Maternal consumption of fish oil programs reduced adiposity in broiler chicks

Beckford, Ronique C.; Howard, Sarah J.; Das, Suchita; Farmer, Abigail T.; Campagna, Shawn R.; Yu, Jiali; Hettich, Robert L.; Wilson, Jeanna L.; Voy, Brynn H.

doi:10.1038/s41598-017-13519-5

Maternal consumption of fish oil programs reduced adiposity in broiler chicks

Journal Article · Fri Oct 13 00:00:00 EDT 2017 · Scientific Reports

DOI:https://doi.org/10.1038/s41598-017-13519-5· OSTI ID:1470893

Beckford, Ronique C. ^[1]; Howard, Sarah J. ^[1]; Das, Suchita ^[1]; Farmer, Abigail T. ^[2]; Campagna, Shawn R. ^[2]; Yu, Jiali ^[3]; ^[4]; Wilson, Jeanna L. ^[5]; ^[6]

Univ. of Tennessee, Knoxville, TN (United States). Department of Animal Science
Univ. of Tennessee, Knoxville, TN (United States). Department of Chemistry
Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology
Univ. of Tennessee, Knoxville, TN (United States). Graduate School of Genome Science and Technology and Chemical Sciences Division
Univ. of Georgia, Athens, GA (United States). Department of Poultry Science
Univ. of Tennessee, Knoxville, TN (United States). Department of Animal Science and Graduate School of Genome Science and Technology

We report that maternal intake of eicosapentaenoic acid (EPA; 20:5 n-3) and docosahexaenoic acid (22:6 n-3) has been associated with reduced adiposity in children, suggesting the possibility to program adipose development through dietary fatty acids before birth. This study determined if enriching the maternal diet in fish oil, the primary source of EPA and DHA, affected adipose development in offspring. Broiler chickens were used because they are obesity-prone, and because fatty acids provided to the embryo can be manipulated through the hen diet. Hens were fed diets supplemented (2.8% wt:wt) with corn oil (CO; n-6) or fish oil (FO; n-3) for 28 d. Chicks from both maternal diet groups were fed the same diet after hatch. Maternal FO consumption enriched chick adipose tissue in EPA and DHA and reduced adiposity by promoting more, but smaller, adipocytes. This adipocyte profile was paralleled by lower expression of the adipogenic regulator PPARG and its co-activator PPARGC1B, and elevated expression of LPL. Proteomics identified 95 differentially abundant proteins between FO and CO adipose tissue, including components of glucose metabolism, lipid droplet trafficking, and cytoskeletal organization. Lastly, these results demonstrate that the maternal dietary fatty acid profile programs offspring adipose development.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1470893

Journal Information:: Scientific Reports, Journal Name: Scientific Reports Journal Issue: 1 Vol. 7; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (79)

