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Adnexal masses during pregnancy: diagnosis,


treatment, and prognosis
Ann M. Cathcart, MD, PhD; Farr R. Nezhat, MD; Jenna Emerson, MD; Tanja Pejovic, MD, PhD; Ceana H. Nezhat, MD;
Camran R. Nezhat, MD

Introduction
The frequency of adnexal masses in Adnexal masses are identified in pregnant patients at a rate of 2 to 20 in 1000,
pregnancy is 2 to 20 in 1000, approxi- approximately 2 to 20 times more frequently than in the age-matched general popu-
mately 2 to 20 times the rate in the age- lation. The most common types of adnexal masses in pregnancy requiring surgical
matched general population.1e4 The management are dermoid cysts (32%), endometriomas (15%), functional cysts (12%),
increased frequency of adnexal masses serous cystadenomas (11%), and mucinous cystadenomas (8%). Approximately 2% of
in pregnancy is largely attributable to adnexal masses in pregnancy are malignant. Although most adnexal masses in preg-
the widespread use of antenatal nancy can be safely observed and approximately 70% spontaneously resolve, a minority
ultrasound, as most masses are asymp- of cases warrant surgical intervention because of symptoms, risk of torsion, or suspicion
tomatic and not identified by physical of malignancy. Ultrasound is the mainstay of evaluation of adnexal masses in pregnancy
examination.5,6 because of accuracy, safety, and availability. Several ultrasound mass scoring systems,
Although most adnexal masses in including the Sassone, Lerner, International Ovarian Tumor Analysis Simple Rules, and
pregnancy spontaneously resolve, inter- International Ovarian Tumor Analysis Assessment of Different NEoplasias in the adneXa
vention may be indicated for symptom- scoring systems have been validated specifically in pregnant populations. Decisions
atic patients or those at high risk of regarding expectant vs surgical management of adnexal masses in pregnancy must
malignancy or torsion.4,5 This article balance the risks of torsion or malignancy with the likelihood of spontaneous resolution
reviewed the differential diagnosis, and the risks of surgery. Laparoscopic surgery is preferred over open surgery when
possible because of consistently demonstrated shorter hospital length of stay and less
postoperative pain and some data demonstrating shorter operative time, lower blood
From the Department of Obstetrics and loss, and lower risks of fetal loss, preterm birth, and low birthweight. The best practices
Gynecology, Oregon Health & Science for laparoscopic surgery during pregnancy include left lateral decubitus positioning after
University, Portland, OR (Drs Cathcart, the first trimester of pregnancy, port placement with respect to uterine size and pathology
Emerson, and Pejovic); Weill Cornell Medical
College, Cornell University, New York, NY (Dr F
location, insufflation pressure of less than 12 to 15 mm Hg, intraoperative maternal
Nezhat); New York University Long Island capnography, pre- and postoperative fetal heart rate and contraction monitoring, and
School of Medicine, Mineola, NY (Dr F Nezhat); appropriate mechanical and chemical thromboprophylaxes. Although planning surgery
Division of Gynecologic Oncology, Oregon for the second trimester of pregnancy generally affords time for mass resolution while
Health & Science University, Portland, OR (Drs optimizing visualization with regards to uterine size and pathology location, necessary
Emerson and Pejovic); Atlanta Center for
Minimally Invasive Surgery and Reproductive
surgery should not be delayed because of gestational age. When performed at a facility
Medicine, Atlanta, GA (Dr CH Nezhat); and with appropriate obstetrical, anesthetic, and neonatal support, adnexal surgery in
Center for Special Minimally Invasive and pregnancy generally results in excellent outcomes for pregnant patients and fetuses.
Robotic Surgery, Palo Alto, CA (Dr CR Nezhat);
University of California San Francisco, San Key words: adnexal mass, Assessment of Different NEoplasias in the adneXa,
Francisco, CA (Dr CR Nezhat); and Stanford biomarker, cyst, cystadenoma, dermoid, endometrioma, hyperreactio luteinalis, Inter-
University Medical Center, Palo Alto, CA (Dr CR national Ovarian Tumor Analysis, laparoscopic, laparoscopy, Lerner, luteoma, malig-
Nezhat). nancy, ovarian cancer, ovarian cyst, ovarian mass, pregnant, robotic surgery, Sassone,
Received Sept. 27, 2022; revised Nov. 15, torsion, ultrasound
2022; accepted Nov. 15, 2022.
A.M.C. is a member of the Product Advisory
Board for Delfina Care Inc, San Jose, CA. F.R.N.,
J.E., T.P., C.H.N., and C.R.N report no conflict workup, and management of adnexal searching for combinations of the
of interest. masses in pregnancy, including special aforementioned key words with “ma-
This study received no funding. considerations regarding surgery in the lignancy,” “ultrasound,” “MRI,” “tumor
Corresponding author: Farr R. Nezhat, MD. pregnant patient. markers,” “CA-125,” “laparoscopy,”
farr@farrnezhatmd.com A literature review was conducted by “laparoscopic,” “robotic,” “pneumo-
0002-9378/$36.00 searching PubMed for articles using key peritoneum,” or “anesthesia.” Original
ª 2022 Elsevier Inc. All rights reserved. words “adnexal mass,” “adnexal research articles addressing the epide-
https://doi.org/10.1016/j.ajog.2022.11.1291
masses,” “ovarian mass,” “ovarian miology, diagnosis, evaluation, and
masses,” “pregnancy,” and “pregnant.” management of adnexal masses in
Additional articles were identified by pregnancy were reviewed.

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Differential diagnosis Luteomas are benign proliferations of


FIGURE 1
Approximately three-quarters of inci- luteinized cells that form solid and often
dentally identified adnexal masses in bilateral tumors that arise in later preg-
Laparoscopic image of twisted
pregnancy are simple cysts <5 cm.4,6,7 nancy, spontaneously regress after preg-
dermoid cyst at 9 weeks
Among masses at least 2.5 to 5.0 cm or nancy, and can be associated with
gestation
with complex features, 68% to 72% hirsutism or virilization in 25% of pa-
spontaneously resolve by 6 weeks after tients. When maternal virilization oc-
delivery.4,5 Of those that require surgical curs, 60% to 70% of female infants are
management or are removed at the time also born with features of viriliza-
of cesarean delivery, dermoid cysts are tion.18,21 Other rare causes of adnexal
most common (32%), followed by se- mass in pregnancy include heterotopic
rous and mucinous cystadenomas pregnancies, estimated to affect 1 in
(19%), endometriomas (15%), and 30,000 spontaneous pregnancies, and
functional cysts (12%) (Table 1 and tubo-ovarian abscesses, which have been
Figures 1e3).8e17 Bilateral adnexal reported in case literature (Figure 5).22-25
masses have been reported in up to 4% Approximately 2% of adnexal masses
of cases; of the published reports, all in pregnancy are malignant.8e17 A
Image reproduced with permission from Nezhat
bilateral masses were benign.10,13,14 population-based study of nearly 5
et al.119
Adnexal masses unique to pregnancy million patients using California hospi-
Cathcart. Diagnosis and management of adnexal masses
include hyperreactio luteinalis (a term tal records identified 87 cases of ovarian during pregnancy. Am J Obstet Gynecol 2023.
referring to the growth of several theca malignancy in pregnancy, 51% of which
lutein cysts) and luteomas.18-20 Hyper- were epithelial tumors, 39% were germ
reactio luteinalis presents as bilateral cell tumors, and 9% were pseudomyx-
ovarian enlargement, usually in the third oma peritonei.2 Epithelial tumors were
trimester of pregnancy, likely because of most commonly serous carcinomas, and endodermal sinus tumors.2,26,27 Sex
ovarian hyperstimulation by human followed by mucinous, endometrioid, cord-stromal tumors are rare in preg-
chorionic gonadotropin (Figure 4).19 and clear cell carcinomas.2,26 Germ cell nancy.26,28 Most ovarian cancers (64%
Hyperreactio luteinalis typically sponta- tumors are most commonly dysgermi- e81%) diagnosed during pregnancy are
neously regresses after delivery. nomas, followed by malignant teratomas stage I, with most of these cases being
stage IA and the minority of these being
stage IC.2,26,27 Ovarian malignancy
diagnosed during pregnancy is more
TABLE 1 likely to be of earlier stage and lower
Histologic subtypes of adnexal masses in pregnancy requiring surgical grade and is associated with more
management
Type of adnexal mass Incidence (range)
Dermoid 32.0% (18.0%e50.0%) FIGURE 2
Ultrasound of ovarian serous
Endometrioma 15.0% (0.0%e24.0%)
cystadenoma at 8 weeks
Functional cyst 12.0% (3.0%e41.0%) gestation
Serous cystadenoma 11.0% (4.0%e19.0%)
Mucinous cystadenoma 8.0% (3.0%e15.0%)
Hyperreactio luteinalis 9.0% (0.0%e14.0%)
Paraovarian or paratubal cyst 6.0% (0.0%e19.0%)
Fibroma 2.0% (0.0%e5.0%)
Malignancy 2.0% (0.0%e6.0%)
Borderline 1.0% (0.0%e8.0%)
Brenner tumor 0.3% (0.0%e3.0%)
Leiomyoma 0.2% (0.0%e3.0%)
The incidence of each histologic subtype of adnexal mass surgically removed during pregnancy was computed from the Image reproduced with permission from Nezhat
retrospective series of Whitecar et al8 (n¼118), Usui et al9 (n¼69), Sherard et al10 (n¼60), Balci et al11 (n¼36), Türkçüoglu
et al12 (n¼35), Ulker et al13 (n¼119), Baser et al14 (n¼146), Goh et al15 (n¼69), Yu et al16 (n¼1303), and Zhang et al17 et al.119
(n¼228). Cathcart. Diagnosis and management of adnexal masses
Cathcart. Diagnosis and management of adnexal masses during pregnancy. Am J Obstet Gynecol 2023. during pregnancy. Am J Obstet Gynecol 2023.

