Volumetric apparent diffusion coefficient histogram analysis for determining the degree of differentiation of periampullary carcinomas: Volumetric ADC histogram analysis of periampullary carcinomas

Mustafa Orhan Nalbant; Ercan  Inci

doi:10.28982/josam.7916

Authors

Mustafa Orhan Nalbant University of Health Sciences, Bakirkoy Dr. Sadi Konuk Training and Research Hospital, Department of Radiology, Istanbul, Turkey https://orcid.org/0000-0002-5277-9111
Ercan Inci University of Health Sciences, Bakirkoy Dr. Sadi Konuk Training and Research Hospital, Department of Radiology, Istanbul, Turkey https://orcid.org/0000-0002-3791-2471

DOI:

https://doi.org/10.28982/josam.7916

Keywords:

apparent diffusion coefficient, differentiation degree, intestinal type periampullary adenocarcinoma, pancreatobiliary type periampullary adenocarcinoma, volumetric histogram analysis

Abstract

Background/Aim: The classification of periampullary adenocarcinomas into pancreatobiliary-type periampullary adenocarcinoma and intestinal-type periampullary adenocarcinoma (PPAC and IPAC, respectively) has gained significant acceptance in the medical community. A patient's prognosis is determined by the degree of differentiation of these tumor types. The objective of the present investigation was to assess the efficacy of volumetric apparent diffusion coefficient (ADC) histogram analysis in assessing the degree of differentiation for these two tumor types.

Methods: This retrospective cohort research evaluated 54 PPAC (45 well-differentiated and nine poorly differentiated) and 15 IPAC (11 well-differentiated and four poorly differentiated) patients. Magnetic resonance imaging (1.5 T MRI) scans were used to evaluate the results. The features of the histogram for the ADC values were computed and incorporated several statistical measures, such as the mean, minimum, median, maximum, and percentiles in addition to the skewness, kurtosis, and variance.

Results: In both PPAC and IPAC patients, the ADC values exhibited lower values in the poorly differentiated group when compared with the well-differentiated group. However, the changes between groups did not reach statistical significance. Among IPAC patients, the well-differentiated group had a larger kurtosis (P=0.048). In IPAC patients, the calculated value for the area under the curve (AUC) of kurtosis was determined to be 0.818. When the threshold was set at 0.123, the specificity and sensitivity were observed to be 90% and 75%, respectively.

Conclusion: Our research indicates that the kurtosis of ADC is an effective indicator to determine the level of IPAC differentiation. Analysis of the histogram at increased b values can provide valuable insights to help determine the degree of differentiation of IPAC using a noninvasive technique.

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References

Sarmiento JM, Nagomey DM, Sarr MG, Farnell MB. Periampullary cancers: are there differences? Surg Clin North Am. 2001;81:543-55. DOI: https://doi.org/10.1016/S0039-6109(05)70142-0

Fernandez-Cruz L. Periampullary carcinoma. In: Holzheimer RG, Mannick JA, editors. Surgical Treatment: Evidence-Based and Problem-Oriented. Munich: Zuckschwerdt; 2001.

Surveillance, Epidemiology, and End Results Program, Cancer Stat Facts: Pancreatic Cancer. NIH. 2022.

Conroy T, Hammel P, Hebbar M, Ben Abdelghani M, Wei AC, Raoul JL, et al. Canadian Cancer Trials Group and the Unicancer-GI–PRODIGE Group. FOLFIRINOX or Gemcitabine as Adjuvant Therapy for Pancreatic Cancer. N Engl J Med. 2018;379:2395-406. DOI: https://doi.org/10.1056/NEJMoa1809775

Ducreux M, Cuhna AS, Caramella C, Hollebecque A, Burtin P, Goéré D, et al. ESMO Guidelines Committee. Cancer of the pancreas: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2015;26:56-68. DOI: https://doi.org/10.1093/annonc/mdv295

Williams JL, Chan CK, Toste PA, Elliott IA, Vasquez CR, Sunjaya DB, et al. Association of Histopathologic Phenotype of Periampullary Adenocarcinomas With Survival. JAMA Surg. 2017;152:82-8. DOI: https://doi.org/10.1001/jamasurg.2016.3466

Westgaard A, Tafjord S, Farstad IN, Cvancarova M, Eide TJ, Mathisen O, et al. Pancreatobiliary versus intestinal histologic type of differentiation is an independent prognostic factor in resected periampullary adenocarcinoma. BMC Cancer. 2008;8:170. DOI: https://doi.org/10.1186/1471-2407-8-170

Bronsert P, Kohler I, Werner M, Makowiec F, Kuesters S, Hoeppner J, et al. Intestinal-type of differentiation predicts favourable overall survival: confirmatory clinicopathological analysis of 198 periampullary adenocarcinomas of pancreatic, biliary, ampullary and duodenal origin. BMC Cancer. 2013;13:428. DOI: https://doi.org/10.1186/1471-2407-13-428

Nishio K, Kimura K, Amano R, Yamazoe S, Ohrira G, Nakata B et al. Preoperative predictors for early recurrence of resectable pancreatic cancer. World J Surg Oncol. 2017;15:16. DOI: https://doi.org/10.1186/s12957-016-1078-z

