Relationship between ovarian cysts

and infertility: what surgery

and when?
Guillaume Legendre, M.D., Laurent Catala, M.D., Catherine Morini ere, M.D., C eline Lacoeuille, M.D.,
Franc oise Boussion, M.D., Loc Sentilhes, M.D., Ph.D., and Philippe Descamps, M.D., Ph.D.
Service de Gyn ecologie-Obst etrique, Centre Hospitalier Universitaire d'Angers, Angers, France
The relationship between ovarian cysts and infertility is a subject of debate, mainly because it is difcult to determine the real impact of
the cyst and its treatment on later fertility. For a long time it was hoped that surgical treatment could prevent potential complications
(such as rupture or malignancy). For presumed benign ovarian tumors, fertility sparing should be the main concern. The goal of this
survey of current knowledge on the subject is to thoroughly explore the potential relationship between cysts, their treatment, and infer-
tility. Our study is based on a review of the literature dealing with the epidemiology of ovarian cysts and the effects of their surgical
management in relation to infertility. Analysis of the epidemiologic data, drawn mainly from comparative studies and cohorts, shows
that the role of cysts in infertility is controversial and that the effects of surgical treatment are often more harmful than the cyst itself to
the ovarian reserve. Surgery does not seem to improve pregnancy rates. When a surgical option is nonetheless chosen, a conservative
laparoscopic approach is more suitable. Besides excision, sclerotherapy and plasma vaporization are promising, offering a greater pres-
ervation of the ovarian parenchyma, especially in endometriomas. These techniques must be better dened. The context of the infertility
is essential, and surgeons and specialists in reproductive medicine should decide management
jointly. (Fertil Steril

2014;101:60814. 2014 by American Society for Reproductive

Medicine.)
Key Words: Ovarian cyst, endometrioma, mature teratoma cyst, infertility, ART, IVF, ovarian
reserve, cystectomy
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A
n ovarian cyst is a common
discovery in women of repro-
ductive age generally as well
as in those undergoing work-ups for
infertility. Surgical management by
laparoscopic cystectomy is often the
rule, to prevent such potential compli-
cations as rupture or malignancy, while
optimizing preservation of fertility (1).
The impact of the cyst on folliculogen-
esis depends on the nature, size, and
number of cysts. Most women consider
it essential that their physicians provide
them with clear information on the
consequences on subsequent fertility
of cysts and their management (2). It
is not, however, always easy to deter-
mine the cyst's relationship to a wom-
an's infertility, which can have many
causes. Further treatment can result in
a nontrivial reduction in ovarian
reserve. The management of ovarian
cysts in an infertile woman raises two
questions: 1) Do these cysts impair the
prognosis of assisted reproductive tech-
nologies (ART)? and 2) How does
treatment of a cyst affect these results?
These two questions obviously depend
on various factors, including the size,
number, and histologic type of cysts.
The roles of therapeutic abstention,
aspiration, vaporization, and cystec-
tomy will be discussed in this review
of the literature.
MATERIALS AND METHODS
This literature review was conducted by
consulting the Medline database for
articles published from January 2000
through August 2013. The articles
were selected by combining the
following key words: ovarian cyst,
endometrioma, mature teratoma cyst,
infertility, ART, IVF, ovarian reserve,
surgery, cystectomy, aspiration. Our se-
lection gave priority to meta-analyses,
literature reviews, randomized
controlled trials, and cohort studies.
The level of evidence (LE) scale proposes
by the Oxford Centre for Evidence-
Based Medicine (www.cebm.net) was
used to classify the selected articles.
IMPACT OF OVARIAN CYSTS
ON FERTILITY
Endometrioma
Endometriosis affects up to 10% of
women of reproductive age (LE1)
(35). At least one endometrioma is
Received December 4, 2013; revised January 6, 2014; accepted January 15, 2014.
G.L. has nothing to disclose. L.C. has nothing to disclose. C.M. has nothing to disclose. C.L. has nothing
to disclose. F.B. has nothing to disclose. L.S. has nothing to disclose. P.D. has nothing to disclose.
Reprint requests: Guillaume Legendre, M.D., Service de Gyn ecologie-Obst etrique, Centre Hospitalier
Universitaire d'Angers, 4, rue Larrey, 49033, Angers Cedex 01, France (E-mail: g_legendre@
hotmail.com).
