Microscopic Manifestations of Maternal Diabetes in Placental Structure
Main Article Content
Abstract
The human placenta is crucial for prenatal development and good pregnancy outcome. Maternal diabetic disorder influences normal intrauterine development of individual and expresses itself in the placenta. Due to the progress in diagnostic methods and methods of metabolic compensation the macroscopic signs associated with maternal diabetes, e.g., placentomegaly, occur nowadays rarely. In the microscopic picture of placenta there are no structural differences specific for maternal diabetes. However, the application of quantitative morphological methods has revealed some differences of normal and diabetic placenta. Stereological studies have shown significantly higher total volume of peripheral villi that distorts shapes and dimensions of pores in the intervillous space, and larger surface areas of peripheral villi and villous capillaries. Methods of confocal microscopy and 3D reconstruction gave the evidence that the fetus reacts on the hypoxia in maternal diabetic environment by enhanced angiogenesis and branching of villous capillaries. The enhanced tissue volumes are conditioned by higher mitotic activity. However, it decreases the proliferative potential of cells taking part in the enlargement of key structures for maternofetal transport at the end of pregnancy. Syncytiotrophoblast produces many factors playing important roles in maternal and fetal regulation and in the placenta itself. Quantitative methods of catalytic histochemistry and immunocytochemistry pointed at the role of maternal diabetes in decreased synthesis of some of those factors (e.g., alkaline phosphatase, SP1 glycoprotein). The presented data show that the quantitative morphological methods contribute to better understanding of the influence of maternal diabetes on fetoplacental unit.
Article Details
How to Cite
JIRKOVSKÁ, Marie.
Microscopic Manifestations of Maternal Diabetes in Placental Structure.
Medical Research Archives, [S.l.], v. 11, n. 7.2, july 2023.
ISSN 2375-1924.
Available at: <https://esmed.org/MRA/mra/article/view/4141>. Date accessed: 22 dec. 2024.
doi: https://doi.org/10.18103/mra.v11i7.2.4141.
Section
Research Articles
The Medical Research Archives grants authors the right to publish and reproduce the unrevised contribution in whole or in part at any time and in any form for any scholarly non-commercial purpose with the condition that all publications of the contribution include a full citation to the journal as published by the Medical Research Archives.
References
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3. Honda M, Toyoda C, Nakabayashi M, Omori Y. Quantitative investigations of placental terminal villi in maternal diabetes mellitus by scanning and transmission electron microscopy. Tohoku J Exp Med. 1992;167(4): 247-257. doi: 10.1620/tjem.167.247.
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5. Teasdale F. Histomorphometry of the placenta of the diabetic women: class A diabetes mellitus. Placenta. 1981; 2(3): 241-252. doi: 10.1016/s0143-4004(81)80007-0.
6. Teasdale F. Histomorphometry of the human placenta in class B diabetes mellitus. Placenta. 1983; 4(1):1-12. doi: 10.1016/s0143-4004(83)80012-5.
7. Teasdale F. Histomorphometry of the human placenta in class C diabetes mellitus. Placenta.1985; 6(1): 69-82. doi: 10.1016/s0143-4004(85)80034-5.
8. Teasdale F, Jean-Jacques G. Morphometry of the microvillous membrane of the human placenta in maternal diabetes mellitus. Placenta. 1986;7 :81-88. doi: 10.1016/s0143-4004(86)80020-0
9. Mayhew TM, Sørensen FB, Klebe JG, Jackson MR. Growth and maturation of villi in placentae from well-controlled diabetic women. Placenta. 1994; 15:57-65. doi: 10.1016/s0143-4004(05)80236-x.
10. Mayhew TM. Paterns of villous and intervillous space growth in human placentas from normal and abnormal pregnancies. Eur J Obstet Gynecol Reprod Biol. 1996;68(1-2):75-82. doi: 10.1016/0301-2115(96)02486-4.
11. Mayhew TM, Sisley I. Quantitative studies on the villi, trophoblast and intervillous pores of placentae from women with well-controlled diabetes mellitus. Placenta. 1998; 19: 371-377. doi: 10.1016/s0143-4004(98)90076-5.
12. Mayhew TM, Jairam IC. Stereological comparison of 3D spatial relationships involving villi and intervillous pores in human placentas from control and diabetic pregnancies. J Anat. 2000; 197:263-274. doi: 10.1046/j.1469-7580.2000.19720263.x.
