Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-23T06:45:59.117Z Has data issue: false hasContentIssue false

Advances in imaging feto-placental vasculature: new tools to elucidate the early life origins of health and disease

Published online by Cambridge University Press:  04 August 2020

Yutthapong Tongpob
Affiliation:
School of Human Sciences, The University of Western Australia, Perth, WA6009, Australia Faculty of Medical Science, Naresuan University, Phitsanulok65000, Thailand
Caitlin Wyrwoll*
Affiliation:
School of Human Sciences, The University of Western Australia, Perth, WA6009, Australia
*
Address for correspondence: Caitlin Wyrwoll, School of Human Sciences, The University of Western Australia, Perth, WA6009, Australia. Email: [email protected]

Abstract

Optimal placental function is critical for fetal development, and therefore a crucial consideration for understanding the developmental origins of health and disease (DOHaD). The structure of the fetal side of the placental vasculature is an important determinant of fetal growth and cardiovascular development. There are several imaging modalities for assessing feto-placental structure including stereology, electron microscopy, confocal microscopy, micro-computed tomography, light-sheet microscopy, ultrasonography and magnetic resonance imaging. In this review, we present current methodologies for imaging feto-placental vasculature morphology ex vivo and in vivo in human and experimental models, their advantages and limitations and how these provide insight into placental function and fetal outcomes. These imaging approaches add important perspective to our understanding of placental biology and have potential to be new tools to elucidate a deeper understanding of DOHaD.

Type
Review
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Gardosi, J, Madurasinghe, V, Williams, M, Malik, A, Francis, A. Maternal and fetal risk factors for stillbirth: population based study. BMJ. 2013; 346, f108.CrossRefGoogle ScholarPubMed
Barker, D, Osmond, C, Grant, S, et al. Maternal cotyledons at birth predict blood pressure in childhood. Placenta. 2013; 34(8), 672675.CrossRefGoogle ScholarPubMed
Thornburg, KL, O’Tierney, PF, Louey, S. Review: the placenta is a programming agent for cardiovascular disease. Placenta. 2010; 31, S54S59.CrossRefGoogle ScholarPubMed
Barker, DJ, Thornburg, KL, Osmond, C, Kajantie, E, Eriksson, JG. The surface area of the placenta and hypertension in the offspring in later life. Int J Dev Biol. 2010; 54(2–3), 525530.CrossRefGoogle ScholarPubMed
Burton, GJ, Fowden, AL, Thornburg, KL. Placental origins of chronic disease. Physiol Rev. 2016; 96(4), 15091565.CrossRefGoogle ScholarPubMed
Junaid, TO, Bradley, RS, Lewis, RM, Aplin, JD, Johnstone, ED. Whole organ vascular casting and microCT examination of the human placental vascular tree reveals novel alterations associated with pregnancy disease. Sci Rep. 2017; 7(1), 4144.CrossRefGoogle ScholarPubMed
Junaid, TO, Brownbill, P, Chalmers, N, Johnstone, ED, Aplin, JD. Fetoplacental vascular alterations associated with fetal growth restriction. Placenta. 2014; 35(10), 808815.CrossRefGoogle ScholarPubMed
Langheinrich, AC, Vorman, S, Seidenstucker, J, et al. Quantitative 3D micro-CT imaging of the human feto-placental vasculature in intrauterine growth restriction. Placenta. 2008; 29(11), 937941.CrossRefGoogle ScholarPubMed
Fisher, AB, Chien, S, Barakat, AI, Nerem, RM. Endothelial cellular response to altered shear stress. Am J Physiol Lung Cell Mol Physiol. 2001; 281(3), L529L533.CrossRefGoogle ScholarPubMed
Davies, PF. Flow-mediated endothelial mechanotransduction. Physiol Rev. 1995; 75(3), 519560.CrossRefGoogle ScholarPubMed
Langille, BL. Arterial remodeling: relation to hemodynamics. Can J Physiol Pharmacol. 1996; 74(7), 834841.CrossRefGoogle ScholarPubMed
Rudolph, AM. Hepatic and ductus venosus blood flows during fetal life. Hepatology. 1983; 3(2), 254258.CrossRefGoogle ScholarPubMed
Courchaine, K, Rykiel, G, Rugonyi, S. Influence of blood flow on cardiac development. Prog Biophys Mol Biol. 2018; 137, 95110.CrossRefGoogle ScholarPubMed
Perez-Garcia, V, Fineberg, E, Wilson, R, et al. Placentation defects are highly prevalent in embryonic lethal mouse mutants. Nature. 2018; 555(7697), 463468.CrossRefGoogle ScholarPubMed
Maslen, CL. Recent advances in placenta-heart interactions. Front Physiol. 2018; 9, 735.CrossRefGoogle ScholarPubMed
Crispi, F, Miranda, J, Gratacos, E. Long-term cardiovascular consequences of fetal growth restriction: biology, clinical implications, and opportunities for prevention of adult disease. Am J Obstet Gynecol. 2018; 218(2S), S869S879.CrossRefGoogle ScholarPubMed
Camm, EJ, Botting, KJ, Sferruzzi-Perri, AN. Near to One’s Heart: The Intimate Relationship Between the Placenta and Fetal Heart. Front Physiol. 2018; 9, 629.CrossRefGoogle ScholarPubMed
Wyrwoll, CS, Noble, J, Thomson, A, et al. Pravastatin ameliorates placental vascular defects, fetal growth, and cardiac function in a model of glucocorticoid excess. Proc Natl Acad Sci U S A. 2016; 113(22), 62656270.CrossRefGoogle Scholar
