MAMC Journal of Medical Sciences

ORIGINAL ARTICLE
Year
: 2018  |  Volume : 4  |  Issue : 3  |  Page : 121--127

The Safety and Efficacy of Frame-Based Stereotactic Biopsy of Brain Lesion


Wisam H Mohammed1, Ahmed R Obaid1, Ali K Al-Shalaji2, Samer S Hoz1, Bishree K Shakir3, Luis R Moscote-Salazar4,  
1 Department of Neurosurgery, Neurosurgery Teaching Hospital, Colombia
2 Department of Neurosurgery, College of Medicine, Baghdad University, Baghdad, Iraq
3 Department of Radiology, College of Medicine, Tikrit University, Tikrit, Iraq
4 Department of Neurosurgery, Cartagena Neurotrauma Research Group (CIB), University of Cartagena, Colombia

Correspondence Address:
Dr. Luis R Moscote-Salazar
Department of Neurosurgery, RED LATINO, Organizacion Latinoamericana de Trauma y Cuidado Neurointensivo, Bogota
Colombia

Abstract

Background Radiological imaging techniques provide early detection of neurological diseases, but they do not always provide an adequate diagnosis. With the help of stereotactic biopsy techniques, it is possible to access deep-brain lesions safely and with high precision, being crucial in the elaboration of therapeutic strategies and prevents unnecessary neurosurgical interventions. Aim To evaluate the safety, diagnostic yields, and associated mortality and morbidity of computed tomography-guided stereotactic biopsy for intracranial lesions. Materials and Methods A retrospective study of all pathologically diagnosed intracranial biopsies, between 2010 and 2016 in Baghdad Neurosurgical Teaching Hospital, was conducted. Stereotactic biopsies were performed by using the Leksell stereotactic frame in 116 patients. Medical charts, radiological studies, and postoperative complications were reviewed, and then the information was analyzed. Results A total of 116 patients underwent stereotactic surgery procedures. Patients consisted of 66 females and 50 males, ages ranging from 7 to 74 years (mean 44.4 ± 19.35 years). General anesthesia was used in 88 patients. The rest were performed under local anesthesia. The overall diagnostic yield was 98.3%. Complications were observed in 8.6% of the cases, with morbidity 5.1% of the cases, and the overall mortality rate was 3.4%. These results are comparable to other reports. Other clinical, radiological, or histological variables were not associated with an increased risk of complications. Conclusion Our findings support that frame-based stereotactic biopsy is a relatively safe and valuable technique that allows the neurosurgeon to obtain tissue samples for histopathological diagnosis of most of the intracranial mass lesions.



How to cite this article:
Mohammed WH, Obaid AR, Al-Shalaji AK, Hoz SS, Shakir BK, Moscote-Salazar LR. The Safety and Efficacy of Frame-Based Stereotactic Biopsy of Brain Lesion.MAMC J Med Sci 2018;4:121-127


How to cite this URL:
Mohammed WH, Obaid AR, Al-Shalaji AK, Hoz SS, Shakir BK, Moscote-Salazar LR. The Safety and Efficacy of Frame-Based Stereotactic Biopsy of Brain Lesion. MAMC J Med Sci [serial online] 2018 [cited 2019 May 20 ];4:121-127
Available from: http://www.mamcjms.in/text.asp?2018/4/3/121/249026


Full Text



 Introduction



Brain biopsy procedure has evolved over the last 4 decades in conjunction with the ability to image brain directly, beginning in the mid-1970s with the biopsy sampling of the lesion in the brain using computed tomographic (CT) scanning.[1] In the early 1980s, CT scanning was incorporated into stereotactic procedures.[2] The word “stereotactic” comes from the Greek word “stereos,” which means three dimensional and “tactus” the Latin word meaning to touch.[3] Therefore, stereotactic is a three-dimensional system used to reach deep objects in the brain and provides a high level of accuracy and safety.[4] In neurosurgery, such a system has many advantages, because the trajectory to deep targets through brain tissues may be hazardous and can be associated with significant complications.[5]

A simple and safe stereotactic biopsy procedure followed by an appropriate adjuvant therapy may avoid major neurosurgical procedures.[6]

Traditionally, frame-based techniques have been the standard method used to achieve a reliable and accurate sampling of intracranial lesions and have shown to be superior to freehand biopsy procedures in terms of morbidity, mortality, and diagnostic yield.[7]

In this study, we are presenting a series of consecutive patients operated for stereotactic brain biopsy at Baghdad Neurosurgical Teaching Hospital (the major neurosurgical referral center in Iraq).

