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Surgical Endoscopy (2019) 33:691–704
https://doi.org/10.1007/s00464-018-6490-8
REVIEW ARTICLE
Clinical response afterlaparoscopic fenestration ofsymptomatic
hepatic cysts: asystematic review andmeta-analysis
LucasH.P.Bernts1· SebastiaanG.Echternach1· WietskeKievit2· CamielRosman3· JoostP.H.Drenth1
Received: 31 May 2018 / Accepted: 11 October 2018 / Published online: 17 October 2018
© The Author(s) 2018
Abstract
Background Laparoscopic fenestration is one of the treatment options for symptomatic hepatic cysts, either solitary or in
context of polycystic liver disease (PLD), but indications, efficacy and surgical techniques are under debate.
Methods A systematic literature search (1950–2017) of PubMed, Embase, Web of Science and the Cochrane Library was
performed (CRD42017071305). Studies assessing symptomatic relief or symptomatic recurrence after laparoscopic fenes-
tration in patients with symptomatic, non-parasitic, hepatic cysts were included. Complications were scored according to
Clavien–Dindo. Methodological quality was assessed by Newcastle–Ottawa scale (NOS) for cohort studies. Pooled estimates
were calculated using a random effects model for meta-analysis.
Results Out of 5277 citations, 62 studies with a total of 1314 patients were included. Median NOS-score was 6 out of 9.
Median follow-up duration was 30months. Symptomatic relief after laparoscopic fenestration was 90.2% (95% CI 84.3–94.9).
Symptomatic recurrence was 9.6% (95% CI 6.9–12.8) and reintervention rate was 7.1% (95% CI 5.0–9.4). Post-operative
complications occurred in 10.8% (95% CI 8.1–13.9) and major complications in 3.3% (95% CI 2.1–4.7) of patients. Proce-
dure-related mortality was 1.0% (95% CI 0.5–1.6). In a subgroup analysis of PLD patients (n = 146), symptomatic recurrence
and reintervention rates were significantly higher with respective rates of 33.7% (95% CI 18.7–50.4) and 26.4% (95% CI
12.6–43.0). Complications were more frequent in PLD patients, with a rate of 29.3% (95% CI 16.0–44.5).
Conclusions Laparoscopic fenestration is an effective procedure for treatment of symptomatic hepatic cysts with a low symp-
tomatic recurrence rate. The symptomatic recurrence rate and risk of complications are significantly higher in PLD patients.
Keywords Hepatic cysts· Polycystic liver disease· Laparoscopic fenestration· Clinical outcomes
Simple hepatic cysts are fluid-filled cavities that arise from
malformations of the ductal plate during embryonic devel-
opment. Simple hepatic cysts are a relatively common
finding as it is estimated to be present in 2.5–18% of the
general population [1, 2]. The presence of multiple cysts,
arbitrarily > 10, is defined as polycystic liver disease (PLD)
[3] and is usually part of the phenotype of two inherited
disorders: autosomal dominant polycystic kidney disease
(ADPKD) or autosomal dominant polycystic liver dis-
ease (ADPLD). Regardless of underlying pathology, these
patients are at risk to develop large cysts, arbitrarily defined
as > 5cm in diameter. Large cysts may cause symptoms
such as pain, loss of appetite, early satiety, nausea or dysp-
nea, sometimes causing a considerable decrease in quality of
life [3, 4]. As such, treatment of large symptomatic cysts is
indicated. Treatment options for large cysts comprise lapa-
roscopic fenestration, also termed laparoscopic deroofing
or unroofing, and percutaneous aspiration sclerotherapy [5].
Laparoscopic fenestration combines cyst fluid aspira-
tion, followed by excision of extra-hepatic cyst wall in a
single laparoscopic procedure. The surgical approach of
large hepatic cysts has gained popularity since the 1990s,
especially after the introduction of laparoscopy. As usual
and Other Interventional Te
chniques
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s0046 4-018-6490-8) contains
supplementary material, which is available to authorized users.
* Joost P. H. Drenth
joostphdrenth@cs.com
1 Department ofGastroenterology andHepatology,
Radboudumc, P.O. Box9101, 6500HBNijmegen,
TheNetherlands
2 Department forHealth Evidence, Radboudumc, Nijmegen,
TheNetherlands
3 Department ofSurgery, Radboudumc, Nijmegen,
TheNetherlands
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692 Surgical Endoscopy (2019) 33:691–704
1 3
in surgical practice, operative treatment has been gradually
adopted in routine clinical care without valid comparison.
Multiple cohort studies, however, suggest that laparoscopic
fenestration is effective and safe in selected populations.
Some surgeons routinely apply omentopexy (also termed
omentoplasty, omental transposition or greater omentum
flap), a procedure that applies omental tissue in the residual
cyst cavity to prevent symptomatic recurrence. The merits
and risks of omentopexy over and beyond mere laparoscopic
fenestration are unexplored.
Percutaneous aspiration sclerotherapy is an alternative
approach that percutaneously places a pigtail catheter in
the cyst cavity to evacuate hepatic cyst fluid. After com-
plete drainage, a sclerosing agent (e.g. ethanol, tetracycline,
polidocanol) is injected in the cyst which destroys the inner
epithelial lining resulting in regression of the cyst. A recent
clinical guideline suggests that symptomatic simple hepatic
cysts may better be managed with laparoscopic fenestration
rather than percutaneous aspiration sclerotherapy with the
restriction of low quality of evidence [6]. It is imperative to
quantify the benefits and risks of laparoscopic fenestration
and to grade the evidence on this topic.
