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Similarities and differences of dietary and other determinants of iodine status in pregnant women from three European birth cohorts

  • Mariana Dineva
  • Margaret P. Rayman
  • Deborah Levie
  • Mònica Guxens
  • Robin P. Peeters
  • Jesus Vioque
  • Llúcia González
  • Mercedes Espada
  • Jesús Ibarluzea
  • Jordi Sunyer
  • Tim I. M. Korevaar
  • Sarah C. BathEmail author
Original Contribution

Abstract

Purpose

As a component of thyroid hormones, adequate iodine intake is essential during pregnancy for fetal neurodevelopment. Across Europe, iodine deficiency is common in pregnancy, but data are lacking on the predictors of iodine status at this life stage. We, therefore, aimed to explore determinants of iodine status during pregnancy in three European populations of differing iodine status.

Methods

Data were from 6566 pregnant women from three prospective population-based birth cohorts from the United Kingdom (ALSPAC, n = 2852), Spain (INMA, n = 1460), and The Netherlands (Generation R, n = 2254). Urinary iodine-to-creatinine ratio (UI/Creat, µg/g) was measured in spot-urine samples in pregnancy (≤ 18-weeks gestation). Maternal dietary intake, categorised by food groups (g/day), was estimated from food-frequency questionnaires (FFQs). Multivariable regression models used dietary variables (energy-adjusted) and maternal characteristics as predictors of iodine status.

Results

Median UI/Creat in pregnant women of ALSPAC, INMA, and Generation R was 121, 151, and 210 µg/g, respectively. Maternal age was positively associated with UI/Creat in all cohorts (P < 0.001), while UI/Creat varied by ethnicity only in Generation R (P < 0.05). Of the dietary predictors, intake of milk and dairy products (per 100 g/day) was positively associated with UI/Creat in all cohorts [ALSPAC (B = 3.73, P < 0.0001); INMA (B = 6.92, P = 0.002); Generation R (B = 2.34, P = 0.001)]. Cohort-specific dietary determinants positively associated with UI/Creat included fish and shellfish in ALSPAC and INMA, and eggs and cereal/cereal products in Generation R.

Conclusions

The cohort-specific dietary determinants probably reflect not only dietary habits but iodine-fortification policies; hence, public-health interventions to improve iodine intake in pregnancy need to be country-specific.

Keywords

Iodine Pregnancy Diet Determinants Milk and dairy products ALSPAC 

Abbreviations

ALSPAC

The Avon Longitudinal Study of Parents and Children

BMI

Body mass index

CI

Confidence interval

CRM

Certified reference material

EXP

Exponentiation

FFQ

Food-frequency questionnaire

INMA

INfancia y Medio Ambiente

IQ

Intelligence quotient

RSD

Relative standard deviation

SD

Standard deviation

SEE

Standard error of estimate

SFFQ

Semi-quantitative food-frequency questionnaire

UI/Creat

Urinary iodine-to-creatinine ratio

UIC

Urinary iodine concentration

UK

United Kingdom

WHO

World Health Organisation

Notes

Acknowledgements

EUthyroid project: This project has received funding from the European Union´s Horizon 2020 research and innovation programme under Grant agreement no. 634453.

ALSPAC: We are extremely grateful to all the families who took part in this study, the midwives for their help in recruiting them, and the whole ALSPAC team, which includes interviewers, computer and laboratory technicians, clerical workers, research scientists, volunteers, managers, receptionists and nurses. The UK Medical Research Council and Wellcome (Grant ref.: 102215/2/13/2) and the University of Bristol provide core support for ALSPAC. This publication is the work of the authors and Dr Bath will serve as a guarantor for the contents of this paper. ALSPAC data collection is funded from a wide range of sources, a comprehensive list of which is available on the ALSPAC website (http://www.bristol.ac.uk/alspac/external/documents/grant-acknowledgements.pdf). The existing iodine measurements in ALSPAC were funded from (1) the NUTRIMENTHE project, which received a research grant from the European Community’s 7th Framework Programme (FP7/2008–2013) under grant agreement 212652 and (2) a Ph.D. studentship that was funded by Wassen International and the Waterloo Foundation (2009–2012). We would like to thank Dr Pauline Emmett for helping with the dietary analysis of the ALSPAC food-frequency questionnaire.

