Nutritional approach to restore impaired intestinal barrier function and growth after neonatal stress in rats
Abstract
OBJECTIVES: Psychological stress during the neonatal period results in intestinal barrier dysfunction and growth alterations later in life. We aimed to restore impaired barrier function and growth rate by a nutritional intervention. METHODS: Male rat pups (n = 84) were assigned to 1 of 2 rearing conditions from postnatal day (PND) 2 to PND14: S, separated 3 h/d from their mothers, or H, 15 min/d handled controls. From PND15 to PND35, rats received a control diet or a similar diet adapted to contain arachidonic and docosahexaenoic acids, galacto- and fructo-oligosaccharides and Lactobacillus paracasei NCC2461. RESULTS: Maternal separation had only a minor impact on the measured gut barrier parameters at PND15, whereas it severely affected them at PND35. At this age, intestinal permeability to macromolecules was higher, mucin content in small intestinal tissues was lower and microbiota composition was altered in S compared with H animals. Feeding the adapted diet normalized the intestinal permeability, although it did not restore intestinal mucin content or microbiota. In addition, the adapted diet improved the growth rate recovery of the S animals after weaning and resulted in increased villus length in small intestine. CONCLUSION: Our results suggest that an adapted diet containing specific long-chain polyunsaturated fatty acids, prebiotics and probiotics can revert the negative imprinting of neonatal stress on both intestinal barrier function and growth.
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Chronic social stress and early life stress alter the diversity and composition of the gut microbiota in rodents.
“Chronic social stress (e.g., social disruption by aggressive co-inhabitants) and early life stress (e.g., maternal separation) have been shown to alter the diversity and composition of the gut microbiota in rodents [65,66,67].”
Cites
Bradford, M. M. (1976) · Analytical Biochemistry · doi:10.1016/0003-2697(76)90527-3 · Cited by 255,302 · see citing works
Association between postnatal catch-up growth and obesity in childhood: prospective cohort study
Ong, K. K. (2000) · BMJ · doi:10.1136/bmj.320.7240.967 · Cited by 1,659 · see citing works
Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P. M., & Meaney, M. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.9.5335 · Cited by 1,437 · see citing works
SÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003 · see citing works
II. Stress and intestinal barrier function
Söderholm, J. D., & Perdue, M. H. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.1.g7 · Cited by 467 · see citing works
Coutinho, S. V., Plotsky, P. M., Sablad, M., Miller, J. C., Zhou, H., Bayati, A. I., McRoberts, J. A., & Mayer, E. A. (2002) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00240.2001 · Cited by 456 · see citing works
V. Stress and irritable bowel syndrome
Mayer, E. A., Naliboff, B. D., Chang, L., & Coutinho, S. V. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.4.g519 · Cited by 413 · see citing works
Isolauri, E., Majamaa, H., Arvola, T., Rantala, I. S., Virtanen, E., & Arvilommi, H. S. (1993) · Gastroenterology · doi:10.1016/0016-5085(93)91059-q · Cited by 374 · see citing works
Söderholm, J. D., Yang, P., Ceponis, P., Vohra, A., Riddell, R., Sherman, P. M., & Perdue, M. H. (2002) · Gastroenterology · doi:10.1053/gast.2002.36019 · Cited by 362 · see citing works
Auestad, N., Montalto, M. B., Hall, R. T., Fitzgerald, K. M., Wheeler, R. E., Connor, W. E., Neuringer, M., Connor, S. L., Taylor, J. A., & Hartmann, E. E. (1997) · Pediatric Research · doi:10.1203/00006450-199701000-00001 · Cited by 317 · see citing works
