Original Article
Percutaneous Drainage Compared with Surgery for Hepatic Hydatid Cysts
N Engl J Med 1997; 337:881-887September 25, 1997
- Abstract
Background
In recent years percutaneous drainage has been used successfully to treat the hepatic hydatid cysts of echinococcal disease. We performed a controlled trial to compare the safety and efficacy of percutaneous drainage with those of surgical cystectomy, the traditional treatment.
Methods
In a prospective study, we randomly assigned 50 patients with hepatic hydatidosis to treatment with percutaneous drainage (25 patients) or cystectomy (25). Albendazole (10 mg per kilogram of body weight per day for eight weeks) was administered to the patients who underwent percutaneous drainage. Serial assessments included clinical and biochemical examinations, ultrasonography, and serologic tests of echinococcal-antibody titers.
Results
The mean (±SD) hospital stay was 4.2±1.5 days in the drainage group and 12.7±6.5 days in the surgery group (P<0.001). Over a mean follow-up period of 17 months, the mean cyst diameter decreased from 8.0±3.0 to 1.4±3.5 cm (P<0.001) after percutaneous drainage and from 9.1±3.0 to 0.9±1.8 cm (P<0.001) after surgery. The final cyst diameter did not differ significantly between the two groups (P = 0.20). The cysts disappeared in 22 patients (88 percent) in the drainage group and in 18 (72 percent) in the surgery group (P = 0.29). After an initial rise, the echinococcal-antibody titers fell progressively and at the last follow-up were negative (<1:160) in 19 patients (76 percent) in the drainage group and 17 (68 percent) in the surgery group (P = 0.74). There were procedure-related complications in 8 patients (32 percent) in the drainage group and 21 (84 percent) in the surgery group, 17 of whom had fever postoperatively (P<0.001).
Conclusions
Percutaneous drainage, combined with albendazole therapy, is an effective and safe alternative to surgery for the treatment of uncomplicated hydatid cysts of the liver and requires a shorter hospital stay.
Media in This Article
Figure 3
Kaplan–Meier Estimate of the Probability of the Disappearance of the Cyst (Cure) in Patients Treated with Percutaneous Drainage or Surgery (P = 0.50 by the Log-Rank Test).Figure 2
Mean (±SE) Cyst Diameter in Patients Treated with Percutaneous Drainage or Surgery.Article Activity
- Article
Human echinococcosis is a zoonotic infection caused by larval forms (metacestodes) of the tapeworm of the genus echinococcus found in the small intestines of carnivores. Human infection is acquired from ingestion of the parasite eggs from infected animals.1 Echinococcus granulosus causes cystic echinococcosis in humans, a condition that is found throughout the world and is endemic in large sheep-raising areas in Europe, Asia, the Mediterranean, South America, and northern Kenya.2 With immigration, the prevalence of the disease has increased in Europe and North America.
The most frequent site of hydatid cysts is the liver (accounting for 50 to 70 percent of cases), followed by the lungs (20 to 30 percent), and less frequently, the spleen, kidneys, heart, bones, central nervous system, and elsewhere. Cystic echinococcosis is usually asymptomatic, but a substantial number of infections cause morbidity, with occasional mortality. Hepatic hydatid cysts can rupture into the peritoneum, leading to anaphylaxis or peritoneal dissemination or both; into the biliary tract, causing cholangitis or cholestasis or both; or into the pleura or lung, causing pleural hydatidosis or bronchial fistula. Cysts may become infected and form liver abscesses. Pressure or mass effects on the bile ducts, portal veins, and hepatic veins and inferior vena cava can cause cholestasis, portal hypertension, and the Budd–Chiari syndrome, respectively.1-3
Surgery is the recommended treatment for hepatic hydatid cysts.1-3 However, drug therapy and percutaneous drainage have recently been introduced as alternative treatments.2 Two benzimidazoles (mebendazole and albendazole) have scolicidal activity but are clinically effective in less than 30 percent of patients with hepatic hydatidosis.4-7 Percutaneous drainage is minimally invasive and very effective in the treatment of hepatic hydatidosis.8-14 Studies of large numbers of patients followed for up to five years have shown that the risk of anaphylaxis is negligible, and regrowth of cysts does not occur.15-17 We previously performed a prospective randomized trial of percutaneous drainage as compared with albendazole therapy in patients with hepatic hydatidosis.18 We now report on a prospective randomized study of percutaneous drainage compared with surgery in 50 patients with hepatic hydatidosis.
Methods
Patients
All patients (>14 years of age) with hydatid cysts in the liver who presented at our institution between September 1992 and August 1995 were considered candidates for the study. A patient was enrolled if he or she had symptoms and signs of a hepatic mass caused by a hydatid cyst and if the cyst had a prominent fluid component that appeared anechoic or hypoechoic with marked enhancement of back-wall echoes. Women were excluded if they were pregnant or intended to conceive during the study period.
Hepatic hydatidosis was diagnosed in 62 patients during the study period, 12 of whom were excluded because of infected cysts (5 patients), cysts with a hyperechoic solid pattern or calcified walls (4), or cysts with biliary rupture (3). Of the remaining 50 patients, 22 were male and 28 were female, with a mean (±SD) age of 34±14 years. All the patients gave written informed consent. On ultrasonographic examination, 32 patients had univesicular cysts, which were rounded with well-defined borders and contained pure fluid, and 18 had multivesicular cysts, with pure fluid in each vesicle. The patients were randomly assigned to receive treatment with percutaneous drainage (25 patients) or surgery (25).
