Clinical Research
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Glioblastoma Multiforme'nin Tedavi Sonrası Psödoprogresyon ile Progresyon Ayrımı: Seri Perfüzyon MR Görüntülemelerde rCBV ve rCBF Değerlerinde Azalma Oranının Yararı

Year 2023, Volume: 2 Issue: 1, 15 - 21, 30.03.2023
https://doi.org/10.57221/izmirtip.1252962

Abstract

Amaç: Radyoterapi (RT) ve Temozolomid (TMZ) tedavisi alan glioblastoma multiforme (GBM) hastalarında erken psödoprogresyonun gerçek progresyondan ayrımında perfüzyon manyetik rezonans görüntülemenin (pMRG) değerinin değerlendirilmesi. Gereç ve Yöntemler: Radyoterapi ve Temozolomid tedavisi alan ve RT öncesi ve sonrası kranial pMRG tetkikleri olan 23 hasta değerlendirildi. Rölatif serebral kan hacmi (rCBV) ve rölatif serebral kan akımı (rCBF) seri MRG tetkikleri ile değerlendirilerek oranlandı. rCBV ve rCBF değerlerinde azalma oranı eşik değerinin belirlenmesi için receiver operating characteristic (ROC) analizi uygulandı. Bulgular: Dokuz (%39) hastada radyolojik progresyon bulguları saptandı. Bu hastalar takip MRG tetkikleri, klinik parametreler ve/veya patolojik bulgular ile birlikte değerlendirildiğinde altısı (%67) gerçek progresyon iken, üçü (%33) psödoprogresyon olarak saptandı. Psödoprogresyon grubunda rCBV ve rCBF azalma oranları sırasıyla 2.928 ve 2.510 olup Mann-Whitney U testine göre fark anlamlı idi (p=0.02). RT öncesi ve sonrası pMRG tetkiklerinde saptanan rCBV ve rCBF azalma oranı eşik değerleri (sırasıyla 1.73 ve 1.62) erken psödoprogresyonu ayırt etmede %100 duyarlı ve %100 özgül olarak bulundu. Sonuç: Radyoterapi ve Temozolomid tedavisi alan GBM hastalarında rCBV ve rCBF azalma oranı erken psödoprogresyonun güvenilir bir göstergesidir.