Shen, H, Cavallero, S, Estrada, KD, et al. Extracardiac control of embryonic cardiomyocyte proliferation and ventricular wall expansion. Cardiovasc Res. 2015; 105(3), 271278.CrossRefGoogle ScholarPubMed
Linask, KK. The heart-placenta axis in the first month of pregnancy: induction and prevention of cardiovascular birth defects. J Pregnancy. 2013; 2013, 320413.CrossRefGoogle ScholarPubMed
Gessert, S, Kuhl, M. The multiple phases and faces of Wnt signaling during cardiac differentiation and development. Circ Res. 2010; 107(2), 186199.CrossRefGoogle ScholarPubMed
Shaut, CA, Keene, DR, Sorensen, LK, Li, DY, Stadler, HS. HOXA13 Is essential for placental vascular patterning and labyrinth endothelial specification. PLoS Genet. 2008; 4(5), e1000073.CrossRefGoogle ScholarPubMed
Hemberger, M, Cross, JC. Genes governing placental development. Trends Endocrinol Metab. 2001; 12(4), 162168.CrossRefGoogle ScholarPubMed
Adams, RH, Porras, A, Alonso, G, et al. Essential role of p38alpha MAP kinase in placental but not embryonic cardiovascular development. Mol Cell. 2000; 6(1), 109116.CrossRefGoogle Scholar
Barak, Y, Nelson, MC, Ong, ES, et al. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell. 1999; 4(4), 585595.CrossRefGoogle ScholarPubMed
Kiserud, T, Ebbing, C, Kessler, J, Rasmussen, S. Fetal cardiac output, distribution to the placenta and impact of placental compromise. Ultrasound Obstet Gynecol. 2006; 28(2), 126136.CrossRefGoogle ScholarPubMed
Kaufmann, P, Bruns, U, Leiser, R, Luckhardt, M, Winterhager, E. The fetal vascularisation of term human placental villi. II. Intermediate and terminal villi. Anat Embryol (Berl). 1985; 173(2), 203214.CrossRefGoogle ScholarPubMed
Kaufmann, P, Sen, DK, Schweikhart, G. Classification of human placental villi. I. Histology. Cell Tissue Res. 1979; 200(3), 409423.CrossRefGoogle ScholarPubMed
Sen, DK, Kaufmann, P, Schweikhart, G. Classification of human placental villi. II. Morphometry. Cell Tissue Res. 1979; 200(3), 425434.CrossRefGoogle ScholarPubMed
Burton, GJ, Fowden, AL. The placenta: a multifaceted, transient organ. Philos Trans R Soc Lond B Biol Sci. 2015; 370(1663), 20140066.CrossRefGoogle ScholarPubMed
Wang, Y, Zhao, S. In Vascular Biology of the Placenta, 2010. Morgan & Claypool Life Sciences, San Rafael (CA).CrossRefGoogle ScholarPubMed
Wooding, P, Burton, G. Comparative placentation: structures, functions and evolution. 2008; pp. 1309. Springer, Verlag Berlin Heidelberg, Germany.CrossRefGoogle Scholar
Furukawa, S, Kuroda, Y, Sugiyama, A. A comparison of the histological structure of the placenta in experimental animals. J Toxicol Pathol. 2014; 27(1), 1118.CrossRefGoogle ScholarPubMed
Leiser, R, Kaufmann, P. Placental structure: in a comparative aspect. Exp Clin Endocrinol. 1994; 102(3), 122134.CrossRefGoogle Scholar
Vercruysse, L, Caluwaerts, S, Luyten, C, Pijnenborg, R. Interstitial trophoblast invasion in the decidua and mesometrial triangle during the last third of pregnancy in the rat. Placenta. 2006; 27(1), 2233.CrossRefGoogle ScholarPubMed
Georgiades, P, Ferguson-Smith, AC, Burton, GJ. Comparative developmental anatomy of the murine and human definitive placentae. Placenta. 2002; 23(1), 319.CrossRefGoogle ScholarPubMed
Matt, DW, Macdonald, GJ. Placental steroid production by the basal and labyrinth zones during the latter third of gestation in the rat. Biol Reprod. 1985; 32(4), 969977.CrossRefGoogle ScholarPubMed
Rossant, J, Cross, JC. Placental development: lessons from mouse mutants. Nat Rev Genet. 2001; 2(7), 538548.CrossRefGoogle ScholarPubMed
Soares, MJ, Chakraborty, D, Karim Rumi, MA, Konno, T, Renaud, SJ. Rat placentation: an experimental model for investigating the hemochorial maternal-fetal interface. Placenta. 2012; 33(4), 233243.CrossRefGoogle ScholarPubMed
Adamson, SL, Lu, Y, Whiteley, KJ, et al. Interactions between trophoblast cells and the maternal and fetal circulation in the mouse placenta. Dev Biol. 2002; 250(2), 358373.CrossRefGoogle ScholarPubMed
Pijnenborg, R, Robertson, WB, Brosens, I, Dixon, G. Review article: trophoblast invasion and the establishment of haemochorial placentation in man and laboratory animals. Placenta. 1981; 2(1), 7191.CrossRefGoogle ScholarPubMed
Higgins, M, Felle, P, Mooney, EE, Bannigan, J, McAuliffe, FM. Stereology of the placenta in type 1 and type 2 diabetes. Placenta. 2011; 32(8), 564569.CrossRefGoogle ScholarPubMed
Mayhew, TM, Manwani, R, Ohadike, C, Wijesekara, J, Baker, PN. The placenta in pre-eclampsia and intrauterine growth restriction: studies on exchange surface areas, diffusion distances and villous membrane diffusive conductances. Placenta. 2007; 28(2–3), 233238.CrossRefGoogle ScholarPubMed
Mayhew, TM, Ohadike, C, Baker, PN, Crocker, IP, Mitchell, C, Ong, SS. Stereological investigation of placental morphology in pregnancies complicated by pre-eclampsia with and without intrauterine growth restriction. Placenta. 2003; 24(2–3), 219226.CrossRefGoogle ScholarPubMed
Mayhew, TM. Recent applications of the new stereology have thrown fresh light on how the human placenta grows and develops its form. J Microsc. 1997; 186(Pt 2), 153163.CrossRefGoogle ScholarPubMed
