A cross-sectional study of fatty acids and brain-derived neurotrophic factor (BDNF) in human milk from lactating women following vegan, vegetarian, and omnivore diets

Abstract

Purpose

Essential fatty acids are critical for brain growth and neurodevelopment in infancy. Maternal diet and supplement use have a significant impact on the fat composition of human milk. The objective of this study is to assess supplement utilization patterns and fatty acid and brain-derived neurotrophic factor (BDNF) concentrations in the breast milk of women following vegan, vegetarian, and omnivore diet patterns.

Methods

This is a cross-sectional, observational study of 74 lactating women in the United States following a vegan (n = 26), vegetarian (n = 22), or omnivore (n = 26) diet pattern. A single breast milk sample was collected from each participant and assessed for fatty acids and BDNF.

Results

Median unsaturated fatty acids in the breast milk of vegan, vegetarian, and omnivores, as a percentage of total fatty acids, was 66.0, 57.8, and 56.2%, respectively (p < 0.001). Total omega-3 percentages were 2.29% for vegans, 1.55% for vegetarians, and 1.46% for omnivores (p < 0.001). Docosahexaenoic acid percentages were not different by diet pattern, but over 80% of participants had milk concentrations below 0.30% of total fatty acids. Reports of omega-3 supplements use (10/74) and weekly seafood consumption (3/74) were limited. BDNF was not detectable in any samples.

Conclusions

Breast milk from vegans had significantly higher unsaturated fat and total omega-3 fats, and lower saturated fats, trans fats, and omega-6 to omega-3 ratios than their vegetarian and omnivore counterparts. Docosahexaenoic acid concentrations in breast milk were low regardless of maternal diet pattern, and were reflective of low seafood intake and supplement use.

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Abbreviations

ALA:

Alpha-linolenic acid

BDNF:

Brain derived neurotrophic factor

BSQ:

Basic screening questionnaire

DHA:

Docosahexaenoic acid

EPA:

Eicosapentaenoic acid

LA:

Linoleic acid (LA)

LCPUFA:

Long chain polyunsaturated fatty acids

References

  1. 1.

    Agriculture Research Service National Nutrient Database (2018) Milk, human, mature, fluid. https://ndb.nal.usda.gov/ndb/foods/. Accessed 12 Jan 2018

  2. 2.

    Dewey KG, Finley DA, Lönnerdal B (1984) Breast milk volume and composition during late lactation (7–20 months). J Pediatr Gastroenterol Nutr 3(5):713–720

    Article  CAS  PubMed  Google Scholar 

  3. 3.

    Allen JC, Keller RP, Archer P, Neville MC (1991) Studies in human lactation: milk composition and daily secretion rates of macronutrients in the first year of lactation. Am J Clin Nutr 54(1):69–80

    Article  CAS  Google Scholar 

  4. 4.

    Shehadeh N, Aslih N, Shihab S, Werman MJ, Sheinman R, Shamir R (2006) Human milk beyond one year post-partum: lower content of protein, calcium, and saturated very long-chain fatty acids. J Pediatr 148(1):122–124

    Article  PubMed  Google Scholar 

  5. 5.

    Choi A, Fusch G, Rochow N, Sheikh N, Fusch C (2015) Establishment of micromethods for macronutrient contents analysis in breast milk. Matern Child Nutr 11(4):761–772

    Article  PubMed  Google Scholar 

  6. 6.

    Perrin MT, Fogleman AD, Newburg DS, Allen JC (2017) A longitudinal study of human milk composition in the second year postpartum: implications for human milk banking. Matern Child Nutr. https://doi.org/10.1111/mcn.12239

    Article  PubMed  Google Scholar 

  7. 7.

    Yuhas R, Pramuk K, Lien EL (2006) Human milk fatty acid composition from nine countries varies most in DHA. Lipids 41(9):851–858

    Article  CAS  PubMed  Google Scholar 

  8. 8.

    Brenna JT, Varamini B, Jensen RG, Diersen-Schade DA, Boettcher JA, Arterburn LM (2007) Docosahexaenoic and arachidonic acid concentrations in human breast milk worldwide. Am J Clin Nutr 85(6):1457–1464

    Article  CAS  PubMed  Google Scholar 

  9. 9.

    Fu Y, Liu X, Zhou B, Jiang AC, Chai L (2016) An updated review of worldwide levels of docosahexaenoic and arachidonic acid in human breast milk by region. Public Health Nutr 19(15):2675–2687

    Article  PubMed  Google Scholar 

  10. 10.

    Brenna JT, Salem N, Sinclair AJ, Cunnane SC (2009) α-Linolenic acid supplementation and conversion to n-3 long-chain polyunsaturated fatty acids in humans. Prostaglandins Leukot Essent Fat Acids 80(2):85–91

    Article  CAS  Google Scholar 

  11. 11.

