Publications by authors named "Glenn T Furuta"

199 Publications

Transition of Care from Pediatric to Adult Care in Eosinophilic Esophagitis: Insights from a Patient Perspective Survey.

J Pediatr Gastroenterol Nutr 2021 Sep 17. Epub 2021 Sep 17.

Gastrointestinal Eosinophilic Diseases Program, Department of Pediatrics, University of Colorado School of Medicine, Digestive Health Institute, Children's Hospital of Colorado Aurora, CO Trinity Partners, LLC, Waltham, MA Shire Human Genetic Therapies, Inc., a Takeda company, Cambridge, MA Takeda Pharmaceuticals USA, Inc., Lexington, MA The Department of Internal Medicine, Division of Gastroenterology, University of Pennsylvania Perelman School of Medicine, Hospital of the University of Pennsylvania, Philadelphia, PA.

Abstract: Eosinophilic esophagitis (EoE) is a chronic immune-mediated disease. Patients with a childhood diagnosis require ongoing disease management in adulthood. However, knowledge of the patient experience during pediatric to adult healthcare transition is lacking. Here, an online survey captured patient perceptions of the challenges faced by patients with EoE in the USA during transition to adult healthcare, and which resources, if implemented, could better support transition. Of 67 respondents, 91% (n = 61) were under adult care at the time of survey completion. Aspects that respondents struggled with most included meal planning, food shopping, cooking/finding foods that did not exacerbate their condition, and knowledge of insurance coverage. Although most respondents reported confidence in having the knowledge to manage their EoE, almost half of the respondents worried about managing their condition in the future. Resources detailing diet, medication and insurance management strategies could support the transition to adult healthcare for patients with EoE.
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http://dx.doi.org/10.1097/MPG.0000000000003303DOI Listing
September 2021

Ciclesonide Impacts Clinicopathological Features of Eosinophilic Esophagitis.

J Allergy Clin Immunol Pract 2021 Jul 19. Epub 2021 Jul 19.

Department of Pediatrics, Gastrointestinal Eosinophilic Diseases Program, Section of Pediatric Gastroenterology, Hepatology and Nutrition, University of Colorado School of Medicine, Aurora, Colo; Digestive Health Institute, Children's Hospital Colorado, Aurora, Colo; Mucosal Inflammation Program, University of Colorado School of Medicine, Aurora, Colo.

Background: Eosinophilic esophagitis (EoE) is a chronic allergen-mediated disease of the esophagus. Pharmacologic treatment has largely relied on repurposing corticosteroids. Ciclesonide (CIC) is a corticosteroid for the treatment of asthma with biochemical properties that improve topical potency.

Objective: To determine whether CIC decreased clinicopathological features of EoE.

Methods: We performed a retrospective cohort study of patients with EoE treated with CIC at a pediatric hospital from 2010 to 2019. Data were extracted from the electronic health record. Patients who were prescribed CIC with pre- and post-CIC endoscopic and histological data available were included for analysis.

Results: A total of 281 patients were treated with CIC and 81 met criteria for inclusion. Use of CIC was associated with reduced symptoms including dysphagia (P < .001), abdominal pain (P < .001), vomiting (P = .01), heartburn (P = .02), and behavior changes (P = .02). Average composite endoscopic reference scores decreased from 2.54 to 1.37 (P < .001), with improvement in exudates, edema, and furrows (all P < .001). Peak eosinophil counts decreased from 48 to 23 eosinophils/hpf (P < .001). Forty-three patients (53%) achieved remission (<15 eosinophils/hpf). Esophageal Candida was reported in 1 patient. Fasting morning cortisol concentrations were low in 10 of 31 patients tested. Six of these 10 patients had abnormal adrenocorticotropic hormone stimulation testing, 5 of 6 diagnosed with adrenal insufficiency before transition to CIC and 3 of 6 with subsequent normalization of adrenal function on CIC therapy.

Conclusions: Patients with EoE treated with CIC experienced significant reductions in clinicopathological features of EoE. CIC can be considered an alternative therapy in patients with known adrenal insufficiency or at risk of developing adrenal insufficiency.
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http://dx.doi.org/10.1016/j.jaip.2021.06.058DOI Listing
July 2021

Development of a core outcome set for therapeutic studies in eosinophilic esophagitis (COREOS).

J Allergy Clin Immunol 2021 Jul 6. Epub 2021 Jul 6.

Inform Diagnostics, Irving, Tex; Department of Pathology, Baylor College of Medicine, Houston, Tex.

Background: End points used to determine treatment efficacy in eosinophilic esophagitis (EoE) have evolved over time. With multiple novel therapies in development for EoE, harmonization of outcomes measures will facilitate evidence synthesis and appraisal when comparing different treatments.

Objective: We sought to develop a core outcome set (COS) for controlled and observational studies of pharmacologic and diet interventions in adult and pediatric patients with EoE.

Methods: Candidate outcomes were generated from systematic literature reviews and patient engagement interviews and surveys. Consensus was established using an iterative Delphi process, with items voted on using a 9-point Likert scale and with feedback from other participants to allow score refinement. Consensus meetings were held to ratify the outcome domains of importance and the core outcome measures. Stakeholders were recruited internationally and included adult and pediatric gastroenterologists, allergists, dieticians, pathologists, psychologists, researchers, and methodologists.

Results: The COS consists of 4 outcome domains for controlled and observational studies: histopathology, endoscopy, patient-reported symptoms, and EoE-specific quality of life. A total of 69 stakeholders (response rate 95.8%) prioritized 42 outcomes in a 2-round Delphi process, and the final ratification meeting generated consensus on 33 outcome measures. These included measurement of the peak eosinophil count, Eosinophilic Esophagitis Histology Scoring System, Eosinophilic Esophagitis Endoscopic Reference Score, and patient-reported measures of dysphagia and quality of life.

Conclusions: This interdisciplinary collaboration involving global stakeholders has produced a COS that can be applied to adult and pediatric studies of pharmacologic and diet therapies for EoE and will facilitate meaningful treatment comparisons and improve the quality of data synthesis.
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http://dx.doi.org/10.1016/j.jaci.2021.07.001DOI Listing
July 2021

Unsedated transnasal esophagoscopy with virtual reality distraction enables earlier monitoring of dietary therapy in eosinophilic esophagitis.