Burton, GJ, Reshetnikova, OS, Milovanov, AP, Teleshova, OV. Stereological evaluation of vascular adaptations in human placental villi to differing forms of hypoxic stress. Placenta. 1996; 17(1), 4955.CrossRefGoogle ScholarPubMed
Jackson, MR, Mayhew, TM, Boyd, PA. Quantitative description of the elaboration and maturation of villi from 10 weeks of gestation to term. Placenta. 1992; 13(4), 357370.CrossRefGoogle ScholarPubMed
Nuzzo, AM, Camm, EJ, Sferruzzi-Perri, AN, et al. Placental adaptation to early-onset hypoxic pregnancy and mitochondria-targeted antioxidant therapy in a rodent model. Am J Pathol. 2018; 188(12), 27042716.CrossRefGoogle Scholar
Higgins, JS, Vaughan, OR, Fernandez de Liger, E, Fowden, AL, Sferruzzi-Perri, AN. Placental phenotype and resource allocation to fetal growth are modified by the timing and degree of hypoxia during mouse pregnancy. J Physiol. 2016; 594(5), 13411356.CrossRefGoogle ScholarPubMed
Sferruzzi-Perri, AN, Lopez-Tello, J, Fowden, AL, Constancia, M. Maternal and fetal genomes interplay through phosphoinositol 3-kinase(PI3K)-p110alpha signaling to modify placental resource allocation. Proc Natl Acad Sci U S A. 2016; 113(40), 1125511260.CrossRefGoogle ScholarPubMed
Vaughan, OR, Sferruzzi-Perri, AN, Coan, PM, Fowden, AL. Adaptations in placental phenotype depend on route and timing of maternal dexamethasone administration in mice. Biol Reprod. 2013; 89(4), 80.CrossRefGoogle ScholarPubMed
Rennie, MY, Detmar, J, Whiteley, KJ, Jurisicova, A, Adamson, SL, Sled, JG. Expansion of the fetoplacental vasculature in late gestation is strain dependent in mice. Am J Physiol Heart Circ Physiol. 2012; 302(6), H1261H1273.CrossRefGoogle ScholarPubMed
Coan, PM, Vaughan, OR, Sekita, Y, et al. Adaptations in placental phenotype support fetal growth during undernutrition of pregnant mice. J Physiol. 2010; 588(Pt 3), 527538.CrossRefGoogle ScholarPubMed
Wyrwoll, CS, Seckl, JR, Holmes, MC. Altered placental function of 11beta-hydroxysteroid dehydrogenase 2 knockout mice. Endocrinology. 2009; 150(3), 12871293.CrossRefGoogle ScholarPubMed
Coan, PM, Angiolini, E, Sandovici, I, Burton, GJ, Constancia, M, Fowden, AL. Adaptations in placental nutrient transfer capacity to meet fetal growth demands depend on placental size in mice. J Physiol. 2008; 586(18), 45674576.CrossRefGoogle ScholarPubMed
Veras, MM, Damaceno-Rodrigues, NR, Caldini, EG, et al. Particulate urban air pollution affects the functional morphology of mouse placenta. Biol Reprod. 2008; 79(3), 578584.CrossRefGoogle ScholarPubMed
Coan, PM, Fowden, AL, Constancia, M, Ferguson-Smith, AC, Burton, GJ, Sibley, CP. Disproportional effects of Igf2 knockout on placental morphology and diffusional exchange characteristics in the mouse. J Physiol. 2008; 586(20), 50235032.CrossRefGoogle ScholarPubMed
Rutland, CS, Latunde-Dada, AO, Thorpe, A, Plant, R, Langley-Evans, S, Leach, L. Effect of gestational nutrition on vascular integrity in the murine placenta. Placenta. 2007; 28(7), 734742.CrossRefGoogle ScholarPubMed
Coan, PM, Ferguson-Smith, AC, Burton, GJ. Ultrastructural changes in the interhaemal membrane and junctional zone of the murine chorioallantoic placenta across gestation. J Anat. 2005; 207(6), 783796.CrossRefGoogle ScholarPubMed
Sibley, CP, Coan, PM, Ferguson-Smith, AC, et al. Placental-specific insulin-like growth factor 2 (Igf2) regulates the diffusional exchange characteristics of the mouse placenta. Proc Natl Acad Sci U S A. 2004; 101(21), 82048208.CrossRefGoogle ScholarPubMed
Coan, PM, Ferguson-Smith, AC, Burton, GJ. Developmental dynamics of the definitive mouse placenta assessed by stereology. Biol Reprod. 2004; 70(6), 18061813.CrossRefGoogle ScholarPubMed
Napso, T, Hung, YP, Davidge, ST, Care, AS, Sferruzzi-Perri, AN. Advanced maternal age compromises fetal growth and induces sex-specific changes in placental phenotype in rats. Sci Rep. 2019; 9(1), 16916.CrossRefGoogle ScholarPubMed
Serman, L, Zunic, I, Vrsaljko, N, et al. Structural changes in the rat placenta during the last third of gestation discovered by stereology. Bosn J Basic Med Sci. 2015; 15(1), 2125.Google ScholarPubMed
Hewitt, DP, Mark, PJ, Waddell, BJ. Glucocorticoids prevent the normal increase in placental vascular endothelial growth factor expression and placental vascularity during late pregnancy in the rat. Endocrinology. 2006; 147(12), 55685574.CrossRefGoogle ScholarPubMed
Wislocki, GB, Dempsey, EW. Electron microscopy of the placenta of the rat. Anat Rec. 1955; 123(1), 3363.CrossRefGoogle ScholarPubMed
Dempsey, EW, Wislocki, GB, Amoroso, EC. Electron microscopy of the pig’s placenta, with especial reference to the cell membranes of the endometrium and chorion. Am J Anat. 1955; 96(1), 65101.CrossRefGoogle ScholarPubMed
Wislocki, GB, Dempsey, EW. Electron microscopy of the human placenta. Anat Rec. 1955; 123(2), 133167.CrossRefGoogle ScholarPubMed
Lee, MM, Yeh, MN. Fetal circulation of the placenta: a comparative study of human and baboon placenta by scanning electron microscopy of vascular casts. Placenta. 1983; 4 Spec No, 515526.Google ScholarPubMed