Generation R: The Generation R Study is conducted by the Erasmus Medical Center in close collaboration with the Faculty of Social Sciences of the Erasmus University Rotterdam, the Municipal Health Service Rotterdam area, Rotterdam, and the Stichting Trombosedienst & Artsenlaboratorium Rijnmond (STAR-MDC), Rotterdam. The Generation R Study is supported by the Erasmus Medical Center, Rotterdam, the Erasmus University Rotterdam, The Netherlands Organization for Health Research and Development (ZonMw), The Netherlands Organization for Scientific Research (NWO), the Ministry of Health, Welfare and Sport. A grant from the Sophia Children’s Hospital Research Funds supports the neurodevelopmental work on thyroid; Robin P. Peeters is supported by a clinical fellowship from ZonMw, project number 90700412.

INMA: This study was funded by grants from UE (FP7-ENV-2011 cod 282957 and HEALTH.2010.2.4.5-1) and Spain: Instituto de Salud Carlos III (Red INMA G03/176; CB06/02/0041; FIS-FEDER: PI041436, PI05/1079, PI06/0867, PI081151, FIS-and PS09/00090, PI11/01007, PI11/02591, PI11/02038, PI13/1944, PI13/2032, PI14/00891, PI14/01687, and PI16/1288; Miguel Servet-FEDER CP11/00178, CP15/00025, and CPII16/00051, MS13/00054), Generalitat Valenciana: FISABIO (UGP 15-230, UGP-15-244, and UGP-15-249), Generalitat de Catalunya-CIRIT 1999SGR 00241, Fundació La marató de TV3 (090430), Department of Health of the Basque Government (2005111093 and 2009111069), and the Provincial Government of Gipuzkoa (DFG06/004 and DFG08/001).

Author contributions

MD performed statistical analyses, interpreted the data, and wrote the first version of the manuscript. MPR, SCB, RPP, TIMK, MG, and DL contributed to statistical analyses, interpretation of the data, and writing of the manuscript. JV, LG, ME, JI, and JS helped with writing of the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All studies in these analyses have been approved by the appropriate ethics committees and have, therefore, been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. Detailed information is included as part of the main text (see “Methods”, sub-section “Ethics”).

Supplementary material

394_2019_1913_MOESM1_ESM.pdf (501 kb)
Supplementary material 1 (PDF 500 KB)