Eicosapentaenoic acid and arachidonic acid differentially regulate adipogenesis, acquisition of a brite phenotype and mitochondrial function in primary human adipocytes Fleckenstein-Elsen, Manuela; Dinnies, Daniela; Jelenik, Tomas Molecular Nutrition & Food Research, Vol. 60, Issue 9 https://doi.org/10.1002/mnfr.201500892	journal	June 2016
DNA Demethylation in Zebrafish Involves the Coupling of a Deaminase, a Glycosylase, and Gadd45 Rai, Kunal; Huggins, Ian J.; James, Smitha R. Cell, Vol. 135, Issue 7 https://doi.org/10.1016/j.cell.2008.11.042	journal	December 2008
Early steps of insulin receptor signaling in chicken and rat: apparent refractoriness in chicken muscle Dupont, Joëlle; Dagou, Carine; Derouet, Michel Domestic Animal Endocrinology, Vol. 26, Issue 2 https://doi.org/10.1016/j.domaniend.2003.09.004	journal	March 2004
APOBEC2 mRNA and protein is predominantly expressed in skeletal and cardiac muscles of chickens Li, Juan; Zhao, Xiao-Ling; Gilbert, Elizabeth Ruth Gene, Vol. 539, Issue 2 https://doi.org/10.1016/j.gene.2014.01.003	journal	April 2014
Transgenic ω-3 PUFA enrichment alters morphology and gene expression profile in adipose tissue of obese mice: Potential role for protectins White, Phillip J.; Mitchell, Patricia L.; Schwab, Michael Metabolism, Vol. 64, Issue 6 https://doi.org/10.1016/j.metabol.2015.01.017	journal	June 2015
Differential effects of eicosapentaenoic acid and docosahexaenoic acid in promoting the differentiation of 3T3-L1 preadipocytes Murali, Ganesan; Desouza, Cyrus V.; Clevenger, Michelle E. Prostaglandins, Leukotrienes and Essential Fatty Acids, Vol. 90, Issue 1 https://doi.org/10.1016/j.plefa.2013.10.002	journal	January 2014
Characterization of major elements of insulin signaling cascade in chicken adipose tissue: Apparent insulin refractoriness Dupont, Joëlle; Métayer-Coustard, Sonia; Ji, Bo General and Comparative Endocrinology, Vol. 176, Issue 1 https://doi.org/10.1016/j.ygcen.2011.12.030	journal	March 2012
MyriMatch: Highly Accurate Tandem Mass Spectral Peptide Identification by Multivariate Hypergeometric Analysis Tabb, David L.; Fernando, Christopher G.; Chambers, Matthew C. Journal of Proteome Research, Vol. 6, Issue 2 https://doi.org/10.1021/pr0604054	journal	February 2007
IDPicker 2.0: Improved Protein Assembly with High Discrimination Peptide Identification Filtering Ma, Ze-Qiang; Dasari, Surendra; Chambers, Matthew C. Journal of Proteome Research, Vol. 8, Issue 8 https://doi.org/10.1021/pr900360j	journal	August 2009
Eicosapentaenoic Acid Induces mRNA Expression of Peroxisome Proliferator-Activated Receptor γ Chambrier, Cécile; Bastard, Jean-Philippe; Rieusset, Jennifer Obesity Research, Vol. 10, Issue 6 https://doi.org/10.1038/oby.2002.70	journal	June 2002
Weight Gain in Infancy and Overweight or Obesity in Childhood across the Gestational Spectrum: a Prospective Birth Cohort Study Wang, Guoying; Johnson, Sara; Gong, Yiwei Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep29867	journal	July 2016
Requirement and role of arachidonic acid in the differentiation of pre-adipose cells Gaillard, D.; Négrel, R.; Lagarde, M. Biochemical Journal, Vol. 257, Issue 2 https://doi.org/10.1042/bj2570389	journal	January 1989
Prostacyclin as a potent effector of adipose-cell differentiation Négrel, R.; Gaillard, D.; Ailhaud, G. Biochemical Journal, Vol. 257, Issue 2 https://doi.org/10.1042/bj2570399	journal	January 1989
Effect of Fasting, Glucose, Amino Acids and Food Intake on In Vivo Insulin Release in the Chicken Simon, J.; Rosselin, G. Hormone and Metabolic Research, Vol. 10, Issue 02 https://doi.org/10.1055/s-0028-1093450	journal	March 1978
Incidence of Childhood Obesity in the United States [Correspondence] No authors listed New England Journal of Medicine, Vol. 370, Issue 17, p. 1659-1661 https://doi.org/10.1056/nejmc1402397	journal	April 2014
Tracking of body mass index in children in relation to overweight in adulthood Guo, Shumei S.; Chumlea, William Cameron The American Journal of Clinical Nutrition, Vol. 70, Issue 1 https://doi.org/10.1093/ajcn/70.1.145s	journal	July 1999