Krebs, C, Winther, H, Dantzer, V, Leiser, R. Vascular interrelationships of near-term mink placenta: light microscopy combined with scanning electron microscopy of corrosion casts. Microsc Res Tech. 1997; 38(1–2), 125136.3.0.CO;2-R>CrossRefGoogle ScholarPubMed
Pfarrer, C, Winther, H, Leiser, R, Dantzer, V. The development of the endotheliochorial mink placenta: light microscopy and scanning electron microscopical morphometry of maternal vascular casts. Anat Embryol (Berl). 1999; 199(1), 6374.CrossRefGoogle ScholarPubMed
Macdonald, AA, Chavatte, P, Fowden, AL. Scanning electron microscopy of the microcotyledonary placenta of the horse (Equus caballus) in the latter half of gestation. Placenta. 2000; 21(5–6), 565574.CrossRefGoogle ScholarPubMed
Detmar, J, Rennie, MY, Whiteley, KJ, et al. Fetal growth restriction triggered by polycyclic aromatic hydrocarbons is associated with altered placental vasculature and AhR-dependent changes in cell death. Am J Physiol Endocrinol Metab. 2008; 295(2), E519530.CrossRefGoogle ScholarPubMed
Whiteley, KJ, Pfarrer, CD, Adamson, SL. Vascular corrosion casting of the uteroplacental and fetoplacental vasculature in mice. Methods Mol Med. 2006; 121, 371392.Google ScholarPubMed
Cahill, LS, Rennie, MY, Hoggarth, J, et al. Feto- and utero-placental vascular adaptations to chronic maternal hypoxia in the mouse. J Physiol. 2018; 596(15), 32853297.CrossRefGoogle ScholarPubMed
Bobinski, R, Pielesz, A, Waksmanska, W, et al. Surface structure changes of pathological placenta tissue observed using scanning electron microscopy - a pilot study. Acta Biochim Pol. 2017; 64(3), 533535.CrossRefGoogle ScholarPubMed
Baykal, C, Sargon, MF, Esinler, I, Onderoglu, S, Onderoglu, L. Placental microcirculation of intrauterine growth retarded fetuses: scanning electron microscopy of placental vascular casts. Arch Gynecol Obstet. 2004; 270(2), 99103.CrossRefGoogle ScholarPubMed
Krebs, C, Macara, LM, Leiser, R, Bowman, AW, Greer, IA, Kingdom, JC. Intrauterine growth restriction with absent end-diastolic flow velocity in the umbilical artery is associated with maldevelopment of the placental terminal villous tree. Am J Obstet Gynecol. 1996; 175(6), 15341542.CrossRefGoogle ScholarPubMed
Burton, GJ. Scanning electron microscopy of intervillous connections in the mature human placenta. J Anat. 1986; 147, 245254.Google ScholarPubMed
Burton, GJ. The fine structure of the human placental villus as revealed by scanning electron microscopy. Scanning Microsc. 1987; 1(4), 18111828.Google ScholarPubMed
Demir, R, Demir, N, Ustunel, I, Erbengi, T, Trak, I, Kaufmann, P. The fine structure of normal and ectopic (tubal) human placental villi as revealed by scanning and transmission electron microscopy. Zentralbl Pathol. 1995; 140(6), 427442.Google ScholarPubMed
Palaiologou, E, Etter, O, Goggin, P, et al. Human placental villi contain stromal macrovesicles associated with networks of stellate cells. J Anat. 2020; 236(1), 132141.CrossRefGoogle ScholarPubMed
Lee, MM, Yeh, MN. Fetal microcirculation of abnormal human placenta. I. Scanning electron microscopy of placental vascular casts from small for gestational age fetus. Am J Obstet Gynecol. 1986; 154(5), 11331139.CrossRefGoogle ScholarPubMed
Lee, MM, Yeh, MN. Fetal microcirculation of abnormal human placenta. II. Scanning electron microscopy of placental vascular casts from fetus with severe erythroblastosis fetalis. Am J Obstet Gynecol. 1986; 154(5), 11391146.CrossRefGoogle ScholarPubMed
Leiser, R, Krebs, C, Ebert, B, Dantzer, V. Placental vascular corrosion cast studies: a comparison between ruminants and humans. Microsc Res Tech. 1997; 38(1–2), 7687.3.0.CO;2-S>CrossRefGoogle ScholarPubMed
Sooranna, SR, Oteng-Ntim, E, Meah, R, Ryder, TA, Bajoria, R. Characterization of human placental explants: morphological, biochemical and physiological studies using first and third trimester placenta. Hum Reprod. 1999; 14(2), 536541.CrossRefGoogle ScholarPubMed
Cronqvist, T, Tannetta, D, Morgelin, M, et al. Syncytiotrophoblast derived extracellular vesicles transfer functional placental miRNAs to primary human endothelial cells. Sci Rep. 2017; 7(1), 4558.CrossRefGoogle ScholarPubMed
Abdel Salam, GA, Alam, OA, Ahmed, UF, Al-Sherbeny, MF. Light and electron microscopic study of placenta in pre-eclampsia: a trial to define underlying changes and its clinical impact. Tanta Medical Journal. 2015; 43(4), 134145.CrossRefGoogle Scholar
Sricharoenvej, S, Tongpob, Y, Lanlua, P, Piyawinijwong, S, Roongruangchai, J, Phoungpetchara, I. Renal microvascular changes in streptozotocin-induced, long-termed diabetic rat. J Med Assoc Thai. 2007; 90(12), 26772682.Google ScholarPubMed
Bamroongwong, S, Somana, R, Rojananeungnit, S, Chunhabundit, P, Rattanachaikunsopon, P. Scanning electron microscopic study of the splenic vascular casts in common tree shrew (Tupaia glis). Anat Embryol (Berl). 1991; 184(3), 301304.CrossRefGoogle Scholar
Liu, YC, Chiang, AS. High-resolution confocal imaging and three-dimensional rendering. Methods. 2003; 30(1), 8693.CrossRefGoogle ScholarPubMed
