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Maternal Flaxseed Oil During Lactation Enhances Bone Development in Male Rat Pups

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Lipids

Abstract

Flaxseed oil is an alpha linolenic acid source important in the growth and body development stage; furthermore, this acid acts on adipose tissue and bone health. The aim of this study was to evaluate body composition, fatty acid composition, hormone profile, retroperitoneal adipocyte area and femur structure of pups at weaning, whose mothers were fed a diet containing flaxseed oil during lactation. After birth, pups were randomly assigned: control (C, n = 12) and flaxseed oil (FO, n = 12), rats whose mothers were treated with diet containing soybean or flaxseed oil. At 21 days, the pups were weaned and body mass, length, body composition, biochemical parameter, leptin, osteoprotegerin, osteocalcin, fatty acids composition, intra-abdominal fat mass and femur structure were analyzed. FO showed (p < 0.05): higher body mass (+12 %) and length (+9 %); body fat mass (g, +45 %); bone mineral density (+8 %), bone mineral content (+55 %) and bone area (+35 %), osteocalcin (+173 %) and osteoprotegerin (+183 %). Arachidonic acid was lower (p < 0.0001), alpha-linolenic and eicosapentaenoic were higher (p < 0.0001). Intra-abdominal fat mass was higher (+25 %), however, the retroperitoneal adipocytes area was lower (−44 %). Femur mass (+10 %), distance between epiphyses (+4 %) and bone mineral density (+13 %) were higher. The study demonstrates that adequate flaxseed oil content during a lactation diet plays an important role in the development of pups.

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Abbreviations

ARA:

Arachidonic acid

AIN:

American Institute of Nutrition

ALA:

Alpha linolenic acid

BMC:

Bone mineral content

BMD:

Bone mineral density

C:

Control group

DXA:

Dual-energy X-ray absorptiometry

EPA:

Eicosapentaenoic acid

FO:

Flaxseed oil group

HDL:

High density lipoprotein

HE:

Hematoxylin–eosin

LNA:

Linoleic acid

LDL:

Low density lipoprotein

OPG:

Osteoprotegerin

PUFA:

Polyunsaturated fatty acids

RANK:

Receptor activator of nuclear factor kappa-B

RANK-L:

Receptor activator of nuclear factor kappa-B ligand

SEM:

Standard error of the mean

References

  1. Langley-Evans SC (2015) Nutrition in early life and the programming of adult disease: a review. J Hum Nutr Diet 28:1–14

    Article  PubMed  Google Scholar 

  2. Mcmanaman JL, Neville MC (2003) Mammary physiology and milk secretion. Adv Drug Deliv Rev 55:629–641

    Article  CAS  PubMed  Google Scholar 

  3. Innis SM (2005) Essential fatty acids transfer and fetal development. Placenta 26:S70–S75

    Article  PubMed  Google Scholar 

  4. Green KH, Wong SCF, Weiler HA (2004) The effect of dietary n-3 long-chain polyunsaturated fatty acids on femur mineral density and biomarkers of bone metabolism in healthy diabetic and dietary-restricted growing rats. Prostaglandins Leukot Essent Fatty Acids 71:121–130

    Article  CAS  PubMed  Google Scholar 

  5. Costa CAS, Carlos AS, Gonzalez GD, Reis RP, Ribeiro MS, dos Santos AS, Monteiro MA, de Moura EG, Nascimento-Saba CCA (2012) Diet containing low n-6/n-3 polyunsaturated fatty acids ratio, provided by canola oil, alters body composition and bone quality in young rats. Eur J Nutr 51:191–198

    Article  PubMed  Google Scholar 

  6. Aguirre L, Napoli N, Waters D, Qualls C, Villareal DT, Armamento-Villareal R (2014) Increasing adiposity is associated with higher adipokine levels and lower bone mineral density in obese older adults. J Clin Endocrinol Metab 99:3290–3297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kruger MC, Coetzee M, Haag M, Weiler H (2010) Long-chain polyunsaturated fatty acids: selected mechanisms of action on bone. Prog Lipid Res 49:438–449

