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Tumor Habitat Analysis Using Longitudinal Physiological MRI to Predict Tumor Recurrence After Stereotactic Radiosurgery for Brain Metastasis

  • Da Hyun Lee (Department of Radiology, Ajou University School of Medicine) ;
  • Ji Eun Park (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center) ;
  • NakYoung Kim (DYNAPEX LLC) ;
  • Seo Young Park (Department of Statistics and Data Science, Korea National Open University) ;
  • Young-Hoon Kim (Department of Neurosurgery, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Young Hyun Cho (Department of Neurosurgery, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Jeong Hoon Kim (Department of Neurosurgery, University of Ulsan College of Medicine, Asan Medical Center) ;
  • Ho Sung Kim (Department of Radiology and Research Institute of Radiology, University of Ulsan College of Medicine, Asan Medical Center)
  • 투고 : 2022.07.21
  • 심사 : 2022.12.11
  • 발행 : 2023.03.01

초록

Objective: It is difficult to predict the treatment response of tissue after stereotactic radiosurgery (SRS) because radiation necrosis (RN) and tumor recurrence can coexist. Our study aimed to predict tumor recurrence, including the recurrence site, after SRS of brain metastasis by performing a longitudinal tumor habitat analysis. Materials and Methods: Two consecutive multiparametric MRI examinations were performed for 83 adults (mean age, 59.0 years; range, 27-82 years; 44 male and 39 female) with 103 SRS-treated brain metastases. Tumor habitats based on contrast-enhanced T1- and T2-weighted images (structural habitats) and those based on the apparent diffusion coefficient (ADC) and cerebral blood volume (CBV) images (physiological habitats) were defined using k-means voxel-wise clustering. The reference standard was based on the pathology or Response Assessment in Neuro-Oncologycriteria for brain metastases (RANO-BM). The association between parameters of single-time or longitudinal tumor habitat and the time to recurrence and the site of recurrence were evaluated using the Cox proportional hazards regression analysis and Dice similarity coefficient, respectively. Results: The mean interval between the two MRI examinations was 99 days. The longitudinal analysis showed that an increase in the hypovascular cellular habitat (low ADC and low CBV) was associated with the risk of recurrence (hazard ratio [HR], 2.68; 95% confidence interval [CI], 1.46-4.91; P = 0.001). During the single-time analysis, a solid low-enhancing habitat (low T2 and low contrast-enhanced T1 signal) was associated with the risk of recurrence (HR, 1.54; 95% CI, 1.01-2.35; P = 0.045). A hypovascular cellular habitat was indicative of the future recurrence site (Dice similarity coefficient = 0.423). Conclusion: After SRS of brain metastases, an increased hypovascular cellular habitat observed using a longitudinal MRI analysis was associated with the risk of recurrence (i.e., treatment resistance) and was indicative of recurrence site. A tumor habitat analysis may help guide future treatments for patients with brain metastases.

키워드

과제정보

This research was supported by the Ministry of Health& Welfare, Republic of Korea (HI21C1161) and by a grant (2021IP0078) from the Asan Institute for Life Sciences, Asan Medical Center, Seoul, Korea.

