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Normal and Abnormal Transformation of the Spiral Arteries During Pregnancy

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Normal and Abnormal Transformation of the Spiral Arteries During Pregnancy Article in press - uncorrected proof J. Perinat. Med. 34 (2006) 447–458 • Copyright ᮊ by Walter de Gruyter • Berlin • New York. DOI 10.1515/JPM.2006.089 Normal and abnormal transformation of the spiral arteries during pregnancy Jimmy Espinoza1,2, Roberto Romero1,3,*, Yeon Keywords: Atherosis; immunohistochemistry; impe- Mee Kim1,4, Juan Pedro Kusanovic1, Sonia dance to blood flow; integrin; physiologic transformation Hassan1,2, Offer Erez1, Francesca Gotsch1, of the spiral arteries; placental bed. Nandor Gabor Than1, Zoltan Papp5 and Chong Jai Kim1,4 1 Perinatology Research Branch, NICHD, NIH, DHHS, Anatomy and physiology of the uterine Detroit MI 48201, and Bethesda MD 20892, USA circulation 2 Department of Obstetrics and Gynecology, Wayne The blood supply of the uterus is provided by the uterine State University School of Medicine, Detroit MI 48201, and ovarian arteries w102x. After entering the myome- USA trium, the uterine arteries give rise to the ‘‘arcuate arter- 3 Center for Molecular Medicine and Genetics, Wayne ies,’’ which branch into the ‘‘radial arteries’’ w102x. The State University School of Medicine, Detroit MI 48201, radial arteries divide into the ‘‘basal arteries,’’ which sup- USA ply the basal portion of the endometrium (critical for 4 Department of Pathology, Wayne State University endometrial regeneration after menstruation) and the School of Medicine, Detroit MI 48201, USA ‘‘spiral arteries,’’ which continue toward the endometrial 5 First Department of Obstetrics and Gynecology, surface w95x. The term ‘‘spiral arteries’’ reflects the coiled Semmelweis University, Budapest, Hungary appearance of these vessels, whose role is to supply blood to the upper functional layer of the endometrium, thought to be shed during menstruation w95x. The spiral Abstract arteries branch into a subepithelial capillary plexus w95x. Markee reported that each spiral artery supplies approx- This article reviews the anatomy and physiology of the imately 4–9 mm2 of endometrial surface w71x. Blood from uterine circulation, with emphasis on the remodeling of the intervillous space is drained through the utero-pla- spiral arteries during normal pregnancy, and the timing cental veins, whose openings are on the floor of the inter- and anatomical pathways of trophoblast invasion of the villous space. The venous endothelium lines part of the spiral arteries. We review the definitions of the placental floor of the intervillous space w62x. The uteroplacental bed and basal plate of the placenta, their relevance to veins undergo less dramatic changes than the arteries. the study of the physiologic transformation of the spiral Trophoblast may or may not invade the venous wall, even arteries, as well as the methods to obtain and examine though free floating endoluminal trophoblast has been placental bed biopsy specimens. We also examine the found in these vessels w36x. role of the extravillous trophoblast in normal and abnor- mal pregnancies, and the criteria used to diagnose failure Endometrial bleeding during menstruation and of physiologic transformation of the spiral arteries. Final- hemostasis ly, we comment on the use of uterine artery Doppler velo- cimetry as a surrogate marker of chronic uteroplacental The endometrium has evolved to meet the needs of ischemia. menstruation, implantation, placentation, as well as post- partum hemostasis. The specific mechanisms responsi- ble for endometrial bleeding (during menstruation) and *Corresponding author: hemostasis (after menstruation) are relevant to the study Roberto Romero, MD Chief, Perinatology Research Branch of pregnancy, since uterine bleeding during pregnancy Intramural Division, NICHD, NIH, DHHS (i.e., hemostatic failure) is a risk factor for adverse preg- National Institute of Child Health nancy outcome w75, 101x. and Human Development Perinatology Research Branch The current understanding of the vascular changes Hutzel Women’s Hospital–4th Floor that occur during menstruation is based upon classic 3990 John R physiologic studies conducted by Markee, who exam- Detroit, MI 48201/USA ined the behavior of endometrium from rhesus monkeys Tel.: q1 (313) 993-2700 Fax: q1 (313) 993-2694 implanted into the anterior chamber of the eye of non- E-mail: [email protected] human primates w71x. The explants underwent a reduc- Article in press - uncorrected proof 448 Espinoza et al., Normal and abnormal transformation of the spiral arteries during pregnancy tion in size of 25–75%, 2–6 days before the onset of bleeding. The spiral arteries became more coiled, and blood flow either slowed down or came to a complete stop. Red blood cells were reported not to move for 60–90 seconds