Fertility and Sterility Vol. 101, No. 3, March 2014 0015-0282/$36.00
Copyright 2014 American Society for Reproductive Medicine, Published by Elsevier Inc.
http://dx.doi.org/10.1016/j.fertnstert.2014.01.021
608 VOL. 101 NO. 3 / MARCH 2014
found in 20%40%of patients with endometriosis (6, 7) and is
often associated with a more severe form of endometriosis
(LE2). Despite the lack of evidence of a causal relation
between endometriosis and infertility, many studies have
examined the impact of endometrioma on fertility. Thus, a
recent study compared the results of ovarian biopsies of a
healthy ovary and those of the contralateral ovary in 11
women with an endometrioma of size <4 cm; it found
signicantly decreased follicular density in the
endometrioma group (6.3/mm
3
vs. 25.1/mm
3
; P.0002;
LE4) (8). These data conrmed the results of earlier studies
on endometriomas measuring 56 cm compared with other
ovarian cysts: The endometriomas were associated with
decreased ovarian volume and reduced follicular density in
the adjacent cortex (LE3) (9, 10). Histologic analysis of the
cortex adjacent to the endometrioma and ndings of
extensive brosis might explain this result.
A recent prospective study compared ovarian reserve,
based on antim ullerian hormone (AMH) and an antral follicle
count (AFC), in patients with endometriomas >2 cm (without
previous surgery) matched with patients of the same age with
no ovarian cysts. Those with endometriomas had reduced
AMH levels (2.81 vs. 4.20; P.02) and AFC (9.73 vs. 14.7;
P<.01; LE3) (11).
The impact of endometriomas on spontaneous ovulation
was studied in a prospective cohort of 70 women with one or
more endometriomas >10 mm in one of the two ovaries; the
authors observed a signicantly lower ovulation rate in
ovaries with endometrioma compared with healthy ovaries
(P.002; LE3) (12). On the other hand, the presence of small
endometriomas (<4 cm) does not appear to inuence the re-
sults of ART (LE2) (1318). These results conrm those of the
earlier meta-analysis by Gupta et al., with a similar clinical
pregnancy rate in the endometrioma group compared with
the control group (odds ratio [OR] 1.07 [95%condence inter-
val (CI) 0.631.81]; LE1) (19).
A recent retrospective study investigating the effect of
one or more endometriomas (>4 cm) on the ovarian response
of 84 patients found that this mass did not affect the number
or size of the cysts or the number of follicles retrieved (LE4)
(20). These results seem to be consistent with those of Almog
et al., who compared the results of IVF in 19 patients with
bilateral endometriomas (LE4) (13). Although these results
might be explained by a lack of power and selection bias,
they also call into question the idea of a cutoff in the size of
endometriomas before ART.
A recent retrospective study of women without surgery
compared 39 women with bilateral endometriomas (2 cm on
average) and 78 matched control subjects with none. Women
with bilateral endometriomas had signicantly fewer follicles
>10 mm and >15 mm, compared with the control group (9.6
and 6.2 vs. 14.1 and 9.6, respectively; P<.001; LE4). However,
although the quantitative response to ovarian stimulation
appeared to be lower, quality was not impaired: The rates of
top-quality embryos, pregnancies, and live births per cycle
were similar in both groups (LE4) (21).
It thus appears that an isolated endometrioma can and
should be ignored, especially if it is asymptomatic. It is quite
difcult to determine accurately the responsibility between
endometriomas and endometriosis regarding infertility (22,
23). Only symptomatic endometriomas should be treated.
Moreover, it does not seem to be acceptable to propose a
cystectomy to a young woman of reproductive age to
prevent the future risk of malignant degeneration or torsion.
Dermoid Cysts
Dermoid cysts account for 70% of ovarian cysts in women
<30 years of age and are bilateral in 10%20% of cases
(LE1) (2431). Although they grow 1.71.8 mm per year,
their management remains controversial. Several series of
expectant management of dermoid cysts estimate the
prevalence of torsion at 3.5%11% (LE2) (27, 32). Most
malignant transformations occur when cyst size is >10 cm
and usually in women older than 50 years (3335).
