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Adnexal masses and pregnancy: A 12-year experience

Gordon B. Sherard III, MD,a Charles A. Hodson, PhD,a H. James Williams, MD,b
Diane A. Semer, MD,a Hamid A. Hadi, MD,a and David L. Tait, MDa
Greenville, NC

OBJECTIVE: Our purpose was to describe pregnancy-associated adnexal masses in eastern North Carolina.
STUDY DESIGN: A retrospective study was performed of 60 adnexal masses resected during pregnancy at
a regional referral hospital from January 1990 to March 2002.
RESULTS: Adnexal masses occurred in 0.15% of pregnancies. Average gestational age at diagnosis and
surgery was 12 and 20 weeks, respectively. Fifty percent of ovarian tumors were mature cystic teratomas, 20%
were cystadenomas, and 13% were functional ovarian cysts. Malignancy occurred in 13%. Tumors with low
malignant potential comprised 63% of malignancies. Average cyst size was 11.5 cm for malignancies and
7.6 cm for benign lesions (P value <.05). The preterm birth rate was 9%, the miscarriage rate was 4.7%
after elective cases, and average Apgar scores were 7.5 and 8.7 at 1 and 5 minutes.
CONCLUSION: The incidence of malignancy in pregnancy-associated adnexal masses was high.
Ultrasonography detected internal excrescences in the majority of tumors with low malignant potential. Fetal
outcomes were not affected. (Am J Obstet Gynecol 2003;189:358-63.)

Key words: Adnexal masses, malignancy, pregnancy

The number of adnexal masses diagnosed concurrently diagnoses most commonly reported for these persistent
with pregnancy has increased as the routine use of masses are functional cysts and mature cystic teratomas.
ultrasonography has increased. The use of ultrasonogra- The incidence of ovarian cancer associated with persistent
phy has resulted in the detection of asymptomatic and adnexal masses in pregnancy varies, with reports as high as
clinically inapparent lesions.1 Historically, adnexal masses 5.9%.2
were diagnosed on physical examination. Earlier diag- The purpose of this article was to characterize the
nosis of pregnancy as a result of very sensitive home adnexal masses associated with pregnancy at a tertiary
pregnancy tests and increased access to prenatal care may care facility and to report on the maternal and fetal
contribute to increased detection of pregnancy-associated outcomes. The description of the mass will include
masses. As more women enter into prenatal care at earlier clinical presentation, ultrasound morphologic features,
gestational ages, the incidence of lesions increases as and histologic diagnosis. Increased data on adnexal
more functional cysts are detected. Currently, adnexal masses in pregnancy will enhance the counseling of
masses have been noted to occur in up to 1% of all patients regarding management options.
gestations.1
The management of adnexal masses associated with Material and methods
pregnancy is variable. The two most common options are
This was a retrospective study of all pregnancy-
operative extirpation of the mass or expectant manage-
associated adnexal masses that were surgically resected
ment. Cyst size, gestational age, and sonographic appear-
at Pitt County Memorial Hospital, a tertiary care facility in
ance all need to be considered when evaluating adnexal
rural eastern North Carolina from January 1990 through
masses and formulating a treatment plan. Previous studies
March 2002. The obstetric database was reviewed for
have both supported and refuted complications associ-
exploratory laparotomy, operative laparoscopy, adnexal
ated with these options of therapy. The histologic
mass, and pelvic mass. The pathology database was also
searched for adnexal, ovarian, or pelvic mass associated
with pregnancy. Data collection included maternal age,
From the Departments of Obstetrics and Gynecology,a and Pathology,b
East Carolina University, Brody School of Medicine, Pitt County race, gravidity, parity, gestational age at diagnosis,
Memorial Hospital. gestational age at surgery, gestational age at delivery,
Presented at Sixty-Fifth Annual Meeting of the South Atlantic ultrasonographic findings, site of lesion, pregnancy com-
Association of Obstetricians and Gynecologists, Hot Springs, Va,
January 25-28, 2003. plications, neonatal complications, birth weight, Apgar
Reprint requests: Gordon B. Sherard III, MD, 201 Pineville Rd, scores, and histologic diagnosis of the adnexal masses.
Spartanburg, SC 29307. E-mail: gsherard@bellsouth.net Mean diameter of the mass was calculated as the sum
2003, Mosby, Inc. All rights reserved.
0002-9378/2003 $30.00 + 0 of three diameters divided by 3. Term deliveries were de-
doi:10.1067/S0002-9378(03)00731-2 fined as occurring after 37 weeks and up to 42 weeks of

