Review

2006;8:1419

10.1576/toag.8.1.014.27203 www.rcog.org.uk/togonline

The Obstetrician & Gynaecologist

Review Management of adnexal masses in pregnancy

Authors Chris P Spencer / Phil J Robarts

Asymptomatic adnexal masses are frequently diagnosed in pregnancy, either at the early booking scan or at the time of caesarean section. They are mostly ovarian in origin. In this article we discuss the role of magnetic resonance imaging, computed tomography, Doppler studies and the use of tumour markers in diagnosis. The majority of ovarian cysts in pregnancy either resolve spontaneously or are due to benign conditions. Ovarian cancer is extremely rare in women of childbearing age and thus most of these cysts can be managed conservatively. If there is a suspicion of malignancy or there is a significant cyst complication, such as torsion, and surgery is planned, this should take place during the second trimester to minimise the risk of miscarriage.
Keywords adnexal masses / magnetic resonance imaging / ovarian cancer / ovarian cysts / pregnancy / ultrasonography
Please cite this article as: Spencer CP, Robarts PJ. Management of adnexal masses in pregnancy. The Obstetrician & Gynaecologist 2006;8:1419.

Author details
Chris P Spencer MD FRCOG Consultant in Obstetrics and Gynaecology St Johns Hospital, Wood Street, Chelmsford, CM2 9BG, UK E-mail: cpspencer@doctors.org.uk (corresponding author) Phil J Robarts FRCOG Consultant in Obstetrics and Gynaecology St Johns Hospital, Chelmsford, UK

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Introduction
Routine sonographic assessment of women in early pregnancy for the purposes of dating, viability and determination of the number of fetuses, as well as the measurement of nuchal fold thickness, has led to an increase in the diagnosis of adnexal masses. Before the routine use of obstetric ultrasound, adnexal masses were only discovered on abdominal or pelvic examination. These masses are now reported in up to 4% of all pregnant women.1 In addition, the incidence of ovarian pathology detected at caesarean section has been reported as being 0.5%.2 The majority of adnexal masses are ovarian in origin, but can also be due to paratubal cysts, chronic fallopian tube disease (hydrosalpinges) and fibroids that appear to be extrauterine. Fibroids that are pedunculated or located in the broad ligament are sometimes seen as separate from the uterus and thus reported as adnexal masses. The causes of adnexal masses are listed in Box 1. Nearly all ovarian masses detected in pregnancy are benign, but the overall reported incidence of ovarian cancer in pregnant women varies from 0.0040.04%.311 The most commonly reported malignancy in pregnancy and the puerperium appears to be breast cancer.11 Most of the ovarian masses diagnosed appear to be borderline with a low malignant potential3,8 and are complex on ultrasound assessment. Malignant tumours vary in size but 75% of them are larger than 5 cm in diameter and most of these have solid, as well as cystic, elements on ultrasound evaluation.4

cases at all,1214 while others have quoted rates of 0.8%,15 3.6%,16 6%,3,17 and even as much as 13%.4 Table 3 summarises these studies over the last two decades. It should be noted that in all these series, the majority of tumours identified have been shown to be early stage borderline tumours. The range of histologies of the invasive tumours are summarised in Box 2.

The role of MRI and CT scanning

MRI can safely be used in pregnancy but is more expensive and more time consuming than ultrasonography. Nevertheless, MRI is particularly good at defining both endometriotic and dermoid cysts (benign teratomas)18,19 and provides superior resolution when compared with CT scanning methods.20 Other advantages of MRI scanning include the ability to create images in several planes and the lack of ionising radiation requirement compared with CT scanning. Consequently, the use of CT scanning in
Ovarian Simple cyst Haemorrhagic cyst Hyperstimulation in women who have undergone fertility treatment Luteoma Endometrioma Brenner tumour Epithelial tumours: serous and mucinous; endometrioid and clear-cell carcinomas Germ cell tumours: mature and immature teratomas, dysgerminomas, endodermal sinus tumours, embryonal carcinomas Sex cord-stromal tumours: fibrothecomas; granulosa cell, sclerosing stromal and Sertoli-Leydig cell tumours Metastatic (secondary) tumours; for example, Krukenberg Lymphoma Tubal Hydrosalpinx Heterotopic pregnancy Paratubal cyst Leiomyoma Non-gynaecological Mesenteric cyst Appendix mass Diverticular disease Pelvic kidney Urachal cyst Box 1 Causes of adnexal masses in women with an intrauterine pregnancy

