Diagn Interv Radiol 2016; 22: 47–51 INTER VENTIONAL R ADIOLOGY

© Turkish Society of Radiology 2016 ORIGINAL ARTICLE

A novel modified PAIR technique using a trocar catheter for

percutaneous treatment of liver hydatid cysts: a six-year experience

Alaaddin Nayman
PURPOSE
Ibrahim Guler We aimed to demonstrate the success and reliability of a novel puncture, aspiration, injection, and
Suat Keskin reaspiration (PAIR) technique in liver hydatid cysts.

Tuba Berra Erdem METHODS

Hale Borazan Percutaneous treatment with ultrasonographic guidance was performed in 493 hepatic hydatid
cysts in 374 patients. Patients were treated with a new PAIR technique by single puncture method
Ahmet Kucukapan using a 6F trocar catheter. The results of this novel technique were evaluated with regards to efficacy
Huseyin Ozbiner and safety of the procedure and complication rates.

Abdussamed Batur RESULTS

Ersen Ertekin Out of 493 cysts, 317 were Gharbi type I (WHO CE 1) and 176 were Gharbi type II (WHO CE 3A). Of
all cysts, 13 were referred to surgery because of cystobiliary fistulization. Recurrence was observed
Bahadir Feyzioglu in 11 cysts one month later. Therefore, the success rate of the PAIR technique was 97.7% (469/480).
Osman Koc Minor complications (fever, urticaria-like reactions, biliary fistula) were seen in 44 treated patients
(12%, 44/374); the only major complication was reversible anaphylactic shock which was observed
Hasan Emin Kaya in two patients (0.5%, 2/374).
Osman Temizoz
CONCLUSION
Adil Kartal This novel modified PAIR technique may be superior to catheterization by Seldinger technique due
Orhan Ozbek to its efficiency, easier application, lower severe complication rate, and lower cost. Further compar-
ative studies are required to confirm our observations.

H
ydatid disease is a parasitic infection caused by the larval stage of the tapeworm
Echinococcus. E. granulosus is the most common cause of hydatid disease in hu-
mans and is found throughout the world. It is endemic in large sheep raising areas
like the Mediterranean region, the Middle East, Southeast and Central Russia, Northern
China, South America, Australia, and New Zealand (1). Hydatid disease usually affects the
liver (50%–70%) and less frequently lung, peritoneum, kidney, brain, mediastinum, heart,
bone, soft tissues, spinal cord, spleen, pleura, adrenal glands, bladder, ovary, scrotum, and
From the Department of Radiology (A.N.  thyroid gland (2). Treatment approaches include medical, surgical, and minimally invasive
naymanalaaddin@[Link], I.G., O.T.) Selçuk procedures. Medical treatment with albendazole or mebendazole alone has a low rate
University School of Medicine, Konya, Turkey; the
of success and high rate of relapse, making this treatment option controversial (3). The
Departments of Radiology (S.K., O.K., H.E.K., O.O.),
Anesthesiology and Reanimation (T.B.E., H.B.), surgical approach has been the gold standard therapy for the hydatid disease for a long
Microbiology (B.F.), and General Surgery (A. Kartal), time (4). However, in recent years, percutaneous treatment of the hydatid cyst emerged
Necmettin Erbakan University School of Medicine,
Konya, Turkey; the Department of Radiology (A. as a potential alternative to surgery, because of its efficiency, reliability, and low morbidity
Kucukapan), Bozüyük State Hospital, Bilecik, Turkey; and mortality rates. The puncture, aspiration, injection, and reaspiration (PAIR) technique,
the Department of Radiology (H.O.), Gümüşhane
State Hospital, Gümüşhane, Turkey; the Department which involves puncture of the cyst wall, aspiration of cyst contents, instillation, and rea-
of Radiology (A.B.), Yüzüncüyıl University School of spiration of the scolicidal agent, has gained international recognition. PAIR technique can
Medicine, Van, Turkey; the Department of Radiology
be achieved by using a coaxial catheter system to aspirate the cyst content and infuse
(E.E.), Adnan Menderes University School of
Medicine, Aydın, Turkey. scolicidal agent at the same time (5). Another technique can be performed by catheter-
ization (3, 6). In our study, we performed the PAIR procedure by directly entering into the
Received 22 January 2015; revision requested 09 March
2015; final revision received 24 May 2015; accepted 25 hydatid cyst cavity through a single puncture using a trocar catheter instead of placing a
May 2015. catheter through stiff wire after puncturing with a Seldinger needle. The primary goal of
Published online 7 September 2015.
the current study was to determine the success and reliability of this technique in patients
DOI 10.5152/dir.2015.15011 with hydatid disease.

