Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets
Open accessAbstract
Cytokines play a central role in immune cell response, but they also participate in the maintenance of tissue integrity. Changes in the cytokine network of the pig gut may be expected at weaning, because abrupt changes in dietary and environmental factors lead to important morphological and functional adaptations in the gut. This study measured the gene expression of 6 inflammatory cytokines along the small intestine (SI) and the proximal colon in 28-d-old piglets (n = 45) at different time points (0, 1, 2, 5 and 8 d) postweaning, using RT-PCR. Villus-crypt architecture and enzymatic activities of lactase and sucrase in the SI were also examined. The results confirmed that weaning is associated with morphological and enzymatic changes in the SI. In addition, the data indicated that cytokine response in the gut could be divided into two periods: an early acute response (0 to 2 d postweaning) and a late long-lasting response (2 to 8 d postweaning). Between d 0 and d 2, the levels of IL-1beta, IL-6, and TNF-alpha messenger RNA (mRNA) increased. Marked upregulation of IL-1beta mRNA occurred in most parts of the intestine, whereas IL-6 and TNF-alpha mRNA markedly increased only at specific sites in the intestine. Between d 2 and d 8, the levels of IL-1beta, IL-6, and TNF-alpha mRNA rapidly returned to preweaning values, except that the level of TNF-alpha mRNA remained high in the distal SI. Levels of IL-12 subunit p40 (IL-12p40) and IL-18 mRNA also decreased, compared to those on d 0. Taken together, these results demonstrate that weaning in piglets is associated with an early and transient response in gene expression of inflammatory cytokines in the gut.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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 piglets, early weaning stress impairs intestinal barrier function and increases inflammation and oxidative stress.
“In piglets, early weaning stress impairs intestinal barrier function (271) and increases inflammation (272) and oxidative stress (273).”
From Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health (2021) · cites this paper as [272]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Method for assay of intestinal disaccharidases
Dahlqvist, A. (1964) · Analytical Biochemistry · doi:10.1016/0003-2697(64)90115-0 · Cited by 2,051 · see citing works
Jung, H. C., Eckmann, L., Yang, S. K., Panja, A. B., Fierer, J., Morzycka-Wroblewska, E., & Kagnoff, M. F. (1995) · Journal of Clinical Investigation · doi:10.1172/jci117676 · Cited by 1,197 · see citing works
Factors influencing the structure and function of the small intestine in the weaned pig: a review
Pluske, J. R., Hampson, D. J., & Williams, I. H. (1997) · Livestock Production Science · doi:10.1016/s0301-6226(97)00057-2 · Cited by 1,099 · see citing works
Probiotics: effects on immunity
Isolauri, E., Sütas, Y., Kankaanpää, P., Arvilommi, H. S., & Salminen, S. (2001) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/73.2.444s · Cited by 1,021 · see citing works
Regulation of interferon-γ production by IL-12 and IL-18
Okamura, H., Kashiwamura, S., Tsutsui, H., Yoshimoto, T., & Nakanishi, K. (1998) · Current Opinion in Immunology · doi:10.1016/s0952-7915(98)80163-5 · Cited by 523 · see citing works
Mahida, Y. R., Wu, K., & Jewell, D. P. (1989) · Gut · doi:10.1136/gut.30.6.835 · Cited by 427 · see citing works
Boudry, G., Péron, V., Huërou‐Luron, I. L., Lallès, J. P., & Sève, B. (2004) · Journal of Nutrition · doi:10.1093/jn/134.9.2256 · Cited by 390 · see citing works
Self-citationR., K., Mahan, D. C., Cross, R. F., et al. (1988) · Journal of Animal Science · doi:10.2527/jas1988.662574x · Cited by 343 · see citing works
Weaning Anorexia May Contribute to Local Inflammation in the Piglet Small Intestine
