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J Neurol Surg A Cent Eur Neurosurg 2024; 85(01): 048-061
DOI: 10.1055/a-1994-8033
Original Article

Diagnostic Accuracy and Field for Improvement of Frameless Stereotactic Brain Biopsy: A Focus on Nondiagnostic Cases

Zhexi He 
1   Department of Surgery, Division of Neurosurgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China
2   Department of Neurosurgery, Tuen Mun Hospital, Hong Kong, China
,
Cannon Xian Lun Zhu
1   Department of Surgery, Division of Neurosurgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China
,
Danny Tat Ming Chan
1   Department of Surgery, Division of Neurosurgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China
,
Tom Chi Yan Cheung
3   Department of Imaging and Interventional Radiology, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China
,
Ho-Keung Ng
4   Department of Anatomical & Cellular Pathology, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China
,
Vincent Chung Tong Mok
5   Department of Medicine and Therapeutics, Division of Neurology, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China
,
Wai Sang Poon
1   Department of Surgery, Division of Neurosurgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, China
› Author Affiliations Funding None.
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Abstract

Background The diagnostic accuracy of frameless stereotactic brain biopsy has been reported, but there is limited literature focusing on the reasons for nondiagnostic cases. In this study, we evaluate the diagnostic accuracy of frameless stereotactic brain biopsy, compare it with the current international standard, and review the field for improvement.

Methods This is a retrospective analysis of consecutive, prospectively collected frameless stereotactic brain biopsies from 2007 to 2020. We evaluated the diagnostic accuracy of the frameless stereotactic brain biopsies using defined criteria. The biopsy result was classified as conclusive, inconclusive, or negative, based on the pathologic, radiologic, and clinical diagnosis concordance. For inconclusive or negative results, we further evaluated the preoperative planning and postoperative imaging to review the errors. A literature review for the diagnostic accuracy of frameless stereotactic biopsy was performed for the validity of our results.

Results There were 106 patients with 109 biopsies performed from 2007 to 2020. The conclusive diagnosis was reached in 103 (94.5%) procedures. An inconclusive diagnosis was noted in four (3.7%) procedures and the biopsy was negative in two (1.9%) procedures. Symptomatic hemorrhage occurred in one patient (0.9%). There was no mortality in our series. Registration error (RE) and inaccurate targeting occurred in three trigonal lesions (2.8%), sampling of the nonrepresentative part of the lesion occurred in two cases (1.8%), and one biopsy (0.9%) for lymphoma was negative due to steroid treatment. The literature review suggested that our diagnostic accuracy was comparable with the published literature.

Conclusion The frameless stereotactic biopsy is a safe procedure with high diagnostic accuracy only if meticulous preoperative planning and careful intraoperative registration is performed. The common pitfalls precluding a conclusive diagnosis are RE and biopsies at nonrepresentative sites.

Keywords

frameless stereotaxy - histology - image-guided surgery - intracranial - neuronavigation

Disclaimer

The study result was presented in the oral format at the Annual Scientific Meeting of the Hong Kong Neurosurgical Society on December 18, 2020, by Dr. He Zhexi and in video format at the 7th World Federation of Neurosurgical Societies (WFNS) Foundation Asian Congress of Neurological Surgeons (ACNS) Winter Web Seminar on February 20, 2021, by Dr. He Zhexi.


A preprint version of the older version of this manuscript is available on Research Square with DOI:10.21203/rs.3.rs-854266/v1 and was cited in the manuscript as Reference 4. The current manuscript included the latest publications in the literature review and updated the discussion.


Availability of Data and Material

The data that support the findings of this study are available upon request from the corresponding author, under the regulations of the Joint Chinese University of Hong Kong – New Territories East Cluster Clinical Research Ethics Committee.


Ethical Approval

This research was conducted ethically in accordance with the World Medical Association Declaration of Helsinki. The study protocol was reviewed and approved by the Joint Chinese University of Hong Kong – New Territories East Cluster Clinical Research Ethics Committee (CREC Ref. No. 2021.354).


Consent to Participate

The study protocol is reviewed and approved by the Joint Chinese University of Hong Kong – New Territories East Cluster Clinical Research Ethics Committee (CREC Ref. No. 2021.354) with the patient consent waived as this research is based on secondary analysis of available data with no additional risk to patients. There is no patient-identifiable information contained in this manuscript.




Publication History

Received: 20 June 2022

Accepted: 05 December 2022

Accepted Manuscript online:
08 December 2022

Article published online:
11 May 2023

© 2023. Thieme. All rights reserved.

