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Published in: BMC Gastroenterology 1/2024

Open Access 01-12-2024 | Autoimmune Pancreatitis | Research

Potential Added Value of 18F-FDG PET Metabolic Parameters in Predicting Disease Relapse in Type 1 Autoimmune Pancreatitis

Authors: Shengxin Chen, Guanyun Wang, Lang Wu, Dexin Chen, Kaixuan Fang, Wenjing Liu, Baixuan Xu, Ya-qi Zhai, Mingyang Li

Published in: BMC Gastroenterology | Issue 1/2024

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Abstract

Background

The predictive value of 18F-fluorodeoxyglucose positron emission tomography/computed tomography (18F-FDG PET/CT) metabolic parameters for predicting AIP relapse is currently unknown. This study firstly explored the value of 18F-FDG PET/CT parameters as predictors of type 1 AIP relapse.

Methods

This multicenter retrospective cohort study analyzed 51 patients who received 18F-FDG PET/CT prior to treatment and did not receive maintenance therapy after remission. The study collected baseline characteristics and clinical data and conducted qualitative and semi-quantitative analysis of pancreatic lesions and extrapancreatic organs. The study used three thresholds to select the boundaries of pancreatic lesions to evaluate metabolic parameters, including the maximum standard uptake value (SUVmax), mean standard uptake value (SUVmean), total lesion glycolysis (TLG), metabolic tumor volume (MTV), and tumor-to-normal liver standard uptake value ratio (SUVR). Univariate and multivariate analyses were performed to identify independent predictors and build a recurrence prediction model. The model was internally validated using the bootstrap method and a nomogram was created for clinical application.

Results

In the univariable analysis, the relapsed group showed higher levels of SUVmax (6.0 ± 1.6 vs. 5.2 ± 1.1; P = 0.047), SUVR (2.3 [2.0–3.0] vs. 2.0 [1.6–2.4]; P = 0.026), and TLG2.5 (234.5 ± 149.1 vs. 139.6 ± 102.5; P = 0.020) among the 18F-FDG PET metabolic parameters compared to the non-relapsed group. In the multivariable analysis, serum IgG4 (OR, 1.001; 95% CI, 1.000–1.002; P = 0.014) and TLG2.5 (OR, 1.007; 95% CI, 1.002–1.013; P = 0.012) were independent predictors associated with relapse of type 1 AIP. A receiver-operating characteristic curve of the predictive model with these two predictors demonstrated an area under the curve of 0.806.

