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Evaluation of Malignancy Risk of Ampullary Tumors Detected by Endoscopy Using 2-[18F]FDG PET/CT

  • Pei-Ju Chuang (Department of Nuclear Medicine, National Taiwan University Hospital) ;
  • Hsiu-Po Wang (Department of Internal Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine) ;
  • Yu-Wen Tien (Department of Surgery, National Taiwan University Hospital, National Taiwan University College of Medicine) ;
  • Wei-Shan Chin (School of Nursing, National Taiwan University College of Medicine) ;
  • Min-Shu Hsieh (Department of Pathology, National Taiwan University Hospital, National Taiwan University College of Medicine) ;
  • Chieh-Chang Chen (Department of Internal Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine) ;
  • Tzu-Chan Hong (Department of Internal Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine) ;
  • Chi-Lun Ko (Department of Nuclear Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine) ;
  • Yen-Wen Wu (School of Medicine, College of Medicine, National Yang Ming Chiao Tung University) ;
  • Mei-Fang Cheng (Department of Nuclear Medicine, National Taiwan University Hospital, National Taiwan University College of Medicine)
  • 투고 : 2023.03.31
  • 심사 : 2023.12.31
  • 발행 : 2024.03.01

초록

Objective: We aimed to investigate whether 2-[18F]fluoro-2-deoxy-D-glucose positron emission tomography/computed tomography (2-[18F]FDG PET/CT) can aid in evaluating the risk of malignancy in ampullary tumors detected by endoscopy. Materials and Methods: This single-center retrospective cohort study analyzed 155 patients (79 male, 76 female; mean age, 65.7 ± 12.7 years) receiving 2-[18F]FDG PET/CT for endoscopy-detected ampullary tumors 5-87 days (median, 7 days) after the diagnostic endoscopy between June 2007 and December 2020. The final diagnosis was made based on histopathological findings. The PET imaging parameters were compared with clinical data and endoscopic features. A model to predict the risk of malignancy, based on PET, endoscopy, and clinical findings, was generated and validated using multivariable logistic regression analysis and an additional bootstrapping method. The final model was compared with standard endoscopy for the diagnosis of ampullary cancer using the DeLong test. Results: The mean tumor size was 17.1 ± 7.7 mm. Sixty-four (41.3%) tumors were benign, and 91 (58.7%) were malignant. Univariable analysis found that ampullary neoplasms with a blood-pool corrected peak standardized uptake value in earlyphase scan (SUVe) ≥ 1.7 were more likely to be malignant (odds ratio [OR], 16.06; 95% confidence interval [CI], 7.13-36.18; P < 0.001). Multivariable analysis identified the presence of jaundice (adjusted OR [aOR], 4.89; 95% CI, 1.80-13.33; P = 0.002), malignant traits in endoscopy (aOR, 6.80; 95% CI, 2.41-19.20; P < 0.001), SUVe ≥ 1.7 in PET (aOR, 5.43; 95% CI, 2.00-14.72; P < 0.001), and PET-detected nodal disease (aOR, 5.03; 95% CI, 1.16-21.86; P = 0.041) as independent predictors of malignancy. The model combining these four factors predicted ampullary cancers better than endoscopic diagnosis alone (area under the curve [AUC] and 95% CI: 0.925 [0.874-0.956] vs. 0.815 [0.732-0.873], P < 0.001). The model demonstrated an AUC of 0.921 (95% CI, 0.816-0.967) in candidates for endoscopic papillectomy. Conclusion: Adding 2-[18F]FDG PET/CT to endoscopy can improve the diagnosis of ampullary cancer and may help refine therapeutic decision-making, particularly when contemplating endoscopic papillectomy.

키워드

과제정보

The authors thank the Center of Statistical Consultation and Research in the Department of Medical Research for statistical assistance, and all colleagues in the Nuclear Medicine Department for image acquisition and processing. The authors also thank the National Taiwan University Hospital and National Taiwan University College of Medicine for their generous support.

