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ORIGINAL ARTICLE
Year : 2005  |  Volume : 53  |  Issue : 2  |  Page : 208-212

Intraoperative ultrasonographic characteristics of malignant intracranial lesions


Department of Neurosurgery, Medical Faculty, Ondokuzmayis University, Samsun, Turkey

Date of Acceptance17-Jan-2005

Correspondence Address:
Cokluk Cengiz
Department of Neurosurgery, Medical Faculty, Ondokuzmayis University, 55139 Samsun
Turkey
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.16412

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 » Abstract 

Aims : The aim of this study was to evaluate the capability of intraoperative ultrasonography (IOUSG) in identifying malignant intraparenchymal tumors during surgical intervention. Settings and Design : Forty patients with intrinsic malignant tumors were evaluated by using IOUSG. Materials and Methods : A real-time ultrasound scanner with a 3- or 5-MHz transducer was used for this study in all cases. The tip of the ultrasound probe was placed on the intact cranial dura mater and then moved in the sagittal and coronal planes. Results : Nineteen of forty patients had lesions that were primary malignant glial tumors. Five of them had previous surgery and radiotherapy. The remaining twenty-one had metastatic tumors. All lesions were well localized and malignant characteristics were well defined by IOUSG. Radiation-induced changes in five lesions in the surrounding brain and tumor parenchyma were described. Conclusion : In conclusion, IOUSG is not only helpful in localizing lesions but it can also be used in determining the malignant characteristics of lesions.


Keywords: Intracranial tumors, intraoperative ultrasonography, malignant brain lesions


How to cite this article:
Cengiz C, Keramettin A. Intraoperative ultrasonographic characteristics of malignant intracranial lesions. Neurol India 2005;53:208-12

How to cite this URL:
Cengiz C, Keramettin A. Intraoperative ultrasonographic characteristics of malignant intracranial lesions. Neurol India [serial online] 2005 [cited 2019 Aug 24];53:208-12. Available from: http://www.neurologyindia.com/text.asp?2005/53/2/208/16412


Ultrasonography has been used as an intraoperative diagnostic tool since 1970.[1],[2],[3],[4],[5],[6],[7],[8],[9],[10] In this study, we investigated and described the ultrasonographic characteristics of malignant lesions, and evaluated the capability of sonography for this purpose.


 » Materials and Methods Top


This retrospective clinical study was approved by the ethical committee of the Ondokuzmayis University, (Medical Faculty).

The study population comprised patients with primary malignant glial and metastatic tumors. Inclusion criteria were as follows in the preoperative stage: (1) previously operated and irradiated recurrent malignant tumors, (2) metastatic malignant lesions originated from another part of the body, (3) intaparenchymal location on computerized tomography (CT) and magnetic resonance imaging (MRI), (4) perilesional edema appearing on CT and MRI, and (5) cystic and/or necrotic parts demonstrated by CT and MRI. At the intraoperative stage, fast histopathological examination (Frozen section) was performed for all lesions. Benign intracranial lesions were excluded from this study.

Forty patients (between 25 and 75 years of age, mean age ± SD; 53.4 ± 12), who underwent surgery for malignant brain tumors during the period between August 2000 and July 2001, were investigated. Twenty-five (62%) patients were male and 15 (38%) female.

Computerized tomography and MRI were performed in all cases at the preoperative stage.

All tumors were evaluated by one of the authors (CC) using a Tosbee real-time ultrasound scanner (Tosbee, Toshiba Inc., Tokyo). A 3- or 5-MHz transducer was used. The transducer and its cord were covered with a sterile, translucent, disposable plastic sheath to maintain sterile surgical conditions. Before covering the system, the tip of the transducer head was plastered with sterile gel to maximize sonographic images. The tip of the transducer was placed gently on the intact cranial dura and moved in the direction of the sagittal and coronal planes. The selected images were printed.

The tumor location under the craniotomy, the margins from the perilesional brain tissue, internal configuration and echogenicity, the changes in the peritumoral area, and the location of the neuroanatomical structures such as the ventricle, falx, and main arteries to the border of the lesions were also imaged and printed.

