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Intraoperative ultrasound for surgical resection of high-grade glioma and glioblastoma: a meta-analysis of 732 patients

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Abstract

Purpose

Here, we conducted a meta-analysis to explore the use of intraoperative ultrasound (iUS)-guided resection in patients diagnosed with high-grade glioma (HGG) or glioblastoma (GBM). Our aim was to determine whether iUS improves clinical outcomes compared to conventional neuronavigation (CNN).

Methods

Databases were searched until April 21, 2023 for randomized controlled trials (RCTs) and observational cohort studies that compared surgical outcomes for patients with HGG or GBM with the use of either iUS in addition to standard approach or CNN. The primary outcome was overall survival (OS). Secondary outcomes include volumetric extent of resection (EOR), gross total resection (GTR), and progression-free survival (PFS). Outcomes were analyzed by determining pooled relative risk ratios (RR), mean difference (MD), and standardized mean difference (SMD) using random-effects model.

Results

Of the initial 867 articles, only 7 articles specifically met the inclusion criteria (1 RCT and 6 retrospective cohorts). The analysis included 732 patients. Compared to CNN, the use of iUS was associated with higher OS (SMD = 0.26,95%CI=[0.12,0.39]) and GTR (RR = 2.02; 95% CI=[1.31,3.1]) for both HGG and GBM. There was no significant difference in PFS or EOR.

Conclusion

The use of iUS in surgical resections for HGG and GBM can improve OS and GTR compared to CNN, but it did not affect PFS. These results suggest that iUS reduces mortality associated with HGG and GBM but not the risk of recurrence. These results can provide valuable cost-effective interventions for neurosurgeons in HGG and GBM surgery.

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References

  1. Mahboob S, McPhillips R, Qiu Z et al (2016) Intraoperative ultrasound-guided resection of gliomas: a Meta-analysis and review of the literature. World Neurosurg 92:255–263

    Article  PubMed  Google Scholar 

  2. Incekara F, Smits M, Dirven L et al (2021) Intraoperative B-Mode Ultrasound guided surgery and the extent of Glioblastoma Resection: a Randomized Controlled Trial. Front Oncol 11:649797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Moiraghi A, Prada F, Delaidelli A et al (2020) Navigated intraoperative 2-Dimensional Ultrasound in High-Grade glioma surgery: impact on extent of resection and patient outcome. Oper Neurosurg (Hagerstown) 18(4):363–373

    Article  PubMed  Google Scholar 

  4. Della Pepa GM, Ius T, La Rocca G et al (2020) 5-Aminolevulinic acid and contrast-enhanced Ultrasound: the combination of the two techniques to optimize the extent of resection in Glioblastoma surgery. Neurosurgery 86(6):E529–E540

    Article  PubMed  Google Scholar 

  5. Stewart LA (2002) Chemotherapy in adult high-grade glioma: a systematic review and meta-analysis of individual patient data from 12 randomised trials. Lancet 359(9311):1011–1018

    Article  CAS  PubMed  Google Scholar 

  6. Ostrom QT, Cioffi G, Gittleman H et al (2019) CBTRUS Statistical Report: primary brain and other Central Nervous System tumors diagnosed in the United States in 2012–2016. Neuro Oncol 21(Supplement5):v1–v100

    Article  PubMed  PubMed Central  Google Scholar 

  7. Korja M, Raj R, Seppä K et al (2019) Glioblastoma survival is improving despite increasing incidence rates: a nationwide study between 2000 and 2013 in Finland. Neuro Oncol 21(3):370–379

    Article  PubMed  Google Scholar 

  8. Domino JS, Ormond DR, Germano IM, Sami M, Ryken TC, Olson JJ (2020) Cytoreductive surgery in the management of newly diagnosed glioblastoma in adults: a systematic review and evidence-based clinical practice guideline update. J Neurooncol 150(2):121–142

    Article  PubMed  Google Scholar 

  9. Brown TJ, Brennan MC, Li M et al (2016) Association of the extent of Resection with Survival in Glioblastoma: a systematic review and Meta-analysis. JAMA Oncol 2(11):1460–1469

