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Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs
Open accessAbstract
The gastrointestinal (GI) barrier serves a critical role in survival and overall health of animals and humans. Several layers of barrier defense mechanisms are provided by the epithelial, immune and enteric nervous systems. Together they act in concert to control normal gut functions (e.g., digestion, absorption, secretion, immunity, etc.) whereas at the same time provide a barrier from the hostile conditions in the luminal environment. Breakdown of these critical GI functions is a central pathophysiological mechanism in the most serious GI disorders in pigs. This review will focus on the development and functional properties of the GI barrier in pigs and how common early life production stressors, such as weaning, can alter immediate and long-term barrier function and disease susceptibility. Specific stress-related pathophysiological mechanisms responsible for driving GI barrier dysfunction induced by weaning and the implications to animal health and performance will be discussed.
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“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 [271]
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Associations between gastrointestinal-tract function and the stress response after weaning in pigs
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Role of vitamins for gastro-intestinal functionality and health of pigs
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Dietary Glutamic Acid Modulates Immune Responses and Gut Health of Weaned Pigs
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Effect of dietary Bacillus coagulans on the performance and intestinal microbiota of weaned piglets
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Impact of Early Weaning on Development of the Swine Gut Microbiome
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“However, due to immature digestive organs, insufficient secretion of gastric acid and digestive enzymes, and low immunity of early weaned pigs, they often display early weaning stress syndrome, which is characterized by digestive dysfunction, growth retardation, and diarrhea [3,4].”
BackgroundZhang, K., Xu, Y., Yang, Y., Guo, M., Zhang, T., Zong, B., Huang, S., Suo, L., Ma, B., Wang, X., et al. (2022) · Animal nutrition · doi:10.1016/j.aninu.2022.04.004 · Cited by 39
“In contrast, other studies challenged the persistent effects of early weaning in animals (Li et al., 2018; McCoard et al., 2020; Moeser et al., 2017).”
ResultIntestinal single-cell atlas reveals novel lymphocytes in pigs with similarities to human cells
Wiarda, J. E., Trachsel, J., Sivasankaran, S. K., Tuggle, C. K., & Loving, C. L. (2022) · Life Science Alliance · doi:10.26508/lsa.202201442 · Cited by 42
“Moreover, pigs serve as models for studying the impact of stress, nutrition, and infectious disease on intestinal physiology and immune status (reviewed by Gonzalez et al [2015], Roura et al [2016], Ziegler et al [2016], Moeser et al [2017], Hryhorowicz et al [2020], and K¨aser [2021]).”
Meng, Q., Zhang, Y., Li, J., Shi, B., Ma, Q., & Shan, A. (2022) · Journal of Nutrition · doi:10.1093/jn/nxac208 · Cited by 37
Evaluating nursery pig responses to in-feed sub-therapeutic antibiotics
Helm, E. T., Curry, S. M., Trachsel, J., Schroyen, M., & Gabler, N. K. (2019) · PLoS ONE · doi:10.1371/journal.pone.0216070 · Cited by 40
Alternatives to antibiotics in pig production: looking through the lens of immunophysiology
Liu, H., Zhu, C., Zhu, M., Yuan, L., Li, S., Gu, F., Hu, P., Chen, S., & Cai, D. (2024) · Stress Biology · doi:10.1007/s44154-023-00134-w · Cited by 37
“This would facilitate the passage of toxic substances and pathogens at the mucosal barrier, and stimulate a vigorous immune response (Moeser et al. 2017; Pluske et al. 2018).”
BackgroundMo, K., Li, J., Liu, F., Xu, Y. X., Huang, X., & Ni, H. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2021.808106 · Cited by 35
“of 48 weaning piglets were randomly allotted to six dietary treatments: (1) basal diet; (2)”
BackgroundMethodLiu, G., Gu, K., Liu, X., Jia, G., Zhao, H. Y., Chen, X., & Wang, J. (2023) · Food Research International · doi:10.1016/j.foodres.2023.112597 · Cited by 36
Moita, V. H. C., Duarte, M. E., da Silva, S. N., & Kim, S. W. (2021) · Animals · doi:10.3390/ani11061591 · Cited by 34
Choi, H., & Kim, S. W. (2023) · Animals · doi:10.3390/ani13132236 · Cited by 33
“After weaning, the mRNA expression of pro-inflammatory cytokines was increased [46], indicating that weaning stress affects cytokine signaling modulation in the small intestine of nursery pigs [47].”
BackgroundNovais, A. K., Martel-Kennes, Y., Roy, C., Deschêne, K., Beaulieu, S., Bergeron, N., Laforest, J.-P., Lessard, M., Matte, J. J., & Lapointe, J. (2019) · animal · doi:10.1017/s1751731119002829 · Cited by 32
Boontiam, W., Bunchasak, C., Kim, Y. Y., Kitipongpysan, S., & Hong, J. (2022) · Animals · doi:10.3390/ani12030350 · Cited by 32
“Newly weaned pigs are usually susceptible to many stressors [30].”
