Association between first-trimester ultrasound imaging of eccentric implantation and retained placenta

Abstract

Objectives

To evaluate first-trimester ultrasound imaging of eccentric implantation in predicting the probability of retained placenta.

Methods

A total of 61 cases with gestational sac eccentrically implanted in first-trimester ultrasound imaging was selected. Demographic and obstetric data were collected through data extraction of the electronic medical record at the time of delivery admission. Baseline characteristics (including age, gestational age of first-trimester ultrasound, size of gestational sac, gestational age of delivery), delivery outcomes (mode of delivery, retained placenta or placental fragments, blood loss, postpartum hemorrhage and postpartum ultrasound imaging) were collected and analyzed.

Results

The risk difference for a woman with eccentric implantation to have a retained placenta was −0.18 (95% CI −0.28 to −0.08, p = 0.000) and the incidence of retained placenta in the study group was higher than in the control group (18% vs. 0%, p = 0.006). First-trimester ultrasound imaging of eccentric implantation was also found to be an independent risk factor for the incidence of inhomogeneous mass in postpartum ultrasound imaging (27.9% vs. 10.8%, adjusted OR 0.19, 95% CI 0.05 to 0.79, p = 0.012). Though 2 cases in the study group suffered postpartum hemorrhage, the risk difference for a woman with eccentric implantation to suffer postpartum hemorrhage was −0.03 (95% CI −0.08 to −0.01, not significant) and eccentric implantation did not increase postpartum hemorrhage rates (3.3% vs. 0%, not significant).

Conclusions

First-trimester ultrasound imaging of eccentric implantation was associated with an increased risk of retained placenta and inhomogeneous mass in postpartum ultrasound imaging.

Keywords:

• Eccentric implantation
• first trimester
• implantation sites
• retained placenta
• ultrasound

Introduction

Retained placenta is considered one of the major causes of primary and secondary postpartum hemorrhage. Though the standard treatment is manual removal or extraction with ring forceps, various medications have been used to prevent the need for manual extraction and the procedures are associated with their own set of risks [1]. Therefore, it is clinically important to identify the risk factors of retained placenta. And then, the physicians can anticipate and prepare for the possibility of a retained placenta that may require additional interventions [2].

Many studies established risk factors for retained placenta, including prior retained placenta, preterm delivery, prior uterine surgery, previous pregnancy termination, miscarriage or curettage, grand multiparity, congenital uterine anomalies, stillbirth and even intergenerational recurrence [2–8]. But a review reported that there was no enough robust to draw firm conclusions on the relevant non-adherent retained placenta risk factors [9].

First-trimester clinical feature and ultrasound imaging were reported to reliably predict the disorder of placenta during delivery [10]. Low implantation pregnancy and angular pregnancy found in first-trimester ultrasound imaging may increase the risk of persistent placenta previa and lead to retained placenta after live birth [11–17]. Therefore, early first-trimester ultrasound assessment and placental location diagnosed can reliably predict the location and disorder of placenta [18].

In spite of eccentric implantation was frequently described by early pregnancy ultrasound examination, there remained limited studies and the outcomes of these pregnancies were still in doubt. The purpose of this study was to retrospectively assess first-trimester ultrasound parameters associated with pregnancy outcomes in women with eccentric implantation identified in the first trimester.

Materials and methods

This was a retrospective study performed at Shandong Province Maternal and Child Health Care Hospital Affiliated to Qingdao University between July 2017 and December 2022. This study was approved by the Ethics Committee of Shandong Province Maternal and Child Health Care Hospital Affiliated to Qingdao University.

We selected all cases with intrauterine gestational sac eccentrically implanted in first-trimester ultrasound imaging from our hospital ultrasound database. Patients included for study were those who met the following proposed criteria: 1) Nonanomalous uterus: not unicornuate, bicornuate, or septate; 2) Gestational sac in the lateral angle of the uterine cavity and completely surrounded by circumferential endometrium. The shape of uterus was regular and there was no bulge protruding outward from uterine angle (Figure 1).

Figure 1. Red arrow showed the gestational sac in lateral upper angle of uterine cavity and yellow arrow showed the endometrium line sign extending from the gestational sac to the endometrial cavity. Green arrow showed the myometrial thickness from the gestational sac to the outer border of the uterus. Blue arrow showed the longitudinal images of the implantation.

And then, we conducted a case-control study with matched pairs (1:1). Control cases with normal intrauterine gestational sac implanted in the uterine cavity undergoing first-trimester ultrasound imaging at the same day were included in the study. Demographic and obstetric data were collected through data extraction of the electronic medical record at the time of delivery admission. Those who delivered at outside institutions, gestational age < 28 weeks, angular pregnancy, Cesarean scar pregnancy, cervical pregnancy and multiple pregnancy were excluded.

