Cervicoisthmic Pregnancy Near Cesarean Scar After Oocyte Donation in Premature Ovarian Failure

Copyright @ 2013 American Society for Colposcopy and Cervical Pathology. Unauthorized reproduction of this article is prohibited.

Cervicoisthmic Pregnancy Near

Cesarean Scar After Oocyte

Donation in Premature Ovarian

Failure: Literature Review Starting

From a Single Case

Salvatore Gizzo, MD,1 Carlo Saccardi, MD, PhD,1 Tito Silvio Patrelli, MD,2

Stefania Di Gangi, MD,1 Francesca De Marchi, MD,1 Anna Bertocco, MD,1

Omar Anis, MD,1 Marco Noventa, MD,1 Donato D’Antona, MD,1

and Giovanni Battista Nardelli, MD1

1Department of Woman and Child Health Y University of Padua, Padova;and 2Department of Obstetrics, Gynaecological and Neonatology

Sciences Y University of Parma, Parma, Italy

h AbstractObjective. This study aimed to identify the best man-

agementoptions indecisionmaking in cases of cervicoisthmicand cesarean scar pregnancies and rare forms of ectopicpregnancies with high rates of pregnancy-relatedmorbidityin the first trimester, more commonly associated with as-sisted reproductive medicine.

Materials and Methods. We performed a literature re-view of the description of a case report of a cervicoisthmicpregnancynear a cesarean scar in aprematureovarian failurewoman. She obtained pregnancy after ovum donation,hormonal therapy, and in vitro fertilization. The researchersfocused on the MEDLINE/PubMed database articles on ec-topic pregnancies, particularly on cesarean scarpregnancies,cervical pregnancies, and ectopic pregnancies after in vitro

fertilization in English-language journals published fromJanuary 1996 to December 2011.

Results. The conservative or nonconservative optionsfor medical or surgical treatments are disposables. More-over, in literature, no consensus was found about the besttreatment method.

Conclusions. Obstetricians shouldpay great attention toa possible cesarean scar pregnancy in patients with riskfactors in theirmedical history. Until now, the rarity of thesefindings does not allow the definition of a commonly ac-cepted management, so the best personalized approachmay be guided by early recognition, close surveillance, andappropriate counseling. Further investigations arenecessaryto recognize high-risk factors for all ectopic pregnancies andthose unique to cesarean scar ectopic pregnancies. h

Key Words AQ1: cervicoisthmic pregnancy, cesarean scar, assistedreproductive therapy, methotrexate therapy, prematureovarian failure, clinical management

Ectopic pregnancy (EP) occurs when the fertilized

ovum is implanted outside the endometrial cavity.

The fallopian tube is the most common location for an EP.

Others sites of implantation can be the ovary, cervix, ab-

domen, uterine cornua, and cesarean scars [1, 2].

A very rare form of EP is cesarean scar pregnancy

(CSP), defined as the implantation of the villi into the

Copyeditor: James Joseph Arguelles

The authors have declared they have no conflicts of interest.Reprint requests to: Salvatore Gizzo, MD, Dipartimento Salute della

Donna e del Bambino, U.O.C. di Ginecologia e Ostetricia, Via Giustiniani 3,35128 Padova, Italy. E-mail: [email protected]

Dr Saccardi monitored the ultrasound; Drs De Marchi and O. Anisfollowed up the patient during recovery, taking care of the patient before,during, and after the medical and surgical treatment; Drs Patrelli, Bertocco,and Noventa reviewed all the English literature on cesarean scar preg-nancy; Drs Gizzo and Di Gangi wrote the article; Drs D’Antona and Nardellisupervised and approved the final version of the article.

� 2013, American Society for Colposcopy and Cervical Pathology

Journal of Lower Genital Tract Disease, Volume 00, Number 00, 2013, 00Y00


uterine muscular layer at the cesarean scar site. Nowa-

days, the increased use of assisted reproduction tech-

niques has been accompanied by a rising number of EPs

[3], and the increased rate of cesarean deliveries has led to

a growing rate of pregnancies implanted in the cesarean

scar [4]. Because of their anatomic localization, these

2 types of pregnancies can lead to very serious compli-

cations, such as uterine rupture and severe hemorrhage.

