THE AMERICAN JOURNAL OF GASTROENTEROLOGY
1, 2000
© 2000 by Am. Coll. of Gastroenterology
Published by Elsevier Science Inc.
A New Therapeutic Approach for the
Treatment of Cystic Echinococcosis: Percutaneous
Albendazole Sulphoxide Injection Without Reaspiration
Emin Deger, M.D., Murat Hokelek, M.D., Ph.D., Bekir Ahmet Deger, M.D., Ediz Tutar, M.D.,
Mehmet Asil, M.D., and Emre Pakdemirli, M.D.
Pamukkale University Faculty of Medicine, Department of Radiology, Denizli; Ondokuz Mayis University
Faculty of Medicine, Department of Microbiology, Samsun; Hacettepe University Faculty of Medicine,
Department of Radiology, Department of Pathology, and Department of Internal Medicine, Ankara, Turkey
OBJECTIVE: In this experimental study, the effectiveness of
intracystic injection of albendazole sulfoxide solution was
investigated as a new approach to percutaneous treatment in
liver hydatid disease.
METHODS: Ten naturally infected sheep were selected and
divided into two groups: a treatment group (n ⫽ 7), and a
control group (n ⫽ 3). Intracystic injection of albendazole
sulfoxide was performed in the first group, whereas the
control group received intracystic distillated water injection
instead. No reaspiration was performed in any group.
RESULTS: During the follow-up period of 6 months, serial
sonographic examination revealed a significant decrease in
the cyst size, progressive solidification, and complete sep-
aration of the germinal and the laminated membranes of
hydatid cysts from the pericysts in the treatment group. In
the control group, diameters and volumes of cysts were
increased. All procedures were done without any complica-
tions. During the follow-up-period, liver function tests were
normal. After 6 months, all sheep were killed and were
examined for macroscopic and microscopic changes. Patho-
logical examination showed pericyst hyalinization, inflam-
matory cells in the cyst wall, degeneration of laminated and
germinal membranes, and necrotic material in the cyst cav-
ity. No viable protoscoleces or daughter cysts were ob-
served.
CONCLUSION: Albendazole sulfoxide injection as a sco-
lecidal agent in the percutaneous treatment of cystic echi-
nococcosis seems to be effective in this animal model.
Further studies are suggested to evaluate the effectiveness of
this procedure in human subjects. (Am J Gastroenterol
2000;95:248 –254. © 2000 by Am. Coll. of Gastroenterol-
ogy)
INTRODUCTION
Hydatid disease is still endemic in many developing coun-
tries and continues to be an important cause of morbidity.
Many therapeutic modalities for the treatment of hydatid
Vol. 95, No.
ISSN 0002-9270/00/$20.00
PII S0002-9270(99)00711-X
disease have been suggested in the literature, including
systemic administration of various chemotherapeutic agents,
surgery, and the percutaneous approach.
Success rates of the systemic chemotherapy vary with the
cyst condition and the chemotherapeutic agent used (1).
Oral benzimidazole derivatives are the most preferred che-
motherapeutic agents and are used in disseminated systemic
disease, in inoperable cases, and for prophylaxis before
surgery (2, 3). However, the efficacy of systemic chemo-
therapy in the treatment of hydatid disease is limited (4 – 6).
Radical surgery remains the most effective treatment mo-
dality (7). However, surgery is not possible if the cyst is
located centrally in the liver or in contiguity with the vas-
cular or biliary structures (8, 9). Conservative surgery seems
to have higher recurrence rates (10). Recurrent diseases and
the presence of multiple cysts also increase perioperative
morbidity and mortality (11, 12). Moreover, patients with
respiratory or cardiovascular problems who carry high risk
for general anesthesia are not good candidates for surgery.
The first report on percutaneous drainage of hydatid cysts
in literature was done by Mueller et al. in 1985 (13). Later
on, aspiration and alcohol injection (14), aspiration and
hypertonic saline injection (15), and concomitant use of
alcohol and hypertonic saline injection (16) were introduced
as new therapeutic approaches in the treatment of cystic
echinococcosis. Percutaneous treatment has gained popular-
ity in recent years. In several studies, percutaneous treat-
ment has been suggested as a safe and effective procedure
(13–20), and this procedure is considered as the treatment of
choice for liver hydatid disease in endemic regions (21).
Advantages of percutaneous treatment over surgery include
short duration of hospitalization, as well as cost-effective-
ness. In addition, it can be performed in surgically high risk
patients, patients with recurrent disease, and in cases in
which surgery is impossible because of the location of the
cyst (20 –22). The percutaneous aspiration-injection-reaspi-
ration (PAIR) method is usually preferred for percutaneous
approach. In this method, the cyst first is punctured and the
cyst content evacuated, followed by injection of scolecidal
AJG – January, 2000
agents such as hypertonic saline or 95% ethanol into the cyst
cavity. Reaspiration of the cyst content is then performed,
and the procedure is terminated (13, 22).
In this experimental study, we used a new technique,
which we suggest be named the “percutaneous drug injec-
tion method” (PEDIM). PEDIM differs from PAIR and
other similar techniques in two aspects. First, instead of a
hypertonic solution, a chemotherapeutic agent (albendazole
sulfoxide) is injected into the cyst cavity; and second, no
reaspiration is performed. This new method seems to be
