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Women’s Imaging • Clinical Perspective

Dibble and Lourenco Imaging of Unusual Implantations

Women’s Imaging Clinical Perspective

Imaging Unusual Pregnancy Implantations: Rare Ectopic and More

Elizabeth H. Dibble1 OBJECTIVE. The purpose of this article is to review key clinical issues and imaging fea- Ana P. Lourenco tures of unusual pregnancy implantations. Examples from different imaging modalities are pro- vided to increase interpreting physicians’ familiarity with the appearance and potential com- Dibble EH, Lourenco AP plications of unusual ectopic, cesarean scar, heterotopic, and rudimentary horn pregnancies. CONCLUSION. Abnormal pregnancy implantations are life-threatening. Interpreting physicians’ familiarity with the appearance of unusual pregnancy implantations is critical for early identification and initiation of appropriate therapy.

hen a female patient of repro- al sac is typically, but not always, visualized ductive age presents with a pos- on transvaginal ultrasound when the β-HCG itive pregnancy test, pain, and level is greater than 2000–3000 IU/L [3, 4]. W β , unusual preg- Although an empty and a -HCG level nancy implantations must be considered. Ec- less than 2000–3000 IU/L may represent an topic pregnancies, or implantations of a fer- intrauterine pregnancy too early to visualize, tilized egg outside the endometrial cavity, is in the differential diag- comprise 2% of all pregnancies [1] and are nosis for any patient with a positive β-HCG almost always nonviable. Although mortality test and an empty endometrial cavity. For rates have decreased over the past 3 decades, β-HCG levels greater than 2000–3000 IU/L, likely because of earlier recognition of ecto- the most likely diagnosis is a nonviable in- pic pregnancy with improvements in labora- trauterine pregnancy, but these levels should tory assay sensitivity, ultrasound technology, prompt a detailed search for an ectopic preg- and minimally invasive surgical options, ec- nancy, keeping in mind that a single β-HCG topic pregnancies remain an important cause level measurement can be very misleading of mortality among women of reproductive and that using β-HCG levels to guide man- age [1, 2]. Once a pregnancy is confirmed by agement can lead to erroneous treatment of the presence of β-HCG in serum or urine, intrauterine pregnancies [4]. transvaginal ultrasound is the imaging mo- Approximately 95% of ectopic pregnan- Keywords: abdominal ectopic pregnancy, cervical ectopic pregnancy, cesarean scar pregnancy, dality of choice for localization of early cies occur in the noninterstitial fallopian , interstitial ectopic pregnancy, pregnancy. Ultrasound can detect intrauter- tube [5] (Fig. 1). Ultrasound findings sug- ovarian ectopic pregnancy, rudimentary horn pregnancy ine and ectopic pregnancies, as well as cesar- gestive of a tubal ectopic pregnancy are well ean scar pregnancies and rudimentary horn documented and include an empty uterus, DOI:10.2214/AJR.15.15290 pregnancies. Ultrasound can also detect em- free fluid (particularly if echogenic), an ad- Received July 16, 2015; accepted after revision bryonic cardiac activity. Transabdominal ul- nexal mass or ring separate from the ova- May 23, 2016. trasound allows a larger FOV that includes ry, the ring of fire sign (although this is also the upper abdomen. Free fluid in the Morison commonly seen around a corpus luteum 1 Both authors: Department of Diagnostic Imaging, pouch or other sources of cyst), and—the most specific finding—extra- Alpert Medical School of Brown University, Rhode Island Hospital, Third Fl Main Bldg, 593 Eddy St, Providence, RI may be identified. uterine embryonic cardiac activity [3]. Intra- 02903. Address correspondence to E. H. Dibble A single measurement of β-HCG does not uterine fluid can be present with an ectopic ([email protected]). reliably distinguish between an intrauterine pregnancy, although it conforms to the shape and ectopic pregnancy or other unusually of the uterine cavity and does not have the AJR 2016; 207:1–13 Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved implanted pregnancy; however, correlation typical smooth-walled appearance of a ges- 0361–803X/16/2076–1 with serial β-HCG level measurements can tational sac [6]. A live intrauterine pregnan- be helpful for accurate interpretation of ul- cy does not exclude an ectopic pregnancy, © American Roentgen Ray Society trasound findings. An intrauterine gestation- particularly with assisted reproduction. Al-