47
 weeks before the procedure to prevent and the biliary tract. If cystography showed
Methods dissemination during the procedure. Each communication between the biliary tract
patient was examined by an anesthesiolo- and the hepatic hydatid cyst cavity, alcohol
Patients
gist during preoperative evaluation and un- was not used because of the risk of induc-
Data from patients who underwent per-
derwent US examination to determine cyst ing secondary sclerosing cholangitis. The
cutaneous treatment for hydatid liver cysts
type, location, number, and size. Complete content of the cyst cavity was aspirated
between January 2008 and December 2013
blood count and coagulation parameters again after the cystograms, followed by
from two institutions were retrospective-
were checked before the intervention, an injection of absolute alcohol (98% ethyl al-
ly reviewed. The local ethics committee
INR value less than 1.5 and platelet count cohol) in a volume equaling two-thirds of
approved the protocol. Our series includ-
higher than 100  000/mL were considered the aspirate. After 20–30 minutes, the pro-
ed 374 patients and a total of 493 cysts of
appropriate. cedure was completed by aspiration of the
Gharbi type 1 (WHO CE 1, i.e., unilocular
Heart rate, arterial oxygen saturation, alcohol from the cyst cavity and fixation of
anechoic lesions with double line sign)
and noninvasive blood pressure were the catheter to the skin.
or Gharbi type 2 (WHO CE 3A, i.e., cysts
monitored. After catheterization of a pe-
with detached membranes). All patients
ripheral vein, lactated Ringer solution 5 Postprocedure
recruited in this study were diagnosed with
mL/kg was administered, and oxygen 4 L/ After the procedure, all patients were
hydatid disease by radiologic and serolog-
min was applied via face mask. Diphen- monitored and observed for early compli-
ic evaluation. Immunohemagglutination
hydramine HCl 20 mg and methyl prednis- cations in the interventional radiology ob-
positivity was questioned in routine sero-
olone 1 mg/kg were applied intravenously servation unit. Patients were reevaluated
logic investigation. Radiologic modalities
to all patients for prevention of allergic 24 hours later, and if their vital signs and
(ultrasonography [US], computed tomog-
reactions and decreasing the anaphylaxis laboratory tests were normal, they were
raphy, and magnetic resonance imaging)
risk. Because of an anaphylaxis risk, epi- discharged from the hospital after catheter
were utilized to differentiate Gharbi type 1
nephrine  was also prepared. Midazolam removal. Removal of the catheters during
hydatid cyst from simple liver cyst. In con-
0.03 mg/kg and fentanyl 50 μg were used the procedure was thought to increase the
trast to simple liver cysts, which often have
for initial sedation and additional midaz- anaphylaxis risk; therefore, all catheters
lobulated contours, type 1 hydatid cysts are
olam 0.01 mg/kg and fentanyl 25 μg were were removed one day after the procedure.
round or ellipsoid due to their hydrostatic
applied when needed. Control cystograms were not obtained pri-
pressure and their walls are thicker than of or to catheter removal. In the follow-up, the
simple cysts. If the differentiation of hydatid Procedure cysts were evaluated by US examination in