 Materials and Methods



This was a retrospective cross-sectional study conducted on patients who had undergone an image-guided stereotactic intracranial biopsy procedure using the Leksell (Elekta, Atlanta, GA, USA) frame and ELECTA software program (Winston-Salem, North Carolina, USA).

Patient population

The study group comprised of 116 patients who had undergone the biopsy procedure performed by an experienced neurosurgeon at the Neurosurgical Teaching Hospital, Baghdad, a tertiary center in Iraq, from September 1, 2010 until 2016. The data were prospectively collected but reviewed in a retrospective manner. Informed patient consent was obtained prior to the procedure from all patients or their legal representatives.

Patient and preoperative characteristics features, such as age, gender, duration of hospital stay, postoperative complications, and biopsy-related death were retrospectively collected from case notes. The following medical conditions were included for statistical analysis: underlying systemic diseases such as diabetes, hypertension, and asthma; previous extracranial malignancy and bleeding tendency. The site of the lesion was obtained from preoperative CT imaging. Information about events associated with the operation, such as total operating time, biopsy method used, and number of biopsies were extracted from the operation report. The diagnosis was obtained from the pathological report, from which the diagnostic yield was determined.

Surgical technique

The frame was applied in the operating room under sterile conditions. The frame was positioned with the patient sitting up facing the surgeon using cotton gauzes as spaces to adjust the vertical height of the frame and intravenous access was obtained. The surgeon started to fix the frame by asking the patient to close his eyes. Pins/screws were inserted on opposite sites and tightened by finger, and then the pin wrenches were used to tighten the pins on the diagonal. Tightening was performed on the diagonal with thumb finger and index grip to avoid over-tightening the screws. Contrast-enhanced CT scans were used to establish the stereotactic coordinates. After that the patient was transferred to the operative room, most of the patients were performed under general anesthesia with endotracheal intubation and some others under local anesthesia because they were unfit for general anesthesia. The patient was positioned in supine position. The (X, Y, Z) axis was calculated from CT scan images, and the system was adjusted according to the result of (X, Y, Z) axis. In general, three sequential biopsies were taken routinely at the suggested target. Biopsies were performed when the patient was normotensive. Backlund’s spiral needle and side-cutting (Sedan) needle were used to perform biopsies in solid lesions. Side-cutting needle was only preferred when biopsy could not be performed with a spiral needle. The procedure time that was measured from the skin incision to suturing, Intraoperative freeze-sectioning of the sample tissue was not performed. CT scan was performed postoperatively only for patients who develop neurological deficits or deteriorated consciousness.

Statistical analysis

Statistical analysis was performed using statistical program. Proportions were compared with Chi-square and Fisher’s exact test. P values <0.05 were considered statistically significant.

 Results



A total of 116 patients who underwent a frame-based stereotactic biopsy using the Leksell frame system were identified.

The mean ± standard deviation (SD) age of the patients was 44.4 ± 19.35 years ranging from 7 to 74 years. Pediatric patients were 16 (13.8%) of the total patients, 50 of the patients were males (43%), and 66 were females (57%). All the patients underwent a cranial CT scan, whereas a cranial MRI was performed in 100, as 16 patients were with brain abscess and needed urgent intervention, so we did the procedure with CT scan.

Most frequent presenting complaints were those of raised intracranial pressure (headache and/or vomiting) in 54 patients (46.5%) followed by focal neurological deficits in 34 patients (29.3%), seizure in 16 patients (13.7%), impaired level of consciousness in eight patients (7%), and gait disturbance in four patients (3.5%).

The localizations of the lesions were 66 (56.9%) patients had lobar lesions [14 frontal (12.1%), 30 parietal (25.9%), two temporal (1.7%), and four occipital (3.4%)], 40 (34.5%) patients had deep-seated lesions [16 of the patients corpus callosum (13.8%), 14 thalamus (12.1%), and 10 basal ganglia (8.6%)], and 10 of the patients had multiple lesions (8.6%).