Arecent retrospective Koreancase-control study foundno
signicant differences in mean AMH levels between women
with dermoid cysts (n 48) and a control group after adjust-
ment for age and body mass index (4.0 vs. 4.0; ns; LE4) (36).
The average size of dermoid cysts in that series was 6.3 cm.
Await-and-see attitude seems to be reasonable for asymptom-
atic women, especially for moderate-sized dermoid cysts (46
cm), where the risk of secondary interventions is low.
IMPACT OF SURGERY FOR OVARIAN CYSTS
ON FERTILITY
Endometrioma
Several series have studied the effect of surgical treatment for
endometriomas onfertility. The meta-analysis byRafet al. re-
ported seven prospective studies and randomized controlled
trials published from2009 to 2011 to investigate postoperative
AMH levels (Table 1) (49). In all, 152 excisions were performed
for endometriomas measuring at least 34 cm. The postopera-
tive AMH level was signicantly lower than the preoperative
level (1.13 [interquartile range 1.88 to 0.37]; P.003),
corresponding to a 30% decrease (LE1). A systematic review
of 11 series conrmed the decline in ovarian reserve assessed
postoperativelybyAMH(50). Those authors didnot pool the re-
sults owing to strong cohort heterogeneity, different study de-
signs, different measurement techniques, and different
numbers of measurements. Most studies, however, found a sig-
nicant decrease in AMH levels, which was greater in women
withbilateral endometriomas (LE1). This decrease inAMHlevel
occurs early, in the 1st week after surgery, and seems to persist
after 69 months (LE1) (50). Two prospective cohort studies
have found a progressive depletion of AMH over successive
measurements (LE3) (11, 47), thus contradicting the data
from an earlier study that found a partial restoration of
ovarian reserve 3 months after cyst excision (LE3) (37). The
AFC also seems to be affected by this surgical treatment: A
recent series found that AFC decreased >10% at 6 months of
cystectomy for endometrioma compared with the
preoperative count (LE3) (51). The impact of surgery on the
ovarian reserve is greater for endometriomas >4 cm. A
retrospective study found a signicant decrease in the AFC,
in the number of dominant follicles, and in the number of
oocytes in women with endometriomas >4 cm compared
VOL. 101 NO. 3 / MARCH 2014 609
Fertility and Sterility
with the contralateral healthy ovary (LE3) (52). Finally, a
comparative study of 18 patients with bilateral
endometriomas and 20 patients with single endometrioma,
found that the decline in ovarian reserve is correlated with
bilaterality (63% vs. 25%; P<.001; LE3) (43).
Nonendometriotic Cysts
A single-center retrospective study of 17 excisions of non-
endometriotic cysts that averaged 37 mm (one serous and
seven dermoid cysts) found that after excision, compared
with a healthy ovary, ovarian reserve decreased in volume
by 40%; the number of dominant follicles also decreased
(LE4) (53). The small prospective cohort study by Chang
et al. found a signicantly greater decrease in the AMH
rate after cystectomy for the seven nonendometriotic cysts
(one mucinous and six dermoid) compared with results after
removal of 13 endometriomas (69% vs. 34% of the preoper-
ative AMH value; LE4) (37).
One small series reported the results of ovarian stimula-
tion and IVF in the presence of dermoid cysts (54). Data from
six patients with dermoid cysts (with a mean size of 2.4 cm)
were analyzed. The authors reported no effects related to the
presence of a cyst or the parameters of stimulation or IVF
(number of oocytes retrieved, E
2
rate; LE4). No malignancy
or complication related to the puncture has been reported.
It is nevertheless important to identify dermoid cysts
during the initial assessment to avoid puncturing them
and thus to reduce the risk of complications (LE4) (55, 56).
HOW DOES TREATMENT AFFECT THE
RESULTS OF ART?
Endometrioma
Several studies have examined the effect of the presence of
an endometrioma at the time of stimulation or oocyte
retrieval. Ultrasound-guided aspiration of the cyst on the
day of the oocyte retrieval should be avoided because of
the high risk of infection of the endometrioma (LE3) (57).