Hence, once the diagnosis of CSP is confirmed, immediate

termination of the pregnancy is recommended because of

its great danger for the patient [5].

Thanks to the improved access to transvaginal ultra-

sound scanning and the rapid assay of serum human

chorionic gonadotropin (hCG), almost all the EPs are now

detected early, so conservative management is possible.

Actually, there is no consensus about the best treatment

method, but the management should consider the mini-

mization of hemorrhage and the patient’s desire of pre-

serving fertility. Medical treatment has been described

with variable success [5, 6].

We reported a case of cervicoisthmic pregnancy ob-

tained after in vitro fertilization (IVF) and embryo transfer

implanted near a cesarean scar. The pregnancy failed to

respond to medical treatment and required surgical in-

terventions. We also reviewed the medical literature in

search of the right management for these patients and the

definition for the best intervention timing.

CASE

A 33-year-old woman, gravida 2 para 1, was admitted to

our hospital for a suspicion of EP at 7 weeks 2 days of

gestation, localized in the cervicoisthmic region of the

uterus. She had a premature ovarian failure 2 years before,

so she obtained pregnancy by assisted reproduction with

an IVF after oocyte donation. The patient had a history

of 1 cesarean delivery for placental abruption during labor

in 2003.

At the first ultrasound at 6 week of gestational age

(g.a.), a twin pregnancy was diagnosed. One of the 2 ges-

tational sacs was localized near a posterior fibroid 5 cm

in diameter and appeared in expulsion with an embryo

without cardiac activity, undergoing an early reabsorption.

Transvaginal sonography performed at 7 weeks 2 days

of g.a. revealed a single, well-growing vital embryo (crown-

rump length = 10 mm, regular trophoblast), with a gesta-

tional sac located in the cervicoisthmic region, exactly near

the scar of the previous cesarean delivery (see F1Figure 1).

Cervical length was 23 mm. There was no free fluid in

the pelvic cavity.

The patient had no symptoms, and her hemodynamic

condition was stable. Pelvic examination showed a

normal-sized uterus and a normal-looking cervix with a

closed os. On admission day, her serum A-hCG level was

17,350 mUI/L.

After informing the patient about the different avail-

able strategies of treatment and the respective advantages

and disadvantages, and considering the patient’s desire

of preserving the uterus to attempt another pregnancy

by oocyte donation, conservative treatment with a single

dose of 50 mg/m2 intravenous methotrexate (MTX),

attended by a rescue therapy with folic acid for the next

days, was proposed.

Figure 1. Transvaginal sonography performed at 7 weeks 2 days of gestational age revealed a single well-growing vital embryo with agestational sac located in the cervicoisthmic region, exactly near the scar of the previous cesarean delivery.

2 & G I Z Z O E T A L .


A total dose of 90 mg (1.80 m2) of MTX was adminis-

tered. No adverse effect of MTX was noted. Two days later,

ultrasound examination revealed the persistence of the

gestational sac in the cervicoisthmic region, with a nonvital

embryo and decreased A-hCG level (6,435 mUI/L).

Despite the fact that patient was asymptomatic and

hemodynamically stable, in the afternoon, surgical treat-

ment by ultrasound-guided curettage, after the appearance

of vaginal bleeding, was performed.

Surgical decision was based on the aim of reducing

the massive hemorrhage after the trophoblastic shedding

from the atonic cervix occurring as a metabolic effect of

MTX because ultrasound evaluation showed an irregular

pattern of the trophoblast, with a large area of abruption

and 3.5 mm of myometrial thickness between the distal

part of the trophoblast and the bladder wall (see F2Figure 2).

During surgery, after the gestational sac was pulled out,

we assisted a profuse vaginal bleeding and a cervical he-

matoma was revealed at the ultrasound evaluation.