Georg Thieme Verlag KG
Rüdigerstraße 14, 70469 Stuttgart, Germany

 

  • References

  • 1 Dhawan S, He Y, Bartek Jr J, Alattar AA, Chen CC. Comparison of frame-based versus frameless intracranial stereotactic biopsy: systematic review and meta-analysis. World Neurosurg 2019; 127: 607-616.e4
    CrossrefPubMedGoogle Scholar
  • 2 Woodworth 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 (02) 233-237
    CrossrefPubMedGoogle Scholar
  • 3 Yuen J, Zhu CX, Chan DT. et al. A sequential comparison on the risk of haemorrhage with different sizes of biopsy needles for stereotactic brain biopsy. Stereotact Funct Neurosurg 2014; 92 (03) 160-169
    CrossrefPubMedGoogle Scholar
  • 4 He Z, Zhu XL, Chan TMD. et al. The diagnostic accuracy and era for improvement for frameless stereotactic brain biopsy: a series of 109 procedures and a systemic review. 2021; (e-pub ahead of print) DOI: 10.21203/rs.3.rs-854266/v1.
    CrossrefPubMedGoogle Scholar
  • 5 Agha RA, Fowler AJ, Rajmohan S, Barai I, Orgill DP. PROCESS Group. Preferred reporting of case series in surgery; the PROCESS guidelines. Int J Surg 2016; 36 (Pt A): 319-323
    CrossrefPubMedGoogle Scholar
  • 6 Krieger MD, Chandrasoma PT, Zee CS, Apuzzo ML. Role of stereotactic biopsy in the diagnosis and management of brain tumors. Semin Surg Oncol 1998; 14 (01) 13-25
    CrossrefPubMedGoogle Scholar
  • 7 Ringel F, Ingerl D, Ott S, Meyer B. VarioGuide: a new frameless image-guided stereotactic system: accuracy study and clinical assessment. Neurosurgery 2009; 64(5, Suppl 2):365–371, discussion 371–373
    PubMedGoogle Scholar
  • 8 Medical Research Council. Aids to Examination of the Peripheral Nervous System. Memorandum No. 45. Superseding War Memorandum No. 7. London: Her Majesty's Stationery Office; 1976
    Google Scholar
  • 9 Kubovsky S, Khriesh A, Moscovici S, Paldor I. Fusion of preoperative and postoperative imaging may predict the diagnostic yield of stereotactic needle brain biopsies. World Neurosurg 2022; 157: e441-e447
    CrossrefPubMedGoogle Scholar
  • 10 Mallereau CH, Chibbaro S, Ganau M. et al. Pushing the boundaries of accuracy and reliability during stereotactic procedures: a prospective study on 526 biopsies comparing the frameless robotic and image-guided surgery systems. J Clin Neurosci 2022; 95: 203-212
    CrossrefPubMedGoogle Scholar
  • 11 Ungar L, Nachum O, Zibly Z. et al. Comparison of frame-based versus frameless image-guided intracranial stereotactic brain biopsy: a retrospective analysis of safety and efficacy. World Neurosurg 2022; 164: e1-e7
    CrossrefPubMedGoogle Scholar
  • 12 Giamouriadis A, Perera D, Safdar A. et al. Safety and accuracy of frameless electromagnetic-navigated (AXIEM™)-guided brain lesion biopsies: a large single-unit study. Acta Neurochir (Wien) 2019; 161 (12) 2587-2593
    CrossrefPubMedGoogle Scholar
  • 13 Sciortino T, Fernandes B, Conti Nibali M. et al. Frameless stereotactic biopsy for precision neurosurgery: diagnostic value, safety, and accuracy. Acta Neurochir (Wien) 2019; 161 (05) 967-974
    CrossrefPubMedGoogle Scholar
  • 14 Mader MM, Rotermund R, Martens T, Westphal M, Matschke J, Abboud T. The role of frameless stereotactic biopsy in contemporary neuro-oncology: molecular specifications and diagnostic yield in biopsied glioma patients. J Neurooncol 2019; 141 (01) 183-194
    CrossrefPubMedGoogle Scholar
  • 15 Kellermann SG, Hamisch CA, Rueß D. et al. Stereotactic biopsy in elderly patients: risk assessment and impact on treatment decision. J Neurooncol 2017; 134 (02) 303-307
    CrossrefPubMedGoogle Scholar
  • 16 Verploegh IS, Volovici V, Haitsma IK. et al. Contemporary frameless intracranial biopsy techniques: might variation in safety and efficacy be expected?. Acta Neurochir (Wien) 2015; 157 (11) 2011-2016 , discussion 2016
