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Asian Journal of Surgery (2018) xx, 1e6

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ORIGINAL ARTICLE

Operative treatment of hepatic hydatid

cysts: A single center experience
Gad Marom a,1, Tawfik Khoury b,1, Samir Abu Gazla a,
Hadar Merhav a, Dan Padawer a, Ariel A. Benson b,
Gidon Zamir a, Lisandro Luques a, Rifaat Safadi b,
Abed Khalaileh a,*

a
Department of Surgery, Hadassah-Hebrew University Medical Center, Ein Kerem, Israel
b
Department of Gastroenterology and Liver Diseases, Hadassah Medical Center, Jerusalem, Israel

Received 2 August 2018; received in revised form 19 September 2018; accepted 27 September 2018

KEYWORDS Summary Background: Hydatid cyst is a zoonotic disease caused by Echinococcus genera.
Echinococcus; Surgery is needed in most cases. We aimed to describe our center’s experience in the surgical
Hydated cyst; management of hepatic hydated cysts (HHC).
Liver surgery; Methods: Data was retrospectively collected for patients who underwent operative manage-
Morbidity; ment for HHC between the years 1994e2014.
Mortality Results: Sixty-nine underwent surgical treatment for HHC. Group A included 34 treated with an
unroofing procedure, group B included 24 patients who underwent hepatectomy and group C
included 11 patients who underwent peri-cystectomy. The median
(range) age for groups
A, B and C were 39.5 (6.5e69), 40 (17e74) and 32 (20e62), respectively (P > 0.1). Post-
operative complications occurred in 16, 11 and 5 patients in group A, B and C, respectively,
as assessed by clavien-dindo classification (CDC). The average CDC was significantly higher
in the hepatectomy group as compared to the unroofing group (2.3 vs.1.5, P Z 0.04). Recur-
rence was significantly higher after the unroofing procedure as compared to the hepatectomy
group (P Z 0.05).
Conclusion: Surgery remains the mainstay of treatment for HHC, once surgery is pursued, the
results are satisfactory.

Abbreviations: HHC, hepatic hydated cyst; CDC, clavien-dindo classification; PAIR, Puncture, Aspiration, Injection of protoscolicidal agent
and Re-aspiration; WHO, world health organization.
* Corresponding author. Department of Surgery, Hadassah-Hebrew University Medical Center, Ein Kerem, POB 1200, IL91120, Israel.
E-mail addresses: [email protected] (G. Marom), [email protected] (T. Khoury), [email protected] (S.A. Gazla),
[email protected] (H. Merhav), [email protected] (D. Padawer), [email protected] (A.A. Benson), rgideonz@
hadassah.org.il (G. Zamir), [email protected] (L. Luques), [email protected] (A. Khalaileh).
1
First two authors contributed equally.

https://doi.org/10.1016/j.asjsur.2018.09.013
1015-9584/ª 2018 Asian Surgical Association and Taiwan Robotic Surgery Association. Publishing services by Elsevier B.V. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Marom G, et al., Operative treatment of hepatic hydatid cysts: A single center experience, Asian
Journal of Surgery (2018), https://doi.org/10.1016/j.asjsur.2018.09.013
 + MODEL
2 G. Marom et al.

ª 2018 Asian Surgical Association and Taiwan Robotic Surgery Association. Publishing services
by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://
creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction retrospectively collected and analyzed. Data collected

