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Fetal Physiologically Based Pharmacokinetic Models: Systems Information on the Growth and Composition of Fetal Organs

  • Khaled Abduljalil
  • Masoud Jamei
  • Trevor N. Johnson
Original Research Article
  • 119 Downloads

Abstract

Background

The growth of fetal organs is a dynamic process involving considerable changes in the anatomical and physiological parameters that can alter fetal exposure to xenobiotics in utero. Physiologically based pharmacokinetic models can be used to predict the fetal exposure as time-varying parameters can easily be incorporated.

Objective

The objective of this study was to collate, analyse and integrate the available time-varying parameters needed for the physiologically based pharmacokinetic modelling of xenobiotic kinetics in a fetal population.

Methods

We performed a comprehensive literature search on the physiological development of fetal organs. Data were carefully assessed, integrated and a meta-analysis was performed to establish growth trends with fetal age and weight. Algorithms and models were generated to describe the growth of these parameter values as functions of age and/or weight.

Results

Fetal physiologically based pharmacokinetic parameters, including the size of the heart, liver, brain, kidneys, lungs, spleen, muscles, pancreas, skin, bones, adrenal and thyroid glands, thymus, gut and gonads were quantified as a function of fetal age and weight. Variability around the means of these parameters at different fetal ages was also reported. The growth of the investigated parameters was not consistent (with respect to direction and monotonicity).

Conclusion

Despite the limitations identified in the availability of some values, the data presented in this article provide a unique resource for age-dependent organ size and composition parameters needed for fetal physiologically based pharmacokinetic modelling. This will facilitate the application of physiologically based pharmacokinetic models during drug development and in the risk assessment of environmental chemicals and following maternally administered drugs or unintended exposure to environmental toxicants in this population.

Notes

Acknowledgements

We thank Miss Eleanor Savill and Ms Rosalie Bower for their assistance with collecting the references and preparing the manuscript.

Compliance with Ethical Standards

Funding

No funding was received for the preparation of this study.

Conflict of interest

Khaled Abduljalil, Masoud Jamei and Trevor N. Johnson are full-time employees of Certara UK Limited. The activities of Certara are supported by a consortium of pharmaceutical companies.

Supplementary material

40262_2018_685_MOESM1_ESM.pdf (503 kb)
Supplementary material 1 (PDF 503 kb)
40262_2018_685_MOESM2_ESM.pdf (1.3 mb)
Supplementary material 2 (PDF 1281 kb)