J Allergy Clin Immunol Pract 2021 Sep 2;9(9):3494-3496. Epub 2021 Jul 2.

Digestive Health Institute, Children's Hospital Colorado, Aurora, Colo; Department of Pediatrics, University of Colorado School of Medicine, Aurora, Colo; Gastrointestinal Eosinophilic Diseases Program, Children's Hospital Colorado, Aurora, Colo.

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http://dx.doi.org/10.1016/j.jaip.2021.06.030DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8459391PMC
September 2021

Do rural health disparities affect prevalence data in pediatric eosinophilic esophagitis?

J Allergy Clin Immunol Pract 2021 06;9(6):2549-2551

Department of Pediatrics, Division of Gastroenterology, Children's Hospital of Philadelphia, Perlman School of Medicine at the University of Pennsylvania, Philadelphia, Pa. Electronic address:

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http://dx.doi.org/10.1016/j.jaip.2021.03.027DOI Listing
June 2021

Long-Lasting Dissociation of Esophageal Eosinophilia and Symptoms Following Dilation in Adults With Eosinophilic Esophagitis.

Clin Gastroenterol Hepatol 2021 May 29. Epub 2021 May 29.

Digestive Health Institute, Children's Hospital Colorado, Gastrointestinal Eosinophilic Diseases Program, Section of Pediatric Gastroenterology, Hepatology and Nutrition, Aurora, Colorado.

Background & Aims: Esophageal dilation improves dysphagia but not inflammation in eosinophilic esophagitis (EoE) patients. We investigated if dilation modifies the association between symptoms and eosinophils per high-power field (eos/hpf).

Methods: Adults enrolled in a multisite prospective Consortium of Gastrointestinal Eosinophilic Disease Researchers OMEGA observational study (NCT02523118) completed the symptom-based EoE activity index (EEsAI) patient-reported outcome instrument and underwent endoscopy with biopsy specimens. Patients were stratified based on dilation status as absent, performed 1 year or less before endoscopy, and performed more than 1 year before endoscopy. Assessments included Spearman correlations of the relationship between symptoms and eos/hpf and linear regression with EEsAI as the outcome, eos/hpf as predictor, and interaction for dilation and eos/hpf.

Results: Among 100 patients (n = 61 males; median age, 37 y), 15 and 40 patients underwent dilation 1 year or less and more than 1 year before index endoscopy, respectively. In nondilated patients, the association between eos/hpf and symptoms was moderate (rho = 0.49; P < .001); for a 10-eos/hpf increase, the predicted EEsAI increased by 2.69 (P = .002). In patients dilated 1 or less and more than 1 year before index endoscopy, this association was abolished (rho = -0.38; P = .157 for ≤1 y and rho = 0.02; P = .883 >1 y); for a 10-eos/hpf increase, the predicted EEsAI changed by -1.64 (P = .183) and 0.78 (P = .494), respectively. Dilation modified the association between symptoms and eos/hpf (P = .005 and P = .187 for interaction terms of eos/hpf and dilation 1 or less years before and more than 1 year before index endoscopy, respectively).

Conclusions: In nondilated EoE adults, eos/hpf correlates modestly with symptoms; this correlation was no longer appreciated in dilated patients, and the dilation effects lasted longer than 1 year. Dilation status should be considered in studies evaluating EoE treatment and for clinical follow-up evaluation.
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http://dx.doi.org/10.1016/j.cgh.2021.05.049DOI Listing
May 2021

Heterogeneity of Intestinal Tissue Eosinophils: Potential Considerations for Next-Generation Eosinophil-Targeting Strategies.

Cells 2021 02 17;10(2). Epub 2021 Feb 17.

Gastrointestinal Eosinophilic Diseases Program, Department of Pediatrics, Digestive Health Institute, Children's Hospital Colorado, University of Colorado School of Medicine, Aurora, CO 80045, USA.

Eosinophils are implicated in the pathophysiology of a spectrum of eosinophil-associated diseases, including gastrointestinal eosinophilic diseases (EGIDs). Biologics that target the IL-5 pathway and are intended to ablate eosinophils have proved beneficial in severe eosinophilic asthma and may offer promise in treating some endotypes of EGIDs. However, destructive effector functions of eosinophils are only one side of the coin; eosinophils also play important roles in immune and tissue homeostasis. A growing body of data suggest tissue eosinophils represent a plastic and heterogeneous population of functional sub-phenotypes, shaped by environmental (systemic and local) pressures, which may differentially impact disease outcomes. This may be particularly relevant to the GI tract, wherein the highest density of eosinophils reside in the steady state, resident immune cells are exposed to an especially broad range of external and internal environmental pressures, and greater eosinophil longevity may uniquely enrich for co-expression of eosinophil sub-phenotypes. Here we review the growing evidence for functional sub-phenotypes of intestinal tissue eosinophils, with emphasis on the multifactorial pressures that shape and diversify eosinophil identity and potential targets to inform next-generation eosinophil-targeting strategies designed to restrain inflammatory eosinophil functions while sustaining homeostatic roles.
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http://dx.doi.org/10.3390/cells10020426DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7922004PMC
February 2021

Type 2 Immunity and Age Modify Gene Expression of Coronavirus-induced Disease 2019 Receptors in Eosinophilic Gastrointestinal Disorders.

J Pediatr Gastroenterol Nutr 2021 05;72(5):718-722

Department of Bioengineering.

