Keywords
► endometriosis
► ascites
► peritonitis
► systematic review
► treatment
Abstract
Endometriosis can have several different presentations, including overt ascites and
peritonitis; increased awareness can improve diagnostic accuracy and patient outcomes.
We aim to provide a systematic review and report a case of endometriosis with this unusual
clinical presentation. The PubMed/MEDLINE database was systematically reviewed until
October 2016. Women with histologically-proven endometriosis presenting with clinically
significant ascites and/or frozen abdomen and/or encapsulating peritonitis were included;
those with potentially confounding conditions were excluded. Our search yielded 37 articles
describing 42 women, all of reproductive age. Ascites was mostly hemorrhagic, recurrent
and not predicted by cancer antigen 125 (CA-125) levels. In turn, dysmenorrhea, dyspar-
eunia and infertility were not consistently reported. The treatment choices and outcomes
were different across the studies, and are described in detail. Endometriosis should be a
differential diagnosis of massive hemorrhagic ascites in women of reproductive age.
Palavras-chave
► endometriose
► ascite
► peritonite
► revisão sistemática
► tratamento
Resumo A endometriose pode ter várias apresentações, incluindo ascite e peritonite, que são
apresentações incomuns. O aumento da conscientização sobre essa doença pode melhorar
a precisão diagnóstica e os resultados das pacientes. Nosso objetivo é fornecer uma revisão
sistemática e relatar um caso de endometriose com esta apresentação clínica incomum. O
banco de dados PubMed/MEDLINE foi revisado sistematicamente até outubro de 2016.
Foram incluídas mulheres com endometriose demonstrada histologicamente, com presença
de ascite clinicamente significativa e/ou abdômen congelado e/ou peritonite encapsulante;
foram excluídas aquelas com comorbidades que pudessem provocar confusão. A pesquisa
selecionou 37 artigos que descrevem 42 mulheres, todas em idade reprodutiva. A ascite foi
principalmente hemorrágica, recorrente, e não indicada pelos níveis de antígeno associado
ao câncer 125 (AC -125). Por sua vez, a dismenorreia, a dispareunia e a infertilidade não foram
relatadas de forma consistente. As escolhas e os resultados do tratamento foram diferentes
entre os estudos, e são descritos em detalhes. A endometriose deveria ser um diagnóstico
diferencial de ascite hemorrágica maciça em mulheres em idade reprodutiva.
received
September 12, 2017
accepted
December 20, 2017
published online
March 19, 2018
DOI https://doi.org/
10.1055/s-0038-1626700.
ISSN 0100-7203.
Copyright © 2018 by Thieme Revinter
Publicações Ltda, Rio de Janeiro, Brazil
THIEME
Review Article 147
Introduction
Endometriosis is de fined as the presence of endometrial
tissue outside of the uterine cavity, which, like the eutopic
endometrium, responds to hormonal stimuli. 1 Although the
symptoms related to endometriosis may be associated with
the location of the implant, they are unrelated to the extent of
the disease, and a variety of clinical presentations have been
described, including the presence of a small amount of
peritoneal fluid.
2 It is very rare, however, for endometriosis
to present as overt ascites, and the presence of such a
condition should prompt the investigation of differential
diagnoses, such as malignancy.
3 The occurrence of encapsu-
lating peritonitis, described as the encapsulation of bowel
loops by a thick fibrinogenous case, is even rarer, with only
five cases previously described in the medical literature.
3–8
Women who present with ascites due to endometriosis
often undergo multiple diagnostic procedures, including
invasive ones, before the underlying cause for ascites is
found.9 This results in increased patient risks and health
care costs. 10 General and emergency physicians, as well as
gynecologists, should be aware of endometriosis as a poten-
tial cause of ascites and encapsulating peritonitis to prompt-
ly diagnose it.
With this in mind, this study aims to bring attention to the
case of a woman presenting with encapsulating peritonitis
and multiple episodes of massive ascites. We also provide a
systematic review of the literature regarding the association
between histologically-proven endometriosis and clinically-
significant ascites, frozen abdomen or encapsulating perito-
nitis, including detailed characteristics of their presenta-
tions, proposed treatments and outcomes.
Methods
For this systematic review, we used the protocol outlined by
the Preferred Reporting Items for Systematic Reviews and
Meta-analyses (PRISMA) Statement (
►Fig. 1 ). The electronic
PubMed database was searched until October 2016 using the
detailed strategy described in ►Table 1 . The case of a woman
with endometriosis, recurrent ascites and encapsulating
peritonitis observed at our clinic is also described. The
review has been approved by the Ethics in Research Com-
mittee under the protocol number 006.01.2017.
Eligibility Criteria
Original articles, clinical trials, case series and case reports of
women of any age with histologically-proven endometriosis,
presenting with clinically signi ficant ascites and/or frozen
abdomen and/or encapsulating peritonitis, published in
English, Portuguese, French or Spanish, were eligible for
this review.
