The DOI matches its Crossref record; 37 of the 37 references it cites were found in a registry or an index.
Neonatal maternal separation predisposes adult rats to colonic barrier dysfunction in response to mild stress
Abstract
Intestinal dysfunction is related to stress and early life events, but the mechanisms are largely unknown. Our aim was to determine whether early trauma predisposes adult rats to intestinal mucosal dysfunction in response to stress. Neonatal Sprague-Dawley rats were individually separated from their mothers for 3 h/day at 4–21 days of age. Between days 80 and 90, separated and control rats were subjected to mild acute stress (30-min water avoidance) or sham stress. Mucosal barrier function and ion transport were assessed in colonic tissues mounted in Ussing chambers. Mild stress increased short-circuit current, conductance, and transepithelial transport of macromolecules in separated rats, while having minimal effects in controls. Pretreatment of the separated rats with a corticotropin-releasing hormone (CRH) antagonist, the peptide α-helical CRH(9–41) injected intraperitoneally 20 min before stress, abolished the stress-induced mucosal changes. Our results indicate that neonatal trauma can induce phenotypic changes in adulthood, including enhanced vulnerability of the gut mucosa to stress via mechanisms involving peripherally located CRH receptors.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“For example, several studies have demonstrated that stressful stimuli can enhance the permeability of the intestinal epithelium, which allows bacterial antigens to penetrate the gut epithelium and triggers an immune response in the intestinal mucosa.23-27”
From Principles and clinical implications of the brain-gut-enteric microbiota axis (2009) · cites this paper as [26]
Citations
Cites
Stress, adaptation, and disease. Allostasis and allostatic load
McEWEN, B. S. (1998) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1998.tb09546.x · Cited by 5,092
Heim, C. (2000) · JAMA · doi:10.1001/jama.284.5.592 · Cited by 1,968
Plotsky, P. M., & Meaney, M. J. (1993) · Molecular Brain Research · doi:10.1016/0169-328x(93)90189-v · Cited by 1,638
The role of corticotropin-releasing factor in depression and anxiety disorders
Arborelius, L., Owens, M., Plotsky, P., & Nemeroff, C. (1999) · Journal of Endocrinology · doi:10.1677/joe.0.1600001 · Cited by 1,378
SÁNCHEZ, M. M., LADD, C. O., & PLOTSKY, P. M. (2001) · Development and Psychopathology · doi:10.1017/s0954579401003029 · Cited by 1,003
Al–Chaer, E. D., Kawasaki, M., & Pasricha, P. J. (2000) · Gastroenterology · doi:10.1053/gast.2000.19576 · Cited by 727
Do early‐life events permanently alter behavioral and hormonal responses to stressors?
Anisman, H., Zaharia, M. D., Meaney, M. J., & Merali, Z. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00025-2 · Cited by 654
Caldji, C., Francis, D., Sharma, S., Plotsky, P., & Meaney, M. (2000) · Neuropsychopharmacology · doi:10.1016/s0893-133x(99)00110-4 · Cited by 600
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
Self-citationCoutinho, 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
Cited by
Sorted by citations
Items 201–244 of 244
The gut microbiota–brain axis and role of probiotics
Sound, R. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-820593-8.00013-6 · Cited by 4
Xu, J., Luo, J., Shang, L., & Kong, W.-M. (2005) · World Chinese Journal of Digestology · doi:10.11569/wcjd.v13.i19.2332 · Cited by 4