References

  1. 1.
    Zhang Z, Unadkat JD. Development of a novel maternal-fetal physiologically based pharmacokinetic model II: verification of the model for passive placental permeability drugs. Drug Metab Dispos. 2017;45:939–46.CrossRefPubMedGoogle Scholar
  2. 2.
    Zhang Z, Imperial MZ, Patilea-Vrana GI, Wedagedera J, Gaohua L, Unadkat JD. Development of a novel maternal-fetal physiologically based pharmacokinetic model I: insights into factors that determine fetal drug exposure through simulations and sensitivity analyses. Drug Metab Dispos. 2017;45:920–38.CrossRefPubMedGoogle Scholar
  3. 3.
    O’Rahilly R, Muller F. Developmental stages in human embryos: revised and new measurements. Cells Tissues Organs. 2010;192:73–84.CrossRefPubMedGoogle Scholar
  4. 4.
    Moore KL, Persaud TVN, Torchia MG. The developing human: clinically oriented embryology. 9th ed. Philadelphia (PA): Saunders, Elsevier; 2013.Google Scholar
  5. 5.
    Sachdeva P, Patel BG, Patel BK. Drug use in pregnancy; a point to ponder! Indian J Pharm Sci. 2009;71:1–7.PubMedCentralCrossRefPubMedGoogle Scholar
  6. 6.
    Colbers A, Greupink R, Burger D. Pharmacological considerations on the use of antiretrovirals in pregnancy. Curr Opin Infect Dis. 2013;26:575–88.CrossRefPubMedGoogle Scholar
  7. 7.
    Cox PB, Marcus MA, Bos H. Pharmacological considerations during pregnancy. Curr Opin Anaesthesiol. 2001;14:311–6.CrossRefPubMedGoogle Scholar
  8. 8.
    Herbst AL, Ulfelder H, Poskanzer DC. Adenocarcinoma of the vagina: association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med. 1971;284:878–81.CrossRefPubMedGoogle Scholar
  9. 9.
    Edelman DA. Diethylstilbestrol exposure and the risk of clear cell cervical and vaginal adenocarcinoma. Int J Fertil. 1989;34:251–5.PubMedGoogle Scholar
  10. 10.
    Drukker A, Guignard JP. Renal aspects of the term and preterm infant: a selective update. Curr Opin Pediatr. 2002;14:175–82.CrossRefPubMedGoogle Scholar
  11. 11.
    Brenner BM, Chertow GM. Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis. 1994;23:171–5.CrossRefPubMedGoogle Scholar
  12. 12.
    Poggi SH, Ghidini A. Importance of timing of gestational exposure to methotrexate for its teratogenic effects when used in setting of misdiagnosis of ectopic pregnancy. Fertil Steril. 2011;96:669–71.CrossRefPubMedGoogle Scholar
  13. 13.
    Sulik KK, Cook CS, Webster WS. Teratogens and craniofacial malformations: relationships to cell death. Development. 1988;103 Suppl.:213–31.Google Scholar
  14. 14.
    Martin-Suarez A, Sanchez-Hernandez JG, Medina-Barajas F, Perez-Blanco JS, Lanao JM, Garcia-Cuenllas Alvarez L, et al. Pharmacokinetics and dosing requirements of digoxin in pregnant women treated for fetal supraventricular tachycardia. Expert Rev Clin Pharmacol. 2017;10:911–7.CrossRefPubMedGoogle Scholar
  15. 15.
    Roberts D, Brown J, Medley N, Dalziel SR. Antenatal corticosteroids for accelerating fetal lung maturation for women at risk of preterm birth. Cochrane Database Syst Rev. 2017;3:CD004454.Google Scholar
  16. 16.
    Miyata I, Abe-Gotyo N, Tajima A, Yoshikawa H, Teramoto S, Seo M, et al. Successful intrauterine therapy for fetal goitrous hypothyroidism during late gestation. Endocr J. 2007;54:813–7.CrossRefPubMedGoogle Scholar
  17. 17.
    Archie JG, Collins JS, Lebel RR. Quantitative standards for fetal and neonatal autopsy. Am J Clin Pathol. 2006;126:256–65.CrossRefPubMedGoogle Scholar
  18. 18.
    Shepard TH, Shi M, Fellingham GW, Fujinaga M, FitzSimmons JM, Fantel AG, et al. Organ weight standards for human fetuses. Pediatr Pathol. 1988;8:513–24.CrossRefPubMedGoogle Scholar
  19. 19.
    Jackson CM. On the prenatal growth of the human body and the relative growth of the various organs and parts. Am J Anat. 1909;9:119–65.CrossRefGoogle Scholar
  20. 20.
    Luecke RH, Wosilait WD, Young JF. Mathematical representation of organ growth in the human embryo/fetus. Int J Biomed Comput. 1995;39:337–47.CrossRefPubMedGoogle Scholar
  21. 21.
    Potter EL, Craig JM. Potter’s pathology of the fetus and infant. St. Louis (MO): Mosby; 1997.Google Scholar
  22. 22.
    Valentin J. Basic anatomical and physiological data for use in radiological protection: reference values: a report of age- and gender-related differences in the anatomical and physiological characteristics of reference individuals. ICRP Publication 89. Ann ICRP. 2002;32:5–265.CrossRefGoogle Scholar
  23. 23.
    Abduljalil K, Furness P, Johnson TN, Rostami-Hodjegan A, Soltani H. Anatomical, physiological and metabolic changes with gestational age during normal pregnancy: a database for parameters required in physiologically based pharmacokinetic modelling. Clin Pharmacokinet. 2012;51:365–96.CrossRefPubMedGoogle Scholar
  24. 24.
    Abduljalil K, Johnson NT, Rostami-Hodjegan A. Fetal physiologically-based pharmacokinetic models: systems information on fetal biometry and gross composition. Clin Pharmacokinet (accepted).Google Scholar
  25. 25.
    Silverwood RJ, Cole TJ. Statistical methods for constructing gestational age-related reference intervals and centile charts for fetal size. Ultrasound Obstet Gynecol. 2007;29:6–13.CrossRefPubMedGoogle Scholar
  26. 26.
    Tanimura T, Nelson T, Hollingsworth RR, Shepard TH. Weight standards for organs from early human fetuses. Anat Rec. 1971;171:227–36.CrossRefPubMedGoogle Scholar
  27. 27.
    Marecki B. Sexual dimorphism of the weight of internal organs in fetal ontogenesis. Anthropol Anz. 1989;47:175–84.PubMedGoogle Scholar
  28. 28.
    Fujikura T, Froehlich LA. Organ-weight-brain-weight ratios as a parameter of prenatal growth: a balanced growth theory of visceras. Am J Obstet Gynecol. 1972;112:896–902.CrossRefPubMedGoogle Scholar
  29. 29.
    Burdi AR, Barr M, Babler WJ. Organ weight patterns in human fetal development. Hum Biol. 1981;53:355–66.PubMedGoogle Scholar
  30. 30.