AJR:207, December 2016 1 Dibble and Lourenco

though the frequency of combined normally cal mass with a T2-hypointense rim [12]. Of sarean scar pregnancy from a low intrauter- implanted intrauterine pregnancies and ecto- note, if a viable intrauterine pregnancy re- ine pregnancy, and an empty can help pic pregnancies (heterotopic pregnancies) in mains in the differential diagnosis, adminis- differentiate a cesarean scar pregnancy from the general population ranges from 1/2100 tration of gadolinium-based contrast agents a cervical ectopic pregnancy or to 1/30,000 pregnancies, the rate associated should be avoided whenever possible. in progress. Cesarean scar pregnancies will with assisted reproductive technology proce- show the absence of normal be- dures is 1–3% [3]. Complications and Management tween the bladder and the , dif- Unusual pregnancy locations include the Surgical treatment is generally reserved ferentiating them from cervicoisthmic preg- cervix, cesarean scars, the interstitial fallo- for patients with hemodynamic instability. nancies [20]. Transvaginal ultrasound is the pian tube, the ovary, and the abdominal cav- There are no consensus guidelines for opti- imaging test of choice; however, physicians ity. Because of their rarity, interpreting phy- mal treatment of the stable patient with a cer- interpreting the examinations may have seen sicians may be unfamiliar with the imaging vical ectopic pregnancy. For stable patients, cesarean scar pregnancies rarely if ever. In appearances of these unusual pregnancy ultrasound-guided transvaginal or transab- these situations, MRI may be useful for prob- sites. When an ectopic pregnancy is suspect- dominal local injection of potassium chloride lem solving when ultrasound is inconclusive ed and cannot be identified in the adnexa, a (KCl) or (MTX) with or with- in determining pregnancy location. MRI can detailed ultrasound evaluation of the cervix, out systemic MTX may be preferred because show thinning of myometrium between the anterior lower uterine segment (if the patient of the low risk of hemorrhage and to preserve gestational sac and the bladder [21]. has a history of cesarean delivery), cornua, future fertility [13]. Uterine artery ligation ovaries, and cul-de-sac should be performed. [14], uterine artery embolization [15], and Complications and Management mechanical tamponade [16] have been used Although there are case reports of full- Cervical Ectopic Pregnancies as adjuncts to medical and surgical manage- term cesarean scar pregnancies, implanta- Frequency and Risk Factors ment to treat or minimize the risk of hemor- tion in fibrous scar tissue rather than normal Cervical ectopic pregnancies comprise rhage. Expectant management with serial ul- myometrium can lead to pregnancy failure, fewer than 1% of ectopic pregnancies [5]. Pro- trasound imaging may be reserved for stable , hemorrhage, previa, posed risk factors include anatomic abnor- low-risk patients with uncertain diagnosis and morbidly adherent placenta [22]. Surgi- malities, fibroids, prior endocervical canal and low or decreasing β-HCG levels. Expect- cal intervention via or laparos- instrumentation, Asherman syndrome, intra- ant management in these cases should be lim- copy is indicated for patients with hemody- uterine device, and in vitro fertilization [7, 8]. ited to just a few days. namic instability. Although most centers still treat scar pregnancies as ectopic pregnancies Appearance and Differential Diagnosis Cesarean Scar Pregnancies given the substantial risks, other centers are A cervical ectopic pregnancy (Fig. 2) may Frequency and Risk Factors changing how they treat these pregnancies. be misdiagnosed as a miscarriage in prog- Cesarean scar pregnancies comprise up Michaels et al. [22] report that the possibili- ress or as a nabothian cyst, although the latter to 6% of abnormal implantations in wom- ty of delivering a live-born neonate is 62.5%, typically occurs in groups and beneath the en with a history of cesarean delivery [17]. but this carries a 37.5% risk of hysterecto- transformation zone. The hourglass uterus is Scar pregnancies are reported with increas- my due to placenta accreta. Thus, it may be an ultrasound sign of cervical ectopic preg- ing frequency in the literature [18] reflecting appropriate to counsel patients on expectant nancy that describes a smaller-than-dates increasing rates of cesarean deliveries. management with the risk of complications uterus with an enlarged cervix and narrow- of accreta versus surgical or medical man- ing at the internal os [9, 10]. A ballooned cer- Appearance and Differential Diagnosis agement to minimize the chance of hyster- vix and a closed internal os are also sugges- A cesarean scar pregnancy (Fig. 4) may be ectomy. For patients who undergo surgical or tive of cervical ectopic pregnancy [9]. The misdiagnosed as a low intrauterine pregnan- medical management, ultrasound-guided lo- sliding sac sign is the movement of a ges- cy, cervical ectopic pregnancy, or miscar- cal injection of MTX or KCl, with or with- tational sac against the endocervical canal riage in progress. Scar pregnancies share a out systemic MTX, and hysteroscopic surgi- and can be seen in a miscarriage in progress common histologic profile with early placen- cal excision were associated with the lowest but not a cervical ectopic pregnancy [11]. M- ta accreta and may have similar pathogenesis complication rate in one review [18]. Uterine mode ultrasound can document cardiac ac- by implanting where there is little or no in- artery embolization can be used before dila- tivity, clearly differentiating a cervical ecto- tervening decidual layer so that trophoblas- tation and curettage to decrease the risk of pic pregnancy from a miscarriage in progress tic tissue invades the surrounding scar and hemorrhage [23]. If the diagnosis is uncer- when present (Fig. 3). Doppler ultrasound myometrium [19]. Cesarean scar pregnan- tain, expectant management may be used for may also show increased surrounding vas- cies are sometimes referred to as cesarean stable low-risk patients with low or decreas- cularity suggestive of ectopic pregnancy. In scar ectopic pregnancies, and though they ing β-HCG levels. the stable patient, serial ultrasound may be are implanted on a region of defective or ab- helpful for clarification, though it should be sent decidua, they are implanted inside the Interstitial Ectopic Pregnancies limited to 2–3 days, at which point a conclu- uterus and thus are not ectopic pregnancies. Frequency and Risk Factors sive diagnosis should be possible. Although Cesarean scar pregnancies tend to be locat- Interstitial ectopic pregnancies implant in Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved it is rarely needed, MRI of cervical ectopic ed eccentrically in the anterior lower uter- the proximal-most portion of the fallopian pregnancies can show the hourglass sign and us just superior to the cervix. The eccentric tube surrounded by myometrium. They com- a lobulated heterogeneous enhancing cervi- anterior location can help differentiate a ce- prise approximately 2% of all ectopic preg-