cyst from simple cyst of the liver could not All procedures were performed by two the first month, sixth month, first year, and
be made by radiologic studies, a more sen- radiologists who have at least three years second year of the procedure. The success
sitive serologic test, i.e., IgE test specific for of experience in nonvascular intervention- criteria of the percutaneous hydatid cyst
the hydatid cyst, was utilized. al radiology. Patients were positioned in treatment included considerable reduction
supine or lateral decubitus position on a in size and volume of the cyst as well as the
Preprocedure fluoroscopy table with C-arm equipment. fluid component of the cavity, irregularity
Written informed consent was obtained Povidone iodine and appropriate draping and thickening of the cyst wall, disappear-
from all participants. All patients, except six were used to attain a sterile condition af- ance of the fluid component and eventual
with albendazole intolerance, were given 10 ter shaving of the abdominal wall covering solidification of the cyst, and no increase in
mg/kg per day albendazole orally for three hepatic region. Local anesthesia (prilocaine size during follow-up.
hydrochloride) was administered before
Main points the puncture of the cyst. We used number Results
• Percutaneous treatment of the hydatid cyst 11 scalpel blade for skin incision after local
emerged as an alternative to surgery with anesthesia. A 6F trocar type all-purpose Our study included 374 patients (161
low morbidity and mortality rates. drainage catheter (SkaterTM, Angiotech males and 213 females; mean age, 48 years;
• The PAIR technique involves puncture of the Pharmaceuticals) was then placed into the age range, 7–81 years) with a total of 493
cyst wall, aspiration of cyst contents, instillation cyst through US guidance. A stopcock was cysts. Of the cysts, 317 were Gharbi type
and reaspiration of the scolicidal agent.
attached to the catheter to prevent air es- I (WHO CE 1) and 176 were Gharbi type II
• In our study, we performed the PAIR procedure cape into the cyst during aspiration and in- (WHO CE 3A). All patients were treated with
by directly entering into the hydatid cyst cavity
jection. All cyst content was aspirated and albendazole for prevention of peritoneal
through a single puncture using a trocar catheter
instead of placing a catheter through stiff wire the cyst was filled with a mixture of nonion- dissemination of the cyst content, except
after puncturing with a Seldinger needle. ic contrast medium and saline solution (½ six patients who were intolerant to the drug.
• This novel modified PAIR technique may contrast medium + ½ saline solution [0.09% Trocar catheter was applied successfully
be superior to catheterization by Seldinger NaCl]) equal to the amount of aspirate. A in all cysts. Mean diameter of the cysts was
technique due to its efficiency, easier cystogram was then obtained in two planes 76 mm, ranging from 33 mm to 221 mm.
application, lower severe complication rate,
and lower cost. (anteroposterior and lateral) to check any In cystograms obtained from 493 cysts,
communication between the cyst cavity cystobiliary fistulization was observed in