Percutaneous Drainage
All patients undergoing percutaneous drainage were treated with albendazole, administered orally in a dose of 10 mg per kilogram of body weight per day for eight weeks.18 Percutaneous drainage was performed on the 10th day of the drug regimen, under aseptic conditions, with continuous ultrasonographic guidance and close monitoring for complications, such as anaphylaxis, asthma, or laryngeal edema. The location of the cyst was defined in three planes with ultrasonography, and the relation of the cyst to the normal liver was delineated. The puncture site was selected so that the cyst could be approached through thick normal liver tissue, preferably by the intercostal route.
The procedure was performed in three steps (Figure 1AFigure 1
Hydatid Cyst of the Liver in a Patient Who Underwent Percutaneous Drainage., Figure 1B, Figure 1C, and Figure 1D). In step 1, the cyst was punctured through the biopsy port of the puncture probe (3.5 MHz) with the use of a 5-French, 40-cm-long transhepatic catheter made of radiopaque polyethylene (Cook Europe, Bjaeverskov, Denmark), and the contents were rapidly aspirated. In the patients with multivesicular cysts, a 22-gauge, 20-cm-long cholangiography needle (Cook Europe) was used to puncture and treat each daughter cyst. In step 2, the cyst cavity was nearly filled with sterile hypertonic (20 percent) saline, which was left in the cavity for 20 minutes. In step 3, the cyst was aspirated completely, and the cavity was irrigated and left partially filled with sterile normal (0.9 percent) saline to minimize exudation or bleeding from the pericyst. During aspiration and irrigation, the separation of the endocyst from the pericyst was observed on real-time ultrasonography.The cyst fluid was subjected to cytologic and microbiologic examination.19,20 For cytologic examination, the fluid was centrifuged and the sediment examined for fragments of the laminated membrane, hooklets, and scoleces. The viability of the scoleces was assessed by observing their motility on immediate microscopy and by staining with neutral eosin. The procedure was considered successful if the reaspirated fluid revealed nonviable scoleces.
After the procedure, the patient was observed for 48 hours and then discharged from the hospital if there were no complications.
Surgery
The surgical procedure was a simple cystectomy and drainage of the residual contents of the cyst cavity.1 The abdomen was opened through a subcostal incision, and the abdominal viscera were examined, with particular attention to potential sites of dissemination, including the pelvis. The operative field was packed with swabs soaked with 10 percent povidone–iodine. The cyst was punctured and decompressed with the use of a 14-gauge needle connected to a 50-ml syringe. A sump-type cannula was introduced through the puncture site, and the cyst contents were aspirated with the use of a large-capacity reservoir and high-pressure suction. A 3-to-4-cm incision was then made at the puncture site, the cyst was opened up, and the remaining contents, including the laminated membrane, were removed with a sponge-holding forceps. The cavity of the cyst was carefully inspected for biliary communication and scrubbed with swabs soaked with povidone–iodine. Intermittent sutures were placed in the cavity of the cyst from inside, and a tube was kept in the cavity for drainage. The drain was removed on the sixth postoperative day. A cavogram was obtained before the removal of the tube in order to rule out biliary communication.
Follow-up
At the time of enrollment, at one and three months, and subsequently every three months, the following studies were performed: a clinical examination, a urine test for albumin and sediment, blood counts, liver-function tests, kidney-function tests (measurements of serum urea and creatinine), abdominal ultrasonography, and measurement of serum echinococcal-antibody titers. The ultimate goal of treatment was the disappearance of the cyst. Other important measures of efficacy included the appearance and size of the cyst over time, the length of the hospital stay, and any complications related to the procedure. A secondary measure of efficacy was the serum echinococcal-antibody titer over time.
All ultrasonographic examinations were documented on hard copies, which were evaluated by two of us in a blinded fashion. Ultrasonography was performed with a real-time, gray-scale ultrasound unit (SSD 630, Aloka, Tokyo, Japan) and a 3.5-MHz probe. The diameter and echo pattern of the cysts were documented. In addition, the liver, biliary tree, and other abdominal organs were carefully examined for evidence of residual cysts.21,22
After percutaneous drainage or surgery, the cysts underwent a sequence of sonographic changes — namely, the appearance of high-level internal echoes (a heterogeneous pattern), obliteration by echogenic material (a pseudotumor pattern), decreased echogenicity, and finally, a normal pattern of echoes. The cyst was considered to have disappeared if it was no longer visualized on ultrasonography and the area was replaced by an ill-defined echogenic area or a normal echo pattern.
IgG antibodies to E. granulosus were measured by an enzyme-linked immunosorbent assay. An antibody titer higher than 1:160 was considered positive.23
The study protocol was approved by the Postgraduate Scientific and Research Committee of the Sheri-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India.