References

  1. 1.
    de Escobar GM, Obregón MJ, del Rey FE (2004) Maternal thyroid hormones early in pregnancy and fetal brain development. Best Pract Res Clin Endocrinol Metab 18:225–248.  https://doi.org/10.1016/j.beem.2004.03.012 CrossRefGoogle Scholar
  2. 2.
    Glinoer D (2007) The importance of iodine nutrition during pregnancy. Public Health Nutr 10:1542–1546.  https://doi.org/10.1017/S1368980007360886 CrossRefGoogle Scholar
  3. 3.
    van Mil NH, Tiemeier H, Bongers-Schokking JJ, Ghassabian A, Hofman A, Hooijkaas H, Jaddoe VWV, de Muinck Keizer-Schrama SM, Steegers EAP, Visser TJ, Visser W, Ross HA, Verhulst FC, de Rijke YB, Steegers-Theunissen RPM (2012) Low urinary iodine excretion during early pregnancy is associated with alterations in executive functioning in children. J Nutr 142:2167–2174.  https://doi.org/10.3945/jn.112.161950 CrossRefGoogle Scholar
  4. 4.
    Bath SC, Steer CD, Golding J, Emmett P, Rayman MP (2013) Effect of inadequate iodine status in UK pregnant women on cognitive outcomes in their children: results from the Avon Longitudinal Study of Parents and Children (ALSPAC). Lancet 382:331–337.  https://doi.org/10.1016/S0140-6736(13)60436-5 CrossRefGoogle Scholar
  5. 5.
    Hynes KL, Otahal P, Hay I, Burgess JR (2013) Mild iodine deficiency during pregnancy is associated with reduced educational outcomes in the offspring: 9-year follow-up of the gestational iodine cohort. J Clin Endocrinol Metab 98:1954–1962.  https://doi.org/10.1210/jc.2012-4249 CrossRefGoogle Scholar
  6. 6.
    Hynes K, Otahal P, Burgess J, Oddy W, Hay I (2017) Reduced educational outcomes persist into adolescence following mild iodine deficiency in utero, despite adequacy in childhood: 15-year follow-up of the gestational iodine cohort investigating auditory processing speed and working memory. Nutrients 9:1354.  https://doi.org/10.3390/nu9121354 CrossRefGoogle Scholar
  7. 7.
    Murcia M, Espada M, Julvez J, Llop S, Lopez-Espinosa M-J, Vioque J, Basterrechea M, Riaño I, González L, Alvarez-Pedrerol M, Tardón A, Ibarluzea J, Rebagliato M (2017) Iodine intake from supplements and diet during pregnancy and child cognitive and motor development: the INMA Mother and Child Cohort Study. J Epidemiol Community Health 0:1–7.  https://doi.org/10.1136/jech-2017-209830 Google Scholar
  8. 8.
    Williams GR (2008) Neurodevelopmental and neurophysiological actions of thyroid hormone. J Neuroendocrinol 20:784–794.  https://doi.org/10.1111/j.1365-2826.2008.01733.x CrossRefGoogle Scholar
  9. 9.
    Glinoer D (2004) The regulation of thyroid function during normal pregnancy: importance of the iodine nutrition status. Best Pract Res Clin Endocrinol Metab 18:133–152.  https://doi.org/10.1016/J.BEEM.2004.03.001 CrossRefGoogle Scholar
  10. 10.
    Delange F (2007) Iodine requirements during pregnancy, lactation and the neonatal period and indicators of optimal iodine nutrition. Public Health Nutr 10:1571–1580.  https://doi.org/10.1017/S1368980007360941 CrossRefGoogle Scholar
  11. 11.
    Zimmermann MB (2008) Methods to assess iron and iodine status. Br J Nutr 99:S2–S9.  https://doi.org/10.1017/S000711450800679X CrossRefGoogle Scholar
  12. 12.
    World Health Organisation (2007) Assessment of iodine deficiency disorders and monitoring their elimination. A guide for programme managers. http://apps.who.int/iris/bitstream/10665/43781/1/9789241595827_eng.pdf. Accessed 20 Sep 2017
  13. 13.
    Rasmussen LB, Andersen S, Ovesen L, Laurberg P (2009) Iodine intake and food choice. In: Preedy VR, Burrow GN, Watson RR (eds) Comprehensive handbook of iodine: nutritional, biochemical, pathological and therapeutic aspects. Elsevier, London, pp 331–337Google Scholar
  14. 14.
    Haldimann M, Alt A, Blanc A, Blondeau K (2005) Iodine content of food groups. J Food Compos Anal 18:461–471.  https://doi.org/10.1016/j.jfca.2004.06.003 CrossRefGoogle Scholar
  15. 15.
