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Age at onset is associated with the seasonal pattern of onset and exacerbation in inflammatory bowel disease

  • Original Article—Alimentary Tract
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Abstract

Background

Environmental factors are suggested to affect the pathogenesis of several diseases, including inflammatory bowel disease (IBD). The seasonality of disease onset and exacerbation in IBD, however, are not well established. We herein aimed to clarify the disease seasonality and to investigate the underlying characteristics in IBD patients exhibiting seasonality of the disease course.

Methods

This was a multicenter observational study comprising 20 institutions (Osaka Gut Forum) in Japan. Data were collected from November 2013 to August 2014 using survey forms for physicians and questionnaires for patients. Multivariate analysis was performed to clarify the independent factors affecting disease seasonality.

Results

A total of 1055 patients, including 298 patients with Crohn’s disease (CD) and 757 patients with ulcerative colitis (UC), were enrolled. The proportion of CD patients with disease onset in the summer was significantly larger than that in the other seasons, while UC patients exhibited no seasonality of disease onset. More than half of the IBD patients (51.1%) experienced seasonal exacerbation of IBD, and winter was the most common season for disease exacerbation in both CD and UC patients. Seasonality of disease onset and exacerbation was observed in young-onset patients (≤40 years old), but not in elderly-onset patients. Age at onset was independently associated with the seasonality of both disease onset and exacerbation.

Conclusions

Seasonality of disease onset and exacerbation was observed especially in young-onset IBD patients. Underlying pathophysiologic triggers for disease initiation and exacerbation may be influenced by age at disease onset.

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Acknowledgements

This work was supported by a Grant-in-Aid from the Japan Society for the Promotion of Science (Grant No. 26460969). We are grateful to Dr. E. Mita (National Hospital Organization Osaka National Hospital), Dr. H. Ito (Kinshukai Infusion Clinic), Dr. M. Yamamoto (Kinki Central Hospital of Mutual Aid Association of Public School Teachers), Dr. K. Tominaga (Kaizuka City Hospital), Dr. T. Kitada (Kawanishi City Hospital), Dr. Y. Okuda (Saiseikai Senri Hospital), and Dr. S. Ishii (Osaka General Medical Center) in the Osaka Gut Forum for their contributions to the data collection. Writing assistance: The manuscript was edited by SciTechEdit International, LLC (7012 East Mountain Brush Circle Highlands Ranch CO 80130 USA).

Author information

Authors and Affiliations

  1. Department of Gastroenterology and Hepatology, Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita, Osaka, 565-0871, Japan

    Manabu Araki, Shinichiro Shinzaki, Satoshi Hiyama, Takahiro Inoue, Hideki Iijima & Tetsuo Takehara

  2. Department of Gastroenterology, National Hospital Organization Osaka National Hospital, Osaka, Japan

    Takuya Yamada

  3. Kinshukai Infusion Clinic, Osaka, Japan

    Shoko Arimitsu

  4. Department of Gastroenterology, Osaka Rosai Hospital, Sakai, Japan

    Masato Komori

  5. Department of Gastroenterology, NTT-West Osaka Hospital, Osaka, Japan

    Narihiro Shibukawa

  6. Department of Gastroenterology, Sumitomo Hospital, Osaka, Japan

    Akira Mukai

  7. Department of Gastroenterology, Toyonaka Municipal Hospital, Toyonaka, Japan

    Sachiko Nakajima

  8. Department of Gastroenterology, Otemae Hospital, Osaka, Japan

    Kazuo Kinoshita

  9. Department of Gastroenterology, Sakai City Hospital, Sakai, Japan

    Shinji Kitamura

  10. Department of Gastroenterology and Hepatology, Itami City Hospital, Itami, Japan

    Yoko Murayama

  11. Department of Gastroenterology, Nishinomiya Municipal Central Hospital, Nishinomiya, Japan

    Hiroyuki Ogawa

  12. Department of Gastroenterology, Hyogo Prefectural Nishinomiya Hospital, Nishinomiya, Japan

    Yuichi Yasunaga

  13. Department of Internal Medicine, Osaka Police Hospital, Osaka, Japan

    Masahide Oshita

  14. Department of Gastroenterology, Yao Municipal Hospital, Yao, Japan

    Hiroyuki Fukui

  15. Department of Gastroenterology, National Hospital Organization Osaka-Minami National Hospital, Kawachinagano, Japan

    Eiji Masuda

  16. Department of Gastroenterology, Higashiosaka Municipal Hospital, Higashiosaka, Japan

    Masahiko Tsujii

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  1. Manabu Araki
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Corresponding author

Correspondence to Hideki Iijima.

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Electronic supplementary material

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535_2017_1313_MOESM1_ESM.docx

Supplementary material 1 (DOCX 15 kb). Supplementary Table 1. Questions regarding onset age and season of onset or exacerbation in the patient questionnaire

535_2017_1313_MOESM2_ESM.docx

Supplementary material 2 (DOCX 15 kb). Supplementary Table 2. Patient characteristics associated with exacerbation seasonality in IBD patients

535_2017_1313_MOESM3_ESM.tif

Supplementary material 3 (TIFF 2040 kb) Supplementary Fig. 1. Study flow chart. A total of 1055 patients were enrolled in the study, excluding 23 patients whose response regarding seasonality of onset or exacerbation was left vacant. We performed two analyses; one was an analysis of the seasonality of onset and the other was an analysis of the seasonality of exacerbation. We excluded 219 patients from the onset evaluation and 172 patients from the exacerbation evaluation because of inadequate responses (n = 836 and 883, respectively). Furthermore, analysis of the season of exacerbation was performed among patients who identified seasonal disease exacerbation [exacerbation seasonality (+)]. Prior to the analysis, we excluded 14 patients who did not respond with a definite season (e.g., turn of season)

535_2017_1313_MOESM4_ESM.tif

Supplementary material 4 (TIFF 942 kb) Supplementary Fig. 2. Ratio of IBD, CD, and UC patients who experienced seasonal exacerbation. More than half the CD and UC patients responded that disease activity was affected in a seasonal manner. A total of 883 IBD patients, comprising 257 CD patients and 626 UC patients, were analyzed

535_2017_1313_MOESM5_ESM.tif

Supplementary material 5 (TIFF 1123 kb) Supplementary Fig. 3. Ratio of IBD patients who experienced seasonal exacerbation subdivided by age at enrollment. One patient whose response to age at enrollment was left vacant was excluded from the exacerbation evaluation cohort, and a total of 882 patients were analyzed. Age at enrollment was not significantly different among the groups (p = 0.53)

535_2017_1313_MOESM6_ESM.tif

Supplementary material 6 (TIFF 3068 kb) Supplementary Fig. 4. Distribution of IBD patients who experienced seasonal exacerbation subdivided by age at onset. Eight patients whose response regarding age at onset was left vacant were excluded from the exacerbated season evaluation cohort, and a total of 429 patients were analyzed. Age at onset was not significantly different among the groups (p = 0.75)

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Araki, M., Shinzaki, S., Yamada, T. et al. Age at onset is associated with the seasonal pattern of onset and exacerbation in inflammatory bowel disease. J Gastroenterol 52, 1149–1157 (2017). https://doi.org/10.1007/s00535-017-1313-6

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  • DOI: https://doi.org/10.1007/s00535-017-1313-6

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