Retrospective Study
Copyright ©The Author(s) 2018. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Feb 7, 2018; 24(5): 623-630
Published online Feb 7, 2018. doi: 10.3748/wjg.v24.i5.623
Impaired granulocyte-macrophage colony-stimulating factor bioactivity accelerates surgical recurrence in ileal Crohn’s disease
Grace Gathungu, Yuanhao Zhang, Xinyu Tian, Erin Bonkowski, Leahana Rowehl, Julia Krumsiek, Billy Nix, Claudia Chalk, Bruce Trapnell, Wei Zhu, Rodney Newberry, Lee Denson, Ellen Li
Grace Gathungu, Julia Krumsiek, Department of Pediatrics, Division of Pediatric Gastroenterology, Stony Brook University, Stony Brook, NY 11794, United States
Yuanhao Zhang, Xinyu Tian, Leahana Rowehl, Ellen Li, Department of Medicine, Division of Gastroenterology, Stony Brook University, Stony Brook, NY 11794, United States
Erin Bonkowski, Claudia Chalk, Bruce Trapnell, Lee Denson, Department of Pediatrics, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH 45229-3026, United States
Billy Nix, Rodney Newberry, Department of Medicine, Washington University St. Louis, St. Louis, MO 63110, United States
Wei Zhu, Applied Mathematics and Statistics, Stony Brook University, Stony Brook, NY 11794, United states
Author contributions: Gathungu G, Li E and Denson L designed and performed the research, contributed to the analysis and wrote the paper; Zhang Y, Tian X, Zhu W, Trapnell B and Newberry R designed the research, contributed to the analysis and supervised the report; Krumsiek J, Rowehl L, Bonkowski E, Chalk C and Nix B performed the research and data extraction and contributed to the analysis.
Supported by (in part) the National Institutes of Health, No. R01 DK098231, R01 DK078683 and No. P30DK052574.
Institutional review board statement: This study was reviewed and approved by the Institutional Review Board at Washington University Hospital.
Informed consent statement: Adult patients are recruited in a consecutive fashion by the Washington University Digestive Diseases Research Tissue Procurement Facility and provide verbal and written consent for chart abstraction, blood, stool, tissue biopsies and/or surgical waste collection with analysis for research purposes and for their information to be stored in the hospital database. The IRB at Washington University approved this consent procedure.
Conflict-of-interest statement: The authors have declared that no potential conflicts (financial, professional, or personal) exist that are relevant to the manuscript.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Grace Gathungu, MD, Assistant Professor, Department of Pediatrics, Division of Pediatric Gastroenterology, Stony Brook University Medical Center, HSC T11-080, Stony Brook, NY 11794, United States. grace.gathungu@stonybrookmedicine.edu
Telephone: +1-631-4448115 Fax: +1-631-4446045
Received: November 14, 2017
Peer-review started: November 16, 2017
First decision: November 30, 2017
Revised: December 5, 2017
Accepted: December 12, 2017
Article in press: December 12, 2017
Published online: February 7, 2018
Processing time: 77 Days and 5 Hours
ARTICLE HIGHLIGHTS
Research background

Crohn’s disease (CD) is a chronic inflammatory disease is characterized by a transmural inflammation that targets any region of the gastrointestinal tract. The transmural involvement particularly involving the ileum, often leads to fibrosis, luminal narrowing, and fistulas. In one population based cohort study of adult patients with CD, the cumulative probability of major abdominal surgery was 38% to 58% within 5 to 20 years after diagnosis. Further, disease recurrence resulting in a second surgery for management of CD may occur in 31% to 50% of patients within 10 years of the initial surgery. There remains a need for serological and genetic markers that can reliably identify patients with increased risk for surgical recurrence.

Research motivation

Granulocyte macrophage colony-stimulating factor (GM-CSF) is a cytokine that promotes myeloid cell development and maturation. Deficiency of this important hematopoietic growth factor can contribute to mucosal inflammation and immunodeficiency. We and others have previously shown, neutralizing GM-CSF auto-antibodies (Ab) are associated with a reduced bioactivity of GM-CSF, impaired neutrophil bacterial killing, and increased rates of intestinal resection for ileal CD. In the present study, we examined the predictive capacity of GM-CSF Ab in surgical recurrence rates after initial ileocolic resection for ileal CD. We also evaluated other clinical, serologic and genetic prognostic factors that might define the subset of patients with shorter time to surgical recurrence.

Research objectives

The development of biomarkers for diagnosis and prognosis of CD is evolving and serological assays like ASCA, ANCA, Anti-glycan antibodies and GM-CSF Ab are important discoveries. Some assays are reliable predictors for diagnosis and for staging severity. Here we demonstrate that GM-CSF Ab is a reliable biomarker for characterizing severity and reliably predicts patients at greater risk for aggressive disease behavior and the need for surgery.

Research methods

We reviewed 412 patients which included in the study had ileal or ileocolonic CD and surgical resection of small bowel or ileocecal region for management of disease from a clinical database at tertiary academic hospital. Serum samples were analyzed for serological assays, which included GM-CSF cytokine, GM-CSF Ab, ASCA IgG and IgA, and genetic markers included SNPs rs2066843, rs2066844, rs2066845, rs2076756 and rs2066847 in NOD2, rs2241880 in ATG16L1, and rs13361189 in IRGM. The predictors of surgical recurrence were assessed by the Cox proportional-hazards models.

Research results

Of 96% patients underwent initial Ileocecal resection (ICR) or Ileal resection (IR) and subsequently 40% of patients required a second ICR/IR for CD. GM-CSF Ab level was elevated at a median of 3.81 mcg/mL. Factors predicting faster time to a second surgery included elevated GM-CSF Ab and elevated GM-CSF cytokine. Factors predicting longer duration between first and second surgery included use of Immunomodulators, the interaction effect of low GM-CSF Ab levels and smoking, and the interaction effect of low GM-CSF cytokine levels and ATG16L1.

Research conclusions

In this study patients with elevated GM-CSF Ab had shorter intervals between the first and second surgery for management of CD. This is the first study to describe this. Therefore routine surveillance of this serological assay may facilitate the identification of patients at risk for disease complications and allow clinicians to optimize medical therapy.

Research perspectives

Elevated GM-CSF Ab is a reliable assay for defining patients who are at a greater risk for surgery. A clinical assay is needed.