A Digestive Cartridge Reduces Parenteral Nutrition Dependence and Increases Bowel Growth in a Piglet Short Bowel Model.
Journal
Annals of surgery
ISSN: 1528-1140
Titre abrégé: Ann Surg
Pays: United States
ID NLM: 0372354
Informations de publication
Date de publication:
01 10 2023
01 10 2023
Historique:
medline:
11
9
2023
pubmed:
17
3
2023
entrez:
16
3
2023
Statut:
ppublish
Résumé
To determine whether the use of an immobilized lipase cartridge (ILC) to hydrolyze fats in enteral nutrition (EN) reduces parenteral nutrition (PN) dependence in a porcine model of short bowel syndrome with intestinal failure (SBS-IF). SBS-IF occurs after intestinal loss resulting in malabsorption and PN dependence. Limited therapeutic options are available for achieving enteral autonomy. Eleven Yorkshire piglets underwent 75% jejunoileal resection and were randomized into control (n=6) and treatment (n = 5) groups. PN was initiated postoperatively and reduced as EN advanced if predefined clinical criteria were fulfilled. Animals were studied for 14 days and changes in PN/EN calories were assessed. Intestinal adaptation, absorption, and nutrition were evaluated at the end of the study (day 15). Comparisons between groups were performed using analysis of covariance adjusted for baseline. ILC animals demonstrated a 19% greater reduction in PN calories ( P < 0.0001) and higher mean EN advancement (66% vs 47% of total calories, P < 0.0001) during the 14-day experiment. Treatment animals had increased intestinal length (19.5 vs 0.7%, P =0.03) and 1.9-fold higher crypt cell proliferation ( P =0.02) compared with controls. By day 15, ILC treatment resulted in higher plasma concentrations of glucagon-like peptide-2 ( P = 0.02), eicosapentaenoic acid ( P < 0.0001), docosahexaenoic acid ( P = 0.004), vitamin A ( P = 0.02), low-density lipoprotein ( P = 0.02), and high-density lipoprotein ( P = 0.04). There were no differences in liver enzymes or total bilirubin between the two groups. ILC use in conjunction with enteral feeding reduced PN dependence, improved nutrient absorption, and increased bowel growth in a porcine SBS-IF model. These results support a potential role for the ILC in clinical SBS-IF.
Sections du résumé
OBJECTIVE
To determine whether the use of an immobilized lipase cartridge (ILC) to hydrolyze fats in enteral nutrition (EN) reduces parenteral nutrition (PN) dependence in a porcine model of short bowel syndrome with intestinal failure (SBS-IF).
BACKGROUND
SBS-IF occurs after intestinal loss resulting in malabsorption and PN dependence. Limited therapeutic options are available for achieving enteral autonomy.
METHODS
Eleven Yorkshire piglets underwent 75% jejunoileal resection and were randomized into control (n=6) and treatment (n = 5) groups. PN was initiated postoperatively and reduced as EN advanced if predefined clinical criteria were fulfilled. Animals were studied for 14 days and changes in PN/EN calories were assessed. Intestinal adaptation, absorption, and nutrition were evaluated at the end of the study (day 15). Comparisons between groups were performed using analysis of covariance adjusted for baseline.
RESULTS
ILC animals demonstrated a 19% greater reduction in PN calories ( P < 0.0001) and higher mean EN advancement (66% vs 47% of total calories, P < 0.0001) during the 14-day experiment. Treatment animals had increased intestinal length (19.5 vs 0.7%, P =0.03) and 1.9-fold higher crypt cell proliferation ( P =0.02) compared with controls. By day 15, ILC treatment resulted in higher plasma concentrations of glucagon-like peptide-2 ( P = 0.02), eicosapentaenoic acid ( P < 0.0001), docosahexaenoic acid ( P = 0.004), vitamin A ( P = 0.02), low-density lipoprotein ( P = 0.02), and high-density lipoprotein ( P = 0.04). There were no differences in liver enzymes or total bilirubin between the two groups.
CONCLUSIONS
ILC use in conjunction with enteral feeding reduced PN dependence, improved nutrient absorption, and increased bowel growth in a porcine SBS-IF model. These results support a potential role for the ILC in clinical SBS-IF.
Identifiants
pubmed: 36924229
doi: 10.1097/SLA.0000000000005839
pii: 00000658-990000000-00404
pmc: PMC10481911
mid: NIHMS1879791
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
e876-e884Subventions
Organisme : NIDDK NIH HHS
ID : T32 DK007754
Pays : United States
Organisme : NHLBI NIH HHS
ID : T32 HL007734
Pays : United States
Informations de copyright
Copyright © 2023 The Author(s). Published by Wolters Kluwer Health, Inc.
Déclaration de conflit d'intérêts
M.P. and K.M.G. receive research support and advisory compensation from Alcresta Therapeutics, Inc. (Newton, MA). G.L. and E.F. were employees of Alcresta Therapeutics, Inc. at the time of the study. The remaining authors report no conflicts of interest.