13. Mayhew TM, Sørensen FB, Klebe JG, Jackson MR. The effects of mode of delivery and sex of newborn on placental morphology in control and diabetic pregnancies. J Anat. 1993;183: 545-552. PMID: 8300431
14. Jauniaux E, Burton GJ. Villous histomorphometry and placental bed biopsy in diabetic pregnancies. Placenta. 2006; 27 (4-5): 468-474. doi: 10.1016/j.placenta.2005.04.010.
15. Nelson SM, Coan PM, Burton, GJ, Lindsay RS. Placental structure in type 1 diabetes: relation to fetal insulin, leptin and IGF-I. Diabetes. 2009; 58 (11): 2634-2641. doi: 10.2337/db09-0739.
16. Higgins M, Felle P, Mooney EE, Bannigan J, McAuliffe FM. Stereology of the placenta in type 1 and 2 diabetes. Placenta. 2011; 32(8): 564-569. doi: 10.1016/j.placenta.2011.04.015.
17. Chernyavsky IL, Jensen OE, Leach L. A mathematical model of intervillous blood flow in the human placentone. Placenta. 2010;31(1):44-52. doi: 10.1016/j.placenta.2009.11.003.
18. Chernyavsky IL, Leach L, Dryden IL, Jensen OE.Transport in the placenta: homogenizing haemodynamics in a disordered medium. Philos Trans A Math Phys Eng Sci. 2011;369(1954):4162-82. doi:10.1098/rsta.2011.0170.
19. Zhou Q, Schirrmann K, Doman E, Chen Q, Singh N, Selvaganapathy PR, Bernabeu MO, Jensen OE, Juel A, Chernyavsky IL, Krüger T. Red blood cell dynamics in extravascular biological tissues modelled as canonical disordered porous media.Interface Focus. 2022; 12(6):20220037. doi: 10.1098/rsfs.2022.0037.
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21. Chen DB, Zheng J. Regulation of placental angiogenesis. Microcirculation.2014; 21:15-25. doi: 10.1111/micc.12093.
22. Loegl J, Nussbaumer E, Hiden U, Majali-Martinez A, Ghaffari-Tabrizi-Wizy N, Cvitic S, Lang I, Desoye G, Huppertz B. Pigment epithelium-derived factor (PEDF): a novel trophoblast-derived factor limiting feto-placental angiogenesis in late pregnancy. Angiogenesis. 2016; 19:373–388. doi: 10.1007/s10456-016-9513-x.
23. Loegl J, Nussbaumer E, Cvitic S, Huppertz B, Desoye G, Hidden U. GDM alters paracrine regulation of feto-placental angiogenesis via trophoblast. Lab Invest. 2017; 97: 409-418. doi: 10.1038/labinvest.2016.149.
24. Jirkovská M, Kubínová L, Janáček J, Moravcová M, Krejčí V, Karen P. Topological properties and spatial organization of villous capillaries in normal and diabetic placentas. J Vasc Res. 2002; 39:268-278. doi: 10.1159/000063692.
25. Jirkovská M, Kučera T, Kaláb J, Jadrníček M, Niedobová V, Janáček J, Kubínová L, Moravcová M, Žižka Z, Krejčí V. The branching pattern of villous capillaries and structural changes of placental terminal villi in type 1 diabetes mellitus. Placenta. 2012; 33:343-35. doi: 10.1016/j.placenta.2012.01.014.
26. Babawale MO, Lovat S, Mayhew TM, Lammiman MJ, James DK, Leach L. Effects of gestational diabetes on junctional adhesion molecules in human term placental vasculature. Diabetologia. 2000;43(9):1185-1196. doi: 10.1007/s001250051511.
27. Leach L, Gray C, Staton S, Babawale MO, Gruchy A, Foster C, Mayhew TM, James DK. Vascular endothelial cadherin and β-catenin in human fetoplacental vessels of pregnancies complicated by Type 1 diabetes: associations with angiogenesis and perturbed barrier function. Diabetologia. 2004;47(4):695-709. doi: 10.1007/s00125-004-1341-7.