McCracken, B. A., Spurlock, M. E., Roos, M. A., Zuckermann, F. A., & Gaskins, H. R. (1999) · Journal of Nutrition · doi:10.1093/jn/129.3.613 · Cited by 333 · see citing works
Tumor necrosis factor-?, interleukin-1?, and interleukin-6 expression in inflammatory bowel disease
Stevens, C., Walz, G., Singaram, C., Lipman, M. L., ZANKER, B., Muggia, A., Antonioli, D. A., Peppercorn, M. A., & Strom, T. B. (1992) · Digestive Diseases and Sciences · doi:10.1007/bf01300378 · Cited by 330 · see citing works
Small Intestine Epithelial Barrier Function Is Compromised in Pigs with Low Feed Intake at Weaning
Spreeuwenberg, M. A. M., Verdonk, J. M. A. J., Gaskins, H. R., & Verstegen, M. W. A. (2001) · Journal of Nutrition · doi:10.1093/jn/131.5.1520 · Cited by 300 · see citing works
Cytokine production by epithelial cells 1
Stadnyk, A. W. (1994) · The FASEB Journal · doi:10.1096/fasebj.8.13.7926369 · Cited by 279 · see citing works
Evidence for an acute phase response in human intestinal epithelial cells
Molmenti, E. P., Ziambaras, T., & Perlmutter, D. H. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)85216-x · Cited by 248 · see citing works
Cytokine regulation of epithelial permeability and ion transport
McKay, D. M., & Baird, A. W. (1999) · Gut · doi:10.1136/gut.44.2.283 · Cited by 201 · see citing works
Measurement of digestive disorders in the piglet at weaning and related risk factors
Madec, F., Bridoux, N., Bounaix, S., & Jestin, A. (1998) · Preventive Veterinary Medicine · doi:10.1016/s0167-5877(97)00057-3 · Cited by 191 · see citing works
Marin, D. E., Țăranu, I., Bunaciu, R. P., Pascale, F., Tudor, D. S., Avram, N., Sarca, M., Cureu, I., CRISTE, R. D., Suta, V., et al. (2002) · Journal of Animal Science · doi:10.2527/2002.8051250x · Cited by 190 · see citing works
Self-citationHampson, D. J., & Kidder, D. (1986) · Research in Veterinary Science · doi:10.1016/s0034-5288(18)30481-8 · Cited by 177 · see citing works
Beagley, K. W., Fujihashi, K., Lagoo, A. S., Lagoo‐Deenadaylan, S., Black, C. A., Murray, A. M., Sharmanov, A. T., Yamamoto, M., McGhee, J. R., Elson, C. O., et al. (1995) · The Journal of Immunology · doi:10.4049/jimmunol.154.11.5611 · Cited by 176 · see citing works
Pitman, R. S., & Blumberg, R. S. (2000) · Journal of Gastroenterology · doi:10.1007/s005350070017 · Cited by 164 · see citing works
Diet-Dependent and Diet-Independent Metabolic Responses Underlie Growth Stasis of Pigs at Weaning
McCracken, B. A., Gaskins, H. R., Ruwe-Kaiser, P. J., et al. (1995) · Journal of Nutrition · doi:10.1093/jn/125.11.2838 · Cited by 153 · see citing works
Inflammatory cytokines in animal health and disease
Murtaugh, M. P., Baarsch, M. J., Zhou, Y., Scamurra, R. W., & Lin, G. (1996) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(96)05698-x · Cited by 151 · see citing works
Panja, A. B., Goldberg, S., Eckmann, L., Krishen, P., & Mayer, L. (1998) · The Journal of Immunology · doi:10.4049/jimmunol.161.7.3675 · Cited by 134 · see citing works
Darwich, L., Pié, S., Rovira, A., Segalés, J., Domingo, M., Oswald, I. P., & Mateu, E. (2003) · Journal of General Virology · doi:10.1099/vir.0.19124-0 · Cited by 128 · see citing works
Self-citationRoute and Type of Nutrition Influence IgA-Mediating Intestinal Cytokines
Wu, Y., Kudsk, K. A., DeWitt, R. C., Tolley, E. A., & Li, J. (1999) · Annals of Surgery · doi:10.1097/00000658-199905000-00008 · Cited by 125 · see citing works
Morphometry and cell proliferation in endoscopic biopsies: Evaluation of a technique
Goodlad, R. A., Levi, S., Lee, C. Y., Mandir, N. K., Hodgson, H. J. F., & Wright, N. A. (1991) · Gastroenterology · doi:10.1016/0016-5085(91)90072-s · Cited by 119 · see citing works
Pluske, J. R., Kerton, D. K., Cranwell, P. D., et al. (2003) · Australian Journal of Agricultural Research · doi:10.1071/ar02156 · Cited by 115 · see citing works
Lymphocyte subsets in jejunal and ileal Peyer's patches of normal and gnotobiotic minipigs.
