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Placental measurements associated with intelligence quotient at age 7 years

Published online by Cambridge University Press:  20 March 2012

D. P. Misra*
Affiliation:
Department of Family Medicine, Wayne State University, Detroit, MI, USA
C. M. Salafia
Affiliation:
Placental Analytics, LLC, Larchmont, NY, USA Institute for Basic Research, Staten Island, NY, USA
A. K. Charles
Affiliation:
Department of Pathology, Princess Margaret Hospital, Perth, WA, Australia
R. K. Miller
Affiliation:
Department of Obstetrics and Gynecology, University of Rochester, Rochester NY, USA
*
*Address for correspondence: Dr D. P. Misra, Department of Family Medicine, Wayne State University, 3939 Woodward Avenue, Room 318, Detroit, MI, USA 48170. (Email dmisra@med.wayne.edu)

Abstract

We hypothesized that placental villous branching that is measured by disk chorionic plate expansion and disk thickness is correlated with factors also involved in regulation of branching growth of other fetal viscera (e.g. lung, kidney) including neuronal dendrites, and thus may be associated with variation in childhood intelligence quotient (IQ). IQ at age 7 years was assessed using the Wechsler Intelligence Scale for Children. Placental measures [placental weight (g), thickness (mm), chorionic plate surface diameters (cm), area (cm2), shape, and cord length and cord eccentricity] were independent variables in regression analyses of age 7-year IQ in 12,926 singleton term live born infants with complete placental data. Analyses were stratified on gender with adjustment for socioeconomic status, race, parity, gestational age, exact age at testing and centered parental ages. After adjustment for covariates, placental measurements were independently associated with IQ at age 7 years but results varied by gender. Chorionic plate diameters were only associated with higher IQ in girls. Placental thickness was positively associated with higher IQ for boys and girls. We have previously shown that placental measures affect age 7-year body mass index and diastolic blood pressure. Here we demonstrate that specific measures, placental chorionic plate diameters in girls and disk thickness, independent of gender, are correlated with age 7-year IQ. Further exploration of the possible interaction of these factors on the placental villous arborization reflected by the chorionic plate expansion and placental thickness that correlate with age 7-year IQ, as well as other age 7 somatic features as previously addressed, is indicated.