BackgroundLaw, K., Lozinski, B., Torres, I., Davison, S., Hilbrands, A., Nelson, E. V., Parra-Suescún, J., Johnston, L. J., & Gomez, A. M. (2021) · mSphere · doi:10.1128/msphere.00663-21 · Cited by 31
“The increased abundance of Lactobacillus at weaning is interesting because of the physiological stress associated with weaning, where enhancing gut health and the immune system is critical (44).”
BackgroundQiao, L., Dou, X., Song, X., Chang, J., Zeng, X., Zhu, L., Yi, H., & Xu, C. (2023) · Animal nutrition · doi:10.1016/j.aninu.2023.08.003 · Cited by 31
Eriksen, E. Ø., Kudirkienė, E., Barington, K., Goecke, N. B., Blirup-Plum, S. A., Nielsen, J. P., Olsen, J. E., Jensen, H. E., Pankoke, K., Larsen, L. E., et al. (2023) · Porcine Health Management · doi:10.1186/s40813-023-00325-x · Cited by 30
The Role of Polyphenols in Regulation of Heat Shock Proteins and Gut Microbiota in Weaning Stress
Hussain, T., Wang, J., Murtaza, G., Metwally, E., Yang, H., Kalhoro, M. S., Kalhoro, D. H., Rahu, B. A., Tan, B., Sahito, R. G. A., et al. (2021) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2021/6676444 · Cited by 32
“The overwhelming status of ROS interferes with cellular function and subsequently affects TJ proteins resulting in increased gut permeability [67].”
BackgroundRajput, M., Momin, T., Singh, A. K., Banerjee, S. J., Villasenor, A., Sheldon, J., Paudel, P., & Rajput, R. K. S. (2022) · Veterinary and Animal Science · doi:10.1016/j.vas.2022.100279 · Cited by 30
“It contains cells that perform barrier function, digestion, and absorption as well as cells of the nervous and immune systems (Mason et al., 2008; A. J. Moeser et al., 2017).”
BackgroundRen, H., Li, K., Min, Y., Qiu, B., Huang, X., Luo, J., Qi, L., Kang, M., Xia, P., Qiao, H., et al. (2023) · Antioxidants · doi:10.3390/antiox12040914 · Cited by 29
“Farmed pigs constantly face various health challenges, such as weaning stress [1], fungal poisoning [2], and endotoxin stress [3].”
BackgroundLi, Z., Lin, Z., Lu, Z., Feng, Z., Chen, Q., Deng, S.-F., Li, Z., Yan, Y., & Ying, Z. (2019) · AMB Express · doi:10.1186/s13568-019-0828-z · Cited by 29
Impact of viral disease hypophagia on pig jejunal function and integrity
Helm, E. T., Curry, S. M., Mille, C. M. D., Schweer, W., Burrough, E. R., & Gabler, N. K. (2020) · PLoS ONE · doi:10.1371/journal.pone.0227265 · Cited by 28
“Reductions in intestinal integrity and function have been documented under a variety of stressors, including heat stress [3, 4], weaning stress [5, 6], and enteric disease challenges such as with Porcine Epidemic Diarrhea Virus [PEDV; 7, 8, 9].”
BackgroundMaintaining continuity of nutrient intake after weaning. I. Review of pre-weaning strategies
Wensley, M. R., Tokach, M. D., Woodworth, J. C., Goodband, R. D., Gebhardt, J. T., DeRouchey, J. M., & McKilligan, D. M. (2021) · Translational Animal Science · doi:10.1093/tas/txab021 · Cited by 33
Wang, Z., Hu, J. H., Yang, X., Yin, L., Wang, M., Yin, Y., Li, J., Yang, H., & Yin, Y. (2021) · Animal nutrition · doi:10.1016/j.aninu.2021.04.008 · Cited by 28
“Since piglets are susceptible to psychological, nutritional and environmental factors during theweaning stage, the homeostasis of the intestine is easily disrupted (Moeser et al., 2017).”
BackgroundXiang, X.-D., Deng, Z., Wang, Y.-W., Sun, H., Wang, L., Han, Y., Wu, Y., Jian-gao, L., & Sun, L. (2021) · Antioxidants · doi:10.3390/antiox10111665 · Cited by 27
“These outcomes are in agreement with previous studies, which showed organic acids can improve intestinal morphology [39].”
ResultZhao, B.-C., Wang, T., Chen, J., Qiu, B.-H., Xu, Y., Zhang, Q., Li, J., Wang, C.-J., Nie, Q.-F., & Li, J. (2023) · Porcine Health Management · doi:10.1186/s40813-023-00317-x · Cited by 27
Pioneering gut health improvements in piglets with phytogenic feed additives
Yu, S. J., Morris, A., Kayal, A., Milošević, I., Van, T. T. H., Bajagai, Y. S., & Stanley, D. (2024) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-023-12925-2 · Cited by 29
“Enhanced intestinal crypt cell proliferation, which requires ample nucleotide supply for DNA replication, might be one possible mechanism underlying this observation (Moeser et al. 2017).”
