T h e La p a ro s c o p i c

Management of
Endometriosis in Patients
with Pelvic Pain
Patrick Yeung Jr, MD

KEYWORDS
 Endometriosis  Excision surgery  Laser surgery  Diagnostic imaging  Pelvic pain
 Recurrence

KEY POINTS
 Diagnostic laparoscopy is indicated for women whose quality of life is significantly
affected, for whom hormonal suppression has failed (or is contraindicated), or who desire
fertility.
 Transvaginal ultrasonographic imaging (which may include evaluation for deep endome-
triosis) can aid in surgical planning.
 Optimal excision or removal of disease is the best way to reduce recurrence rates, and
may also be a way to conserve normal ovaries and avoid surgical menopause, even
when hysterectomy or definitive therapy is indicated.
 Early diagnosis and treatment may be the best way to prevent the development of exten-
sive disease and, perhaps, to preserve fertility.

Video of ureterolysis accompanies this article at http://

www.obgyn.theclinics.com/

INTRODUCTION

Endometriosis is estimated to be present in 1 of every 10 women.1,2 It is a condition

whereby endometrial glands and stroma (normally found within the endometrial cavity
and shed during the menstrual period) are found outside the uterine cavity. Endome-
triosis is an underdiagnosed and undertreated problem, and multiple studies have
shown that it can take an average of up to 12 years to diagnose (especially in teen-
agers) from the time of onset of symptoms to the diagnosis at laparoscopy.3–6 This
delay in diagnosis can contribute to impaired quality of life and may have implications
for fertility.7–9

Center for Endometriosis, Division of Minimally Invasive Gynecologic Surgery, Department of

Obstetrics, Gynecology & Women’s Health, Saint Louis University, 6420 Clayton Road, Suite
290, St Louis, MO 63117, USA
E-mail address: pyeung1@slu.edu

Obstet Gynecol Clin N Am 41 (2014) 371–383

http://dx.doi.org/10.1016/j.ogc.2014.05.002 obgyn.theclinics.com
0889-8545/14/$ – see front matter Ó 2014 Elsevier Inc. All rights reserved.
372 Yeung Jr

Laparoscopy is the gold standard for the diagnosis of endometriosis, by visualiza-

tion of implants characteristic of endometriosis or, better still, by histology of excised
lesions.10 Laparoscopy is also the preferred route for treatment (when possible) of
endometriosis because laparoscopy affords the benefits of magnification, illumination,
and high-definition optics to better visualize the disease.
Although there is no cure for endometriosis, optimal laparoscopic management can
benefit patients with pain (and improve fertility) and improve their quality of life.11–13
Patients with endometriosis might benefit from early diagnosis and laparoscopic man-
agement, before progression of the disease, and providers should know when to oper-
ate and when to refer these patients.8

ENDOMETRIOSIS AND PAIN

Endometriosis is known to be associated with pain, and should be thought of as part of

a comprehensive evaluation for pain.9 During the adolescent period at least 75% of
patients who failed medical treatment were found to have endometriosis.7 Some algo-
rithms recommend a diagnostic laparoscopy later in the evaluation after all other
causes of pain have been ruled out or treated, including interstitial cystitis, vaginismus
or myofascial pain, and pudendal neuralgia. Others recommend diagnostic laparos-
copy sooner because endometriosis, unlike other causes of pain, can affect fertility,
and surgical management for endometriosis may improve or preserve fertility.9,14
Although it is known that endometriosis and pain are associated, the exact causal
relationship is not clear. Of note, the extent of disease (based on the most widely
used revised American Society of Reproductive Medicine [r-ASRM] classification
system15) does not correlate well with the severity of symptoms.16 The way that endo-
metriosis is currently classified is based on extent of disease, the presence of endo-
metriomas, and adnexal or cul-de-sac adhesions. Deep endometriosis (or deep
infiltrating endometriosis [DIE]) is not a part of the current classification system. How-
ever, there is evidence to show that the location of deep endometriosis has some cor-
relation to the location of pain,17 whereas the location of superficial endometriosis
does not.18 Newer classification systems are being developed to include DIE.19