After gross resection of tumors, the ultrasonographic examination was repeated to check tumor bed and the residual tumor.

Descriptive statistical analysis was used in this study.


 » Results Top


Of the 40 lesions analyzed in this study, 19 (47%) were intrinsic primary malignant glial tumors and 21 (53%) were metastatic tumors. Computerized tomography and MRI showed irregular contour, irregular contrast enhancement, necrotic parts, and perilesional edema in all patients. The distribution of lesions is shown in [Table - 1].

Thirty-two cases showed a cystic part on CT and MRI. The ultrasonographic appearance of malignant cysts was as low echogenic areas. Free necrotic particles and double density were commonly present in malignant cysts. The solid component surrounding the cysts was thick. The external surface of solid parts was regular but internal surfaces facing cysts were irregular, sometimes including the part projecting into the cyst. [Figure - 1] demonstrates general features of malignant cysts.

Sixty-three percent of the patients had multiple necrotic parts, and the remaining 37% had a single necrosis located in the central part of the lesion. The necrotic part of malignant lesions can be solitary or multiple, and has a mixechogenic appearance. The most hypoechogenic part was commonly located in the central portion. The shape and configuration of the necrotic part may be different from one to another type of malignant lesion. Some characters of necrotic tumors are seen in [Figure - 2].

All malignant lesions showed perilesional edema on CT and MRI. In intraoperative sonographic examination, malignant perilesional areas were seen as two different echogenic zones. The tumors were surrounded by a first, very thin hypoechogenic zone. The echogenicity of the first zone was similar to brain tissue. The second zone was a vasogenic edematous zone. The ultrasonographic appearance of this zone was hyperechogenic and was similar to that of solid tumor parts. The ultrasonographic appearance of perilesional areas, and solid and necrotic parts is shown in [Figure - 3].

Neuroradiological examination showed that perilesional edema, necrosis, irregular contour, and contrast enhancement were present in all previously irradiated recurrent intrinsic glial tumors.

The ultrasonographic appearance of five previously irradiated malignant glial tumors was hyperechogenic compared to the surrounding brain. Our observations showed that the density of peritumoral edemas was lower than those of unradiated cases and that the density of the brain is lower than that of normal brain. The growth pattern of tumors was demonstrated to be of both distortive and invasive character. [Figure - 4] demonstrates some characteristic features of radiation-induced changes in the brain and tumor.

The main ultrasonographic characteristics of malignant brain lesions are shown in [Table - 2].


 » Discussion Top


This study indicates that intraoperative ultrasonographic examination is not only useful in the location of cystic, necrotic and solid parts of tumors but may also distinguish malignant features of lesions at the beginning of surgery. Preoperative CT and MRI may reveal information about the pathological nature of the lesion. The features obtained from these neuroradiological modalities, such as necrotic parts, perilesional edema, irregular contour, and irregular contrast enhancement can be considered as the malignant characteristics [Table - 3]. Previous articles have reported that sonography can be used in the location of tumors, definition of their margins, differentiation of internal characteristics, and detection of residual tumors.[3],[4],[5],[6],[7],[8],[9],[10],[11],[12] Intraoperative MRI is clearly superior to intraoperative ultrasound examination to investigate the completeness of tumor resection during surgery, but it is much cheaper and thus more easily available. It is also shown that IOUSG can enhance the orientation of the surgeon by showing the depth, size, location, and characteristics of the lesion.[6],[7] Intraoperative ultrasonography may also be used as intraoperative image guidance in figuring out 'where am I' after splitting of the brain parenchyma and dissection of the brain sulcus. We usually use small cotton paddy during this stage. The major constraint of ultrasonographic examination is that it requires a high level of skill and experience in the investigator. Surgical removal is especially difficult in low-grade glial tumors due to poor demarcation between lesion and brain.[13] Intraoperative ultrasonography can provide diagnosis of the demarcation line, border of lesion, and edematous tissue.[6],[7],[13] The borders of malignant tumors have features different from those of benign tumors and they can be easily detected by IOUSG.

