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CURRENTOPINION Management of the adnexal mass in pregnancy

William Goha, Justin Bohrerb, and Ivica Zaludc

Purpose of reviewWith the increased use of ultrasonography in the first trimester, up to 1% of all pregnancies are diagnosedwith an adnexal mass. Yet, the management of asymptomatic adnexal masses in pregnancy continues tobe controversial as management guidelines are mainly based on casecontrol or observational studies. Thepurpose of this article was to review the recent literature and provide clinical guidance on patientmanagement.

Recent findingsThis review will highlight the increasing sensitivity of ultrasound imaging in diagnosing the rare malignantlesion, allowing for antenatal expectant management of benign asymptomatic adnexal masses untildelivery or postpartum. The recent literature also highlights the well tolerated use of laparoscopy for theantenatal removal of suspicious or symptomatic masses and that expectant management of asymptomaticmasses does not increase the risk of adverse pregnancy outcomes.

SummaryMost adnexal masses are benign and ultrasound characteristics can help guide the assessment ofasymptomatic ovarian masses. When surgical management is chosen, laparoscopy can be safelyperformed in pregnancy. Ovarian torsion is a complication for persistent masses in pregnancy.

Keywordsadnexal mass, expectant management, laparoscopy, pregnancy

INTRODUCTIONThe incidental finding of an adnexal mass in preg-nancy has become a more common clinicalscenario, and the reported incidence of ovarianmasses in pregnancy has increased with the routineuse of ultrasonography [1]. Although most ovarianmasses are self-limiting, a minority will go on todevelop complications that may have an adverseeffect onmaternal or fetal health. Thus, the presenceof a mass is relevant to the practicing clinician.Because of the unique circumstances of pregnancy,there is controversy surrounding the diagnosticevaluation and appropriate management of thesepatients.

INCIDENCEThe reported incidence of adnexal masses in preg-nancy varies widely and is dependent on the criteriadefining themass that includes size and longevity ofthe lesion [2,3]. An overwhelming majority of smallcysts discovered in the first trimester will be corpusluteum or other functional cysts and will regressspontaneously [4]. In a study of over 10000 preg-nancies, Glanc et al. [5] found a 5.3% incidence of

simple ovarian cysts defined as greater than or equalto 3 cm in the first trimester. Only 1.5% of patientsin this cohort had persistent cysts beyond 14 weeksgestation. Goh et al. [6&&] analyzed 24868 pregnan-cies and found a 4.9% incidence of adnexal massesin pregnancy. A large (defined as greater than orequal to 5 cm) persistent mass was observed in only0.7% of individuals in this population. Bernhardet al. [4] analyzed over 18000 obstetrical ultrasoundsand found a rate of 2.3% incidence of adnexalmasses in pregnancy. A total of 75% were simplecysts measuring less than 5 cm. No adverse out-comes (defined as surgical intervention, ovariantorsion or malignancy) were associated with thesepregnancies. The remainder were large and complex

aHawaii Permanente Medical Group, Honolulu, Hawaii, bUniversity ofWisconsin School of Medicine, Madison,Wisconsin and cJohn A. BurnsSchool of Medicine, University of Hawaii, Honolulu, Hawaii, USA

Correspondence toWilliamGoh, MD, MSCR, MoanaluaMedical Center,3288 Moanalua Road, Honolulu, HI 96819, USA. E-mail: wgoh@hawaii.edu

Curr Opin Obstet Gynecol 2014, 26:4953

DOI:10.1097/GCO.0000000000000048

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REVIEW

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masses, and there was an over 90% spontaneousresolution rate with observation in this subgroup.

DIFFERENTIAL DIAGNOSISAlthough the majority of adnexal masses resolvewithout intervention, some persist and can beassociated with adverse outcomes. Ultrasoundcharacteristics of a persistent mass can aid in gen-erating a differential diagnosis (Table 1).

Most simple cysts are physiological or func-tional cysts, or unilocular serous or mucinouscystadenomas [7]. Complex ultrasound featurescan be associated with corpus luteum, teratomas,endometriomas, or theca lutein cysts. Solid massesmay represent fibromas or leiomyomas. Data fromseveral series are remarkably consistent in predictingadnexal disease [6&&,7]. The most common adnexalmasses found in pregnancy are dermoids, followedby cystadenomas.