    Horta BL, Victora CG (2013) Long-term effects of breastfeeding: a systematic review [Internet]. The World Health Organization. http://apps.who.int/iris/bitstream/10665/79198/1/9789241505307_eng.pdf. Accessed 10 Jan 2018

  12. 12.

    Smithers LG, Kramer MS, Lynch JW (2015) Effects of breastfeeding on obesity and intelligence: causal insights from different study designs. JAMA Pediatr 169(8):707–708

    Article  PubMed  Google Scholar 

  13. 13.

    Heird WC, Lapillonne A (2005) The role of essential fatty acids in development. Annu Rev Nutr 25(1):549–571

    Article  CAS  PubMed  Google Scholar 

  14. 14.

    Innis SM (2000) The role of dietary n-6 and n-3 fatty acids in the developing brain. Dev Neurosci 22(5–6):474–480

    Article  CAS  PubMed  Google Scholar 

  15. 15.

    Austad N, Halter R, Hall RT, Blatter M, Bogle ML, Burks W et al (2001) Growth and development in term infants fed long-chain polyunsaturated fatty acids: a double-masked, randomized, parallel, prospective, multivariate study. Pediatrics 108(2):372–381

    Article  Google Scholar 

  16. 16.

    Innis SM (2014) Impact of maternal diet on human milk composition and neurological development of infants. Am J Clin Nutr 99(3):734S–741S

    Article  CAS  PubMed  Google Scholar 

  17. 17.

    Wu A, Ying Z, Gomez-Pinilla F (2004) Dietary omega-3 fatty acids normalize bdnf levels, reduce oxidative damage, and counteract learning disability after traumatic brain injury in rats. J Neurotrauma 21(10):1457–1467

    Article  PubMed  Google Scholar 

  18. 18.

    Rathod R, Khaire A, Kemse N, Kale A, Joshi S (2014) Maternal omega-3 fatty acid supplementation on vitamin B12 rich diet improves brain omega-3 fatty acids, neurotrophins and cognition in the Wistar rat offspring. Brain Dev 36(10):853–863

    Article  PubMed  Google Scholar 

  19. 19.

    Bondar NP, Merkulova TI (2016) Brain-derived neurotrophic factor and early-life stress: multifaceted interplay. J Biosci Publ Indian Acad Sci 41(4):751–758

    CAS  Google Scholar 

  20. 20.

    Ferreira CF, Bernardi JR, Bosa VL, Schuch I, Goldani MZ, Kapczinski F et al (2014) Correlation between n-3 polyunsaturated fatty acids consumption and BDNF peripheral levels in adolescents. Lipids Health Dis 13:44. https://doi.org/10.1186/1476-511X-13-44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Matsuoka Y, Nishi D, Tanima Y, Itakura M, Kojima M, Hamazaki K et al (2015) Serum pro-BDNF/BDNF as a treatment biomarker for response to docosahexaenoic acid in traumatized people vulnerable to developing psychological distress: a randomized controlled trial. Transl Psychiatry 5(7):e596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Nassar MF, Younis NT, El-Arab SE, Fawzi FA (2011) Neuro-developmental outcome and brain-derived neurotrophic factor level in relation to feeding practice in early infancy. Matern Child Nutr 7(2):188–197

    Article  PubMed  Google Scholar 

  23. 23.

    Li R, Xia W, Zhang Z, Wu K (2011) S100B protein, brain-derived neurotrophic factor, and glial cell line-derived neurotrophic factor in human milk. PLoS One 6(6):e21663

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Dangat K, Kilari A, Mehendale S, Lalwani S, Joshi S (2013) Higher levels of brain derived neurotrophic factor but similar nerve growth factor in human milk in women with preeclampsia. Int J Dev Neurosci 31(3):209–213

    Article  CAS  PubMed  Google Scholar 

  25. 25.

    Ismail AM, Babers GM, El Rehany MA (2015) Brain-derived neurotrophic factor in sera of breastfed epileptic infants and in breastmilk of their mothers. Breastfeed Med 10(5):277–282

    Article  PubMed  Google Scholar 

  26. 26.

    Potter JM, Nestel PJ (1976) The effects of dietary fatty acids and cholesterol on the milk lipids of lactating women and the plasma cholesterol of breast-fed infants. Am J Clin Nutr 29(1):54–60

    Article  CAS  PubMed  Google Scholar 

  27. 27.

