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Reduced Maternal Erythrocyte Long Chain Polyunsaturated Fatty Acids Exist in Early Pregnancy in Preeclampsia

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Lipids

Abstract

The present prospective study examines proportions of maternal erythrocyte fatty acids across gestation and their association with cord erythrocyte fatty acids in normotensive control (NC) and preeclamptic pregnancies. We hypothesize that maternal fatty acid status in early pregnancy influences fetal fatty acid stores in preeclampsia. 137 NC women and 58 women with preeclampsia were included in this study. Maternal blood was collected at 3 time points during pregnancy (16–20th weeks, 26–30th weeks and at delivery). Cord blood was collected at delivery. Fatty acids were analyzed using gas chromatography. The proportions of maternal erythrocyte α-linolenic acid, docosahexaenoic acid, nervonic acid, and monounsaturated fatty acids (MUFA) (p < 0.05 for all) were lower while total n-6 fatty acids were higher (p < 0.05) at 16–20th weeks of gestation in preeclampsia as compared with NC. Cord 18:3n-3, 22:6n-3, 24:1n-9, MUFA, and total n-3 fatty acids (p < 0.05 for all) were also lower in preeclampsia as compared with NC. A positive association was observed between maternal erythrocyte 22:6n-3 and 24:1n-9 at 16–20th weeks with the same fatty acids in cord erythrocytes (p < 0.05 for both) in preeclampsia. Our study for the first time indicates alteration in maternal erythrocyte fatty acids at 16th weeks of gestation which is further reflected in cord erythrocytes at delivery in preeclampsia.

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Abbreviations

ALA, 18:3n-3:

α-Linolenic acid

ARA, 20:4n-6:

Arachidonic acid

BMI:

Body mass index

DGLA, 20:3n-6:

Dihomogamma linolenic acid

DHA, 22:6n-3:

Docosahexaenoic acid

EFA:

Essential fatty acids

EDTA:

Ethylenediaminetetraacetic acid

LNA, 18:2n-6:

Linoleic acid

LCPUFA:

Long chain polyunsaturated fatty acids

MUFA:

Monounsaturated fatty acids

NA, 24:1n-9:

Nervonic acid

NC:

Normotensive control

PUFA:

Polyunsaturated fatty acids

SFA:

Saturated fatty acids

References

  1. Roberts JM, Pearsons G, Cutler J, Lindheimer M (2003) Summary of the NHLBI Working Group on research on hypertension during pregnancy. Hypertension 41:437–445

    Article  PubMed  CAS  Google Scholar 

  2. George EM, Granger JP (2010) Recent insights into the pathophysiology of preeclampsia. Expert Rev Obstet Gynecol 5:557–566

    Article  PubMed  PubMed Central  Google Scholar 

  3. Davis EF, Lazdam M, Lewandowski AJ, Worton SA, Kelly B, Kenworthy Y, Adwani S, Wilkinson AR, McCormick K, Sargent I, Redman C, Leeson P (2012) Cardiovascular risk factors in children and young adults born to preeclamptic pregnancies: a systematic review. Pediatrics 129:e1552–e1561

    Article  PubMed  Google Scholar 

  4. Hakim J, Senterman MK, Hakim AM (2013) Preeclampsia is a biomarker for vascular disease in both mother and child: the need for a medical alert system. Int J Pediatr 2013:953150

    Article  PubMed  PubMed Central  Google Scholar 

  5. Bell MJ (2010) A historical overview of preeclampsia-eclampsia. J Obstet Gynecol Neonatal Nurs 39:510–518

    Article  PubMed  PubMed Central  Google Scholar 

  6. Wu G, Imhoff-Kunsch B, Girard AW (2012) Biological mechanisms for nutritional regulation of maternal health and fetal development. Paediatr Perinat Epidemiol 26:4–26

    Article  PubMed  Google Scholar 

  7. Duttaroy AK (2000) Transport mechanisms for long-chain polyunsaturated fatty acids in the human placenta. Am J Clin Nutr 71:315–322

    Google Scholar 

  8. Al MD, van Houwelingen AC, Badart-Smook A, Hasaart TH, Roumen FJ, Hornstra G (1995) The essential fatty acid status of mother and child in pregnancy-induced hypertension: a prospective longitudinal study. Am J Obstet Gynecol 172:1605–1614

