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Extraintestinal Manifestations in Patients with Inflammatory Bowel Disease: Study Based on the ENEIDA Registry

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Abstract

Background

Patients with inflammatory bowel disease (IBD) may present extraintestinal manifestations (EIMs) that affect the joints, skin, eyes, and hepatobiliary area, among others.

Aims

Our aim was to analyse the prevalence and characteristics of EIMs in patients with IBD and to identify the possible risk factors associated with the development of EIMs in the largest series published to date.

Methods

Observational, cross-sectional study including patients from the Spanish ENEIDA registry promoted by GETECCU. We retrospectively identified all cases of EIMs in the ENEIDA registry until January 2018.

Results

The study included 31,077 patients, 5779 of whom had at least one EIM (global prevalence 19%; 95% CI 18.2–19.0). Among the different types of EIMs, rheumatic manifestations had a prevalence of 13% (95% CI 12.9–13.7; 63% of EIMs), with a prevalence of 5% (95% CI 4.7–5.2) for mucocutaneous manifestations, 2.1% (95% CI 1.9–2.2) for ocular manifestations, and 0.7% (95% CI 0.6–0.8) for hepatobiliary manifestations. The multivariable analysis showed that the type of IBD (Crohn’s disease, p < 0.001), gender (female, p < 0.001), the need for an immunomodulator (p < 0.001) or biologic drugs (p < 0.001), a previous family history of IBD (p < 0.001), and an extensive location of IBD (p < 0.001) were risk factors for the presence of EIMs.

Conclusions

One-fifth of patients with IBD may have associated EIMs, with rheumatic manifestations as the most frequent (> 60% of EIMs). Female patients with severe Crohn’s disease represent the group with the highest risk of developing EIMs. These patients should therefore be specially monitored and referred to the corresponding specialist when suggestive symptoms appear.

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Acknowledgments

We thank Montero Traducciones, S.L. (Brunete, Spain), for his invaluable help in improving the English. Alicia Algaba has served as a speaker and has received research grant or advisory fees from MSD, Lilly, Roche, Takeda, and Janssen. Iván Guerra has served as speaker or consultant for Takeda, Kern Pharma, Abbvie, and Janssen. Elena Ricart has served as speaker, has received research funding, or has participated in educational and advisory events for MSD, AbbVie, Takeda, Pfizer, Janssen, Frezenius Kabi, Chiesi, and Ferring. Eva Iglesias has served as speaker, a consultant, an advisory member for, or has received research funding from MSD, Abbvie, Kern Pharma, Takeda, and Janssen. Miriam Mañosa has served as a speaker or has received research or education funding from MSD, Abbvie, Hospira, Pfizer, Takeda, Janssen, Ferring, Shire Pharmaceuticals, Dr. Falk Pharma, and Tillotts Pharma. Javier Gisbert has served as a speaker, a consultant, and advisory member for or has received research funding from MSD, Abbvie, Hospira, Pfizer, Kern Pharma, Biogen, Takeda, Janssen, Roche, Sandoz, Celgene, Ferring, Faes Farma, Shire Pharmaceuticals, Dr. Falk Pharma, Tillotts Pharma, Chiesi, Casen Fleet, Gebro Pharma, Otsuka Pharmaceutical, and Vifor Pharma. Jordi Guardiola has served as a speaker, a consultant, an advisory member for, or has received research funding from MSD, Abbvie, Kern Pharma, Takeda, Janssen, Pfizer, Ferring, and GE Healthcare. Ruth de Francisco has served as a speaker or has received research or education funding from MSD, Abbvie, Takeda, Janssen, Faes, Tillots, and Ferring. Pilar Nos has served as speaker, has received research funding, or has participated in educational events for MSD, AbbVie, Takeda, Pfizer, Janssen, Faes, Otsuka, Chiesi, and Ferring. Jesús Barrio has served as a speaker or has received research funding or advisory fees from MSD, AbbVie, Takeda, Janssen, and Ferring. María Dolores Martín-Arranz has received fees as a speaker, consultant, and advisory member for or has received research funding from MSD, AbbVie, Hospira, Pfizer, Takeda, Janssen, Shire Pharmaceuticals, Tillotts Pharma, and Faes Pharma. Xavier Calvet has received grants for research from Abott, MSD, and Vifor or fees for advisory boards from Abott, MSD, Takeda, Pfizer, Janssen, and Vifor and has given lectures for Abott, MSD, Janssen, Pfizer, Takeda, Shire, and Allergan. Santiago García-López has served as speaker, has received research funding, or has participated in educational and advisory events for MSD, AbbVie, Takeda, Pfizer, Janssen, Chiesi, and Ferring. María Esteve reports personal fees from Janssen, Pfizer, Menarini, Tillots Pharma, Takeda, and grants from MSD and Abbvie, outside the submitted work. José L Pérez-Calle has served as speaker, has received research funding from MSD, AbbVie, Janssen, Pfizer, and Takeda, Dr. Falk, and Ferring. Mariana García-Sepulcre has served as speaker, has received research funding, or has participated in educational events for MSD, AbbVie, Takeda, and Janssen. Rufo Lorente has served as speaker, has received research funding, or has participated in educational events for MSD, AbbVie, Takeda, Pfizer, Janssen, Dr Falk, and Ferring. Isabel Blázquez Gómez has served as a speaker or has received research or educational funding from AbbVie and Kern Pharma. Pedro Almela has served as a speaker, a consultant, and advisory member for or has received research funding from MSD, Abbvie, Takeda, Janssen, Gebro Pharma, and Tillotts Pharma. Eugeni Domènech has served as a speaker or has received research or education funding or advisory fees from MSD, AbbVie, Takeda, Kern Pharma, Pfizer, Janssen, Celgene, Adacyte Therapeutics, Otsuka Pharmaceuticals, Ferring, Shire Pharmaceuticals, Tillots, Thermofisher, Grifols, and Gebro. Fernando Bermejo has served as a speaker, a consultant, and advisory member for or has received research funding from MSD, Abbvie, Pfizer, Takeda Janssen, and Gebro.