    Iodine Global Network (2017) Global Scorecard of Iodine Nutrition in 2017 in the general population and in pregnant women (PW). http://www.ign.org/cm_data/IGN_Global_Scorecard_AllPop_and_PW_May2017.pdf. Accessed 24 Sep 2017
  16. 16.
    Boyd A, Golding J, Macleod J, Lawlor DA, Fraser A, Henderson J, Molloy L, Ness A, Ring S, Smith GD (2013) Cohort profile: The “Children of the 90s”—the index offspring of the avon longitudinal study of parents and children. Int J Epidemiol 42:111–127.  https://doi.org/10.1093/ije/dys064 CrossRefGoogle Scholar
  17. 17.
    Fraser A, Macdonald-Wallis C, Tilling K, Boyd A, Golding J, Davey smith G, Henderson J, Macleod J, Molloy L, Ness A, Ring S, Nelson SM, Lawlor DA (2013) Cohort profile: The avon longitudinal study of parents and children: ALSPAC mothers cohort. Int J Epidemiol 42:97–110.  https://doi.org/10.1093/ije/dys066 CrossRefGoogle Scholar
  18. 18.
    Kooijman MN, Kruithof CJ, van Duijn CM, Duijts L, Franco OH, van IJzendoorn MH, de Jongste JC, Klaver CCW, van der Lugt A, Mackenbach JP, Moll HA, Peeters RP, Raat H, Rings EHHM, Rivadeneira F, van der Schroeff MP, Steegers EAP, Tiemeier H, Uitterlinden AG, Verhulst FC, Wolvius E, Felix JF, Jaddoe VWV (2016) The generation R Study: design and cohort update 2017. Eur J Epidemiol 31:1243–1264.  https://doi.org/10.1007/s10654-016-0224-9 CrossRefGoogle Scholar
  19. 19.
    Guxens M, Ballester F, Espada M, Fernández MF, Grimalt JO, Ibarluzea J, Olea N, Rebagliato M, Tardón A, Torrent M, Vioque J, Vrijheid M, Sunyer J (2012) Cohort profile: the INMA—INfancia y Medio Ambiente—(Environment and Childhood) Project. Int J Epidemiol 41:930–940.  https://doi.org/10.1093/ije/dyr054 CrossRefGoogle Scholar
  20. 20.
    ALSPAC (2018) Data dictionary. http://www.bristol.ac.uk/alspac/researchers/our-data/. Accessed 20 Mar 2018
  21. 21.
    Ghassabian A, Steenweg-de Graaff J, Peeters RP, Ross HA, Jaddoe VW, Hofman A, Verhulst FC, White T, Tiemeier H (2014) Maternal urinary iodine concentration in pregnancy and children’s cognition: results from a population-based birth cohort in an iodine-sufficient area. BMJ Open 4:e005520–e005520.  https://doi.org/10.1136/bmjopen-2014-005520 CrossRefGoogle Scholar
  22. 22.
    Murcia M, Rebagliato M, Espada M, Vioque J, Santa Marina L, Alvarez-Pedrerol M, Lopez-Espinosa M-J, León G, Iñiguez C, Basterrechea M, Guxens M, Lertxundi A, Perales A, Ballester F, Sunyer J, INMA Study Group (2010) Iodine intake in a population of pregnant women: INMA mother and child cohort study, Spain. J Epidemiol Community Health 64:1094–1099.  https://doi.org/10.1136/jech.2009.092593 CrossRefGoogle Scholar
  23. 23.
    Stiles J, Jernigan TL (2010) The basics of brain development. Neuropsychol Rev 20:327–348.  https://doi.org/10.1007/s11065-010-9148-4 CrossRefGoogle Scholar
  24. 24.
    Vejbjerg P, Knudsen N, Perrild H, Laurberg P, Andersen S, Rasmussen LB, Ovesen L, Jørgensen T (2009) Estimation of iodine intake from various urinary iodine measurements in population studies. Thyroid 19:1281–1286.  https://doi.org/10.1089/thy.2009.0094 CrossRefGoogle Scholar
  25. 25.
    König F, Andersson M, Hotz K, Aeberli I, Zimmermann MB (2011) Ten repeat collections for urinary iodine from spot samples or 24-h samples are needed to reliably estimate individual iodine status in women. J Nutr 141:2049–2054.  https://doi.org/10.3945/jn.111.144071 CrossRefGoogle Scholar
  26. 26.
    Andersen S, Karmisholt J, Pedersen KM, Laurberg P (2008) Reliability of studies of iodine intake and recommendations for number of samples in groups and in individuals. Br J Nutr 99:813–818.  https://doi.org/10.1017/S0007114507842292 Google Scholar
  27. 27.
    Rasmussen LB, Ovesen L, Christiansen E (1999) Day-to-day and within-day variation in urinary iodine excretion. Eur J Clin Nutr 53:401–407CrossRefGoogle Scholar
  28. 28.