48 • January–February 2016 • Diagnostic and Interventional Radiology Nayman et al.

13 cases (Fig. 1). These cysts were consid- by MRI for multiple cysts), and serologic treatment is surgical; however, mortality
ered inappropriate for alcohol injection tests were not utilized. (0%–6.3%), complication (12.5%–80%), and
and referred to surgery. In the remaining Complications were usually minor and recurrence (2.2%–22%) rates of this mo-
480 cysts of 361 patients, 469 cysts (97.7%) transient. Minor complications were fever dality are high (8–10). Medical treatment
were treated successfully (Figs. 2, 3), while (n=14, 3.7%), urticaria-like reactions (pru- alone is not efficient, but it can be used as
11 cysts (2.2%) recurred. A distended ap- ritus, mild skin rash, transient allergic reac- an adjunct before or after the percutaneous
pearance or lack of reduction in cyst size tion) (n=23, 6.1%), and biliary fistula (n=7, treatment as a prophylaxis for abdominal
was considered as a sign of recurrence. 1.9%). The only major complication was dissemination (9, 11). Percutaneous treat-
All recurrences were detected in the first anaphylaxis observed in two cases (0.55%), ment of the hydatid cyst is a reliable, effi-
month. A second percutaneous interven- which quickly resolved by immediate inter- cient, and comfortable option, which has
tion was performed for all of the 11 recur- vention of the anesthesiology team. These been used widely in the last two decades.
rent cysts and nine of them were treated two patients had been given albendazole In our study, treatment of the hydatid cyst
successfully. Cystobiliary fistulas were prophylactically. No deaths occurred related was performed effectively by single punc-
detected during the second intervention to percutaneous treatment per se or its com- ture catheterization as a modification of the
in the remaining two recurrent cysts and plications. No alcoholemia was seen in any of PAIR procedure.
these cases were referred to surgery (Fig. the cases during or after the procedure. In a meta-analysis, the success rate of hy-
4). Cysts with reduced size and loss of dis- All patients were hospitalized overnight datid cyst treatment by the PAIR procedure
tended appearance after the first month because of catheterization; 46 patients were with albendazole or mebendazole prophy-
showed no increase in size at six-month, hospitalized 2–17 days (mean, 1.6 days) due laxis was found to be higher than that of
one-year, or two-year follow-up exams. to complications. Prolonged hospitalization surgery. The success rates of the PAIR and
Mean follow-up time was 21.6±1.8 months
of the patient who stayed in the hospital for surgery were reported as 95.8% (737/769)
and there were no further follow-ups after
17 days was due to patient’s multiple cysts and 89.8% (855/952), respectively, and the
two years. During the follow-up the pa-
which required four sessions of the proce- difference was statistically significant. The
tients were evaluated by US (additionally
dure. This patient had urticaria as well. success rate was 97.7% (469/480) in our
study. In addition, lower recurrence rates
Discussion were reported in percutaneous treatment
compared with surgery (12). In our study,
Our results suggest that our novel modi- the recurrence rate was 2.2%.
fied PAIR technique may have easy applica- Previous studies in which the patients
tion, high success rate, lower severe com- were given albendazole or mebendazole
plication rate, and lower cost. In addition, preoperatively and postoperatively varied
to the best of our knowledge, this is the in terms of dose and duration of the med-
largest study on percutaneous treatment of ication. In studies reporting the length of
hydatid cysts in the literature. medical treatment period precisely, pa-
The gold standard treatment of the hy- tients were given albendazole or meben-
datid cyst remains controversial. In WHO dazole for a median of 7 days (range, 4
informal working group on echinococcosis hours to 15 days) before the drainage and
2010 guidelines, it is stated that possible for a median of 28 days (range, 4 hours to
methods for the treatment of the hydatid 6 months) after the procedure. Albendazole
Figure 1. Cystogram in the anteroposterior plane
obtained during the procedure shows cystobiliary cyst have not been compared and there is 10–20 mg/kg per day or mebendazole 10–
communication. no “best treatment option” (7). Traditional 50 mg/kg per day have been used in differ-