Maternal Care, Gene Expression, and the Development of Individual Differences in Stress Reactivity
Francis, D. D., Champagne, F. A., Liu, D., & Meaney, M. J. (1999) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1999.tb08106.x · Cited by 288 · see citing works
Caplan, M. S., Miller–Catchpole, R., Kaup, S. M., Russell, T., Lickerman, M. J., Amer, M. D., Xiao, Y., & Thomson, R. (1999) · Gastroenterology · doi:10.1016/s0016-5085(99)70450-6 · Cited by 269 · see citing works
Castagliuolo, I., LaMont, J. T., Qiu, B., Fleming, S. M., Bhaskar, K. R., Nikulásson, S. Þ., Kornetsky, C. H., & Pothoulakis, C. (1996) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1996.271.5.g884 · Cited by 251 · see citing works
Söderholm, J. D., Yates, D. A., Gareau, M. G., Yang, P.-C., MacQueen, G., & Perdue, M. H. (2002) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.00314.2002 · Cited by 243 · see citing works
Barreau, F., Ferrier, L., Fioramonti, J., & Bueno, L. P. (2004) · Gut · doi:10.1136/gut.2003.024174 · Cited by 240 · see citing works
IV. Modulation of intestinal inflammation by stress: basic mechanisms and clinical relevance
Collins, S. M. (2001) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.2001.280.3.g315 · Cited by 224 · see citing works
Stress stimulates transepithelial macromolecular uptake in rat jejunum
Kiliaan, A. J., Saunders, P. R., Bijlsma, P. B., Berin, M. C., Taminiau, J. A., Groot, J. A., & Perdue, M. H. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.275.5.g1037 · Cited by 223 · see citing works
Effects of oligosaccharide on the faecal flora and non-specific immune system in elderly people
Guigoz, Y., Rochat, F., Perruisseau-Carrier, G., Rochat, I., & Schiffrin, E. J. (2002) · Nutrition Research · doi:10.1016/s0271-5317(01)00354-2 · Cited by 221 · see citing works
Self-citationDietary Oligofructose and Inulin Protect Mice from Enteric and Systemic Pathogens and Tumor Inducers
Buddington, K. K., Donahoo, J. B., & Buddington, R. K. (2002) · Journal of Nutrition · doi:10.1093/jn/132.3.472 · Cited by 211 · see citing works
Ferrier, L., Mazelin, L., Cénac, N., Desreumaux, P., Janin, A., Émilie, D., Colombel, J., Villar, R. G., Fioramonti, J., & Bueno, L. P. (2003) · Gastroenterology · doi:10.1016/s0016-5085(03)01057-6 · Cited by 197 · see citing works
Verdú, E. F., Bercík, P., Bergonzelli, G. E., Huang, X.-X., Blennerhasset, P., Rochat, F., Fiaux, M., Mansourian, R., Corthésy-Theulaz, I., & Collins, S. M. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.06.007 · Cited by 180 · see citing works
Self-citationInnis, S. M., Adamkin, D. H., Hall, R. T., et al. (2002) · The Journal of Pediatrics · doi:10.1067/mpd.2002.123282 · Cited by 149 · see citing works
Dietary Fructooligosaccharides Increase Intestinal Permeability in Rats
ten Bruggencate, S. J. M., Bovee-Oudenhoven, I. M. J., Lettink-Wissink, M. L. G., & van der Meer, R. (2005) · Journal of Nutrition · doi:10.1093/jn/135.4.837 · Cited by 147 · see citing works
Howard, M. D., Gordon, D. T., Pace, L. W., et al. (1995) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199510000-00007 · Cited by 123 · see citing works
Dulloo, A. G., Jacquet, J., & Montani, J.-P. (2002) · International Journal of Obesity · doi:10.1038/sj.ijo.0802127 · Cited by 121 · see citing works
Caplan, M. S., Russell, T., Xiao, Y., et al. (2001) · Pediatric Research · doi:10.1203/00006450-200105000-00007 · Cited by 114 · see citing works
Fontaine, N., Meslin, J. C., Lory, S., & Andrieux, C. (1996) · British Journal Of Nutrition · doi:10.1079/bjn19960194 · Cited by 105 · see citing works
