with contrast enhanced ultrasound [J]. Biomed Res Int, 2014, 2014: 484261.
5	Gildenberg PL, Woo SY. Multimodality program involving stereotactic surgery in brain tumor management [J]. Stereotact Funct Neurosurg, 2000, 75(2-3): 147-152.
6	Duffau H. New concepts in surgery of WHO grade II gliomas: functional brain mapping, connectionism and plasticity--a review [J]. J Neurooncol, 2006, 79(1): 77-115.
7	Haider SA, Lim S, Kalkanis SN, et al. The impact of 5-aminolevulinic acid on extent of resection in newly diagnosed high grade gliomas: a systematic review and single institutional experience [J]. J Neurooncol, 2019, 141(3): 507-515.
8	Wei L, Roberts DW, Sanai N, et al. Visualization technologies for 5-ALA-based fluorescence-guided surgeries [J]. J Neurooncol, 2019, 141(3): 495-505.
9	Morshed RA, Young JS, Han SJ, et al. Perioperative outcomes following reoperation for recurrent insular gliomas [J]. J Neurosurg, 2018, 131(2): 467-473.
10	Sanai N, Berger MS. Surgical oncology for gliomas: the state of the art [J]. Nat Rev Clin Oncol, 2018, 15(2): 112-125.
11	Dallabona M, Sarubbo S, Merler S, et al. Impact of mass effect, tumor location, age, and surgery on the cognitive outcome of patients with high-grade gliomas: a longitudinal study [J]. Neurooncol Pract, 2017, 4(4): 229-240.
12	Spena G, D'Agata F, Panciani PP, et al. Practical prognostic score for predicting the extent of resection and neurological outcome of gliomas in the sensorimotor area [J]. Clin Neurol Neurosurg, 2018, 164: 25-31.
13	Nossek E, Korn A, Shahar T, et al. Intraoperative mapping and monitoring of the corticospinal tracts with neurophysiological assessment and 3-dimensional ultrasonography-based navigation [J]. J Neurosurg, 2011, 114(3): 738-746.
14	Doglietto F, Belotti F, Panciani P, et al. High-definition 3-dimensional exoscope for 5-ALA glioma surgery: 3-dimensional operative video [J]. Oper Neurosurg, 2020, 18(3): E82.
15	Panciani PP, Fontanella M, Garbossa D, et al. 5-aminolevulinic acid and neuronavigation in high-grade glioma surgery: results of a combined approach [J]. Neurocirugia (Astur), 2012, 23(1): 23-28.
16	Panciani PP, Fontanella M, Schatlo B, et al. Fluorescence and image guided resection in high grade glioma [J]. Clin Neurol Neurosurg, 2012, 114(1): 37-41.
17	Wu DF, He W, Lin S, et al. Using real-time fusion imaging constructed from contrast-enhanced ultrasonography and magnetic resonance imaging for high-grade glioma in neurosurgery [J]. World Neurosurg, 2019, 125: e98-e109.
18	Van Dreden P, Elalamy I, Gerotziafas GT. The role of tissue factor in cancer-related hypercoagulability, tumor growth, angiogenesis and metastasis and future therapeutic strategies [J]. Crit Rev Oncog, 2017, 22(3-4): 219-248.
19	Ramjiawan RR, Griffifioen AW, Duda DG. Antiangiogenesis for cancer revisited: is there a role for combinations with immunotherapy? [J]. Angiogenesis, 2017, 20(2): 185-204.
20	Huang Y, Goel S, Duda DG, et al. Vascular normalization as an emerging strategy to enhance cancer immunotherapy [J]. Cancer Res, 2013, 73(10): 2943-2948.
21	Bonekamp D, Deike K, Wiestler B, et al. Association of overall survival in patients with newly diagnosed glioblastoma with contrast-enhanced perfusion MRI: comparison of intraindividually matched T1- and T2 (*)-based bolus techniques [J]. J Magn Reson Imaging, 2015, 42(1): 87-96.
22	Prada F, Bene MD, Fornaro R, et al. Identifification of residual tumor with intraoperative contrastenhanced ultrasound during glioblastoma resection [J]. Neurosurg Focus, 2016, 40(3): E7.
23	Artzi M, Blumenthal DT, Bokstein F, et al. Classifification of tumor area using combined DCE and DSC MRI in patients with glioblastoma [J]. J Neurooncol, 2015, 121(2): 349-357.
24	Del Bene M, Perin A, Casali C, et al. Advanced ultrasound imaging in glioma surgery: beyond gray-scale B-mode [J]. Front Oncol, 2018, 8: 576.
25	葛亚娟, 杨磊, 高军喜, 等. 术中超声造影定量分析在诊断不同级别胶质瘤瘤体及瘤周水肿的临床价值 [J]. 中国超声医学杂志, 2015, 31(3): 193-196.
26	吴意赟, 张心怡, 蔡婷, 等. 超声造影在颅内病变手术中的应用 [J]. 肿瘤影像学, 2020, 29(6): 536-540.
27	Prada F, Perin A, Martegani A, et al. Intraoperative contrast-enhanced ultrasound for brain tumor surgery [J]. Neurosurgery, 2014, 74(5): 542-552.

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Application value of intraoperative contrast-enhanced ultrasound in surgical resection of glioma

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Application value of intraoperative contrast-enhanced ultrasound in surgical resection of glioma