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Thứ Năm, 14 tháng 2, 2013



Fig. 4—Uterine arteriovenous malformation (AVM) in two different patients.

A and B, 36-year-old woman who presented with persistent hemorrhage after dilation and curettage for retained products of conception (RPOC). Transverse images from transvaginal ultrasound (A) show echogenic material within uterine cavity, with increased flow on color Doppler sonography (B). Spectral Doppler sonography shows low resistance waveform and peak systolic velocity of approximately 60 cm/s (not shown). Possibility of AVM was raised. Pathologic examination after hysterectomy revealed adherent RPOC and no AVM.

C–F, 22-year-old woman who presented with intermittent heavy vaginal bleeding 6 weeks after elective first trimester termination. Physiologic bleeding was noted in first month after procedure, which accelerated 2 weeks before presentation. Serum β-HCG was nondetectable. Transvaginal ultrasound (C) shows clot within endometrial cavity with eccentric vascular mass in fundus. Waveform on spectral Doppler sonography was low resistance, with peak systolic velocity greater than 90 cm/s (not shown). Vascular malformation was suspected, and patient was referred for angiography. Multiple images from pelvic angiogram show prominent right uterine arteries (arrow, D). Subsequently, there is vascular blush of presumed AVM in fundus (arrow, E) and then early filling of draining vein (arrow, F). This was embolized with cessation of patient bleeding. No pathologic analysis was available to confirm vascular malformation. Although history and angiographic features were suggestive of AVM, chronic RPOC can simulate ultrasound and angiographic appearance of AVM and cannot be excluded as reason for bleeding in this case.

The postpartum period is defined as beginning immediately after the delivery of the infant and placenta and typically is considered to continue for 6–8 weeks as the physiologic changes of pregnancy slowly revert to baseline. The period after a spontaneous or elective abortion is less well defined, but complications are often grouped into early complications occurring immediately or within the first days after the procedure and delayed complications occurring beyond that time [1, 2].

Pregnancy remains a major cause of mortality in the 21st century in the United States. A recent analysis placed the pregnancy-related mortality rate at 14.5 deaths/100,000 live births, with more than three quarters of deaths occurring in the postpartum period (most commonly related to hemorrhagic or embolic conditions) [3]. In addition to these life-threatening complications, other conditions such as endometritis and retained products of conception (RPOC) are relatively common after birth or termination and may require hospitalization or additional procedures [4, 5]. Finally, almost one third of births in the United States are now performed by cesarean section, which results in the possibility for both immediate and delayed complications [6]. Because of their prevalence, a radiologist must be familiar with the various postpartum complications and the role imaging plays in their clinical evaluation.


Imaging the Postpartum Uterus

The postpartum uterus typically requires 6–8 weeks to involute and return to its typical nongravid size and appearance on ultrasound [7]. Although ultrasound is often performed in this period to evaluate for abnormalities such as RPOC, imaging of the postpartum uterus is complicated: the postpartum uterus has a variable appearance, and there is significant overlap between the normal and abnormal uterus (Fig. 1). For example, echogenic material is frequently seen within the uterus in patients with bleeding, but this was found in one study not to be predictive of need for further intervention [8]. In a prospective study of asymptomatic women with physiologic levels of vaginal bleeding after delivery, an echogenic endometrial mass was present in half of the patients 7 days postpartum and in 21% of subjects at 2 weeks [9]. The entire postpartum uterus can appear hypervascular on color Doppler images, which will typically spontaneously resolve without incident [10]. The presence of gas within the endometrial cavity, either on CT or as echogenic shadowing foci on ultrasound, may also be a normal finding for several weeks after delivery [10, 11].


RPOC and Postpartum Hemorrhage

RPOC is a nonspecific term that encompasses residual fetal or placental tissue remaining after delivery, miscarriage, or termination.
The frequency of RPOC has been variably described. It most commonly occurs with spontaneous abortions, with a frequency of up to 22% [4]. However, RPOC are quite uncommon after elective termination [12]. Primary postpartum hemorrhage is defined as blood loss greater than 500 mL after vaginal birth and greater than 1000 mL after cesarean section. The most ommon cause is an atonic uterus, which does not contract to halt hemorrhage. Atony can result from numerous causes, such as extended labor, multiple gestations or a large fetus, or use of oxytocin for induction or augmentation. Incomplete delivery of the placenta is an important cause of uterine atony and is often suspected when the placenta fails to deliver, delivers incompletely, or has evidence of fragmentation.