The primary outcome was the occurrence of retained placenta during delivery. Though a placenta is deemed retained if not expelled within 30 min postpartum, waiting a prolonged amount of time before removing the placenta may lead to postpartum hemorrhage. Therefore, the diagnosis of retained placenta was made by the most senior physician in the labor and delivery ward at the time. Retained placenta included the need for manual placental removal and partial placental evacuation requiring manual removal. Baseline characteristics (including age, gestational age at first-trimester ultrasound, mean size of gestational sac, gestational age of delivery), delivery outcomes (mode of delivery, blood loss, postpartum hemorrhage and postpartum ultrasound imaging) were also collected and analyzed. All methods were carried out in accordance with relevant guidelines and regulations.

Statistical analysis

The statistical analysis of the data was conducted using SPSS, version 26.0. Data are presented as mean ± standard deviation (SD) or median (interquartile range) for continuous variables, and as frequency or percentage for categorical variables. For baseline characteristics analysis, the statistical differences were tested with t-test or one-way ANOVA for continuous variables and chi-square or fisher test for categorical variables. A logistic regression analysis was performed using R version 4.3.2 to identify independent risk factors. Risk difference (RD) and odds ratios (OR) for independent risk factors were calculated. A p-value of less than 0.05 was considered statistically significant.

Results

A total of 92 cases with gestational sac eccentrically implanted and 92 controls were selected. All the cases were reviewed and 31 women from the study group and 55women form the control group were excluded (Figure 2).

Figure 2. Flow diagram of study.

Comparison of characteristics and outcomes between the two groups was shown in Table 1. There were no significant differences with maternal age, gestational age at first-trimester ultrasound and delivery between the two groups. The mean size of gestational sac of the study group was smaller than the control group (p = 0.008). There were no significant differences with mode of delivery and blood loss between the two groups. Though 2 cases in the study group suffered postpartum hemorrhage, The risk difference for a woman with eccentric implantation to suffer postpartum hemorrhage was −0.03 (95% CI −0.08 to −0.01, not significant) and eccentric implantation did not increase postpartum hemorrhage rates (3.3% vs. 0%, not significant). The risk difference for a woman with eccentric implantation to have a retained placenta was −0.18 (95% CI −0.28 to −0.08, p = 0.000), and the incidence of retained placenta in the study group was higher than in the control group (18% vs. 0%, p = 0.006). First-trimester ultrasound imaging of eccentric implantation was also found to be an independent risk factor for the incidence of inhomogeneous mass in postpartum ultrasound imaging (27.9% vs. 10.8%, adjusted OR 0.19, 95% CI 0.05 to 0.79, p = 0.012) (Figure 3).

Figure 3. The inhomogeneous mass in lateral upper angle of uterine cavity after delivery. The red arrows showed the mass and it may be created by a decrease in the area of the placental implantation site. The yellow arrow showed the endometrium line.

Table 1. Comparison of characteristics and outcomes between the two groups.

	Study group (n = 61)	Control group (n = 37)	t/F/χ^2	p values
Age (years)	30.5 ± 3.4	29.6 ± 4.0	1.297	0.258
Gestational age at first-trimester ultrasound (weeks)	6.6 (5.7, 7.1)	6.7 (6.3, 7.4)	2.288	0.13
Mean size of gestational sac (mm)	16.8 ± 8.3	21.5 ± 8.3	7.227	0.008
Gestational age at delivery (weeks)	39.0 ± 1.5	39.1 ± 2.0	0.21	0.648
Mode of delivery			2.514	0.113
Vaginal delivery, n (%)	33 (54.1)	26 (70.3)
Cesarean section, n (%)	28 (45.9)	11 (29.7)
Retained placenta, n (%)	11 (18)	0 (0)		0.006^a,b
Blood loss (ml)	316.7 ± 122.3	284.1 ± 52.4	2.367	0.127
Postpartum hemorrhage, n (%)	2 (3.3)	0 (0)		0.525^a,b
Inhomogeneous mass in postpartum ultrasound imaging, n (%)	17 (27.9)	4 (10.8)	3.98	0.046^b

^a The statistical differences were tested with fisher test and statistical significance was set at p < 0.05.

^b Risk difference (RD) and odds ratios (OR) for independent risk factors were calculated. For a woman with eccentric implantation, the RD to have a retained placenta was -0.18 (95% CI -0.28 to -0.08, p = 0.000), the RD to suffer postpartum hemorrhage was -0.03 (95% CI -0.08 to -0.01, p = 0.150) and the adjusted OR to have an inhomogeneous mass in postpartum ultrasound imaging was 0.19 (95% CI 0.05 to 0.79, p = 0.012).

