Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates

Jayda Lee Ann Siggers; Mette Viberg Østergaard; Richard Harvey Siggers; Kerstin Skovgaard; Lars Mølbak; Thomas Thymann; Mette Schmidt; Hanne Kristine Møller; Stig Purup; Lisbeth Nielsen Fink; Hanne Frøkiær; Mette Boye; Per Torp Sangild; Stine Brandt Bering

doi:10.1152/ajpgi.00278.2012

Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates

Jayda Lee Ann Siggers, Mette Viberg Østergaard, Richard Harvey Siggers, Kerstin Skovgaard, Lars Mølbak, Thomas Thymann, Mette Schmidt, Hanne Kristine Møller, Stig Purup, Lisbeth Nielsen Fink, Hanne Frøkiær, Mette Boye, Per Torp Sangild, Stine Brandt Bering

Department of Nutrition, Exercise and Sports

52 Citations (Scopus)

Abstract

Preterm neonates are susceptible to gastrointestinal disorders such as necrotizing enterocolitis (NEC). Maternal milk and colostrum protects against NEC via growth promoting, immunomodulatory, and antimicrobial factors. The fetal enteral diet amniotic fluid (AF), contains similar components, and we hypothesized that postnatal AF administration reduces inflammatory responses and NEC in preterm neonates. Preterm pigs (92% gestation) were delivered by caesarean section and fed parental nutrition (2 days) followed by enteral (2 days) porcine colostrum (COLOS, n = 7), infant formula (FORM, n = 13), or AF supplied before and after introduction of formula (AF, n = 10) in experiment 1, and supplied only during the enteral feeding period in experiment 2 (FORM, n = 16; AF, n = 14). The NEC score was reduced in both AF and COLOS pigs, relative to FORM, when AF was provided prior to full enteral feeding (9.9 and 7.7 compared with 17.3, P < 0.05). There was no effect of AF when provided only during enteral feeding. AF pigs showed decreased bacterial abundance in colon and intestinal inflammation-related genes (e.g., TNF-α, IL-1α, IL-6, NOS) were downregulated, relative to FORM pigs with NEC. Anti-inflammatory properties of AF were supported by delayed maturation and decreased TNF-α production in murine dendritic cells, as well as increased proliferation and migration, and downregulation of IL-6 expression in intestinal cells (IEC-6, IPEC-J2). Like colostrum, AF may reduce NEC development in preterm neonates by suppressing the proinflammatory responses to enteral formula feeding and gut colonization when provided before the onset of NEC.

Original language	English
Journal	American Journal of Physiology: Gastrointestinal and Liver Physiology
Volume	304
Issue number	10
Pages (from-to)	G864-G875
Number of pages	12
ISSN	0193-1857
DOIs	https://doi.org/10.1152/ajpgi.00278.2012
Publication status	Published - 2013

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10.1152/ajpgi.00278.2012

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Siggers, J. L. A., Østergaard, M. V., Siggers, R. H., Skovgaard, K., Mølbak, L., Thymann, T., Schmidt, M., Møller, H. K., Purup, S., Fink, L. N., Frøkiær, H., Boye, M., Sangild, P. T., & Bering, S. B. (2013). Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates. American Journal of Physiology: Gastrointestinal and Liver Physiology, 304(10), G864-G875. https://doi.org/10.1152/ajpgi.00278.2012

Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates. / Siggers, Jayda Lee Ann; Østergaard, Mette Viberg; Siggers, Richard Harvey et al.
In: American Journal of Physiology: Gastrointestinal and Liver Physiology, Vol. 304, No. 10, 2013, p. G864-G875.

Research output: Contribution to journal › Journal article › Research › peer-review

Siggers, JLA, Østergaard, MV, Siggers, RH, Skovgaard, K, Mølbak, L, Thymann, T, Schmidt, M, Møller, HK, Purup, S, Fink, LN, Frøkiær, H, Boye, M, Sangild, PT & Bering, SB 2013, 'Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates', American Journal of Physiology: Gastrointestinal and Liver Physiology, vol. 304, no. 10, pp. G864-G875. https://doi.org/10.1152/ajpgi.00278.2012

