Diagnostic Value of Diffusion-Weighted MRI for Tumor Characterization, Differentiation and Monitoring in Pediatric Patients with Neuroblastic Tumors

Abstract

Purpose We explored the diagnostic value of diffusion-weighted MRI (DWI) for tumor characterization, differentiation and therapy monitoring in pediatric patients with extracranial neuroblastic tumors.

Materials and Methods All 29 patients (14 girls, median age: 3 years) with neuroblastoma (NB, n = 19), ganglioneuroblastoma (GNB, n = 4) and ganglioneuroma (GN, n = 6) who had had at least one in-house DWI examination since 2005 were identified and retrospectively analyzed. Two independent blinded readers measured ADC values (unit: 10−3 mm²/s) and signal intensity ratios (SIRs) of the primary tumor and, if applicable, of the tumor after chemotherapy, metastases and tumor relapse.

Results The pre-treatment ADC was 0.90 ± 0.23 in NB/GNB and 1.70 ± 0.36 in GN without overlap between the two entities for both readers, 0.67 ± 0.14 in metastases and 0.72 ± 0.18 in tumor relapse. With chemotherapy, mean ADC increased to 1.54 ± 0.33 in NB/GNB and to 1.23 ± 0.27 in metastases (p < 0.05). The median SIRs of various tumor lesions vs. liver, vs. muscle tissue and vs. adjacent tissue were significantly higher on DWI (range: 2.4 – 9.9) than on ce-T1w (range: 1.0 – 1.8, all p < 0.05). The coefficient of variation (CV) was ≤ 8.0 % for ADC and ≤ 16.4 % for signal intensity data.

Conclusion Based on mean ADC, DWI distinguishes between NB/GNB and GN with high certainty and provides plausible quantitative data on tumor response to therapy. Lesion conspicuity, as measured by SIR, is superior on DWI, compared to ce-T1w. DWI as a noninvasive, radiation-free and widely available imaging technique should be an integral part of MR imaging for neuroblastic tumors and should undergo prospective evaluation in multicenter studies.

Key Points 

• DWI reliably distinguishes neuroblastoma/ganglioneuroblastoma from ganglioneuroma, based on the mean ADC.

• DWI provides plausible quantitative data on tumor response to chemotherapy.

• DWI offers highly superior lesion conspicuity compared to contrast-enhanced T1w imaging.

• DWI should be considered a standard for imaging neuroblastic tumors.

Citation Format

• Neubauer H, Li M, Müller VR et al. Diagnostic Value of Diffusion-Weighted MRI for Tumor Characterization, Differentiation and Monitoring in Pediatric Patients with Neuroblastic Tumors. Fortschr Röntgenstr 2017; 189: 640 – 650

Zusammenfassung

Ziel Untersucht wurde die diagnostische Aussagekraft der diffusionsgewichteten MRT (DWI) für die Tumorcharakterisierung, Tumordifferenzierung und Verlaufskontrolle bei Kindern mit extrakraniellen neuroblastischen Tumoren.

Material und Methoden Alle 29 Patienten (14 Mädchen, medianes Alter 3 Jahre) mit Neuroblastom (NB, n = 19), Ganglioneuroblastom (GNB, n = 4) und Ganglioneurom (GN, n = 6) und mindestens einer DWI-Studie in domo seit 2005 wurden retrospektiv analysiert. Zwei unabhängige geblindete Untersucher bestimmten die ADC-Werte (Einheit: 10−3 mm²/s) und Signalintensitätsquotienten (SIR) für Primärtumor und, falls zutreffend, für Tumor nach Chemotherapie, Metastasen und Tumorrezidiv.

Ergebnisse Initial betrugen der ADC-Wert 0,90 ± 0,23 für NB/GNB und 1,70 ± 0,36 für GN ohne Überlappung beider Entitäten bei beiden Untersuchern, 0,67 ± 0,14 für Metastasen und 0,72 ± 0,18 für Rezidive. Unter Chemotherapie stieg der ADC auf 1,54 ± 0,33 bei NB/GNB und 1,23 ± 0,27 bei Metastasen (p < 0,05). Die medianen SIR der Tumorläsionen vs. Leber, vs. Muskel und vs. benachbartes Gewebe waren signifikant höher in der DWI (min...max 2,4...9,9) als in ce-T1w (1,0...1,8, alle p < 0,05). Der Variationskoeffizient (CV) lag ≤ 8,0 % für ADC und ≤ 16,4 % für SIR.

Schlussfolgerung DWI unterscheidet anhand des ADC zuverlässig zwischen NB/GNB und GN und liefert plausible quantitative Daten zum Therapieansprechen. Die Sichtbarkeit von Tumorherden, gemessen als SIR, ist in der DWI deutlich besser als in der ce-T1w. DWI als nicht-invasive und weithin verfügbare Bildgebungstechnik ohne Strahlenexposition sollte integraler Bestandteil jeder MR-Bildgebung bei neuroblastischen Tumoren sein und sollte in multizentrischen Studien prospektiv evaluiert werden.

Kernaussagen 

• DWI differenziert anhand des ADC-Werts zuverlässig zwischen Neuroblastom/Ganglioneuroblastom und Ganglioneurom.

• Die DWI liefert plausible quantitative Daten zum Therapieansprechen.

• Die Erkennbarkeit von Tumorherden ist höher mit DWI als mit ce-T1w.

• DWI sollte als Standardtechnik für die MR-Bildgebung neuroblastischer Tumoren betrachtet werden.