Because it was impossible to perform a conservative

surgical treatment by transcervical route, and because it

was very difficult to stop the uterine hemorrhage and the

significant AQ2bleeding because of the onset of hemodynamic

instability, urgent laparotomy was carried out.

At the abdominal opening, we found a hemoperitoneum

and retroperitoneal hematomas. The uterus, the fallopian

tubes, and the ovaries appeared normal, without ad-

vanced trophoblastic invasion of the anterior uterine

wall. We had to perform total hysterectomy even if there

is significant anemia because of the overall blood loss

amounting to 4.0 L and the patient underwent blood

transfusion of 10 concentrated red blood cell and plasma

infusion bags. AQ3The day after surgery, the patient needed

an intensive care observation, but her conditions remained

stable and she was able to return to our unit. The patient

was finally discharged 5 days after hysterectomy in good

general condition. Histologic examination of the uterus

revealed infiltration of the trophoblastic cells involving

the upper part of the endocervical canal at 2 mm from

the fibroid tissue of the previous cesarean scar near

the isthmus. The timeline of events is shown in T1Table 1.

Figure 2. Ultrasound evaluation showed an irregular pattern oftrophoblast with a large area of abruption and 3.5 mm ofmyometrial thickness between the distal part of the trophoblastand the bladder wall.

Table 1. Timeline of Case Events

Time Events

HDAQ4 0 Admission to hospitalY Ultrasound scan: a single well-growing vital embryo (crown-rump length = 10 mm, regular trophoblast);

the gestational sac located in the cervicoisthmic region, near the scar of the previous cesarean deliveryY A-hCG level: 17,350 mUI/LY Chamber G8 g.w.Y No symptoms

HD 1 Administration of a single dose of 50 mg/m2 intravenous methotrexateHD 2 Rescue therapy with folic acidHD 3 Morning:

Y Ultrasound scan: persistence of the gestational sac in the cervicoisthmic region; nonvital embryo; large area ofabruption and 3.5 mm of myometrial thickness between the distal part of the trophoblast and the bladder wall

Y A-hCG level: 6,435 mUI/LAfternoon:Y Persistent vaginal bleeding Y ultrasound-guided curettageY Trophoblast abruption, persistent cervical atonia, cervical hematoma Y total hysterectomy by urgent laparotomy

HD 4 Intensive care observationHD 5 Return to our unitHD 6Y7 ObservationHD 8 Discharge

A-hCG, A human chorionic gonadotropin.

Managing Cesarean Scar Pregnancy After IVF Cycle AQ8& 3


Decidual-like transformation of the stromal cells was

located only focally under the villi, whereas secretive

glandular cells were not detected. The minimal distance

between the villi and the anterior wall of the uterus was

1.5 mm. The isthmic mucosa demonstrated no progestin-

like stromal modifications. The uterine body presented

only 3 microfoci of decidual-like transformation of super-

ficial stromal cells and multiple focuses of adenomyosis.

Focal fibrosis was also noted near the embryonic tissues,

compatible with the scar site of the previous cesarean

delivery.

DISCUSSION

Nontubal EPs account for only 5% of all EPs, but they are

the most common cause of pregnancy-related morbidity

in the first trimester [1]. An uncommon form of EP is

the CSP. Cesarean scar pregnancy is defined as the im-

plantation of the villi into the uterine muscular layer at

the cesarean scar site. Its incidence ranges from 1:1,800 in

developed countries to 1:2,216 pregnancies in nondeveloped

countries, with a rate of 6% in all EPs among women with

at least 1 cesarean delivery [7, 8].

Nowadays, the etiology remains unclear, but predis-

posing risk factors include anatomic anomalies, previous

cervical interventions resulting in damage of the endo-

cervical mucosa (previous curettage, cervical or uterine

surgery, and cesarean delivery), Asherman syndrome, and

IVF [9]. Previous cesarean delivery, pelvic inflammatory

disease, previous tubal surgery, previous EP, and use of

an intrauterine device have been associated with a higher

risk of EP, but half of all the women with an EP do not

show any known risk factors [10].

