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Cholecystokinin/Cholecystokinin-1 receptor-mediated peripheral activation of the afferent vagus by enteral nutrients attenuates inflammation in rats.
Ann Surg. 2010 Aug; 252(2):376-82.AnnS

Abstract

OBJECTIVE

The current study investigates activation of the nutritional anti-inflammatory pathway by lipid-rich nutrition.

BACKGROUND

Enteral nutrition activates humoral and neural pathways to regulate food intake and sustain energy balance. Recently, we demonstrated that enteral nutrition and in particular lipid-rich nutrition modulates inflammation and prevents organ damage.

METHODS

Male rats were fasted or fed lipid-rich nutrition before hemorrhagic shock. Disruption of afferent vagal fibers with capsaicin (deafferentation) was used to investigate involvement of afferent fibers. Peripheral activation of afferent vagal fibers via cholecystokinin (CCK)-mediated activation of CCK-1 receptors was investigated using administration of the selectively peripheral acting CCK-1 receptor antagonist, A70104 and PEGylated-CCK9. Tissue and blood were collected 90 minutes after shock to assess systemic inflammation and intestinal integrity.

RESULTS

Deafferentation reversed the inhibitory effect of lipid-rich nutrition on systemic levels of tumor necrosis factor-alpha and interleukin-6, and on intestinal leakage of horseradish peroxidase and bacterial translocation. Furthermore, the protective effects of lipid-rich nutrition were negated by A70104, indicating that lipid-rich nutrition triggers peripheral CCK-1 receptors on vagal afferents to modulate inflammation. These findings were substantiated by the fact that pretreatment of fasted rats with PEGylated-CCK9, which acts on peripheral CCK-1 receptors, attenuated systemic inflammation, and loss of intestinal integrity.

CONCLUSION

These data demonstrate that enteral lipid-rich nutrition modulates inflammation and preserves intestinal integrity via CCK release which activates CCK-1 receptors located on afferent vagal fibers. Taken together, the current study reveals a novel gut-brain-immune axis and provides new insight into the applicability of enteral nutrition to treat inflammatory conditions.

Authors+Show Affiliations

Department of Surgery, NUTRIM School for Nutrition, Toxicology and Metabolism, Maastricht University Medical Center, Maastricht, The Netherlands.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't

Language

eng

PubMed ID

20585240

Citation

Lubbers, Tim, et al. "Cholecystokinin/Cholecystokinin-1 Receptor-mediated Peripheral Activation of the Afferent Vagus By Enteral Nutrients Attenuates Inflammation in Rats." Annals of Surgery, vol. 252, no. 2, 2010, pp. 376-82.
Lubbers T, de Haan JJ, Luyer MD, et al. Cholecystokinin/Cholecystokinin-1 receptor-mediated peripheral activation of the afferent vagus by enteral nutrients attenuates inflammation in rats. Ann Surg. 2010;252(2):376-82.
Lubbers, T., de Haan, J. J., Luyer, M. D., Verbaeys, I., Hadfoune, M., Dejong, C. H., Buurman, W. A., & Greve, J. W. (2010). Cholecystokinin/Cholecystokinin-1 receptor-mediated peripheral activation of the afferent vagus by enteral nutrients attenuates inflammation in rats. Annals of Surgery, 252(2), 376-82. https://doi.org/10.1097/SLA.0b013e3181dae411
Lubbers T, et al. Cholecystokinin/Cholecystokinin-1 Receptor-mediated Peripheral Activation of the Afferent Vagus By Enteral Nutrients Attenuates Inflammation in Rats. Ann Surg. 2010;252(2):376-82. PubMed PMID: 20585240.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Cholecystokinin/Cholecystokinin-1 receptor-mediated peripheral activation of the afferent vagus by enteral nutrients attenuates inflammation in rats. AU - Lubbers,Tim, AU - de Haan,Jacco J, AU - Luyer,Misha D P, AU - Verbaeys,Isabelle, AU - Hadfoune,M'hamed, AU - Dejong,Cornelis H C, AU - Buurman,Wim A, AU - Greve,Jan Willem M, PY - 2010/6/30/entrez PY - 2010/6/30/pubmed PY - 2010/9/16/medline SP - 376 EP - 82 JF - Annals of surgery JO - Ann Surg VL - 252 IS - 2 N2 - OBJECTIVE: The current study investigates activation of the nutritional anti-inflammatory pathway by lipid-rich nutrition. BACKGROUND: Enteral nutrition activates humoral and neural pathways to regulate food intake and sustain energy balance. Recently, we demonstrated that enteral nutrition and in particular lipid-rich nutrition modulates inflammation and prevents organ damage. METHODS: Male rats were fasted or fed lipid-rich nutrition before hemorrhagic shock. Disruption of afferent vagal fibers with capsaicin (deafferentation) was used to investigate involvement of afferent fibers. Peripheral activation of afferent vagal fibers via cholecystokinin (CCK)-mediated activation of CCK-1 receptors was investigated using administration of the selectively peripheral acting CCK-1 receptor antagonist, A70104 and PEGylated-CCK9. Tissue and blood were collected 90 minutes after shock to assess systemic inflammation and intestinal integrity. RESULTS: Deafferentation reversed the inhibitory effect of lipid-rich nutrition on systemic levels of tumor necrosis factor-alpha and interleukin-6, and on intestinal leakage of horseradish peroxidase and bacterial translocation. Furthermore, the protective effects of lipid-rich nutrition were negated by A70104, indicating that lipid-rich nutrition triggers peripheral CCK-1 receptors on vagal afferents to modulate inflammation. These findings were substantiated by the fact that pretreatment of fasted rats with PEGylated-CCK9, which acts on peripheral CCK-1 receptors, attenuated systemic inflammation, and loss of intestinal integrity. CONCLUSION: These data demonstrate that enteral lipid-rich nutrition modulates inflammation and preserves intestinal integrity via CCK release which activates CCK-1 receptors located on afferent vagal fibers. Taken together, the current study reveals a novel gut-brain-immune axis and provides new insight into the applicability of enteral nutrition to treat inflammatory conditions. SN - 1528-1140 UR - https://www.unboundmedicine.com/medline/citation/20585240/Cholecystokinin/Cholecystokinin_1_receptor_mediated_peripheral_activation_of_the_afferent_vagus_by_enteral_nutrients_attenuates_inflammation_in_rats_ L2 - https://Insights.ovid.com/pubmed?pmid=20585240 DB - PRIME DP - Unbound Medicine ER -