and Cesarean Scar
Costs of the Rising
Cesarean Section Rate
The cesarean delivery rate in the United States rose to 31.1% of all births in 2006,1an
increase over the 2005 rate and another consecutive record high. The percentage of
all births delivered by cesarean section has climbed 50% over the last decade from
a nadir of 20.7% in 1996. Although the risks to women during the current pregnancy
from cesarean section may not be excessive when compared with those associated
with vaginal delivery, the risks to subsequent pregnancies are not given enough con-
sideration in the risk-benefit calculus when determining the route of delivery. For
example, family size may be limited by the increasing risks of repetitive cesarean sec-
tions. Inaddition, the riskfor antenatal stillbirth maybe increased in womenwith aprior
cesarean section when compared with women with prior vaginal births.2Perhaps the
greatest risk to future pregnancies is an increase in disorders caused by abnormal
placentation, including placenta accreta and cesarean section scar ectopic pregnan-
cies. The focus of this review is to describe how uterine scarring from cesarean section
may lead to these serious disorders and how to diagnose and manage these
CESAREAN SECTION LEADS TOABNORMAL PLACENTAL IMPLANTATION
The placenta begins to form between days 13 and 15 after ovulation, and, initially
during the embryonic period, chorionic villi composed of trophoblast cells cover the
entire surface of the gestational sac. As the fetal period begins, the villi overlying
the decidua capsularis degenerate to form the chorion laeve, while the villi over the
decidua basalis proliferate to form the definitive placenta.3
Division of Maternal-Fetal Medicine, Department of Obstetrics and Gynecology, 622 West
168th Street, PH 16-66, Columbia University, New York, NY 10032, USA
E-mail address: firstname.lastname@example.org
? Abnormal placental implantation ? Placenta accreta
?Cesarean scar ectopic pregnancies
Clin Perinatol 35 (2008) 519–529
0095-5108/08/$ – see front matter ª 2008 Elsevier Inc. All rights reserved.
Normal implantation of the placenta is critical to the success of the pregnancy, and
this process is tightly regulated. A large number of cytokines, steroid hormones, im-
munologic factors, prostaglandins, and other mediators are critical to successful pla-
centation.4Strong evidence suggests that local oxygen levels have an important role
in regulating differentiation and proliferation of the trophoblast. This observation has
led to speculation that localized disturbances in oxygen tension in the endometrium
and myometrium of a cesarean scar may contribute to abnormalities of placentation.
The early embryo develops in a relatively hypoxic environment. Direct measures of
oxygen concentration in the endometrium shows tension levels between 2% and 5%.5
Initially, invading trophoblast cells plug the lumina of the decidual vessels, further con-
tributing to the physiologic hypoxia. In addition, the basal laminae of proliferating
cytotrophoblast is thicker in early pregnancy, slowing oxygen diffusion to the embryo.
Not until 10 to 12 weeks of pregnancy does blood flow into the intervillous space
This physiologic hypoxia appears to stimulate the cytotrophoblast cells to undergo
mitosis, which is different than most other cell types. Under these conditions, the
cytotrophoblast invades the endometrium, reaching the spiral arterioles, and then dif-
ferentiates into a vascular phenotype.6In vitro work demonstrates that oxygen tension
determines whether cytotrophoblast cells proliferate or invade, regulating placental
growth and architecture.7Because the early embryo requires a hypoxic environment,
it may preferentially implant into a cesarean section scar, which tends to be acellular
and avascular. This tendency may explain the increased risk for placenta previa and
accreta in individuals with an increasing number of cesarean sections.8Alternatively,
the placenta may preferentially develop in a hypoxic scar, not involuting over this area,
as it would in an unscarred uterus.
Trophoblast implanting over an avascular scar may invade more deeply into the
uterine wall because of the prolonged maintenance of an invasive phenotype. This
delay in arrest of mitosis with subsequent initiation of differentiation is likely secondary
to the absence of underlying tissue with normal vasculature and high oxygen tension.