The vast majority of masses in pregnancy arebenign, but up to 5% do represent a malignanttumor [8]. Using a population-based review of over3 million deliveries, Smith et al. found that ovariancancer was the fifth most common malignancy

diagnosed during pregnancy (0.04 cases per 1000pregnancies) after breast, thyroid, and Hodgkinsdisease. Leiserowitz et al. [9] analyzed Californiahospital discharge records from 1991 to 1999 andfound a 0.93% incidence of ovarian malignancy inpregnancy or approximately 1 cancer per 56000deliveries. A total of 1.25% of these masses wereborderline tumors. Therefore, the cumulative inci-dence of clinically relevant ovarian neoplasms inpregnancy was 1 in 23800 deliveries. The summarystages of ovarian cancer and borderline tumors werelocalized 65.5%/81.7%, regional 6.9%/7.8%, remote23%/4.4%, and unknown 4.6%/6.1%, respectively.The specific maternal mortality rate in this cohortwas 4.7%. When the Leiserowitz cohort wasexamined pathologically, 51% were epithelial(both malignant and borderline) [9]. Germ celltumors accounted for 39% of this cohort, and wereprimarily dysgerminomas andmalignant teratomas.The lower stage and higher proportion of germ celltumors are in line with the generally younger age ofpregnant women.

DIAGNOSTIC MODALITIESAdnexal masses in pregnancy can be evaluated asgiven below:

UltrasoundUltrasound (both transvaginal and transabdominal)is often the best first-line imaging modality used toevaluate adnexal masses in pregnancy [10&]. Therehave been numerous scoring systems proposed todiagnose ovarian malignancy, but no single systemhas been shown to be sufficiently accurate [11].Sonographic features associated with an increasedrisk of malignancy include size greater than 7 cm,solid components or heterogeneous/complexappearance, excrescences/papillary projections,internal septations, bilaterality, irregular borders,solid components, increased vascularity, low resist-ance blood flow, and ascites [11]. Zanetta et al. [12]prospectively followed 82 cysts in 79 pregnantwomen. Expectant management was used exceptin symptomatic patients or suspected malignancy(which they defined as solid parts, irregular capsuleor border, ascites, and irregular vascularization).This group showed that ultrasound allows for thedifferential diagnosis of benign complexmasses andeven borderline-like tumors. Similarly, other studieshave shown that the more complex a mass is onultrasound (septations and solid components), thehigher the risk of malignancy [13]. Conversely,Whitecar et al. [3] showed that 89 of 91 massesdiagnosed with a simple cyst on ultrasound were

KEY POINTS

! Most adnexal masses in pregnancy are benign.! When malignant, adnexal masses in pregnancy tendto be low stage and nonepithelial.

! Laparoscopy in the second trimester can be safelyperformed for persistent masses.

! Ovarian torsion may complicate patients who aremanaged expectantly.

Table 1. Differential diagnosis of an adnexal mass inpregnancy

Benign Malignant

Corpus luteum Germ cell tumors

Simple cyst Epithelial tumors

Hemorrhagic cyst Low malignant potential

Dermoid Invasive

Cystadenoma Sex cord stromal tumors

Endometrioma

Pedunculated fibroid

Ovarian hyperstimulation

Hydrosalpinx

Paraovarian/tubal cyst

Theca lutein cyst

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found to be benign when examined pathologically.Doppler flow evaluations have been used to improvethe sensitivity of ultrasound in diagnosing ovariancancer in nonpregnant patients. Unfortunately,there is a significant overlap in the blood flowpatterns between malignant and benign lesions inpregnancy [14].

MRIUnlike CT, which exposes the mother and fetus to24 rads per examination, MRI is considered to bewell tolerated in pregnancy and can be useful inevaluating up to 20% of sonographically indetermi-nate adnexal lesions [15]. Masses of uncertain originand solid or complex cystic lesions can be evaluatedwith MRI, which has been shown to be accurate foridentifying the origin of a mass and characterizingits tissue content. MRI may also be useful in evalu-ating the extent of invasivemalignant disease and indiagnosing the bowel processes such as appendicitisor inflammatory bowel disease. We must emphasizethough that the use of MRI in pregnancy should beconsidered only when there is an inconclusiveultrasound result.

