The enigma of primary and secondary encapsulating peritoneal sclerosis
Allam et al. BMC Surgery
The enigma of primary and secondary encapsulating peritoneal sclerosis
Hisham Allam 0
Omer Al Yahri 0
Sharon Mathew 0
Adham Darweesh 3
Ahmed Nafea Suliman 0
Sherif Abdelaziem 0
Mohamed Khairat 0
Adriana Toro 2
Isidoro Di Carlo 0 1
0 Departments of General Surgery, Hamad General Hospital , Al Rayyan Road, 3050 Doha , Qatar
1 Department of Surgical Sciences and Advanced Technologies “G.F. Ingrassia”, University of Catania , Catania , Italy
2 Department of General Surgery, Barone I. Romeo Hospital , Patti, Messina , Italy
3 Department of Radiology, Hamad General Hospital , Doha , Qatar
Background: Encapsulating Peritoneal Sclerosis (EPS) describes a variety of diseases that are frequently confused with different names and different etiopathogeneses. The aim of this article is to report personal experience of focusing on correct classification and the status of current diagnosis and treatment. Methods: A retrospective analysis was performed. Age, sex, ethnic origin, past medical history, symptoms and their duration, radiological tools and signs, laboratory tests, preoperative diagnosis, surgical approach, intraoperative findings, pathological findings, hospital stay, morbidity and mortality were studied. Results: A total of seven patients, including six males and one female, aged from 24 to 72 years were observed. Four patients had recurrent abdominal colic pain for 3 months, 1, 2 and 9 years; two patients also reported recurrent attacks but without any specification of the duration. All seven patients presented at the emergency department with abdominal pain that was mainly diffused over the entire abdomen. Six patients were submitted to a CT scan. Only in two patients was the diagnosis of EPS made preoperatively. All seven patients were submitted to open surgery. The hospital stay was between 4 and 60 days. One patient had morbidity, and one patient died of MOF. Conclusions: Currently, the correct identification of EPS is more easily possible than in the past, but the diagnosis is still a challenge. Surgery must be performed as soon as possible to avoid a poorer quality of life.
Encapsulating peritoneal sclerosis; Peritoneal encapsulation; Abdominal cocoon syndrome
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Background
Encapsulating peritoneal sclerosis (EPS) is an uncommon
chronic syndrome, usually presenting clinically as
intermittent, acute or sub-acute gastrointestinal obstruction
[1]. EPS can be divided into primary and secondary [2].
Primary EPS is also defined as idiopathic [3]. Primary EPS
have been also defined in 1978 as abdominal cocoon
syndrome [4]. The cause of primary EPS is still
unknown; [4, 5].
Secondary EPS is related to many conditions and
causes; the most common is peritoneal dialysis (Table 1).
Both forms (primary and secondary) are different from
peritoneal encapsulation (PE). This disease was reported
for the first time in 1868 by Cleland [6], and it is
represented by an accessory peritoneal membrane. More
than the result of inflammation should be considered with
a duplication of the peritoneum; this is found incidentally
in the majority of cases. The peritoneal membrane in this
disease is secured laterally to the ascending and
descending colon, cranially to the transverse mesocolon, and
caudally to the posterior parietal peritoneum. It has two
openings: one at the entrance of the intestine at the
duodenojejunal junction, and the other at the ileocecal
junction for the exit of the last loop. The absence of
sclerosis represents the difference with the EPS, in fact
the coverage of the intestine is only a layer of serosa
membrane like the peritoneum.
Many tools can be used to diagnose EPS. Instead of
utilizing the past medical history and the radiological finding,
preoperative diagnosis remains challenging, and in a high
percentage of cases, the diagnosis is reached at the time of
the surgical procedure.
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1) Peritoneal encapsulation
2) Sclerosing encpsulating peritonitis
a) Primary or idiopatic or abdominal cocoon syndrome
b) Secondary
The aim of this article is to report a valuable number
of patients who were observed in our hospital, focusing
on correct classification and the status of current
diagnosis and treatment.
Methods
A retrospective analysis was performed on patients
admitted to the Hamad General Hospital Department of Surgery,
General Surgery section, in the last 10 years from January
2005 to September 2015. Age, sex, ethnic origin, past
medical history, symptoms and their duration, radiological tools
and signs, laboratory tests, preoperative diagnosis, surgical
approach, intraoperative findings, pathological
examinations, hospital stay, morbidity and mortality were studied.
After this primary evaluation, all patients were classified by
primary or secondary EPS, and all of the data have been
revaluated to note the differences.
Results
In the period of the study, 10 patients were observed.