2 AJR:207, December 2016 Imaging of Unusual Pregnancy Implantations

nancies [5, 24]. Possible risk factors for inter- KCl can preserve future fertility; ultrasound- brial end of the or rupture of stitial ectopic pregnancy include prior ectopic guided local injection of MTX or KCl alone a tubal ectopic pregnancy [38, 39]. Proposed pregnancy, prior (particularly allows continuation of a concomitant intra- risk factors are those of ectopic pregnancies ipsilateral salpingectomy), uterine anomalies, uterine pregnancy if present [13]. in general and include tubal damage, pelvic use of assisted reproductive technologies, and inflammatory disease, , and as- pelvic inflammatory disease [25, 26]. Ovarian Ectopic Pregnancies sisted reproduction [2, 40, 41]. Frequency and Risk Factors Appearance and Differential Diagnosis Ovarian ectopic pregnancies (Fig. 7) com- Appearance and Differential Diagnosis Interstitial pregnancies can be mistaken prise 1–3% of all ectopic pregnancies [5, 24, Early abdominal ectopic pregnancies may for normal intrauterine pregnancies, particu- 31] and up to 6% of such pregnancies in asso- be misdiagnosed as tubal if located in the larly normal intrauterine pregnancies located ciation with assisted reproductive technology adnexa. They can present at advanced gesta- eccentrically in the uterine cavity. Interstitial procedures [32]. tional age, even at term. A full-term abdomi- ectopic pregnancies (Figs. 5 and 6) are ec- nal ectopic pregnancy has been delivered by centrically located lateral to the round liga- Appearance and Differential Diagnosis laparotomy [42]. Late-term abdominal preg- ment and tend to be surrounded by less than In the absence of a yolk sac or fetal pole, nancies can resemble intrauterine pregnan- 5 mm of visible myometrium; normal intra- an ovarian ectopic pregnancy may be misdi- cies, rudimentary horn pregnancies, or uter- uterine pregnancies will have at least 5 mm agnosed as a or ruptured ine rupture. They may be associated with of surrounding myometrium on all sides and hemorrhagic cyst. Both ovarian ectopic preg- elevated maternal serum α-fetoprotein lev- are medial to the round ligament [27]. The nancies and corpus luteum cysts can have el, particularly when visceral implantation interstitial line sign is an ultrasound sign of marked peripheral vascularity (the ring of fire of the placenta is extensive [43]. Ultrasound that describes an echo- sign). Identification of a separate corpus lute- findings seen in abdominal ectopic pregnan- genic line extending from the superolateral um cyst can be helpful [33]. A wide echogen- cies include the absence of myometrial tissue to the center of the interstitial ic ring with a small internal echolucent area continuing from the uterus around the ges- gestational sac [28], though it can be diffi- has been described as a sign of an ovarian ec- tational sac, abnormal placentation, oligohy- cult to identify. Three-dimensional sonogra- topic pregnancy, and the absence of this sign dramnios, and unusual fetal lie [42]. A mis- phy is very helpful for differentiating inter- may be secondary to rupture [31]. Distal tub- shapen gestational sac and flattened placenta stitial pregnancies from normal intrauterine al ectopic pregnancies in close approximation may help distinguish an abdominal ectopic pregnancies. Three-dimensional ultrasound to the ovary may be misdiagnosed as ovarian from a late-presenting tubal ectopic pregnan- is the best way to show the entire uterine cav- ectopic pregnancies. Free movement between cy, which is more likely to show a rounded ity and an overview of the cornua, showing the ovary and an on palpation gestational sac and crescentic placenta [44]. that an interstitial ectopic pregnancy is im- (the sliding organs sign) [34] can be useful in Careful sonographic evaluation of the myo- planted outside the uterine cavity but within separating intra- from extraovarian masses metrium can also help distinguish a late-pre- the interstitial portion of the fallopian tube in but is not helpful in distinguishing between senting abdominal ectopic pregnancy from the myometrium [29]. If 3D ultrasound is not ovarian ectopic pregnancies, corpus luteum an intrauterine gestation. The embryo can available or if the sonographer or interpret- cysts, and hemorrhagic ovarian cysts. implant on the omentum, serosa, or pouches ing physician has limited experience with 3D surrounding the uterus and adnexa; the bow- ultrasound or interstitial ectopic pregnancies, Complications and Management el; abdominal organs; the retroperitoneum; MRI can confirm the diagnosis of interstitial Ovarian ectopic pregnancies are often and the abdominal wall [45]. RBCs tagged pregnancy with surrounding myometrium treated surgically with oophorectomy or with 99mTc have been used to locate the pla- and an intact junctional zone between the wedge resection [35] and may be diagnosed centa in an intraabdominal pregnancy after mass and the endometrial cavity [30]. definitively only at surgery. By American nonvisualization using ultrasound and arte- Society for Reproductive Medicine commit- riography [46], and CT has been used to lo- Complications and Management tee opinion, MTX is not recommended as a cate a pregnancy after negative Because interstitial pregnancies are sur- first-line treatment of ovarian ectopic preg- [47]. MRI can confirm lack of myometrium rounded by myometrium, they can expand nancies [36]. around an abdominal ectopic pregnancy [48] and present at later stages than other tub- and can clarify anatomic relationships, vas- al pregnancies, potentially leading to cata- Abdominal Ectopic Pregnancies cular supply, and placental adherence [49], strophic hemorrhage. The proximity of uter- Frequency and Risk Factors which can help with preoperative planning ine and ovarian vessels to the cornua makes Abdominal ectopic pregnancies (Figs. 8 and prediction of potential complications the risk of significant hemorrhage particu- and 9) are intraperitoneal pregnancies ex- during or after medical or surgical treatment. larly high. Ruptured interstitial ectopic preg- cluding tubal and ovarian pregnancies. In- nancies will typically require laparotomy. traligamentous pregnancy may be consid- Complications and Management Laparoscopy, hysteroscopic suction, and ered an extraperitoneal form of abdominal As for ovarian ectopic pregnancies, MTX uterine artery embolization have been used ectopic pregnancy. Abdominal ectopic preg- is not recommended as a first-line treatment successfully for nonruptured interstitial ec- nancies comprise approximately 1% of all of abdominal ectopic pregnancies by Ameri- Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved topic pregnancies [27]. For stable patients, ectopic pregnancies [5, 24, 37] and have a can Society for Reproductive Medicine com- medical treatment with systemic MTX or ul- mortality rate of 5% [37]. They can result mittee opinion [36], but early gestations may trasound-guided local injection of MTX or from extrusion of the gestation from the fim- be amenable to primary medical treatment