Supporting Institution

yok

Project Number

yok

References

  • Referans1.Yousem DM, Grossman RI. Neuroradiology: The Requisites. 3rd ed. Philadelphia: Mosby; 2010. p 58-104.
  • Referans2.Gunderson LL, Tepper JE. Clinical Radiation Oncology. 2nd ed. Philadelphia: Elsevier Churchill Livingstone; 2007. p 515-37.
  • Referans3.O'Reilly SM, Newlands ES, Glaser MG, Brampton M, Rice-Edwards JM, Illingworth RD et al. Temozolomide: a new oral cytotoxic chemotherapeutic agent with promising activity against primary brain tumours. Eur J Cancer. 1993;29:940-2.
  • Referans4.Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96.
  • Referans5.Brandes AA, Tosoni A, Spagnolli F, Frezza G, Leonardi M, Calbucci F et al. Disease progression or pseudoprogression after concomitant radio chemotherapy treatment: pitfalls in neurooncology. Neuro Oncol. 2008;10:361-7.
  • Referans6.Brandsma D, Stalpers L, Taal W, Sminia P, van den Bent MJ. Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol. 2008;9:453-61.
  • Referans7.Le Fèvre C, Constans JM, Chambrelant I, Antoni D, Bund C, Leroy-Freschini B et al. Pseudoprogression versus true progression in glioblastoma patients: A multiapproach literature review. Part 2 - Radiological features and metric markers. Crit Rev Oncol Hematol. 2021;159:103230.
  • Referans8.Sugahara T, Korogi Y, Tomiguchi S, Shigematsu Y, Ikushima I, Kira T et al. Posttherapeutic intraaxial brain tumor: the value of perfusion-sensitive contrast-enhanced MR imaging for differentiating tumor recurrence from nonneoplastic contrast-enhancing tissue. AJNR Am J Neuroradiol. 2000;21:901-9.
  • Referans9.Sidibe I, Tensaouti F, Roques M, Cohen-Jonathan-Moyal E, Laprie A. Pseudoprogression in glioblastoma: role of metabolic and functional MRI-systematic review. Biomedicines. 2022;10:285.
  • Referans10.Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28:1963-72.
  • Referans11.Athanassiou H, Synodinou M, Maragoudakis E, Paraskevaidis M, Verigos C, Misailidou D et al. Randomized phase II study of temozolomide and radiotherapy compared with radiotherapy alone in newly diagnosed glioblastoma multiforme. J Clin Oncol. 2005;23:2372–7.
  • Referans12.Tsakiris C, Siempis T, Alexiou GA, Zikou A, Sioka C, Voulgaris S et al. Differentiation between true tumor progression of glioblastoma and pseudoprogression using diffusion-weighted imaging and perfusion-weighted imaging: systematic review and meta-analysis. World Neurosurg. 2020;144:e100-e109.
  • Referans13.Hyare H, Thust S, Rees J. Advanced MRI Techniques in the Monitoring of Treatment of Gliomas. Curr Treat Options Neurol. 2017;19:11.
  • Referans14.Valk PE, Dillon WP. Radiation injury of the brain. AJNR Am J Neuroradiol. 1991;12:45-62. 15.Galldiks N, Kocher M, Langen KJ. Pseudoprogression after glioma therapy: an update. Expert Rev Neurother. 2017;17:1109-15.
  • Referans16.Rabin BM, Meyer JR, Berlin JW, Marymount MH, Palka PS, Russell EJ. Radiation-induced changes in the central nervous system and head and neck. Radiographics. 1996;16:1055-72.
  • Referans17.Taal W, Brandsma D, de Bruin HG, Bromberg JE, Swaak-Kragten AT, Smitt PA et al. Incidence of early pseudo-progression in a cohort of malignant glioma patients treated with chemoirradiation with temozolomide. J Clin Oncol. 2008;113:405-10.
  • Referans18.Gerstner ER, McNamara MB, Norden AD, Lafrankie D, Wen PY. Effect of adding temozolomide to radiation therapy on the incidence of pseudo-progression. J Neurooncol. 2009;94:97-101.
  • Referans19.de Wit MC, de Bruin HG, Eijkenboom W, Sillevis Smitt PA, van den Bent MJ. Immediate post-radiotherapy changes in malignant glioma can mimic tumor progression. Neurology. 2004;63:535–7.
  • Referans20.Gahramanov S, Varallyay C, Tyson RM, Lacy C, Fu R, Netto JP et al. Diagnosis of pseudoprogression using MRI perfusion in patients with glioblastoma multiforme may predict improved survival. CNS Oncol. 2014;3:389-400.
  • Referans21.Kerkhof M, Tans PL, Hagenbeek RE, Lycklama À Nijeholt GJ, Holla FK, Postma TJ, et al. Visual inspection of MR relative cerebral blood volume maps has limited value for distinguishing progression from pseudoprogression in glioblastoma multiforme patients. CNS Oncol. 2017;6:297-306.
  • Referans22.Clarke JL, Abrey LE, Karimi S, Lassman AB. Pseudoprogression (PsPr) after concurrent radiotherapy (RT) and temozolomide (TMZ) for newly diagnosed glioblastoma multiforme (GBM). Paper presented at: ASCO Annual meeting May 30–June 3, 2008, Chicago, IL, USA. J Clin Oncol. 2008:26(suppl; abstr 2025). doi: 10.1200/jco.2008.26.15_suppl.2025.
  • Referans23.Young RJ, Gupta A, Shah AD, Graber JJ, Chan TA, Zhang Z, et al. MRI perfusion in determining pseudoprogression in patients with glioblastoma. Clin Imaging. 2013;37:41-9.
  • Referans24.Thomas AA, Arevalo-Perez J, Kaley T, Lyo J, Peck KK, Shi W et al. Dynamic contrast enhanced T1 MRI perfusion differentiates pseudoprogression from recurrent glioblastoma. J Neurooncol. 2015;125:183-90.
  • Referans25.Bobek-Billewicz B, Stasik-Pres G, Majchrzak H, Zarudzki L. Differentiation between brain tumor recurrence and radiation injury using perfusion, diffusion-weighted imaging and MR spectroscopy. Folia Neuropathol. 2010;48:81-92.
  • Referans26.Heidemans-Hazelaar C, Verbeek AY, Oosterkamp Sr. HM, Van der Kallen B, Vecht CJ. Use of perfusion MR imaging for differentiation between tumor progression and pseudo-progression in recurrent glioblastoma multiforme. Paper presented at: ASCO Annual meeting June 04–08, 2010, Chicago, IL, USA. J Clin Oncol. 2010:28 (suppl; abstr 2026). doi: 10.1200/jco.2010.28.15_suppl.2026.
  • Referans27.Graber JJ, Young RJ, Gupta A. Magnetic resonance (MR) perfusion imaging to differentiate early progression from pseudoprogression following chemoradiotherapy for glioblastoma (GBM). Paper presented at: ASCO Annual meeting I June 03–07, 2011, Chicago, IL, USA. J Clin Oncol 2011:29 (suppl; abstr 2009). doi: 10.1200/jco.2011.29.15_suppl.2009.
  • Referans28.Kong DS, Kim ST, Kim EH, Lim DH, Kim WS, Suh YL, et al. Diagnostic dilemma of pseudoprogression in the treatment of newly diagnosed glioblastomas: the role of assessing relative cerebral blood volume and oxygen-6-methylguanine-DNA methyltransferase promoter methylation status. AJNR Am J Neuroradiol. 2011;32:382-7.
  • Referans29.Provanzale JM, Mukundan S, Barboriak DP. Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology. 2006;239:632-49.
  • Referans30.Gahramanov S, Raslan AM, Muldoon LL, Hamilton BE, Rooney WD, Varallyay CG et al. Potential for differentiation of pseudoprogression from true tumor progression with dynamic susceptibility-weighted contrast-enhanced magnetic resonance imaging using ferumoxytol vs. gadoteridol: a pilot study. Int Radiat Oncol Biol Phys. 2011;79:514-23.
  • Referans31.Tsien C, Galbán CJ, Chenevert TL, Johnson TD, Hamstra DA, Sundgren PC et al. Parametric response map as an imaging biomarker to distinguish progression from pseudoprogression in high-grade glioma. J Clin Oncol. 2010;28:2293-9.
  • Referans32.Boxerman JL, Ellingson BM, Jeyapalan S, Elinzano H, Harris RJ, Rogg JM et al. Longitudinal DSC-MRI for distinguishing tumor recurrence from pseudoprogression in patients with a high-grade Glioma. Am J Clin Oncol. 2017;40:228-34.

Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in rCBV and rCBF Values on Serial Perfusion MRIs

Year 2023, Volume: 2 Issue: 1, 15 - 21, 30.03.2023
https://doi.org/10.57221/izmirtip.1252962

Abstract

Aim: To assess the value of perfusion magnetic resonance imaging (pMRI) in the differentiation of early pseudoprogression from true progression in glioblastoma multiforme (GBM) patients taking Temozolomide (TMZ) with radiotherapy (RT) treatment. Materials and Methods: Pre-RT and post-RT cranial pMRI scans of 23 GBM patients treated with RT-TMZ were reviewed. Relative cerebral blood volume (rCBV) and relative cerebral blood flow (rCBF) of the residual enhancing lesions were measured on serial pMRI scans and proportioned. Receiver operating characteristic (ROC) analysis was performed to determine a threshold ratio of decrease in rCBV and rCBF. Results: There were nine patients (39%) with signs of radiological progression, of whom six (67%) had real progression and three (33%) had pseudoprogression based on follow-up MRI studies, clinical parameters and/or pathology. Ratio of decrease was 2.928 in rCBV and 2.510 in rCBF in the pseudoprogression group, which were significant according to Mann-Whitney U test (p=0.02). Cut-off ratio of decrease value of 1.73 for rCBV and 1.62 for rCBF between pre-RT and post-RT pMRI study, could differentiate the presence of early pseudoprogression with 100% sensitivity and 100% specificity.
Conclusion: Ratio of decrease in rCBV and rCBF is a reliable predictor of early pseudoprogression in GBM patients under RT-TMZ treatment.