The purpose of this study was therefore to assess the effi-
cacy and safety of laparoscopic fenestration using a system-
atic review of the literature. The primary goal of treatment is
alleviation of clinical symptoms, hence our focus on cohort
studies and clinical trials that assessed symptomatic relief
or symptomatic recurrence. We aim to give a comprehen-
sive summary of reported efficacy and safety rates of laparo-
scopic fenestration to aid in clinical decision-making when
faced with symptomatic hepatic cysts.
Materials andmethods
We conducted a systematic review of studies that evaluated
the efficacy of laparoscopic fenestration for symptomatic
simple hepatic cysts. This study was reported according to
the Preferred Reporting Items for Systematic Reviews and
Meta-Analyses (PRISMA) guidelines [7] and the Meta-anal-
ysis of Observational Studies in Epidemiology (MOOSE)
checklist [8] (Supplementary File 1). The study protocol was
registered in the Prospero database of systematic reviews
(CRD42017071305) on 10 July 2017.
Eligibility criteria
We included cohort studies and clinical trials of adult
patients with one or more simple (non-parasitic, non-neo-
plastic) and symptomatic hepatic cysts (excluding chole-
dochal cysts or hepatic foregut cysts), either solitary or
in context of PLD, that underwent laparoscopic surgery
with minimal resection of healthy liver parenchyma (e.g.
fenestration, deroofing, unroofing). We included studies that
assessed symptomatic relief and/or symptomatic recurrence.
We excluded case reports, overlapping datasets, reviews,
unpublished data and conference abstracts. We excluded
studies with a mean or median follow-up < 6months. For
practical reasons, only articles in the following languages
were included: Dutch, English, French, German, Italian and
Spanish.
Literature search strategy
We systematically searched the electronic databases of Pub-
Med MEDLINE, Embase, Web of Science and the Cochrane
Library from inception to 18 July 2017, without any restric-
tions. The search strategy combined terms related to hepatic
cysts and laparoscopic interventions. The search terms were
composed in collaboration with an experienced medical
librarian. Exact search terms are presented in Supplemen-
tary File 2. If no full-text article was available, the original
authors were emailed in order to gain access. References of
included studies were checked for additional studies missed
in the primary search. All identified records were exported
to citation management program EndNote X8 (Clarivate
Analytics, Philadelphia, PA, USA) for deduplication, which
was performed according to a published protocol [9]. After
deduplication, all records were exported to the browser-
based systematic review management program Covidence
(Veritas Health Innovation, Melbourne, Australia. Avail-
able at http://www.covid ence.org). First, two investigators
(LB and SE) independently screened title and abstract to
determine the eligibility of each study. Second, the full-text
of all included abstracts was independently assessed by the
same investigators. Disagreements in both screening phases
were resolved through discussion between the two investiga-
tors. Any remaining disagreement between reviewers was
resolved through discussion with a third reviewer (CR, JD).
Data extraction
All data were extracted using standardised forms by one
investigator (LB). Cases of uncertainty about data extrac-
tion were resolved through discussion between two inves-
tigators. Original data of four studies were requested by
email. One author was able to send the additional data
required for inclusion [10]. Data extraction was checked
for errors by random sampling of 10% of included studies
by a second investigator (SE), which did not show any
errors. Our primary outcomes were symptomatic relief
(i.e. full or partial symptomatic relief) directly after sur-
gery and symptomatic recurrence (recurrent symptoms
with refilling or recurrent symptoms without confirma-
tion of refilling on imaging) during long-term follow-up.
Secondary outcomes were study characteristics, patient
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693Surgical Endoscopy (2019) 33:691–704
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characteristics, reintervention rates, operative time, hospi-
tal stay, conversion to laparotomy and surgical technique.
Reported rates of procedure-related complications and
mortality were extracted. Reported post-operative com-
plications were scored according to the Clavien–Dindo
classification [11] by one investigator (LB). Grade I and
II were regarded as minor complications and grade III, IV
and V as major complications.
Risk ofbias assessment
We used the Newcastle–Ottawa scale for cohort stud-
ies to assess the risk of bias within individual studies.
Adaptations were made a priori to make the scale more
specific for our research question (Supplementary File 3).
Using this scale, studies were scored on selection of study
groups, the inclusion of a control group, the comparability
of groups and the ascertainment of outcome of interest.
Studies were independently scored by two investigators
(LB, SE). Disagreements were resolved through discussion
between two investigators.
Data synthesis andanalysis
For meta-analysis of reported rates, pooled estimates and
95% confidence intervals (CI) were calculated using a ran-
dom effects model for meta-analysis of prevalence, using
MetaXL 5.2 (EpiGear, Sunrise Beach, Australia. Available
at http://www.epige ar.com). When comparing means, not
overlapping 95% CI were considered significant. When com-
paring medians, p value was calculated with Mann–Whitney
test in GraphPad Prism 5 (GraphPad Software, La Jolla, CA,
USA), p < 0.05 was considered significant.
