Consensus recommendations on standardized magnetic resonance imaging protocols for multicenter canine brain tumor clinical trials

The National Cancer Institute Comparative Brain Tumor Consortium, Patient Outcomes Working Group, propose a consensus document in support of standardized magnetic resonance imaging protocols for canine brain tumor clinical trials. The intent of this manuscript is to address the widely acknowledged need to ensure canine brain tumor imaging protocols are relevant and have sufficient equivalency to translate to human studies such that: (1) multi-institutional studies can be performed with minimal inter-institutional variation, and (2) imaging protocols are consistent with human consensus recommendations to permit reliable translation of imaging data to human clinical trials. Consensus recommendations include pre- and postcontrast three-dimensional T1-weighted images, T2-weighted turbo spin echo in all three planes, T2*-weighted gradient recalled echo, T2-weighted fluid attenuated inversion recovery, and diffusion weighted imaging/diffusion tensor imaging in transverse plane; field of view of ≤150 mm; slice thickness of ≤2 mm, matrix ≥ 256 for two-dimensional images, and 150 or 256 for three-dimensional images.

[1]  J. Cairncross,et al.  Prospective study of postoperative magnetic resonance imaging in patients with malignant gliomas. , 1997, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[2]  Yong-li Li,et al.  Comparison of volumetric methods for tumor measurements on two and three dimensional MRI in adult glioblastoma , 2011, Neuroradiology.

[3]  P. Choyke,et al.  Diffusion-weighted magnetic resonance imaging as a cancer biomarker: consensus and recommendations. , 2009, Neoplasia.

[4]  J. Edwards,et al.  Seizure-induced brain lesions: a wide spectrum of variably reversible MRI abnormalities. , 2013, European journal of radiology.

[5]  Susan M. Chang,et al.  Response Assessment in Neuro-Oncology Clinical Trials. , 2017, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[6]  G. Beauchamp,et al.  Effect of acquisition time and chemical fat suppression on meningeal enhancement on MR imaging in dogs. , 2012, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[7]  D. Brachman,et al.  Pathology concordance levels for meningioma classification and grading in NRG Oncology RTOG Trial 0539. , 2016, Neuro-oncology.

[8]  Wenzhen Zhu,et al.  Comparative study of 3D-SPGR vs 2D-SE T1WI after enhancement in the brain. , 2003, Journal of Huazhong University of Science and Technology. Medical sciences = Hua zhong ke ji da xue xue bao. Yi xue Ying De wen ban = Huazhong keji daxue xuebao. Yixue Yingdewen ban.

[9]  C. Kuhl,et al.  Brain tumors: full- and half-dose contrast-enhanced MR imaging at 3.0 T compared with 1.5 T--Initial Experience. , 2005, Radiology.

[10]  F. Bova,et al.  Frameless stereotactic radiosurgery for the treatment of primary intracranial tumours in dogs. , 2015, Veterinary and comparative oncology.

[11]  E. Melhem,et al.  Dynamic T1‐weighted spin‐echo MR imaging: The role of digital subtraction in the demonstration of enhancing brain lesions , 1999, Journal of magnetic resonance imaging : JMRI.

[12]  K. E. Chow,et al.  EARLY POSTOPERATIVE MAGNETIC RESONANCE IMAGING FINDINGS IN FIVE DOGS WITH CONFIRMED AND SUSPECTED BRAIN TUMORS. , 2015, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[13]  Patrick Y Wen,et al.  Application of Novel Response/Progression Measures for Surgically Delivered Therapies for Gliomas: Response Assessment in Neuro-Oncology (RANO) Working Group , 2012, Neurosurgery.

[14]  K Sartor,et al.  Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. , 1994, Neurosurgery.

[15]  E. Riedesel,et al.  Normal canine brain maturation at magnetic resonance imaging. , 2010, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[16]  C. Glaser,et al.  Understanding 3D TSE Sequences: Advantages, Disadvantages, and Application in MSK Imaging , 2015, Seminars in Musculoskeletal Radiology.

[17]  J. Griffin,et al.  Comparison of two fat-suppressed magnetic resonance imaging pulse sequences to standard t2-weighted images for brain parenchymal contrast and lesion detection in dogs with inflammatory intracranial disease. , 2015, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[18]  F. Ståhlberg,et al.  Brain lesion contrast in MR imaging , 1997, Acta radiologica.