A recently updated Cochrane Database meta-analysis
focused on the management of endometriomas before
ART (58). Four trials (31 patients) were selected for this
meta-analysis; none reported results about the live birth
rate. One trial compared the use of GnRH agonists versus
GnRH antagonists. The number of mature oocytes and the
ovarian response (studied by E
2
rate on the day of ovulation
induction) in the agonist group were higher than in the
antagonist group, but the groups did not differ in their clin-
ical pregnancy rates. Surgery (aspiration or cystectomy)
does not seemto improve pregnancy rates. Aspiration, how-
ever, is associated with a larger number of mature oocytes
and a greater biologic ovarian response than abstention,
whereas cystectomy is associated with a lower ovarian
reserve than abstention. The cystectomy and aspiration
groups had identical numbers of oocytes and E
2
rates (LE1).
A meta-analysis by Tsoumpou et al. compared the
results of ve studies (surgery for endometrioma vs. absten-
tion) and found no benet to surgery for clinical pregnan-
cies (LE1) (59).
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610 VOL. 101 NO. 3 / MARCH 2014
VIEWS AND REVIEWS
Nonendometriotic Cysts
The literature is devoid of data assessing the impact of treat-
ment of nonendometriotic cysts before ART.
SURGICAL TECHNIQUES OF CYSTECTOMY
(EXCISION)
In all cases where fertility preservation is a priority, surgical
management should rst focus on conservative treatment.
Of course, excision should always be preferred to ovariec-
tomy. Surgeons must take the time to wait for the pathologic
analysis of the lesions before performing extensive and irre-
versible surgical procedures. If frozen section is not available,
they must operate in two steps. Laparoscopy is considered to
be the criterion standard (LE2) (6062). Bipolar energy should
be preferred to monopolar, and coagulation should be as
parsimonious and as selective as possible. In particular,
coagulation of the cyst walls should be avoided (LE2) (63).
For dermoid cysts, laparoscopic cystectomy should always
be preferred. A study of 55 patients who underwent surgery for
dermoid cysts measuring 215 cmfound a residual presence of
ovarian parenchyma (>3 cm
3
) 612 months later, even when
no parenchyma was visible before surgery (LE3) (64). A recent
randomized trial compared two different techniques (mesial
incision vs. antimesial incision) for the risk of a dermoid cyst
rupture. The authors sought as a secondary objective to analyze
the impact on fertility of these two techniques and reported
that FSH levels decreased less at 3 months and 12 months
when the incision was mesial (LE2) (65).
Some authors have also studied the impact on ovarian
reserve of the hemostasis technique in surgery on endome-
triomas. Thus, two recent randomized trials found no differ-
ences in benets for fertility between bipolar coagulation
and hemostatic suture of the ovary (LE2) (66, 67).
ALTERNATIVE TO EXCISION
Surgical techniques other than cyst excision are available
only for endometriomas. Needle aspiration of a dermoid
cyst must not be considered, owing to the risk of chemical
peritonitis, and for this reason only excision is appropriate.
Similarly, no argument appears to support the utility of
ne-needle aspiration of a unilocular cyst; such cysts should
be treated by either surveillance or excision, depending on
their size.
Abstention is a possible approach for endometriomas,
according to the results of controlled trials (6870) and a
recent meta-analysis (LE1) (59). It does, however, have two
risks that must be avoided: borderline tumor or ovarian
carcinoma (0.8%) (71) and infection if the endometrioma is
punctured during oocyte retrieval (57, 72).
Role of Ablation
Ameta-analysis by the Cochrane Collaboration (73) identied
two randomized trials showing the effect of ablation and
coagulation (74, 75). The primary end points of these trials
were pain (dysmenorrhea, dyspareunia, and pelvic pain),
and response was better with excision. In hypofertile
women trying to conceive, excision was associated with a
higher rate of spontaneous pregnancy than ablation (OR
5.21 [95% CI 2.0413.29]). The rates of recurrence (OR 0.41
[0.180.93]) and of secondary surgery (OR 0.21 [95% CI
0.050.79]) were lower in the excision group (LE2). There
was, however, insufcient evidence to recommend excision
rather than ablation followed by coagulation in patients
treated with ovarian stimulation and uterine insemination
(OR 1.40 [95% CI 0.474.17]) (73). Another recent
randomized trial found better ART results after bipolar
coagulation than after excision for the management of
bilateral endometriomas: Although both treatments
signicantly impaired ovarian volume and AFC compared
with the preoperative assessment, the damage was
signicantly more severe in the excision group (76) (LE2).