Considering these factors, or their associationVeven

more so if they are presentVa cervical stenosis may pro-

mote the descending of the embryo and its cervical im-

plantation.AQ5 Furthermore, cervical pregnancy can be

favored if there is too rapid transport of the fertilized

oocyte or if the endometrium is not mature enough to

receive it [11].

Implantation at the cesarean scar is one of the rarest

forms of EP because it is a gestation completely surrounded

by the myometrium and the fibrous tissue of the scar and it

is separated from the endometrial cavity or the fallopian

tube [5]. Its incidence is about 1:2,000 of all pregnancies,

and it seems to increase in recent literature [7]. This could

be explained by a true increase in cesarean birth rate

worldwide or even by an improved diagnostic accuracy

because of the routine early ultrasound.

Invasion of the myometrium through a microscopic

tract most probably explains implantation at the scar,

such as intramural implantation. With intramural preg-

nancy, such a tract is believed to develop from trauma of a

previous uterine surgery. In the endometrium, there can

also be tiny dehiscent tracts or minute wedge defects that

are the persistent form of damage to the basalis decidua

due to uterine surgery. The time interval between such

trauma and a subsequent pregnancy may affect the events

of implantation [5].

Generally, symptoms are vaginal bleeding that is usu-

ally painless or is associated with abdominal pain and

urinary symptoms, especially in advanced pregnancies.

Godin AQ6et al. [12] at first, and then many other authors

[13Y16], tried to individuate strict ultrasound criteria for

CSP diagnosis. Actually, sonographic criteria for scar

pregnancy diagnosis are identification of the gestational

sac or placenta within the cervix, absent intrauterine

pregnancy, visualization of a normal endometrial stripe,

hourglass-shaped uterus with a bulging cervical canal and

a sac with active cardiac activity below the internal os to

indicate a viable pregnancy [12Y14, 17, 18]. Moreover, a

myometrial thinning caused by the distension of the ges-

tational sac predisposes the patient to uterine rupture, so its

sonographic study may be useful in the management [15].

We searched MEDLINE/PubMed databases for arti-

cles on EPs, focusing particularly on CSPs, cervical preg-

nancies, and EPs after IVF in English-language journals

published from January 1996 to December 2011.

Nowadays, it is well known that the use of IVF and

ovulation induction both increase the probability of an

EP [16]. The pathogenesis is still unclear. Some authors

advanced hypothesis on reflux of the embryos into the

cervix during or after embryo transfer, on cervical ma-

nipulation, and misplacement of embryos or possible

isthmocele (a reservoir-like pouch defect on the anterior

wall of the uterine isthmus located at the site of a previous

cesarean delivery scar) as important potential risk factors

for cervical or scar pregnancies related to assisted re-

productive techniques [19Y21].

Only few reported cases of scar pregnancies and no

consistent observational studies are available to create

specific treatment recommendations. The better treat-

ment should be individualized on the single patient,

considering the age, the desire of preserving fertility,

the hemodynamic conditions, and the surgeon’s ability.

Therefore, interruption of EPs seems appropriate once

the correct diagnosis is made to avoid subsequent risks

such as uterine rupture or life-threatening hemorrhages.

The physicians’ aims should be the performance of feti-

cide before uterine rupture and the removal of the gesta-

tional sac, preserving fertility [5].

4 & G I Z Z O E T A L .


Several forms of treatment have been reported, divid-

ing the surgical to the nonsurgical methodsVthe first ones

not excluding the others.

Primary surgical intervention is considered the most

conservative and definitive therapeutic strategy: it is car-

ried out by excision of the EP and eventual repair of

the uterine scar. On the other hand, medical therapy is a

noninvasive therapeutic strategy; it avoids further damage

of the uterus, maximizing the chance of preservation

of fertility according to the patient’s desire. Moreover,

Trio et al. [22], in a study of more than 67 patients with

EP, proposed an expectant management in cases with

less than 3.5 cm of ectopic gestational tissue dimensions,

and self-decreasing A-hCG values, in women with stable

hemodynamic conditions. In their study, the authors

described spontaneous resolution in 73% of cases, even

more if the initial serum concentration of hCG was

less than 1,000 mUI/L. Therefore, they gained time in

choosing the appropriate treatment for each patient

between medical and surgical options.