    Pearce EN, Lazarus JH, Smyth PP, He X, Smith DF, Pino S, Braverman LE (2009) Urine test strips as a source of iodine contamination. Thyroid.  https://doi.org/10.1089/thy.2009.0120 Google Scholar
  29. 29.
    Pearce EN, Lazarus JH, Smyth PPA, He X, Dall’Amico D, Parkes AB, Burns R, Smith DF, Maina A, Bestwick JP, Jooman M, Leung AM, Braverman LE (2010) Perchlorate and thiocyanate exposure and thyroid function in first-trimester pregnant women. J Clin Endocrinol Metab 95:3207–3215.  https://doi.org/10.1210/jc.2010-0014 CrossRefGoogle Scholar
  30. 30.
    Bath SC, Pop VJM, Furmidge-Owen VL, Broeren MAC, Rayman MP (2017) Thyroglobulin as a functional biomarker of iodine status in a cohort study of pregnant women in the United Kingdom. Thyroid 27:426–433.  https://doi.org/10.1089/thy.2016.0322 CrossRefGoogle Scholar
  31. 31.
    Emmett P, Symes C, Braddon F, Heaton K (1992) Validation of a new questionnaire for assessing habitual intakes of starch, non-starch poly-saccharides, sugars and alcohol. J Hum Nutr Diet 5:245–254CrossRefGoogle Scholar
  32. 32.
    Rogers I, Emmett P, ALSPAC Study Team (1998) Diet during pregnancy in a population of pregnant women in South West England. Eur J Clin Nutr 52:246–250CrossRefGoogle Scholar
  33. 33.
    Klipstein-Grobusch K, den Breeijen JH, Goldbohm R, Geleijnse JM, Hofman A, Grobbee DE, Witteman JC (1998) Dietary assessment in the elderly: validation of a semiquantitative food frequency questionnaire. Eur J Clin Nutr 52:588–596.  https://doi.org/10.1038/sj.ejcn.1600611 CrossRefGoogle Scholar
  34. 34.
    Timmermans S, Steegers-Theunissen RPM, Vujkovic M, Bakker R, Den Breeijen H, Raat H, Russcher H, Lindemans J, Hofman A, Jaddoe VWV, Steegers EAP (2011) Major dietary patterns and blood pressure patterns during pregnancy: the Generation R study. Am J Obstet Gynecol 205:337.e1–337.e12.  https://doi.org/10.1016/j.ajog.2011.05.013 CrossRefGoogle Scholar
  35. 35.
    Steenweg-de Graaff J, Tiemeier H, Steegers-Theunissen RPM, Hofman A, Jaddoe VWV, Verhulst FC, Roza SJ (2014) Maternal dietary patterns during pregnancy and child internalising and externalising problems. The Generation R Study. Clin Nutr 33:115–121.  https://doi.org/10.1016/j.clnu.2013.03.002 CrossRefGoogle Scholar
  36. 36.
    Slimani N, Fahey M, Welch A, Wirfält E, Stripp C, Bergström E, Linseisen J, Schulze M, Bamia C, Chloptsios Y, Veglia F, Panico S, Bueno-de-Mesquita H, Ocké M, Brustad M, Lund E, González C, Barcos A, Berglund G, Winkvist A, Mulligan A, Appleby P, Overvad K, Tjønneland A, Clavel-Chapelon F, Kesse E, Ferrari P, Van Staveren W, Riboli E (2002) Diversity of dietary patterns observed in the European Prospective Investigation into Cancer and Nutrition (EPIC) project. Public Health Nutr 5:1311.  https://doi.org/10.1079/PHN2002407 CrossRefGoogle Scholar
  37. 37.
    Willett WC, Sampson L, Stampfer MJ, Rosner B, Bain C, Witschi J, Hennekens CH, Speizer FE (1985) Reproducibility and validity of a semiquantitative food frequency questionnaire. Am J Epidemiol 122:51–65.  https://doi.org/10.1093/acprof CrossRefGoogle Scholar
  38. 38.
    Vioque J, Weinbrenner T, Asensio L, Castelló A, Young IS, Fletcher A (2007) Plasma concentrations of carotenoids and vitamin C are better correlated with dietary intake in normal weight than overweight and obese elderly subjects. Br J Nutr 97:977.  https://doi.org/10.1017/S0007114507659017 CrossRefGoogle Scholar
  39. 39.
    Vioque J, Navarrete-Muñoz E-M, Gimenez-Monzó D, García-de-la-Hera M, Granado F, Young IS, Ramón R, Ballester F, Murcia M, Rebagliato M, Iñiguez C (2013) Reproducibility and validity of a food frequency questionnaire among pregnant women in a Mediterranean area. Nutr J 12:26.  https://doi.org/10.1186/1475-2891-12-26 CrossRefGoogle Scholar
  40. 40.
    Bowen E, Heron J, Waylen A, Wolke D (2005) Domestic violence risk during and after pregnancy: findings from a British longitudinal study. BJOG An Int J Obstet Gynaecol 112:1083–1089.  https://doi.org/10.1111/j.1471-0528.2005.00653.x CrossRefGoogle Scholar