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abstract = "Preterm neonates are susceptible to gastrointestinal disorders such as necrotizing enterocolitis (NEC). Maternal milk and colostrum protects against NEC via growth promoting, immunomodulatory, and antimicrobial factors. The fetal enteral diet amniotic fluid (AF), contains similar components, and we hypothesized that postnatal AF administration reduces inflammatory responses and NEC in preterm neonates. Preterm pigs (92% gestation) were delivered by caesarean section and fed parental nutrition (2 days) followed by enteral (2 days) porcine colostrum (COLOS, n = 7), infant formula (FORM, n = 13), or AF supplied before and after introduction of formula (AF, n = 10) in experiment 1, and supplied only during the enteral feeding period in experiment 2 (FORM, n = 16; AF, n = 14). The NEC score was reduced in both AF and COLOS pigs, relative to FORM, when AF was provided prior to full enteral feeding (9.9 and 7.7 compared with 17.3, P < 0.05). There was no effect of AF when provided only during enteral feeding. AF pigs showed decreased bacterial abundance in colon and intestinal inflammation-related genes (e.g., TNF-α, IL-1α, IL-6, NOS) were downregulated, relative to FORM pigs with NEC. Anti-inflammatory properties of AF were supported by delayed maturation and decreased TNF-α production in murine dendritic cells, as well as increased proliferation and migration, and downregulation of IL-6 expression in intestinal cells (IEC-6, IPEC-J2). Like colostrum, AF may reduce NEC development in preterm neonates by suppressing the proinflammatory responses to enteral formula feeding and gut colonization when provided before the onset of NEC.",

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T1 - Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates

AU - Siggers, Jayda Lee Ann

AU - Østergaard, Mette Viberg

AU - Siggers, Richard Harvey

AU - Skovgaard, Kerstin

AU - Mølbak, Lars

AU - Thymann, Thomas

AU - Schmidt, Mette

AU - Møller, Hanne Kristine

AU - Purup, Stig

AU - Fink, Lisbeth Nielsen

AU - Frøkiær, Hanne

AU - Boye, Mette

AU - Sangild, Per Torp

AU - Bering, Stine Brandt

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N2 - Preterm neonates are susceptible to gastrointestinal disorders such as necrotizing enterocolitis (NEC). Maternal milk and colostrum protects against NEC via growth promoting, immunomodulatory, and antimicrobial factors. The fetal enteral diet amniotic fluid (AF), contains similar components, and we hypothesized that postnatal AF administration reduces inflammatory responses and NEC in preterm neonates. Preterm pigs (92% gestation) were delivered by caesarean section and fed parental nutrition (2 days) followed by enteral (2 days) porcine colostrum (COLOS, n = 7), infant formula (FORM, n = 13), or AF supplied before and after introduction of formula (AF, n = 10) in experiment 1, and supplied only during the enteral feeding period in experiment 2 (FORM, n = 16; AF, n = 14). The NEC score was reduced in both AF and COLOS pigs, relative to FORM, when AF was provided prior to full enteral feeding (9.9 and 7.7 compared with 17.3, P < 0.05). There was no effect of AF when provided only during enteral feeding. AF pigs showed decreased bacterial abundance in colon and intestinal inflammation-related genes (e.g., TNF-α, IL-1α, IL-6, NOS) were downregulated, relative to FORM pigs with NEC. Anti-inflammatory properties of AF were supported by delayed maturation and decreased TNF-α production in murine dendritic cells, as well as increased proliferation and migration, and downregulation of IL-6 expression in intestinal cells (IEC-6, IPEC-J2). Like colostrum, AF may reduce NEC development in preterm neonates by suppressing the proinflammatory responses to enteral formula feeding and gut colonization when provided before the onset of NEC.

AB - Preterm neonates are susceptible to gastrointestinal disorders such as necrotizing enterocolitis (NEC). Maternal milk and colostrum protects against NEC via growth promoting, immunomodulatory, and antimicrobial factors. The fetal enteral diet amniotic fluid (AF), contains similar components, and we hypothesized that postnatal AF administration reduces inflammatory responses and NEC in preterm neonates. Preterm pigs (92% gestation) were delivered by caesarean section and fed parental nutrition (2 days) followed by enteral (2 days) porcine colostrum (COLOS, n = 7), infant formula (FORM, n = 13), or AF supplied before and after introduction of formula (AF, n = 10) in experiment 1, and supplied only during the enteral feeding period in experiment 2 (FORM, n = 16; AF, n = 14). The NEC score was reduced in both AF and COLOS pigs, relative to FORM, when AF was provided prior to full enteral feeding (9.9 and 7.7 compared with 17.3, P < 0.05). There was no effect of AF when provided only during enteral feeding. AF pigs showed decreased bacterial abundance in colon and intestinal inflammation-related genes (e.g., TNF-α, IL-1α, IL-6, NOS) were downregulated, relative to FORM pigs with NEC. Anti-inflammatory properties of AF were supported by delayed maturation and decreased TNF-α production in murine dendritic cells, as well as increased proliferation and migration, and downregulation of IL-6 expression in intestinal cells (IEC-6, IPEC-J2). Like colostrum, AF may reduce NEC development in preterm neonates by suppressing the proinflammatory responses to enteral formula feeding and gut colonization when provided before the onset of NEC.

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DO - 10.1152/ajpgi.00278.2012

M3 - Journal article

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SP - G864-G875

JO - American Journal of Physiology: Gastrointestinal and Liver Physiology

JF - American Journal of Physiology: Gastrointestinal and Liver Physiology

IS - 10

ER -

Postnatal amniotic fluid intake reduces gut inflammatory responses and necrotizing enterocolitis in preterm neonates

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