    Yahvah KM, Brooker SL, Williams JE, Settles M, McGuire MA, McGuire MK (2015) Elevated dairy fat intake in lactating women alters milk lipid and fatty acids without detectible changes in expression of genes related to lipid uptake or synthesis. Nutr Res 35(3):221–228

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    Bravi F, Wiens F, Decarli A, Pont AD, Agostoni C, Ferraroni M (2016) Impact of maternal nutrition on breast-milk composition: a systematic review. Am J Clin Nutr 104(3):646

    Article  CAS  PubMed  Google Scholar 

  29. 29.

    Haddad EH, Berk LS, Kettering JD, Hubbard RW, Peters WR (1999) Dietary intake and biochemical, hematologic, and immune status of vegans compared with nonvegetarians. Am J Clin Nutr 70(3):586s–593s

    Article  CAS  PubMed  Google Scholar 

  30. 30.

    Davis BC, Kris-Etherton PM (2003) Achieving optimal essential fatty acid status in vegetarians: current knowledge and practical implications. Am J Clin Nutr 78(3):640S–646S

    Article  CAS  PubMed  Google Scholar 

  31. 31.

    Sanders TA, Ellis FR, Dickerson JW (1978) Studies of vegans: the fatty acid composition of plasma choline phosphoglycerides, erythrocytes, adipose tissue, and breast milk, and some indicators of susceptibility to ischemic heart disease in vegans and omnivore controls. Am J Clin Nutr 31(5):805–813

    Article  CAS  PubMed  Google Scholar 

  32. 32.

    Specker BL, Wey HE, Miller D (1987) Differences in fatty acid composition of human milk in vegetarian and nonvegetarian women: long-term effect of diet. J Pediatr Gastroenterol Nutr 6(5):764–768

    Article  CAS  PubMed  Google Scholar 

  33. 33.

    Sanders TA, Reddy S (1992) The influence of a vegetarian diet on the fatty acid composition of human milk and the essential fatty acid status of the infant. J Pediatr 120(4):71–77

    Article  Google Scholar 

  34. 34.

    Makrides M, Neumann MA, Gibson RA (1996) Effect of maternal docosahexaenoic acid (DHA) supplementation on breast milk composition. Eur J Clin Nutr 50(6):352–357

    CAS  PubMed  Google Scholar 

  35. 35.

    Fidler N, Sauerwald T, Pohl A, Demmelmair H, Koletzko B (2000) Docosahexaenoic acid transfer into human milk after dietary supplementation: a randomized clinical trial. J Lipid Res 41(9):1376–1383

    CAS  PubMed  Google Scholar 

  36. 36.

    Francois CA, Connor SL, Bolewicz LC, Connor WE (2003) Supplementing lactating women with flaxseed oil does not increase docosahexaenoic acid in their milk. Am J Clin Nutr 77(1):226–233

    Article  CAS  PubMed  Google Scholar 

  37. 37.

    Boris J, Jensen B, Salvig JD, Secher NJ, Olsen SF (2004) A randomized controlled trial of the effect of fish oil supplementation in late pregnancy and early lactation on the n-3 fatty acid content in human breast milk. Lipids 39(12):1191–1196

    Article  CAS  PubMed  Google Scholar 

  38. 38.

    Bergmann RL, Haschke-Becher E, Klassen-Wigger P, Bergmann KE, Richter R, Dudenhausen JW et al (2008) Supplementation with 200 mg/day docosahexaenoic acid from mid-pregnancy through lactation improves the docosahexaenoic acid status of mothers with a habitually low fish intake and of their infants. Ann Nutr Metab 52(2):157–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Pawlak R, Vos P, Shahab-Ferdows S, Hampel D, Allen LH, Perrin MT (2018) Vitamin B12 content in breast milk of vegan, vegetarian, and non-vegetarian lactating women in the United States. Am J Clin Nutr https://doi.org/10.1093/ajcn/nqy104

    Article  PubMed  Google Scholar 

  40. 40.

    Miller EM, Aiello MO, Fujita M, Hinde K, Milligan L, Quinn E (2013) Field and laboratory methods in human milk research. Am J Hum Biol 25(1):1–11

    Article  PubMed  Google Scholar 

  41. 41.

    Du J, Gay MC, Lai CT, Trengove RD, Hartmann PE, Geddes DT (2017) Comparison of gravimetric, creamatocrit and esterified fatty acid methods for determination of total fat content in human milk. Food Chem 217:505–510

    Article  CAS  PubMed  Google Scholar 

  42. 42.

    Bannon CD, Craske JD, Felder DL, Garland IJ, Norman LM (1987) Analysis of fatty acid methyl esters with high accuracy and reliability:VI. Rapid analysis by split injection capillary gas-liquid chromatography. J Chromatogr 407:231–241

    Article  CAS  PubMed  Google Scholar 

  43. 43.