The capsule is the best demarcation line for intrinsic and extrinsic lesions. However, this is not always the case as some noncapsular tumors can be well demarcated from surrounding neural tissues. The external surface of the capsule is the best area for surgical retraction and dissection. The echogenicity of the capsule is usually denser than that of the solid part of the tumor. However, sometimes it is difficult to distinguish between these two parts. The configuration of the capsule is usually irregular in malignant tumors but tends to be more regular and smooth in benign tumors.

High-grade glial tumors generally have irregular margins. This feature reflects their invasive character. Surgical dissection of these tissues from the brain is extremely difficult. This is similar with those of some metastatic tumors. However, many metastatic lesions have regularly configured borders. Some malignant tumors may have both regular and irregular parts throughout their margin.

Necrotic components are dead parts of lesions and commonly found in malignant tumors. They do not have any vital metabolic reactions and blood circulation. The sonographic appearance of these parts is as low echogenic areas located somewhere in the tumor parenchyma. The necrotic parts are always surrounded by a solid part. Their margins are irregular. Dead necrotic pools may have some tumor particles in their fluid. During sonographic examination, these particles can be seen as freely moving particles when using the sonographic transducer with light pressure. The necrotic part of tumors is generally located in the central or paracentral area. But this concept is not true in tumors that generally originate and are fed from one area. In this type of tumor, the necrotic parts are located in the most remote part of the feeding point.

Other dead parts of tumors are cysts. The characteristic sonographic appearance of cysts is as hypoechogenic areas. Cysts can be associated with benign and malignant tumors. Sonographically, cysts are seen as hypoechogenic areas totally enclosed by a solid part or a membranous structure. Malignant tumors usually have thick a wall, and are commonly associated with malignant perilesional changes. Our ultrasonographic experience of benign cystic lesions is that they have very thin, hyperechogenic cystic walls without perilesional changes. Cysts do not have any gross particles in their fluid. The inner surface of the cyst wall is generally smooth and sometimes associated with trabecules.

Malignant perilesional areas have two different echogenic zones. The first ribbon-like zone encloses the mass and does not include vasogenic edema. The ultrasonographic appearance is hypoechogenic compared to normal brain, but hyperechogenic compared to those of CSF. The zone is compressed by the mass effect of the lesion. The elasticity and biomechanical properties are changed by the growing mass of tumors.[14],[15] Ischemic and gliotic changes are present in this zone.[14],[15],[16] Its blood supply is decreased by the tumor mass.[17] The second zone is a vasogenic edema zone that begins at the border of the first zone. The echogenicity of this zone is similar to solid parts of tumors. The edema associated with metastatic and primary brain tumors is an extracellular vasogenic edema, which extends along the white matter.[14],[15],[16],[17],[18] The cause of this edema is disruption or defective function of the blood-brain barrier. It is usually steroid responsive. There is no relationship between tumor size and the density of the edema. Even small tumors can be associated with aggressive and dense hyperechogenic edema. The density of the edema gradually decreases with increasing distance from the tumor. Malignant perilesional edema is irregular, has a finger-like shape, and can easily be detected by ultrasonography.


 » Conclusions Top


Intraoperative ultrasonography can easily detect the location of intracranial tumors in the brain. We investigated the criteria for distinguishing malignant lesions. Important information about the characteristics of brain tumors can be obtained by ultrasonographic examination of the lesions. The contour of tumors and perilesional changes are the main characteristics. The presence of cysts and necrosis and their characteristics are also important.

Irregular border, necrotic parts, invasive growth pattern, and dense perilesional edema can all be attributed to malignancy.