    Baker GL. Human adipose tissue composition and age. Am J Clin Nutr. 1969;22:829–35.CrossRefPubMedGoogle Scholar
  31. 31.
    Brans YW, Shannon DL. Chemical changes in human skeletal muscle during fetal development. Biol Neonate. 1981;40:21–8.CrossRefPubMedGoogle Scholar
  32. 32.
    Dickerson JW. Changes in the composition of the human femur during growth. Biochem J. 1962;82:56–61.PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Dickerson JW, Widdowson EM. Chemical changes in skeletal muscle during development. Biochem J. 1960;74:247–57.PubMedCentralCrossRefPubMedGoogle Scholar
  34. 34.
    Dobbing J, Sands J. Quantitative growth and development of human brain. Arch Dis Child. 1973;48:757–67.PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Fee BA, Weil WB Jr. Body composition of infants of diabetic mothers by direct analysis. Ann N Y Acad Sci. 1963;110:869–97.CrossRefPubMedGoogle Scholar
  36. 36.
    Fomon SJ, Haschke F, Ziegler EE, Nelson SE. Body composition of reference children from birth to age 10 years. Am J Clin Nutr. 1982;35:1169–75.CrossRefPubMedGoogle Scholar
  37. 37.
    ICRP. Report of the Task Group on Reference Man. ICRP Publication 23, International Commission on Radiological Protection. Oxford: Pergamon Press; 1975.Google Scholar
  38. 38.
    Iob V, Swanson WW. The extracellular and intracellular water in bone and cartlage. J Biol Chem. 1938;122:485–90.Google Scholar
  39. 39.
    Iyengar L, Apte SV. Nutrient stores in human foetal livers. Br J Nutr. 1972;27:313–7.CrossRefPubMedGoogle Scholar
  40. 40.
    Shah RS, Rajalakshmi R. Studies on human fetal tissues: II. Lipid composition of human fetal tissues in relation to gestational age, fetal size and maternal nutritional status. Indian J Pediatr. 1988;55:272–82.CrossRefPubMedGoogle Scholar
  41. 41.
    Swanson WW. IOB V. Growth and chemical composition of the human skeleton. Am J Dis Child. 1940;59:107–11.Google Scholar
  42. 42.
    White DR, Widdowson EM, Woodard HQ, Dickerson JW. The composition of body tissues (II): fetus to young adult. Br J Radiol. 1991;64:149–59.CrossRefPubMedGoogle Scholar
  43. 43.
    Widdowson EM. Growth and composition of the fetus and newborn. In: Assali NS, editor. Biology of gestation. Vol 2. The fetus and neonate. New York (NY): Academic Press; 1968. p. 1–49.Google Scholar
  44. 44.
    Widdowson EM, Dickerson JW. The effect of growth and function on the chemical composition of soft tissues. Biochem J. 1960;77:30–43.PubMedCentralCrossRefPubMedGoogle Scholar
  45. 45.
    Winick M. Changes in nucleic acid and protein content of the human brain during growth. Pediatr Res. 1968;2:352–5.CrossRefPubMedGoogle Scholar
  46. 46.
    Valenti O, Di Prima FA, Renda E, Faraci M, Hyseni E, De Domenico R, et al. Fetal cardiac function during the first trimester of pregnancy. J Prenat Med. 2011;5:59–62.PubMedCentralPubMedGoogle Scholar
  47. 47.
    Thayyil S, Schievano S, Robertson NJ, Jones R, Chitty LS, Sebire NJ, et al. A semi-automated method for non-invasive internal organ weight estimation by post-mortem magnetic resonance imaging in fetuses, newborns and children. Eur J Radiol. 2009;72:321–6.CrossRefPubMedGoogle Scholar
  48. 48.
    Blackburn ST. Maternal, fetal and neonatal physiology: a clinical perspective. 3rd ed. Philadelphia: Saunders Elsevier; 2007.Google Scholar
  49. 49.
    Khwaja OS, Pomeroy SL, Ullrich NJ. Development of the nervous system. In: Polin RA, Fox WW, Abman SH, editors. Fetal and neonatal physiology. 4th ed. Philadelphia (PA): Elsevier; 2011. p. 1745–62.CrossRefGoogle Scholar
  50. 50.
    Samuelsen GB, Larsen KB, Bogdanovic N, Laursen H, Graem N, Larsen JF, et al. The changing number of cells in the human fetal forebrain and its subdivisions: a stereological analysis. Cereb Cortex. 2003;13:115–22.CrossRefPubMedGoogle Scholar
  51. 51.
    Breeze AC, Gallagher FA, Lomas DJ, Smith GC, Lees CC. Postmortem fetal organ volumetry using magnetic resonance imaging and comparison to organ weights at conventional autopsy. Ultrasound Obstet Gynecol. 2008;31:187–93.CrossRefPubMedGoogle Scholar
  52. 52.
    Duck FA. Physical properties of tissue. London: Academic; 1990.Google Scholar
  53. 53.
    Johansson M, Strahm E, Rane A, Ekstrom L. CYP2C8 and CYP2C9 mRNA expression profile in the human fetus. Front Genet. 2014;5:58.PubMedCentralCrossRefPubMedGoogle Scholar
  54. 54.
    Fanni D, Fanos V, Ambu R, Lai F, Gerosa C, Pampaloni P, et al. Overlapping between CYP3A4 and CYP3A7 expression in the fetal human liver during development. J Matern Fetal Neonatal Med. 2014:1–5.Google Scholar
  55. 55.
    Hakkola J, Raunio H, Purkunen R, Saarikoski S, Vahakangas K, Pelkonen O, et al. Cytochrome P450 3A expression in the human fetal liver: evidence that CYP3A5 is expressed in only a limited number of fetal livers. Biol Neonate. 2001;80:193–201.CrossRefPubMedGoogle Scholar
  56. 56.
    Hakkola J, Pasanen M, Purkunen R, Saarikoski S, Pelkonen O, Maenpaa J, et al. Expression of xenobiotic-metabolizing cytochrome P450 forms in human adult and fetal liver. Biochem Pharmacol. 1994;48:59–64.CrossRefPubMedGoogle Scholar
  57. 57.
    Hines RN. The ontogeny of drug metabolism enzymes and implications for adverse drug events. Pharmacol Ther. 2008;118:250–67.CrossRefPubMedGoogle Scholar
  58. 58.
    Gasser B, Mauss Y, Ghnassia JP, Favre R, Kohler M, Yu O, et al. A quantitative study of normal nephrogenesis in the human fetus: its implication in the natural history of kidney changes due to low obstructive uropathies. Fetal Diagn Ther. 1993;8:371–84.CrossRefPubMedGoogle Scholar
  59. 59.
    Rosati P, Guariglia L. Transvaginal sonographic assessment of the fetal urinary tract in early pregnancy. Ultrasound Obstet Gynecol. 1996;7:95–100.CrossRefPubMedGoogle Scholar
  60. 60.
    Vlajkoviç S, Dakoviç-Bjelakoviç M, Čukuranoviç R, Krivokuça D. The average volume of fetal kidney during different periods of gestation. Acta Medica Medianae. 2005;44:47–50.Google Scholar
