Australian and New Zealand Journal of Obstetrics and Gynaecology 2014; 54: 162165

DOI: 10.1111/ajo.12189

Original Article

Pelvic inammatory disease in women with endometriosis is more

severe than in those without
Shai E. ELIZUR,1 Oshrit LEBOVITZ,1 Adi Y. WEINTRAUB,1,2 Vered H. EISENBERG,1
Daniel S. SEIDMAN,1 Mordechai GOLDENBERG1 and David SORIANO1
1
Department of Obstetrics and Gynecology, Sheba Medical Center, Tel Hashomer, Ramat Gan, Afliated to Sackler Faculty of Medicine,
Tel-Aviv University, Tel Aviv, and 2Faculty of Health Sciences, Department of Obstetrics and Gynecology, Soroka University Medical
Center, Ben-Gurion University of the Negev, Beer-Sheva, Israel

Aims: To determine the incidence and severity of acute pelvic inammatory disease (PID) or tubo-ovarian abscess
(TOA) in hospitalised women with and without a history of endometriosis.
Methods: Retrospective analysis of hospital records retrieved for all women hospitalised with PID or TOA between
January 2008 and December 2011 in a tertiary referral centre. Women were compared with regard to a history of
endometriosis for demographic, clinical and fertility data.
Results: 26 (15%) of the 174 women hospitalised due to PID or TOA were excluded because of age older than 45 years,
leaving 148 for analysis. The mean age was 35.7  9.3 years and mean duration of hospitalisation was 5.9  3.7 days.
The women were divided into two groups: Group 1 with endometriosis (n = 21) and Group 2 without endometriosis
(n = 127). Women in Group 1 as compared with Group 2 were signicantly more likely to have undergone a fertility
procedure prior to being admitted to the hospital with PID (9/27 (45%) vs 22/121 (17%), P < 0.001); particularly in vitro
fertilisation (IVF) (7/ 27 (33%) vs 12/121 (9%), P < 0.006); Women in Group 1 more frequently experienced a severe
and complicated course involving longer duration of hospitalisation (8.8  4.7 vs 4.4  2.3 days, P < 0.0001) and
antibiotic treatment failure (10/27 (48%) vs 8/121 (6%), P < 0.0001).
Conclusions: Pelvic inammatory disease in women with endometriosis is more severe and refractory to antibiotic
treatment, often requiring surgical intervention. It is likely that endometriosis is a risk factor for the development of severe
PID, particularly after IVF treatment.
Key words: endometriosis, in vitro fertilisation, laparoscopy, pelvic inammatory disease, tubo-ovarian abscess.

Introduction
Acute pelvic inammatory disease (PID) is an infection of
the upper genital tract that primarily affects young,
sexually active women. Risk factors for PID include age
younger than 25 years; young age at rst sexual encounter
(<15 years); use of nonbarrier contraception; new,
multiple or symptomatic sex partners; a history of PID or
sexually transmitted disease; or recent intrauterine
contraceptive device insertion.1,2
Some reports,311 but not all,12 suggest that women
with endometriosis are at an increased risk of developing
PID. Furthermore, it has been suggested that pelvic
infections in women with endometriosis tend to be more

Correspondence: Dr Vered H. Eisenberg, Department of

Obstetrics and Gynecology, Sheba Medical Center, Tel
Hashomer 52621, Israel. Email: veredeis@bezeqint.net
Received 29 September 2013; accepted 9 January 2014.

162

severe and prolonged compared with those without

endometriosis. The aim of this study was to determine the
incidence and severity of pelvic inammatory disease
(PID) or tubo-ovarian abscess (TOA) in hospitalised
women with and without a history of endometriosis.