AJR:207, December 2016 3 Dibble and Lourenco

with local administration of MTX [45, 47], al ectopic pregnancies [63]. Tsafrir et al. [64] pregnancies [70]. Rarely, an undiagnosed reserving surgery for patients for whom med- proposed the following criteria for diagnos- and unruptured rudimentary horn pregnan- ical management fails. There are multiple ing rudimentary horn pregnancies by ultra- cy continues to term and is delivered by ce- case reports of successful treatment via lapa- sound: pseudopattern of an asymmetric bi- sarean section [71]. Treatment of rudimenta- roscopy [41, 50, 51]. In the setting of implan- cornuate uterus, absent visual continuity ry horn pregnancies has consisted of various tation on a vascular surface, laparotomy may between the and the lumen of surgical techniques to remove the pregnancy be preferentially performed to allow rapid the pregnant horn, and the presence of myo- and the rudimentary horn to prevent future hemostasis. For all surgical approaches, care- metrial tissue surrounding the gestational occurrences [64]. Case reports of attempt- ful consideration must be given to placental sac (Fig. 10). In a prospective observational ed medical management exist, sometimes in extraction or plan to leave in situ, and tech- study, Mavrelos et al. [63] reported that the cases of misdiagnosis [72], but the rudimen- niques such as placental blood supply liga- critical sonographic finding was detection of tary horns are eventually excised [72, 73]. tion, preoperative arterial embolization, and a single interstitial tube in an empty uterus MRI can be helpful in predicting outcome MTX administration have been used to mini- adjacent to the pregnancy, which could be and surgical morbidity; placenta accreta sug- mize the risk of hemorrhage [45, 52, 53]. identified in both early and advanced preg- gests poorer outcomes, which can help guide nancies. They also found that free mobil- treatment planning [68]. Rudimentary Horn Pregnancies ity of a rudimentary horn pregnancy and a Frequency and Risk Factors vascular pedicle joining the gestational sac Heterotopic Pregnancies Müllerian duct anomalies result from ab- to the unicornuate uterus were helpful signs Frequency and Risk Factors normal development of the paired mülleri- [63]. Thin surrounding myometrium and pla- A heterotopic pregnancy is an intrauterine an ducts, which normally form the uterus, centa accreta, when present, are other clues pregnancy plus one or more abnormally im- fallopian tubes, cervix, and proximal vagi- to the presence of a rudimentary horn preg- planted pregnancies, including noninterstitial na during weeks 6–12 of embryogenesis. A nancy [64]. Three-dimensional ultrasound is tubal ectopic pregnancies and the unusual im- unicornuate uterus results from the normal a reproducible method of diagnosing mülle- plantation sites described in the previous sec- development of one müllerian duct and the rian duct anomalies [65] and, because of its tions. The frequency of a spontaneous het- failure of the contralateral müllerian duct to relative speed and low cost compared with erotopic pregnancy in the general population elongate normally between weeks 6 and 9 of MRI, may be the imaging test of choice for ranges from 1/2100 to 1/30,000 pregnancies embryogenesis. The prevalence of müllerian evaluating suspected müllerian duct anoma- [3], with the 1/30,000 estimate based on a the- duct anomalies in the general population is lies. It can be helpful in characterizing the oretic calculation [74]; the frequency associat- about 5% [54]. Unicornuate uteri comprise contour of the uterus and the presence of a ed with assisted reproductive technology pro- 10–20% of müllerian duct anomalies [55]; rudimentary horn [56]. MRI is also highly cedures, however, is much higher at 1–3% [75]. approximately one-third of these are isolated accurate for diagnosing and characterizing The most important risk factor is a history of unicornuate uteri with no rudimentary con- müllerian duct anomalies [66] and can reveal assisted reproduction, particularly when multi- tralateral horn, approximately one-third have the contour of the uterus, the unicornuate ple embryos are transferred; another risk fac- a rudimentary horn that does not contain any uterus’s connection to the rudimentary horn, tor is a history of tubal disease [76]. Although endometrium, and approximately one-third cavitary communication [64], and continuity most patients with heterotopic pregnancies will have a rudimentary horn that contains endo- of the rudimentary horn lumen with the cer- have at least one risk factor, nearly one-third of metrium. The cavities of rudimentary horns vix [67]. MRI can be helpful in evaluating for patients in one study had no risk factors [76]. that contain endometrium can communi- abnormal placentation, evaluating the vascu- cate with the endometrium of the contralat- lar supply of the pregnancy [68], and in sur- Appearance and Differential Diagnosis eral horn (approximately one-third of endo- gical planning [64]. The appearance on ultrasound is that of metrium-containing rudimentary horns) or a normal intrauterine pregnancy plus one or not (approximately two-thirds of endometri- Complications and Management more abnormally implanted pregnancies. The um-containing rudimentary horns) [56]. The Rudimentary horn pregnancies have an abnormal implantation is most often a tub- frequency of rudimentary horn pregnancies increased risk of miscarriage, preterm la- al ectopic pregnancy [76] (Fig. 11). Ectopic has been reported at 1/76,000 and 1/100,000 bor, and uterine rupture [69], which can be pregnancy may be eliminated from the dif- pregnancies [57, 58]. Eighty-five percent of life-threatening. Fifty percent of rudimenta- ferential diagnosis once an intrauterine ges- rudimentary horn pregnancies occur in non- ry horn pregnancies rupture, 80% before the tation has been documented, but for patients communicating rudimentary horns [59]. third trimester [59]. The maternal mortality with risk factors for heterotopic pregnancy, a rate has improved dramatically over the past detailed search for an additional implantation Appearance and Differential Diagnosis century and is currently less than 0.5% [59]. must be performed. In patients who have un- An enlarging gravid rudimentary horn can Placenta accreta and thinned myometrium dergone ovarian hyperstimulation, enlarged make detailed anatomic evaluation difficult; predispose to uterine rupture [64], although ovaries can render the search for an ectopic rudimentary horn pregnancies can be mis- varying amounts of myometrium in the rudi- pregnancy more difficult [77]. Depending taken for pregnancies [60], mentary horn can accommodate the growing on the location of the abnormally implanted interstitial ectopic pregnancies [61], and ab- often into the second and sometimes pregnancy, the differential diagnosis may in- Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved dominal ectopic pregnancies [62]. Early in even the third trimester. When diagnosis is clude a normal intrauterine pregnancy plus a the pregnancy, rudimentary horn pregnan- delayed, ruptured rudimentary horn preg- nabothian cyst (cervical ectopic pregnancy), cies can be mistaken for noninterstitial tub- nancies can present as abdominal ectopic a corpus luteum or hemorrhagic