  61. 61.
    Geelhoed JJ, Taal HR, Steegers EA, Arends LR, Lequin M, Moll HA, et al. Kidney growth curves in healthy children from the third trimester of pregnancy until the age of two years: the Generation R Study. Pediatr Nephrol. 2010;25:289–98.CrossRefPubMedGoogle Scholar
  62. 62.
    Jovevska S, Tofoski G. Comparison between ultrasound (US) and macrodisection measurements of human foetal kidney. Prilozi. 2008;29:337–44.PubMedGoogle Scholar
  63. 63.
    Vlajkovic S, Vasovic L, Dakovic-Bjelakovic M, Cukuranovic R. Age-related changes of the human fetal kidney size. Cells Tissues Organs. 2006;182:193–200.CrossRefPubMedGoogle Scholar
  64. 64.
    Vlajkovic S, Dakovic-Bjelakovic M, Cukuranovic R, Popovic J. Evaluation of absolute volume of human fetal kidney’s cortex and medulla during gestation. Vojnosanit Pregl. 2005;62:107–11.CrossRefPubMedGoogle Scholar
  65. 65.
    Hinchliffe SA, Sargent PH, Howard CV, Chan YF, van Velzen D. Human intrauterine renal growth expressed in absolute number of glomeruli assessed by the disector method and Cavalieri principle. Lab Invest. 1991;64:777–84.PubMedGoogle Scholar
  66. 66.
    Haycock GB. Development of glomerular filtration and tubular sodium reabsorption in the human fetus and newborn. Br J Urol. 1998;81(Suppl. 2):33–8.CrossRefPubMedGoogle Scholar
  67. 67.
    Seikaly MG, Arant BS Jr. Development of renal hemodynamics: glomerular filtration and renal blood flow. Clin Perinatol. 1992;19:1–13.CrossRefPubMedGoogle Scholar
  68. 68.
    Rabinowitz R, Peters MT, Vyas S, Campbell S, Nicolaides KH. Measurement of fetal urine production in normal pregnancy by real-time ultrasonography. Am J Obstet Gynecol. 1989;161:1264–6.CrossRefPubMedGoogle Scholar
  69. 69.
    Manalich R, Reyes L, Herrera M, Melendi C, Fundora I. Relationship between weight at birth and the number and size of renal glomeruli in humans: a histomorphometric study. Kidney Int. 2000;58:770–3Google Scholar
  70. 70.
    Trnka P, Hiatt MJ, Tarantal AF, Matsell DG. Congenital urinary tract obstruction: defining markers of developmental kidney injury. Pediatr Res. 2012;72:446–54.CrossRefPubMedGoogle Scholar
  71. 71.
    Sulak O, Cankara N, Malas MA, Koyuncu E, Desdicioglu K. Anatomical development of urinary bladder during the fetal period. Clin Anat. 2008;21:683–90.CrossRefPubMedGoogle Scholar
  72. 72.
    Hedriana HL, Moore TR. Ultrasonographic evaluation of human fetal urinary flow rate: accuracy limits of bladder volume estimations. Am J Obstet Gynecol. 1994;170:1250–4.CrossRefPubMedGoogle Scholar
  73. 73.
    Woolf AS. Perspectives on human perinatal renal tract disease. Semin Fetal Neonatal Med. 2008;13:196–201.CrossRefPubMedGoogle Scholar
  74. 74.
    Lee SM, Park SK, Shim SS, Jun JK, Park JS, Syn HC. Measurement of fetal urine production by three-dimensional ultrasonography in normal pregnancy. Ultrasound Obstet Gynecol. 2007;30:281–6.CrossRefPubMedGoogle Scholar
  75. 75.
    Maged AM, Abdelmoneim A, Said W, Mostafa WA. Measuring the rate of fetal urine production using three-dimensional ultrasound during normal pregnancy and pregnancy-associated diabetes. J Matern Fetal Neonatal Med. 2014;27(17):1790–4.CrossRefPubMedGoogle Scholar
  76. 76.
    Touboul C, Boulvain M, Picone O, Levaillant JM, Frydman R, Senat MV. Normal fetal urine production rate estimated with 3-dimensional ultrasonography using the rotational technique (virtual organ computer-aided analysis). Am J Obstet Gynecol. 2008;199(1):57.e1–5.Google Scholar
  77. 77.
    Bouwens L, Lu WG, De Krijger R. Proliferation and differentiation in the human fetal endocrine pancreas. Diabetologia. 1997;40:398–404.CrossRefPubMedGoogle Scholar
  78. 78.
    Robb P. The development of the islets of Langerhans in the human foetus. Q J Exp Physiol Cogn Med Sci. 1961;46:335–43.PubMedGoogle Scholar
  79. 79.
    Desdicioglu K, Malas MA, Evcil EH. Foetal development of the pancreas. Folia Morphol (Warsz). 2010;69:216–24.PubMedGoogle Scholar
  80. 80.
    Krakowiak-Sarnowska E, Flisinski P, Szpinda M, Sarnowski J, Lisewski P, Flisinski M. Morphometry of the pancreas in human foetuses. Folia Morphol (Warsz). 2005;64:29–32.PubMedGoogle Scholar
  81. 81.
    Langston C, Kida K, Reed M, Thurlbeck WM. Human lung growth in late gestation and in the neonate. Am Rev Respir Dis. 1984;129:607–13.PubMedGoogle Scholar
  82. 82.
    Votino C, Verhoye M, Segers V, Cannie M, Bessieres B, Cos T, et al. Fetal organ weight estimation by postmortem high-field magnetic resonance imaging before 20 weeks’ gestation. Ultrasound Obstet Gynecol. 2012;39:673–8.CrossRefPubMedGoogle Scholar
  83. 83.
    Ishak N, Sozo F, Harding R, De Matteo R. Does lung development differ in male and female fetuses? Exp Lung Res. 2014;40:30–9.CrossRefPubMedGoogle Scholar
  84. 84.
    Blackfan KD. Growth and development of the child. Part II: anatomy and physiology. Report of the Committee on Growth and Development. New York (NY): The Century Company; 1933.Google Scholar
  85. 85.
    Modi N, Hutton JL. Urinary creatinine excretion and estimation of muscle mass in infants of 25–34 weeks gestation. Acta Paediatr Scand. 1990;79:1156–62.CrossRefPubMedGoogle Scholar
  86. 86.
    Malina RM. Growth of muscle tissue and muscle mass. In: Falkner F, Tanner JM, editors. Human growth: a comprehensive treatise. 2nd ed. New York (NY): Plenum Press; 1986. p. 77–99.Google Scholar
  87. 87.
    Bruce A. Skeletal muscle lipids. II. Changes in phospholipid composition in man from fetal to middle age. J Lipid Res. 1974;15:103–8.PubMedGoogle Scholar
  88. 88.
    Dale BA, Holbrook KA, Kimball JR, Hoff M, Sun TT. Expression of epidermal keratins and filaggrin during human fetal skin development. J Cell Biol. 1985;101:1257–69.CrossRefPubMedGoogle Scholar
  89. 89.