a b c

Figure 2. a–c. A 13-year-old girl with hepatomegaly. CT image obtained before the intervention (a) shows a giant type I hydatid cyst of the liver. Cystogram
in the anteroposterior plane obtained during the procedure (b) shows no cystobiliary communication. Sonogram obtained at six-month follow-up (c) shows
increasingly settling solid component.

A novel PAIR technique for percutaneous treatment of liver hydatid cysts • 49

 a b abscess, peritoneal leakage, subcapsular
hematoma, active arterial hemorrhage,
intracystic bleeding or gallbladder hem-
orrhage, pleural effusion/pneumothorax,
transient hypernatremia, and other unclas-
sified reversible complications. Lethal ana-
phylactic shock is the most feared compli-
cation of the percutaneous treatment of the
hydatid disease. The rates of reversible and
irreversible anaphylactic shock were report-
ed as 1.67% (99/5943) and 0.03% (2/5943),
respectively in a meta-analysis by Neumayr
c d
et al. (16). No fatal anaphylactic shock  oc-
curred in our study, but reversible anaphy-
lactic shock was encountered in two cases
(0.55%, 2/370).
Surgical treatment of the hydatid cyst is
associated with prolonged hospitalization.
The length of stay in hospital was report-
ed to be 10 days on average (range, 4.6–15
days) (17, 18). Laparoscopic surgery of the
hydatid cyst, which requires a shorter hos-
pitalization than laparotomy, became pop-
ular in recent years and the length of hospi-
Figure 3. a–d. A 63-year-old woman with twenty-three hydatid cysts in the liver and one in the spleen. talization for this method was reported as
All cysts were treated in four sessions. Coronal T2-weighted image (a) shows multiple cysts in the liver. In 4.7 days (range, 2–8 days) in a meta-analysis
every session, the patient was given a maximum of 30 mL prilocaine hydrochloride prophylactically for (19). The mean length of hospital stay in the
the prevention of methemoglobinemia related to local anesthetics overdose (b). After administration of
local anesthesia in three different regions, eight cysts were treated using trocar. Fluoroscopic image (c) literature for percutaneous treatment of
shows the ablation of the cysts with alcohol. Size reduction in all cysts and detachment of membranes the hydatid cyst is 2.4 days (range, 1.6–4.2
are seen in coronal T2-weighted image (d) obtained one year later. days); however, outpatient percutaneous
treatment has also been reported (12, 15).
ent studies. In our study, patients received instantly with direct single puncture and In our study, the mean length of hospital-
albendazole 10 mg/kg per day before the PAIR is performed. This technique allows ization was 1.6 days (range, 1–17 days), con-
procedure, for three weeks. Hypertonic sa- catheterization and PAIR procedure to be sistent with the previous literature.
line or absolute alcohol is frequently used performed in an easy manner. The larger series in the literature mostly
as scolicidal agents. Administration of silver Among percutaneous treatment options, discuss surgical treatment options, whereas
nitrate, mebendazole, albendazole, and po- PAIR procedure performed with Chiba, percutaneous treatment series include few-
lidocanol has been reported in individual Seldinger, or guiding needle is more cost-ef- er patients. To the best of our knowl­edge,
our study is the largest series reporting per-
studies (12–14). Absolute alcohol was the fective compared with catheterization. How-
cutaneous treatment in the literature (20).
scolicidal agent in our study. No scolicidal ever, it has some disadvantages such as the
Our study has some limitations. The main
agents were used in patients with cystobi- difficulty of keeping the tip of the needle
limitation of this study is its retrospective
liary fistulas due to possible chemical scle- steady within the cavity of the cysts that are
and nonrandomized nature. The fact that
rosing effects of these compounds (13). located in regions hard to reach such as the
we included consecutive subjects with
In the Seldinger technique, after the dome of the liver, or clogging of the needle
Gharbi type 1 and 2 cysts, but not subjects
puncture of the cyst using a Seldinger, Chi- tip by membranes during the PAIR steps.
with Gharbi type 3 or 4 is another limitation.
ba, or guiding needle, the cyst is drained to Catheterization by Seldinger technique is a Exclusion of patients with cystobiliary fistu-
a certain extent to reduce the inner hydro- more controlled and comfortable method las from PAIR procedure can be considered
static pressure and prevent dissemination than the PAIR procedure (15). Our meth- as another limitation as well.
during catheterization. Then the tract is od may be superior to catheterization by In conclusion, this study confirms that it
dilated with fascial dilator and the catheter Seldinger technique (via Seldinger needle, is possible to treat hydatid disease in a min-
is placed. Manipulation of the dilator and stiff wire, dilator, catheter) owing to its easier imally invasive manner with a new modified
catheter over the wire during the proce- application and lower cost. PAIR technique. Percutaneous treatment of
dure may cause leakage of the cyst content The potential complications of pre- and hydatid cyst with a trocar catheter may be at
into the abdominal cavity and this can re- postprocedure include fever, hypotensive least as effective and applicable as the stan-
sult in anaphylaxis. In the trocar technique, reaction, vasovagal reaction, nausea, vomit- dard catheterization technique and it may
the catheter is placed into the cyst cavity ing, biliary fistula/rupture, cavity infection/ be an effective alternative to conventional

50 • January–February 2016 • Diagnostic and Interventional Radiology Nayman et al.

