Inadequate maternal vascular response to placentation in pregnancies complicated by pre‐eclampsia and by small‐for‐gestational age infants
Abstract
Summary. An examination of the maternal vascular response to placentation shows that physiological changes in the placental bed normally extend from the decidua into the inner myometrium. In pre‐eclampsia and in a proportion of pregnancies with small‐for‐gestational age infants (SGA) the physiological changes are restricted to the decidual segments alone. In addition, complete absence of physiological changes throughout the entire length of some spiral arteries is seen in pre‐eclampsia and SGA. This new observation is confirmed in a study of basal plates of placentas from abnormal pregnancies. Intraluminal endovascular trophoblast may be seen in the placental bed spiral arteries in the third trimester in pre‐eclampsia and SGA, a feature not seen beyond the second trimester in normal pregnancy. These findings point to a defect in the normal interaction between migratory trophoblast and maternal uterine tissues in pre‐eclampsia and in SGA.
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Endothelial cell dysfunction has been associated with placental pathology and disease states.
“Since endothelial cell dysfunction has been associated with placental pathology and disease states29–32,”
From Conditional loss of ERK1 and ERK2 results in abnormal placentation and delayed parturition in the mouse (2019) · cites this paper as [31]
High resistance changes in the uterine artery Doppler waveform are correlated with FGR/SGA and pre-eclampsia.
“It has been known since the 1980s that high resistance changes in the uterine artery (UtA) Doppler waveform were correlated with FGR/SGA and pre-eclampsia, this has been studied extensively since [44].”
From Volume and vascularity: Using ultrasound to unlock the secrets of the first trimester placenta (2019) · cites this paper as [44]
Cites
INTRAUTERINE GROWTH AS ESTIMATED FROM LIVEBORN BIRTH-WEIGHT DATA AT 24 TO 42 WEEKS OF GESTATION
Lubchenco, L. O., Hansman, C., Dressler, M., & Boyd, E. (1963) · PEDIATRICS · doi:10.1542/peds.32.5.793 · Cited by 1,865 · see citing works
Boyd, J. D., & Hamilton, W. J. (1970) · Palgrave Macmillan UK eBooks · doi:10.1007/978-1-349-02807-8 · Cited by 948 · see citing works
The role of the spiral arteries in the pathogenesis of pre-eclampsia.
Brosens, I. A., Robertson, W. B., & Dixon, H. G. (1970) · PubMed · Cited by 894 · see citing works
Self-citationThe physiological response of the vessels of the placental bed to normal pregnancy
Brosens, I. A., Robertson, W. B., & Dixon, H. G. (1967) · The Journal of Pathology and Bacteriology · doi:10.1002/path.1700930218 · Cited by 792 · see citing works
Self-citationTHE ASSESSMENT OF FETAL GROWTH
Thomson, A. M. W., Billewicz, W. Z., & Hytten, F. E. (1968) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1968.tb01615.x · Cited by 756 · see citing works
Pijnenborg, R., Bland, J. M., Robertson, W. B., & Brosens, I. A. (1983) · Placenta · doi:10.1016/s0143-4004(83)80043-5 · Cited by 733 · see citing works
Self-citationIon exchange resins in the treatment and prophylaxis of pre-eclampsia.