28. Emmrich, P., Fuchs, U., Heinke, P., Jutzi, E. & Gődel, E. Epithelial and capillary basal laminae of the placenta in maternal diabetes mellitus. Lab Invest.1976; 35(1): 87-92. PMID: 940324.
29. Jirkovská, M. Comparison of the thickness of the capillary basement membrane of the human placenta under normal conditions and in type I diabetes. Funct Dev Morphol.1991;1(3): 9-16. PMID: 1802047.
30. Jirkovská M, Kučera T, Dvořáková V, Jadrníček M, Moravcová, M, Žižka Z, Krejčí V. Impact of maternal diabetes type 1 on proliferative potential, differentiation, and apoptotic activity in villous capillaries of term placenta. Placenta.2016; 40:1-7. doi. Org/10.1016/j. placenta.2016.02.003.
31. Zhang, E.G., Burton G.J., Smith S.K. & Charnock-Jones, D.SPlacental vessel adaptation during gestation and to high altitude: changes in diameter and perivascular cell coverage. Placenta. 2002;23(10):751-762. doi: 10.1016/s0143-4004(02)90856-8.
32. Kučera T, Vyletěl I, Moravcová M, Krejčí V, Žižka Z, Jirkovská M. Pericyte coverage of fetoplacental vessels in pregnancies complicated by type 1 diabetes mellitus. Placenta. 2010; 31: 1120-1122. doi: 10.1016/j.placenta.2010.09.014.
33. G. Unek, A. Ozmen, I. Mendilcioglu, M. Simek, E.T. Korgun. Immunohistochemical distribution of cell cycle proteins p27, p57, cyclin D3, PCNA and Ki67in normal and diabetic human placentas. J Mol Hist. 2014; 45:21-34. doi: 10.1007/s10735-013-9534-3.
34. Kaltenbach F.J., O. Fettig, M.L. Krieger. Autoradiographische Untersuchungen über das Proliferationsverhalten der menschlichen Plazenta unter normalen und pathologischen Bedingungen. Arch Gynäk. 1974; 216:369-386. In German. doi: 10.1007/BF01347141.
35. J. Hustin, J.M. Foidart, R. Lambotte. Cellular proliferation in villi of normal and pathological pregnancies, Gynecol Obstet Invest. 1984;17: 1-9. doi: 10.1159/000299115.
36. Jirkovská M, Kučera T, Dvořáková V, Jadrníček M, Moravcová, M, Žižka Z, Krejčí V. Impact of maternal diabetes type 1 on proliferative potential, differentiation, and apoptotic activity in villous capillaries of term placenta. Placenta.2016; 40:1-7. doi. org/10.1016/j. placenta.2016.02.003.
37. Jirkovská M. Structural characteristic of growth, maturation, and spatial arrangement of capillary bed in normal and pathologic placenta. doi:http:// dx.doi.org/10.5772/intechopen.1001353.
38. Jirkovská M, Korabečná M, Laššáková S. Telomeres, and telomerase activity in the human placenta. In: Morrish TA (ed.), Telomerase and non-Telomerase Mechanisms of Telomere Maintenance. IntechOpen London 2020. doi:org/10.5772/intechopen.
39. Edelson PK, Sawyer MR, Gray KJ, Cantonwine DE, McElrath TF, Phillippe M. Increase in short telomeres during the third trimester in human placenta. PLoS One. 2022; 17: e0271415. doi: 10.1371/journal.pone.0271415.
40. Lai T-P, Simpson M, Patel K, Verhulst S, Noh J, Roche N, Heller D, Guirguis G, Shay JW, Herbig U, Aviv A. Telomeres, and replicative cellular aging of the human placenta and chorioamniotic membranes. Sci Rep. 2021; 11:5115. doi: 10.1038/s41598-021-84728-2.
41. Alba Greco M, Kamat BR, Demopoulos RI. Placental protein distribution in maternal diabetes mellitus. Pediatr Pathol. 1989; 9:679-690.
42. Jirkovská M, Šmídová J, Bendl J,Krofta L. Quantitative histochemische Studie über die Aktivität der Na, K-ATPase in der diabetischen Plazenta. Abstract. Diabetes und Stoffwechsel. 1995.4:13.
43. Jirkovská M, Šmídová J, Palouš D. Quantitative histochemical study on alkaline phosphatase activity in normal and diabetic placenta. Abstract. Histochem J.1997; 29:717.