Abstract: Infection with severe acute respiratory syndrome coronavirus-2 (SARS-CoV-2) can lead to coronavirus-induced disease 2019 (COVID-19). The gastrointestinal (GI) tract is now an appreciated portal of infection. SARS-CoV-2 enters host cells via angiotensin-converting enzyme-2 (ACE2) and the serine protease TMPRSS2. Eosinophilic gastrointestinal disorders (EGIDs) are inflammatory conditions caused by chronic type 2 (T2) inflammation. the effects of the T2 atopic inflammatory milieu on SARS-COV-2 viral entry gene expression in the GI tract is poorly understood. We analyzed tissue ACE2 and TMPRSS2 gene expression in pediatric eosinophilic esophagitis (EoE), eosinophilic gastritis (EG), and in normal adult esophagi using publicly available RNA-sequencing datasets. Similar to findings evaluating the airway, there was no difference in tissue ACE2/TMPRSS2 expression in EoE or EG when compared with control non-EoE/EG esophagus/stomach. ACE2 gene expression was significantly lower in esophagi from children with or without EoE and from adults with EoE as compared with normal adult esophagi. Type 2 immunity and pediatric age could be protective for infection by SARS-CoV-2 in the gastrointestinal tract because of decreased expression of ACE2.
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http://dx.doi.org/10.1097/MPG.0000000000003032DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8048378PMC
May 2021

Influence of Acid Blockade on the Aerodigestive Tract Microbiome in Children With Cystic Fibrosis.

J Pediatr Gastroenterol Nutr 2021 04;72(4):520-527

Department of Pediatrics, University of Colorado Anschutz Medical Campus, Aurora, CO.

Background: Acid blockade is commonly prescribed in patients with cystic fibrosis (CF). Growing concerns, however, exist about its possible role in the pathophysiology of pulmonary infections. We aimed to investigate if acid blockade alters esophageal and respiratory microbiota leading to dysbiosis and inflammation.

Methods: We performed a cross sectional study of children with CF who were either prescribed acid blockade or not. Samples from the gastrointestinal and respiratory tracts were obtained and microbiome analyzed. Mixed effect models were used to compare outcomes between cohorts and across sampling sites. A random subject intercept was included to account for the multiple sampling sites per individual.

Results: A cohort of 25 individuals, 44% girls with median age of 13.8 years [IQR 11.2--14.8] were enrolled. Alpha diversity, total bacterial load, and beta diversity were similar across anatomic compartments, across the upper gastrointestinal tract, and in respiratory samples. Similar alpha diversity, total bacterial load, and beta diversity results were also observed when comparing individuals on versus those off acid blockade. IL-8 was elevated in the distal versus proximal esophagus in the whole cohort (P < 0.01). IL-8 concentrations were similar in the distal esophagus in patients on and off acid blockade, but significantly greater in the proximal esophagus of subjects on treatment (P < 0.01).

Conclusions: On the basis of these data, acid blockade use does not appear to influence the microbiome of the aerodigestive tract in children with cystic fibrosis suggesting a complex interplay between these medications and the bacterial composition of the esophagus and lung.
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http://dx.doi.org/10.1097/MPG.0000000000003010DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8315410PMC
April 2021

Lower esophageal sphincter muscle of patients with achalasia exhibits profound mast cell degranulation.

Neurogastroenterol Motil 2021 05 6;33(5):e14055. Epub 2020 Dec 6.

Department of Medicine, Center forEsophageal Diseases/Baylor University Medical Center, Center for Esophageal Research/Baylor Scott & White Research Institute, Dallas, TX, USA.

Background: Eosinophils and mast cells are key effectors of allergy. When they accumulate in the esophagus, their myoactive, pro-inflammatory, and cytotoxic products potentially could cause achalasia-like motility abnormalities and neuronal degeneration. We hypothesized that there is an allergy-mediated form of achalasia.

Methods: LES muscle samples obtained during Heller myotomy from patients with achalasia or EGJ outflow obstruction (EGJOO) and from organ donor controls were immunostained for tryptase. Eosinophil and mast cell density, and mast cell degranulation were assessed. LES muscle was evaluated by qPCR for genes mediating smooth muscle Ca handling and contraction.

Key Results: There were 13 patients (7 men, median age 59; 10 achalasia, 3 EGJOO) and 7 controls (4 men, median age 42). Eosinophils were infrequent in LES muscle, but mast cells were plentiful. Patients and controls did not differ significantly in LES mast cell density. However, 12 of 13 patients exhibited profound LES mast cell degranulation involving perimysium and myenteric plexus nerves, while only mild degranulation was seen in 2 of 7 controls. Hierarchical clustering analysis of qPCR data revealed two "mototype" LES gene expression patterns, with all type II patients in one mototype, and type I and III patients in the other.

Conclusions & Inferences: LES muscle of patients with achalasia or EGJOO exhibits striking mast cell degranulation, and patients with different achalasia manometric phenotypes exhibit different LES patterns of expression for genes mediating Ca handling and muscle contraction. Although these findings are not definitive, they support our hypothesis that achalasia can be allergy-driven.
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http://dx.doi.org/10.1111/nmo.14055DOI Listing
May 2021

Case Series: Role of Pill Esophagram to Identify Pediatric Patients With Eosinophilic Esophagitis Amenable to Therapeutic Dilation.

J Pediatr Gastroenterol Nutr 2020 10;71(4):530-532

Gastrointestinal Eosinophilic Diseases Program, Section of Pediatric Gastroenterology, Hepatology and Nutrition, Department of Pediatrics, University of Colorado School of Medicine, Digestive Health Institute.

Eosinophilic esophagitis (EoE) is a chronic disease of the esophagus that leads to esophageal remodeling. Dysphagia is a common symptom that likely results from the inflammatory process or remodeling. Identifying patients that may benefit from dilation can be challenging because of difficulties in detecting subtle narrowing in patients with EoE. Here we report the benefits of a pill esophagram in the detection of esophageal narrowing in EoE. We identified a series of children with EoE and symptoms of dysphagia who underwent barium esophagram with a barium-coated pill to assess symptoms. Three subjects had a normal fluoroscopic esophagram but had pill retention for greater than 5 minutes. Subsequent esophagoscopy and esophageal dilation revealed mucosal rent after dilation. Subtle esophageal narrowing may not be captured with barium esophagram alone in children with EoE and dysphagia. Use of the barium pill in symptomatic patients can assist in identifying patients who may benefit from esophageal dilation.
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http://dx.doi.org/10.1097/MPG.0000000000002823DOI Listing
October 2020

Parent Perspectives on Exclusive Enteral Nutrition for the Treatment of Pediatric Crohn Disease.

J Pediatr Gastroenterol Nutr 2020 12;71(6):744-748

Department of Pediatrics, Digestive Health Institute.