    CrossrefPubMedGoogle Scholar
  • 17 Lu Y, Yeung C, Radmanesh A, Wiemann R, Black PM, Golby AJ. Comparative effectiveness of frame-based, frameless, and intraoperative magnetic resonance imaging-guided brain biopsy techniques. World Neurosurg 2015; 83 (03) 261-268
    CrossrefPubMedGoogle Scholar
  • 18 Khatab S, Spliet W, Woerdeman PA. Frameless image-guided stereotactic brain biopsies: emphasis on diagnostic yield. Acta Neurochir (Wien) 2014; 156 (08) 1441-1450
    CrossrefPubMedGoogle Scholar
  • 19 Air EL, Warnick RE, McPherson CM. Management strategies after nondiagnostic results with frameless stereotactic needle biopsy: retrospective review of 28 patients. Surg Neurol Int 2012; 3 (Suppl. 04) S315-S319
    PubMedGoogle Scholar
  • 20 Harrisson SE, Shooman D, Grundy PL. A prospective study of the safety and efficacy of frameless, pinless electromagnetic image-guided biopsy of cerebral lesions. Neurosurgery 2012; 70(1, Suppl Operative):29–33, discussion 33
    PubMedGoogle Scholar
  • 21 Frati A, Pichierri A, Bastianello S. et al. Frameless stereotactic cerebral biopsy: our experience in 296 cases. Stereotact Funct Neurosurg 2011; 89 (04) 234-245
    CrossrefPubMedGoogle Scholar
  • 22 Æbelø AM, Noer VR, Schulz MK, Kristensen BW, Pedersen CB, Poulsen FR. Frameless stereotactic neuronavigated biopsy: a retrospective study of morbidity, diagnostic yield, and the potential of fluorescence—a single-center clinical investigation. Clin Neurol Neurosurg 2019; 181: 28-32
    CrossrefPubMedGoogle Scholar
  • 23 Bradac O, Steklacova A, Nebrenska K, Vrana J, de Lacy P, Benes V. Accuracy of VarioGuide frameless stereotactic system against frame-based stereotaxy: prospective, randomized, single-center study. World Neurosurg 2017; 104: 831-840
    CrossrefPubMedGoogle Scholar
  • 24 Mansour MH. Incidence of miss targeting in frame-based stereotactic brain surgery. Egypt J Hosp Med 2018; 73 (09) 7454-7457
    CrossrefPubMedGoogle Scholar
  • 25 Giannini C, Dogan A, Salomão DR. CNS lymphoma: a practical diagnostic approach. J Neuropathol Exp Neurol 2014; 73 (06) 478-494
    CrossrefPubMedGoogle Scholar
  • 26 Deckert M, Engert A, Brück W. et al. Modern concepts in the biology, diagnosis, differential diagnosis and treatment of primary central nervous system lymphoma. Leukemia 2011; 25 (12) 1797-1807
    CrossrefPubMedGoogle Scholar
  • 27 Birski M, Furtak J, Krystkiewicz K. et al. Endoscopic versus stereotactic biopsies of intracranial lesions involving the ventricles. Neurosurg Rev 2021; 44 (03) 1721-1727
    CrossrefPubMedGoogle Scholar
  • 28 Lunsford LD, Niranjan A, Khan AA, Kondziolka D. Establishing a benchmark for complications using frame-based stereotactic surgery. Stereotact Funct Neurosurg 2008; 86 (05) 278-287
    CrossrefPubMedGoogle Scholar
  • 29 Lee J, Huang Z, Lee S. Accurate stereotaxic localization using computerized tomography with geometric correction. Biomed Eng Appl Basis Commun 2002; 14 (05) 189-196
    CrossrefPubMedGoogle Scholar
  • 30 Atsumi H, Matsumae M. Fusing of preoperative magnetic resonance and intraoperative O-arm images in deep brain stimulation enhance intuitive surgical planning and increase accuracy of lead placement. Neurol Med Chir (Tokyo) 2021; 61 (05) 341-346
    CrossrefPubMedGoogle Scholar
  • 31 Sharma M, Rhiew R, Deogaonkar M, Rezai A, Boulis N. Accuracy and precision of targeting using frameless stereotactic system in deep brain stimulator implantation surgery. Neurol India 2014; 62 (05) 503-509
    CrossrefPubMedGoogle Scholar