4 AJR:207, December 2016 Imaging of Unusual Pregnancy Implantations

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32. Marcus SF, Brinsden PR. Primary ovarian preg- 46. Martin B, Payan JM, Jones JS, Buse MG. uterine horn. Eur J Obstet Gynecol Reprod Biol nancy after in vitro fertilization and embryo trans- Placental localization in us- 1994; 56:143–145 fer: report of seven cases. Fertil Steril 1993; ing technetium-99m-labeled red blood cells. 62. Holden R, Hart P. First-trimester rudimentary 60:167–169 J Nucl Med 1990; 31:1106–1109 horn pregnancy: prerupture ultrasound diagnosis. 33. Tsubamoto H, Wakimoto Y, Wada R, Takeyama 47. Anderson PM, Opfer EK, Busch JM, Obstet Gynecol 1983; 61:56S–58S R, Ito Y, Harada K. Detection of unruptured ovar- Magann EF. An early abdominal wall ectopic 63. Mavrelos D, Sawyer E, Helmy S, Holland ian pregnancy subsequently successfully treated pregnancy successfully treated with ultrasound TK, Ben-Nagi J, Jurkovic D. Ultrasound diagnosis by conservative laparoscopic surgery: a case re- guided intralesional methotrexate: a case report. of ectopic pregnancy in the non-communicating port and review of the literature. Clin Exp Obstet Obstet Gynecol Int 2009; 2009:247452 horn of a unicornuate uterus (cornual pregnancy). Gynecol 2013; 40:604–606 48. Parker RA, 3rd, Yano M, Tai AW, ­Friedman Ultrasound Obstet Gynecol 2007; 30:765–770 34. Jurkovic D, Mavrelos D. Catch me if you M, Narra VR, Menias CO. MR imaging findings of 64. Tsafrir A, Rojansky N, Sela HY, Gomori scan: ultrasound diagnosis of ectopic pregnancy. ectopic pregnancy: a pictorial review. RadioGraphics JM, Nadjari M. Rudimentary horn pregnancy: Ultrasound Obstet Gynecol 2007; 30:1–7 2012; 32:1445–1460; discussion, 1460–1442 first-trimester prerupture sonographic diagnosis 35. Raziel A, Schachter M, Mordechai E, Friedler S, 49. Lockhat F, Corr P, Ramphal S, Moodley J. The and confirmation by magnetic resonance imaging. 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Abdominal preg- Renzo GC. Early ultrasonographic diagnosis and lapa- and clinical diagnosis. AJR 2007; 189:1294–1302 nancy in the United States: frequency and mater- roscopic treatment of abdominal pregnancy. Eur J 67. Siwatch S, Mehra R, Pandher DK, Huria A. Rudi- nal mortality. Obstet Gynecol 1987; 69:333–337 Obstet Gynecol Reprod Biol 2004; 113:103–105 mentary horn pregnancy: a 10-year experience 38. Giannopoulos T, Katesmark M. Ruptured 52. Cardosi RJ, Nackley AC, Londono J, Hoffman and review of literature. Arch Gynecol Obstet tubal ectopic pregnancy with secondary implanta- MS. Embolization for advanced abdominal preg- 2013; 287:687–695 tion in the pouch of Douglas. J Obstet Gynaecol nancy with a retained placenta: a case report. 68. Ozeren S, Caliskan E, Corakci A, Ozkan S, 2004; 24:199–200 J Reprod Med 2002; 47:861–863 Demirci A. Magnetic resonance imaging and an- 39. Rana P, Kazmi I, Singh R, et al. Ectopic pregnancy: 53. Jazayeri A, Davis TA, Contreras DN. Diagnosis giography for the prerupture diagnosis of rudi- a review. Arch Gynecol Obstet 2013; 288:747–757 and management of abdominal pregnancy: a case mentary uterine horn pregnancy. Acta Radiol 40. Perkins KM, Boulet SL, Kissin DM, Jamieson DJ; report. J Reprod Med 2002; 47:1047–1049 2004; 45:878–881 National ART Surveillance (NASS) Group. Risk 54. Chan YY, Jayaprakasan K, Zamora J, Thornton 69. Jayasinghe Y, Rane A, Stalewski H, Grover S. The of ectopic