참고문헌

  1. Campbell DR Jr, Lee JH. A comprehensive approach to the management of benign and malignant ampullary lesions: management in hereditary and sporadic settings. Curr Gastroenterol Rep 2020;22:46
  2. Ramai D, Ofosu A, Singh J, John F, Reddy M, Adler DG. Demographics, tumor characteristics, treatment, and clinical outcomes of patients with ampullary cancer: a surveillance, epidemiology, and end results (SEER) cohort study. Minerva Gastroenterol Dietol 2019;65:85-90 https://doi.org/10.23736/S1121-421X.18.02543-6
  3. Vanbiervliet G, Strijker M, Arvanitakis M, Aelvoet A, Arnelo U, Beyna T, et al. Endoscopic management of ampullary tumors: European Society of Gastrointestinal Endoscopy (ESGE) guideline. Endoscopy 2021;53:429-448 https://doi.org/10.1055/a-1397-3198
  4. Itoi T, Ryozawa S, Katanuma A, Kawashima H, Iwasaki E, Hashimoto S, et al. Clinical practice guidelines for endoscopic papillectomy. Dig Endosc 2022;34:394-411 https://doi.org/10.1111/den.14233
  5. Panzeri F, Crippa S, Castelli P, Aleotti F, Pucci A, Partelli S, et al. Management of ampullary neoplasms: a tailored approach between endoscopy and surgery. World J Gastroenterol 2015;21:7970-7987 https://doi.org/10.3748/wjg.v21.i26.7970
  6. Ardengh JC, Kemp R, Lima-Filho ER, Dos Santos JS. Endoscopic papillectomy: the limits of the indication, technique and results. World J Gastrointest Endosc 2015;7:987-994 https://doi.org/10.4253/wjge.v7.i10.987
  7. Moon JH, Choi HJ, Lee YN. Current status of endoscopic papillectomy for ampullary tumors. Gut Liver 2014;8:598-604 https://doi.org/10.5009/gnl14099
  8. Yamamoto K, Iwasaki E, Itoi T. Insights and updates on endoscopic papillectomy. Expert Rev Gastroenterol Hepatol 2020;14:435-444 https://doi.org/10.1080/17474124.2020.1766965
  9. Sahar N, Krishnamoorthi R, Kozarek RA, Gluck M, Larsen M, Ross AS, et al. Long-term outcomes of endoscopic papillectomy for ampullary adenomas. Dig Dis Sci 2020;65:260-268 https://doi.org/10.1007/s10620-019-05812-2
  10. Spadaccini M, Fugazza A, Frazzoni L, Leo MD, Auriemma F, Carrara S, et al. Endoscopic papillectomy for neoplastic ampullary lesions: a systematic review with pooled analysis. United European Gastroenterol J 2020;8:44-51 https://doi.org/10.1177/2050640619868367
  11. Winter JM, Cameron JL, Olino K, Herman JM, de Jong MC, Hruban RH, et al. Clinicopathologic analysis of ampullary neoplasms in 450 patients: implications for surgical strategy and long-term prognosis. J Gastrointest Surg 2010;14:379-387 https://doi.org/10.1007/s11605-009-1080-7
  12. ASGE Standards of Practice Committee; Chathadi KV, Khashab MA, Acosta RD, Chandrasekhara V, Eloubeidi MA, Faulx AL, et al. The role of endoscopy in ampullary and duodenal adenomas. Gastrointest Endosc 2015;82:773-781 https://doi.org/10.1016/j.gie.2015.06.027
  13. Angthong W, Jiarakoop K, Tangtiang K. Differentiation of benign and malignant ampullary obstruction by multi-row detector CT. Jpn J Radiol 2018;36:477-488 https://doi.org/10.1007/s11604-018-0746-z
  14. Artifon EL, Couto D Jr, Sakai P, da Silveira EB. Prospective evaluation of EUS versus CT scan for staging of ampullary cancer. Gastrointest Endosc 2009;70:290-296 https://doi.org/10.1016/j.gie.2008.11.045