    Article  PubMed  CAS  Google Scholar 

  9. Otto SJ, Houwelingen AC, Antal M, Manninen A, Godfrey K, Lopez-Jaramillo P, Hornstra G (1997) Maternal and neonatal essential fatty acid status in phospholipids: an international comparative study. Eur J Clin Nutr 51:232–242

    Article  PubMed  CAS  Google Scholar 

  10. Haggarty P (2004) Effect of placental function on fatty acid requirements during pregnancy. Eur J Clin Nutr 58:1559–1570

    Article  PubMed  CAS  Google Scholar 

  11. Haggarty P (2014) Meeting the fetal requirement for polyunsaturated fatty acids in pregnancy. Curr Opin Clin Nutr Metab Care 17:151–155

    Article  PubMed  CAS  Google Scholar 

  12. Carlson SE, Colombo J, Gajewski BJ, Gustafson KM, Mundy D, Yeast J, Georgieff MK, Markley LA, Kerling EH, Shaddy DJ (2013) DHA supplementation and pregnancy outcomes. Am J Clin Nutr 97:808–815

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. Elias SL, Innis SM (2001) Infant plasma trans, n-6, and n-3 fatty acids and conjugated linoleic acids are related to maternal plasma fatty acids, length of gestation, and birth weight and length. Am J Clin Nutr 73:807–814

    PubMed  CAS  Google Scholar 

  14. Koletzko B, Braun M (1991) Arachidonic acid and early human growth: is there a relation? Ann Nutr Metab 35:128–131

    Article  PubMed  CAS  Google Scholar 

  15. Simpson JL, Bailey LB, Pietrzik K, Shane B, Holzgreve W (2011) Micronutrients and women of reproductive potential: required dietary intake and consequences of dietary deficiency or excess. Part II–vitamin D, vitamin A, iron, zinc, iodine, essential fatty acids. J Matern Fetal Neonatal Med 24:1–24

    Article  PubMed  CAS  Google Scholar 

  16. Wainwright PE (2002) Dietary essential fatty acids and brain function: a developmental perspective on mechanisms. Proc Nutr Soc 61:61–69

    Article  PubMed  CAS  Google Scholar 

  17. Bradbury J (2011) Docosahexaenoic acid (DHA): an ancient nutrient for the modern human brain. Nutrients 3:529–554

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  18. Lund EK (2013) Health benefits of seafood; is it just the fatty acids? Food Chem 140:413–420

    Article  PubMed  CAS  Google Scholar 

  19. Jump DB (2002) The biochemistry of n-3 polyunsaturated fatty acids. J Biol Chem 277:8755–8758

    Article  PubMed  CAS  Google Scholar 

  20. Heaton AE, Meldrum SJ, Foster JK, Prescott SL, Simmer K (2013) Does docosahexaenoic acid supplementation in term infants enhance neurocognitive functioning in infancy? Front Hum Neurosci 7:774

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. SanGiovanni JP, Chew EY (2005) The role of omega-3 long-chain polyunsaturated fatty acids in health and disease of the retina. Prog Retin Eye Res 24:87–138

    Article  PubMed  CAS  Google Scholar 

  22. Wauben IPM, Wainwright PE (1999) The influence of neonatal nutrition on behavioural development: a critical appraisal. Nutr Rev 57:35–44

    Article  PubMed  CAS  Google Scholar 

  23. Rutherford MA, Supramaniam V, Ederies A, Chew A, Bassi L, Groppo M, Anjari M, Counsell S, Ramenghi LA (2010) Magnetic resonance imaging of white matter diseases of prematurity. Neuroradiology 52:505–521

    Article  PubMed  Google Scholar 

  24. Georgieff MK (2007) Nutrition and the developing brain: nutrient priorities and measurement. Am J Clin Nutr 85:614S–620S

    PubMed  CAS  Google Scholar 

  25. Cetin I, Koletzko B (2008) Long-chain omega-3 fatty acid supply in pregnancy and lactation. Curr Opin Clin Nutr Metab Care 11:297–302

    Article  PubMed  CAS  Google Scholar 

  26. Mackay VA, Huda SS, Stewart FM, Tham K, McKenna LA, Martin I, Jordan F, Brown EA, Hodson L, Greer IA, Meyer BJ, Freeman DJ (2012) Preeclampsia is associated with compromised maternal synthesis of long-chain polyunsaturated fatty acids, leading to offspring deficiency. Hypertension 60:1078–1085