 
 » References Top

1.Lang FF, Sawaya R. Surgical management of cerebral metastases. Neurosurg Clin of North Am. 1996;7:459-84.   Back to cited text no. 1  [PUBMED]  
2.Yaºargil MG. Microneurosurgery. CNS Tumors: Surgical anatomy, neuropathology, neuroradiology, neurophysiology, clinical considerations, operability, treatment options. 2nd Ed. New York: Georg Thieme verlag; 1994.  Back to cited text no. 2    
3.Auer LM, van Velthoven V. Intraoperative ultrasound (US) imaging. Comparison of pathomorphological findings in US and CT. Acta Neurochir (Wien) 1990;104:84-95.  Back to cited text no. 3    
4.Brownbill D. The clinical value of echoencephalography. Aust NZ J Surg 1970;40:74-8.  Back to cited text no. 4    
5.Glasauer FE, Schlagenhauff RE. The use of intraoperative echoencephalography. Neurology 1970;20:1103-7.  Back to cited text no. 5    
6.Gronningsaeter A, Unsgard G, Ommedal S, Angelsen BA. Ultrasound-guided neurosurgery: A feasibility study in the 3-30 MHz frequency range. Br J Neurosurg 1996;10:161-8.  Back to cited text no. 6  [PUBMED]  
7.Hammoud MA, Ligon BL, elSouki R, Shi WM, Schomer DF, Sawaya R. Use of intraoperative ultrasound for localizing tumors and determining the extent of resection: A comparative study with magnetic resonance imaging. J Neurosurg 1996;84:737-41.  Back to cited text no. 7  [PUBMED]  
8.Kumar P, Sukthankar R, Damany BJ, Mishra J, Jha AN. Evaluation of intraoperative ultrasound in neurosurgery. Ann Acad Med Singapore 1993;23:422-7.   Back to cited text no. 8    
9.Szczerbicki M, Jarek K, Kozlowski J. Intraoperative ultrasonography of brain tumors. Neurol Neurochir Pol 1996;30:831-8.  Back to cited text no. 9  [PUBMED]  
10.Tada M, Kaneko S, Imai T, Abe H, Tsuru M, Shirato H, et al . Intraoperative sonography for brain tumor surgery. Hokkaido Igaku Zasshi 1985;60:82-90.  Back to cited text no. 10    
11.Knake JE, Bowerman RA, Silver TM, McCracken S. Neurosurgical applications of intraoperative ultrasound. Radiol Clin North Am 1985;23:73-90.  Back to cited text no. 11  [PUBMED]  
12.Quencer RM, Montalvo BM. Intraoperative cranial sonography. Neuroradiology 1986;28:528-50.  Back to cited text no. 12  [PUBMED]  
13.Knake JE, Chandler WF, Gabrielsen TO, Latack JT, Gabarski SS. Intraoperative sonographic delineation of low grade brain neoplasms defined poorly by computed tomography. Radiology 1984;151:735-9.  Back to cited text no. 13    
14.Bertossi M, Virgintino D, Maiorano E, Occhiogrosso M, Roncali L. Ultrastructural and morphometric investigation of human brain capillaries in normal and peritumoral tissues. Ultrastruct Pathol 1997;21:41-9.  Back to cited text no. 14  [PUBMED]  
15.Kida S, Ellison DW, Steart PV, Weller RO. Characterization of perivascular cells in astrocytic tumours and peritumoral oedematous brain. Neuropathol Appl Neurobiol 1995;21:121-9.  Back to cited text no. 15  [PUBMED]  
16.Groger U, Huber P, Reulen HJ. Formation and resolution of human peritumoral brain edema. Acta Neurochir Suppl (Wien) 1994;60:373-4.  Back to cited text no. 16  [PUBMED]  
17.Strugar J, Rothbart D, Harrington W, Criscuolo GR. Vascular permeability factor in brain metastases: Correlation with vasogenic brain edema and tumor angiogenesis. J Neurosurg 1994;81:560-6.  Back to cited text no. 17  [PUBMED]  
18.Chang CC, Shinonaga M, Kuwabara T. Effect of dexamethasone on neurotransmitter amines in a rat glioma model. Adv Neurol 1990;52:483-9.  Back to cited text no. 18  [PUBMED]  


Figures

[Figure - 1], [Figure - 2], [Figure - 3], [Figure - 4]

Tables

[Table - 1], [Table - 2], [Table - 3]

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