Fishmeal supplementation during ovine pregnancy and lactation protects against maternal stress-induced programming of the offspring immune system

BMC Veterinary Research

Niel A. Karrow¹  Timothy R. H. Regnault²  Brian W. McBride¹  Herman J. Boermans³  Margaret Quinton¹  Ousama AlZahal¹  Mamun M. Or’Rashid¹  Rebecca E. Fisher-Heffernan¹ 

[1] Department of Animal and Poultry Science, University of Guelph, 50 Stone Road East, Building 70, Guelph, Canada;Department of Physiology and Pharmacology, Western University, London, ON, Canada;Department of Biomedical Sciences, University of Guelph, Guelph, ON, Canada

关键词: Fetal programming;    Dermal hypersensitivity test;    Sheep;    Fishmeal;   

Others  :  1228767
DOI  :  10.1186/s12917-015-0573-8

 received in 2015-04-28, accepted in 2015-10-05,  发布年份 2015

【 摘 要 】

Background

Prenatally stressed offspring exhibit increased susceptibility to inflammatory disorders due to in utero programming. Research into the effects of n-3 PUFAs shows promising results for the treatment and prevention of these disorders. The purpose of this study was to investigate whether maternal fishmeal supplementation during pregnancy and lactation protects against programming of the offspring’s immune response following simulated maternal infection.

Methods

In order to accomplish this, 53 ewes were fed a diet supplemented with fishmeal (FM; rich in n-3 PUFA) or soybean meal (SM; rich in n-6 PUFAs) from day 100 of gestation (gd 100) through lactation. On gd135, half the ewes from each dietary group were challenged with either 1.2 μg/kg Escherichia coli lipopolysaccharide (LPS) endotoxin to simulate a bacterial infection, or saline as the control. At 4.5 months of age the offspring’s dermal immune response was assessed by cutaneous hypersensitivity testing with ovalbumin (OVA) and candida albicans (CAA) 21 days after sensitization. Skinfold measurements were taken and serum blood samples were also collected to assess the primary and secondary antibody immune response.

Results

Offspring born to SM + LPS mothers had a significantly greater change in skinfold thickness in response to both antigens as well as a greater secondary antibody response to OVA compared to all treatments.

Conclusions

Supplementation during pregnancy with FM appears to protect against adverse fetal programming that may occur during maternal infection and this may reduce the risk of atopic disease later in life.

【 授权许可】

   
2015 Fisher-Heffernan et al.

【 图 表 】

Fig. 1.

Fig. 2.