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Ultrasound is highly accurate, low


FIGURE 3 FIGURE 5
cost, readily available, and safe in preg-
Photograph of left ovarian nancy. Ultrasonographic features of
Laparoscopic image of a tubo-
mucinous cystadenoma removed adnexal masses in pregnancy are similar
ovarian abscess in pregnancy
during cesarean delivery to those observed outside preg-
nancy.30,31 Teratomas feature complex
echo patterns with hyperechoic areas
and distal shadowing because of the
presence of fat, solid, and calcified
components (Figure 6).32,33 Endome-
triomas are complex unilocular or mul-
tilocular cysts featuring diffuse low-level
internal echoes (Figure 7).34 Simple cysts
are anechoic and unilocular with a Image reproduced with permission from Nezhat
smooth thin wall, whereas hemorrhagic et al.119
Cathcart. Diagnosis and management of adnexal masses
cysts may contain hypoechoic internal during pregnancy. Am J Obstet Gynecol 2023.
Image reproduced with permission from Nezhat debris (Figures 8e10).30 Cystadenomas
et al.119 may be simple cysts or have thin septa-
Cathcart. Diagnosis and management of adnexal masses
during pregnancy. Am J Obstet Gynecol 2023.
tions; serous cystadenomas are typically total of 559 adnexal masses, 46 (8%) of
anechoic, whereas mucinous cys- which were malignant.39
tadenomas may have low-level internal Several ultrasound scoring systems
favorable outcomes than that diagnosed echoes because of mucin content originally developed for malignancy
outside of pregnancy.2 (Figure 11).35 Hyperreactio luteinalis is prediction in nonpregnant patients have
characterized by enlarged ovaries with been assessed in pregnant populations,
Evaluation many peripheral thin-walled cysts. including the Sassone, Lerner, Interna-
Initial identification of the adnexal mass in Luteomas can mimic neoplasms on ul- tional Ovarian Tumor Analysis (IOTA)
pregnancy is frequently performed by ul- trasound and appear as heterogenous, Simple Rules, and IOTA Assessment of
trasound, which should be accompanied irregular solid masses.36 Leiomyomas Different NEoplasias in the adneXa
by history and physical examination, appear hypoechoic and round and may (ADNEX) scoring systems (Table 2).40-45
including bimanual and rectovaginal develop cystic spaces as they degen- The Sassone and Lerner models each
evaluation.29 Among symptomatic pa- erate.30 Ultrasonographic features sug- assign points based on 4 ultrasound
tients, the most common complaint is gesting malignancy include thick or variables, with a cutoff of summed
pain.29 irregular septations, mural nodules, points used to discriminate malignant
solid or papillary components, and a masses.42,43 The IOTA Simple Rules
diameter >5 cm (Figures 12 and define malignant and benign ultrasound
FIGURE 4
13).30,37,38 features, with masses exhibiting at least 1
Ultrasound of enlarged A 1997 study by Bromley and Bena-
hyperstimulated ovary with benign or malignant feature classified as
cerraf32 found that 95% of dermoid tu-
multiple peripherally located mors, 80% of endometriomas, and 71%
cysts of simple cysts were correctly charac- FIGURE 6
terized by ultrasonography in a series of Ultrasound showing a dermoid
125 pregnant patients at a single center. cyst with complex echo pattern
Only 10.7% of lesions had ultrasound
characteristics suggestive of malignancy,
and of these cases, 1 patient did have
ovarian cancer. No case of malignancy
was incorrectly diagnosed as benign.31 A
2021 meta-analysis of studies assessing
ultrasound accuracy in diagnosing ma-
lignant masses in pregnancy reported a
pooled sensitivity of 64% (95% confi-
dence interval [CI], 30%e88%), speci-
Image reproduced with permission from Nezhat
ficity of 88% (95% CI, 64%e97%),
et al.119
positive likelihood ratio of 5.6 (95% CI,
Cathcart. Diagnosis and management of adnexal masses Cathcart. Diagnosis and management of adnexal masses
during pregnancy. Am J Obstet Gynecol 2023. 1.2e25.4), and negative likelihood ratio during pregnancy. Am J Obstet Gynecol 2023.
of 0.4 (95% CI, 0.15e1.00) among a

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FIGURE 7 FIGURE 9 FIGURE 11


Ultrasound showing an Ultrasound showing a cystic Ultrasound showing a mucinous
endometrioma with diffuse low- mass with focal intracystic cystadenoma with low-level
level echoes echogenicity internal echoes

Cathcart. Diagnosis and management of adnexal masses


during pregnancy. Am J Obstet Gynecol 2023.

Cathcart. Diagnosis and management of adnexal masses


during pregnancy. Am J Obstet Gynecol 2023. Cathcart. Diagnosis and management of adnexal masses
during pregnancy. Am J Obstet Gynecol 2023. for characterizing large masses;
gastrointestinal-related processes, such as
appendicitis and Crohn disease; tubo-
such and masses exhibiting either no ovarian abscesses; hemorrhagic fibroid
patient age, serum CA-125, and presence
feature or both benign and malignant degeneration; and ovarian torsion. When
of ascites into its risk calculation; these
features classified as inconclusive.44 The cancer is confirmed or strongly suspected,
features may not have the same weight of
IOTA ANDEX involves the input of 3 MRI is also useful in assessing the extent of
clinical relevance in a pregnant popula-
clinical features and 6 ultrasound fea- disease during pregnancy.49,50 T2-
tion, which could explain its relative
tures into a Web-based calculator.45,46 A weighted imaging and diffusion-weighted
underperformance in gravid patients.
recent single-institution study of 153 imaging are valuable techniques for the
Although ultrasound often provides
patients, including 12 patients with ma- characterization of fluid, inflammation,
sufficient information about the risk of
lignancy, found the IOTA Simple Rules abscesses, and tumors in the pelvis without
malignancy in pregnancy, magnetic
to have a sensitivity of 92% and a spec- the need for gadolinium-based contrast,
resonance imaging (MRI) can be a
ificity of 69% for predicting malignancy which is avoided because of concerns for
useful secondary imaging modality
in pregnant patients.47 Another multi- fetal safety.49,51 Although computed to-
center study of 236 patients comparing mography (CT) can be used in pregnancy,
the Sassone, Lerner, and IOTA ADNEX its use results in fetal ionizing radiation
FIGURE 10
models found the Sassone model to exposure (2.5 to 50.0 mGy for CT
MRI showing large left ovarian
perform the best with a sensitivity of pelvimetry) and a theoretical risk of fetal
cystic mass with benign
69% and a specificity of 85%.48 The thyroid suppression.51 As ultrasound and
appearance
IOTA ANDEX model incorporates MRI generally provide adequate

FIGURE 8
FIGURE 12
Ultrasound showing a
hemorrhagic cyst with Ultrasound showing an ovarian
hypoechoic debris adult granulosa cell tumor

MRI, magnetic resonance imaging.