참고문헌

  1. Le Rhun E, Guckenberger M, Smits M, Dummer R, Bachelot T, Sahm F, et al. EANO-ESMO clinical practice guidelines for diagnosis, treatment and follow-up of patients with brain metastasis from solid tumours. Ann Oncol 2021;32:1332-1347 https://doi.org/10.1016/j.annonc.2021.07.016
  2. Graber JJ, Cobbs CS, Olson JJ. Congress of neurological surgeons systematic review and evidence-based guidelines on the use of stereotactic radiosurgery in the treatment of adults with metastatic brain tumors. Neurosurgery 2019;84:E168-E170 https://doi.org/10.1093/neuros/nyy543
  3. Patel TR, McHugh BJ, Bi WL, Minja FJ, Knisely JP, Chiang VL. A comprehensive review of MR imaging changes following radiosurgery to 500 brain metastases. AJNR Am J Neuroradiol 2011;32:1885-1892 https://doi.org/10.3174/ajnr.A2668
  4. Chao ST, Ahluwalia MS, Barnett GH, Stevens GH, Murphy ES, Stockham AL, et al. Challenges with the diagnosis and treatment of cerebral radiation necrosis. Int J Radiat Oncol Biol Phys 2013;87:449-457 https://doi.org/10.1016/j.ijrobp.2013.05.015
  5. Kickingereder P, Dorn F, Blau T, Schmidt M, Kocher M, Galldiks N, et al. Differentiation of local tumor recurrence from radiation-induced changes after stereotactic radiosurgery for treatment of brain metastasis: case report and review of the literature. Radiat Oncol 2013;8:52
  6. Shah R, Vattoth S, Jacob R, Manzil FF, O'Malley JP, Borghei P, et al. Radiation necrosis in the brain: imaging features and differentiation from tumor recurrence. Radiographics 2012;32:1343-1359 https://doi.org/10.1148/rg.325125002
  7. Rahmathulla G, Marko NF, Weil RJ. Cerebral radiation necrosis: a review of the pathobiology, diagnosis and management considerations. J Clin Neurosci 2013;20:485-502 https://doi.org/10.1016/j.jocn.2012.09.011
  8. Murphy ES, Xie H, Merchant TE, Yu JS, Chao ST, Suh JH. Review of cranial radiotherapy-induced vasculopathy. J Neurooncol 2015;122:421-429 https://doi.org/10.1007/s11060-015-1732-2
  9. Knitter JR, Erly WK, Stea BD, Lemole GM, Germano IM, Doshi AH, et al. Interval change in diffusion and perfusion MRI parameters for the assessment of pseudoprogression in cerebral metastases treated with stereotactic radiation. AJR Am J Roentgenol 2018;211:168-175 https://doi.org/10.2214/AJR.17.18890
  10. Sawlani V, Davies N, Patel M, Flintham R, Fong C, Heyes G, et al. Evaluation of response to stereotactic radiosurgery in brain metastases using multiparametric magnetic resonance imaging and a review of the literature. Clin Oncol (R Coll Radiol) 2019;31:41-49 https://doi.org/10.1016/j.clon.2018.09.003
  11. Barajas RF, Chang JS, Sneed PK, Segal MR, McDermott MW, Cha S. Distinguishing recurrent intra-axial metastatic tumor from radiation necrosis following gamma knife radiosurgery using dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. AJNR Am J Neuroradiol 2009;30:367-372 https://doi.org/10.3174/ajnr.A1362
  12. Hoefnagels FW, Lagerwaard FJ, Sanchez E, Haasbeek CJ, Knol DL, Slotman BJ, et al. Radiological progression of cerebral metastases after radiosurgery: assessment of perfusion MRI for differentiating between necrosis and recurrence. J Neurol 2009;256:878-887 https://doi.org/10.1007/s00415-009-5034-5
  13. Mitsuya K, Nakasu Y, Horiguchi S, Harada H, Nishimura T, Bando E, et al. Perfusion weighted magnetic resonance imaging to distinguish the recurrence of metastatic brain tumors from radiation necrosis after stereotactic radiosurgery. J Neurooncol 2010;99:81-88 https://doi.org/10.1007/s11060-009-0106-z
  14. O'Connor JP, Rose CJ, Waterton JC, Carano RA, Parker GJ, Jackson A. Imaging intratumor heterogeneity: role in therapy response, resistance, and clinical outcome. Clin Cancer Res 2015;21:249-257 https://doi.org/10.1158/1078-0432.CCR-14-0990
  15. Dextraze K, Saha A, Kim D, Narang S, Lehrer M, Rao A, et al. Spatial habitats from multiparametric MR imaging are associated with signaling pathway activities and survival in glioblastoma. Oncotarget 2017;8:112992-113001 https://doi.org/10.18632/oncotarget.22947
  16. Lee DH, Park JE, Kim N, Park SY, Kim YH, Cho YH, et al. Tumor habitat analysis by magnetic resonance imaging distinguishes tumor progression from radiation necrosis in brain metastases after stereotactic radiosurgery. Eur Radiol 2022;32:497-507 https://doi.org/10.1007/s00330-021-08204-1
  17. Sakuramachi M, Igaki H, Ikemura M, Yamashita H, Okuma K, Sekiya N, et al. Detection of residual metastatic tumor in the brain following gamma knife radiosurgery using a single or a series of magnetic resonance imaging scans: an autopsy study. Oncol Lett 2017;14:2033-2040 https://doi.org/10.3892/ol.2017.6359
  18. von Elm E, Altman DG, Egger M, Pocock SJ, Gotzsche PC, Vandenbroucke JP; STROBE Initiative. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Lancet 2007;370:1453-1457 https://doi.org/10.1016/S0140-6736(07)61602-X
  19. National Comprehensive Cancer Network. NCCN clinical practice guidelines in oncology. Central nervous system cancers, version 3.2020. J Natl Compr Canc Netw 2020;18:1537-1570 https://doi.org/10.6004/jnccn.2020.0052
