Cesarean scar pregnancy

Cesarean scar pregnancy (CSP) is an abnormal implantation of the gestational sac in the area of the prior caesarean delivery (CD) scar, potentially leading to life-threatening complications, including severe haemorrhage, uterine rupture and development of placenta accreta spectrum (PAS) disorders (1). CPS is generally considered a peculiar type of ectopic pregnancy, although within the uterine cavity and can result in a liveborn infant if first and second trimester complications do not occur, despite the large majority of women with this condition develop PAS.
CSP is not a unique condition but encompasses different clinical phenotypes according to the size of the prior cesarean delivery (CD) scar, degree of implantation of the gestational sac in the area of the scar and residual myometrial thickness.

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The estimated incidence of CSP is approximately 1:1800-1:2000 pregnancies after CD (1).  However, the incidence of CSP varies widely in the published literature as there is currently no large population study assessing the occurrence of CSP in all women with prior CD. 

A prerequisite for the occurrence of CSP is the presence of cesarean scar defect which can result in defective decidualization and predispose to the abnormal implantation of the gestational sac (2,3). The risk of CSP increase with increasing number of prior CD. It is suggested that decidual defect following the iatrogenic creation of a CD scar has an adverse effect on early implantation of the pregnancy, although the actual reason for the implantation of the gestational sac in the area of a prior CD scar is yet to be determined.  (3-5,3)
Several risk factors may predispose a woman to persistent uterine scar defect after CD. The type of uterine closure of the incision is controversial. A recent systematic review reported that the incidence of the niche or defect formation in a subsequent pregnancy is similar for single- and double-layer closure following a CD (6). Other reported risk factors for CSP are CD during second stage of labor, retroflexed uterus, gestational diabetes, increased maternal body mass index, perioperative fever and infection and myomectomy. (5-8)

CSP has been associated with a multitude of adverse short and long terms outcomes such as massive haemorrhage, uterine rupture and need for hysterectomy and the occurrence of placenta accreta spectrum (PAS) disorders. Despite these associations, the natural history of CSP is not well established, as previously published studies reported mainly cases undergoing treatment or those with a retrospective diagnosis of the anomaly after the occurrence of an adverse outcome, such as maternal hemorrhage or uterine rupture.
A recent systematic review on the outcomes of CSP when managed expectantly have demonstrated that in cases with fetal or embryonic heartbeat detected at the time of the diagnosis of CSP, 13% of women experienced an uncomplicated miscarriage, 20% required medical intervention. Uterine rupture during the first or second trimester of pregnancy occurred in 10% of cases, while hysterectomy was required in 15% of all cases. Of note, 77% of cases progressed to the third trimester of pregnancy, of whom 39% experienced severe bleeding. Finally, 75% had a surgical or pathological diagnosis of PAS at delivery and around two-thirds of them had placenta percreta. In women with CSP but no embryonic/fetal cardiac activity, an uncomplicated miscarriage occurred in 69% of cases, while surgical or medical intervention during or immediately after miscarriage was required in 31%. Uterine rupture during the first trimester of pregnancy occurred in 13% of cases, but hysterectomy was not required in any case (9). 

CSP has similar histopathological characteristics to those seen in pregnancies with PAS disorders. Such association was first described in a study by Timor-Tritsch et al reporting that blinded analysis of anatomical specimen from CSP and PAS had the same histopathological features of placenta accreta (10,11)
A document devoted to providing the necessary steps towards consistency in the definitions of CSP and PAS markers and the approach to their accurate antenatal diagnosis to optimize maternal and fetal outcomes was published relying on the pathology and pathophysiology (12)