Essential fatty acids in mothers and their neonates Hornstra, Gerard The American Journal of Clinical Nutrition, Vol. 71, Issue 5 https://doi.org/10.1093/ajcn/71.5.1262s	journal	May 2000
Distribution, interconversion, and dose response of n−3 fatty acids in humans Arterburn, Linda M.; Hall, Eileen Bailey; Oken, Harry The American Journal of Clinical Nutrition, Vol. 83, Issue 6 https://doi.org/10.1093/ajcn/83.6.1467s	journal	June 2006
Fat Utilization and Lipogenesis in the Young Pig Allee, G. L.; Baker, D. H.; Leveille, G. A. The Journal of Nutrition, Vol. 101, Issue 10 https://doi.org/10.1093/jn/101.10.1415	journal	October 1971
Glyceroneogenesis Is Reduced and Glucose Uptake Is Increased in Adipose Tissue from Cafeteria Diet–Fed Rats Independently of Tissue Sympathetic Innervation Chaves, Valéria E.; Frasson, Danúbia; Martins-Santos, Maria E. S. The Journal of Nutrition, Vol. 136, Issue 10 https://doi.org/10.1093/jn/136.10.2475	journal	October 2006
Docosahexaenoic Acid Inhibits Adipocyte Differentiation and Induces Apoptosis in 3T3-L1 Preadipocytes Kim, Hye-Kyeong; Della-Fera, MaryAnne; Lin, Ji The Journal of Nutrition, Vol. 136, Issue 12 https://doi.org/10.1093/jn/136.12.2965	journal	December 2006
Function of GATA Transcription Factors in Preadipocyte-Adipocyte Transition Tong, Q. Science, Vol. 290, Issue 5489 https://doi.org/10.1126/science.290.5489.134	journal	October 2000
Regulation of Hepatic De Novo Lipogenesis in Humans Hellerstein, M. K.; Schwarz, J-M; Neese, R. A. Annual Review of Nutrition, Vol. 16, Issue 1 https://doi.org/10.1146/annurev.nu.16.070196.002515	journal	July 1996
Nutritional manipulations in the perinatal period program adipose tissue in offspring Lukaszewski, Marie-Amélie; Eberlé, Delphine; Vieau, Didier American Journal of Physiology-Endocrinology and Metabolism, Vol. 305, Issue 10 https://doi.org/10.1152/ajpendo.00231.2013	journal	November 2013
A simple method to determine fat cell size and number in four mammalian species Di Girolamo, M.; Mendlinger, S.; Fertig, Jw American Journal of Physiology-Legacy Content, Vol. 221, Issue 3 https://doi.org/10.1152/ajplegacy.1971.221.3.850	journal	September 1971
Molecular and metabolic profiles suggest that increased lipid catabolism in adipose tissue contributes to leanness in domestic chickens Ji, Bo; Middleton, Jesse L.; Ernest, Ben Physiological Genomics, Vol. 46, Issue 9 https://doi.org/10.1152/physiolgenomics.00163.2013	journal	May 2014
Studies of Human Adipose Tissue ADIPOSE CELL SIZE AND NUMBER IN NONOBESE AND OBESE PATIENTS Salans, Lester B.; Cushman, Samuel W.; Weismann, Rodger E. Journal of Clinical Investigation, Vol. 52, Issue 4 https://doi.org/10.1172/jci107258	journal	April 1973
The growth of adipose tissue in children and adolescents. Cross-sectional and longitudinal studies of adipose cell number and size. Knittle, J. L.; Timmers, K.; Ginsberg-Fellner, F. Journal of Clinical Investigation, Vol. 63, Issue 2 https://doi.org/10.1172/jci109295	journal	February 1979
Uncovering the novel characteristics of Asian honey bee, Apis cerana, by whole genome sequencing Park, Doori; Jung, Je Won; Choi, Beom-Soon BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/1471-2164-16-1	journal	January 2015
Suppressive actions of eicosapentaenoic acid on lipid droplet formation in 3T3-L1 adipocytes Manickam, Elizabeth; Sinclair, Andrew J.; Cameron-Smith, David Lipids in Health and Disease, Vol. 9, Issue 1 https://doi.org/10.1186/1476-511x-9-57	journal	January 2010
Mapping of leptin and its syntenic genes to chicken chromosome 1p Seroussi, Eyal; Pitel, Frédérique; Leroux, Sophie BMC Genetics, Vol. 18, Issue 1 https://doi.org/10.1186/s12863-017-0543-1	journal	August 2017
Transcriptional analysis of abdominal fat in chickens divergently selected on bodyweight at two ages reveals novel mechanisms controlling adiposity: validating visceral adipose tissue as a dynamic endocrine and metabolic organ Resnyk, C. W.; Carré, W.; Wang, X. BMC Genomics, Vol. 18, Issue 1 https://doi.org/10.1186/s12864-017-4035-5	journal	August 2017