BackgroundIntraepithelial T Cells Diverge by Intestinal Location as Pigs Age
Wiarda, J. E., Trachsel, J., Bond, Z. F., Byrne, K. A., Gabler, N. K., & Loving, C. L. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01139 · Cited by 26
Li, Y., Liu, Y., Wu, J., Chen, Q., Zhou, Q., Wu, F., Zhang, R., Fang, Z., Lin, Y., Xu, S., et al. (2021) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-021-00625-8 · Cited by 26
“For weaning piglets, weaning stress is a vital factor that causing immunological and intestinal impairments [34].”
BackgroundKobuvirus shedding dynamics in a swine production system and their association with diarrhea.
Nantel-Fortier, N., Lachapelle, V., Letellier, A., L'Homme, Y., & Brassard, J. (2019) · Veterinary Microbiology · doi:10.1016/j.vetmic.2019.07.023 · Cited by 22
Relationship between weaning age and antibiotic usage on pig growth performance and mortality
Faccin, J. E. G., Tokach, M. D., Allerson, M. W., Woodworth, J. C., DeRouchey, J. M., Dritz, S. S., Bortolozzo, F. P., & Goodband, R. D. (2020) · Journal of Animal Science · doi:10.1093/jas/skaa363 · Cited by 25
Impact of supplemental liquid feed pre-weaning and piglet weaning age on feed intake post-weaning
Kobek‐Kjeldager, C., Vodolazs'ka, D., Lauridsen, C., Canibe, N., & Pedersen, L. J. (2021) · Livestock Science · doi:10.1016/j.livsci.2021.104680 · Cited by 25
Role of milk carbohydrates in intestinal health of nursery pigs: a review
Jang, K. B., & Kim, S. W. (2022) · Journal of Animal Science and Biotechnology/Journal of animal science and biotechnology · doi:10.1186/s40104-021-00650-7 · Cited by 28
“Thus, the neonates would take up to 6 weeks to develop a stable immunity in nursery pigs [114].”
BackgroundSong, M., Kim, B., Cho, J. H., Kyoung, H., Park, S., Cho, J.-Y., Park, K. I., Kim, H. B., & Lee, J. J. (2022) · Journal of Animal Science and Technology · doi:10.5187/jast.2022.e28 · Cited by 28
“After weaning, piglets suffer from several stresses due to physiological, environmental, and immunological changes [16,17].”
Background4-Phenylbutyric acid accelerates rehabilitation of barrier function in IPEC-J2 cell monolayer model
Jiang, Q., Yin, J., Chen, J., Ma, X., Wu, M., Li, X., Kang, Y., Tan, B., & Yin, Y. (2021) · Animal nutrition · doi:10.1016/j.aninu.2021.02.003 · Cited by 24
“Oxidative dyshomeostasis is involved in weaning stress-induced intestinal barrier damage (Moeser et al., 2017).”
BackgroundUerlings, J., Sureda, E. A., Schroyen, M., Kroeske, K., Tanghe, S., Vos, M. D., Bruggeman, G., Wavreille, J., Bindelle, J., Purcaro, G., et al. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.650211 · Cited by 24
“Moreover, as the mucosal immune system is still immature and a stable commensal microbiota is not yet established (4), this period is often associated with disturbed microbiota and the proliferation of pathogens in the hindgut, resulting in post-weaning diarrhea (5, 6).”
BackgroundLiu, N., Ma, X., & Jiang, X. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.872990 · Cited by 25
Duarte, M. E., Stahl, C. H., & Kim, S. W. (2023) · Antioxidants · doi:10.3390/antiox12051040 · Cited by 26
“The impaired intestinal immune system increases pigs susceptibility to pathogen invasion [3,4].”
Background
Metadata
- Authors
- Moeser, A. J., Pohl, C. S., & Rajput, M.
- Affiliations
- Michigan State University (US)
- Corresponding author
- Moeser, Adam J.
- Venue
- Animal nutrition
- Publisher
- Elsevier BV
- Published
- 2017-12
- Volume
- 3
- Issue
- 4
- Pages
- 313-321
- ISSN
- 2405-6383 (ISSN-L)
- 2405-6545
- PMC
- PMC5941262
- OpenAlex
- W2732972012
- Cited by
- 452
- References
- 95
- Citations by year
- 2026: 54 · 2025: 53 · 2024: 61 · 2023: 63 · 2022: 85 · 2021: 60 · 2020: 38 · 2019: 34 · 2018: 4
- FWCI
- 2.53
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Animal nutrition (publishedVersion, cc-by-nc-nd)
- Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- National Institutes of Health (HD072968)
- USDA National Institute of Food and Agriculture (2017-67015-26673)
- 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 › Medicine › Gastroenterology › Gastrointestinal motility and disorders
- Keywords
- weaning stress, gastrointestinal barrier, pigs, gut health, intestinal epithelium, enteric nervous system, intestinal immunity, disease susceptibility, early life stress, barrier dysfunction
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