Type
Original Article
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012

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References

1. Hemachandra, AH, Klebanoff, MA, Duggan, AK, Hardy, JB, Furth, SL. The association between intrauterine growth restriction in the full-term infant and high blood pressure at age 7 years: results from the Collaborative Perinatal Project. Int J Epidemiol. 2006; 35, 871877.CrossRefGoogle ScholarPubMed
2. Thame, M, Osmond, C, Wilks, RJ, et al. . Blood pressure is related to placental volume and birth weight. Hypertension. 2000; 35, 662667.CrossRefGoogle ScholarPubMed
3. Risnes, KR, Romundstad, PR, Nilsen, TIL, Eskild, A, Vatten, LJ. Placental weight relative to birth weight and long-term cardiovascular mortality: findings from a cohort of 31,307 men and women. Am J Epidemiol. 2009; 170, 622631.CrossRefGoogle Scholar
4. Gatford, KL, Simmons, RA, De Blasio, MJ, Robinson, JS, Owens, JA. Review: Placental programming of postnatal diabetes and impaired insulin action after IUGR. Placenta. 2010; 31(Suppl.), S60S65.CrossRefGoogle ScholarPubMed
5. Gheorghe, CP, Goyal, R, Mittal, A, Longo, LD. Gene expression in the placenta: maternal stress and epigenetic responses. Int J Dev Biol. 2010; 54, 507523.CrossRefGoogle ScholarPubMed
6. Thompson, JA, Regnault, TRH. In utero origins of adult insulin resistance and vascular dysfunction. Semin Reprod Med. 2011; 29, 211224.CrossRefGoogle ScholarPubMed
7. Rees, S, Inder, T. Fetal and neonatal origins of altered brain development. Early Hum Dev. 2005; 81, 753761.CrossRefGoogle ScholarPubMed
8. Coe, CL, Lubach, GR. Prenatal origins of individual variation in behavior and immunity. Neurosci Biobehav Rev. 2005; 29, 3949.CrossRefGoogle ScholarPubMed
9. Liu, Y, Zhi, M, Li, X. Parental age and characteristics of the offspring. Ageing Res Rev. 2011; 10, 115123.CrossRefGoogle ScholarPubMed
10. Campbell, DM, Hall, MH, Barker, DJ, et al. . Diet in pregnancy and the offspring's blood pressure 40 years later. Br J Obstet Gynaecol. 1996; 103, 273280.CrossRefGoogle ScholarPubMed
11. Barker, DJ, Bull, AR, Osmond, C, Simmonds, SJ. Fetal and placental size and risk of hypertension in adult life. BMJ. 1990; 301, 259262.CrossRefGoogle ScholarPubMed
12. Eriksson, J, Forsen, T, Tuomilehto, J, Osmond, C, Barker, D. Fetal and childhood growth and hypertension in adult life. Hypertension. 2000; 36, 790794.CrossRefGoogle ScholarPubMed
13. Whincup, P, Cook, D, Papacosta, O, Walker, M. Birth weight and blood pressure: cross sectional and longitudinal relations in childhood. BMJ. 1995; 311, 773776.CrossRefGoogle ScholarPubMed
14. Misra, D, CM, S, Chadha, K, Charles, A, Miller, RK. Birthweights smaller or larger than the placenta predict BMI and blood pressure at age 7 years. J Dev Orig Health Dis. 2010; 1, 123130.CrossRefGoogle ScholarPubMed
15. Misra, DP, Salafia, CM, Miller, RK, Charles, AK. Non-linear and gender-specific relationships among placental growth measures and the fetoplacental weight ratio. Placenta. 2009; 30, 10521057.CrossRefGoogle ScholarPubMed
16. Salafia, CM, Maas, E, Thorp, JM, et al. . Measures of placental growth in relation to birth weight and gestational age. Am J Epidemiol. 2005; 162, 991998.CrossRefGoogle ScholarPubMed
17. Salafia, CM, Misra, DP, Yampolsky, M, Charles, AK, Miller, RK. Allometric metabolic scaling and fetal and placental weight. Placenta. 2009; 30, 355360.CrossRefGoogle ScholarPubMed
18. Salafia, CM, Zhang, J, Charles, AK, et al. . Placental characteristics and birthweight. Paediatr Perinat Epidemiol. 2008; 22, 229239.CrossRefGoogle ScholarPubMed
19. Salafia, CM, Zhang, J, Miller, RK, et al. . Placental growth patterns affect birth weight for given placental weight. Birth Defects Res A Clin Mol Teratol. 2007; 79, 281288.CrossRefGoogle ScholarPubMed
20. Camp, BW, Broman, SH, Nichols, PL, Leff, M. Maternal and neonatal risk factors for mental retardation: defining the ‘at-risk’ child. Early Hum Dev. 1998; 50, 159173.CrossRefGoogle ScholarPubMed
21. Ellman, LM, Yolken, RH, Buka, SL, Torrey, EF, Cannon, TD. Cognitive functioning prior to the onset of psychosis: the role of fetal exposure to serologically determined influenza infection. Biol Psychiatry. 2009; 65, 10401047.CrossRefGoogle Scholar
22. Gray, KA, Klebanoff, MA, Brock, JW, et al. . In utero exposure to background levels of polychlorinated biphenyls and cognitive functioning among school-age children. Am J Epidemiol. 2005; 162, 1726.CrossRefGoogle ScholarPubMed
23. Holden, KR, Mellits, ED, Freeman, JM. Neonatal seizures. I. Correlation of prenatal and perinatal events with outcomes. Pediatrics. 1982; 70, 165176.CrossRefGoogle ScholarPubMed