Nonsurgical Methods

The most common medications used for early induction

of abortion, namely, mifepristone, MTX, misoprostol,

and also chemical agents, such as hyperosmolar glucose,

urea, and actinomycin, have been investigated.

Systemic MTX therapy is a widespread option in

conservative management. Many studies showed an

overall success rate of primary systemic MTX treatment

ranging from 40% to 54.5% and 91% according to the

presence or absence of fetal cardiac activity and to the use

or non-use of local therapy in association [6, 23, 24].

Prognostic factors for primary MTX therapy failure are

the presence of embryo cardiac activity, an initial serum

hCG level more than 10,000 mUI/L, more than 9 weeks

of g.a., and a crown-rump length longer than 10 mm [24].

In cases of CSPs, MTX administration can be the best

management for asymptomatic and hemodynamically

stable women, with normal liver and renal function,

normal blood cell count, with an unruptured CSP of less

than 8 g.w.AQ7 , and a myometrial thickness less than 2 mm

between the CSP and the bladder [25]. Indeed, CSPs have

been shown to respond well to a dose of 50 mg/m2, es-

pecially in those with A-hCG levels less than 5 IU/mL

[26]. However, patients treated with MTX should be

strictly followed up with serial A-hCG. On the other

hand, there are no reported adverse effects such as nau-

sea, stomatitis, alopecia, and others in the treatment

of CSP after systemic administration of the drug with

standard doses of 50 mg/m2 [27]. Analysis of published

case reports shows that medical treatment with MTX is

successful in 71% to 80% of cases, with 6% of women

requiring hysterectomy [7].

An effective alternative to systemic MTX management

is MTX intra-amniotic injections administered by sonog-

raphically guided percutaneous or transvaginal routes [5].

Because of the short half-life of MTX (about 10 h), some

authors proposed a systemic repeated-dose regimen or

intrasac injection of MTX because it achieves a high local

concentration and thus more rapidly interrupting the

pregnancy [26].

Other drugs are available for intra-amniotic injection,

such as potassium chloride, hypertonic glucose, and mi-

fepristone, but there are not many studies of comparison

between their advantages. One study seems to show better

results for MTX versus those for hypertonic glucose [28].

Intra-amniotic treatment is preferred in unruptured non-

viable EP; it helps the preservation of the uterus and the

fallopian tubes for future pregnancies. Direct administra-

tion of MTX into the amniotic sac, compared with par-

enteral administration, results in many advantages such

as greater effectiveness, shorter time treatment, reduced

dosage, and absence of adverse effects and toxicity [5].

Some studies have shown a successful conservative

management with the combination of local MTX injec-

tion followed by curettage. In these cases, curettage has

been considered necessary to reduce the massive hemor-

rhage after the trophoblastic shedding from the atonic

cervix, occurring as a metabolic effect of MTX [24, 29,

30]. Kirk et al. [6] suggested that cervical pregnancies

with vital embryos should be treated by local MTX or

potassium chloride injection, with or without subsequent

curettage. If these techniques are not available, an alter-

native therapy can be multiple-dose systemic MTX.

Surgical Methods

Regarding the role of uterine curettage, a review of the

literature by Arslan et al. [31] showed that either it was

unsuccessful or it caused complications in 90% of the

women with a CSP, requiring major surgical treatment.

This result is in accord with that of Wang et al. [32] who

registered a failure rate of 70% in a case series of 8 CSPs.