Conclusion

18F-FDG PET/CT metabolic parameters, particularly TLG2.5, are potential predictors for relapse in patients with type 1 AIP. A multiparameter model that includes IgG4 and TLG2.5 can enhance the ability to predict AIP relapse.
Literature
1.
go back to reference Yoshida K, Toki F, Takeuchi T, Watanabe S, Shiratori K, Hayashi N. Chronic pancreatitis caused by an autoimmune abnormality. Proposal of the concept of autoimmune pancreatitis. Dig Dis Sci. 1995;40(7):1561–8.CrossRefPubMed Yoshida K, Toki F, Takeuchi T, Watanabe S, Shiratori K, Hayashi N. Chronic pancreatitis caused by an autoimmune abnormality. Proposal of the concept of autoimmune pancreatitis. Dig Dis Sci. 1995;40(7):1561–8.CrossRefPubMed
2.
go back to reference Blaho M, Dite P, Kunovsky L, Kianicka B. Autoimmune pancreatitis - an ongoing challenge. Adv Med Sci. 2020;65(2):403–8.CrossRefPubMed Blaho M, Dite P, Kunovsky L, Kianicka B. Autoimmune pancreatitis - an ongoing challenge. Adv Med Sci. 2020;65(2):403–8.CrossRefPubMed
3.
go back to reference Hart PA, Kamisawa T, Brugge WR, Chung JB, Culver EL, Czako L, Frulloni L, Go VL, Gress TM, Kim MH, et al. Long-term outcomes of autoimmune pancreatitis: a multicentre, international analysis. Gut. 2013;62(12):1771–6.CrossRefPubMed Hart PA, Kamisawa T, Brugge WR, Chung JB, Culver EL, Czako L, Frulloni L, Go VL, Gress TM, Kim MH, et al. Long-term outcomes of autoimmune pancreatitis: a multicentre, international analysis. Gut. 2013;62(12):1771–6.CrossRefPubMed
4.
go back to reference Kubota K, Kamisawa T, Hirano K, Hirooka Y, Uchida K, Ikeura T, Shiomi H, Ohara H, Shimizu K, Arakura N, et al. Clinical course of type 1 autoimmune pancreatitis patients without steroid treatment: a Japanese multicenter study of 97 patients. J Hepatobiliary Pancreat Sci. 2018;25(4):223–30.CrossRefPubMed Kubota K, Kamisawa T, Hirano K, Hirooka Y, Uchida K, Ikeura T, Shiomi H, Ohara H, Shimizu K, Arakura N, et al. Clinical course of type 1 autoimmune pancreatitis patients without steroid treatment: a Japanese multicenter study of 97 patients. J Hepatobiliary Pancreat Sci. 2018;25(4):223–30.CrossRefPubMed
5.
go back to reference Lee HW, Moon SH, Kim MH, Cho DH, Jun JH, Nam K, Song TJ, Park DH, Lee SS, Seo DW, et al. Relapse rate and predictors of relapse in a large single center cohort of type 1 autoimmune pancreatitis: long-term follow-up results after steroid therapy with short-duration maintenance treatment. J Gastroenterol. 2018;53(8):967–77.CrossRefPubMed Lee HW, Moon SH, Kim MH, Cho DH, Jun JH, Nam K, Song TJ, Park DH, Lee SS, Seo DW, et al. Relapse rate and predictors of relapse in a large single center cohort of type 1 autoimmune pancreatitis: long-term follow-up results after steroid therapy with short-duration maintenance treatment. J Gastroenterol. 2018;53(8):967–77.CrossRefPubMed
6.
go back to reference Xin L, Meng QQ, Hu LH, Lin H, Pan J, Hao L, Liu PP, Qian W, Wang LW, Li ZS. Prediction and Management for Relapse of type 1 autoimmune pancreatitis after initial steroid treatment: a long-term follow-up from China. Pancreas. 2018;47(9):1110–4.CrossRefPubMed Xin L, Meng QQ, Hu LH, Lin H, Pan J, Hao L, Liu PP, Qian W, Wang LW, Li ZS. Prediction and Management for Relapse of type 1 autoimmune pancreatitis after initial steroid treatment: a long-term follow-up from China. Pancreas. 2018;47(9):1110–4.CrossRefPubMed
7.
go back to reference Suzuki D, Shimizu K, Tokushige K. Relative rise of serum IgG4 levels after steroid therapy for autoimmune pancreatitis predicts the likelihood of relapse. Pancreas. 2018;47(4):412–7.CrossRefPubMed Suzuki D, Shimizu K, Tokushige K. Relative rise of serum IgG4 levels after steroid therapy for autoimmune pancreatitis predicts the likelihood of relapse. Pancreas. 2018;47(4):412–7.CrossRefPubMed
8.