Materials and Methods

We performed a retrospective survey of medical records of
all women who were hospitalised at our tertiary referral
centre with the diagnosis of pelvic inammatory disease
(PID) or tubo-ovarian abscess (TOA) between January
2008 and December 2011. The study received the
approval of our local institutional ethical review board.
The clinical variables which were retrieved were as
follows: age, gravidity, parity, medical background, previous
infertility treatment or any medical procedure up to four
weeks prior to admission, duration of hospitalisation, and
type of treatments or interventions during hospitalisation.
As our primary aim was to determine the incidence of
endometriosis among reproductive age women hospitalised

2014 The Royal Australian and New Zealand College of Obstetricians and Gynaecologists
The Australian and
New Zealand Journal
of Obstetrics and
Gynaecology

with PID or TOA, we excluded from the analysis all women

older than 45 years. According to the clinical protocol at
our institution, all women received intravenous antibiotic
treatment upon admission. Treatment failure was
determined when there was no clinical improvement after
48 h of antibiotic treatment, based on the presence of
continuing fever, leucocytosis, intractable pain, persistent
mass on ultrasound (US) or signs of sepsis or septicaemia.
In all of these situations, an invasive procedure was
warranted.
Endometriosis staging was determined based on the
Revised American Society for Reproductive Medicine
classication of endometriosis, 1996.9 Statistical analysis
was performed using Stat-Direct software (StatsDirect Ltd.,
Altrincham, Chesire, UK). Students T-test, Mann
Whitney and Fisher exact tests were used for data analysis
as appropriate. A P value <0.05 was considered signicant.

Results
Between January 2008 and December 2011, 174 women
were hospitalised due to PID or TOA in the Chaim Sheba
medical center, a large tertiary referral centre in Israel.
Twenty-six women (15%) were older than 45 years and
were thus excluded from further analysis (Fig. 1). The
mean age was 35.7  9.3 years (mean  SD), and mean

duration of hospitalisation was 5.9  3.7 days. Forty-eight

women (32.5%) had undergone a medical procedure up to
four weeks prior to their admission. Twenty-three women
(16%) carried an IUD at the time of admission. Twentyone (14%) of the women had a medical history of
endometriosis. The study population was divided into two
groups: Group 1 with endometriosis (n = 21) and Group
2 (n = 127) without endometriosis. Women with
endometriosis were evaluated separately to test for the
signicance of endometriosis in the severity of PID. All of
the women with endometriosis had severe endometriosis
stage III-IV.9 Of these, 16 (76%) had previously been
operated for the treatment of severe and symptomatic
endometriosis and staging was known from the previous
procedure. Table 1 shows a comparison between the
groups with regard to signicant demographic and clinical
variables.
Women with endometriosis had signicantly lower
gravidity and parity compared to women without
endometriosis, and had more often undergone fertility
treatments (in particular, IVF treatments). The PID or
TOA in women with endometriosis was more often severe
and involved a more complicated pelvic infection with a
signicantly longer duration of hospitalisation and
increased risk of antibiotic treatment failure as compared
with women without endometriosis. Nearly half of the
hospitalised women with endometriosis (48%) failed initial
intravenous antibiotic treatment and required further
invasive procedures or surgical interventions. In contrast,
only 6% of hospitalised women without endometriosis

S. E. Elizur et al.

laparoscopy and 4 CT-guided abscess aspiration. All

women who were operated underwent fertility sparing
procedures.