24. Klebanoff, MA, Berendes, HW. Aspirin exposure during the first 20 weeks of gestation and IQ at four years of age. Teratology. 1988; 37, 249255.CrossRefGoogle ScholarPubMed
25. LeWinn, KZ, Stroud, LR, Molnar, BE, et al. . Elevated maternal cortisol levels during pregnancy are associated with reduced childhood IQ. Int J Epidemiol. 2009; 38, 17001710.CrossRefGoogle ScholarPubMed
26. Strauss, RS, Dietz, WH. Growth and development of term children born with low birth weight: effects of genetic and environmental factors. J Pediatr. 1998; 133, 6772.CrossRefGoogle ScholarPubMed
27. Broman, S. Prenatal risk factors for mental retardation in young children. Public Health Rep. 1987; 102(Suppl. 4), 5557.Google ScholarPubMed
28. Craven, CM, Zhao, L, Ward, K. Lateral placental growth occurs by trophoblast cell invasion of decidual veins. Placenta. 2000; 21, 160169.CrossRefGoogle ScholarPubMed
29. Benirschke, K, Kaufmann, P, Baergen, R. Architecture of normal villous trees. In The Human Placenta, 5th edn (eds. Benirschke K, Kaufman P), 2006; pp. 121141. Springer: New York.Google Scholar
30. Sagol, S, Sagol, O, Ozdemir, N. Stereological quantification of placental villus vascularization and its relation to umbilical artery Doppler flow in intrauterine growth restriction. Prenat Diagn. 2002; 22, 398403.CrossRefGoogle ScholarPubMed
31. Mitra, SC, Seshan, SV, Riachi, LE. Placental vessel morphometry in growth retardation and increased resistance of the umbilical artery Doppler flow. J Matern Fetal Med. 2000; 9, 282286.3.0.CO;2-J>CrossRefGoogle ScholarPubMed
32. Sebire, NJ, Talbert, D. ‘Cor placentale’: placental intervillus/intravillus blood flow mismatch is the pathophysiological mechanism in severe intrauterine growth restriction due to uteroplacental disease. Med Hypotheses. 2001; 57, 354357.CrossRefGoogle ScholarPubMed
33. Saha, S, Barnett, AG, Foldi, C, et al. . Advanced paternal age is associated with impaired neurocognitive outcomes during infancy and childhood. PLoS Med. 2009; 6, e40.CrossRefGoogle ScholarPubMed
34. Baptiste-Roberts, K, Salafia, CM, Nicholson, WK, et al. . Gross placental measures and childhood growth. J Matern Fetal Neona. 2009; 22, 1323.CrossRefGoogle ScholarPubMed
35. Benirschke, K. Examination of the Placenta; Collaborative Study on Cerebral Palsy, Mental Retardation and Other Neurological and Sensory Disorders of Infancy and Childhood, 1961: National Institute of Neurologic Disease and Blindness, US Department of Health, Education and Welfare. Washington, DC.Google Scholar
36. Wood, F. Comment: effect of centering on collinearity and interpretation of the constant. Am Stat. 1984; 38, 8890.Google Scholar
37. Myrianthopoulos, N, French, K. An application of the U.S. Bureau of the Census socioeconomic index to a large, diversified patient population. Soc Sci Med. 1968; 2, 283299.CrossRefGoogle ScholarPubMed
38. Wechsler. Manual for the Wechsler Intelligence Scale for Children 1949. The Psychological Corporation: New York.Google Scholar
39. Clark, EAS, Mele, L, Wapner, RJ, et al. . Association of fetal inflammation and coagulation pathway gene polymorphisms with neurodevelopmental delay at age 2 years. Am J Obstet Gynecol. 2010; 203, 83.e183.e10.CrossRefGoogle ScholarPubMed
40. Salafia, CM, Misra, DP, Yampolsky, M, Charles, AK, Miller, RK. Allometric metabolic scaling and fetal and placental weight. Placenta. 2009; 30, 355360.CrossRefGoogle ScholarPubMed
41. Salafia, CM, Yampolsky, M, Shlakhter, A, Mandel, DH, Schwartz, N. Variety in placental shape: when does it originate? Placenta. 2012; 33, 164170.CrossRefGoogle ScholarPubMed
42. Naglieri, J, Goldstein, S. Understanding the strengths and weaknesses of intelligence and achievement tests. In Practitioner's Guide to Assessing Intelligence and Achievement (eds. Naglieri J, Goldstein S), 2009; pp. 3–10. John Wiley and Sons: Hoboken, NJ.Google Scholar
43. Zacchigna, S, Ruiz de Almodovar, C, Carmeliet, P. Similarities between angiogenesis and neural development: what small animal models can tell us. Curr Top Dev Biol. 2008; 80, 155.Google ScholarPubMed
44. Eichmann, A, Le Noble, F, Autiero, M, Carmeliet, P. Guidance of vascular and neural network formation. Curr Opin Neurobiol. 2005; 15, 108115.CrossRefGoogle ScholarPubMed
45. Autiero, M, De Smet, F, Claes, F, Carmeliet, P. Role of neural guidance signals in blood vessel navigation. Cardiovasc Res. 2005; 65, 629638.CrossRefGoogle ScholarPubMed
46. Davies, JA. Do different branching epithelia use a conserved developmental mechanism? Bioessays. 2002; 24, 937948.CrossRefGoogle ScholarPubMed
47. Patel, N, Sharpe, PT, Miletich, I. Coordination of epithelial branching and salivary gland lumen formation by Wnt and FGF signals. Dev Biol. 2011; 358, 156167.CrossRefGoogle ScholarPubMed