Funding

The Eneida Registry is funded by AbbVie, Takeda, Pfizer, AMGEN, Kern Pharmaceuticals, and Merck Sharp and Dohme.

Author information

Authors and Affiliations

  1. Department of Gastroenterology of Hospital Universitario de Fuenlabrada, Madrid, Spain

    Alicia Algaba, Iván Guerra, Laura Jiménez & Fernando Bermejo

  2. Instituto de Investigación Sanitaria Hospital La Paz (IdiPaz), Madrid, Spain

    Alicia Algaba, Iván Guerra, Laura Jiménez & Fernando Bermejo

  3. Department of Gastroenterology of Hospital Clinic, Barcelona, Spain

    Elena Ricart

  4. Institut d’Investigacions Biomèdiques August Pi I Sunyer (IDIBAPS), Barcelona, Spain

    Elena Ricart

  5. Centro de Investigación Biomédica en Red de Enfermedades Hepáticas y Digestivas (CIBERehd), Madrid, Spain

    Elena Ricart, Miriam Mañosa, Javier P. Gisbert, Pilar Nos, Xavier Calvet, María Esteve, Luis Bujanda, Alfredo J. Lucendo & Eugeni Domenech

  6. Department of Gastroenterology of Hospital Universitario Reina Sofía, Córdoba, Spain

    Eva Iglesias

  7. Instituto Maimónides de Investigación Biomédica de Córdoba (IMIBIC), Córdoba, Spain

    Eva Iglesias

  8. Department of Gastroenterology of Hospital Universitari Germans Trias i Pujol, Barcelona, Spain

    Miriam Mañosa & Eugeni Domenech

  9. Department of Gastroenterology of Hospital Universitario de La Princesa, Madrid, Spain

    Javier P. Gisbert

  10. Instituto de Investigación Sanitaria Princesa (IIS-IP), Madrid, Spain

    Javier P. Gisbert

  11. Universidad Autónoma de Madrid, Madrid, Spain

    Javier P. Gisbert

  12. Department of Gastroenterology of Hospital Universitari de Bellvitge, Barcelona, Spain

    Jordi Guardiola

  13. Institut d’Investigació Biomèdica de Bellvitge (IDIBELL), Barcelona, Spain

    Jordi Guardiola

  14. Department of Gastroenterology of Hospital Clínico de Valencia, Valencia, Spain

    Miguel Mínguez

  15. Universitat of Valencia, Valencia, Spain

    Miguel Mínguez

  16. Department of Gastroenterology of Hospital Universitario Marqués de Valdecilla, Santander, Spain

    Beatriz Castro

  17. Instituto de Investigación Marqués de Valdecilla, Santander, Spain

    Beatriz Castro

  18. Department of Gastroenterology of Hospital Universitario Central de Asturias, Asturias, Spain

    Ruth de Francisco

  19. Instituto de Investigación Sanitaria del Principado de Asturias (ISPA), Oviedo, Spain

    Ruth de Francisco

  20. Gastroenterology Department, Hospital Universitari i Politècnic La Fe, Valencia, Spain

    Pilar Nos

  21. Department of Gastroenterology of Hospital de la Santa Creu i Sant Pau, Barcelona, Spain

    Federico Bertoletti

  22. Department of Gastroenterology of Hospital Universitario Ramón y Cajal, Madrid, Spain

    Francisco Mesonero

  23. Department of Gastroenterology of Hospital Universitario Rio Hortega, Valladolid, Spain

    Jesús Barrio

  24. Department of Gastroenterology of La Paz Hospital, Madrid, Spain

    María Dolores Martín-Arranz

  25. Innate Immunity Group, IdiPAZ Institute for Health Research, La Paz Hospital, Madrid, Spain

    María Dolores Martín-Arranz

  26. Department of Gastroenterology of Corporació Sanitària Universitària Parc Taulí, Sabadell, Spain

    Xavier Calvet

  27. Universitat Autònoma de Barcelona, Barcelona, Spain

    Xavier Calvet

  28. Department of Gastroenterology of Hospital Universitario Miguel Servet, Zaragoza, Spain

    Santiago García-López

  29. Department of Gastroenterology of Hospital Universitario de Burgos, Burgos, Spain

    Beatriz Sicilia

  30. Department of Gastroenterology of Hospital Clínico de Málaga, Málaga, Spain

    Gillermo Alcaín

  31. Department of Gastroenterology of Hospital Universitari Mútua Terrassa, Barcelona, Spain

    María Esteve

  32. Gastroenterology Department, Hospital del Mar, Barcelona, Spain

    Lucía Márquez

  33. IMIM (Hospital del Mar Medical Research Institute), Barcelona, Spain

    Lucía Márquez

  34. Department of Gastroenterology of Consorci Sanitari Terrassa, Barcelona, Spain

    Marta Piqueras

  35. Department of Gastroenterology of Hospital Universitario Fundación Alcorcón, Madrid, Spain

    José L. Perez-Calle

  36. Department of Gastroenterology of Hospital Donostia/Instituto Biodonostia, San Sebastián, Guipúzcoa, Spain

    Luis Bujanda