Heterogeneity for pooled estimates was assessed using
the I2 statistic, which describes the percentage of total vari-
ation across studies that is due to heterogeneity rather than
chance. As we included a large number of studies, Cochran’s
Q and p values are less practical for assessing heterogeneity
[12]. Low, moderate and high heterogeneity was defined as
an I2 value above 25%, 50% or 75%, respectively [12]. All
I2 values were calculated with MetaXL.
Publication bias was assessed by generating funnel plots,
where the standard error is plotted against the double arc-
sine transformed prevalence estimates of individual studies.
Likelihood of publication bias was quantified using the Luis
Furuya-Kanamori asymmetry index (LFK-index). An LFK-
index within 1 or − 1 indicates no asymmetry. An LFK-index
exceeding 1 or − 1 but within 2 or − 2 indicates minor asym-
metry. An LFK-index exceeding 2 or − 2 indicates major
asymmetry [13]. LFK-indices and funnel plots were gener-
ated with MetaXL.
Subgroup analyses
Potential causes of heterogeneity, as such influences on
pooled estimates, were investigated by performing pre-
specified subgroup analyses of underlying disease, different
surgical techniques, study design, publication date and fol-
low-up duration. Subgroups of non-categorical parameters
were made by splitting included studies into two groups: 1:
equal or below the median and 2: above the median.
All figures were made with Microsoft PowerPoint 2007
(Microsoft Corporation, Redmond, WA, USA) and Graph-
Pad Prism 5.
Results
Systematic search
The systematic search identified 5278 citations. Ulti-
mately, 62 studies were included for this systematic review
(Fig.1A). Citations are presented in the supplementary files.
Study characteristics
The 62 included studies comprising a total of 1314 patients
(Table1). Studies from 5 different continents were included
and most included studies were performed in Europe
(Fig.1B). The median number of patients per study was
17 (total range 3–66). Of all included studies, 5 were pro-
spective cohort studies, 10 were retrospective analyses of
prospectively collected data, 28 were retrospective cohort
studies and 19 studies did not give an explicit statement on
data collection. Publication dates ranged from 1994 to 2017.
Study periods ranged between 1982 and 2015 (Fig.2G).
Median follow-up duration was 30months (IQR 19–48)
(Fig.2A).
Of all included patients, 74% was female and 33% had
PLD. Median age at time of operation was 58.7years (IQR
54.5–62.0) (Fig.2B). Average preoperative cyst diameter
was 11.9cm (95% CI 11.1–12.7) (Fig.2C). In 10 studies
that did not exclusively operate on solitary cysts, median
number of treated cysts was 1.4 (IQR 1.3–2.0; total range
1.2–37.7). Individual study results are presented in Supple-
mentary File 4A–B.
Efficacy
There were 27 studies that reported the proportion of
patients with full or partial symptomatic relief after surgery.
Symptomatic relief was based on clinical follow-up data in
25 studies, on a structured telephone interview in one study
[14] and on a specific questionnaire in another study [15].
Pooled symptomatic relief was 90.2% (95% CI 84.3–94.9).
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694 Surgical Endoscopy (2019) 33:691–704
1 3
Symptomatic recurrence during follow-up was 9.6% (95% CI
6.9–12.8). The rate of reintervention for the same cyst was
7.1% (95% CI 5.0–9.4) (Table2). Mean time until sympto-
matic recurrence was 16.1months in 10 patients. Mean time
until reintervention was 22.1months in 13 patients.
Safety
Conversion from laparoscopic to open surgery during the
procedure was necessary in 4.5% (95% CI 3.2–6.0), typically
because of intra-operative bleeding, difficult positioning or
extensive adhesions. Median hospital stay was 5.0days
(IQR 3.7–6.0) (Fig.2D). Post-operative complication rate
was 10.8% (95% CI 8.1–13.9), generally consisting of
either bile leakage, ascites, pleural effusion or infections.
Out of 136 reported post-operative complications, 115
could be scored according to the Clavien–Dindo classifica-
tion (Fig.2F). Of scored complications, 71.3% were minor
and 28.7% were major. Overall, the pooled estimate of hav-
ing a major complication after surgery was 3.3% (95% CI
Fig. 1 A PRISMA diagram.
Flow chart representing lit-
erature search and elements of
systematic review (identification
and screening). B Illustrative
schematic of country of origin
of included studies. The number
of inclusions per continent is
shown
10
6
33
2
0
Database search (18-7-2017)
n = 5277
PubMed: 1513
Embase: 2457
Web of Science: 1181
Cochrane Library: 0126
Records after duplicates
removed
n = 2936
Additional records identified
through cross-referencing
n = 1
Screening of title
and abstract
n = 2937
Full-text assessment
n = 248
Studies included for
review
n = 62
Records excluded:
n = 186
Reasons:
- Conference abstract (35)
- Review (28)
- No full-text available (27)
- Double patient data (24)
- Language (22)
- Wrong intervention (21)
- Wrong outcome (12)
- Duplicates (6)
- Commentary (4)
- Case report (3)
- Wrong population (2)
- Follow-up <6 months (2)
Idenficaon
Screening
Records excluded:
n = 2689
11
A
B
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695Surgical Endoscopy (2019) 33:691–704
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2.1–4.7). The pooled estimate of procedure-related mortality
was 1.0% (95% CI 0.5–1.6) (Table2). This was based on a
single patient from a series of 9 patients [16]. The patient
presented with severe PLD symptoms. After an uneventful
in-hospital stay, acute renal insufficiency ensued 20 days
after discharge, followed by hepatorenal failure. The patient
succumbed 15 days later. Other studies showed no proce-
dure-related mortality.