Effect of prenatal DHA supplementation on the infant epigenome: results from a randomized controlled trial van Dijk, Susan J.; Zhou, Jing; Peters, Timothy J. Clinical Epigenetics, Vol. 8, Issue 1 https://doi.org/10.1186/s13148-016-0281-7	journal	November 2016
Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern? Massiera, Florence; Saint-Marc, Perla; Seydoux, Josiane Journal of Lipid Research, Vol. 44, Issue 2 https://doi.org/10.1194/jlr.m200346-jlr200	journal	November 2002
Thematic Review Series: Proteomics. Proteomic analysis of lipid-protein complexes Vaisar, Tomas Journal of Lipid Research, Vol. 50, Issue 5 https://doi.org/10.1194/jlr.r900005-jlr200	journal	February 2009
Adipose Tissue Thymidine Kinase Activity in Man Baum, David; Beck, Rebecca Q.; Hammer, Lawrence D. Pediatric Research, Vol. 20, Issue 2 https://doi.org/10.1203/00006450-198602000-00004	journal	February 1986
Rab18 localizes to lipid droplets and induces their close apposition to the endoplasmic reticulum-derived membrane Ozeki, S. Journal of Cell Science, Vol. 118, Issue 12 https://doi.org/10.1242/jcs.02401	journal	June 2005
Perilipin Overexpression in White Adipose Tissue Induces a Brown Fat-Like Phenotype Sawada, Takashi; Miyoshi, Hideaki; Shimada, Kohei PLoS ONE, Vol. 5, Issue 11 https://doi.org/10.1371/journal.pone.0014006	journal	November 2010
RNA-Seq Analysis of Abdominal Fat in Genetically Fat and Lean Chickens Highlights a Divergence in Expression of Genes Controlling Adiposity, Hemostasis, and Lipid Metabolism Resnyk, Christopher W.; Chen, Chuming; Huang, Hongzhan PLOS ONE, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pone.0139549	journal	October 2015
Relationship of Childhood Obesity to Coronary Heart Disease Risk Factors in Adulthood: The Bogalusa Heart Study Freedman, D. S.; Khan, L. K.; Dietz, W. H. PEDIATRICS, Vol. 108, Issue 3 https://doi.org/10.1542/peds.108.3.712	journal	September 2001
In Vivo Lipogenesis in the Domestic Chicken Leveille, G. A.; O'Hea, E. K.; Chakrabarty, K. Experimental Biology and Medicine, Vol. 128, Issue 2 https://doi.org/10.3181/00379727-128-33022	journal	June 1968
Adipose Tissue Metabolism and Its Control in Birds Leclercq, B. Poultry Science, Vol. 63, Issue 10 https://doi.org/10.3382/ps.0632044	journal	October 1984
Dietary Modification of Yolk Lipid with Menhaden Oil Hargis, P. S.; Van Elswyk, M. E.; Hargis, B. M. Poultry Science, Vol. 70, Issue 4 https://doi.org/10.3382/ps.0700874	journal	April 1991
Dietary Oils with Added Tocopherols: Effects on Egg or Tissue Tocopherols, Fatty Acids, and Oxidative Stability Cherian, G.; Wolfe, F. W.; Sim, J. S. Poultry Science, Vol. 75, Issue 3 https://doi.org/10.3382/ps.0750423	journal	March 1996
Obesity and Endocrine Dysfunction Programmed by Maternal Smoking in Pregnancy and Lactation Lisboa, Patricia Cristina; de Oliveira, Elaine; de Moura, Egberto Gaspar Frontiers in Physiology, Vol. 3 https://doi.org/10.3389/fphys.2012.00437	journal	January 2012
Prenatal fatty acid status and child adiposity at age 3 y: results from a US pregnancy cohort Donahue, Sara MA; Rifas-Shiman, Sheryl L.; Gold, Diane R. The American Journal of Clinical Nutrition, Vol. 93, Issue 4 https://doi.org/10.3945/ajcn.110.005801	journal	February 2011
Perinatal risk factors for childhood obesity and metabolic dysregulation Catalano, Patrick M.; Farrell, Kristen; Thomas, Alicia The American Journal of Clinical Nutrition, Vol. 90, Issue 5 https://doi.org/10.3945/ajcn.2008.27416	journal	September 2009
LC‐MS Data Processing with MAVEN: A Metabolomic Analysis and Visualization Engine Clasquin, Michelle F.; Melamud, Eugene; Rabinowitz, Joshua D. Current Protocols in Bioinformatics, Vol. 37, Issue 1 https://doi.org/10.1002/0471250953.bi1411s37	journal	March 2012
Perilipin is located on the surface layer of intracellular lipid droplets in adipocytes. Blanchette-Mackie, E. J.; Dwyer, N. K.; Barber, T. Journal of Lipid Research, Vol. 36, Issue 6 https://doi.org/10.1016/S0022-2275(20)41129-0	journal	June 1995
