Parenteral nutrition increases susceptibility of ileum to invasion by e coli

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

Research output: Contribution to journalArticle

12 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)583-591
Number of pages9
JournalJournal of Surgical Research
Volume183
Issue number2
DOIs
StatePublished - Aug 1 2013

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Parenteral Nutrition
Ileum
Secretory Phospholipase A2
Escherichia coli
Enteral Nutrition
Host-Pathogen Interactions
Infection
Diet

All Science Journal Classification (ASJC) codes

  • Surgery

Cite this

Pierre, J., Heneghan, A. F., Meudt, J. M., Shea, M. P., Krueger, C. G., Reed, J. D., ... Shanmuganayagam, D. (2013). Parenteral nutrition increases susceptibility of ileum to invasion by e coli. Journal of Surgical Research, 183(2), 583-591. https://doi.org/10.1016/j.jss.2013.01.054

Parenteral nutrition increases susceptibility of ileum to invasion by e coli. / Pierre, Joseph; Heneghan, Aaron F.; Meudt, Jennifer M.; Shea, Michael P.; Krueger, Christian G.; Reed, Jess D.; Kudsk, Kenneth A.; Shanmuganayagam, Dhanansayan.

In: Journal of Surgical Research, Vol. 183, No. 2, 01.08.2013, p. 583-591.

Research output: Contribution to journalArticle

Pierre, J, Heneghan, AF, Meudt, JM, Shea, MP, Krueger, CG, Reed, JD, Kudsk, KA & Shanmuganayagam, D 2013, 'Parenteral nutrition increases susceptibility of ileum to invasion by e coli', Journal of Surgical Research, vol. 183, no. 2, pp. 583-591. https://doi.org/10.1016/j.jss.2013.01.054
Pierre, Joseph ; Heneghan, Aaron F. ; Meudt, Jennifer M. ; Shea, Michael P. ; Krueger, Christian G. ; Reed, Jess D. ; Kudsk, Kenneth A. ; Shanmuganayagam, Dhanansayan. / Parenteral nutrition increases susceptibility of ileum to invasion by e coli. In: Journal of Surgical Research. 2013 ; Vol. 183, No. 2. pp. 583-591.
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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.",
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AU - Pierre, Joseph

AU - Heneghan, Aaron F.

AU - Meudt, Jennifer M.

AU - Shea, Michael P.

AU - Krueger, Christian G.

AU - Reed, Jess D.

AU - Kudsk, Kenneth A.

AU - Shanmuganayagam, Dhanansayan

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N2 - 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.

AB - 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.

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