Lisman, BA, van den Hoff, MJ, Boer, K, Bleker, OP, van Groningen, K, Exalto, N. The architecture of first trimester chorionic villous vascularization: a confocal laser scanning microscopical study. Hum Reprod. 2007; 22(8), 22542260.CrossRefGoogle ScholarPubMed
Merz, G, Schwenk, V, Shah, RG, Necaise, P, Salafia, CM. Clarification and 3-D visualization of immunolabeled human placenta villi. Placenta. 2017; 53, 3639.CrossRefGoogle ScholarPubMed
Plitman Mayo, R, Abbas, Y, Charnock-Jones, DS, Burton, GJ, Marom, G. Three-dimensional morphological analysis of placental terminal villi. Interface Focus. 2019; 9(5), 20190037.CrossRefGoogle ScholarPubMed
Perazzolo, S, Lewis, RM, Sengers, BG. Modelling the effect of intervillous flow on solute transfer based on 3D imaging of the human placental microstructure. Placenta. 2017; 60, 2127.CrossRefGoogle ScholarPubMed
Jirkovska, M, Janacek, J, Kalab, J, Kubinova, L. Three-dimensional arrangement of the capillary bed and its relationship to microrheology in the terminal villi of normal term placenta. Placenta. 2008; 29(10), 892897.CrossRefGoogle ScholarPubMed
Plitman Mayo, R, Charnock-Jones, DS, Burton, GJ, Oyen, ML. Three-dimensional modeling of human placental terminal villi. Placenta. 2016; 43, 5460.CrossRefGoogle ScholarPubMed
Jirkovska, M, Kucera, T, Kalab, J, et al. The branching pattern of villous capillaries and structural changes of placental terminal villi in type 1 diabetes mellitus. Placenta. 2012; 33(5), 343351.CrossRefGoogle ScholarPubMed
Sargent, JA, Roberts, V, Gaffney, JE, Frias, AE. Clarification and confocal imaging of the nonhuman primate placental micro-anatomy. Biotechniques. 2019; 66(2), 7984.CrossRefGoogle ScholarPubMed
De Clercq, K, Persoons, E, Napso, T, et al. High-resolution contrast-enhanced microCT reveals the true three-dimensional morphology of the murine placenta. Proc Natl Acad Sci U S A. 2019; 116(28), 1392713936.CrossRefGoogle ScholarPubMed
Rennie, MY, Cahill, LS, Adamson, SL, Sled, JG. Arterio-venous fetoplacental vascular geometry and hemodynamics in the mouse placenta. Placenta. 2017; 58, 4651.CrossRefGoogle ScholarPubMed
Rennie, MY, Rahman, A, Whiteley, KJ, Sled, JG, Adamson, SL. Site-specific increases in utero- and fetoplacental arterial vascular resistance in eNOS-deficient mice due to impaired arterial enlargement. Biol Reprod. 2015; 92(2), 48.CrossRefGoogle ScholarPubMed
Rennie, MY, Detmar, J, Whiteley, KJ, et al. Vessel tortuousity and reduced vascularization in the fetoplacental arterial tree after maternal exposure to polycyclic aromatic hydrocarbons. Am J Physiol Heart Circ Physiol. 2011; 300(2), H675H684.CrossRefGoogle ScholarPubMed
Mohammadi, H, Papp, E, Cahill, L, et al. HIV antiretroviral exposure in pregnancy induces detrimental placenta vascular changes that are rescued by progesterone supplementation. Sci Rep. 2018; 8(1), 6552.CrossRefGoogle ScholarPubMed
Chi, L, Ahmed, A, Roy, AR, et al. G9a controls placental vascular maturation by activating the Notch Pathway. Development. 2017; 144(11), 19761987.CrossRefGoogle ScholarPubMed
Yang, J, Yu, LX, Rennie, MY, Sled, JG, Henkelman, RM. Comparative structural and hemodynamic analysis of vascular trees. Am J Physiol Heart Circ Physiol. 2010; 298(4), H1249H1259.CrossRefGoogle ScholarPubMed
Conroy, AL, Silver, KL, Zhong, K, et al. Complement activation and the resulting placental vascular insufficiency drives fetal growth restriction associated with placental malaria. Cell Host Microbe. 2013; 13(2), 215226.CrossRefGoogle ScholarPubMed
Bappoo, N, Kelsey, LJ, Parker, L, et al. Viscosity and haemodynamics in a late gestation rat feto-placental arterial network. Biomech Model Mechanobiol. 2017; 16(4), 13611372.CrossRefGoogle Scholar
Tongpob, Y, Xia, S, Wyrwoll, C, Mehnert, A. Quantitative characterization of rodent feto-placental vasculature morphology in micro-computed tomography images. Comput Methods Programs Biomed. 2019; 179, 104984.CrossRefGoogle ScholarPubMed
Pratt, R, Hutchinson, JC, Melbourne, A, et al. Imaging the human placental microcirculation with micro-focus computed tomography: optimisation of tissue preparation and image acquisition. Placenta. 2017; 60, 3639.CrossRefGoogle ScholarPubMed
Aughwane, R, Schaaf, C, Hutchinson, JC, et al. Micro-CT and histological investigation of the spatial pattern of feto-placental vascular density. Placenta. 2019; 88, 3643.CrossRefGoogle ScholarPubMed
Langheinrich, AC, Wienhard, J, Vormann, S, Hau, B, Bohle, RM, Zygmunt, M. Analysis of the fetal placental vascular tree by X-ray micro-computed tomography. Placenta. 2004; 25(1), 95100.CrossRefGoogle ScholarPubMed
Vasquez, SX, Gao, F, Su, F, et al. Optimization of microCT imaging and blood vessel diameter quantitation of preclinical specimen vasculature with radiopaque polymer injection medium. PLoS One. 2011; 6(4), e19099.CrossRefGoogle ScholarPubMed
Ghanavati, S, Yu, LX, Lerch, JP, Sled, JG. A perfusion procedure for imaging of the mouse cerebral vasculature by X-ray micro-CT. J Neurosci Methods. 2014; 221, 7077.CrossRefGoogle ScholarPubMed
