Skip to main content

Advertisement

SpringerLink
Log in

Autoimmune pancreatitis complicated with inflammatory bowel disease and comparative study of type 1 and type 2 autoimmune pancreatitis

  • Original Article—Liver, Pancreas, and Biliary Tract
  • Published:
Journal of Gastroenterology Aims and scope Submit manuscript

Abstract

Background

Two types of autoimmune pancreatitis (AIP) have been reported, lymphoplasmacytic sclerosing pancreatitis and idiopathic duct-centric chronic pancreatitis (IDCP), which are now recognized as type 1 and type 2 AIP, respectively. Since the clinical features of type 2 AIP have not been fully elucidated and this condition is frequently accompanied by inflammatory bowel disease (IBD), we performed a nationwide survey of patients with AIP complicated with IBD to precisely characterize this disease entity.

Methods

We collected 138 cases of pancreatitis with complicating IBD from affiliated institutes specializing in AIP or IBD, and comparative study between the IDCP groups and type 1 AIP was performed.

Results

Histological examination revealed 15 AIP cases to be IDCP of institutional diagnosis, among which 11 cases were upgraded to IDCP of central diagnosis by an expert pathologist. The IDCP group exhibited younger onset age, no gender bias, frequent abdominal pain, and normal IgG4 value, similar to those of type 2 AIP reported previously. We also witnessed a lower prevalence of jaundice in type 2 AIP than in type 1 AIP that corresponded to imaging findings of less frequent pancreatic head swelling and scarce bile duct stenosis.

Conclusions

A characteristic feature of type 2 AIP compared with type 1 AIP is a low frequency of obstructive jaundice that is related to rare lower bile duct stricture due to lower prevalence of pancreatic head swelling. Contrary to type 1 AIP, lower bile duct stricture in this condition has no apparent relation to sclerosing cholangitis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Kawa S, Hamano H, Kiyosawa K. Autoimmune pancreatitis and IgG4-related disease. In: Rose N, MacKay I, editors. The autoimmune diseases. 5th ed. St Louis: Academic Press; 2013. p. 935–49.

    Google Scholar 

  2. Toki F, Kozu T, Oi I, Nakasato T, Suzuki M, Hanyu F. An unusual type of chronic pancreatitis showing diffuse irregular narrowing of the entire main pancreatic duct on ERCP—a report of four cases. Endoscopy. 1992;24:640.

    Google Scholar 

  3. 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;40:1561–8.

    Article  CAS  PubMed  Google Scholar 

  4. Hamano H, Kawa S, Horiuchi A, Unno H, Furuya N, Akamatsu T, et al. High serum IgG4 concentrations in patients with sclerosing pancreatitis. New Engl J Med. 2001;344:732–8.

    Article  CAS  PubMed  Google Scholar 

  5. Hamano H, Kawa S, Ochi Y, Unno H, Shiba N, Wajiki M, et al. Hydronephrosis associated with retroperitoneal fibrosis and sclerosing pancreatitis. Lancet. 2002;359:1403–4.

    Article  PubMed  Google Scholar 

  6. Kawaguchi K, Koike M, Tsuruta K, Okamoto A, Tabata I, Fujita N. Lymphoplasmacytic sclerosing pancreatitis with cholangitis: a variant of primary sclerosing cholangitis extensively involving pancreas. Hum Pathol. 1991;22:387–95.

    Article  CAS  PubMed  Google Scholar 

  7. Notohara K, Burgart LJ, Yadav D, Chari S, Smyrk TC. Idiopathic chronic pancreatitis with periductal lymphoplasmacytic infiltration: clinicopathologic features of 35 cases. Am J Surg Pathol. 2003;27:1119–27.

    Article  PubMed  Google Scholar 

  8. Zamboni G, Luttges J, Capelli P, Frulloni L, Cavallini G, Pederzoli P, et al. Histopathological features of diagnostic and clinical relevance in autoimmune pancreatitis: a study on 53 resection specimens and 9 biopsy specimens. Virchows Arch. 2004;445:552–63.

    Article  PubMed  Google Scholar 

  9. Sugumar A, Kloppel G, Chari ST. Autoimmune pancreatitis: pathologic subtypes and their implications for its diagnosis. Am J Gastroenterol. 2009;104:2308–10.

    Article  PubMed  Google Scholar 

  10. Chari ST, Kloeppel G, Zhang L, Notohara K, Lerch MM, Shimosegawa T. Histopathologic and clinical subtypes of autoimmune pancreatitis: the Honolulu consensus document. Pancreatology. 2010;10:664–72.

    Article  PubMed  Google Scholar 

  11. Shimosegawa T, Chari ST, Frulloni L, Kamisawa T, Kawa S, Mino-Kenudson M, et al. International consensus diagnostic criteria for autoimmune pancreatitis: guidelines of the International Association of Pancreatology. Pancreas. 2011;40:352–8.