Tumor markersThe interpretation of tumor markers in pregnancyposes a unique challenge. CA-125, a commonlyused epithelial ovarian cancer tumor marker, canbe elevated in pregnancy during the first trimesterandpostpartum innormal pregnancy [16]. After thefirst trimester, however, a severely elevated CA-125(100010000) in the second trimester or beyondshould alert the clinician to the possibility of amalignancy. Other serum markers used for aneu-ploidy screeningmay also be elevated with an ovar-ian malignancy in pregnancy. Alpha feto-proteinelevations (greater than nine multiples of themedian) can be seen with germ cell tumors [17].Other tumormarkers such as beta human chorionicgonadotropin and lactate dehydrogenase are oflimited value in pregnancy because they can bealtered by pregnancy alone. As a general rule, tumormarkers should not be routinely drawn in thesetting of pregnancy because of the limitationspreviously discussed. However, if tumor markershave been drawn, or an abnormality is incidentallydetected using a marker for aneuploidy screening,the results should be interpreted cautiously takinginto consideration the physiologic changes ofpregnancy.

COMPLICATIONS OF ADNEXAL MASSESThe complications associated with persistentmassesinclude the following:

Ovarian torsionTorsion of the adnexa accounts for 3% of all surgicalemergencies of acute gynecologic complaints [18].The incidence of ovarian torsion in pregnancy is feltto be a rare event, with a reported incidence of110 per 10000 spontaneous pregnancies [19]. Inamulticenter cohort, Goh et al. [6&&] found that of 12of 118 patients admitted with an adnexal mass andpain, 10 of 118 were found to have ovarian torsion(8.5% incidence). This was similar to an earlier studyby Schmeler et al. [20] that found a 6.8% incidenceof ovarian torsion in masses measuring greater than5 cm in pregnancy. Hasson et al. [19] showed thatthe presentation of adnexal torsion is similar inpregnant and nonpregnant women, and themajority complained of acute abdominal or pelvicpain that lasted for several hours. Patients in thiscasecontrol cohort described the pain as acute,sharp, and intermittent or constant. Interestingly,43% of pregnant women with ovarian torsion didnot have peritoneal irritation signs compared to19% of nonpregnant patients. A total of 63% ofpregnant women had associated nausea and vomit-ing. In both pregnant and nonpregnant torsions,there was high false-negative normal Doppler bloodflow in patients later found to have surgically con-firmed adnexal torsion. Pregnancies conceivedthrough assisted reproductive techniques are at anincreased risk of ovarian torsion, likely because ofthe increased risk of ovarian hyperstimulation.Smorgick et al. [21] reviewed 38 cases of surgicallyproven torsion in pregnancy and found that 49%were conceived either through ovulation inductionor in-vitro fertilization. The size of an adnexal massmay play a role in the risk of torsion. Koo et al. [18]found that amass size of 610 cmhad a significantlyhigher risk of torsion than a mass less than 6 cm. Aswith the risk of malignancy, masses of 1015 cmwere not at increased risk of torsion when comparedwith masses less than 6 cm. Yen et al. [22] prospec-tively followed 174 pregnant patients with adnexalmasses and found that masses measuring between 6and 8 cm in size had a 22% incidence of ovariantorsion.

Ovarian torsion occurs most commonly in thefirst trimester [18,22]. Koo et al. [18] found an inci-dence of 68% in the first trimester, 20% in thesecond, and 22% in the third. Yen et al. [22] foundthat 60% of ovarian torsions occurred between the10th and 17th week of gestation, and only 6%occurred after 20 weeks.

Labor dystocia and ovarian ruptureOther adverse effects from an adnexal mass havebeen reported in pregnancy. Goh et al. [6&&] found

Management of the adnexal mass in pregnancy Goh et al.

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that 25% of patients who had an adnexal massunderwent a cesarean section for labor dystocia.There are reports of hemoperitoneum resulting fromovarian rupture from enlarged adnexal masses [23].

MalignancyThe management of ovarian malignancy in preg-nancy should be multidisciplinary comprisingof obstetricians, neonatologists, medical and gyne-cologic oncologists, and psychologists [24&]. Aftersurgery, chemotherapy regimens are generally pre-scribed, but these drugs have risks of fetal toxicitythat are mainly related to the gestational age.During organogenesis (between weeks 4 and 12 ofgestation), there is a high susceptibility to terato-gens and fetalmalformation [25]. During the secondand third trimester, chemotherapy can be associatedwith growth restriction and prematurity, thoughthe risk of malformations is low [26].