358
Volume 189, Number 2 Sherard et al 359
Am J Obstet Gynecol

Table I. Maternal demographics (n = 56) Table II. Neonatal data (n = 42)

Average maternal age 27 y (15-41y) Gestational age at delivery 37.5 2.5 wk


Average gravidity 2.4 (1-7) Term delivery 69% (n = 29)
Average parity 0.9 (0-5) Preterm delivery 24% (n = 10)
Nulliparous 45% (n = 25) Spontaneous abortion 4.7% (n = 2)
Race Elective abortion 2.3% (n = 1)
African-American 59% (n = 33) Route of delivery
White 36% (n = 20) Vaginal delivery 44% (n = 19)
Other 5% (n = 3) Cesarean delivery 54% (n = 23)
Complications of pregnancy Curettage 2% (n = 1)
Diabetes 9% (n = 5) Average birth weight 2877 911 g
Hypertension 5% (n = 3) Average Apgar score
Asthma 2% (n = 1) 1 min 7.5 0.59
Sickle cell disease/trait 4% (n = 2) 5 min 8.7 0.19
Thyroid dysfunction 2% (n = 1)
Advanced maternal age 12.5% (n = 7)
Lupus erythematosus 2% (n = 1)
Rh negative (nonsensitized) 9% (n = 5)
Twins 3% (n = 3) Fifty-four operations (96%) were by laparotomy and the
Tobacco use 2% (n = 1) two most recent surgeries were laparoscopic procedures.
Pyelonephritis 2% (n = 1) Ninety-eight percent (55/56) of our cases were elective
cases. One emergency surgery for adnexal torsion was
preformed. Vertical midline incisions were used in the
gestation and preterm deliveries were defined as occur- majority of the laparotomy cases. The two laparoscopic
ring before 37 weeks of gestation. The decision on cases were preformed at 15 and 17 weeks gestation for one
whether to operate was determined by the staff physician mature cystic teratoma and one functional cyst, respec-
and/or maternal fetal medicine specialist. Microsoft tively. Traditional pressure values of 15 mm Hg were used
Excel statistical software was used to preform two-tailed for insufflation.
t tests on the mean cyst diameter. Neonatal information was only available for 42 of 56
patients (75%) as a result of patients returning to the
Results referring physicians after evaluation and management of
There were 37,929 deliveries during the study period. the adnexal mass. Term delivery occurred in 69% of
Sixty-three patients with adnexal masses were identified patients. Preterm deliveries included two sets of twins and
through our database searches. Of the 63 patients, 7 were two inductions of labor for nonreassuring fetal status.
lost to follow-up and not included in our study resulting in Mean 1 and 5 minute Apgar scores were 7.5 and 8.7
a final study group of 56 patients. After patients with (Table II).
bilateral disease were included, the total number of Fifty percent (30/60) of the lesions were mature cystic
adnexal masses was 60, giving an incidence of 0.15% teratomas, 13% were functional ovarian cysts, and 20%
(1/632 pregnancies) in our series. were benign cystadenomas. The incidence of cancer
Mean maternal age and parity were 27 years and 1, associated with adnexal masses in pregnancy was 13%.
respectively (Table I). The mean gestational age at Low malignant potential tumors comprised 63% (5/8) of
diagnosis of the adnexal mass was 12 weeks and the mean malignant neoplasms, whereas the remaining 37% (3/8)
gestational age at surgery was 20 weeks. Fourteen cases displayed stromal invasion (Table III).
(22%) were diagnosed during the first trimester at an The mean cyst size for nonmalignant masses was 7.6 cm
average gestational age of 9 weeks (6-11 weeks). After (range 3 cm to 15cm) and 11.5 cm for malignant masses
documenting no spontaneous resolution, these masses (range 6 cm to 17 cm). Septations were found equivalently
were removed at an average gestational age of 17 weeks. in malignant and nonmalignant processes. Internal
During the 12th to 20th gestational week, 17 more masses excrescences were found in 50% of malignant tumors
were discovered at an average gestational age of 16 weeks and not in any benign lesions (Table IV).
(12-20 weeks). The average gestational age at surgery was The Federation of International Gynecology and
23 weeks for these masses. Thirty-one of the 56 (55%) Obstetrics (FIGO) system was used to surgically stage
study patients underwent surgery on or before comple- the ovarian cancers. Cell washings, peritoneal biopsies,
tion of the 20th gestational week. The remainder had lymph node sampling, and partial omentectomies were
operations either at cesarean section or immediately post performed. At diagnosis, all the cancers were FIGO stage
partum. Nine patients were followed up expectantly after IA. Maternal data for patients with ovarian cancer is
diagnosis with the average length of antepartum follow-up presented in Table V. Ascites, a frequent coexisting con-
lasting 17 weeks (range 7-26 weeks). Seventeen patients dition with ovarian cancer, was detected by ultrasonogra-
had masses removed at cesarean section and 5 patients phy in two cases in our series. One case was a luteoma
had laparotomies in the immediate postpartum period. (functional cyst) and the other was an immature teratoma
360 Sherard et al August 2003
Am J Obstet Gynecol