    Article  PubMed  PubMed Central  Google Scholar 

  10. Trifiletti DM, Alonso C, Grover S, Fadul CE, Sheehan JP, Showalter TN (2017) Prognostic implications of extent of Resection in Glioblastoma: analysis from a large database. World Neurosurg 103:330–340

    Article  PubMed  Google Scholar 

  11. Delgado-López PD, Corrales-García EM (2016) Survival in glioblastoma: a review on the impact of treatment modalities. Clin Transl Oncol 18(11):1062–1071

    Article  PubMed  Google Scholar 

  12. Marenco-Hillembrand L, Wijesekera O, Suarez-Meade P et al (2020) Trends in glioblastoma: outcomes over time and type of intervention: a systematic evidence based analysis. J Neurooncol 147(2):297–307

    Article  PubMed  Google Scholar 

  13. Xiong Z, Luo C, Wang P et al (2022) The intraoperative utilization of Multimodalities could improve the prognosis of adult glioblastoma: a single-Center Observational Study. World Neurosurg 165:e532–e545

    Article  PubMed  Google Scholar 

  14. Barak T, Vetsa S, Nadar A et al (2021) Surgical strategies for older patients with glioblastoma. J Neurooncol 155(3):255–264

    Article  PubMed  PubMed Central  Google Scholar 

  15. Roder C, Bisdas S, Ebner FH et al (2014) Maximizing the extent of resection and survival benefit of patients in glioblastoma surgery: high-field iMRI versus conventional and 5-ALA-assisted surgery. Eur J Surg Oncol 40(3):297–304

    Article  CAS  PubMed  Google Scholar 

  16. Page MJ, McKenzie JE, Bossuyt PM et al (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 372:n71

    Article  PubMed  PubMed Central  Google Scholar 

  17. Cumpston M, Li T, Page MJ et al (2019) Updated guidance for trusted systematic reviews: a new edition of the Cochrane Handbook for Systematic Reviews of Interventions. Cochrane Database Syst Rev 10:ED000142

    PubMed  Google Scholar 

  18. Sterne JA, Hernán MA, Reeves BC et al (2016) ROBINS-I: a tool for assessing risk of bias in non-randomised studies of interventions. BMJ 355:i4919

    Article  PubMed  PubMed Central  Google Scholar 

  19. Sterne JAC, Savović J, Page MJ et al (2019) RoB 2: a revised tool for assessing risk of bias in randomised trials. BMJ 366:l4898

    Article  PubMed  Google Scholar 

  20. Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, Welch VA (2023) Cochrane Handbook for Systematic Reviews of Interventions version 6.3. Cochrane. Published Febryary 2022. Accessed July 24, http://www.training.cochrane.org/handbook

  21. Wilson DB (2023) Ph.D. (n.d.). Practical Meta-Analysis Effect Size Calculator [Online calculator]. Campbell Collaboration. Accessed June 15, https://www.campbellcollaboration.org/research-resources/effect-size-calculator.html

  22. DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188

    Article  CAS  PubMed  Google Scholar 

  23. Higgins JPT, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560

    Article  PubMed  PubMed Central  Google Scholar 

  24. Wang J, Liu X, Ba YM et al (2012) Effect of sonographically guided cerebral glioma surgery on survival time. J Ultrasound Med 31(5):757–762

    Article  ADS  PubMed  Google Scholar 

  25. Neidert MC, Hostettler IC, Burkhardt JK et al (2016) The influence of intraoperative resection control modalities on survival following gross total resection of glioblastoma. Neurosurg Rev 39(3):401–409

    Article  PubMed  Google Scholar 

  26. Moiyadi AV, Kannan S, Shetty P (2015) Navigated intraoperative ultrasound for resection of gliomas: predictive value, influence on resection and survival. Neurol India 63(5):727–735