  15. Cannon ME, Carpenter SL, Elta GH, Nostrant TT, Kochman ML, Ginsberg GG, et al. EUS compared with CT, magnetic resonance imaging, and angiography and the influence of biliary stenting on staging accuracy of ampullary neoplasms. Gastrointest Endosc 1999;50:27-33 https://doi.org/10.1016/S0016-5107(99)70340-8
  16. Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging 2015;42:328-354 https://doi.org/10.1007/s00259-014-2961-x
  17. Mohamadien NRA, Sayed MHM. Correlation between semiquantitative and volumetric 18F-FDG PET/computed tomography parameters and Ki-67 expression in breast cancer. Nucl Med Commun 2021;42:656-664 https://doi.org/10.1097/MNM.0000000000001376
  18. Brito AF, Abrantes AM, Ribeiro M, Oliveira R, Casalta-Lopes J, Goncalves AC, et al. Fluorine-18 fluorodeoxyglucose uptake in hepatocellular carcinoma: correlation with glucose transporters and p53 expression. J Clin Exp Hepatol 2015;5:183-189 https://doi.org/10.1016/j.jceh.2015.05.003
  19. Iwamoto M, Kawada K, Nakamoto Y, Itatani Y, Inamoto S, Toda K, et al. Regulation of 18F-FDG accumulation in colorectal cancer cells with mutated KRAS. J Nucl Med 2014;55:2038-2044 https://doi.org/10.2967/jnumed.114.142927
  20. Kim BJ, Jang HJ, Kim JH, Kim HS, Lee J. KRAS mutation as a prognostic factor in ampullary adenocarcinoma: a metaanalysis and review. Oncotarget 2016;7:58001-58006 https://doi.org/10.18632/oncotarget.11156
  21. Kubota K, Fujita Y, Sato T, Watanabe S, Hosono K, Yoneda M, et al. Tumor diameter and Ki-67 expression in biopsy could be diagnostic markers discriminating from adenoma and early stage cancer in patients with ampullary tumors. J Hepatobiliary Pancreat Sci 2013;20:531-537 https://doi.org/10.1007/s00534-013-0594-2
  22. Chakraborty S, Ecker BL, Seier K, Aveson VG, Balachandran VP, Drebin JA, et al. Genome-derived classification signature for ampullary adenocarcinoma to improve clinical cancer care. Clin Cancer Res 2021;27:5891-5899 https://doi.org/10.1158/1078-0432.CCR-21-1906
  23. Chuang PJ, Wang HP, Lin YJ, Chen CC, Tien YW, Hsieh MS, et al. Preoperative 2-[18F]FDG PET-CT aids in the prognostic stratification for patients with primary ampullary carcinoma. Eur Radiol 2021;31:8040-8049 https://doi.org/10.1007/s00330-021-07923-9
  24. Park YM, Seo HI. Predictive value of metabolic activity detected by pre-operative 18F FDG PET/CT in ampullary adenocarcinoma. Medicine (Baltimore) 2021;100:e27561
  25. Watanabe A, Harimoto N, Araki K, Kubo N, Igarashi T, Tsukagoshi M, et al. FDG-PET for preoperative evaluation of tumor invasion in ampullary cancer: a retrospective analysis. J Surg Oncol 2021;124:317-323 https://doi.org/10.1002/jso.26513
  26. Jamar F, Buscombe J, Chiti A, Christian PE, Delbeke D, Donohoe KJ, et al. EANM/SNMMI guideline for 18F-FDG use in inflammation and infection. J Nucl Med 2013;54:647-658 https://doi.org/10.2967/jnumed.112.112524
  27. Cheng MF, Wang HP, Tien YW, Liu KL, Yen RF, Tzen KY, et al. Usefulness of PET/CT for the differentiation and characterization of periampullary lesions. Clin Nucl Med 2013;38:703-708 https://doi.org/10.1097/RLU.0b013e31829b266a
  28. Lasnon C, Desmonts C, Quak E, Gervais R, Do P, Dubos-Arvis C, et al. Harmonizing SUVs in multicentre trials when using different generation PET systems: prospective validation in non-small cell lung cancer patients. Eur J Nucl Med Mol Imaging 2013;40:985-996 https://doi.org/10.1007/s00259-013-2391-1