Statistical Analysis
Serum antibody titers were analyzed with the use of the log of the antibody values. Comparisons of discrete variables were analyzed with Fisher's exact test, and comparisons of continuous variables were analyzed with a two-sample t-test for two independent samples and a paired t-test for paired observations. In addition, we calculated the difference between group means (for continuous variables) and odds ratios (for proportions), along with 95 percent confidence intervals. Repeated-measures analysis of variance was used to compare multiple variables over time between the two groups. A Kaplan–Meier analysis was used to determine the proportion of patients in whom cysts disappeared (those with cures) on long-term follow-up, and these differences were evaluated with the log-rank test. Except where otherwise noted, all values are expressed as means ±SD. All P values are two-sided, and a P value of less than 0.05 was considered to indicate statistical significance.24
Results
The base-line characteristics of the patients in the two groups did not differ significantly (Table 1Table 1
Base-Line Characteristics of the Patients in the Two Treatment Groups.). All the patients received the assigned treatment. Percutaneous drainage was successful in all 25 patients assigned to this treatment. Likewise, cystectomy and tube drainage were successful in all 25 patients assigned to surgery. The hospital stay was significantly shorter for the patients treated with percutaneous drainage than for those treated with surgery. After discharge from the hospital, all patients were followed, and the mean follow-up period did not differ significantly between the two treatment groups (Table 2Table 2
Outcomes and Complications after Percutaneous Drainage or Surgery.).Cyst Size
In the drainage group, the mean diameter of the cyst was 8.0±3.0 cm before treatment and 1.4±3.5 cm at the last follow-up examination (P<0.001; mean difference, 7.2; 95 percent confidence interval, 5.1 to 9.4). The cyst diameter in the surgery group decreased from 9.1±3.0 cm before treatment to 0.9±1.8 cm at the last examination (P<0.001; mean difference, 8.6; 95 percent confidence interval, 7.1 to 10.1). The analysis of cyst diameter at follow-up excluded data from two patients in each group, who received additional treatments because of cyst infection (in one patient) or biliary rupture (in three). The cyst diameters at the last follow-up examination (Table 2) and across the 10 examinations (Figure 2Figure 2
Mean (±SE) Cyst Diameter in Patients Treated with Percutaneous Drainage or Surgery.) did not differ significantly between the two treatment groups.Disappearance of Cysts
In 22 patients (88 percent) in the drainage group and 18 (72 percent) in the surgery group, the cysts disappeared (P = 0.29; odds ratio, 2.9; 95 percent confidence interval, 0.6 to 10.6). The probability that cysts would disappear over follow-up periods in the two groups did not differ significantly (P = 0.5 by the log-rank test) (Figure 3Figure 3
Kaplan–Meier Estimate of the Probability of the Disappearance of the Cyst (Cure) in Patients Treated with Percutaneous Drainage or Surgery (P = 0.50 by the Log-Rank Test).). After percutaneous drainage, 14 univesicular cysts (88 percent) had disappeared, compared with 8 multivesicular cysts (89 percent) (P = 0.94). Similarly, after surgery, 11 univesicular cysts (69 percent) had disappeared, as compared with 7 multivesicular cysts (78 percent) (P = 0.99). None of the patients had an increase in the diameter of the cyst or growth of secondary vesicles in or outside the liver during follow-up.Serologic Studies
Three patients (12 percent) in the drainage group and six (24 percent) in the surgery group had a fourfold rise in antibody titers in the first three months after the procedure (P = 0.46; odds ratio, 2.3; 95 percent confidence interval, 0.5 to 8.9). The antibody titers across the 10 follow-up examinations were higher in the surgery group than in the drainage group (P<0.05 by repeated-measures analysis of variance). At the last follow-up examination, 19 patients (76 percent) in the drainage group and 17 (68 percent) in the surgery group had negative titers (<1:160) (P = 0.74).
Complications
Table 2 shows the complications in the two treatment groups. After percutaneous drainage, one patient had transient hypotension, and two patients had urticaria. Three patients (12 percent) in the drainage group and 17 (68 percent) in the surgery group had fever within 24 hours after the procedure (P<0.001; odds ratio, 15.6; 95 percent confidence interval, 3.4 to 64.7). Cultures of cyst fluid obtained from the cysts during puncture or from the drainage tube failed to document a microbial cause of fever. In all 20 patients, the fever resolved within 48 hours with symptomatic treatment. The drainage tube was removed on the sixth postoperative day from all except two patients in the surgery group. One patient required prolonged drainage, with the tube removed after three weeks. The other patient had evidence of infection in the cyst within three days after surgery, requiring reexploration and drainage of the cyst abscess. One patient in the drainage group had evidence of infection in the cyst at 18 months, requiring surgical exploration and drainage of the cyst abscess. One patient in the drainage group and two patients in the surgery group had biliary symptoms (cholangitis in two patients and cholestasis in one) at three months. Cyst–biliary communication was suspected on the basis of ultrasonographic studies and was confirmed by endoscopic retrograde cholangiopancreatography. Two patients (one in each group) were treated with endoscopic sphincterotomy and basketing of the contents of the ruptured cyst, and the third patient (in the surgery group) underwent reexploration, drainage of the bile duct, and a repair of the incisional hernia. There were no procedure-related deaths in either group.
Discussion
In our study, the surgical treatment for managing hydatid cysts in the liver was simple cystectomy.25 We first used the technique of percutaneous drainage of hydatid cysts in 1988, and we used this approach in 75 patients before performing the current study.10 Patients treated with percutaneous drainage received albendazole therapy on the basis of data from our previous randomized, prospective study of drainage versus albendazole therapy.18 Since there are no published data on the merits of albendazole therapy in patients undergoing surgery for hepatic hydatidosis, the drug was not used in the patients in the surgery group. We believe that the use of different scolicidal agents in the two treatment groups did not influence the results of the study. Our aim was not to compare the efficacy of different scolicidal agents but instead to compare the therapeutic effects of a new procedure with those of standard surgical treatment.26-29 During surgery, we did not inject the scolicidal agent into an intact cyst but instead swabbed the residual cyst cavity with povidone–iodine, after the laminated membrane and daughter cysts had been removed.26 The instillation of scolicidal agents into the cyst cavity at surgery has been associated with severe systemic or biliary complications, possibly caused by breaks in the laminated membrane and contact between the scolicidal agent and liver tissue around the cyst, with eventual systemic absorption or biliary spillage.30,31 In fact, most investigators who have extensive experience with the surgical treatment of hepatic hydatidosis do not instill scolicidal agents in the cyst cavity. During percutaneous drainage, the scolicidal agent is instilled in the cyst cavity through a needle puncture under ultrasonographic guidance, and the instilled fluid does not come into contact with the pericyst. Systemic absorption or biliary spillage is thus avoided. We have not observed any systemic or biliary complications related to the instillation of the scolicidal agent in the cyst cavity during percutaneous drainage.