Rothkötter, H. ‐., & Pabst, R. (1989) · PubMed · Cited by 111 · see citing works
Intestinal epithelial cells as watchdogs for the natural immune system
Eckmann, L. (1995) · Trends in Microbiology · doi:10.1016/s0966-842x(00)88894-0 · Cited by 109 · see citing works
A reverse transcription-polymerase chain reaction method to analyze porcine cytokine gene expression
Dozois, C. M., Oswald, É., Gautier, N., Serthelon, J.-P., Fairbrother, J. M., & Oswald, I. P. (1997) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(97)00039-1 · Cited by 106 · see citing works
Self-citationKandil, H. M., Berschneider, H. M., & Argenzio, R. A. (1994) · Gut · doi:10.1136/gut.35.7.934 · Cited by 90 · see citing works
Pié, S., Matsiota-Bernard, P., Truffa‐Bachi, P., & Nauciel, C. (1996) · Infection and Immunity · doi:10.1128/iai.64.3.849-854.1996 · Cited by 88 · see citing works
Self-citationBINNS, R. M., & LICENCE, S. T. (1985) · Springer eBooks · doi:10.1007/978-1-4613-2463-8_81 · Cited by 81 · see citing works
Marion, J., Biernat, M., Thomas, F., et al. (2002) · annales de biologie animale biochimie biophysique · doi:10.1051/rnd:2002030 · Cited by 76 · see citing works
Effect of proinflammatory interleukins on jejunal nutrient transport
Hardin, J. W., Kroeker, K. I., Chung, B., & Gall, D. (2000) · Gut · doi:10.1136/gut.47.2.184 · Cited by 73 · see citing works
Ziambaras, T., Rubin, D. C., & Perlmutter, D. H. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.2.1237 · Cited by 65 · see citing works
Cytokines and Inflammatory Bowel Disease: A Review
McClane, S. J., & Rombeau, J. L. (1999) · Journal of Parenteral and Enteral Nutrition · doi:10.1177/014860719902300506 · Cited by 58 · see citing works
Cytokines as markers for infections and their effect on growth performance and well-being in the pig
Fossum, C. (1998) · Domestic Animal Endocrinology · doi:10.1016/s0739-7240(98)80001-5 · Cited by 51 · see citing works
Fournout, S., Dozois, C. M., Odin, M., et al. (2000) · Infection and Immunity · doi:10.1128/iai.68.2.839-847.2000 · Cited by 50 · see citing works
Inflammatory Cytokines and Mucosal Injury
Williams, D. A. (2001) · JNCI Monographs · doi:10.1093/oxfordjournals.jncimonographs.a003435 · Cited by 48 · see citing works
Cytokine mRNA expression in pigs infected with Schistosoma japonicum
Oswald, I. P., Dozois, C. M., BARLAGNE, R., et al. (2001) · Parasitology · doi:10.1017/s0031182001007399 · Cited by 48 · see citing works
Self-citationSchaeffer, C., Diab-Assef, M., Plateroti, M., et al. (2000) · Gut · doi:10.1136/gut.47.2.192 · Cited by 42 · see citing works
Manzano, M., Abadía‐Molina, A. C., Olivares, E. G., et al. (2002) · Journal of Nutrition · doi:10.1093/jn/132.9.2757 · Cited by 35 · see citing works
Early cytokine response of gnotobiotic piglets to Salmonella enterica serotype Typhimurium
pl�chal, I., Trebichavsk�, I., Muneta, Y., et al. (2002) · Veterinary Research · doi:10.1051/vetres:2002017 · Cited by 29 · see citing works
Vázquez, E., Gil, Á., & Rueda, R. (2001) · BioFactors · doi:10.1002/biof.5520150101 · Cited by 28 · see citing works
Zachrisson, K., Neopikhanov, V., Wretlind, B., et al. (2001) · Cytokine · doi:10.1006/cyto.2001.0917 · Cited by 26 · see citing works
Mengheri, E., Ciapponi, L., Vignolini, F., et al. (1996) · Life Sciences · doi:10.1016/0024-3205(96)00446-8 · Cited by 21 · see citing works
Vázquez, E., Gil, Á., Olivares, E. G., et al. (2000) · Cytokine · doi:10.1006/cyto.2000.0706 · Cited by 20 · see citing works
Cloning, chromosomal location, and tissue expression of the gene for pig interleukin-18
Fournout, S., Dozois, C. M., Martine Yerle, B., Pinton, P., Fairbrother, J. M., Oswald, É., & Oswald, I. P. (2000) · Immunogenetics · doi:10.1007/s002510050630 · Cited by 16 · see citing works
Self-citationIncreased Small Bowel Epithelial Turnover in Interleukin-1 Receptor Knockout Mice
Wolf, S. E., DebRoy, M. A., Ikeda, H., et al. (2000) · Annals of Surgery · doi:10.1097/00000658-200007000-00006 · Cited by 13 · see citing works
Trebichavský, I., Dlabač, V., & Řeháková, Z. (1999) · Veterinary Immunology and Immunopathology · doi:10.1016/s0165-2427(98)00208-6 · Cited by 4 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Boudry, G., Pe ´ron, V., Lalle `s, J. P. & Se `ve, B. (2003) Weaning induces transient and long-lasting modifications of secretory and absorptive physiology of piglets small intestine (Ball, R. O., ed.), University of Alberta. Presented at the 9th International Symposium on Digestive Physiology in Pigs, May 14 -17, 2003, Banff, AB, Canada.