Neuropathophysiology of the Irritable Bowel Syndrome
Wood, J. D. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-809954-4.00067-0 · Cited by 3
Yang, P., & Wang, C.-S. (2006) · Digestive Diseases and Sciences · doi:10.1007/s10620-005-9003-2 · Cited by 3
Self-citationSattayachiti, S., Chumpong, P., Niyomdecha, S., Cheaha, D., & Konthapakdee, N. (2024) · Biology · doi:10.3390/biology13090707 · Cited by 2
On mechanisms of increased intestinal wall permeability under stress
Олегович, В. А., Бобынцев, И. И., & Медведева, О. А. (2022) · Человек и его здоровье · doi:10.21626/vestnik/2022-2/05 · Cited by 3
An unusual finding in a patient with iron deficiency anaemia
Leyden, J. E., O’Shea, C., Hegarty, S., & MacMathúna, P. (2005) · Gut · doi:10.1136/gut.2005.067082 · Cited by 1
Videlock, E. J., & Chang, L. (2015) · Wiley eBooks · doi:10.1002/9781118512074.ch75 · Cited by 2
Murison, R. C. C., & Milde, A. M. (2007) · Elsevier eBooks · doi:10.1016/b978-012373947-6.00169-0 · Cited by 2
McConn, B. R., Kpodo, K. R., Rivier, J., Behan, D. P., Richert, B. T., Radcliffe, J. S., Lay, D. C., Jr., & Johnson, J. S. (2023) · Frontiers in Physiology · doi:10.3389/fphys.2023.1266409 · Cited by 1
Hasegawa, R., Nakaya, K., Kanazawa, M., & Fukudo, S. (2025) · BioPsychoSocial Medicine · doi:10.1186/s13030-025-00324-0 · Cited by 1
Huang, L. Y., Zheng, Y., Liu, Q., Feng, Y., Ma, Z., Zhao, X., Xinru, W. E. I., Xinyue, Y. U., Xia, L. V., Lv, J., et al. (2025) · Bioscience of Microbiota Food and Health · doi:10.12938/bmfh.2025-031 · Cited by 1
Microbial shifts in early life: the pediatric gut microbiome and its role in health and disease
Waghmode, S., Viswanathan, R., Koligudde, V., Umare, P., & Lavania, M. (2026) · Gut Microbes · doi:10.1080/19490976.2026.2681763 · Cited by 1
Perinatal Immune Activation and Risk of Autism
Theoharides, T. C., Angelidou, A., Alysandratos, K., Asadi, S., Francis, K., Lykouras, L., & Kalogeromitros, D. C. (2011) · InTech eBooks · doi:10.5772/17436 · Cited by 1
Digestive-Absorption Functions in Fetuses, Infants, and Children
Neu, J., & Mshvildadze, M. (2011) · Elsevier eBooks · doi:10.1016/b978-1-4160-3479-7.10115-6 · Cited by 1
The Gut Microbiome in Pediatrics
Cresci, G., & Teitelbaum, J. E. (2021) · Elsevier eBooks · doi:10.1016/b978-0-323-67293-1.00004-9 · Cited by 1
Modulation nutritionnelle du développement postnatal des fonctions neuro-digestives
Vanhaecke, T. (2016) · theses.fr (ABES) · doi:10.70675/314bdbdfz4219z4db8zacd3z796751145682 · Cited by 1
Dietary fat and bile acids in the pathogenesis of gut barrier dysfunction
Stenman, L. K. (2013) · Työväentutkimus Vuosikirja
Visceral hypersensitivity in Irritable Bowel Syndrome:pathophysiological mechanisms
Kerckhoffs, A. P. M. (2009) · Utrecht University Repository (Utrecht University)
Corticotropin releasing factor receptors in functional and inflammatory gastrointestinal disorders
Tsatsoulis, A. A. (2007) · Annals of Gastroenterology
Walter, S. (2006) · KTH Publication Database DiVA (KTH Royal Institute of Technology)
Inflammation, Microflora, Motility, and Visceral Sensitivity
Michail, S. K., & Ng, M.-W. (2012) · Humana Press eBooks · doi:10.1007/978-1-60761-709-9_5
Wood, J. D. (2004)
Medland, J. E. (2015) · NCSU Libraries Repository (North Carolina State University Libraries)
Guilarte, M. (2014) · TDX (Tesis Doctorals en Xarxa)
Neu, J. (2021) · Elsevier eBooks · doi:10.1016/b978-0-12-820590-7.00009-7 · Cited by 13
田绍平 (2004) · 职业技术教育研究
Bueno, L. P. (2004) · Wiley eBooks · doi:10.1002/9780470760307.ch19