  41. 41.
    Winsper C, Zanarini M, Wolke D (2012) Prospective study of family adversity and maladaptive parenting in childhood and borderline personality disorder symptoms in a non-clinical population at 11 years. Psychol Med 42:2405–2420.  https://doi.org/10.1017/S0033291712000542 CrossRefGoogle Scholar
  42. 42.
    Barr DB, Wilder LC, Caudill SP, Gonzalez AJ, Needham LL, Pirkle JL (2005) Urinary creatinine concentrations in the U.S. population: implications for urinary biologic monitoring measurements. Environ Health Perspect 113:192–200.  https://doi.org/10.1289/ehp.7337 CrossRefGoogle Scholar
  43. 43.
    Baba Y, Furuta I, Zhai T, Ohkuchi A, Yamada T, Takahashi K, Matsubara S, Minakami H (2017) Effect of urine creatinine level during pregnancy on dipstick test. J Obstet Gynaecol Res 43:967–973.  https://doi.org/10.1111/jog.13327 CrossRefGoogle Scholar
  44. 44.
    Sterne JAC, White IR, Carlin JB, Spratt M, Royston P, Kenward MG, Wood AM, Carpenter JR (2009) Multiple imputation for missing data in epidemiological and clinical research: potential and pitfalls. BMJ 338:b2393.  https://doi.org/10.1136/BMJ.B2393 CrossRefGoogle Scholar
  45. 45.
    Crawley H, Mills A, Patel S, Great B (1993) Ministry of agriculture F and F. In: Food portion sizes. H.M.S.O, LondonGoogle Scholar
  46. 46.
    World Health Organisation (2007) Iodine deficiency in Europe: a continuing public health problem. http://apps.who.int/iris/handle/10665/43398. Accessed 1 Oct 2017
  47. 47.
    Phillips DI (1997) Iodine, milk, and the elimination of endemic goitre in Britain: the story of an accidental public health triumph. J Epidemiol Community Health 51:391–393CrossRefGoogle Scholar
  48. 48.
    Bath SC, Button S, Rayman MP (2014) Availability of iodised table salt in the UK—is it likely to influence population iodine intake? Public Health Nutr 17:450–454.  https://doi.org/10.1017/S1368980012005496 CrossRefGoogle Scholar
  49. 49.
    Glinoer D (1997) The regulation of thyroid function in pregnancy: pathways of endocrine adaptation from physiology to pathology. Endocr Rev 18:404–433.  https://doi.org/10.1210/edrv.18.3.0300 CrossRefGoogle Scholar
  50. 50.
    Cheung KL, Lafayette RA (2013) Renal physiology of pregnancy. Adv Chronic Kidney Dis 20:209–214.  https://doi.org/10.1053/j.ackd.2013.01.012 CrossRefGoogle Scholar
  51. 51.
    Fuse Y, Shishiba Y, Irie M (2013) Gestational changes of thyroid function and urinary iodine in thyroid antibody-negative Japanese women. Endocr J 60:1095–1106.  https://doi.org/10.1507/endocrj.EJ13-0184 CrossRefGoogle Scholar
  52. 52.
    Bath SC, Furmidge-Owen VL, Redman CW, Rayman MP (2015) Gestational changes in iodine status in a cohort study of pregnant women from the United Kingdom: season as an effect modifier. Am J Clin Nutr 101:1180–1187.  https://doi.org/10.3945/ajcn.114.105536 CrossRefGoogle Scholar
  53. 53.
    Li C, Peng S, Zhang X, Xie X, Wang D, Mao J, Teng X, Shan Z, Teng W (2016) The urine iodine to creatinine as an optimal index of iodine during pregnancy in an iodine adequate area in China. J Clin Endocrinol Metab 101:1290–1298.  https://doi.org/10.1210/jc.2015-3519 CrossRefGoogle Scholar
  54. 54.
    Brander L, Als C, Buess H, Haldimann F, Harder M, Hänggi W, Herrmann U, Lauber K, Niederer U, Zürcher T, Bürgi U, Gerber H (2003) Urinary iodine concentration during pregnancy in an area of unstable dietary iodine intake in Switzerland. J Endocrinol Invest 26:389–396.  https://doi.org/10.1007/BF03345192 CrossRefGoogle Scholar
  55. 55.
    Stilwell G, Reynolds PJ, Parameswaran V, Blizzard L, Greenaway TM, Burgess JR (2008) The influence of gestational stage on urinary iodine excretion in pregnancy. J Clin Endocrinol Metab 93:1737–1742.  https://doi.org/10.1210/jc.2007-1715 CrossRefGoogle Scholar
  56. 56.