Cited by
Sorted by citations
Diet and the Microbiota–Gut–Brain Axis: Sowing the Seeds of Good Mental Health
Berding, K., Vlckova, K., Marx, W., Schellekens, H., Stanton, C., Clarke, G., Jacka, F., Dinan, T. G., & Cryan, J. F. (2021) · Advances in Nutrition · doi:10.1093/advances/nmaa181 · Cited by 451 · see citing works
Furbeyre, H., van Milgen, J., Mener, T., Gloaguen, M., & Labussière, E. (2017) · Animal · doi:10.1017/s1751731116001543 · Cited by 111 · see citing works
Roselli, M., Finamore, A., Britti, M. S., Bosi, P., Oswald, I., & Mengheri, E. (2005) · Animal Research · doi:10.1051/animres:2005012 · Cited by 97 · see citing works
Yu, K., Canalias, F., Solà-Oriol, D., Arroyo, L., Pato, R., Saco, Y., Terré, M., & Bassols, A. (2019) · Frontiers in Veterinary Science · doi:10.3389/fvets.2019.00123 · Cited by 82 · see citing works
Taranu, I., Marin, D., Braicu, C., Pistol, G., Sorescu, I., Pruteanu, L., Berindan Neagoe, I., & Vodnar, D. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19071923 · Cited by 26 · see citing works
- Authors
- Lallès, J. P., Sève, B., Pié, S., Blazy, F., Laffitte, J., & Oswald, I. P.
- Affiliations
- Institut National de Recherche pour l'Agriculture, l'Alimentation et l'Environnement (FR)
- Corresponding author
- Oswald, I.P.
- Venue
- The Journal of Nutrition
- Publisher
- Elsevier BV
- Published
- 2004-03
- Volume
- 134
- Issue
- 3
- Pages
- 641-647
- ISSN
- 0022-3166 (ISSN-L)
- OpenAlex
- W2108599358
- Cited by
- 587
- References
- 50
- Citations by year
- 2026: 20 · 2025: 22 · 2024: 29 · 2023: 36 · 2022: 56 · 2021: 52 · 2020: 52 · 2019: 31 · 2018: 46 · 2017: 22 · 2016: 35 · 2015: 27 · 2014: 23 · 2013: 20 · 2012: 27
- FWCI
- 19.18
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Journal of Nutrition (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- European Commission
- National Institutes of Health
- National Institute on Aging
- Topics
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Animal Nutrition and Physiology
- Health Sciences › Veterinary › Small Animals › Veterinary medicine and infectious diseases
- Health Sciences › Veterinary › Small Animals › Animal health and immunology
- Keywords
- weaning, inflammatory cytokines, piglets, small intestine, colon, gene expression, IL-1β, interleukin-6, TNF-α, interleukin-12p40, IL-18, lactase, sucrase, intestinal adaptation
- MeSH terms
- Animals, Gene Expression Regulation, Inflammation, Interleukins, Intestinal Mucosa, Sucrase, Swine, Time Factors, Tumor Necrosis Factor-alpha, Weaning, Cytokines, DNA Primers, Immunity, Mucosal, Reverse Transcriptase Polymerase Chain Reaction, Lactase
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