Operative technique
Median operative time was 83.5 min (IQR 72–120)
(Fig.2E). The use of omentopexy was explicitly mentioned
in 31 studies that included a total of 824 patients. The
pooled estimate for use of omentopexy was 14.8% (95% CI
5.8–26.6), with a total range from 0 to 100% between stud-
ies. The use of concomitant cholecystectomy was mentioned
in 37 studies that included a total of 822 patients. In 21.5%
(95% CI 15.8–27.8) of patients, concomitant cholecystec-
tomy was performed; cited reasons were gallstones on image
studies or cyst location adjacent to the gallbladder.
Risk ofbias
An evaluation of the quality of individual studies is pre-
sented in Table3, which provides details of risk of bias
within studies, as reflected by adjusted Newcastle–Ottawa
Scale (NOS) scoring. Overall, median score for ‘selection of
study groups’ was 3 out of 4; median score for ‘comparabil-
ity of groups’ was 0 out of 2 and median score for ‘ascertain-
ment of outcome of interest’ was 3 out of 3. Median of the
total NOS-score was 6 out of 9.
Table 1 Summary of included studies
# First author Year Np
1 Ammori 2002 3
2 Andriani 2000 17
3 Ardito 2013 47
4 Bai 2007 44
5 Caetano 2006 12
6 Cappellani 2002 9
7 De Reuver 2017 35
8 Debs 2016 27
9 Descottes 2000 15
10 Diez 1998 10
11 Emmermann 1997 18
12 Fabiani 2005 26
13 Faulds 2010 5
14 Fiamingo 2003 15
15 Gall 2009 61
16 Gamblin 2008 46
17 Gigot 2001 19
18 Gocho 2013 6
19 Hansen 1997 19
20 Hansman 2001 6
21 Heintz 1995 3
22 Hsu 2005 5
23 Kabbej 1996 13
24 Kamphues 2011 43
25 Katkhouda 2000 25
26 Kisiel 2017 48
27 Koea 2008 24
28 Konstadoulakis 2005 9
29 Koperna 1997 10
30 Kornprat 2004 21
31 Kwon 2003 14
32 Lee 2014 29
33 Lolle Noerregaard 2014 29
34 Manterola 2016 41
35 Marks 1998 17
36 Martin 1998 20
37 Martinez-Perez 2016 12
38 Maruyama 2013 16
39 Mazoch 2011 15
40 Mazza 2009 66
41 Morino 1994 11
42 Neri 2006 15
43 Palanivelu 2006 27
44 Pante 2014 7
45 Petri 2002 34
46 Regev 2001 18
47 Robinson 2005 11
48 Roesch Dietlen 1999 7
49 Sasi Szabo 2006 25
50 Schachter 2001 14
Last name of first author, year of publication
Np number of included patients per study
Table 1 (continued)
# First author Year Np
51 Scheuerlein 2013 47
52 Sendt 2009 27
53 Tagaya 2003 5
54 Tan 2005 10
55 Tocchi 2002 8
56 Torices 2004 21
57 Torres 2009 13
58 Treckmann 2010 42
59 Van Keimpema 2008 12
60 Wahba 2011 23
61 Wu 2014 30
62 Zacherl 2000 7
Total 1994–2017 1314
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696 Surgical Endoscopy (2019) 33:691–704
1 3
Heterogeneity
Pooled estimates of outcomes were assessed for heterogene-
ity and publication bias. The I2 value for symptomatic relief
was 72%, for symptomatic recurrence 68%, for reinterven-
tion 50%, for complications 62%, indicating moderate het-
erogeneity. The I2 value for intra-operative conversions and
for mortality was 0%, indicating negligible heterogeneity.
Publication bias
LFK-index for reintervention was 0.91, for complications
0.42 and for intra-operative conversions 0.19, indicat-
ing no asymmetry. LFK-index for symptomatic relief was
− 1.09, for symptomatic recurrence 1.11, indicating minor
asymmetry. LFK-index for mortality was 2.87, indicating
major asymmetry. Funnel plots are shown in Fig.3.
