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. 2013 Aug;183(2):583-91.
doi: 10.1016/j.jss.2013.01.054. Epub 2013 Feb 24.

Parenteral nutrition increases susceptibility of ileum to invasion by E coli

Joseph F Pierre  1 , Aaron F Heneghan, Jennifer M Meudt, Michael P Shea, Christian G Krueger, Jess D Reed, Kenneth A Kudsk, Dhanansayan Shanmuganayagam
Affiliations

Parenteral nutrition increases susceptibility of ileum to invasion by E coli

Joseph F Pierre et al. J Surg Res. 2013 Aug.

Abstract

Background: Parenteral nutrition (PN), with the lack of enteral feeding, compromises mucosal immune function and increases the risk of infections. We developed an ex vivo intestinal segment culture (EVISC) model to study the ex vivo effects of PN on susceptibility of the ileum to invasion by extra-intestinal pathogenic Escherichia coli (ExPEC) and on ileal secretion of antimicrobial secretory phospholipase A2 (sPLA2) in response to the pathogen.

Materials and methods: Study 1: Using mouse (n = 7) ileal tissue, we examined the effects of ileal region (proximal versus distal) and varying ExPEC inoculum concentrations on ex vivo susceptibility to ExPEC invasion and sPLA2 secretion. Study 2: Ten mice were randomized to oral chow or intravenous PN feeding for 5 d (n = 5/group). Using the EVISC model, we compared the susceptibility of ileal tissue to invasion by ExPEC and sPLA2 secretion in response to the pathogen.

Results: Study 1: The proximal ileum was more susceptible to invasion (P < 0.0001) and secreted lower amounts of sPLA2 (P = 0.0002) than the distal ileum. Study 2: Ileal tissue from PN-fed animals was more susceptible (approximately 4-fold, P = 0.018) to invasion than those from chow-fed animals. Ileal tissue from PN-fed animals secreted less sPLA2 (P < 0.02) than those from chow-fed animals.

Conclusions: The data illustrate EVISC as a reproducible model for studying host-pathogen interactions and the effects of diet on susceptibility to infections. Specifically, the findings support our hypothesis that PN with the lack of enteral feeding decreases mucosal responsiveness to pathogen exposure and provides a plausible mechanism by which PN is associated with increased risk of infectious complication.

Keywords: Enteroinvasion; Escherichia coli; Extra-intestinal pathogens; Ex vivo; Paneth cells; Parenteral nutrition; Polarized in vitro organ culture; Secretory phospholipase A2.

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Figures

Figure 1
Figure 1. A graphical representation of the EVISC model setup
Figure shows the assembly of the spacer and the intestinal segment into each cell culture insert that is then placed into a well of a 12-well cell culture plate.
Figure 2
Figure 2. Effects of ileal region (proximal vs. distal ileal segments) and ExPEC inoculum concentration on susceptibility of ileal tissue to invasion by ExPEC
Figures show (A) total invasion and (B) invasivity (Invaded CFU/Inoculum CFU). Means without a common letter differ, P < 0.05.
Figure 3
Figure 3. Representative scanning electron photomicrographs of the invasion of ileal epithelial cells by ExPEC
(A) Shows the adhesion of ExPEC to apical surface of cells via surface virulence factor (fimbriae; example indicated by white arrow), (B) Shows ExPEC invasion of the epithelium cells by initiating uptake, a mechanism commonly utilized by microbial pathogens to gain entry into non-phagocytic host cells (37, 38). The observed photomicrographs are identical to what we have previously observed in our studies exploring the invasion of enterocytes (Caco-2 cells) in culture by ExPEC (data not shown).
Figure 4
Figure 4. Effects of ileal region (proximal vs. distal ileal segments) and ExPEC inoculum concentration on sPLA2 secretion by mucosal tissue in response to pathogen exposure
sPLA2 activity in the culture media is taken to be a measure of sPLA2 secretion. Means without a common letter differ, P < 0.05.
Figure 5
Figure 5. Effect of chow- and PN- feeding on susceptibility of ileal tissue to invasion by ExPEC
Figures show (A) total invasion and (B) invasivity (Invaded CFU/Inoculum CFU). * Denotes statistical difference (P=0.0018) between mucosal tissues from PN- and chow-fed mice.
Figure 6
Figure 6. Effect of chow- and PN- feeding on sPLA2 secretion by mucosal tissue in response to pathogen exposure
sPLA2 activity in the culture media is taken to be a measure of sPLA2 secretion. * Denotes statistical difference (P=0.01) between secretions by mucosal tissues from PN- and chow-fed mice.
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