44. Hirschmugl B, Crozier S, Matthews N, Kitzinger E, Klymiuk I, Inskip HM, Harvey NC, Cooper C, Sibley CP, Glazier J, Wadsack C, Godfrey KM, Desoye G, Lewis RM. Relation of placental alkaline phosphatase expression in human term placenta with maternal and offspring fat mass. Int J Obes (Lond). 2018;42(6):1202-1210. doi: 10.1038/s41366-018-0136-8.
45. Hastie R, Lappas M. The effect of pre-existing maternal obesity and diabetes on placental mitochondrial content and electron transport chain activity. Placenta.2014; 35: 673-683. doi.org/10.1016/j.placenta.2014.06.368.
2. Benirschke K, Burton GJ, Baergen RN. Pathology of the Human Placenta. 6th ed. Berlin Heidelberg: Springer-Verlag; 2012. doi: 10.1007/978-3-642-23941-0.
3. Honda M, Toyoda C, Nakabayashi M, Omori Y. Quantitative investigations of placental terminal villi in maternal diabetes mellitus by scanning and transmission electron microscopy. Tohoku J Exp Med. 1992;167(4): 247-257. doi: 10.1620/tjem.167.247.
4. Björk O, Persson B. Villous structure in different parts of the cotyledon in placentas of insulin-dependent diabetic women. A morphometric study. Acta Obstet Gynecol Scand. 1984; 63(1):37-43. doi: 10.3109/00016348409156271.
5. Teasdale F. Histomorphometry of the placenta of the diabetic women: class A diabetes mellitus. Placenta. 1981; 2(3): 241-252. doi: 10.1016/s0143-4004(81)80007-0.
6. Teasdale F. Histomorphometry of the human placenta in class B diabetes mellitus. Placenta. 1983; 4(1):1-12. doi: 10.1016/s0143-4004(83)80012-5.
7. Teasdale F. Histomorphometry of the human placenta in class C diabetes mellitus. Placenta.1985; 6(1): 69-82. doi: 10.1016/s0143-4004(85)80034-5.
8. Teasdale F, Jean-Jacques G. Morphometry of the microvillous membrane of the human placenta in maternal diabetes mellitus. Placenta. 1986;7 :81-88. doi: 10.1016/s0143-4004(86)80020-0
9. Mayhew TM, Sørensen FB, Klebe JG, Jackson MR. Growth and maturation of villi in placentae from well-controlled diabetic women. Placenta. 1994; 15:57-65. doi: 10.1016/s0143-4004(05)80236-x.
10. Mayhew TM. Paterns of villous and intervillous space growth in human placentas from normal and abnormal pregnancies. Eur J Obstet Gynecol Reprod Biol. 1996;68(1-2):75-82. doi: 10.1016/0301-2115(96)02486-4.
11. Mayhew TM, Sisley I. Quantitative studies on the villi, trophoblast and intervillous pores of placentae from women with well-controlled diabetes mellitus. Placenta. 1998; 19: 371-377. doi: 10.1016/s0143-4004(98)90076-5.
12. Mayhew TM, Jairam IC. Stereological comparison of 3D spatial relationships involving villi and intervillous pores in human placentas from control and diabetic pregnancies. J Anat. 2000; 197:263-274. doi: 10.1046/j.1469-7580.2000.19720263.x.
13. Mayhew TM, Sørensen FB, Klebe JG, Jackson MR. The effects of mode of delivery and sex of newborn on placental morphology in control and diabetic pregnancies. J Anat. 1993;183: 545-552. PMID: 8300431
14. Jauniaux E, Burton GJ. Villous histomorphometry and placental bed biopsy in diabetic pregnancies. Placenta. 2006; 27 (4-5): 468-474. doi: 10.1016/j.placenta.2005.04.010.
15. Nelson SM, Coan PM, Burton, GJ, Lindsay RS. Placental structure in type 1 diabetes: relation to fetal insulin, leptin and IGF-I. Diabetes. 2009; 58 (11): 2634-2641. doi: 10.2337/db09-0739.
16. Higgins M, Felle P, Mooney EE, Bannigan J, McAuliffe FM. Stereology of the placenta in type 1 and 2 diabetes. Placenta. 2011; 32(8): 564-569. doi: 10.1016/j.placenta.2011.04.015.