48. Mayhew, TM. Fetoplacental angiogenesis during gestation is biphasic, longitudinal and occurs by proliferation and remodelling of vascular endothelial cells. Placenta. 2002; 23, 742750.CrossRefGoogle ScholarPubMed
49. Benirshcke, K, Kaufmann, P, Baergen, R. Fetoplacental angiogenesis as the driving force for villous development. In The Human Placenta, 5th edn (eds. Benirschke K, Kaufman P), 2006; pp. 146154. Springer, New York.Google Scholar
50. Kingdom, J, Huppertz, B, Seaward, G, Kaufmann, P. Development of the placental villous tree and its consequences for fetal growth. Eur J Obstet Gynecol Reprod Biol. 2000; 92, 3543.CrossRefGoogle ScholarPubMed
51. Storkebaum, E, Lambrechts, D, Carmeliet, P. VEGF: once regarded as a specific angiogenic factor, now implicated in neuroprotection. Bioessays. 2004; 26, 943954.CrossRefGoogle ScholarPubMed
52. Hu, Y, Wang, Y-d, Guo, T, et al. . Identification of brain-derived neurotrophic factor as a novel angiogenic protein in multiple myeloma. Cancer Genet Cytogenet. 2007; 178, 110.CrossRefGoogle ScholarPubMed
53. Li, Q, Ford, MC, Lavik, EB, Madri, JA. Modeling the neurovascular niche: VEGF- and BDNF-mediated cross-talk between neural stem cells and endothelial cells: an in vitro study. J Neurosci Res. 2006; 84, 16561668.CrossRefGoogle ScholarPubMed
54. Newton, SS, Duman, RS. Regulation of neurogenesis and angiogenesis in depression. Curr Neurovasc Res. 2004; 1, 261267.CrossRefGoogle ScholarPubMed
55. Kutcher, ME, Klagsbrun, M, Mamluk, R. VEGF is required for the maintenance of dorsal root ganglia blood vessels but not neurons during development. FASEB J. 2004; 18, 19521954.CrossRefGoogle Scholar
56. Van Den Bosch, L, Storkebaum, E, Vleminckx, V, et al. . Effects of vascular endothelial growth factor (VEGF) on motor neuron degeneration. Neurobiol Dis. 2004; 17, 2128.CrossRefGoogle ScholarPubMed
57. Carmeliet, P, Storkebaum, E. Vascular and neuronal effects of VEGF in the nervous system: implications for neurological disorders. Semin Cell Dev Biol. 2002; 13, 3953.CrossRefGoogle ScholarPubMed
58. Jin, K, Zhu, Y, Sun, Y, et al. . Vascular endothelial growth factor (VEGF) stimulates neurogenesis in vitro and in vivo. Proc Natl Acad Sci U S A. 2002; 99, 1194611950.CrossRefGoogle ScholarPubMed
59. Jin, KL, Mao, XO, Greenberg, DA. Vascular endothelial growth factor: direct neuroprotective effect in in vitro ischemia. Proc Natl Acad Sci U S A. 2000; 97, 1024210247.CrossRefGoogle ScholarPubMed
60. JrLouissaint, A, Rao, S, Leventhal, C, Goldman, SA. Coordinated interaction of neurogenesis and angiogenesis in the adult songbird brain. Neuron. 2002; 34, 945960.CrossRefGoogle ScholarPubMed
61. Pitzer, MR, Sortwell, CE, Daley, BF, et al. . Angiogenic and neurotrophic effects of vascular endothelial growth factor (VEGF165): studies of grafted and cultured embryonic ventral mesencephalic cells. Exp Neurol. 2003; 182, 435445.CrossRefGoogle ScholarPubMed
62. Rosenstein, JM, Mani, N, Khaibullina, A, Krum, JM. Neurotrophic effects of vascular endothelial growth factor on organotypic cortical explants and primary cortical neurons. J Neurosci. 2003; 23, 1103611044.CrossRefGoogle ScholarPubMed
63. Sondell, M, Lundborg, G, Kanje, M. Vascular endothelial growth factor has neurotrophic activity and stimulates axonal outgrowth, enhancing cell survival and Schwann cell proliferation in the peripheral nervous system. J Neurosci. 1999; 19, 57315740.CrossRefGoogle ScholarPubMed
64. Sondell, M, Sundler, F, Kanje, M. Vascular endothelial growth factor is a neurotrophic factor which stimulates axonal outgrowth through the flk-1 receptor. Eur J Neurosci. 2000; 12, 42434254.CrossRefGoogle ScholarPubMed
65. Reynolds, LP, Borowicz, PP, Caton, JS, et al. . Uteroplacental vascular development and placental function: an update. Int J Dev Biol. 2010; 54, 355366.CrossRefGoogle ScholarPubMed
66. Helmestam, M, Stavreus-Evers, A, Olovsson, M. Cadmium chloride alters mRNA levels of angiogenesis related genes in primary human endometrial endothelial cells grown in vitro. Reprod Toxicol (Elmsford, N Y). 2010; 30, 370376.CrossRefGoogle ScholarPubMed
67. Thaxton, JE, Sharma, S. Interleukin-10: a multi-faceted agent of pregnancy. Am J Reprod Immunol (New York, N Y). 1989; 63, 482491.CrossRefGoogle Scholar
68. Giudice, LC. Microarray expression profiling reveals candidate genes for human uterine receptivity. Am J Pharmacogenomics. 2004; 4, 299312.CrossRefGoogle ScholarPubMed
69. Yampolsky, M, CM, S, Shlakhter, O, et al. . Variable placental thickness affects placental functional efficiency independent of other placental shape abnormalities. J Dev Orig Health Dis. 2011; 2, 205211.CrossRefGoogle ScholarPubMed