Références
Wales PW, de Silva N, Kim J, et al. Neonatal short bowel syndrome: population-based estimates of incidence and mortality rates. J Pediatr Surg. 2004;39:690–695.
Squires RH, Duggan C, Teitelbaum DH, et al. Natural history of pediatric intestinal failure: initial report from the Pediatric Intestinal Failure Consortium. J Pediatr. 2012;161:723–8 e2.
O’Keefe SJ, Buchman AL, Fishbein TM, et al. Short bowel syndrome and intestinal failure: consensus definitions and overview. Clin Gastroenterol Hepatol. 2006;4:6–10.
Buchman AL. Etiology and initial management of short bowel syndrome. Gastroenterology. 2006;130(2 suppl 1):S5–S15.
Pironi L, Arends J, Baxter J, et al. ESPEN endorsed recommendations. Definition and classification of intestinal failure in adults. Clin Nutr. 2015;34:171–180.
Seddik TB, Tian L, Nespor C, et al. Risk factors of ambulatory central line-associated bloodstream infection in pediatric short bowel syndrome. JPEN J Parenter Enteral Nutr. 2020;44:500–506.
Duro D, Mitchell PD, Kalish LA, et al. Risk factors for parenteral nutrition-associated liver disease following surgical therapy for necrotizing enterocolitis: A Glaser Pediatric Research Network Study [corrected]. J Pediatr Gastroenterol Nutr. 2011;52:595–600.
Seetharam P, Rodrigues G. Short bowel syndrome: a review of management options. Saudi J Gastroenterol. 2011;17:229–235.
Martin CR, Stoll B, Cluette-Brown J, et al. Use of a novel docosahexaenoic acid formulation vs control in a neonatal porcine model of short bowel syndrome leads to greater intestinal absorption and higher systemic levels of DHA. Nutr Res. 2017;39:51–60.
Freedman S, Orenstein D, Black P, et al. Increased fat absorption from enteral formula through an in-line digestive cartridge in patients with cystic fibrosis. J Pediatr Gastroenterol Nutr. 2017;65:97–101.
Alcresta Therapeutics Inc. Compatible Formulas and Pumps 2021. Accessed January 1, 2023. https://www.relizorb.com/docs/pdfs/Compatible-Formulas-and-Pumps.pdf
Esterbauer H. Cytotoxicity and genotoxicity of lipid-oxidation products. Am J Clin Nutr. 1993;57(suppl 5):779S–785S; discussion 785S–786S.
Halliwell B, Chirico S. Lipid peroxidation: its mechanism, measurement, and significance. Am J Clin Nutr. 1993;57(suppl 5):715S–724S; discussion 724S–725S.
Alexander DD, Bylsma LC, Elkayam L, et al. Nutritional and health benefits of semi-elemental diets: a comprehensive summary of the literature. World J Gastrointest Pharmacol Ther. 2016;7:306–319.
Suri M, Turner JM, Sigalet DL, et al. Exogenous glucagon-like peptide-2 improves outcomes of intestinal adaptation in a distal-intestinal resection neonatal piglet model of short bowel syndrome. Pediatr Res. 2014;76:370–377.
Naberhuis JK, Deutsch AS, Tappenden KA. Teduglutide-stimulated intestinal adaptation is complemented and synergistically enhanced by partial enteral nutrition in a neonatal piglet model of short bowel syndrome. JPEN J Parenter Enteral Nutr. 2017;41:853–865.
Tsikis ST, Fligor SC, Secor JD, et al. An in-line digestive cartridge increases enteral fat and vitamin absorption in a porcine model of short bowel syndrome. Clin Nutr. 2022;41:1093–1101.
Committee for the Update of the Guide for the Care and Use of Laboratory Animals IfLAR, Division on Earth and Life Studies, and National Research Council. Guide for the care and use of laboratory animals, 8th edn. National Academies Press; 2010.
Tsikis ST, Fligor SC, Secor JD, et al. Outcomes and perioperative nutritional management in a porcine model of short bowel syndrome. J Surg Res. 2022;274:59–67.
Hua Z, Turner JM, Mager DR, et al. Effects of polymeric formula vs elemental formula in neonatal piglets with short bowel syndrome. JPEN J Parenter Enteral Nutr. 2014;38:498–506.
Wykes LJ, Ball RO, Pencharz PB. Development and validation of a total parenteral nutrition model in the neonatal piglet. J Nutr. 1993;123:1248–1259.
Villalona G, Price A, Blomenkamp K, et al. No gut no gain! enteral bile acid treatment preserves gut growth but not parenteral nutrition-associated liver injury in a novel extensive short bowel animal model. JPEN J Parenter Enteral Nutr. 2018;42:1238–1251.
Hua Z, Turner JM, Sigalet DL, et al. Role of glucagon-like peptide-2 deficiency in neonatal short-bowel syndrome using neonatal piglets. Pediatr Res. 2013;73:742–749.
