Nutrition
Volume 26, Issue 4 , Pages 423-431 , April 2010

Developmental and neurobehavioral effects of perinatal exposure to diets with different ω-6:ω-3 ratios in mice

  • María E. Santillán, Ph.D.

      Affiliations

    • Instituto de Fisiología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Córdoba, Argentina
    • Corresponding Author InformationCorresponding author. Tel.: +54-351-451-3735; fax: +54-351-433-2019.
  • ,
  • Laura M. Vincenti, Ph.D.

      Affiliations

    • Instituto de Fisiología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Córdoba, Argentina
  • ,
  • Ana C. Martini, Ph.D.

      Affiliations

    • Instituto de Fisiología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Córdoba, Argentina
    • Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Córdoba, Argentina
  • ,
  • Marta Fiol de Cuneo, M.D., Ph.D.

      Affiliations

    • Instituto de Fisiología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Córdoba, Argentina
    • Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Córdoba, Argentina
  • ,
  • Rubén D. Ruiz, M.D., Ph.D.

      Affiliations

    • Instituto de Fisiología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Córdoba, Argentina
    • Consejo Nacional de Investigaciones Científicas y Tecnológicas (CONICET), Córdoba, Argentina
  • ,
  • Arnaldo Mangeaud, Ph.D.

      Affiliations

    • Cátedra de Estadística y Biometría, Facultad de Ciencias Exactas Físicas y Naturales Universidad Nacional de Córdoba, Córdoba, Argentina
  • ,
  • Graciela Stutz, M.D., Ph.D.

      Affiliations

    • Instituto de Fisiología, Facultad de Ciencias Médicas, Universidad Nacional de Córdoba, Córdoba, Argentina

Received 22 December 2008 ,Accepted 7 June 2009.