Diagnosis of adnexal masses

The use of ultrasound in early pregnancy, both abdominal and transvaginal, is the most commonly employed imaging modality. If the woman is assessed by bimanual examination, an adnexal mass can be detected if it is at least 5 cm in diameter. Tables 1 and 2 summarise the ultrasound appearances of the various adnexal conditions encountered. Ultrasound images of various adnexal masses are shown in Figures 14. Other radiological techniques include magnetic resonance imaging (MRI) and computed tomography (CT). Although the overall incidence of adnexal masses in pregnancy is approximately 4%,12 the incidence of complex or simple persistent cysts measuring more than 6 cm is only 0.07%.13 Three-quarters of these persistent cysts are complex in nature and the majority of complex cysts are either benign teratomas or endometriomas. Other pathologies include paratubal cysts and cystadenomas. According to several studies, the rate of ovarian cancer in adnexal masses varies considerably. Some researchers have found no confirmed cancer
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Type of mass

Ultrasound appearance

Resolution rate (%) 90100 if ,5 cm in diameter 90100

Simple ovarian cysts Unilocular, thin-walled, (follicular, corpus anechoic luteal) Haemorrhagic cysts Anechoic with echogenic material within cyst Hyperstimulated Massively enlarged, ovaries thin-walled, multilocular cysts Ascites may be present

Table 1 Ultrasound appearance of common ovarian cysts in pregnancy and resolution rates

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Table 2 Ultrasound appearances of adnexal pathology

Pathology Teratoma Endometrioma Malignant/ borderline ovarian tumour

Ultrasound appearance Complex mass with solid and cystic areas due to presence of fat, bone, sebaceous material and hair Diffuse ground glass pattern due to presence of old blood (chocolate) within the cyst Complex, multi-septate mass with solid and cystic areas Papillary projections or mural nodules Ascites may be present Appearance may be bilateral in up to 25% of cases Tubular-shaped structure with anechoic content and incomplete septum of tubal wall Always stays the same size during pregnancy Hypoechoic, round, solid masses Cystic change may occur if red degeneration develops

Hydrosalpinx

Leiomyoma

Figure 1 Simple ovarian cyst

pregnancy has little place in modern obstetric practice. As with other non-pregnant patients, there are contraindications to the use of MRI in pregnancy and these include the presence of ferromagnetic aneurysm clips and severe maternal claustrophobia. Although the movement of the fetus can produce erroneous images, this can be reduced with the use of fast imaging techniques. Using MRI, endometriotic cysts typically appear to have a homogenous high-signal intensity on T1weighted images and a low-signal intensity on T2weighted images. The high fat and sebum content of dermoid cysts can be detected easily using MRI scanning; these cysts typically demonstrate highsignal intensities on T1-weighted images and reduced signal intensities on fat-suppressed images. In addition, MRI can be useful in confirming the diagnosis of large degenerating leiomyomas, which can resemble ovarian tumours. These typically show high-signal intensity on T1weighted imaging and have characteristic appearances on T2-weighted imaging. MRI can be particularly helpful in the assessment of an ovarian mass that is thought to be malignant partly because of its ability to identify vegetations in a cystic tumour and necrosis in a solid tumour.21 Enhanced accuracy of MRI can be obtained with the use of gadolinium contrast enhancement,22 but the use of this agent in pregnancy is contraindicated due to its ability to cross the placenta and unknown half-life within the fetal circulation.

Figure 2 Benign ovarian teratoma

The role of tumour markers

Figure 3 Endometriotic cyst

In the non-pregnant state, CA125 is the most reliable serum marker for epithelial ovarian carcinoma as it is raised in over 75% of cases.23 In addition, measurement of serum CA125 levels is useful in determining a womans response to postoperative chemotherapy and in detecting early relapse in women who have already received a diagnosis of ovarian cancer. Serum alphafetoprotein (AFP) and beta-hCG (human chorionic gonadotrophin) levels are also very useful in the preoperative evaluation and management of ovarian germ cell tumours in non-pregnant women. In addition, elevated serum inhibin levels can be detected in women with granulosa cell tumours of the ovary and mucinous carcinomas. During pregnancy, however, serum AFP, betahCG and inhibin levels are all raised due to placental synthesis and thus the use of these markers in evaluating suspicious ovarian cysts is limited. Serum CA125 levels also become elevated during pregnancy24 due to decidual cell production,25 with levels rising as pregnancy progresses. Some researchers have suggested using a cut-off level of 112 U/ml as the upper limit of normal, compared with 35 U/ml in the non 2006 Royal College of Obstetricians and Gynaecologists