easier to perform and takes less time. The aim of this study
was to evaluate the effectiveness of intracystic albendazole
sulfoxide injection using this new method in the treatment of
liver hydatid disease in an animal model.
MATERIALS AND METHODS
All experiments were performed according to the European
Community rules of animal care (23). Ten sheep naturally
infected with Echinococcus granulosus were identified with
portable ultrasound (SIUI CTS-285, Guangdong, China)
using a 3.5- MHz focused transducer and were selected for
the present study. Sheep were divided into two subgroups,
as the treatment group (n ⫽ 7) and the control group (n ⫽
3). All cysts were localized in the liver and classified as type
1 according to the classification of Gharbi et al. (24) (Fig.
1A and Fig. 2A). The maximal cyst diameter varied between
2.5 and 6 cm (Tables 1 and 2). Albendazole sulfoxide
solution was prepared in the following way: 50 mg albenda-
zole sulfoxide (SmithKline Beecham, London, England)
was dissolved in sterile distilled water, brought to a final
volume of 100 ml, and the solution mixed with a magnetic
mixer.for 6 h at room temperature The solution was then
sterilized by ultraviolet.
Before percutaneous injection, blood samples were ob-
tained for serum glutamic oxaloacetic (SGOT) and glutamic
pyruvic (SGPT) transaminases, ␥-glutamyl transferase
(GGT), alkaline phosphatase (ALP), and total bilirubin to
test liver functions.
In each sheep, only one cyst was punctured. The approx-
imate volume of the cyst was calculated. Before the proce-
dure, the puncture site was anesthetized locally by using
prilocine 0.5%. An 18-g seldinger (Dispomedica GmbH
22041, Hamburg, Germany) needle was inserted under
sonographic guidance via the transhepatic route into the cyst
(Fig. 2B). The approximate dose of albendazole sulfoxide
needed to achieve an intracystic concentration of 10 mg/dl
was calculated, and the same volume of cystic fluid was
aspirated before injection. Aspirated fluid material was im-
mediately taken for cytological and microbiological exam-
ination. For cytological examination, the fluid was centri-
fuged and the sediment was examined for fragments of the
laminated membrane, hooklets, and scoleces. The viability
of scoleces was assessed by observing their motility at
immediate microscopy and staining with neutral eosin (25).
Cyst fluid was also tested for the eventual presence of
New Approach for Treating Cystic Echinococcosis 249
bilirubin with urinary sticks (Chemstrip-Iris Urine Test
Strips, IRIStrips, Boehringer Mannheim, GmbH, Mann-
heim, Germany) to exclude the presence of any biliary
connections. After cyst puncture, the procedure was contin-
ued only if hydatid cyst fluid contained laminated mem-
branes, scoleces, or hooklets on immediate microscopy.
After aspirating cystic fluid, the calculated amount of al-
bendazole sulfoxide solution was injected into the cystic
cavity to avoid any change in cyst volumes and intracystic
pressures (Fig. 1B). In the control group, sterile distilled
water was injected into the cysts instead of albendazole
sulfoxide. No reaspiration was performed in any group.
After injecting albendazole sulfoxide solution, the needle
was withdrawn immediately. Follow-up was performed
daily in the first week, then weekly during the next 6
months. At each visit, sonographic examination of each
sheep was performed to determine the changes in cyst size,
morphological changes in cyst contents and cyst wall, local
recurrence or secondary dissemination, and blood samples
were obtained for the liver function tests. Decreases in cyst
size and progressive solidification of cyst contents were
regarded as positive criteria for healing. At the end of 6
months, all sheep were killed with ether anesthesia and the
livers were completely excised for histopathological evalu-
ation. After fixation in buffered formalin, tissues were em-
bedded in paraffin, and 5-␮m thick preparations were ob-
tained and stained with hematoxylin-eosin, which were
evaluated by light microscopy.
RESULTS
Cyst puncture was performed successfully without any com-
plication in all 10 sheep. Results of parasitological exami-
nations were positive for hydatid disease and viable proto-
scoleces were present in all cysts. Aspirated fluids were
negative for bilirubin, which was regarded as an indicator of
absence of biliary fistulization. In the treatment group, the
earliest change was detachment of the laminated membranes
from the pericyst (Fig. 1C). This occurred within 3 days.
Serial sonographic examinations showed a significant de-
crease in cyst diameters and volumes (Table 1). Analysis by
the Wilcoxon signed rank test revealed that size reduction of
the cysts were significant (p ⬍ 0.05). In the follow-up
period, the cysts were observed to be filled with echogenic
material on serial ultrasonographic examinations, and pro-
gressive solidification of the cysts occurred together with an
increase in cyst wall thickness (Fig. 1 day and Fig. 2c).
Serum ALP, GGT, SGOT, and SGPT values, and total
bilirubin levels were normal before the procedure, and re-
mained within normal limits during the follow-up period in
both groups.
Gross examination of the excised livers showed that mac-
roscopic appearance of treated cysts differed significantly
from untreated cysts. Treated cysts were filled with amor-
phous solid gray material (Fig. 3).
Pathological examination showed pericyst hyalinization,
250 Deger et al. AJG – Vol. 95, No. 1, 2000

