Multiplexed immunohistochemical evaluation of small bowel inflammatory and epithelial parameters in environmental enteric dysfunction.


Journal

The American journal of clinical nutrition
ISSN: 1938-3207
Titre abrégé: Am J Clin Nutr
Pays: United States
ID NLM: 0376027

Informations de publication

Date de publication:
Sep 2024
Historique:
received: 09 09 2023
revised: 15 01 2024
accepted: 22 02 2024
medline: 20 9 2024
pubmed: 20 9 2024
entrez: 20 9 2024
Statut: ppublish

Résumé

Environmental enteric dysfunction (EED) is characterized by reduced absorptive capacity and barrier function of the small intestine, leading to poor ponderal and linear childhood growth. To further define gene expression patterns that are associated with EED to uncover new pathophysiology of this disorder. Duodenal biopsies from cohorts of children with EED from Bangladesh, Pakistan and Zambia were analyzed by immunohistochemistry (IHC) to interrogate gene products that distinguished differentiation and various biochemical pathways in immune and epithelial cells, some identified by prior bulk RNA sequence analyses. Immunohistochemical staining was digitally quantified from scanned images and compared to cohorts of North American children with celiac disease (gluten-sensitive enteropathy) or with no known enteric disease and no pathologic abnormality (NPA) detected in their clinical biopsies. After multivariable statistical analysis, we identified statistically significant (P < 0.05, 2-tailed t-test) elevated signals representing cluster of differentiation 45 (80%; 95% confidence interval [CI]: 24%, 127%), lipocalin 2 (659%; 95% CI: 198%, 1838%), and regenerating family 1 beta (221%; 95% CI: 47%, 600%) and lower signals corresponding to granzyme B (-74%; 95% CI: -82%, -62%), and sucrase isomaltase (-58%; 95% CI: -75%, -29%) in EED biopsies compared with NPA biopsies. Computerized algorithms also detected statistically significant elevation in intraepithelial lymphocytes (49%; 95% CI: 9%, 105%) and proliferation of leukocytes (267%; 95% CI: 92%, 601%) in EED biopsies compared with NPA biopsies. Our results support a model of chronic epithelial stress that decreases epithelial differentiation and absorptive function. The close association of several IHC parameters with manual histologic scoring suggests that automated digital quantification of IHC panels complements traditional histomorphologic assessment in EED.

Sections du résumé

BACKGROUND BACKGROUND
Environmental enteric dysfunction (EED) is characterized by reduced absorptive capacity and barrier function of the small intestine, leading to poor ponderal and linear childhood growth.
OBJECTIVES OBJECTIVE
To further define gene expression patterns that are associated with EED to uncover new pathophysiology of this disorder.
METHODS METHODS
Duodenal biopsies from cohorts of children with EED from Bangladesh, Pakistan and Zambia were analyzed by immunohistochemistry (IHC) to interrogate gene products that distinguished differentiation and various biochemical pathways in immune and epithelial cells, some identified by prior bulk RNA sequence analyses. Immunohistochemical staining was digitally quantified from scanned images and compared to cohorts of North American children with celiac disease (gluten-sensitive enteropathy) or with no known enteric disease and no pathologic abnormality (NPA) detected in their clinical biopsies.
RESULTS RESULTS
After multivariable statistical analysis, we identified statistically significant (P < 0.05, 2-tailed t-test) elevated signals representing cluster of differentiation 45 (80%; 95% confidence interval [CI]: 24%, 127%), lipocalin 2 (659%; 95% CI: 198%, 1838%), and regenerating family 1 beta (221%; 95% CI: 47%, 600%) and lower signals corresponding to granzyme B (-74%; 95% CI: -82%, -62%), and sucrase isomaltase (-58%; 95% CI: -75%, -29%) in EED biopsies compared with NPA biopsies. Computerized algorithms also detected statistically significant elevation in intraepithelial lymphocytes (49%; 95% CI: 9%, 105%) and proliferation of leukocytes (267%; 95% CI: 92%, 601%) in EED biopsies compared with NPA biopsies.
CONCLUSIONS CONCLUSIONS
Our results support a model of chronic epithelial stress that decreases epithelial differentiation and absorptive function. The close association of several IHC parameters with manual histologic scoring suggests that automated digital quantification of IHC panels complements traditional histomorphologic assessment in EED.

Identifiants

pubmed: 39300661
pii: S0002-9165(24)00279-X
doi: 10.1016/j.ajcnut.2024.02.033
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

S31-S40

Informations de copyright

Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.

Auteurs

Kelley VanBuskirk (K)

Department of Global Health, University of Washington School of Public Health, Seattle, WA, United States.

Monica Mweetwa (M)

Tropical Gastroenterology and Nutrition Group, University of Zambia School of Medicine, Lusaka, Zambia.

Tad Kolterman (T)

Department of Pathology, University of Virginia School of Medicine, Charlottesville, VA, United States.

Shyam Raghavan (S)

Department of Pathology, University of Virginia School of Medicine, Charlottesville, VA, United States.

Tahmeed Ahmed (T)

Nutrition Research Division, International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

S Asad Ali (SA)

Department of Paediatrics and Child Health, Aga Khan University, Karachi, Pakistan.

Sm Khodeza Nahar Begum (SKN)

Department of Pathology, Bangladesh Specialized Hospital, Dhaka, Bangladesh.

Ellen Besa (E)

Tropical Gastroenterology and Nutrition Group, University of Zambia School of Medicine, Lusaka, Zambia.

Donna M Denno (DM)

Department of Pediatrics, University of Washington School of Medicine, Seattle, WA, United States.

Zehra Jamil (Z)

Department of Biological and Biomedical Sciences, Aga Khan University, Karachi, Pakistan.

Paul Kelly (P)

Blizard Institute, Barts & the London School of Medicine, Queen Mary University of London, London, United Kingdom.

Mustafa Mahfuz (M)

Nutrition Research Division, International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Sean R Moore (SR)

Department of Pediatrics, University of Virginia School of Medicine, Charlottesville, VA, United States.

Samer Mouksassi (S)

Certara, Princeton, NJ, United States.

William A Petri (WA)

Department of Medicine, University of Virginia School of Medicine, Charlottesville, VA, United States.

Phillip I Tarr (PI)

Department of Pediatrics, Washington University School of Medicine, St. Louis, MO, United States.

Peter B Sullivan (PB)

Department of Paediatrics, Children's Hospital, University of Oxford, Oxford, United Kingdom.

Christopher A Moskaluk (CA)

Department of Pathology, University of Virginia School of Medicine, Charlottesville, VA, United States. Electronic address: cam5p@virginia.edu.

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Classifications MeSH