Incidencia de obesidad infantil en Estados Unidos Escobar, C.; Divisón, J. A.; Seguí Díaz, M. SEMERGEN - Medicina de Familia, Vol. 40, Issue 4 https://doi.org/10.1016/j.semerg.2014.03.013	journal	May 2014
Lipidomics: An analysis of cellular lipids by ESI-MS Milne, Stephen; Ivanova, Pavlina; Forrester, Jeffrey Methods, Vol. 39, Issue 2 https://doi.org/10.1016/j.ymeth.2006.05.014	journal	June 2006
Early infant adipose deposition is positively associated with the n-6 to n-3 fatty acid ratio in human milk independent of maternal BMI Rudolph, M. C.; Young, B. E.; Lemas, D. J. International Journal of Obesity, Vol. 41, Issue 4 https://doi.org/10.1038/ijo.2016.211	journal	November 2016
Diverse and divergent protein post-translational modifications in two growth stages of a natural microbial community Li, Zhou; Wang, Yingfeng; Yao, Qiuming Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms5405	journal	July 2014
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Huang, Da Wei; Sherman, Brad T.; Lempicki, Richard A. Nature Protocols, Vol. 4, Issue 1 https://doi.org/10.1038/nprot.2008.211	journal	December 2008
Lipid metabolism is associated with developmental epigenetic programming Marchlewicz, Elizabeth H.; Dolinoy, Dana C.; Tang, Lu Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep34857	journal	October 2016
Fatty acid recycling in adipocytes: a role for glyceroneogenesis and phosphoenolpyruvate carboxykinase Forest, C.; Tordjman, J.; Glorian, M. Biochemical Society Transactions, Vol. 31, Issue 6 https://doi.org/10.1042/bst0311125	journal	December 2003
Incidence of Childhood Obesity in the United States [Correspondence] No authors listed New England Journal of Medicine, Vol. 370, Issue 17, p. 1659-1661 https://doi.org/10.1056/NEJMc1402397	journal	April 2014
Incidence of Childhood Obesity in the United States Cunningham, Solveig A.; Kramer, Michael R.; Narayan, K. M. Venkat New England Journal of Medicine, Vol. 370, Issue 5 https://doi.org/10.1056/NEJMoa1309753	journal	January 2014
Regulated Localization of Rab18 to Lipid Droplets Martin, Sally; Driessen, Kim; Nixon, Susan J. Journal of Biological Chemistry, Vol. 280, Issue 51 https://doi.org/10.1074/jbc.M506651200	journal	October 2005
Distribution, interconversion, and dose response of n−3 fatty acids in humans Arterburn, Linda M.; Hall, Eileen Bailey; Oken, Harry The American Journal of Clinical Nutrition, Vol. 83, Issue 6 https://doi.org/10.1093/ajcn/83.6.1467S	journal	June 2006
Role of phosphatidylserine synthase in shaping the phospholipidome of Candida albicans Cassilly, Chelsi D.; Farmer, Abigail T.; Montedonico, Anthony E. FEMS Yeast Research, Vol. 17, Issue 2 https://doi.org/10.1093/femsyr/fox007	journal	February 2017
The Loss of Adipokine Genes in the Chicken Genome and Implications for Insulin Metabolism Đaković, Nataša; Térézol, Morgane; Pitel, Frédérique Molecular Biology and Evolution, Vol. 31, Issue 10 https://doi.org/10.1093/molbev/msu208	journal	July 2014
MetaboAnalyst 3.0—making metabolomics more meaningful Xia, Jianguo; Sinelnikov, Igor V.; Han, Beomsoo Nucleic Acids Research, Vol. 43, Issue W1 https://doi.org/10.1093/nar/gkv380	journal	April 2015
Docosahexaenoic acid increases cellular adiponectin mRNA and secreted adiponectin protein, as well as PPARγ mRNA, in 3T3-L1 adipocytes Oster, Richard T.; Tishinsky, Justine M.; Yuan, Zongfei Applied Physiology, Nutrition, and Metabolism, Vol. 35, Issue 6 https://doi.org/10.1139/H10-076	journal	December 2010
A Rapid Method of Total Lipid Extraction and Purification Bligh, E. G.; Dyer, W. J. Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 8 https://doi.org/10.1139/o59-099	journal	August 1959
A Rapid Method of Total Lipid Extraction and Purification Bligh, E. G.; Dyer, W. J. Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 1 https://doi.org/10.1139/y59-099	journal	January 1959