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Qiu C, Sanchez SE, Larrabure G, David R, Bralley JA, Williams MA (2006) Erythrocyte omega-3 and omega-6 polyunsaturated fatty acids and preeclampsia risk in Peruvian women. Arch Gynecol Obstet 274:97–103

    Article  PubMed  CAS  Google Scholar 

  28. Wang Y, Walsh SW, Kay HH (2005) Placental tissue levels of nonesterified polyunsaturated fatty acids in normal and preeclamptic pregnancies. Hypertens Pregnancy 24:235–245

    Article  PubMed  CAS  Google Scholar 

  29. Williams MA, Zingheim RW, King IB, Zebelman AM (1995) Omega-3 fatty acids in maternal erythrocytes and risk of preeclampsia. Epidemiology 6:232–237

    Article  PubMed  CAS  Google Scholar 

  30. Mahomed K, Williams MA, King IB, Mudzamiri S, Woelk GB (2007) Erythrocyte omega-3, omega-6 and trans fatty acids in relation to risk of preeclampsia among women delivering at Harare Maternity Hospital, Zimbabwe. Physiol Res 56:37–50

    PubMed  CAS  Google Scholar 

  31. Bakheit KH, Ghebremeskel K, Pol K, Elbashir MI, Adam I (2010) Erythrocyte omega-3 and omega-6 fatty acids profile in Sudanese women with pre-eclampsia. J Obstet Gynaecol 30:151–154

    Article  PubMed  CAS  Google Scholar 

  32. Kulkarni A, Mehendale S, Pisal H, Kilari A, Dangat K, Salunkhe S, Taralekar V, Joshi S (2011) Association of omega-3 fatty acids and homocysteine concentrations in pre-eclampsia. Clin Nutr 30:60–64

    Article  PubMed  CAS  Google Scholar 

  33. Kulkarni AV, Mehendale SS, Yadav HR, Joshi SR (2011) Reduced placental docosahexaenoic acid levels associated with increased levels of sFlt-1 in preeclampsia. Prostaglandins Leukot Essent Fatty Acids 84:51–55

    Article  PubMed  CAS  Google Scholar 

  34. Dangat KD, Mehendale SS, Yadav HR, Kilari AS, Kulkarni AV, Taralekar VS, Joshi SR (2010) Long-chain polyunsaturated fatty acid composition of breast milk in pre-eclamptic mothers. Neonatology 97:190–194

    Article  PubMed  CAS  Google Scholar 

  35. Mehendale S, Kilari A, Dangat K, Taralekar V, Mahadik S, Joshi S (2008) Fatty acids, antioxidants, and oxidative stress in pre-eclampsia. Int J Gynaecol Obstet 100:234–238

    Article  PubMed  CAS  Google Scholar 

  36. Wadhwani N, Patil V, Pisal H, Joshi A, Mehendale S, Gupte S, Wagh G, Joshi S (2014) Altered maternal proportions of long chain polyunsaturated fatty acids and their transport leads to disturbed fetal stores in preeclampsia. Prostaglandins Leukot Essent Fatty Acids 91:21–30

    Article  PubMed  CAS  Google Scholar 

  37. Sun Q, Ma J, Campos H, Hankinson SE, Hu FB (2007) Comparison between plasma and erythrocyte fatty acid content as biomarkers of fatty acid intake in US women. Am J Clin Nutr 86:74–81

    PubMed  CAS  Google Scholar 

  38. American College of Obstetricians and Gynecologists (ACOG) (2013) Report of the American College of Obstetricians and Gynecologists’ task force on hypertension in pregnancy. Obstet Gynecol 122:1122–1131

    Article  Google Scholar 

  39. Kilari AS, Mehendale SS, Dangat KD, Yadav HR, Gupta A, Taralekar VS, Joshi SR (2010) Long chain polyunsaturated fatty acids in mothers of preterm babies. J Perinat Med 38:659–664

    PubMed  Google Scholar 

  40. Kilari AS, Mehendale SS, Dangat KD, Yadav HR, Kulakarni AV, Dhobale MV, Taralekar VS, Joshi SR (2009) Long chain polyunsaturated fatty acids in mothers and term babies. J Perinat Med 37:513–518

    PubMed  CAS  Google Scholar 

  41. Dhobale M, Mehendale S, Pisal H, D’Souza V, Joshi S (2012) Association of brain-derived neurotrophic factor and tyrosine kinase B receptor in pregnancy. Neuroscience 216:31–37