go back to reference Kubota K, Kamisawa T, Okazaki K, Kawa S, Hirano K, Hirooka Y, Uchida K, Shiomi H, Ohara H, Shimizu K, et al. Low-dose maintenance steroid treatment could reduce the relapse rate in patients with type 1 autoimmune pancreatitis: a long-term Japanese multicenter analysis of 510 patients. J Gastroenterol. 2017;52(8):955–64.CrossRefPubMed Kubota K, Kamisawa T, Okazaki K, Kawa S, Hirano K, Hirooka Y, Uchida K, Shiomi H, Ohara H, Shimizu K, et al. Low-dose maintenance steroid treatment could reduce the relapse rate in patients with type 1 autoimmune pancreatitis: a long-term Japanese multicenter analysis of 510 patients. J Gastroenterol. 2017;52(8):955–64.CrossRefPubMed
9.
go back to reference Nakamura A, Ozawa M, Watanabe T, Ito T, Muraki T, Hamano H, Koinuma M, Kawa S. Predictive factors for autoimmune pancreatitis relapse after 3 years of maintenance therapy. Pancreas. 2018;47(10):1337–43.CrossRefPubMed Nakamura A, Ozawa M, Watanabe T, Ito T, Muraki T, Hamano H, Koinuma M, Kawa S. Predictive factors for autoimmune pancreatitis relapse after 3 years of maintenance therapy. Pancreas. 2018;47(10):1337–43.CrossRefPubMed
10.
go back to reference Okazaki K, Chari ST, Frulloni L, Lerch MM, Kamisawa T, Kawa S, Kim MH, Levy P, Masamune A, Webster G, et al. International consensus for the treatment of autoimmune pancreatitis. Pancreatology. 2017;17(1):1–6.CrossRefPubMed Okazaki K, Chari ST, Frulloni L, Lerch MM, Kamisawa T, Kawa S, Kim MH, Levy P, Masamune A, Webster G, et al. International consensus for the treatment of autoimmune pancreatitis. Pancreatology. 2017;17(1):1–6.CrossRefPubMed
11.
go back to reference Mi L, Zhao Y, Zhao X, Yin F, Yin X, Li N, Shi J, Han X, Duan X, Zhao M, et al. (18)F-Fluorodeoxyglucose positron emission tomography-computed tomography metabolic parameters before and after Neoadjuvant chemotherapy can predict the postoperative prognosis of locally advanced gastric Cancer. Cancer Biother Radiopharm. 2021;36(8):662–71.PubMed Mi L, Zhao Y, Zhao X, Yin F, Yin X, Li N, Shi J, Han X, Duan X, Zhao M, et al. (18)F-Fluorodeoxyglucose positron emission tomography-computed tomography metabolic parameters before and after Neoadjuvant chemotherapy can predict the postoperative prognosis of locally advanced gastric Cancer. Cancer Biother Radiopharm. 2021;36(8):662–71.PubMed
12.
go back to reference Jo JH, Chung HW, So Y, Yoo YB, Park KS, Nam SE, Lee EJ, Noh WC. FDG PET/CT to predict recurrence of early breast invasive ductal carcinoma. Diagnostics (Basel). 2022;12(3):694.CrossRefPubMedPubMedCentral Jo JH, Chung HW, So Y, Yoo YB, Park KS, Nam SE, Lee EJ, Noh WC. FDG PET/CT to predict recurrence of early breast invasive ductal carcinoma. Diagnostics (Basel). 2022;12(3):694.CrossRefPubMedPubMedCentral
13.
go back to reference Glaudemans AW, de Vries EF, Galli F, Dierckx RA, Slart RH, Signore A. The use of (18)F-FDG-PET/CT for diagnosis and treatment monitoring of inflammatory and infectious diseases. Clin Dev Immunol. 2013;2013:623036.CrossRefPubMedPubMedCentral Glaudemans AW, de Vries EF, Galli F, Dierckx RA, Slart RH, Signore A. The use of (18)F-FDG-PET/CT for diagnosis and treatment monitoring of inflammatory and infectious diseases. Clin Dev Immunol. 2013;2013:623036.CrossRefPubMedPubMedCentral
14.
go back to reference Shimosegawa T, Chari ST, Frulloni L, Kamisawa T, Kawa S, Mino-Kenudson M, Kim MH, Kloppel G, Lerch MM, Lohr M, et al. International consensus diagnostic criteria for autoimmune pancreatitis: guidelines of the International Association of Pancreatology. Pancreas. 2011;40(3):352–8.CrossRefPubMed Shimosegawa T, Chari ST, Frulloni L, Kamisawa T, Kawa S, Mino-Kenudson M, Kim MH, Kloppel G, Lerch MM, Lohr M, et al. International consensus diagnostic criteria for autoimmune pancreatitis: guidelines of the International Association of Pancreatology. Pancreas. 2011;40(3):352–8.CrossRefPubMed