w71x. Menstrual bleeding was considered to occur when vessels vasodilated after a period of intense vasoconstriction. Five mechanisms were pro- posed to account for the bleeding: (1) blood could pass through a damaged arteriole and form a hematoma, which would then rupture into the uterine cavity; (2) blood would pass directly from a ruptured arteriole into the uterine cavity; (3) red blood cells would extravasate by crossing the wall of the arterioles; (4) venous bleeding, which may occur either through the damaged venous wall or drainage following extravasation from arterioles; and (5) secondary bleeding may happen following violent Figure 1 Microscopic demonstration of physiologic transfor- movement. Markee proposed that 75% of bleeding mation of the myometrial segment of the spiral artery in normal derived from arterioles, and 25% from the venules. Ces- pregnancy at term. The placental bed biopsy specimen was sation of bleeding is thought to be due to vasoconstric- immunostained for cytokeratin-7 to locate trophoblasts (arrow- tion w71x. heads) infiltrating the arterial wall, and additional Periodic Acid Schiff (PAS) staining was performed to identify fibrinoid (arrows). The fact that menstrual fluid generally does not clot Spiral arterial lumen is dilated, and fibrinoid replaces the media w x 94 should not be taken as an indication that coagulation and intima. L: spiral aterial lumen (Cytokeratin 7-PAS staining, is not important for uterine hemostasis. For instance, =100). patients with Von Willebrand disease have excessive menstrual blood loss w29x. During normal menstruation, platelets and fibrin plugs are formed within the lumen of erally stains positive on Periodic Acid Schiff (PAS) stain- w x the spiral vessels w23x. Consumption of platelets and ing 16 (Figure 1). Brosens et al. proposed that these fibrinogen is thought to result in decreased concentra- structural changes, particularly the destruction of muscle tions of platelets and fibrinogen in menstrual fluid w28x. in the media, would lead to loss in vasomotor control w x Lockwood et al. proposed that tissue factor and plas- 16 . Collectively, these changes are thought to maximize minogen activator inhibitor-1 (PAI-1) are implicated in the delivery of maternal blood to the intervillous space both decidual hemostasis during implantation and bleed- by making the arterial lumen wider, as well as reducing ing during menstruation w67x. Tissue factor would induce the responsiveness of these vessels to vasoconstrictor coagulation and prevent hemorrhage during implanta- agents. Invasion of the utero-placental veins has been tion, while PAI-1 would prevent extracellular matrix deg- implicated as a mechanism responsible for the lateral w x radation and fibrinolysis. At the end of the menstrual placental growth 25 . Much less is known, however, cycle, progesterone withdrawal would reduce tissue fac- about changes in the morphology of the utero- w x tor and PAI-1 production and facilitate menstruation w67x. placental veins during pregnancy 36 . Timing and anatomical pathways of Changes in the uterine circulation during trophoblast invasion of the spiral arteries pregnancy Robertson et al. w86x and Pijnenborg et al. w82x proposed The spiral arteries in the placental bed are normally trans- that trophoblast invasion occurs in two stages: (1) the formed into large dilated vessels undergoing dramatic transformation of the decidual segment of the spiral structural changes in their vessel wall. The spiral arteries arteries by a ‘‘wave’’ of endovascular trophoblast migra- are also known as the utero-placental arteries w16x. The tion in the first trimester; and (2) the transformation of the terms ‘‘physiologic changes’’ or ‘‘physiologic transfor- myometrial segments of the spiral arteries in the second mation’’ of the spiral arteries were first introduced by trimester w82, 86x. In 1972, Brosens and colleagues w17x Brosens, Robertson and Dixon in 1967 to emphasize that reported that in patients with preeclampsia and SGA, the these changes were part of normal pregnancy. The key physiologic transformation of spiral arteries is limited to findings of physiologic transformation are: (1) dilatation the decidual segment of the uteroplacental arteries, and of the lumen; (2) trophoblast invasion of the vessel wall Robertson proposed that this process is due to inhibition which includes both the media and endothelium; and (3) of the second ‘‘wave’’ of endovascular trophoblast migra- replacement of the muscular and elastic tissue of the tion that occurs from about 16 weeks onwards w51x. arterial wall by a thick layer of fibrinoid material that gen- However, Lyall et al. have concluded that morphological Article in press - uncorrected proof Espinoza et al., Normal and abnormal transformation of the spiral arteries during pregnancy 449 poses that trophoblast cells gain access to the
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