Objectives: Exclusive enteral nutrition (EEN) is infrequently used in the United States but is an effective treatment for pediatric Crohn disease (CD). Limited data exists regarding patient and parent perspectives on this treatment modality. The aim of this study was to determine parent and provider perspectives regarding EEN and understand parent-cited barriers to its use.

Methods: We surveyed the parents/guardians of children ages 1 through 17 with CD in our institution regarding EEN. Healthcare provider perspectives regarding reason for stopping EEN and those cited by survey respondents were compared using retrospective chart review.

Results: One hundred fifteen (62.5%) out of 184 recipients responded to the survey. Ninety percentage of respondents had heard of EEN but of these, 26% had not discussed it with their gastroenterologist. Thirty-eight patients (33%) were treated in the past and 15 (13%) were currently on EEN. Common barriers cited by current EEN users were cost/finances and difficult social situations. Of the children who stopped EEN, most did so as parents felt it was not working (n = 14, 37%). In these cases, their primary gastroenterologist cited treatment failure for 4 cases and nonadherence for 6.

Conclusions: Despite the efficacy of EEN and interest in dietary treatments by patients with CD, there are many barriers surrounding effective communication and successful implementation of dietary therapies. Future research is needed regarding patient-physician communication, cost mitigation, and coping with the social limitations of dietary therapies.
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http://dx.doi.org/10.1097/MPG.0000000000002847DOI Listing
December 2020

Food-induced immediate response of the esophagus-A newly identified syndrome in patients with eosinophilic esophagitis.

Allergy 2021 01 19;76(1):339-347. Epub 2020 Aug 19.

Department of Gastroenterology and Hepatology, University Hospital Zurich, Zurich, Switzerland.

Background: Dysphagia is the main symptom of adult eosinophilic esophagitis (EoE). We describe a novel syndrome, referred to as "food-induced immediate response of the esophagus" (FIRE), observed in EoE patients.

Methods: Food-induced immediate response of the esophagus is an unpleasant/painful sensation, unrelated to dysphagia, occurring immediately after esophageal contact with specific foods. Eosinophilic esophagitis experts were surveyed to estimate the prevalence of FIRE, characterize symptoms, and identify food triggers. We also surveyed a large group of EoE patients enrolled in the Swiss EoE Cohort Study for FIRE.

Results: Response rates were 82% (47/57) for the expert and 65% (239/368) for the patient survey, respectively. Almost, 90% of EoE experts had observed the FIRE symptom complex in their patients. Forty percent of EoE patients reported experiencing FIRE, more commonly in patients who developed EoE symptoms at a younger age (mean age of 46.4 years vs 54.1 years without FIRE; P < .01) and in those with high allergic comorbidity. Food-induced immediate response of the esophagus symptoms included narrowing, burning, choking, and pressure in the esophagus appearing within 5 minutes of ingesting a provoking food that lasted less than 2 hours. Symptom severity rated a median 7 points on a visual analogue scale from 1 to 10. Fresh fruits/vegetables and wine were the most frequent triggers. Endoscopic food removal was significantly more commonly reported in male patients with vs without FIRE (44.3% vs 27.6%; P = .03).

Conclusions: Food-induced immediate response of the esophagus is a novel syndrome frequently reported in EoE patients, characterized by an intense, unpleasant/painful sensation occurring rapidly and reproducibly in 40% of surveyed EoE patients after esophageal contact with specific foods.
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http://dx.doi.org/10.1111/all.14495DOI Listing
January 2021

Technical Review on the Management of Eosinophilic Esophagitis: A Report From the AGA Institute and the Joint Task Force on Allergy-Immunology Practice Parameters.

Gastroenterology 2020 05;158(6):1789-1810.e15

Center for Esophageal Diseases and Swallowing, Division of Gastroenterology and Hepatology, University of North Carolina School of Medicine, Chapel Hill, North Carolina.

Eosinophilic esophagitis (EoE) is a chronic inflammatory condition of the esophagus. Many new studies have been reported recently that describe EoE management. An expert panel was convened by the American Gastroenterological Association Institute and the Joint Task Force on Allergy-Immunology Practice Parameters to provide a technical review to be used as the basis for an updated clinical guideline. This technical review was developed using the Grading of Recommendations Assessment, Development, and Evaluation (GRADE) framework. Eighteen focused EoE management questions were considered, with 15 answered using the GRADE framework and 3 with a narrative summary. There is moderate certainty in the evidence that topical glucocorticosteroids effectively reduce esophageal eosinophil counts to <15 per high-power field over a short-term treatment period of 4-12 weeks, but very low certainty about the effects of using topical glucocorticosteroids as maintenance therapy. Multiple dietary strategies may be effective in reducing esophageal eosinophil counts to <15 per high-power field over a short-term treatment period, with moderate certainty for elemental diets, low certainty for empiric 2-, 4-, and 6-food elimination diets, and very low certainty that allergy-based testing dietary eliminations have a higher failure rate compared to empiric diet elimination. There is very low certainty for the effect of proton pump inhibitors in patients with esophageal eosinophilia. Although esophageal dilation appears to be relatively safe, there is no evidence that it reduces esophageal eosinophil counts. There is very low certainty in the effects of multiple other medical treatments for EoE: anti-interleukin-5 therapy, anti-interleukin-13 therapy, anti-IgE therapy, montelukast, cromolyn, and anti-TNF therapy.
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http://dx.doi.org/10.1053/j.gastro.2020.02.039DOI Listing
May 2020

Technical review on the management of eosinophilic esophagitis: a report from the AGA institute and the joint task force on allergy-immunology practice parameters.

Ann Allergy Asthma Immunol 2020 05;124(5):424-440.e17

Center for Esophageal Diseases and Swallowing, Division of Gastroenterology and Hepatology, University of North Carolina School of Medicine, Chapel Hill, North Carolina.