17. Chernyavsky IL, Jensen OE, Leach L. A mathematical model of intervillous blood flow in the human placentone. Placenta. 2010;31(1):44-52. doi: 10.1016/j.placenta.2009.11.003.
18. Chernyavsky IL, Leach L, Dryden IL, Jensen OE.Transport in the placenta: homogenizing haemodynamics in a disordered medium. Philos Trans A Math Phys Eng Sci. 2011;369(1954):4162-82. doi:10.1098/rsta.2011.0170.
19. Zhou Q, Schirrmann K, Doman E, Chen Q, Singh N, Selvaganapathy PR, Bernabeu MO, Jensen OE, Juel A, Chernyavsky IL, Krüger T. Red blood cell dynamics in extravascular biological tissues modelled as canonical disordered porous media.Interface Focus. 2022; 12(6):20220037. doi: 10.1098/rsfs.2022.0037.
20. Burton, G.J. & Jauniaux, E. Sonographic, stereological and Doppler flow velocimetric assessments of placental maturity. Br J Obstet Gynaecol. 1995;102(10):818-825. doi: 10.1111/j.1471-0528.1995.tb10849.x.
21. Chen DB, Zheng J. Regulation of placental angiogenesis. Microcirculation.2014; 21:15-25. doi: 10.1111/micc.12093.
22. Loegl J, Nussbaumer E, Hiden U, Majali-Martinez A, Ghaffari-Tabrizi-Wizy N, Cvitic S, Lang I, Desoye G, Huppertz B. Pigment epithelium-derived factor (PEDF): a novel trophoblast-derived factor limiting feto-placental angiogenesis in late pregnancy. Angiogenesis. 2016; 19:373–388. doi: 10.1007/s10456-016-9513-x.
23. Loegl J, Nussbaumer E, Cvitic S, Huppertz B, Desoye G, Hidden U. GDM alters paracrine regulation of feto-placental angiogenesis via trophoblast. Lab Invest. 2017; 97: 409-418. doi: 10.1038/labinvest.2016.149.
24. Jirkovská M, Kubínová L, Janáček J, Moravcová M, Krejčí V, Karen P. Topological properties and spatial organization of villous capillaries in normal and diabetic placentas. J Vasc Res. 2002; 39:268-278. doi: 10.1159/000063692.
25. Jirkovská M, Kučera T, Kaláb J, Jadrníček M, Niedobová V, Janáček J, Kubínová L, Moravcová M, Žižka Z, Krejčí V. The branching pattern of villous capillaries and structural changes of placental terminal villi in type 1 diabetes mellitus. Placenta. 2012; 33:343-35. doi: 10.1016/j.placenta.2012.01.014.
26. Babawale MO, Lovat S, Mayhew TM, Lammiman MJ, James DK, Leach L. Effects of gestational diabetes on junctional adhesion molecules in human term placental vasculature. Diabetologia. 2000;43(9):1185-1196. doi: 10.1007/s001250051511.
27. Leach L, Gray C, Staton S, Babawale MO, Gruchy A, Foster C, Mayhew TM, James DK. Vascular endothelial cadherin and β-catenin in human fetoplacental vessels of pregnancies complicated by Type 1 diabetes: associations with angiogenesis and perturbed barrier function. Diabetologia. 2004;47(4):695-709. doi: 10.1007/s00125-004-1341-7.
28. Emmrich, P., Fuchs, U., Heinke, P., Jutzi, E. & Gődel, E. Epithelial and capillary basal laminae of the placenta in maternal diabetes mellitus. Lab Invest.1976; 35(1): 87-92. PMID: 940324.
29. Jirkovská, M. Comparison of the thickness of the capillary basement membrane of the human placenta under normal conditions and in type I diabetes. Funct Dev Morphol.1991;1(3): 9-16. PMID: 1802047.
30. Jirkovská M, Kučera T, Dvořáková V, Jadrníček M, Moravcová, M, Žižka Z, Krejčí V. Impact of maternal diabetes type 1 on proliferative potential, differentiation, and apoptotic activity in villous capillaries of term placenta. Placenta.2016; 40:1-7. doi. Org/10.1016/j. placenta.2016.02.003.