Figure 1A–D: Sonographic appearances of the treated cyst of sheep 3. A: A cystic lesion, purely anechoic before the treatment. It is located
in the posterior lobe of the right lobe (between cursors). Note that cyst had well defined borders without any calcification or internal septa.
B: After albendazole sulphoxide injection, strong echoes were seen in the cyst cavity. C: Two days later, complete membrane detachment
was seen. D: Six months later, cyst cavity were completely solidified and mix echo pattern with strong echoes representing calcification
(between cursors) were seen.

lymphocyte predominant inflammatory cells in the cyst
wall, degeneration of laminated and germinal membranes,
dystrophic calcifications, and necrotic material filling the
cyst cavity (Fig. 4). In all histological sections, there were
no viable protoscoleces and daughter cysts (Fig. 5A). Patho-
logical examination of portal areas showed that there were
no ductal epithelial proliferation, ductal dilation, or fibrosis
suggesting hepatobiliary toxicity. Microscopic examination
was done in all sheep and similar findings were observed in
all treated cysts, thereby confirming the success of the
treatment.
Diameter and volume of cysts were found to be increased
in the control group during follow-up (Table 2). Patholog-
ical examination of the livers of the sheep in this group
revealed the presence of viable protoscoleces and daughter
cysts in histological sections (Fig. 5B).
DISCUSSION
Hydatid cyst disease is still a major health problem in
endemic areas. Systemic chemotherapy, surgery and percu-
taneous application of various agents are different treatment
modalities used in the treatment of hydatid cyst disease. The
success of systemic chemotherapy is limited and radical
AJG – January, 2000 New Approach for Treating Cystic Echinococcosis 251