Brosens, I. A., Wb, R., & Dixon, H. (1953) · PubMed · Cited by 706 · see citing works
Self-citationFox, H., & Elston, C. W. (1978) · PubMed · Cited by 621 · see citing works
NEW DOPPLER TECHNIQUE FOR ASSESSING UTEROPLACENTAL BLOOD FLOW
Campbell, S. C., Griffin, D. R., Pearce, J. M., DIAZ‐RECASENS, J., Cohen‐Overbeek, T. E., Willson, K., & Teague, M. J. (1983) · The Lancet · doi:10.1016/s0140-6736(83)91970-0 · Cited by 574 · see citing works
Fetal growth retardation and the arteries of the placental bed
Brosens, I., Dixon, H. G., & Robertson, W. B. (1977) · BJOG: An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1977.tb12676.x · Cited by 430 · see citing works
Self-citationTHE MATERNAL PLACENTAL BLOOD FLOW IN NORMOTENSIVE AND HYPERTENSIVE WOMEN
Browne, J. C. M., & Veall, N. (1953) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1953.tb07668.x · Cited by 420 · see citing works
The pathological response of the vessels of the placental bed to hypertensive pregnancy
Robertson, W. B., Brosens, I. A., & Dixon, H. G. (1967) · The Journal of Pathology and Bacteriology · doi:10.1002/path.1700930219 · Cited by 403 · see citing works
Self-citationGerretsen, G., Huisjes, H. J., & Elema, J. D. (1981) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1981.tb02222.x · Cited by 370 · see citing works
The pattern of interstitial trophoblasticinvasion of the myometrium in early human pregnancy
Pijnenborg, R., Bland, J. M., Robertson, W. B., Dixon, G., & Brosens, I. A. (1981) · Placenta · doi:10.1016/s0143-4004(81)80027-6 · Cited by 354 · see citing works
Self-citationUteroplacental vascular pathology
Robertson, W. B., Brosens, I. A., & Dixon, G. (1975) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/0028-2243(75)90130-6 · Cited by 290 · see citing works
Self-citationUteroplacental blood flow velocity‐time waveforms in normal and complicated pregnancy
Trudinger, B., Giles, W. B., & Cook, C. M. (1985) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1985.tb01046.x · Cited by 279 · see citing works
SHEPPARD, B. L., & Bonnar, J. (1976) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1976.tb00781.x · Cited by 232 · see citing works
Wolf, F. D., Brosens, I. A., & Renaer, M. (1980) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1980.tb04601.x · Cited by 173 · see citing works
Self-citationLunell, N. O., Nylund, L., Lewander, R., Sarby, B., & Thornström, S. (1982) · Clinical and Experimental Hypertension Part B Hypertension in Pregnancy · doi:10.3109/10641958209037184 · Cited by 170 · see citing works
CHORIODECIDUAL AND MYOMETRIAL BLOOD-FLOW
Dixon, H. G., Browne, J. C. M., & Davey, D. A. (1963) · The Lancet · doi:10.1016/s0140-6736(63)93054-x · Cited by 126 · see citing works
THE ULTRASTRUCTURE OF THE ARTERIAL SUPPLY OF THE HUMAN PLACENTA IN EARLY AND LATE PREGNANCY
SHEPPARD, B. L., & Bonnar, J. (1974) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1974.tb00507.x · Cited by 98 · see citing works
Maternal vascular lesions in placentae of small-for-gestational-age infants
ALTHABE, O. H., Labarrere, C. A., & Telenta, M. (1985) · Placenta · doi:10.1016/s0143-4004(85)80056-4 · Cited by 81 · see citing works
THE ANATOMY OF THE MATERNAL SIDE OF THE PLACENTA
Brosens, I. A., & Dixon, H. G. (1966) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1966.tb05175.x · Cited by 81 · see citing works
Self-citationHustin, J., Foidart, J., & Lambotte, R. (1983) · PubMed · Cited by 81 · see citing works
Comparison of Uteroplacental Blood Flow in Normal and in Intrauterine Growth-Retarded Pregnancy
Lunell, N. O., Sarby, B., Lewander, R., & Nylund, L. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000299924 · Cited by 79 · see citing works
Lancaster, P. A. L. (1982) · PubMed · Cited by 76 · see citing works
Chronic villitis of unknown etiology and maternal arterial lesions in preeclamptic pregnancies
Labarrere, C. A., & ALTHABE, O. H. (1985) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/0028-2243(85)90077-2 · Cited by 71 · see citing works