Discussion
Our study found that women with endometriosis had
more severe pelvic infections requiring prolonged
hospitalisation and more frequently necessitating surgical
intervention. In women with endometriosis, PID and TOA
were more likely to develop following infertility
interventions, particularly IVF treatment. Grammatikakis
et al.4 found that the prevalence of PID in women with
endometriosis is higher than the prevalence in the general
population, but their study only looked at women who
were operated due to endometriotic ovarian cysts. In our
study, we included all women hospitalised with PID or
TOA regardless of the cause. The prevalence of
endometriosis in our study population (14%) is higher
than the reported prevalence of pelvic endometriosis (6
10%).13 A possible explanation for this is that the study
population consisted of hospitalised women who probably
represent patients with more severe endometriosis than the
general population.
There are several possible explanations for the role of
endometriosis in the development of pelvic infection.
Ovarian endometriomas have been shown to be associated
with TOA.3,4 This might be due to the bloody content of
the endometrioma that serves as a culture medium for
bacteria and facilitates the spread of infection. In addition,
as endometriosis is associated with infertility,14,15 many
women with endometriosis undergo various fertility
procedures, including IVF treatments. These procedures
increase the risk of developing pelvic infection. Indeed, we
have shown that 45% of hospitalised women with
endometriosis underwent some fertility procedure,
especially IVF, up to four weeks prior to their admission.
This emphasises the role of fertility procedures and
treatments as a risk factor for PID in women with
endometriosis.
Benaglia et al.12 reported an extremely low incidence of
TOA following IVF treatment and oocyte retrieval in
patient with US suspected endometrioma. In his study,
most of the patients had unilateral small sized (<3 cm)
endometriomas. None of the women underwent
laparoscopies, so the severity of their disease was
unknown.
To minimise the risk of endometrioma infection during
oocyte aspiration, it is probably advisable to avoid
puncturing the endometrioma. Disinfecting the vagina
with povidone-iodine followed by sterile isotonic saline
solution and prescribing antibiotics through out the
procedure might be considered as well.12
Secondly, severe pelvic adhesions and the obliteration of
the cul-de-sac may cause technical difculties during
oocyte retrieval in women with severe endometriosis.
There is also a risk of bowel punctue during follicle

164

aspiration from a xed ovary. Surgical removal of

endometriosis implants and extensive adhesiolysis prior to
IVF might theoretically diminish this problem. However,
surgical morbidity and the high postoperative recurrence
rate of endometriosis16 should be considered. In our
study, 76% of the women with endometriosis had
previously undergone at least one surgical procedure due
to endometriosis and some of them had undergone several
operations. Therefore, the role of surgery in decreasing the
risk of pelvic infection is questionable.
Interestingly, in almost half (10/21) of the patients in
the endometriosis group, we could not identify a preceding
medical intervention. We suggest two explanations for
this. First, these women might have undergone some
medical intervention more than four weeks prior to their
admission, causing a slowly developing infection with a
delayed clinical presentation. Secondly, the bloody content
of endometriosis implants and especially endometriomas
may serve as a culture medium for bacteria and facilitate
the spread of infection even without a preceding invasive
procedure. It was previously shown that Escherichia coli
colony formation in menstrual blood from women with
endometriosis was higher compared with control women.17
Therefore, menstrual blood from women with endometriosis may serve as an additional source of infection in
these women. Furthermore, endometriosis are ups may
be similar to PID in symptomatology and may be an
additional cause for the increased incidence of
endometriosis in patients diagnosed with PID.
Our nding suggests that once pelvic infection occurred
in women with endometriosis, one can expect a prolonged
and complicated hospitalisation. This was observed despite
a very rigid treatment protocol which demands invasive
intervention if there is no improvement after 48 h of
intravenous antibiotic treatment. This emphasises the need
to eradicate pelvic endometriosis implants during
endometriosis procedures to facilitate the treatment of
severe pelvic infections if and when these occur.
Our study has several weaknesses that we would like to
acknowledge. Firstly, it was retrospective. Secondly, the
treating physicians were not blinded to the clinical status
of the women with regard to their endometriosis.
Presumably, this may have had an effect on the
management plan and may have altered the clinical
course. This may have lead to a potential bias that could
not have been avoided, as such knowledge cannot be
withheld.
In conclusion, endometriosis is a risk factor for the
development of severe pelvic infection especially following
IVF treatments. Furthermore, pelvic infection in women
with endometriosis tends to be more serious and resistant
to antibiotic treatment, frequently requiring surgical
intervention. Practitioners should be aware, when
admitting women with PID and TOA, that if the women
has a history of endometriosis, she is likely to require
more aggressive management especially following a recent
IVF treatment.

2014 The Royal Australian and New Zealand College of Obstetricians and Gynaecologists

Severe pelvic infection in women with endometriosis

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