HORMONAL VERSUS SURGICAL MANAGEMENT

Hormonal suppression is often recommended as first-line treatment for pain thought

to arise from endometriosis.10 Hormonal suppression can improve symptoms such
as pelvic pain and dysmenorrhea. Empiric therapy with hormonal suppression,
including a gonodotropin-releasing hormone agonist (GnRHa) or birth control pills,
is often used to control symptoms, as a form of diagnostic trial, and to prevent pro-
gression of disease. However, a response to empiric therapy (meaning improvement
in symptoms), for example, with a GnRHa, is not diagnostic for the presence of endo-
metriosis.10 Failure of pain to respond adequately to hormonal suppression should be
investigated further for endometriosis.
Hormone suppression may do little to prevent recurrence or progression of the
actual disease. A study of 90 patients by Doyle and colleagues20 in 2009 showed
that hormonal suppression given after surgery worsened (10%) or did not change
staging or extent of the disease (70%) in 4 of every 5 women. Moreover, studies
have shown that the need for hormonal suppression to control pain in earlier years
may be a marker for more advanced disease. Studies by Chapron and colleagues21–23
in 2011 showed that patients with severe endometriosis, when questioned about their
adolescent history, had greater school absenteeism and an earlier or extended need
for hormonal suppression to control pain in the adolescent years.
 Endometriosis in Patients with Pelvic Pain 373

Finally, hormonal suppression does not improve fertility, neither while the patient is
on suppression nor in the future.24,25

DIAGNOSIS
History and Evaluation
Symptoms characteristic of endometriosis include the following: dysmenorrhea,
chronic pelvic pain (more than 3 months of pelvic pain outside the menstrual period,
between the umbilicus and the thighs), deep dyspareunia, period-related dyschezia,
and period-related dysuria.10 Chronic pelvic pain has many different potential causes
and is often multifactorial. Causes of chronic pelvic pain include endometriosis, pelvic
inflammatory disease, interstitial cystitis, urinary tract infection, myofascial pain or
vaginismus, and irritable bowel syndrome, to name a few.26 A thorough evaluation
and testing of the causes of chronic pain should be performed as directed by the his-
tory. Moreover, chronic pelvic pain can lead to centralization or sensitization to pain,
which may need to be addressed. Under such circumstances the brain is sensitized to
feeling pain even when the source of pain is treated or diminished.27 A multimodal
team approach is often the best way to treat chronic pelvic pain. Within the evaluation
for chronic pelvic pain, endometriosis should be especially addressed if fertility or
future fertility is desired.28

Indications for Laparoscopy

Providers who care for women should have a high index of suspicion for endometriosis
when symptoms affect activities of daily living or quality of life. Examples include pel-
vic pain or dysmenorrhea that leads to absenteeism from school or work, deep dys-
pareunia that prohibits intercourse, or the need for narcotics to deal with pelvic
pain.12 In the adolescent population in particular, patients who have chronic pelvic
pain but whose symptoms fail to improve with hormonal suppression have a very
high prevalence of endometriosis. Experts have recommended that expectant man-
agement is inappropriate in patients with a visual analog scale score of greater than
7 or in patients with a poor quality of life as subjectively assessed by the patient.29
Infertility is another reason to perform laparoscopy for endometriosis. Historically,
all patients with infertility have received a routine laparoscopy for evaluation of endo-
metriosis given the known association of endometriosis with infertility. Current recom-
mendations for laparoscopy because of fertility concerns include: age younger than
30 years; when in vitro fertilization (IVF) is not an option; or when a patient has failed
2 attempts at IVF.28 The laparoscopic management of endometriosis has been shown
to improve both pain30 and fertility outcomes.13,31 In a recent study by Lee and col-
leagues,32 42% of patients (with endometriosis ranging from stages I to IV) conceived
successfully without hormonal treatment or artificial reproductive technologies within
a year after surgery. In another study by Darai and colleagues33 in 2005, pregnancy
rates for a cohort of 34 women requiring colorectal bowel resection for advanced dis-
ease was 45% within 24 months.