The final diameter of the cyst and its disappearance on follow-up (overall and across the 10 examinations) did not differ significantly between the two treatment groups. After percutaneous drainage, the cyst was filled with nonviable remnants of the scoleces, daughter cysts, and laminated membrane, resulting in the obliteration of the cyst cavity. In contrast, at surgery all the contents of the cyst were removed, leaving a cavity that was subsequently filled by the exudate from the pericyst. It is generally believed that drainage is indicated only for univesicular cysts, and the procedure may be technically difficult in the case of multivesicular cysts. However, data from this study and our earlier studies show that percutaneous drainage is effective for both univesicular and multivesicular cysts.10,18
After both percutaneous drainage and surgery, the titer of antibodies to E. granulosus rose, possibly because of spillage and systemic absorption of the contents of the cyst. A rise in the antibody titer was more frequent and higher in the surgery group than in the drainage group, suggesting that there was more spillage of the cyst contents after surgery.
The complications were similar in the two groups. Fever after either procedure may have resulted from a reaction to the absorbed scolicidal agent or cyst contents or from aseptic inflammation of the cyst cavity.10,18 The significantly higher percentage of patients with fever after surgery was presumably due to systemic absorption of larger quantities of the scolicidal agent or hydatid contents or both during surgery than during percutaneous drainage. The abscess in one patient in the postoperative period was caused by ineffective cyst drainage. However, the delayed development of an abscess in another patient after percutaneous drainage was presumably related to delayed resolution, with residual dead cyst contents forming a focus for bacterial infection. Cyst–biliary communication after percutaneous drainage or surgery is caused by decompression of the cyst and can be managed endoscopically.10,18,32 One patient in the drainage group had short-lasting hypotension, and two patients in the drainage group had urticaria. Although serious allergic manifestations after the puncture of a cyst are reported to be rare, one of our patients may have had anaphylaxis. This possibility makes close monitoring mandatory during percutaneous drainage, with facilities available for treating potential complications, especially anaphylaxis and laryngeal edema.10,17,18
Percutaneous drainage of uncomplicated hepatic hydatid cysts can be performed safely and results in the disappearance of the cyst. The efficacy of percutaneous drainage is similar to that of standard treatment with cystectomy, in terms of reducing the size of the cyst and causing its disappearance over a period of up to two years. The advantages of percutaneous drainage include a shorter hospital stay and a lower complication rate.
Source Information
From the Departments of Gastroenterology (M.S.K., G.J., B.A.K., G.N.Y., A.H.S., S.G.J.) and General Surgery (N.A.W.), Sheri-Kashmir Institute of Medical Sciences, Srinagar, Kashmir, India.
Address reprint requests to Professor Khuroo, Section of Gastroenterology, Department of Medicine (MBC 46), King Faisal Specialist Hospital and Research Centre, P.O. Box 3354, Riyadh 11211, Saudi Arabia.
- References
References
1
Milicevic M. Hydatid disease. In: Blumgart LH, ed. Surgery of the liver and biliary tract. 2nd ed. Vol. 2. Edinburgh, Scotland: Churchill Livingstone, 1994:1121-50.
2
Ammann RW ,Eckert J . Cestodes: Echinococcus. Gastroenterol Clin North Am 1996;25:655-689
CrossRef | Web of Science | Medline3
WHO Informal Working Group on Echinococcosis
Web of Science | Medline4
Gil-Grande LA ,Boixeda D ,Garcia-Hoz F , et al. Treatment of liver hydatid disease with mebendazole: a prospective study of thirteen cases. Am J Gastroenterol 1983;78:584-588
Web of Science | Medline5
Morris DL ,Dykes PW ,Marriner S , et al. Albendazole -- objective evidence of response in human hydatid disease. JAMA 1985;253:2053-2057
CrossRef | Web of Science | Medline6
Teggi A ,Lastilla MG ,De Rosa F . Therapy of human hydatid disease with mebendazole and albendazole. Antimicrob Agents Chemother 1993;37:1679-1684
Web of Science | Medline7
Gil-Grande LA ,Rodriguez-Caabeiro F ,Prieto JG , et al. Randomised controlled trial of efficacy of albendazole in intra-abdominal hydatid disease. Lancet 1993;342:1269-1272
CrossRef | Web of Science | Medline8
Filice C ,Pirola F ,Brunetti E ,Dughetti S ,Strosselli M ,Foglieni CS . A new therapeutic approach for hydatid liver cysts: aspiration and alcohol injection under sonographic guidance. Gastroenterology 1990;98:1366-1368
Web of Science | Medline9
Gargouri M ,Ben Amor N ,Ben Chehida F , et al. Percutaneous treatment of hydatid cysts (Echinococcus granulosus). Cardiovasc Intervent Radiol 1990;13:169-173
CrossRef | Web of Science | Medline10
Khuroo MS ,Zargar SA ,Mahajan R . Echinococcus granulosus cysts in the liver: management with percutaneous drainage. Radiology 1991;180:141-145
Web of Science | Medline11
Acunas B ,Rozanes I ,Celik L , et al. Purely cystic hydatid disease of the liver: treatment with percutaneous aspiration and injection of hypertonic saline. Radiology 1992;182:541-543
Web of Science | Medline12
Giorgio A ,Tarantino L ,Francica G , et al. Unilocular hydatid liver cysts: treatment with US-guided, double percutaneous aspiration and alcohol injection. Radiology 1992;184:705-710
Web of Science | Medline13
Simonetti G ,Profili S ,Sergiacomi GL ,Meloni GB ,Orlacchio A . Percutaneous treatment of hepatic cysts by aspiration and sclerotherapy. Cardiovasc Intervent Radiol 1993;16:81-84
CrossRef | Web of Science | Medline14
Bastid C, Azar C, Doyer M, Sahel J. Percutaneous treatment of hydatid cysts under sonographic guidance. Dig Dis Sci 1994;39;1576-80.