Figure 2A–C: Sonographic appearances of the treated cyst of sheep

7. A: A round anechoic cyst with posterior reinforcement before the
treatment. B: During PEDIM session; the needle tip is seen in the
cyst cavity as a strong linear echo. C: Six months later; thickening
of germinative membrane and progressive solidification beginning
from periphery is observed.

surgery is not possible in all cases, for various reasons, as
mentioned before. Therefore, percutaneous methods are
gaining popularity in the treatment of this disease. Various
chemical agents such as alcohol or hypertonic saline are
used in percutaneous studies. There is no study in the
literature in which a chemotherapeutic agent is used percu-
taneously, so we decided to carry out this study with al-
bendazole sulfoxide, which is a well known scolecidal drug.
In this study, we applied albendazole sulfoxide to the
animals, as its scolecidal activity has been confirmed in
previous in vitro studies and the scolecidal concentration is
well established. In vitro studies with albendazole sulfoxide

Table 1. Changes Observed on Ultrasound (US) Scans in the Treatment Group During Follow-up
Size Before Final Cyst Size Volume
Sheep No. Treatment (mm) Final US Pattern (mm) Reduction (%)
1 28 ⫻ 32 ⫻ 38 Solid, inhomogeneous 20 ⫻ 18 ⫻ 25 71
2 31 ⫻ 30 ⫻ 32 Solid, inhomogeneous 18 ⫻ 14 ⫻ 20 83
3 50 ⫻ 45 ⫻ 50 Solid, mix echo 30 ⫻ 35 ⫻ 28 74
4 42 ⫻ 50 ⫻ 55 Solid, homogeneous 25 ⫻ 25 ⫻ 32 83
5 35 ⫻ 35 ⫻ 40 Partially cystic 30 ⫻ 27 ⫻ 23 60
6 45 ⫻ 43 ⫻ 45 Partially cystic 30 ⫻ 25 ⫻ 25 79
7 35 ⫻ 35 ⫻ 40 Partially cystic 30 ⫻ 27 ⫻ 23 60
252 Deger et al. AJG – Vol. 95, No. 1, 2000

Table 2. Volume Changes and Final Ultrasound (US) Patterns of Cysts in the Control Group During Follow-up
Size Before Final US Final Cyst Size Volume
Sheep No. Treatment (mm) Pattern (mm) Changes (%)
1 33 ⫻ 31 ⫻ 27 Pure anechoic 35 ⫻ 31 ⫻ 28 10% increase
2 47 ⫻ 44 ⫻ 45 Pure anechoic 48 ⫻ 46 ⫻ 46 9% increase
3 40 ⫻ 44 ⫻ 38 Pure anechoic 41 ⫻ 44 ⫻ 40 11% increase

show that scolecidal effect is observed at a concentration of asite. Thus, the results of the studies on sheep may be
500 –1000 ␮g;/L (26 –28). Erzurumlu et al. demonstrated applicable to human subjects as well.
that a 10-mg/dl albendazole sulfoxide solution completely Our study demonstrated that percutaneous application of
kills scoleces in vitro (29). Moreover, albendazole sulfoxide albendazole sulfoxide is quite easy to perform and it is an
is not toxic to the liver and biliary structures at applied effective method for the treatment of liver hydatid disease.
concentrations, decreasing the possibility of chemical scle- First, it takes a shorter time to perform than any other
rosing cholangitis, which is a well known complication of percutaneous methods, because in the PAIR method, for the
chemical scolecidal agents (30). These authors showed that effect of chemical scolecidal agent to take place it is left in
direct application of a 10-mg/dl albendazole sulfoxide so- the cyst cavity approximately 10 –20 min or more, than
lution to the biliary system of rabbit intraoperatively did not reaspiration of cyst content is performed. There is no need
cause any side effects to the liver and biliary system (29). for such procedures in our method. Second, no recurrence
Albendazole interferes glucose absorption through the was observed in any of the seven treated sheep used in the
cyst wall (31, 32). Although albendazole reaches a high study. Reductions in cyst size, solidification of cyst content,
blood concentration after oral administration, cystic fluid and absence of fluid content are all accepted criteria of
concentration of the drug is low and clinical outcome is healing as stated in the literature (38). Our findings are
unpredictable (4, 33, 34). Moreover, serious complications consistent with these criteria. Statistical analyses showed a
such as hepatotoxic jaundice and granulocytopenia may significant decrease in cyst size, and pathological studies
sometimes be encountered, requiring monitoring of blood
profile and liver functions during systemic therapy (35, 36).
It is metabolized in the liver via monoamine oxidase. Per-
cutaneous application of this drug offers the advantage of
reaching high intracystic drug concentrations. Therefore,
higher scolecidal activity can be obtained with fewer sys-
temic adverse effects. In addition, because no reaspiration
was done, the scolecidal effect continues for a long time.
In this study, naturally infected sheep were selected for
two reasons, as Akhan et al. previously pointed out (37).
First, it is difficult to create an experimental hydatid disease
in the liver; and second, both human subjects and sheep
share the similarity of being intermediate hosts of the par-