 8. Mentes A. Hydatid liver disease: a perspective in
treatment. Dig Dis 1994; 12:150–160. [CrossRef]
9. Akhan O, Ozmen MN, Dincer A, Sayek I, Goc-
493 cysts/374 patients men A. Liver hydatid disease: long-term results
of percutaneous treatment. Radiology 1996;
317 cysts 176 cysts
198:259–264. [CrossRef]
(Gharbi type 1) (Gharbi type 2) 10. Dawson JL, Stamatakis JD, Stringer MD, Wil-
liams R. Surgical treatment of hepatic hydatid
First treatment disease. Br J Surg 1988; 75:946–950. [CrossRef]
11. Akhan O, Gumus B, Akinci D, Karcaaltincaba M,
Ozmen M. Diagnosis and percutaneous treat-
ment of soft-tissue hydatid cysts. Cardiovasc
480 cysts treated 13 cystobiliary Intervent Radiol 2007; 30:419–425. [CrossRef]
12. Smego RA, Bhatti S, Khaliq AA, Beg MA. Per-
successfully fistula cutaneous aspiration-injection-reaspiration
drainage plus albendazole or mebendazole for
One-month follow-up hepatic cystic echinococcosis: a meta-analysis.
Clin Infect Dis 2003; 37:1073–1083. [CrossRef]
13. Paksoy Y, Odev K, Sahin M, Arslan A, Koc O.
Percutaneous treatment of liver hydatid cysts:
comparison of direct injection of albenda-
No recurrence Recurrence Surgery
zole and hypertonic saline solution. AJR Am J
Roentgenol 2005; 185:727–734. [CrossRef]
(469 cysts) (11 cysts) 14. Ormeci N, Soykan I, Bektas A, et al. A new
percutaneous approach for the treatment of
Second treatment hydatid cysts of the liver. Am J Gastroenterol
2001; 96:2225–2230. [CrossRef]
15. Koroglu M, Erol B, Gurses C, et al. Hepatic cys-
tic echinococcosis: Percutaneous treatment as
an outpatient procedure. Asian Pac J Trop Med
9 cysts treated 2 cystobiliary 2014; 7:212–215. [CrossRef]
successfully fistula 16. Neumayr A, Troia G, de Bernardis C, et al. Jus-
tified concern or exaggerated fear: the risk of
anaphylaxis in percutaneous treatment of cystic
echinococcosis-a systematic literature review.
PLoS Negl Trop Dis 2011; 5:1154. [CrossRef]
6-month, 1-year, and 2-year follow-ups 17. Gupta N, Javed A, Puri S, Jain S, Singh S, Agarwal
AK. Hepatic hydatid: PAIR, drain or resect? J Gas-
trointest Surg 2011; 15:1829–1836. [CrossRef]
18. Birnbaum DJ, Hardwigsen J, Barbier L, Bouchi-
ba N, Le Treut YP. Is hepatic resection the best
treatment for hydatid cyst? J Gastrointest Surg
No recurrence 2012; 16:2086–2093. [CrossRef]
19. Citgez B, Battal M, Cipe G, Karatepe O, Mus-
(478 cysts) lumanoglu M. Feasibility and safety of laparo-
scopic hydatid surgery: a systematic review.
Figure 4. Patient and hydatid cysts flowchart. Of 374 patients with 493 hydatid cysts enrolled in the Hepatogastroenterology 2013; 60:784–788.
study, fifteen were not able to receive PAIR treatment and were redirected to surgery. Recurrence was 20. Agaev R. Surgical treatment of hepatic echino-
observed in 11 cysts at one month. There was no recurrence in 478 cysts at six-month, one-year, and coccosis and its complications. Khirurgiia 2000;
two-year follow-ups. 2:32–36.

PAIR procedure or standard catheterization 4. Yagci G, Ustunsoz B, Kaymakcioglu N, et al. Re-

method, considering its cost-effectiveness sults of surgical, laparoscopic, and percutane-
ous treatment for hydatid disease of the liver:
and low complication rates. 10 years experience with 355 patients. World J
Surg 2005; 29:1670–1679. [CrossRef]
Conflict of interest disclosure 5. Gabal AM, Khawaja FI, Mohammad GA. Mod-
The authors declared no conflicts of interest. ified PAIR technique for percutaneous treat-
ment of high-risk hydatid cysts. Cardiovasc
Intervent Radiol 2005; 28:200–208. [CrossRef]
References 6. Giorgio A, Di Sarno A, de Stefano G, et al. Per-
1. Safioleas MC, Misiakos EP, Kouvaraki M, Sta-
cutaneous treatment of hydatid liver cyst. Re-
matakos MK, Manti CP, Felekouras ES. Hydatid
cent Pat Antiinfect Drug Discov 2009; 4:29–36.
disease of the liver: a continuing surgical prob-
[CrossRef]
lem. Arch Surg 2006; 141:1101–1108. [CrossRef]
7. Brunetti E, Kern P, Vuitton DA. Writing Panel
2. Polat P, Kantarci M, Alper F, Suma S, Koruyucu
for the W-I. Expert consensus for the diagnosis
MB, Okur A. Hydatid disease from head to toe.
and treatment of cystic and alveolar echino-
Radiographics 2003; 23:475–494. [CrossRef]
coccosis in humans. Acta Trop 2010; 114:1–16.
3. Akhan O, Ozmen MN. Percutaneous treat-
[CrossRef]
ment of liver hydatid cysts. Eur J Radiol 1999;
32:76–85. [CrossRef]

A novel PAIR technique for percutaneous treatment of liver hydatid cysts • 51