Diagnosis

The sample obtained by the procedure was diagnostic in 114 (98.3%) patients. The diagnosis was not clear in two (1.7%) patients; however, a decision regarding the treatment strategy was possible based on clinical information and laboratory investigation. No statistical significance was found between the diagnosis and age, gender the lesion locations, and laterality of the lesions.

Radiological demonstrations relating to mass effect, edema, consistency of the lesion (cystic or solid), contrast enhancement, and heterogeneous or homogenous lesional components were not predictive issues for the development of complications showed in [Table 1] and [Table 2].{Table 1}{Table 2}

Histopathological result

Of all the cases in this study, there is no correlation between the types of tumor whether benign 4 (3.4%) or malignant 4 (3.4%) in development of complications. This is displayed in [Table 3].{Table 3}

Complications

Overall, 10 patients (8.6%) developed complications associated with the stereotactic biopsy. Morbidity rate was 5.2% (six of the patients). Characteristics and consequences of the complications detected in this study are summarized in [Table 4].{Table 4}

 Discussion



Although advances in the modern imaging techniques offer early detection of the brain lesions, they fail to give a precise histopathological diagnosis, which is essential in the planning of a rational treatment strategy. Tumors suggesting a benign pathology in radiological examination might end-up with a malignant histopathological diagnosis, or radiologically malignant tumors might turn out to be benign lesions histopathologically.[8]

Iraq is a developing country; there had been an indefinite knowledge about stereotactic technique; it began as simple trails in Iraq in 20th century and proceeded after first deep-brain stimulation surgery in the hospital of neuroscience in Baghdad in 2007. Iraq needs evolution in stereotaxic surgery like any other country to get a biopsy with a best result, minimum complications, and shorter duration. It is felt important to review the outcome of a series of patients who underwent this procedure in our neurosurgical practice.

Diagnostic yield

The diagnostic yield is defined as determining the precise pathology and, in the case of a tumor, precise tumor type and grade. The size and the number of biopsies are limited in the biopsy of brain lesion (SBB) procedure and may not be representative of the whole lesion. The diagnostic yield of SBB ranges from 80% to 96.7% in the literatures.[2],[9] SBB has a higher diagnostic rate in homogenous lesions, but the accuracy is lesser in heterogeneously enhanced lesions. A number of methods have been promoted to increase the accuracy of the SBB such as targeting multiple regions of the lesion, suspending the localization scan after the administration of contrast medium to improve resolution and target selection, using intraoperative cytological examinations or frozen section, utilizing modern histopathological techniques (e.g., immunohistochemistry), and using positron emission tomography (PET) or magnetic resonance (MR)-spectroscopy techniques for stereotactic biopsy.[8],[9]

In our study, the diagnostic yield was 98.3%; this lies within the range of yield reported by other authors 99.3%,[10] 94%,[11] 90.6%,[12] 89.8%,[13] and 83.6%.[14] These recent series do not mention pathologic confirmation.

Patient demographics and lesion characteristics

In patients older than 3 years of age, stereotactic biopsy has been reported to be a safe procedure as long as the frame screws are fixed wisely.[15] The youngest patient in our sample was 7 years old, who underwent biopsy with general anesthesia. From the above, we beleive that any age can undergo stereotactic brain biopsy, and there is no age limit for stereotaxic biopsy procedure because it is used for obtaining biopsies for different intracranial lesions.

Clinical and diagnostic variables

In our study, most frequent presenting complaint was features of raised intracranial pressure (ICP) (46.5%), focal neurological deficit was (29.3%), whereas in Ersahin et al.,[16] most frequent presenting complaint was weakness in lower and/or upper extremities (30.3%) followed by seizure (22.4%), and headache (19.3%).

Most of the surgeons carry out stereotactic biopsy with local anesthesia.[17],[18] Except for 28 patients (24.1%), all our procedures (75.9%) were performed under general anesthesia as against 85.8% reported by Alkhani et al.[19]. However, in the last 2 years of the study, local anesthesia became the most commonly used type of anesthesia, unless the patient could not tolerate the procedure under local anesthesia.