Three of these patients were previously published as
case reports [6, 7], and they will not be further reported
on here. Thus, we have analyzed the remaining seven
patients who have not yet been reported. The patients
were six males and one female, aged from 24 to 72 years
(mean age 44.5 years). The nationalities of the patients
were three Egyptians, two Indians, one Sudanese and one
Nepalese. Three patients had no comorbidities and were
considered to have primary EPS; the remaining four
patients had comorbidities. In one case, the patient had a
Mediterranean fever that was diagnosed more than 10 years
ago. In three cases, the patients were submitted to
peritoneal dialysis, in one case for 32 months and in the second
case, for 8 months; the duration was not reported in the
last case. All seven patients presented at the emergency
department with abdominal pain that was mainly diffused
over the entire abdomen; in addition to the main
symptoms, five patients had nausea, vomiting and constipation.
One patient had only diffuse abdominal pain and anorexia.
Four patients had recurrent abdominal colic pain for 3
months, 1, 2 and 9 years; two patients also reported
recurrent attacks but without any specification of the duration.
One patient had no history of a previous attack of
abdominal pain. Six patients were submitted to a CT scan. Only
in two patients was the diagnosis made preoperatively: in
one case, as a partial encapsulation and in the second one,
as a complete encapsulation of the small bowel (Fig. 1). In
the remaining four cases, the diagnosis was of intestinal
occlusion without any specifications. The last patient was
submitted to an X-ray examination that showed intestinal
occlusion but the diagnosis was erroneous because the
patient presented a bulk on the right side of the umbilicus
that was diagnosed as an obstructed Spigelian hernia. Five
patients presented with a slight elevation of WBC that was
normal in one patient and not reported in the last one. All
seven patients were submitted to open surgery. Five
patients had the entire small bowel encapsulated (Fig. 2); one
patient had an encasement of the last part of the jejunum,
ileum, appendix and cecum. The last patient had an
encasement of the small bowel and cecum with multiple
perforations between the last ileal loop and the cecum. All
patients were submitted to excision of the membranes and
adhesiolysis of the loops (Fig. 3), except the patient who
was affected by multiple perforations that was submitted to
excision of the membrane, adhesiolysis and right
hemicolectomy. In all seven cases, pathological examinations
showed the presence of hyalinized membranous
fibrocollagenous tissue compatible with a diagnosis of EPS.
The hospital stay was between 4 and 60 days. One patient
had morbidity; the patient came back to the hospital after
1 week with the symptoms of intestinal occlusion. The
patient was treated with bowel rest and parenteral nutrition,
and he resolved spontaneously after 4 days. Then, he was
discharged and no further complaints have been recorded.
One patient died after the initial resection of the last loops
of the ileum and the right colectomy. The patient
developed a wound infection, wound dehiscence and purulent
peritonitis with septic shock. He underwent a second
operation 2 weeks after the first procedure, and a couple of
small bowel perforations were found. Both the first and
second procedures were very difficult because of the
extensive adhesions between the bowel loops. Instead
of several operations and multiple treatments, the patient
Fig. 1 Contrast-enhanced CT scan of the abdomen showing a
conglomerate of multiple small-bowel loops seen in the center of
the abdomen, surrounded by a thick enhanced saclike structure
Fig. 2 View when entering the abdominal cavity
developed an entero-cutaneous fistula and consequently
abdominal sepsis and septic shock, and he died as a result
of multiple organ failure after 60 days of hospitalization.
All of the analyzed data have been used after classifying
the patients as having primary and secondary EPS. All of
the differences in the two groups are shown in Table 2.
Discussion
One of main issues of peritoneal encapsulation and EPS
is the different forms and different definitions that are
frequently used in the wrong manner, resulting in
confusion regarding all of the forms. Differentiation is simply
done by pathological examinations of the membranes. In
the case of PE, the membrane is covered by
mesothelium because it is an accessory peritoneal membrane
that is a kind of malformation. In contrast, in primary
and secondary EPS, the membrane that encases the
intestine is fibrous, containing inflammatory cells; this is a
consequence of the fact that this condition is acquired
as a result of an inflammation of the peritoneal serosa
that can be stimulated by many factors. EPS can be
secondary to the activity of multiple factors that can be
responsible for the inflammation of a systemic activity
Fig. 3 After division of the membrane and freeing the bowel loops
[8–11] or for local and/or systemic irritant factors [12–14].
