Abstract
Study objective: Complete eradication of parametrial nodules of Deep Infiltrating Endometriosis (DIE) is
associated with a high risk of iatrogenic nerves damage and pelvic organs dysfunction. The aim of this study
is to evaluate the effect of laparoscopic excision of parametrial DIE on quality of life, pain symptoms and
post- operative voiding function (bladder and rectal).
Design: Retrospective observational study.
Setting: All patients undergoing laparoscopic nerve-sparing excision of parametrial DIE by a single expert
surgeon between January 2013 and March 2017 were included in the study.
Patients: Fifty-one patients were included in the final analysis.
Intervention: Quality of life (QoL) and Functional outcomes were evaluated using validated questionnaires
(EHP-30, NBD score, ICIQ-FLUTS), administered preoperatively and after surgery. Pain scores were
collected using Visual Analogue Scale (VAS).
Measurement and Main Results: EHP-30 scores had a significant improvement in all the domains
analyzed. No differences were found in terms of urinary function. The NBD score showed that intestinal
dysfunction was. reported as very minor by 76.4%, minor by 11.8%, moderate by 5.9% and severe by
5.95% of patients. Pain symptoms (VAS score) decreased significantly after surgery except for chronic
pelvic pain (p value < .05).
Conclusion
Laparoscopic nerve-sparing radical excision of parametrial DIE can favorably impact on
patients QoL and reduces pain score and intestinal dysfunction.
Keywords
Deep Endometriosis; Laparoscopy; Nerve-Sparing; Parametrial Endometriosis; QoL
Abbreviations: DIE: Deep Infiltrating Endometriosis; VAS: Visual Analogue Scale; NBD: Neurogenic Bowel
Dysfunction; QoL: Quality of Life
ARTICLE INFO
Received:
July 06, 2023
Published:
July 13, 2023
Citation: Carlo Alboni, Veronica Sam -
pogna, Mirvana Airoud, Stefania Mal -
musi, Antonino Farulla, Giuseppe
Colucci, Ludovica Camacho Mattos,
Annarita Pecchi, Giorgia Gaia and An -
tonio La Marca. Functional Outcomes
and Quality of Life After Laparoscopic
Nerve-Sparing Radical Treatment of
Parametrial Deep Infiltrating Endome -
triosis. Biomed J Sci & Tech Res 51(3)-
2023. BJSTR. MS.ID.008116.
Copyright@ : Veronica Sampogna | Biomed J Sci & Tech Res | BJSTR. MS.ID.008116.
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DOI: 10.26717/BJSTR.2023.51.008116
Introduction
Endometriosis is a chronic inflammatory disease, characterized
by ectopic proliferation of endometrial glands and stroma [1-3]. The
deep infiltrating endometriosis (DIE) is a specific clinical entity char-
acterized by an extension of the disease more than 5 mm under the
peritoneal surface, retroperitoneal fibrosis and neural tropism with
distortion of the regular pelvic anatomy [4]. DIE affects most fre -
quently uterosacral ligaments (69.2%), rectovaginal septum (14.5%),
bowel (9.9%) and bladder (4.2%) [5]. In recent years a growing atten-
tion was pointed out on parametrial localization of DIE with studies
investigating diagnosis, treatments and clinical outcomes [6-8]. The
lateral parametrium contains the nerve branches of autonomic pelvic
organs innervation, therefore the complete eradication of the disease
is associated with the risk of serious impairment of rectal, bladder
and sexual function due to the iatrogenic disruption of inferior hypo-
gastric plexus Radical resection of the posterior parametrium, corre-
sponding to the uterosacral ligament plus rectovaginal ligaments and
lateral ligament of the rectum, can also result in injury to the hypo -
gastric nerves, pelvic splanchnic nerves and to the anterior branches
of the sacral sympathetic chains. Different authors have described
the nerve-sparing approach in case of DIE nodules [9-11]. In 2012,
a prospective cohort study compared the laparoscopic nerve-spar -
ing approach to the classical laparoscopic procedure demonstrating
the feasibility of radical removal of infiltrating endometriosis tissue
from parametrial structures avoiding disruption of autonomic pelvic
organs innervation [12].