    Li J, Fu X, Sun X, Sun T, Sheng Z. The interaction between epidermal growth factor and matrix metalloproteinases induces the development of sweat glands in human fetal skin. J Surg Res. 2002;106:258–63.CrossRefPubMedGoogle Scholar
  90. 90.
    Roe HE. The weight of the skin and tela subcutanea of the human fetus. Anat Rec. 1933;55:127–37.CrossRefGoogle Scholar
  91. 91.
    Usher R, McLean F. Intrauterine growth of live-born Caucasian infants at sea level: standards obtained from measurements in 7 dimensions of infants born between 25 and 44 weeks of gestation. J Pediatr. 1969;74:901–10.CrossRefPubMedGoogle Scholar
  92. 92.
    Wilmer HA. Quantitative growth of skin and subcutaneous tissue in relation to human surface area. Proc Soc Exp Biol Med. 1940;43:386–8.CrossRefGoogle Scholar
  93. 93.
    Baker PN, Johnson IR, Gowland PA, Hykin J, Harvey PR, Freeman A, et al. Fetal weight estimation by echo-planar magnetic resonance imaging. Lancet. 1994;343:644–5.CrossRefPubMedGoogle Scholar
  94. 94.
    Friis-Hansen B. Body composition during growth: in vivo measurements and biochemical data correlated to differential anatomical growth. Pediatrics. 1971;47:Suppl. 2:264.Google Scholar
  95. 95.
    Lapillonne AA, Glorieux FH, Salle BL, Braillon PM, Chambon M, Rigo J, et al. Mineral balance and whole body bone mineral content in very low-birth-weight infants. Acta Paediatr. 1994;405:117–22.CrossRefGoogle Scholar
  96. 96.
    Demarini S, Koo WW, Hockman EM. Bone, lean and fat mass of newborn twins versus singletons. Acta Paediatr. 2006;95:594–9.CrossRefPubMedGoogle Scholar
  97. 97.
    Lapillonne A, Braillon P, Claris O, Chatelain PG, Delmas PD, Salle BL. Body composition in appropriate and in small for gestational age infants. Acta Paediatr. 1997;86:196–200.CrossRefPubMedGoogle Scholar
  98. 98.
    Salle BL, Rauch F, Travers R, Bouvier R, Glorieux FH. Human fetal bone development: histomorphometric evaluation of the proximal femoral metaphysis. Bone. 2002;30:823–8.CrossRefPubMedGoogle Scholar
  99. 99.
    Harvey NC, Mahon PA, Robinson SM, Nisbet CE, Javaid MK, Crozier SR, et al. Different indices of fetal growth predict bone size and volumetric density at 4 years of age. J Bone Miner Res. 2010;25:920–7.PubMedCentralPubMedGoogle Scholar
  100. 100.
    Walsh JM, Kilbane M, McGowan CA, McKenna MJ, McAuliffe FM. Pregnancy in dark winters: implications for fetal bone growth? Fertil Steril. 2013;99:206–11.CrossRefPubMedGoogle Scholar
  101. 101.
    Kara SA, Toppare MF. Ultrasonographic dimensions of the vertical span of the fetal iliac bone and relationship with some fetal parameters. Prenatal Diagn. 1998;18:127–32.CrossRefGoogle Scholar
  102. 102.
    Scheuer JL, Musgrave JH, Evans SP. The estimation of late fetal and perinatal age from limb bone length by linear and logarithmic regression. Ann Hum Biol. 1980;7:257–65.CrossRefPubMedGoogle Scholar
  103. 103.
    Trotter M, Peterson RR. Weight of bone in the fetus during the last half of pregnancy. Clin Orthop Relat Res. 1969;65:46–50.CrossRefPubMedGoogle Scholar
  104. 104.
    Hudson G. Bone-marrow volume in the human foetus and newborn. Br J Haematol. 1965;11:446–52.CrossRefPubMedGoogle Scholar
  105. 105.
    Braillon PM, Buenerd A, Lapillonne A, Bouvier R. Skeletal and total body volumes of human fetuses: assessment of reference data by spiral CT. Pediatr Radiol. 2002;32:354–9.CrossRefPubMedGoogle Scholar
  106. 106.
    Hudson G. Organ size of human foetal bone marrow. Nature. 1965;205:96–7.CrossRefPubMedGoogle Scholar
  107. 107.
    Wilpshaar J, Joekes EC, Lim FT, Van Leeuwen GA, Van den Boogaard PJ, Kanhai HH, et al. Magnetic resonance imaging of fetal bone marrow for quantitative definition of the human fetal stem cell compartment. Blood. 2002;100:451–7.CrossRefPubMedGoogle Scholar
  108. 108.
    Bronshtein M, Tzidony D, Dimant M, Hajos J, Jaeger M, Blumenfeld Z. Transvaginal ultrasonographic measurements of the fetal adrenal glands at 12 to 17 weeks of gestation. Am J Obstet Gynecoly. 1993;169:1205–10.CrossRefGoogle Scholar
  109. 109.
    Brugger PC, Prayer D. Fetal abdominal magnetic resonance imaging. Eur J Radiol. 2006;57:278–93.CrossRefPubMedGoogle Scholar
  110. 110.
    De Leon-Luis J, Gamez F, Pintado P, Antolin E, Perez R, Ortiz-Quintana L, et al. Sonographic measurements of the thymus in male and female fetuses. J Ultrasound Med. 2009;28:43–8.CrossRefPubMedGoogle Scholar
  111. 111.
    Zalel Y, Gamzu R, Mashiach S, Achiron R. The development of the fetal thymus: an in utero sonographic evaluation. Prenat Diagn. 2002;22:114–7.CrossRefPubMedGoogle Scholar
  112. 112.
    Liberti EA, Villa N, Melhem SA, Matson E, Konig B Jr, Adamo J. A morphometrical study of human fetal thymus. Z Mikrosk Anat Forsch. 1989;103:309–15.PubMedGoogle Scholar
  113. 113.
    Patel J, Landers K, Li H, Mortimer RH, Richard K. Thyroid hormones and fetal neurological development. J Endocrinol. 2011;209:1–8.CrossRefPubMedGoogle Scholar
  114. 114.
    Hobel CJ. Fetal thyroid. Clin Obstet Gynecol. 1980;23:779–90.CrossRefPubMedGoogle Scholar
  115. 115.
    Cohen O, Pinhas-Hamiel O, Sivan E, Dolitski M, Lipitz S, Achiron R. Serial in utero ultrasonographic measurements of the fetal thyroid: a new complementary tool in the management of maternal hyperthyroidism in pregnancy. Prenat Diagn. 2003;23:740–2.CrossRefPubMedGoogle Scholar
  116. 116.
    Ares S, Pastor I, Quero J, Morreale de Escobar G. Thyroid gland volume as measured by ultrasonography in preterm infants. Acta Paediatr. 1995;84:58–62.CrossRefPubMedGoogle Scholar
  117. 117.
    Bocian-Sobkowska J, Wozniak W, Malendowicz LK. Morphometric studies on the development of the human thyroid gland. II. The late fetal life. Histol Histopathol. 1997;12:79–84.PubMedGoogle Scholar
  118. 118.
    Guihard-Costa AM, Menez F, Delezoide AL. Organ weights in human fetuses after formalin fixation: standards by gestational age and body weight. Pediatr Dev Pathol. 2002;5:559–78.CrossRefPubMedGoogle Scholar
  119. 119.