Because other causes that may occur concurrently with
endometriosis can cause the clinical presentations de-
scribed, we excluded papers describing patients with: cancer
of the ovaries, appendix or peritoneum, or other intra-
abdominal cancers; tuberculosis; ovarian hyperstimulation
syndrome; ovarian induction or other known causes of
massive ascites; and ascites beginning in the immediate or
early post-operative period of exploratory laparotomy/lapa-
roscopy. Animal studies; articles published in languages
other than the aforementioned ones; and reviews of the
literature were also excluded.
Study Selection
The references retrieved were independently screened by two
investigators, KA and TM. Initially, the screening was made by
title and abstract; then, the full-text versions of the selected
papers were obtained, and each article was reviewed for final
inclusion. If a consensus could not be reached, another author
(LB) made the final decision regarding inclusion.
Data Extraction
A standardized table was used for data extraction on each
selected paper, and information regarding the first author,
the country of origin, the journal and year of publication, the
study type, patient/sample age, patient origin or ethnicity,
the clinical presentation, the proposed treatment, and the
outcome were included. The characteristics of the ascitic
fluid and data regarding the presence or absence of encap-
sulating peritonitis were also recorded. Data extraction was
performed independently by two investigators (KA and TM).
Case Description
A 28-year-old woman presented to the internal medicine
clinic at our institution with wasting syndrome, increased
abdominal girth, progressive shortness of breath, dark stools
and decreased appetite. She also complained of progressive
abdominal and thoracic pain during menses, as well as cyclic
dyspareunia that had started five years before. She denied
infertility or any other chronic medical conditions. Her
cancer antigen 125 (CA-125) values were 107.8 and 889.6
on two measurements performed when she was an internal
medicine inpatient.
Abdominal ultrasound and contrasted computed tomog-
raphy (CT) studies showed loculated, cystic -like ascites pro-
ducing a mass effect. A paracentesis procedure revealed a
thick, hemorrhagic fluid with low albumin, high cellularity
and large concentration of red blood cells (
►Fig. 2 ). The fluid
analysis was negative for bacterial growth or cancer cells.
During the diagnostic laparoscopy, multiple adhesions and
peritoneal lesions were noticed, and the patient ’sa b d o m e n
was described as “frozen,” due to the presence of encapsu-
lating peritonitis, which did not enable the separation of the
peritoneal layers and the confection of the pneumoperito-
neum. Eight liters of fluid were removed. Histopathology of a
peritoneal biopsy taken at this time described chronic peri-
tonitis and scarce hemosiderin deposits.
One month after the initial imaging exam, another con-
trasted abdominal CT suggested the presence of sclerosing
encapsulating peritonitis (
►Fig. 3 ). At this point, the patient
was referred to our gynecology clinic due to suspected
endometriosis. This diagnosis was further suggested by a
gynecological exam, ultrasound mapping and a magnetic
resonance imaging (MRI) scan, which showed evidence of
fibrosis in the anterior vaginal fornix, multiple peritoneal
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al.148
nodules, and apparently hemorrhagic bilateral ovarian cysts.
The chest CT and the colonoscopy at that time were normal.
A new laparoscopy was performed, and a biopsy con-
firmed the diagnosis of endometriosis. Due to peritoneal
adhesions, it was not possible to access the pelvic and
abdominal organs. This patient was treated with goserelin
acetate, with good clinical response. At the six-month follow-
up, she was asymptomatic and had regained a considerable
amount of weight.
Results
Study Characteristics
Our systematic review yielded 37 articles describing 42
patients with clinically signi ficant ascites, encapsulating
peritonitis, or frozen abdomen. One author had a series of
three cases, while another had a series of four cases; all of the
remaining articles reported only one case each.
11,12 The
publication dates ranged from 1978 to 2016.
Patient Characteristics and Clinical Presentation
The ages of the women who ful filled the eligibility criteria
ranged from 20 years to 47 years. 13,14
A total of 8 women in the included articles were
described as “black”;3 ,a s “African-American ”;a n d2 ,a s
“Afro-Caribbean. ”12,13,15–22 One patient described herself as
“African;” another patient, as “caucasian;” a third one, as
“Hispanic;” and another one, as “negro.”23–26 Seven studies
did not describe ethnicity, but reported that the patients
were Nigerian ( n ¼ 3), Malay ( n ¼ 2), Brazilian ( n ¼ 1) or
Japanese ( n ¼ 1).
