Placenta accreta spectrum (PAS), an abnormal placental attachment induced by the invasion of placental villi into the myometrium, is a life-threatening severe obstetric disease [1, 2, 3]. Placenta previa covers the endocervical os. In China, the frequency of PAS associated with placenta previa increases annually, with the risk of a second cesarean delivery reaching as high as 3.4% in some cases [4].

The risk of intraoperative bleeding in PAS with placenta previa is substantially higher than that in placenta previa alone. According to Bailit et al. [5], the median estimated intraoperative blood loss of PAS is 2000 mL, reaching 8000 mL in emergency surgeries. Several models have been developed to predict significant intraoperative bleeding and massive blood transfusions in obstetric patients [6, 7, 8, 9, 10]. However, these models are mainly based on patients with placenta previa, and the risk variables derived from them are inconsistent [11]. A few studies linked massive bleeding with PAS to the post-placental clear space, cross-border blood vessels in the region of sub-placental vascularity, interruption or disappearance of the bladder line, and the presence of the cervical blood sinus [4, 12].

Study has associated placental thickness (PT) in the lower uterine segment with PAS [13]. Predictive models for PAS include PT as a risk factor [14]. Another study suggested that PT exceeding 5 cm may be associated with intraoperative bleeding $>$2000 mL in patients with PAS; however, the authors concluded that it was not an independent risk factor [4]. Whether an increased PT is associated with severe intraoperative bleeding in patients with PAS and placenta previa remains unclear, and research to date on this topic is limited. Therefore, this study investigated the relationship between PT and the risk of major bleeding in patients with PAS and placenta previa to determine which patients were at greater risk of intraoperative major bleeding.

This retrospective cohort study included 317 patients with suspected PAS and placenta previa and examined the independent association between PT and intraoperative hemorrhage. Our study found that an increasing PT was associated with an increased risk of massive bleeding in patients with PAS placenta previa who underwent CS. We found that PT was significantly increased in patients with massive bleeding. To the best of our knowledge, this is the first study to report the association between PT and massive bleeding in patients with PAS and placenta previa.

Curve fitting revealed that intraoperative bleeding increased as PT increased. The relationship between PT and intraoperative hemorrhage was linear. In the subgroup analyses, the correlation between PT and the risk of major bleeding was not statistically different. This further suggests that the risk of major bleeding is related to the PAS type, with higher PT values predicting a higher PAS grade. When it can be accurately determined preoperatively, PT can assist in determining the risk of intraoperative hemorrhage.

Massive bleeding is the major cause of preventable peripartum mortality. As much as 70–93% of these deaths are deemed preventable [20]. A rapid diagnosis and early multidisciplinary management can improve the maternal prognosis. The early identification of the risk of hemorrhage facilitates appropriate preoperative countermeasures such as cross-matching, establishing extensive venous access, and autologous blood recovery [21, 22]. Most cases of massive bleeding during CS are caused by placental abnormalities. These risk factors include maternal history and placental characteristics observed on ultrasonography [23]. The clinical features included maternal age, gestational age 37 weeks, preoperative bleeding, number of prior CS, PAS, a sponge-like appearance of the cervix, grade of lacunae, presence of a hypoechoic layer, depth of the placenta invading the uterine muscle wall, and an anterior placenta. Most of these features are used to diagnose PAS.

However, different PAS scores are associated with different bleeding risks. Wang et al. [4] showed that the risk of intraoperative hemorrhage in PAS is associated with the post-placental clear space, cross-border blood vessels in the region of sub-placental vascularity, interruption or disappearance of the bladder line, and presence of the cervical blood sinus. These ultrasound features are specific to some patients with PAS and not universal. An experienced sonographer may obtain these indicators; however, subjective factors cannot be excluded [13]. When diagnosed with suspected PAS, a more objective indicator for predicting the risk of major bleeding is needed.

Many studies have used PT to predict fetal and maternal health [24, 25]. The condition of the placenta can be a predictor of many events that occur in the mother and fetus [26]. Another study demonstrated a correlation between the PT and neonatal weight [27]. Li et al. [28] showed a correlation between PT and PAS. A threshold of 4.5 cm can help screen for patients with placenta previa and risk factors for PAS. There was a trend toward an increased PT in patients with different PAS types. PT was significantly greater in the penetrating PAS group than in the other two types. This may be related to an increased number of lacunae in the placenta. When more severe placental implantation occurs, lacunae of varying sizes develop within the placenta, thereby increasing the PT. The proportion of intra-placental lacunae increases with the degree of placental implantation. An increase in PT suggests a significantly higher likelihood of implantation or penetration. The underlying cause of an abnormally thick PT in women with PAS is unclear. However, this may be related to poor vascularization of the lower uterus and cervix as well as placental implantation in the cesarean scar, which limits placental migration [29]. One study showed that antenatally measured PT has a linear correlation with blood loss in patients with PAS [30]. Our study confirmed this finding. An increased PT suggests increased placental implantation and invasion into the myometrium and corresponding vessels. This may affect uterine contractions and complicate surgical hemostasis when the placenta peels off.

This study has some limitations. Moreover, it is limited by factors that limit all retrospective designs such as confounders and selection bias. The study was retrospective; therefore, PT was not measured prospectively. All ultrasound-related metrics were obtained by reviewing the patients ultrasound reports; therefore, some of the ultrasound metrics were not presented in the ultrasound reports, such as intraplacental hypoechogenicity. Therefore, relevant indicators were not included in the regression model, which may have been a confounding factor affecting the final results.

In conclusion, an increased PT in the lower uterine segment is associated with intraoperative hemorrhage in patients with PAS and placental previa. Preoperatively, an increased PT can provide an indicator for the assessment of intraoperative bleeding risk. The risk of intraoperative hemorrhage was significantly higher in the higher PT (Q4) than lower PT (Q1) group. A thickened PT seems to be a warning sign of massive bleeding during surgery for PAS with placenta previa.

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

FH participated in the design of the study, data collection and analysis, and manuscript drafting. JW and KW designed the study and drafted and revised the manuscript. TY, WW, YX, QLX, QJX, and JZ acquired and interpreted the data and followed the patients. QJX and JZ performed the data analysis and interpretation. All authors have read and approved the final version of the manuscript. All authors contributed to the editorial revision of the manuscript and agreed to take responsibility for all aspects of this work.

Ethical approval was obtained from the Ethics Committee of First Affiliated Hospital of Chongqing Medical University (approval number: 2021–059). All procedures were performed in accordance with the principles of the Declaration of Helsinki. The Ethics Committee of the First Affiliated Hospital of Chongqing Medical University waived the requirement for informed consent. The medical records used in this study were obtained from previous diagnoses and treatments. Exemption from informed consent will not adversely affect the rights or health of the subjects. The participants’ privacy and personal identities were protected.

Not applicable.

This research received no external funding.

The authors declare no conflict of interest.