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Surgical treatment of hydatid disease of the liver: 25 years of experience
The American Journal of Surgery (2011) 201, 797– 804
Clinical Science
Surgical treatment of hydatid disease of the liver: 25 years of experience Sandro Tagliacozzo, M.D., Michelangelo Miccini, Ph.D., Stefano Amore Bonapasta, M.D., Matteo Gregori, M.D., Adriano Tocchi, M.D.* Division of Gastroenterologic and Hepato-Bilio Pancreatic Surgery, First Department of Surgery, Sapienza University Medical School, Rome, Italy KEYWORDS: Liver hydatid disease; Cystopericystectomy; Hepatic resection
Abstract BACKGROUND: The aim of this study was to evaluate the results of conservative and radical treatment of liver hydatid disease. METHODS: Records of patients who underwent surgery for liver hydatid disease between 1980 and 2005 were reviewed. Outcomes measured were operative morbidity and mortality, hospital stay, and recurrence. RESULTS: Two hundred fourteen patients underwent conservative treatment (external drainage, marsupialization, omentoplasty), and 240 had radical surgery (hepatic resection, cystopericystectomy). Operative morbidity was 79.9% and 16.2% for conservative and radical procedures, respectively (P ⬍ .001). Operative mortality was 6.5% for conservative procedures and 9.2% for radical procedures (P ⫽ .3). The recurrence rate was 30.4% in patients having conservative surgery and 1.2% in patients undergoing radical surgery (P ⬍ .001). No recurrences occurred in patients with clear cysts after conservative surgery. CONCLUSIONS: Cystopericystectomy was a safe and effective procedure that achieved excellent immediate and long-term results. Hepatic resection should be considered only in exceptional cases, because it involves the unnecessary sacrifice of healthy hepatic parenchyma. Conservative surgery and alternative procedures should be restricted to the treatment of clear cysts and to patients who cannot undergo radical surgery. © 2011 Elsevier Inc. All rights reserved.
Hydatid disease (HD) is a zoonotic disease caused by the larval form of Echinococcus. The most common form is E granulosus, which gives rise to cysts, primarily in the liver. HD has a worldwide distribution and is endemic in many countries in the Mediterranean region, the Middle East and Far East, and South Africa.1 Because of increasing immigration, the disease is becoming more frequent outside endemic areas. In recent years, knowledge of its etiology and * Corresponding author. Tel.: 39-6-4462127; fax: 39-6-4959357. E-mail address: [email protected] Manuscript received December 2, 2009; revised manuscript February 8, 2010
0002-9610/$ - see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.amjsurg.2010.02.011
pathogenesis has largely contributed to improved prevention and reduced the incidence of HD.2,3 Clarifying some aspects of the biology of the parasite and of its interaction with the human host represents the scientific basis for a more rational approach to surgery of liver HD (LHD).4 – 6
Pathophysiologic basis of surgical management The adult tape worm consists of a head (scolex) and 3 following segments (proglottides). The scolex has 4 suckers and a prominent rostellum armed with a double row of 30 to 36 hooks. Sexual, mature organs and countless eggs are contained in the more distal of the 3 proglottides. Each egg
798 consists of a shell containing 6 hook-armed embryo hexacanth (6 hooks), as shown in Figure 1. The adult tapeworm lives in the small bowel of its most common definitive host, the dog, attached to the mucosa by its hooklets. Infected eggs pass out with dog feces and contaminate soil, water, and plants. Humans become infected via accidental ingestion of eggs. Once inside the human intestine, the eggs open, and the embryo hexacanth attaches to and then crosses the intestinal mucosa and via the portal system migrates to the liver, where the parasite develops into the larval stage, which is the hydatid cyst. The growth of the cyst leads to the formation of a connective lamina in the surrounding parenchyma (ectocyst or pericyst). The parasite-derived endocyst may consist of either 1 or 2 layers. The outer one, the laminated layer, is a totally acellular membrane permeable to water and electrolytes, which protects the cyst from host enzymes, bile, and bacteria. The inner layer, the germinal layer, is the living element of the parasite (Fig. 2). Cysts with the sole laminated layer are sterile cysts, also called univesicular or clear cysts, whereas cysts provided with both laminated and germinal layers are fertile or multivesicular cysts. Invaginations of the germinal layer form brood capsules, each containing 5 to 10 protoscolices. When brood capsules open, protoscolices are released into the cystic fluid, giving rise to daughter cysts, a process called endogenic vesiculation. The process of vesiculation occurs not only inside but also outside the cyst within the pericyst (exogenous vesiculation). We have retrospectively reviewed and analyzed the changes in the approach and results of surgical treatment of
The American Journal of Surgery, Vol 201, No 6, June 2011
Figure 2 Schematic drawing of a liver hydatid cyst. BC ⫽ brood capsule; DC ⫽ daughter cyst; GL ⫽ germinal layer; L ⫽ liver; LL ⫽ laminated layer; P ⫽ pericyst; S ⫽ protoscolex.
LHD according to our evolving, personal knowledge of the pathophysiology of the parasite.
Methods Patients
Figure 1 Echinococcus granulosus. Adult form of tapeworm. E ⫽ egg; H ⫽ hook; P ⫽ proglottides; S ⫽ head or scolex; SO ⫽ sexual organs.