The Potential Benefit of Early Diagnosis and Treatment of Endometriosis

Endometriosis is thought to be a progressive disease, although not in all cases.8,34
Thus extensive or deep disease can arise from superficial disease. Some have touted
the benefits of diagnosing and treating endometriosis earlier in the disease process,
even in adolescence, which could improve lifelong pain and quality of life, and reduce
the rate of progression to more advanced disease.13 Early intervention and optimal
removal of disease, by reducing the rate of recurrence or progression, has the
374 Yeung Jr

potential to improve or preserve downstream fertility,12 although this has to be sys-

tematically studied.

Preoperative Examination
The goal of surgery should be to “see and treat” laparoscopy when possible.35 That is,
at laparoscopy the disease is fully identified and optimally treated at the same time.
The best way to achieve this is with thorough preoperative planning that includes his-
tory, physical examination, and preoperative imaging, usually transvaginal ultrasonog-
raphy (TVUS). A physical examination should include assessment of the uterosacral
ligaments (thickening, shortening, nodularity), mobility of the uterus and adnexa,
adnexal masses, and a rectovaginal examination for cul-de-sac nodularity. Deep dis-
ease may be able to be diagnosed or suspected preoperatively, and ideally managed
at surgery in a multidisciplinary fashion if necessary.36 A history of dyschezia may in-
crease suspicion for deep disease. A fixed or immobile uterus, or cul-de-sac nodular-
ity, would imply an obliterated cul-de-sac or deep endometriosis.

Preoperative Imaging
TVUS is the imaging modality of choice for the assessment of suspected endometrio-
mas or deep endometriosis. TVUS is an excellent imaging modality for female repro-
ductive organs, and can be performed in the gynecologist office setting, although it is
fairly operator-dependent.10 With proper training and experience in specialized cen-
ters, TVUS with bowel preparation (TVUS-BP), whereby the distal bowel has been
emptied by an enema, has been shown to be as accurate as pelvic magnetic reso-
nance imaging in diagnosing deep endometriosis in the posterior cul-de-sac.37–40
Preoperative ultrasonography may indicate deep disease directly, or indirectly if an
endometrioma larger than 8 cm or bilateral endometriomas are suspected.41,42 In
2010 Goncalves and colleagues,37 in a study involving 194 patients, showed the ability
of TVUS-BP to predict the number of lesions in cases of deep endometriosis with a
sensitivity and specificity of 97% and 100%, respectively (for a single bowel nodule),
and with a positive predictive value (PPV) and negative predictive value (NPV) of 100%
and 98%, respectively. Regarding the diagnosis of infiltration of the submucosal/
mucosal layer, TVUS-BP had a sensitivity of 83%, specificity 94%, PPV 77%, and
NPV 96%. Clearly this type of accurate imaging would be invaluable in helping to
define the surgical strategy.
If the surgeon or center is not able to manage deep endometriosis suspected before
surgery or discovered at the time of surgery, the patient should be referred to a sur-
geon or center that is able to manage deep or extensive endometriosis.13,43

SURGICAL TECHNIQUES

The goals of laparoscopic surgery for endometriosis are: optimal removal or treatment
of all visible and deep disease; restoration and preservation of anatomy and function;
and adhesion prevention.29 Pelvic pain and fertility can be improved with surgical
intervention.30,31

Near-Contact Laparoscopy
For early or mild forms of endometriosis (r-ASRM Stage 1–2), optimal excision de-
pends first on recognizing endometriosis in all of its forms.11 The most common
way to diagnose endometriosis is to visualize typical implants that have a “powder-
burn” appearance. However, a histologic diagnosis is more accurate, especially
when the lesions have a more atypical or subtle appearance. Atypical lesions include
 Endometriosis in Patients with Pelvic Pain 375

