Uterine artery pulsatility index in hypertensive pregnancies: When does the index normalize in the puerperium?

Article information

Obstet Gynecol Sci. 2016;59(6):463-469

Publication date (electronic) : 2016 November 15

doi : https://doi.org/10.5468/ogs.2016.59.6.463

, Su Jin Sung ¹, Sung Il Choo ¹, Jeong Yeon Cho ², Hye Jin Yang ¹, Chan-Wook Park ¹, Joong Shin Park ¹, Hee Chul Syn ¹

¹Department of Obstetrics and Gynecology, Seoul National University College of Medicine, Seoul, Korea.

²Department of Radiology and Institute of Radiation Medicine, Seoul National University College of Medicine, Seoul, Korea.

Corresponding author: Jong Kwan Jun. Department of Obstetrics and Gynecology, Seoul National University College of Medicine, 103 Daehak-ro, Jongno-gu, Seoul 03080, Korea. Tel: +82-2-2072-2826, Fax: +82-2-762-3599, jhs0927@snu.ac.kr

Received 2016 May 30; Revised 2016 August 16; Accepted 2016 September 03.

Abstract

Objective

To investigate whether the uterine artery pulsatility index (UtA PI) of hypertensive pregnancies is higher than that of normal pregnancies in the puerperium, as well as in the antepartum period.

Methods

The UtA PI was measured in hypertensive (group 1) and normal pregnancies (group 2) during antepartum, immediate postpartum or late postpartum periods. Using the transvaginal approach, the bilateral uterine artery indices were measured.

Results

One hundred twenty-two women were enrolled: group 1, hypertensive disease in pregnancy (11 cases in antepartum, 13 cases in immediate postpartum and 10 cases in late postpartum period); group 2, normal pregnancies (32 cases in antepartum, 29 cases in immediate postpartum and 27 cases in late postpartum). In antepartum and immediate postpartum periods, the mean UtA PI and the proportion of cases with an early diastolic notch were higher in group 1 than in group 2 (antepartum mean UtA PI, 1.14 in group 1 vs. 0.68 in group 2, P<0.001; early diastolic notch, 46% vs. 9%, P<0.05; immediate postpartum mean UtA PI, 1.30 vs. 1.08, P<0.05; early diastolic notch, 85% vs. 48%, P<0.05). In late postpartum period, the mean value of UtA PI of group 1 was still higher than that of group 2, although the proportion of cases with an early diastolic notch was not different (mean UtA PI, 1.43 vs. 1.20, P<0.05; early diastolic notch, 60% vs. 52%, P=0.73).

Conclusion

The UtA PI in hypertensive pregnancies was still higher than normal pregnancies in puerperal periods, suggesting that more than several weeks are required to resolve increased uterine artery vascular impedance.

Keywords: Doppler; Hypertension; Postpartum period; Pre-eclampsia; Uterine artery

Introduction

In placentation of normal pregnancies, the spiral arteries are invaded by endovascular trophoblast, resulting in extensive remodeling of these arteries. Because of this change, the uterine artery Doppler in normal pregnancies is characterized by low resistance and a high-flow pattern. However, in hypertensive pregnancies, incomplete trophoblast invasion results in an abnormal uterine artery Doppler pattern, which is characterized by an increased pulsatility index (PI) and an early diastolic notch [1 2 3 4].

Based on the pathophysiology, it has been reported that abnormal uterine artery Doppler in hypertensive pregnancies is associated with adverse perinatal outcomes, such as early delivery and low birthweight [5 6 7 8 9]. Moreover, it has also been reported that the increased PI of the uterine arteries in the 1st trimester may be used in prediction of hypertension and small for gestational age [10 11 12 13 14 15 16 17 18].

Delivery is thought to be the definitive treatment of hypertensive disease in pregnancy, because the placenta is removed and maternal hypertension is resolved in the postpartum period. However, whether or not increased uterine impedance is resolved after delivery is unclear.

In the puerperal period, uterine involution involves not only uterine muscle and endometrium but also the uterine arteries and branches, resulting in dynamic changes of uterine artery Doppler. There have been several reports on the postpartum changes of uterine artery Doppler in normal pregnancies [19 20 21 22 23 24 25 26]. In most of these studies, uterine artery indices such as the resistance and pulsatility indices increased during the postpartum period [19 20 22 23 24 26], although some could not find significant changes during the postpartum period [21 25]. However, there is a paucity of information regarding the postpartum uterine artery Doppler in hypertensive pregnancies.

The objective of this study was to investigate whether the uterine artery pulsatility index (UtA PI) of hypertensive pregnancies is higher than that of normal pregnancies in the postpartum period as in the antepartum period.