    Ho SS, Metreweli C. Normal fetal thyroid volume. Ultrasound Obstet Gynecol. 1998;11:118–22.CrossRefPubMedGoogle Scholar
  120. 120.
    Ozguner G, Sulak O. Size and location of thyroid gland in the fetal period. Surg Radiol Anat. 2014;36:359–67.CrossRefPubMedGoogle Scholar
  121. 121.
    Savin-Žegarac S, Cvejic D, Nedić O, Radosavljević R, Ivana MP. Iodine and iodothyronine content in human neonate thyroid gland. Arch Biol Sci. 2002;54(3–4):69–74.CrossRefGoogle Scholar
  122. 122.
    Shepard TH, Andersen HJ, Andersen H. The human fetal thyroid. I. Its weight in relation to body weight, crown-rump length, foot length and estimated gestation age. Anat Rec. 1964;148:123–8.CrossRefPubMedGoogle Scholar
  123. 123.
    Valentin J. Basic anatomical and physiological data for use in radiological protection: reference values: ICRP Publication 89. Ann ICRP. 2002;32:1–277.CrossRefGoogle Scholar
  124. 124.
    Seely BL, Burrow GN. Thyroid disease and pregnancy. In: Creasy RK, Resnik R, editors. Maternal fetal medicine: principle and practice. Philadelphia (PA): WB Saunders; 1994. p. 979–1001.Google Scholar
  125. 125.
    Weaver LT. Anatomy and embryology. In: Walker WA, Dune PR, Hamilton RJ, editors. Pediatric gastrointestinal disease. 2nd ed. St. Louis (MO): Mosby; 1996.Google Scholar
  126. 126.
    Pritchard JA. Fetal swallowing and amniotic fluid volume. Obstet Gynecol. 1966;28:606–10.PubMedGoogle Scholar
  127. 127.
    Menard D. Functional development of the human gastrointestinal tract: hormone- and growth factor-mediated regulatory mechanisms. Can J Gastroenterol. 2004;18:39–44.CrossRefPubMedGoogle Scholar
  128. 128.
    Grand RJ, Watkins JB, Torti FM. Development of the human gastrointestinal tract: a review. Gastroenterology. 1976;70:790–810.PubMedGoogle Scholar
  129. 129.
    Bates MD, Balistreri WF. The gastrointestinal tract: development of the human digestive system. In: Fanaroff AA, Martin RJ, editors. Neonatal-perinatal medicine: diseases of the fetus and infant. 7th ed. St. Louis (MO): Mosby; 2002.Google Scholar
  130. 130.
    Malo C. Multiple pathways for amino acid transport in brush border membrane vesicles isolated from the human fetal small intestine. Gastroenterology. 1991;100:1644–52.CrossRefPubMedGoogle Scholar
  131. 131.
    Lebenthal A, Lebenthal E. The ontogeny of the small intestinal epithelium. JPEN J Parenter Enteral Nutr. 1999;23(5 Suppl.):S3–6.CrossRefPubMedGoogle Scholar
  132. 132.
    Goldstein I, Reece EA, Yarkoni S, Wan M, Green JL, Hobbins JC. Growth of the fetal stomach in normal pregnancies. Obstet Gynecol. 1987;70:641–4.PubMedGoogle Scholar
  133. 133.
    Nagata S, Koyanagi T, Fukushima S, Akazawa K, Nakano H. Change in the three-dimensional shape of the stomach in the developing human fetus. Early Hum Dev. 1994;37:27–38.CrossRefPubMedGoogle Scholar
  134. 134.
    Gworys B, Jeka S, Brukiewa R, Rymko M. Dynamics of stomach growth in the human fetal period: a post mortem study. Int J Morphol. 2012;30:461–6.CrossRefGoogle Scholar
  135. 135.
    Sase M, Asada H, Okuda M, Kato H. Fetal gastric size in normal and abnormal pregnancies. Ultrasound Obstet Gynecol. 2002;19:467–70.CrossRefPubMedGoogle Scholar
  136. 136.
    Hata T, Tanaka H, Noguchi J, Inubashiri E, Yanagihara T, Kondoh S. Three-dimensional sonographic volume measurement of the fetal stomach. Ultrasound Med Biol. 2010;36:1808–12.CrossRefPubMedGoogle Scholar
  137. 137.
    Ben-Haroush A, Yogev Y, Peled Y, Bar J, Hod M, Pardo J. Correlation between fetal gastric size and amniotic fluid volume. J Clin Ultrasound. 2005;33:119–22.CrossRefPubMedGoogle Scholar
  138. 138.
    Vierordt H. Anatomische Physiologische Und Physikalische Daten Und Tabellen Zum Gebrauche Für Mediziner. Jena: Verlag von Gustav Fischer; 1906.Google Scholar
  139. 139.
    Touloukian RJ, Smith GJ. Normal intestinal length in preterm infants. J Pediatr Surg. 1983;18:720–3.CrossRefPubMedGoogle Scholar
  140. 140.
    Struijs MC, Diamond IR, de Silva N, Wales PW. Establishing norms for intestinal length in children. J Pediatr Surg. 2009;44:933–8.CrossRefPubMedGoogle Scholar
  141. 141.
    Shanklin DR, Cooke RJ. Effects of intrauterine growth on intestinal length in the human fetus. Biol Neonate. 1993;64:76–81.CrossRefPubMedGoogle Scholar
  142. 142.
    Marnerides A, Ghazi S, Sundberg A, Papadogiannakis N. Development of fetal intestinal length during 2nd-trimester in normal and pathologic pregnancies. Pediatr Dev Pathol. 2012;15:24–9.CrossRefPubMedGoogle Scholar
  143. 143.
    FitzSimmons J, Chinn A, Shepard TH. Normal length of the human fetal gastrointestinal tract. Pediatr Pathol. 1988;8:633–41.CrossRefPubMedGoogle Scholar
  144. 144.
    Desdicioglu K, Malas MA, Evcil EH. Development of the fetal duodenum: a postmortem study. Fetal Diagn Ther. 2009;26:16–23.CrossRefPubMedGoogle Scholar
  145. 145.
    Rao-Mohandas KG, Somayaji SN, Bairy KL, Nayak S, Vincent R. A study to evaluate the relationship between the age of the fetus and intestinal length. Eur J Anat. 2006;10:151–2.Google Scholar
  146. 146.
    Weaver LT, Austin S, Cole TJ. Small intestinal length: a factor essential for gut adaptation. Gut. 1991;32:1321–3.PubMedCentralCrossRefPubMedGoogle Scholar
  147. 147.
    Malas MA, Aslankoc R, Ungor B, Sulak O, Candir O. The development of jejunum and ileum during the fetal period. Early Hum Dev. 2003;74:109–24.CrossRefPubMedGoogle Scholar
  148. 148.
    Herlinger H. Anatomy of the small intestine. In: Herlinger H, Maglinte D, Birnbaum BAE, editors. Clinical imaging of the small intestine. 2nd ed. New York (NY): Springer-Verlag New York, Inc.; 1999: p. 3–12.Google Scholar
  149. 149.
    Shah RS, Rajalakshmi R. Studies on human fetal tissues: I. Fetal weight and tissue weights in relation to gestational age, fetal size and maternal nutritional status. Indian J Pediatr. 1988;55:261–71.CrossRefPubMedGoogle Scholar
  150. 150.