MANAGEMENTThe management options of adnexal masses inpregnancy are as follows:

SurgeryWhen there is a suspicion for malignancy or if apatient has symptoms, surgical intervention is war-ranted. Traditionally, if the mass was solid or hadmixed solid and cystic features and ascites, a midlinelaparotomy was performed to remove the mass,obtain a diagnosis, examine the contralateral ovary,obtain peritoneal washings, and complete a stagingprocedure if malignancy was confirmed [17]. Untilthe 1990s, pregnancy had been considered a contra-indication to use laparoscopy. The laparoscopicapproach in pregnancy for maternal ovarian torsionoffers several advantages over an open laparotomy,including decreased postoperative pain, lowernarcotic use, and lower wound infection rates [27].Koo et al. [28] analyzed 88 pregnancies who under-went laparoscopic surgery for adnexalmasses inpreg-nancy (mean gestational age 11.6 weeks) and foundthat obstetrical complications such as low birthweight, preterm birth, tocolysis, low Apgar scores,and fetal anomalies were acceptable. Some concernsfor laparoscopic surgery in pregnancy are decreaseduterine blood flow, carbon dioxide absorption, fetalhypotension, and fetal hypoxia [17]. In an analysis ofwomen undergoing both first and second trimesterlaparoscopic procedures, mean uterine resistanceindexandumbilical arterypulsatility index remainedconstant during the procedures, indicating thatlaparoscopy did notmodify uteroplacental perfusion[29&].

The incidental detection of adnexal masses atthe time of a cesarean delivery is not rare with anincidence of 1 of 329 [30]. Up to 5% of the masseswere bilateral and the majority were preoperativelyundiagnosed mature cystic teratomas. The recom-mendation would be cystectomy for a simple cystand excision when the mass is large or hetero-geneous in nature for pathologic analysis [31].Schwartz et al. also recommend removal of para-ovarian or paratubal cysts so as not to confoundfurther imaging studies.

ExpectantThe benefits of expectant management includeavoidance of surgery and its associated compli-cations. The risk of expectant management is therisk of ovarian torsion that could have been avoidedwith a laparoscopic procedure, along with the risk ofpregnancy loss with emergent surgery. Goh et al.[6&&] reviewed 126 pregnancies complicated by per-sistent ovarian masses greater than or equal to 5 cm.A total of 0.3% of this cohort were admitted for painand 8.3% eventually were diagnosed with ovariantorsion. They found that the majority of patientswith adnexal masses can be conservatively managedif there are no ultrasound findings suspicious formalignancy, without a significant increase in ante-natal or postpartum complications. Schmeler et al.[20] reviewed 177 pregnancies with adnexal masses.One-third of this cohort had surgery for torsion andsuspicions for malignancy. The remaining patientswere observed and operated via cesarean section orpostpartum again without significant differences onobstetrical outcomes between the patients who hadantepartum surgery and those managed expect-antly. There is no consensus on the managementstrategies of ovarian masses with reference to thesize of the mass. Recently, Koo et al. [18] analyzedover 470 women with adnexal masses who under-went surgery during their pregnancies. Masses of atleast 15 cm had a 12-fold higher risk of malignancycompared with the masses that measured less than6 cm. For masses of 1015 cm, however, the risk ofmalignancy was not higher than those ofmasses lessthan 6 cm. Earlier reviews [32] have used cutoffs of5 cm to triage patients after a diagnosis of adnexalmasses is made. Glanc et al. recommend serial ultra-sounds in asymptomatic womenwith amass greaterthan 5 cm until 16 weeks to allow for spontaneousresolution of the mass. If the mass increased in sizeor complexity, then further evaluation (by imagingor surgery) was recommended.

CONCLUSIONThe majority of adnexal masses diagnosed duringpregnancy will be benign. Laparoscopy in

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pregnancy is well tolerated and should be theprimary option in the symptomatic patient or ifcancer is suspected. For asymptomatic patients,both prophylactic removal of the mass and expect-antmanagement are the reasonable options. Expect-ant management may best serve patients whowish to avoid the risks associated with surgery inpregnancy. However, these patients should becounseled on the risk of torsion and the possibleneed for a more invasive procedure later ingestation. Additional prospective studies are neededto determine the best treatment plan for patientswith an adnexal mass in pregnancy.

Acknowledgements

None.

Conflicts of interest

Declaration of interest: The authors report no conflicts ofinterest.

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