Register      Login
Reproduction, Fertility and Development Reproduction, Fertility and Development Society
Vertebrate reproductive science and technology
RESEARCH ARTICLE

Substitution of starch for palm oil during gestation: impact on offspring survival and hepatic gene expression in the pig

K. L. Almond A E , H. P. Fainberg D , M. A. Lomax B , P. Bikker C F , M. E. Symonds A and A. Mostyn D G
+ Author Affiliations
- Author Affiliations

A Early Life Nutrition Research Unit, Academic Child Health, Obsetrics and Gynaecology, School of Medicine, University Hospital, The University of Nottingham, Nottingham, NG7 2UH, UK.

B Division of Nutritional Sciences, School of Biosciences, Sutton Bonington Campus, University of Nottingham, LE12 5RD, UK.

C Schothorst Feed Research, Meerkoetenweg 26, 8218 Lelystad, PO Box 533, 8200 AM Lelystad, The Netherlands.

D School of Veterinary Medicine and Science, Sutton Bonington Campus, University of Nottingham, LE12 5RD, UK.

E Present address: Primary Diets, Melmerby Industrial Estate, Melmerby, Ripon, North Yorkshire, HG4 5HP, UK.

F Present address: Wageningen UR Livestock Research, PO Box 338, 6700 AH Wageningen, The Netherlands.

G Corresponding author. Email: alison.mostyn@nottingham.ac.uk

Reproduction, Fertility and Development 27(7) 1057-1064 https://doi.org/10.1071/RD14058
Submitted: 4 July 2013  Accepted: 5 March 2014   Published: 10 April 2014

Abstract

Piglet neonatal mortality rates are high (~20%), so nutritional strategies to reduce this are highly desirable. Maternal fat substitution (FS) may promote the preweaning survival of piglets by improving their energy status. Therefore, the aim of the present study was to investigate the effects of FS throughout pregnancy on offspring viability, together with the gene expression of stress-related markers in the liver. Sixteen pregnant sows were randomly allocated to one of two isocaloric diets, control (C) or FS in the form of palm oil, fed from 0 to 110 days gestation. Glucose tolerance was examined on Day 108. Median and low birthweight offspring were allocated to tissue sampling at either 7 days or 6 months postnatal age. In response to a glucose tolerance test, FS sows exhibited a raised glucose area under the curve with no change in basal glucose. Average piglet mortality (up to Day 28) was increased fourfold in the FS group, with surviving median-sized piglets exhibiting significantly lower fatty acid binding protein 1 (FABP1) expression at 7 days. There were no effects on the abundance of any other stress- or metabolic-related genes examined. Thus, this study demonstrates that maternal FS throughout gestation causes maternal glucose intolerance that may be linked to the observed increase in piglet mortality. However, the surviving offspring do not exhibit any detectable differences in postnatal growth or hepatic gene profile in later life.

Additional keywords: development, liver, nutrition, pregnancy.


References

Armitage, J. A., Taylor, P. D., and Poston, L. (2005). Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J. Physiol. 565, 3–8.
Experimental models of developmental programming: consequences of exposure to an energy rich diet during development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXkslyrurk%3D&md5=f85fa6c8dcacb86bd1f1bbd974b732c2CAS | 15695245PubMed |

Azain, M. J. (1993). Effects of adding medium-chain triglycerides to sow diets during late gestation and early lactation on litter performance. J. Anim. Sci. 71, 3011–3019.
| 1:CAS:528:DyaK2cXltlKjsw%3D%3D&md5=945a5990c5ccbfc7290bc9a9717e4b1dCAS | 8270522PubMed |

Binas, B., and Erol, E. (2007). FABPs as determinants of myocellular and hepatic fuel metabolism. Mol. Cell. Biochem. 299, 75–84.
FABPs as determinants of myocellular and hepatic fuel metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXltFSrtL4%3D&md5=86c281cbd2268342614d23f1a26343e6CAS | 17001451PubMed |

Boyd, R. D., Moser, B. D., Peo, E. R., and Cunningham, P. J. (1978). Effect of energy source prior to parturition and during lactation on tissue lipid, liver glycogen and plasma levels of some metabolites in the newborn pig. J. Anim. Sci. 47, 874–882.
| 1:CAS:528:DyaE1MXkvFGj&md5=e660adc3439353a720c7bb9d778dcbf8CAS | 738973PubMed |

Bruce, K. D., Cagampang, F. R., Argenton, M., Zhang, J., Ethirajan, P. L., Burdge, G. C., Bateman, A. C., Clough, G. F., Poston, L., Hanson, M. A., McConnell, J. M., and Byrne, C. D. (2009). Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression. Hepatology 50, 1796–1808.
Maternal high-fat feeding primes steatohepatitis in adult mice offspring, involving mitochondrial dysfunction and altered lipogenesis gene expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1SjurvO&md5=3a1877b03e2af541da270db862e7dc9aCAS | 19816994PubMed |