There has been a growing interest in recent years on analyzing
QoL after laparoscopic surgery for endometriosis. However, only a
few studies have specifically addressed data on functional outcomes
after DIE excision, and, to the best of our knowledge, no one was pub-
lished investigating patient’s QoL with specific validated question -
naires [13,14]. The aim of this study is to use validated questionnaires
to evaluate patients’ response to laparoscopic nerve- sparing excision
of parametrial DIE in terms of self-perceived well-being, pain relief
and voiding function.
Materials and methods
This study was approved by the local Ethics Committee (protocol
number 0024582/19), and all patients expressed their informed con-
sent to anonymous data collection. All patients that underwent lap -
aroscopic surgery for endometriosis in the period between January
2013 and March 2017 at Obstetrics and Gynecology Division of the
Sassuolo Civil Hospital and at the Endometriosis tertiary level referral
center of the University Hospital of Modena were enrolled. All sur -
geries were performed by the same surgeon with high expertise in
laparoscopic treatment of endometriosis (C.A.) Medical records from
patients with histologically confirmed laparoscopic resection of pos -
terior and/or lateral parametrium were collected. Exclusion criteria
were as follows: age < 18 years, preoperative diagnosis of neurogenic
bladder and bowel inflammatory disease, absence of sexual activity
and failure to complete the study questionnaires. All patients under -
went speculum examination, pelvic bimanual vagino-rectal evaluation
and transvaginal ultrasound performed by an expert sonographer ex-
pert in endometriosis diagnosis. A transabdominal ultrasound scan
of the kidneys was also routinely performed to rule out hydrouret -
eronephrosis. Eventually, they underwent pelvic magnetic resonance
with rectal injection of 10-50 ml of sterile gel to confirm dimension
and depth of infiltration of the bowel lesions (if any) and to define
the parametrial/ureteral involvement. All patients signed a specific
informed consent before surgery, specifying all surgical procedures
necessary for their complete excision and the potential risks (vascu -
lar, neurologic, urologic and intestinal) related to the type of surgery.
All patients were submitted to nerve sparing excision of DIE ac -
cording to Negrar Method [15]. In case of bowel lesions infiltrating
the muscularis interna and causing a stenosis of more than 50% of
the lumen in patients symptomatic for bowel dysfunction, a segmen -
tal resection with Knight-Griffen technique and end-to-end anasto -
mosis was performed by a general surgeon. A protective ileostomy
was routinely done in case of ultra-low rectal segmental resection
(resection margin < 5 cm from the dental line). The data on patient
age, parity, body mass index, previous abdominopelvic surgery, oper-
ating time, amount of blood loss, use of hormonal therapy, length of
hospital stay were recorded, while intraoperative, early and late post-
operative complications were analyzed according to the Clavien-Din-
do classification system [16]. Pain symptoms were investigated using
the Visual Analogue Scale (VAS) and the different need of analgesic
drugs was evaluated at the preoperative visit and at the follow up
evaluation after three months. For the comparative analysis of dys -
menorrhea with VAS scale, patients underwent hysterectomy and pa-
tients with post-operative continuous hormonal therapy were exclud-
ed (22 patients). Quality of life and functional and status outcomes
were collected using the Italian validated version of Endometriosis
Health Profile-30 (EHP-30) and International Consultation on Incon -
tinence-Female Lower Urinary Tract Symptoms (ICIQ-FLUTS) [17]
and the Italian translation of Neurogenic Bowel Dysfunction (NBD)
[18], administered one month before surgery and three months after
the intervention.
The EHP-30 was used to evaluate the global health profile of the
patients [19] and consists of 30 questions about pain, control and
powerlessness, emotional well-being, social support and self-image.
