Skip to main content Accessibility help
  • Get access
    Check if you have access via personal or institutional login
  • Cited by 3
  • Print publication year: 2010
  • Online publication date: July 2010

Chapter 3 - Defective spiral artery remodeling

from Section 2: - Placental bed vascular disorders


1. RobertsonW B, KhongT Y, BrosensIet al. The placental bed biopsy: review from three European centers. Am J Obstet Gynecol 1986; 155: 401–12.
2. DixonH G, RobertsonW B. A study of the vessels of the placental bed in normotensive and hypertensive women. J Obstet Gynaecol Br Emp 1958; 65: 803–9.
3. BrosensI. A study of the spiral arteries of the decidua basalis in normotensive and hypertensive pregnancies. J Obstet Gynaecol Br Cwth 1964; 71: 222–30.
4. BrosensI, RobertsonW B, DixonH G. The physiological response of the vessels of the placental bed to normal pregnancy. J Pathol Bacteriol 1967; 93: 569–79.
5. BrosensI A, RobertsonW B, DixonH G. The role of the spiral arteries in the pathogenesis of preeclampsia. Obstet Gynecol Annu 1972; 1: 177–91.
6. BrosensI, RenaerM. On the pathogenesis of placental infarcts in pre-eclampsia. J Obstet Gynaecol Br Commonw 1972; 79: 794–9.
7. KhongT Y, De WolfF, RobertsonW B, BrosensI. Inadequate maternal vascular response to placentation in pregnancies complicated by pre-eclampsia and by small-for-gestational age infants. Br J Obstet Gynaecol 1986; 93: 1049–59.
8. MeekinsJ W, PijnenborgR, HanssensM, McFadyenI R, van AsscheA. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 1994; 101: 669–74.
9. PijnenborgR, AnthonyJ, DaveyD Aet al. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 1991; 98: 648–55.
10. HanssensM, PijnenborgR, KeirseM Jet al. Renin-like immunoreactivity in uterus and placenta from normotensive and hypertensive pregnancies. Eur J Obstet Gynecol Reprod Biol 1998; 81: 177–84.
11. KimY M, BujoldE, ChaiworapongsaTet al. Failure of physiologic transformation of the spiral arteries in patients with preterm labor and intact membranes. Am J Obstet Gynecol 2003; 189: 1063–9.
12. GuzinK, TomrukS, TuncayY Aet al. The relation of increased uterine artery blood flow resistance and impaired trophoblast invasion in pre-eclamptic pregnancies. Arch Gynecol Obstet 2005; 272: 283–8.
13. SheppardB L, BonnarJ. The ultrastructure of the arterial supply of the human placenta in pregnancy complicated by fetal growth retardation. Br J Obstet Gynaecol 1976; 83: 948–59.
14. BrosensI, DixonH G, RobertsonW B. Fetal growth retardation and the arteries of the placental bed. Br J Obstet Gynaecol 1977; 84: 656–63.
15. De WolfF, BrosensI, RenaerM. Fetal growth retardation and the maternal arterial supply of the human placenta in the absence of sustained hypertension. Br J Obstet Gynaecol 1980; 87: 678–85.
16. ZeekP M, AssaliN S. Vascular changes in the decidua associated with eclamptogenic toxemia of pregnancy. Am J Clin Pathol 1950; 20: 1099–109.
17. HertigA T. Vascular pathology in hypertensive albuminuric toxemias of pregnancy. Clinics 1945; 4: 602–14.
18. KitzmillerJ L, WattN, DriscollS G. Decidual arteriopathy in hypertension and diabetes in pregnancy: immunofluorescent studies. Am J Obstet Gynecol 1981; 141: 773–9.
19. SheppardB L, BonnarJ. An ultrastructural study of utero-placental spiral arteries in hypertensive and normotensive pregnancy and fetal growth retardation. Br J Obstet Gynaecol 1981; 88: 695–705.
20. AlthabeO, LabarrereC, TelentaM. Maternal vascular lesions in placentae of small-for-gestational-age infants. Placenta 1985; 6: 265–76.
21. KhongT Y. Acute atherosis in pregnancies complicated by hypertension, small-for-gestational-age infants, and diabetes mellitus. Arch Pathol Lab Med 1991; 115: 722–5.
22. AbramowskyC R, VegasM E, SwinehartG, GyvesM T. Decidual vasculopathy of the placenta in lupus erythematosus. N Engl J Med 1980; 303: 668–72.
23. De WolfF, CarrerasL O, MoermanPet al. Decidual vasculopathy and extensive placental infarction in a patient with repeated thromboembolic accidents, recurrent fetal loss, and a lupus anticoagulant. Am J Obstet Gynecol 1982; 142: 829–34.
24. HustinJ, FoidartJ M, LambotteR. Maternal vascular lesions in pre-eclampsia and intrauterine growth retardation: light microscopy and immunofluorescence. Placenta 1983; 4: 489–98.
25. EmmrichP, BirkeR, GödelE. Morphology of myometrial and decidual arteries in normal pregnancy, in toxemia of pregnancy, and in maternal diabetes. Pathol Microbiol (Basel) 1975; 43: 38–61.
26. DriscollS G. The pathology of pregnancy complicated by diabetes mellitus. Med Clin N Am 1965; 49: 1053–67.
27. KhongT Y, PearceJ M, RobertsonW B. Acute atherosis in preeclampsia: maternal determinants and fetal outcome in the presence of the lesion. Am J Obstet Gynecol 1987; 157: 360–3.
28. MaqueoM, AzuelaJ C, de la VegaM D. Placental pathology in eclampsia and preeclampsia. Obstet Gynecol 1964; 24: 350–6.