Cathcart. Diagnosis and management of adnexal masses Cathcart. Diagnosis and management of adnexal masses Cathcart. Diagnosis and management of adnexal masses
during pregnancy. Am J Obstet Gynecol 2023. during pregnancy. Am J Obstet Gynecol 2023. during pregnancy. Am J Obstet Gynecol 2023.

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metastatic breast cancer, but its use has also


FIGURE 13
been reported in patients with ovarian and
Ultrasound showing an endometrioid ovarian adenocarcinoma with cervical cancer.53 In a retrospective analysis
papillary projections of 63 patients with cancer who underwent
PET during pregnancy, PET modified the
clinical stage in 60% of patients and sub-
sequently affected first-line treatment.54
Suggestions to optimize safety include us-
ing a lower dose of 18F-FDG in pregnant
patients than in nonpregnant patients,
performing PETalone rather than PET-CT
when possible, and employing vigorous
hydration and urinary catheterization to
facilitate rapid elimination of the
radiopharmaceutical.52

Biomarkers
Tumor markers are less reliable in preg-
nant patients than in nonpregnant pa-
tients, with studies of normal ranges in
Cathcart. Diagnosis and management of adnexal masses during pregnancy. Am J Obstet Gynecol 2023.
pregnancy reporting differing and
sometimes contradictory results.55
Nevertheless, if malignancy is strongly
information without these added risks, CT radiation exposure of 1 to 12 mGy.52,53 suspected or identified, tumor marker
is considered a third-line imaging modality Literature regarding PET use in preg- trends may be valuable. In general, the
in pregnancy. Of note, 18F-FDG positron nancy suggests overall safety but is limited tumor marker CA-125 can be elevated in
emission tomography (PET) use in preg- to case reports and small series; published normal pregnancy, whereas CEA,
nancy has been rarely reported in the experience with PET in pregnancy is pre- inhibin B, antimüllerian hormone, and
literature and carries an estimated fetal dominantly in the setting of lymphoma or lactate dehydrogenase (LDH) remain
within normal limits.55-58 CA-125 ele-
vations are expected beginning in the
TABLE 2
first trimester of pregnancy with re-
Ultrasound adnexal mass scoring systems validated in pregnancy
ported mean values ranging from 19 to
System Features Sensitivity Specificity 85 U/mL and a maximum reported value
Sassone Inner wall structure, wall thickness, septa, and 69% 85% of 550 U/mL.55 CA-125 levels are usually
echogenicity at or below the normal range cutoff value
Lerner Wall structure, shadowing, septa, and echogenicity 77% 69% in the second and third trimesters of
pregnancy but can remain persistently
IOTA Benign features: 92% 69%
Simple Unilocular cyst, presence of solid components <7 mm, elevated in some healthy patients, with a
Rules presence of acoustic shadows, smooth multilocular maximum reported value of 73 U/mL in
tumor with the largest diameter <10 cm, and no the second trimester of pregnancy and
Doppler blood flow 2420 U/mL in the third trimester of
Malignant features:
pregnancy.55 Pregnancy-associated con-
Irregular solid tumor, presence of ascites, at least 4
papillary structures, irregular multilocular solid tumor ditions can cause derangements in tu-
with the largest diameter 10 cm, and high Doppler mor markers; for example, LDH can be
blood flow elevated in preeclampsia.55,59 Alpha-
IOTA Clinical features: 62% 85% fetoprotein is often elevated in preg-
ADNEX Age, serum CA-125, oncology center (yes or no) nancies complicated by neural tube
Ultrasonographic features: defects; however, extremely elevated
Maximum lesion diameter, maximum diameter of the values (>10,000 ng/mL) should raise
largest solid part, more than 10 cyst locules, number of
papillary projections, acoustic shadows, and ascites concern for the presence of a germ cell
tumor.60
Ultrasound scoring systems which have been validated in pregnancy for prediction of malignancy in adnexal masses.42-45
Reported sensitivity and specificity are for the prediction of malignancy in pregnant populations specifically.47,48
ADNEX, Assessment of Different NEoplasias in the adneXa; IOTA, International Ovarian Tumor Analysis. Management
Cathcart. Diagnosis and management of adnexal masses during pregnancy. Am J Obstet Gynecol 2023. Risks associated with adnexal masses in
pregnancy principally include labor

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benefits of delaying treatment must be


FIGURE 14
balanced against maternal risk. In the
Management of the adnexal mass during pregnancy second and third trimesters of preg-
nancy, some studies have found an as-
sociation between chemotherapy
exposure and small-for-gestational-age
neonates, whereas others have shown
no increased incidence of adverse fetal
outcomes.26,74,75,76 Overall, the number
of pregnant patients receiving chemo-
therapy in published cohort studies and
case series is small, and the long-term
effects of antenatal chemotherapy
exposure are unknown. For nonpreg-
nant patients with ovarian cancer, any
chemotherapy delay has been associated
with worse overall survival even after
controlling for comorbidities associated
with therapy delay.77-79 Chemotherapy
planning for the pregnant patient must
Adapted with permission from Nezhat et al.119 involve shared decision-making with
Cathcart. Diagnosis and management of adnexal masses during pregnancy. Am J Obstet Gynecol 2023. acknowledgment of the limitations of
available data. Recommendations for
chemotherapy in pregnancy include
dosing based on actual weight and at the
obstruction, torsion, and malignancy. patients, torsion is an emergency and same dose per weight or body area as in
Approximately 70% of incidentally requires immediate surgical manage- nonpregnant patients and allowing a 3-
identified adnexal masses in pregnancy ment when identified. week window between the last cycle of
spontaneously resolve, with a strong in- In the nonemergent setting, the deci- chemotherapy and delivery for maternal
verse correlation between resolution rate sion for expectant management vs sur- and fetal bone marrow recovery.80
and both size and complexity.4e6,15 gical intervention must balance the risks Breastfeeding during chemotherapy is
Obstruction of labor has been reported of torsion or malignancy with the like- not advised.81,82
in 3% of cases with cysts >3 cm, and lihood of spontaneous resolution and
hospital admission for pain has been the risks of intervention. Consensus Surgical considerations
reported in 2% to 10% of patients.5,6,15 opinion suggests intervening on masses Pregnant patients undergoing pelvic
Reported rates of torsion in large case present after the first trimester of preg- surgery are at an increased risk of fetal
series range from 3% to 12%, with cysts nancy that are >10 cm or have other loss, stillbirth, preterm birth, and having
undergoing torsion having a mean size sonographic features concerning malig- a low birthweight infant compared with
of 10 cm.5,12,15,61-63 A high index of nancy.72 If ovarian malignancy is diag- the general population. The magnitude
suspicion for torsion must be main- nosed at the time of laparoscopic of these relative risks in different studies
tained for the pregnant patient with an surgery, extensive surgery should be varies from negligible to two-fold.83-86
adnexal mass and acute lower abdominal avoided. Good practice includes removal Elective surgery is safer than emergent
pain, as 38% to 60% of pregnant patients of the involved ovary and fallopian tube surgery; a meta-analysis of 67,111 preg-
with torsion have normal Doppler flow and possibly omentum, allowing for nant patients undergoing abdomi-
on ultrasound.64-66 Patients with torsion completion surgery after delivery.73 nopelvic surgery found a higher rate of
in pregnancy are at risk of recurrence; Practical guidelines reflecting several fetal loss with emergent surgery than
the rates of torsion recurrence in the decision points in the management of with elective adnexal surgery (5% vs 1%)
same pregnancy have been reported at adnexal masses in pregnancy are pre- and a higher rate of preterm birth (12%
4% to 15%, with higher rates among sented in Figure 14. vs 4%).87 Maternal mortality is rare, with
patients who undergo surgical detorsion For proven ovarian malignancy in an overall pooled proportion of 0.04% in
alone vs cyst drainage.67,68 Some studies pregnancy, special consideration must that study.87 In general, it is difficult to
have found an increased risk of miscar- be taken as to the use of chemotherapy. separate the risks of surgery from the
riage and preterm delivery after torsion, In general, chemotherapy is avoided in risks of the underlying condition when
whereas other studies have found no the first trimester of pregnancy because assessing adverse pregnancy outcomes.85
adverse maternal or perinatal of the risk of teratogenicity and sponta- The first case of laparoscopic manage-
outcome.69-71 As in nonpregnant neous abortion, although the fetal ment of an ovarian mass during pregnancy