Prenatal diagnosis of CSP implies a careful evaluation of the relationship between the gestational sac and the prior CD scar (1). The following diagnostic criteria should be fulfilled: 
•    Empty uterine cavity
•    Gestational sac or solid mass of trophoblast located anteriorly at the level of the internal os embedded at the site of the previous lower uterine segment caesarean section scar.
•    Thin or absent layer of myometrium between the gestational sac and the bladder.
•    Evidence of prominent trophoblastic/placental circulation on Doppler examination.
•    Empty endocervical canal (Figure 1a-m, video 1a-g)
The best imaging modality to diagnose a CSP is transvaginal ultrasound with a partially full bladder which allows a more objective assessment of the relationship between gestational sac implantation and the myometrium. First trimester MRI does not seem to add substantial information for the diagnosis and for the stratification of the severity of CSP.
Gestational age at ultrasound has also significant impact on the detection rate of CSP. Prenatal diagnosis of CSP is easier in the early first trimester of pregnancy (<9 weeks of gestation). With advancing gestation, the upper pole of the gestational sac grows toward the uterine fundus thus making prenatal identification of CSP more challenging (Figure 2, a-c) (10) This makes the assessment of the low implantation of the gestational sac more difficult to detect (13,14). However, as the GS extends to the fundus, the placenta is still “in the Niche” of the prior scar, making this is a useful marker for the diagnosis of PAS in the late first trimester (15)
Few studies have addressed the use of ultrasound in predicting the severity and the risk of short- and long-term morbidities in women affected by CSP. 
The most reported are:
•    “In-the-niche vs on-the-scar classification”. It refers to the shape of the CD scar and to the type of placenta location and implantation in such area.  “In-the-niche” refers to the placenta implantation into a deficient or dehiscent scar. Conversely, the definition for “on-the-scar” is that the placenta implanted partially or fully on top of a well-healed scar (Figure 3, a-b). (16) Kaelin Agten et al. reported that women with CSP implanted “on-the-scar” had a substantially better outcome compared with those in whom the CSP was implanted “in-the-niche.”. All women with a good outcome had a myometrial thickness of 4mm or more in their first trimester scan. In contrast, myometrial thickness in that one patient with CSP “on the scar” who developed PAS measured only 2mm
•    Cross-over sign. It refers to the relationship between the antero-posterior diameters of gestational sac and the CD scar (17,18). In a sagittal view of the uterus, a straight longitudinal line was drawn connecting the internal cervical os and the uterine fundus through the endometrium (endometrial line) (Figure 4, a-d). Then the gestational sac is identified and its superior-inferior (S-I) diameter perpendicular to the endometrial line traced. According to the relationship between the endometrial line and the S-I diameter of the ectopic sac, we divided the patients into two different groups: 
1.    COS1 insertion: when the gestational sac was implanted within the previous CS and ≥ two thirds of the S-I diameter of the gestational sac was above the endometrial line towards the anterior uterine wall 
2.    COS2 insertion: when the gestational sac was implanted within the previous CS and < two thirds of the S-I diameter of the gestational sac was above the endometrial line. Furthermore, these cases were divided into two different categories according to the presence (COS2+) or not (COS2-) of an intersection between the S-I diameter of the ectopic sac and the endometrial line.
Cali et al reported that women with COS-1 had a higher mean estimated blood loss, number of packed red blood cell units required during or after the operation and a higher risk of progressing towards the most severe types of PAS disorders, mainly placenta percreta, compared to COS-2.

“Above vs below-the midpoint of the uterus-line”: It refers to the relative location of the center of gestational sac to the midpoint of the uterus along a longitudinal line between the external cervical os and the uterine fundus (19). In a sagittal plane of the uterus, a straight longitudinal line is drawn connecting the external os of the cervix and the uterine fundus. The distance between the cervix and the fundus is measured, representing the uterine size (distance A). On the same image the midpoint section of the uterine size is marked by a line that transected the above line by half at 90 degrees (midpoint of uterus). Then, the external cervical os and the centre of the gestational sacs is visually determined and marked. The distance from the external cervical os to the centre of the gestational sac (distance B) is measured using the protractor. This represented the distance and the location of the sac in relation to the cervix and is termed “cervix-to-centre-of-sac distance”. The distance between the centre of gestational sac and the midpoint axis of the uterus is then calculated (B-M). The most distant edge of the gestational sac from the external cervical os is also marked to calculate the distance from the external cervical os to the most distant edge of the gestational sac. The distance from the external cervical os to the most distant edge of the gestational sac (distance C) is measured (in millimeters) using the protractor. This represented the furthest boundary of the sac in relation to the cervix and is termed “cervix-to-most-distant-edge-of-sac distance” The distance between the most distal edge of the gestational sac and the midpoint axis of the uterus is calculated (C-M) (Figure 5, a-b).
Timor-Tritsch et al. reported that the location of the center of the gestational sac relative to the midpoint axis of the uterus between 5-10 weeks of gestation differentiated between IUP and CSP (mean 17.8 vs e10.6 mm, respectively), indicating that most CSPs are located proximally to the midpoint axis of the uterus whereas most normal IUPs are located distally from the midpoint of the uterus. Using location of the center of the gestational sac as a marker of CSPs between 5-10 weeks of gestation yielded the following characteristics of diagnostic accuracy: sensitivity 93.0% and specificity 98.9%.   
When combining the three sonographic markers and placing the defining coordinates for COS-1 and sac implantation below the uterine midline and in the niche on a sagittal ultrasound image of the uterus, it is possible to identify an area that we call high-risk-for-PAS triangle (Figure 6) (19). If the center of the gestational sac is in the niche, the pregnancy is at high risk for PAS. This diagram may enable an easy visual perception and application of the three sonographic markers to prognosticate the risk for CSP and PAS disorder, although it requires validation in large prospective studies.
However, these US signs have not been tested prospectively to predict short term complications such as uterine rupture and it is not possible to differentiate women who will experience such outcome from those who will progress through the third trimester of pregnancy. The inability of prenatal imaging to accurately predict short- and long-term outcome of CSP should be emphasized during parental counselling.