15.
go back to reference Masamune A, Nishimori I, Kikuta K, Tsuji I, Mizuno N, Iiyama T, Kanno A, Tachibana Y, Ito T, Kamisawa T, et al. Randomised controlled trial of long-term maintenance corticosteroid therapy in patients with autoimmune pancreatitis. Gut. 2017;66(3):487–94.CrossRefPubMed Masamune A, Nishimori I, Kikuta K, Tsuji I, Mizuno N, Iiyama T, Kanno A, Tachibana Y, Ito T, Kamisawa T, et al. Randomised controlled trial of long-term maintenance corticosteroid therapy in patients with autoimmune pancreatitis. Gut. 2017;66(3):487–94.CrossRefPubMed
16.
go back to reference Kim HM, Chung MJ, Chung JB. Remission and relapse of autoimmune pancreatitis: focusing on corticosteroid treatment. Pancreas. 2010;39(5):555–60.CrossRefPubMed Kim HM, Chung MJ, Chung JB. Remission and relapse of autoimmune pancreatitis: focusing on corticosteroid treatment. Pancreas. 2010;39(5):555–60.CrossRefPubMed
17.
go back to reference Hirano K, Tada M, Isayama H, Sasahira N, Umefune G, Akiyama D, Watanabe T, Saito T, Takagi K, Takahara N, et al. Outcome of long-term maintenance steroid therapy cessation in patients with autoimmune pancreatitis: a prospective study. J Clin Gastroenterol. 2016;50(4):331–7.CrossRefPubMed Hirano K, Tada M, Isayama H, Sasahira N, Umefune G, Akiyama D, Watanabe T, Saito T, Takagi K, Takahara N, et al. Outcome of long-term maintenance steroid therapy cessation in patients with autoimmune pancreatitis: a prospective study. J Clin Gastroenterol. 2016;50(4):331–7.CrossRefPubMed
18.
go back to reference Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, Verzijlbergen FJ, Barrington SF, Pike LC, Weber WA, et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging. 2015;42(2):328–54.CrossRefPubMed Boellaard R, Delgado-Bolton R, Oyen WJ, Giammarile F, Tatsch K, Eschner W, Verzijlbergen FJ, Barrington SF, Pike LC, Weber WA, et al. FDG PET/CT: EANM procedure guidelines for tumour imaging: version 2.0. Eur J Nucl Med Mol Imaging. 2015;42(2):328–54.CrossRefPubMed
19.
go back to reference Ohtani M, Ofuji K, Akazawa Y, Saito Y, Nosaka T, Ozaki Y, Takahashi K, Naito T, Matsuda H, Hiramatsu K, et al. Clinical usefulness of [18F]-Fluoro-2-Deoxy-d-glucose-positron emission tomography/computed tomography for distinguishing between autoimmune pancreatitis and pancreatic Cancer. Pancreas. 2021;50(7):1014–9.CrossRefPubMed Ohtani M, Ofuji K, Akazawa Y, Saito Y, Nosaka T, Ozaki Y, Takahashi K, Naito T, Matsuda H, Hiramatsu K, et al. Clinical usefulness of [18F]-Fluoro-2-Deoxy-d-glucose-positron emission tomography/computed tomography for distinguishing between autoimmune pancreatitis and pancreatic Cancer. Pancreas. 2021;50(7):1014–9.CrossRefPubMed
20.
go back to reference Okazaki K, Kawa S, Kamisawa T, Ikeura T, Itoi T, Ito T, Inui K, Irisawa A, Uchida K, Ohara H, et al. Amendment of the Japanese consensus guidelines for autoimmune pancreatitis, 2020. J Gastroenterol. 2022;57(4):225–45.CrossRefPubMedPubMedCentral Okazaki K, Kawa S, Kamisawa T, Ikeura T, Itoi T, Ito T, Inui K, Irisawa A, Uchida K, Ohara H, et al. Amendment of the Japanese consensus guidelines for autoimmune pancreatitis, 2020. J Gastroenterol. 2022;57(4):225–45.CrossRefPubMedPubMedCentral
21.
go back to reference Kubota K, Watanabe S, Uchiyama T, Kato S, Sekino Y, Suzuki K, Mawatari H, Iida H, Endo H, Fujita K, et al. Factors predictive of relapse and spontaneous remission of autoimmune pancreatitis patients treated/not treated with corticosteroids. J Gastroenterol. 2011;46(6):834–42.CrossRefPubMed Kubota K, Watanabe S, Uchiyama T, Kato S, Sekino Y, Suzuki K, Mawatari H, Iida H, Endo H, Fujita K, et al. Factors predictive of relapse and spontaneous remission of autoimmune pancreatitis patients treated/not treated with corticosteroids. J Gastroenterol. 2011;46(6):834–42.CrossRefPubMed