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was published more than 30 years ago.88 differences in blood loss and operative of the combination of increased oxygen
Since that time, several studies comparing time generally of small magnitude.93-96 consumption, increased CO2 production,
outcomes after laparoscopy and laparot- Experience with robotic surgery for and decreased functional residual capacity.
omy in pregnancy have established the adnexal masses in pregnancy is limited During surgery, this predisposition is
relative safety of laparoscopy.89-96 Lapa- but appears safe. Of note, 1 retrospective exacerbated by increased thoracic pressure
roscopy has been consistently shown to be cohort study of 19 pregnant patients with pneumoperitoneum and Trendelen-
associated with shorter hospital length of undergoing robotic resection of adnexal burg positioning.107,108 Theoretically,
stay and less postoperative pain and can be masses compared with 50 consecutive cardiac changes associated with pneumo-
associated with less manipulation of pelvic laparoscopic controls found a decreased peritoneum could result in decreased
organs and better surgical exposure. Re- length of stay and blood loss with robotic uterine blood flow, and elevated maternal
sults regarding operative time, blood loss, surgery and no difference in intra- PaCO2 could limit transplacental fetal CO2
fetal loss, preterm birth, and birthweight operative or postoperative complica- excretion and worsen fetal respiratory
are mixed, with some studies showing no tions or pregnancy outcomes.97 A acidosis. Gravid sheep models have
difference between laparoscopy and lapa- second case series of 6 pregnant patients demonstrated maternal hypercapnia,
rotomy and others showing improved undergoing robotic-assisted ovarian decreased uterine blood flow, increased
outcomes with laparoscopy.89-96 cystectomy reported 1 case of preterm fetal PaCO2, decreased fetal pH, and
Chen et al89 reported a randomized premature rupture of membranes at 30 decreased fetal oxygenation with pneu-
trial of 69 pregnant patients with adnexal weeks of gestation after a robotic pro- moperitoneum.109-111 However, a more
masses requiring surgery who were cedure at 21 weeks of gestation and no recent study in humans found no signifi-
randomly assigned to either laparoscopy other intraoperative or pregnancy cant change in maternal PaCO2 or pH
or laparotomy. Patients had a mean cyst complication.98 during laparoscopic surgery.112 A second
diameter of 8 cm and a mean gestational Regarding surgery timing, elective study in human patients found no differ-
age at surgery of 16 weeks. The laparos- cases should be postponed until after ence in uterine artery resistance index or
copy group had a shorter length of stay delivery, whereas emergent cases should umbilical artery pulsatility index at various
(3 vs 6 days), less postoperative fever never be delayed. Historically, 16 to 20 points during surgery.113 A small but stat-
(3% vs 14%), a lower postoperative pain weeks of gestation has been recom- ically significant decrease in fetal heart rate,
score, and less adhesive disease at the mended as the optimal timing for non- although still within normal limits, was
time of cesarean delivery. The propor- emergent laparoscopic cases because of observed during desufflation despite
tion of patients undergoing cesarean the theoretical decreased risk of miscar- normal uterine blood blow, but was not felt
delivery, gestational age at delivery, riage or preterm labor and improved to be related to fetal perfusion.113
Apgar scores, and birthweight was visualization.37,99 Laparoscopy is not al- Effects of general anesthesia on the
equivalent between groups.89 ways feasible at later gestational ages developing fetus, and in particular neu-
Shigemi et al90 reported a retrospec- owing to the impact of uterine size on rocognitive effects, are incompletely
tive cohort study, including 740 pro- intra-abdominal visualization and known. Animal models suggest agents
pensity score-matched pairs of patients impeded access to pelvic structures. acting via the GABA and NMDA path-
undergoing laparoscopy or laparotomy Nevertheless, recent studies have shown ways may have neurotoxic fetal effects,
in pregnancy, and similarly found a no significant association between the whereas dexmedetomidine attenuates
decreased length of stay for patients trimester of operation and adverse out- this effect.114 However, no data have
undergoing laparoscopy and decreased comes, including surgical complications, corroborated these findings in humans.
rate of blood transfusion and shorter fetal loss, and preterm birth, and several To date, available data regarding the
operative times. In addition, Shigemi case series have reported the safety of long-term safety of antenatal exposure to
et al90 found a significantly decreased laparoscopy in both the first and third general anesthesia are limited to case
risk of a composite of adverse fetal out- trimesters of pregnancy.100-106 Videos reports. In 1 case series of 11 children
comes, including fetal loss, premature depicting laparoscopic ovarian cys- with antenatal exposure to laparoscopic
delivery, and stillbirth with laparoscopy, tectomy at 16 weeks gestation and surgery, no developmental or physical
compared with laparotomy (0.4% vs management of unintentional fetoscopy abnormality was noted at a follow-up of
1.8%, P¼0.01). during laparoscopy are provided in 1 to 8 years.115 The American College
Of 2 recent large meta-analyses, one Figures 15 and 16, respectively. of Obstetricians and Gynecologists
found shorter hospital stay with no The physiology of maternal and fetal currently advises that there is no human
difference in blood loss, operative time, responses to pneumoperitoneum during evidence for an adverse effect of anes-
fetal loss, or preterm birth with lapa- laparoscopic is incompletely understood. thetics or sedatives on the developing
roscopy,91 whereas the other had similar Early observations drawn from gravid fetal brain and no evidence of terato-
findings except for reduced blood loss sheep models have subsequently been genic effects of anesthetics at any gesta-
and 51% lower odds of preterm labor found to differ substantially from obser- tional age.116
with laparoscopy.92 Smaller studies have vations in humans. Pregnancy predisposes The best practices for laparoscopic
reported similar results, with any to hypoxia during apneic episodes because surgery in pregnant patients are

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TABLE 3
Recommendations for laparoscopy during pregnancy
Recommending
Consideration Recommendation organization
Preoperative planning Non-urgent surgery should be postponed until after pregnancy. ACOG, BSGE
Pregnancy should not be a reason to delay urgent surgery. ACOG, BSGE
Laparoscopy can be safely performed during any trimester of SAGES
pregnancy.
There should be early involvement of an obstetrical BSGE
anesthesiologist with preoperative review of features related to
the pregnancy and patient comorbidities.
Surgery should be performed at an institution with obstetrical, ACOG, BSGE
neonatal, and pediatric services.
If expertise to undertake laparoscopic surgery in pregnancy is BSGE
lacking, laparotomy is acceptable.
Anesthesia Modern anesthetic agents have not been shown to be teratogenic ACOG, BSGE
when used in standard doses.
There is no evidence that in utero human exposure to anesthesia ACOG
affects the developing fetal brain.
Patient positioning After the first trimester of pregnancy, left lateral decubitus or SAGES
partial left lateral decubitus position is recommended.
Port placement Initial access can be safely achieved via open (Hasson), Veress SAGES
needle, or optical trocar technique but must account for fundal
height.
Uterine size should be determined by palpation or ultrasound. BSGE
The benefits of the Hasson entry may include reduced risk of BSGE
uterine trauma or spillage of ovarian cysts.
Primary port location (umbilical, supra-umbilical, or Palmers’ BSGE
point) should be chosen according to uterine size, location of
pathology and operator experience
Ipsilateral secondary port placement may prevent the need for BSGE
instrumentation across the gravis uterus.
Insufflation pressure CO2 insufflation of 10e15 mm Hg is appropriate but should be SAGES
adjusted to the patient’s physiology.
Initial insufflation pressure of 20e25 mm Hg is appropriate for BSGE
port placement but operating pressure should be 12 mm Hg.
Creation of pneumoperitoneum and maternal repositioning should BSGE
be gradual.
Intraoperative CO2 monitoring Intraoperative CO2 monitoring by capnography should be used. SAGES
Capnography should be used and maternal hypo- and hypercapnia BSGE
should be avoided.
Laparoscope choice Both 5- and 10-mm diameter laparoscopes are appropriate. Use BSGE
of a 30-degree laparoscope may be helpful.
Energy modalities Ultrasound, bipolar, and monopolar energy sources are safe to use BSGE
during laparoscopy in pregnancy.
Cathcart. Diagnosis and management of adnexal masses during pregnancy. Am J Obstet Gynecol 2023. (continued)