【 参考文献 】

• [1]Collier CH, Risnes K, Norwitz ER, Bracken MB, Illuzzi JL. Maternal infection in pregnancy and risk of asthma in offspring. Matern Child Health J. 2013; 17(10):1940-50.
• [2]de Marco R, Pesce G, Girardi P, Marchetti P, Rava M, Ricci P, Marcon A. Foetal exposure to maternal stressful events increases the risk of having asthma and atopic diseases in childhood. Pediatr Allergy Immunol. 2012; 23(8):724-9.
• [3]Mizuno M, Siddique K, Baum M, Smith SA. Prenatal programming of hypertension induces sympathetic overactivity in response to physical stress. Hypertension. 2013; 61(1):180-6.
• [4]King V, Dakin RS, Liu L, Hadoke PW, Walker BR, Seckl JR, Norman JE, Drake AJ. Maternal obesity has little effect on the immediate offspring but impacts on the next generation. Endocrinology. 2013; 154(7):2514-24.
• [5]Entringer S, Buss C, Swanson JM, Cooper DM, Wing DA, Waffarn F, Wadhwa PD. Fetal programming of body composition, obesity, and metabolic function: the role of intrauterine stress and stress biology. J Nutr Metab. 2012; 2012:632548.
• [6]Ornoy A. Prenatal origin of obesity and their complications: gestational diabetes, maternal overweight and the paradoxical effects of fetal growth restriction and macrosomia. Reprod Toxicol. 2011; 32(2):205-12.
• [7]Brew BK, Marks GB. Perinatal factors and respiratory health in children. Clin Exp Allergy. 2012; 42(11):1621-9.
• [8]Duijts L. Fetal and infant origins of asthma. Eur J Epidemiol. 2012; 27(1):5-14.
• [9]Banjanin S, Kapoor A, Matthews SG. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs. J Physiol. 2004; 558(Pt 1):305-18.
• [10]Portha B, Chavey A, Movassat J. Early-life origins of type 2 diabetes: fetal programming of the beta-cell mass. Exp Diabetes Res. 2011; 2011:105076.
• [11]Knackstedt MK, Hamelmann E, Arck PC. Mothers in stress: consequences for the offspring. Am J Reprod Immunol. 2005; 54(2):63-9.
• [12]Nafstad P, Magnus P, Jaakkola JJ. Risk of childhood asthma and allergic rhinitis in relation to pregnancy complications. J Allergy Clin Immunol. 2000; 106(5):867-73.
• [13]Warner JA, Warner JO. Early life events in allergic sensitisation. Br Med Bull. 2000; 56(4):883-93.
• [14]Soto-Ramirez N, Karmaus W, Zhang H, Liu J, Billings D, Gangur V, Amrol D, da Costa KA, Davis S, Goetzl L. Fatty acids in breast milk associated with asthma-like symptoms and atopy in infancy: a longitudinal study. J Asthma. 2012; 49(9):926-34.
• [15]Wright RJ. Prenatal maternal stress and early caregiving experiences: implications for childhood asthma risk. Paediatr Perinat Epidemiol. 2007; 21 Suppl 3:8-14.
• [16]Cookson H, Granell R, Joinson C, Ben-Shlomo Y, Henderson AJ. Mothers’ anxiety during pregnancy is associated with asthma in their children. J Allergy Clin Immunol. 2009; 123(4):847-53.e11.
• [17]Priftis KN, Papadimitriou A, Anthracopoulos MB, Fretzayas A, Chrousos GP. Endocrine-immune interactions in adrenal function of asthmatic children on inhaled corticosteroids. Neuroimmunomodulation. 2009; 16(5):333-9.
• [18]Buske-Kirschbaum A, Ebrecht M, Hellhammer DH. Blunted HPA axis responsiveness to stress in atopic patients is associated with the acuity and severeness of allergic inflammation. Brain Behav Immun. 2010; 24(8):1347-53.
• [19]Coe CL, Kramer M, Kirschbaum C, Netter P, Fuchs E. Prenatal stress diminishes the cytokine response of leukocytes to endotoxin stimulation in juvenile rhesus monkeys. J Clin Endocrinol Metab. 2002; 87(2):675-81.
• [20]Agarwal SK, Marshall GD. Glucocorticoid-induced type 1/type 2 cytokine alterations in humans: a model for stress-related immune dysfunction. J Interferon Cytokine Res. 1998; 18(12):1059-68.