Eosinophilic esophagitis (EoE) is a chronic inflammatory condition of the esophagus. Many new studies have been reported recently that describe EoE management. An expert panel was convened by the American Gastroenterological Association Institute and the Joint Task Force on Allergy-Immunology Practice Parameters to provide a technical review to be used as the basis for an updated clinical guideline. This technical review was developed using the Grading of Recommendations Assessment, Development, and Evaluation (GRADE) framework. Eighteen focused EoE management questions were considered, with 15 answered using the GRADE framework and 3 with a narrative summary. There is moderate certainty in the evidence that topical glucocorticosteroids effectively reduce esophageal eosinophil counts to <15 per high-power field over a short-term treatment period of 4-12 weeks, but very low certainty about the effects of using topical glucocorticosteroids as maintenance therapy. Multiple dietary strategies may be effective in reducing esophageal eosinophil counts to <15 per high-power field over a short-term treatment period, with moderate certainty for elemental diets, low certainty for empiric 2-, 4-, and 6-food elimination diets, and very low certainty that allergy-based testing dietary eliminations have a higher failure rate compared to empiric diet elimination. There is very low certainty for the effect of proton pump inhibitors in patients with esophageal eosinophilia. Although esophageal dilation appears to be relatively safe, there is no evidence that it reduces esophageal eosinophil counts. There is very low certainty in the effects of multiple other medical treatments for EoE: anti-interleukin-5 therapy, anti-interleukin-13 therapy, anti-IgE therapy, montelukast, cromolyn, and anti-TNF therapy.
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http://dx.doi.org/10.1016/j.anai.2020.03.021DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8171057PMC
May 2020

Esophageal type 2 cytokine expression heterogeneity in eosinophilic esophagitis in a multisite cohort.

J Allergy Clin Immunol 2020 06 19;145(6):1629-1640.e4. Epub 2020 Mar 19.

Division of Allergy and Immunology, Department of Pediatrics, Cincinnati Children's Hospital Medical Center, University of Cincinnati College of Medicine, Cincinnati, Ohio. Electronic address:

Background: There is strong evidence for a role of type 2 cytokines in the pathogenesis of eosinophilic esophagitis (EoE); however, heterogeneity in type 2 gene expression has not been examined.

Objective: We examined type 2 immunity-associated gene expression in esophageal biopsy specimens, aiming to determine the degree of cytokine heterogeneity and its potential clinical significance.

Methods: Patients (n = 312) were recruited from 10 sites associated with the Consortium of Eosinophilic Gastrointestinal Disease Researchers. In addition to histologic and endoscopic assessment, esophageal biopsy specimens were examined for expression of 96 genes within the EoE diagnostic panel.

Results: Five subgroups of patients with active EoE were identified by unsupervised clustering based on expression of IL4, IL5, IL13, C-C motif chemokine ligand 26 (CCL26), thymic stromal lymphopoietin (TSLP), Charcot-Leyden crystal (CLC), C-C motif chemokine receptor 3 (CCR3), and CPA3. These groups differed in age (P < .02) and EoE diagnostic panel score (P < 1.08E-30) but not in eosinophil levels. The group V patients had the highest expression of IL5, TSLP, and CCL26 and genes associated with tissue remodeling, such as COL8A1, actin γ-2 (ACTG2), and tetraspanin 12 (TSPAN12). IL5 and IL13 were highly expressed in group IV; however, groups IV and V differed in age (34 vs 14 years [P < .05]). Groups II and III, which exhibited intermediate expression of IL5 and CPA3, were differentiated by high TSLP and IL13 in group III.

Conclusion: We observed heterogeneous type 2 gene expression among patients with active EoE. Type 2 gene overexpression was not directly proportional to disease features; this was especially true for tissue remodeling events. These findings highlight a clinical opportunity for leveraging molecular endotypes to implement personalized medicine in EoE.
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http://dx.doi.org/10.1016/j.jaci.2020.01.051DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7309223PMC
June 2020

Hypoxia and Innate Immunity: Keeping Up with the HIFsters.

Annu Rev Immunol 2020 04 21;38:341-363. Epub 2020 Jan 21.

UCD Conway Institute, Systems Biology Ireland and School of Medicine, University College Dublin, Belfield, Dublin 4, Ireland.

Recent years have witnessed an emergence of interest in understanding metabolic changes associated with immune responses, termed immunometabolism. As oxygen is central to all aerobic metabolism, hypoxia is now recognized to contribute fundamentally to inflammatory and immune responses. Studies from a number of groups have implicated a prominent role for oxygen metabolism and hypoxia in innate immunity of healthy tissue (physiologic hypoxia) and during active inflammation (inflammatory hypoxia). This inflammatory hypoxia emanates from a combination of recruited inflammatory cells (e.g., neutrophils, eosinophils, and monocytes), high rates of oxidative metabolism, and the activation of multiple oxygen-consuming enzymes during inflammation. These localized shifts toward hypoxia have identified a prominent role for the transcription factor hypoxia-inducible factor (HIF) in the regulation of innate immunity. Such studies have provided new and enlightening insight into our basic understanding of immune mechanisms, and extensions of these findings have identified potential therapeutic targets. In this review, we summarize recent literature around the topic of innate immunity and mucosal hypoxia with a focus on transcriptional responses mediated by HIF.
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http://dx.doi.org/10.1146/annurev-immunol-100819-121537DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7924528PMC
April 2020

Approaches and Challenges to Management of Pediatric and Adult Patients With Eosinophilic Esophagitis.

Gastroenterology 2020 03 10;158(4):840-851. Epub 2019 Dec 10.

Digestive Health Institute, Children's Hospital Colorado, Gastrointestinal Eosinophilic Diseases Program, University of Colorado School of Medicine, Aurora, Colorado.

Treatment of eosinophilic esophagitis has progressed from elemental formula for children and esophageal dilation for adults to selective exclusion of food triggers and swallowed topical corticosteroids. Management guidelines are available from the American Gastroenterological Association and the Joint Task Force on Allergy Immunology Practice Parameters. We cannot, however, evaluate the efficacy of treatments without a definition of response. We propose a treat-to-target approach, based on symptoms and findings from endoscopy and histology. This approach addresses dissociations between outcomes, such as symptom persistence despite normalization of histologic features and symptom resolution after esophageal dilation despite histologic features of active disease. Eosinophilic esophagitis can now be treated with biologic agents that target specific immune pathways, and findings from prospective trials have indicated that less-restrictive, empiric, elimination diets can be effective and reduce the need for repeated endoscopic assessment of disease activity during food reintroduction. We also discuss eosinophilic esophagitis subtypes, factors associated with disease, and advances in management.
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http://dx.doi.org/10.1053/j.gastro.2019.09.052DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8063595PMC
March 2020

Association Between Endoscopic and Histologic Findings in a Multicenter Retrospective Cohort of Patients with Non-esophageal Eosinophilic Gastrointestinal Disorders.