“red flame” lesions, white fibrotic lesions, vesicular or miliary lesions, and retraction
pockets (sometimes called Allen-Masterson pockets) (Figs. 1 and 2).44 Careful and
systematic near-contact laparoscopy should be used to find all lesions suspicious
for endometriosis (Fig. 3).44
Removal of Deep Disease
For more advanced (or deep) endometriosis (r-ASRM Stage 2–4), optimal excision de-
pends on not just recognition of peritoneal or superficial disease, but on recognition of
deep disease and restoration of anatomy.45 Surgery in these cases often includes bilat-
eral ureterolysis, cystectomy, adhesiolysis, and enterolysis, and opening of an obliter-
ated cul-de-sac or “frozen” pelvis. Of note, adhesions distort not just anatomy but also
visualization of endometriosis, so adhesiolysis alone is insufficient to achieve an
optimal surgical result. Once adhesions have been reduced, excision of the peritoneum
or deep disease must occur for proper treatment of endometriosis (Fig. 4). It has been
suggested that surgery for ovarian endometriosis alone is insufficient treatment.42,46
Evidence shows that treatment of deep endometriosis, including bowel endometriosis
and ovarian endometriomas, has been shown to benefit both pain and pregnancy out-
comes,13 with low recurrence rates.47,48 Some have recommended that centers of
excellence be created to manage difficult or challenging cases of endometriosis.49
Excision Versus Ablation
There is an ongoing debate about the best surgical method to treat endometriosis.
Published comparative studies50,51 do not account for surgical experience, nor of
the presence of deep endometriosis. There are several surgical scenarios in which
excision (removing the disease whereby a specimen is produced and sent to histol-
ogy) is intuitively superior to ablation (destruction of the disease with energy without
a specimen being produced). Such situations would include: deep endometriosis
(whereby ablation would just treat the “tip of the iceberg”); ovarian endometriomas
(which can be thought of as a form of deep endometriosis, see later discussion); endo-
metriosis over a vital organ such as the bladder, bowel, or ureter; a patch of endome-
triosis or an area of peritoneum after adhesiolysis; a retraction pocket of peritoneum
often caused by endometriosis. It is sometimes difficult to know when a superficial
lesion involves deeper tissue, and excision has been advocated by some investigators
for all cases of endometriosis.12,52

Fig. 1. Atypical and subtle phenotype of adolescent endometriosis as widespread brown

lesions.
376 Yeung Jr

Fig. 2. Atypical and subtle phenotype of adolescent endometriosis as widespread vesicular

or miliary lesions.

Energy Sources
Energy sources that have been used (for excision or ablation) include monopolar scis-
sors, “cold” scissors, ultrasonic energy (harmonic scalpel), and lasers (potassium
titanyl phosphate or KTP, neodymium-doped yttrium aluminum garnet or Nd:YAG,
carbon dioxide or CO2). The type of energy used is not as important as understanding
the energy and being able to use the energy source to achieve optimal surgical treat-
ment of the disease. For example, with monopolar energy, because the energy arcs
from the tip of the instrument to the tissue (and then through the body to ground),
the type of current and the presenting surface area (power density) of the instrument
are important variables. It is recommended with monopolar energy (35–40 W and
sometimes higher) to minimize the surface area of the presenting tip (using the utmost
tip of the scissors) and to use cut current to increase cutting precision and reduce
lateral thermal injury. With the free-beam CO2 laser, higher power (in the range of
12–15 W) can increase the precision of the laser as a cutting instrument, although
one must be careful not to let the laser dwell in one place over vital structures. Safe
practice, knowledge of the energy, and proper training are important for whichever en-
ergy source is used.

Fig. 3. The goal of endometriosis surgery is optimal excision of all visible lesions, both
typical and atypical, with minimal char and good hemostasis.
 Endometriosis in Patients with Pelvic Pain 377

Fig. 4. (A, B) The goal of surgery for endometriosis with an obliterated cul-de-sac is restora-
tion of anatomy and excision of visible or deep disease.