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TABLE 3
Recommendations for laparoscopy during pregnancy (continued)
Recommending
Consideration Recommendation organization
Fetal heart rate monitoring Fetal heart rate monitoring may assist in maternal positioning and ACOG
cardiorespiratory management and may influence a decision to
deliver the fetus.
Simultaneous fetal heart rate tracing and contraction monitoring ACOG
should be performed before and after surgery for viable fetuses.
Preoperative and postoperative fetal heart rate detection by ACOG
Doppler is sufficient for previable fetuses.
Intraoperative fetal heart rate monitoring may be appropriate ACOG
when the fetus is viable, monitoring is possible, and emergent
cesarean delivery would be considered.
Preoperative and postoperative fetal heart rate monitoring are BSGE, SAGES
recommending past the age of viability, but intraoperative fetal
heart rate monitoring is not recommended.
Tocolytics Routine prophylactic use of tocolytics is not recommended. BSGE, SAGES
Antenatal corticosteroids Corticosteroid administration should be considered for patients ACOG, BSGE
with fetuses at viable premature gestational ages.
Anti-D immunoglobulin Prophylactic anti-D immunoglobulin administration is not BSGE
required.
Antibiotics Routine antibiotics are not required unless infection is suspected. BSGE
Venous thromboembolism prophylaxis Patients should be screened for venous thromboembolism risk ACOG
and have the appropriate perioperative prophylaxis.
Pharmacologic prophylaxis with low-molecular-weight heparin BSGE
should be considered.
Intra- and postoperative sequential compression devices and SAGES
early postoperative ambulation are recommended.
Evidence-based recommendations for laparoscopy in pregnancy were obtained from the ACOG,116 the BSGE,117 and the SAGES.118
ACOG, American College of Obstetricians and Gynecologists; BSGE, British Society for Gynaecological Endoscopy; SAGES, Society of American Gastrointestinal and Endoscopic Surgeons.
Cathcart. Diagnosis and management of adnexal masses during pregnancy. Am J Obstet Gynecol 2023.

summarized in Table 3.116-118 These Conclusion basis of expert clinical opinion,


include left lateral decubitus positioning The diagnosis of adnexal masses in balancing the risks and benefits of
after the first trimester of pregnancy, pregnancy has become more common as intervention for a particular patient, and
port placement with respect to uterine routine first-trimester ultrasound has allowing for shared decision-making.
size and pathology location, insufflation become widespread. Most adnexal The last decade of experience has so-
pressure of less than 12 to 15 mm Hg, masses identified in pregnancy are sim- lidified laparoscopy as preferable to lap-
intraoperative maternal capnography, ple cysts less than 5 cm, can be safely arotomy because of decreased patient
and pre- and postoperative fetal heart observed, and ultimately spontaneously pain and length of hospital stay. Small
rate and contraction monitoring. Ante- resolve. benefits in terms of reduced operative
natal corticosteroids for fetal benefit may Ultrasound remains the most impor- time, blood loss, and adverse fetal out-
be considered based on the clinical sce- tant tool in the workup of adnexal comes have also been demonstrated,
nario, whereas routine use of tocolytics, masses because of its safety, availability, although inconsistently. Importantly,
anti-D immune globulin, and antibiotics and predictive ability for differentiating laparotomy is still considered safe in
are not recommended. As pregnancy is a benign and malignant masses. Although pregnancy when appropriate expertise
hypercoagulable state, patients should be several formalized ultrasound-based for laparoscopic surgery is unavailable or
screened for venous thromboembolism scoring systems have been validated anatomic features, such as uterine and
risk, and appropriate mechanical and specifically in pregnant populations, the mass size, preclude laparoscopy.
chemical thromboprophylaxes should be ultimate decision for when to intervene Long-term studies on childhood and
administered. on a mass in pregnancy is made on the later-life outcomes after antenatal