Placenta accreta occurs when the placenta becomes abnormally adherent to the
myometrium rather than the uterine decidua (Fig. 1). If the placenta invades into the
Fig.1. Intraoperative finding of focal placenta accreta, with an area of placenta abnormally
adherent to the myometrium (arrows).
myometrium, it is termed increta. A placenta percreta invades to the level of the serosa
or continues into adjacent organs.
Rates of placenta accreta appear to be rising, although the reported incidence
varies widely. In a 1977 report, Breen and colleagues9found that the incidence in
the published literature ranged between 1 in 540 to 1 in 70,000 deliveries. More
recently, Miller and colleagues10reported an incidence of histologically confirmed pla-
centa accreta of 1 in 2510 for a 10-year period ending in 1994. Over a 20-year period
ending in 2002, Wu and colleagues11determined an incidence of 1 in 533. The differ-
ences most likely reflect methods in case ascertainment. For example, a regional
referral center would be expected to have a higher concentration of cases than a
general survey across a wide geographic area.
Risk factors associated with placenta accreta are prior uterine surgery, including
cesarean section, uterine curettage, advancing maternal age, and increasing parity.
Other associations include prior myomectomy, manual removal of the placenta, prior
hysteroscopic surgery, and prior pelvic irradiation. Cases of placenta accreta follow-
ing endometrial ablation12and uterine artery embolization13have been reported.
Placenta previa is an independent risk factor for concurrent accreta, even in the
absence of other risk factors.
Approximately 50% of pregnancies complicated by accreta are preceded by
a cesarean delivery in a prior pregnancy.11As cesarean rates have continued to rise
and the numbers of women with repeat surgeries increase as well, cesarean section
will become an even more prevalent antecedent to pregnancies complicated by pla-
centa accreta. Ina prospective observational study, the Maternal-Fetal Medicine Units
Network evaluated the risk of placenta accreta with increasing numbers of cesarean
sections. They found that the risk for placenta accreta was 0.24%, 0.32%, 0.57%,
2.13%, 2.33%, and 6.74% in women undergoing their first, second, third, fourth, fifth,
and sixth or more cesarean delivery, respectively.8If women were diagnosed with pla-
centa previa, the risk for placenta accreta was 3%, 11%, 40%, 61%, and 67% for the
first, second, third, fourth, and fifth or more cesarean section, respectively. The risk for
hysterectomy climbed to 2.5% with a woman’s fourth cesarean and to 9% with the
sixth or more cesarean.
The exact mechanism by which a prior cesarean section predisposes to placenta
accreta is uncertain. Traditional teaching has been that, with each cesarean section,
theendometrium underlyingthe implantation siteisdamagedandbecomes unsuitable
for subsequent placentation. Subsequent pregnancies are more likely to become im-
planted in the lower uterine segment by a process of elimination;14however, it seems
equally likely that, with each successive cesarean section, the uterine scar becomes
more accessible to the implanting embryo because successive incisions are created
higher in the uterine wall to avoid bladder injury from adhesions or because elective
repeat surgeries occur without labor. Whether placenta accreta occurs more fre-
quently following sections not preceded by labor is unknown. Sonographic evaluation
ofpost cesearean uterine scars imaged during subsequent pregnancies demonstrates
that surgery performed in labor is more likely to occur in the cervix.15Only about half of
women whose cesarean sections are performed without labor have a detectable
cervical scar, suggesting that the incision is created in the myometrium.