• [21]Foolad N, Brezinski EA, Chase EP, Armstrong AW. Effect of nutrient supplementation on atopic dermatitis in children: a systematic review of probiotics, prebiotics, formula, and fatty acids. JAMA Dermatol. 2013; 149(3):350-5.
• [22]Romero VC, Somers EC, Stolberg V, Clinton C, Chensue S, Djuric Z, Berman DR, Treadwell MC, Vahratian AM, Mozurkewich E. Developmental programming for allergy: a secondary analysis of the Mothers, omega-3, and mental health study. Am J Obstet Gynecol. 2013; 208(4):316.e1-316.e6.
• [23]Pilkington SM, Massey KA, Bennett SP, Al-Aasswad NM, Roshdy K, Gibbs NK, Friedmann PS, Nicolaou A, Rhodes LE. Randomized controlled trial of oral omega-3 PUFA in solar-simulated radiation-induced suppression of human cutaneous immune responses. Am J Clin Nutr. 2013; 97(3):646-52.
• [24]Mizota T, Fujita-Kambara C, Matsuya N, Hamasaki S, Fukudome T, Goto H, Nakane S, Kondo T, Matsuo H. Effect of dietary fatty acid composition on Th1/Th2 polarization in lymphocytes. J Parenter Enteral Nutr. 2009; 33(4):390-6.
• [25]Furuhjelm C, Warstedt K, Larsson J, Fredriksson M, Bottcher MF, Falth-Magnusson K, Duchen K. Fish oil supplementation in pregnancy and lactation may decrease the risk of infant allergy. Acta Paediatr. 2009; 98(9):1461-7.
• [26]Heinzmann A, Mao XQ, Akaiwa M, Kreomer RT, Gao PS, Ohshima K, Umeshita R, Abe Y, Braun S, Yamashita T, Roberts MH, Sugimoto R, Arima K, Arinobu Y, Yu B, Kruse S, Enomoto T, Dake Y, Kawai M, Shimazu S, Sasaki S, Adra CN, Kitaichi M, Inoue H, Yamauchi K, Tomichi N, Kurimoto F, Hamasaki N, Hopkin JM, Izuhara K, Shirakawa T, Deichmann KA. Genetic variants of IL-13 signalling and human asthma and atopy. Hum Mol Genet. 2000; 9(4):549-59.
• [27]D’Vaz N, Meldrum SJ, Dunstan JA, Martino D, McCarthy S, Metcalfe J, Tulic MK, Mori TA, Prescott SL. Postnatal fish oil supplementation in high-risk infants to prevent allergy: randomized controlled trial. Pediatrics. 2012; 130(4):674-82.
• [28]Palmer AJ, Ho CK, Ajibola O, Avenell A. The role of omega-3 fatty acid supplemented parenteral nutrition in critical illness in adults: a systematic review and meta-analysis. Crit Care Med. 2013; 41(1):307-16.
• [29]Or-Rashid MM, Fisher R, Karrow N, AlZahal O, McBride BW. Plasma fatty acid profile of gestating ewes supplemented with fishmeal. Am J Anim Vet Sci. 2012; 7(2):67-74.
• [30]Stryker JA, Fisher R, You Q, Or-Rashid MM, Boermans HJ, Quinton M, McBride BW, Karrow NA. Effects of dietary fish meal and soybean meal on the ovine innate and acquired immune response during pregnancy and lactation. Animal. 2013; 7(1):151-9.
• [31]Wang Z, Goonewardene LA. The use of MIXED models in the analysis of animal experiments with repeated measures data. Can J Anim Sci. 2004; 84:1-11.
• [32]Fisher RE, Or’Rashid M, Quinton M, AlZahal O, Boermans HJ, McBride BW, Karrow NA. Maternal supplementation with fishmeal protects against late gestation endotoxin-induced fetal programming of the ovine hypothalamic-pituitary-adrenal axis. J Dev Orig Health Dis. 2014; 5(3):206-13.
• [33]Ciaccio CE, Girdhar M. Effect of maternal omega3 fatty acid supplementation on infant allergy. Ann Allergy Asthma Immunol. 2014; 112(3):191-4.
• [34]Li J, Xun P, Zamora D, Sood A, Liu K, Daviglus M, Iribarren C, Jacobs D, Shikany JM, He K. Intakes of long-chain omega-3 (n-3) PUFAs and fish in relation to incidence of asthma among American young adults: the CARDIA study. Am J Clin Nutr. 2013; 97(1):173-8.
