Placental mesenchymal dysplasia with battledore insertion of the umbilical cord and retroplacental hematoma: a case report

¹Team of Congenital Anomalies Research, Faculty of Medicine and Pharmacy, Mohammed V University in Rabat, Rabat, Morocco, ²Department of Pathology, Ibn Sina University Hospital Center IBN SINA in Rabat, Rabat, Morocco, ³Unit of Dysmorphology and Congenital Anomalies, Pediatrics Department II of the Children's Hospital, University Hospital Center IBN SINA in Rabat, Rabat, Morocco, ⁴Department of Obstetrics and Gynecology, Oncology and High-Risk Pregnancies, Maternity Hospital Souissi, University Hospital Center IBN SINA in Rabat, Rabat, Morocco

^&Corresponding author
Chaimae Hilali, Team of Congenital Anomalies Research, Faculty of Medicine and Pharmacy, Mohammed V University in Rabat, Rabat, Morocco

Introduction    

Placental mesenchymal dysplasia (PMD) is an uncommon placental vascular abnormality with an estimated incidence of 0.02%. However, it's difficult to determine precisely because the term "placental mesenchymal dysplasia" has only been used since the 1990s [1]. Macroscopically, PMD is characterized by placentomegaly and cystic vesicles. Microscopically, it shows dilated, avascular stroma in the villi, chorangiomatosis, and mesenchymal hyperplasia without trophoblastic hyperplasia [2]. Placental mesenchymal dysplasia must be differentiated from hydatidiform mole, which shows syncytiotrophoblastic hyperplasia, cisterns within molar villi, and typically results in an absent or deformed fetus. In contrast, PMD is characterized by pseudocysts rather than true molar cysts, and often has a normal fetus with prolonged gestation without considerable maternal morbidity [1]. Nonetheless, PMD is linked to maternal and neonatal complications, including intrauterine growth restriction (IUGR), preterm delivery, and premature rupture of membranes. Intrauterine fetal death (IUFD), Beckwith-Wiedemann Syndrome (BWS), a hepatic tumor, and infrequently, an omphalocele without BWS [2,3]. Placental mesenchymal dysplasia is also frequently associated with umbilical cord abnormalities, such as marginal insertion. Battledore placenta, where the umbilical cord inserts at the placental margin, occurs in 7%-9% of singleton births and 24%-33% of twin pregnancies and may lead to reduced perfusion and adverse outcomes [4]. Herein, we report a case of PMD in a 42-year-old Moroccan woman with a history of three miscarriages, initially suspected as a partial molar pregnancy, presenting with clinical signs of placental abruption and a favorable pregnancy outcome. Additionally, we provide a brief review of the literature to help share knowledge and raise awareness of this pathology in our context.

Patient and observation     

Patient information: we report the case of a 42-year-old Moroccan woman, gravida 4, para 1, with no known medical history (she has no known general pathology, such as diabetes and/or hypertension), who was operated on for a cervical polyp. Her obstetrical history included three miscarriages at 2, 1.5, and 1 month, the causes of which are unknown due to the unavailability of complete clinical data on the patient, and the current pregnancy was not being monitored. Genetic analysis revealed normal results, with no evidence of androgenetic/biparental mosaicism (ABM) or other genetic abnormalities.

Clinical findings: the patient had a blood pressure of 110/70 mm Hg (systolic blood pressure of 110 mm Hg and diastolic blood pressure of 70 mm Hg) and a temperature of 37°C. She exhibited uterine contractions and black bleeding, raising suspicion of a retroplacental hematoma. This was suggestive of placental abruption and posed a threat of premature delivery. Ultrasound findings initially suggested a partial molar pregnancy due to an enlarged placenta with multiple cystic areas and a hypoechoic retroplacental zone.

Timeline of current episode: at 34 weeks and 5 days of gestation, the patient presented with symptoms of uterine contractions and black bleeding, raising concerns about a retroplacental hematoma and a potential threat of premature delivery. The pregnancy had been misdiagnosed earlier as a partial molar pregnancy based on abnormal ultrasound findings, which persisted due to the lack of regular prenatal monitoring. Following her admission to the labor ward, an emergency caesarean section was performed, resulting in the delivery of a live male premature newborn weighing 2250g with a pink-toned reactive appearance. The fetal Apgar scores at birth were 7, 8, and 9. A retroplacental hematoma was confirmed intraoperatively, and the newborn was admitted to the neonatal unit for respiratory distress. Post-delivery, the placenta was sent from the Gynecological and Obstetrical Department to the Department of Pathology for histopathological examination.

