Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
REVIEW

Associations between gastrointestinal-tract function and the stress response after weaning in pigs

J. R. Pluske A B , D. W. Miller A , S. O. Sterndale A and D. L. Turpin A
+ Author Affiliations
- Author Affiliations

A Agricultural Sciences, College of Science, Health, Engineering and Education, Murdoch University, Murdoch, WA 6150, Australia.

B Corresponding author. Email: J.Pluske@murdoch.edu.au

Animal Production Science 59(11) 2015-2022 https://doi.org/10.1071/AN19279
Submitted: 13 May 2019  Accepted: 10 July 2019   Published: 16 September 2019

Abstract

Psychosocial stress is a major factor driving gastrointestinal-tract (GIT) pathophysiology and disease susceptibility in both humans and animals. Young weaned pigs typically undergo psychosocial and environmental stressors associated with production practices, including separation from their dam, mixing and crowding stress, transport and changed temperature and air-quality parameters, all of which can have significant deleterious impacts not only on performance but also on GIT structure and function, and, therefore, pig health and welfare. Strategies addressing some of these issues are explored in the current review, as well as discussion pertaining to sexual dimorphism in young pigs linked to stressful experiences, with young female pigs seemingly adversely affected more than their male counterparts. However, mechanisms governing susceptibility to stress-induced GIT functionality and disease remain inadequately understood.

Additional keywords: dimorphism, gender, health, management, stocking density.


References

Andersen IL, Andenæs H, Knut EB, Jensen P, Bakken M (2000) The effects of weight asymmetry and resource distribution on aggression in groups of acquainted pigs. Applied Animal Behaviour Science 68, 107–120.
The effects of weight asymmetry and resource distribution on aggression in groups of acquainted pigs.Crossref | GoogleScholarGoogle Scholar | 10771319PubMed |

Anonymous (2016) MEPs vote to ban prophylactic use of antibiotics in animals. The Veterinary Record 178, 201-202
MEPs vote to ban prophylactic use of antibiotics in animals.Crossref | GoogleScholarGoogle Scholar |

Bischoff SC (2011) ‘Gut health’: a new objective in medicine? BMC Medicine 9, 24
‘Gut health’: a new objective in medicine?Crossref | GoogleScholarGoogle Scholar | 21401922PubMed |

Bruininx EM, van der Peet-Schwering CM, Schrama JW, Veriejken PF, Vesseur PC, Everts H, den Hartog LA, Beynen AC (2001) Individually measured feed intake characteristics and growth performance of group-housed weanling pigs: effects of sex, initial body weight, and body weight distribution within groups. Journal of Animal Science 79, 301–308.
Individually measured feed intake characteristics and growth performance of group-housed weanling pigs: effects of sex, initial body weight, and body weight distribution within groups.Crossref | GoogleScholarGoogle Scholar | 11219437PubMed |

Callahan SR, Cross AJ, DeDecker AE, Lindemann MD, Estienne MJ (2017) Effects of group-size-floor space allowance during the nursery phase of production on growth, physiology, and hematology in replacement gilts. Journal of Animal Science 95, 201–211.

Campbell JM, Crenshaw JD, Polo J (2013) The biological stress of early weaned piglets. Journal of Animal Science and Biotechnology 4, 19
The biological stress of early weaned piglets.Crossref | GoogleScholarGoogle Scholar | 23631414PubMed |

Celi P, Cowieson AJ, Fru-Nji F, Steinert RE, Kluenter A-M, Verlhac V (2017) Gastrointestinal functionality in animal nutrition and health: New opportunities for sustainable animal production. Animal Feed Science and Technology 234, 88–100.
Gastrointestinal functionality in animal nutrition and health: New opportunities for sustainable animal production.Crossref | GoogleScholarGoogle Scholar |

Celi P, Verlhac V, Estefania PC, Schmeisser J, Kluenter A-M (2019) Biomarkers of gastrointestinal functionality in animal nutrition and health. Animal Feed Science and Technology 250, 9–31.
Biomarkers of gastrointestinal functionality in animal nutrition and health.Crossref | GoogleScholarGoogle Scholar |

Diana A, Boyle LA, Leonard FC, Carroll C, Sheehan E, Murphy D, Manzanilla EG (2019) Removing prophylactic antibiotics from pig feed: how does it affect their performance and health? BMC Veterinary Research 15, 67
Removing prophylactic antibiotics from pig feed: how does it affect their performance and health?Crossref | GoogleScholarGoogle Scholar | 30808361PubMed |