    Gerchman F, Tong J, Utzschneider KM, Zraika S, Udayasankar J, McNeely MJ, Carr DB, Leonetti DL, Young BA, de Boer IH, Boyko EJ, Fujimoto WY, Kahn SE (2009) Body mass index is associated with increased creatinine clearance by a mechanism independent of body fat distribution. J Clin Endocrinol Metab 94:3781–3788.  https://doi.org/10.1210/jc.2008-2508 CrossRefGoogle Scholar
  57. 57.
    O’Brien KM, Upson K, Cook NR, Weinberg CR (2016) Environmental chemicals in urine and blood: improving methods for creatinine and lipid adjustment. Environ Health Perspect 124:220–227CrossRefGoogle Scholar
  58. 58.
    James GD, Sealey JE, Alderman M, Ljungman S, Mueller FB, Pecker MS, Laragh JH (1988) A longitudinal study of urinary creatinine and creatinine clearance in normal subjects: race, sex, and age differences. Am J Hypertens 1:124–131.  https://doi.org/10.1093/ajh/1.2.124 CrossRefGoogle Scholar
  59. 59.
    Brantsæter AL, Haugen M, Julshamn K, Alexander J, Meltzer HM (2009) Evaluation of urinary iodine excretion as a biomarker for intake of milk and dairy products in pregnant women in the Norwegian Mother and Child Cohort Study (MoBa). Eur J Clin Nutr 63:347–354.  https://doi.org/10.1038/sj.ejcn.1602952 CrossRefGoogle Scholar
  60. 60.
    Brantsæter AL, Abel MH, Haugen M, Meltzer HM (2013) Risk of suboptimal iodine intake in pregnant norwegian women. Nutrients 5:424–440.  https://doi.org/10.3390/nu5020424 CrossRefGoogle Scholar
  61. 61.
    Gunnarsdottir I, Gustavsdottir AG, Steingrimsdottir L, Maage A, Johannesson AJ, Thorsdottir I (2013) Iodine status of pregnant women in a population changing from high to lower fish and milk consumption. Public Health Nutr 16:325–329.  https://doi.org/10.1017/S1368980012001358 CrossRefGoogle Scholar
  62. 62.
    Mian C, Vitaliano P, Pozza D, Barollo S, Pitton M, Callegari G, Di Gianantonio E, Casaro A, Acamulli DN, Busnardo B, Mantero F, Girelli ME (2009) Iodine status in pregnancy: Role of dietary habits and geographical origin. Clin Endocrinol (Oxf) 70:776–780.  https://doi.org/10.1111/j.1365-2265.2008.03416.x CrossRefGoogle Scholar
  63. 63.
    Torres MT, Francés L, Vila L, Manresa JM, Falguera G, Prieto G, Casamitjana R, Toran P (2017) Iodine nutritional status of women in their first trimester of pregnancy in Catalonia. BMC Pregnancy Childbirth 17:249.  https://doi.org/10.1186/s12884-017-1423-4 CrossRefGoogle Scholar
  64. 64.
    Bath SC, Walter A, Taylor A, Wright J, Rayman MP (2014) Iodine deficiency in pregnant women living in the South East of the UK: the influence of diet and nutritional supplements on iodine status. Br J Nutr 111:1622–1631.  https://doi.org/10.1017/S0007114513004030 CrossRefGoogle Scholar
  65. 65.
    Blumenthal N, Byth K, Eastman CJ (2012) Iodine intake and thyroid function in pregnant women in a private clinical practice in Northwestern Sydney before mandatory fortification of bread with iodised salt. J Thyroid Res 2012:1–6.  https://doi.org/10.1155/2012/798963 CrossRefGoogle Scholar
  66. 66.
    Soriguer F, Gutierrez-Repiso C, Gonzalez-Romero S, Olveira G, Garriga MJ, Velasco I, Santiago P, de Escobar GM, Garcia-Fuentes E, Iodine Deficiency Disorders Group of Spanish Society of Endocrinology and Nutrition (2011) Iodine concentration in cow’s milk and its relation with urinary iodine concentrations in the population. Clin Nutr 30:44–48.  https://doi.org/10.1016/j.clnu.2010.07.001 CrossRefGoogle Scholar
  67. 67.
    National Institute for Public Health and the Environment (RIVM) (2016) Dutch food composition database (NEVO) online version 2016/5.0. In: RIVM, Bilthoven. http://nevo-online.rivm.nl/. Accessed 19 Jan 2018
  68. 68.
    Lee SM, Lewis J, Buss DH, Holcombe GD, Lawrance PR (1994) Iodine in British foods and diets. Br J Nutr 72:435.  https://doi.org/10.1079/BJN19940045 CrossRefGoogle Scholar
  69. 69.