15
Akhan O ,Ozmen MN ,Dincer A ,Sayek IS ,Gocmen A . Liver hydatid disease: long-term results of percutaneous treatment. Radiology 1996;198:259-264
Web of Science | Medline16
Schiller CF . Complications of echinococcus cyst rupture: a study of 30 cases. JAMA 1966;195:220-222
CrossRef | Web of Science | Medline17
Placer C ,Bordas JM ,Frias FJ ,Sacristan B . The management of hydatid liver cysts with aspiration and alcohol. Gastroenterology 1991;100:290-290
Web of Science | Medline18
Khuroo MS ,Dar MY ,Yattoo GN , et al. Percutaneous drainage versus albendazole therapy in hepatic hydatidosis: a prospective, randomized study. Gastroenterology 1993;104:1452-1459
Web of Science | Medline19
Smyth JD ,Barrett NJ . Procedures for testing the viability of human hydatid cysts following surgical removal, especially after chemotherapy. Trans R Soc Trop Med Hyg 1980;74:649-652
CrossRef | Web of Science | Medline20
Gori S ,Campatelli A ,Luchi S ,Paladini A ,Savalli E ,Scasso A . Cytology in the percutaneous treatment of hydatid cysts: a report of four cases. Acta Cytol 1993;37:423-426
Web of Science | Medline21
Zargar SA ,Khuroo MS ,Khan BA ,Dar MY ,Alai MS ,Koul P . Intrabiliary rupture of hepatic hydatid cyst: sonographic and cholangiographic appearances. Gastrointest Radiol 1992;17:41-45
CrossRef | Medline22
Yalin R ,Aktar AO ,Acikgozoglu S . Computed tomography and sonography of hydatid cysts of the liver after surgical treatment. J Med Imaging 1989;3:301-30523
Wattal C ,Malla N ,Khan IA ,Agarwal SC . Comparative evaluation of enzyme-linked immunosorbent assay for the diagnosis of pulmonary echinococcosis. J Clin Microbiol 1986;24:41-46
Web of Science | Medline24
Munro BH, Visintainer MA, Page EB. Statistical methods for health care workers. Philadelphia: J.B. Lippincott, 1986.
25
Morris DL . Echinococcus of the liver. Gut 1994;35:1517-1518
CrossRef | Web of Science | Medline26
Ekrami Y . Surgical treatment of hydatid disease of the liver. Arch Surg 1976;111:1350-1352
Web of Science | Medline27
Langer JC ,Rose DB ,Keystone JS ,Taylor BR ,Langer B . Diagnosis and management of hydatid disease of the liver: a 15-year North American experience. Ann Surg 1984;199:412-417
CrossRef | Web of Science | Medline28
Sayek I ,Yalin R ,Sanac Y . Surgical treatment of hydatid disease of the liver. Arch Surg 1980;115:847-850
Web of Science | Medline29
Karavias DD ,Vagianos CE ,Bouboulis N ,Rathosis S ,Androulakis J . Improved techniques in the surgical treatment of hepatic hydatidosis. Surg Gynecol Obstet 1992;174:176-180
Web of Science | Medline30
Castellano G ,Moreno-Sanchez D ,Gutierrez J ,Moreno-Gonzalez E ,Colina F ,Solis-Herruzo JA . Caustic sclerosing cholangitis: report of four cases and a cumulative review of the literature. Hepatogastroenterology 1994;41:458-470
Web of Science | Medline31
Tsimoyiannis EC ,Grantzis E ,Moutesidou K ,Lekkas ET . Secondary sclerosing cholangitis: after injection of formaldehyde into hydatid cysts in the liver. Eur J Surg 1995;161:299-300
Medline32
al Karawi MA ,Yasawy MI ,el Shiekh Mohamed AR . Endoscopic management of biliary hydatid disease: report on six cases. Endoscopy 1991;23:278-281
CrossRef | Web of Science | Medline
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Hiizir Yakup Akyıldız, Alper Akcan, İbrahim Karahan, Can Kucuk, Erdogan Sözüer, Hüseyin Esin. (2009) Recurrent liver hydatid disease: when does it become symptomatic and how does one diagnose it?. Clinical Imaging 33:1, 55-58
CrossRef24
P. Marco Fisichella, Kristen Donaldson, W. Scott Helton. (2008) Hepatic and Splenic Hydatidosis Managed with Percutaneous Aspiration, Injection, and Reaspiration (PAIR) of the Hepatic Cyst and Laparoscopic Splenectomy. Journal of Gastrointestinal Surgery 12:9, 1615-1617
CrossRef25
A. Giorgio, G. Stefano, V. Esposito, G. Liorre, A. Sarno, V. Giorgio, V. Sangiovanni, M. D. Iannece, N. Mariniello. (2008) Long-Term Results of Percutaneous Treatment of Hydatid Liver Cysts: a Single Center 17 Years Experience. Infection 36:3, 256-261
CrossRef26
P. Antonopoulos, K. Tavernaraki, G. Charalampopoulos, F. Constantinidis, A. Petroulakis, Ch. Drossos. (2008) Hydatid hepatic cysts rupture into the biliary tract, the peritoneal cavity, the thoracic cavity and the hepatic subcapsular space: specific computed tomography findings. Abdominal Imaging 33:3, 294-300