Colonic mucin release in response to immobilization stress is mast cell dependent
Castagliuolo, I., Wershil, B. K., Karalis, K. P., Pasha, A., Nikulásson, S. Þ., & Pothoulakis, C. (1998) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1998.274.6.g1094 · Cited by 102 · see citing works
Heyman, M., & Desjeux, J. F. (1992) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199207000-00008 · Cited by 97 · see citing works
Avishai‐Eliner, S., Yi, S., Newth, C. J. L., & Baram, T. Z. (1995) · Neuroscience Letters · doi:10.1016/0304-3940(95)11606-w · Cited by 88 · see citing works
Montagné, L., Toullec, R., & Lallès, J. P. (2000) · Journal of Dairy Science · doi:10.3168/jds.s0022-0302(00)74910-1 · Cited by 64 · see citing works
Diaphragmatic fatigue assessed by 31P-magnetic resonance spectroscopy in vivo
Nichols, D. G., Buck, J. R., Eleff, S. M., Shungu, D. C., Robotham, J. L., Koehler, R. C., & Traystman, R. J. (1993) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.1993.264.5.c1111 · Cited by 63 · see citing works
Dietary calcium inhibits the intestinal colonization and translocation of Salmonella in rats
Bovee-Oudenhoven, I. M., Termont, D., Weerkamp, A. H., et al. (1997) · Gastroenterology · doi:10.1053/gast.1997.v113.pm9247475 · Cited by 61 · see citing works
Lenz, H. J. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.4.1417 · Cited by 49 · see citing works
López-Pedrosa, J. M., Ramírez, M., Torres, M. I., et al. (1999) · Journal of Nutrition · doi:10.1093/jn/129.6.1149 · Cited by 44 · see citing works
Thoreux, K., Balas, D., Bouley, C., et al. (1998) · Digestion · doi:10.1159/000007514 · Cited by 44 · see citing works
Ackerman, S. H., Hofer, M. A., & Weiner, H. (1978) · Gastroenterology · doi:10.1016/s0016-5085(19)31674-9 · Cited by 42 · see citing works
Effects of oligosaccharides on functional parameters of the intestinal tract of growing pigs.
Breves, G., Szentkuti, L., & Schröder, B. (2001) · PubMed · Cited by 37 · see citing works
Synbiotics to strengthen gut barrier function and reduce morbidity in critically ill patients
Bengmark, S. (2004) · Clinical Nutrition · doi:10.1016/j.clnu.2004.01.005 · Cited by 36 · see citing works
Jones, R. E. (1972) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/0005-2736(72)90187-3 · Cited by 35 · see citing works
Meslin, J., Andrieux, C., Sakata, T., et al. (1993) · British Journal Of Nutrition · doi:10.1079/bjn19930090 · Cited by 35 · see citing works
Allori, C., Agüero, G., Holgado, A. P. D. R., et al. (2000) · Journal of Food Protection · doi:10.4315/0362-028x-63.1.83 · Cited by 32 · see citing works
Dietary Lipid Composition Modifies Intestinal Morphology and Nutrient Transport in Young Rats
Perin, N., Jarocka-Cyrta, E., Keelan, M., et al. (1999) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1097/00005176-199901000-00012 · Cited by 29 · see citing works
Adhesive Mucous Gel Layer and Mucus Release as Intestinal Barrier in Rats
Boshi, Y., Nezu, R., Cui, L., et al. (1996) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/014860719602000298 · Cited by 27 · see citing works
Neurohumoral pathways mediating stress-induced inhibition of gastric acid secretion in rats
Lenz, H. J., & Drüge, G. (1990) · Gastroenterology · doi:10.1016/0016-5085(90)91080-p · Cited by 26 · see citing works
Boshi, Y., Nezu, R., Khan, J., et al. (1996) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/014860719602000606 · Cited by 26 · see citing works
Iiboshi, Y., Nezu, R., Khan, J., et al. (1996) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/0148607196020006406 · Cited by 25 · see citing works
Endopeptidase inhibition and intestinal antigen processing in mice.
