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ABSTRACT BACKGROUND/OBJECTIVES Maternal dietary patterns were associated with embryonic growth and congenital anomalies. We aim to evaluate associations between early first trimester
maternal dietary patterns and embryonic morphological development among pregnancies with non-malformed outcome. SUBJECTS/METHODS A total of 228 strictly dated, singleton pregnancies without
congenital malformations were enrolled in a periconceptional hospital-based cohort. Principal component analysis was performed to extract early first trimester maternal dietary patterns from
food frequency questionnaires. Serial transvaginal three-dimensional ultrasound (3D US) scans were performed between 6+0 and 10+2 gestational weeks and internal and external morphological
criteria were used to define Carnegie stages in a virtual reality system. Associations between dietary patterns and Carnegie stages were investigated using linear mixed models. RESULTS A
total of 726 3D US scans were included (median: three scans per pregnancy). The ‘high fish and olive oil and low meat’ dietary pattern was associated with accelerated embryonic development
in the study population (_β_ = 0.12 (95%CI: 0.00; 0.24), _p_ < 0.05). Weak adherence to this dietary pattern delayed embryonic development by 2.1 days (95%CI: 1.6; 2.6) compared to strong
adherence. The ‘high vegetables, fruit and grain’ dietary pattern accelerated embryonic development in the strictly dated spontaneous pregnancy subgroup without adjustment for energy
intake. CONCLUSIONS Early first trimester maternal dietary patterns impacts human embryonic morphological development among pregnancies without congenital malformations. The clinical meaning
of delayed embryonic development needs further investigation. Access through your institution Buy or subscribe This is a preview of subscription content, access via your institution ACCESS
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access 20 November 2023 REFERENCES * Fleming TP, Watkins AJ, Sun C, Velazquez MA, Smyth NR, Eckert JJ. Do little embryos make big decisions? How maternal dietary protein restriction can
permanently change an embryo’s potential, affecting adult health. Reprod Fertil Dev. 2015;27:684–92. Article CAS PubMed Google Scholar * Williams L, Seki Y, Vuguin PM, Charron MJ. Animal
models of in utero exposure to a high fat diet: a review. Biochim Biophys Acta. 2014;1842:507–19. Article CAS PubMed Google Scholar * Sinclair KD, Watkins AJ. Parental diet, pregnancy
outcomes and offspring health: metabolic determinants in developing oocytes and embryos. Reprod Fertil Dev. 2013;26:99–114. Article CAS PubMed Google Scholar * Steegers-Theunissen RP,
Twigt J, Pestinger V, Sinclair K. The periconceptional period, reproduction and long-term health of offspring: the importance of one-carbon metabolism. Hum Reprod Update. 2013;19:640–55.
Article CAS PubMed Google Scholar * Bouwland-Both MI, Steegers-Theunissen RP, Vujkovic M, Lesaffre EM, Mook-Kanamori DO, Hofman A, et al. A periconceptional energy-rich dietary pattern
is associated with early fetal growth: the Generation R study. BJOG. 2013;120:435–45. Article CAS PubMed Google Scholar * van Uitert EM, van Ginkel S, Willemsen SP, Lindemans J, Koning
AH, Eilers PH, et al. An optimal periconception maternal folate status for embryonic size: the Rotterdam Predict study. BJOG. 2014;121:821–9. Article CAS PubMed Google Scholar *
O’Rahilly R. Human embryo. Nature. 1987;329:385. Article PubMed Google Scholar * O’Rahilly R, Müller F. Developmental stages in human embryos: revised and new measurements. Cells Tissues
Organs. 2010;192:73–84. Article PubMed Google Scholar * Blaas HG. The examination of the embryo and early fetus: how and by whom? Ultrasound Obstet Gynecol. 1999;14:153–8. Article CAS
PubMed Google Scholar * Blaas HG, Eik-Nes SH, Berg S, Torp H. In-vivo three-dimensional ultrasound reconstructions of embryos and early fetuses. Lancet. 1998;352:1182–6. Article CAS
PubMed Google Scholar * Rousian M, Koning AH, van Oppenraaij RH, Hop WC, Verwoerd-Dikkeboom CM, van der Spek PJ, et al. An innovative virtual reality technique for automated human
embryonic volume measurements. Hum Reprod. 2010;25:2210–6. Article CAS PubMed Google Scholar * Verwoerd-Dikkeboom CM, Koning AH, Hop WC, Rousian M, Van Der Spek PJ, Exalto N, et al.