    American Oil Chemists’ Society and Firestone D (2004) Official methods and recommended practices of the American Oil Chemists’ Society. AOCS, Champaign

    Google Scholar 

  44. 44.

    Okragly AJ, Haak-Frendscho M (1997) An acid-treatment method for the enhanced detection of GDNF in biological samples. Exp Neurol 145(2):592–596

    Article  CAS  PubMed  Google Scholar 

  45. 45.

    United States, Department of Health and Human Services, United States, Department of Agriculture, United States, Dietary Guidelines Advisory Committee (2015) Dietary guidelines for Americans, 2015–2020. https://health.gov/dietaryguidelines/2015/guidelines. Accessed 18 Jan 2018

  46. 46.

    Jahns L, Raatz SK, Johnson LK, Kranz S, Silverstein JT, Picklo MJ (2014) Intake of seafood in the US varies by age, income, and education level but not by race-ethnicity. Nutrients 6(12):6060–6075

    Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Koletzko B, Boey CCM, Campoy C, Carlson SE, Chang N, Guillermo-tuazon MA et al (2014) Current information and asian perspectives on long-chain polyunsaturated fatty acids in pregnancy, lactation, and infancy: systematic review and practice recommendations from an early nutrition academy workshop. Ann Nutr Metab 65(1):49–80

    Article  CAS  PubMed  Google Scholar 

  48. 48.

    Delgado-Noguera MF, Calvache JA, Bonfill Cosp X, Kotanidou EP, Galli-Tsinopoulou A (2015) Supplementation with long chain polyunsaturated fatty acids (LCPUFA) to breastfeeding mothers for improving child growth and development. Cochrane Database Syst Rev. https://doi.org/10.1002/14651858.CD007901.pub3

    Article  PubMed  Google Scholar 

  49. 49.

    Brenna JT, Lapillonne A (2009) Background paper on fat and fatty acid requirements during pregnancy and lactation. Ann Nutr Metab 55(1–3):97–122

    Article  CAS  PubMed  Google Scholar 

  50. 50.

    Kris-Etherton PM, Grieger JA, Etherton TD (2009) Dietary reference intakes for DHA and EPA. Prostaglandins Leukot Essent Fatty Acids 81:2–3

    Article  CAS  Google Scholar 

  51. 51.

    Federal Register (2015) Final determination regarding partially hydrogenated oils. https://www.federalregister.gov/documents/2015/06/17/2015-14883/final-determination-regarding-partially-hydrogenated-oils. Accessed 20 Jan 2018

  52. 52.

    Innis SM (1999) Trans fatty acids in human milk are inversely associated with concentrations of essential all-cis n-6 and n-3 fatty acids and determine trans, but not n-6 and n-3, fatty acids in plasma lipids of breast-fed infants. Am J Clin Nutr 70(3):383–390

    Article  CAS  PubMed  Google Scholar 

  53. 53.

    Mosley EE, Wright AL, McGuire MK, McGuire MA (2005) Trans fatty acids in milk produced by women in the United States. Am J Clin Nutr 82(6):1292–1297

    Article  CAS  PubMed  Google Scholar 

  54. 54.

    Friesen R, Innis SM (2006) Trans fatty acids in human milk in Canada declined with the introduction of trans fat food labeling. J Nutr 136(10):2558–2561

    Article  CAS  PubMed  Google Scholar 

  55. 55.

    Wang DD, Leung CW, Li Y, Ding EL, Chiuve SE, Hu FB et al (2014) Trends in dietary quality among adults in the United States, 1999 through 2010. JAMA Intern Med 174(10):1587

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Dangat K, Kilari A, Joshi S, Mehendale S, Lalwani S (2014) Preeclampsia alters milk neurotrophins and long chain polyunsaturated fatty acids. Int J Dev Neurosci 33(1):115–121

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This research received funding from the Academy of Nutrition and Dietetics, Vegetarian Nutrition Dietary Practice Group.

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Contributions

MTP and RP designed the study. MTP, RP, LLD, AC and LF conducted research. MTP analyzed data and wrote paper. MTP has primary responsibility for final content. All authors read and approved the final manuscript.

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Correspondence to Maryanne T. Perrin.

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On behalf of all authors, the corresponding author states that there is no conflict of interest.

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Perrin, M.T., Pawlak, R., Dean, L.L. et al. A cross-sectional study of fatty acids and brain-derived neurotrophic factor (BDNF) in human milk from lactating women following vegan, vegetarian, and omnivore diets. Eur J Nutr 58, 2401–2410 (2019). https://doi.org/10.1007/s00394-018-1793-z

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Keywords

  • Human milk
  • Breast milk
  • Brain derived neurotrophic factor
  • Docosahexaenoic acid
  • Vegetarian
  • Vegan