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Fish Oil and Olive Oil Supplementation in Late Pregnancy and Lactation Differentially Affect Oxidative Stress and Inflammation in Sows and Piglets

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Lipids

Abstract

This study was conducted to compare the effects of fish oil and olive oil supplementation in late pregnancy and during lactation on oxidative stress and inflammation in sows and their piglets. A total of 24 sows were fed a basal diet supplemented with additional corn starch (CON), fish oil (FO) or olive oil (OO). Sows fed an OO diet during late gestation had a higher piglet birth weight compared with CON-fed and FO-fed sows (P < 0.05). Furthermore, sows from the OO group had a higher milk fat content than sows from CON and FO groups, and a lower pre-weaning mortality of piglets was observed in the OO group (P < 0.05). Maternal FO supplementation resulted in increased malondialdehyde concentration in sow plasma, colostrum, milk and piglet plasma than in CON and OO groups (P < 0.05). However, an increased total antioxidant capacity (T-ACC) and activities of glutathione peroxidase (GSH-Px) and total superoxide dismutase (T-SOD) were also observed in the FO group (P < 0.05). Sows fed an OO diet had significantly decreased interleukin-1β (IL-1β), interleukin-6 (IL-6) and tumor necrosis factor-α (TNF-α) concentrations in milk compared with CON and FO fed sows (P < 0.05). Moreover, lower plasma IL-1β and TNF-α levels were observed in piglets from the OO group compared with the CON group (P < 0.05). Collectively, these results suggest that an OO diet is most beneficial in late gestation and during lactation in sows. However, FO increases the susceptibility to oxidative stress in sows and piglets.

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Abbreviations

CON:

Control

CP:

Crude Protein

DE:

Digestible Energy

DHA:

Docosahexaenoic acid (C22:6n-3)

EPA:

Eicosapentaenoic acid (C20:5n-3)

FO:

Fish oil

GSH-Px:

Glutathione peroxidase

IL-1β:

Interleukin-1β

IL-6:

Interleukin-6

MDA:

Malondialdehyde

MUFA:

Monounsaturated fatty acid

OO:

Olive oil

PUFA:

Polyunsaturated fatty acid

T-AOC:

Total antioxidant capacity

T-SOD:

Total superoxide dismutase

TNF-α:

Tumor necrosis factor -alpha

References

  1. Herrera E, Ortega-Senovilla H (2010) Maternal lipid metabolism during normal pregnancy and its implications to fetal development. Clin Lipodol 5:899–911

    Article  CAS  Google Scholar 

  2. Kim SW, Weaver AC, Shen YB, Zhao Y (2013) Improving efficiency of sow productivity: nutrition and health. J Anim Sci Biotechnol 4:26

    Article  PubMed Central  PubMed  Google Scholar 

  3. Berchieri-Ronchi CB, Kim SW, Zhao Y, Correa CR, Yeum KJ, Ferreira AL (2011) Oxidative stress status of highly prolific sows during gestation and lactation. Animal 5:1774–1779

    Article  CAS  PubMed  Google Scholar 

  4. Cindrova-Davies T, Yung HW, Johns J, Spasic-Boskovic O, Korolchuk S, Jauniaux E, Burton GJ, Charnock-Jones DS (2007) Oxidative stress, gene expression, and protein changes induced in the human placenta during labor. Am J Pathol 171:1168–1179

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  5. Osman I, Young A, Ledingham M, Thomson A, Jordan F, Greer I, Norman J (2003) Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol Hum Reprod 9:41–45

    Article  CAS  PubMed  Google Scholar 

  6. Agarwal A, Gupta S, Sharma RK (2005) Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 3:1–21

    Article  CAS  Google Scholar 

  7. Jabbour HN, Sales KJ, Catalano RD, Norman JE (2009) Inflammatory pathways in female reproductive health and disease. Reproduction 138:903–919

    Article  CAS  PubMed  Google Scholar 

  8. de la Puerta R, Marquez-Martin A, Fernandez-Arche A, Ruiz-Gutierrez V (2009) Influence of dietary fat on oxidative stress and inflammation in murine macrophages. Nutrition 25:548–554