    Article  PubMed  CAS  Google Scholar 

  42. Wadhwani NS, Pisal HR, Mehendale SS, Joshi SR (2015) A prospective study of maternal fatty acids, micronutrients and homocysteine and their association with birth outcome. Matern Child Nutr 11:559–573

    Article  PubMed  Google Scholar 

  43. van Gool CJ, Thijs C, Dagnelie PC, Henquet CJ, van Houwelingen AC, Schrander J, Menheere PP, van den Brandt PA (2004) Determinants of neonatal IgE level: parity, maternal age, birth season and perinatal essential fatty acid status in infants of atopic mothers. Allergy 59:961–968

    Article  PubMed  Google Scholar 

  44. Baack ML, Puumala SE, Messier SE, Pritchett DK, Harris WS (2015) What is the relationship between gestational age and docosahexaenoic acid (DHA) and arachidonic acid (ARA) levels?. Prostaglandins Leukot Essent Fatty Acids. 100:5–11. doi:10.1016/j.plefa.2015.05.003 (In press)

    Article  PubMed  CAS  Google Scholar 

  45. Yeh LL, Kuller LH, Bunker CH, Ukoli FA, Huston SL, Terrell DF (1996) The role of socioeconomic status and serum fatty acids in the relationship between intake of animal foods and cardiovascular risk factors. Ann Epidemiol 6(4):290–298

    Article  PubMed  CAS  Google Scholar 

  46. Cohen BE, Garg SK, Ali S, Harris WS, Whooley MA (2008) Red blood cell docosahexaenoic acid and eicosapentaenoic acid concentrations are positively associated with socioeconomic status in patients with established coronary artery disease: data from the Heart and Soul Study. J Nutr 138:1135–1140

    PubMed  PubMed Central  CAS  Google Scholar 

  47. Sands SA, Reid KJ, Windsor SL, Harris WS (2005) The impact of age, body mass index, and fish intake on the EPA and DHA content of human erythrocytes. Lipids 40:343–347

    Article  PubMed  CAS  Google Scholar 

  48. Hamosh M, Goldman AS (eds) (2012) Human lactation 2: maternal and environmental factors. Springer Science & Business Media, Berlin

    Google Scholar 

  49. Fuhrman BJ, Barba M, Krogh V, Micheli A, Pala V, Lauria R, Chajes V, Riboli E, Sieri S, Berrino F, Muti P (2006) Erythrocyte-membrane phospholipid composition as a biomarker of dietary fat. Ann Nutr Metab 50:95–102

    Article  PubMed  CAS  Google Scholar 

  50. Katan MB, Deslypere JP, van Birgelen AP, Penders M, Zegwaard M (1997) Kinetics of the incorporation of dietary fatty acids into serum cholesteryl esters, erythrocyte membranes, and adipose tissue: an 18-month controlled study. J Lipid Res 38:2012–2022

    PubMed  CAS  Google Scholar 

  51. Hon GM, Abel S, Smuts CM, van Jaarsveld P, Hassan MS, van Rensburg SJ, Erasmus RT, Matsha T (2012) Gas chromatography results interpretation: absolute amounts versus relative percentages. In: Bekir Salih, Ömür Çelikbıçak (eds) Gas Chromatography–Biochemicals, Narcotics Essential Oils, In Tech

  52. Weiler H, Fitzpatrick-Wong S, Schellenberg J, McCloy U, Veitch R, Kovacs H, Kohut J, Kin Yuen C (2005) Maternal and cord blood long-chain polyunsaturated fatty acids are predictive of bone mass at birth in healthy term-born infants. Pediatr Res 58:1254–1258

    Article  PubMed  CAS  Google Scholar 

  53. Wetzka B, Nüsing R, Charnock-Jones DS, Schäfer W, Zahradnik HP, Smith SK (1997) Cyclooxygenase-1 and -2 in human placenta and placental bed after normal and preeclamptic pregnancies. Hum Reprod 12:2313–2320

    Article  PubMed  CAS  Google Scholar 

  54. Patterson E, Wall R, Fitzgerald GF, Ross RP, Stanton C (2012) Health implications of high dietary omega-6 polyunsaturated fatty acids. J Nutr Metab 2012:539426

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  55. Uauy R, Mena P, Rojas C (2000) Essential fatty acids in early life: structural and functional role. Proc Nutr Soc 59:3–15