22.
go back to reference Maire F, Le Baleur Y, Rebours V, Vullierme MP, Couvelard A, Voitot H, Sauvanet A, Hentic O, Levy P, Ruszniewski P, et al. Outcome of patients with type 1 or 2 autoimmune pancreatitis. Am J Gastroenterol. 2011;106(1):151–6.CrossRefPubMed Maire F, Le Baleur Y, Rebours V, Vullierme MP, Couvelard A, Voitot H, Sauvanet A, Hentic O, Levy P, Ruszniewski P, et al. Outcome of patients with type 1 or 2 autoimmune pancreatitis. Am J Gastroenterol. 2011;106(1):151–6.CrossRefPubMed
24.
go back to reference Zhang J, Jia G, Zuo C, Jia N, Wang H. (18)F- FDG PET/CT helps differentiate autoimmune pancreatitis from pancreatic cancer. BMC Cancer. 2017;17(1):695.CrossRefPubMedPubMedCentral Zhang J, Jia G, Zuo C, Jia N, Wang H. (18)F- FDG PET/CT helps differentiate autoimmune pancreatitis from pancreatic cancer. BMC Cancer. 2017;17(1):695.CrossRefPubMedPubMedCentral
25.
go back to reference Nakajo M, Jinnouchi S, Fukukura Y, Tanabe H, Tateno R, Nakajo M. The efficacy of whole-body FDG-PET or PET/CT for autoimmune pancreatitis and associated extrapancreatic autoimmune lesions. Eur J Nucl Med Mol Imaging. 2007;34(12):2088–95.CrossRefPubMed Nakajo M, Jinnouchi S, Fukukura Y, Tanabe H, Tateno R, Nakajo M. The efficacy of whole-body FDG-PET or PET/CT for autoimmune pancreatitis and associated extrapancreatic autoimmune lesions. Eur J Nucl Med Mol Imaging. 2007;34(12):2088–95.CrossRefPubMed
26.
go back to reference Mitamura K, Arai-Okuda H, Yamamoto Y, Norikane T, Takami Y, Fujimoto K, Wakiya R, Ozaki H, Dobashi H, Nishiyama Y. Disease activity and response to therapy monitored by [(18)F]FDG PET/CT using volume-based indices in IgG4-related disease. EJNMMI Res. 2020;10(1):153.CrossRefPubMedPubMedCentral Mitamura K, Arai-Okuda H, Yamamoto Y, Norikane T, Takami Y, Fujimoto K, Wakiya R, Ozaki H, Dobashi H, Nishiyama Y. Disease activity and response to therapy monitored by [(18)F]FDG PET/CT using volume-based indices in IgG4-related disease. EJNMMI Res. 2020;10(1):153.CrossRefPubMedPubMedCentral
27.
go back to reference Ishii Y, Serikawa M, Sasaki T, Fujimoto Y, Yamaguchi A, Ogawa T, Noma B, Okazaki A, Yukutake M, Ishigaki T, et al. Impact of sclerosing dacryoadenitis/sialadenitis on relapse during steroid therapy in patients with type 1 autoimmune pancreatitis. Scand J Gastroenterol. 2019;54(2):259–64.CrossRefPubMed Ishii Y, Serikawa M, Sasaki T, Fujimoto Y, Yamaguchi A, Ogawa T, Noma B, Okazaki A, Yukutake M, Ishigaki T, et al. Impact of sclerosing dacryoadenitis/sialadenitis on relapse during steroid therapy in patients with type 1 autoimmune pancreatitis. Scand J Gastroenterol. 2019;54(2):259–64.CrossRefPubMed
28.
go back to reference Kuruma S, Kamisawa T, Tabata T, Hara S, Fujiwara T, Kuwata G, Egarashira H, Koizumi K, Setoguchi K, Fujiwara J, et al. Clinical characteristics of patients with autoimmune pancreatitis with or without Mikulicz's disease and Mikulicz's disease alone. Gut Liver. 2013;7(1):96–9.CrossRefPubMed Kuruma S, Kamisawa T, Tabata T, Hara S, Fujiwara T, Kuwata G, Egarashira H, Koizumi K, Setoguchi K, Fujiwara J, et al. Clinical characteristics of patients with autoimmune pancreatitis with or without Mikulicz's disease and Mikulicz's disease alone. Gut Liver. 2013;7(1):96–9.CrossRefPubMed
Metadata
Title
Potential Added Value of 18F-FDG PET Metabolic Parameters in Predicting Disease Relapse in Type 1 Autoimmune Pancreatitis
Authors
Shengxin Chen
Guanyun Wang
Lang Wu
Dexin Chen
Kaixuan Fang
Wenjing Liu
Baixuan Xu
Ya-qi Zhai
Mingyang Li
Publication date
01-12-2024
Publisher
BioMed Central
Published in
BMC Gastroenterology / Issue 1/2024
Electronic ISSN: 1471-230X
DOI
https://doi.org/10.1186/s12876-023-03113-7

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