Chugh, BP, Lerch, JP, Yu, LX, et al. Measurement of cerebral blood volume in mouse brain regions using micro-computed tomography. Neuroimage. 2009; 47(4), 13121318.CrossRefGoogle ScholarPubMed
Jorgensen, SM, Demirkaya, O, Ritman, EL. Three-dimensional imaging of vasculature and parenchyma in intact rodent organs with X-ray micro-CT. Am J Physiol. 1998; 275(3), H1103H1114.Google ScholarPubMed
Kampschulte, M, Schneider, CR, Litzlbauer, HD, et al. Quantitative 3D micro-CT imaging of human lung tissue. Rofo. 2013; 185(9), 869876.Google ScholarPubMed
Op Den Buijs, J, Bajzer, Z, Ritman, EL. Branching morphology of the rat hepatic portal vein tree: a micro-CT study. Ann Biomed Eng. 2006; 34(9), 14201428.CrossRefGoogle ScholarPubMed
Ananda, S, Marsden, V, Vekemans, K, et al. The visualization of hepatic vasculature by X-ray micro-computed tomography. J Electron Microsc (Tokyo). 2006; 55(3), 151155.CrossRefGoogle ScholarPubMed
Kline, TL, Zamir, M, Ritman, EL. Relating function to branching geometry: a micro-CT study of the hepatic artery, portal vein, and biliary tree. Cells Tissues Organs. 2011; 194(5), 431442.CrossRefGoogle ScholarPubMed
Nordsletten, DA, Blackett, S, Bentley, MD, Ritman, EL, Smith, NP. Structural morphology of renal vasculature. Am J Physiol Heart Circ Physiol. 2006; 291(1), H296H309.CrossRefGoogle ScholarPubMed
Bentley, MD, Ortiz, MC, Ritman, EL, Romero, JC. The use of microcomputed tomography to study microvasculature in small rodents. Am J Physiol Regul Integr Comp Physiol. 2002; 282(5), R12671279.CrossRefGoogle ScholarPubMed
Garcia-Sanz, A, Rodriguez-Barbero, A, Bentley, MD, Ritman, EL, Romero, JC. Three-dimensional microcomputed tomography of renal vasculature in rats. Hypertension. 1998; 31(1 Pt 2), 440444.CrossRefGoogle ScholarPubMed
Marxen, M, Thornton, MM, Chiarot, CB, et al. MicroCT scanner performance and considerations for vascular specimen imaging. Med Phys. 2004; 31(2), 305313.CrossRefGoogle ScholarPubMed
Zhou, YQ, Cahill, LS, Wong, MD, Seed, M, Macgowan, CK, Sled, JG. Assessment of flow distribution in the mouse fetal circulation at late gestation by high-frequency Doppler ultrasound. Physiol Genomics. 2014; 46(16), 602614.CrossRefGoogle ScholarPubMed
Power, RM, Huisken, J. A guide to light-sheet fluorescence microscopy for multiscale imaging. Nat Methods. 2017; 14(4), 360373.CrossRefGoogle ScholarPubMed
Reynaud, EG, Peychl, J, Huisken, J, Tomancak, P. Guide to light-sheet microscopy for adventurous biologists. Nat Methods. 2015; 12(1), 3034.CrossRefGoogle ScholarPubMed
Cai, R, Pan, C, Ghasemigharagoz, A, et al. Panoptic imaging of transparent mice reveals whole-body neuronal projections and skull-meninges connections. Nat Neurosci. 2019; 22(2), 317327.CrossRefGoogle ScholarPubMed
Henning, Y, Osadnik, C, Malkemper, EP. EyeCi: optical clearing and imaging of immunolabeled mouse eyes using light-sheet fluorescence microscopy. Exp Eye Res. 2019; 180, 137145.CrossRefGoogle ScholarPubMed
Ding, Y, Bailey, Z, Messerschmidt, V, et al. Light-sheet fluorescence microscopy for the study of the murine heart. J Vis Exp. 2018; 139, e57769.Google Scholar
Li, T, Hui, H, Hu, C, Ma, H, Yang, X, Tian, J. Multiscale imaging of colitis in mice using confocal laser endomicroscopy, light-sheet fluorescence microscopy, and magnetic resonance imaging. J Biomed Opt. 2019; 24(1), 18.Google ScholarPubMed
Kagami, K, Shinmyo, Y, Ono, M, Kawasaki, H, Fujiwara, H. Three-dimensional visualization of intrauterine conceptus through the uterine wall by tissue clearing method. Sci Rep. 2017; 7(1), 5964.CrossRefGoogle ScholarPubMed
Mano, T, Albanese, A, Dodt, HU, et al. Whole-brain analysis of cells and circuits by tissue clearing and light-sheet microscopy. J Neurosci. 2018; 38(44), 93309337.CrossRefGoogle ScholarPubMed
Isaacson, D, McCreedy, D, Calvert, M, et al. Imaging the developing human external and internal urogenital organs with light sheet fluorescence microscopy. Differentiation. 2019; 111, 1221.CrossRefGoogle ScholarPubMed
Buytaert, J, Goyens, J, De Greef, D, Aerts, P, Dirckx, J. Volume shrinkage of bone, brain and muscle tissue in sample preparation for micro-CT and light sheet fluorescence microscopy (LSFM). Microsc Microanal. 2014; 20(4), 12081217.CrossRefGoogle Scholar
Abramowicz, JS, Sheiner, E. Ultrasound of the placenta: a systematic approach. Part I: imaging. Placenta. 2008; 29(3), 225240.CrossRefGoogle ScholarPubMed
Abramowicz, JS, Sheiner, E. Ultrasound of the placenta: a systematic approach. Part II: functional assessment (Doppler). Placenta. 2008; 29(11), 921929.CrossRefGoogle Scholar
Kingdom, JC, Audette, MC, Hobson, SR, Windrim, RC, Morgen, E. A placenta clinic approach to the diagnosis and management of fetal growth restriction. Am J Obstet Gynecol. 2018; 218(2S), S803S817.CrossRefGoogle ScholarPubMed
Collins, SL, Birks, JS, Stevenson, GN, Papageorghiou, AT, Noble, JA, Impey, L. Measurement of spiral artery jets: general principles and differences observed in small-for-gestational-age pregnancies. Ultrasound Obstet Gynecol. 2012; 40(2), 171178.CrossRefGoogle ScholarPubMed
Mathewlynn, S, Collins, SL. Volume and vascularity: using ultrasound to unlock the secrets of the first trimester placenta. Placenta. 2019; 84, 3236.CrossRefGoogle ScholarPubMed