Secondary postpartum hemorrhage occurs when bleeding begins more than 24 hours after delivery; it is less common than primary hemorrhage but can cause significant morbidity and mortality [13]. RPOC is an important cause of secondary hemorrhage, and ultrasound is often requested for evaluation, whereas RPOC causing primary hemorrhage are often suspected and treated at the time of delivery without imaging.

Placenta accreta is a spectrum of conditions involving a placenta that is abnormally adherent to the endometrium and is an important cause of RPOC and postpartum hemorrhage [14]. Placenta accreta vera occurs when the chorionic villi contact but do not invade the myometrium, placenta increta occurs when there is myometrial invasion, and placenta percreta involves invasion to or through the uterine serosa. Placenta accreta typically develops where there is a deficiency of the decidua basalis (e.g., cesarean scar) and is particularly likely in patients with placental previa or multiple cesarean sections. However, it can also occur after termination and prior uterine procedures and with advanced maternal age, uterine anomalies, Asherman syndrome, or subserosal fibroids [15]. The imaging of placenta accreta will be discussed in greater detail later in this article (see the Delayed Cesarean Complications subsection).

Ultrasound Appearance of RPOC

Although it can be also be a normal postpartum finding, the presence of an echogenic mass in the endometrium appears to be the most accurate sign of RPOC, as determined by a retrospective review of 163 patients with suspicion for RPOC that reported sensitivity and specificity of 79% and 89%, respectively [16]. Increased color Doppler flow, which can also be physiologic in the postpartum period, was found in the same study to be more prevalent with RPOC than without it (79% vs 40%) (Figs. 2 and 3). Another cohort study of 265 women found that the presence of an intrauterine mass on routine postpartum ultrasound in asymptomatic women with uneventful deliveries was found to be predictive of future hemorrhage and the need for surgical intervention [17]. However, a smaller study did not show this result [8]. The significance of apparent endometrial stripe thickening, typically greater than 10 or 13 mm, has been reported in one study to be a useful indicator of RPOC [18], whereas multiple others have not [8, 17, 19, 20].

The most important message regarding RPOC is that no single factor has perfect positive or negative predictive values. Because both clinical signs and symptoms and ultrasound findings have high false-positive rates, being conservative in diagnosing RPOC and not relying on a single indicator are important principles that should guide reporting [21].

Uncommon Causes of Hemorrhage

Subinvolution of the placental site is a likely underrecognized cause of postpartum hemorrhage because it can be diagnosed only by pathologic analysis after hysterectomy or sufficient uterine curettage. In this condition, even in the absence of a cause such as RPOC, the uteroplacental arteries fail to regress and result in significant bleeding. There may be an immunologic basis for this condition through a common mediator that causes these vessels to regress prematurely in eclampsia [22]. This condition has no characteristic imaging findings.

Uterine arteriovenous malformations (AVMs) are an exceedingly rare cause of postpartum bleeding. They can be congenital or acquired as a result of hormonal stimulation, but the most common cause is likely iatrogenic. A mass in the postpartum uterus
with vascularity on ultrasound is much more likely to represent RPOC than AVM. AVM can be considered when RPOC have been excluded and the mass is hypoechoic on B mode images and located within the myometrium [23] (Fig. 4). The presence of low-resistance waveforms and peak velocities greater than 80 cm/s have been described as features suggestive of AVM over other causes [24].

Some authors think that uterine vascular malformations have been overdiagnosed recently because hypervascular masses that simulate the appearance of a true vascular malformation can develop around RPOC in the endometrial cavity or myometrium.

The possibility of a vascular malformation in postpartum patients may delay curettage for fear of provoking hemorrhage, despite a lack of definitive evidence to suggest this as a complication [25]. Conservative therapy and observation have been suggested for stable patients with a suspected vascular malformation, and embolization or hysterectomy is recommended only for unstable patients.

A traumatic pseudoaneurysm may appear and behave similarly but is likewise quite rare. Turbulent bidirectional flow within the
pseudoaneurysm may resemble the Chinese-Taoist yin and yang symbol (yin-yang sign) on color Doppler images, as pseudoaneurysms do elsewhere in the body [26].


Interventional Radiology and Postpartum Hemorrhage

In cases of life-threatening postpartum hemorrhage that does not respond to uterine massage and medical therapy, the traditional
method of treatment has been hysterectomy. Although definitive, it is an invasive procedure that sacrifices future fertility. Uterine artery embolization is an alternative method for treatment of postpartum hemorrhage [27].