  37. Universidad del País Vasco UPV/EHU, San Sebastián, Guipúzcoa, Spain

    Luis Bujanda

  38. Department of Gastroenterology of Hospital General Universitario Elche, Alicante, Spain

    Mariana García-Sepulcre

  39. Department of Gastroenterology of Hospital Universitario de Salamanca, Salamanca, Spain

    Alejandra Fernández

  40. Department of Gastroenterology of Hospital de Galdakao, Vizcaya, Spain

    Irene Moraleja

  41. Gastroenterology Department, Hospital General Universitario de Ciudad Real, Ciudad Real, Spain

    Rufo Humberto Lorente

  42. Department of Gastroenterology of Hospital de Sant Joan Despí Moisès Broggi, Barcelona, Spain

    Orlando García-Bosch

  43. Department of Gastroenterology of Hospital General San Jorge, Huesca, Spain

    Ana Lambán

  44. Department of Gastroenterology of Hospital de Torrejón, Madrid, Spain

    Isabel Blázquez

  45. Department of Gastroenterology of Hospital Universitario Nuestra Señora Candelaria, Santa Cruz de Tenerife, Spain

    Esther Rodríguez

  46. Department of Gastroenterology of Hospital General Universitario de Valencia, Valencia, Spain

    José M. Huguet

  47. Department of Gastroenterology of Hospital General de Tomelloso, Ciudad Real, Spain

    Alfredo J. Lucendo

  48. Department of Gastroenterology of Hospital General Universitari de Castelló, Castellón, Spain

    Pedro Almela

  49. Department of Gastroenterology of Hospital Dr. Josep Trueta, Girona, Spain

    David Busquets

  50. Department of Gastroenterology of Hospital Universitario Áraba, Vitoria-Gasteiz, Álava, Spain

    Patricia Ramírez de la Piscina

  51. Department of Gastroenterology of Hospital Sant Jaume de Calella, Barcelona, Spain

    Marcela Pérez

Authors
  1. Alicia Algaba
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  2. Iván Guerra
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  3. Elena Ricart
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  4. Eva Iglesias
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  5. Miriam Mañosa
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  6. Javier P. Gisbert
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  7. Jordi Guardiola
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  8. Miguel Mínguez
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  9. Beatriz Castro
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  10. Ruth de Francisco
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  11. Pilar Nos
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  12. Federico Bertoletti
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  13. Francisco Mesonero
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  14. Jesús Barrio
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  15. María Dolores Martín-Arranz
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  16. Xavier Calvet
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  17. Santiago García-López
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  18. Beatriz Sicilia
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  19. Gillermo Alcaín
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  20. María Esteve
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  21. Lucía Márquez
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  22. Marta Piqueras
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  23. Laura Jiménez
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Consortia

the Spanish GETECCU Group (ENEIDA Project)

Corresponding author

Correspondence to Alicia Algaba.

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Ethical approval

This study was approved by the ENEIDA Committee and by the Ethics Committee of the Hospital Universitario de Fuenlabrada. The ENEIDA project was approved by the ethics committees of each participating hospital. Informed consent was obtained in writing from each patient.

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Algaba, A., Guerra, I., Ricart, E. et al. Extraintestinal Manifestations in Patients with Inflammatory Bowel Disease: Study Based on the ENEIDA Registry. Dig Dis Sci 66, 2014–2023 (2021). https://doi.org/10.1007/s10620-020-06424-x

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  • DOI: https://doi.org/10.1007/s10620-020-06424-x

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