Mulcahy, C, Mone, F, McParland, P, et al. The impact of aspirin on ultrasound markers of uteroplacental flow in low-risk pregnancy: secondary analysis of a multicenter RCT. Am J Perinatol. 2019; 36(8), 855863.Google ScholarPubMed
Stevenson, GN, Noble, JA, Welsh, AW, Impey, L, Collins, SL. Automated visualization and quantification of spiral artery blood flow entering the first-trimester placenta, using 3-D power Doppler ultrasound. Ultrasound Med Biol. 2018; 44(3), 522531.CrossRefGoogle ScholarPubMed
Costa, J, Rice, H, Cardwell, C, Hunter, A, Ong, S. An assessment of vascularity and flow intensity of the placenta in normal pregnancy and pre-eclampsia using three-dimensional ultrasound. J Matern Fetal Neonatal Med. 2010; 23(8), 894899.CrossRefGoogle ScholarPubMed
Hata, T, Tanaka, H, Noguchi, J, Hata, K. Three-dimensional ultrasound evaluation of the placenta. Placenta. 2011; 32(2), 105115.CrossRefGoogle ScholarPubMed
Looney, P, Stevenson, GN, Nicolaides, KH, et al. Fully automated, real-time 3D ultrasound segmentation to estimate first trimester placental volume using deep learning. JCI Insight. 2018; 3(11), e120178.CrossRefGoogle ScholarPubMed
Lin, M, Mauroy, B, James, JL, Tawhai, MH, Clark, AR. A multiscale model of placental oxygen exchange: the effect of villous tree structure on exchange efficiency. J Theor Biol. 2016; 408, 112.CrossRefGoogle ScholarPubMed
Yu, Y, Yang, O, Fazli, L, Rennie, PS, Gleave, ME, Dong, X. Progesterone receptor expression during prostate cancer progression suggests a role of this receptor in stromal cell differentiation. Prostate. 2015; 75(10), 10431050.CrossRefGoogle ScholarPubMed
Morris, RK, Malin, G, Robson, SC, Kleijnen, J, Zamora, J, Khan, KS. Fetal umbilical artery Doppler to predict compromise of fetal/neonatal wellbeing in a high-risk population: systematic review and bivariate meta-analysis. Ultrasound Obstet Gynecol. 2011; 37(2), 135142.CrossRefGoogle Scholar
Salati, JA, Roberts, VHJ, Schabel, MC, et al. Maternal high-fat diet reversal improves placental hemodynamics in a nonhuman primate model of diet-induced obesity. Int J Obes (Lond). 2019; 43(4), 906916.CrossRefGoogle Scholar
Rahman, A, Zhou, YQ, Yee, Y, et al. Ultrasound detection of altered placental vascular morphology based on hemodynamic pulse wave reflection. Am J Physiol Heart Circ Physiol. 2017; 312(5), H1021H1029.CrossRefGoogle ScholarPubMed
Hernandez-Andrade, E, Ahn, H, Szalai, G, et al. Evaluation of utero-placental and fetal hemodynamic parameters throughout gestation in pregnant mice using high-frequency ultrasound. Ultrasound Med Biol. 2014; 40(2), 351360.CrossRefGoogle ScholarPubMed
Lo, JO, Schabel, MC, Roberts, VH, et al. First trimester alcohol exposure alters placental perfusion and fetal oxygen availability affecting fetal growth and development in a non-human primate model. Am J Obstet Gynecol. 2017; 216(3), e301e302, e308.Google Scholar
Lopez-Tello, J, Barbero, A, Gonzalez-Bulnes, A, et al. Characterization of early changes in fetoplacental hemodynamics in a diet-induced rabbit model of IUGR. J Dev Orig Health Dis. 2015; 6(5), 454461.CrossRefGoogle Scholar
Foster, FS, Hossack, J, Adamson, SL. Micro-ultrasound for preclinical imaging. Interface Focus. 2011; 1(4), 576601.CrossRefGoogle ScholarPubMed
Maneas, E, Aughwane, R, Huynh, N, et al. Photoacoustic imaging of the human placental vasculature. J Biophotonics. 2019; e201900167. doi: 10.1002/jbio.201900167.CrossRefGoogle Scholar
Yamaleyeva, LM, Brosnihan, KB, Smith, LM, Sun, Y. Preclinical ultrasound-guided photoacoustic imaging of the placenta in normal and pathologic pregnancy. Mol Imaging. 2018; 17, 1536012118802721.CrossRefGoogle ScholarPubMed
Arthuis, CJ, Novell, A, Raes, F, et al. Real-time monitoring of placental oxygenation during maternal hypoxia and hyperoxygenation using photoacoustic imaging. PLoS One. 2017; 12(1), e0169850.CrossRefGoogle ScholarPubMed
Lawrence, DJ, Huda, K, Bayer, CL. Longitudinal characterization of local perfusion of the rat placenta using contrast-enhanced ultrasound imaging. Interface Focus. 2019; 9(5), 20190024.CrossRefGoogle ScholarPubMed
Otake, Y, Kanazawa, H, Takahashi, H, Matsubara, S, Sugimoto, H. Magnetic resonance imaging of the human placental cotyledon: proposal of a novel cotyledon appearance score. Eur J Obstet Gynecol Reprod Biol. 2019; 232, 8286.CrossRefGoogle ScholarPubMed
Allen, BC, Leyendecker, JR. Placental evaluation with magnetic resonance. Radiol Clin North Am. 2013; 51(6), 955966.CrossRefGoogle ScholarPubMed
Damodaram, M, Story, L, Eixarch, E, et al. Placental MRI in intrauterine fetal growth restriction. Placenta. 2010; 31(6), 491498.CrossRefGoogle ScholarPubMed
Sinding, M, Peters, DA, Frokjaer, JB, et al. Prediction of low birth weight: comparison of placental T2* estimated by MRI and uterine artery pulsatility index. Placenta. 2017; 49, 4854.CrossRefGoogle ScholarPubMed
Damodaram, MS, Story, L, Eixarch, E, et al. Foetal volumetry using magnetic resonance imaging in intrauterine growth restriction. Early Hum Dev. 2012; 88 (Suppl 1), S35S40.CrossRefGoogle ScholarPubMed