Discussion

In this study, the cases included were only described as eccentric implantation pregnancy in first-trimester ultrasound imaging. Though there was no agreed sonographic criteria for angular pregnancy, the gestational sac of eccentric implantation was usually considered to be implanted more closer proximity to the uterine cavity than angular pregnancy [19,20]. We excluded the suspecting angular pregnancy because angular pregnancy was also often used interchangeably with interstitial pregnancies and must be with retention of the placenta in the uterine angle at the time of delivery.

There were many implantation sites to be described by an early pregnancy ultrasound examination when gestational sac implanted within the uterine (endometrial) cavity due to the triangular-shaped uterine cavity. Low and eccentric implantation was the most common ultrasound findings except normally sited pregnancies. The disorder of placenta was usually associated with the implantation sites. Low implantation and angular pregnancies led to placenta previa or retained placenta [11–17].

In our study, we found that the incidence of retained placenta in first-trimester ultrasound imaging of eccentric implantation pregnancies was 18%, higher than normal implantation pregnancies. We speculated about the main reason for retained placenta in our study was that the retained placenta was incarceration in the uterine angle at the time of delivery. After fetal delivery, the uterus consists of an almost solid mass of muscle spontaneously contracts, the eccentric implanted placenta was forced proximity to the lateral upper angle of the uterine cavity, and then the placenta was incarceration (Figure 4). In clinical practices, when suspecting and diagnosing retained placenta, the location of gestational sac at the first-trimester ultrasound imaging should be reviewed. Practices within suspecting and diagnosing retained placenta with eccentric implantation may be broadly considered as either physiological or active management. In contrast, the placenta must be hardly pulled out of upper-lateral angle of uterine cavity with the uterus contraction.

Figure 4. We speculated about the reasons for retained placenta in our study. a) showed that the placental implantation site in upper-lateral angle of uterine cavity after birth of the infant. b) showed placental spatial relations after birth. The placenta was forced to protrude into upper-lateral angle of uterine cavity after the uterus spontaneously contracted.

This procedure can explain the results of prior studies. There are no enough robust to draw firm conclusions for the risk factors of non-adherent retained placenta after vaginal delivery and retained placenta can occur without identifiable antepartum risk factors [9,21]. Our study also confirmed that the results of the other prior studies. Lateral and fundal placental localization was more commonly associated with the retained placenta [22] and anterior placental location did not increase the risk of retained placenta in women with a previous cesarean section [7,8,23].

Though the incidence of postpartum hemorrhage did not increase in the eccentric implantation pregnancies in our study, there were still 2 women who suffered postpartum hemorrhage. The results were similar to prior study. It is reported that postpartum blood loss does not correlate with third stage duration in women with retained placenta [24]. In spite of the results, a remained placenta was, furthermore, present in the majority of most severe cases with postpartum hemorrhage [25].

There are also some interesting secondary results in our study. We found that the mean size of gestational sac of the study group was smaller than control group. The implantation sites may associate with the growth of gestational sac. Further study should be focused on this in detail.

The strengths of this study are its case-control design. Retrospective collection of cases has enabled us to exclude obstetric interventions. This is the first study investigating the association between first-trimester ultrasound imaging of eccentric implantation and retained placenta. In clinical practice, first-trimester ultrasound imaging should be taken into consideration when suspecting and diagnosing retained placenta. The main limitation of this study is not prospective sampling and sample size which may make it underpowered. We did not find an agreed sonographic criteria to distinguish the angular pregnancy and eccentric implantation pregnancy. Some angular pregnancies may be included.

First-trimester ultrasound imaging of eccentric implantation was associated with an increased risk of retained placenta and procedure of manual removal or extraction with ring forceps in third stage of labor. Agreed sonographic criteria should be provided to improve terminology for angular pregnancy and eccentric implantation pregnancy description on ultrasound. Careful history-taking and clinical judgment should be taken into consideration when suspecting and diagnosing retained placenta, especially the location of gestational sac at the first-trimester ultrasound imaging. The risks of eccentric implantation at the first-trimester ultrasound imaging should be discussed with pregnancy women in prenatal care including the retained placenta and the use of manual removal or extraction with ring forceps. An early pregnancy ultrasound examination should be used to confirm the location of pregnancy and to evaluate whether a normally implanted pregnancy has the potential of further development beyond the first trimester.

Acknowledgement

We thank all women who participated in this study and all the research staff.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Availability of data and materials

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

Additional information

Funding

The author(s) reported there is no funding associated with the work featured in this article.