Burns, C. M., Rutherford, M. A., Boardman, J. P., and Cowan, F. M. (2008). Patterns of cerebral injury and neurodevelopmental outcomes after symptomatic neonatal hypoglycemia. Pediatrics 122, 65–74.
Patterns of cerebral injury and neurodevelopmental outcomes after symptomatic neonatal hypoglycemia.Crossref | GoogleScholarGoogle Scholar | 18595988PubMed |

Dalrymple, R. H., and Hamm, R. (1973). A method for the extraction of glycogen and metabolites from a single muscle sample. Int. J. Food Sci. Technol. 8, 439–444.
A method for the extraction of glycogen and metabolites from a single muscle sample.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE2cXpsVeisg%3D%3D&md5=fe4948f7cd4b74d9592e04a1d5480256CAS |

Folch, J., Lees, M., and Stanley, G. H. S. (1957). A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497–509.
| 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D&md5=7af8b449eecca02927736f072881bbefCAS | 13428781PubMed |

Gordon, J. I., Elshourbagy, N., Lowe, J. B., Liao, W. S., Alpers, D. H., and Taylor, J. M. (1985). Tissue specific expression and developmental regulation of two genes coding for rat fatty acid binding proteins. J. Biol. Chem. 260, 1995–1998.
| 1:CAS:528:DyaL2MXht12nsLg%3D&md5=d71415560a59dd9b4c7b3be05ffee4c9CAS | 2579065PubMed |

Guo, F., and Jen, C. (1995). High-fat feeding during pregnancy and lactation affects offspring metabolism in rats Physiol. Behav. 57, 681–686.
High-fat feeding during pregnancy and lactation affects offspring metabolism in ratsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXktlGju70%3D&md5=bec488e8e9100c7ca694c777d58384e0CAS | 7777603PubMed |

Hyatt, M. A., Gardner, D. S., Sebert, S., Wilson, V., Davidson, N., Nigmatullina, Y., Chan, L. L. Y., Budge, H., and Symonds, M. E. (2011). Suboptimal maternal nutrition, during early fetal liver development, promotes lipid accumulation in the liver of obese offspring. Reproduction 141, 119–126.
Suboptimal maternal nutrition, during early fetal liver development, promotes lipid accumulation in the liver of obese offspring.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisVehs7Y%3D&md5=58e26e31cf814e81b01061962ad15a13CAS | 21045167PubMed |

Jen, K. L., Juuhl, N., and Lin, P. K. H. (1988). Repeated pregnancy without lactation: effects on carcass composition and adipose tissue cellularity in rats. J. Nutr. 118, 93–98.
| 1:STN:280:DyaL1c%2FovF2ksA%3D%3D&md5=296990b4f53a9fff5563092fc136266fCAS | 3335944PubMed |

Khan, I. Y., Taylor, P. D., Dekou, V., Seed, P. T., Lakasing, L., Graham, D., Dominiczak, A. F., Hanson, M. A., and Poston, L. (2003). Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension 41, 168–175.
Gender-linked hypertension in offspring of lard-fed pregnant rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xps1Ogsrs%3D&md5=a491c77f64c7367b5ce31a2e5b0f10d4CAS | 12511548PubMed |

Khan, I. Y., Dekou, V., Douglas, G., Jenson, R., Hanson, M. A., Poston, L., and Taylor, P. D. (2005). A high-fat diet during pregnancy or suckling induces cardiovascular dysfunction in adult offspring. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R127–R133.
| 1:CAS:528:DC%2BD2MXhtVCqu7w%3D&md5=fbcfad4869dc2f62ada82d29395bc5fcCAS | 15308487PubMed |

Laws, J., Amusquivar, E., Laws, A., Herrera, E., Lean, I. J., Dodds, P. F., and Clarke, L. (2009). Supplementation of sow diets with oil during gestation: sow body condition, milk yield and milk composition. Livest. Sci. 123, 88–96.
Supplementation of sow diets with oil during gestation: sow body condition, milk yield and milk composition.Crossref | GoogleScholarGoogle Scholar |

Le Dividich, J., Mormede, P., Catheline, M., and Caritez, J. C. (1991). Body composition and cold resistance of the neonatal pig from European (Large White) and Chinese (Meishan) breeds. Biol. Neonate 59, 268–277.
Body composition and cold resistance of the neonatal pig from European (Large White) and Chinese (Meishan) breeds.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXktVGksro%3D&md5=b55fea40a024942e2b405ade2e019650CAS | 1873362PubMed |