Avni, R, Neeman, M, Garbow, JR. Functional MRI of the placenta--from rodents to humans. Placenta. 2015; 36(6), 615622.CrossRefGoogle ScholarPubMed
Sorensen, A, Peters, D, Frund, E, Lingman, G, Christiansen, O, Uldbjerg, N. Changes in human placental oxygenation during maternal hyperoxia estimated by blood oxygen level-dependent magnetic resonance imaging (BOLD MRI). Ultrasound Obstet Gynecol. 2013; 42(3), 310314.CrossRefGoogle Scholar
Sorensen, A, Sinding, M, Peters, DA, et al. Placental oxygen transport estimated by the hyperoxic placental BOLD MRI response. Physiol Rep. 2015; 3(10), e12582.CrossRefGoogle ScholarPubMed
Ingram, E, Morris, D, Naish, J, Myers, J, Johnstone, E. MR imaging measurements of altered placental oxygenation in pregnancies complicated by fetal growth restriction. Radiology. 2017; 285(3), 953960.CrossRefGoogle ScholarPubMed
Aimot-Macron, S, Salomon, LJ, Deloison, B, et al. In vivo MRI assessment of placental and foetal oxygenation changes in a rat model of growth restriction using blood oxygen level-dependent (BOLD) magnetic resonance imaging. Eur Radiol. 2013; 23(5), 13351342.CrossRefGoogle Scholar
Chalouhi, GE, Alison, M, Deloison, B, et al. Fetoplacental oxygenation in an intrauterine growth restriction rat model by using blood oxygen level-dependent MR imaging at 4.7 T. Radiology. 2013; 269(1), 122129.CrossRefGoogle Scholar
Kording, F, Forkert, ND, Sedlacik, J, et al. Automatic differentiation of placental perfusion compartments by time-to-peak analysis in mice. Placenta. 2015; 36(3), 255261.CrossRefGoogle ScholarPubMed
Alison, M, Quibel, T, Balvay, D, et al. Measurement of placental perfusion by dynamic contrast-enhanced MRI at 4.7 T. Invest Radiol. 2013; 48(7), 535542.CrossRefGoogle ScholarPubMed
Tomlinson, TM, Garbow, JR, Anderson, JR, Engelbach, JA, Nelson, DM, Sadovsky, Y. Magnetic resonance imaging of hypoxic injury to the murine placenta. Am J Physiol Regul Integr Comp Physiol. 2010; 298(2), R312319.CrossRefGoogle ScholarPubMed
Deloison, B, Siauve, N, Aimot, S, et al. SPIO-enhanced magnetic resonance imaging study of placental perfusion in a rat model of intrauterine growth restriction. BJOG. 2012; 119(5), 626633.CrossRefGoogle Scholar
Lemery Magnin, M, Fitoussi, V, Siauve, N, et al. Assessment of placental perfusion in the preeclampsia L-NAME rat model with high-field dynamic contrast-enhanced MRI. Fetal Diagn Ther. 2018; 44(4), 277284.CrossRefGoogle ScholarPubMed
Solomon, E, Avni, R, Hadas, R, et al. Major mouse placental compartments revealed by diffusion-weighted MRI, contrast-enhanced MRI, and fluorescence imaging. Proc Natl Acad Sci U S A. 2014; 111(28), 1035310358.CrossRefGoogle ScholarPubMed
Erlich, A, Nye, GA, Brownbill, P, Jensen, OE, Chernyavsky, IL. Quantifying the impact of tissue metabolism on solute transport in feto-placental microvascular networks. Interface Focus. 2019; 9(5), 20190021.CrossRefGoogle ScholarPubMed
Erlich, A, Pearce, P, Mayo, RP, Jensen, OE, Chernyavsky, IL. Physical and geometric determinants of transport in fetoplacental microvascular networks. Sci Adv. 2019; 5(4), eaav6326.CrossRefGoogle ScholarPubMed
Lofthouse, EM, Perazzolo, S, Brooks, S, et al. Phenylalanine transfer across the isolated perfused human placenta: an experimental and modeling investigation. Am J Physiol Regul Integr Comp Physiol. 2016; 310(9), R828836.CrossRefGoogle ScholarPubMed
Pearce, P, Brownbill, P, Janacek, J, et al. Image-based modeling of blood flow and oxygen transfer in feto-placental capillaries. PLoS One. 2016; 11(10), e0165369.CrossRefGoogle ScholarPubMed
Plitman Mayo, R, Olsthoorn, J, Charnock-Jones, DS, Burton, GJ, Oyen, ML. Computational modeling of the structure-function relationship in human placental terminal villi. J Biomech. 2016; 49(16), 37803787.CrossRefGoogle ScholarPubMed
Widdows, KL, Panitchob, N, Crocker, IP, et al. Integration of computational modeling with membrane transport studies reveals new insights into amino acid exchange transport mechanisms. FASEB J. 2015; 29(6), 25832594.CrossRefGoogle ScholarPubMed
Panitchob, N, Widdows, KL, Crocker, IP, et al. Computational modelling of placental amino acid transfer as an integrated system. Biochim Biophys Acta. 2016; 1858(7 Pt A), 14511461.CrossRefGoogle ScholarPubMed
Panitchob, N, Widdows, KL, Crocker, IP, et al. Computational modelling of amino acid exchange and facilitated transport in placental membrane vesicles. J Theor Biol. 2015; 365, 352364.CrossRefGoogle ScholarPubMed
Gill, JS, Salafia, CM, Grebenkov, D, Vvedensky, DD. Modeling oxygen transport in human placental terminal villi. J Theor Biol. 2011; 291, 3341.CrossRefGoogle ScholarPubMed
Lecarpentier, E, Bhatt, M, Bertin, GI, et al. Computational fluid dynamic simulations of maternal circulation: wall shear stress in the human placenta and its biological implications. PLoS One. 2016; 11(1), e0147262.CrossRefGoogle ScholarPubMed
Clark, AR, Lin, M, Tawhai, M, Saghian, R, James, JL. Multiscale modelling of the feto-placental vasculature. Interface Focus. 2015; 5(2), 20140078.CrossRefGoogle ScholarPubMed