Wb, R., Brosens, I., & Landells, W. (1985) · PubMed · Cited by 52 · see citing works
Self-citationThe Blood Vessels of The Human Endometrium
Dalgaard, J. B. (1946) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016344609154461 · Cited by 26 · see citing works
Prolapse of the Uterus and Vagina Clinical and Therapeutic Aspects: Review of Six Hundred Cases
Danielson, C. (1957) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016345709157423 · Cited by 19 · see citing works
Studies on the Vasculature of the Corpus of the Human Uterus
Lundgren, N. (1957) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016345709155391 · Cited by 11 · see citing works
Kopelman, A. E. (1975) · Archives of Pediatrics and Adolescent Medicine · doi:10.1001/archpedi.1975.02120490072034 · Cited by 5 · see citing works
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The “Great Obstetrical Syndromes” are associated with disorders of deep placentation
Brosens, I., Pijnenborg, R., Vercruysse, L., & Romero, R. (2011) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2010.08.009 · Cited by 1,568 · see citing works
Self-citationNatural killer cells and pregnancy
Moffett-King, A. (2002) · Nature Reviews Immunology · doi:10.1038/nri886 · Cited by 1,235 · see citing works
Pathophysiology of placental-derived fetal growth restriction
Burton, G. J., & Jauniaux, E. (2018) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.11.577 · Cited by 1,070 · see citing works
Pre-eclampsia part 1: current understanding of its pathophysiology
Chaiworapongsa, T., Chaemsaithong, P., Yeo, L., & Romero, R. (2014) · Nature Reviews Nephrology · doi:10.1038/nrneph.2014.102 · Cited by 956 · see citing works
Cnossen, J. S., Morris, R. K., ter Riet, G., Mol, B. W. J., van der Post, J. A. M., Coomarasamy, A., Zwinderman, A. H., Robson, S. C., Bindels, P. J. E., Kleijnen, J., et al. (2008) · Canadian Medical Association Journal · doi:10.1503/cmaj.070430 · Cited by 719 · see citing works
Comparative Developmental Anatomy of the Murine and Human Definitive Placentae
Georgiades, P., Ferguson-Smith, A. C., & Burton, G. J. (2002) · Placenta · doi:10.1053/plac.2001.0738 · Cited by 641 · see citing works
Teixeira, J. M. A., Fisk, N. M., & Glover, V. (1999) · BMJ · doi:10.1136/bmj.318.7177.153 · Cited by 526 · see citing works
Placental Debris, Oxidative Stress and Pre-eclampsia
Redman, C. W. G., & Sargent, I. L. (2000) · Placenta · doi:10.1053/plac.2000.0560 · Cited by 508 · see citing works
Burton, G. J., Yung, H.-W., Cindrova-Davies, T., & Charnock-Jones, D. S. (2009) · Placenta · doi:10.1016/j.placenta.2008.11.003 · Cited by 502 · see citing works
Yung, H.-W., Calabrese, S., Hynx, D., Hemmings, B. A., Cetin, I., Charnock-Jones, D. S., & Burton, G. J. (2008) · The American Journal of Pathology · doi:10.2353/ajpath.2008.071193 · Cited by 388 · see citing works
DiFederico, E., Genbacev, O., & Fisher, S. J. (1999) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)65123-1 · Cited by 348 · see citing works
Maternal-fetal conditions necessitating a medical intervention resulting in preterm birth
Ananth, C. V., & Vintzileos, A. M. (2006) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2006.05.021 · Cited by 330 · see citing works
Placental Pathology in Early-Onset and Late-Onset Fetal Growth Restriction
Mifsud, W., & Sebire, N. J. (2014) · Fetal Diagnosis and Therapy · doi:10.1159/000359969 · Cited by 328 · see citing works
Shams, M., Kilby, M. D., Somerset, D. A., Howie, A. J., Gupta, A., Wood, P. J., Afnan, M., & Stewart, P. M. (1998) · Human Reproduction · doi:10.1093/humrep/13.4.799 · Cited by 276 · see citing works
Beyond oxygen: complex regulation and activity of hypoxia inducible factors in pregnancy
Pringle, K. G., Kind, K. L., Sferruzzi-Perri, A. N., Thompson, J. G., & Roberts, C. T. (2010) · Human Reproduction Update · doi:10.1093/humupd/dmp046 · Cited by 259 · see citing works
The placenta in fetal growth restriction: What is going wrong?