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exposure to surgery are lacking, and 8. Whitecar MP, Turner S, Higby MK. Adnexal 24. Tal J, Haddad S, Gordon N, Timor-Tritsch I.
although small studies support the safety of masses in pregnancy: a review of 130 cases Heterotopic pregnancy after ovulation induction
undergoing surgical management. Am J Obstet and assisted reproductive technologies: a liter-
surgery, data limitations must be Gynecol 1999;181:19–24. ature review from 1971 to 1993. Fertil Steril
acknowledged in preoperative patient 9. Usui R, Minakami H, Kosuge S, Iwasaki R, 1996;66:1–12.
counseling. Nevertheless, the real risks of Ohwada M, Sato I. A retrospective survey of 25. Kim YA, Chun KC, Koh JW, Song HS,
delaying diagnosis and treatment of ma- clinical, pathologic, and prognostic features of Kim HS. How to approach the rupture of tubo-
lignancy or creating a need for emergent adnexal masses operated on during pregnancy. ovarian abscess during pregnancy: a case
J Obstet Gynaecol Res 2000;26:89–93. report and literature review. J Obstet Gynaecol
surgery are well-established for the preg- 10. Sherard GB 3rd, Hodson CA, Williams HJ, Res 2021;47:1199–203.
nant patient and fetus, and necessary sur- Semer DA, Hadi HA, Tait DL. Adnexal masses 26. Blake EA, Kodama M, Yunokawa M, et al.
gery should not be delayed due to and pregnancy: a 12-year experience. Am J Feto-maternal outcomes of pregnancy compli-
pregnancy or gestational age. Careful pre- Obstet Gynecol 2003;189:358–62. discussion cated by epithelial ovarian cancer: a systematic
operative planning and treatment by an 362e3. review of literature. Eur J Obstet Gynecol
11. Balci O, Gezginc K, Karatayli R, Acar A, Reprod Biol 2015;186:97–105.
experienced surgeon at a facility with Celik C, Colakoglu MC. Management and out- 27. Kodama M, Grubbs BH, Blake EA, et al.
anesthetic, obstetric, and neonatal support comes of adnexal masses during pregnancy: a Feto-maternal outcomes of pregnancy compli-
generally results in excellent outcomes for 6-year experience. J Obstet Gynaecol Res cated by ovarian malignant germ cell tumor: a
the pregnant patient and fetus. - 2008;34:524–8. systematic review of literature. Eur J Obstet
12. Türkçüog lu I, Meydanli MM, Engin-Ustün Y, Gynecol Reprod Biol 2014;181:145–56.
Ustün Y, Kafkasli A. Evaluation of histopatho- 28. Young RH, Dudley AG, Scully RE. Gran-
ACKNOWLEDGMENTS logical features and pregnancy outcomes of ulosa cell, Sertoli-Leydig cell, and unclassified
The authors thank Dr Andrea Tinelli for providing pregnancy associated adnexal masses. sex cord-stromal tumors associated with preg-
the ultrasound image in Figure 2; Dr Thomas J Obstet Gynaecol 2009;29:107–9. nancy: a clinicopathological analysis of thirty-six
Trevett for the ultrasound image in Figure 9; Dr 13. Ulker V, Gedikbasi A, Numanoglu C, cases. Gynecol Oncol 1984;18:181–205.
Bryann Bromley for the ultrasound image in Saygi S, Aslan H, Gulkilik A. Incidental adnexal 29. Cavaco-Gomes J, Jorge Moreira C,
Figure 13; Drs Kimberly Kho, Nicholas Nezhat, masses at cesarean section and review of the Rocha A, Mota R, Paiva V, Costa A. Investigation
and Bob Fay for contributions to the video in literature. J Obstet Gynaecol Res 2010;36: and management of adnexal masses in preg-
Figure 16; and Dr David Abel for helpful com- 502–5. nancy. Scientifica (Cairo) 2016;2016:3012802.
ments regarding PET use in pregnancy. 14. Baser E, Erkilinc S, Esin S, et al. Adnexal 30. Chiang G, Levine D. Imaging of adnexal
masses encountered during cesarean delivery. masses in pregnancy. J Ultrasound Med
Int J Gynaecol Obstet 2013;123:124–6. 2004;23:805–19.
15. Goh WA, Rincon M, Bohrer J, et al. Persis- 31. Bromley B, Benacerraf B. Adnexal masses
REFERENCES tent ovarian masses and pregnancy outcomes. during pregnancy: accuracy of sonographic
1. Nazer A, Czuzoj-Shulman N, Oddy L, J Matern Fetal Neonatal Med 2013;26: diagnosis and outcome. J Ultrasound Med
Abenhaim HA. Incidence of maternal and 1090–3. 1997;16:447–52. quiz 453.
neonatal outcomes in pregnancies complicated 16. Yu C, Wang J, Lu W, Xie X, Cheng X, Li X. 32. Caspi B, Appelman Z, Rabinerson D,
by ovarian masses. Arch Gynecol Obstet Analysis of adnexal mass managed during ce- Elchalal U, Zalel Y, Katz Z. Pathognomonic echo
2015;292:1069–74. sarean section. Adv Clin Exp Med 2019;28: patterns of benign cystic teratomas of the ovary:
2. Leiserowitz GS, Xing G, Cress R, 447–52. classification, incidence and accuracy rate of
Brahmbhatt B, Dalrymple JL, Smith LH. Adnexal 17. Zhang Z, Zheng X, Zhang M, et al. Patho- sonographic diagnosis. Ultrasound Obstet
masses in pregnancy: how often are they ma- logical features of persistent adnexal masses in Gynecol 1996;7:275–9.
lignant? Gynecol Oncol 2006;101:315–21. pregnancy. Ann Transl Med 2021;9:973. 33. Outwater EK, Siegelman ES, Hunt JL.
3. Hermans AJ, Kluivers KB, Janssen LM, et al. 18. Masarie K, Katz V, Balderston K. Pregnancy Ovarian teratomas: tumor types and imaging
Adnexal masses in children, adolescents and luteomas: clinical presentations and manage- characteristics. RadioGraphics 2001;21:
women of reproductive age in the Netherlands: a ment strategies. Obstet Gynecol Surv 2010;65: 475–90.
nationwide population-based cohort study. 575–82. 34. Patel MD, Feldstein VA, Chen DC,
Gynecol Oncol 2016;143:93–7. 19. Watkins JC, Lebok P, Young RH. Hyper- Lipson SD, Filly RA. Endometriomas: diagnostic
4. Bernhard LM, Klebba PK, Gray DL, reactio luteinalis (multiple luteinized follicle cysts): performance of US. Radiology 1999;210:
Mutch DG. Predictors of persistence of adnexal a report of 10 cases. Int J Gynecol Pathol 739–45.
masses in pregnancy. Obstet Gynecol 1999;93: 2021;40:427–34. 35. Marko J, Marko KI, Pachigolla SL,
585–9. 20. Wang CW, Liu WM, Chen CH. Hyperreactio Crothers BA, Mattu R, Wolfman DJ. Mucinous
5. Condous G, Khalid A, Okaro E, Bourne T. luteinalis mimicking malignancy during preg- neoplasms of the ovary: radiologic-pathologic
Should we be examining the ovaries in preg- nancy with elevated CA-125. Taiwan J Obstet correlation. RadioGraphics 2019;39:982–97.
nancy? Prevalence and natural history of Gynecol 2019;58:885–7. 36. Khurana A, OʼBoyle M. Luteoma of preg-
adnexal pathology detected at first-trimester 21. Wang L, Zhou C, Jiang J, Zhang Z, Li X, nancy. Ultrasound Q 2017;33:90–2.
sonography. Ultrasound Obstet Gynecol Zhang W. Clinicopathologic features of preg- 37. Hoover K, Jenkins TR. Evaluation and
2004;24:62–6. nancy luteoma. Int J Gynaecol Obstet 2022;159: management of adnexal mass in pregnancy. Am
6. Zanetta G, Mariani E, Lissoni A, et al. 351–6. J Obstet Gynecol 2011;205:97–102.
A prospective study of the role of ultrasound in 22. Talbot K, Simpson R, Price N, Jackson SR. 38. Brown DL, Dudiak KM, Laing FC. Adnexal
the management of adnexal masses in preg- Heterotopic pregnancy. J Obstet Gynaecol masses: US characterization and reporting.
nancy. BJOG 2003;110:578–83. 2011;31:7–12. Radiology 2010;254:342–54.
7. Hill LM, Connors-Beatty DJ, Nowak A, 23. Maleki A, Khalid N, Rajesh Patel C, El- 39. Gaughran JE, Naji O, Al Sabbagh MQ,
Tush B. The role of ultrasonography in the Mahdi E. The rising incidence of heterotopic Sayasneh A. Is ultrasound a reliable and repro-
detection and management of adnexal masses pregnancy: current perspectives and associa- ducible method for assessing adnexal masses in
during the second and third trimesters of preg- tions with in-vitro fertilization. Eur J Obstet pregnancy? A systematic review. Cureus
nancy. Am J Obstet Gynecol 1998;179:703–7. Gynecol Reprod Biol 2021;266:138–44. 2021;13:e19079.

610 American Journal of Obstetrics & Gynecology JUNE 2023


Descargado para Anonymous User (n/a) en Ricardo Palma University de ClinicalKey.es por Elsevier en julio 19, 2023. Para uso
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ajog.org Expert Reviews