Antenatal diagnosis of placenta accreta should begin with a high index of suspicion in
women having risk factors for this condition. Ultrasound is the most common modality
Accreta and Cesarean Scar Pregnancy
used to make the diagnosis. The sensitivity of ultrasound in detecting placenta accreta
in high-risk patients (ie, those with a placenta previa and a history of cesarean section)
is approximately 80%, with a specificity of 95%.16,17Patients with placental locations
away from the lower uterine segment may be more difficult to detect before the time of
Ultrasound findings typical of placenta accreta and percreta are shown in Figs. 2
and 3A. Findings include the absence of a hypolucent area forming a distinct boundary
between the placenta and the myometrium, sonolucent lakes of slow flow within the
placenta, and increased vascularity demonstrated by color Doppler.16,18Hypervascu-
larity of the bladder and uterine serosa may also be observed. In addition, the placenta
may appear enlarged or bulky. Diagnosis of placenta accreta is typically made in the
second trimester at the time of routine fetal anatomic screening.
Sonographic signs of accreta may be evident in the first trimester. Comstock and
colleagues19published a retrospective review of ultrasound images before 10 weeks
gestational age in women later found to have placenta accreta. Six patients had low-
lying gestational sacs, with most appearing to be attached to the uterine scar with
thinning of the myometrium. In early gestation, distinguishing a pregnancy likely to
become an accreta from a cesarean scar ectopic pregnancy may be difficult. Although
in a ‘‘scar gestation,’’ the gestational sac is usually not contained within the uterine
cavity, absolute distinctions are likely artificial, and these two entities more likely
form a continuum with overlap in outcome and clinical management.
MRI may be a useful adjunct in the diagnosis of accreta (Fig. 3B, C). Although not
used as a screening tool, it may be helpful in cases with inconclusive ultrasound find-
ings. Moreover, it appears to be a better test for determining the extent of myometrial
invasion.20Warshak and colleagues16found that when MRI was performed following
a suspicious or inconclusive ultrasound, sensitivity increased from 77% to 88% and
specificity from 96% to 100%.
Biologic markers have the potential to further improve the diagnostic accuracy of
placenta accreta. Elevated levels of maternal serum creatinine kinase,21alpha feto-
protein, and b-human chorionic gonadotropin (bhCG)22have been reported in affected
pregnancies. Mazouni and colleagues23have proposed that assessment of maternal
blood for cell-free fetal DNA, placental mRNA, and the use of DNA microarray for pla-
cental-specific genes may be useful tools, but data do not yet exist to determine
whether they will be useful clinically.
Fig.2. A discrete area of abnormal invasion of the placenta into the myometrium (arrows) in
a patient with two prior cesarean sections and placenta previa. There is loss of the normal
hypoechoic rim of myometrial tissue beneath the placenta.
Significant hemorrhage and severe maternal morbidity at the time of delivery are
common in cases of placenta accreta. The bleeding may become massive in cases
of placenta percreta. Infection, bladder injury, ureteral ligation or fistula formation,
and spontaneous uterine rupture are well-known complications of an abnormally inva-
At the author’s center, 33 women were treated with either placenta accreta or per-
creta confirmed by histopathology between 2001 and 2006. Approximately 50% of
these cases were recognized before delivery. None were treated conservatively,
and all had hysterectomy. Estimated blood loss during surgery ranged between
2500 and 5000 mL, with an average of 3000 mL. On average, women received 10 units
of packed red blood cells, with a range of 3 to 29 units. Admission to the ICU was
required for 51.6% of women and 29% had intraoperative complications. Almost
40% had postpartum complications.
Fig.3. (A) Placenta percreta in a patient with one prior cesarean section and placenta previa.
A bulky heterogenous placenta with multiple venous lakes with flow is demonstrated by
power Doppler study. (B) Coronal T2-weighted MRI images of the same placenta percreta
in (A). There is marked heterogeneity of signal intensity within the placenta, typical of pla-
centa accreta. The placenta bulges anteriorly into the bladder, distorting the normal uterine
architecture. The placenta can be seen invading laterally through the myometrium into the
right pelvic side wall in both views. MRI delineates the extent of invasion more accurately
than ultrasound. (C) Axial T2-weighted MRI images of the same placenta percreta in (A),
again showing marked heterogeneity of signal intensity within the placenta, typical
of placenta accreta, and bulging into the bladder.