included demographics, cyst localization and character-
Hydatid cyst of the liver is a chronic, parasitic disease that istics, surgical treatment, preoperative liver function,
varies in severity. It is caused by the larva stage of the general condition of the patients defined by stable vital
Echinococcus Granulosus Cestode. The disease can affect signs, conscious and comfortable patient, operative time,
animals as well as humans. Although many organs may be operative blood loss, blood transfusion amount,
affected, the liver is the most commonly affected organ morbidity, follow-up periods and the outcome of treated
occurring in approximately 5e70% of cases.1 patients. Furthermore, the patients were followed for
Hepatic hydatid cysts (HHC) are either discovered as an early post-operative complications including fever
incidental finding or when they become symptomatic.2 The defined by temperature of more than 37.6 Celsius; bile
cysts develop when a connective tissue capsule, a peri- leak defined by abnormal fluid accumulation in the
cyst, is formed around the parasite to isolate it from the abdominal drain with high bilirubin concentration or as
host. The peri-cyst is an important landmark for surgical diagnosed by cholangiography; pneumonia defined by
resection. Several treatment options are available for HHC, clinical presentation of respiratory infection (cough,
including medical, percutaneous or surgical, however, a dyspnea, fever) coupled with high white blood count and
watchful waiting strategy may be employed in asymptom- radiological appearance of consolidation in lungs; surgical
atic, uncomplicated and small lesions.3 There is no “best” site infection defined by abnormal purulent discharge
treatment option strategy for HHC and no head-to head coupled with clinical and laboratory signs of infection;
randomized clinical trial has compared the different pleural effusion defined by abnormal fluid accumulation
treatment options. In the past, surgical intervention was in the pleural cavity diagnosed by chest imaging;
the primary approach for patients with HHC.4 however in anaphylaxis defined as a serious life-threatening allergic
recent years medical treatment based on the use anti- reaction characterized by itchy rash, throat or tongue
parasitic agents is used.5 Although treatment success is swelling, shortness of breath and hypotension and Iatro-
achieved in approximately one third of patients treated genic diaphragmatic injury which in our series diagnosed
medically.6 percutaneous treatment is often applied in the intra-operatively.
treatment of HHC patients who are either uncomplicated or All patients included in this study were treated sur-
are poor surgical candidates and it can be performed either gically. Inclusion criteria were according to the world
via PAIR (Puncture, Aspiration, Injection of protoscolicidal health organization (WHO) and included large liver cysts
agent and Re-aspiration) or catheter-assisted endocyst (>5 cm) with multiple daughter cysts; single liver cysts
removal with varying success Currently, surgical manage- (>5 cm), cyst that were located superficially that pose
ment is reserved for either complicated cysts (e.g. ruptured the risk to rupture spontaneously or as a result of
cyst, cysts with biliary fistulae, cysts compressing vital trauma; viable cysts with signs of active infection; cysts
structures, cysts with secondary infection or hemorrhage) communicating with the biliary tree, cysts that cause
or for cysts that are not suitable for percutaneous treat- local pressure to adjacent organs and complicated cysts
ment such as cystic echinococcosis World Health Organi- (such as bleeding into the cyst or rupture).3,6 Exclusion
zation (WHO) classification stage CE2 and CE3b.3,7 The criteria included patients who refused surgery, pregnant
surgical options include unroofing, peri-cystectomy and woman, patient with concomitant severe cardio-
even hepatectomy. pulmonary diseases. In addition, surgery is contra-
The aim of this study is to present the experience of our indicated in patients with cysts that are difficult to
institution in the surgical management of liver hydatid access, inviable cysts, either partly or totally calcified
disease over a period exceeding 20 years. Specifically, we cysts, and in patients with small cysts.
aimed to compare the outcomes of the various surgical Patients were divided into three groups, according to
options (peri-cystectomy, cyst unroofing, and hepatec- the surgical procedure that was performed, including
tomy) including cure rate, recurrence rate, morbidity and unroofing procedure, hepatectomy and peri-cystectomy
mortality. (which is removal of the cyst as a whole without opening
it, by dissecting through the peri-cystic layer, (the outer
inactive part of the hydatid cyst that is composed of host
2. Materials and methods liver tissue)).
All patients with signs of an active cyst received Alben-
The medical records of all patients who underwent sur- dazole pre-operatively for 3e4 weeks (at a dose of 10 mg/
gical treatment for isolated hepatic echinococcal disease kg) and subsequently for 4 weeks after the operation. Broad
at the Department of Surgery, Hadassah-Hebrew Univer- spectrum antibiotics were administered peri-operatively in
sity Medical Center, during a period of over twenty years all cases. The study was approved by the hospital IRB
from January 1994 until December 2014 were committee.