pregnancy associated with assisted re- JG, Raine-Fenning N, Coomarasamy A. The prev- presentation and early diagnosis of the rudimen- productive technology in the United States, 2001- alence of congenital uterine anomalies in un- tary uterine horn. Obstet Gynecol 2005; 2011. Obstet Gynecol 2015; 125:70–78 selected and high-risk populations: a systematic 105:1456–1467 41. Srinivasan A, Millican S. Laparoscopic review. Hum Reprod Update 2011; 17:761–771 70. Rana A, Gurung G, Rawal S, Bista KD, Adhukari management of an abdominal pregnancy. Case 55. Junqueira BL, Allen LM, Spitzer RF, Lucco KL, S, Ghimire RK. Surviving 27 weeks fetus expelled Rep Obstet Gynecol 2014; 2014:562731 Babyn PS, Doria AS. Müllerian duct anomalies out of the ruptured rudimentary horn and detected 42. Varma R, Mascarenhas L, James D. Suc- and mimics in children and adolescents: correla- a month later as a secondary abdominal pregnan- cessful outcome of advanced abdominal pregnan- tive intraoperative assessment with clinical imag- cy. J Obstet Gynaecol Res 2008; 34:247–251 cy with exclusive omental insertion. Ultrasound ing. RadioGraphics 2009; 29:1085–1103 71. Cheng C, Tang W, Zhang L, et al. Unruptured Obstet Gynecol 2003; 21:192–194 56. Troiano RN, McCarthy SM. Müllerian duct pregnancy in a noncommunicating rudimentary 43. Shumway JB, Greenspoon JS, Khouzami AN, anomalies: imaging and clinical issues. Radiology horn at 37 weeks with a live fetus: a case report. Platt LD, Blakemore KJ. alpha fe- 2004; 233:19–34 J Biomed Res 2015; 29:83–86 toprotein (AFAFP) and maternal serum alpha fe- 57. Johansen K. Pregnancy in a rudimentary horn: two 72. Handa Y, Hoshi N, Yamada H, et al. Tubal preg- toprotein (MSAFP) in abdominal pregnancies: case reports. Obstet Gynecol 1969; 34:805–808 nancy in a unicornuate uterus with rudimentary correlation with extent and site of placental im- 58. Nahum GG. Rudimentary uterine horn pregnan- horn: a case report. Fertil Steril 1999; 72:354–356 plantation and clinical implications. J Matern cy: a case report on surviving twins delivered 73. Edelman AB, Jensen JT, Lee DM, Nichols MD. ­Fetal Med 1996; 5:120–123 eight days apart. J Reprod Med 1997; 42:525–532 Successful medical of a pregnancy with- 44. Liu J, Khan A, Johnson S, Grigorian C, Li T. The 59. Nahum GG. Rudimentary uterine horn pregnan- in a noncommunicating rudimentary uterine horn. usefulness of gestational sac and placental sono- cy: the 20th-century worldwide experience of 588 Am J Obstet Gynecol 2003; 189:886–887 graphic morphology in differentiating between cases. J Reprod Med 2002; 47:151–163 74. DeVoe RW, Pratt JH. Simultaneous intrauterine second-trimester tubal and abdominal pregnancy: 60. Daskalakis G, Pilalis A, Lykeridou K, Antsaklis and extrauterine pregnancy. Am J Obstet Gynecol case report and a review of literature. J Clin A. Rupture of noncommunicating rudimentary 1948; 56:1119–1126 U­ltrasound 2014; 42:162–168 uterine horn pregnancy. Obstet Gynecol 2002; 75. Fernandez H, Gervaise A. Ectopic pregnancies Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved 45. Poole A, Haas D, Magann EF. Early abdominal 100:1108–1110 after treatment: modern diagnosis and ectopic pregnancies: a systematic review of the lit- 61. Tsuda H, Fujino Y, Umesaki N, Yamamoto K, therapeutic strategy. Hum Reprod Update 2004; erature. Gynecol Obstet Invest 2012; 74:249–260 Ogita S. Preoperative diagnosis of a rudimentary 10:503–513