Key words

neuroblastoma - ganglioneuroblastoma - ganglioneuroma - therapy response - MR imaging - MR diffusion/perfusion

• References

• 1 Joshi VV. Peripheral neuroblastic tumors: pathologic classification based on recommendations of international neuroblastoma pathology committee (modification of Shimada classification). Pediatr Dev Pathol 2000; 3: 184-199
• 2 Spix C. Aareleid T. Stiller C. et al. Survival of children with neuroblastoma. Time trends and regional differences in Europe, 1978–1992. Eur J Cancer 2001; 37: 722-729
• 3 Maris JM. Recent advances in neuroblastoma. N Engl J Med 2010; 362: 2202-2211
• 4 Lonergan GJ. Schwab CM. Suarez ES. et al. Neuroblastoma, ganglioneuroblastoma, and ganglioneuroma: radiologic-pathologic correlation. Radiographics 2002; 22: 911-934
• 5 McCarville MB. What MRI can tell us about neurogenic tumors and rhabdomyosarcoma. Pediatr Radiol 2016; 46: 881-890
• 6 Brisse HJ. McCarville MB. Granata C. et al. Guidelines for imaging and staging of neuroblastic tumors: consensus report from the International Neuroblastoma Risk Group Project. Radiology 2011; 261: 243-257
• 7 Ley S. Ley-Zaporozhan J. Günther P. et al. Neuroblastoma imaging. Roefo 2011; 183: 217-225
• 8 Pinto NR. Applebaum MA. Volchenboum SL. et al. Advances in Risk Classification and Treatment Strategies for Neuroblastoma. J Clin Oncol 2015; 33: 3008-3017
• 9 Kocaoglu M. Bulakbasi N. Sanal HT. et al. Pediatric abdominal masses: diagnostic accuracy of diffusion weighted MRI. Magn Reson Imaging 2010; 28: 629-636
• 10 Uhl M. Altehoefer C. Kontny U. et al. MRI-diffusion imaging of neuroblastomas: first results and correlation to histology. Eur Radiol 2002; 12: 2335-2338
• 11 Gahr N. Darge K. Hahn G. et al. Diffusion-weighted MRI for differentiation of neuroblastoma and ganglioneuroblastoma/ganglioneuroma. Eur J Radiol 2011; 79: 443-446
• 12 Serin HI. Gorkem SB. Doganay S. et al. Diffusion weighted imaging in differentiating malignant and benign neuroblastic tumors. Jpn J Radiol 2016; 34: 620-624
• 13 Pai Panandiker AS. Coleman J. Shulkin B. Whole Body Pediatric Neuroblastoma Imaging: 123I-mIBG and Beyond. Clin Nucl Med 2015; 40: 737-739
• 14 Demir S. Altinkaya N. Kocer NE. Variations in apparent diffusion coefficient values following chemotherapy in pediatric neuroblastoma. Diagn Interv Radiol 2015; 21: 184-188
• 15 Brodeur GM. Pritchard J. Berthold F. et al. Revisions of the international criteria for neuroblastoma diagnosis, staging, and response to treatment. J Clin Oncol 1993; 11: 1466-1477
• 16 Sauer A. Müller V. Pabst T. et al. Diffusion-weighted MRI for diagnosis and differential diagnosis of lymphatic malformation in paediatric patients. Cancer Research Frontiers 2016; 2: 300-310
• 17 Neubauer H. Evangelista L. Hassold N. et al. Musculoskeletal tumorous and tumour-like lesions: diagnostic utility of diffusion-weighted MRI for detection and differentiation in pediatric patients. World J Pediatr 2012; 8: 342-349
• 18 Lee JW. Cho A. Yun M. et al. Prognostic value of pretreatment FDG PET in pediatric neuroblastoma. Eur J Radiol 2015; 84: 2633-2639
• 19 Li M. Winkler B. Pabst T. et al. Fast MR imaging of the paediatric abdomen with CAIPIRINHA-accelerated T1w 3D-FLASH and with high-resolution T2w HASTE: a study on image quality. Gastroenterol Res Pract 2015;
• 20 Li M. Dick A. Hassold N. et al. CAIPIRINHA-accelerated T1w 3D-FLASH for small-bowel MR imaging in paediatric patients with Crohn disease: assessment of image quality and diagnostic performance. World J Pediatr 2016; 12: 455-462
• 21 Sharp SE. Trout AT. Weiss BD. et al. MIBG in Neuroblastoma Diagnostic Imaging and Therapy. Radiographics 2016; 36: 258-278
• 22 Andrich MP. Shalaby-Rana E. Movassaghi N. et al. The role of 131 iodine-metaiodobenzylguanidine scanning in the correlative imaging of patients with neuroblastoma. Pediatrics 1996; 97: 246-250
• 23 Kim YY. Shin HJ. Kim MJ. et al. Comparison of effective radiation doses from X-ray, CT, and PET/CT in pediatric patients with neuroblastoma using a dose monitoring program. Diagn Interv Radiol 2016; 22: 390-394
• 24 Federman N. Feig SA. PET/CT in evaluating pediatric malignancies: a clinician’s perspective. J Nucl Med 2007; 48: 1920-1922
• 25 Chawla SC. Federman N. Zhang D. et al. Estimated cumulative radiation dose from PET/CT in children with malignancies: a 5-year retrospective review. Pediatr Radiol 2010; 40: 681-686
• 26 Stojanov D. Aracki-Trenkic A. Benedeto-Stojanov D. Gadolinium deposition within the dentate nucleus and globus pallidus after repeated administrations of gadolinium-based contrast agents – current status. Neuroradiology 2016; 58: 433-441