Dialisys represents the most common cause of secondary
EPS and it is well established that is related to the chronic
exposure to bioincompatible dialysate. This exposure may
represent the initial step for the fibrotic process, that may
evolve until EPS [15]. In fact multiple and repetitive
episodes of tissue injury with consequent inflammation and
deposit of fibrin, permit to alert the mesothelial cells and
fibroblast, with development and deposition of matrix that
represents the precursor of EPS [15].
EPS can also be primary or idiopathic and can also be
defined as “abdominal cocoon syndrome”; in this case,
the cause is still unknown and it can present both in
adolescent and in adults. Different from secondary EPS,
this form can be without adhesions between the loops
[16]. The abdominal cocoon has differentiation in
relation to the extent of the encapsulation and the affected
organ (Table 3) [17, 18]. Some case reports have
confused primary abdominal cocoon syndrome and
peritoneal encapsulation in the past [19–22]. The etiology of
primary EPS is still debated. Both sexes are at risk, but,
as in the major report in the literature [23], our
experience shows that males are the predominant sex. Primary
EPS has been reported in adolescent females from
tropical or subtropical countries but also adult cases have
been reported from temperate zone as well [23]. One of
the main hypotheses circulating about the etiology has
been retrograde menstruation with consequent viral
infection [23]. This hypothesis has not still been validated
as a result of the fact that men and premenopausal
women are also affected by this form of the disease.
In our case series, all three cases of primary EPS were
male patients. All are young and this reflects the fact that
the country of Qatar is full of young male expatriates that
are construction laborers; none of the three patients came
from tropical or subtropical countries. Additionally, in the
second group, not all patients were from tropical or
subtropical countries, but all of these patients have a
comorbidity that can be considered as the cause of the
secondary EPS. In this second group, in contrast, the
age reflects the comorbidities that are the cause of the
EPS except in the patient who was affected by the
Mediterranean familial fever (a recurrent polyserositis
mainly affecting the peritoneum) who was aged 24 years;
the other three patients were aged more than 50 years.
Obviously, our case series is limited in number, but the
fact that all patients do not come from tropical or
subtropical countries leaves open the possibility regarding
the origin of the countries.
The phisiopatology of EPS is based on alteration of the
intestinal functions associated to the reabsorptive
functions. This fibrotic process may cause a reduction in
motility, up to ileus, encapsulation and the destruction of
the myenteric plexus [24].
Table 2 Mean characteristics of both group of the patients: primary and secondary SEP
Symptoms of presentation at emergency
1 Indian
1 Egyptian
1 Nepali No comorbidities
33 years mean age (30–36)
1 pt abdominal pain
3th no previous attack
1 pt Spigelian hernia
2 pts increased slightly
1 pt not reported
3 males, 1 female
53,5 mean age (24–72)
2 Egiptian
1 Sudani
3pts CKD with PD
1 pt Mediterranean fever
3pts abdominal pain, nausea, vomiting, constipation
1 pt abdominal pain and anorexia
2 pts previous attack but not specified the time
4 pts general intestinal occlusion
3 pts increased slightly
3pts encasement of entire small bowel
1 pt excision of membranes, adhesiolisis and RH
2 pts encasement of entire small bowel
1 pt encasement of entire small bowel, an cecum
3 pts excision of membranes and adhesiolisis
3 pts exicision of membranes and adhesiolisis
1 pt Early post operative small bowel obstruction
Nb number, Pts patients, CKD Chronic Kidney Disease, PD peritoneal dialysis, WBC White Blood Cells, CT Computed Tomography, MOF Multi Organ Failure
The preeminent clinical signs of this disease are
abdominal pain, nausea, vomiting and occasional constipation.
Recurrent episodes of peritonitis, with negative culture,
spontaneously regressed, in association with anemia, low
albumin and high C-reactive protein, can be found in
case of EPS [15]. These are non-specific signs of acute
Complete encasement of the whole intestine and other
orgen like appendix, ascending colon cecum, ovaries by
a fibrocollagenous membrane.
abdominal obstruction, but clinically can help the past
medical history. In fact, all of these patients, as in our
case series, had previous attacks of colic pain,
demonstrating that the majority of patients have a repetitive
chronic symptomatology. This can happen for many
years before the right diagnosis is achieved. In patients
with primary EPS, the positive anamnesis for several colic
pain occurrences in the past is the only sign that can help.
In contrast, in secondary EPS, the previous attack of colic
pain in association with the risk factors can be more useful
in formulating the clinical diagnosis.
In effect, because the disease is very rare, the correct
diagnosis with radiological tools depends both on the
armamentarium and the skillfulness of the radiologist.