    Stevenson MC, Drake C, Givens DI (2018) Further studies on the iodine concentration of conventional, organic and UHT semi-skimmed milk at retail in the UK. Food Chem 239:551–555.  https://doi.org/10.1016/J.FOODCHEM.2017.06.135 CrossRefGoogle Scholar
  70. 70.
    Dahl L, Johansson L, Julshamn K, Meltzer HM (2004) The iodine content of Norwegian foods and diets. Public Health Nutr 7:569–576.  https://doi.org/10.1079/PHN2003554 CrossRefGoogle Scholar
  71. 71.
    Verkaik-Kloosterman J, Buurma-Rethans E, Dekkers A (2012) The iodine intake of children and adults in the Netherlands: Results of the Dutch National Food Consumption Survey 2007–2010—RIVM. http://www.rivm.nl/en/Documents_and_publications/Scientific/Reports/2012/april/The_iodine_intake_of_children_and_adults_in_the_Netherlands_Results_of_the_Dutch_National_Food_Consumption_Survey_2007_2010. Accessed 1 Oct 2017
  72. 72.
    Cross AJ, Major JM, Sinha R (2011) Urinary biomarkers of meat consumption. Cancer Epidemiol Biomark Prev 20:1107–1111.  https://doi.org/10.1158/1055-9965.EPI-11-0048 CrossRefGoogle Scholar
  73. 73.
    Lykken GI, Jacob RA, Munoz JM, Sandstead HH (1980) A mathematical model of creatine metabolism in normal males–comparison between theory and experiment. Am J Clin Nutr 33:2674–2685CrossRefGoogle Scholar
  74. 74.
    Shim J-S, Oh K, Kim HC (2014) Dietary assessment methods in epidemiologic studies. Epidemiol Health 36:e2014009.  https://doi.org/10.4178/epih/e2014009 CrossRefGoogle Scholar
  75. 75.
    Knudsen N, Christiansen E, Brandt-Christensen M, Nygaard B, Perrild H (2000) Age-and sex-adjusted iodineacreatinine ratio. A new standard in epidemiological surveys? Evaluation of three different estimates of iodine excretion based on casual urine samples and comparison to 24 h values. Eur J Clin Nutr 54:361–363CrossRefGoogle Scholar
  76. 76.
    Willett W (2012) Nutritional epidemiology, Third edit. Oxford University Press, Oxford; New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Mariana Dineva
    • 1
  • Margaret P. Rayman
    • 1
  • Deborah Levie
    • 2
    • 3
    • 4
    • 5
    • 6
    • 7
  • Mònica Guxens
    • 4
    • 5
    • 6
    • 7
  • Robin P. Peeters
    • 3
  • Jesus Vioque
    • 7
    • 8
  • Llúcia González
    • 9
    • 10
  • Mercedes Espada
    • 11
    • 12
  • Jesús Ibarluzea
    • 7
    • 12
    • 13
    • 14
  • Jordi Sunyer
    • 5
    • 6
    • 7
    • 15
  • Tim I. M. Korevaar
    • 2
    • 3
  • Sarah C. Bath
    • 1
    Email author
  1. 1.Department of Nutritional Sciences, Faculty of Health and Medical SciencesUniversity of SurreyGuildfordUK
  2. 2.The Generation R Study GroupErasmus University Medical CentreRotterdamThe Netherlands
  3. 3.Department of Internal Medicine, Academic Centre for Thyroid DiseasesErasmus University Medical CentreRotterdamThe Netherlands
  4. 4.Department of Child and Adolescent Psychiatry/PsychologyErasmus University Medical Centre-Sophia Children’s HospitalRotterdamThe Netherlands
  5. 5.ISGlobalBarcelonaSpain
  6. 6.Pompeu Fabra UniversityBarcelonaSpain
  7. 7.Spanish Consortium for Research on Epidemiology and Public Health (CIBERESP)Instituto de Salud Carlos IIIMadridSpain
  8. 8.Nutritional Epidemiology UnitMiguel Hernández University, ISABIAL-FISABIOAlicanteSpain
  9. 9.Epidemiology and Environmental Health Joint Research UnitFISABIO-Universitat Jaume I-Universitat de ValènciaValenciaSpain
  10. 10.Predepartamental Unit of MedicineUniversity Jaume ICastellóSpain
  11. 11.Departamento de Salud del Gobierno Vasco, Public Health Laboratory of BilbaoBasque GovernmentDerioSpain
  12. 12.BIODONOSTIA Health Research InstituteDonostia-San SebastiánSpain
  13. 13.Departamento de Salud del Gobierno VascoSubdirección de Salud Pública de GuipúzcoaDonostia-San SebastiánSpain
  14. 14.Facultad de PsicologíaUniversity of the Basque Country UPV/EHUDonostia-San SebastiánSpain
  15. 15.Hospital del Mar Research Institute (IMIM)BarcelonaSpain

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