Embolization has been used to treat uterine atony resulting from multiple causes. Embolization is the therapy of choice for rare vascular causes of postpartum hemorrhage, such as uterine pseudoaneurysms and vascular malformations. Embolization as well as balloon occlusion of the iliac arteries has also been used in prophylaxis and treatment of placenta accreta. Embolization has been reported to be efficacious in small case series, especially when performed as a prophylactic measure when the diagnosis is known [28, 29]. The role of balloon occlusion of the iliac arteries is more controversial, with varying efficacy reported in the literature [30, 31].

The rate of successful treatment with embolization is high (near 90%) and appears to have a negligible effect on future fertility [25]. Often, uterine artery embolization can successfully control hemorrhage even if there is no evidence of active extravasation
(Fig. 5). Because uterine fibroid embolization has emerged as a modality for treatment of symptomatic uterine leiomyoma, interventional radiologists are likely to be increasingly comfortable utilizing similar techniques for the control of postpartum hemorrhage.

Endometritis and Postpartum Infection

Endometritis, or infection of the uterine decidua, is the most common cause of postpartum fever. Although a low-grade fever is expected in the first 24 hours after vaginal delivery or cesarean section, fever after this period is suspicious for endometrial infection.

Endometritis is more common after cesarean section, with rates up to 30 times higher than that after spontaneous vaginal delivery [32]. The rates are higher when prophylactic antibiotics are not used, such as for emergent cesarean sections or some cases of therapeutic abortions [6, 33].

Endometritis is a clinical diagnosis, but uterine imaging is sometimes requested to guide therapeutic decisions. Typically, endometritis is treated with broad spectrum antibiotics, but if RPOC, infected hematoma, or uterine abscess are present, evacuation may be required.
Not surprisingly, the evaluation of endometritis is fraught with the same issues as for other postpartum imaging, with considerable overlap between physiologic and abnormal findings. Patients with clinical endometritis can have normal ultrasound findings, echogenic material within the uterus can be normal in postpartum women and may not reflect infected hematoma or RPOC, and endometrial gas can be a normal finding for up to 3 weeks after delivery and does not always indicate infection [34] (Fig. 6). Again, not being overly reliant on or definitive according to a single finding and integrating the imaging findings into the complete clinical picture is crucial.

One potential but rare complication of endometrial infection is pelvic septic thrombophlebitis. This occurs in approximately one in 2000 deliveries and 1–2% of cases of endometritis; it appears to be more prevalent when the infection spreads to the parametrial tissues [32]. CT or MRI is preferred over ultrasound in the evaluation of patients for whom conventional antibiotic therapy has failed and who are suspected of having underlying conditions, such as septic thrombophlebitis or an abscess. Both modalities will typically show an expanded ovarian vein with internal thrombus (Fig. 7). Enhancement of the vessel wall may also be present. Treatment is anticoagulation in addition to antibiotic therapy.

Thrombotic Complications

Pregnancy has long been recognized as a prothrombotic state. The mechanism of this thrombophilia is thought to be due to increased levels of fibrin and the other coagulation factors, as well as systemic up-regulation of plasma prothrombotic mediators.
This synergizes with the slowed lower extremity venous velocities that develop in the third trimester to predispose patients to deep vein thrombosis and pulmonary embolism [35]. Complications of venous thromboembolism are the leading cause of mortality of pregnant and recently pregnant women within the developed world [36].
Like other changes of pregnancy, the prothrombotic state of pregnancy does not immediately revert to normal after delivery.
The rate of pulmonary embolism has been found to be highest in the postpartum period, and it requires 4 weeks for the risk of venous thromboembolism to return to normal population levels after delivery [37].

The evaluation of pregnant and postpartum women with suspected pulmonary embolism has been extensively discussed and
remains a controversial topic [38, 39]. In the postpartum period, concerns about fetal exposure to ionizing radiation or gadolinium is no longer a factor. However, ionizing radiation exposure to actively dividing and lactating breast tissue remains an important issue.

Many practicing radiologists continue to recommend CT angiography because of its high sensitivity and specificity and its ability to evaluate for other causes of dyspnea or chest pain [38, 40]. However, ventilation perfusion or perfusion-only scintigraphy has advantages, including a lower dose to breast tissue [41, 42]. In addition, in pregnant patients, there is a reported higher rate of nondiagnostic CT angiograms potentially due to alterations in maternal cardiac output [43]; this could extend into the postpartum period as well. Because of this continued debate, provider and patient preference will likely decide which test is favored in an institution.

