Middle East Fertility Society Journal

Vol. 11, No. 1, 2006

Copyright Middle East Fertility Society

DEBATE

Is it of value to treat endometriosis prior to IVF?

Comment by: Efstratios M Kolibianakis, M.D.

Basil C Tarlatzis, M.D.
Thessaloniki, Greece

INTRODUCTION
Although endometriosis is a common finding in
infertile women (1), the mechanism by which it is
associated with infertility remains unclear. Not
unexpectedly, the optimal treatment for women
with endometriosis, who wish to become pregnant,
is debatable.
Women, who suffer from infertility and are
diagnosed with endometriosis, may undergo
surgical or medical treatment with the aim to
enhance their reproductive potential or proceed
immediately to IVF. In the first case, expectant
management is advocated for a variable period of
time. If conception does not occur, IVF is usually
the proposed method of treatment, although
ovarian stimulation with intrauterine insemination
might be an option in certain cases with mild or
minimal endometriosis. On the other hand, IVF
may be immediately selected as the preferred mode
of treatment, either due to other coexisting factors
(e.g. severe male infertility, tubal infertility, female
age etc) or because treatment of endometriosis is
considered as not beneficial, and in cases where it
involves destruction of ovarian tissue, as
potentially harmful.
It is not the purpose of the current review to
discuss which the best treatment strategy is for
infertile patients diagnosed with endometriosis
(medical or surgical treatment and follow-up or
immediately IVF treatment). A solid answer to the
above dilemma requires data form prospective

24

Debate

randomized trials in which infertile patients with

endometriosis
are
allocated
to
proceed
immediately to IVF treatment for a certain number
of cycles or undergo surgical or medical treatment
and expectant management for a certain period of
time. Although such trials currently do not exist,
indirect evidence, suggest that the fecundity is not
improved with medical vs. placebo treatment (2) in
patients with endometriosis. Moreover, it appears
that the use of laparoscopic surgery in the
treatment of minimal and mild endometriosis
improves success rates (3), while pregnancy rates
after laparoscopic treatment of endometriomas
vary from 23-67% in follow-up studies (4-6).
The question the current review focuses on is
whether medical or surgical treatment of
endometriosis is of value in patients for whom a
decision has been taken to proceed to IVF in order
to achieve pregnancy.
Is there a need to treat endometriosis in patients
undergoing IVF?
The meta-analysis by Barnhart et al (7) showed
that the chance of achieving pregnancy after IVF
was significantly lower for patients with
endometriosis (odds ratio, 0.56; 95% confidence
interval, 0.44-0.70), as compared to those with
tubal factor and it was accompanied by a decrease
in fertilization rates, implantation rates and in the
number of oocytes retrieved. Moreover, the
probability of pregnancy was reduced in women
with severe endometriosis as compared to those
with mild disease. Although the above metaanalysis did not consider whether patients analyzed
had been treated with medical or surgical treatment
prior to IVF, it is reasonable to assume that if the

Is it of value to treat endometriosis prior to IVF?

MEFSJ

Table 1. Comparison of pregnancy rates per cycle achieved in patients with endometriosis undergoing IVF after prolonged
downregulation with GnRH agonists or after long, short protocol or no downregulation

Prolonged agonist
downregulation protocol

No
downregulation

Long agonist
protocol

Short/ ultrashort
agonist protocol

pregnancy rate per cycle (number of cycles)

Retrospective studies
Dicker et al (1990) a
Nakamura et al (1992)
Chedid et al (1995)b
Prospective studies
Remorgida et al (1990)c
Dicker et al (1992)
Marcus and Edwards (1994)
Randomized controlled trials
Surrey et al (2002)

30% ( n=40)
67% (n=21)
45.7% (n=35)

0% ( n=48)

50.0% (n=20)
25% (n=48)
34.8% (n=23)

30.0% (n=20)
3.9% (n=51)

p<0.0001
p<0.05
ns

27% (n=11)
38.9%( n=108)
30.0% (n=20)
10.7(n=158)

80% (n=25)

53.85% (n=26)

ns
p<0.0001
p<0.001
p<0.05

the same patients were used after they had failed to achieved pregnancy with gonadotrophin stimulation only
IVF/GIFT
c
GIFT
Modified from Zikopoulos et al (2004).
b

probability of pregnancy after IVF is significantly

decreased, then treatment of endometriosis
immediately before the IVF cycle might be
associated with an improved outcome.
Medical treatment of endometriosis prior to
IVF
Medical treatment of endometriosis involves
use of several agents, including oral
contraceptives, or progestins. However, available
studies evaluating medical treatment prior to IVF
have so far focused on prolonged GnRH agonist
treatment or use of danazol or gestrinone.
Prolonged treatment with GnRH analogues
The assumption for using prolonged GnRH
analogue treatment, beyond the period of two-three
weeks used in the classic long protocol, is that, in this
way, initiation of ovarian stimulation is performed
after significant remission of endometriotic disease
has been achieved. This is mediated through the
interference of GnRH agonists with paracrine and
endocrine mechanisms, which are implicated in the
pathogenesis of endometriosis (8).
Several retrospective and prospective studies
have evaluated the prolonged use of GnRH agonist
downregulation in patients with endometriosis