    Article  PubMed  Google Scholar 

  12. Song TJ, Kim JH, Kim MH, Jang JW, do Park H, Lee SS, et al. Comparison of clinical findings between histologically confirmed type 1 and type 2 autoimmune pancreatitis. J Gastroenterol Hepatol. 2012;27:700–8.

    Article  CAS  PubMed  Google Scholar 

  13. Kloppel G, Detlefsen S, Chari ST, Longnecker DS, Zamboni G. Autoimmune pancreatitis: the clinicopathological characteristics of the subtype with granulocytic epithelial lesions. J Gastroenterol. 2010;45:787–93.

    Article  PubMed  Google Scholar 

  14. Kusuda T, Uchida K, Satoi S, Koyabu M, Fukata N, Miyoshi H, et al. Idiopathic duct-centric pancreatitis (IDCP) with immunological studies. Intern Med. 2010;49:2569–75.

    Article  PubMed  Google Scholar 

  15. Ishikawa T, Itoh A, Kawashima H, Ohno E, Matsubara H, Itoh Y, et al. Endoscopic ultrasound-guided fine needle aspiration in the differentiation of type 1 and type 2 autoimmune pancreatitis. World J Gastroenterol. 2012;18:3883–8.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Maire F, Le Baleur Y, Rebours V, Vullierme MP, Couvelard A, Voitot H, et al. Outcome of patients with type 1 or 2 autoimmune pancreatitis. Am J Gastroenterol. 2011;106:151–6.

    Article  CAS  PubMed  Google Scholar 

  17. Oishi Y, Yao T, Matsui T, Ueki T, Sakurai T, Sakaguchi S. Abnormal pancreatic imaging in Crohn’s disease: prevalence and clinical features. J Gastroenterol. 2004;39:26–33.

    Article  PubMed  Google Scholar 

  18. Kanno A, Ishida K, Hamada S, Fujishima F, Unno J, Kume K, et al. Diagnosis of autoimmune pancreatitis by EUS-FNA by using a 22-gauge needle based on the International Consensus Diagnostic Criteria. Gastrointest Endosc. 2012;76:594–602.

    Article  PubMed  Google Scholar 

  19. Ikeura T, Takaoka M, Uchida K, Shimatani M, Miyoshi H, Kusuda T, et al. Autoimmune pancreatitis with histologically proven lymphoplasmacytic sclerosing pancreatitis with granulocytic epithelial lesions. Intern Med. 2012;51:733–7.

    Article  PubMed  Google Scholar 

  20. Ueki T, Kawamoto K, Otsuka Y, Minoda R, Maruo T, Matsumura K et al. Prevalence and clinicopathological features of autoimmune pancreatitis in the Japanese patients with inflammatory bowel disease. Pancreas (in press).

  21. Okano A, Hajiro K, Takakuwa H, Nishio A. Pseudotumorous pancreatitis associated with ulcerative colitis. Intern Med. 2001;40:1205–8.

    Article  CAS  PubMed  Google Scholar 

  22. Toda N, Akahane M, Kiryu S, Matsubara Y, Yamaji Y, Okamoto M, et al. Pancreas duct abnormalities in patients with ulcerative colitis: a magnetic resonance pancreatography study. Inflamm Bowel Dis. 2005;11:903–8.

    Article  PubMed  Google Scholar 

  23. Nve E, Ribe D, Navines J, Villanueva MJ, Franch G, Torrecilla A, et al. Idiopathic fibrosing pancreatitis associated with ulcerative colitis. HPB: Off J Int Hepato Pancreato Biliary Assoc. 2006;8:153–5.

    CAS  Google Scholar 

  24. Shimosegawa T. The amendment of the Clinical Diagnostic Criteria in Japan (JPS2011) in response to the proposal of the International Consensus of Diagnostic Criteria (ICDC) for autoimmune pancreatitis. Pancreas. 2012;41:1341–2.

    Article  PubMed  Google Scholar 

  25. Pitchumoni CS, Rubin A, Das K. Pancreatitis in inflammatory bowel diseases. J Clin Gastroenterol. 2010;44:246–53.

    Article  CAS  PubMed  Google Scholar 

  26. Park SH, Kim D, Ye BD, Yang SK, Kim JH, Yang DH, et al. The characteristics of ulcerative colitis associated with autoimmune pancreatitis. J Clin Gastroenterol. 2013;47:520–5.

    Article  CAS  PubMed  Google Scholar 

  27. Hart PA, Kamisawa T, Brugge WR, Chung JB, Culver EL, Czako L, et al. Long-term outcomes of autoimmune pancreatitis: a multicentre, international analysis. Gut. 2013;62:1771–6.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Sah RP, Chari ST, Pannala R, Sugumar A, Clain JE, Levy MJ, et al. Differences in clinical profile and relapse rate of type 1 versus type 2 autoimmune pancreatitis. Gastroenterology. 2010;139:140–8 quiz e112–143.