Endo Y, Fujimoto M, Ito N, Takahashi Y, Kitago M, Gotoh M, et al. Clinicopathological impacts of DNA methylation alterations on pancreatic ductal adenocarcinoma: prediction of early recurrence based on genome-wide DNA methylation profiling. J Cancer Res Clin Oncol. 2021;147:1341-1354. DOI: https://doi.org/10.1007/s00432-021-03541-6

Hasan S, Jacob R, Manne U, Paluri R. Advances in pancreatic cancer biomarkers. Oncol Rev. 2019;13:410. DOI: https://doi.org/10.4081/oncol.2019.410

Just N. Improving tumour heterogeneity MRI assessment with histograms. Br J Cancer. 2014;111:2205-13. DOI: https://doi.org/10.1038/bjc.2014.512

Li A, Xing W, Li H, Hu Y, Hu D, Li Z, et al. Subtype Differentiation of Small (≤ 4 cm) Solid Renal Mass Using Volumetric Histogram Analysis of DWI at 3-T MRI. AJR Am J Roentgenol. 2018;211:614-23. DOI: https://doi.org/10.2214/AJR.17.19278

Lu JY, Yu H, Zou XL, Li Z, Hu XM, Shen YQ, et al. Apparent diffusion coefficient-based histogram analysis differentiates histological subtypes of periampullary adenocarcinoma. World J Gastroenterol. 201928;25:6116-28. DOI: https://doi.org/10.3748/wjg.v25.i40.6116

Kamarajah SK. Pancreaticoduodenectomy for periampullary tumours: a review article based on Surveillance, End Results and Epidemiology (SEER) database. Clin Transl Oncol. 2018;20:1153-1160. DOI: https://doi.org/10.1007/s12094-018-1832-5

Al-Hawary MM, Kaza RK, Francis IR. Optimal Imaging Modalities for the Diagnosis and Staging of Periampullary Masses. Surg Oncol Clin N Am. 2016;25:239-53. DOI: https://doi.org/10.1016/j.soc.2015.12.001

Acharya A, Markar SR, Sodergren MH, Malietzis G, Darzi A, Athanasiou T, et al. Meta-analysis of adjuvant therapy following curative surgery for periampullary adenocarcinoma. Br J Surg. 2017;104:814-22. DOI: https://doi.org/10.1002/bjs.10563

Kumari N, Prabha K, Singh RK, Baitha DK, Krishnani N. Intestinal and pancreatobiliary differentiation in periampullary carcinoma: the role of immunohistochemistry. Hum Pathol. 2013;44:2213-9. DOI: https://doi.org/10.1016/j.humpath.2013.05.003

Zhou H, Schaefer N, Wolff M, Fischer HP. Carcinoma of the ampulla of Vater: comparative histologic/immunohistochemical classification and follow-up. Am J Surg Pathol. 2004;28:875-82. DOI: https://doi.org/10.1097/00000478-200407000-00005

Sandhu V, Bowitz Lothe IM, Labori KJ, Lingjærde OC, Buanes T, Dalsgaard AM, et al. Molecular signatures of mRNAs and miRNAs as prognostic biomarkers in pancreatobiliary and intestinal types of periampullary adenocarcinomas. Mol Oncol. 2015;9:758-71. DOI: https://doi.org/10.1016/j.molonc.2014.12.002

Sandhu V, Wedge DC, Bowitz Lothe IM, Labori KJ, Dentro SC, Buanes T, et al. The Genomic Landscape of Pancreatic and Periampullary Adenocarcinoma. Cancer Res. 2016;76:5092-102. DOI: https://doi.org/10.1158/0008-5472.CAN-16-0658

Kalluri Sai Shiva UM, Kuruva MM, Mitnala S, Rupjyoti T, Guduru Venkat R, Botlagunta S, et al. MicroRNA profiling in periampullary carcinoma. Pancreatology. 2014;14:36-47. DOI: https://doi.org/10.1016/j.pan.2013.10.003

Surov A, Meyer HJ, Wienke A. Correlation between apparent diffusion coefficient (ADC) and cellularity is different in several tumors: a meta-analysis. Oncotarget. 2017;8:59492-9. DOI: https://doi.org/10.18632/oncotarget.17752

Meyer HJ, Leifels L, Hamerla G, Höhn AK, Surov A. ADC-histogram analysis in head and neck squamous cell carcinoma. Associations with different histopathological features including expression of EGFR, VEGF, HIF-1α, Her 2 and p53. A preliminary study. Magn Reson Imaging. 2018;54:214-7. DOI: https://doi.org/10.1016/j.mri.2018.07.013

Iima M, Le Bihan D. Clinical Intravoxel Incoherent Motion and Diffusion MR Imaging: Past, Present, and Future. Radiology. 2016;278:13-32. DOI: https://doi.org/10.1148/radiol.2015150244

Shindo T, Fukukura Y, Umanodan T, Takumi K, Hakamada H, Nakajo M, et al. Histogram Analysis of Apparent Diffusion Coefficient in Differentiating Pancreatic Adenocarcinoma and Neuroendocrine Tumor. Medicine (Baltimore). 2016;95:2574. DOI: https://doi.org/10.1097/MD.0000000000002574