[19]  A. Omuro,et al.  Diffusion and Perfusion MRI to Differentiate Treatment-Related Changes Including Pseudoprogression from Recurrent Tumors in High-Grade Gliomas with Histopathologic Evidence , 2015, American Journal of Neuroradiology.

[20]  C. Matula,et al.  Magnetic Resonance Imaging Contrast Enhancement of Brain Tumors at 3 Tesla Versus 1.5 Tesla , 2002, Investigative radiology.

[21]  B. Meij,et al.  Hypophysectomy as a treatment for canine and feline Cushing's disease. , 2001, The Veterinary clinics of North America. Small animal practice.

[22]  C. Jack,et al.  Alzheimer's Disease Neuroimaging Initiative , 2008 .

[23]  M. Podell,et al.  International Veterinary Epilepsy Task Force recommendations for a veterinary epilepsy-specific MRI protocol , 2015, BMC Veterinary Research.

[24]  D. Scoffings,et al.  Imaging of the post-operative cranium. , 2010, Radiographics : a review publication of the Radiological Society of North America, Inc.

[25]  R. Ruthazer,et al.  Magnetic resonance imaging apparent diffusion coefficients for histologically confirmed intracranial lesions in dogs. , 2011, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[26]  E. Hattingen,et al.  Time window for postoperative reactive enhancement after resection of brain tumors: less than 72 hours. , 2014, Neurosurgical focus.

[27]  P. Dickinson Advances in Diagnostic and Treatment Modalities for Intracranial Tumors , 2014, Journal of veterinary internal medicine.

[28]  P. Wen,et al.  Response Assessment in Neuro-Oncology , 2011, Current oncology reports.

[29]  K Farahani,et al.  Effect of field strength on susceptibility artifacts in magnetic resonance imaging. , 1990, Computerized medical imaging and graphics : the official journal of the Computerized Medical Imaging Society.

[30]  J. Lee,et al.  Improved motion-sensitized driven-equilibrium preparation for 3D turbo spin echo T1 weighted imaging after gadolinium administration for the detection of brain metastases on 3T MRI. , 2016, The British journal of radiology.

[31]  M. Berger,et al.  Canine spontaneous glioma: a translational model system for convection-enhanced delivery. , 2010, Neuro-oncology.

[32]  R. M. Simpson,et al.  Creation of an NCI comparative brain tumor consortium: informing the translation of new knowledge from canine to human brain tumor patients. , 2016, Neuro-oncology.

[33]  John H. Sampson,et al.  A Novel Method for Volumetric MRI Response Assessment of Enhancing Brain Tumors , 2011, PloS one.

[34]  B. Meij,et al.  The Influence of Pituitary Size on Outcome After Transsphenoidal Hypophysectomy in a Large Cohort of Dogs with Pituitary‐Dependent Hypercortisolism , 2016, Journal of veterinary internal medicine.

[35]  Zhu Wenzhen,et al.  Comparative study of 3D-SPGR vs 2D-SE T1WI after enhancement in the brain , 2008, Journal of Huazhong University of Science and Technology [Medical Sciences].

[36]  Naoya Hashimoto,et al.  Immunotherapy response assessment in neuro-oncology: a report of the RANO working group. , 2015, The Lancet. Oncology.

[37]  M. Roos,et al.  Irradiation of brain tumors in dogs with neurologic disease. , 2005, Journal of veterinary internal medicine.

[38]  I. Polis,et al.  Comparison between symptomatic treatment and lomustine supplementation in 71 dogs with intracranial, space-occupying lesions. , 2014, Veterinary and comparative oncology.

[39]  E. Merkle,et al.  A review of MR physics: 3T versus 1.5T. , 2007, Magnetic resonance imaging clinics of North America.

[40]  Kenneth R. Maravilla,et al.  Distinction between glioma progression and post-radiation change by combined physiologic MR imaging , 2010, Neuroradiology.

[41]  M. Kent,et al.  Treatment of MRI‐Diagnosed Trigeminal Peripheral Nerve Sheath Tumors by Stereotactic Radiotherapy in Dogs , 2016, Journal of veterinary internal medicine.

[42]  A Gregory Sorensen,et al.  Emerging techniques and technologies in brain tumor imaging. , 2014, Neuro-oncology.

[43]  M. Kent,et al.  Perfusion and Volume Response of Canine Brain Tumors to Stereotactic Radiosurgery and Radiotherapy , 2016, Journal of veterinary internal medicine.

