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Chronic Granulomatous Disease-Associated IBD Resolves and Does Not Adversely Impact Survival Following Allogeneic HCT

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A Correction to this article was published on 29 August 2020

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Abstract

Introduction

Inflammatory bowel disease (IBD) affects approximately 1/3 of patients with chronic granulomatous disease (CGD). Comprehensive investigation of the effect of allogeneic hematopoietic cell transplantation (HCT) on CGD IBD and the impact of IBD on transplant outcomes is lacking.

Methods

We collected data retrospectively from 145 patients with CGD who had received allogeneic HCT at 26 Primary Immune Deficiency Treatment Consortium (PIDTC) centers between January 1, 2005 and June 30, 2016.

Results

Forty-nine CGD patients with IBD and 96 patients without IBD underwent allogeneic HCT. Eighty-nine percent of patients with IBD and 93% of patients without IBD engrafted (p = 0.476). Upper gastrointestinal acute GVHD occurred in 8.5% of patients with IBD and 3.5% of patients without IBD (p = 0.246). Lower gastrointestinal acute GVHD occurred in 10.6% of patients with IBD and 11.8% of patients without IBD (p = 0.845). The cumulative incidence of acute GVHD grades II–IV was 30% (CI 17–43%) in patients with IBD and 20% (CI 12–29%) in patients without IBD (p = 0.09). Five-year overall survival was equivalent for patients with and without IBD: 80% [CI 66–89%] and 83% [CI 72–90%], respectively (p = 0.689). All 33 surviving evaluable patients with a history of IBD experienced resolution of IBD by 2 years following allogeneic HCT.

Conclusions

In this cohort, allogeneic HCT was curative for CGD-associated IBD. IBD should not contraindicate HCT, as it does not lead to an increased risk of mortality.

This study is registered at clinicaltrials.gov NCT02082353.

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Change history

  • 29 August 2020

    The original version of this article unfortunately contained the missing author, Caridad Martinez. The authors would like to correct the list. We apologize for any inconvenience that this may have caused. The correct author list is shown above.

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Acknowledgements

We thank Elizabeth Dunn and Tara Bani-Hashemi for project management and assistance. We thank all of the study coordinators for collection of clinical data from PIDTC sites. We thank all of the clinical care teams who provided care for patients.

Funding

The PIDTC is supported by the Division of Allergy, Immunology and Transplantation, National Institute of Allergy and Infectious Diseases (NIAID); and the Office of Rare Diseases Research (ORDR), National Center for Advancing Translational Sciences (NCATS), National Institutes of Health (NIH), Bethesda, MD; Public Health Service grant/cooperative agreements U54-AI082973 (PI: MJ Cowan), U54-NS064808 and U01-TR001263 (PI: JP Krischer) and R13-AI094943 (PI: MJ Cowan).

The PIDTC is a part of the Rare Diseases Clinical Research Network (RDCRN) of ORDR, NCATS. The content and opinions expressed are solely the responsibility of the authors and do not represent the official policy or position of the NIAID, ORDR, NCATS, NIH, or any other agency of the US Government.

Support was also provided by the Division of Intramural Research, NIAID, NIH (EMK, LDN, HLM, PG and DG).

Author information

Author notes

  1. Rebecca A. Marsh, Jennifer W. Leiding, Brent R. Logan, Harry Malech, Suhag Parikh, and Elizabeth M. Kang contributed equally to this work.

Authors and Affiliations

  1. Department of Pediatrics, University of Cincinnati, and Division of Bone Marrow Transplantation and Immune Deficiency, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA

    Rebecca A. Marsh & Jack J. Bleesing

  2. Division of Allergy and Immunology, Department of Pediatrics, Johns Hopkins-All Children’s Hospital, University of South Florida, St. Petersburg, FL, USA

    Jennifer W. Leiding

  3. Division of Biostatistics, Medical College of Wisconsin, Milwaukee, WI, USA

    Brent R. Logan, Ziyan Yin & Kadam Patel

  4. Division of Allergy, Immunology, and Transplantation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA

    Linda M. Griffith

  5. Allergy and Immunology, The Children’s Hospital of Philadelphia, Philadelphia, PA, USA

    Danielle E. Arnold, Kathleen E. Sullivan & Jennifer Heimall

  6. Immunology-Rheumatology Division, Department of Pediatrics, University of Montreal, Montreal, QC, Canada

    Elie Haddad

  7. Division of Immunity and Viral Infections, Institut de Recherches Cliniques de Montréal, Montréal, QC, Canada; and Department of Medicine, Université de Montréal, Montréal, QC, Canada