Dig Dis Sci 2020 07 26;65(7):2024-2035. Epub 2019 Nov 26.

Center for Esophageal Diseases and Swallowing and Center for Gastrointestinal Biology and Disease, Division of Gastroenterology and Hepatology, Department of Medicine, University of North Carolina School of Medicine, CB #7080, Chapel Hill, NC, 27599, USA.

Background: Little is known about the endoscopic and histologic findings of non-esophageal eosinophilic gastrointestinal diseases (EGID).

Aim: To characterize the presenting endoscopic and histologic findings in patients with eosinophilic gastritis (EG), eosinophilic gastroenteritis (EGE), and eosinophilic colitis (EC) at diagnosis and 6 months after initiating the treatment.

Methods: We conducted a retrospective cohort study at 6 US centers associated with the Consortium of Eosinophilic Gastrointestinal Researchers. Data abstracted included demographics, endoscopic findings, tissue eosinophil counts, and associated histologic findings at diagnosis and, when available, after initial treatment.

Results: Of 373 subjects (317 children and 56 adults), 142 had EG, 123 EGE, and 108 EC. Normal endoscopic appearance was the most common finding across all EGIDs (62% of subjects). Baseline tissue eosinophil counts were quantified in 105 (74%) EG, 36 (29%) EGE, and 80 (74%) EC subjects. The mean peak gastric eosinophil count across all sites was 87 eos/hpf for EG and 78 eos/hpf for EGE. The mean peak colonic eosinophil count for EC subjects was 76 eos/hpf (range 10-500). Of the 29% of subjects with post-treatment follow-up, most had an improvement in clinical, endoscopic, and histologic findings regardless of treatment utilized. Reductions in tissue eosinophilia correlated with improvements in clinical symptoms as well as endoscopic and histologic findings.

Conclusions: In this large cohort, normal appearance was the most common endoscopic finding, emphasizing the importance of biopsy, regardless of endoscopic appearance. Decreased tissue eosinophilia was associated with improvement in symptoms, endoscopic, and histologic findings, showing that disease activity is reversible.
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http://dx.doi.org/10.1007/s10620-019-05961-4DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7315780PMC
July 2020

Advancing patient care through the Consortium of Eosinophilic Gastrointestinal Disease Researchers (CEGIR).

J Allergy Clin Immunol 2020 01 20;145(1):28-37. Epub 2019 Nov 20.

Division of Gastroenterology, Northwestern University Feinberg School of Medicine, Chicago, Ill.

Recent advances in rare disease research are accelerated by the work of consortia that have been supported by the National Institutes of Health. Development of such consortia rely on multidisciplinary relationships and engagement with patient advocacy groups, as well as the National Institutes of Health and industry and academic partners. In this rostrum we present the development of such a process that focuses on eosinophilic gastrointestinal diseases. Principal investigators, patient advocacy groups, research assistants, and trainees work together to perform natural history studies that promote clinical trial readiness tools, conduct clinical trials, train a new generation of investigators, and perform innovative pilot studies.
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http://dx.doi.org/10.1016/j.jaci.2019.11.012DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6981250PMC
January 2020

Molecular, endoscopic, histologic, and circulating biomarker-based diagnosis of eosinophilic gastritis: Multi-site study.

J Allergy Clin Immunol 2020 01 16;145(1):255-269. Epub 2019 Nov 16.

Division of Allergy and Immunology, University of Cincinnati College of Medicine and Cincinnati Children's Hospital Medical Center, Cincinnati, Ohio. Electronic address:

Background: Eosinophilic gastritis (EG) is a clinicopathologic disorder with marked gastric eosinophilia and clinical symptoms. There is an unmet need among patients with EG for more precise diagnostic tools.

Objective: We aimed to develop tissue- and blood-based diagnostic platforms for EG.

Methods: Patients with EG and control subjects without EG were enrolled across 9 Consortium of Eosinophilic Gastrointestinal Disease Researchers-associated sites. An EG Diagnostic Panel (EGDP; gastric transcript subset) and EG blood biomarker panel (protein multiplex array) were analyzed. EGDP scores were derived from the expression of 18 highly dysregulated genes, and blood EG scores were derived from dysregulated cytokine/chemokine levels.

Results: Gastric biopsy specimens and blood samples from 185 subjects (patients with EG, n = 74; control subjects without EG, n = 111) were analyzed. The EGDP (1) identified patients with active EG (P < .0001, area under the curve ≥ 0.95), (2) effectively monitored disease activity in longitudinal samples (P = .0078), (3) highly correlated in same-patient samples (antrum vs body, r = 0.85, P < .0001), and (4) inversely correlated with gastric peak eosinophil levels (r = -0.83, P < .0001), periglandular circumferential collars (r = -0.73, P < .0001), and endoscopic nodularity (r = -0.45, P < .0001). For blood-based platforms, eotaxin-3, thymus and activation-regulated chemokine, IL-5, and thymic stromal lymphopoietin levels were significantly increased. Blood EG scores (1) distinguished patients with EG from control subjects without EG (P < .0001, area under the curve ≥ 0.91), (2) correlated with gastric eosinophil levels (plasma: r = 0.72, P = .0002; serum: r = 0.54, P = .0015), and (3) inversely correlated with EGDP scores (plasma: r = -0.64, P = .0015; serum: r = -0.46, P = .0084). Plasma eotaxin-3 levels strongly associated with gastric CCL26 expression (r = 0.81, P < .0001).

Conclusion: We developed tissue- and blood-based platforms for assessment of EG and uncovered robust associations between specific gastric molecular profiles and histologic and endoscopic features, providing insight and clinical readiness tools for this emerging rare disease.
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http://dx.doi.org/10.1016/j.jaci.2019.11.007DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6949389PMC
January 2020

Adrenal Insufficiency in Children With Eosinophilic Esophagitis Treated With Topical Corticosteroids.