Additional thrombotic complications in pregnancy include ovarian vein thrombosis and thrombophlebitis, as mentioned previously in this article. Thrombosis of a dural sinus or cerebral vein is a rare but important cause of postpartum headache, altered mental status, seizure, and other neurologic symptoms and occurs more frequently in the postpartum period than during pregnancy [44].

These patients tend to have better outcomes when treated, compared with other patient groups with venous sinus thrombosis. CT or MR venography should be considered for the evaluation of new neurologic symptoms in the postpartum period. The sensitivity of unenhanced head CT for the detection of venous sinus thrombosis is relatively low (25–64%).
Venous sinus thrombosis should be suspected as a potential underlying cause of brain parenchymal abnormalities (e.g., edema or hemorrhage) in the postpartum period [45] (Fig. 8).

Finally, amniotic fluid embolism is a rare but feared complication of labor. Because of trauma to the ovarian veins during labor, amniotic fluid is able to enter the venous circulation [46]. The classic clinical presentation is rapid onset of shock and respiratory collapse.
Chest radiographs will typically show new bilateral pulmonary opacities that appear similar to acute pulmonary edema.

Cesarean Delivery and Other Surgical Complications

Immediate or Early Complications

As discussed earlier, the rate of cesarean delivery has increased substantially in the past two decades and is now the most commonly performed surgical procedure in U.S. hospitals [6]. The potential reasons for this increase include changing patient demographics (such as increased frequency of multiple births), but it is more likely a reflection of changes in patient and physician preference and medicolegal concerns.

Cesarean section has a much higher rate of endometritis compared with vaginal delivery, and endometritis is the most common complication after cesarean section [47]. The risks common to any surgical procedure are also present after cesarean section, such as significant bleeding and hematoma or wound infection. Wound infection has been estimated to occur in about 5% of cases, most of which will be diagnosed and treated clinically without requiring imaging [48].

When endometritis is diagnosed, either clinically or with the aid of imaging, the typical treatment is antibiotics. The majority of women will do well on this treatment, although a low percentage of cases (8–10%) will be complicated by pelvic abscess or thrombophlebitis [32, 49]. A rare but feared complication of endometrial infection is uterine rupture due to infection and necrosis. Analogous to infectious dehiscence of a fascial incision or surgical anastomosis, the myometrial incision can become infected and dehisce, resulting in uterine rupture. This condition is rare, with an estimated incidence of one in every 700–2400 cesarean births [50]. Uterine dehiscence may be suspected if the discontinuity is felt on bimanual examination. For this condition, MRI appears to have superior accuracy over CT, which may not be able to differentiate phlegmon or abscess in the region of the scar from true dehiscence [51]. Findings that have been described on MRI include a lack of apposition of the endometrium and serosa at the incision site and discontinuity of the myometrium with associated fluid collection, hematoma, or regions of low signal intensity suggestive of gas. Conservative management in cases of partial dehiscence has been proposed with some success, but most patients undergo hysterectomy.

Although smaller bladder wall hematomas have been seen in normal cesarean section, the presence of large hematomas (> 5 cm) has been associated with infective uterine rupture. Although detection of uterine discontinuity has been described on ultrasound, its sensitivity compared with that of MRI or CT has not been established in the literature.

Intraoperative complications of cesarean section are not rare, especially when the indication is emergent; one study found a 12.1% rate of intraoperative complications. The majority of these complications are blood loss and inadvertent injury to the uterus, along with cervical lacerations; injury to the bladder, ureter, and bowel are more rare (1%) [52]. Patients who require peripartum hysterectomy (i.e., hysterectomy performed immediately after a delivery or as part of a surgical delivery) need special attention.

Peripartum hysterectomy can be either planned, as in the case of suspected abnormal placentation, or emergent, because of bleeding complications. Peripartum hysterectomy is associated with much higher rates of intraoperative bleeding, urinary tract injuries, infections, and the need for additional operation or procedures [53, 54] (Fig. 9).

When imaging is requested to evaluate for postcesarean or other surgical complications, the standard contrast-enhanced CT of the abdomen and pelvis acquired in venous phase is often sufficient if the clinical concern is infection. If significant abdominal ascites is known or identified on the examination, obtaining a series in the excretory phase or performing a CT cystogram should be considered to evaluate for ureteral or bladder injury. If uterine dehiscence is suspected either clinically or on prior CT, contrast-enhanced pelvic MRI appears to be the superior diagnostic modality.


Delayed Cesarean Complications

In addition to the complications already discussed, there are complications of cesarean section that may not become apparent until weeks or months after delivery or until future pregnancies. These complications are primarily related to the uterine scar. Although longterm complications secondary to bowel or urinary tract injury are possible, they are rare.