  20. Isensee F, Schell M, Pflueger I, Brugnara G, Bonekamp D, Neuberger U, et al. Automated brain extraction of multisequence MRI using artificial neural networks. Hum Brain Mapp 2019;40:4952-4964 https://doi.org/10.1002/hbm.24750
  21. Reinhold JC, Dewey BE, Carass A, Prince JL. Evaluating the impact of intensity normalization on MR image synthesis. Proc SPIE Int Soc Opt Eng 2019;10949:109493H
  22. Weisskoff R, Boxerman J, Sorensen A, Kulke S, Campbell T, Rosen B. Simulataneous blood volume and permeability mapping using a single Gd-based contrast injection. Proceedings of the Society of Magnetic Resonance, Second Annual Meeting; 1994 Aug 6-12; San Francisco, CA, USA: SMR, 1994. p.279
  23. Gull SF. Bayesian inductive inference and maximum entropy. In: Erickson GJ, Smith CR, eds. Maximum-entropy and Bayesian methods in science and engineering. Dordrecht: Springer, 1988:53-74
  24. Dice LR. Measures of the amount of ecologic association between species. Ecology 1945;26:297-302 https://doi.org/10.2307/1932409
  25. Ingrisch M, Schneider MJ, Norenberg D, Negrao de Figueiredo G, Maier-Hein K, Suchorska B, et al. Radiomic analysis reveals prognostic information in T1-weighted baseline magnetic resonance imaging in patients with glioblastoma. Invest Radiol 2017;52:360-366 https://doi.org/10.1097/RLI.0000000000000349
  26. Fox J, Weisberg S. Cox proportional-hazards regression for survival data. An R and S-PLUS companion to applied regression. New York: SAGE Publications, Inc., 2002
  27. Tomaszewski MR, Gillies RJ. The biological meaning of radiomic features. Radiology 2021;298:505-516 https://doi.org/10.1148/radiol.2021202553
  28. Enderling H, Alfonso JCL, Moros E, Caudell JJ, Harrison LB. Integrating mathematical modeling into the roadmap for personalized adaptive radiation therapy. Trends Cancer 2019;5:467-474 https://doi.org/10.1016/j.trecan.2019.06.006
  29. Ballman KV. Biomarker: predictive or prognostic? J Clin Oncol 2015;33:3968-3971 https://doi.org/10.1200/JCO.2015.63.3651
  30. Gavrilovic IT, Posner JB. Brain metastases: epidemiology and pathophysiology. J Neurooncol 2005;75:5-14 https://doi.org/10.1007/s11060-004-8093-6
  31. Eichler AF, Chung E, Kodack DP, Loeffler JS, Fukumura D, Jain RK. The biology of brain metastases-translation to new therapies. Nat Rev Clin Oncol 2011;8:344-356 https://doi.org/10.1038/nrclinonc.2011.58
  32. Liu Q, Zhang H, Jiang X, Qian C, Liu Z, Luo D. Factors involved in cancer metastasis: a better understanding to "seed and soil" hypothesis. Mol Cancer 2017;16:176
  33. Kano H, Kondziolka D, Lobato-Polo J, Zorro O, Flickinger JC, Lunsford LD. T1/T2 matching to differentiate tumor growth from radiation effects after stereotactic radiosurgery. Neurosurgery 2010;66:486-491; discussion 491-492 https://doi.org/10.1227/01.NEU.0000360391.35749.A5
  34. Cha J, Kim ST, Kim HJ, Kim HJ, Kim BJ, Jeon P, et al. Analysis of the layering pattern of the apparent diffusion coefficient (ADC) for differentiation of radiation necrosis from tumour progression. Eur Radiol 2013;23:879-886 https://doi.org/10.1007/s00330-012-2638-4
  35. Stockham AL, Tievsky AL, Koyfman SA, Reddy CA, Suh JH, Vogelbaum MA, et al. Conventional MRI does not reliably distinguish radiation necrosis from tumor recurrence after stereotactic radiosurgery. J Neurooncol 2012;109:149-158 https://doi.org/10.1007/s11060-012-0881-9
  36. Hainc N, Alsafwani N, Gao A, O'Halloran PJ, Kongkham P, Zadeh G, et al. The centrally restricted diffusion sign on MRI for assessment of radiation necrosis in metastases treated with stereotactic radiosurgery. J Neurooncol 2021;155:325-333 https://doi.org/10.1007/s11060-021-03879-4
  37. Galban CJ, Chenevert TL, Meyer CR, Tsien C, Lawrence TS, Hamstra DA, et al. Prospective analysis of parametric response map-derived MRI biomarkers: identification of early and distinct glioma response patterns not predicted by standard radiographic assessment. Clin Cancer Res 2011;17:4751-4760 https://doi.org/10.1158/1078-0432.CCR-10-2098
  38. Vogelbaum MA, Brown PD, Messersmith H, Brastianos PK, Burri S, Cahill D, et al. Treatment for brain metastases: ASCOSNO-ASTRO guideline. J Clin Oncol 2022;40:492-516 https://doi.org/10.1200/JCO.21.02314
  39. Sala E, Mema E, Himoto Y, Veeraraghavan H, Brenton JD, Snyder A, et al. Unravelling tumour heterogeneity using next-generation imaging: radiomics, radiogenomics, and habitat imaging. Clin Radiol 2017;72:3-10 https://doi.org/10.1016/j.crad.2016.09.013
  40. Napel S, Mu W, Jardim-Perassi BV, Aerts HJWL, Gillies RJ. Quantitative imaging of cancer in the postgenomic era: radio(geno)mics, deep learning, and habitats. Cancer 2018;124:4633-4649 https://doi.org/10.1002/cncr.31630
  41. Crispin-Ortuzar M, Gehrung M, Ursprung S, Gill AB, Warren AY, Beer L, et al. Three-dimensional printed molds for image-guided surgical biopsies: an open source computational platform. JCO Clin Cancer Inform 2020;4:736-748 https://doi.org/10.1200/CCI.20.00026
  42. Kazerouni AS, Hormuth DA 2nd, Davis T, Bloom MJ, Mounho S, Rahman G, et al. Quantifying tumor heterogeneity via MRI habitats to characterize microenvironmental alterations in HER2+ breast cancer. Cancers (Basel) 2022;14:1837