Project Number

yok

References

  • Referans1.Yousem DM, Grossman RI. Neuroradiology: The Requisites. 3rd ed. Philadelphia: Mosby; 2010. p 58-104.
  • Referans2.Gunderson LL, Tepper JE. Clinical Radiation Oncology. 2nd ed. Philadelphia: Elsevier Churchill Livingstone; 2007. p 515-37.
  • Referans3.O'Reilly SM, Newlands ES, Glaser MG, Brampton M, Rice-Edwards JM, Illingworth RD et al. Temozolomide: a new oral cytotoxic chemotherapeutic agent with promising activity against primary brain tumours. Eur J Cancer. 1993;29:940-2.
  • Referans4.Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJ et al. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352:987–96.
  • Referans5.Brandes AA, Tosoni A, Spagnolli F, Frezza G, Leonardi M, Calbucci F et al. Disease progression or pseudoprogression after concomitant radio chemotherapy treatment: pitfalls in neurooncology. Neuro Oncol. 2008;10:361-7.
  • Referans6.Brandsma D, Stalpers L, Taal W, Sminia P, van den Bent MJ. Clinical features, mechanisms, and management of pseudoprogression in malignant gliomas. Lancet Oncol. 2008;9:453-61.
  • Referans7.Le Fèvre C, Constans JM, Chambrelant I, Antoni D, Bund C, Leroy-Freschini B et al. Pseudoprogression versus true progression in glioblastoma patients: A multiapproach literature review. Part 2 - Radiological features and metric markers. Crit Rev Oncol Hematol. 2021;159:103230.
  • Referans8.Sugahara T, Korogi Y, Tomiguchi S, Shigematsu Y, Ikushima I, Kira T et al. Posttherapeutic intraaxial brain tumor: the value of perfusion-sensitive contrast-enhanced MR imaging for differentiating tumor recurrence from nonneoplastic contrast-enhancing tissue. AJNR Am J Neuroradiol. 2000;21:901-9.
  • Referans9.Sidibe I, Tensaouti F, Roques M, Cohen-Jonathan-Moyal E, Laprie A. Pseudoprogression in glioblastoma: role of metabolic and functional MRI-systematic review. Biomedicines. 2022;10:285.
  • Referans10.Wen PY, Macdonald DR, Reardon DA, Cloughesy TF, Sorensen AG, Galanis E et al. Updated response assessment criteria for high-grade gliomas: response assessment in neuro-oncology working group. J Clin Oncol. 2010;28:1963-72.
  • Referans11.Athanassiou H, Synodinou M, Maragoudakis E, Paraskevaidis M, Verigos C, Misailidou D et al. Randomized phase II study of temozolomide and radiotherapy compared with radiotherapy alone in newly diagnosed glioblastoma multiforme. J Clin Oncol. 2005;23:2372–7.
  • Referans12.Tsakiris C, Siempis T, Alexiou GA, Zikou A, Sioka C, Voulgaris S et al. Differentiation between true tumor progression of glioblastoma and pseudoprogression using diffusion-weighted imaging and perfusion-weighted imaging: systematic review and meta-analysis. World Neurosurg. 2020;144:e100-e109.
  • Referans13.Hyare H, Thust S, Rees J. Advanced MRI Techniques in the Monitoring of Treatment of Gliomas. Curr Treat Options Neurol. 2017;19:11.
  • Referans14.Valk PE, Dillon WP. Radiation injury of the brain. AJNR Am J Neuroradiol. 1991;12:45-62. 15.Galldiks N, Kocher M, Langen KJ. Pseudoprogression after glioma therapy: an update. Expert Rev Neurother. 2017;17:1109-15.
  • Referans16.Rabin BM, Meyer JR, Berlin JW, Marymount MH, Palka PS, Russell EJ. Radiation-induced changes in the central nervous system and head and neck. Radiographics. 1996;16:1055-72.
  • Referans17.Taal W, Brandsma D, de Bruin HG, Bromberg JE, Swaak-Kragten AT, Smitt PA et al. Incidence of early pseudo-progression in a cohort of malignant glioma patients treated with chemoirradiation with temozolomide. J Clin Oncol. 2008;113:405-10.
  • Referans18.Gerstner ER, McNamara MB, Norden AD, Lafrankie D, Wen PY. Effect of adding temozolomide to radiation therapy on the incidence of pseudo-progression. J Neurooncol. 2009;94:97-101.