The most important signs are the thickening of the
peritoneum, bowel encapsulation, intestinal obstruction,
presence of cocoon, and detection of calcification. X-Ray
examination may show air fluid levels and bowel
obstruction in association with abdominal calcifications, but all
these signs are not sufficient to diagnose EPS [25]. A CT
scan is the most useful in establishing a preoperative
diagnosis. The appearance of a conglomeration of all small
bowel loops encased by a capsule dense with contrast free
in the periphery can be considered characteristics of this
disease using a CT scan (Fig. 1) The contrast-enhanced
CT may have a sensitivity of 100% and a specificity of 94%
for diagnosing EPS [26]. Bowel loops collected into the
centre of the abdomen as a sign of adhesions, enhanced
thickened peritoneum with calcifications [27] and
lobulated ascites in the omentum or between the bowel loops
are the signs shown by Magnetic Resonance Imaging [28].
Surprisingly, in our case series the correct diagnosis was
made in only two cases of primary EPS. In contrast, all the
patients of the secondary EPS, (that had more clinical
helping factors) had only a generic intestinal occlusion
diagnosis. An MRI was reported only one time, and the result
was considered equal to the CT scan [29]. Ultrasonography
cannot help in the specific diagnosis; they can only permit
a generic diagnosis of abdominal occlusion [2].
The histopathology of this disease is not pathognomonic,
and a diagnosis after the resected specimen is still achieved
in concomitance to the clinical and radiological findings.
There is no consensus about the treatment of EPS.
Patients with mild abdominal pain could be treated
conservatively as long as the symptoms regress with
nasogastric tube decompression, bowel rest and nutritional
support [6]. These patients usually have a malnutrition
status that reflects the chronicity of the disease. Total
parenteral nutrition does not have any curative effect and it
have to be used in patient to restore the nutritional status
especially before surgery [30]. Additionally, continuous
attacks of abdominal pain can result in patients’
malnutrition because of a limitation of food intake as a result of
nausea and vomiting. This also reflects a poor quality of
life, especially as in our young patient, who was affected
by familial Mediterranean fever in which the colicky
attacks are present for 9 years. A special case of secondary
EPS can be treated with steroids, tamoxifen or sirolimus
[31]. Surgical treatment has improved in the last decades.
Peritonectomy and careful lysis with resection of the
peritoneum and fibrous tissue, in association with separation
of adhesions to release the bowel, represents the treatment
of choice. Post operative mortality ranges from 19 to
34.5%, [32] with recurrence rate at around 25%. Some
Authors have used the Noble plicature with a decrease
in the recurrence rate to 12,3% [33].
An immediate early postoperative small bowel
obstruction can be recorded in the immediate post-operative
period because a long operative dissection of the loops
frequently results in edema. This very early post-operative
complication represents a very difficult reoperation for the
patient [34] and should be treated by bowel rest and
parenteral nutrition. The use of somatostatin, in association
with a low dose of steroid, has been suggested for
treatment of this early complication [23]. Additionally,
intraoperative stenting of the intestinal loops has been suggested
to improve post-operative results and avoid the previously
listed complications [23].
In our experience patients have been operated as soon
as possible. In fact, the disease does not regress and the
quality of life of patients can be poor in relation to the
intensity and frequency of the attacks. Furthermore,
patients having attacks for many years who have not
submitted to surgery can have a more difficult adhesive
situation that increases the morbidity and mortality as
reported in our patients. An incidental appendectomy
is suggested by some authors to avoid a difficult
appendectomy if the patient developed acute appendicitis
[35] later on. All our patients were treated surgically
with the excision of all membranes (Fig. 2) and
adesiolysis (Fig. 3).
Conclusions
Currently, the correct identification of the form of EPS
and PE is more easily possible than in the past, but the
diagnosis is still a challenge. In our opinion, surgery has
to be done as soon as possible to avoid a poor quality of
life with recurrent episodes of occlusion and difficult
adhesions that can cause morbidity and mortality.
Availability of data and materials
Data supporting the present findings can be obtained, if needed, after getting
permission from the Hamad Medical Corporation. A waiver of consent was
granted for this study as there was no direct contact with patients and all data
were retrieved retrospectively under full confidentiality to protect patients’ privacy.
Authors’ contributions
HA, IDC: Study conception and design. OAY, SM: Acquisition of data. AD,
ANS, AT: Analysis and interpretation of data. SA, MK, AT: Drafting of
manuscript. IDC: Critical revision of manuscript. All authors read and
approved the final manuscript.
Ethics approval and consent to participate
This retrospective study was approved with the ethical board of Hamad
General Hospital (Hamad Research Center), and was conducted in accordance
with the Declaration of Helsinki.
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