Materials and methods

1. Study design

In this cross-sectional study, we measured the UtA PI in singleton pregnancies during the antepartum, immediate postpartum, and late postpartum periods. Each woman underwent Doppler examination once among these three periods. Antepartum measurement was performed at 24 to 40 weeks gestation, and immediate postpartum measurement was performed several days after delivery (usually 2 days). Late postpartum measurement was performed several weeks after delivery (usually 3 to 5 weeks). The institutional review board of Seoul National University Hospital approved this study, and patients gave their written consent for the collection of data for research purpose.

Cases were divided into 2 groups according to the presence or absence of hypertensive disease in pregnancy: group 1, women with hypertensive disease in pregnancy, including gestational hypertension, preeclampsia, eclampsia, chronic hypertension or superimposed preeclampsia; group 2, women with normotensive pregnancies.

2. Doppler measurement of the uterine arteries

Ultrasound examinations of the bilateral uterine arteries were performed by the transvaginal approach, using an Accuvix XQ (Medison, Seoul, Korea). The participants were asked to empty the bladder before the examinations and placed in the dorsal lithotomy position. The main uterine artery was identified at the level of the internal cervical os with color Doppler, and then pulsed Doppler was used to obtain the mean value of three consecutive data of the UtA PI. The same process was repeated for the contralateral uterine artery. The mean value of the bilateral uterine arteries was used for data analysis. The presence or absence of early diastolic notches was also documented. In women during the antepartum period, a Doppler examination of the fetal umbilical artery was also performed. All measurements were performed by a single examiner (LSM).

3. Statistical analysis

Statistical analyses were performed using SPSS ver. 12.0.1 (SPSS Inc., Chicago, IL, USA). Comparisons of continuous variables between groups were performed with the Mann-Whitney U-test. Proportions were compared with the Fisher’s exact test. A P-value of <0.05 was considered significant.

Results

1. Characteristics of the study population

One hundred twenty-two women were enrolled: group 1, women with hypertensive disease in pregnancy (11 cases in the antepartum period, 13 cases in the immediate postpartum period, and 10 cases in the late postpartum period); group 2, women with normal pregnancies (32 cases in the antepartum period, 29 cases in the immediate postpartum period, and 27 cases in the late postpartum period). Cases with fetal anomalies, intrauterine growth restriction without hypertensive disease, other obstetric or medical diseases that can affect the uterine circulation (including diabetes, autoimmune diseases, or uterine malformations) and placenta previa were excluded.

Table 1 shows the clinical characteristics of the study population. In the antepartum period, there were no significant differences in maternal age, parity, gestational age at the time of measurement, estimated fetal weight, and amniotic fluid index. However cases in group 1 had a higher UtA PI, an earlier gestational age at delivery, and a smaller birthweight than cases in group 2.

Table 1

Clinical characteristics of the study population

In the immediate and late postpartum periods, there were no significant differences in maternal age, parity, postpartum measurement days, and uterine size at the time of measurement between the two groups. However, cases in group 1 had an earlier gestational age at delivery and a smaller birthweight than cases in group 2.

2. Doppler measurements of the uterine arteries

In the antepartum and immediate postpartum periods, the mean value of UtA PI in group 1 was higher than in group 2 (Table 2). The proportion of cases with an early diastolic notch in at least one side was higher in group 1 than that in group 2 (antepartum period mean UtA PI, 1.14 in group 1 vs. 0.68 in group 2, P<0.001; percentage of early diastolic notch, 46% vs. 9%, P<0.05; immediate postpartum period mean UtA PI, 1.30 vs. 1.08, P<0.05; percentage of early diastolic notch, 85% vs. 48%, P<0.05).

Table 2

Doppler measurements of the uterine artery

The mean value of UtA PI in group 1 in the late postpartum period was also higher than that in group 2. The proportion of cases with an early uterine artery notch was higher in group 1 than that in group 2, but this difference did not reach statistical significance (mean UtA PI, 1.43 vs. 1.20, P<0.05; percentage of early diastolic notch, 60% vs. 52%, P=0.73).

Discussion

The principal finding of our study is that the mean value of UtA PI of hypertensive pregnancies was still higher than that of normal pregnancies in the immediate and late puerperal period, as well as in the antepartum period.

In hypertensive pregnancies, blood pressure is normalized and proteinuria disappears within several days after delivery. Does clinical improvement coincide with resolution of underlying basic pathophysiologic change? We adopt a uterine artery Doppler as an indirect method to identify it, and showed that the uterine artery impedance did not resolve, even several weeks after the delivery of the placenta.