    Article  CAS  PubMed  Google Scholar 

  8. Dirienzo MA, Lemke SL, Petersen BJ, Smith KM (2008) Effect of substitution of high stearic low linolenic acid soybean oil for hydrogenated soybean oil on fatty acid intake. Lipids 43:451–456

    Article  CAS  PubMed  Google Scholar 

  9. Ghibaudi L, Cook J, Farley C, Hwa JJ (2002) Fat intake affects adiposity, comorbidity factors, and energy metabolism of Prague-dawley rats. Obes Res 10:956–963

    Article  CAS  PubMed  Google Scholar 

  10. Lane K, Derbyshire E, Li W, Brennan C (2014) Bioavailability and potential uses of vegetarian sources of omega-3 fatty acids: a review of the literature. Crit Rev Food Sci Nutr 54:572–579

    Article  CAS  PubMed  Google Scholar 

  11. Riediger ND, Othman R, Fitz Pierce GN, Suh M, Moghadasian MH (2008) Low n-6:n-3 fatty acid ratio, with fish- or flaxseed oil, in a high fat diet improves plasma lipids and beneficially alters tissue fatty acid composition in mice. Eur J Nutr 47:153–160

    Article  CAS  PubMed  Google Scholar 

  12. Fishbeck KL, Rasmussen KM (1987) Effect of repeated reproductive cycles on maternal nutritional status, lactational performance and litter growth in ad libitum-fed and chronically food-restricted rats. J Nutr 117:1967–1975

    Google Scholar 

  13. Reeves PG, Nielsen FH, Fahey GCF (1993) AIN-93 purified diet of laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodents diet. J Nutr 123:1939–1951

    CAS  PubMed  Google Scholar 

  14. Costa CAS, Carlos AS, Santos AS, Monteiro AM, de Moura EG, Nascimento-Saba CCA (2011) Abdominal adiposity, insulin and bone quality in young male rats fed a high-fat diet containing soybean or canola oil. Clinics (São Paulo) 66:1811–1816

    Article  Google Scholar 

  15. Tsujio M, Mizorogi T, Kitamura I, Maeda Y, Nishijima K, Kuwahara S, Ohno T, Niida S, Nagaya M, Saito R, Tanaka S (2009) Bone mineral analysis through dual energy X-ray absorptiometry in laboratory animals. J Vet Med Sci 71:1493–1497

    Article  PubMed  Google Scholar 

  16. Lukaski HC, Hall CB, Marchello MJ, Siders WA (2001) Validation of dual X-ray absorptiometry for body-composition assessment of rats exposed to dietary stressors. Nutrition 17:607–613

    Article  CAS  PubMed  Google Scholar 

  17. AOAC (2002) Official methods of analysis. AOAC International, Gaithersburg

    Google Scholar 

  18. AOCS, Official Method Ce 1 h-05 (2005) Determination of cis-, trans-, saturated, monounsaturated, and polyunsaturated fatty acids in vegetable or non-ruminant animal oils and fats by capillary GLC. AOCS Press, Champaign

    Google Scholar 

  19. Costa CAS, Silva PCA, Ribeiro DC, Pereira AD, Santos AS, Mais LA, Ruffoni LDG, Santana FC, Abreu MDC, Boueri BFC, Pessanha CR, Nonaka KO, Mancini-Filho J, Nascimento-Saba CCA, Boaventura GT (2015) Body adiposity and bone parameters of male rats from mothers fed diet containing flaxseed flour during lactation. J Dev Orig Health Dis 7:1–6

    Google Scholar 

  20. Ribeiro DC, Pereira AD, Silva PCA, Santos AS, Santana FC, Boueri BFC, Pessanha CR, Abreu MDC, Mancini-Filho J, Silva EM, Nascimento-Saba CCA, Costa CAS, Boaventura GB (2015) Flaxseed flour (Linum usitatissimum) consumption improves bone quality and decreases the adipocyte area of lactating rats in the post-weaning period. Int J Food Sci Nutr 67:29–34