References 

  1. Simopoulos A. Omega-3 fatty acids in health and disease and in growth and development. Am J Clin Nutr. 1991;54:438–463
  2. Hulbert AJ, Else PL. Mechanisms underlying the cost of living in animals. Annu Rev Physiol. 2000;62:207–235
  3. Mitmesser SH, Jensen CL. Roles of long-chain polyunsaturated fatty acids in the term infant: developmental benefits. Neonatal Netw. 2007;26:229–234
  4. McGregor J, Allen K, Harris M, Reece M, Wheeler M, French J, et al. The omega-3 story: Nutritional prevention of preterm birth and other adverse pregnancy outcomes. Obstet Gynecol Surv. 2001;56:S1–13
  5. Crawford MA, Hassam AG, Rivers JP. Essential fatty acid requirements in infancy. Am J Clin Nutr. 1978;31:2181–2185
  6. Cheatham CL, Colombo J, Carlson SE. N-3 fatty acids and cognitive and visual acuity development: methodologic and conceptual considerations. Am J Clin Nutr. 2006;83(Suppl):1458S–66
  7. Innis SM, Friesen RW. Essential n-3 fatty acids in pregnant women and early visual acuity maturation in term infants. Am J Clin Nutr. 2008;87:548–557
  8. Ozias MK, Carlson SE, Levant B. Maternal parity and diet (n-3) polyunsaturated fatty acid concentration influence accretion of brain phospholipid docosahexaenoic acid in developing rats. J Nutr. 2007;137:125–129
  9. Guesnet P, Alasnier C, Alessandri JM. Modifying the n-3 fatty acid content of the maternal diet to determine the requirements of the fetal and suckling rat. Lipids. 1997;32:527–534
  10. Simopoulos AP, Leaf A, Salem N. Workshop on the essentiality of and recommended dietary intakes for omega-6 and omega-3 fatty acids. J Am Coll Nutr. 1999;18:487–489
  11. Simopoulos AP. The importance of the ratio of omega-6/omega-3 essential fatty acids. Biomed Pharmacother. 2002;56:365–379
  12. Auestad N, Scott DT, Janowsky JS, Jacobsen C, Carroll RE, Montalto MB, et al. Visual, cognitive, and language assessments at 39 months: a follow-up study of children fed formulas containing long-chain polyunsaturated fatty acids to 1 year of age. Pediatrics. 2003;112(3 pt 1):e177–e183
  13. Carrie I, Smirnova M, Clement M, De JD, Frances H, Bourre JM. Docosahexaenoic acid–rich phospholipid supplementation: effect on behavior, learning ability, and retinal function in control and n-3 polyunsaturated fatty acid deficient old mice. Nutr Neurosci. 2002;5:43–52
  14. Wainwright PE. Dietary essential fatty acids and brain function: a developmental perspective on mechanisms. Proc Nutr Soc. 2002;61:61–69
  15. Church MW, Jen KL, Dowhan LM, Adams BR, Hotra JW. Excess and deficient omega-3 fatty acid during pregnancy and lactation cause impaired neural transmission in rat pups. Neurotoxicol Teratol. 2008;30:107–117
  16. Tofail F, Kabir I, Hamadani J, Chowdhury F, Yesmin S, Mehreen F, et al. Supplementation of fish-oil and soy-oil during pregnancy and psychomotor development of infants. J Health Popul Nutr. 2006;24:48–56
  17. Lavialle M, Champeil-Potokar G, Alessandri JM, Balasse L, Guesnet P, Papillon C, et al. An (n-3) polyunsaturated fatty acid-deficient diet disturbs daily locomotor activity, melatonin rhythm, and striatal dopamine in Syrian hamsters. J Nutr. 2008;138:1719–1724
  18. Kihara T, Surjono T, Sakamoto M, Matsuo T, Yasuda Y, Tanimura T. Effects of prenatal rubratoxin-B exposure on behaviors of mouse offspring. Toxicol Sci. 2001;61:368–373
  19. Vorhees CV, Butcher RE, Brunner RL, Sobotka TJ. A developmental test battery for neurobehavioral toxicity in rats: a preliminary analysis using monosodium glutamate calcium carrageenan, and hydroxyurea. Toxicol Appl Pharmacol. 1979;50:267–282
  20. Pellis SM, Pellis VC, Chen YC, Barzci S, Teitelbaum P. Recovery from axial apraxia in the lateral hypothalamic labyrinthectomized rat reveals three elements of contact-righting: cephalocaudal dominance, axial rotation, and distal limb action. Behav Brain Res. 1989;35:241–251
  21. Metz GA, Schwab ME. Behavioral characterization in a comprehensive mouse test battery reveals motor and sensory impairments in growth-associated protein-43 null mutant mice. Neuroscience. 2004;129:563–574
  22. Yoshida S, Numachi Y, Matsuoka H, Sato M. The absence of impairment of cliff avoidance reaction induced by subchronic methamphetamine treatment in inbred strains of mice. Tohoku J Exp Med. 2000;190:205–212
  23. Wainwright PE, Jalali E, Mutsaers LM, Bell R, Cvitkovic S. An imbalance of dietary essential fatty acids retards behavioral development in mice. Physiol Behav. 1999;66:833–839
  24. Shaikh SR, Edidin M. Polyunsaturated fatty acids, membrane organization, T cells, and antigen presentation. Am J Clin Nutr. 2006;84:1277–1289
  25. Ledger H. Body composition as a basis for a comparative study of some East African mammals. Symp Zool Soc Lond. 1968;21:289–310
  26. Wei Wo CK, Draper HH. Vitamin E status of Alaskan Eskimos. Am J Clin Nutr. 1975;28:808–813
  27. Mairesse G, Thomas M, Gardeur JN, Brun-Bellut J. Effects of geographic source, rearing system, and season on the nutritional quality of wild and farmed Perca fluviatilis. Lipids. 2006;41:221–229