[44]  N. Jeffery,et al.  Systematic Review of Brain Tumor Treatment in Dogs , 2015, Journal of veterinary internal medicine.

[45]  S. Schatzberg,et al.  Magnetic resonance imaging for the differentiation of neoplastic, inflammatory, and cerebrovascular brain disease in dogs. , 2012, Journal of veterinary internal medicine.

[46]  T. Cascino,et al.  Response criteria for phase II studies of supratentorial malignant glioma. , 1990, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[47]  M. van Glabbeke,et al.  New guidelines to evaluate the response to treatment in solid tumors , 2000, Journal of the National Cancer Institute.

[48]  Veterinary cooperative oncology group - common terminology criteria for adverse events (VCOG-CTCAE) following chemotherapy or biological antineoplastic therapy in dogs and cats v1.1. , 2016, Veterinary and comparative oncology.

[49]  S. Hecht,et al.  Use of the T2*-weighted gradient recalled echo sequence for magnetic resonance imaging of the canine and feline brain. , 2014, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[50]  M. C. Han,et al.  Contrast enhancement of brain tumors at different MR field strengths: comparison of 0.5 T and 2.0 T. , 1994, AJNR. American journal of neuroradiology.

[51]  M. Okada,et al.  [New response evaluation criteria in solid tumours-revised RECIST guideline (version 1.1)]. , 2009, Gan to kagaku ryoho. Cancer & chemotherapy.

[52]  S. Schatzberg,et al.  Evaluation of standard magnetic resonance characteristics used to differentiate neoplastic, inflammatory, and vascular brain lesions in dogs. , 2014, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[53]  S. Stuckey,et al.  Transient Seizure‐Related MRI Abnormalities , 2009, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[54]  Siegfried Trattnig,et al.  Effect of Contrast Dose and Field Strength in the Magnetic Resonance Detection of Brain Metastases , 2003, Investigative radiology.

[55]  Marion Smits,et al.  Consensus recommendations for a standardized Brain Tumor Imaging Protocol in clinical trials. , 2015, Neuro-oncology.

[56]  R. Packer,et al.  Magnetic Resonance Imaging Appearance and Mechanism of Action of Five Hemostatic Agents Used in Neurosurgery. , 2016, Veterinary surgery : VS.

[57]  Mark Dewhirst,et al.  Perspectives from man’s best friend: National Academy of Medicine’s Workshop on Comparative Oncology , 2016, Science Translational Medicine.

[58]  N. Jeffery,et al.  Findings on low-field cranial MR images in epileptic dogs that lack interictal neurological deficits. , 2008, Veterinary journal.

[59]  Debiao Li,et al.  Whole‐brain intracranial vessel wall imaging at 3 Tesla using cerebrospinal fluid–attenuated T1‐weighted 3D turbo spin echo , 2017, Magnetic resonance in medicine.

[60]  Martin Bendszus,et al.  Response assessment criteria for brain metastases: proposal from the RANO group. , 2015, The Lancet. Oncology.

[61]  Anwar R. Padhani,et al.  Diffusion-weighted (DW) and dynamic contrast-enhanced (DCE) magnetic resonance imaging (MRI) for monitoring anticancer therapy , 2010, Targeted Oncology.

[62]  M. Shiroishi,et al.  Brain tumors: a multimodality approach with diffusion-weighted imaging, diffusion tensor imaging, magnetic resonance spectroscopy, dynamic susceptibility contrast and dynamic contrast-enhanced magnetic resonance imaging. , 2013, Magnetic resonance imaging clinics of North America.

[63]  Michael W. Weiner,et al.  Impact of the Alzheimer's Disease Neuroimaging Initiative, 2004 to 2014 , 2015, Alzheimer's & Dementia.

[64]  D. Thamm,et al.  Response evaluation criteria for solid tumours in dogs (v1.0): a Veterinary Cooperative Oncology Group (VCOG) consensus document. , 2015, Veterinary and comparative oncology.

[65]  T. Chenevert,et al.  Diffusion-weighted MRI for assessment of early cancer treatment response. , 2010, Current pharmaceutical biotechnology.

[66]  P. Morgan,et al.  Response Assessment in Pediatric Neuro-Oncology: Implementation and Expansion of the RANO Criteria in a Randomized Phase II Trial of Pediatric Patients with Newly Diagnosed High-Grade Gliomas , 2016, American Journal of Neuroradiology.