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76. Talbot K, Simpson R, Price N, Jackson 80. Bedaiwy MA, Volsky J, Lazebnik N, Liu J. Lapa- 2012; 120:449–452 SR. Heterotopic pregnancy. J Obstet Gynaecol roscopic single-site linear salpingostomy for the 84. Refaat B, Dalton E, Ledger WL. Ectopic pregnan- 2011; 31:7–12 management of heterotopic pregnancy: a case re- cy secondary to -embryo trans- 77. Soriano D, Shrim A, Seidman DS, Goldenberg M, port. J Reprod Med 2014; 59:522–524 fer: pathogenic mechanisms and management Mashiach S, Oelsner G. Diagnosis and treatment of het- 81. Tsakos E, Tsagias N, Dafopoulos K. Suggested strategies. Reprod Biol Endocrinol 2015; 13:30 erotopic pregnancy compared with ectopic pregnancy. method for the management of heterotopic cervi- 85. Sijanovic S, Vidosavljevic D, Sijanovic I. Metho- J Am Assoc Gynecol Laparosc 2002; 9:352–358 cal pregnancy leading to term delivery of the intra- trexate in local treatment of cervical heterotopic 78. Clayton HB, Schieve LA, Peterson HB, Jamieson uterine pregnancy: case report and literature re- pregnancy with successful perinatal outcome: case DJ, Reynolds MA, Wright VC. A comparison of view. J Minim Invasive Gynecol 2015; 22:896–901 report. J Obstet Gynaecol Res 2011; 37:1241–1245 heterotopic and intrauterine-only pregnancy out- 82. Prorocic M, Vasiljevic M, Tasic L, Smiljkovic O. 86. Baxi A, Kaushal M, Karmalkar H, Sahu P, Kadhi comes after assisted reproductive technologies in Treatment of early heterotopic interstitial (cornu- P, Daval B. Successful expectant management of the United States from 1999 to 2002. Fertil Steril al) gestation with subsequent delivery of an intra- tubal heterotopic pregnancy. J Hum Reprod Sci 2007; 87:303–309 uterine pregnancy: case report. Clin Exp Obstet 2010; 3:108–110 79. Soriano D, Vicus D, Schonman R, et al. Long- Gynecol 2012; 39:396–398 87. Woodfield CA, Lazarus E, Chen KC, term outcome after laparoscopic treatment of het- 83. Allison JL, Aubuchon M, Leasure JD, Schust DJ. Mayo-Smith WW. Abdominal pain in pregnancy: erotopic pregnancy: 19 cases. J Minim Invasive Hyperosmolar glucose injection for the treatment diagnoses and imaging unique to pregnancy—re- Gynecol 2010; 17:321–324 of heterotopic ovarian pregnancy. Obstet Gynecol view. AJR 2010; 194:[web]WS14–WS30

A B

Fig. 1—32-year-old woman with tubal ectopic pregnancy who presented with left lower quadrant abdominal pain and palpable adnexal mass on physical examination. A, Sagittal gray-scale endovaginal ultrasound image shows empty endometrial cavity (arrow). B, Gray-scale endovaginal ultrasound image through left adnexa shows mass (arrow), separate from left ovary, containing yolk sac and embryonic pole. C, M-mode ultrasound image shows cardiac activity within this live ectopic pregnancy. Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved C

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Fig. 2—39-year-old woman with suspected cervical ectopic pregnancy who presented with abnormally increasing β-HCG levels and pain. Sagittal gray-scale transvaginal ultrasound image shows hourglass-shaped gestational sac (within calipers) containing yolk sac (arrow) located in cervix. Differential diagnosis considerations include cervical ectopic pregnancy or miscarriage in progress. In this case, real-time imaging showed sac was not mobile within endocervical canal, favoring ectopic pregnancy over miscarriage in progress.