  • Referans19.de Wit MC, de Bruin HG, Eijkenboom W, Sillevis Smitt PA, van den Bent MJ. Immediate post-radiotherapy changes in malignant glioma can mimic tumor progression. Neurology. 2004;63:535–7.
  • Referans20.Gahramanov S, Varallyay C, Tyson RM, Lacy C, Fu R, Netto JP et al. Diagnosis of pseudoprogression using MRI perfusion in patients with glioblastoma multiforme may predict improved survival. CNS Oncol. 2014;3:389-400.
  • Referans21.Kerkhof M, Tans PL, Hagenbeek RE, Lycklama À Nijeholt GJ, Holla FK, Postma TJ, et al. Visual inspection of MR relative cerebral blood volume maps has limited value for distinguishing progression from pseudoprogression in glioblastoma multiforme patients. CNS Oncol. 2017;6:297-306.
  • Referans22.Clarke JL, Abrey LE, Karimi S, Lassman AB. Pseudoprogression (PsPr) after concurrent radiotherapy (RT) and temozolomide (TMZ) for newly diagnosed glioblastoma multiforme (GBM). Paper presented at: ASCO Annual meeting May 30–June 3, 2008, Chicago, IL, USA. J Clin Oncol. 2008:26(suppl; abstr 2025). doi: 10.1200/jco.2008.26.15_suppl.2025.
  • Referans23.Young RJ, Gupta A, Shah AD, Graber JJ, Chan TA, Zhang Z, et al. MRI perfusion in determining pseudoprogression in patients with glioblastoma. Clin Imaging. 2013;37:41-9.
  • Referans24.Thomas AA, Arevalo-Perez J, Kaley T, Lyo J, Peck KK, Shi W et al. Dynamic contrast enhanced T1 MRI perfusion differentiates pseudoprogression from recurrent glioblastoma. J Neurooncol. 2015;125:183-90.
  • Referans25.Bobek-Billewicz B, Stasik-Pres G, Majchrzak H, Zarudzki L. Differentiation between brain tumor recurrence and radiation injury using perfusion, diffusion-weighted imaging and MR spectroscopy. Folia Neuropathol. 2010;48:81-92.
  • Referans26.Heidemans-Hazelaar C, Verbeek AY, Oosterkamp Sr. HM, Van der Kallen B, Vecht CJ. Use of perfusion MR imaging for differentiation between tumor progression and pseudo-progression in recurrent glioblastoma multiforme. Paper presented at: ASCO Annual meeting June 04–08, 2010, Chicago, IL, USA. J Clin Oncol. 2010:28 (suppl; abstr 2026). doi: 10.1200/jco.2010.28.15_suppl.2026.
  • Referans27.Graber JJ, Young RJ, Gupta A. Magnetic resonance (MR) perfusion imaging to differentiate early progression from pseudoprogression following chemoradiotherapy for glioblastoma (GBM). Paper presented at: ASCO Annual meeting I June 03–07, 2011, Chicago, IL, USA. J Clin Oncol 2011:29 (suppl; abstr 2009). doi: 10.1200/jco.2011.29.15_suppl.2009.
  • Referans28.Kong DS, Kim ST, Kim EH, Lim DH, Kim WS, Suh YL, et al. Diagnostic dilemma of pseudoprogression in the treatment of newly diagnosed glioblastomas: the role of assessing relative cerebral blood volume and oxygen-6-methylguanine-DNA methyltransferase promoter methylation status. AJNR Am J Neuroradiol. 2011;32:382-7.
  • Referans29.Provanzale JM, Mukundan S, Barboriak DP. Diffusion-weighted and perfusion MR imaging for brain tumor characterization and assessment of treatment response. Radiology. 2006;239:632-49.
  • Referans30.Gahramanov S, Raslan AM, Muldoon LL, Hamilton BE, Rooney WD, Varallyay CG et al. Potential for differentiation of pseudoprogression from true tumor progression with dynamic susceptibility-weighted contrast-enhanced magnetic resonance imaging using ferumoxytol vs. gadoteridol: a pilot study. Int Radiat Oncol Biol Phys. 2011;79:514-23.
  • Referans31.Tsien C, Galbán CJ, Chenevert TL, Johnson TD, Hamstra DA, Sundgren PC et al. Parametric response map as an imaging biomarker to distinguish progression from pseudoprogression in high-grade glioma. J Clin Oncol. 2010;28:2293-9.
  • Referans32.Boxerman JL, Ellingson BM, Jeyapalan S, Elinzano H, Harris RJ, Rogg JM et al. Longitudinal DSC-MRI for distinguishing tumor recurrence from pseudoprogression in patients with a high-grade Glioma. Am J Clin Oncol. 2017;40:228-34.
There are 31 citations in total.

