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4. Elective cesarean delivery affects gut maturation and delays microbial colonization but does not increase necrotizing enterocolitis in preterm pigs

Author

Siggers, R.H., Thymann, T., Jensen, B.B., Molbak, L., Heegaard, P.M.H., Schmidt, M., Buddington, R.K., and Sangild, P.T.

Subjects
Cesarean section -- Physiological aspects, Intestines -- Properties, Microbial colonies -- Properties, Enterocolitis, Neonatal necrotizing -- Physiological aspects, Enterocolitis, Pseudomembranous -- Physiological aspects, Swine -- Physiological aspects, Swine -- Diseases, Intestines -- Microbiology, Intestines -- Research, Biological sciences
Abstract

Although preterm birth and formula feeding increase the risk of necrotizing enterocolitis (NEC), the influences of cesarean section (CS) and vaginal delivery (VD) are unknown. Therefore, gut characteristics and NEC incidence and severity were evaluated in preterm pigs (92% gestation) delivered by CS or VD. An initial study showed that newborn CS pigs (n = 6) had decreased gastric acid secretion, absorption of intact proteins, activity of brush-border enzymes and pancreatic hydrolases, plasma cortisol, rectal temperature, and changes in blood chemistry, indicating impaired respiratory function, compared with VD littermates (n = 6). In a second experiment, preterm CS (n = 16) and VD (n = 16) pigs were given total parenteral nutrition (36 h) then fed porcine colostrum (VD-COL, n = 6; CS-COL, n = 6) or infant milk formula (VD-FORM, n = 10; CS-FORM, n = 10) for 2 days. Across delivery, FORM pigs showed significantly higher NEC incidence, tissue proinflammatory cytokines (IFN-7 and IL-6), Clostridium colonization, and impaired intestinal function, compared with COL pigs. NEC incidence was equal for CS (6/16) and VD (6/16) pigs, CS pigs had decreased bacterial diversity and density, higher villus heights, and increased brush-border enzyme activities (lactase, aminopeptidases) compared with VD pigs. In particular, VD-FORM pigs showed reduced mucosal proportions, reduced lactase and aminopeptidases, and increased proinflammatory cytokine IL-6 compared with CS-FORM (P < 0.06). Despite the initial improvement of intestinal and metabolic functions following VD, gut function, and inflammation were similar, or more negatively affected in VD neonates than CS neonates. Both delivery modes exhibited positive and negative influences on the preterm gut, which may explain the similar NEC incidence. vaginal; cesarean section; bacteria; birth; intestine

Published
2008

9. The intestinal trophic response to enteral food is reduced in parenterally fed preterm pigs and is associated with more nitrergic neurons

Author

Oste, M., Van Ginneken, C.J., Van Haver, E.R., Bjornvad, C.R., Thymann, T., and Sangild, P.T.

Subjects
Infants -- Physiological aspects, Intestinal mucosa -- Growth, Intestinal mucosa -- Research, Parenteral feeding -- Health aspects, Parenteral therapy -- Health aspects, Company growth, Food/cooking/nutrition
Abstract

In term neonates, total parenteral nutrition (TPN) induces mucosal atrophy, whereas the first intake of milk is followed by intestinal growth. This may be explained in part by an NO-mediated increased blood flow. We hypothesized that the immature gut has an altered response to TPN and enteral nutrition. In Expt. 1, preterm caesarean-delivered pigs were administered elemental nutrients for 3 d, infused parenterally (TPN, n = 7) or enterally (TENT, n = 7). In Expt. 2, preterm pigs were fed sow's colostrum, cow's colostrum, or infant formula for 2 d after a 3-d TPN period (TPN-SOW, TPN-COW, TPN-FORM, n = 8-11). Intestinal morphology and the number of enteric neurons containing nitric oxide synthase-1 (NOS-1) were quantified. Both the TPN and TENT groups had increases in intestinal mass, circumference, and mucosal mass, volume, and surface density, relative to values at birth (+30-50%, P < 0.05). In Expt. 2, the magnitudes of the intestinal trophic responses to feeding were similar to those in Expt. 1, but were also associated with an increased number of nitrergic myenteric neurons and some mucosal damage, most frequently observed for the formula group. We conclude that 1) a short period of TPN does not induce mucosal atrophy in preterm pigs, whereas elemental nutrients infused luminally do not mimic the trophic response seen with milk diets, 2) enteral feeding of preterm pigs after a short period of TPN is associated with a modest, diet-dependent trophic response that may be related in part to the actions of an increased population of enteric NOS-1 neurons. KEY WORDS: * preterm * nitric oxide * enteral nutrition * parenteral nutrition * stereology

