Donor-dependent fecal microbiota transplantation efficacy against necrotizing enterocolitis in preterm pigs
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Donor-dependent fecal microbiota transplantation efficacy against necrotizing enterocolitis in preterm pigs. / Hui, Yan; Vestergaard, Gisle; Deng, Ling; Kot, Witold Piotr; Thymann, Thomas; Brunse, Anders; Nielsen, Dennis Sandris.
In: npj Biofilms and Microbiomes, Vol. 8, No. 1, 48, 2022.Research output: Contribution to journal › Journal article › Research › peer-review
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TY - JOUR
T1 - Donor-dependent fecal microbiota transplantation efficacy against necrotizing enterocolitis in preterm pigs
AU - Hui, Yan
AU - Vestergaard, Gisle
AU - Deng, Ling
AU - Kot, Witold Piotr
AU - Thymann, Thomas
AU - Brunse, Anders
AU - Nielsen, Dennis Sandris
N1 - © 2022. The Author(s).
PY - 2022
Y1 - 2022
N2 - The development of necrotizing enterocolitis (NEC), a life-threatening inflammatory bowel disease affecting preterm infants, is connected with gut microbiota dysbiosis. Using preterm piglets as a model for preterm infants we recently showed that fecal microbiota transplantation (FMT) from healthy suckling piglet donors to newborn preterm piglets decreased the NEC risk. However, in a follow-up study using donor stool from piglets recruited from another farm, this finding could not be replicated. This allowed us to study donor-recipient microbiota dynamics in a controlled model system with a clear difference in NEC phenotype. Preterm piglets (n = 38) were randomly allocated to receive control saline (CON), or rectal FMT using either the ineffective (FMT1) or the effective donor stool (FMT2). All animals were followed for four days before necropsy and gut pathological evaluation. Donor and recipient colonic gut microbiota (GM) were analyzed by 16 S rRNA gene amplicon sequencing and shotgun metagenomics. As expected, only FMT2 recipients were protected against NEC. Both FMT groups had shifted GM composition relative to CON, but FMT2 recipients had a higher lactobacilli relative abundance compared to FMT1. Limosilactobacillus reuteri and Lactobacillus crispatus strains of FMT recipients showed high phylogenetic similarity with their respective donors, indicating engraftment. Moreover, the FMT2 group had a higher lactobacilli replication rate and harbored specific glycosaminoglycan-degrading Bacteroides. In conclusion, subtle species-level donor differences translate to major changes in engraftment dynamics and the ability to prevent NEC. This could have implications for proper donor selection in future FMT trials for NEC prevention.
AB - The development of necrotizing enterocolitis (NEC), a life-threatening inflammatory bowel disease affecting preterm infants, is connected with gut microbiota dysbiosis. Using preterm piglets as a model for preterm infants we recently showed that fecal microbiota transplantation (FMT) from healthy suckling piglet donors to newborn preterm piglets decreased the NEC risk. However, in a follow-up study using donor stool from piglets recruited from another farm, this finding could not be replicated. This allowed us to study donor-recipient microbiota dynamics in a controlled model system with a clear difference in NEC phenotype. Preterm piglets (n = 38) were randomly allocated to receive control saline (CON), or rectal FMT using either the ineffective (FMT1) or the effective donor stool (FMT2). All animals were followed for four days before necropsy and gut pathological evaluation. Donor and recipient colonic gut microbiota (GM) were analyzed by 16 S rRNA gene amplicon sequencing and shotgun metagenomics. As expected, only FMT2 recipients were protected against NEC. Both FMT groups had shifted GM composition relative to CON, but FMT2 recipients had a higher lactobacilli relative abundance compared to FMT1. Limosilactobacillus reuteri and Lactobacillus crispatus strains of FMT recipients showed high phylogenetic similarity with their respective donors, indicating engraftment. Moreover, the FMT2 group had a higher lactobacilli replication rate and harbored specific glycosaminoglycan-degrading Bacteroides. In conclusion, subtle species-level donor differences translate to major changes in engraftment dynamics and the ability to prevent NEC. This could have implications for proper donor selection in future FMT trials for NEC prevention.
KW - Animals
KW - Enterocolitis, Necrotizing/prevention & control
KW - Fecal Microbiota Transplantation
KW - Follow-Up Studies
KW - Humans
KW - Infant, Newborn
KW - Infant, Premature
KW - Phylogeny
KW - Swine
U2 - 10.1038/s41522-022-00310-2
DO - 10.1038/s41522-022-00310-2
M3 - Journal article
C2 - 35680942
VL - 8
JO - n p j Biofilms and Microbomes
JF - n p j Biofilms and Microbomes
SN - 2055-5008
IS - 1
M1 - 48
ER -
ID: 310964919