J Pediatr Gastroenterol Nutr 2020 03;70(3):324-329

Division of Pediatric Gastroenterology, Hepatology, and Nutrition, University of Illinois College of Medicine/Children's Hospital of Illinois, Peoria, IL.

Objectives: The aim of the study was to identify practices of gastroenterologists screening for adrenal insufficiency (AI) and report prevalence of AI in children with eosinophilic esophagitis (EoE) treated with topical corticosteroids (TCS); compare serum dehydroepiandrosterone sulfate (DHEA-S) levels to morning serum cortisol (MSC) levels as screening tool for AI.

Methods: A multipart study was conducted. In part 1, a survey about screening practices for AI in children with EoE on TCS was sent to gastroenterologists belonging to a PedsGI listserv and to EoE consortia. In part 2, children with EoE on TCS for ≥6 months were prospectively screened for AI with MSC levels. For subjects with a MSC level of <10 μg/dL, a repeat MSC level and/or confirmatory adrenocorticotropic hormone (ACTH) stimulation testing was offered. AI was defined by peak serum cortisol level <18 μg/dL. In part 3, DHEA-S levels were drawn with MSC levels.

Results: Seven percent (16/238) of gastroenterologists screened for AI. Providers in EoE consortia were more likely to screen than nonconsortia providers [9/21(43%) vs 7/217(3%); P = 0.0001]. Thirty-seven children were prospectively screened for AI, and 51% (19/37) had a low MSC level. Ten patients had a low-dose ACTH stimulation test (LDST) after 1 or more low MSC levels. Five percent (2/37) of patients were diagnosed with AI. DHEA-S and MSC levels had a moderate correlation (rs = 0.44, P = 0.03).

Conclusions: Gastroenterologists belonging to EoE consortia were more likely to screen for AI. Prevalence of AI in our prospective cohort was 5%. DHEA-S has a moderate correlation with MSC levels, but more data is required to assess utility as a screening tool for AI.
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http://dx.doi.org/10.1097/MPG.0000000000002537DOI Listing
March 2020

One-Hour Esophageal String Test: A Nonendoscopic Minimally Invasive Test That Accurately Detects Disease Activity in Eosinophilic Esophagitis.

Am J Gastroenterol 2019 10;114(10):1614-1625

Department of Pediatrics, Gastrointestinal Eosinophilic Diseases Program.

Objectives: Eosinophilic esophagitis (EoE), a chronic food allergic disease, lacks sensitive and specific peripheral biomarkers. We hypothesized that levels of EoE-related biomarkers captured using a 1-hour minimally invasive Esophageal String Test (EST) would correlate with mucosal eosinophil counts and tissue concentrations of these same biomarkers. We aimed to determine whether a 1-hour EST accurately distinguishes active from inactive EoE or a normal esophagus.

Methods: In a prospective, multisite study, children and adults (ages 7-55 years) undergoing a clinically indicated esophagogastroduodenoscopy performed an EST with an esophageal dwell time of 1 hour. Subjects were divided into 3 groups: active EoE, inactive EoE, and normal esophageal mucosa. Eosinophil-associated protein levels were compared between EST effluents and esophageal biopsy extracts. Statistical modeling was performed to select biomarkers that best correlated with and predicted eosinophilic inflammation.

Results: One hundred thirty-four subjects (74 children, 60 adults) with active EoE (n = 62), inactive EoE (n = 37), and patient controls with a normal esophagus (n = 35) completed the study. EST-captured eosinophil-associated biomarkers correlated significantly with peak eosinophils/high-power field, endoscopic visual scoring, and the same proteins extracted from mucosal biopsies. Statistical modeling, using combined eotaxin-3 and major basic protein-1 concentrations, led to the development of EoE scores that distinguished subjects with active EoE from inactive EoE or normal esophagi. Eighty-seven percent of children, 95% of parents, and 92% of adults preferred the EST over endoscopy if it provided similar information.

Discussion: The 1-hour EST accurately distinguishes active from inactive EoE in children and adults and may facilitate monitoring of disease activity in a safe and minimally invasive fashion.
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http://dx.doi.org/10.14309/ajg.0000000000000371DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6784776PMC
October 2019

Symptom Burden and Quality of Life Over Time in Pediatric Eosinophilic Esophagitis.

J Pediatr Gastroenterol Nutr 2019 12;69(6):682-689

University of Colorado School of Medicine.

Objective: The aim of the study was to evaluate whether children with eosinophilic esophagitis (EoE) demonstrated an association between health-related quality of life (HRQoL) improvements and symptom reduction during 12 months of treatment; to examine age-related EoE discrete symptom presentation; and to describe residual symptom and HRQoL burden.

Methods: Children ages 2 to 18 years with EoE were assessed at the onset of treatment and 12 months later at 4 tertiary care centers. Continuous measures of symptoms and symptom severity were based on 8 discrete EoE symptoms. HRQoL was measured with the Pediatric Quality of Life (PedsQL) parent-proxy (PR) report, child self-report (CR), and Family Impact Module. Mixed-effects modeling was used to test changes over time for symptom burden and child and family HRQoL.

Results: One hundred nine children were followed (ages 2-18 years, mean age 7.6 [4.6] years, 77% boys, 87% white). Baseline symptom number mean was 3.5 (standard deviation = 2.3, range 0-8) and symptom severity mean was 5.5 (standard deviation = 4.3, range 0-24). EoE symptom number and symptom severity decreased significantly over the 12 months (P = 0.013, P < 0.001, respectively). PedsQL PR Total, Physical, Psychosocial, and Family Impact scores all improved significantly (P = 0.001, 0.012, 0.012, 0.015, respectively) but PedsQL child self-report scores did not. Symptom reduction correlated with PR PedsQL improvement (P = 0.01). Few discrete symptoms completely remitted, but lowered severity ratings indicated clinically significant improvement.