Currently is the only questionnaire that evaluates QoL specifically in
patients with endometriosis. For bowel function the NBD score was
used [20]: this questionnaire evaluates intestinal dysfunction and
its impact on quality of life in patients with neurological lesions; it is
based on 10 items assessing defecation and faecal incontinence with
a score ranging from 0 (very low disfunction) to 47 (severe disfunc -
tion). The urinary function was evaluated using ICIQ-FLUTS [21,22].
this questionnaire includes 22 items relating to bladder filling, uri -
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42799
nation and incontinence; for each question, a score from 0 to 4 is
assigned. Higher scores correspond to a higher level of dysfunction.
Data were expressed as mean±standard deviation or median (range)
for numerical variables and as numbers (percentages) for categori -
cal variables. The Wilcoxon test was used to compare any change in
variables before and after the surgical treatment. P value of <0.05 de-
noted statistical significance. All statistical analyses were performed
using SPSS software (version 21, SPSS, Inc., Chicago, IL, USA).
Results
During the study period a total of 65 patients underwent
nerve-sparing surgery for parametrial deep infiltrating endometrio -
sis. 51 patients met the inclusion criteria and were included for the
study analyses. Demographic characteristics of patients are provided
in (Table 1). Mean age was 36.6 ± 6.2 years. Eight patients had had
previous surgery for endometriosis (15.6%) and 27 were nulliparous
(53%). Operative details and procedures are summarized in (Table
2). Dysmenorrhea was the most frequent symptom (84.3%), followed
by dyspareunia (74.5%), ovulatory pain (70.6%), dyschezia (51%),
chronic pelvic pain (35.3%) and stranguria (27.5%). Laparoscopic
approach was used in all cases, no conversion to open surgery oc -
curred. Laparoscopic segmental bowel resection was performed in
15 (%) patients, while discoid resection was performed in only one
(%). Three (%) patients needed protective ileostomy for ultra-low
rectal anastomosis. The mean operating time was 239 +/-111 min -
utes. The mean estimated blood loss during surgery was 165 +/- 59.9
mL (range 50-1020 mL). The mean hospital stay was 6 days (range
3-12 days). In 37 patients (62.7%) parametrial endometriosis was
unilateral, in 13 patients (22% of cases) both posterior and lateral
parametrium were involved and in 9 patients (15.3% of cases) poste-
rior and lateral parametria were involved bilaterally. Right posterior
parametrium was involved in 38% of cases (19/50), while the left one
was involved in 40% of cases (20/50). Right lateral parametrium was
involved by endometriosis in 59.1% of cases (13/22), the left one was
involved in 31.8% of cases (7/22), and lateral parametria were in -
volved bilaterally in 9.1% of cases (2/22).
Table 1: Demographic characteristics of patients.
Age, years 36 +/- 6.2
Weight, kg 62.1 +/- 12.9
BMI, Kg/m2 22.7 +/- 3.9
Nationality
· Caucasian 90.1% (46/51)
· North African 5.9% (3/51)
· Asian 2% (1/51)
· Latin American 2% (1/51)
Marital Status
· Married 72.5% (37/51)
· Divorced 11.8% (6/51)
· Nubile 13.7% (7/51)
· Widow 2% (1/51)
Education
· Secondary school 21.6% (11/51)
· High school 56.8% (29/51)
· Degree 21.6% (11/51)
Occupation
· Employed 88.2% (45/51)
· Unemployed 9.8% (5/51)
· Students 2% (1/51)
Medical History
· No prior history 33.3% (17/51)
Note: Values are given as mean +/- standard deviation or absolute number
(percentage).
Table 2: Detail of operative procedures.