There are two differential diagnostic entities of CSP: cervical pregnancy and a failed intrauterine pregnancy or miscarriage in progress “caught” by a sonogram in transition, still close to the area of the internal os or the upper cervical canal. Cervical pregnancy is a rare condition in which the gestational sac implants in the posterior cervix (Figure 7) It is important to mention that while CSP is rare, cervical pregnancy is even more so and even more importantly cervical pregnancies rarely if at all will occur in patients with previous CDs. An embryo or fetus expelled from the uterine cavity and passing through the cervical canal most of the time does not have an actively beating heart and will exhibit a to-and-fro “sliding” movement of the conceptus that can easily be differentiated from a CSP.  A true CSP does not move away if pushed with the probe. Furthermore, women experiencing miscarriage have an open internal cervical os, the gestational sac is locating in the endocervical canal and there is no evidence of peritrophoblastic blood flow. Finally, a miscarried conceptus will usually cause pain passing through the cervix, while a CSP is usually painless. 
To make it easy for the “front-line” obstetricians and gynecologists we suggest using a simple differential diagnostic ultrasound application that will help in correctly differentiating a CSP from an intrauterine pregnancy. We suggest to draw a line perpendicular to the anteroposterior, longitudinal axis of the uterus on the US picture. If the center of the gestational sac is seen below that line, closer to the cervix, it is almost sure that it is a scar pregnancy (or in rare cases a cervical pregnancy as mentioned above). If the center of the sac is above that line, closer to the uterine fundus, it is a normal intrauterine pregnancy. This algorithm performs best before 8 weeks (1).

An earliest and timely diagnosis of CSP renders the clinician the best opportunity to manage it regardless of terminating or continuing it (20).  As opposed to an early diagnosis it is never too late to change an earlier misdiagnosis and take the necessary steps to change the course of managing it.  Every effort should be made to find the earliest ultrasound pictures and retroactively re-evaluate if sonographic criteria of CSP were present.  Clinicians should be cognizant that at or after 7 gestational weeks the chorionic/gestational sac “morphs/moves” toward the uterine cavity populating it. This picture of the sac with the fetus, now seen in “the uterus” renders false reassurance to the obstetrician and thereby the patient considering the pregnancy as normal in location (Figure 2). This scenario, despite the history of a previous CD, a possible placenta previa, and the image of an anteflexed/retroverted uterus with a sac in the cavity unfortunately leads to a mistaken diagnosis and may result in complications since the real pathognomonic sign of a CSP, namely the low anterior location of the implanted placenta, the increased vascularity at the placental/bladder interface, were  not detected, or were disregarded  resulting in complications and a difficult pregnancy management.  It should be born in mind again and again that, while the gestational sac with the embryo/fetus, starting around week 7, “moves” slowly, into the uterine cavity, the “anchor” of the pregnancy, namely the placenta, stays firmly in the site of implantation rendering the pregnancy its proper name and diagnosis of being a CSP, and thus a precursor of possible placenta accreta. 

There are compelling reasons to screen for CSP in early pregnancy.  No matter if it is terminated or continued CSP is a potentially high-risk pregnancy. If terminated, the earlier it is done, the less the risk however it can still result in complications (1). We voiced our opinion for early, 5-7 weeks routine screening of patients with previous cesarean deliveries (CD) however the respective societies argued that more research is needed and that cost versus benefit calculations to institute mandated screening for CSP would be essential before making any formal recommendation (21). Of note, the Italian Society of Ultrasound (SIEGO) does clearly recommended such screening.  The Society of Maternal Fetal Medicine also recommends (but does not mandate) an US evaluation of pregnant patient with a history of previous CD (13).  The value of performing an US examination before 9 weeks gestation was also evaluated and the results clearly demonstrated that early first trimester diagnosis (<9wks) of CSP is associated with a significantly lower risk of maternal complications (14)
The two most important and necessary clinical scenarios when screening for CSP are: is the gestational sac/placenta low lying and did the patient have a previous Cesarean delivery? (17)