40. Lee SJ, Oh HR, Na S, Hwang HS, Lee SM. cancer assessment: a review. J Clin Med aspiration and drainage are important in pre-
Ultrasonographic ovarian mass scoring system 2022;11:3820. venting recurrence. Isr Med Assoc J 2021;23:
for predicting malignancy in pregnant women 54. Despierres M, Boudy AS, Selleret L, et al. 48–51.
with ovarian mass. Obstet Gynecol Sci 2022;65: Feasibility, safety and impact of (18F)-FDG PET/ 69. Dvash S, Pekar M, Melcer Y, Weiner Y,
1–13. CT in patients with pregnancy-associated can- Vaknin Z, Smorgick N. Adnexal torsion in preg-
41. Czekierdowski A, Stachowicz N, Smolen  A, cer: experience of the French CALG (Cancer nancy managed by laparoscopy is associated
et al. Sonographic assessment of complex ul- Associé à La Grossesse) network. Acta Oncol with favorable obstetric outcomes. J Minim
trasound morphology adnexal tumors in preg- 2022;61:302–8. Invasive Gynecol 2020;27:1295–9.
nant women with the use of IOTA Simple Rules 55. Han SN, Lotgerink A, Gziri MM, Van 70. Daykan Y, Bogin R, Sharvit M, et al. Adnexal
Risk and ADNEX scoring systems. Diagnostics Calsteren K, Hanssens M, Amant F. Physiologic torsion during pregnancy: outcomes after sur-
(Basel) 2021:11. variations of serum tumor markers in gyneco- gical intervention-a retrospective case-control
42. Sassone AM, Timor-Tritsch IE, Artner A, logical malignancies during pregnancy: a sys- study. J Minim Invasive Gynecol 2019;26:
Westhoff C, Warren WB. Transvaginal sono- tematic review. BMC Med 2012;10:86. 117–21.
graphic characterization of ovarian disease: 56. Ercan Ş, Kaymaz Ö, Yücel N, Orçun A. 71. Rottenstreich M, Rotem R, Hirsch A, et al.
evaluation of a new scoring system to predict Serum concentrations of CA 125, CA 15-3, CA Maternal and perinatal outcomes following lap-
ovarian malignancy. Obstet Gynecol 1991;78: 19-9 and CEA in normal pregnancy: a longitu- aroscopy for suspected adnexal torsion during
70–6. dinal study. Arch Gynecol Obstet 2012;285: pregnancy: a multicenter cohort study. Arch
43. Lerner JP, Timor-Tritsch IE, Federman A, 579–84. Gynecol Obstet 2020;302:1413–9.
Abramovich G. Transvaginal ultrasonographic 57. Petraglia F, Luisi S, Benedetto C, et al. 72. Montes De Oca MK, Dotters-Katz SK,
characterization of ovarian masses with an Changes of dimeric inhibin B levels in maternal Kuller JA, Previs RA. Adnexal masses in preg-
improved, weighted scoring system. Am J serum throughout healthy gestation and in nancy. Obstet Gynecol Surv 2021;76:437–50.
Obstet Gynecol 1994;170:81–5. women with gestational diseases. J Clin Endo- 73. Benigno BB. Ovarian cancer in pregnancy.
44. Timmerman D, Testa AC, Bourne T, et al. crinol Metab 1997;82:2991–5. In: Nezhat CH, Kavic MS, Lanzafame RJ,
Simple ultrasound-based rules for the diagnosis 58. Sarandakou A, Protonotariou E, Rizos D. Lindsay MK, Polk TM, eds. Non-obstetric sur-
of ovarian cancer. Ultrasound Obstet Gynecol Tumor markers in biological fluids associated gery during pregnancy. Cham, Germany:
2008;31:681–90. with pregnancy. Crit Rev Clin Lab Sci 2007;44: Springer; 2019.
45. Van Calster B, Van Hoorde K, Valentin L, 151–78. 74. De Haan J, Verheecke M, Van Calsteren K,
et al. Evaluating the risk of ovarian cancer before 59. Korenaga TK, Tewari KS. Gynecologic et al. Oncological management and obstetric
surgery using the ADNEX model to differentiate cancer in pregnancy. Gynecol Oncol 2020;157: and neonatal outcomes for women diagnosed
between benign, borderline, early and advanced 799–809. with cancer during pregnancy: a 20-year inter-
stage invasive, and secondary metastatic tu- 60. Nawa A, Obata N, Kikkawa F, et al. Prog- national cohort study of 1170 patients. Lancet
mours: prospective multicentre diagnostic nostic factors of patients with yolk sac tumors of Oncol 2018;19:337–46.
study. BMJ 2014;349. g5920. the ovary. Am J Obstet Gynecol 2001;184: 75. Pei Y, Gou Y, Li N, Yang X, Han X, Huiling L.
46. Van Calster B, Van Hoorde K, Froyman W, 1182–8. Efficacy and safety of platinum-based chemo-
et al. Practical guidance for applying the ADNEX 61. Koo YJ, Kim TJ, Lee JE, et al. Risk of torsion therapy for ovarian cancer during pregnancy: a
model from the IOTA group to discriminate be- and malignancy by adnexal mass size in preg- systematic review and meta-analysis. Oncol
tween different subtypes of adnexal tumors. nant women. Acta Obstet Gynecol Scand Ther 2022;10:55–73.
Facts Views Vis Obgyn 2015;7:32–41. 2011;90:358–61. 76. Amant F, Vandenbroucke T, Verheecke M,
47. Rabiej-Wronska E, Wiechec M, Pitynski K, 62. Yen CF, Lin SL, Murk W, et al. Risk analysis et al. Pediatric outcome after maternal cancer
Wiercinska E, Kotlarz A. Ultrasound differentia- of torsion and malignancy for adnexal masses diagnosed during pregnancy. N Engl J Med
tion between benign versus malignant adnexal during pregnancy. Fertil Steril 2009;91: 2015;373:1824–34.
masses in pregnant patients. Ginekol Pol 1895–902. 77. Seagle BL, Butler SK, Strohl AE, Nieves-
2022;93:643–9. 63. Schmeler KM, Mayo-Smith WW, Peipert JF, Neira W, Shahabi S. Chemotherapy delay after
48. Lee SJ, Kim YH, Lee MY, et al. Ultrasono- Weitzen S, Manuel MD, Gordinier ME. Adnexal primary debulking surgery for ovarian cancer.
graphic evaluation of ovarian mass for predicting masses in pregnancy: surgery compared with Gynecol Oncol 2017;144:260–5.
malignancy in pregnant women. Gynecol Oncol observation. Obstet Gynecol 2005;105: 78. Joseph N, Clark RM, Dizon DS, et al. Delay
2021;163:385–91. 1098–103. in chemotherapy administration impacts survival
49. Horowitz JM, Hotalen IM, Miller ES, 64. Wang YX, Deng S. Clinical characteristics, in elderly patients with epithelial ovarian cancer.
Barber EL, Shahabi S, Miller FH. How can pelvic treatment and outcomes of adnexal torsion in Gynecol Oncol 2015;137:401–5.
MRI with diffusion-weighted imaging help my pregnant women: a retrospective study. BMC 79. Nasioudis D, Mastroyannis SA, Ko EM, et al.
pregnant patient? Am J Perinatol 2020;37: Pregnancy Childbirth 2020;20:483. Delay in adjuvant chemotherapy administration
577–88. 65. Hasson J, Tsafrir Z, Azem F, et al. Com- for patients with FIGO stage I epithelial ovarian
50. Lee JH, Roh HJ, Ahn JW, et al. The diag- parison of adnexal torsion between pregnant carcinoma is associated with worse survival; an
nostic accuracy of magnetic resonance imaging and nonpregnant women. Am J Obstet Gynecol analysis of the National Cancer Database.
for maternal acute adnexal torsion during preg- 2010;202:536.e1–6. Gynecol Oncol 2022;166:263–8.
nancy: single-institution clinical performance 66. Smorgick N, Pansky M, Feingold M, 80. Amant F, Berveiller P, Boere IA, et al. Gy-
review. J Clin Med 2020;9:2209. Herman A, Halperin R, Maymon R. The clinical necologic cancers in pregnancy: guidelines
51. Committee Opinion No. 723: guidelines for characteristics and sonographic findings of based on a third international consensus
diagnostic imaging during pregnancy and maternal ovarian torsion in pregnancy. Fertil meeting. Ann Oncol 2019;30:1601–12.
lactation. Obstet Gynecol 2017;130:e210–6. Steril 2009;92. 1983e7. 81. Pistilli B, Bellettini G, Giovannetti E, et al.
52. Takalkar AM, Khandelwal A, Lokitz S, 67. Pansky M, Feingold M, Maymon R, Ben Chemotherapy, targeted agents, antiemetics
Lilien DL, Stabin MG. 18F-FDG PET in preg- Ami I, Halperin R, Smorgick N. Maternal adnexal and growth-factors in human milk: how should
nancy and fetal radiation dose estimates. J Nucl torsion in pregnancy is associated with signifi- we counsel cancer patients about breastfeed-
Med 2011;52:1035–40. cant risk of recurrence. J Minim Invasive Gynecol ing? Cancer Treat Rev 2013;39:207–11.
53. Parpinel G, Laudani ME, Giunta FP, 2009;16:551–3. 82. Damoiseaux D, Calpe S, Rosing H, et al.
Germano C, Zola P, Masturzo B. Use of positron 68. Melcer Y, Dvash S, Maymon R, et al. Torsion Presence of five chemotherapeutic drugs in
emission tomography for pregnancy-associated of functional adnexal cysts in pregnancy: breast milk as a guide for the safe use of