Figure 4 Complex ovarian cyst

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Author Hasan42 Ballard40 Struyk41 Hopkins43 Nelson1 Hogston5 Ashkenazy6 Thornton31 Tchabo10 Hess17 Koonings2 Sunoo44 El-Yahia45 Platek13 Ueda38 Bromley15 Hill12 Whitecar3 Bernhard7 Zanetta16 Sherard4 Condous14 Lee39 Schmeler46

Year 1983 1984 1984 1986 1986 1986 1987 1987 1987 1988 1988 1990 1991 1995 1996 1997 1998 1999 1999 2003 2003 2004 2004 2005

Number of women with adnexal mass (surgical) 10 (10) 93 (93) 90 (69) 23 (23) 38 (5) 137 (21) 38 (38) 131 (81) 12 (12) 54 (54) 91 (91) 228 (228) 67 (67) 31 (19) 106 (106) 125 (96) 328 (18) 130 (130) 432 (25) 82 (23) 56 (56) 161 (7) 89 (89) 63 (59)

Incidence per live births 1 in 900 1 in 594 1 in 640 1 in 556 1 in 88 1 in 191 1 in 2328 1 in 346 1 in 2334 1 in 1300 1 in 197 1 in 163 1 in 653 1 in 1399 1 in 79 Not recorded 1 in 444 1 in 1312 1 in 43 1 in 84 1 in 602 1 in 19 Not recorded 1 in 2000

Commonest lesion found Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Corpus luteal cyst Simple cyst Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma/cystadenoma Benign cystic teratoma Hydatid cyst of Morgagni Benign cystic teratoma Functional cyst (simple/haemorrhagic) Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Benign cystic teratoma Serous cystadenoma Benign cystic teratoma Benign cystic teratoma

Number of women with malignant tumours* (%) 1 (10) 2 (2.2) 3 (4) 1 (0.73) 2 (5.3) 7 (8.6) 1 (8.3) 2 (5.9) 3 (4.5) 5 (4.7) 1 (0.8) 8 (6.1) 1 (0.23) 3 (3.6) 8 (14.2) 1 (0.62) 2 (2.2) 5/59{ (8.5)

Table 3 Summary of published studies of adnexal masses in pregnancy

*Including borderline tumours

pregnant state.26 The usefulness of this marker in pregnancy is still restricted and if an ovarian mass is thought to look suspicious, further evaluation with MRI may be preferable. Certain malignant germ cell tumours, such as ovarian dysgerminomas, have been found to be associated with raised serum lactate dehydrogenase (LDH) levels.27 However, due to the rarity of this neoplasm, data regarding this association are sparse.

Immature teratoma Serous/mucinous cystadenocarcinoma Dysgerminoma Granulosa cell tumour Sertoli-Leydig cell tumour (androblastoma, arrhenoblastoma) Burkitts lymphoma

Box 2 Histology type of invasive ovarian cancer in adnexal masses

The role of Doppler studies

The use of colour flow Doppler imaging to distinguish benign from malignant ovarian masses in the non-pregnant state has been studied.28,29 Malignant masses are usually vascular while benign lesions demonstrate little or no blood flow. In tumours that have malignant potential, the resistance and pulsatility indices are usually less than 1, but this pattern is also seen in many benign conditions such as endometriomas, corpus luteal cysts and other benign complex ovarian masses. In addition, due to increased pelvic vascularity in pregnancy, the degree of overlap of these indices in both benign and malignant lesions makes Doppler imaging unreliable in this setting.30

size. Further ultrasound assessment should take place at 4-week intervals to determine whether the cyst is becoming larger. In the majority of cases, both simple cysts larger than 6 cm and all complex cysts resolve during the course of the pregnancy.7 Adnexal masses that undergo torsion are usually dermoids or cystadenomas. If this complication occurs, it does so during the first trimester or in the immediate puerperium (up to 14 days after delivery) and more commonly on the right side. Ovarian dermoids that measure less than 6 cm are unlikely to grow significantly in pregnancy and can be managed conservatively as the risk of complications, such as torsion, is thought to be low.32 The woman should be rescanned in the postnatal period to determine further management of any ovarian dermoid that has not resolved spontaneously. Persistent, simple, unilocular cysts without any solid elements that are larger than 10 cm can be aspirated either transvaginally or abdominally under ultrasound guidance using a fine needle (greater than 20 gauge).33 This procedure is only indicated if the cyst is causing pain or thought to be increasing the risks of fetal malpresentation or obstructed labour due to its location in the pelvis.13,33 Although not commonly employed, this technique seems to be a reasonable alternative to surgery in suitable women and appears to be
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Management in pregnancy
Management in pregnancy depends on the size of the adnexal mass, its sonographic appearance and any associated clinical symptoms, although the majority of women are likely to be asymptomatic. Simple cysts that are less than 5 cm in diameter do not need further evaluation and rescanning is only required if there is a clinical indication, such as pelvic pain. The majority of simple cysts resolve spontaneously during the course of pregnancy7,31 and women should be reassured as such. Cysts that have a complex nature, i.e. solid and cystic elements, need further evaluation irrespective of
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Box 3 Complications of ovarian cysts in pregnancy

