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Impact of dietary induced precocious gut maturation on cecal microbiota and its relation to the blood-brain barrier during the postnatal period in rats

Marungruang, Nittaya LU ; Arévalo Sureda, Ester LU ; Lefrançoise , Anais; Weström, Björn LU ; Nyman, Margareta LU ; Prykhodko, Olena LU and Hållenius, Frida LU (2018) In Neurogastroenterology and Motility 30(6).
Abstract
Background
Precocious maturation of the gastrointestinal barrier (GIB) in newborn mammals can be induced by dietary provocation, but how this affects the gut microbiota and the gut‐brain axis remains unknown. The objective of this study was to investigate effects of induced GIB maturation on gut microbiota composition and blood‐brain barrier (BBB) permeability.
Methods
Suckling rats were studied at 72 h after gavage with phytohemagglutinin (PHA) or microbial protease (PT) to induce maturation of GIB. For comparison, untreated suckling and weaned rats were included (n = 10). Human serum albumin (HSA) was administered orally and analyzed in blood to assess permeability of the GIB, while intraperitoneally injected bovine serum... (More)
Background
Precocious maturation of the gastrointestinal barrier (GIB) in newborn mammals can be induced by dietary provocation, but how this affects the gut microbiota and the gut‐brain axis remains unknown. The objective of this study was to investigate effects of induced GIB maturation on gut microbiota composition and blood‐brain barrier (BBB) permeability.
Methods
Suckling rats were studied at 72 h after gavage with phytohemagglutinin (PHA) or microbial protease (PT) to induce maturation of GIB. For comparison, untreated suckling and weaned rats were included (n = 10). Human serum albumin (HSA) was administered orally and analyzed in blood to assess permeability of the GIB, while intraperitoneally injected bovine serum albumin (BSA) was measured in the brain tissue for BBB permeability. The cecal microbial composition, plasma lipopolysaccharide‐binding protein (LBP) levels and short‐chain fatty acids in serum and brain were analyzed.
Key Results
Cessation of HSA passage to blood after PHA or PT treatment was similar to that seen in weaned rats. Interestingly, concomitant increases in cecal Bacteroidetes and plasma LBP levels were observed after both PHA and PT treatments. The BBB passage of BSA was surprisingly elevated after weaning, coinciding with lower plasma LBP levels and specific microbial taxa and increased acetate uptake into the brain.
Conclusions & Inferences
This study provides evidence that the gut microbiota alteration following induced precocious GIB maturation may induce low‐grade systemic inflammation and alter SCFAs utilization in the brain which may also play a potential role in GIB‐BBB dysfunction disorders in neonates. (Less)
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author
organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Neurogastroenterology and Motility
volume
30
issue
6
pages
13 pages
publisher
Wiley-Blackwell
external identifiers
  • scopus:85047858278
ISSN
1350-1925
DOI
language
English
LU publication?
yes
id
2a326c7f-5fb9-4142-ae9c-5e727700b456
date added to LUP
2018-04-25 20:28:26
date last changed
2018-06-17 05:32:00
@article{2a326c7f-5fb9-4142-ae9c-5e727700b456,
  abstract     = {Background<br>
Precocious maturation of the gastrointestinal barrier (GIB) in newborn mammals can be induced by dietary provocation, but how this affects the gut microbiota and the gut‐brain axis remains unknown. The objective of this study was to investigate effects of induced GIB maturation on gut microbiota composition and blood‐brain barrier (BBB) permeability.<br>
Methods<br>
Suckling rats were studied at 72 h after gavage with phytohemagglutinin (PHA) or microbial protease (PT) to induce maturation of GIB. For comparison, untreated suckling and weaned rats were included (n = 10). Human serum albumin (HSA) was administered orally and analyzed in blood to assess permeability of the GIB, while intraperitoneally injected bovine serum albumin (BSA) was measured in the brain tissue for BBB permeability. The cecal microbial composition, plasma lipopolysaccharide‐binding protein (LBP) levels and short‐chain fatty acids in serum and brain were analyzed.<br>
Key Results<br>
Cessation of HSA passage to blood after PHA or PT treatment was similar to that seen in weaned rats. Interestingly, concomitant increases in cecal Bacteroidetes and plasma LBP levels were observed after both PHA and PT treatments. The BBB passage of BSA was surprisingly elevated after weaning, coinciding with lower plasma LBP levels and specific microbial taxa and increased acetate uptake into the brain.<br>
Conclusions &amp; Inferences<br>
This study provides evidence that the gut microbiota alteration following induced precocious GIB maturation may induce low‐grade systemic inflammation and alter SCFAs utilization in the brain which may also play a potential role in GIB‐BBB dysfunction disorders in neonates.},
  articleno    = {e13285},
  author       = {Marungruang, Nittaya and Arévalo Sureda, Ester and Lefrançoise  , Anais and Weström, Björn and Nyman, Margareta and Prykhodko, Olena and Hållenius, Frida},
  issn         = {1350-1925},
  language     = {eng},
  month        = {01},
  number       = {6},
  pages        = {13},
  publisher    = {Wiley-Blackwell},
  series       = {Neurogastroenterology and Motility},
  title        = {Impact of dietary induced precocious gut maturation on cecal microbiota and its relation to the blood-brain barrier during the postnatal period in rats},
  url          = {http://dx.doi.org/},
  volume       = {30},
  year         = {2018},
}