A B

Fig. 3—23-year-old woman with cervical ectopic pregnancy who presented with abnormally increasing β-HCG levels after receiving methotrexate treatment for presumed tubal ectopic pregnancy. A, Sagittal gray-scale endovaginal ultrasound image shows normal endometrium (white arrow) and gestational sac with yolk sac and embryo within cervix (black

Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved arrow). B, Transverse gray-scale endovaginal ultrasound image shows gestational sac (arrow) and surrounding nabothian cysts in cervix. C, M-mode ultrasound image shows cardiac activity in this live cervical ectopic pregnancy. C

8 AJR:207, December 2016 Imaging of Unusual Pregnancy Implantations

A B Fig. 4—39-year-old woman with cesarean section scar pregnancy. A and B, Sagittal gray-scale transabdominal (A) and transvaginal (B) ultrasound images show eccentrically located gestational sac (arrow, A) low within anterior uterine wall, at expected site of cesarean section scar. C, Unenhanced sagittal T2-weighted MR image shows mass (arrow) centered in myometrium at expected site of cesarean section scar. Patient was treated with intraoperative injection of methotrexate into gestational sac.

C

A B Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved Fig. 5—36-year-old woman with interstitial ectopic pregnancy. A, Sagittal gray-scale transvaginal ultrasound image of uterus shows no intrauterine pregnancy (endometrium marked with calipers). B, Sagittal gray-scale transvaginal ultrasound image through right cornua shows exophytic mass (within calipers) with yolk sac and live embryo. No definite myometrium is visible surrounding gestational sac. Patient was treated with methotrexate. (Fig. 5 continues on next page)

AJR:207, December 2016 9 Dibble and Lourenco

Fig. 5 (continued)—36-year-old woman with interstitial ectopic pregnancy. C, Several days later, patient presented with increasing pain. Axial image from contrast-enhanced CT obtained at that time shows hemoperitoneum (asterisk) surrounding ruptured hypervascular interstitial ectopic pregnancy.

C

Fig. 6—36-year-old woman with interstitial ectopic pregnancy. A, Sagittal gray-scale transvaginal ultrasound image of uterus shows normal endometrium (arrow). B, Transverse gray-scale transvaginal ultrasound image shows gestational sac in region of right cornua (arrow) without clear myometrium surrounding gestational sac. C, Color Doppler transvaginal ultrasound image shows peripheral hypervascularity around this gestational sac. Diagnosis of interstitial ectopic pregnancy was made, and patient was treated surgically. A Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved

B C

10 AJR:207, December 2016 Imaging of Unusual Pregnancy Implantations

A B

C D Fig. 7—37-year-old woman with intraovarian ectopic pregnancy who became pregnant via assisted reproductive technologies. A, Sagittal gray-scale ultrasound image of uterus shows normal endometrium (arrow) and no intrauterine pregnancy. B, Gray-scale ultrasound image of left ovary shows intraovarian gestational sac with yolk sac (arrow). C, Color Doppler ultrasound image of intraovarian gestational sac shows peripheral hypervascularity. D, M-mode ultrasound image shows cardiac activity in embryo. Real-time examination showed gestational sac and ovary could not be separated, which was diagnostic of intraovarian ectopic pregnancy. FHR = fetal heart rate. Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved

AJR:207, December 2016 11 Dibble and Lourenco

A B Fig. 8—38-year-old woman with abdominal ectopic pregnancy. (Reprinted from [87]) A, Transabdominal gray-scale ultrasound image shows uterus (white arrow) with empty uterine cavity (black arrow). B, Sagittal transabdominal gray-scale ultrasound image shows uterine fundus (white arrow) and fetus superior to uterine fundus (black arrow) consistent with abdominal ectopic pregnancy.

Fig. 9—25-year-old woman with abdominal ectopic pregnancy who presented with pain, bleeding, and abnormally increasing β-HCG levels. Transvaginal gray- scale ultrasound image through pelvis shows mass in cul-de-sac with adjacent free fluid. Intrauterine pregnancy was not present. Mass in cul-de-sac was confirmed to be abdominal ectopic pregnancy at surgery, because both fallopian tubes were normal. Early intraabominal ectopic pregnancies are generally not distinguishable from more common intratubal ectopic pregnancies. Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved

12 AJR:207, December 2016 Imaging of Unusual Pregnancy Implantations

A B Fig. 10—27-year-old woman with rudimentary horn pregnancy who presented with pain and positive β-HCG level. A, Transverse transabdominal gray-scale ultrasound image through uterus shows two uterine horns (white arrows) with saclike structure in left horn (black arrow), which appears asymmetrically smaller than right horn. B, Transverse transvaginal gray-scale ultrasound image through uterus also shows these findings and shows myometrial tissue surrounding gestational sac arrows( ) and no communication between two cavities. Real-time scanning showed no continuity between cervical canal and lumen of pregnant horn. Surgical resection confirmed unicornuate uterus with pregnancy in noncommunicating rudimentary horn.

A B

Fig. 11—32-year-old woman with heterotopic pregnancy and history of assisted reproduction who presented with pain. A, Transverse transvaginal gray-scale ultrasound image through uterus shows intrauterine gestation with yolk sac visible (black arrow) and free fluid in cul-de- sac (white arrow). B, Transverse transvaginal gray-scale ultrasound image through left adnexa shows 6.6-cm mass (between calipers). C, Sagittal transvaginal gray-scale ultrasound image through left adnexa shows Downloaded from www.ajronline.org by Dartmouth - Hitchcock Med Ctr on 08/31/16 IP address 130.189.10.65. Copyright ARRS. For personal use only; all rights reserved same mass (white arrow) plus adjacent complex free fluid (black arrow). Findings are highly suspicious for heterotopic pregnancy, which was confirmed surgically in ampullary portion of left fallopian tube. C

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