3,6,8,27–30 Ethnicity or origin was not de-
scribed at all for the remaining 16 patients. 5,7,11,14,31 –42
Records identified through a database
search
(n = 234)
ScreeningIncluded Eligibility Identification
Additional records identified through
other sources
(n = 2)
Records after duplicates were removed
(n = 233)
Records screened
(n = 233)
Records excluded
(n = 163)
Full-text articles assessed for
eligibility
(n=70)
Full-text articles excluded, with
reasons (n = 33):
- Full-texts unavailable online (21)
- No histologically-proven
endometriosis (3)
- Ascites not clinically significant
(3)
- Post-operative ascites (2)
- Post-chemotherapy ascites (1)
- Post ovarian stimulation ascites
(1)
- Post-trauma ascites (1)
- Presence of abdominopelvic
abscess (1)
Studies included in the
qualitative synthesis
(n = 37)
Fig. 1 Flow diagram describing the steps in the study sel ection for inclusion in this systematic review.
Table 1 Detailed search strategy used in the advanced tool of
the PubMed/MEDLINE database
Search Keywords
#1 peritoneal fibrosis OR encapsulating
peritoneal sclerosis OR sclerosing
encapsulating peritonitis
OR abdominal cocoon OR frozen
abdomen OR ascites
#2 endometriosis OR endometrioma OR
endometriotic OR hemosiderophage
Final search #1 AND #2
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 149
The ascites was of acute onset in 8 women, and gradual in
24 patients ( ►Supplementary Material 1) . The type of onset
was not reported in six cases.
In most patients, the ascites was described as “hemor-
rhagic” and “recurrent,” but descriptions such as “yellow,”
“clear yellow, ”“ brownish green ” and “loculated” were also
observed.3,6,8,13,25,32,33 Ascites was present but not charac -
terized in five cases. 5,14,15,19,34
The volume of asciticfluid was not shown in some studies, but
there are reports of 4.2 L, 4.8 L, 5.0 L and 7 L.13,29,36,41There was
associated pleural effusion in eleven patients.3,12,18,19,21,23,32,33,40
Liver involvement by endometriosis was cited in four cases,
including one with cysts and another with non-specified focal
lesions.
3,34
Twenty-two articles reported CA-125 levels. Normal
levels were observed in six patients. The biomarker was
elevated (> 35 U/mL) in 14 patients, ranging from 49 U/mL
to > 5,000 U/mL. One case had normal CA-125 levels at
first, but they became elevated (455 U/mL) after ascites
recurrence.
12
The most common main clinical presentation was abdo-
minal distension, which was sometimes accompanied by
other symptoms such as abdominal pain, abdominal tender-
ness, abdominal mass, shortness of breath, signs of hypovole-
mia, weight loss, nausea or vomiting, asthenia, malaise,
cachexia or loss of appetite. In 25 of the 42 women described,
at least one symptom of the classic dysmenorrhea, dyspareunia
and infertility triad was reported. Of these, dysmenorrhea
was the most common, and it was reported in 20
women.
8,11–13,15,16,18,20,22–24,27,30–32,36,38–41 Infertility was
reported in 11 patients. 11,18,19,22–24,29–31,40,41 Dyspareunia
was reported in 4 patients. 15,22,24,36 All three symptoms
were present in two studies. 22,24 However, in 15 articles
(describing 17 patients), the presence or absence of dysmenor-
rhea was not mentioned at all.
5–7,12,14,19,21,25,26,28,29,33–35,37 A
total of 33 studies (with 38 patients) were regarding the
presence or absence of dyspareunia,3,5–8,11–14,16–21,25–35,37–42
and 25 studies (with 28 patients) were regarding the presence
or absence of infertility.3,5–8,11–17,21,25–28,32–39 Fifteen articles
did not mention if any of these three symptoms were present or
absent in the cases they reported.
5–7,12,14,21,25,26,28,33–35,37
Besides our patient, only five cases of encapsulating
peritonitis due to endometriosis have been described in
the medical literature.
3,5–8
Treatments Used and Outcomes
The treatment choices for the patients included in this
review involved hormonal therapies, surgery, anti-in flam-
matory drugs (steroidal or non-steroidal) or a combination of
Fig. 2 Thick, hemorrhagic ascitic fluid sample.
Fig. 3 Contrasted computed tomography (CT) showing massive ascites, centrally encased bowels, and thickened peritoneum.