Subgroup analyses
Polycystic liver disease
We performed a subgroup analysis of 15 studies that
included only PLD patients or reported outcomes of PLD
patients separately and compared these to the overall
results (Table2). Symptomatic recurrence and reinter-
vention rates were significantly higher with respective
rates of 33.7% (95% CI 18.7–50.4) and 26.4% (95% CI
12.6–43.0). Post-operative complications were more fre-
quent in PLD patients with a pooled estimate of 29.3%
AB C
EF G
D
Fig. 2 A–E Analysis of continuous data: reported medians and
means, Ns, number of studies. For reported means, the vertical line
represents the median of means. C Preoperative cyst size, diameter in
centimetres. F Scoring of post-operative complications according to
Clavien–Dindo. G Timeframes wherein patients were included (study
periods) are shown per study, sorted chronologically on first inclusion
Table 2 Overall versus PLD
outcomes
Asterisk (*): statistically significant difference
PLD polycystic liver disease, Ns number of studies, Np number of patients, PE pooled estimate, CI confi-
dence interval
Outcome Ns Overall PLD
NpPE (%) 95% CI I2 (%) NsNpPE (%) 95% CI I2 (%)
Recurrence 62 1314 9.6 6.9–12.8 68 15 146 33.7* 18.7–50.4 76
Reintervention 56 1176 7.1 5.0–9.4 50 10 109 26.4* 12.6–43.0 69
Complications 60 1276 10.8 8.1–13.9 62 13 129 29.3* 16.0–44.5 69
Major 56 1106 3.3 2.2–4.7 27 13 129 7.2 2.1–14.6 46
Conversions 44 889 4.5 3.2–6.0 0 9 83 8.2 3.2–15.0 0
Mortality 60 1271 1.0 0.5–1.6 0 13 135 2.3 0.4–5.6 0
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697Surgical Endoscopy (2019) 33:691–704
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(95% CI 16.0–44.5) (Fig.4A). Out of 37 reported post-
operative complications, all could be scored according
to Clavien–Dindo. Of scored complications, 70.3% were
minor and 29.7% were major. Overall, the pooled estimate
of having a major complication after surgery was 7.2%
(95% CI 2.1–14.6). Conversion rate and procedure-related
mortality did not differ significantly from overall results.
Data were insufficient to analyse symptomatic relief in the
PLD subgroup.
Omentopexy
For analysis of the effect of omentopexy on symptomatic
recurrence rates, 31 studies that specified the use of omen-
topexy were split into two groups. As the median of addi-
tional omentopexy was 0%, studies were split accordingly.
Group 1: no omentopexy performed. Group 2: omentopexy
performed in 1 or more patients (total range 11–100%). For
group 1, pooled symptomatic recurrence was 8.7% (95%
Table 3 Risk of bias assessment
(NOS)
Color coding: 01234
Author S. C. O. ScoreAuthor S. C. O. Score
0–40–2 0–30–9 0–40–2 0–30–9
Ammori 3 0 36Lee 3 0
36
Andriani 3 0 25Lolle Noerregaard 3 0
25
Ardito 2 0 35Manterola 2 0
35
Bai 3 0 25Marks 3 0
14
Caetano 3 0 25Marn 3 0
36
Cappellani 3 0 36Marnez-Perez 3 0
36
De Reuver 3238Maruyama 2 0
35
Debs 3 0 25Mazoch 3 0
25
Descoes 2 0 35Mazza 3 0
36
Diez 3 0 25Morino 3 0
25
Emmermann 3 0 36Ner 3 0
36
Fabiani 3 0 25Palanivelu 3 0
36
Faulds 3 0 25Pante 2 0
35
Fiamingo 3 0 36Petri 2 0
24
Gall 3 0 14Regev 2 0
35
Gamblin 3 0 36Robinson 3 0
36
Gigot 3 0 36Roesch Dietle 3 0
36
Gocho 3 0 36Sasi Szabo 3 0
36
Hansen 3 0 36Schachter 3 0
25
Hansman 2 0 24Scheuerlein 3 0
36
Heintz 3 0 25Sendt 3 0
36
Hsu 3 0 25Tagaya 3 0
36
Kabbej 3 0 36Tan 3 0
36
Kamphues 3 0 25Tocchi 3 0
36
Katkhouda 3 0 36Torices 3 0
36
Kisiel 3 0 14Torres3 0
36
Koea 3 0 36Treckmann 3 0
25
Konstadoulakis 3 0 36Van Keimpema 3 0
25
Koperna 3 0 36Wahba 3 0
25
Kornprat 3 0 36Wu 2 0
35
Kwon 3 0 36Zacherl 3 0
36
Median 30
36
NOS Newcastle–Ottawa Scale, S selection of the study groups, C the comparability of the groups, O
ascertainment of outcome of interest, Score total NOS-Score
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698 Surgical Endoscopy (2019) 33:691–704
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CI 3.4–16.0). For group 2, it was 5.7% (95% CI 3.0–9.3).
In addition, we assessed the effect of omentopexy on post-
operative complication rates in the same groups. For group
1, pooled complication rate was 8.4% (95% CI 5.2–12.2).
For group 2, it was 11.0% (95% CI 5.8–17.5). In summary,
there were no significant differences in pooled estimates
of symptomatic recurrence rates and complication rates
between groups. Data were insufficient to correct for cyst
location and cyst size. (Fig.4B–D).