    E. Liana Falcone

  8. Department of Pediatrics, Duke University, Durham, NC, USA

    Erin Arbuckle

  9. Fred Hutchinson Cancer Research Center, Seattle Children’s Hospital, The University of Washington School of Medicine, Seattle, WA, USA

    Lauri M. Burroughs

  10. Seattle Children’s Hospital, Seattle, WA, USA

    Suzanne Skoda-Smith

  11. Division of Bone Marrow Transplant, Aflac Cancer and Blood Disorders Center, Children’s Healthcare of Atlanta, Emory University School of Medicine, Atlanta, GA, USA

    Shanmuganathan Chandrakasan

  12. Division of Hematology/Oncology and Hematopoietic Stem Cell Transplantation, The Center for Cancer and Blood Disorders, Children’s Hospital/Louisiana State University Medical Center, New Orleans, LA, USA

    Lolie C. Yu

  13. Cancer and Blood Disorders Institute, Johns Hopkins All Children’s Hospital, St. Petersburg, FL, USA

    Benjamin R. Oshrine

  14. Manitoba Blood and Marrow Transplant Program, CancerCare Manitoba, University of Manitoba, Winnipeg, MB, Canada

    Geoffrey D. E. Cuvelier

  15. Fred Hutchinson Cancer Research Center, Seattle Children’s Hospital, The University of Washington School of Medicine, Seattle, WA, USA

    Monica S. Thakar

  16. Division of Allergy and Immunology, Department of Pediatrics, University of Utah School of Medicine, Salt Lake City, UT, USA

    Karin Chen

  17. CHU Sainte-Justine, Hematology-Oncology Division, Department of Pediatrics, University of Montreal, Montreal, QC, Canada

    Pierre Teira

  18. Division of Pediatric Hematology/Oncology/Bone Marrow Transplantation, Washington University School of Medicine and St. Louis Children’s Hospital, St. Louis, MO, USA

    Shalini Shenoy

  19. Pediatric Blood and Marrow Transplant Program, Division of Hematology, Oncology, and Blood and Marrow Transplantation, Medical College of Wisconsin, Milwaukee, WI, USA

    Rachel Phelan

  20. Department of Pediatrics, Baylor College of Medicine, Houston, TX, USA, and Section of Allergy, Immunology and Retrovirology, Texas Children’s Hospital William T. Shearer Center for Human Immunobiology, Houston, TX, USA

    Lisa R. Forbes

  21. Blood and Marrow Transplant Program, Johns Hopkins All Children’s Hospital, St. Petersburg, FL, USA

    Deepak Chellapandian

  22. Division of Blood and Marrow Transplantation, Children’s National Medical Center, Washington, DC, USA, and Department of Pediatrics, The George Washington University, Washington, DC, USA

    Blachy J. Dávila Saldaña

  23. Division of Stem Cell Transplantation and Regenerative Medicine, Stanford School of Medicine, Lucille Packard Children’s Hospital, Palo Alto, CA, USA

    Ami J. Shah

  24. Division of Stem Cell Transplantation and Regenerative Medicine, Department of Pediatrics, Stanford School of Medicine, Stanford, CA, USA

    Katja G. Weinacht

  25. Division of Pediatric Allergy and Immunology, Mayo Clinic, Rochester, MN, USA

    Avni Joshi

  26. Department of Pediatrics, BMT Service, Memorial Sloan Kettering Cancer Center, New York, NY, USA

    Farid Boulad

  27. Texas Transplant Institute, Methodist Children’s Hospital, San Antonio, TX, USA

    Troy C. Quigg

  28. Pediatric Allergy, Immunology, and Blood and Marrow Transplant Division, San Francisco Benioff Children’s Hospital, San Francisco, CA, USA

    Christopher C. Dvorak, Morton J. Cowan & Jennifer M. Puck

  29. Genetic Immunotherapy Section, Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA

    Debi Grossman, Pamela Graham, Harry L. Malech & Elizabeth M. Kang

  30. Department of Pediatrics, Divisions of Immunology/Rheumatology, University of Washington and Seattle Children’s Hospital, Seattle, WA, USA