    Article  PubMed  CAS  Google Scholar 

  56. Harris WS (2006) The omega-6/omega-3 ratio and cardiovascular disease risk: uses and abuses. Curr Atheroscler Rep 8:453–459

    Article  PubMed  CAS  Google Scholar 

  57. Simopoulos AP (2002) Omega-3 fatty acids in inflammation and autoimmune diseases. J Am Coll Nutr 21:495–505

    Article  PubMed  CAS  Google Scholar 

  58. Bascuñán KA, Valenzuela R, Chamorro R, Valencia A, Barrera C, Puigrredon C, Sandoval J, Valenzuela A (2014) Polyunsaturated fatty acid composition of maternal diet and erythrocyte phospholipid status in Chilean pregnant women. Nutrients 6:4918–4934

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Ntoumani E, Strandvik B, Sabel KG (2013) Nervonic acid is much lower in donor milk than in milk from mothers delivering premature infants–of neglected importance? Prostaglandins Leukot Essent Fatty Acids 89:241–244

    Article  PubMed  CAS  Google Scholar 

  60. Assies J, Pouwer F, Lok A, Mocking RJ, Bockting CL, Visser I, Abeling NG, Duran M, Schene AH (2010) Plasma and erythrocyte fatty acid patterns in patients with recurrent depression: a matched case-control study. PLoS One 5:e10635

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  61. Luxwolda MF, Kuipers RS, Sango WS, Kwesigabo G, Dijck-Brouwer DA, Muskiet FA (2012) A maternal erythrocyte DHA content of approximately 6 g % is the DHA status at which intrauterine DHA biomagnifications turns into bioattenuation and postnatal infant DHA equilibrium is reached. Eur J Nutr 51:665–675

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  62. Novak EM, King DJ, Innis SM (2012) Low linoleic acid may facilitate Δ6 desaturase activity and docosahexaenoic acid accretion in human fetal development. Prostaglandins Leukot Essent Fatty Acids 86:93–98

    Article  PubMed  CAS  Google Scholar 

  63. Arterburn LM, Hall EB, Oken H (2006) Distribution, interconversion, and dose response of n-3 fatty acids in humans. Am J Clin Nutr 83:1467S–1476S

    PubMed  CAS  Google Scholar 

  64. Xu H, Shatenstein B, Luo ZC, Wei S, Fraser W (2009) Role of nutrition in the risk of preeclampsia. Nutr Rev 67:639–657

    Article  PubMed  Google Scholar 

  65. Roberts JM, Balk JL, Bodnar LM, Belizan JM, Bergel E, Martinez A (2003) Nutrient involvement in preeclampsia. J Nutr 133:1684S–16892S

    PubMed  CAS  Google Scholar 

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Acknowledgments

The authors acknowledge all the subjects who volunteered in this study and nurses of Bharati Hospital and Gupte Hospital who helped in collecting the samples. The authors also acknowledge the Department of Biotechnology (DBT), Ministry of Science and Technology, India for partially funding this study (No BT/PR-10593/MED/12/396/2008). We also thank Council of Scientific and Industrial Research (CSIR), New Delhi, India for granting the Senior Research Fellowship (SRF) to Nisha S. Wadhwani.

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Authors and Affiliations

  1. Department of Nutritional Medicine, Interactive Research School for Health Affairs (IRSHA), Bharati Vidyapeeth Deemed University, Pune Satara Road, Pune, 411043, India

    Nisha S. Wadhwani, Ankita S. Narang & Sadhana R. Joshi

  2. Department of Obstetrics and Gynaecology, Bharati Medical College and Hospital, Bharati Vidyapeeth Deemed University, Pune, 411043, India

    Savita S. Mehendale & Girija N. Wagh

  3. Gupte Hospital and Research Centre, Pune, 411004, India

    Sanjay A. Gupte

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  1. Nisha S. Wadhwani
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  2. Ankita S. Narang
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  3. Savita S. Mehendale
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  4. Girija N. Wagh
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  5. Sanjay A. Gupte
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  6. Sadhana R. Joshi
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Correspondence to Sadhana R. Joshi.

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Wadhwani, N.S., Narang, A.S., Mehendale, S.S. et al. Reduced Maternal Erythrocyte Long Chain Polyunsaturated Fatty Acids Exist in Early Pregnancy in Preeclampsia. Lipids 51, 85–94 (2016). https://doi.org/10.1007/s11745-015-4098-5

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