Concomitant cholecystectomy
For analysis of the effect of concomitant cholecystectomy
on symptomatic recurrence rates, 37 studies that specified
the use of cholecystectomy were split into two groups. As
the median proportion of patients that underwent additional
cholecystectomy was 18.2%, studies were divided accord-
ingly. Group A: cholecystectomy in 18.2% of patients or
less (total range 0–18.2%). Group B: cholecystectomy in
Fig. 3 Funnel plots of meta-
analysis outcomes. The mod-
elled standard error is plotted
against the double arcsine trans-
formed estimates of individual
studies. Luis Furuya-Kanamori
asymmetry index (LFK-index)
is also shown
Double Arcsin Rate
32
Standard error
Standard error
Standard error
Standard error
Standard error
Standard error
0,55
0,5
0,45
0,4
0,35
0,3
0,25
0,2
0,15
Double Arcsin Rate
10
0,55
0,5
0,45
0,4
0,35
0,3
0,25
0,2
0,15
Double Arcsin Rate
210
0,55
0,5
0,45
0,4
0,35
0,3
0,25
0,2
0,15
Double Arcsin Rate
10
0,55
0,5
0,45
0,4
0,35
0,3
0,25
0,2
0,15
Double Arcsin Rate
210
0,55
0,5
0,45
0,4
0,35
0,3
0,25
0,2
0,15
Double Arcsin Rate
10
0,55
0,5
0,45
0,4
0,35
0,3
0,25
0,2
0,15
Symptomatic Relief
LFK-index:-1.09
Symptomatic Recurrence
LFK-index:1.11
Mortality
LFK-index:2.87
Complications
LFK-index:0.42
Re-intervention
LFK-index:0.91
Conversions
LFK-index:0.19
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699Surgical Endoscopy (2019) 33:691–704
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more than 18.2% of patients (total range 21–80%). For
group A, pooled symptomatic recurrence was 9.3% (95%
CI 6.0–13.3). For group B, it was 7.3% (95% CI 3.0–13.3).
Next, we focused on the effect of concomitant cholecys-
tectomy on post-operative complication rates in the same
groups. For group A, pooled complication rate was 9.1%
(95% CI 5.0–14.2). For group B, it was 7.6% (95% CI
3.5–12.9). These data are consistent with the absence of
significant differences in pooled estimates of symptomatic
recurrence rates and complication rates between groups
(Fig.4F–H).
Follow-up duration
We were interested in the effect of prolonged follow-up on
symptomatic recurrence rates. To this end, we selected 27
studies that specified mean follow-up and distinguished
into two groups. The median of reported mean follow-up
duration was 30months, and we categorised studies in two
groups accordingly. Group I: mean follow-up duration of
30months or less (total range 6–30months). Group II: mean
follow-up duration of more than 30 months (total range
36–86.4). For group I, pooled symptomatic recurrence was
11.5% (95% CI 5.2–19.7). For group II, it was 6.8% (95% CI
1.9–13.9). Thus, there was no significant effect of length of
follow-up after six months on reported symptomatic recur-
rence rates (Fig.4E).
Publication date
Publication dates ranged between 1994 and 2017, with the
year 2005 as the median. Pooled symptomatic relief for
studies published from 1994 to 2005 was 90.4% (95% CI
84.0–95.4), and for studies published from 2006 to 2017 it
was 92.2% (95% CI 82.0–98.7). Symptomatic recurrence
for studies published from 1994 to 2005 was 9.8% (95% CI
5.9–14.6) and for studies published from 2006 to 2017 it was
9.1% (95% CI 4.4–13.5). Next, we assessed the effect of pub-
lication date on conversion rates. In studies published from
1994 to 2005, the pooled conversion rate was 6.8% (95%
CI 4.3–9.8) and for studies published from 2006 to 2017 it
was 3.4% (95% CI 2.1–5.0). It must be noted that there were
four studies with a conversion rate of 10% or higher and all
were published before 2006 [16–19]. In studies published
from 1994 to 2005, the pooled complication rate was 12.4%
(95% CI 8.2–17.4) and for studies published from 2006 to
AB CD E
FGHI J
KLMN O
Fig. 4 Subgroup analyses. Ns: number of studies. Np: number of
patients. Interrupted lines: pooled estimates. Error bars: 95% confi-
dence intervals. A Outcomes for the polycystic liver disease (PLD)
subgroup and overall results. B Percentage of patients that underwent
omentopexy per included cohort. C, D Outcomes for omentopexy
subgroups (Group 1: no omentopexy, Group 2: omentopexy). E Out-
comes for mean follow-up subgroups (Group I: ≤38 months, Group
II: >38 months). F Percentage of patients that underwent concomi-
tant cholecystectomy per included cohort. G, H Outcomes for con-
comitant cholecystectomy subgroups (Group A: ≤ 21.5%, Group B:
> 21.5%). I–L Outcomes for publication year subgroups (1994–2005
and 2006–2017). M–O Outcomes for data collection subgroups (pro-
spective and retrospective)
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700 Surgical Endoscopy (2019) 33:691–704
1 3
2017 it was 9.9% (95% CI 6.4–14.1). In studies published
from 1994 to 2005, the median hospital stay was 5.3days
(IQR 4.0–6.3). In studies published from 2006 to 2017, the
median hospital stay was 4.7days (IQR 3.5–5.7), medians
were not significantly different (p = 0.23). We can conclude
that there were no significant effects of publication date on
outcomes (Fig.4I–L).
Data collection
To assess the effect of original study design on our primary
outcomes, we performed a subgroup analysis on 15 studies
that performed data collection prospectively and 27 studies
that did retrospectively. In the prospective subgroup, sympto-
matic relief was 95.3% (95% CI 86.8–100.0%), symptomatic
recurrence was 7.9% (95% CI 3.0–14.8) and complication
rate was 6.9% (95% CI 3.0–12.2). In the retrospective sub-
group, symptomatic relief was 88.9% (95% CI 79.1–96.1),
symptomatic recurrence was 12.5% (95% CI 8.3–17.4) and
complication rate was 9.6% (95% CI 6.8–12.9). We can state
that there were no significant effects of data collection on
outcomes (Fig.4M–O).