Accreta and Cesarean Scar Pregnancy
O’Brien and colleagues24published survey data on outcomes following placenta
percreta. Only half of the cases were suspected antepartum. Forty percent of the
patients required transfusion with more than 10 units of packed red blood cells; ure-
teral ligation or fistula formation complicated 10% of cases; infection affected 31%;
and perinatal death occurred in 9%. Maternal death occurred in 7% of cases.
Basic principles in the approach to the patient with placenta accreta are outlined
herein. Because of the severe morbidity and the potential for maternal death, careful
planning to reduce morbidity is essential.
Although guidelines for the management of these complicated cases are limited,
a multidisciplinary approach to a suspected placenta accreta or percreta should max-
imize the management of hemorrhage and minimize maternal and neonatal morbidity.
This team may include obstetricians and maternal fetal specialists, gynecologic oncol-
ogists or other surgeons with expertise in extensive pelvic surgery, obstetric anesthe-
sia, interventional radiology, and representatives from the blood bank and operating
room. At the author’s center, all cases of suspected placenta accreta are seen by
critical care obstetrics or maternal fetal medicine specialists before surgery and are
counseled about the possible clinical outcomes. The appropriate delivery venue and
timing for delivery are determined in consultation with the surgical support team,
the operating room staff, and obstetric anesthesia. When clinical suspicion is high,
delivery is generally performed at 36 weeks gestational age without amniocentesis
because of the low risk to the fetus compared with the potential major maternal com-
plications of emergency delivery without appropriate resources in place.
The surgical approach is almost always through a vertical skin incision regardless of
any previous scar. An expert pelvic surgeon, often a gynecologic oncologist, should
be present from the outset of surgery. Adequate volumes of packed red blood cells
(20 units), platelets (12 units), fresh frozen plasma (20 units), and clotting factors are
prepared before surgery. Cell saver technology can be safely used during a cesarean
section and isfrequently employed. In selectcases of placenta percreta, interventional
radiology and a vascular surgery team are consulted before surgery, and prophylactic
arterial embolization or aortic dissection may follow delivery of the fetus before initia-
tion of hysterectomy. Topical hemostatic agents, which are often used during liver
surgery, are available before the operation is started. Activated factor VII may be
employed to treat postpartum hemorrhage.25
In some cases, despite extensive planning and expertise, hemorrhage cannot be
controlled intraoperatively. In such cases, the abdomen can be packed to control
bleeding and allow time for adequate transfusion of volume, red blood cells, and clot-
ting factors, as well as correction of metabolic acidosis. We prepare an umbrella
pack26before surgery in the event that this maneuver is required. Following this treat-
ment, the fascia is temporarily closed with towel clamps, the subcutaneous tissue
dressed with moist pads, and the patient transferred to the ICU with a plan to return
to the operating room after she has been stabilized. Active communication between
the operating and anesthesia teams during the entire surgery is essential so that all
are aware of the patient’s status and can rapidly react when necessary.
Because of the severe morbidity involved with surgical management, especially
when cases of placenta accreta or percreta are diagnosed intraoperatively, ‘‘conser-
vative’’ approaches in which the placenta is left in situ are becoming more common.
Timmermans and colleagues27reviewed 60 cases of abnormally invasive placentation
managed by leaving the placenta in situ without hysterectomy. Twenty-six women
were managed without any additional interventions. In most of these patients
(19/26), the placenta had been partially removed. In 4 of these 26, conservative ther-
apy failed. Twenty-two women received adjuvant methotrexate. In most of these
women (19/22), the entire placenta was left in situ. In five, therapy failed. Twelve
women were managed with arterial embolization. In most of these patients (9/12),
the diagnosis was made antepartum and the placenta was completely left in situ. In
three patients, therapy failed. Overall, 11 women experienced infection (11/60),
21 women experienced vaginal bleeding (21/60), and 4 experienced disseminated
intravascular coagulopathy (4/60). Spontaneous loss of placental tissue was noted
in 16 women. Subsequent pregnancies were reported in eight women. It was con-
cluded that conservative management of abnormally invasive placentation can be
effective and fertility can be preserved, but it should only be considered in highly
selected cases when blood loss is minimal and there is desire for fertility preservation.