Reliability of three-dimensional sonographic measurements in early pregnancy using virtual reality. Ultrasound Obstet Gynecol. 2008;32:910–6. Article CAS PubMed Google Scholar *
Verwoerd-Dikkeboom CM, Koning AH, van der Spek PJ, Exalto N, Steegers EA. Embryonic staging using a 3D virtual reality system. Hum Reprod. 2008;23:1479–84. Article CAS PubMed Google
Scholar * Steegers-Theunissen RP, Verheijden-Paulissen JJ, van Uitert EM, Wildhagen MF, Exalto N, Koning AH, et al. Cohort profile: the rotterdam periconceptional cohort (predict study).
Int J Epidemiol. 2016;45:374–81. Article PubMed Google Scholar * Robinson HP. Sonar measurement of fetal crown rump length as means of assessing maturity in first trimester of pregnancy.
Br Med J. 1973;4:28–31. Article CAS PubMed PubMed Central Google Scholar * Siebelink E, Geelen A, de Vries JH. Self-reported energy intake by FFQ compared with actual energy intake to
maintain body weight in 516 adults. Br J Nutr. 2011;106:274–81. Article CAS PubMed Google Scholar * Verkleij-Hagoort AC, de Vries JH, Stegers MP, Lindemans J, Ursem NT,
Steegers-Theunissen RP. Validation of the assessment of folate and vitamin B12 intake in women of reproductive age: the method of triads. Eur J Clin Nutr. 2007;61:610–5. Article CAS PubMed
Google Scholar * Netherlands Nutrition Centre. NEVO-tabel; Nederlands Voedingsstoffenbestand 2011, RIVM/Voedingscentrum, Den Haag. 2011,
https://www.rivm.nl/en/Topics/D/Dutch_Food_Composition_Database/Publications. * Marjonen H, Sierra A, Nyman A, Rogojin V, Gröhn O, Linden AM, et al. Early maternal alcohol consumption alters
hippocampal DNA methylation, gene expression and volume in a mouse model. PLoS One. 2015;10:e0124931. Article CAS PubMed PubMed Central Google Scholar * van Uitert EM, van der
Elst-Otte N, Wilbers JJ, Exalto N, Willemsen SP, Eilers PH, et al. Periconception maternal characteristics and embryonic growth trajectories: the Rotterdam Predict Study. Hum Reprod.
2013;28:3188–96. Article CAS PubMed Google Scholar * Hoffmann K, Schulze MB, Achienkiewitz A, Nothlings U, Boeing H. Application of a new statistical method to derive dietary patterns in
nutritional epidemiology. Am J Epidemiol. _2004_;159:935–44. Article PubMed Google Scholar * Vujkovic M, Ocke MC, van der Spek PJ, Yazdanpanah N, Steegers EA, Steegers-Theunissen RP.
Maternal western dietary patterns and the risk of developing a cleft lip with or without a cleft palate. Obstet Gynecol. 2007;110:378–84. Article PubMed Google Scholar * Rousian M, Koning
AH, van der Spek PJ, Steegers EA, Exalto N. Virtual reality for embryonic measurements requiring depth perception. Fertil Steril. 2011;95:773–4. Article PubMed Google Scholar *
Ramirez-Zea M. Validation of three predictive equations for basal metabolic rate in adults. Public Health Nutr. 2005;8:1213–28. Article PubMed Google Scholar * Parisi F, Rousian M,
Huijgen NA, Koning AH, Willemsen SP, de Vries JH, et al. Periconceptional maternal ‘high fish and olive oil, low meat’ dietary pattern is associated with increased embryonic growth: The
Rotterdam Periconceptional Cohort (Predict Study). Ultrasound Obstet Gynecol. 2017;50:709–16. Article CAS PubMed Google Scholar * Rogers I, Emmett P, Ness A, Golding J. Maternal fish
intake in late pregnancy and the frequency of low birth weight and intrauterine growth retardation in a cohort of British infants. J Epidemiol Community Health. 2004;58:486–92. Article CAS
PubMed PubMed Central Google Scholar * Thorsdottir I, Birgisdottir BE, Halldorsdottir S, Geirsson RT. Association of fish and fish liver oil intake in pregnancy with infant size at
birth among women of normal weight before pregnancy in a fishing community. Am J Epidemiol. 2004;160:460–5. Article PubMed Google Scholar * Stratakis N, Roumeliotaki T, Oken E, Barros H,
Basterrechea M, Charles MA, et al. Fish intake in pregnancy and child growth: a pooled analysis of 15 European and US birth cohorts. JAMA Pediatr. 2016;170:381–90. Article PubMed PubMed
Central Google Scholar * Braga DP, Halpern G, Setti AS, Figueira RC, Iaconelli A Jr, Borges E Jr.. The impact of food intake and social habits on embryo quality and the likelihood of
blastocyst formation. Reprod Biomed Online. 2015;31:30–38. Article PubMed Google Scholar * Hammiche F, Vujkovic M, Wijburg W, de Vries JH, Macklon NS, Laven JS, et al. Increased
preconception omega-3 polyunsaturated fatty acid intake improves embryo morphology. Fertil Steril. 2011;95:1820–3. Article CAS PubMed Google Scholar * Obermann-Borst SA, Vujkovic M, de
Vries JH, Wildhagen MF, Looman CW, de Jonge R, et al. A maternal dietary pattern characterised by fish and seafood in association with the risk of congenital heart defects in the offspring.