    Zilianti M, Fernandez S. Correlation of ultrasonic images of fetal intestine with gestational age and fetal maturity. Obstet Gynecol. 1983;62:569–73.PubMedGoogle Scholar
  151. 151.
    Nyberg DA, Mack LA, Patten RM, Cyr DR. Fetal bowel: normal sonographic findings. J Ultrasound Med. 1987;6:3–6.CrossRefPubMedGoogle Scholar
  152. 152.
    Malas MA, Aslankoc R, Ungor B, Sulak O, Candir O. The development of large intestine during the fetal period. Early Hum Dev. 2004;78:1–13.CrossRefPubMedGoogle Scholar
  153. 153.
    Aoki S, Hata T, Senoh D, KM, Hata K, Takamiya O, et al. Ultrasonographic measurement of fetal colon. Acta Neanatol Jpn. 1989;25:559–62.Google Scholar
  154. 154.
    Goldstein I, Lockwood C, Hobbins JC. Ultrasound assessment of fetal intestinal development in the evaluation of gestational age. Obstet Gynecol. 1987;70:682–6.PubMedGoogle Scholar
  155. 155.
    Parulekar SG. Sonography of normal fetal bowel. J Ultrasound Med. 1991;10:211–20.CrossRefPubMedGoogle Scholar
  156. 156.
    Malas MA, Gokcimen A, Sulak O. Growing of caecum and vermiform appendix during the fetal period. Fetal Diagn Ther. 2001;16:173–7.CrossRefPubMedGoogle Scholar
  157. 157.
    Zalel Y, Perlitz Y, Gamzu R, Peleg D, Ben-Ami M. In-utero development of the fetal colon and rectum: sonographic evaluation. Ultrasound Obstet Gynecol. 2003;21:161–4.CrossRefPubMedGoogle Scholar
  158. 158.
    Rubesova E, Vance CJ, Ringertz HG, Barth RA. Three-dimensional MRI volumetric measurements of the normal fetal colon. AJR Am J Roentgenol. 2009;192:761–5.CrossRefPubMedGoogle Scholar
  159. 159.
    Clatworthy H Jr, Anderson RG. Development and growth of the human embryo and fetus: a graphic representation of some aspects. Am J Dis Child. 1944;67(3):167–75.CrossRefGoogle Scholar
  160. 160.
    ICRP. Human alimentary tract model for radiological protection. Ann ICRP. 2006.  https://doi.org/10.1016/j.icrp.2006.03.001.CrossRefGoogle Scholar
  161. 161.
    Scammon RE. Some graphs and tables illustrating the growth of the human stomach. Am J Dis Child. 1919;17:395–422.Google Scholar
  162. 162.
    Hata K, Hata T, Kitao M. Ultrasonographic identification and measurement of the human fetal pancreas in utero. Int J Gynaecol Obstet. 1988;26:61–4.CrossRefPubMedGoogle Scholar
  163. 163.
    Sampaio FJ. Analysis of kidney volume growth during the fetal period in humans. Urol Res. 1992;20:271–4.CrossRefPubMedGoogle Scholar
  164. 164.
    Xu D, Chen M, Pan XL, Xia LP, Wang H. Dexamethasone induces fetal developmental toxicity through affecting the placental glucocorticoid barrier and depressing fetal adrenal function. Environ Toxicol Pharmacol. 2011;32:356–63.CrossRefPubMedGoogle Scholar
  165. 165.
    Ping J, Wang JF, Liu L, Yan YE, Liu F, Lei YY, et al. Prenatal caffeine ingestion induces aberrant DNA methylation and histone acetylation of steroidogenic factor 1 and inhibits fetal adrenal steroidogenesis. Toxicology. 2014;321:53–61.CrossRefPubMedGoogle Scholar
  166. 166.
    Sayed MM. Effect of prenatal exposure to nicotine/thiocyanate on the pituitary–adrenal axis of 1-month-old rat offspring. Egypt J Histol. 2016;39:307–16.CrossRefGoogle Scholar
  167. 167.
    Viau M, Collin-Faure V, Richaud P, Ravanat JL, Candeias SM. Cadmium and T cell differentiation: limited impact in vivo but significant toxicity in fetal thymus organ culture. Toxicol Appl Pharmacol. 2007;223:257–66.CrossRefPubMedGoogle Scholar
  168. 168.
    Holladay SD, Smith BJ. Fetal hematopoietic alterations after maternal exposure to benzo[a]pyrene: a cytometric evaluation. J Toxicol Environ Health. 1994;42:259–73.CrossRefPubMedGoogle Scholar
  169. 169.
    Holladay SD, Luster MI. Alterations in fetal thymic and liver hematopoietic cells as indicators of exposure to developmental immunotoxicants. Environ Health Perspect. 1996;104(Suppl. 4):809–13.PubMedCentralCrossRefPubMedGoogle Scholar
  170. 170.
    Thayyil S, Cleary JO, Sebire NJ, Scott RJ, Chong K, Gunny R, et al. Post-mortem examination of human fetuses: a comparison of whole-body high-field MRI at 9.4 T with conventional MRI and invasive autopsy. Lancet. 2009;374:467–75.CrossRefPubMedGoogle Scholar
  171. 171.
    Araujo Junior E, Nardozza LM, Rolo LC, Nowak PM, Filho JB, Moron AF. Reference range of embryo volume by 3-D sonography using the XI VOCAL method at 7 to 10 + 6 weeks of pregnancy. Am J Perinatol. 2010;27:501–5.CrossRefPubMedGoogle Scholar
  172. 172.
    Kehl S, Kalk AL, Eckert S, Schaible T, Sutterlin M, Neff W, et al. Assessment of lung volume by 3-dimensional sonography and magnetic resonance imaging in fetuses with congenital diaphragmatic hernias. J Ultrasound Med. 2011;30:1539–45.CrossRefPubMedGoogle Scholar
  173. 173.
    Strizek B, Cos Sanchez T, Khalife J, Jani J, Cannie M. Impact of operator experience on the variability of fetal lung volume estimation by 3D-ultrasound (VOCAL) and magnetic resonance imaging in fetuses with congenital diaphragmatic hernia. J Matern Fetal Neonatal Med. 2015;28(7):858–64.CrossRefPubMedGoogle Scholar
  174. 174.
    Won HS, Lee SJ, Jun SM. Clinical application and usefulness of XI VOCAL in volume measurement [White paper]. Seoul: Medison Co, Ltd; 2006: 1–3.Google Scholar
  175. 175.
    Barreto EQ, Milani HJ, Haratz KK, Araujo Junior E, Nardozza LM, Moron AF. Reference intervals for fetal heart volume from 3-dimensional sonography using the extended imaging virtual organ computer-aided analysis method at gestational ages of 20 to 34 weeks. J Ultrasound Med. 2012;31:673–8.CrossRefPubMedGoogle Scholar
  176. 176.
    Chang FM, Hsu KF, Ko HC, Yao BL, Chang CH, Yu CH, et al. Fetal heart volume assessment by three-dimensional ultrasound. Ultrasound Obstet Gynecol. 1997;9:42–8.CrossRefPubMedGoogle Scholar
  177. 177.
    Cussen L, Scurry J, Mitropoulos G, McTigue C, Gross J. Mean organ weights of an Australian population of fetuses and infants. J Paediatr Child Health. 1990;26:101–3.CrossRefPubMedGoogle Scholar