Table III. Adnexal mass pathology Table V. Ovarian cancer demographics

Calculated mean cyst size Average maternal age 22 y (15-38y)


Histologic diagnosis % (cm) Average gravidity 2.3 (1-5)
Average parity 1 (0-3)
Mature cystic teratoma (n = 30) 50 6.2 2.1 (3-11) Nulliparous 57% (n = 4)
Cystadenoma (n = 12) 20 11 3.9 (4-13) Race
Functional (n = 8) 13 7.4 3 (4-13) African American 43% (n = 3)
Cancer (n = 8)* 13 11.5 3.9 (6-17) White 57% (n = 4)
Fibroma (n = 1) 2 3 Site
Paratubal (n = 1) 2 7 Right 57% (n = 4)
Left 29% (n = 2)
*Four papillary serous, low malignant potential; 1 mucinous, Bilateral 14% (n = 1)
low malignant potential; 2 immature teratomas; 1 dysgerminoma.

Table IV. Ultrasound data (n = 40) Multiple authors have recommended conservative
management of adnexal masses #6 cm. Grimes et al4
Benign (n = 32) Malignant (n = 8)
reported 185 adnexal masses; 111 cysts were diagnosed
Morphology during pregnancy and expectantly managed. Ninety-two
Complex 66% (n = 21) 87.5% (n = 7) of 98 (94%) cysts that were less than 6 cm spontaneously
Solid 13% (n = 4) 12.5 (n = 1)
resolved. These authors proposed that the pedicle is able
Cystic 22% (n = 7) 0%
Discriminator to resist torsion as long as the cyst is not greater than 6 cm.
Internal excrescences 0% 50% (n = 4) A separate study reporting on 137 masses noted that 31 of
Echogenic focus 3% (n = 1) 0%
38 (82%) cysts less than 6 cm resolved.5 All cysts 5 cm or
Septated 9% (n = 3) 13% (n = 1)
less resolved in the largest series that described 131
pregnancy-associated adnexal masses.6
In addition to the possibility of spontaneous cyst
that actually had an intact ovarian capsule at time of resolution, the decision to postpone surgery until after
operation. The ultrasound was misleading because of the the first trimester has been based on cases described in the
extremely large nature (>2 L) of the cystic component of Emil Novak Tumor registry. One third of all surgeries
the neoplasm. preformed in the first trimester ended in spontaneous
abortion in that series.7 These data are a common
Comment guideline for timing elective operative removal of adnexal
In our large series of adnexal masses in pregnancy, we masses in pregnancy.
found the distribution of histology variable from other Expectant management has been associated with
reports. Although the incidence of cystadenomas asso- adverse pregnancy outcome if the mass undergoes
ciated with adnexal masses in pregnancy was similar in torsion, rupture, or hemorrhage. Hess et al2 reported 15
our study compared with prior studies, we had several of 54 (28%) patients with adnexal masses found in
findings that differed from what had previously been pregnancy required emergency laparotomy (6 acute
reported. The 50% incidence of mature cystic teratomas hemorrhage, 7 cyst torsion). Of these patients requiring
in our series was increased over the previously reported emergency surgery, 6 of 15 (40%) had adverse pregnancy
20% to 30% incidence. Functional cysts occurred in only outcomes postoperatively, four spontaneous abortions
13% of our cases compared with previous ranges and two preterm births. Of the remaining 39 patients who
between 22% to 54%. The most striking finding in our had elective removal of an adnexal mass, only 1 (2%) had
series, however, was the increased incidence of malig- an adverse pregnancy outcome. Interestingly, seven cases
nancy in persistent adnexal masses in pregnancy. The in this series involved the removal of a corpus luteum,
13% incidence is over twice the previously reported including five that had to have emergency surgery. Two
incidence of 2% to 6%.3 patients had postoperative spontaneous abortions for an
Pregnancy outcomes in our series are consistent with incidence of 29% (2/7).
previous reports. The postoperative spontaneous abor- In our study, 2 of 42 (4.7%) patients with available
tion rate after elective removal was 4.6%. One emergency delivery data had an adverse pregnancy outcome after
surgery was preformed in a patient at 20 weeks gestational elective removal of an adnexal mass. One patient had
age as a result of ovarian torsion; she was delivered a spontaneous abortion immediately after surgery at 16
uneventfully at term. The overall incidence of preterm weeks. The other patient had premature rupture of
birth was 24% (10/42). When adjusted for two pairs of membranes at 18 weeks after amniocentesis for advanced
twins and two inductions of labor for fetal indications, the maternal age at 15 weeks and surgery at 15.3 weeks of
rate of preterm delivery decreases to 9%. gestation.
Volume 189, Number 2 Sherard et al 361
Am J Obstet Gynecol