    Article  PubMed  Google Scholar 

  9. Salas-Salvado J, Garcia-Arellano A, Estruch R, Marquez-Sandoval F, Corella D, Fiol M, Gomez-Gracia E, Vinoles E, Aros F, Herrera C, Lahoz C, Lapetra J, Perona JS, Munoz-Aguado D, Martinez-Gonzalez MA, Ros E (2008) Components of the Mediterranean-type food pattern and serum inflammatory markers among patients at high risk for cardiovascular disease. Eur J Clin Nutr 62:651–659

    Article  CAS  PubMed  Google Scholar 

  10. Mena MP, Sacanella E, Vazquez-Agell M, Morales M, Fito M, Escoda R, Serrano-Martinez M, Salas-Salvado J, Benages N, Casas R, Lamuela-Raventos RM, Masanes F, Ros E, Estruch R (2009) Inhibition of circulating immune cell activation: a molecular antiinflammatory effect of the Mediterranean diet. Am J Clin Nutr 89:248–256

    Article  CAS  PubMed  Google Scholar 

  11. Leonard SG, Sweeney T, Bahar B, Lynch BP, O’Doherty JV (2010) Effect of maternal fish oil and seaweed extract supplementation on colostrum and milk composition, humoral immune response, and performance of suckled piglets. J Anim Sci 88:2988–2997

    Article  CAS  PubMed  Google Scholar 

  12. Hornstra G (2000) Essential fatty acids in mothers and their neonates. Am J Clin Nutr 71(suppl):1262S–1269S

    CAS  PubMed  Google Scholar 

  13. Rooke JA, Sinclair AG, Edwards SA (2001) Feeding tuna oil to the sow at different times during pregnancy has different effects on piglet long-chain polyunsaturated fatty acid composition at birth and subsequent growth. Br J Nutr 86:21–30

    Article  CAS  PubMed  Google Scholar 

  14. Esposito K, Marfella R, Ciotola M, Di Palo C, Giugliano F, Giugliano G, D’Armiento M, D’Andrea F, Giugliano D (2004) Effect of a Mediterranean-style diet on endothelial dysfunction and markers of vascular inflammation in the metabolic syndrome: a randomized trial. JAMA 292:1440–1446

    Article  CAS  PubMed  Google Scholar 

  15. Mataix J, Battino M, Ramirez-Tortosa MC, Bertoli E, Quiles JL (2008) Virgin olive oil: a key healthy component of the Mediterranean diet. Mediterr J Nutr Metab 1:69–75

    Article  Google Scholar 

  16. Tripoli E, Giammanco M, Tabacchi G, Di Majo D, Giammanco S, La Guardia M (2005) The phenolic compounds of olive oil: structure, biological activity and beneficial effects on human health. Nutr Res Rev 18:98–112

    Article  CAS  PubMed  Google Scholar 

  17. Tanghe S, Millet S, De Smet S (2013) Echium oil and linseed oil as alternatives for fish oil in the maternal diet: blood fatty acid profiles and oxidative status of sows and piglets. J Anim Sci 91:3253–3264

    Article  CAS  PubMed  Google Scholar 

  18. Li H, Wan HF, Mercier Y, Zhang XL, Wu CM, Wu XQ, Tang L, Che LQ, Lin Y, Xu SY, Tian G, Wu D, Fang ZF (2014) Changes in plasma amino acid profiles, growth performance and intestinal antioxidant capacity of piglets following increased consumption of methionine as its hydroxy analogue. Br J Nutr 112:855–867

    Article  CAS  PubMed  Google Scholar 

  19. Folch J, Lees M, Sloane-Stanley GH (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  20. Molina MT, Vazquez CM, Ruiz-Gutierrez V (1989) Changes in both acyl-CoA: cholesterol acyltransferase activity and microsomal lipid com-position in rat liver induced by distal small-bowel resection. Biochem J 260:115–119

    CAS  PubMed Central  PubMed  Google Scholar 

  21. Grotto D, Santa Maria LD, Boeira S, Valentini J, Charão MF, Moro AM, Nascimento PC, Pomblum VJ, Garcia SC (2007) Rapid quantification of malondialdehyde in plasma by high performance liquid chromatography–visible detection. J Pharm Biomed Anal 43:619–624

    Article  CAS  PubMed  Google Scholar 

  22. Hu H, Wang M, Zhan X, Li X, Zhao R (2011) Effect of different selenium sources on productive performance, serum and milk Se concentrations, and antioxidant status of sows. Biol Trace Elem Res 142:471–480