Figure 4. Histological examination of the treated cyst of sheep 4.

Figure 3. Macroscopic appearance of the liver of sheep 4. Treated Necrotic material within the cyst cavity, degeneration of laminated
cyst is filled with white– grey necrotic material (arrowhead). At the and germinal membranes, pericyst hyalinization, and lymphocyte
bottom, untreated cysts are also seen. infiltration are seen (hematoxylin and eosin, ⫻40).
AJG – January, 2000
Figure 5A and B: Microscopic comparison of a treated cyst and a
cyst in the control group. A: Histological examination of sheep 6.
There are no viable protoscolices or daughter cysts, suggesting that
recurrence would not take place (hematoxylin and eosin, ⫻100). B:
Histological examination of sheep 2 of control group. Protosco-
lices, and intact laminated and germinal membrane are seen. Note
that there are no inflammatory cells around cyst (hematoxylin and
eosin, ⫻40).
also confirmed the success of the method. In pathological
examinations, no viable scoleces were seen, suggesting that
possibility of recurrence is quite low.
We hypothesized that the effects of albendazole sulfoxide
may be due to its intrinsic scolecidal activity because the
solution at concentrations of 10 mg/dl is not hypertonic.
Also, detachment of membranes were observed approxi-
mately 2 days after the procedure, which occurs within 10
min when a hyperosmolar agent is used (37, 39). This would
also be attributed to the chemotherapeutic effect of albenda-
zole sulfoxide.
Our results also showed that percutaneous administration
of albendazole sulfoxide solution has no toxic effect to the
liver and biliary system. There were no increases in liver
enzymes and serum bilirubin levels during the follow-up
period and, furthermore, histological examinations of the
liver revealed no signs of hepatotoxicity. It appears that it
New Approach for Treating Cystic Echinococcosis 253
can, therefore, safely be used for percutaneous injection
therapy.
No systemic chemotherapy was given to any sheep in our
study, because systemic chemotherapy would have inter-
fered with the results of percutaneous injection, making the
interpretation of the results difficult. However, inasmuch as
hydatid cyst disease is a systemic disease with possible
involvement of many organs, we suggest concomitant use of
systemic chemotherapy if there is any evidence of dissem-
ination. We think that such a therapy would yield better
results than either systemic chemotherapy or percutaneous
treatment alone. Further studies are suggested to determine
the results of such treatment.
In conclusion, intracystic albendazole sulfoxide applica-
tion is a highly effective and safe method, and it can be used
successfully to treat cysts of hydatid disease without any
significant side effects. Time gain, cost-effectiveness, and
probable low risk of caustic cholangitis also makes this new
approach noteworthy. However further data are needed to
determine the long term consequences of the method.
ACKNOWLEDGMENTS
The authors thank Dr. Ibrahim Haznedaroglu for his impor-
tant editorial contribution. This work was supported Smith
Kline Beecham Pharmaceuticals.
Reprint requests and correspondence: Emin Deger, M.D., Halk
sokak 15/2 Yenisehir, 06420 Ankara, Turkey.
Received Feb. 1, 1999; accepted June 23, 1999.
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