Regarding the type of needle, we used side-opening (Sedan) needle in 81% of cases and Backlund’s needle in 19%; in Kim’s study,[9] using Backlund’s spiral needle instead of Sedan’s side-hole cutting needle was very helpful in obtaining adequate tissue from the mass lesion with a hard consistency such as chondrosarcoma and in piercing the cystic lesion such as neurocysticercosis. Regardless of the texture, however, the aspiration of a tough-walled cyst is very difficult, because the cyst wall is rather compressed rather than pierced by the biopsy needle.

Complications

In our study, the complications rate was 8.6%. The most frequent complications were hemorrhage occurred in 5.2% and infection occurred in 1.7% with abscess collection in a case of congenital heart disease. CT scan was selectively done only in those cases with suspected bleeding or deterioration in patient condition. However, a cranial CT may be required when a bleeding is suspected during the procedure or to verify the target direction.[9] For example, Kim et al.[9] have routinely used CT scans for the determination of asymptomatic bleeding after biopsy.

Clinical variables

Variables that have been assessed for a possible association with the increased risk of operative complications include comorbid conditions such as hypertension.[20],[21],[22] In our patients with uncontrolled hypertension, diabetes, or other comorbid conditions, these conditions were first addressed to achieve adequate control, then the biopsy was performed. Only two patients (1.7%) with underlying malignancy developed complication; however, there was no statistical significance between underlying malignancy and the complication rate.

Radiological variables

Radiological findings such as lesion enhancement, mass effect, cystic lesion, and edema were not associated with a higher tendency for complications in our series. The complications occurred with mass effect (3.5%) and with cystic lesion (1.7%). Similar results were observed in the series by Grossman et al.,[21] Woodworth et al.,[23] and Chen et al.[12]

Perioperative predictors

Sedan side-cutting needle and Backlund’s spiral needle were used as the biopsy instruments to provide more voluminous tissue samples as compared to forceps. Although the rate is little higher with the use of Bucklund’s (9.1%) versus (8.5%) Sedan side-cutting needle, there was no statistical significance between needle type and the complication rate; however, the side-cutting needles tend to have higher incidence of symptomatic hemorrhage, which may be related to the increased sample size or the tearing nature as the needle turns within the tumor tissue.

The operating time for the frame-based technique in our series was less (mean ± SD, 38.3 ± 30.7 min) in comparison to Dammers et al.[24] (mean ± SD, 149 ± 32 min). A possible explanation for the shorter procedure time is that we measure only the time from skin incision to suturing; ignoring the time for frame placement in the operation theater, after which the patient is transported to the radiology department for imaging and transferred back to the operation theatre to complete the biopsy procedure.

Hospital duration post-stereotactic procedure in our series was less (mean 2.3 days, range from 1 to 7 days) in comparison to craniotomy and resection in Jackson et al.[2] (mean 4 days, range from 3 to 20 days). Complications that required additional surgery caused an increase in length of hospital stay.

Mortality and morbidity

Complication and definitive diagnostic rates vary in studies conducted so far. It is shown that the good results of SB, meaning low levels of complication rate together with high levels of conclusive diagnostic rates, is in direct correlation with surgical technique, experience of the neuropathologist and the surgeon.[9],[19],[21],[22],[25] Comparison of our series with the results of other large series was shown in [Table 5].{Table 5}

The relatively higher mortality rate we saw might reflect our definition of a biopsy-related death as death within 30 days postoperatively. In some previous reports, the time span has been only up to 7[9],[21] or 14 days,[23] in most it is not clear what definition is used. Surgeon experience was not able to avoid any of the major complications, nondiagnoses, or misdiagnoses; it is clear that every new case should be managed individually and precisely.

Despite the limited number of patients, our data suggest that frame-based stereotactic brain biopsy is a relatively safe and efficacious method in the diagnosis of intracranial lesions with a high rate of diagnostic yield and with acceptable complication rates (which are infrequent but can be disastrous). Operative risk is a function of several independent variables, including lesion properties (location, histology), preoperative medical diseases, and operative technique. This analysis suggests that the morbidity of stereotactic brain biopsy may be minimized by risk factor modification.