The effect of pregnancy on mature cystic teratomas has weighted scoring systems (including septations, wall
also been evaluated and one study noted increased structure, and echogenicity) exist. The difficulty in
complications. Torsion occurred in 19% and rupture in differentiating certain benign conditions from malig-
17% of these cysts in pregnancy.8 Because of the high nancy has yielded positive predictive values around
incidence of adverse pregnancy outcomes in association 30%.14 In another study, the ultrasound in 15% of the
with emergency surgery previously reported, some au- cases was frankly misleading.15 Included were 6% of
thors recommend elective removal of all masses that cases interpreted as benign when a malignancy was
persist until 16 weeks and are 6 cm or greater regardless of documented by histologic study. Twenty-two percent of
appearance on imaging studies, unless it is suspected to be ultrasonographic simple cysts were noted on pathologic
a leiomyoma.2 examination to be low malignant potential tumors in
Conversely, torsion occurred in only 1 of 139 conserva- a separate study.6 In our cases, 80% (4/5) of masses that
tively managed patients in the study by Grimes et al.4 At were of low malignant potential had ultrasonographic
surgery, the ovarian pedicle was untwisted and a cys- morphologic features significant for papillary excres-
tectomy was performed on a 10-cm cyst. The patient had cences detected on the internal cyst wall.
no postoperative pregnancy-related complications. There Solid tumors are another frequently cited reason for
were no complications in a study that expectantly followed surgery over concerns for malignancy. Of the six solid
up 49 patients with presumed dermoids. Pregnancy did tumors in our series, four (66%) were benign, including
not affect the growth of mature cystic teratomas 6 cm or a luteoma, a fibroma, and two mature cystic teratomas.
less in these patients.9 Twelve patients were followed up, There were two malignancies (33%), an immature
and there was no incidence of torsion in another study.10 teratoma and a dysgerminoma (Table V). Color-flow
In the 9 patients we managed conservatively with mature Doppler imaging has also been used as an adjunct in
cystic teratomas (average cyst size 6.3 cm), torsion did not evaluating adnexal masses. Building on the presence of
occur. The length of follow-up for these patients ranged neovascularization and the associated low resistance
from 7weeks to 26 weeks. Only 1 patient in our series was vessels (because of the absence of muscularis develop-
diagnosed with torsion (on initial presentation for care at ment) in malignancy, descriptions of pulsatility and
20 weeks gestation) and taken to the operating room. resistance indices have been published.16 However, no
Postoperatively, she had no further antenatal com- such data have been reported for adnexal masses in
plications and was delivered at term. pregnancy.
Gross and microscopic examination to exclude a malig- Magnetic resonance imaging (MRI) is another imaging
nant neoplasm is an indication for operative intervention. modality that has been used to assist in the characteriza-
The reported incidence of ovarian cancer in pregnancy tion of adnexal masses. In one published study, magnetic
ranges from 1:5000 to 1:47,000 live births with 2% to 6% of resonance imaging (MRI) was used in the differentiation
persistent adnexal masses being malignant.7,10 Tumors between solid ovarian masses and leiomyoma.17 More
with low malignant potential and epithelial cancers are information and studies on the benefits of MRI are
the most common ovarian cancers found in pregnancy.11 needed before its routine use in the work-p of pregnancy-
In our series, 13% (8/60) of persistent adnexal masses associated adnexal masses.
were malignant. The malignancy rate in our series was 1 in In summation, we found a much higher than expected
4741 pregnancies. In agreement with a previously re- malignancy rate. We postulate that as a regional center,
ported study describing ovarian cancer in pregnancy, the our malignancy rate is higher because lesions that are
majority of cancers in our series were tumors of low smaller or more benign appearing are managed by private
malignant potential.12 practitioners and not referred. Importantly, the size of the
Size has been used as an indicator for surgery in ovarian mass diagnosed in pregnancy was not absolutely
nonpregnant patients. Historic recommendations have predictive of malignancy. However, all masses less than
been to remove masses that were larger than 8 cm or 6 cm were noted to be benign. Morphologic study, as
masses between 5 and 8 cm that did not resolve after 8 characterized by ultrasonography, detected internal
weeks in menstruating women.13 In our series, the average papillary excrescences in 50% of malignancies in our
mean cyst size was 11.5 cm for malignant lesions and 11 cm series. Neonatal outcome was not adversely affected in
for cystadenomas (P value not significant) (Table III). either elective cases or our only emergency surgery.
However, the average mean cyst size for all benign lesions Our data support that of other published studies, to
was 7.6 cm (P value <.05). Thus, using size alone as an manage masses conservatively, performing surgery in the
absolute discriminator does not appear to be predictive, second trimester. We conclude that patients with persis-
unless the lesion is less than 6 cm. tent adnexal masses greater than 6 cm should undergo
Ultrasound evaluation of adnexal masses has been surgical removal, be appropriately counseled as to the
utilized in the attempt to differentiate between malignant possibility of an underlying malignancy, and be prepared
and benign tumors. Different evaluation techniques using for possible ovarian cancer staging.
362 Sherard et al August 2003
Am J Obstet Gynecol