Please cite this article in press as: Marom G, et al., Operative treatment of hepatic hydatid cysts: A single center experience, Asian
Journal of Surgery (2018), https://doi.org/10.1016/j.asjsur.2018.09.013
 + MODEL
Surgery for hepatic hydated cysts 3

2.1. Surgical approach selection tests applied were two-tailed. Categorical variables
(gender, general condition and pre-operative liver function)
The decision regarding the type of the surgery was indi- was performed via Chi square test. P value of 0.05 or less
vidualized according to each case and according to the was considered statistically significant.
hepato-biliary surgeon who performed the surgery. Gener-
ally, the unified criteria used to choose the surgical inter- 3. Results
vention type was based on cyst location, cyst depth and
cyst proximity to vascular and biliary organs. Laparoscopic
3.1. Demographics
peri-cystectomy was performed for single peripheral lesion
more than 5 cm not involving the biliary structures.
Unroofing was utilized for peripheral multiple structures Overall, 69 patients underwent surgical treatment for HHC
with proximity to biliary and vascular structures. For deep at the Hadassah Hebrew University Medical Center between
lesions affecting one lobe which were very close or con- 1994 and 2014. Fig. 1 demonstrating the distribution of our
nected to a vascular structure, hepatectomy was per- patient’s cohort. Group A included 34 patients who were
formed. Overall each individual decision regarding the type treated by unroofing procedure. Group B included 24 pa-
of surgery was chosen so as to prevent recurrence and tients who underwent hepatectomy and group C included
minimize complications. 11 patients who underwent peri-cystectomy. The median
(range) age for groups A, B and C were 39.5 (6.5e69), 40
(17e74) and 32 (20e62), respectively (P > 0.1). Forty-four
2.2. Statistical analysis percent, 32% and 27% in groups A, B and C were males,
respectively (P Z 0.4). Baseline demographics, operative
All analysis was performed using Excel 2003 (Microsoft, details and cyst characteristics are shown in Table 1.
Redmond, WA, United States). Continuous variables were
expressed as median þ range. The comparison of two in- 3.2. Post-operative complications, length of
dependent groups was performed using Student’s t-test. All hospitalization and follow-up

Post-operative complications were classified according to

the Clavien-Dindo classification (CDC).8 graded between 1
and 5. In the unroofing group there were 16 complications,
including eight patients with fever (grade 1 CDC), four pa-
tients had anemia (grade 1 CDC), one patient had a
collection that was drained via computed tomography
guidance (grade 3 CDC), 2 patients had bile leak (one of
whom was treated with ERCP) (grade 3 CDC) and 1 patient
had anaphylaxis with hypotension who required vasopressor
therapy with noradrenaline (grade 4 CDC). In the hepa-
tectomy group, eleven complications were documented, as
three patients developed fever (grade 1 CDC), one patient
had a surgical site infection (grade 2 CDC), one patient had
Figure 1 Demonstrating the flow chart of our cohort. anemia (grade 1 CDC), one patient developed a pleural

Table 1 baselines characteristics.

Unroofing (group A) Hepatectomy (group B) Peri-cystectomy (group C) P value
Age (years), median 39.5 (6.5e69) 40 (17e74) 32 (20e62) >0.1
(range)
Male (%) 44 29 27 0.4
Maximal cyst size (cm), 7.5 (0.5e15) 9 (1e20) 8 (4e20) 1.1 for A vs. C
median (range) 0.02 for A vs. B
0.3 for B vs. C
Average number of cysts 1.9 1.4 1.27 >0.14
Normal pre-operative liver 73 54 91 0.001 for A vs. C
function (%) 0.005 for A vs. B
0.001 for B vs. C
Good general condition (%) 97 92 100 >0.15
Operative hours, median (range) 4 (2e10.5) 5.75 (3e9) 5.5 (2e7.5) 0.12 for A vs. C
0.01 for A vs. B
0.3 for B vs. C
Average operative blood loss (units) 0.2 0.75 0 >0.12
Average blood unit transfusion (n) 0.24 0.7 0 >0.17

Please cite this article in press as: Marom G, et al., Operative treatment of hepatic hydatid cysts: A single center experience, Asian
Journal of Surgery (2018), https://doi.org/10.1016/j.asjsur.2018.09.013
 + MODEL
4 G. Marom et al.