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al.150
Table 2 Treatment choices and respective outcomes in each study. Outcomes written as described in each article
Treatment for ascites Outcome
Dun et al, 2016 29 Leuprolide þ oral norethindrone Ascites persisted
Laparoscopic evacuation of ascites and
excision of endometriosis
No recurrence (6-month follow-up)
Hasdemir et al, 2015 40 Leuprorelin acetate for 6 months Resolution of symptoms until 2 months
after cessation
Dienogest Resolution of symptoms (3-month follow-
up)
Hinduja et al, 2016 42 Leuprolide 3.75 mg monthly Recurrence after 6 months
TAH þ BSO Ascitic fluid leakage through vaginal suture
l i n e( 1 0d a y sa f t e rt h eo p e r a t i o n )
Short-acting GnRH agonist þ oral danazol
followed by GnRH only
No recurrence (1-year follow-up)
Setubal et al, 2015 24 Continuous OCP for 3 months Ascites persisted
GnRH agonist, then laparoscopic excision
of lesions followed by GnRH agonist
Minimal ascites
Underwent IVF protocol Minimal ascites
OCP Symptom-free
Appleby et al, 2014 28 GnRH antagonist No recurrence (6-month follow-up)
Asano et al, 2014 30 GnRH agonist Ascites recurred
Oral dienogest No recurrence (1-year follow-up)
Bignall et al, 2014
22 GnRH agonists Ascites recurred
GnRH agonists þ tibolone þ NSAIDs þ
pregabalin
Symptoms well-controlled
Cosma et al, 2014 41 Laparoscopic excision of lesions Modest recurrence (250 mL) after 42 days
Shabeerali et al, 2012 11 CASE 1: GnRH analogue No recurrence (6-month follow-up)
CASE 2: Subtotal abdominal
hysterectomy þ BSO
No recurrence (1-year follow-up)
CASE 3: GnRH analogues for 1 year; then,
TAH þ BSO
Partial response; then, relatively asympto-
matic at 1-year follow-up
Ferrero and Remorgida, 2011
36 Norethindrone acetate (25 mg daily) No recurrence (1-year follow-up)
Ignacio et al, 2010 18 GnRH analogue No recurrence (8-month follow-up)
Lin et al, 2010 37 Laparoscopic electrocauterization of
lesions
Condition stabilized
Suchetha et al, 2010 7 GnRH analogues for 1 year Good response
Park et al, 2009 39 Laparoscopic excision of endometrioma
þ GnRH agonist for 6 months þ tibolone
No recurrence (1-year follow-up)
Sait, 2008 38 Bilateral ovarian cystectomies þ GnRH
analogue for 6 months followed by OCP
No recurrence (2-year follow-up)
Santos et al, 2007 6 Laparoscopy þ laparotomy NR. Patient died after 5 months
Palayekar et al, 2007 20 TAH þ BSO No recurrence (1-year follow-up)
Fortier et al, 2005 23 Ovarian cystectomy þ GnRH analogue for
6m o n t h sþ laparoscopic excision of
lesions þ oral progesterone for 6 months
Two recurrences
Ceased treatment and started clomiphene
due to pregnancy desire
Ascites recurrence
GnRH for 2 months Ascites recurrence
GnRH for 6 months Ascites recurrence
Mohd Noor et al, 2004 8 Laparotomy þ excision of lesions No recurrence (4-week follow-up)
Zeppa et al, 2004 35 NR NR
(Continued )
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 151
them. Ascites recurrence or persistence was frequent. Three
articles did not report how the patients were managed
(►Table 2 ).3,14,35
The hormonal therapies used included long-acting go-
nadotropin-releasing hormone (GnRH) agonists (namely
goserelin and leuprolide), short-acting GnRH agonists,
GnRH antagonists, progestational hormones (speci fically
dienogest, medroxyprogesterone and norethindrone), estra-
diol, conjugated estrogens, synthetic combined hormones
(namely tibolone), steroids with antigonadotropic and anti-
estrogenic activity (danazol), and oral contraceptive pills
(OCPs).
Other conservative treatments used were isolated pred-
nisolone, which did not prevent ascites recurrence, and
Table 2 (Continued )
Treatment for ascites Outcome
Cheong and Lim, 2003 3 NR NR
Jeanes et al, 2002 34 Double hysterectomy þ left oophorect-
omy followed by estradiol for 6 months
followed by goserelin
No recurrence (3-year follow-up)
Moffatt and Mitchell, 2002 19 Leuprolide þ premarin Recurrence after 4 weeks
TAH þ BSO þ leuprolide No recurrence (9-month follow-up)
Bhojawala et al, 2000 17 TAH þ RSO No recurrence (6-week follow-up)
Samora-Mata and Feste, 1999 25 TAH þ RSO NR
Myneyyirci-Delale et al, 1998 12 Laparoscopic excision of lesions followed
by GnRH agonist for 6 months; then,
excision of new ovarian cyst þ danazol
daily for 6 months followed by norethin-
drone acetate
Recurrence after 1 year; then, no recur-
rence (3-year follow-up)
Laparotomy þ monthly depo provera
injections; then, TAH þ BSO
Recurrence after 3 years; then, no recur-
rence (6-month follow-up)
Appendectomy and left ovarian wedge
resection þ lupron
No recurrence
L y s i so fa d h e s i o n sþ LSO followed by
lupron followed by norethindrone acetate
NR
Frigerio et al, 1997
5 TAH þ BSO þ appendectomy þ omen-
tectomy
No recurrence (3-year follow-up)
Mejia et al, 1997 16 Laparotomy No recurrence (15-month follow-up)
Flanagan and Barnes, 1996 21 Laparotomy þ GnRH agonist for 6 months Recurrence (twice in 1 year)
Prednisolone 30 mg daily Recurrence