Dunshea FR (2001) Sexual dimorphism in growth of sucking and growing pigs. Asian-Australasian Journal of Animal Sciences 14, 1610–1615.
Sexual dimorphism in growth of sucking and growing pigs.Crossref | GoogleScholarGoogle Scholar |

Dunshea FR, Kerton DJ, Cranwell PD, Campbell RG, Mullan BP, King RH, Pluske JR (2002) Interactions between weaning age, weaning weight, sex and enzyme supplementation on growth performance of pigs. Australian Journal of Agricultural Research 53, 939–945.
Interactions between weaning age, weaning weight, sex and enzyme supplementation on growth performance of pigs.Crossref | GoogleScholarGoogle Scholar |

Dunshea FR, Kerton DJ, Cranwell PD, Campbell RG, Mullan BP, King RH, Pluske JR (2003) Lifetime and post-weaning determinants of performance indices of pigs. Australian Journal of Agricultural Research 54, 363–370.
Lifetime and post-weaning determinants of performance indices of pigs.Crossref | GoogleScholarGoogle Scholar |

Fouhse JM, Zijlstra RT, Willing BP (2016) The role of gut microbiota in the health and disease of pigs. Animal Frontiers 6, 30–36.
The role of gut microbiota in the health and disease of pigs.Crossref | GoogleScholarGoogle Scholar |

Gimsa U, Tuchscherer M, Kanitz E (2018) Psychosocial stress and immunity: what can we learn from pig studies? Frontiers in Behavioral Neuroscience 12, 64
Psychosocial stress and immunity: what can we learn from pig studies?Crossref | GoogleScholarGoogle Scholar | 29666573PubMed |

de Groot J, Ruis MAW, Scholten JW, Koolhaas JM, Boersma WJA (2001) Long-term effects of social stress on antiviral immunity in pigs. Physiology & Behavior 73, 145–158.
Long-term effects of social stress on antiviral immunity in pigs.Crossref | GoogleScholarGoogle Scholar |

Guevarra RB, Hong SH, Cho JH, Kim BR, Shin J, Lee JH, Kang BN, Kim YH, Wattanaphansak S, Isaacson RE, Song M, Kim HB (2018) The dynamics of the piglet gut microbiome during the weaning transition in association with health and nutrition. Journal of Animal Science and Biotechnology 9, 54
The dynamics of the piglet gut microbiome during the weaning transition in association with health and nutrition.Crossref | GoogleScholarGoogle Scholar | 30069307PubMed |

Haleem DJ, Kennett G, Curzon G (1988) Adaptation of female rats to stress: shift to male pattern by inhibition of corticosterone synthesis. Brain Research 458, 339–347.
Adaptation of female rats to stress: shift to male pattern by inhibition of corticosterone synthesis.Crossref | GoogleScholarGoogle Scholar | 2463050PubMed |

Heinsbroek RP, Van Haaren F, Feenstra MG, Endert E, Van de Poll NE (1991) Sex- and time-dependent changes in neurochemical and hormonal variables induced by predictable and unpredictable footshock. Physiology & Behavior 49, 1251–1256.
Sex- and time-dependent changes in neurochemical and hormonal variables induced by predictable and unpredictable footshock.Crossref | GoogleScholarGoogle Scholar |

Hennig-Pauka I, Menzel A, Boehme TR, Schierbaum H, Ganter M, Schulz J (2019) Haptoglobin and C-reactive protein: non-specific markers for nursery conditions in swine. Frontiers in Veterinary Science 6, 92
Haptoglobin and C-reactive protein: non-specific markers for nursery conditions in swine.Crossref | GoogleScholarGoogle Scholar | 31001544PubMed |

Hwang H-S, Lee J-K, Eom T-K, Son S-H, Hong J-K, Kim K-H, Rhim S-J (2016) Behavioral characteristics of weaned piglets mixed in different groups. Asian–Australasian Journal of Animal Sciences 29, 1060–1064.
Behavioral characteristics of weaned piglets mixed in different groups.Crossref | GoogleScholarGoogle Scholar | 26954152PubMed |