    Article  PubMed  Google Scholar 

  29. Kamisawa T, Chari ST, Giday SA, Kim MH, Chung JB, Lee KT, et al. Clinical profile of autoimmune pancreatitis and its histological subtypes: an international multicenter survey. Pancreas. 2011;40:809–14.

    Article  CAS  PubMed  Google Scholar 

  30. Hirano K, Tada M, Isayama H, Yamamoto K, Mizuno S, Yagioka H, et al. Endoscopic evaluation of factors contributing to intrapancreatic biliary stricture in autoimmune pancreatitis. Gastrointest Endosc. 2010;71:85–90.

    Article  PubMed  Google Scholar 

  31. Naitoh I, Nakazawa T, Ohara H, Ando T, Hayashi K, Tanaka H, et al. Endoscopic transpapillary intraductal ultrasonography and biopsy in the diagnosis of IgG4-related sclerosing cholangitis. J Gastroenterol. 2009;44:1147–55.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported partially by the Research Program of Intractable Disease provided by the Ministry of Health, Labor, and Welfare of Japan. We thank Trevor Ralph for his English editorial assistance.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Center for Health, Safety, and Environmental Management, Shinshu University, 3-1-1 Asahi, Matsumoto, 390-8621, Japan

    Shigeyuki Kawa

  2. Department of Gastroenterology and Hepatology, Kansai Medical University, Osaka, Japan

    Kazuichi Okazaki

  3. Department of Anatomic Pathology, Kurashiki Central Hospital, Kurashiki, Japan

    Kenji Notohara

  4. Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Japan

    Mamoru Watanabe

  5. Department of Gastroenterology and Hepatology, Graduate School of Tokyo Medical and Dental University, Tokyo, Japan

    Tooru Shimosegawa

Authors
  1. Shigeyuki Kawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kazuichi Okazaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kenji Notohara
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mamoru Watanabe
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tooru Shimosegawa
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

Study Group for Pancreatitis Complicated with Inflammatory Bowel Disease organized by The Research Committee for Intractable Pancreatic Disease (Chairman: Tooru Shimosegawa) and The Research Committee for Intractable Inflammatory Bowel Disease (Chairman: Mamoru Watanabe), both of which are supported by the Ministry of Health, Labour, and Welfare of Japan

Corresponding author

Correspondence to Shigeyuki Kawa.

Additional information

Members of the study group are listed in Appendix.

Electronic supplementary material

Appendix

Appendix

Study Group for Pancreatitis Complicated with Inflammatory Bowel Disease organized by The Research Committee for Intractable Pancreatic Disease (Chairman: Tooru Shimosegawa) and The Research Committee for Intractable Inflammatory Bowel Disease (Chairman: Mamoru Watanabe), both of which are supported by the Ministry of Health, Labour, and Welfare of Japan.

Toshiharu Ueki,1 Toshiyuki Matsui,1 Atsushi Kanno,2 Takayuki Watanabe,3 Kazushige Uchida,4 Masashi Taguchi,5 Hisato Igarashi,6 Tetsuhide Ito,6 Hiroaki Igarashi,7 Takeshi Kawanobe,7 Hideki Iijima,8 Yutaka Kohgo,9 Takahiro Ito,9 Reiko Kunisaki,10 Masakazu Nagahori,11 Takao Itoi,12 Mitsuyoshi Honjo,12 Junichi Sakagami,13 Hiroaki Yasuda,13 Katsuyoshi Hatakeyama,14 Tsuneo Iiai,14 Yoshiki Hirooka,15 Hajime Sumi,16 Kenji Watanabe,17 Makoto Sasaki,18 Akira Ando,19 Osamu Inatomi,19 Fukunori Kinjo,20 Atsushi Iraha, 20 Naotaka Fujita,21 Kaori Mas, 21 Takashi Kagaya,22 Hiroyuki Miyakawa,23 Keiya Okamura,23 Toshifumi Hibi,24 Yuji Nakamura,24 Katsuyuki Fukuda,25 Tsukasa Ikeura,4 Takuya Ishikawa,26 Fumiaki Ueno,27 Akihiko Satoh,28 Masato Uemura,29 Hirohito Tsubouchi,30 Keita Funakawa, 30 Masahiro Iizuka,31 Atsushi Yoden,32 Kensuke Kubota,33 Yuji Funayama,34 Takaaki Eguchi,35 Yoh Ishiguro,36 Natsumi Uehara,37 Norikazu Arakura,38 Terumi Kamisawa,39 Isao Nishimori,40 Hirotaka Ohara,41 Nobumasa Mizuno,42 Kenji Hirano,43 Atsushi Masamune, 2 Kazuhiro Kikuta,2