Sun, C., Groom, K. M., Oyston, C., Chamley, L. W., Clark, A. R., & James, J. L. (2020) · Placenta · doi:10.1016/j.placenta.2020.05.003 · Cited by 253 · see citing works
Prediction of small-for-gestation neonates from biophysical and biochemical markers at 11-13 weeks
Karagiannis, G., Akolekar, R., Sarquis, R., Wright, D., & Nicolaides, K. H. (2011) · Fetal Diagnosis and Therapy · doi:10.1159/000321694 · Cited by 195 · see citing works
Animal models of fetal growth restriction: Considerations for translational medicine
Swanson, A. M., & David, A. L. (2015) · Placenta · doi:10.1016/j.placenta.2015.03.003 · Cited by 183 · see citing works
Diagnosis and management of fetal growth restriction
Bamfo, J. E. A. K., & Odibo, A. O. (2011) · Journal of Pregnancy · doi:10.1155/2011/640715 · Cited by 178 · see citing works
Groom, K. M., & David, A. L. (2018) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.11.565 · Cited by 170 · see citing works
Zamudio, S. (2003) · High Altitude Medicine & Biology · doi:10.1089/152702903322022785 · Cited by 161 · see citing works
Khong, Y., & Brosens, I. (2011) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2010.10.012 · Cited by 153 · see citing works
Self-citationHarris, L. K., Keogh, R. J., Wareing, M., Baker, P. N., Cartwright, J. E., Aplin, J. D., & Whitley, G. S. J. (2006) · The American Journal of Pathology · doi:10.2353/ajpath.2006.060265 · Cited by 147 · see citing works
Preterm birth, ovarian endometriomata, and assisted reproduction technologies
Fernando, S., Breheny, S., Jaques, A. M., Halliday, J. L., Baker, G., & Healy, D. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.01.096 · Cited by 150 · see citing works
miR-210 Targets Iron-Sulfur Cluster Scaffold Homologue in Human Trophoblast Cell Lines
Lee, D.-C., Romero, R., Kim, J.-S., Tarca, A. L., Montenegro, D., Pineles, B. L., Kim, E., Lee, J., Kim, S. Y., Draghici, S., et al. (2011) · The American Journal of Pathology · doi:10.1016/j.ajpath.2011.04.035 · Cited by 135 · see citing works
Brosens, I., Pijnenborg, R., & Benagiano, G. (2013) · Placenta · doi:10.1016/j.placenta.2012.11.017 · Cited by 135 · see citing works
Zhang, E. G., Smith, S. K., Baker, P. N., & Charnock-Jones, D. S. (2001) · Molecular Medicine · doi:10.1007/bf03401869 · Cited by 125 · see citing works
Keogh, R. J., Harris, L. K., Freeman, A., Baker, P. N., Aplin, J. D., Whitley, G. S., & Cartwright, J. E. (2007) · Circulation Research · doi:10.1161/01.res.0000261352.81736.37 · Cited by 114 · see citing works
Oxygenation of the placental–fetal unit in humans
Schneider, H. (2011) · Respiratory Physiology & Neurobiology · doi:10.1016/j.resp.2011.05.009 · Cited by 84 · see citing works
The role of androgens and the androgen receptor in cycling endometrium
Cloke, B., & Christian, M. (2012) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.06.031 · Cited by 77 · see citing works
Hafner, E., Metzenbauer, M., Stümpflen, I., Waldhör, T., & Philipp, K. (2010) · Placenta · doi:10.1016/j.placenta.2010.06.011 · Cited by 67 · see citing works
Remodelling of Uteroplacental Arteries is Decreased in High Altitude Placentae
Tissot van Patot, M., Grilli, A., Chapman, P., Broad, E., Tyson, W., Heller, D. S., Zwerdlinger, L., & Zamudio, S. (2003) · Placenta · doi:10.1053/plac.2002.0899 · Cited by 67 · see citing works