Jayaraman B, Nyachoti CM (2017) Husbandry practices and gut health outcomes in weaned piglets: a review. Animal Nutrition 3, 205–211.
Husbandry practices and gut health outcomes in weaned piglets: a review.Crossref | GoogleScholarGoogle Scholar | 29767154PubMed |

Kamphuis PJ, Bakker JM, Broekhoven MH, Kunne C, Croiset G, Lentjes EG, Tilders FJ, van Bel F, Wiegant VM (2002) Enhanced glucocorticoid feedback inhibition of hypothalamo–pituitary–adrenal responses to stress in adult rats neonatally treated with dexamethasone. Neuroendocrinology 76, 158–169.
Enhanced glucocorticoid feedback inhibition of hypothalamo–pituitary–adrenal responses to stress in adult rats neonatally treated with dexamethasone.Crossref | GoogleScholarGoogle Scholar | 12218348PubMed |

Kitay JI (1961) Sex differences in adrenal cortical secretion in the rat. Endocrinology 68, 818–824.
Sex differences in adrenal cortical secretion in the rat.Crossref | GoogleScholarGoogle Scholar | 13756461PubMed |

Kitay JI (1963) Pituitary-adrenal function in the rat after gonadectomy and gonadal hormone replacement. Endocrinology 73, 253–260.
Pituitary-adrenal function in the rat after gonadectomy and gonadal hormone replacement.Crossref | GoogleScholarGoogle Scholar | 14076206PubMed |

Kogut MH, Arsenault RJ (2016) Editorial: gut health: the new paradigm in food animal production. Frontiers in Veterinary Science 3, 71
Editorial: gut health: the new paradigm in food animal production.Crossref | GoogleScholarGoogle Scholar | 27630994PubMed |

Lallès JP, Bosi P, Smidt H, Stokes CR (2007a) Nutritional management of gut health in pigs around weaning. The Proceedings of the Nutrition Society 66, 260–268.
Nutritional management of gut health in pigs around weaning.Crossref | GoogleScholarGoogle Scholar | 17466106PubMed |

Lallès J-P, Bosi P, Smidt H, Stokes CR (2007b) Weaning: a challenge to gut physiologists. Livestock Science 108, 82–93.
Weaning: a challenge to gut physiologists.Crossref | GoogleScholarGoogle Scholar |

Li Y, Cai HY, Liu GH, Dong XL, Chang WH, Zhang S, Zheng AJ, Chen GL (2009) Effects of stress simulated by dexamethasone on jejunal glucose transport in broilers. Poultry Science 88, 330–337.
Effects of stress simulated by dexamethasone on jejunal glucose transport in broilers.Crossref | GoogleScholarGoogle Scholar | 19151348PubMed |

Li Y, Song Z, Kerr KA, Moeser AJ (2017) Chronic social stress in pigs impairs intestinal barrier and nutrient transporter function, and alters neuro-immune mediator and receptor expression. PLoS ONE 12, e0171617
Chronic social stress in pigs impairs intestinal barrier and nutrient transporter function, and alters neuro-immune mediator and receptor expression.Crossref | GoogleScholarGoogle Scholar | 29281706PubMed |

Mackey EM, Ayyadurai S, Pohl CS, D’Costa S, Li Y, Moeser AJ (2016) Sexual dimorphism in the mast cell transcriptome and the pathophysiological responses to immunological and psychological stress. Biology of Sex Differences 7, 60
Sexual dimorphism in the mast cell transcriptome and the pathophysiological responses to immunological and psychological stress.Crossref | GoogleScholarGoogle Scholar |

McLamb BL, Gibson AJ, Overman EL, Stahl CH, Moeser AJ (2013) Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli challenge and exacerbates intestinal injury and clinical disease. PLoS One 8, e59838
Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli challenge and exacerbates intestinal injury and clinical disease.Crossref | GoogleScholarGoogle Scholar | 23637741PubMed |

Medland JE, Pohl CS, Edwards LL, Frandsen S, Bagley K, Li Y, Moeser AJ (2016) Early life adversity in piglets induces long-term upregulation of the enteric cholinergic nervous system and heightened, sex-specific secretomotor neuron responses. Neurogastroenterology and Motility 28, 1317–1329.
Early life adversity in piglets induces long-term upregulation of the enteric cholinergic nervous system and heightened, sex-specific secretomotor neuron responses.Crossref | GoogleScholarGoogle Scholar | 27134125PubMed |