Dg, H., Mj, R., Miller, S. D., et al. (1993) · PubMed · Cited by 13 · see citing works
Heyman, M., & Desjeux, J. F. (1992) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1002/j.1536-4801.1992.tb10601.x · Cited by 11 · see citing works
Howard, M. D., Gordon, D. T., Pace, L. W., et al. (1995) · Journal of Pediatric Gastroenterology and Nutrition · doi:10.1002/j.1536-4801.1995.tb11790.x · Cited by 8 · see citing works
de Regil, L. M., & de la Barca, A. M. C. (2004) · International Journal of Food Sciences and Nutrition · doi:10.1080/09637480410001666478 · Cited by 7 · see citing works
The Effect of Exogenous Steroids and Steroid Inhibitors on IgG Transmission in Young Rats
Morris, B., & Morris, R. (2009) · Biology of the Neonate · doi:10.1159/000241360 · Cited by 5 · see citing works
Bailey (1999) · doi:10.1002/(sici)1098-2302(199909)35:2
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Foster, J. A., & McVey Neufeld, K.-A. (2013) · Trends in Neurosciences · doi:10.1016/j.tins.2013.01.005 · Cited by 2,460 · see citing works
The gut microbiota–brain axis in behaviour and brain disorders
Morais, L. H., Schreiber, H. L., & Mazmanian, S. K. (2021) · Nature Reviews Microbiology · doi:10.1038/s41579-020-00460-0 · Cited by 2,149 · see citing works
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Desbonnet, L., Garrett, L., Clarke, G., Kiely, B., Cryan, J. F., & Dinan, T. G. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.005 · Cited by 999 · see citing works
Gareau, M. G., Jury, J., MacQueen, G., Sherman, P. M., & Perdue, M. H. (2007) · Gut · doi:10.1136/gut.2006.117176 · Cited by 472 · see citing works
The microbiome: stress, health and disease
Moloney, R. D., Desbonnet, L., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Mammalian Genome · doi:10.1007/s00335-013-9488-5 · Cited by 430 · see citing works
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O’Mahony, S. M., Hyland, N. P., Dinan, T. G., & Cryan, J. F. (2011) · Psychopharmacology · doi:10.1007/s00213-010-2010-9 · Cited by 415 · see citing works
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Borre, Y. E., Moloney, R. D., Clarke, G., Dinan, T. G., & Cryan, J. F. (2014) · Advances in Experimental Medicine and Biology · doi:10.1007/978-1-4939-0897-4_17 · Cited by 329 · see citing works
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Hemmings, S. M. J., Malan-Müller, S., van den Heuvel, L. L., Demmitt, B. A., Stanislawski, M. A., Smith, D. G., Bohr, A. D., Stamper, C. E., Hyde, E. R., Morton, J. T., et al. (2017) · Psychosomatic Medicine · doi:10.1097/psy.0000000000000512 · Cited by 208 · see citing works
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- Authors
- García‐Ródenas, C. L., Bergonzelli, G. E., Nutten, S., Schumann, A., Cherbut, C., Turini, M., Ornstein, K., Rochat, F., & Corthésy‐Theulaz, I.
- Affiliations
- Nutrition and Health Department Nestlé Research Center Lausanne Switzerland
- Corresponding author
- García‐Ródenas, Clara L.
- Venue
- Journal of Pediatric Gastroenterology and Nutrition
- Publisher
- Wiley
- Published
- 2006-07
- Volume
- 43
- Issue
- 1
- Pages
- 16-24
- ISSN
- 0277-2116 (ISSN-L)
- 1536-4801
- OpenAlex
- W2060992938
- Cited by
- 114
- References
- 53
- Citations by year
- 2025: 2 · 2024: 9 · 2023: 3 · 2022: 3 · 2021: 11 · 2020: 11 · 2019: 8 · 2018: 6 · 2017: 7 · 2016: 3 · 2015: 7 · 2014: 11 · 2013: 8 · 2012: 6
- FWCI
- 2.35
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Pediatric Gastroenterology and Nutrition (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Nursing › Nutrition and Dietetics › Infant Nutrition and Health
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gut microbiota and health
- Keywords
- neonatal stress, maternal separation, intestinal barrier function, intestinal permeability, growth rate, long-chain polyunsaturated fatty acids, docosahexaenoic acid, arachidonic acid, prebiotics, galactooligosaccharides, fructooligosaccharides, probiotics, gut microbiota, intestinal mucin, villus length, dietary intervention, developmental programming
- MeSH terms
- Animals, Animals, Newborn, Body Weight, Disease Models, Animal, Docosahexaenoic Acids, Eating, Food, Formulated, Homeostasis, Intestinal Absorption, Intestinal Mucosa, Intestine, Small, Lactobacillus, Male, Maternal Deprivation, Mucins, Oligosaccharides, Permeability, Stress, Psychological, Time Factors, Weaning, Arachidonic Acid, Probiotics, Rats, Long-Evans, Rats
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