  • 32 Eigenbrod S, Trabold R, Brucker D. et al. Molecular stereotactic biopsy technique improves diagnostic accuracy and enables personalized treatment strategies in glioma patients. Acta Neurochir (Wien) 2014; 156 (08) 1427-1440
    CrossrefPubMedGoogle Scholar
  • 33 Eckel-Passow JE, Lachance DH, Molinaro AM. et al. Glioma groups based on 1p/19q, IDH, and TERT promoter mutations in tumors. N Engl J Med 2015; 372 (26) 2499-2508
    CrossrefPubMedGoogle Scholar
  • 34 Hegi ME, Diserens AC, Gorlia T. et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med 2005; 352 (10) 997-1003
    CrossrefPubMedGoogle Scholar
  • 35 Weise LM, Harter PN, Eibach S. et al. Confounding factors in diagnostics of MGMT promoter methylation status in glioblastomas in stereotactic biopsies. Stereotact Funct Neurosurg 2014; 92 (03) 129-139
    CrossrefPubMedGoogle Scholar
  • 36 Katzendobler S, Do A, Weller J. et al. Diagnostic yield and complication rate of stereotactic biopsies in precision medicine of gliomas. Front Neurol 2022; 13: 822362
    CrossrefPubMedGoogle Scholar
  • 37 Shankar GM, Francis JM, Rinne ML. et al. Rapid intraoperative molecular characterization of glioma. JAMA Oncol 2015; 1 (05) 662-667
    CrossrefPubMedGoogle Scholar
  • 38 Jackson RJ, Fuller GN, Abi-Said D. et al. Limitations of stereotactic biopsy in the initial management of gliomas. Neuro-oncol 2001; 3 (03) 193-200
    CrossrefPubMedGoogle Scholar
  • 39 Reithmeier T, Lopez WO, Doostkam S. et al. Intraindividual comparison of histopathological diagnosis obtained by stereotactic serial biopsy to open surgical resection specimen in patients with intracranial tumours. Clin Neurol Neurosurg 2013; 115 (10) 1955-1960
    CrossrefPubMedGoogle Scholar
  • 40 Kim 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 (07) 547-554 , discussion 554–555
    CrossrefPubMedGoogle Scholar
  • 41 Pasternak KA, Schwake M, Warneke N. et al. Evaluation of 311 contemporary cases of stereotactic biopsies in patients with neoplastic and non-neoplastic lesions-diagnostic yield and management of non-diagnostic cases. Neurosurg Rev 2021; 44 (05) 2597-2609
    CrossrefPubMedGoogle Scholar
  • 42 Riche M, Amelot A, Peyre M, Capelle L, Carpentier A, Mathon B. Complications after frame-based stereotactic brain biopsy: a systematic review. Neurosurg Rev 2021; 44 (01) 301-307
    CrossrefPubMedGoogle Scholar
  • 43 Kesserwan MA, Shakil H, Lannon M. et al. Frame-based versus frameless stereotactic brain biopsies: a systematic review and meta-analysis. Surg Neurol Int 2021; 12: 52
    CrossrefPubMedGoogle Scholar
  • 44 Riche M, Marijon P, Amelot A. et al. Severity, timeline, and management of complications after stereotactic brain biopsy. J Neurosurg 2021; 136 (03) 867-876
    CrossrefPubMedGoogle Scholar
  • 45 Mathon B, Marijon P, Riche M, Amelot A. PSL Brain-Biopsy Study Group. Letter to the Editor regarding “Hemorrhagic attitude in frameless and frame-based stereotactic biopsy for deep-seated primary central nervous system lymphomas in immunocompetent patients: a multicentric analysis of the last twenty years.”. World Neurosurg 2021; 152: 242-243
    CrossrefPubMedGoogle Scholar
  • 46 Grossman 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 (06) 627-631 , discussion 631
    CrossrefPubMedGoogle Scholar
  • 47 Shakal AAS, Mokbel EAH. Hemorrhage after stereotactic biopsy from intra-axial brain lesions: incidence and avoidance. J Neurol Surg A Cent Eur Neurosurg 2014; 75 (03) 177-182
    PubMedGoogle Scholar
  • 48 He Z, Wong ST, Yam KY. Newly-diagnosed, histologically-confirmed central nervous system tumours in a regional hospital in Hong Kong : an epidemiological study of a 21-year period. J Korean Neurosurg Soc 2020; 63 (01) 119-135
    CrossrefPubMedGoogle Scholar