Koh H, Lee MJ, Kim MJ, et al. Simple diagnostic approach to childhood fecal retention using the Leech score and Bristol stool form scale in medical practice. J Gastroenterol Hepatol. 2010;25:334–338.
Dao DT, Anez-Bustillos L, Finkelstein AM, et al. Trends of INR and fecal excretion of vitamin K during cholestasis reversal: implications in the treatment of neonates with intestinal failure-associated liver disease. JPEN J Parenter Enteral Nutr. 2020;44:951–958.
Harris WS, Varvel SA, Pottala JV, et al. Comparative effects of an acute dose of fish oil on omega-3 fatty acid levels in red blood cells versus plasma: implications for clinical utility. J Clin Lipidol. 2013;7:433–440.
Tsikis ST, Fligor SC, Hirsch TI, et al. Lipopolysaccharide-induced murine lung injury results in long-term pulmonary changes and downregulation of angiogenic pathways. Sci Rep. 2022;12:10245.
Chen XJ, Ren SM, Dong JZ, et al. Ginkgo biloba extract-761 protects myocardium by regulating Akt/Nrf2 signal pathway. Drug Des Devel Ther. 2019;13:647–655.
Turner JM, Wales PW, Nation PN, et al. Novel neonatal piglet models of surgical short bowel syndrome with intestinal failure. J Pediatr Gastroenterol Nutr. 2011;52:9–16.
Lim DW, Levesque CL, Vine DF, et al. Synergy of glucagon-like peptide-2 and epidermal growth factor coadministration on intestinal adaptation in neonatal piglets with short bowel syndrome. Am J Physiol Gastrointest Liver Physiol. 2017;312:G390–G404.
Tsikis ST, Hirsch TI, Fligor SC, et al. Direct thrombin inhibitors as alternatives to heparin to preserve lung growth and function in a murine model of compensatory lung growth. Sci Rep. 2022;12:21117.
Tak E, Kim M, Cho Y, et al. Expression of neurofibromin 1 in colorectal cancer and cetuximab resistance. Oncol Rep. 2022;47:15.
Onufer EJ, Han YH, Czepielewski RS, et al. Effects of high-fat diet on liver injury after small bowel resection. J Pediatr Surg. 2020;55:1099–1106.
Goulet O, Abi Nader E, Pigneur B, et al. Short bowel syndrome as the leading cause of intestinal failure in early life: some insights into the management. Pediatr Gastroenterol Hepatol Nutr. 2019;22:303–329.
Stevens J, Wyatt C, Brown P, et al. Absorption and safety with sustained use of RELiZORB evaluation (ASSURE) study in patients with cystic fibrosis receiving enteral feeding. J Pediatr Gastroenterol Nutr. 2018;67:527–532.
Yang CF, Duro D, Zurakowski D, et al. High prevalence of multiple micronutrient deficiencies in children with intestinal failure: a longitudinal study. J Pediatr. 2011;159:39–44. e1.
Neelis E, Rijnen N, Sluimer J, et al. Bone health of children with intestinal failure measured by dual energy X-ray absorptiometry and digital X-ray radiogrammetry. Clin Nutr. 2018;37:687–694.
Lam K, Schwartz L, Batisti J, et al. Single-center experience with the use of teduglutide in adult patients with short bowel syndrome. JPEN J Parenter Enteral Nutr. 2018;42:225–230.
Zong W, Troutt R, Merves J. Blenderized enteral nutrition in pediatric short gut syndrome: Tolerance and clinical outcomes. Nutr Clin Pract. 2022;37:913–920.
Samela K, Mokha J, Emerick K, et al. Transition to a tube feeding formula with real food ingredients in pediatric patients with intestinal failure. Nutr Clin Pract. 2017;32:277–281.
Goulet O, Olieman J, Ksiazyk J, et al. Neonatal short bowel syndrome as a model of intestinal failure: physiological background for enteral feeding. Clin Nutr. 2013;32:162–171.
Karmaker A, Costanzo CM, Schwartz MZ. Is OM-3 synergistic with GLP-2 in intestinal failure? J Surg Res. 2017;207:7–12.
Yang Q, Lan T, Chen Y, et al. Dietary fish oil increases fat absorption and fecal bile acid content without altering bile acid synthesis in 20-d-old weanling rats following massive ileocecal resection. Pediatr Res. 2012;72:38–42.
Sathe MN, Patel D, Stone A, et al. Evaluation of the effectiveness of in-line immobilized lipase cartridge in enterally fed patients with cystic fibrosis. J Pediatr Gastroenterol Nutr. 2021;72:18–23.
Food and Drug Administration (FDA). De novo classification request for RELIZORB(TM). Accessed January 1, 2023. https://www.accessdata.fda.gov/cdrh_docs/reviews/DEN150001.pdf
Thymann T, Stoll B, Mecklenburg L, et al. Acute effects of the glucagon-like peptide 2 analogue, teduglutide, on intestinal adaptation in short bowel syndrome. J Pediatr Gastroenterol Nutr. 2014;58:694–702.