Mereu A, Tedó G, Moeser AJ, Rimbach G, Ipharraguerre IR (2015) Cromolyn-mediated improvement of intestinal barrier function is associated with enhanced piglet performance after weaning. BMC Veterinary Research 11, 274
Cromolyn-mediated improvement of intestinal barrier function is associated with enhanced piglet performance after weaning.Crossref | GoogleScholarGoogle Scholar | 26510713PubMed |

Primary Industries Standing Committee (2008) ‘Model code of practice for the welfare of animals: pigs.’ 3rd edn. PISC report no. 92. (CSIRO Publishing: Melbourne)

Moeser AJ, Ryan KA, Nighot PK, Blikslager AT (2007) Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs. American Journal of Physiology. Gastrointestinal and Liver Physiology 293, G413–G421.
Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs.Crossref | GoogleScholarGoogle Scholar | 17525151PubMed |

Moeser AJ, Pohl CS, Rajput M (2017) Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs. Animal Nutrition 3, 313–321.
Weaning stress and gastrointestinal barrier development: Implications for lifelong gut health in pigs.Crossref | GoogleScholarGoogle Scholar | 29767141PubMed |

Pluske JR, Hampson DJ, Williams IH (1997) Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215–236.
Factors influencing the structure and function of the small intestine in the weaned pig: a review.Crossref | GoogleScholarGoogle Scholar |

Pluske JR, Pethick DW, Hopwood DE, Hampson DJ (2002) Nutritional influences on some major enteric bacterial diseases of pigs. Nutrition Research Reviews 15, 333–371.
Nutritional influences on some major enteric bacterial diseases of pigs.Crossref | GoogleScholarGoogle Scholar | 19087411PubMed |

Pluske JR, Kerton DJ, Cranwell PD, Campbell RG, Mullan BP, King RH, Power GN, Pierzynowski SG, Westrom B, Rippe C, Peulen O, Dunshea FR (2003) Age, sex and weight at weaning influence the physiological and gastrointestinal development of weanling pigs. Australian Journal of Agricultural Research 54, 515–527.
Age, sex and weight at weaning influence the physiological and gastrointestinal development of weanling pigs.Crossref | GoogleScholarGoogle Scholar |

Pluske JR, Kim JC, Black JR (2018a) Manipulating the immune system for pigs to optimise performance. Animal Production Science 58, 666–680.
Manipulating the immune system for pigs to optimise performance.Crossref | GoogleScholarGoogle Scholar |

Pluske JR, Turpin DL, Kim JC (2018b) Gastrointestinal tract (gut) health in the young pig. Animal Nutrition 4, 187–196.
Gastrointestinal tract (gut) health in the young pig.Crossref | GoogleScholarGoogle Scholar | 30140758PubMed |

Pohl CS, Medland JE, Moeser AJ (2015) Early-life stress origins of gastrointestinal disease: animal models, intestinal pathophysiology, and translational implications. American Journal of Physiology, Gastrointestinal and Liver Physiology 309, G927–G941.
Early-life stress origins of gastrointestinal disease: animal models, intestinal pathophysiology, and translational implications.Crossref | GoogleScholarGoogle Scholar | 26451004PubMed |

Pohl CS, Medland JE, Mackey E, Edwards LL, Bagley KD, Dewilde MP, Williams KJ, Moeser AJ (2017) Early weaning stress induces chronic functional diarrhea, intestinal barrier defects, and increased mast cell activity in a porcine model of early life adversity. Neurogastroenterology and Motility 29, e13118
Early weaning stress induces chronic functional diarrhea, intestinal barrier defects, and increased mast cell activity in a porcine model of early life adversity.Crossref | GoogleScholarGoogle Scholar | 28573751PubMed |

Rault JL, Lawrence AJ, Ralph CR (2018) Brain-derived neurotrophic factor in serum as an animal welfare indicator of environmental enrichment in pigs. Domestic Animal Endocrinology 65, 67–70.
Brain-derived neurotrophic factor in serum as an animal welfare indicator of environmental enrichment in pigs.Crossref | GoogleScholarGoogle Scholar | 30007130PubMed |

Regitz-Zagrosek V (2012) Sex and gender differences in health. EMBO Reports 13, 596–603.
Sex and gender differences in health.Crossref | GoogleScholarGoogle Scholar | 22699937PubMed |