1Department of Gastroenterology, Fukuoka University Chikushi Hospital, Fukuoka, Japan

2Division of Gastroenterology, Tohoku University Graduate School of Medicine, Sendai, Japan

3Department of Gastroenterology, Shinshu University School of Medicine, Matsumoto, Japan

4Department of Gastroenterology and Hepatology, Kansai Medical University, Osaka, Japan

5Third Department of Internal Medicine, School of Medicine, University of Occupational and Environmental Health, Kitakyushu, Japan

6Department of Medicine and Bioregulatory Science, Kyushu University, Fukuoka, Japan

7Department of Gastroenterology and Hepatology, Kawakita General Hospital, Suginami-ku, Tokyo, Japan

8Department of Gastroenterology and Hepatology, Osaka University Graduate School of Medicine, Suita, Japan

9Division of Gastroenterology and Hematology/Oncology, Department of Medicine, Asahikawa Medical University, Asahikawa, Japan

10Inflammatory Bowel Disease Center, Yokohama City University Medical Center, Yokohama, Japan

11Department of Gastroenterology and Hepatology, Graduate School of Tokyo Medical and Dental University, Tokyo, Japan

12Department of Gastroenterology and Hepatology, Tokyo Medical University, Tokyo, Japan

13Department of Gastroenterology and Hepatology, Kyoto Prefectural University of Medicine, Kyoto, Japan

14Division of Digestive and General Surgery, Niigata University Graduate School of Medical and Dental Sciences, Niigata, Japan

15Department of Endoscopy, Nagoya University Hospital, Nagoya, Japan

16Department of Gastroenterology and Hepatology, Nagoya University School of Medicine, Nagoya, Japan

17Department of Gastroenterology, Osaka City University Graduate School of Medicine, Osaka, Japan

18Department of Gastroenterology, Aichi Medical University School of Medicine, Nagakute, Japan

19Division of Gastroenterology, Shiga University of Medical Science, Otsu,Japan

20Department of Endoscopy, University of the Ryukyus, Okinawa, Japan

21Department of Radiology, Sendai City Medical Center, Sendai, Japan

22Department of Gastroenterology, Graduate School of Medicine, Kanazawa University, Kanazawa, Japan

23Second Department of Gastroenterology, Sapporo Kosei General Hospital, Sapporo, Japan

24Department of Internal Medicine, Keio University School of Medicine, Tokyo, Japan

25Department of Gastroenterology, St Luke’s International Hospital, Tokyo, Japan

26Department of Gastroenterology, Japanese Red Cross Nagoya Daiichi Hospital, Nagoya, Japan

27Department of Medicine, Ofuna Chuo Hospital, Kamakura, Japan

28Department of Internal Medicine, Kurihara Central Hospital, Kurihara, Japan

29Third Department of Internal Medicine, Nara Medical University Hospital, Kashihara, Japan

30Digestive and Lifestyle Diseases, Kagoshima University Graduate School of Medical and Dental Sciences, Kagoshima, Japan

31Department of Gastroenterology, Akita Red Cross Hospital, Akita, Japan

32Department of Pediatrics, Osaka Medical College, Osaka, Japan

33Division of Gastroenterology, Yokohama City University Graduate School of Medicine, Yokohama, Japan

34Department of Colorectal Surgery, Tohoku Rosai Hospital, Sendai, Japan

35Department of Gastroenterology and Hepatology, Osakafu Saiseikai Nakatsu Hospital, Osaka, Japan

36Department of Gastroenterology and Hematology, Hirosaki University Graduate School of Medicine, Hirosaki, Japan

37Division of Gastroenterology and Hematology, Department of Internal Medicine, Faculty of Medicine, University of Miyazaki, Miyazaki, Japan

38Endoscopic Examination Center, Shinshu University School of Medicine, Matsumoto, Japan

39Department of Internal Medicine, Tokyo Metropolitan Komagome Hospital, Tokyo, Japan

40Nishimori Clinic, Kochi, Japan

41Department of Community-Based Medical Education, Nagoya City University Graduate School of Medical Sciences, Nagoya, Japan

42Department of Gastroenterology, Aichi Cancer Center Hospital, Nagoya, Japan

43Department of Gastroenterology, Graduate School of Medicine, University of Tokyo, Tokyo, Japan

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kawa, S., Okazaki, K., Notohara, K. et al. Autoimmune pancreatitis complicated with inflammatory bowel disease and comparative study of type 1 and type 2 autoimmune pancreatitis. J Gastroenterol 50, 805–815 (2015). https://doi.org/10.1007/s00535-014-1012-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00535-014-1012-5

Keywords

Search

Navigation