OPERATIVE PROCEDURES
endometrioma enucleation 31/51 (60.8%)
monolateral adnexectomy 8/51 (15.7%)
ovarian fossa peritoneum removal 25/51 (49%)
Total hysterectomy 5/51 (10%)
Rectosigmoid endometriosis
removal 31/51 (60.7%)
-Shaving 15/51 (29.4%)
-bowel resection 15/51 (29.4%)
-discoid resection 1/51 (2%)
protective ileostomy 3/51 (5.9%)
Lateral parametrium removal 15/51 (29.4%)
Unilateral 13/15 (86.6%)
right 7/15 (46.6%)
left 6/15 (40%)
Bilateral 2/15 (13.4%)
Posterior parametrium removal 44/51 (86.3%)
Unilateral 36/51 (70.6%)
right 16/44 (36.4%)
left 20/44 (45.4%)
Bilateral 8/51 (15.7%)
Note: Values are given as absolute number (percentage).
The average size of parametrial nodules was 2 +/- 0.5 cm. No case
of intrinsic ureteral endometriosis was found. No intraoperative com-
plications occurred. Three postoperative complications were regis -
tered: one hemoperitoneum (class IIIb), one rectovaginal fistula (class
IIIb) and one case of stenosis of colorectal anastomosis requiring en-
doscopic balloon dilation (class IIIa). Twenty-seven patients (52.9%)
were undertaking hormonal therapy at the 3-month post-operative
follow up visit. Pain symptoms severity expressed in VAS score, except
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CPP , were significantly decreased after the operation (p value < .05)
as shown in (Table 3). The EHP-30 score before and after surgery are
shown in (Table 4). Surgery improved significantly QoL in many of the
domains analyzed such as pain, control and powerlessness, emotional
well-being, social support, self-image, satisfaction of treatment, sex -
ual life. It was not possible to evaluate the “infertility” and “relation -
ship with children” modules because respectively 21 (41.2%) and 31
(60.8%) patients did not answer the questions. Limited to the small
sample analyzed, however, even in these two modules a statistical -
ly significant improvement was observed. No significative disfunc -
tion were found at post-operative ICIQ-FLUTS questionnaire. Bowel
function improved after surgery in patients’ subjective perception,
although the results are controversial: the NBD score showed that in-
testinal dysfunction in the whole group was related to constipation,
while the surgery was resolutive for diarrhea. Most of the patients
showed mild dysfunction (76.4%), while only three patients had se -
vere dysfunction (5.9%).
Table 3: VAS score before and after surgery*.
Median + IQR
before
Median + IQR
after p-value
Dysmenorrhea 8 + 5.5 2 + 5.25 0.01
Dyspareunia 6 + 3 4 + 3 0.012
Chronic pelvic
pain 0 + 3.5 0 + 0 0.823
Dyschezia 2 + 7.5 0 + 2.5 0.001
Strangury 0 + 4 0 + 0 0.01
Note: VAS score before and after surgery, values are given in median +
IQR (interquartile range) *no continues hormonal therapy l contraceptives.
Table 4: EHP-30 scores before and after surgery.
EHP-30 questionnaire BEFORE SURGERY AFTER SURGERY P-value
Pain 47.2 (+/- 25.3) 10.1 (+/- 14.8) < .001
Control and powerlessness 56.3 (+/- 25.7) 13.2 (+/- 15.6) < .001
Emotion 53.4 (+/- 24) 23.3 (+/- 20.7) < .001
Social support 38.8 (+/- 26.5) 22.2 (+/- 21.5) < .001
Self-image 30.7 (+/- 23.9) 19.7 (+/- 22.5) < .001
work module 38.8 (+/- 28.3) 9.3 (+/- 16.7) < .001
relationship with children 20 (+/- 26.1) 6 (+/- 12.9) 0.002
sexual intercourse 49.2 (+/- 27.8) 20.6 (+/- 22.6) < .001
medical profession 21 (+/- 26.7) 3.9 (+/- 8.7) < .001
treatment module 38.3 (+/- 29.1) 15.5 (+/- 21.9) < .001
infertility module 48.8 (+/- 27.8) 30.2 (+/- 30.0) .007
Note: Values are given as mean +/- standard deviation or absolute number (percentage), if not otherwise expressed.