CrossRef27
Benedikt V. Czermak, Okan Akhan, Renate Hiemetzberger, Bettina Zelger, Wolfgang Vogel, Werner Jaschke, Michael Rieger, Sang Yoon Kim, Jae Hoon Lim. (2008) Echinococcosis of the liver. Abdominal Imaging 33:2, 133-143
CrossRef28
Gabriel Rodrigues, Prasad Seetharam. (2008) Management of Hydatid Disease (Echinococcosis) in Pregnancy. Obstetrical & Gynecological Survey 63:2, 116-123
CrossRef29
Bernhard Stamm, Marcela Fejgl, Cornelia Hueber. (2008) Satellite cysts and biliary fistulas in hydatid liver disease. A retrospective study of 17 liver resections. Human Pathology 39:2, 231-235
CrossRef30
L. Thanos, S. Mylona, P. Brontzakis, N. Ptohis, K. Karaliotas. (2008) A Complicated Postsurgical Echinococcal Cyst Treated with Radiofrequency Ablation. CardioVascular and Interventional Radiology 31:1, 215-218
CrossRef31
Dionysios Voros, Dimitrios Katsarelias, Giorgos Polymeneas, Andreas Polydorou, Leda Pistiolis, Angelos Kalovidouris, Athanasios Gouliamos. (2007) Treatment of Hydatid Liver Disease. Surgical Infections 8:6, 621-628
CrossRef32
J. Borchardt. (2007) Echinokokkose der Lunge. Der Pneumologe 4:6, 400-408
CrossRef33
Kais Maazoun, Mongi Mekki, Fatma Zohra Chioukh, Lassaad Sahnoun, Amine Ksia, Riadh Jouini, Mohamed Jallouli, Imed Krichene, Mohsen Belghith, Abdellatif Nouri. (2007) Laparoscopic treatment of hydatid cyst of the liver in children. A report on 34 cases. Journal of Pediatric Surgery 42:10, 1683-1686
CrossRef34
Matthew E. Falagas, Ioannis A. Bliziotis. (2007) Albendazole for the Treatment of Human Echinococcosis: A Review of Comparative Clinical Trials. The American Journal of the Medical Sciences 334:3, 171-179
CrossRef35
Yeh, Wendy W., Saint, Sanjay, Weinberger, Steven E., . (2007) A Growing Problem. New England Journal of Medicine 357:5, 489-494
Full Text36
Philip S Craig, Donald P McManus, Marshall W Lightowlers, Jose A Chabalgoity, Hector H Garcia, Cesar M Gavidia, Robert H Gilman, Armando E Gonzalez, Myriam Lorca, Cesar Naquira, Alberto Nieto, Peter M Schantz. (2007) Prevention and control of cystic echinococcosis. The Lancet Infectious Diseases 7:6, 385-394
CrossRef37
Necati Örmeci, Ramazan Idilman, Serdar Akyar, Murat Palabıyıkoğlu, Sahin Çoban, Hakan Erdem, Fuat Ekiz. (2007) Hydatid cysts in muscle: a modified percutaneous treatment approach. International Journal of Infectious Diseases 11:3, 204-208
CrossRef38
Stavros Gourgiotis, Charalabos Stratopoulos, Panagiotis Moustafellos, Nikitas Dimopoulos, George Papaxoinis, Vasilis Vougas, Evangelos Hadjiyannakis. (2007) Surgical Techniques and Treatment for Hepatic Hydatid Cysts. Surgery Today 37:5, 389-395
CrossRef39
Salam Daradkeh, Husam EL-Muhtaseb, Ghassan Farah, Ahmad S. Sroujieh, Mahmoud Abu-Khalaf. (2007) Predictors of morbidity and mortality in the surgical management of hydatid cyst of the liver. Langenbeck's Archives of Surgery 392:1, 35-39
CrossRef40
E. Zerem, R. Jusufovic. (2006) Percutaneous treatment of univesicular versus multivesicular hepatic hydatid cysts. Surgical Endoscopy 20:10, 1543-1547
CrossRef41
S. Men, C. Yücesoy, T. R. Edgüer, B. Hekimoğlu. (2006) Percutaneous treatment of giant abdominal hydatid cysts: long-term results. Surgical Endoscopy 20:10, 1600-1606
CrossRef42
Adnan Kabaalioğlu, Kağan Çeken, Emel Alimoglu, Ali Apaydin. (2006) Percutaneous imaging-guided treatment of hydatid liver cysts: Do long-term results make it a first choice?. European Journal of Radiology 59:1, 65-73
CrossRef43
PHILIPPE G. MEYER, CLAIRE BONNEVILLE, GILLES A. ORLIAGUET, PHILIPPE DESSEMME, PHILIPPE BLAKIME, PIERRE A. CARLI, YANN REVILLON. (2006) Grand mal seizures: an unusual and puzzling primary presentation of ruptured hepatic hydatid cyst. Pediatric Anesthesia 16:6, 676-679
CrossRef44
Christopher Bell, Joshua Yorgason, Michael E. Jessen, Shellie Josephs, Tulika Jain, D. Rohan Jeyarajah. (2006) Management of Hepatic and Intracardiac Echinococcal Cysts: Case Report and Review of the Literature. Surgical Infections 7:3, 309-313
CrossRef45
Siavosh Nasseri-Moghaddam, Amir Abrishami, Siavosh Nasseri-Moghaddam. 2006. Percutaneous needle aspiration, injection, and reaspiration with or without benzimidazole coverage for uncomplicated hepatic hydatid cysts. .