    Article  PubMed  Google Scholar 

  21. Tinoco SMB, Sichieri R, Setta CL, Moura AS, Carmo MG (2009) n-3 polyunsaturated fatty acids in milk is associated to weight gain and growth in premature infants. Lipids Health Dis 26:8–23

    Google Scholar 

  22. Korotkova M, Gabrielsson B, Hanson LA, Strandvik B (2002) Maternal dietary intake of essential fatty acids affects adipose tissue growth and leptin mRNA expression in suckling rat pups. Pediatr Res 52:78–84

    Article  CAS  PubMed  Google Scholar 

  23. Fernandes FS, de Souza AS, do Carmo Dd, Boaventura GT (2001) Maternal intake of flaxseed-based diet (Linum usitatissimum) on hippocampus fatty acid profile: implications for growth, locomotor activity and spatial memory. Nutrition 27:1040–1047

    Article  Google Scholar 

  24. Glickman SG, Marn CS, Supiano MA, Dengel DR (2004) Validity and reliability of dual-energy X-ray absorptiometry for the assessment of abdominal adiposity. J Appl Physiol 97:509–514

    Article  PubMed  Google Scholar 

  25. Goyal A, Sharma V, Upadhyay N, Gill S, Sihag M (2014) Flax and flaxseed oil: an ancient medicine & modern functional food. J Food Sci Technol 51:1633–1653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Pacheco JT, Daleprame B, Boaventura GT (2011) Impact of dietary flaxseed (Linum usitatissimum) supplementation on biochemical profile in healthy rats. Nutr Hosp 26:798–802

    CAS  Google Scholar 

  27. Cardozo LFMF, Chagas MA, Soares LL, Troina AA, Boaventura GT (2010) Exposure to flaxseed during lactation does not alter prostate area or epithelium height but changes lipid profile in rats. Nutr Hosp 25:250–255

    CAS  Google Scholar 

  28. Cassani RSL, Fassini PG, Silvah JH, Lima CMM, Marchini JS (2015) Impact of weight loss diet associated with flaxseed on inflammatory markers in men with cardiovascular risk factors: a clinical study. Nutr J 14:1–8

    Article  Google Scholar 

  29. Kawakami Y, Yamanaka-Okumura H, Naniwa-Kuroki Y, Sakuma M, Taketaki Y, Takeda E (2015) Flaxseed oil intake reduces serum small dense low-density lipoprotein concentrations in Japanese men: randomized, double blind, crossover study. Nutr J 14:1–9

    Article  CAS  Google Scholar 

  30. Pirillo A, Catapano AL (2015) Update on the management of severe hypertriglyceridemia—focus on free fatty acid forms of omega-3. Drug Des Dev Ther 9:2129–2137

    Google Scholar 

  31. Choi SH, Choi-Kwon S (2015) The effects of the DASH diet education program with omega-3 fatty acid supplementation on metabolic syndrome parameters in elderly women with abdominal obesity. Nutr Res Pract 9:150–157

    Article  PubMed  Google Scholar 

  32. Jeong I, Cho SW, Kim SW, Choi HJ, Park SY, Lee HK, Cho SH, Oh BH, Shin CS (2010) Lipid profiles and bone mineral density in pre- and postmenopausal women in Korea. Calcif Tissue Int 87:507–512

    Article  CAS  PubMed  Google Scholar 

  33. Brownbill RA, Ilich JZ (2006) Lipid profile and bone paradox: higher serum lipids are associated with higher bone mineral density in postmenopausal women. J Womens Health 15:261–270

    Article  CAS  Google Scholar 

  34. Cui LH, Shin MH, Chung EK, Lee YH, Kweon SS, Park KS, Choi JS (2005) Association between bone mineral densities and serum lipid profiles of pre- and post-menopausal rural women in South Korea. Osteoporos Int 16:1975–1981