Published
2005

12. Structural brain maturation differs between preterm and term piglets, whereas brain activity does not

Author

Plomgaard, A M, Andersen, A D, Petersen, T H, van de Looij, Y, Thymann, T, Sangild, P T, Thomsen, C, Sizonenko, S V, Greisen, G, Plomgaard, A M, Andersen, A D, Petersen, T H, van de Looij, Y, Thymann, T, Sangild, P T, Thomsen, C, Sizonenko, S V, and Greisen, G

Abstract

AIM: The aim of the study was to investigate whether amplitude-integrated electroencephalography (aEEG) and cerebral magnetic resonance imaging (MRI) in preterm piglets would provide measures of cerebral functional, microstructural and anatomical maturation, which might reflect the signs of functional brain immaturity, documented in preterm piglets.METHODS: During July-October 2013 at the NEOMUNE Centre, Copenhagen University, Denmark, 31 preterm (90% gestation) and 10 term piglets underwent aEEG on days 1, 2, 4 and 11, and MRI on day 25. Physical activity levels were recorded.RESULTS: Preterm showed delayed neonatal arousal and physical activity, relative to term piglets. Preterm piglets had lower growth rates and brain volume than term piglets, but aEEG patterns were similar. MRI mean diffusivity was also similar, but fractional anisotropy (FA) was lower in preterm piglets (p < 0.001).CONCLUSION: Functional brain maturation, as assessed by aEEG, was relatively advanced in preterm piglets. Conversely, the low FA in the preterm piglets suggests that the white matter microstructure remains less mature in preterm compared to term piglets at postnatal day 25. The results might be utilised to define whether and how preterm piglets may contribute to preclinical models for brain development in preterm infants.

Published
2019

17. The preterm pig as a model of premature infant gait ataxia

Author

Bergström, A., Ryom, K., Vanden Hole, C., Andersen, A. D., Skovgaard, Kerstin, Van Ginneken, C., Thymann, T., Sangild, P. T., Bergström, A., Ryom, K., Vanden Hole, C., Andersen, A. D., Skovgaard, Kerstin, Van Ginneken, C., Thymann, T., and Sangild, P. T.

Abstract

Aims/background Compromised gait, balance and motor coordination (ataxia) as observed in cases of cerebral palsy is a serious complication to premature birth. The cerebellum is a central region with regards to these brain functions and its development shows high sensitivity to premature birth. Our group has over many years refined a pig model of premature birth focusing on gut and immune system development. Phenotypically, we have observed distinct motoric problems e.g. falls, tiptoe walking and swaying in preterm pigs relative to term born counterparts, indicating compromised brain function. The aim of this study was to compare gait patterns and cerebellar neurodevelopmental gene expression of preterm and term piglets. Methods We compared gait patterns and T-maze performance of caesarean born preterm (3 litters, 90% gestation) and term born pigs (1 litter, 100% gestation) recorded at five distinct postnatal days. MatLab was used to determine a list of spatiotemporal gait characteristics e.g. stride length/ frequency, ”duty factor” and asymmetry indices. These data were paralleled by qPCR of >60 selected neurodevelopmental genes of isolated cerebellar tissue. Results While most genes did not differ significantly, we found higher (fold change [1,5-2]) mRNA levels of Midkine, Doublecortin, Neurotrophin3, p75 and Ephrin-B1 in preterms. Preliminary results from gait and T-maze showed significant functional differences between terms and preterms. Conclusions The preterm pig shows functional delays relative to terms, yet the limited cerebellar gene expression differences (mainly related to angiogenesis) suggest other brain regions e.g. motor cortex and basal ganglia to also be involved in compromised gait.

Published
2016

18. Glucagon-like peptide 2 treatment may improve intestinal adaptation during weaning

Author

Thymann, T., Le Huërou-Luron, Isabelle, Petersen, Y. M., Hedemann, M S, Elinf, J., Jensen, B. B., Holst, J.J., Hartmann, B., Sangild, P. T., University of Copenhagen = Københavns Universitet (KU), Alimentation Adaptations Digestives, Nerveuse et Comportementales (ADNC), Institut National de la Recherche Agronomique (INRA), Aarhus University [Aarhus], Danish Directorate for Food, Fisheries and Agri Business, and Danish Medical Research Council

Subjects
Intestines, Swine, weaning, [SDV]Life Sciences [q-bio], Glucagon-Like Peptide 2, pigs, Animals, adaptation, Weaning, dietary transition, intestine, glucagon-like peptide 2, Animals, Suckling
Abstract