Bi L, Dong Y, Jing C, Wu Q, Xiu J, Cai S, et al. Differentiation of pancreatobiliary-type from intestinal-type periampullary carcinomas using 3.0T MRI. J Magn Reson Imaging. 2016;43:877-86. DOI: https://doi.org/10.1002/jmri.25054

Pereira JA, Rosado E, Bali M, Metens T, Chao SL. Pancreatic neuroendocrine tumors: correlation between histogram analysis of apparent diffusion coefficient maps and tumor grade. Abdom Imaging. 2015;40:3122-8. DOI: https://doi.org/10.1007/s00261-015-0524-7

Hoffman DH, Ream JM, Hajdu CH, Rosenkrantz AB. Utility of whole-lesion ADC histogram metrics for assessing the malignant potential of pancreatic intraductal papillary mucinous neoplasms (IPMNs). Abdom Radiol (NY). 2017;42:1222-8. DOI: https://doi.org/10.1007/s00261-016-1001-7

De Robertis R, Maris B, Cardobi N, Tinazzi Martini P, Gobbo S, Capelli P, et al. Can histogram analysis of MR images predict aggressiveness in pancreatic neuroendocrine tumors? Eur Radiol. 2018;28:2582-91. DOI: https://doi.org/10.1007/s00330-017-5236-7

De Robertis R, Beleù A, Cardobi N, Frigerio I, Ortolani S, Gobbo S, et al. Correlation of MR features and histogram-derived parameters with aggressiveness and outcomes after resection in pancreatic ductal adenocarcinoma. Abdom Radiol (NY). 2020;45:3809-18. DOI: https://doi.org/10.1007/s00261-020-02509-3

Igarashi T, Shiraishi M, Watanabe K, Ohki K, Takenaga S, Ashida H, et al. 3D quantitative analysis of diffusion-weighted imaging for predicting the malignant potential of intraductal papillary mucinous neoplasms of the pancreas. Pol J Radiol. 2021;86:298-308. DOI: https://doi.org/10.5114/pjr.2021.106427

Agrawal S, Daruwala C, Khurana J. Distinguishing autoimmune pancreatitis from pancreaticobiliary cancers: current strategy. Ann Surg. 2012;255:248-58. DOI: https://doi.org/10.1097/SLA.0b013e3182324549

Kim JH, Kim MH, Byun JH, Lee SS, Lee SJ, Park SH, et al. Diagnostic Strategy for Differentiating Autoimmune Pancreatitis From Pancreatic Cancer: Is an Endoscopic Retrograde Pancreatography Essential? Pancreas. 2012;41:639-47. DOI: https://doi.org/10.1097/MPA.0b013e31823a509b

Hedfi M, Charfi M, Nejib FZ, Benlahouel S, Debaibi M, Ben Azzouz S, et al. Focal Mass-Forming Autoimmune Pancreatitis Mimicking Pancreatic Cancer: Which strategy? Tunis Med. 2019;97:731-5.

Wolske KM, Ponnatapura J, Kolokythas O, Burke LMB, Tappouni R, Lalwani N. Chronic Pancreatitis or Pancreatic Tumor? A Problem-solving Approach. Radiographics. 2019;39:1965-82. DOI: https://doi.org/10.1148/rg.2019190011

Hur BY, Lee JM, Lee JE, Park JY, Kim SJ, Joo I, et al. Magnetic resonance imaging findings of the mass-forming type of autoimmune pancreatitis: comparison with pancreatic adenocarcinoma. J Magn Reson Imaging. 2012;36:188-97. DOI: https://doi.org/10.1002/jmri.23609

Choi SY, Kim SH, Kang TW, Song KD, Park HJ, Choi YH. Differentiating Mass-Forming Autoimmune Pancreatitis From Pancreatic Ductal Adenocarcinoma on the Basis of Contrast-Enhanced MRI and DWI Findings. AJR Am J Roentgenol. 2016;206:291-300. DOI: https://doi.org/10.2214/AJR.15.14974

Muhi A, Ichikawa T, Motosugi U, Sou H, Sano K, Tsukamoto T, et al. Mass-forming autoimmune pancreatitis and pancreatic carcinoma: differential diagnosis on the basis of computed tomography and magnetic resonance cholangiopancreatography, and diffusion-weighted imaging findings. J Magn Reson Imaging. 2012;35:827-36. DOI: https://doi.org/10.1002/jmri.22881

Kamisawa T, Takuma K, Anjiki H, Egawa N, Hata T, Kurata M, et al. Differentiation of autoimmune pancreatitis from pancreatic cancer by diffusion-weighted MRI. Am J Gastroenterol. 2010;105:1870-5. DOI: https://doi.org/10.1038/ajg.2010.87

Jia H, Li J, Huang W, Lin G. Multimodel magnetic resonance imaging of mass-forming autoimmune pancreatitis: differential diagnosis with pancreatic ductal adenocarcinoma. BMC Med Imaging. 2021;21:149. DOI: https://doi.org/10.1186/s12880-021-00679-0