Treating Endometriomas
Evidence supports cystectomy (removal of the entire cyst wall) over incision and
drainage for the treatment of ovarian endometriomas or “chocolate cysts,” pain, recur-
rence, and fertility.53 In cases where a cycle-day 3 follicle-stimulating hormone levels
and antimullerian hormone (AMH) levels suggest reduced ovarian reserve, patients
should be given an opportunity to harvest ova for future use if desired. Cystectomy
has not been shown to negatively affect controlled hyperstimulation results.54 Cystec-
tomy has been shown to reduce AMH levels,55,56 although it would seem that good sur-
gical technique in finding the true plane between the cyst wall and the normal ovarian
tissue is important.57 In addition, it is unclear whether the presence of an untreated
endometrioma is also associated with a similar decline in AMH.58 Overall, most fertility
specialists (95%) would offer cystectomy for endometriomas in patients for whom IVF
is not an option, or for larger endometriomas (>3 cm) for patients undergoing IVF.59

Other Techniques
Ureterolysis is an important technique that should be used when lesions are found
over the ureter. Gynecologists who treat endometriosis should be familiar and
comfortable with performing ureterolysis when appropriate. Ureterolysis involves
freeing the ureter off the peritoneum, usually by sweeping parallel to the direction of
the ureter on the medial side (Video 1). Bilateral ureterolysis is also an essential step
when approaching an obliterated cul-de-sac.
Exploration and dissection of the retroperitoneal space and ureterolysis are impor-
tant techniques for any surgeon treating advanced endometriosis or deep disease.
Knowledge of the retroperitoneal anatomy, the course of the ureter, and how to control
bleeding by procedures such as hypogastric artery or uterine artery ligations will aid in
excising deep pelvic endometriosis. Treatment of an obliterated cul-de-sac requires a
systematic approach to restoring the anatomy and removing the disease, which usu-
ally involves cystectomy, bilateral ureterolysis, and a lateral to medial approach to
release the bowel from the retrocervical or rectovaginal space. Vignali and col-
leagues48 showed that surgical completeness of removal of deep disease will affect
the rate of recurrence of endometriosis.

Preoperative Bowel Preparation

Preoperative bowel preparation has traditionally been used for diagnostic/operative
laparoscopy for endometriosis, especially in cases when bowel endometriosis, deep
endometriosis, or an obliterated cul-de-sac is suspected. Systematic reviews no
longer recommend preoperative bowel preparation for gynecologic surgery, because
378 Yeung Jr

it has not been shown to decrease the risk of bowel repair leakage or the need for co-
lostomy.60,61 That said, it is important to discuss the use of preoperative bowel prep-
aration with the colorectal or general surgeon participating in the patient’s care.

Definitive Surgery
Many consider definitive surgery for endometriosis to be total hysterectomy and bilat-
eral salpingo-oophorectomy. The reasoning is to remove the uterus and thus the risk
of adenomyosis (and, because menstruation is often painful, even without a patho-
logic diagnosis of adenomyosis), and to cause a surgical menopause to remove the
stimulation of endometriosis left in the pelvis. The problem with this approach is
that the actual disease remains and can still cause symptoms (especially deep endo-
metriosis), and the benefits of ovarian hormone production have been lost, including
cardiovascular and bone health. Another surgical approach that should be consid-
ered, especially in younger women who have completed childbearing, is to optimally
remove the endometriosis and the uterus (again to reduce the risk of adenomyosis)
with the fallopian tubes (not needed without the uterus and to reduce the risk of
ovarian cancer62), but to conserve at least one, or both, ovaries.

Recurrence Rates
Recurrence rates of actual disease depend on the technique used, especially for deep
endometriosis. Rates of recurrence (or persistence) of endometriosis after ablation are
approximately 20% to 50% in 2 years63,64 (approaching 50% by 5 years65), but as low
as 0% at 2 years after optimal excision.11 Of note, adding hormonal suppression after
surgery does not further reduce the rate of actual recurrence of disease beyond the
benefit of what is done at surgery, as noted by Doyle and colleagues20 (see earlier dis-
cussion). Recurrence of pain does not necessarily indicate recurrence or persistence
of endometriosis. In particular, when optimal endometriosis surgery has been
achieved, other causes of pain should be evaluated before repeat surgery.
Recurrence rates after conservative surgery, even for advanced or deep disease, can
be low (<10% in 3 years),48 which depends on the surgical completeness of removing
the disease. It has been suggested that extensive endometriosis can be avoided by
early diagnosis and intervention in the disease, even in the adolescent years.11,13