Several mechanisms can be offered for this finding. First, the increased uterine artery impedance may be the result of remaining defective trophoblast invasion in the area of the basal zone of the decidua basalis (zona basalis) and myometrium, which remains even after delivery of the placenta [27]. Second, atherosis within the spiral arterioles can remain in the placental bed, to which the decreased placental perfusion has been also attributed [28 29 30 31]. Third, persistently increased maternal vascular tone could affect uterine arterial impedance. The last explanation is unlikely, because the persistence of maternal hypertension in the postpartum period was not associated with increased UtA PI in our data. In immediate postpartum period, 69 % (9/13) of women in group 1 had persistent hypertension, but the mean value of UtA PI was not different between women with persistent hypertension and those with resolved hypertension (UtA PI, 1.41 in women with persistent hypertension vs. 1.05 in women with resolved hypertension, P=0.15). In late postpartum period, 30 % (3/10) of women in group 1 had persistent hypertension, but the mean value of UtA PI was not different between women with persistent hypertension and those with resolved hypertension (UtA PI, 1.34 vs. 1.47, P=1.0). Fourth, different antepartum uterine artery indices between normotensive women and hypertensive women can result in different postpartum uterine artery indices, even after similar postpartum changes in uterine artery.

The antepartum mean UtA PI in group 1 was 1.14 measured at a mean gestational age of 33.8 weeks. The reported 95th percentile value of uterine artery PI at 34 weeks of gestation was 1.185 [32]. This means that the mean value of uterine artery PI was around the upper cut-off values of normal range. Another study also reported the mean values of UtA PI within normal range even in hypertensive group [33].

In the current study, we used transvaginal probe for measurement of uterine artery indices. Because trans-abdominal approach is not practical in postpartum, we adopted a transvaginal approach method to standardize the measurement technique during the antepartum and postpartum periods. The reliability of transvaginal measurement of uterine artery Doppler in the antepartum period was reported by several investigators [34 35].

Recently, the study about postpartum uterine artery Doppler velocimetry among patients with preeclampsia and the study about uterine artery impedance during puerperium in chronic hypertensive pregnancies were reported [33 36]. We included not only preeclampsia but also other hypertensive diseases such as gestational hypertension, chronic hypertension and superimposed preeclampsia in group 1. Increased uterine artery impedance is observed not only in preeclampsia but also other hypertensive diseases in pregnancy, because the defective trophoblast invasion, which is thought to be the main mechanism of uteroplacental insufficiency, could be identified in hypertensive diseases other than preeclampsia [4 37].

We demonstrate that the mean value of UtA PI in hypertensive women was still higher than that in normotensive women even in the late postpartum period, and the mean of postpartum day at measurement in the late postpartum period was 28 days in the current study. A more extended period of follow-up would be needed, considering that it would take more than several weeks for uterine artery indices to return to the non-pregnant state, as shown in studies on the postpartum uterine artery Doppler of normal pregnancies [19 24 26 38 39]. We believe this kind of information would enhance our understanding on vascular changes during postpartum in hypertensive women.

The clinical significance of postpartum uterine artery Doppler measurement needs further studies. The association between postpartum uterine artery Doppler and long-term cardiovascular or neurovascular consequences, or the association between postpartum uterine artery Doppler and other vascular indices such as arterial stiffness can be next research issues.

This study also confirms that in the antepartum and immediate postpartum periods the proportion of cases with early diastolic notch was significantly higher in group 1 than in group 2. But the difference for presence of early diastolic notch between the two groups of cases was disappeared in the late postpartum periods, mainly because of the increasing frequency of early diastolic notch in postpartum period in group 2 (normal pregnancy). The finding that the proportion of cases with early diastolic notch was increasing in normal pregnancy is consistent to the findings of other reports [33 38]. This trend may be based on a process for uterine artery to return to the non-pregnant state.

In conclusion, UtA PI of hypertensive pregnancies was still higher than that of normal pregnancies in the immediate and late puerperal periods. This data suggests that longer period may be needed for the resolution of vascular change than resolution of clinical parameters during postpartum in hypertensive women.

Notes

Conflict of interest: No potential conflict of interest relevant to this article was reported.

References

1. Meekins JW, Pijnenborg R, Hanssens M, McFadyen IR, van Asshe A. A study of placental bed spiral arteries and trophoblast invasion in normal and severe pre-eclamptic pregnancies. Br J Obstet Gynaecol 1994;101:669–674. 7947500.

2. Madazli R, Budak E, Calay Z, Aksu MF. Correlation between placental bed biopsy findings, vascular cell adhesion molecule and fibronectin levels in pre-eclampsia. BJOG 2000;107:514–518. 10759271.