effusion necessitating pleural paracentesis (grade 3 CDC), operatively, post-operatively or pre- and post-operatively
one patient had a skin rash that was treated conservatively (P Z 0.5).
(grade 2 CDC), one patient had a fluid collection that was
drained under the CT guidance (grade 3 CDC), two patients
suffered from a bile leak treated with ERCP (grade 3) and 4. Discussion
one patient died (grade 5 CDC). While in the peri-
cystectomy group, five complications were reported, Echinococcosis is an endemic disease in many parts of the
including three patients with fever (grade 1 CDC), one pa- world but is not considered to be endemic to Israel. To the
tient with pneumonia (grade 2 CDC) and one patient had best of our knowledge, this is the largest study of surgical
iatrogenic diaphragmatic injury (grade 3 CDC) (Table 2). treatment of HHC in Israel. In this study we reviewed the
Moreover, the median (range) length of hospitalization in characteristics of patients treated surgically for HHC.
groups A, B and C was 12 (3e35), 11 (3e70) and 11 (5e19) Overall, all patients underwent surgical intervention as
days, respectively (P > 0.05). Moreover, the median length indicated for HHC. There was no difference in cyst number
of hospitalization of right and left hepatectomy was 12 among the different surgical groups.
(3e70) and 10 (5e31), respectively (P Z 0.1). The follow- In this study, the decision regarding the type of surgery
up period in group A and group A were 32.4 and 2.9 was based mainly on surgeon preference according to cyst
months, respectively, while in group C, all patient were lost location, depth and proximity to vital organs. Peri-
follow-up after the surgery. cystectomy was attempted in all patients when techni-
cally feasible (single peripheral cyst). In some cases, spe-
cifically when the cyst was too deep, there were multiple
3.3. Hepatic hydatid cyst recurrence cysts, or there was proximity to vital organs, unroofing of
the cyst or hepatectomy was chosen to minimize compli-
Unroofing surgical intervention was the only factor con- cations. Our institution has our own criteria for operation
nected to HHC recurrence as cyst recurrence occurred in 6 and standardization of treatment. We prefer unroofing as
patients (18%) those who underwent unroofing as compared the first line procedure for most of HHC. Similarly to our
to 1 patient (4%) in the hepatectomy group (P Z 0.05), approach, still, many prefer performing unroofingypartial
while we couldn’t know about the recurrence rate among cystectomy, as the procedure is simpler and easier to
the peri-cystectomy group given that all patients in this perform.9 However, one of the main disadvantages of
group were lost follow-up following the surgery. The pa- conservative surgery such as unroofing is a higher recur-
tient in the hepatectomy group who experienced recur- rence rate.10 Similarly, the recurrence rate in our study was
rence was treated by partial hepatectomy, while in the higher in the unroofing surgical intervention group. Thirty-
unroofing group, 4 patients were treated by partial hepa- four patients in our study underwent unroofing, and of
tectomy and the other two patients were followed-up by them 18% had recurrence of HHC. Most patients with
radiological imaging studies. recurrent HHC were surgically treated by partial hepatec-
There was a trend for higher recurrence rates with tomy to eliminate the subsequent risk of recurrence.
increasing cyst size, as HHC size of 7 cm or greater showed Earlier study by Yuskel et al reported that more radical
cyst recurrence after surgical management, while no HHC hepatic surgery diminish early recurrence of HHC.11
recurrence when the size of the cyst was less than Another potential limitation of unroofing is the occur-
7 cm (P Z 0.08) (Fig. 2). Moreover, there was no difference rence of anaphylaxis, as this can be a catastrophic side
in HHC recurrence among all groups whether medical effect and necessitates careful planning to avoid intra-
therapy with albendazole was administered pre- abdominal spillage of the cyst contents into the peritoneal

Table 2 Post-operative complications.

Procedure Unroofing (group A) Hepatectomy (Group B) Peri-cystectomy (Group C) P value
Fever 8 3 3 >0.1
Anemia 4 1 0 0.1
Bile leak 2 2 0 >0.1
Collection 1 1 0 >0.2
Pneumonia 0 0 1 0.03 for A vs. C
0.07 for B vs. C
Iatrogenic diaphragmatic injury 0 0 1 0.03 for A vs. C
0.07 for B vs. C
Surgical site infection 0 1 0 >0.1
Pleural effusion 0 1 0 >0.1
Anaphylaxis 1 0 0 >0.2
Average CDC gradea 1.5 2.3 1.6 0.04 for A vs. B
0.4 for A vs. C
Total 16 11 5
a
CDC: clavien-dindo classification.