  178. 178.
    Gruenwald P, Hoang Ngoc M. Evaluation of body and organ weights in perinatal pathology. I. Normal standards derived from autopsies. Am J Clin Pathol. 1960;34:247–53.CrossRefPubMedGoogle Scholar
  179. 179.
    Hansen K, Sung CJ, Huang C, Pinar H, Singer DB, Oyer CE. Reference values for second trimester fetal and neonatal organ weights and measurements. Pediatr Dev Pathol. 2003;6:160–7.CrossRefPubMedGoogle Scholar
  180. 180.
    Marecki B. Changes in the weight of internal organs in the fetal ontogenesis. Z Morphol Anthropol. 1989;77:235–45.PubMedGoogle Scholar
  181. 181.
    Maroun LL, Graem N. Autopsy standards of body parameters and fresh organ weights in nonmacerated and macerated human fetuses. Pediatr Dev Pathol. 2005;8:204–17.CrossRefPubMedGoogle Scholar
  182. 182.
    Mitropoulos G, Scurry J, Cussen L. Organ weight/bodyweight ratios: growth rates of fetal organs in the latter half of pregnancy with a simple method for calculating mean organ weights. J Paediatr Child Health. 1992;28:236–9.CrossRefPubMedGoogle Scholar
  183. 183.
    Peralta CF, Cavoretto P, Csapo B, Falcon O, Nicolaides KH. Lung and heart volumes by three-dimensional ultrasound in normal fetuses at 12–32 weeks’ gestation. Ultrasound Obstet Gynecol. 2006;27:128–33.CrossRefPubMedGoogle Scholar
  184. 184.
    Phillips JB, Billson VR, Forbes AB. Autopsy standards for fetal lengths and organ weights of an Australian perinatal population. Pathology. 2009;41:515–26.CrossRefPubMedGoogle Scholar
  185. 185.
    Schulz DM, Giordano DA, Schulz DH. Weights of organs of fetuses and infants. Arch Pathol. 1962;74:244–50.PubMedGoogle Scholar
  186. 186.
    Ozguner G, Sulak O, Koyuncu E. A morphometric study of suprarenal gland development in the fetal period. Surg Radiol Anat. 2012;34:581–7.CrossRefPubMedGoogle Scholar
  187. 187.
    Singer DB, Sung CJ, Wigglesworth JS. Fetal growth and maturation: with standards for body and organ development. In: Wigglesworth JS, Singer DB, editors. Textbook of fetal and perinatal pathology. London: Blackwell Scientific Publications; 1991. p. 11–47.Google Scholar
  188. 188.
    Duncan KR, Issa B, Moore R, Baker PN, Johnson IR, Gowland PA. A comparison of fetal organ measurements by echo-planar magnetic resonance imaging and ultrasound. BJOG. 2005;112:43–9.CrossRefPubMedGoogle Scholar
  189. 189.
    Gielecki J, Zurada A, Kozlowska H, Nowak D, Loukas M. Morphometric and volumetric analysis of the middle cerebral artery in human fetuses. Acta Neurobiol Exp (Wars). 2009;69:129–37.PubMedGoogle Scholar
  190. 190.
    Boito SM, Laudy JA, Struijk PC, Stijnen T, Wladimiroff JW. Three-dimensional US assessment of hepatic volume, head circumference, and abdominal circumference in healthy and growth-restricted fetuses. Radiology. 2002;223:661–5.CrossRefPubMedGoogle Scholar
  191. 191.
    Casey ML, Carr BR. Growth of the kidney in the normal human fetus during early gestation. Early Hum Dev. 1982;6:11–4.CrossRefPubMedGoogle Scholar
  192. 192.
    Jeanty P, Dramaix-Wilmet M, Elkhazen N, Hubinont C, van Regemorter N. Measurements of fetal kidney growth on ultrasound. Radiology. 1982;144:159–62.CrossRefPubMedGoogle Scholar
  193. 193.
    Michielsen K, Meersschaert J, De Keyzer F, Cannie M, Deprest J, Claus F. MR volumetry of the normal fetal kidney: reference values. Prenatal Diagn. 2010;30:1044–8.CrossRefGoogle Scholar
  194. 194.
    Tedesco GD, Bussamra LC, Araujo Junior E, Britto IS, Nardozza LM, Moron AF, et al. Reference range of fetal renal volume by three-dimensional ultrasonography using the VOCAL method. Fetal Diagn Ther. 2009;25:385–91.CrossRefPubMedGoogle Scholar
  195. 195.
    van Vuuren SH, Damen-Elias HA, Stigter RH, van der Doef R, Goldschmeding R, de Jong TP, et al. Size and volume charts of fetal kidney, renal pelvis and adrenal gland. Ultrasound Obstet Gynecol. 2012;40:659–64.CrossRefPubMedGoogle Scholar
  196. 196.
    Bahmaie A, Hughes SW, Clark T, Milner A, Saunders J, Tilling K, et al. Serial fetal lung volume measurement using three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2000;16:154–8.CrossRefPubMedGoogle Scholar
  197. 197.
    Gerards FA, Engels MA, Twisk JW, van Vugt JM. Normal fetal lung volume measured with three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2006;27:134–44.CrossRefPubMedGoogle Scholar
  198. 198.
    Moeglin D, Talmant C, Duyme M, Lopez AC. Fetal lung volumetry using two- and three-dimensional ultrasound. Ultrasound Obstet Gynecol. 2005;25:119–27.CrossRefPubMedGoogle Scholar
  199. 199.
    Pohls UG, Rempen A. Fetal lung volumetry by three-dimensional ultrasound. Ultrasound Obstet Gynecol. 1998;11:6–12.CrossRefPubMedGoogle Scholar
  200. 200.
    Ruano R, Joubin L, Aubry MC, Thalabard JC, Dommergues M, Dumez Y, et al. A nomogram of fetal lung volumes estimated by 3-dimensional ultrasonography using the rotational technique (virtual organ computer-aided analysis). J Ultrasound Med. 2006;25:701–9.CrossRefPubMedGoogle Scholar
  201. 201.
    Hata T, Kuno A, Dai SY, Inubashiri E, Hanaoka U, Kanenishi K, et al. Three-dimensional sonographic volume measurement of the fetal spleen. J Obstet Gynaecol Res. 2007;33:600–5.CrossRefPubMedGoogle Scholar
  202. 202.
    Welcker H, Brandt A. Gewichtswerthe der Körper-organe bei dem Menschen und den Thieren: ein Beitrag zur vergleichenden Anatomie und Entwickelungsgeschichte. Arch f Anthrop. 1902;28:1–89.Google Scholar
  203. 203.
    Trotter M, Peterson RR. Weight of bone in the fetus: a preliminary report. Growth. 1968;32:83–90.PubMedGoogle Scholar
  204. 204.
    Ozguner G, Sulak O. Size and location of thyroid gland in the fetal period. Surg Radiol Anat. 2014;36(4):359–67.CrossRefPubMedGoogle Scholar

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Authors and Affiliations

  1. 1.Certara UK Limited (Simcyp)SheffieldUK

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