    Article  PubMed  Google Scholar 

  27. Sæther CA, Torsteinsen M, Torp SH, Sundstrøm S, Unsgård G, Solheim O (2012) Did survival improve after the implementation of intraoperative neuronavigation and 3D ultrasound in glioblastoma surgery? A retrospective analysis of 192 primary operations. J Neurol Surg Cent Eur Neurosurg 73(2):73–78

    Article  Google Scholar 

  28. Jusue-Torres I, Lee J, Germanwala AV, Burns TC, Parney IF (2023) Effect of extent of resection on survival of patients with glioblastoma, IDH-wild-type, WHO grade 4 (WHO 2021): systematic review and meta-analysis. World Neurosurg 171:e524–e532

    Article  PubMed  Google Scholar 

  29. Karschnia P, Young JS, Dono A et al (2023) Prognostic validation of a new classification system for extent of resection in glioblastoma: a report of the RANO resect group. Neuro Oncol 25(5):940–954

    Article  CAS  PubMed  Google Scholar 

  30. Jenkinson MD, Barone DG, Bryant A et al (2018) Intraoperative imaging technology to maximise extent of resection for glioma. Cochrane Database Syst Rev 1:CD012788

    PubMed  Google Scholar 

  31. Pichardo-Rojas PS, Angulo-Lozano JC, Alvarez-Castro JA et al Intraoperative MRI-Guided Resection of Glioblastoma: A Meta-Analysis of 1,847 patients. World Neurosurg. Published online December 2023. https://doi.org/10.1016/j.wneu.2023.12.042

  32. Goel NJ, Bird CE, Hicks WH, Abdullah KG (2021) Economic implications of the modern treatment paradigm of glioblastoma: an analysis of global cost estimates and their utility for cost assessment. J Med Econ 24(1):1018–1024

    Article  PubMed  Google Scholar 

  33. Fountain DM, Bryant A, Barone DG et al (2021) Intraoperative imaging technology to maximise extent of resection for glioma: a network meta-analysis. Cochrane Database Syst Rev 1(1):CD013630

    PubMed  Google Scholar 

  34. Verdugo E, Puerto I, Medina MÁ (2022) An update on the molecular biology of glioblastoma, with clinical implications and progress in its treatment. Cancer Commun (Lond) 42(11):1083–1111

    Article  PubMed  Google Scholar 

  35. Brandes AA, Franceschi E, Tosoni A et al (2008) MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients. J Clin Oncol 26(13):2192–2197

    Article  PubMed  Google Scholar 

  36. Wick W, Gorlia T, Bendszus M et al (2017) Lomustine and Bevacizumab in progressive glioblastoma. N Engl J Med 377(20):1954–1963

    Article  CAS  PubMed  Google Scholar 

  37. Batchelor TT, Mulholland P, Neyns B et al (2013) Phase III randomized trial comparing the efficacy of cediranib as monotherapy, and in combination with lomustine, versus lomustine alone in patients with recurrent glioblastoma. J Clin Oncol 31(26):3212–3218

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Plaha P, Camp S, Cook J et al (2022) FUTURE-GB: functional and ultrasound-guided resection of glioblastoma - a two-stage randomised control trial. BMJ Open 12(11):e064823

    Article  PubMed  PubMed Central  Google Scholar 

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Authors

Contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by Pavel S. Pichardo-Rojas, Carlos Zarate, Julieta Arguellez-Hernández, Aldo Barrón-Lomelí, Roberto Sanchez-Velez, Amir Hjeala-Varas, and Ernesto Gutierrez-Herrera. The first draft of the manuscript was written by Pavel S. Pichardo-Rojas and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

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Correspondence to Pavel S. Pichardo-Rojas.

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Pichardo-Rojas, P.S., Zarate, C., Arguelles-Hernández, J. et al. Intraoperative ultrasound for surgical resection of high-grade glioma and glioblastoma: a meta-analysis of 732 patients. Neurosurg Rev 47, 120 (2024). https://doi.org/10.1007/s10143-024-02354-8

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  • DOI: https://doi.org/10.1007/s10143-024-02354-8

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