3. Prefumo F, Sebire NJ, Thilaganathan B. Decreased endovascular trophoblast invasion in first trimester pregnancies with high-resistance uterine artery Doppler indices. Hum Reprod 2004;19:206–209. 14688183.

4. Pijnenborg R, Anthony J, Davey DA, Rees A, Tiltman A, Vercruysse L, et al. Placental bed spiral arteries in the hypertensive disorders of pregnancy. Br J Obstet Gynaecol 1991;98:648–655. 1883787.

5. Urban G, Vergani P, Ghidini A, Tortoli P, Ricci S, Patrizio P, et al. State of the art: non-invasive ultrasound assessment of the uteroplacental circulation. Semin Perinatol 2007;31:232–239. 17825679.

6. van Asselt K, Gudmundsson S, Lindqvist P, Marsal K. Uterine and umbilical artery velocimetry in pre-eclampsia. Acta Obstet Gynecol Scand 1998;77:614–619. 9688238.

7. Frusca T, Soregaroli M, Platto C, Enterri L, Lojacono A, Valcamonico A. Uterine artery velocimetry in patients with gestational hypertension. Obstet Gynecol 2003;102:136–140. 12850619.

8. Li H, Gudnason H, Olofsson P, Dubiel M, Gudmundsson S. Increased uterine artery vascular impedance is related to adverse outcome of pregnancy but is present in only one-third of late third-trimester pre-eclamptic women. Ultrasound Obstet Gynecol 2005;25:459–463. 15846767.

9. de Melo BC, de Amorim MM, Katz L, Coutinho I, Verissimo G. Uterine artery Doppler in the third trimester of pregnancy and postnatal outcome of patients with severe preeclampsia. Hypertens Pregnancy 2010;29:135–147. 19899954.

10. Khaw A, Kametas NA, Turan OM, Bamfo JE, Nicolaides KH. Maternal cardiac function and uterine artery Doppler at 11-14 weeks in the prediction of pre-eclampsia in nulliparous women. BJOG 2008;115:369–376. 18190374.

11. Plasencia W, Maiz N, Bonino S, Kaihura C, Nicolaides KH. Uterine artery Doppler at 11+0 to 13+6 weeks in the prediction of pre-eclampsia. Ultrasound Obstet Gynecol 2007;30:742–749. 17899573.

12. Pilalis A, Souka AP, Antsaklis P, Basayiannis K, Benardis P, Haidopoulos D, et al. Screening for pre-eclampsia and small for gestational age fetuses at the 11-14 weeks scan by uterine artery Dopplers. Acta Obstet Gynecol Scand 2007;86:530–534. 17464579.

13. Staboulidou I, Soergel P, Schippert C, Hertel H, Hillemanns P, Scharf A. The significance of uterine notching in Doppler sonography in early pregnancy as a predictor for pathologic outcome of the pregnancy. Arch Gynecol Obstet 2007;276:21–28. 17265036.

14. Pilalis A, Souka AP, Antsaklis P, Daskalakis G, Papantoniou N, Mesogitis S, et al. Screening for pre-eclampsia and fetal growth restriction by uterine artery Doppler and PAPP-A at 11-14 weeks’ gestation. Ultrasound Obstet Gynecol 2007;29:135–140. 17221926.

15. Papageorghiou AT, Campbell S. First trimester screening for preeclampsia. Curr Opin Obstet Gynecol 2006;18:594–600. 17099328.

16. Nicolaides KH, Bindra R, Turan OM, Chefetz I, Sammar M, Meiri H, et al. A novel approach to first-trimester screening for early pre-eclampsia combining serum PP-13 and Doppler ultrasound. Ultrasound Obstet Gynecol 2006;27:13–17. 16374755.

17. Gomez O, Martinez JM, Figueras F, Del Rio M, Borobio V, Puerto B, et al. Uterine artery Doppler at 11-14 weeks of gestation to screen for hypertensive disorders and associated complications in an unselected population. Ultrasound Obstet Gynecol 2005;26:490–494. 16184511.

18. Harrington K, Goldfrad C, Carpenter RG, Campbell S. Transvaginal uterine and umbilical artery Doppler examination of 12-16 weeks and the subsequent development of pre-eclampsia and intrauterine growth retardation. Ultrasound Obstet Gynecol 1997;9:94–100. 9132263.

19. Kirkinen P, Dudenhausen J, Baumann H, Huch A, Huch R. Postpartum blood flow velocity waveforms of the uterine arteries. J Reprod Med 1988;33:745–748. 3050078.