 Conclusions



Our findings support that frame-based stereotactic biopsy is a relatively safe and valuable technique that allows the neurosurgeon to obtain tissue samples for histopathological diagnosis of intracranial mass lesions in almost any region.[36]

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1Ostertag CB, Mennel HD, Kiessling M. Stereotactic biopsy of brain tumors. Surg Neurol 1980;14:275-83.
2Jackson RJ, Fuller GN, Abi-Said D, Lang FF, Gokaslan ZL, Shi WM. Limitations of stereotactic biopsy in the initial management of gliomas. Neuro-oncol 2001;3:193-200.
3Gildenberg PL. Stereotactic versus stereotaxic. Neurosurgery 1993;32:965-6.
4Alker G, Kelly PJ. An overview of CT based stereotactic systems for the localization of intracranial lesions. Comput Radiol 1984;8:193-6.
5Kollias S, Bernays R, Marugg R, Romanowski B, Yonekawa Y, Valavanis A. Target definition and trajectory optimization for interactive MR-guided biopsies of brain tumors in an open configuration MRI system. JMRI 1998;8:143-59.
6Kondziolka D, Duma CM, Lunsford LD. Factors that enhance the likelihood of successful stereotactic treatment of brain abscesses. Acta Neurochir (Wien) 1994;127:85-90.
7Wen DY, Hall WA, Miller DA, Seljeskog EL, Maxwell RE. Targeted brain biopsy: A comparison of freehand computed tomography-guided and stereotactic techniques. Neurosurgery 1993;32:407-12.
8Plunkett R, Allison RR, Grand W. Stereotactic neurosurgical biopsy is an underutilized modality. Neurosurg Rev 1999;22:117-20.
9Kim JE, Kim DG, Paek SH, Jung HW. Stereotactic biopsy for intracranial lesions: Reliability and its impact on the planning of treatment. Acta Neurochir (Wien) 2003;145:547-55.
10Shooman D, Belli A, Grundy PL. Image-guided frameless stereotactic biopsy without intraoperative neuropathological examination. J Neurosurg 2010;113:170-8.
11Owen CM, Linskey ME. Frame-based stereotaxy in a frameless era: Current capabilities, relative role, and the positive and negative predictive values of blood through the needle. J Neurooncol 2009;93:139-49.
12Chen CC, Hsu PW, Erich Wu TW, Lee ST, Chang CN, Wei KC et al. Stereotactic brain biopsy: Single center retrospective analysis of complications. Clin Neurol Neurosurg 2009;111:835-9.
13Air EL, Leach JL, Warnick RE, McPherson CM. Comparing the risks of frameless stereotactic biopsy in eloquent and noneloquent regions of the brain: A retrospective review of 284 cases. J Neurosurg 2009;111:820-4.
14Teixeira MJ, Fonoff ET, Mandel M, Alves HL, Rosemberg S. Stereotactic biopsies of brain lesions. Arq Neuropsiquiatr 2009;67:74-7.
15Can S, Turkmenoglu O, Tanik C, Uysal E, Ozoner B, Kaldırımoglu S et al. Computerized tomography-guided stereotactic biopsy of intracranial lesions: Report of 500 consecutive cases. Turk Neurosurg 2016;27:1-6.
16Ersahin M, Karaaslan N, Gurbuz MS, Hakan T, Berkman MZ, Ekinci O et al. The safety and diagnostic value of frame-based and CT-guided stereotactic brain biopsy technique. Turk Neurosurg 2011;21:582-90.
17Dammers R, Schouten JW, Haitsma IK, Vincent AJ, Kros JM, Dirven CM. Towards improving the safety and diagnostic yield of stereotactic biopsy in a single centre. Acta Neurochir (Wien) 2010;152:1915-21.
18Heper AO, Erden E, Savas A, Ceyhan K, Erden I, Akyar S et al. An analysis of stereotactic biopsy of brain tumors and nonneoplastic lesions: A prospective clinicopathologic study. Surg Neurol 2005;2:S82-8.
19Alkhani AM, Ghosheh JM, Al-Otaibi F, Ghomraoui AH, Kanaan IN, Hassounah MI. Diagnostic yield of stereotactic brain biopsy. Neurosciences 2008;13:142-5.