Leuprorelin for 5 months Recurrence
Myers et al, 1995
33 TAH þ BSO þ lysis of adhesions No recurrence (8-month follow-up)
Jose et al, 1994 32 LSO Recurrence after 1 year
Laparotomy þ danazol NR
Schlueter an McClennan, 1994
13 Leuprolide acetate monthly No recurrence (3-month follow-up)
Williams and Wagaman, 1991 15 Medroxyprogesterone acetate Recurrence after 1 month
Depot lupron for 3 months Some ascites
TAH þ BSO Recurrence after 3 months
Tenckhoff catheter placed for 2 weeks No recurrence (9-month follow-up)
Chichareon and Wattanakitkrailert,
1988
31
TAH þ BSO No recurrence (6-month follow-up)
Olubuyide et al, 1988 27 Oral norethisterone No recurrence (1-year follow-up)
Naraynsingh et al, 1985 26 Depo provera for 6 months No recurrence (4-year follow-up)
Cantor et al, 1979 14 NR NR
Abbreviations: BSO, bilateral salpingo-oophorectomy; GnRH, gonadotrop in-releasing hormone; IVF, in vitro fertilization; LSO, left salpingo-
oophorectomy; NR, not reported; NSAIDs, non-steroidal anti-in flammatory drugs; OCP, oral contraceptive pills; RSO, right salpingo-oophorectomy;
TAH, total abdominal hysterectomy.
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al.152
nonsteroidal anti-in flammatory drugs (NSAIDs) in combina-
tion with pregabalin and hormonal therapies, which were
effective in controlling the symptoms.
The surgical procedures involved drainage of the ascites,
excision or electrocauterization of the endometriotic lesions
through laparotomy or laparoscopy, lysis of adhesions, abdom-
inal hysterectomy, uni- or bilateral salpingo-oophorectomy,
ovarian cystectomy, omentectomy, appendectomy, placement
of Tenckhoff catheter and/or ovarian wedge resection.
After the initial treatment, due to the desire to achieve
pregnancy, one woman underwent in vitro fertilization (IVF),
with minimal ascites afterwards.
24 Another patient started
clomiphene, with ascites recurrence. 23
A summary of the treatments used for ascites and its
respective outcomes, including the time until recurrence, is
shown in ►Table 2 .
Discussion
All patients shown in this review were of childbearing age,
likely due to hormonal levels and occurrence of menses. This
is, indeed, the most common age range for the presentation
of endometriosis in general, which can also rarely occur in
older women.
43 Endometriosis most commonly affected
women of African descent, but it was present in patients
of multiple other ethnicities, implying that this diagnosis
should not be restricted to patient origin, and must be
suspected if the clinical presentation is suitable.
Fluid accumulation was most commonly progressive, but
acute onset of symptoms has also been described. The
reasons for such a presentation remain unclear, but can be
related to the rapid accumulation of fluid and to the sponta-
neous rupture of a cyst.
37
Endometriosis-associated ascites is rare, and encapsulat-
ing peritonitis is even less common. Since we excluded
women with potentially confounding conditions, it appears
that endometriosis itself is the cause of such clinical pre-
sentations. It has been hypothesized that the peritoneal
irritation caused by endometriosis results in extensive fibro-
sis and in flammation, further optimizing the microenviron-
ment for more secondary implants, which in turn exacerbate
inflammation. In fact, this theory could also explain the high
rate of recurrence of ascites due to endometriosis (
►Table 2 ),
ultimately resulting in encapsulating peritonitis, which is
described in our case and in four other ones.
Abdominal distension related to ascites was the most
common clinical sign, but non-speci fic signs and symptoms
such as malaise and weight loss were also described
(►Supplementary Material 1 ). Additionally, most women
had symptoms suggestive of endometriosis, but these were
not always reported, bringing attention to the high level of
suspicion needed to diagnose this condition. Not all women
present with classic symptoms; however, in order for diag-
nostic accuracy to be improved, physicians in general (in-
cluding emergency room physicians) need to ask about them
specifically during history-taking.
Moreover, in some cases, ascitic volume was large and
related to pleural effusion, resembling Meigs syndrome.
Great volumes can be caused by the rapid production of
fluid, in association with the obstruction of subdiaphrag-
matic lymph vessels. In turn, pleural fluid may be due to the
transdiaphragmatic flow of ascites through the lymphatic
channels, as has been proposed by Meigs et al,
44 or due to
local reactive in flammation.38
The fluid was generally hemorrhagic, but could have
different aspects, such as clear yellow or green-brownish
color. On this matter, Bernstein proposed a mechanism by
which chocolate cysts would rupture into the peritoneal
cavity, leading to irritation and ascites formation; corre-
spondingly, other explanations relate to excessive ovarian
transudation, super ficial endometriosis, open endometriosis
lesions or angiogenesis.