Cyst rupture Cyst haemorrhage Torsion (up to 5%) Obstructed labour Fetal malpresentation

is not thought to be necessary, but if uterine irritability occurs, then standard tocolytic regimens can be employed. Adnexal pathology detected for the first time at caesarean section has been reported in the region of 0.5%,2 but this figure is likely to be lower in areas where routine antenatal ultrasound is employed for dating and fetal anatomy assessment purposes. If adnexal pathology is discovered at caesarean section, the options include: conservative management, ovarian cystectomy or oophorectomy. Simple cysts that are smaller than 5 cm in diameter can be left alone but larger cysts or those appearing complex should be treated by cystectomy. Care should be exercised in removing cysts in order to avoid intra-abdominal contamination. The most common lesions found are dermoid cysts, paratubal cysts, cystadenomas, endometriotic cysts and corpus luteal cysts.2 After cyst removal, the contents should be inspected thoroughly before closing the mothers abdomen. If there are any signs of malignancy, such as the presence of solid excrescences, the ovary should be removed completely or, if available, rapid frozen section assessment performed. The contralateral ovary should be examined thoroughly and, if indicated, biopsied accordingly.

well tolerated and without short or long-term complications. Local anaesthesia is normally used for the skin and antibiotic cover given. All fluid aspirated should be sent for cytological analysis and the woman subsequently rescanned to determine whether cyst recurrence has taken place. The risk of this is thought to be in the region of 3350%33 and the mother should therefore be counselled that further aspirations can be required during the rest of the pregnancy. Fine needle aspirations should be done after 14 weeks of gestation in order to minimise disturbance to the corpus luteum. The indications for surgery will depend on the degree of suspicion of malignancy in the mass or the development of cyst complications (Box 3). If there is doubt regarding the diagnosis, MRI can prove useful as a tool to help distinguish dermoids and endometriomas from malignant neoplasms. If elective surgery is embarked upon, this should be done after 14 weeks gestation to minimise the risk of fetal loss due to miscarriage, although this risk is very small.34,35 This recommendation is based on the principle that the developing pregnancy is dependent on the corpus luteum during the first trimester and much less so after 12 weeks. The standard approach is to perform the surgery via a laparotomy but laparoscopic surgery has been used, although it is skill-dependent and more time consuming than open surgery.36 If laparoscopic surgery is performed during the second trimester, an open method (Hasson) is preferred to avoid uterine injury from the primary trocar introduction.37 The routine use of tocolytic drugs
Figure 5 Clinical algorithm for the management of ovarian cysts in pregnancy.

Conclusions
Over the last 20 years, the use of ultrasound in pregnancy has dramatically increased and many centres now offer early dating scans as well as 20week fetal anomaly scans. Consequently, the numbers of ovarian cysts diagnosed has increased, leading to a greater probability of operative intervention. The majority of these ovarian cysts in pregnancy either resolve spontaneously or are

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due to benign conditions, such as dermoids or endometriomas. Ovarian cancer is extremely rare in women of childbearing age and thus most of these cysts can be managed conservatively. In terms of malignancy potential, those that are malignant are likely to be borderline. Unless there is a suspicion of malignancy or there is a significant cyst complication, such as torsion, surgery is not indicated. MRI is a safe and useful tool to help evaluate cysts in more detail in situations where ultrasound provides an inconclusive answer. If surgery is planned, this should take place during the second trimester to minimise the risk of miscarriage. Whether surgery is done laparoscopically or using a traditional open approach is largely dependent on operator experience and patient preference. In some situations, there may be grounds for performing an elective caesarean section at term in addition to dealing with a large, complex ovarian tumour that has persisted during the pregnancy but which has not required earlier operative intervention. Aspiration of ovarian cysts is only indicated where they appear simple on ultrasound and where they are causing pain or are thought to be obstructing the birth canal. If surgery does not take place, then ultrasound follow-up during and after pregnancy may be advised accordingly. Figure 5 provides a clinical algorithm for the management of ovarian cysts in pregnancy. References
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