    Article  CAS  PubMed  Google Scholar 

  23. Hernández P, Zomeño L, Ariño B, Blasco A (2004) Antioxidant, lipolytic and proteolytic enzyme activities in pork meat from different genotypes. Meat Sci 66:525–529

    Article  PubMed  Google Scholar 

  24. Yin J, Wu MM, Xiao H, Ren WK, Duan JL, Yang G, Li TJ, Yin YL (2013) Development of an antioxidant system after early weaning in piglets. J Anim Sci 92:612–619

    Article  PubMed  Google Scholar 

  25. Laws J, Litten JC, Laws A, Lean IJ, Dodds PF, Clarke L (2009) Effect of type and timing of oil supplements to sows during pregnancy on the growth performance and endocrine profile of low and normal birth weight offspring. Br J Nutr 101:240–249

    Article  CAS  PubMed  Google Scholar 

  26. Schwartz GJ, Fu J, Astarita G, Li X, Gaetani S, Campolongo P, Piomelli D (2008) The lipid messenger OEA links dietary fat intake to satiety. Cell Metab 8:281–288

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  27. Diep TA, Madsen AN, Holst B, Kristiansen MM, Wellner N, Hansen SH, Hansen HS (2011) Dietary fat decreases intestinal levels of the anorectic lipids through a fat sensor. FASEB J 25:765–774

    Article  CAS  PubMed  Google Scholar 

  28. De Fonseca FR, Navarro M, Gomez R, Escuredo L, Nava F, Fu J, Piomelli D (2001) An anorexic lipid mediator regulated by feeding. Nature 414:209–212

    Article  Google Scholar 

  29. Cools A, Maes D, Papadopoulos G, Vandermeiren JA, Meyer E, Demeyere K, De Smet S, Janssens GP (2011) Dose-response effect of fish oil substitution in parturition feed on erythrocyte membrane characteristics and sow performance. J Anim Physiol Anim Nutr (Berl) 95:125–136

    Article  CAS  Google Scholar 

  30. González-Ortiz G, Sala R, Canovas E, Abed N, Barroeta AC (2013) Consumption of dietary n-3 fatty acids decreases fat deposition and adipocyte size, but increases oxidative susceptibility in broiler chickens. Lipids 48:705–717

    Article  PubMed  Google Scholar 

  31. García-Rodríguez CE, Helmersson-Karlqvist J, Dolores Mesa M, Miles EA, Noakes PS, Vlachava M, Kremmyda L, Diaper ND, Godfrey KM, Calder PC (2011) Does increased intake of salmon increase markers of oxidative stress in pregnant women? The Salmon in Pregnancy Study. Antioxid Redox Sign 15:2819–2823

    Article  Google Scholar 

  32. Anjum FM, Haider MF, Khan MI, Sohaib M, Arshad MS (2013) Impact of extruded flaxseed meal supplemented diet on growth performance, oxidative stability and quality of broiler meat and meat products. Lipids Health Dis 12:13

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Nguyen TV, Yuan L, Azevedo MS, Jeong KI, González AM, Saif LJ (2007) Transfer of maternal cytokines to suckling piglets: in vivo and in vitro models with implications for immunomodulation of neonatal immunity. Vet Immunol Immunopathol 117:236–248

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Leme AS, Hubeau C, Xiang Y, Goldman A, Hamada K, Suzaki Y, Kobzik L (2006) Role of breast milk in a mouse model of maternal transmission of asthma susceptibility. J Immunol 176:762–769

    Article  CAS  PubMed  Google Scholar 

  35. Ustundag B, Yilmaz E, Dogan Y, Akarsu S, Canatan H, Halifeoglu I, Aygun AD (2005) Levels of cytokines (IL-1 β, IL-2, IL-6, IL-8, TNF-α) and trace elements (Zn, Cu) in breast milk from mothers of preterm and term Infants. Mediat Inflamm 2005:331–336

    Article  Google Scholar 

  36. Field CJ (2005) The immunological components of human milk and their effect on immune development in infants. J Nutr 135:1–4