Whether adjuvant methotrexate or selective arterial embolization is beneficial is uncer-
tain. Undetectable hCG values do not seem to guarantee complete resorption of
retained placental tissue.
CESAREAN SCAR ECTOPIC PREGNANCIES
The first case of a pregnancy implanted into a cesarean scar was reported in 1978.28
As of 2006, there were 161 instances reported in either case reports or case series.29
The frequency of this condition is uncertain and depends on several factors, including
the use of routine first-trimester ultrasound. Two recent studies have estimated an
incidence of approximately 1 in 2000 pregnancies.30,31
As is true for placenta accreta, the exact cause of implantation of the gestation into
the scar of a previous cesearean section is not well understood. Investigators have
speculated that cesarean scar pregnancies result from implantation through a micro-
scopic fistula between the endometrial cavity and the scar;32however, as described
previously, because the early placenta is an invasive organ capable of digesting extra-
cellular matrix proteins, a preexisting tract would not be necessary.
It is reasonable to suppose that the pathologic mechanisms of placenta accreta and
scar pregnancies are similar with the site and level of invasion being different. With
placenta accreta, the placenta is abnormally adherent to the myometrium with the
gestational sac growing into the lumen of the uterus. A cesarean scar ectopic preg-
nancy is implanted entirely within the cesarean scar and is surrounded by myometrium
and fibrous tissue.29It is possible that some placenta accretas and especially percre-
tas began as cesarean ectopic pregnancies, with the thickness of the scar and the
degree of invasion dictating the subsequent course. Support for a similar pathophys-
iology of these two entities comes from reports of cesarean scar ectopic pregnancies
diagnosed early in gestation which were managed expectantly, resulting in near-term
delivery of a viable neonate.33Many of these cases behaved similar to placenta
percreta, with massive hemorrhage necessitating hysterectomy. One might also spec-
ulate that several case reports of second-trimester and early third-trimester uterine
rupture supposedly due to placenta percreta34,35would have been diagnosed as
cesarean scar pregnancies if early ultrasound had been performed.
Ultrasound Diagnosis of a Cesarean Scar Pregnancy
Jurkovic and colleagues30used the following criteria to diagnose early cesarean scar
pregnancies by transvaginal sonography (Fig. 4):
1. The uterine cavity is empty.
2. The gestational sac is located anteriorly at the level of the internal os, covering the
visible or presumed site of the cesarean section scar.
Accreta and Cesarean Scar Pregnancy
3. Doppler study suggests a functional placental circulation defined by increased
vascularity by color flow evaluation, apeak velocity greater than20 cm/s,and apul-
satility index of less than 1.
4. There is no ‘‘sliding organs sign,’’ defined as the inability to displace the gestational
sac with gentle pressure applied by the transvaginal probe.
MRI36and hysteroscopy37have been proposed as adjuncts to ultrasound, but at
least in early pregnancy, transvaginal ultrasound is an accurate diagnostic tool, and
additional modalities are rarely necessary.
Clinical Course and Management of Cesarean Scar Pregnancies
Because most cases of cesarean scar pregnancies identified early in gestation have
been terminated, there are insufficient data to adequately quantify the maternal risks
of continuing the pregnancy or to predict the likelihood of successfully continuing to
viability. Jurkovic and colleagues30reported on 18 cesarean scar pregnancies diag-
nosed in the first trimester of which three were followed expectantly. None of these
progressed past 17 weeks, and one woman experienced severe hemorrhage requiring
emergency hysterectomy. Because of the potential for severe morbidity associated
with this diagnosis, the best medical advice based on current information is for preg-
The most effective therapy to terminate a cesarean scar ectopic pregnancy
is unknown, and treatment should be individualized. Both medical and surgical
approaches have proven successful. Systemic38and local injection36of methotrexate
has been described in published reports. Other agents injected directly into the fetus
within a cesarean scar pregnancy have included potassium chloride and hyperosmo-
lar glucose. Surgical sac aspiration37has proven successful. Several other surgical
approaches, including hysteroscopic,39laparascopic,40and open removal,29have
been successfully used.