CROHN'S DISEASE: AETIOLOGY, PATHOLOGY, DIAGNOSIS AND MEDICAL TREATMENT
(2008) · Elsevier eBooks · doi:10.1016/b978-0-7020-2723-9.50047-6
García, S. I., Ordoñez, S., Pau, E. C. D. S., & Marcos-Zambrano, L. J. (2022) · medRxiv · doi:10.1101/2022.06.17.22276351
Gut–brain communication: a novel application of probiotics
Das, S., Undhad, T. J., & Hati, S. (2022) · Elsevier eBooks · doi:10.1016/b978-0-12-822238-6.00017-0
Microbiome and Circadian Rhythms: Implications for Sleep, Aging, and Therapeutic Strategies
Najumuddin, Ullah, I., Taqveem, A., & Khurshid, M. (2024) · Springer eBooks · doi:10.1007/978-981-97-3790-1_10
Negative impact of stress on gut-brain axis
Das, M., Goyal, A. K., & Patra, S. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-21680-0.00008-0
Ranjbarinasab, Z., Esmaeilipour, O., Mazhari, M., Shahdadi, F., & Barazandeh, A. (2025) · Spanish Journal of Agricultural Research · doi:10.5424/sjar/2025232-21109
The Gut Microbiome in Pediatrics
Cresci, G., Sukumar, K., & Teitelbaum, J. E. (2025) · Elsevier eBooks · doi:10.1016/b978-0-443-11760-2.00004-5
Promoting Gut Microbiome Diversity in Anorexic Patients: A Neurobiological Review
Shankar, A., Wong, H., Kwe, I., & Wang, L. (2025) · Berkeley Pharma Tech Journal of Medicine · doi:10.52243/bptjm.v5i1.72
The oxytocinergic descending control of pain and its modulation by neonatal maternal separation
Melchior, M. (2018) · theses.fr (ABES) · doi:10.70675/368c73c0ze731z4b57zb52cz8f31049fb33c
Role of the gut-brain axis in early stress-induced emotional vulnerability
Rincel, M. (2017) · theses.fr (ABES) · doi:10.70675/5e8a972cz9ad1z42aezb89cze6474124ef90
Mucosal barriers and gut microbiota: Traditional concepts and recent advances
Yu, L. C.-H. (2026) · Elsevier eBooks · doi:10.1016/b978-0-443-40306-4.00003-x
Chiba, C. H. (2013) · Acervo Digital da Universidade Estadual Paulista (Universidade Estadual Paulista)
Metadata
- Authors
- Söderholm, J. D., Yates, D. A., Gareau, M. G., Yang, P.-C., MacQueen, G., & Perdue, M. H.
- Affiliations
- Intestinal Disease Research Program, Department of Pathology and Molecular Medicine, and
- McMaster University (CA)
- Venue
- American Journal of Physiology-Gastrointestinal and Liver Physiology
- Publisher
- American Physiological Society
- Published
- 2002-12-01
- Volume
- 283
- Issue
- 6
- Pages
- G1257-G1263
- ISSN
- 0193-1857 (ISSN-L)
- 1522-1547
- OpenAlex
- W2113258076
- Cited by
- 243
- References
- 37
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 6 · 2023: 9 · 2022: 9 · 2021: 15 · 2020: 9 · 2019: 7 · 2018: 15 · 2017: 6 · 2016: 14 · 2015: 14 · 2014: 18 · 2013: 7 · 2012: 11
- FWCI
- 5.81
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Gastrointestinal and Liver Physiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
- Health Sciences › Medicine › Gastroenterology › Digestive system and related health
- Keywords
- neonatal maternal separation, intestinal barrier, water avoidance stress, corticotropin-releasing factor, CRH receptors, short-circuit current, transepithelial transport, early trauma, stress vulnerability
- MeSH terms
- Animals, Animals, Newborn, Behavior, Animal, Biological Transport, Colonic Diseases, Corticotropin-Releasing Hormone, Electric Conductivity, Epithelium, Female, Intestinal Mucosa, Maternal Deprivation, Peptide Fragments, Stress, Physiological, Weight Gain, Rats, Sprague-Dawley, Receptors, Corticotropin-Releasing Hormone, Rats
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review