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DR JERRY F. MATKINS JR, Gastonia, NC. The detection techniques to differentiate benign and malignant lesions.
of adnexal masses in pregnancy has become increasingly Magnetic resonance imaging, color Doppler ultrasound,
more common, and therefore the dilemma of how to and aspiration cytology, while sometimes helpful in
manage these patients has become one that is faced more specific cases, have all been disappointing in providing
frequently. In the era before ultrasound, when palpation adequate predictive power on which to base management
was relied on to diagnose adnexal masses, the detection decisions.7,8
rate was reported to be 1 in 591 pregnancies.1 By 1986, as The risks of active management of pregnancy-associ-
ultrasound became more commonly used, the reported ated adnexal masses lie in the risk of surgical exploration
incidence of adnexal masses in pregnancy was 1 in 190.2 itself. Although laparotomy or laparoscopy in a nonemer-
Because ultrasound has become more precise over the gency setting has been shown to be fraught with fewer
past 15 years, that detection rate has climbed to as high as complications than emergency procedures or those in the
one mass detected in every 50 pregnancies.3 Certainly all second or third trimesters, adverse outcomes are not
of these lesions are not clinically significant, so we cannot unknown in these patients.4,5
say with assurance that our increased technologic As clinicians, many if not all of us have been faced with
capabilities have resulted in better management of this dilemma. Patients and their spouses are often equally
patients. In fact, we may have only succeeded in raising afraid of the consequences of aggressive and conservative

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