BJOG. 2011;118:1205–15. Article CAS PubMed Google Scholar * Ramaiyan B, Bettadahalli S, Talahalli RR. Dietary omega-3 but not omega-6 fatty acids down-regulate maternal dyslipidemia
induced oxidative stress: A three generation study in rats. Biochem Biophys Res Commun. 2016;477:887–94. Article CAS PubMed Google Scholar * Ornoy A. Embryonic oxidative stress as a
mechanism of teratogenesis with special emphasis on diabetic embryopathy. Reprod Toxicol. 2007;24:31–41. Article CAS PubMed Google Scholar * Waters SM, Coyne GS, Kenny DA, MacHugh DE,
Morris DG. Dietary n-3 polyunsaturated fatty acid supplementation alters the expression of genes involved in the control of fertility in the bovine uterine endometrium. Physiol Genom.
2012;44:878–88. Article CAS Google Scholar * Sidhu KS. Health benefits and potential risks related to consumption of fish or fish oil. Regul Toxicol Pharmacol. 2003;38:336–44. Article
CAS PubMed Google Scholar * Higa R, Roberti SL, Musikant D, Mazzucco MB, White V, Jawerbaum A. Effects of maternal dietary olive oil on pathways involved in diabetic embryopathy. Reprod
Toxicol. 2014;49:185–95. Article CAS PubMed Google Scholar * Xia W, Chiu YH, Williams PL, Gaskins AJ, Toth TL, Tanrikut C, et al. Men’s meat intake and treatment outcomes among couples
undergoing assisted reproduction. Fertil Steril. 2015;104:972–9. Article PubMed PubMed Central Google Scholar * Knudsen VK, Orozova-Bekkevold IM, Mikkelsen TB, Wolff S, Olsen SF. Major
dietary patterns in pregnancy and fetal growth. Eur J Clin Nutr. 2008;62:463–70. Article CAS PubMed Google Scholar * Larqué E, Zamora S, Gil A. Dietary trans fatty acids in early life: a
review. Early Hum Dev. 2001;65(Suppl):S31–S41. Article PubMed Google Scholar * Zhu J, Li M, Chen L, Liu P, Qiao J. The protein source in embryo culture media influences birthweight: a
comparative study between G1 v5 and G1-PLUS v5. Hum Reprod. 2014;29:1387–92. Article CAS PubMed Google Scholar * Mantikou E, Youssef MA, van Wely M, van der Veen F, Al-Inany HG, Repping
S, et al. Embryo culture media and IVF/ICSI success rates: a systematic review. Hum Reprod Update. 2013;19:210–20. Article CAS PubMed Google Scholar * Holst S, Kjær SK, Jørgensen ME,
Damm P, Jensen A. Fertility problems and risk of gestational diabetes mellitus: a nationwide cohort study. Fertil Steril. 2016;106:427. e1 Article PubMed Google Scholar * Jacques M,
Freour T, Barriere P, Ploteau S. Adverse pregnancy and neo-natal outcomes after assisted reproductive treatment in patients with pelvic endometriosis: a case-control study. Reprod Biomed
Online. 2016;32:626–34. Article PubMed Google Scholar * Bottomley C, Daemen A, Mukri F, Papageorghiou AT, Kirk E, Pexsters A, et al. Assessing first trimester growth: the influence of
ethnic background and maternal age. Hum Reprod. 2009;24:284–90. Article PubMed Google Scholar * Mook-Kanamori DO, Steegers EA, Eilers PH, Raat H, Hofman A, Jaddoe VW. Risk factors and
outcomes associated with first-trimester fetal growth restriction. JAMA. 2010;303:527–34. Article CAS PubMed Google Scholar * Jaddoe VW, de Jonge LL, Hofman A, Franco OH, Steegers EA,
Gaillard R. First trimester growth restriction and cardiovascular risk factors in childhood. BMJ. 2014;348:g14. Article CAS PubMed PubMed Central Google Scholar * Vujkovic M, Steegers
EA, Looman CW, Ocké MC, van der Spek PJ, Steegers-Theunissen RP. The maternal Mediterranean dietary pattern is associated with a reduced risk of spina bifida in the offspring. BJOG.