    Article  CAS  PubMed  Google Scholar 

  35. Hsu Y, Venners SA, Terwedow HA, Fenf Y, Niu T, Li Z, Laird N, Brain JD, Commings SR, Bouxsein ML, Rosen CJ, Xu X (2006) Relation of body composition, fat mass, and serum lipids to osteoporotic fractures and bone mineral density in Chinese men and women. Am J Clin Nutr 83:146–154

    CAS  PubMed  Google Scholar 

  36. Raclot T, Groscolas R (1994) Individual fish-oil n-3 polyunsaturated fatty acid deposition and mobilization rates for adipose tissue of rats in a nutritional steady state. Am J Clin Nutr 60:72–78

    CAS  PubMed  Google Scholar 

  37. Massiera F, Saint-Marc P, Seydoux J, Murata T, Kobayashi T, Narumiya S, Guesnet P, Amri EZ, Negrel R, Ailhaud G (2003) Arachidonic acid and prostacyclin signaling promote adipose tissue development: a human health concern? J Lipid Res 44:271–279

    Article  CAS  PubMed  Google Scholar 

  38. Lukas R, Gigliotti JC, Smith BJ, Altman S, Tou JC (2011) Consumption of different sources of omega-3 polyunsaturated fatty acids by growing female rats affects long bone mass and microarchitecture. Bone 49:455–462

    Article  CAS  PubMed  Google Scholar 

  39. Thorsen K, Nordstrom P, Lorentzon R, Dahlén GH (1999) The relation between bone mineral density, insulin-like growth factor I, lipoprotein (a), body composition, and muscle strength in adolescent males. J Clin Endocrinol Metab 84:3025–3029

    Article  CAS  PubMed  Google Scholar 

  40. Boyle WJ, Simonet WS, Lacery DL (2003) Osteoclast differentiation and activation. Nature 423:337–342

    Article  CAS  PubMed  Google Scholar 

  41. Farquharson C, Staines K (2011) The skeleton: no bones about it. J Endocrinol 211:107–108

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This project and scholarships were supported by Brazilian foundations, such as, The State of Rio de Janeiro Carlos Chagas Filho Research Foundation (FAPERJ), Coordination for the Enhancement of Higher Education Personnel (CAPES) and National Counsel of Technological and Scientific Development (CNPq). We are thankful to the Laboratory of Nutrition and Functional Assessment (LANUFF), College of Nutrition, Fluminense Federal University for technical assistance and use of DXA equipment.

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Authors and Affiliations

  1. Laboratory of Experimental Nutrition, Department of Nutrition and Dietetics, Fluminense Federal University, Rua Mário Santos Braga 30, Niterói, RJ, 24020-140, Brazil

    Aline D’Avila Pereira, Danielle Cavalcante Ribeiro, Carlos Alberto Soares da Costa & Gilson Teles Boaventura

  2. Laboratory of Lipids, Department of Food Science and Experimental Nutrition, Faculty of Pharmaceutical Sciences, University of São Paulo, São Paulo, Brazil

    Fernanda Carvalho de Santana & Jorge Mancini-Filho

  3. Physiological Sciences, Institute of Biology Roberto Alcantara Gomes, State University of Rio de Janeiro, Rio de Janeiro, Brazil

    Aline de Sousa dos Santos & Celly Cristina Alves do Nascimento-Saba

  4. Department of Statistics, Fluminense Federal University, Niterói, RJ, Brazil

    Luis Guillermo Coca Velarde

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  1. Aline D’Avila Pereira
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  2. Danielle Cavalcante Ribeiro
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Correspondence to Aline D’Avila Pereira.

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Pereira, A.D., Ribeiro, D.C., de Santana, F.C. et al. Maternal Flaxseed Oil During Lactation Enhances Bone Development in Male Rat Pups. Lipids 51, 923–929 (2016). https://doi.org/10.1007/s11745-016-4165-6

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  • DOI: https://doi.org/10.1007/s11745-016-4165-6

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