The high failure rate of curettage may be explained by

the difficulties in removing the trophoblastic tissue that

is unreachable by the curette and, moreover, by the very

high risk of uterine rupture with a subsequent severe

hemorrhage for damages to the uterine artery system

[33]. For the latter reason, to prevent profuse bleeding,



various hemostatic measures, yet successfully used, are

available, for example, local injection of vasopressin,

intrauterine balloon tamponade by Foley catheter, and

Shirodkar suture. Uterine artery embolization (UAE) or

ligation alone or followed by curettage or conservative

surgery has terminated cervical pregnancies without sig-

nificant hemorrhage, preserving the uterus [34Y36]. In

a randomized trial, pretreatment UAE with either UAE

or systemic MTX in 72 women with CSP who underwent

suction curettage was associated with significantly de-

creased blood loss and length of hospitalization [37].

Zakaria et al. [38] were the first to reveal the use of

multidose MTX therapy in association with UAE or UAE

and intra-amniotic KCl to be safe and effective for the

conservative management of cervical EPs. Curettage after

UAE has been reported as another approach to the con-

servative management of cervical pregnancy [39].

The recent introduction of hysteroscopy as an opera-

tive option in intrauterine diseases made it an interesting

minimally invasive therapeutic approach, even for preg-

nancy evacuation. Wang et al. reported in 2005 a suc-

cessful hysteroscopic management of CSP for the first

time in English literature. In 2006, they have also pub-

lished 6 other successful cases of EP with no complications

and no need of blood transfusion, thus opening a new

window in the surgical management [40]. Even laparo-

scopic conservative resection is suitable but only if the

woman presents stable conditions and the surgeon is

skilled and trained, because the pregnancy may be incised

and removed in an endobag but the conversion in lapa-

rotomy has to be possible and rapid in case of difficult

hemostasis or uncontrollable bleeding [5, 34]. Laparot-

omy is reserved for hemodynamically unstable patients

and for a failed laparoscopic surgery; furthermore, it

is mandatory when uterine rupture is confirmed or

strongly suspected. In a review until August 2002, hys-

terectomy was performed in 7 of 19 cases of CSP either

as a primary procedure or for failure of other strategies

of treatment [34].

Our experience supports that early recognition of

a scar pregnancy is the key factor in trying to assume a

conservative management, especially in patients with

risks factors according to their medical history. In our

case, the previous cesarean delivery, the IVF technique

adopted to achieve pregnancy, and the sonographic evi-

dence indicated the need for a close surveillance because

of the high risk of complications in the conservative

management. When there is fetal cardiac activity and

more than 12 weeks of gestation, conservative therapeutic

options are not so effective, and there is a higher risk of

surgical management. Moreover, according to literature

data, systemic MTX is less effective in pregnancy with

A-hCG levels greater than 5,000 mUI/L. Nevertheless,

we tried the medical conservative management and a

close follow-up in respect of the woman’s desire of

attempting a new pregnancy because the patient was

asymptomatic. The patient finally underwent surgical

management, but she was satisfied because of our attempt

to preserve her fertility according to her strong desire of

childbearing.

CONCLUSIONS

Concerning CSP, insufficient evidence exist to recommend

a single optimal management and there are no consensus

guidelines for treatment.

The therapeutic option has to be chosen considering

the clinical manifestation, the available techniques, and

the surgeon’s skills, besides the patient’s preferences and

desire of preserving fertility. Patients should be counseled

concerning the unavoidable need of interrupting the preg-

nancy, the risk of a massive hemorrhage, and the eventual

subsequent hysterectomy.

A careful medical history with the evaluation of the

eventually present risk factors might help the clinicians

in advising the patient and in alerting the sonographer

about the possible finding of a CSP during early pregnancy

scanning. Further investigations are necessary to recog-

nize high-risk factors for all EPs and those unique to ce-

sarean scar ectopic.

Acknowledgment

The authors thank all the staff of the Gynaecologic and Ob-stetric Unit at the University of Padua. AQ9

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8 & G I Z Z O E T A L .


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Cervicoisthmic Pregnancy Near Cesarean Scar After Oocyte Donation in Premature Ovarian Failure

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