2009;116:408–15. Article CAS PubMed Google Scholar * Gluckman PD, Hanson MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res.
2004;56:311–7. Article Google Scholar * Skinner MK. What is an epigenetic transgenerational phenotype? F3 or F2. Reprod Toxicol. 2008;25:2–6. Article CAS PubMed Google Scholar *
Steegers-Theunissen RP, Steegers EA. Embryonic health: new insights, mHealth and personalised patient care. Reprod Fertil Dev. 2015;27:712–5. Article PubMed Google Scholar Download
references ACKNOWLEDGEMENTS We thank the Rotterdam periconception cohort team for contributions to recruitment, data collection, and cleaning. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS *
Department of Obstetrics and Gynecology, Erasmus MC, University Medical Centre, PO Box 2040, 3000 CA, Rotterdam, Netherlands Francesca Parisi, Melek Rousian, Régine P. M.
Steegers-Theunissen, Sten P. Willemsen & Eric A. P. Steegers * Department of Pediatrics, Division of Neonatology, Erasmus MC, University Medical Centre, 3015 GD, Rotterdam, Netherlands
Régine P. M. Steegers-Theunissen * Department of Bioinformatics, Erasmus MC, University Medical Centre, Dr. Molewaterplein 50-60, 3015 GE, Rotterdam, Netherlands Anton H. J. Koning *
Department of Biostatistics, Erasmus MC, University Medical Centre, PO Box 2040, 3000 CA, Rotterdam, Netherlands Sten P. Willemsen * Human Nutrition, Wageningen University, Bomenweg 2, 6700
EV, Wageningen, Netherlands Jeanne H. M. de Vries * Department of Biomedical and Clinical Sciences, Hospital Luigi Sacco, Università degli Studi di Milano, Milan, Italy Irene Cetin Authors *
Francesca Parisi View author publications You can also search for this author inPubMed Google Scholar * Melek Rousian View author publications You can also search for this author inPubMed
Google Scholar * Régine P. M. Steegers-Theunissen View author publications You can also search for this author inPubMed Google Scholar * Anton H. J. Koning View author publications You can
also search for this author inPubMed Google Scholar * Sten P. Willemsen View author publications You can also search for this author inPubMed Google Scholar * Jeanne H. M. de Vries View
author publications You can also search for this author inPubMed Google Scholar * Irene Cetin View author publications You can also search for this author inPubMed Google Scholar * Eric A.
P. Steegers View author publications You can also search for this author inPubMed Google Scholar CORRESPONDING AUTHOR Correspondence to Régine P. M. Steegers-Theunissen. ETHICS DECLARATIONS
CONFLICT OF INTEREST No conflicts of interests are declared. RST is CSO of the startup company Slimmere Zorg and CEO of eHealth Care Solutions. RIGHTS AND PERMISSIONS Reprints and
permissions ABOUT THIS ARTICLE CITE THIS ARTICLE Parisi, F., Rousian, M., Steegers-Theunissen, R.P.M. _et al._ Early first trimester maternal ‘high fish and olive oil and low meat’ dietary
pattern is associated with accelerated human embryonic development. _Eur J Clin Nutr_ 72, 1655–1662 (2018). https://doi.org/10.1038/s41430-018-0161-7 Download citation * Received: 27
November 2017 * Revised: 23 January 2018 * Accepted: 04 March 2018 * Published: 20 April 2018 * Issue Date: December 2018 * DOI: https://doi.org/10.1038/s41430-018-0161-7 SHARE THIS ARTICLE
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