45–47
Part of the included studies also measured and reported
serum CA-125 levels. This biomarker is known to not be
accurate for the diagnosis of endometriosis in general;
likewise, it was not reliable in the diagnosis of endometriosis
presenting with ascites. Although no statistical comparisons
were made, it is clear that the values were not intimately
correlated to the characteristics of ascites. Furthermore,
endometriosis caused CA-125 levels > 5,000 U/mL in one
case, which commonly indicates malignancy; this further
contributes to the need of including endometriosis in the list
of differentials of suspected malignancies due to massive
ascites.
Several treatment choices were observed in the included
articles; the options were similar to the therapies available
for endometriosis in general. For the speci fic treatment of
women presenting with ascites, no speci fic protocol exists,
and empirical data does not evidently favor one therapy over
another (
►Table 2 ).
Among the strengths of our review are the fact that only
articles with histologically proven endometriosis were se-
lected; the exclusion of patients with conditions that com-
monly cause ascites; and the systematic approach. It is
limited, however, in that articles in only four languages
were included, and in the fact that some older articles
initially screened could not be included because they were
not available online, even for purchase. Further research is
needed to better de fine optimal diagnostic and therapeutic
approaches in women with unusual presentations of
endometriosis.
Conclusion
Clinically signi ficant ascites, frozen abdomen and/or encap-
sulating peritonitis related to endometriosis are rare con-
ditions. It can present with abdominal distension, symptoms
classically related to endometriosis, and other non-speci fic
symptoms. The clinical presentations were heterogeneous.
Endometriosis should be a differential diagnosis of massive
hemorrhagic ascites in women of reproductive age, but the
exclusion of other potential causes, especially malignancy, is
needed for the diagnosis of this condition. The treatment
options include hormonal therapy, anti-in flammatory drugs
and/or surgery. There are no speci fic protocols for the
treatment of this condition.
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 153
Contributors
Magalhaes TF, Augusto KL, Mota LP, Costa AR, Puster RA,
and Bezerra LRPS contributed with the project and inter-
pretation of data, writing of the article, critical review of
the intellectual content and final approval of the version
to be published.
Conflicts of Interest
The authors have no con flicts of interest to declare.
References
1 Chen P, Wang DB, Liang YM. Evaluation of estrogen in endome-
triosis patients: Regulation of GATA-3 in endometrial cells and
effects on Th2 cytokines. J Obstet Gynaecol Res 2016;42(06):
669–677. Doi: 10.1111/jog.12957
2 Vinci G, Arkwright S, Audebourg A, et al. Correlation between the
clinical parameters and tissue phenotype in patients affected by
deep-infiltrating endometriosis. Reprod Sci 2016;23(09):1258-
–1268. Doi: 10.1177/1933719116638188
3 Cheong EC, Lim DT. Massive ascites –an uncommon presentation
of endometriosis. Singapore Med J 2003;44(02):98 –100
4 Obaid O, Alhalabi D, Ghonami M. Intestinal obstruction in a
patient with sclerosing encapsulating peritonitis. Case Rep Surg
2017;2017:8316147
5 Frigerio L, Taccagni GL, Mariani A, Mangili G, Ferrari A. Idiopathic
sclerosing peritonitis associated with florid mesothelial hyper-
plasia, ovarian fibromatosis, and endometriosis: a new disorder of
abdominal mass. Am J Obstet Gynecol 1997;176(03):721 –722.