International audience; Transition from sow's milk to solid feed is associated with intestinal atrophy and diarrhea. We hypothesized that the intestinotrophic hormone glucagon-like peptide 2 (GLP-2) would induce a dose- and health status-dependent effect on gut adaptation. In Exp. 1, weaned pigs (average BW at weaning 4.98 ± 0.18 kg) were kept in a high-sanitary environment and injected with saline or short-acting GLP-2 (80 μg/(kg BW·12 h); n = 8). Under these conditions, there was no diarrhea and GLP-2 did not improve gastrointestinal structure or function. In Exp. 2, weaned pigs (average BW at weaning 6.68 ± 0.27 kg) were kept in a low-sanitary environment, leading to weaning diarrhea, and injected with saline or short-acting GLP-2 (200 µg/(kg BW·12 h); n = 11). Treatment with GLP-2 increased goblet cell density (P < 0.05) and reduced short chain fatty acid concentration in the colon (P < 0.01) but had limited effects on diarrhea. In Exp. 3, weaned pigs (average BW at weaning 6.90 ± 0.32 kg) were kept in a low-sanitary environment and injected with saline or a long-acting acylated GLP-2 analogue (25 µg/(kg BW·12 h); n = 8). In this experiment, GLP-2 increased intestinal weight (+22%; P < 0.01) and activity of brush border enzymes (+50-100%; P < 0.05). Circulating GLP-2 levels were in the pharmacological range in Exp. 3 (constant levels >20,000 pmol/L) and Exp. 2 (increases to 20,000 pmol/L for a few hours each day) while they were in the supraphysiological range in Exp. 1 (50-200 pmol/L). In conclusion, GLP-2 may improve gut structure and function in weanling pigs. However, the effects may be significant only under conditions of diarrhea and if GLP-2 exposure time is extended using long-acting analogues.

Published
2014

20. Casein addition to a whey-based formula has limited effects on gut function in preterm pigs

Author

Thymann, T., Støy, Ann Cathrine Findal, Bering, S. B., Mølbak, Lars, and Sangild, P. T.

Subjects
animal structures, fluids and secretions, digestive, oral, and skin physiology, food and beverages
Abstract

Preterm infants are susceptible to necrotizing enterocolitis (NEC). Using preterm pigs, we determined whether a whey–casein-based formula would be superior to a formula based on whey protein alone. Twenty cesarean-derived preterm pigs (92% gestation) were given total parenteral nutrition for 36 h followed by 30 h of enteral feeding with whey [protein fraction of milk formula based on whey (WHEY); n = 11] or casein and/or whey [protein fraction of milk formula based on a combination of casein and whey (CASEIN); n = 9]-based formulas. Sugar absorptive function was investigated at 6 and 30 h after initiation of enteral feeding using bolus feedings with galactose and mannitol. Pigs were killed after the last in vivo sugar absorption test and evaluated for NEC and the mid intestine was used for ex vivo measurements of hexose absorption. Microbiota profile and short chain fatty acid (SCFA) levels were studied in gut contents. Severity of NEC lesions was similar between diet groups but galactose absorption was markedly higher in CASEIN than in WHEY (P

Published
2012

34. Dietary long-chain n-3 PUFA, gut microbiota and fat mass in early postnatal piglet development—exploring a potential interplay

Author

Andersen, A.D., Mølbak, Lars, Thymann, T., Michaelsen, K.F., Lauritzen, L., Andersen, A.D., Mølbak, Lars, Thymann, T., Michaelsen, K.F., and Lauritzen, L.

Abstract

Dietary n-3PUFA and gut bacteria, particularly Bacteroidetes, have been suggested to be related to adiposity. We investigated if n-3PUFA affected fat storage and cecal bacteria in piglets. Twenty-four 4-day-old piglets were allocated to formula rich in n-3PUFA (∼3E%) from fish oil (FO) or n-6PUFA from sunflower oil (SO) for 14 days. We assessed body weight, fat accumulation by dual-energy X-ray absorptiometry and microbial molecular fingerprints. Dietary PUFA-composition was reflected in higher erythrocyte n-3PUFA in the FO- than the SO-group (P

Published
2011

36. Diet- and colonization-dependent gut inflammation in preterm neonates

Author

Sangild, P.T., Thymann, T., Siggers, R.H., Siggers, J., Bjørnvad, C.R., Cilieborg, Malene Skovsted, Møller, Hans, Boye, Mette, Burrin, D., Sangild, P.T., Thymann, T., Siggers, R.H., Siggers, J., Bjørnvad, C.R., Cilieborg, Malene Skovsted, Møller, Hans, Boye, Mette, and Burrin, D.

Published
2007

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