20. Sohn C, Fendel H, Kesternich P. Involution-induced changes in arterial uterine blood flow. Z Geburtshilfe Perinatol 1988;192:203–209. 3062954.

21. Thoresen M, Wesche J. Doppler measurements of changes in human mammary and uterine blood flow during pregnancy and lactation. Acta Obstet Gynecol Scand 1988;67:741–745. 3250187.

22. Logvinenko AV, Nikonov AP. Diagnostic value of Doppler ultrasonography in the evaluation of the status of uterine blood flow in puerperium. Akush Ginekol (Mosk) 1991;4:37–40.

23. Reles A, Ertan AK, Kainer F, Dudenhausen JW. Doppler ultrasound images of the uterine artery and uterine involution in normal puerperium. Gynakol Geburtshilfliche Rundsch 1992;32:66–72.

24. Tekay A, Jouppila P. A longitudinal Doppler ultrasonographic assessment of the alterations in peripheral vascular resistance of uterine arteries and ultrasonographic findings of the involuting uterus during the puerperium. Am J Obstet Gynecol 1993;168(1 Pt 1):190–198. 8420326.

25. Nakai Y, Imanaka M, Nishio J, Maeda T, Ozaki A, Sun TT, et al. Uterine blood flow velocity waveforms during early postpartum course following caesarean section. Eur J Obstet Gynecol Reprod Biol 1997;74:121–124. 9306102.

26. Mulic-Lutvica A, Eurenius K, Axelsson O. Longitudinal study of Doppler flow resistance indices of the uterine arteries after normal vaginal delivery. Acta Obstet Gynecol Scand 2007;86:1207–1214. 17882552.

27. Cunningham FG, Bloom SL, Hauth JC, Gilstrap L III, Wenstrom KD. Implantation, embryogenesis, and placental development. In : Cunningham FG, ed. Williams obstetrics 22nd edth ed. New York (NY): McGraw-Hill; 2005. p. 49.

28. De Wolf F, De Wolf-Peeters C, Brosens I, Robertson WB. The human placental bed: electron microscopic study of trophoblastic invasion of spiral arteries. Am J Obstet Gynecol 1980;137:58–70. 7369289.

29. Rogers BB, Bloom SL, Leveno KJ. Atherosis revisited: current concepts on the pathophysiology of implantation site disorders. Obstet Gynecol Surv 1999;54:189–195. 10071838.

30. Lain KY, Roberts JM. Contemporary concepts of the pathogenesis and management of preeclampsia. JAMA 2002;287:3183–3186. 12076198.

31. Redman CW, Sargent IL. Pre-eclampsia, the placenta and the maternal systemic inflammatory response: a review. Placenta 2003;24(Suppl A):S21–S27. 12842410.

32. Merz E. Ultrasound in obstetrics and gynecology New York (NY): Thieme; 2005.

33. Guedes-Martins L, Saraiva J, Felgueiras O, Carvalho M, Cerdeira A, Macedo F, et al. Uterine artery impedance during puerperium in normotensive and chronic hypertensive pregnant women. Arch Gynecol Obstet 2015;291:1237–1246. 25472737.

34. Papageorghiou AT, To MS, Yu CK, Nicolaides KH. Repeatability of measurement of uterine artery pulsatility index using transvaginal color Doppler. Ultrasound Obstet Gynecol 2001;18:456–459. 11844164.

35. Tekay A, Jouppila P. Intraobserver reproducibility of transvaginal Doppler measurements in uterine and intraovarian arteries in regularly menstruating women. Ultrasound Obstet Gynecol 1996;7:129–134. 8776238.

36. Weintraub AY, Aricha-Tamir B, Steiner N, Hamou BE, Baron J, Hershkovitz R. Postpartum uterine artery Doppler velocimetry among patients following a delivery complicated with preeclampsia. Hypertens Pregnancy 2013;32:450–458. 23957256.

37. Moodley J, Ramsaroop R. Placental bed morphology in black women with eclampsia. S Afr Med J 1989;75:376–378. 2711267.

38. Guedes-Martins L, Gaio AR, Saraiva J, Cunha A, Macedo F, Almeida H. Uterine artery impedance during the first eight postpartum weeks. Sci Rep 2015;5:8786. 25739463.

39. Diniz CP, Araujo Junior E, Lima MM, Guazelli CA, Moron AF. Ultrasound and Doppler assessment of uterus during puerperium after normal delivery. J Matern Fetal Neonatal Med 2014;27:1905–1911. 24410084.

Article information Continued

(open-access, http://creativecommons.org/licenses/by-nc/3.0/) :

Articles published in Obstet Gynecol Sci are open-access, distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.