20McGirt MJ, Woodworth GF, Coon AL, Frazier JM, Amundson E, Garonzik I. Independent predictors of morbidity after image-guided stereotactic brain biopsy: A risk assessment of 270 cases. J Neurosurg 2005;102:897-901.
21Grossman R, Sadetzki S, Spiegelmann R, Ram Z. Haemorrhagic complications and the incidence of asymptomatic bleeding associated with stereotactic brain biopsies. Acta Neurochir (Wien) 2005;147:627-31.
22Kongkham PN, Knifed E, Tamber MS, Bernstein M. Complications in 622 cases of frame-based stereotactic biopsy, a decreasing procedure. Can J Neurol Sci 2008;35:79-84.
23Woodworth GF, McGirt MJ, Samdani A, Garonzik I, Olivi A, Weingart JD. Frameless image-guided stereotactic brain biopsy procedure: Diagnostic yield, surgical morbidity, and comparison with the frame-based technique. J Neurosurg 2006;104:233-7.
24Dammers R, Haitsma IK, Schouten JW, Kros JM, Avezaat CJ, Vincent AJ. Safety and efficacy of frameless and frame-based intracranial biopsy techniques. Acta Neurochir (Wien) 2008;150:23-9.
25Tilgner J, Manfred H, Ostertag C, Benedikt V. Validation of intraoperative diagnosis using smear preparations from stereotactic brain biopsies: Intraoperative versus final diagnosis-influence of clinical factors. Neurosurgery 2005;56:257-65.
26Kaakaji W, Barnett GH, Bernhard D, Warbel A, Valaitis K, Stamp S. Clinical and economic consequences of early discharge of patients following supratentorial stereotactic brain biopsy. J Neurosurg 2001;94:892-8.
27Paleologos TS, Dorward NL, Wadley JP, Thomas DG. Clinical validation of true frameless stereotactic biopsy: Analysis of the first 125 consecutive cases. Neurosurgery 2001;49:830-7.
28Ulm AJ, Bova FJ, Friedman WA. Stereotactic biopsy aided by a computer graphics workstation: Experience with 200 consecutive cases. Surg Neurol 2001;56:366-71.
29Dorward NL, Paleologos TS, Alberti O, Thomas DG. The advantages of frameless stereotactic biopsy over frame-based biopsy. Br J Neurosurg 2002;16:110-8.
30Aker FV, Hakan T, Karadereler S, Erkan M. Accuracy and diagnostic yield of stereotactic biopsy in the diagnosis of brain masses: Comparison of results of biopsy and resected surgical specimens. Neuropathology 2005;25:207-13.
31Smith JS, Quiñones-Hinojosa A, Barbaro NM, McDermott MW. Frame-based stereotactic biopsy remains an important diagnostic tool with distinct advantages over frameless stereotactic biopsy. J Neurooncol 2005;73:173-9.
32Ferreira MP, Ferreira NP, Pereira Filho Ade A, Pereira Filho Gde A, Franciscatto AC. Stereotactic computed tomography-guided brain biopsy: Diagnostic yield based on a series of 170 patients. Surg Neurol 2006;65(S1):27-32.
33Shastri-Hurst N, Tsegaye M, Robson DK, Lowe JS, Macarthur DC. Stereotactic brain biopsy: An audit of sampling reliability in a clinical case series. Br J Neurosurg 2006;20:222-6.
34Landriel F, Hem S, Hasdeu S, Kitroser M, Peña L, Ajler P et al. Biopsia estereotáctica cerebral guiada tomográficamente análisis de una serie de 192 casos. Rev Argent Neuroc 2008;22:110-3.
35Kickingereder P, Willeit P, Simon T, Ruge M. Diagnostic value and safety of stereotactic biopsy for brainstem tumors: A systematic review and analysis of 1480 cases. Neurosurgery 2013;72:873-82.
36Hakan T, Aker FV. Evaluation of 126 consecutive cases of stereotactic procedures: Brain biopsy, diagnostic yield, accuracy, non-diagnostic results, hemorrhagic complications and follow up. Turk Neurosurg 2016;26:890-9.