CrossRef46
Juan Ignacio González-Muñoz, María Angoso-Clavijo, Alfonso Marcos-Sánchez, Juan Antonio García-Jiménez, Aldolfo Cascón-Sánchez, Enrique García-Castillo, Ángel Prado-Morales. (2006) Quiste hidatídico esplénico gigante. Cirugía Española 79:2, 120-122
CrossRef47
Carlos Manterola, Manuel Vial, Angélica Melo, Carlos Oberg, Flery Fonseca. (2006) Viability and Fertility of Human Hepatic Hydatid Cysts. World Journal of Surgery 30:2, 227-232
CrossRef48
Gokhan Yagci, Bahri Ustunsoz, Nihat Kaymakcioglu, Ugur Bozlar, Semih Gorgulu, Abdurrahman Simsek, Ali Akdeniz, Sadettin Cetiner, Turgut Tufan. (2005) Results of Surgical, Laparoscopic, and Percutaneous Treatment for Hydatid Disease of the Liver: 10 Years Experience with 355 Patients. World Journal of Surgery 29:12, 1670-1679
CrossRef49
Vincent W. T. Lam, Neil D . Merrett. (2005) Drainage of hepatic hydatid cyst with a surgiport. ANZ Journal of Surgery 75:11, 1022-1023
CrossRef50
Pedro L. Moro, Hector H. Garcia, Armando E. Gonzales, Juan J. Bonilla, Manuela Verastegui, Robert H. GilmanMD. (2005) Screening for cystic echinococcosis in an endemic region of Peru using portable ultrasonography and the enzyme-linked immunoelectrotransfer blot (EITB) assay. Parasitology Research 96:4, 242-246
CrossRef51
Ahmet Yigit Goktay, Mustafa Secil, Aytac Gulcu, Munevver Hosgor, Irfan Karaca, Mustafa Olguner, Feza M. Akgur, Oguz Dicle. (2005) Percutaneous Treatment of Hydatid Liver Cysts in Children as a Primary Treatment: Long-term Results. Journal of Vascular and Interventional Radiology 16:6, 831-839
CrossRef52
Abdelwahab M. Gabal, Fazal I. Khawaja, Ghanem A. Mohammad. (2005) Modified PAIR Technique for Percutaneous Treatment of High-Risk Hydatid Cysts. CardioVascular and Interventional Radiology 28:2, 200-208
CrossRef53
Roland Chautems, Leo H. Bühler, Benjamin Gold, Emile Giostra, Pierre Poletti, Michael Chilcott, Philippe Morel, Gilles Mentha. (2005) Surgical management and long-term outcome of complicated liver hydatid cysts caused by Echinococcus granulosus. Surgery 137:3, 312-316
CrossRef54
Raymond A. Smego, Peter Sebanego. (2005) Treatment options for hepatic cystic echinococcosis. International Journal of Infectious Diseases 9:2, 69-76
CrossRef55
Chadli Dziri, Karim Haouet, Abe Fingerhut. (2004) Treatment of Hydatid Cyst of the Liver: Where Is the Evidence?. World Journal of Surgery 28:8, 731-736
CrossRef56
John R. Haaga, Dean Nakamoto. (2004) Computed tomography-guided drainage of intra-abdominal infections. Current Infectious Disease Reports 6:2, 105-114
CrossRef57
Christian Hofstetter, Eduardo Segovia, Rafael Vara-Thorbeck. (2004) Treatment of uncomplicated hydatid cyst of the liver by closed marsupialization and fibrin glue obliteration. World Journal of Surgery 28:2, 173-178
CrossRef58
M.A. Silva, D.F. Mirza, S.R. Bramhall, A.D. Mayer, P. McMaster, J.A.C. Buckels. (2004) Treatment of Hydatid Disease of the Liver. Digestive Surgery 21:3, 227-234
CrossRef59
F. Giuliante, F. D’Acapito, M. Vellone, I. Giovannini, G. Nuzzo. (2003) Risk for laparoscopic fenestration of liver cysts. Surgical Endoscopy 17:11, 1735-1738
CrossRef60
R. A. Smego, S. Bhatti, A. A. Khaliq, M. A. Beg. (2003) Percutaneous Aspiration-Injection-Reaspiration Drainage Plus Albendazole or Mebendazole for Hepatic Cystic Echinococcosis: A Meta-analysis. Clinical Infectious Diseases 37:8, 1073-1083
CrossRef61
MW Butler, RH Mullan, KE Schaffer, TB Crotty, DA Luke, SC Donnelly. (2003) Pulmonary cystic hydatid disease in Ireland. Irish Journal of Medical Science 172:4, 204-205
CrossRef62
P.K. Chowbey, S. Shah, R. Khullar, A. Sharma, V. Soni, M. Baijal, A. Vashistha, A. Dhir. (2003) Minimal Access Surgery for Hydatid Cyst Disease: Laparoscopic, Thoracoscopic, and Retroperitoneoscopic Approach. Journal of Laparoendoscopic & Advanced Surgical Techniques 13:3, 159-165
CrossRef63
Y. Wang, X. Zhang, B. Bartholomot, B. Liu, J. Luo, T. Li, X. Wen, H. Zheng, H. Zhou, H. Wen, N. Davaadorj, L. Gambolt, T. Mukhar, K. Al-Qaoud, S. Abdel-Hafez, P. Giraudoux, D.A. Vuitton, A. Fraser, M.T. Rogan, P.S. Craig. (2003) Classification, follow-up and recurrence of hepatic cystic echinococcosis using ultrasound images. Transactions of the Royal Society of Tropical Medicine and Hygiene 97:2, 203-211