Please cite this article in press as: Marom G, et al., Operative treatment of hepatic hydatid cysts: A single center experience, Asian
Journal of Surgery (2018), https://doi.org/10.1016/j.asjsur.2018.09.013
 + MODEL
Surgery for hepatic hydated cysts 5

Figure 2 Demonstrating a trend for cyst recurrence at cyst size of 7 cm.

cavity.12 In our study, one patient (2.9%) developed study was slightly higher than that reported in the litera-
anaphylaxis in the unroofing group which resolved with ture, however, the mortality rate of 1.4% was within the
immediate therapy with vasopressors and steroids while range or lower than that reported.15 Moreover, in the
no episode occurred in the other groups. Previous studies unroofing and peri-cystectomy groups, most of the post-
have shown an increased morbidity of HHC treated with operative complications were mild consisting of fever and
radical surgical intervention such as hepatectomy which anemia. As we showed in this retrospective cohort, major
indirectly lengthens hospital stay.13 In our study there was morbidity is not common in surgical management of HHC as
no significant difference in length of hospitalization it would be expected for a benign disease. Furthermore,
among the different surgical groups, moreover, right mortality was rare which shows that even in non-endemic
hepatectomy was associated with longer hospital stay as area, the surgical results for HHC are satisfactory.
compared to left hepatectomy, although the difference The present study had several limitations. Firstly, it was
was not statistically significant (P Z 0.1). Recent studies a retrospective study, thereby increasing the risk of data
showed that pre-and post-operative administration of collection bias and, secondly that the study was performed
medical anti-parasitic agents reduced the risk of in a single center. Second, patients in the peri-cystectomy
anaphylactoid reactions and prevented recurrence.14 were lost follow-up after the surgery, thus we couldn’t
However, in our study, pre-, þ/ post-operative medical assess the recurrence rate in this group. Nonetheless, this is
treatment with albendazole did not impact the recurrence the largest study regarding surgical management of HHC
rate, thus questioning the necessity for anti-parasitic originating in Israel. In conclusion, hydatid cyst disease in
management in the perioperative timeframe. This obser- Israel is infrequent. Surgical intervention is undoubtedly
vation needs further validation by performing prospective reasonable with regards to morbidity, recurrence, and
randomized trials. mortality.
Overall, the complication rate among all patients who
underwent unroofing was 47%, with most having fever and
anemia. In the peri-cystectomy group, the complication Author contribution
rate was 45.5% of which half were mild fever and the
complication rate in the hepatectomy group was 46% with Abed Khalaileh contributed to the concept and design of
one case of post-surgical mortality. Notably, most compli- the study. All authors contributed to data collection and
cations in the hepatectomy group necessitated endoscopic analysis. Abed Khalaileh, Gad Marom and Tawfik Khoury
and radiological treatment. The complication rate as esti- contributed to data interpretation and statistical analysis.
mated by Clavien-Dindo classification was significantly Abed Khalaileh, Gad Marom and Tawfik Khoury wrote the
higher in the hepatectomy group as compared to the final version of the manuscript. All authors approved the
unroofing group (P Z 0.04). The complication rate in our final version to be published.

Please cite this article in press as: Marom G, et al., Operative treatment of hepatic hydatid cysts: A single center experience, Asian
Journal of Surgery (2018), https://doi.org/10.1016/j.asjsur.2018.09.013
 + MODEL
6 G. Marom et al.

Conflict of interest 7. Junghanss T, da Silva AM, Horton J, Chiodini PL, Brunetti E.

Clinical management of cystic echinococcosis: state of the art,
problems, and perspectives. Am J Trop Med Hyg. Sep 2008;
The authors declare no conflict of interest regarding this 79(3):301e311.
manuscript. 8. Dindo D, Demartines N, Clavien PA. Classification of surgical
complications: a new proposal with evaluation in a cohort of
Acknowledgment 6336 patients and results of a survey. Ann Surg. Aug 2004;
240(2):205e213.
9. Nepalia S, Joshi A, Shende A, Sharma SS. Management of
None. echinococcosis. J Assoc Phys India. Jun 2006;54:458e462.
10. Aydin U, Yazici P, Onen Z, et al. The optimal treatment of
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Please cite this article in press as: Marom G, et al., Operative treatment of hepatic hydatid cysts: A single center experience, Asian
Journal of Surgery (2018), https://doi.org/10.1016/j.asjsur.2018.09.013