Discussion
The parametrium has been described as the supporting system
of the uterus that anchors the organ to the lateral pelvic wall and has
both supply-drainage and fascial functions. More often DIE lesions
are at the level of the posterior and lateral part of the parametrium
associated to retrocervical, bowel and ureteral nodules [23]. This pat-
tern of lesions distribution can be associated with ureteral and bowel
function impairment and often with chronic pelvic pain symptoms
expressed as dyspareunia and dyschezia [8,24]. Due to these symp -
toms, endometriosis may have a profound impact on quality of life
and mental health of the patients affected. In 2004 (Abbot, et al. [25])
demonstrated that surgical excision of endometriosis determines
a symptomatic improvement. significantly more than placebo. Ac -
cording to this evidence, surgical eradication of DIE represents the
treatment of choice in symptomatic patients unresponsive to medical
treatment. The preservation of the pelvic autonomic system may be
challenging in case of large nodules and surgical treatment of deep
infiltrating endometriosis needs adequate surgical skills and exper -
tise to minimize the risk of surgical complication; in fact only a few
series, with limited sample size, have demonstrated the feasibility
of nerve-sparing surgery in case of parametrial DIE [26-28] To the
best of our knowledge this study is the first to analyze the impact of
laparoscopic nerve-sparing surgery for parametrial deep infiltrating
endometriosis on quality of life using EHP-30 questionnaire. We ob -
served that this type of surgery improved quality of life of patients
and reduced all the painful symptoms, except for chronic pelvic pain.
This evidence suggests that a “symptom guided approach” and a
radical surgery are associated with better postoperative outcomes.
The main post-operative improvement in term of quality of life re -
lates to domains affecting social and relationship life. This represents
an important goal considering that the average age of the patients
enrolled is 36 years, with a percentage of working and married wom-
en being respectively 88.2% and 72.5%, and that 47% of them are
engaged in the management of children. Furthermore, the eventual -
ity of surgical complications associated with this technique was low.
Patients reported a subjective improvement in bowel function at NBD
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questionnaire, excepted for constipation. This evidence is in accor -
dance with a retrospective study by (Abo, et al. [29]) on 371 women
undergoing surgery for colorectal endometriosis. The results of the
ICIQ-FLUTS questionnaire on urinary function showed that incon -
tinence was more frequent in patients undergoing posterior para -
metrial resection than those undergoing lateral or resection of both
parametria. However, a conclusion can’t be achieved because of size
discrepancy between the three groups (36/51 patients underwent
resection of the posterior parametrium, 7/51 of the lateral parame -
trium and 8/51 of both parametria). The main bias of our study is
related to the lack of pre-operative data on urinary function. Many
authors have studied the incidence of urinary symptoms in patients
with endometriosis (Fauconnier, et al. [24]).
Related specific symptoms to anatomical locations of DIE but did
not evaluate the correlation between urinary symptoms and posteri-
or DIE; (Darai, et al. [30]) reported a high incidence of urinary symp-
toms in patients with deep infiltrating endometriosis, but without
being able to correlate the presence of symptoms with well-defined
anatomical lesions. Among the possible limitations of this study, we
mention the small sample size, the lack of a comparison arm of pa -
tients not receiving nerve-sparing approach and the short follow up
[31,32]. On the other hand, our study provides the first analysis of
the impact of nerve-sparing surgery on quality of life, using validated
questionnaires and it gives good and promising results for the sys -
tematic use of this type of approach.
Conclusion
In conclusion, the use of nerve sparing technique by expert sur -
geons warrants good results in term of improvement of QoL and pain
control and provides good functional outcomes. The development of
surgical skills based on anatomical knowledge can lead to a more ex -
tensive use of the nerve-sparing technique with a persistent improve-
ment in the quality of life of the patients with parametrial localization
of DIE.
Conflict of Interest
Authors have no conflict of interest and economic interest to de -
clare. The authors declare no conflict of interest. This research re -
ceived no specific grant from any funding agency in the public, com -
mercial, or not-for-profit sectors. The data that support the finding of
this study are available from the corresponding authors upon reason-
able request.
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