CrossRef64
Cabot, Richard C.Harris, Nancy Lee, McNeely, William F., Shepard, Jo-Anne O., Ebeling, Sally H.Ellender, Stacey M.Peters, Christine C., Baden, Lindsey R., Elliott, Danielle D., . (2003) Case 4-2003. New England Journal of Medicine 348:5, 447-455
Full Text65
Ersan Özaslan, Yusuf Bayraktar. (2002) Endoscopic Therapy in the Management of Hepatobiliary Hydatid Disease. Journal of Clinical Gastroenterology 35:2, 160-174
CrossRef66
Kaya Yorganci, Iskender Sayek. (2002) Surgical treatment of hydatid cysts of the liver in the era of percutaneous treatment. The American Journal of Surgery 184:1, 63-69
CrossRef67
S NAIK. (2002) Tropical Liver Disease. Medicine 30:11, 41-44
CrossRef68
Richard D. Pearson. (2002) Albendazole versus placebo for the treatment of Echinococcus granulosus. Current Infectious Disease Reports 4:1, 47-49
CrossRef69
M Haddad. (2001) PERCUTANEOUS TREATMENT OF HEPATIC ECHINOCOCCAL CYST. Clinical Radiology 56:12, 1003-1004
CrossRef70
Davey M. Smith, Leland S. Rickman. (2001) Echinococcosis: A Drop of Water???Review on Human Disease, Diagnosis, and Management. Infectious Diseases in Clinical Practice 10:7, 355-359
CrossRef71
Y.H. Wang, M.T. Rogan, D.A. Vuitton, H. Wen, B. Bartholomot, C.N.L. Macpherson, P.F. Zou, Z.X. Ding, H.X. Zhou, X.F. Zhang, J. Luo, H.B. Xiong, Y. Fu, A. McVie, P. Giraudoux, W.G. Yang, P.S. Craig. (2001) Cystic echinococcosis in semi-nomadic pastoral communities in north-west China. Transactions of the Royal Society of Tropical Medicine and Hygiene 95:2, 153-158
CrossRef72
K. Thursky, J. Torresi. (2001) Primary Muscle Hydatidosis of the Thigh: Management of a Complicated Case with Combination Adjunctive Albendazole and Praziquantel Chemotherapy. Clinical Infectious Diseases 32:3, e65-e68
CrossRef73
Herbert B. Tanowitz, Louis M. Weiss, Murray Wittner. (2001) Tapeworms. Current Infectious Disease Reports 3:1, 77-84
CrossRef74
Vivek Kaul, Frank Friedenberg, Kenneth D. Rothstein. (2000) Hepatic cysts. Current Treatment Options in Gastroenterology 3:6, 439-443
CrossRef75
Z BOSANAC. (2000) Percutaneous Drainage of Hydatid Cyst in the Liver as a Primary Treatment: Review of 52 Consecutive Cases with Long-term Follow-up. Clinical Radiology 55:11, 839-848
CrossRef76
Maurice C. Haddad, Bassam M. Sammak, Mohammad Al-Karawi. (2000) Percutaneous treatmerit of heterogertous predorninantly solid echopattern echinococcal cysts of the liver. Cardiovascular and Interventional Radiology 23:2, 121-125
CrossRef77
Mikio Kimura, Taichi Nakamura, Aikichi Iwamoto, Yoji Nishimura, Tami Egawa, Akira Ito. (1999) Cystic Echinococcosis in a Jordanian Patient: Albendazole in a Short-Term Immigrant. Journal of Travel Medicine 6:4, 249-253
CrossRef78
Okan Akhan, Mustafa N Özmen. (1999) Percutaneous treatment of liver hydatid cysts. European Journal of Radiology 32:1, 76-85
CrossRef79
Ghulam Nabi Yattoo, Mohammad Sultan Khuroo, Showkat Ali Zargar, Fayaz Ahmad Bhat, Bashir Ahmad Sofi. (1999) C ASE R EPORT: Percutaneous drainage of the pancreatic head hydatid cyst with obstructive jaundice. Journal of Gastroenterology and Hepatology 14:9, 931-934
CrossRef80
J. M. Debonne, F. Klotz, P. Rey, T. Coton, P. Legall, D. Carre, M. Guisset. (1999) Actualités thérapeutiques du kyste hydatique du foie. Acta Endoscopica 29:4, 453-466
CrossRef81
D.B. Lewall. (1998) Hydatid disease: Biology, pathology, imaging and classification. Clinical Radiology 53:12, 863-874
CrossRef82
Calin V. Maniu, Jose-Maria Acostamadiedo, Salvador Alvarez. (1998) 73-Year-Old Man With Hepatomegaly and Weight Loss. Mayo Clinic Proceedings 73:9, 899-902
CrossRef83
Andrew P. Ustianowski, Alimuddin Zumla. (1998) Hydatid disease. Clinical Microbiology and Infection 4:7, 405-409
CrossRef84
(1998) Percutaneous Drainage of Hydatid Cysts. New England Journal of Medicine 338:6, 391-393
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