• [35]Makrides M, Gunaratne AW, Collins CT. Dietary n-3 LC-PUFA during the perinatal period as a strategy to minimize childhood allergic disease. Nestle Nutr Inst Workshop Ser. 2013; 77:155-62.
• [36]Park HJ, Park JS, Hayek MG, Reinhart GA, Chew BP. Dietary fish oil and flaxseed oil suppress inflammation and immunity in cats. Vet Immunol Immunopathol. 2011; 141(3–4):301-6.
• [37]Lauritzen L, Kjaer TM, Porsgaard T, Fruekilde MB, Mu H, Frokiaer H. Maternal intake of fish oil but not of linseed oil reduces the antibody response in neonatal mice. Lipids. 2011; 46(2):171-8.
• [38]de Matos OG, Amaral SS, Pereira da Silva PE, Perez DA, Alvarenga DM, Ferreira AV, Alvarez-Leite J, Menezes GB, Cara DC. Dietary supplementation with omega-3-PUFA-rich fish oil reduces signs of food allergy in ovalbumin-sensitized mice. Clin Dev Immunol. 2012; 2012:236564.
• [39]Warstedt K, Furuhjelm C, Duchen K, Falth-Magnusson K, Fageras M. The effects of omega-3 fatty acid supplementation in pregnancy on maternal eicosanoid, cytokine, and chemokine secretion. Pediatr Res. 2009; 66(2):212-7.
• [40]Dunstan JA, Mori TA, Barden A, Beilin LJ, Taylor AL, Holt PG, Prescott SL. Fish oil supplementation in pregnancy modifies neonatal allergen-specific immune responses and clinical outcomes in infants at high risk of atopy: a randomized, controlled trial. J Allergy Clin Immunol. 2003; 112(6):1178-84.
• [41]Bazinet RP, Douglas H, McMillan EG, Wilkie BN, Cunnane SC. Dietary 18:3omega3 influences immune function and the tissue fatty acid response to antigens and adjuvant. Immunol Lett. 2004; 95(1):85-90.
• [42]Vineyard KR, Warren LK, Kivipelto J. Effect of dietary omega-3 fatty acid source on plasma and red blood cell membrane composition and immune function in yearling horses. J Anim Sci. 2010; 88(1):248-57.
• [43]Gottrand F. Long-chain polyunsaturated fatty acids influence the immune system of infants. J Nutr. 2008; 138(9):1807S-12.
• [44]Han SC, Kang GJ, Ko YJ, Kang HK, Moon SW, Ann YS, Yoo ES. Fermented fish oil suppresses T helper 1/2 cell response in a mouse model of atopic dermatitis via generation of CD4 + CD25 + Foxp3+ T cells. BMC Immunol. 2012; 13:44.
• [45]Robinson DS. The role of regulatory T lymphocytes in asthma pathogenesis. Curr Allergy Asthma Rep. 2005; 5(2):136-41.
• [46]Saito S, Nakashima A, Shima T, Ito M. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol. 2010; 63(6):601-10.
• [47]Chau JT. The effect of prenatal stress on a mouse model of allergic airway disease. 2013.
• [48]Prescott SL, Clifton V. Asthma and pregnancy: emerging evidence of epigenetic interactions in utero. Curr Opin Allergy Clin Immunol. 2009; 9(5):417-26.
• [49]Yessoufou A, Ple A, Moutairou K, Hichami A, Khan NA. Docosahexaenoic acid reduces suppressive and migratory functions of CD4 + CD25+ regulatory T-cells. J Lipid Res. 2009; 50(12):2377-88.
• [50]Seymour BW, Friebertshauser KE, Peake JL, Pinkerton KE, Coffman RL, Gershwin LJ. Gender differences in the allergic response of mice neonatally exposed to environmental tobacco smoke. Dev Immunol. 2002; 9(1):47-54.
• [51]Melgert BN, Postma DS, Kuipers I, Geerlings M, Luinge MA, van der Strate BW, Kerstjens HA, Timens W, Hylkema MN. Female mice are more susceptible to the development of allergic airway inflammation than male mice. Clin Exp Allergy. 2005; 35(11):1496-503.
• [52]Or-Rashid MM, Fisher R, Karrow N, AlZahal O, McBride BW. Fatty acid profile of colostrum and milk of ewes supplemented with fish meal and the subsequent plasma fatty acid status of their lambs. J. Anim. Sci. 2010; 88:2092-2102.