  28. Kaya Y, Emin Erdem M. Seasonal comparison of wild and farmed brown trout (Salmo trutta forma fario L., 1758): crude lipid, gonadosomatic index and fatty acids. Int J food Sci Nutr. 2008;24:1–11
  29. Simopoulos AP. New products from the agri-food industry: the return of n-3 fatty acids into the food supply. Lipids. 1999;34(Suppl):S297–S301
  30. Bourre JM. Effect of increasing the omega-3 fatty acid in the diets of animals on the animal products consumed by humans. Med Sci (Paris). 2005;21:773–779
  31. Armitage J, Taylor P, Poston L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005;565:3–8
  32. Taylor PD, Khan IY, Lakasing L, Dekou V, O'Brien-Coker I, Mallet AI, et al. Uterine artery function in pregnant rats fed a diet supplemented with animal lard. Exp Physiol. 2003;88:389–398
  33. Keesey RE, Hirvonen MD. Body weight set-points: determination and adjustment. J Nutr. 1997;127:1875S–1878
  34. Knopp RH, Saudek CD, Arky RA, O'Sullivan JB. 2 Phases of adipose tissue metabolism in pregnancy: maternal adaptations for fetal growth. Endocrinology. 1973;92:984–988
  35. Otway S, Robinson DS. The significance of changes in tissue clearing-factor lipase activity in relation to the lipaemia of pregnancy. Biochem J. 1968;106:677–682
  36. Hamosh M, Clary TR, Chernick SS, Scow RO. Lipoprotein lipase activity of adipose and mammary tissue and plasma triglyceride in pregnant and lactating rats. Biochim Biophys Acta. 1970;210:473–482
  37. Robinson DS, Wing DR. Clearing factor lipase and its role in the regulation of triglyceride utilization. Studies on the enzyme in adipose tissue. Adv Exp Med Biol. 1972;26:71–76
  38. Wainwright PE, Xing HC, Mutsaers L, McCutcheon D, Kyle D. Arachidonic acid offsets the effects on mouse brain and behavior of a diet with a low (n-6):(n-3) ratio and very high levels of docosahexaenoic acid. J Nutr. 1997;127:184–193
  39. Church MW, Jen KL, Stafferton T, Hotra JW, Adams BR. Reduced auditory acuity in rat pups from excess and deficient omega-3 fatty acid consumption by the mother. Neurotoxicol Teratol. 2007;29:203–210
  40. Lands WE, Morris A, Libelt B. Quantitative effects of dietary polyunsaturated fats on the composition of fatty acids in rat tissues. Lipids. 1990;25:505–516
  41. Rosenfeld CS, Roberts RM. Maternal diet and other factors affecting offspring sex ratio: a review. Biol Reprod. 2004;71:1063–1070
  42. Austad S, Sunquist M. Sex-ratio manipulation in the common opossum. Nature. 1986;324:58–60
  43. Fountain ED, Mao J, Whyte JJ, Mueller KE, Ellersieck MR, Will MJ, et al. Effects of diets enriched in omega-3 and omega-6 polyunsaturated fatty acids on offspring sex-ratio and maternal behavior in mice. Biol Reprod. 2008;78:211–217
  44. Korotkova M, Gabrielsson B, Lonn M, Hanson LA, Strandvik B. Leptin levels in rat offspring are modified by the ratio of linoleic to alpha-linolenic acid in the maternal diet. J Lipid Res. 2002;43:1743–1749
  45. Amusquivar E, Ruperez FJ, Barbas C, Herrera E. Low arachidonic acid rather than alpha-tocopherol is responsible for the delayed postnatal development in offspring of rats fed fish oil instead of olive oil during pregnancy and lactation. J Nutr. 2000;130:2855–2865
  46. Komlos J, Breitfelder A. Differences in the physical growth of US-born black and white children and adolescents ages 2–19, born 1942–2002. Ann Hum Biol. 2008;35:11–21
  47. Hundley BT. U.S. black women shrinking, data show; 2008. Available at: http://seattletimes.nwsource.com/html/health/2008560510_shrink26html. Accessed October 9, 2009.
  48. Goyens PL, Spilker ME, Zock PL, Katan MB, Mensink RP. Conversion of alpha-linolenic acid in humans is influenced by the absolute amounts of alpha-linolenic acid and linoleic acid in the diet and not by their ratio. Am J Clin Nutr. 2006;84:44–53
  49. Hilakivi-Clarke L, Clarke R, Onojafe I, Raygada M, Cho E, Lippman M. A maternal diet high in n-6 polyunsaturated fats alters mammary gland development, puberty onset, and breast cancer risk among female rat offspring. Proc Natl Acad Sci U S A. 1997;94:9372–9377
  50. Hilakivi-Clarke L, Stoica A, Raygada M, Martin MB. Consumption of a high-fat diet alters estrogen receptor content, protein kinase C activity, and mammary gland morphology in virgin and pregnant mice and female offspring. Cancer Res. 1998;58:654–660
  51. Abayasekara DR, Wathes DC. Effects of altering dietary fatty acid composition on prostaglandin synthesis and fertility. Prostaglandins Leukot Essent Fatty Acids. 1999;61:275–287
  52. Oken E, Osterdal ML, Gillman MW, Knudsen VK, Halldorsson TI, Strom M, et al. Associations of maternal fish intake during pregnancy and breastfeeding duration with attainment of developmental milestones in early childhood: a study from the Danish National Birth Cohort. Am J Clin Nutr. 2008;88:789–796
  53. Buck Louis GM, Gray LE, Marcus M, Ojeda SR, Pescovitz OH, Witchel SF, et al. Environmental factors and puberty timing: expert panel research needs. Pediatrics. 2008;121(Suppl 3):S192–S207

 This study was assisted by research grants from SECyT-UNC, Ministerio de Ciencia y Tecnología, Córdoba, and SECyT-UNLaR.

PII: S0899-9007(09)00251-2

doi: 10.1016/j.nut.2009.06.005

Nutrition
Volume 26, Issue 4 , Pages 423-431 , April 2010