[67]  Gary Kelloff,et al.  The Quantitative Imaging Network: NCI's Historical Perspective and Planned Goals. , 2014, Translational oncology.

[68]  B. Erickson,et al.  Optimal Presentation Modes for Detecting Brain Tumor Progression , 2011, American Journal of Neuroradiology.

[69]  Dima Suki,et al.  Association of the Extent of Resection With Survival in Glioblastoma: A Systematic Review and Meta-analysis. , 2016, JAMA oncology.

[70]  C. Khanna,et al.  Response evaluation criteria for peripheral nodal lymphoma in dogs (v1.0)--a Veterinary Cooperative Oncology Group (VCOG) consensus document. , 2010, Veterinary and comparative oncology.

[71]  L Junck,et al.  Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. , 2011, The Lancet. Oncology.

[72]  N. Rofsky,et al.  Image subtraction in gadolinium-enhanced MR imaging. , 1996, AJR. American journal of roentgenology.

[73]  C. Khanna,et al.  Defining the Value of a Comparative Approach to Cancer Drug Development , 2015, Clinical Cancer Research.

[74]  Eudocia Q Lee,et al.  Assessment of Brain Tumor Response: RANO and Its Offspring , 2016, Current Treatment Options in Oncology.

[75]  P. Dickinson,et al.  Reversible magnetic resonance imaging abnormalities in dogs following seizures. , 1999, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[76]  Andrew D. Miller,et al.  Characteristics and Survival of 121 Cats Undergoing Excision of Intracranial Meningiomas (1994-2011). , 2015, Veterinary surgery : VS.

[77]  Thomas L Ellis,et al.  Safety and feasibility of the NanoKnife system for irreversible electroporation ablative treatment of canine spontaneous intracranial gliomas. , 2015, Journal of neurosurgery.

[78]  M. Khan,et al.  The recurrence of intracranial meningiomas after surgical treatment. , 1983, Journal of neurosurgery.

[79]  Susan M. Chang,et al.  Endpoints for clinical trials and revised assessment in neuro-oncology. , 2012, Current opinion in neurology.

[80]  Mitsuru Ikeda,et al.  Contrast-enhanced MR imaging of metastatic brain tumor at 3 tesla: utility of T(1)-weighted SPACE compared with 2D spin echo and 3D gradient echo sequence. , 2008, Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine.

[81]  M. Christian,et al.  [New guidelines to evaluate the response to treatment in solid tumors]. , 2000, Bulletin du cancer.

[82]  S. Frean,et al.  Appearance of the canine meninges in subtraction magnetic resonance images. , 2014, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[83]  J. Uhm Updated Response Assessment Criteria for High-Grade Gliomas: Response Assessment in Neuro-Oncology Working Group , 2010 .

[84]  Diffusion-weighted magnetic resonance imaging of the normal canine brain. , 2014, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[85]  M. Sullivan,et al.  Effect of delayed acquisition times on gadolinium-enhanced magnetic resonance imaging of the presumably normal canine brain. , 2011, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[86]  S. Schatzberg,et al.  Magnetic resonance imaging features of intracranial astrocytomas and oligodendrogliomas in dogs. , 2011, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[87]  K. Togashi,et al.  T1-weighted MR imaging of glioma at 3T: a comparative study of 3D MPRAGE vs. conventional 2D spin-echo imaging. , 2016, Clinical imaging.

[88]  R. Dodge,et al.  Analysis of survival in a retrospective study of 86 dogs with brain tumors. , 1991, Journal of veterinary internal medicine.

[89]  J. Henson,et al.  Brain Tumor Imaging in Clinical Trials , 2008, American Journal of Neuroradiology.

[90]  Charles A. Gooding,et al.  Computed tomography and magnetic resonance imaging , 1990 .

[91]  John H. Sampson,et al.  A novel, reproducible, and objective method for volumetric magnetic resonance imaging assessment of enhancing glioblastoma. , 2014, Journal of neurosurgery.

[92]  Paulo A. Garcia,et al.  Invited review--neuroimaging response assessment criteria for brain tumors in veterinary patients. , 2014, Veterinary radiology & ultrasound : the official journal of the American College of Veterinary Radiology and the International Veterinary Radiology Association.

[93]  Dongsheng Duan,et al.  A One Health overview, facilitating advances in comparative medicine and translational research , 2016, Clinical and Translational Medicine.