29. McFadyenI R, PriceA B, GeirssonR T. The relation of birthweight to histological appearances in vessels of the placental bed. Br J Obstet Gynaecol 1986; 93: 476–81.
30. De WolfF, RobertsonW B, BrosensI. The ultrastructure of acute atherosis in hypertensive pregnancy. Am J Obstet Gynecol 1975; 123: 164–74.
31. KhongT Y, MottC. Immunohistologic demonstration of endothelial disruption in acute atherosis in pre-eclampsia. Eur J Obstet Gynecol Reprod Biol 1993; 51: 193–7.
32. MeekinsJ W, PijnenborgR, HanssensM, Van AsscheA, McFadyenI R. Immunohistochemical detection of lipoprotein(a) in the wall of placental bed spiral arteries in normal and severe preeclamptic pregnancies. Placenta 1994; 15: 511–24.
33. KosM, CzernobilskyB, HlupicL, KunjkoK. Pathological changes in placentas from pregnancies with preeclampsia and eclampsia with emphasis on persistence of endovascular trophoblastic plugs. Croat Med J 2005; 46: 404–9.
34. KhongT Y, RobertsonW B. Spiral artery disease. In: CoulamC B, FaulkW P, McIntyreJ A, eds. Immunological obstetrics. New York: W.W. Norton; 1992: pp. 492–501.
35. JauniauxE, HempstockJ, GreenwoldN, BurtonG J. Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol 2003; 162: 115–25.
36. KhongT Y, SawyerI H, HeryetA R. An immunohistologic study of endothelialization of uteroplacental vessels in human pregnancy – evidence that endothelium is focally disrupted by trophoblast in preeclampsia. Am J Obstet Gynecol 1992; 167: 751–6.
37. KhongT Y, ChambersH M. Alternative method of sampling placentas for the assessment of uteroplacental vasculature. J Clin Pathol 1992; 45: 925–7.
38. LyallF. The human placental bed revisited. Placenta 2002; 23: 555–62.
39. RenaerM, BrosensI. [Spiral arterioles in the decidua basalis in hypertensive complications of pregnancy.] Ned Tijdschr Verloskd Gynaecol 1963; 63: 103–18.
40. GerretsenG, HuisjesH J, ElemaJ D. Morphological changes of the spiral arteries in the placental bed in relation to pre-eclampsia and fetal growth retardation. Br J Obstet Gynaecol 1981; 88: 876–81.
41. RobsonS C, SimpsonH, BallE, LyallF, BulmerJ N. Punch biopsy of the human placental bed. Am J Obstet Gynecol 2002; 187: 1349–55.
42. HarsemN K, StaffA C, HeL, RoaldB. The decidual suction method: a new way of collecting decidual tissue for functional and morphological studies. Acta Obstet Gynecol Scand 2004; 83: 724–30.
43. BoydJ D, HamiltonW J. The human placenta. Cambridge: Heffer and Sons; 1970.
44. BrosensI A. The utero-placental vessels at term: the distribution and extent of physiological changes. Trophoblast Res 1988; 3: 61–7.
45. De WolfF, De Wolf-PeetersC, BrosensI, RobertsonW B. The human placental bed: electron microscopic study of trophoblastic invasion of spiral arteries. Am J Obstet Gynecol 1980; 137: 58–70.
46. BallE, BulmerJ N, AyisS, LyallF, RobsonS C. Late sporadic miscarriage is associated with abnormalities in spiral artery transformation and trophoblast invasion. J Pathol 2006; 208: 535–42.
47. CravenC M, MorganT, WardK. Decidual spiral artery remodelling begins before cellular interaction with cytotrophoblasts. Placenta 1998; 19: 241–52.
48. BrosensJ J, PijnenborgR, BrosensI A. The myometrial junctional zone spiral arteries in normal and abnormal pregnancies: a review of the literature. Am J Obstet Gynecol 2002; 187: 1416–23.
49. BrosensJ J, ParkerM, McIndoeA, PijnenborgR, BrosensI A. A role for menstruation in preconditioning the uterus for successful pregnancy. Am J Obstet Gynecol 2009; 200: 615.e1–615.e6.
50. VoigtH J, BeckerV. Doppler flow measurements and histomorphology of the placental bed in uteroplacental insufficiency. J Perinat Med 1992; 20: 139–47.
51. LinS, ShimizuI, SueharaN, NakayamaM, AonoT. Uterine artery Doppler velocimetry in relation to trophoblast migration into the myometrium of the placental bed. Obstet Gynecol 1995; 85: 760–5.
52. SagolS, ÖzkinayE, ÖztekinK, ÖzdemirN. The comparison of uterine artery Doppler velocimetry with the histopathology of the placental bed. Aust N Z J Obstet Gynaecol 1999; 39: 324–9.
53. AardemaM W, OosterhofH, TimmerA, van RooyI, AarnoudseJ G. Uterine artery Doppler flow and uteroplacental vascular pathology in normal pregnancies and pregnancies complicated by pre-eclampsia and small for gestational age fetuses. Placenta 2001; 22: 405–11.
54. MadazliR, SomunkiranA, CalayZ, IlvanS, AksuM F. Histomorphology of the placenta and the placental bed of growth restricted foetuses and correlation with the Doppler velocimetries of the uterine and umbilical arteries. Placenta 2003; 24: 510–6.
55. MatijevicR, MeekinsJ W, WalkinshawS A, NeilsonJ P, McFadyenI R. Spiral artery blood flow in the central and peripheral areas of the placental bed in the second trimester. Obstet Gynecol 1995; 86: 289–92.
56. DeurlooK L, SpreeuwenbergM D, BolteA C, Van VugtJ M. Color Doppler ultrasound of spiral artery blood flow for prediction of hypertensive disorders and intra uterine growth restriction: a longitudinal study. Prenat Diagn 2007; 27: 1011–6.