Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.

Previous abdominal surgery (PAS) increases risk of small bowel obstruction (SBO) due to adhesions, and appendectomy (appy) is an independent risk factor for abdominal adhesion-related complications. Peritoneal inflammation, e.g., acute appendicitis (AA), causes formation of reactive ascitic fluid (r...

Full description

Saved in:
Bibliographic Details
Main Authors: Melissa A Hausburg, Kaysie L Banton, Christopher D Cassidy, Robert M Madayag, Carlos H Palacio, Jason S Williams, Raphael Bar-Or, Rebecca J Ryznar, David Bar-Or
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0317056
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832582980802969600
author Melissa A Hausburg
Kaysie L Banton
Christopher D Cassidy
Robert M Madayag
Carlos H Palacio
Jason S Williams
Raphael Bar-Or
Rebecca J Ryznar
David Bar-Or
author_facet Melissa A Hausburg
Kaysie L Banton
Christopher D Cassidy
Robert M Madayag
Carlos H Palacio
Jason S Williams
Raphael Bar-Or
Rebecca J Ryznar
David Bar-Or
author_sort Melissa A Hausburg
collection DOAJ
description Previous abdominal surgery (PAS) increases risk of small bowel obstruction (SBO) due to adhesions, and appendectomy (appy) is an independent risk factor for abdominal adhesion-related complications. Peritoneal inflammation, e.g., acute appendicitis (AA), causes formation of reactive ascitic fluid (rA) that activates peritoneum surface mesothelial cells (MCs) to form adhesions. Pathologic adhesions may arise if restoration of MC-regulated fibrinolysis and secretion of glycocalyx (GCX) are disrupted. Proteins affecting these processes may originate from peritoneal rA. This is a prospective observational IRB-approved study at three Level 1 trauma centers where rA is collected prior to surgical intervention for non-perforated AA or adhesiolysis for SBO. Samples from 48 appy and 15 SBO patients were used to treat human MCs and subjected to quantification of 85 inflammatory mediators. Results were compared between patients with surgically naïve abdomens (naïve) and patients with >1 PAS. Select rA caused MCs to form clusters of fibroblastic cells, extracellular matrix fibers (FIB), and secretion of GCX. PAS and naïve patient rA fluids were clustered into "fiber-GCX" (FIB-GCX) groups: highFIB-highGCX, highFIB-lowGCX, noFIB-highGCX, noFIB-lowGCX, and noFIB-noGCX. Between groups, 26 analytes were differentially abundant including innate immune response, wound healing, and mucosal defense proteins. Factors that contributed to the differences between groups were rA-induced highFIB and history of PAS. Overall, PAS patient rA showed a muted immune response compared to rA from naïve patients. Our data suggest that abdominal surgery may negatively impact future immune responses in the abdomen. Further, quantifying immunomodulators in peritoneal rA may lead to the development a personalized approach to post-surgical adhesion treatment and prevention.
format Article
id doaj-art-d96483f0ab144eeb98340b480ff61b91
institution Kabale University
issn 1932-6203
language English
publishDate 2025-01-01
publisher Public Library of Science (PLoS)
record_format Article
series PLoS ONE
spelling doaj-art-d96483f0ab144eeb98340b480ff61b912025-01-29T05:30:45ZengPublic Library of Science (PLoS)PLoS ONE1932-62032025-01-01201e031705610.1371/journal.pone.0317056Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.Melissa A HausburgKaysie L BantonChristopher D CassidyRobert M MadayagCarlos H PalacioJason S WilliamsRaphael Bar-OrRebecca J RyznarDavid Bar-OrPrevious abdominal surgery (PAS) increases risk of small bowel obstruction (SBO) due to adhesions, and appendectomy (appy) is an independent risk factor for abdominal adhesion-related complications. Peritoneal inflammation, e.g., acute appendicitis (AA), causes formation of reactive ascitic fluid (rA) that activates peritoneum surface mesothelial cells (MCs) to form adhesions. Pathologic adhesions may arise if restoration of MC-regulated fibrinolysis and secretion of glycocalyx (GCX) are disrupted. Proteins affecting these processes may originate from peritoneal rA. This is a prospective observational IRB-approved study at three Level 1 trauma centers where rA is collected prior to surgical intervention for non-perforated AA or adhesiolysis for SBO. Samples from 48 appy and 15 SBO patients were used to treat human MCs and subjected to quantification of 85 inflammatory mediators. Results were compared between patients with surgically naïve abdomens (naïve) and patients with >1 PAS. Select rA caused MCs to form clusters of fibroblastic cells, extracellular matrix fibers (FIB), and secretion of GCX. PAS and naïve patient rA fluids were clustered into "fiber-GCX" (FIB-GCX) groups: highFIB-highGCX, highFIB-lowGCX, noFIB-highGCX, noFIB-lowGCX, and noFIB-noGCX. Between groups, 26 analytes were differentially abundant including innate immune response, wound healing, and mucosal defense proteins. Factors that contributed to the differences between groups were rA-induced highFIB and history of PAS. Overall, PAS patient rA showed a muted immune response compared to rA from naïve patients. Our data suggest that abdominal surgery may negatively impact future immune responses in the abdomen. Further, quantifying immunomodulators in peritoneal rA may lead to the development a personalized approach to post-surgical adhesion treatment and prevention.https://doi.org/10.1371/journal.pone.0317056
spellingShingle Melissa A Hausburg
Kaysie L Banton
Christopher D Cassidy
Robert M Madayag
Carlos H Palacio
Jason S Williams
Raphael Bar-Or
Rebecca J Ryznar
David Bar-Or
Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.
PLoS ONE
title Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.
title_full Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.
title_fullStr Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.
title_full_unstemmed Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.
title_short Mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites: Insights into immunoregulation of abdominal adhesion.
title_sort mesothelial cell responses to acute appendicitis or small bowel obstruction reactive ascites insights into immunoregulation of abdominal adhesion
url https://doi.org/10.1371/journal.pone.0317056
work_keys_str_mv AT melissaahausburg mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT kaysielbanton mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT christopherdcassidy mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT robertmmadayag mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT carloshpalacio mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT jasonswilliams mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT raphaelbaror mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT rebeccajryznar mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion
AT davidbaror mesothelialcellresponsestoacuteappendicitisorsmallbowelobstructionreactiveascitesinsightsintoimmunoregulationofabdominaladhesion