 Endometriosis at Cesarean Section Scar

Endometriosis can develop in the abdominal incision site after cesarean section (also known as a scar endometrioma). Scar endometriosis is a rare complication with a reported incidence ranging from 0.03% to 1.5% [55]. However, it is still the most common manifestation of extragenital endometriosis [56]. This condition can have a variety of clinical presentations. Pain can be constant or cyclically related to the menstrual cycle. A palpable mass may or may not be present. Patients will often not have a  history of preexisting endometriosis, and delays in diagnosis are not rare.

On ultrasound, scar endometriomas can have a varied appearance based on size [55]. Small-to-moderate endometriomas in the abdominal wall are solid masses that have less-well-defined borders and are less homogeneously hypoechoic than pelvic endometriomas.

As they become larger (> 3 cm), more cystic regions and even less-well-defined borders have been described. Flow may be present on Doppler images in endometriomas of any size.

Postcesarean Placenta Accreta

The frequency of placenta accreta has been increasing in the last decades likely as a result of increased utilization of cesarean section. Accreta now affects one in 500 pregnancies; there is a high association with placenta previa as well [57]. Making the diagnosis of placenta accreta before the delivery is crucial because it has been shown to reduce maternal morbidity [58, 59].

At the time of the fetal anatomy scan (18–20 weeks), dedicated evaluation of the placenta and lower uterine segment is suggested for any patient with a history of repeated cesarean sections or with placenta previa. The sensitivity of ultrasound for the detection of accreta has been reported to be as high as 90% [58] and as low as 30% in a small study of 13 patients [60]. Several ultrasound features have been identified to suggest placenta accreta. The most sensitive sign is the presence of multiple placental lacunae [61]. The pathophysiology of lacunae are unknown, but they appear as hypoechoic foci that represent abnormal clusters of vessels with less well-defined borders than normal venous lakes and often will show turbulent flow on color Doppler images. They have been described as giving the placenta a “Swiss cheese” or “moth-eaten” appearance. Several additional signs have been described that include loss of the retroplacental clear space, gap in the retroplacental blood flow, thinning and distortion of the myometrium, irregularity of the bladder-uterine interface, and bulging of the placenta into the urinary bladder.

If placenta accreta is convincing on ultrasound, many clinicians will proceed with cesarean section and potential hysterectomy.
If the finding is unclear, MRI of the pelvis has been suggested as an alternative modality. The value of MRI has been variably reported: studies have shown superior sensitivity and specificity [62] and equivalent sensitivity and specificity to ultrasound, which may be helpful in indeterminate cases [63], but another study failed to show that the information obtained by MRI changed clinical management or outcomes [64]. The most well-described MRI findings for placental invasion are bulging of the placenta that distorts the normal uterine contour, the presence of dark intraplacental bands on T2-weighted images, and a heterogeneous appearance of the placenta [65] (Fig. 10).

Cesarean Scar Implantation or Ectopic Pregnancy

A pregnancy that develops within a prior cesarean section scar has previously been considered one of the rarest forms of abnormal implantation [66]. It has been suggested that these are not ectopic pregnancies because they can, in rare circumstances, be carried to term; however, these are considered as ectopic pregnancies for the purpose of this discussion because there is implantation outside of the normal decidua and a high rate of complications.

Although rare, the incidence of cesarean scar implantation appears to be increasing. Again, this is likely because of the increasing rate of cesarean delivery and increased recognition [67]. On ultrasound, care must be taken to definitively identify the gestational sac within the low transverse incision and not in the adjacent adnexa, which cansimulate this condition (Fig. 11). Recognition of ectopic pregnancy within the uterus itself is crucial because of the risk of uterine rupture and catastrophic bleeding.

Although the rate of cesarean scar ectopic pregnancy appears to be increasing, definitive guidelines for management have yet to be outlined. A variety of treatment options have been used, ranging from observation, medical treatment either systemic or locally injected, local resection utilizing hysteroscopy or laparoscopy, laparotomy either for local resection of the gestational sac or total hysterectomy, treatment with uterine artery embolization, to a combination of these approaches.



The significant overlap between the pathologic and physiologic changes of the postpartum uterus presents many difficulties to interpreting ultrasound examinations in the postpartum period. In addition, increasing rates of delivery by cesarean section have the possibility to increase the frequency of early and late complications. It is crucial for radiologists to be aware of the most common postpartum complications on which they will be asked to consult and the strengths and limitations of the various imaging modalities, so that they could assist in the appropriate care of these patients.

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