    Troy Torgerson

  31. Division of Pediatric Blood and Marrow Transplant, Duke University Medical Center, Durham, NC, USA

    Vinod Prasad

  32. Pediatric Allergy and Immunology, Cardinal Glennon Children’s Medical Center, Saint Louis University, St. Louis, MO, USA

    Alan Knutsen

  33. UPMC Children’s Hospital of Pittsburgh, Pittsburgh, PA, USA

    Hey Chong

  34. Center for Cancer and Blood Disorders, Phoenix Children’s Hospital, Phoenix, AZ, USA

    Holly Miller

  35. Department of Pediatrics/Immunology, University of Washington and Seattle Children’s Hospital, Seattle, WA, USA

    M. Teresa de la Morena

  36. American Family Children’s Hospital, University of Wisconsin, Madison, WI, USA

    Kenneth DeSantes

  37. Laboratory of Clinical Immunology and Microbiology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD, USA

    Luigi D. Notarangelo

  38. David Geffen School of Medicine at University of California, Los Angeles, CA, USA

    Donald B. Kohn

  39. Aflac Center and Blood Disorders Center, Children’s Healthcare of Atlanta, Emory University, Atlanta, GA, USA

    Elizabeth Stenger

  40. Hematology-Oncology, Boston Children’s Hospital, Boston, MA, USA

    Sung-Yun Pai

  41. Division of Allergy and Immunology, Department of Pediatrics, Medical College of Wisconsin, Milwaukee, WI, USA

    John M. Routes

  42. Blood and Marrow Transplant Program, Division of Hematology, Oncology and Blood and Marrow Transplantation, Children’s Hospital Los Angeles, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

    Neena Kapoor & Michael A. Pulsipher

  43. Division of Pediatric Blood and Marrow Transplant, Duke University, Durham, NC, USA

    Suhag Parikh

Authors
  1. Rebecca A. Marsh
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  2. Jennifer W. Leiding
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  3. Brent R. Logan
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  4. Linda M. Griffith
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  54. Elizabeth M. Kang
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Consortia

submitted on behalf of the Primary Immune Deficiency Treatment Consortium

Contributions

The eligibility review expert panel (MJC, DBK, EMK, RAM, LMG, SP, JMP, LDN, EH, JWL, ES, MAP) reviewed each submitted case to assess eligibility criteria. The study was designed by EMK, HLM, LDN, and LMG. MJC, JMP, EH, DBK, LMG, LDN, and SYP served as senior leadership on the PIDTC Steering Committee. RAM, JWL, HLM, SP, and EMK wrote the first draft of the manuscript. BRL, ZY, and KP performed statistical analyses. RAM, JWL, DA, EH, ELF, EA, JJB, KES, JH, LMB, SSS, SC, LY, BRO, GC, MT, KC, PT, SS, RP, LF, DC, BJDS, AJS, KW, AJ, FB, TQ, CCD, DG, TT, PG, VP, AK, HC, HM, MTLM, KDS, MJC, LDN, DBK, ES, SYP, JMR, JMP, NK, MAP, HLM, SP, and EMK contributed patients and/or provided clinical care and/or entered patient data. All authors edited the manuscript and contributed to the subsequent versions.

LMG, an employee of DAIT, NIAID, the funding source, also participated as a PIDTC study team member in the interpretation of data, writing of the manuscript, and decision to submit the manuscript for publication.

Corresponding author

Correspondence to Elizabeth M. Kang.

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The authors declare that they have no competing interests.

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Key Points

• CGD-associated inflammatory bowel disease (IBD) resolves after allogeneic hematopoietic cell transplant (HCT).

• Five-year survival following allogeneic HCT was greater than 80% in this PIDTC CGD cohort, and baseline IBD did not adversely affect survival.

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Marsh, R.A., Leiding, J.W., Logan, B.R. et al. Chronic Granulomatous Disease-Associated IBD Resolves and Does Not Adversely Impact Survival Following Allogeneic HCT. J Clin Immunol 39, 653–667 (2019). https://doi.org/10.1007/s10875-019-00659-8

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