Discussion
Efficacy andsafety
This systematic review describes the safety and efficacy of
laparoscopic fenestration in 1314 patients reported in 62
individual studies. We document that laparoscopic fenes-
tration of large, symptomatic cysts is effective and results in
symptomatic relief in the large majority of patients. Symp-
tomatic recurrence after fenestration is low (9.6%) as is the
reintervention rate for the same cyst (7.1%). Omentopexy
after cyst fenestration did not improve efficacy, but also was
not associated with a higher complication rate.
Laparoscopic fenestration appears to be a safe procedure
and while procedure-related complications do occur in 11%
of patients, scoring according to Clavien–Dindo shows that
these are mostly minor and amenable to treatment. We were
unable to assess the relation between pre-surgical cyst size,
complication rate and recurrence rate. Concomitant chol-
ecystectomy is feasible, but does not contribute to the overall
success of the procedure but similarly does not result in a
higher complication rate.
The average interval between surgery and symptomatic
recurrence was 16months, and mean time until reinterven-
tion was 22months. This interval should be interpreted very
carefully because of the small sample size, but underscores
the need for long-term follow-up when investigating cyst
recurrence in future studies.
Patients with PLD may possess one or more large cysts
against the background of multiple smaller cysts in sur-
rounding liver. Symptoms in PLD may be attributed to
these large cysts and it may be tempting to perform lapa-
roscopic fenestration here. We found that this subgroup
is at a high risk for complications and that long-term
symptomatic relief is less well achieved. Potential causes
of the elevated risk of complications are the changes in
hepatic anatomy in PLD and the use of extensive fenes-
tration, with some studies fenestrating over 30 cysts per
patient [16, 20]. The elevated recurrence rate is probably
related to the different natural history of PLD and large
solitary cysts. Hepatic cysts, regardless whether they are
solitary or multiple, arise as a result from inactivation of
2 alleles from PLD genes. PLD is a genetic disorder and
patients have a germline mutation in one of the PLD genes
and must acquire only one additional somatic mutation to
develop cysts. Patients with solitary large cysts need to
acquire somatic mutations on 2 PLD genes to develop the
phenotype [3]. Thus, the risk for recurrence is low in these
patients. This contrasts with the situation in PLD where
the liver volume increases with 1.8% every 6–12months.
As a consequence, the natural growth of PLD will rapidly
overtake the potential volume-curtailing effect of lapa-
roscopic fenestration of a single, albeit large, cyst. The
implication is that the threshold for laparoscopic fenestra-
tion in PLD must be high in view of the limited long-term
efficacy and higher risks.
Percutaneous aspiration sclerotherapy is a valid alter-
native strategy for large simple hepatic cysts. A recent
systematic review found that aspiration sclerotherapy
reduces symptoms in 72–100% while symptoms disap-
peared in 56–100% of patients. Aspiration sclerotherapy
comes with complications such as pain, ethanol intoxica-
tion, cyst bleeding and rarely cyst infections [21]. It is
essential to understand the dynamics of fluid reaccumula-
tion and disappearance after aspiration sclerotherapy to
appreciate the merits of the procedure. Within days after
complete evacuation of the cyst using aspiration sclero-
therapy, cyst fluid reaccumulates only to disappear slowly
over (at least) 26weeks [22]. As a corollary, aspiration
sclerotherapy takes months to achieve its full effect, com-
pared to the immediate effect of fenestration. Despite these
differences, it still needs to be determined which treatment
is superior or which patient subgroup has the most benefit
from either procedure. As percutaneous aspiration scle-
rotherapy and laparoscopic fenestration have never been
compared directly in a controlled setting, we believe that
a randomised trial that focuses primarily on symptomatic
relief and symptomatic recurrence should be conducted.
Subgroup analyses might elucidate patient-related factors
that make either procedure better suited.
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701Surgical Endoscopy (2019) 33:691–704
1 3
Surgical technique
The question here is whether the evolution of laparoscopic
fenestration is complete. In our dataset, we did not find a
significant change in rates of efficacy, complications, con-
versions to laparotomy or length of hospital stay over time.
Although conversion rates above 10% only occurred before
2006. The basic surgical technique used is straightforward
and entails laparoscopy, aspiration of cyst fluid first and
finally wide deroofing of the cyst wall (near the transition
zone between cyst wall and normal hepatic parenchyma).
There are innovations such as the use of robot-assisted
laparoscopic fenestration for giant hepatic cysts [23], sin-
gle incision laparoscopic surgery [24–30] or 3D-vision
supported surgery [31]. In addition, the use of indocyanine
green fluorescent imaging intra-operatively may facilitate
better assessment of bile duct communication or identi-
fication of bile duct injuries [32–36]. However, the addi-
tive value of these techniques for cyst fenestration remains
unclear.
Cyst recurrence is an issue and is thought to result from
incomplete deroofing or development of a false lumen
by adjacent tissues [37, 38]. To reduce recurrence risk,
omentopexy is advocated in view of the hypothesis that
omental tissue resorbs fluid and keeps the residual cavity
open. Some authors cite specific indications to perform
omentopexy such as a small exposed cyst wall, intrahe-
patic cysts, cyst size > 10cm, cysts located posteriorly or
in segment 7 and 8 or if < 50% of cyst wall can be resected
[15, 39–45]. Other researchers refrain from omentopexy
because of questionable evidence, similar recurrence rates
without omentopexy, additional complications (e.g. omen-
tal bleeding) or extension of operating time [16, 46–49].