Adhesion Prevention
Adhesion prevention is very important for reducing pain, avoiding complications such
as bowel obstruction,66 and preserving fertility.67 Some have criticized excision

Table 1
Summary of fluid agents studied for the prevention of adhesions

Company Product Notes

— Hyaluronic acid Fluids that contain this product may
decrease scar tissue formation. Intergel
(ferric hyaluronate) has been taken off
the market for safety concerns
Baxter, Nottingham, UK Icodextran 4%, Adept There is insufficient evidence to
recommend its use
Confluent Surgical, Spraygel There is insufficient evidence to
Waltham, MA, USA recommend its use

Adapted from Ahmad G, Duffy JM, Farquhar C, et al. Barrier agents for adhesion prevention after
gynaecological surgery. Cochrane Database Syst Rev 2008;(2):CD000475.
 Endometriosis in Patients with Pelvic Pain 379

Table 2
Summary of barriers studied for the prevention of adhesions

Company Product Notes

Genzyme, Middleton, Seprafilm Limited evidence in preventing adhesion following
WI, USA myomectomy
Johnson & Johnson, Interceed Shown to reduce new and reformation of adhesions
Somerville, NJ, USA
W.L. Gore & Associates, GoreTex Shown to be more effective than placebo and
Newark, DE, USA Interceed in the prevention of adhesions

Adapted from Farquhar C, Vandekerckhove P, Watson A, et al. Barrier agents for preventing
adhesions after surgery for subfertility [systematic review]. Cochrane Database Syst Rev 2008;(2):
CD000475.

surgery for being adhesiogenic,68 but this has never been studied in comparison with
ablation surgery for endometriosis. Good surgical technique is most important for
minimizing adhesions, including achieving good hemostasis and minimizing char or
desiccated tissue.69 Adjunctives for adhesion prevention have been studied, and
include the use of instillates70 (Table 1) and barriers71 (Table 2). Of all the barriers,
GoreTex (W.L. Gore and Associates, Newark, DE, USA) has been shown to be the
most effective, but it requires being secured in place and usually requires a second
laparoscopy to remove it. There is some evidence to suggest that peritoneal closure
may help to reduce adhesions in comparison with nonclosure.72 Ovarian adhesions
and ovarian surgery (such as cystectomy) are risk factors for developing new and
recurrent adhesions.68,73 In the General Surgery literature, Seprafilm (Genzyme, Mid-
dleton, WI, USA) has been shown to reduce abdominal adhesions,74 and the use of a
Seprafilm slurry has been described for its use at laparoscopy.75 Further research is
required to develop safe and effective adhesion prevention products.76

SUMMARY

Laparoscopic surgery has a clear, established role in the diagnosis and treatment of
endometriosis of pelvic pain and infertility. Patients with pain (affecting quality of
life), especially with infertility, should be offered diagnostic laparoscopy. A high index
of suspicion will lead to early diagnosis and treatment of endometriosis, and better
outcomes for patients. Excision surgery can more completely treat the disease than
can ablation. Appropriate patient selection, and preoperative planning, will ideally
lead to “see and treat” laparoscopy. The goal of laparoscopic management of endo-
metriosis is the optimal removal or treatment of all visible lesions, both typical and
atypical, and deep disease. Hysterectomy may be needed for suspicion of adenomyo-
sis in patients with dysmenorrhea who have borne children, although ovarian conser-
vation can be achieved if the endometriosis is optimally treated. Referral to a center or
surgeon with expertise in the laparoscopic treatment of endometriosis is always an
option for difficult cases or deep disease. The development of dedicated centers of
expertise for treating endometriosis with appropriately trained surgeons and a
committed multidisciplinary expert team is recommended.

SUPPLEMENTARY DATA

Video related to this article can be found online at http://dx.doi.org/10.1016/j.ogc.

2014.05.002.
380 Yeung Jr

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