Doi: 10.1016/S0002-9378(97)70581-7
6 Santos VM, Barbosa ER Jr, Lima SH, Porto AS. Abdominal cocoon
associated with endometriosis. Singapore Med J 2007;48(09):
e240–e242
7 Suchetha S, Rema P, Mathew AP, Sebastian P. Endometriosis with
massive hemorrhagic ascites. Indian J Cancer 2010;47(02):
224–225. Doi: 10.4103/0019-509X.63004
8 Mohd Noor NH, Zaki NM, Kaur G, Naik VR, Zakaria AZ. Abdominal
cocoon in association with adenomyosis and leiomyomata of the
uterus and endometriotic cyst : unusual presentation. Malays J
Med Sci 2004;11(01):81 –85
9 Gupta D, Hull ML, Fraser I, et al. Endometrial biomarkers for the
non-invasive diagnosis of endometriosis. Cochrane Database
Syst Rev 2016;4:CD012165. Doi: 10.1002/14651858.CD012165
10 Liu E, Nisenblat V, Farquhar C, et al. Urinary biomarkers for the
non-invasive diagnosis of endometriosis. Cochrane Database Syst
Rev 2015;(12):CD012019. Doi: 10.1002/14651858.CD012019
11 Shabeerali TU, Rajan R, Kuruvilla AP, et al. Hemorrhagic ascites:
are we missing endometriosis? Indian J Gastroenterol 2012;31
(04):195–197. Doi: 10.1007/s12664-012-0221-1
12 Muneyyirci-Delale O, Neil G, Serur E, Gordon D, Maiman M, Sedlis
A. Endometriosis with massive ascites. Gynecol Oncol 1998;69
(01):42–46. Doi: 10.1006/gyno.1998.4953
13 Schlueter FJ, McClennan BL. Massive ascites and pleural effusions
associated with endometriosis. Abdom Imaging 1994;19(05):
475–476
14 Cantor JO, Fenoglio CM, Richart RM. A case of extensive abdominal
endometriosis. Am J Obstet Gynecol 1979;134(07):846 –847. Doi:
10.1016/0002-9378(79)90958-X
15 Williams RS, Wagaman R. Endometriosis associated with massive
ascites and absence of pelvic peritoneum. Am J Obstet Gynecol
1991;164(1 Pt 1):45 –46. Doi: 10.1016/0002-9378(91)90621-W
16 Mejia EM, Alvarez OA, Lee M. Endometriosis with massive bloody
ascites. J Am Board Fam Pract 1997;10(01):59 –61
17 Bhojawala J, Heller DS, Cracchiolo B, Sama J. Endometriosis
presenting as bloody pleural effusion and ascites-report of a
case and review of the literature. Arch Gynecol Obstet 2000;
264(01):39–41. Doi: 10.1007/PL00007484
18 Ignacio MM, Joseph N, Hélder F, Mamourou K, Arnaud W. Massive
ascites, pleural effusion, and diaphragmatic implants in a patient
with endometriosis. Eur J Obstet Gynecol Reprod Biol 2010;149
(01):117–118. Doi: 10.1016/j.ejogrb.2009.10.017
19 Moffatt SD, Mitchell JD. Massive pleural endometriosis. Eur J
Cardiothorac Surg 2002;22(02):321 –323. Doi: 10.1016/S1010-
7940(02)00277-4
20 Palayekar M, Jenci J, Carlson JA Jr. Recurrent hemorrhagic ascites:
a rare presentation of endometriosis. Obstet Gynecol 2007;110(2
Pt 2):521 –522
21 Flanagan KL, Barnes NC. Pleural fluid accumulation due to intra-
abdominal endometriosis: a case report and review of the litera-
ture. Thorax 1996;51(10):1062–1063. Doi: 10.1136/thx.51.10.1062
22 Bignall J, Arambage K, Vimplis S. Endometriosis: a rare and
interesting cause of recurrent haemorrhagic ascites. BMJ Case
Rep 2014;2014:bcr2013010052. Doi: 10.1136/bcr-2013-010052
23 F o r t i e rD ,D e d e c k e rF ,G a b r i e l eM ,G r a e s s l i nO ,B a r a uG .[ E n d o m e t r i o s i s
with ascites and pleural effusion: a case report]. Gynecol Obstet Fertil
2005;33(7-8):508–510. Doi: 10.1016/j.gyobfe.2005.05.014
24 Setubal A, Sidiropoulou Z, Soares S, Barbosa C. Endometriosis and
ascites: a strategy to achieve pregnancy. J Minim Invasive Gynecol
2015;22(06):1104–1108. Doi: 10.1016/j.jmig.2015.05.013
25 Samora-Mata J, Feste JR. Endometriosis ascites: a case report. JSLS
1999;3(03):229–231
26 Naraynsingh V, Raju GC, Ratan P, Wong J. Massive ascites due to
omental endometriosis. Postgrad Med J 1985;61(716):539 –540.
Doi: 10.1136/pgmj.61.716.53
27 Olubuyide IO, Adebajo AO, Adeleye JA, Solanke TF. Massive ascites
associated with endometriosis in a Nigerian African. Int J Gynae-
col Obstet 1988;27(03):439 –441. Doi: 10.1016/0020-7292(88)
90127-0
28 Appleby R, Saroya H, Postgate A, Meer Z. A young woman with
abdominal distension. BMJ Case Rep 2014;2014:bcr2014203726.