Diagnostic assessment: the histopathological examination revealed significant abnormalities. Macroscopic examination showed that the placenta was thickened and very voluminous for gestational age, measuring 2x18 in length and 5 cm in thickness and weighing 890g, which was twice as much as normal values (400/415g), indicating placentomegaly. The remaining umbilical cord was sent to the department of pathology with a length of 44cm and a diameter of 1cm, as well as a marginal insertion (battledore) (Figure 1 A), coiled and a little yellow in appearance, with two arteries and one vein on the section. The very large, dilated, thrombosed, and tortuous chorionic vessels, giving a varicose appearance (Figure 1 B), were observed in the chorionic plate (Figure 2 A). The basal plate (Figure 2 B) was shredded, resulting in a "hairy" appearance and the presence of vesicles. After 24 hours of fixation in 10% buffered formalin, examination of the slices of the sections taken revealed large thrombosed and dilated chorionic vessels (Figure 3 A), as well as the presence of numerous old and recent foci of infarcts (Figure 3 B), and the existence of several cystic cavities with clear viscous contents (Figure 3 C). Several samples were taken from macroscopically normal apparent tissue and pathological sites. Histological examination of the placenta revealed, according to the consensus statement of the Amsterdam Placental Workshop Group, the presence of maternal vascular malperfusion (MVM) lesions represented by zones of chronic (old) and acute (recent) extensive infarcts (Figure 4 A) and retroplacental hematoma at the basal plate (Figure 4 B).

The cystic cavities with viscous contents observed macroscopically correspond histologically to pseudocysts of the villous stems (Figure 4 C), resembling the cisterns of the molar villi. However, syncytiotrophoblastic hyperplasia, a key feature of hydatidiform mole, was absent in this case. In addition, lesions of fetal vascular malperfusion (FVM) are frequent, in the form of vascular thrombosis (Figure 5 A); vascular ectasia (Figure 5 B), in which the vessels are thick-walled, highly ecstatic, and dilated; areas of avascular villi (Figure 5 C), fibrous, surrounded by a crown of fibrinoid substance that occupies the intervillous space; and chorangiosis (Figure 5 D), which is represented by intense congestion of the villi and an increase in vascular sections. However, there are inflammatory lesions that is associated with PMD, represented specifically by acute fetal inflammatory response stage 1 (umbilical phlebitis) (Figure 6 A) and stage 3 (necrotizing funisitis) (Figure 6 B). Additionally, the histological examination of the placenta revealed the presence of hyperplasia of the amniotic membranes (Figure 6 C), and the ischemic necrosis lesions with fibrinoid deposition (Figure 6 D). The practice of anatomopathological examination of the placenta faces several challenges, including limited interest among practitioners, lack of standardization in histological reporting, and insufficient multidisciplinary consultation. Additionally, there is a lack of available data for monitoring the pregnancies of patients before their hospitalizations, the unrepresentative sample, and the absence of national standardized curves adapted to our population.

Diagnosis: histopathological findings confirmed the diagnosis of this case as PMD.

Follow-up and outcome of interventions: postoperatively, the patient recovered without significant complications. She received routine follow-up care. The premature newborn was admitted to the neonatal unit due to respiratory distress. Despite the initial challenges, the newborn responded well to supportive neonatal care.

Patient perspective: the patient's recovery without significant complications pleased the patient.

Informed consent: it was obtained from the patient for publication.

Discussion     

Placental mesenchymal dysplasia is an increasingly recognized placental anomaly. Most cases of PMD have no definite clinical manifestation; it is most commonly confused with a partial mole in early pregnancy, particularly on ultrasound examination [1]. While this present case, with a live foetus, it was initially misdiagnosed as a partial molar pregnancy based on ultrasound findings. However, the placental macroscopic examination of the case revealed the identification of the grape-like vesicles and, histologically, large cystic stem villi with cisterns without syncytiotrophoblastic hyperplasia, as well as the identification of distinctive vascular anomalies, enabling the diagnosis of PMD to be confirmed rather than molar pregnancy. Placental Mesenchymal Dysplasia is a rare placental vascular and connective tissue anomaly, often associated with serious foetal and/or maternal complications [3]. There is an association between PMD and placental abruption. In this case, there was a suspicion of a retroplacental hematoma suggestive of placental abruption, which was confirmed by macroscopic and microscopic examination of the delivered placenta. The literature on this topic is limited. Ferreira C et al. [5]. Illustrate a case of bad outcome and postnatal histological diagnosis of PMD with several maternal and fetal complications. An ultrasound scan revealed IUGR and placentomegaly with a heterogeneous, hypoechoic retroplacental zone, leading to an urgent caesarean section due to suspected placental abruption. Sheeja S et al. [6] investigated the histological characteristics of PMD in two distinct cases with distinct disease outcomes: one in the context of UIFD and the other in the context of live birth. A large placenta with numerous vesicles and mesenchymal dysplasia was observed in both cases during the placental examination. Retroplacental clots were observed in one case. The two cases showed focal areas of chorangiosis and retroplacental hemorrhage. The diagnosis of PMD has been confirmed by all of these observations.

Macroscopically, the placenta in the current case, as well as in the literature, generally shows placental hypertrophy, or placentomegaly, with cystic cavities interspersed with normal parenchyma, mimicking a partial mole. The chorionic vessels are tortuous, dilated, and may be thrombosed or have aneurysms [2]. Allias et al. [7] also found that its basal plate is often a little shredded, resulting in a "hairy" appearance of the placenta. PMD is often associated with various umbilical cord abnormalities, including abnormal cord insertion, excessive cord length, a tortuous spiral, and a single umbilical artery [4]. It is possible that abnormal umbilical cords may contribute to the vascular anomalies in PMD [4]. In this case, the umbilical cord had a battledore insertion. Histologically, the current findings were consistent with those of some previous studies showing that the placenta with PMD generally reveals enlarged, oedematous stem villi. Moderately to severely ectatic thick-walled vessels with fresh or mature thrombi obstructing the arterial and venous lumens, as well as fibromuscular hyperplasia. The cystic cavities with clear viscous contents observed macroscopically correspond histologically to pseudocysts within the villous stems, resembling the cisterns of the molar villi [2,7].

