Continuous parenteral and enteral nutrition induces metabolic dysfunction in neonatal pigs

TY - JOUR

T1 - Continuous parenteral and enteral nutrition induces metabolic dysfunction in neonatal pigs

AU - Stoll, Barbara

AU - Puiman, Patrycja Jolanta

AU - Cui, Liwei

AU - Chang, Xiaoyan

AU - Benight, Nancy Marie

AU - Bauchart-Thevret, Caroline

AU - Hartmann, Bolette

AU - Holst, Jens Juul

AU - Burrin, Douglas Guy

PY - 2012/9

Y1 - 2012/9

N2 - Background: We previously showed that parenteral nutrition (PN) compared with formula feeding results in hepatic insulin resistance and steatosis in neonatal pigs. The current aim was to test whether the route of feeding (intravenous [IV] vs enteral) rather than other feeding modalities (diet, pattern) had contributed to the outcome. Methods: Neonatal pigs were fed enterally or parenterally for 14 days with 1 of 4 feeding modalities as follows: (1) enteral polymeric formula intermittently (FORM), (2) enteral elemental diet (ED) intermittently (IEN), (3) enteral ED continuously (CEN), and (4) parenteral ED continuously (PN). Subgroups of pigs underwent IV glucose tolerance tests (IVGTT) and hyperinsulinemic-euglycemic clamps (CLAMP). Following CLAMP, pigs were euthanized and tissues collected for further analysis. Results: Insulin secretion during IVGTT was significantly higher and glucose infusion rates during CLAMP were lower in CEN and PN than in FORM and IEN. Endogenous glucose production rate was suppressed to zero in all groups during CLAMP. In the fed state, plasma glucose-dependent insulinotropic polypeptide (GIP), glucagon-like peptide (GLP)-1, and GLP- 2 were different between feeding modalities. Insulin receptor phosphorylation in liver and muscle was decreased in IEN, CEN, and PN compared with FORM. Liver weight was highest in PN. Steatosis and myeloperoxidase (MPO) activity tended to be highest in PN and CEN. Enterally fed groups had higher plasma GLP-2 and jejunum weight compared with PN. Conclusions: PN and enteral nutrition (EN) when given continuously as an elemental diet reduces insulin sensitivity and the secretion of key gut incretins. The intermittent vs continuous pattern of EN produced the optimal effect on metabolic function. (JPEN J Parenter Enteral Nutr. 2012;36:538-550).

AB - Background: We previously showed that parenteral nutrition (PN) compared with formula feeding results in hepatic insulin resistance and steatosis in neonatal pigs. The current aim was to test whether the route of feeding (intravenous [IV] vs enteral) rather than other feeding modalities (diet, pattern) had contributed to the outcome. Methods: Neonatal pigs were fed enterally or parenterally for 14 days with 1 of 4 feeding modalities as follows: (1) enteral polymeric formula intermittently (FORM), (2) enteral elemental diet (ED) intermittently (IEN), (3) enteral ED continuously (CEN), and (4) parenteral ED continuously (PN). Subgroups of pigs underwent IV glucose tolerance tests (IVGTT) and hyperinsulinemic-euglycemic clamps (CLAMP). Following CLAMP, pigs were euthanized and tissues collected for further analysis. Results: Insulin secretion during IVGTT was significantly higher and glucose infusion rates during CLAMP were lower in CEN and PN than in FORM and IEN. Endogenous glucose production rate was suppressed to zero in all groups during CLAMP. In the fed state, plasma glucose-dependent insulinotropic polypeptide (GIP), glucagon-like peptide (GLP)-1, and GLP- 2 were different between feeding modalities. Insulin receptor phosphorylation in liver and muscle was decreased in IEN, CEN, and PN compared with FORM. Liver weight was highest in PN. Steatosis and myeloperoxidase (MPO) activity tended to be highest in PN and CEN. Enterally fed groups had higher plasma GLP-2 and jejunum weight compared with PN. Conclusions: PN and enteral nutrition (EN) when given continuously as an elemental diet reduces insulin sensitivity and the secretion of key gut incretins. The intermittent vs continuous pattern of EN produced the optimal effect on metabolic function. (JPEN J Parenter Enteral Nutr. 2012;36:538-550).

KW - Administration, Intravenous

KW - Animals

KW - Animals, Newborn

KW - Blood Glucose

KW - Endpoint Determination

KW - Enteral Nutrition

KW - Fatty Liver

KW - Female

KW - Food, Formulated

KW - Glucagon-Like Peptide 1

KW - Glucagon-Like Peptide 2

KW - Incretins

KW - Inflammation

KW - Insulin

KW - Insulin Resistance

KW - Intestine, Small

KW - Liver

KW - Metabolic Diseases

KW - Nonlinear Dynamics

KW - Organ Size

KW - Parenteral Nutrition

KW - Swine

U2 - 10.1177/0148607112444756

DO - 10.1177/0148607112444756

M3 - Journal article

C2 - 22549765

SN - 0148-6071

VL - 36

SP - 538

EP - 550

JO - Journal of Parenteral and Enteral Nutrition

JF - Journal of Parenteral and Enteral Nutrition

IS - 5

ER -