Vol. 11, No. 1, 2006

Debate

(Table 1). The control group in these studies

received either no downregulation or was treated
according to the short or long agonist protocol.
Moreover, patients analyzed were diagnosed with
various stages of endometriosis, while it is not
clear if and what kind of treatment was applied
prior to inclusion in the study.
The majority of retrospective studies conclude
that the reproductive outcome in women with
endometriosis undergoing IVF is improved after
prolonged downregulation with GnRH agonist
before starting ovarian stimulation (Table I). This
is also supported by two prospective studies
performed and by one randomized controlled trial
(RCT)
(9),
which
compared
prolonged
downregulation to the long agonist protocol. The
quality of that RCT, however, is questionable since
the two groups of patients compared differed in the
severity of endometriosis present, while the
pregnancy rates achieved were unusually high.
It is evident from the above that there is a need
for well designed prospective RCTs that will
address the question whether prolonged
downregulation with GnRH agonists is associated
or not with an increased probability of pregnancy.
On the basis of the current low-quality evidence, it
appears that such an intervention is beneficial.
What needs to be accurately reported and taken

Is it of value to treat endometriosis prior to IVF?

25

into consideration in the design of future relevant

trials is whether the patients allocated to receive
prolonged downregulation have been treated
already with surgical or medical therapy and the
severity of endometriosis disease at the time of
diagnosis and treatment initiation.
It has to be noted though that prolonged
administration of GnRH agonist results in hypoestrogenemia which is associated with hot flushes,
sweating, headache, mood changes, atrophy of
secondary sexual tissues, and, most importantly
with decrease in bone mineralization (10). The
need for an add back therapy is considered
necessary in these cases (11).
A promising way to achieve prolonged
downregulation appears to be the use of GnRH
antagonists in weekly depot doses. Although
antagonists have not been used as a treatment of
endometriosis in patients scheduled to undergo
IVF, they have been successfully used in the
treatment of endometriosis associated pain. Their
immediate action in combination with the lack of
need for add back therapy (when used in weekly
depot doses) brings them in an advantageous
position as compared to GnRH agonists.
Sequential treatment maintains basic estrogen
production during treatment, while it does not
influence the regression of the disease.
Suppression of endometriosis prior to IVF
without the use of GnRH analogs
Suppression of endometriosis prior to initiation
of ovarian stimulation for IVF has also been
implemented with the use of danazol or gestrinone
(12). However, no difference was shown in
pregnancy rate after pretreatment for 6-9 months as
compared to untreated patients with endometriosis
(21% vs. 15%).
Should endometriomas be removed in patients
who are going to be treated by IVF?
During investigation of infertility, diagnosis of
endometriomas can be performed via laparoscopy
and at the same time endometriomas can be removed.
Endometriomas, however, can also be diagnosed by
ultrasound without the need for a laparoscopy (13).
Various methods have been employed for

26

Debate

removal of endometriomas (14), including total

resection and cauterization of the cyst wall. To
show reliably, however, that treatment of
endometriomas in patients scheduled for IVF has a
beneficial effect on reproductive outcome, a
prospective randomized trial in which patients with
endometriomas are allocated to undergo removal
of endometriomas or IVF needs to be performed.
Such data do not exist to date.
In the design of such a study, patients should be
stratified according to whether the endometriomas
present have already been treated and are not
anymore present, have recurred following
treatment or have never been treated. In addition,
stratification should occur according to cyst size or
localization to one or both ovaries.
Arguments
in
endometriomas

favor

of

removing

* Endometriomas may interfere with ovarian

stimulation (35)
* Endometriomas may impose difficulties during
oocyte retrieval.
* Endometriomas have been considered
responsible for producing substances that are toxic
to maturing oocytes affecting cleavage after
fertilization (15).
* Endometriomas may themselves be responsible
for compromising ovarian reserve by destroying
ovarian tissue through their expansion (16).
* Without laparoscopic evaluation, the diagnosis of
malignant transformation (approximately 1%)
might be delayed (17).
* Endometriomas may be associated with the
occurrence of pelvic abscess (18) or rupture and
acute abdomen (19).
Studies to support removal of endometriomas
prior to IVF
Available data are based on retrospective studies
comparing the reproductive outcome of patients with
endometriomas who undergo surgical treatment to
that of patients with no endometriosis (20-23) and
appear to support that removal of endometriomas
does not compromise IVF outcome.
Moreover, Yanushpolsky et al (24) suggested that
the presence of endometriomas at the time of

Is it of value to treat endometriosis prior to IVF?