Uterine curettage has been performed to treat cesarean scar pregnancies, but this
approach appears to have a high failure rate. Wang and colleagues40reported a failure
in 12 of 17 women who underwent uterine curettage as their initial treatment modality.
PREVENTION OFPLACENTA ACCRETA AND CESAREAN SCAR PREGNANCIES
Many placenta accretas and all cesarean scar pregnancies occur following a previous
cesarean delivery. The obvious approach to reduce the incidence of these two entities
Fig. 4. A midline sagittal image of a cesarean scar pregnancy obtained by transvaginal
sonography. The gestational sac is implanted anteriorly between the cervix and an empty
uterine cavity. The sac is bulging toward the bladder anteriorly.
is to reduce the primary cesarean section rate and to revisit the idea of vaginal birth
after a first cesarean. At the very least, women considering elective cesarean section
should be aware that they may be putting their next pregnancy at increased risk for
a potentially devastating complication.
Future studies are needed to evaluate whether surgical techniques are available to
reduce the likelihood of a subsequent abnormal placental implantation. Perhaps,
modification of the approach to uterine closure may be beneficial, or administration
of biologic agents to improve healing and revascularization of the cesarean scar could
be effective. It is not known whether a single-layer closure or two-layer closure is more
likely to result in accretas or scar pregnancies in subsequent pregnancies. Similarly,
many surgeons close the uterus with a running locked suture that is more likely to
lead to necrosis and fibrosis at the incision site. It is theoretically possible that avoid-
ance of the locking technique could reduce abnormal placental implantation, and
future studies should evaluate this approach.
Delaying cesarean section until the cervix has effaced and the lower segment is
developed would make it more likely that the uterine incision is made in the cervix
rather than in the isthmus of the uterus. Although some surgeons advocate performing
cesarean section without creating a bladder flap, it may be beneficial to dissect the
bladder as inferiorly as possible so that the uterine incision can be made in the cervix.
Both of these measures have the potential to ‘‘hide’’ the scar from the implanting
embryo in subsequent pregnancies, reducing the risk of abnormally invasive
Early transvaginal ultrasound in all women with prior cesarean sections should be
considered to screen for developing placenta accretas or cesarean scar pregnancies.
First-trimester diagnosis may significantly reduce the morbidity associated with these
conditions by allowing for medical or minimally invasive surgical treatment which
cannot be performed later in gestation.
The incidence of abnormally invasive placentation resulting in placenta accreta or
cesarean scar pregnancy is increasing because of the rising cesarean section rate.
Women considering elective cesarean section should be counseled about the risks
to future pregnancies. Obstetricians should consider the risk to future pregnancies
when weighing the need for a cesarean delivery.
Placenta accreta and cesarean scar pregnancies may result in profuse hemorrhage
with a risk for serious maternal morbidity and mortality, especially when this condition
is not discovered until the time of delivery. A multidisciplinary approach to placenta
percreta in specialized centers has the potential to improve outcomes.
Accurate diagnosis relies on a high degree of suspicion and characteristic findings
on ultrasound, with MRI used when ultrasound is inconclusive or when placenta per-
creta is suspected. Determining the extent of placental invasion is helpful in planning
the surgical approach. Early transvaginal ultrasound should be considered in patients
with multiple prior cesarean sections to look for cesarean scar pregnancies. Future
research may be directed at determining whether modifying surgical techniques can
lower the incidence of abnormal placentation in future pregnancies.
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