  29. Sunderland JJ, Christian PE. Quantitative PET/CT scanner performance characterization based upon the society of nuclear medicine and molecular imaging clinical trials network oncology clinical simulator phantom. J Nucl Med 2015;56:145-152 https://doi.org/10.2967/jnumed.114.148056
  30. Koppula BR, Fine GC, Salem AE, Covington MF, Wiggins RH, Hoffman JM, et al. PET-CT in clinical adult oncology: III. Gastrointestinal malignancies. Cancers (Basel) 2022;14:2668
  31. Sher A, Lacoeuille F, Fosse P, Vervueren L, Cahouet-Vannier A, Dabli D, et al. For avid glucose tumors, the SUV peak is the most reliable parameter for [(18)F]FDG-PET/CT quantification, regardless of acquisition time. EJNMMI Res 2016;6:21
  32. Jia G, Zhang J, Li R, Yan J, Zuo C. The exploration of quantitative intra-tumoral metabolic heterogeneity in dual-time 18F-FDG PET/CT of pancreatic cancer. Abdom Radiol (NY) 2021;46:4218-4225 https://doi.org/10.1007/s00261-021-03068-x
  33. Unal I. Defining an optimal cut-point value in ROC analysis: an alternative approach. Comput Math Methods Med 2017;2017:3762651
  34. Choi HJ, Kang CM, Jo K, Lee WJ, Lee JH, Ryu YH, et al. Prognostic significance of standardized uptake value on preoperative 18F-FDG PET/CT in patients with ampullary adenocarcinoma. Eur J Nucl Med Mol Imaging 2015;42:841-847 https://doi.org/10.1007/s00259-014-2907-3
  35. Wen G, Gu J, Zhou W, Wang L, Tian Y, Dong Y, et al. Benefits of 18F-FDG PET/CT for the preoperative characterisation or staging of disease in the ampullary and duodenal papillary. Eur Radiol 2020;30:5089-5098 https://doi.org/10.1007/s00330-020-06864-z
  36. Kawada N, Uehara H, Hosoki T, Takami M, Shiroeda H, Arisawa T, et al. Usefulness of dual-phase 18F-FDG PET/CT for diagnosing small pancreatic tumors. Pancreas 2015;44:655-659 https://doi.org/10.1097/MPA.0000000000000313
  37. Raj P, Kaman L, Singh R, Dahyia D, Bhattacharya A, Bal A. Sensitivity and specificity of FDG PET-CT scan in detecting lymph node metastasis in operable periampullary tumours in correlation with the final histopathology after curative surgery. Updates Surg 2013;65:103-107 https://doi.org/10.1007/s13304-013-0205-4
  38. Chen CH, Yang CC, Yeh YH, Chou DA, Nien CK. Reappraisal of endosonography of ampullary tumors: correlation with transabdominal sonography, CT, and MRI. J Clin Ultrasound 2009;37:18-25 https://doi.org/10.1002/jcu.20523
  39. Alexakis N, Gomatos IP, Sbarounis S, Toutouzas K, Katsaragakis S, Zografos G, et al. High serum CA 19-9 but not tumor size should select patients for staging laparoscopy in radiological resectable pancreas head and peri-ampullary cancer. Eur J Surg Oncol 2015;41:265-269 https://doi.org/10.1016/j.ejso.2014.09.006
  40. Lin MS, Huang JX, Yu H. Elevated serum level of carbohydrate antigen 19-9 in benign biliary stricture diseases can reduce its value as a tumor marker. Int J Clin Exp Med 2014;7:744-750
  41. Jin X, Wu Y. Diagnostic utility of clinical and biochemical parameters in pancreatic head malignancy patients with normal carbohydrate antigen 19-9 levels. Afr Health Sci 2015;15:123-130 https://doi.org/10.4314/ahs.v15i1.17
  42. Shi X, Yang J, Liu M, Zhang Y, Zhou Z, Luo W, et al. Circular RNA ANAPC7 inhibits tumor growth and muscle wasting via PHLPP2-AKT-TGF-β signaling axis in pancreatic cancer. Gastroenterology 2022;162:2004-2017.e2 https://doi.org/10.1053/j.gastro.2022.02.017