31. Zhang, E.G., Burton G.J., Smith S.K. & Charnock-Jones, D.SPlacental vessel adaptation during gestation and to high altitude: changes in diameter and perivascular cell coverage. Placenta. 2002;23(10):751-762. doi: 10.1016/s0143-4004(02)90856-8.
32. Kučera T, Vyletěl I, Moravcová M, Krejčí V, Žižka Z, Jirkovská M. Pericyte coverage of fetoplacental vessels in pregnancies complicated by type 1 diabetes mellitus. Placenta. 2010; 31: 1120-1122. doi: 10.1016/j.placenta.2010.09.014.
33. G. Unek, A. Ozmen, I. Mendilcioglu, M. Simek, E.T. Korgun. Immunohistochemical distribution of cell cycle proteins p27, p57, cyclin D3, PCNA and Ki67in normal and diabetic human placentas. J Mol Hist. 2014; 45:21-34. doi: 10.1007/s10735-013-9534-3.
34. Kaltenbach F.J., O. Fettig, M.L. Krieger. Autoradiographische Untersuchungen über das Proliferationsverhalten der menschlichen Plazenta unter normalen und pathologischen Bedingungen. Arch Gynäk. 1974; 216:369-386. In German. doi: 10.1007/BF01347141.
35. J. Hustin, J.M. Foidart, R. Lambotte. Cellular proliferation in villi of normal and pathological pregnancies, Gynecol Obstet Invest. 1984;17: 1-9. doi: 10.1159/000299115.
36. Jirkovská M, Kučera T, Dvořáková V, Jadrníček M, Moravcová, M, Žižka Z, Krejčí V. Impact of maternal diabetes type 1 on proliferative potential, differentiation, and apoptotic activity in villous capillaries of term placenta. Placenta.2016; 40:1-7. doi. org/10.1016/j. placenta.2016.02.003.
37. Jirkovská M. Structural characteristic of growth, maturation, and spatial arrangement of capillary bed in normal and pathologic placenta. doi:http:// dx.doi.org/10.5772/intechopen.1001353.
38. Jirkovská M, Korabečná M, Laššáková S. Telomeres, and telomerase activity in the human placenta. In: Morrish TA (ed.), Telomerase and non-Telomerase Mechanisms of Telomere Maintenance. IntechOpen London 2020. doi:org/10.5772/intechopen.
39. Edelson PK, Sawyer MR, Gray KJ, Cantonwine DE, McElrath TF, Phillippe M. Increase in short telomeres during the third trimester in human placenta. PLoS One. 2022; 17: e0271415. doi: 10.1371/journal.pone.0271415.
40. Lai T-P, Simpson M, Patel K, Verhulst S, Noh J, Roche N, Heller D, Guirguis G, Shay JW, Herbig U, Aviv A. Telomeres, and replicative cellular aging of the human placenta and chorioamniotic membranes. Sci Rep. 2021; 11:5115. doi: 10.1038/s41598-021-84728-2.
41. Alba Greco M, Kamat BR, Demopoulos RI. Placental protein distribution in maternal diabetes mellitus. Pediatr Pathol. 1989; 9:679-690.
42. Jirkovská M, Šmídová J, Bendl J,Krofta L. Quantitative histochemische Studie über die Aktivität der Na, K-ATPase in der diabetischen Plazenta. Abstract. Diabetes und Stoffwechsel. 1995.4:13.
43. Jirkovská M, Šmídová J, Palouš D. Quantitative histochemical study on alkaline phosphatase activity in normal and diabetic placenta. Abstract. Histochem J.1997; 29:717.
44. Hirschmugl B, Crozier S, Matthews N, Kitzinger E, Klymiuk I, Inskip HM, Harvey NC, Cooper C, Sibley CP, Glazier J, Wadsack C, Godfrey KM, Desoye G, Lewis RM. Relation of placental alkaline phosphatase expression in human term placenta with maternal and offspring fat mass. Int J Obes (Lond). 2018;42(6):1202-1210. doi: 10.1038/s41366-018-0136-8.
45. Hastie R, Lappas M. The effect of pre-existing maternal obesity and diabetes on placental mitochondrial content and electron transport chain activity. Placenta.2014; 35: 673-683. doi.org/10.1016/j.placenta.2014.06.368.