Lai, J., Garcia-Tizon Larroca, S., Peeva, G., Poon, L. C., Wright, D., & Nicolaides, K. H. (2014) · Fetal Diagnosis and Therapy · doi:10.1159/000359968 · Cited by 63 · see citing works
Collins, S. L., Birks, J. S., Stevenson, G. N., Papageorghiou, A. T., Noble, J. A., & Impey, L. (2012) · Ultrasound in Obstetrics & Gynecology · doi:10.1002/uog.10149 · Cited by 55 · see citing works
A review of inter- and intraspecific variation in the eutherian placenta
Gundling, W. E., & Wildman, D. E. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0072 · Cited by 58 · see citing works
Szalai, G., Romero, R., Chaiworapongsa, T., Xu, Y., Wang, B., Ahn, H., Xu, Z., Chiang, P. J., Sundell, B., Wang, R., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0119547 · Cited by 46 · see citing works
Volume and vascularity: Using ultrasound to unlock the secrets of the first trimester placenta
Mathewlynn, S., & Collins, S. L. (2019) · Placenta · doi:10.1016/j.placenta.2019.06.379 · Cited by 30 · see citing works
Abdominal pregnancy: a perfusion confusion?
Collins, S. L., Grant, D., Black, R. S., Vellayan, M., & Impey, L. (2011) · Placenta · doi:10.1016/j.placenta.2011.07.032 · Cited by 27 · see citing works
Elliot, M. G., & Crespi, B. J. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2014.0069 · Cited by 26 · see citing works
Collins, S. L., Welsh, A. W., Impey, L., Noble, J. A., & Stevenson, G. N. (2017) · PLOS ONE · doi:10.1371/journal.pone.0178675 · Cited by 25 · see citing works
Brown, J. L., Sones, J. L., Angulo, C. N., Abbott, K., Miller, A. D., Boehm, U., & Roberson, M. S. (2019) · Scientific Reports · doi:10.1038/s41598-019-45997-0 · Cited by 13 · see citing works
- Authors
- KHONG, T. Y., DE WOLF, F., ROBERTSON, W. B., & BROSENS, I.
- Affiliations
- St George's Hospital (GB)
- KU Leuven (BE)
- Corresponding author
- KHONG, T. Y.
- Venue
- BJOG: An International Journal of Obstetrics & Gynaecology
- Publisher
- Wiley
- Published
- 1986-10
- Volume
- 93
- Issue
- 10
- Pages
- 1049-1059
- ISSN
- 0306-5456 (ISSN-L)
- 1470-0328
- 1471-0528
- OpenAlex
- W2111984223
- Cited by
- 1,591
- References
- 32
- Citations by year
- 2026: 12 · 2025: 8 · 2024: 21 · 2023: 34 · 2022: 32 · 2021: 32 · 2020: 45 · 2019: 38 · 2018: 50 · 2017: 49 · 2016: 46 · 2015: 57 · 2014: 76 · 2013: 65 · 2012: 57
- FWCI
- 25.44
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- BJOG An International Journal of Obstetrics & Gynaecology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Obstetrics and Gynecology › Pregnancy and preeclampsia studies
- Life Sciences › Immunology and Microbiology › Immunology › Reproductive System and Pregnancy
- Health Sciences › Medicine › Psychiatry and Mental health › Neurological Complications and Syndromes
- Keywords
- preeclampsia, small for gestational age, placentation, spiral arteries, decidua, myometrium, endovascular trophoblast, trophoblast migration, placental bed, basal plate, abnormal pregnancy
- MeSH terms
- Female, Humans, Infant, Newborn, Infant, Small for Gestational Age, Placenta, Placentation, Pre-Eclampsia, Pregnancy, Pregnancy Complications, Cardiovascular
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