Roy C (2017) ‘Optimize nursery space allowance for good start.’ National Hog Farmer. Available at https://www.nationalhogfarmer.com/animal-health/optimize-nursery-space-allowance-good-start [Verified 15 August 2019]

Rushen J (1987) A difference in weight reduces fighting when unacquainted newly weaned pigs first meet. Canadian Journal of Animal Science 67, 951–960.
A difference in weight reduces fighting when unacquainted newly weaned pigs first meet.Crossref | GoogleScholarGoogle Scholar |

Shah SC, Khalili H, Gower-Rousseau C, Olen O, Benchimol EI, Lynge E, Nielsen KR, Brassard P, Vutcovici M, Bitton A, Bernstein CN, Leddin D, Tamim H, Stefansson T, Loftus EV, Moum B, Tang W, Ng SC, Gearry R, Sincic B, Bell S, Sands BE, Lakatos PL, Végh Z, Ott C, Kaplan GG, Burisch J, Colombel JF (2018) Sex-based differences in incidence of inflammatory bowel diseases: pooled analysis of population-based studies from western countries. Gastroenterology 155, 1079–1089.e3.
Sex-based differences in incidence of inflammatory bowel diseases: pooled analysis of population-based studies from western countries.Crossref | GoogleScholarGoogle Scholar | 29958857PubMed |

Smith F, Clark JE, Overman BL, Tozel CC, Huang JH, Rivier JEF, Blikslager AT, Moeser AJ (2010) Early weaning stress impairs development of mucosal barrier function in the porcine intestine. American Journal of Physiology. Gastrointestinal and Liver Physiology 298, G352–G363.
Early weaning stress impairs development of mucosal barrier function in the porcine intestine.Crossref | GoogleScholarGoogle Scholar | 19926814PubMed |

Squires JE (2010) ‘Applied animal endocrinology.’ 2nd edn. (CABI: Wallingford, UK)

Stojanac N, Stevancevic O, Potkonjak A, Savic B, Stancic I, Vracar V (2014) The impact of space allowance on productivity performance and Salmonella spp. shedding in nursery pigs. Livestock Science 164, 149–153.
The impact of space allowance on productivity performance and Salmonella spp. shedding in nursery pigs.Crossref | GoogleScholarGoogle Scholar |

Tindsley WEC, Lean IJ (1984) Effects on weight range at allocation on production and behaviour in fattening pig groups. Applied Animal Behaviour Science 12, 79–92.
Effects on weight range at allocation on production and behaviour in fattening pig groups.Crossref | GoogleScholarGoogle Scholar |

Turpin DL, Langendijk P, Chen TY, Pluske JR (2016) Intermittent suckling in combination with an older weaning age improves growth, feed intake and aspects of gastrointestinal tract carbohydrate absorption in pigs after weaning. Animals (Basel) 6, 66
Intermittent suckling in combination with an older weaning age improves growth, feed intake and aspects of gastrointestinal tract carbohydrate absorption in pigs after weaning.Crossref | GoogleScholarGoogle Scholar |

Wolter BF, Ellis M, DeDecker JM, Curtis SE, Hollis GR, Shanks RD, Parr EN, Webel DW (2002) Effects of double stocking and weighing frequency on pig performance in wean-to-finish production systems. Journal of Animal Science 80, 1442–1450.
Effects of double stocking and weighing frequency on pig performance in wean-to-finish production systems.Crossref | GoogleScholarGoogle Scholar | 12078723PubMed |

Wooten H, McGlone JJ, Wachtel M, Thompson G, Rakhshandeh AR, Rakhshandeh A (2019) A glucocorticoid receptor agonist improves post-weaning growth performance in segregated early-weaned pigs. Animal 10, 1–10.
A glucocorticoid receptor agonist improves post-weaning growth performance in segregated early-weaned pigs.Crossref | GoogleScholarGoogle Scholar |

Yoshimura S, Sakamoto S, Kudo H, Sassa S, Kumai A, Okamoto R (2003) Sex-differences in adrenocortical responsiveness during development in rats. Steroids 68, 439–445.
Sex-differences in adrenocortical responsiveness during development in rats.Crossref | GoogleScholarGoogle Scholar | 12798494PubMed |