Doi: 10.1136/bcr-2014-203726
29 Dun EC, Wong S, Lakhi NA, Nehzat CH. Recurrent massive ascites
due to mossy endometriosis. Fertil Steril 2016;106(06):e14. Doi:
10.1016/j.fertnstert.2016.07.1119
30 Asano R, Nakazawa T, Hirahara F, Sakakibara H. Dienogest was
effective in treating hemorrhagic ascites caused by endometrio-
sis: a case report. J Minim Invasive Gynecol 2014;21(06):1110-
–1112. Doi: 10.1016/j.jmig.2014.04.014
31 Chichareon SB, Wattan akitkrailert S. Endometriosis with asci tes.
Acta Obstet Gynecol Scand 1988;67(02):187 –188. Doi: 10.3109/
00016348809004198
32 Jose R, George SS, Seshadri L. Massive ascites associated with
endometriosis. Int J Gynaecol Obstet 1994;44(03):287 –288. Doi:
10.1016/0020-7292(94)90185-6
33 Myers TJ, Arena B, Granai CO. Pelvic endometriosis mimicking
advanced ovarian cancer: presentation with pleural effusion,
ascites, and elevated serum CA 125 level. Am J Obstet Gynecol
1995;173(3 Pt 1):966 –967
34 Jeanes AC, Murray D, Davidson B, Hamilton M, Watkinson AF. Case
report: hepatic and retro-peritoneal endometriosis presenting as
obstructive jaundice with ascites: a case report and review of the
literature. Clin Radiol 2002;57(03):226 –229. Doi: 10.1053/
crad.2001.0667
35 Zeppa P, Vetrani A, Cozzolino I, Palombini L. Endometrial glands in
ascites secondary to endometriosis. Diagn Cytopathol 2004;30
(02):131–132. Doi: 10.1002/dc.10390
36 Ferrero S, Remorgida V. Endometriosis presenting with hemor-
rhagic ascites. Arch Gynecol Obstet 2011;283(06):1429 –1430.
Doi: 10.1007/s00404-010-1796-3
37 Lin JN, Lin HL, Huang CK, et al. Endometriosis presenting as bloody
ascites and shock. J Emerg Med 2010;38(01):30–32. Doi: 10.1016/
j.jemermed.2008.03.031
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al.154
38 Sait KH. Massive ascites as a presentation in a young woman with
endometriosis: a case report. Fertil Steril 2008;90(05):2015.e17-
–2015.e19
39 Park BJ, Kim TE, Kim YW. Massive peritoneal fluid and markedly
elevated serum CA125 and CA19-9 levels associated with an
ovarian endometrioma. J Obstet Gynaecol Res 2009;35(05):
935–939. Doi: 10.1111/j.1447-0756.2009.01122.x
40 Hasdemir PS, Ikiz N, Ozcakir HT, Kara E, Guvenal T. Endometriosis
associated with relapsing ascites and pleural effusions. J Obstet
Gynaecol 2015;35(04):419. Doi: 10.3109/01443615.2014.948823
41 Cosma S, Ceccaroni M, Benedetto C. A pseudoneoplastic finding of
deep endometriosis: laparoscopic triple segmental bowel resec -
tion. Wideochir Inne Tech Malo Inwazyjne 2014;9(03):463 –467.
Doi: 10.5114/wiitm.2014.41617
42 Hinduja I, Kapadia K, Udwadia F, Bhilawadikar R, Adhe A, Zaveri K.
Unusual presentation of endometriosis with haemorrhagic
ascites - A case report. J Obstet Gynaecol 2016;36(01):133 –134.
Doi: 10.3109/01443615.2015.1030605
43 Streuli I, Gaitzsch H, Wenger JM, Petignat P. Endometriosis after
menopause: physiopathology and management of an uncommon
condition. Climacteric 2017;20(02):138 –143. Doi: 10.1080/
13697137.2017.1284781
44 Meigs JV, Armstrong SH, Hamilton HH. A further contribution to
the syndrome of fibroma of the ovary with fluid in the abdomen
and chest, Meigs’ syndrome. Am J Obstet Gynecol 1943;46:19 –37.
Doi: 10.1016/S0002-9378(16)40440-0
45 Bernstein JS, Perlow V, Brenner JJ. Massive ascites due to endo-
metriosis. Am J Dig Dis 1961;6:1 –6. Doi: 10.1007/BF02239240
46 Sherer DM, Eliakim R, Abula fia O. The role of angiogenesis in the
accumulation of peritoneal fluid in benign conditions and the
development of malignant ascites in the female. Gynecol Obstet
Invest 2000;50(04):217 –224. Doi: 10.1159/00001032
47 Ussia A, Betsas G, Corona R, De Cicco C, Koninckx PR. Patho-
physiology of cyclic hemorrhagic ascites and endometriosis.
J Minim Invasive Gynecol 2008;15(06):677 –681. Doi: 10.1016/j.
jmig.2008.08.012
Rev Bras Ginecol Obstet Vol. 40 No. 3/2018
Ascites and Encapsulating Peritonitis in Endometriosis Magalhães et al. 155
Text is read by the "Ask this paper" AI Q&A widget below.
Extraction quality varies by source — PMC NXML preserves structure
cleanly, OA-HTML may include some navigation residue, and OA-PDF can
have broken hyphenation. The publisher copy
(via DOI)
is the canonical version.