Studies of Human Adipose Tissue ADIPOSE CELL SIZE AND NUMBER IN NONOBESE AND OBESE PATIENTS Salans, Lester B.; Cushman, Samuel W.; Weismann, Rodger E. Journal of Clinical Investigation, Vol. 52, Issue 4 https://doi.org/10.1172/JCI107258	journal	April 1973
The growth of adipose tissue in children and adolescents. Cross-sectional and longitudinal studies of adipose cell number and size. Knittle, J. L.; Timmers, K.; Ginsberg-Fellner, F. Journal of Clinical Investigation, Vol. 63, Issue 2 https://doi.org/10.1172/JCI109295	journal	February 1979
Suppressive actions of eicosapentaenoic acid on lipid droplet formation in 3T3-L1 adipocytes Manickam, Elizabeth; Sinclair, Andrew J.; Cameron-Smith, David Lipids in Health and Disease, Vol. 9, Issue 1 https://doi.org/10.1186/1476-511X-9-57	journal	January 2010
Messenger RNA sequencing and pathway analysis provide novel insights into the biological basis of chickens’ feed efficiency Zhou, Nan; Lee, William R.; Abasht, Behnam BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1364-0	journal	March 2015
Correspondence on Lovell et al.: identification of chicken genes previously assumed to be evolutionarily lost Bornelöv, Susanne; Seroussi, Eyal; Yosefi, Sara Genome Biology, Vol. 18, Issue 1 https://doi.org/10.1186/s13059-017-1231-1	journal	June 2017
Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern? Massiera, Florence; Saint-Marc, Perla; Seydoux, Josiane Journal of Lipid Research, Vol. 44, Issue 2 https://doi.org/10.1194/jlr.M200346-JLR200	journal	November 2002
Thematic Review Series: Proteomics. Proteomic analysis of lipid-protein complexes Vaisar, Tomas Journal of Lipid Research, Vol. 50, Issue 5 https://doi.org/10.1194/jlr.R900005-JLR200	journal	February 2009
Effects of Dietary Carbohydrate Source on Growth, Plasma Metabolites and Lipogenesis in Rats, Pigs and Chicks Waterman, R. A.; Romsos, D. R.; Tsai, A. C. Experimental Biology and Medicine, Vol. 150, Issue 1 https://doi.org/10.3181/00379727-150-39006	journal	October 1975
Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century Blasbalg, Tanya L.; Hibbeln, Joseph R.; Ramsden, Christopher E. The American Journal of Clinical Nutrition, Vol. 93, Issue 5 https://doi.org/10.3945/ajcn.110.006643	journal	March 2011
Maternal plasma PUFA concentrations during pregnancy and childhood adiposity: the Generation R Study Vidakovic, Aleksandra Jelena; Gishti, Olta; Voortman, Trudy The American Journal of Clinical Nutrition, Vol. 103, Issue 4 https://doi.org/10.3945/ajcn.115.112847	journal	February 2016
Effect of long-chain polyunsaturated fatty acid supplementation during pregnancy or lactation on infant and child body composition: a systematic review Muhlhausler, Beverly S.; Gibson, Robert A.; Makrides, Maria The American Journal of Clinical Nutrition, Vol. 92, Issue 4 https://doi.org/10.3945/ajcn.2010.29495	journal	August 2010
The Developmental Origins, Mechanisms, and Implications of Metabolic Syndrome Bruce, Kimberley D.; Hanson, Mark A. The Journal of Nutrition, Vol. 140, Issue 3 https://doi.org/10.3945/jn.109.111179	journal	January 2010
Additional file 7: of Transcriptional analysis of abdominal fat in chickens divergently selected on bodyweight at two ages reveals novel mechanisms controlling adiposity: validating visceral adipose tissue as a dynamic endocrine and metabolic organ Resnyk, C.; Carré, W.; Wang, X. Figshare https://doi.org/10.6084/m9.figshare.c.3855622_d7	dataset	January 2017

Similar Records

Replacing fish oil and astaxanthin by microalgal sources produced different metabolic responses in juvenile rainbow trout fed 2 types of practical diets

Journal Article · Sun Dec 20 19:00:00 EST 2020 · Journal of Animal Science · OSTI ID:2287675

Replacing fish oil and astaxanthin by microalgal sources produced different metabolic responses in juvenile rainbow trout fed 2 types of practical diets

Journal Article · Sun Dec 20 23:00:00 EST 2020 · Journal of Animal Science · OSTI ID:1848484

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Maternal consumption of fish oil programs reduced adiposity in broiler chicks

Citation Formats

References (79)

Similar Records

Related Subjects