Details

Primary Language English
Subjects Clinical Sciences
Journal Section Research Articles
Authors

Olgun Şahin 0000-0003-0366-9220

Hilal Şahin 0000-0001-8726-8998

Mehmet Cem Çallı 0000-0002-4422-4212

Project Number yok
Publication Date March 30, 2023
Submission Date February 22, 2023
Published in Issue Year 2023 Volume: 2 Issue: 1

Cite

APA Şahin, O., Şahin, H., & Çallı, M. C. (2023). Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in rCBV and rCBF Values on Serial Perfusion MRIs. İzmir Tıp Fakültesi Dergisi, 2(1), 15-21. https://doi.org/10.57221/izmirtip.1252962
AMA Şahin O, Şahin H, Çallı MC. Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in rCBV and rCBF Values on Serial Perfusion MRIs. İzmir Tıp Fak. Derg. March 2023;2(1):15-21. doi:10.57221/izmirtip.1252962
Chicago Şahin, Olgun, Hilal Şahin, and Mehmet Cem Çallı. “Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in RCBV and RCBF Values on Serial Perfusion MRIs”. İzmir Tıp Fakültesi Dergisi 2, no. 1 (March 2023): 15-21. https://doi.org/10.57221/izmirtip.1252962.
EndNote Şahin O, Şahin H, Çallı MC (March 1, 2023) Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in rCBV and rCBF Values on Serial Perfusion MRIs. İzmir Tıp Fakültesi Dergisi 2 1 15–21.
IEEE O. Şahin, H. Şahin, and M. C. Çallı, “Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in rCBV and rCBF Values on Serial Perfusion MRIs”, İzmir Tıp Fak. Derg., vol. 2, no. 1, pp. 15–21, 2023, doi: 10.57221/izmirtip.1252962.
ISNAD Şahin, Olgun et al. “Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in RCBV and RCBF Values on Serial Perfusion MRIs”. İzmir Tıp Fakültesi Dergisi 2/1 (March 2023), 15-21. https://doi.org/10.57221/izmirtip.1252962.
JAMA Şahin O, Şahin H, Çallı MC. Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in rCBV and rCBF Values on Serial Perfusion MRIs. İzmir Tıp Fak. Derg. 2023;2:15–21.
MLA Şahin, Olgun et al. “Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in RCBV and RCBF Values on Serial Perfusion MRIs”. İzmir Tıp Fakültesi Dergisi, vol. 2, no. 1, 2023, pp. 15-21, doi:10.57221/izmirtip.1252962.
Vancouver Şahin O, Şahin H, Çallı MC. Distinction of Pseudoprogression and Progression in Glioblastoma Multiforme After Treatment: Utility of Ratio of Decrease in rCBV and rCBF Values on Serial Perfusion MRIs. İzmir Tıp Fak. Derg. 2023;2(1):15-21.