The Openings of Uteroplacental Vessels With Villous Infiltration at Different Gestational Ages

The number of uteroplacental vessels flowing into the intervillous space has been studied in the placentas of humans and rhesus monkeys. Frank and Kaufmann1 and Boyd and Hamilton2 have reviewed these studies. According to Frank and Kaufmann,1 the number of spiral arteries that perfuse the placenta is still unknown. The study made by Boyd and Hamilton2 showed an increase in the number of spiral arteries during the course of human pregnancy. Ramsey3 reported that the number of such arteries in the rhesus monkey decreased in the later stages of pregnancy. Harris and Ramsey4 recorded a marked reduction in the number of functional uteroplacental arteries as human pregnancy advances. These conflicting views need further study in order to elucidate the truth.

Villous infiltration into uteroplacental vessels has been neglected in routine histologic examination. The openings of the vessels are usually available for examination in the thin basal plate because of placental separation. Differentiation between arteries and veins of the vessels is often difficult in the basal plate, because all vessels have veinlike structures.5,6 Although the total number of openings in the placenta was not counted in this study, the frequency of openings with or without villous infiltration can be compared in different gestational age groups. Villous infiltration and proliferation in the vessels have not been widely reported, and these villous activities seem to be essential to placental development. The purpose of this study was to clarify the foregoing conflicting findings regarding villous infiltration and proliferation in the vessels by using retrospective histologic slides of placentas at different gestational ages.

Placentas from single births delivered spontaneously or by cesarean section, ranging in gestational age from 13 to 41 weeks, were included in this study. Placentas were obtained from surgical pathology cases at St Luke's International Hospital from 1999 to 2000. During this period, 255 placentas were sampled, consisting of gestational age groups of 67 cases of 41 to 37 weeks, 102 cases of 36 to 30 weeks, 46 cases of 29 to 20 weeks, and 40 cases of 19 to 13 weeks. These placentas were selected from cases without major maternal complications, such as diabetes mellitus or pre-eclampsia. Cases of placenta previa and spontaneous abortion were included in this study. The placental sections examined were about 2.0 × 3.0 cm and spanned the entire thickness of the placenta, including the basal plate. The width of the basal plate in each section was measured, and the mean width was 2.2 ± 0.4 cm. Sections in which the basal plate was missing, incomplete, or lacerated were excluded from this study. Each slide contained one section of a block obtained from the central, intermediate, or marginal area. Hematoxylin-eosin–stained sections were examined for openings, with or without villous infiltration, in uteroplacental vessels of the basal plate. Elastic staining was done in 50 selective sections to differentiate uteroplacental arteries from the veins. Van Gieson was used as a counterstain in orcein and Weigert elastic preparations. The placental sections, excluding the membranes and umbilical cord, varied in the number of sections per case. Because the number of openings increased incrementally, the frequency was obtained by dividing the number of openings by the number of sections.

The basal plate available after parturition for placental examination was thin. Placental separation usually occurred along the transverse line of uteroplacental vessels, below the vessels' openings (Figure 1). The thin basal plate was transversed by the openings of uteroplacental vessels, but the vessels were often missing because of placental separation. The openings were located longitudinally because the placentas were cut vertically in routine placental examinations. The openings were completely or partially infiltrated by chorionic villi and were sometimes divided into 2 or more lumens (Figure 2). These divided openings were classified as 1 opening when counted, either with or without villous infiltration. The vessels of the basal plate were not counted in this study, because the number of vessels varied with the depth of placental separation. Differences in frequencies and mean values were calculated using the test of significant difference in proportions and the t test, respectively.

In the Table, the frequency of openings per section is listed in the gestational age groups of 41 to 37 weeks, 36 to 30 weeks, 29 to 20 weeks, and 19 to 13 weeks. The frequency of total openings was significantly lower in the 41 to 37 weeks group (1.2) than in the 36 to 30 weeks group (2.0), the 29 to 20 weeks group (2.2), and the 19 to 13 weeks group (2.4) (P < .001). The frequency of openings with villous infiltration was significantly lower in the 41 to 37 weeks group (0.9) than in the 36 to 30 weeks group (1.6), the 29 to 20 weeks group (1.7), and the 19 to 13 weeks group (1.9) (P < .001). The frequency of openings without villous infiltration was significantly lower in the 41 to 37 weeks group (0.3) than in the 19 to 13 weeks group (0.5) (P < .001), but it was not different from those in the 36 to 30 weeks group (0.3) and the 29 to 20 weeks group (0.4). The mean number of sections in the 41 to 37 weeks group (5.4 ± 0.7) was significantly higher than in the 19 to 13 weeks group (4.2 ± 1.2) (P < .001), but it was not different from those of the 36 to 30 weeks group (5.0 ± 1.1) and the 29 to 20 weeks group (5.0 ± 1.1).

Chorionic villi infiltrated deeply into the openings of uteroplacental vessels and extended to the vessels (Figure 1). The villi proliferated extensively in the vessels under the basal plate, as they did in the extension of intervillous space (Figure 3). Villous expansion and endovascular trophoblastic invasion were found in the marginal uteroplacental vessel (Figure 4). The vascular endothelium was destroyed by villous proliferation and trophoblastic invasion in this vessel (Figure 5). There was a complete absence of muscular and elastic tissues in uteroplacental vessels and in the openings located in the basal plate. Elastic staining was negative, and fibrinoid deposition was sometimes found in these vessels.

The number of arteries into the intervillous space decreases in the late stages of pregnancy in humans and monkeys.3,4 According to Harris and Ramsey,4 the number of arteries was gradually reduced by the penetration of trophoblast, because the proximal parts of the arteries were destroyed. Such vascular remodeling may be produced by villous infiltration and proliferation, in addition to endovascular trophoblastic invasion. The moderate decrease in the frequency of openings in the group of 41 to 37 weeks gestational age suggests that the amount of intervillous blood flow is limited in full-term and postterm pregnancy. Because fetal growth continues until 42 weeks of gestation,7 an imbalance between increasing fetal growth and limited intervillous blood flow is expected in postterm pregnancy. This placental dysfunction could be partly responsible for the increase of perinatal mortality in postterm pregnancy.8 The decrease in the frequency of openings in mature placentas may prevent excessive fetal development before delivery. In normal pregnancy, Doppler ultrasound measurements revealed a possibility of decreasing blood flow in uterine arteries with increasing gestational age.9 Konje et al,10 with the use of color power angiography, observed that blood volume flow in uterine arteries increased with gestation, but there was a corresponding decrease in blood flow per kilogram of estimated fetal weight.

Chorionic villi infiltrated the openings of and proliferated in uteroplacental vessels. Villous infiltration into the vessels is considered a normal finding at different gestational ages and can provide trophoblast for uteroplacental arteries. Trophoblastic invasion has been found in uteroplacental arteries.11 Villous sprouting of mesenchymal villi, which are the forerunners of other villous types, is interpreted as the fundamental mechanism of human placental development.12 If villous sprouting and proliferation occur only in the intervillous space, it is difficult to explain the mechanism of marginal placental development. Villous and trophoblastic proliferation in marginal uteroplacental vessels is the most likely cause of marginal placental development.