    CAS  PubMed  Google Scholar 

  37. Covas MI (2007) Olive oil and the cardiovascular system. Pharmacol Rev 55:175–186

    CAS  Google Scholar 

  38. Covas MI, Konstantinidou V, Fito M (2009) Olive oil and cardiovascular health. J Cardiovasc Pharmacol 54:477–482

    Article  CAS  PubMed  Google Scholar 

  39. Pérez-Jiménez F, Ruano J, Pérez-Martínez P, López-Segura F, López-Miranda J (2007) The influence of olive oil on human health: not a question of fat alone. Mol Nutr Food Res 51:1199–1208

    Article  PubMed  Google Scholar 

  40. Perona JS, Cabello-Moruno R, Ruiz-Gutiérrez V (2006) The role of virgin olive oil components in the modulation of endothelial function. J Nutr Biochem 17:429–445

    Article  CAS  PubMed  Google Scholar 

  41. Miles EA, Zoubouli P, Calder PC (2005) Differential anti-inflammatory effects of phenolic compounds from extra virgin olive oil identified in human whole blood cultures. Nutrition 21:389–394

    Article  CAS  PubMed  Google Scholar 

  42. Cicerale S, Lucas LJ, Keast RSJ (2012) Antimicrobial, antioxidant and anti-inflammatory phenolic activities in extra virgin olive oil. Curr Opin Biotech 23:129–135

    Article  CAS  PubMed  Google Scholar 

  43. Chartrand R, Matte JJ, Lessard M, Chouinard PY, Giguere A, Laforest JP (2003) Effect of dietary fat sources on systemic and intrauterine synthesis of prostaglandins during early pregnancy in gilts. J Anim Sci 81:726–734

    CAS  PubMed  Google Scholar 

  44. Bosco N, Brahmbhatt V, Oliveira M, Martin FP, Lichti P, Raymond F, Mansourian R, Metairon S, Pace-Asciak C, Bastic SV, Rezzi S, Haller D, Benyacoub J (2013) Effects of increase in fish oil intake on intestinal eicosanoids and inflammation in a mouse model of colitis. Lipids Health Dis 12:81

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. González-Périz A, Horrillo R, Ferré N, Gronert K, Dong B, Morán-Salvador E, Clària J (2009) Obesity-induced insulin resistance and hepatic steatosis are alleviated by ω-3 fatty acids: a role for resolvins and protectins. FASEB J 23:1946–1957

    Article  PubMed Central  PubMed  Google Scholar 

  46. González-Périz A, Planagumà A, Gronert K, Miquel R, López-Parra M, Titos E, Clària J (2006) Docosahexaenoic acid (DHA) blunts liver injury by conversion to protective lipid mediators: protectin D1 and 17S-hydroxy-DHA. FASEB J 20:2537–2539

    Article  PubMed  Google Scholar 

  47. Edwards IJ, O’Flaherty JT (2008) Omega-3 fatty acids and PPARγ in cancer. PPAR research 2008: 358052–358052

  48. Jump DB (2002) The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem 277:8755–8758

    Article  CAS  PubMed  Google Scholar 

  49. Vaisman N, Zaruk Y, Shirazi I, Kaysar N, Barak V (2005) The effect of fish oil supplementation on cytokine production in children. Eur Cytokine Netw 16:194–198

    CAS  PubMed  Google Scholar 

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Acknowledgments

The present study was supported by National Key Technology Support Program (2012BAD39B00), Academy of Kechuang Feed Industry in Sichuan (2013NZ0056), Research Team of Youth Scientific and Technical Innovation of Sichuan (13CXTD0004), Program for Changjiang Scholars and Innovative Research Team in University (IRT13083).

Conflict of interest

All authors have no conflict of interest in connection with this manuscript.

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    Authors and Affiliations

    1. Key Laboratory for Animal Disease-Resistance Nutrition of the Ministry of Agriculture of China, Institute of Animal Nutrition, Sichuan Agricultural University, Ya′an, 625014, Sichuan, China

      Yong Shen, Haifeng Wan, Jiatao Zhu, Zhengfeng Fang, Lianqiang Che, Shengyu Xu, Yan Lin, Jian Li & De Wu

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    1. Yong Shen
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    Correspondence to De Wu.

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    Y. Shen and H. Wan contributed equally to this work.

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    Shen, Y., Wan, H., Zhu, J. et al. Fish Oil and Olive Oil Supplementation in Late Pregnancy and Lactation Differentially Affect Oxidative Stress and Inflammation in Sows and Piglets. Lipids 50, 647–658 (2015). https://doi.org/10.1007/s11745-015-4024-x

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