After prenatal diagnosis of CSP, parents should be counselled about the short and long-term risks, including uterine rupture, severe haemorrhage, and progression towards PAS disorders. Currently, there is no study which is prospectively reporting the role of ultrasound in predicting the short-term outcome of women affected by CSP. Although cases characterized by a deep implantation of the gestational sac in the area of the prior CD scar and a small residual myometrial thickness (<2 mm) are at higher risk of first and early second trimester uterine rupture, it is not completely possible to rule out this potential risk. Therefore, when a diagnosis of CSP is made and parents wish to continue pregnancy, they should be informed that uterine rupture may unexpectedly occur at any time during pregnancy. In cases where the pregnant woman opted for termination, serial ultrasound and clinical evaluation should be undertaken in order to identify signs of impending uterine rupture in a timely fashion. Second and third trimester ultrasound evaluation should confirm the presence and the severity of PAS disorders. Finally, women should be delivered in centres with high expertise in the surgical management of PAS since, although US diagnosis of PAS can be reliably achieved in centers with expertise, with an accuracy of about 90%, (22), this rate falls to 50%, mainly due to insufficient clinical suspicion and/or knowledge of risk factors.

Parents should be informed that, in cases where pregnancy termination is an option, it should be performed early in gestation. A recent systematic review assessing the role of gestational age in affecting the outcome of CSP undergoing pregnancy termination has demonstrated that a composite adverse outcome complicated 6% of CSP diagnosed at ≤9 weeks and 32% of those diagnosed >9 weeks. Massive haemorrhage occurred in 4% of women with early and in 28% of those with late first trimester diagnosis of CSP. Uterine rupture occurred in 2.5% of women with a prenatal diagnosis of CSP at ≤ 9 weeks and in 7.5% of those with CSP after 9 weeks’ gestation, while an emergency intervention involving hysterectomy was required in 4% and 16%, respectively. When computing the risk, early diagnosis of CSP was associated with a significantly lower risk (85%) of composite adverse outcome (OR: 0.14; 95 % CI 0.1-0.4) (14)

In cases where the embryonic or fetal heartbeat is not detected and CSP is diagnosed in the early first trimester of pregnancy, a follow-up ultrasound scan in one week is reasonable in order to confirm that the pregnancy is not progressing, as a significant proportion of CSP with no fetal heart activity will resolve spontaneously.
In cases where the pregnant women opted for termination and fetal heart beats are present in a CSP diagnosed in the late first trimester, treatment should be undertaken with no delay.
A large variety of treatment options applied individually or in combination for CSP has been reported in the published literature however, there are no randomized controlled trials comparing them. Furthermore, these studies are also hampered by a wide heterogeneity in gestational age at treatment and inclusion of symptomatic cases. 
The most commonly reported interventions are systemic or local injection of methotrexate in the gestational sac, uterine artery embolization, suction curettage, laparoscopic or laparotomic resection, compression through a single or double catheter balloon (23). In the collective authors’ experience, the most adopted treatments are (25-27):
1.    Compression of the CSP with a double catheter balloon, occasionally followed by uterine suction 
2.    Local injection of methotrexate in the gestational sac followed by compression of the CSP with a double catheter balloon
Follow-up after treatment of CSP includes serial US and clinical examination in order to confirm that the pregnancy has resolved. A complete resolution of CSP is confirmed by the lack of heart activity, if present, stable maternal vital signs and absence of heavy bleeding. Presence of massive vascularization weeks after treatment of CSP should raise the suspicion of the occurrence of acquired uterine artery malformation, also known as enhanced myometrial vascularity, anomalies characterized by an abnormal connection between arteries and veins, bypassing the capillary system, which may put the woman at risk of spontaneous severe haemorrhage (28)

Only few studies have explored the recurrence risk and obstetric outcome after a prior CSP. A recent systematic review of the published literature reported that CSP recurred in 18% of cases. Among women who wished to conceive, the pregnancy was achieved in 71% of cases. When considering the type of management adopted (surgical vs non-surgical), the recurrence of CSP was 21% in women undergoing surgical and 15% in those undergoing non-surgical treatment. In women experiencing an intrauterine pregnancy after a prior CSP, the rate of uterine rupture was 1.5%. Miscarriage, preterm birth and PAS disorders complicated 19%, 10% and 4% of pregnancies, respectively (28) 
There are no randomized trials investigation the prevention of CSP. Uterine dehiscence is the strongest risk factor for the occurrence of CSP. An incompletely healed scar is associated with several gynaecological symptoms, including spotting, dysmenorrhoea, chronic pelvic pain, and dyspareunia. Currently, the indication to treat uterine niche is mainly based upon the presence of such symptom and it is yet to be established whether elective repair of the niche may reduce the risk of CSP. (28)
There are numerous publications about different suture methods at the time of closure of the incision after the CD.  None so far resulted in a significant prevention of the post CD niche risk considered by many as one of the reasons that the fertilized egg implants in it. Recently, interesting data were published focusing on an “endometrial free” uterine incision closure technique that resulted in diminished niche formation. (29)
Larger clinical trials are needed to produce robust evidence on how to best manage these high-risk pregnancies.

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