Lymphoid Aggregates Remodel Lymphatic Collecting Vessels that Serve Mesenteric Lymph Nodes in Crohn Disease

Am J Pathol. 2016 Dec;186(12):3066-3073. doi: 10.1016/j.ajpath.2016.07.026. Epub 2016 Oct 13.

Abstract

Early pathological descriptions of Crohn disease (CD) argued for a potential defect in lymph transport; however, this concept has not been thoroughly investigated. In mice, poor healing in response to infection-induced tissue damage can cause hyperpermeable lymphatic collecting vessels in mesenteric adipose tissue that impair antigen and immune cell access to mesenteric lymph nodes (LNs), which normally sustain appropriate immunity. To investigate whether analogous changes might occur in human intestinal disease, we established a three-dimensional imaging approach to characterize the lymphatic vasculature in mesenteric tissue from controls or patients with CD. In CD specimens, B-cell-rich aggregates resembling tertiary lymphoid organs (TLOs) impinged on lymphatic collecting vessels that enter and exit LNs. In areas of creeping fat, which characterizes inflammation-affected areas of the bowel in CD, we observed B cells and apparent innate lymphoid cells that had invaded the lymphatic vessel wall, suggesting these cells may be mediators of lymphatic remodeling. Although TLOs have been described in many chronic inflammatory states, their anatomical relationship to preestablished LNs has never been revealed. Our data indicate that, at least in the CD-affected mesentery, TLOs are positioned along collecting lymphatic vessels in a manner expected to affect delivery of lymph to LNs.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, N.I.H., Extramural

MeSH terms

  • Adult
  • Animals
  • B-Lymphocytes / pathology
  • Crohn Disease / diagnostic imaging*
  • Crohn Disease / pathology
  • Crohn Disease / surgery
  • Female
  • Humans
  • Ileum / diagnostic imaging
  • Ileum / pathology
  • Imaging, Three-Dimensional
  • Inflammation
  • Intestines / pathology
  • Intestines / surgery
  • Lymph Nodes / diagnostic imaging*
  • Lymph Nodes / pathology
  • Lymph Nodes / surgery
  • Lymphatic Vessels / diagnostic imaging*
  • Lymphatic Vessels / pathology
  • Lymphatic Vessels / surgery
  • Male
  • Mesentery / diagnostic imaging
  • Mesentery / pathology
  • Mesentery / surgery
  • Mice
  • Middle Aged
  • Tertiary Lymphoid Structures / diagnostic imaging
  • Tertiary Lymphoid Structures / pathology