Leturque, A., Ferre, P., Satabin, P., Kervran, A., and Girard, J. (1980). In vivo insulin resistance during pregnacy in the rat Diabetologia 19, 521–528.
In vivo insulin resistance during pregnacy in the ratCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXnslersQ%3D%3D&md5=0bcc0b9be47fd784e0845804fd716b7bCAS | 7007133PubMed |

Lomax, M. A., Karamanlidis, G., Laws, J., Cremers, S. G., Weinberg, P. D., and Clarke, L. (2013). Pigs fed saturated fat/cholesterol have a blunted hypothalamic–pituitary–adrenal function, are insulin resistant and have decreased expression of IRS-1, PGC1alpha and PPARalpha. J. Nutr. Biochem. 24, 656–663.
Pigs fed saturated fat/cholesterol have a blunted hypothalamic–pituitary–adrenal function, are insulin resistant and have decreased expression of IRS-1, PGC1alpha and PPARalpha.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVymsLfF&md5=5dd3db9903cfbbe9e6665e29febf4aa4CAS | 22819557PubMed |

Milligan, B. N., Fraser, D., and Kramer, D. L. (2002). Within-litter birth weight variation in the domestic pig and its relation to pre-weaning survival, weight gain, and variation in weaning weights. Livest. Prod. Sci. 76, 181–191.
Within-litter birth weight variation in the domestic pig and its relation to pre-weaning survival, weight gain, and variation in weaning weights.Crossref | GoogleScholarGoogle Scholar |

Pettigrew, J. E. (1981). Supplemental dietary fat for peripartal sows: a review. J. Anim. Sci. 53, 107–117.

Pluske, J. R., Williams, I. H., and Aherne, F. X. (1995). Nutrition of the neonatal pig. In ‘The Neonatal Pig: Development and Survival’. (Ed. M. A. Varley.) pp. 187–235. (CAB International: Wallingford.)

Randall, G. C. B. (1972). Observations on parturition in the sow. II. Factors influencing stillbirth and perinatal mortality. Vet. Rec. 90, 183–186.
Observations on parturition in the sow. II. Factors influencing stillbirth and perinatal mortality.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaE387lvFakuw%3D%3D&md5=1736149326d04f5d900fcebadbbd52eeCAS |

Seerley, R. W., Pace, T. A., Foley, C. W., and Scarth, R. D. (1974). Effect of energy intake prior to parturition on milk lipids and survival rate, thermostability and carcass composition of piglets. J. Anim. Sci. 38, 64–70.
| 1:CAS:528:DyaE2cXhtlWqsbc%3D&md5=af6833c1a717cfa1d7c14bde435e47edCAS | 4855840PubMed |

Seerley, R. W., Synder, R. A., and McCampbell, H. C. (1981). The influence of sow dietary lipids and choline on piglet survival, milk and carcass composition. J. Anim. Sci. 52, 542–550.
| 1:CAS:528:DyaL3MXhsFGgurw%3D&md5=a4072d370d99854fee05422ce2f543dbCAS | 7263527PubMed |

Taylor, P. D., McConnell, J., Khan, I. Y., Holemans, K., Lawrence, K. M., Asare-Anane, H., Persaud, S., Jones, P. M., Petrie, L., Hanson, M. A., and Poston, L. (2005). Impaired glucose homeostasis and mitochondrial abnormalities in offspring of rats fed a fat-rich diet in pregnancy. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R134–R139.
| 1:CAS:528:DC%2BD2MXhtVCqu7o%3D&md5=236b91d22c12e39892a7c82de9a47264CAS | 15388492PubMed |

Vaillancourt, J.-P., Stein, T. E., Marsh, W. E., Leman, A. D., and Dial, G. D. (1990). Validation of producer-recorded causes of preweaning mortality in swine. Prev. Vet. Med. 10, 119–130.
Validation of producer-recorded causes of preweaning mortality in swine.Crossref | GoogleScholarGoogle Scholar |

van der Peet-Schwering, C. M. C., Kemp, B., Binnendijk, G. P., den Hartog, L. A., Vereijken, P. F. G., and Verstegen, M. W. A. (2004). Effects of additional starch or fat in late-gestating high nonstarch polysaccharide diets on litter performance and glucose tolerance in sows. J. Anim. Sci. 82, 2964–2971.
| 1:CAS:528:DC%2BD2cXnvVWksrw%3D&md5=5d7b524045d64fd08178f070d86df47bCAS |

Vandesompele, J., De Preter, K., Pattyn, F., Poppe, B., Van Roy, N., De Paepe, A., and Speleman, F. (2002). Acurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 3, research0034–research0034.11.
Acurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes.Crossref | GoogleScholarGoogle Scholar | 12184808PubMed |

Varley, M. (1995). ‘The Neonatal Pig: Development and Survival.’ (CAB International: Wallingford.)