In certain instances, there are MVM lesions characterized by intervillous thrombosis or infarcts, although they are infrequent and relatively extensive [7]. In this present case, however, there were extensive chronic and acute infarcts, as well as a retroplacental hematoma. Similarly, several previous studies have linked PMD to infarcts [6,8]. Furthermore, vascular malformations associated with PMD may constitute a form of congenital mesodermal malformation, and there may be a correlation to simultaneous mesodermal abnormalities in the newborn, such as hepatic and cutaneous hemangiomas [2,3]. In addition, umbilical cord insertion anomalies cause foetal hypoxia, which can lead to placental remodelling such as hypervascularisation (chorioangiomas and chorangiosis) [2,4], in the current case, we observed chorangiosis, which is characterized by the presence of more than 10 capillaries per terminal villi in 10 villi in many regions of the placenta. Another study additionally found an association between chorangiosis and PMD [6]. Moreover, the case presents inflammatory lesions that are associated with PMD, represented specifically by the acute fetal inflammatory response stage 1 (umbilical phlebitis) and stage 3 (necrotizing funiculitis). Additionally, hyperplasia of the amniotic membranes, and ischemic necrosis lesions with fibrinoid deposition are also present.

Furthermore, the present case involved a male fetus, which might have contributed to the favourable outcome. Literature suggests that PMD affecting a male infant could involve different mechanisms leading to a better outcome, potentially due to male-specific placental functions and DNA methylation patterns [9,10]. Given that PMD typically shows a female predominance and poor outcomes, it is plausible that PMD involving a male infant might have distinct aspects compared to the more common PMD cases involving female infants [9]. These differences might be related to sex-specific features of the placenta [9]. It is established that there are sex-specific differences in fetal growth and survival, likely due to variations in gene, steroid, and protein expression in the human placenta [9]. In adverse maternal environments, male placentas tend to prioritize continuous growth, which may help mitigate growth restriction, even though they are more vulnerable to adverse conditions. Female fetuses, in contrast, often exhibit adaptive responses that prioritize survival over growth, potentially leading to increased incidence of IUGR in female infants with PMD [9]. Furthermore, discussions on PMD pathogenesis include considerations of genomic imprinting and DNA methylation, with some reports highlighting sex-related differences in the sensitivity to DNA methylation and fetal sex differences in placental DNA methylation [10]. These morphological features of the placenta supported the diagnosis of this case as PMD, underscoring the importance of accurate diagnosis and management to mitigate potential risks and ensure the success of subsequent pregnancies.

Conclusion     

This case emphasizes the importance of accurately diagnosing PMD through detailed histological evaluation to distinguish it from molar pregnancies, particularly by identifying pseudocysts without syncytiotrophoblastic hyperplasia and complex vascular anomalies. It also underscores the association of PMD with retro-placental hematoma, marginal cord insertion, and acute fetal inflammatory response, highlighting the complexity of this condition. The key takeaway from this case is the need for thorough placental assessment to ensure appropriate management and prognosis in both current and future pregnancies. Early prenatal recognition of PMD could prevent unnecessary interventions such as abortions.

Competing interests     

The authors declare no competing interests.

Authors' contributions     

Patient management: Chaimae Hilali. Data collection: Chaimae Hilali. Manuscript drafting: Chaimae Hilali. Manuscript revision: Chaimae Hilali, Asmaa Mdaghri Alaoui, Najat Lamalmi and Mounia Yousfi Malki. All authors have read and approved the final version of the manuscript.

Figures     

Figure 1: the fresh appearance of the placenta after delivery: A) varicose dilation and thrombosis of chorionic vessels; B) umbilical cord with marginal insertion (battledore)

Figure 2: chorionic and basal plate of the placenta: A) chorionic plate of placenta; B) basal plate of placenta

Figure 3: placental section slices after fixation: A) thrombosed and dilated chorionic vessels; B) old and recent infarcts; (C) cystic cavities with clear viscous contents

Figure 4: histological lesions of maternal vascular malperfusion: A) infarct; B) retroplacental hematoma; C) pseudocysts of the villous stems

Figure 5: histological lesions of fetal vascular malperfusion: A) vascular thrombosis; B) highly ectasic and dilated chorionic vessels; C) avascular villi; D) chorangiosis

Figure 6: histological lesions of fetal inflammatory response and others placental abnormalities: A) acute fetal inflammatory response stage 1 (umbilical phlebitis); B) acute fetal inflammatory response stage 3 (necrotizing funisitis); C) hyperplasia of the amniotic membranes; D) ischemic necrosis lesions with fibrinoid deposition

References