Conclusions: Year-long treatment in multidisciplinary tertiary centers reduced most symptoms and improved parent-reported HRQoL in children with EoE. The frequency of residual symptoms and persistently lower HRQoL, however, underscore the chronic nature of pediatric EoE.
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http://dx.doi.org/10.1097/MPG.0000000000002479DOI Listing
December 2019

Opportunities for Innovation and Improved Care Using Telehealth for Nutritional Interventions.

Gastroenterology 2019 09 13;157(3):594-597. Epub 2019 Jun 13.

Department of Pediatrics, University of Colorado, Children's Hospital Colorado, Digestive Health Institute, Aurora, Colorado. Electronic address:

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http://dx.doi.org/10.1053/j.gastro.2019.04.052DOI Listing
September 2019

Climbing New Mountains: How Antibodies Blocking α4β7 Integrins Tamed Eosinophilic Inflammation of the Intestinal Tract.

Dig Dis Sci 2019 08;64(8):2068-2071

Department of Pediatrics, Gastrointestinal Eosinophilic Diseases Program, Section of Pediatric Gastroenterology, Hepatology and Nutrition, University of Colorado School of Medicine, 12700 East 19th Avenue, Research 2 P15-6026 Mail Stop: C-226, Aurora, CO, 80045, USA.

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http://dx.doi.org/10.1007/s10620-019-05706-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6946547PMC
August 2019

Epithelial HIF-1α/claudin-1 axis regulates barrier dysfunction in eosinophilic esophagitis.

J Clin Invest 2019 07 2;129(8):3224-3235. Epub 2019 Jul 2.

Gastrointestinal Eosinophilic Diseases Program, Department of Pediatrics, University of Colorado School of Medicine; Digestive Health Institute, Children's Hospital Colorado; Aurora, Colorado, USA.

Epithelial barrier dysfunction is a significant factor in many allergic diseases, including eosinophilic esophagitis (EoE). Infiltrating leukocytes and tissue adaptations increase metabolic demands and decrease oxygen availability at barrier surfaces. Understanding of how these processes impact barrier is limited, particularly in allergy. Here, we identified a regulatory axis whereby the oxygen-sensing transcription factor HIF-1α orchestrated epithelial barrier integrity, selectively controlling tight junction CLDN1 (claudin-1). Prolonged experimental hypoxia or HIF1A knockdown suppressed HIF-1α-dependent claudin-1 expression and epithelial barrier function, as documented in 3D organotypic epithelial cultures. L2-IL5OXA mice with EoE-relevant allergic inflammation displayed localized eosinophil oxygen metabolism, tissue hypoxia, and impaired claudin-1 barrier via repression of HIF-1α/claudin-1 signaling, which was restored by transgenic expression of esophageal epithelial-targeted stabilized HIF-1α. EoE patient biopsy analysis identified a repressed HIF-1α/claudin-1 axis, which was restored via pharmacologic HIF-1α stabilization ex vivo. Collectively, these studies reveal HIF-1α's critical role in maintaining barrier and highlight the HIF-1α/claudin-1 axis as a potential therapeutic target for EoE.
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http://dx.doi.org/10.1172/JCI126744DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6668670PMC
July 2019

Increasing Rates of Diagnosis, Substantial Co-Occurrence, and Variable Treatment Patterns of Eosinophilic Gastritis, Gastroenteritis, and Colitis Based on 10-Year Data Across a Multicenter Consortium.

Am J Gastroenterol 2019 06;114(6):984-994

Center for Esophageal Diseases and Swallowing and Center for Gastrointestinal Biology and Disease, Division of Gastroenterology and Hepatology, Department of Medicine, University of North Carolina School of Medicine, Chapel Hill, North Carolina, USA.

Objectives: The literature related to eosinophilic gastritis (EG), gastroenteritis (EGE), and colitis (EC) is limited. We aimed to characterize rates of diagnosis, clinical features, and initial treatments for patients with EG, EGE, and EC.

Methods: In this retrospective study, data were collected from 6 centers in the Consortium of Eosinophilic Gastrointestinal Researchers from 2005 to 2016. We analyzed demographics, time trends in diagnosis, medical history, presenting symptoms, disease overlap, and initial treatment patterns/responses.

Results: Of 373 subjects (317 children and 56 adults), 38% had EG, 33% EGE, and 29% EC. Rates of diagnosis of all diseases increased over time. There was no male predominance, and the majority of subjects had atopy. Presenting symptoms were similar between diseases with nausea/vomiting and abdominal pain, the most common. One hundred fifty-four subjects (41%) had eosinophilic inflammation outside of their primary disease location with the esophagus the second most common gastrointestinal (GI) segment involved. Multisite inflammation was more common in children than in adults (68% vs 37%; P < 0.001). Initial treatment patterns varied highly between centers. One hundred-nine subjects (29%) had follow-up within 6 months, and the majority had clinical, endoscopic, and histologic improvements.

Conclusions: In this cohort, EG, EGE, and EC were diagnosed more frequently over time, and inflammation of GI segments outside the primary disease site co-occurrence of atopy was common with a lack of male predominance. Symptoms were similar between diseases, and initial treatment strategies were highly variable. Future investigation should assess the cause of the increased prevalence of eosinophilic GI disorders and prospectively assess outcomes to establish treatment algorithms.
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http://dx.doi.org/10.14309/ajg.0000000000000228DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6554065PMC
June 2019

Overestimation of the diagnosis of eosinophilic colitis with reliance on billing codes.

J Allergy Clin Immunol Pract 2019 Sep - Oct;7(7):2434-2436. Epub 2019 Mar 25.

Center for Pediatric Eosinophilic Diseases, Division of Gastroenterology and Hepatology & Nutrition, Children's Hospital of Philadelphia, Perelman School of Medicine at the University of Pennsylvania, Philadelphia, Pa.

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http://dx.doi.org/10.1016/j.jaip.2019.03.020DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8146896PMC
October 2020

Mobile health tool detects adherence rates in pediatric patients with eosinophilic esophagitis.

J Allergy Clin Immunol Pract 2019 Sep - Oct;7(7):2437-2439. Epub 2019 Mar 23.

Department of Family Medicine, University of Colorado School of Medicine, Aurora, Colo.

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http://dx.doi.org/10.1016/j.jaip.2019.03.016DOI Listing
October 2020
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