Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm Pigs

Sepsis, the clinical manifestation of serious infection, may disturb normal brain development, especially in preterm infants with an immature brain. We hypothesized that neonatal sepsis induces systemic metabolic alterations that rapidly affect metabolic signatures in immature brain and cerebrospina...

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Main Authors: Masoumeh Alinaghi, Ping-Ping Jiang, Anders Brunse, Per Torp Sangild, Hanne Christine Bertram
Format: Article
Language:English
Published: MDPI AG 2019-01-01
Series:Metabolites
Subjects:
Online Access:http://www.mdpi.com/2218-1989/9/1/13
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author Masoumeh Alinaghi
Ping-Ping Jiang
Anders Brunse
Per Torp Sangild
Hanne Christine Bertram
author_facet Masoumeh Alinaghi
Ping-Ping Jiang
Anders Brunse
Per Torp Sangild
Hanne Christine Bertram
author_sort Masoumeh Alinaghi
collection DOAJ
description Sepsis, the clinical manifestation of serious infection, may disturb normal brain development, especially in preterm infants with an immature brain. We hypothesized that neonatal sepsis induces systemic metabolic alterations that rapidly affect metabolic signatures in immature brain and cerebrospinal fluid (CSF). Cesarean-delivered preterm pigs systemically received 109 CFU/kg Staphylococcus epidermidis (SE) and were provided total parenteral nutrition (n = 9) or enteral supplementation with bovine colostrum (n = 10) and compared with uninfected pigs receiving parenteral nutrition (n = 7). Plasma, CSF, and brain tissue samples were collected after 24 h and analyzed by 1H NMR-based metabolomics. Both plasma and CSF metabolomes revealed SE-induced changes in metabolite levels that reflected a modified energy metabolism. Hence, increased plasma lactate, alanine, and succinate levels, as well as CSF lactate levels, were observed during SE infection (all p < 0.05, ANOVA analysis). Myo-inositol, a glucose derivative known for beneficial effects on lung maturation in preterm infants, was also increased in plasma and CSF following SE infection. Enteral colostrum supplementation attenuated the lactate accumulation in blood and CSF. Bloodstream infection in preterm newborns was found to induce a rapid metabolic shift in both plasma and CSF, which was modulated by colostrum feeding.
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spelling doaj.art-1667152041384a51a2ff2069263067172022-12-21T19:20:03ZengMDPI AGMetabolites2218-19892019-01-01911310.3390/metabo9010013metabo9010013Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm PigsMasoumeh Alinaghi0Ping-Ping Jiang1Anders Brunse2Per Torp Sangild3Hanne Christine Bertram4Department of Food Science, Aarhus University, Kirstinebjergvej 10, 5792 Aarslev, DenmarkComparative Pediatrics and Nutrition, Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg, DenmarkComparative Pediatrics and Nutrition, Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg, DenmarkComparative Pediatrics and Nutrition, Department of Veterinary and Animal Sciences, Faculty of Health and Medical Sciences, University of Copenhagen, 1870 Frederiksberg, DenmarkDepartment of Food Science, Aarhus University, Kirstinebjergvej 10, 5792 Aarslev, DenmarkSepsis, the clinical manifestation of serious infection, may disturb normal brain development, especially in preterm infants with an immature brain. We hypothesized that neonatal sepsis induces systemic metabolic alterations that rapidly affect metabolic signatures in immature brain and cerebrospinal fluid (CSF). Cesarean-delivered preterm pigs systemically received 109 CFU/kg Staphylococcus epidermidis (SE) and were provided total parenteral nutrition (n = 9) or enteral supplementation with bovine colostrum (n = 10) and compared with uninfected pigs receiving parenteral nutrition (n = 7). Plasma, CSF, and brain tissue samples were collected after 24 h and analyzed by 1H NMR-based metabolomics. Both plasma and CSF metabolomes revealed SE-induced changes in metabolite levels that reflected a modified energy metabolism. Hence, increased plasma lactate, alanine, and succinate levels, as well as CSF lactate levels, were observed during SE infection (all p < 0.05, ANOVA analysis). Myo-inositol, a glucose derivative known for beneficial effects on lung maturation in preterm infants, was also increased in plasma and CSF following SE infection. Enteral colostrum supplementation attenuated the lactate accumulation in blood and CSF. Bloodstream infection in preterm newborns was found to induce a rapid metabolic shift in both plasma and CSF, which was modulated by colostrum feeding.http://www.mdpi.com/2218-1989/9/1/13NMR metabolomicsneonatal sepsispreterm infantsbloodstream infectioncerebrospinal fluidStaphylococcus epidermidisbrain metabolitescerebral metabolismenteral feedingbioactive dairy components
spellingShingle Masoumeh Alinaghi
Ping-Ping Jiang
Anders Brunse
Per Torp Sangild
Hanne Christine Bertram
Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm Pigs
Metabolites
NMR metabolomics
neonatal sepsis
preterm infants
bloodstream infection
cerebrospinal fluid
Staphylococcus epidermidis
brain metabolites
cerebral metabolism
enteral feeding
bioactive dairy components
title Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm Pigs
title_full Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm Pigs
title_fullStr Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm Pigs
title_full_unstemmed Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm Pigs
title_short Rapid Cerebral Metabolic Shift during Neonatal Sepsis Is Attenuated by Enteral Colostrum Supplementation in Preterm Pigs
title_sort rapid cerebral metabolic shift during neonatal sepsis is attenuated by enteral colostrum supplementation in preterm pigs
topic NMR metabolomics
neonatal sepsis
preterm infants
bloodstream infection
cerebrospinal fluid
Staphylococcus epidermidis
brain metabolites
cerebral metabolism
enteral feeding
bioactive dairy components
url http://www.mdpi.com/2218-1989/9/1/13
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