MEFSJ

oocyte retrieval is associated with increased rates

of early pregnancy losses.
A retrospective study by Suganuma et al. (25)
compared treatment of endometriomas prior to IVF
either by laparotomy/laparoscopy or aspiration
with or without alcohol fixation to no treatment. A
higher fertilization rate was observed in the group
of patients treated with aspiration as compared to
those treated with surgery or those who did not
receive treatment.

compared to non-removal by Garcia-Velasco et al

(36) in a retrospective, matched case-control study.
It was suggested that removal of endometriomas
was associated with lower E2 and a higher
requirement of FSH as compared to non-removal,
and no differences in pregnancy rates (25.4% vs.
22.7%, respectively).

Arguments in
endometriomas

On the basis of retrospective studies, it appears

that the use of prolonged GnRH agonist
downregulation is beneficial in patients with
endometriosis. No benefit from medical
suppression of endometriosis by gestrinone or
danazol prior to ovarian stimulation for IVF has
been shown. A promising approach for medical
treatment of patients with endometriosis prior to
initiation of an IVF cycle appears to be the use of
GnRH antagonists. There is a need for prospective
randomized trials in which patients with
endometriomas undergo surgical treatment or not
to evaluate the usefulness of their removal prior to
ovarian stimulation. Currently, it is not clear
whether endometriomas should be removed or the
patient should proceed immediately to IVF,
although the latter may be the case, where
recurrence of endometriomas occurs after previous
excision (37).

favor

of

not

removing

* Endometriomas resection prior to IVF may

compromise or destroy adjacent normal ovarian
tissue by removal of part of the ovarian cortex (2627) or compromising ovarian artery blood flow
(28) leading to a reduced ovarian reserve. This is a
source of concern especially in cases that a repeat
surgery is considered.
* Removal of endometriomas although classified as
minimal invasive surgery it is a procedure which can
be accompanied by life threatening complications
(14). It is therefore imperative that it should be
performed, as a routine, only on the basis of sound
evidence, which is currently lacking.
* Although aspiration of endometriomas is less
prone to destroy ovarian tissue it has been
associated with an increased risk of infection
despite the use of prophylactic antibiotics (29).

CONCLUSIONS

REFERENCES

Studies to support that removal of endometriomas

is not necessary prior to IVF
1.

There is support from retrospective studies that

IVF in the presence of endometriomas is not
associated with a compromised outcome (30-33).
On the other hand, evidence exists to support that
surgery for ovarian endometriomas may damage
ovarian reserve, potentially resulting in poor
ovarian response to COH (34).
In a prospective study Pabuccu et al (35)
compared women with endometriomas resected,
aspirated at the time of oocyte retrieval or left
untreated and women with tubal factor infertility.
No difference in the probability of pregnancy after
IVF was observed between the groups compared.
Moreover, removal of endometriomas was

Vol. 11, No. 1, 2006

Debate

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Efstratios M Kolibianakis, M.D.

Basil C Tarlatzis, M.D.
Unit for Human Reproduction,
1st Department of Obstetrics and Gynaecology,
Aristotle University of Thessaloniki
E-mail: stratis.kolibianakis@otenet.gr

Comment by: Johnny Awwad, M.D.

Beirut, Lebanon

Endometriosis is an enigmatic and progressive

benign gynecological condition with protean
presentations
and
overlapping
clinical
manifestations. It may be found in up to 40-50% of
women presenting with infertility and 5-10% of
fertile women. Proposed classifications are
frequently non-reflective of the actual clinical
impact of the disease in women. Because of the

Vol. 11, No. 1, 2006

Debate

absence of proper standardization for severity and

progression and the availability of a wide array of
treatment options, meaningful interpretation of the
medical literature on this subject may prove to be
very difficult. The multifactorial nature of the
mechanisms by which the disease manifests itself
and affects clinical outcome has also rendered this
task even more complex.
A debated and still controversial subject in this
context is whether endometriosis should be treated
prior to Assisted Reproductive Technology (ART)
cycles.
The merits of the surgical treatment of
endometriosis on ART outcome
Unfortunately, randomized controlled trials
specifically aimed to investigate whether surgical
treatment prior to ART improves the final
reproductive outcome in endometriosis-associated
infertility are currently lacking. Alternatively,
investigators have attempted to establish benefits
of the surgical treatment by using various
retrospective study designs, all of which remain
short of being conclusive because of inherent
limitations intimately linked to the nature of such
investigative strategies.
Most studies have focused on the surgical
management
of
women
with
late-stage
endometriosis and ovarian involvement in relation
to the ART outcome. In a case-control study,
Garcia-Velasco et al. (1) compared the ART
performance of women who underwent
laparoscopic cystectomy for an endometrioma (3
cm in size) with those with an existing
endometrioma of similar size who never had
surgical treatment. They showed that laparoscopic
cystectomy prior to ART did not improve the
number of oocytes collected, number of embryos
obtained or pregnancy rates. Women who
underwent surgical excision required significantly
higher doses of gonadotropins and achieved
significantly lower peaks of estradiol on the day of
human
chorionic
gonadotropin
injection.
Proceeding directly to ART in women with an
asymptomatic (<3 cm) ovarian endometrioma
reduced both the time and cost to pregnancy.
Wong et al (2) also failed to demonstrate a
statistically
significant
improvement
in

Is it of value to treat endometriosis prior to IVF?

29