Our systematic review did not identify advantages or
disadvantages of omentopexy as adjunct to the surgical
procedure. One caveat is that the data were limited and no
correction for cyst size and cyst location could be made.
We included only studies that explicitly mentioned omen-
topexy in the subgroup analysis and it is possible that we
missed data from studies that used the procedure but did
not report that. Randomised clinical trial data are lacking
but a single retrospective study compared fenestration with
or without omentopexy and did not report a significant
benefit [49]. In view of the limited benefit, the customary
use of omentopexy with laparoscopic fenestration is ques-
tionable. Other options are in development to curtail cyst
recurrence after deroofing such as ethanol sclerotherapy
[50–53], argon beam coagulation [54, 55] or wide electro-
coagulation [56], but evidence to support their use is lim-
ited and the provided data were not sufficient to perform a
subgroup analysis of these techniques.
Strengths andlimitations ofthestudy
There are a number of strengths and limitations that result
from the very nature of a systematic review. The compliance
with the recommendations of the PRISMA and MOOSE
guidelines is a major strength of our systematic review. This
included a pre-published protocol, an up-to-date extensive
literature search, independent screening of all references
by two authors and independent risk of bias assessment
of included studies by two authors. Data extraction was
checked for errors by random sampling of 6 studies by a sec-
ond investigator and was found 100% accurate. Contact with
the corresponding authors of the included studies for addi-
tional information provided an extra inclusion. We excluded
studies with a mean or median follow-up < 6months to
reduce biases in reported recurrence rates. Selection bias
was reduced by excluding case series and all articles were
methodically checked for presence of duplicate datasets. A
limitation of our review is that we could not include some
studies because of language restrictions and unavailable full-
text articles. This resulted in exclusion of some substantial
Russian [57, 58], Ukrainian [59], Romanian [60], Hungar-
ian [61] and Chinese [62, 63] cohorts, which is a possible
source of bias and may result in lower generalisability in
other countries. In addition, an important question is if the
location of the treated hepatic cyst correlates with a differ-
ent clinical response. It has been reported that unfavourably
located cysts have a higher tendency for recurrence [17].
Unfortunately, the provided data were not sufficient to ana-
lyse this question in a subgroup analysis.
In our risk of bias assessment, studies scored well on
selection of the study groups and ascertainment of outcome
of interest. However, studies scored very low on compara-
bility of groups, as most studies did not include a control
group. The implication is that the data collection resulted
in a robust dataset but that comparison to untreated patients
and correction for centre-dependent biases is not possible.
We observed moderate heterogeneity for the outcomes
symptomatic relief, symptomatic recurrence, reinterven-
tion and complication rate. This is in part attributable to the
diverse patient populations (PLD, solitary cysts or both).
Our subgroup analyses established that omentopexy, chol-
ecystectomy, follow-up duration, publication date and data
collection did not significantly affect the results and are an
improbable cause of heterogeneity. Remaining causes of het-
erogeneity, that could not be assessed, are clinical diversity
(e.g. centre, surgical expertise) and methodological diversity
(e.g. study design, reporting).
Most outcomes had an LFK-index demonstrating minor
or no asymmetry in the publication bias assessment, except
for mortality. In theory, this could indicate that stud-
ies with high mortality were less likely to be published.
However, as most studies had a prevalence of 0% and the
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702 Surgical Endoscopy (2019) 33:691–704
1 3
one reported procedure-related death occurred in a small
cohort, the pooled mortality rate and LFK-index are prob-
ably overestimated.
No randomised controlled trials were included, and most
included studies used patient records or prospective data-
bases. Only few studies used a validated questionnaire to
assess symptoms and none used specific questionnaires such
as the PLD-Q or POLCA [3]. In addition, not all studies
had a clear definition of symptomatic recurrence and it is
unclear if imaging had been performed for all patients during
follow-up. In order to address this issue, we pooled patients
with recurrent symptoms with evidence of radiological
recurrence and patients with recurrent symptoms. By pool-
ing both categories it is possible that we included patients
with recurrent symptoms without radiological recurrence.
This could have affected our results. However, in included
studies, only 3 out of 1203 patients had recurrent symptoms
without radiological recurrence. We suggest that any future
studies use validated questionnaires and standard imaging
techniques at pre-set time points.
Conclusions
In conclusion, this systematic review provides evidence
that laparoscopic fenestration is an effective treatment for
symptomatic simple hepatic cysts with a low symptomatic
recurrence rate. The symptomatic recurrence rate and risk
of complications are significantly higher in PLD patients.
Acknowledgements The authors thank OnYing Chan, Radboud Uni-
versity Medical Centre, for assistance with database searches and Philip
de Reuver, MD PhD, Royal North Shore Hospital and North Shore Pri-
vate Hospital, Australia, for providing additional data on their studies.
Compliance with ethical standards
Disclosures Drs. Lucas H.P. Bernts, Sebastiaan G. Echternach, Wiet-
ske Kievit, Camiel Rosman and Joost P.H. Drenth have no conflicts of
interest or financial ties to disclose.
Open Access This article is distributed under the terms of the Crea-
tive Commons Attribution 4.0 International License (http://creat iveco
mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribu-
tion, and reproduction in any medium, provided you give appropriate
credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
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