In addition, the number of mature follicles and oocytes
retrieved was signicantly higher in the ablation group.
Ablation may therefore be an alternative to excision before
IVF for women with bilateral endometriomas. Indeed, in
case of bilateral endometriomas a risk of premature ovarian
failure (2.4%) has been demonstred by Busacca et al. after
surgical excision (LE3) (77).
Role of Aspiration and Sclerotherapy
An older retrospective study compared the results of 100
excisions with those of 31 aspirations in patients younger
than 40 years. The risk of recurrence was signicantly higher
in the aspiration group than in the laparoscopic excision
group (84% vs. 4%, respectively; P<.001; LE3) (78).
Hsieh et al. reported a role for sclerotherapy in the recur-
rence of endometriomas, specically for 108 women with
recurrence of endometriomas (>3 cm) (79). In the early
2000s, reports of sclerotherapy with ethanol from Japan
were particularly positive in cases of endometriomas, with
recurrence rates of 8%15% at 1 year, which was far lower
than those of a simple aspiration (80%) and similar to surgery
(LE3) (80, 81). A preliminary prospective nonrandomized
study evaluating the efcacy of ethanol sclerotherapy in 31
patients with recurrent endometriomas of 26 cm
(compared with 26 patients with repeated surgery) found
higher clinical and cumulative pregnancy rates in the
sclerotherapy group compared with the repeated-excision
group (48 vs. 19% [P.04] and 55% vs. 27% [P.03], respec-
tively; LE4) (82).
Role of Vaporization
Role of CO
2
laser vaporization. A recent randomized trial
compared the long-term results of excision and CO
2
laser
vaporization (83). The primary end point was the endome-
trioma recurrence rate. The 5-year cumulative recurrence
rate per patient in the vaporization group was 37%, compared
with 22% in the excision group (P.2). Pregnancy rates were
similar between the two groups at 1 year and 5 years (19%and
38%, respectively after excision vs. 21%and 44%after vapor-
ization; ns; LE2).
Role of plasma energy. A retrospective comparative study of
30 patients with endometriomas >30 mm evaluated the
effects of plasma energy versus excision on ovarian reserve.
VOL. 101 NO. 3 / MARCH 2014 611
Fertility and Sterility
Plasma energy technique showed a milder impairment of the
ovarian reserve as assessed by AFC and of ovarian volume
(LE4) (84).
Acohort of 55 patients treated for endometrioma ablation
with plasma energy and followed for at least 1 year found a
recurrence rate of 11% and a pregnancy rate of 67% at the
3-year follow-up among patients wishing to become preg-
nant (n 33; LE4) (85).
Despite limited data, plasma energy seems to have a
promising role in the management of ovarian endometriomas
in women wishing to conceive. Patients with bilateral endo-
metriomas, a history of ovarian surgery, or >35 years of
age, may benet to a greater extent from plasma ablation
than from excision.
CONCLUSION
Ovarian cysts in infertile patients create a complex situation,
and management is correlated with characteristics of the
cystsnature, size, number, unilaterality or bilateralityas
well as other indicators of fertility, including age, ovarian
reserve, associated pathologies, and sperm variables. For
many practitioners, the main concern about an ovarian cyst
is, understandably, to not miss a malignant tumor. The role
of imaging, including better ultrasound assessments due to
the International Tumor Ovarian Analysis group classication
(86), should help to improve characterization of ovarian cysts
and better assess the value of expectant management. Except
in cases of endometrioma, the literature contains relatively
little data that can actually guide the clinician's practice.
Different guidelines existAmerican (American Society for
Reproductive Medicine), European (European Society for
Human Reproduction and Embryology), British (Royal
College of Obstetricians and Gynaecologists), French
(College National des Gynecologues et Obstetriciens), and
Canadian (Society of Obstetricians and Gynaecologists of
Canada) but they do not generate a clear cutoff size
indicating a need for a treatment before ART (e.g., 3, 4, or 6
cm). The indications for alternative techniques for
management of endometriomas, such as sclerotherapy and
plasma vaporization, must be better dened, although they
appear to be promising with improved ovarian tissue sparing
and thus better sparing of follicular reserves. Not enough is
known about dermoid cysts to guide their management in
infertile women, but a wait-and-see attitude seems to be
reasonable for asymptomatic women.
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