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chemotherapy during breastfeeding: results mass in pregnancy: what is the ideal surgical 108. Chohan L, Nijjar JB. Minimally invasive
from a case series. Clin Pharmacol Ther approach? J Minim Invasive Gynecol 2011;18: surgery in pregnancy. Clin Obstet Gynecol
2022;112:404–10. 720–5. 2020;63:379–91.
83. Cho HW, Cho GJ, Noh E, Hong JH, Kim M, 95. Ngu SF, Cheung VY, Pun TC. Surgical 109. Uemura K, McClaine RJ, de la Fuente SG,
Lee JK. Pregnancy outcomes following laparo- management of adnexal masses in pregnancy. et al. Maternal insufflation during the second
scopic and open surgery in pelvis during preg- JSLS 2014;18:71–5. trimester equivalent produces hypercapnia,
nancy: a nationwide population-based study in 96. Carter JF, Soper DE. Operative laparoscopy acidosis, and prolonged hypoxia in fetal sheep.
Korea. J Korean Med Sci 2021;36:e192. in pregnancy. JSLS 2004;8:57–60. Anesthesiology 2004;101:1332–8.
84. Reedy MB, Källén B, Kuehl TJ. Laparoscopy 97. Eichelberger KY, Cantrell LA, Balthazar U, 110. Hunter JG, Swanstrom L, Thornburg K.
during pregnancy: a study of five fetal outcome Boggess KA, Strauss RA, Boggess JF. Robotic Carbon dioxide pneumoperitoneum induces
parameters with use of the Swedish Health Reg- resection of adnexal masses during pregnancy. fetal acidosis in a pregnant ewe model. Surg
istry. Am J Obstet Gynecol 1997;177:673–9. Am J Perinatol 2013;30:371–5. Endosc 1995;9:272–7. discussion 277e9.
85. Aylin P, Bennett P, Bottle A, et al. Estimating 98. Carter S, Depasquale S, Stallings S. Ro- 111. Curet MJ, Vogt DA, Schob O, Qualls C,
the risk of adverse birth outcomes in pregnant botic-assisted laparoscopic ovarian cystectomy Izquierdo LA, Zucker KA. Effects of CO2 pneu-
women undergoing non-obstetric surgery using during pregnancy. AJP Rep 2011;1:21–4. moperitoneum in pregnant ewes. J Surg Res
routinely collected NHS data: an observational 99. Tazuke SI, Nezhat FR, Nezhat CH, 1996;63:339–44.
study. Southampton, United: NIHR Journals Li- Seidman DS, Phillips DR, Nezhat CR. Laparo- 112. Bhavani-Shankar K, Steinbrook RA,
brary; 2016. scopic management of pelvic pathology during Brooks DC, Datta S. Arterial to end-tidal carbon
86. Mazze RI, Kallén B. Reproductive outcome pregnancy. J Am Assoc Gynecol Laparosc dioxide pressure difference during laparoscopic
after anesthesia and operation during preg- 1997;4:605–8. surgery in pregnancy. Anesthesiology 2000;93:
nancy: a registry study of 5405 cases. Am J 100. Zou G, Xu P, Zhu L, Ding S, Zhang X. 370–3.
Obstet Gynecol 1989;161:1178–85. Comparison of subsequent pregnancy out- 113. Candiani M, Maddalena S, Barbieri M,
87. Cusimano MC, Liu J, Azizi P, et al. Adverse comes after surgery for adnexal masses per- Izzo S, Alberico D, Ronzoni S. Adnexal masses
fetal outcomes and maternal mortality following formed in the first and second trimester of in pregnancy: fetomaternal blood flow indices
non-obstetric abdominopelvic surgery in preg- pregnancy. Int J Gynaecol Obstet 2020;148: during laparoscopic surgery. J Minim Invasive
nancy: a systematic review and meta-analysis. 305–9. Gynecol 2012;19:443–7.
Ann Surg 2021 [Epub ahead of print]. 101. Weiner E, Mizrachi Y, Keidar R, Kerner R, 114. Olutoye OA, Style C, Menchaca A. Neu-
88. Nezhat F, Nezhat C, Silfen SL, Fehnel SH. Golan A, Sagiv R. Laparoscopic surgery per- rocognitive effects of fetal exposure to anes-
Laparoscopic ovarian cystectomy during preg- formed in advanced pregnancy compared to thesia. Anesthesiol Clin 2021;39:851–69.
nancy. J Laparoendosc Surg 1991;1:161–4. early pregnancy. Arch Gynecol Obstet 115. Rizzo AG. Laparoscopic surgery in preg-
89. Chen L, Ding J, Hua K. Comparative anal- 2015;292:1063–8. nancy: long-term follow-up. J Laparoendosc
ysis of laparoscopy versus laparotomy in the 102. Ko ML, Lai TH, Chen SC. Laparoscopic Adv Surg Tech A 2003;13:11–5.
management of ovarian cyst during pregnancy. management of complicated adnexal masses in 116. ACOG Committee Opinion No. 775: non-
J Obstet Gynaecol Res 2014;40:763–9. the first trimester of pregnancy. Fertil Steril obstetric surgery during pregnancy. Obstet
90. Shigemi D, Aso S, Matsui H, Fushimi K, 2009;92:283–7. Gynecol 2019;133:e285–6.
Yasunaga H. Safety of laparoscopic surgery for 103. Minig L, Otaño L, Cruz P, Patrono MG, 117. Ball E, Waters N, Cooper N, et al. Evi-
benign diseases during pregnancy: a nationwide Botazzi C, Zapardiel I. Laparoscopic surgery for dence-based guideline on laparoscopy in preg-
retrospective cohort study. J Minim Invasive treating adnexal masses during the first trimester nancy: commissioned by the British Society for
Gynecol 2019;26:501–6. of pregnancy. J Minim Access Surg 2016;12: Gynaecological Endoscopy (BSGE) endorsed
91. Cagino K, Li X, Thomas C, Delgado D, 22–5. by the Royal College of Obstetricians & Gynae-
Christos P, Acholonu U Jr. Surgical manage- 104. Lenglet Y, Roman H, Rabishong B, et al. cologists (RCOG). Facts Views Vis Obgyn
ment of adnexal masses in pregnancy: a sys- Laparoscopic management of ovarian cysts 2019;11:5–25.
tematic review and meta-analysis. J Minim during pregnancy. Gynecol Obstet Fertil 118. Pearl JP, Price RR, Tonkin AE,
Invasive Gynecol 2021;28:1171–82.e2. 2006;34:101–6. Richardson WS, Stefanidis D. SAGES guidelines
92. Ye P, Zhao N, Shu J, et al. Laparoscopy 105. Mathevet P, Nessah K, Dargent D, for the use of laparoscopy during pregnancy.
versus open surgery for adnexal masses in Mellier G. Laparoscopic management of adnexal Surg Endosc 2017;31:3767–82.
pregnancy: a meta-analytic review. Arch Gyne- masses in pregnancy: a case series. Eur J 119. Nezhat F, Wang P, Tinelli A. Adnexal mass
col Obstet 2019;299:625–34. Obstet Gynecol Reprod Biol 2003;108:217–22. in pregnancy. In: Nezhat CH, Kavic MS,
93. Koo YJ, Kim HJ, Lim KT, et al. Laparotomy 106. Buser KB. Laparoscopic surgery in the Lanzafame RJ, Lindsay MK, Polk TM, eds. Non-
versus laparoscopy for the treatment of adnexal pregnant patient: results and recommendations. obstetric surgery during pregnancy. Cham,
masses during pregnancy. Aust N Z J Obstet JSLS 2009;13:32–5. Germany: Springer; 2019.
Gynaecol 2012;52:34–8. 107. O’Rourke N, Kodali BS. Laparoscopic 120. Kho KA, Nezhat C. Management of unin-
94. Balthazar U, Steiner AZ, Boggess JF, surgery during pregnancy. Curr Opin Anaes- tentional fetoscopy. J Minim Invasive Gynecol
Gehrig PA. Management of a persistent adnexal thesiol 2006;19:254–9. 2009;16:S6–7.

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