Patients were identified by a computer-based indexing system containing data on all patients admitted for LHD at the First Department of Surgery of the University of Rome “La Sapienza” Medical School between January 1, 1980, and January 1, 2005. The overall study group was divided into 2 subgroups: group A (1980 –1992) and group B (1993–2005). Criteria for exclusion from this study were previous medical or surgical treatment for HD, concomitant extrahepatic HD, and the presence of a bronchobiliary fistula. No laparoscopic procedure was performed in the current series. Suitable records of all patients were extracted from the computer database and retrospectively analyzed. Variables considered for analysis were age, gender, length of clinical history, number of hepatic cysts, and site. According to their location, cysts were divided into superficial and deep or vasculobiliary cysts. Cysts extrinsic to the hepatic parenchyma, however distant from main intrahepatic vessels and vena cava, were defined as superficial cysts. Cysts deeply located in the hepatic parenchyma, near the pedicles and stems of the main intrahepatic vessels and vena cava, were defined as vasculobiliary cysts. Further-
S. Tagliacozzo et al. Table 1
Surgical treatment of hepatic hydatidosis
Clinical and demographic data
Variable Age (y) Gender Male Female Clinical presentation Abdominal pain History of jaundice Abdominal mass History of fever Nausea and vomiting Asymptomatic Duration of symptoms (mo) Comorbidity Obesity* Cardiovascular disease Lung disease Diabetes mellitus Neurologic disease
Value 51 (15–77) 152 (33.5%) 302 (66.5%) 328 315 281 124 106 43 16
(72.2%) (69.3%) (61.8%) (27.3%) (23.3%) (9.4%) (2–72)
32 28 11 10 7
(7.0%) (6.1%) (2.4%) (2.2%) (1.5%)
Data are expressed as mean (range) or as number (percentage). *Body mass index ⱖ30 kg/m2.
more, cysts were classified according to their content as clear or sterile cysts and multivesicular or fertile cysts. Comorbidity, surgical procedures used, operative morbidity and mortality, length of postoperative hospital stay, and recurrence were other variables considered.
Surgery Surgical access consisted of laparotomy (median or subcostal incision) and, mostly in the first period, thoracophrenolaparotomy. Surgical procedures were classified as radical or conservative. Liver resection, cystopericystectomy (CP), and subtotal pericystectomy were grouped as radical procedures and partial cystectomy with tube drainage, omentoplasty, or “capitonage” as conservative approaches. All clear cysts were treated with conservative procedures. Radical and conservative procedures were never done together. Intraoperative cholangiography was always associated with both types of procedures. Cholecystectomy and either surgical papillotomy or T-tube biliary drainage were associated when cystobiliary communication or elevated pressure in the biliary tract were detected by intraoperative cholangiography and in case lesions of the intrahepatic biliary system were determined during the course of surgery. More recently, in case of preoperative diagnosis of cystobiliary communication, the biliary tract has been cleared preoperatively by endoscopy. All surgical procedures were performed by 2 of the authors (S.T., A.T.).
Outcomes The early outcome was determined from the medical records. Postoperative complications were classified as lo-
799
cal when they occurred at the site of surgery or as general complications otherwise. After discharge, patients were followed periodically in the 3rd, 5th, and 12th postoperative months during the first year and thereafter every year. The follow-up procedures included physical examination, serologic tests, plain abdominal radiography, and ultrasound and computed tomography after these diagnostic procedures became available. The median follow-up period was 87 months (range, 36 –190 months). The last control was performed in January 2009. Reappearance of live cysts at the site of a previously treated cyst was defined as local recurrence.
Histology Histology of the cystic wall and pericyst was performed in all specimens from radical procedures.
Statistical analysis Comparisons of the continuous variable were performed using Student’s t test, and categorical variables were compared using Pearson’s 2 test. Statistical analyses were performed with Statistica 5’97 (StatSoft, Inc, Tulsa, OK). P values ⬍.05 were regarded as statistically significant.
Results The present study included 454 patients. Table 1 lists their demographic and clinical characteristics. Results of serologic tests (hemagglutination, complement fixation) were positive in 69% of 454 patients. A total of 695 hepatic cysts were treated. Table 2 shows the characteristics of the cysts and their distribution. Cysts were solitary in 296 pa-
Table 2
Characteristics of cysts
Variable
Value
Total number Type Multivesicular Clear Size (cm) Number of cysts per patient 1 2 3 ⬎3 Location Right lobe Deep Left lobe Deep Bilobar Deep
695 639 (87.7%) 56 (12.3%) 19 (3–41) 296 103 34 21
(65.1%) (22.6%) (7.4%) (4.6%)
458 314 203 72 34 31
(65.8%) (68.5%) (29.2%) (35.4%) (4.8%) (91.1%)
Data are expressed as number (percentage) or as mean (range).
800 Table 3
The American Journal of Surgery, Vol 201, No 6, June 2011 Surgical treatments
Treatment
Table 5 Number of Patients
Radical treatment Hepatic resection Right extended Right Left Sectoriectomy CP Total Subtotal Conservative treatment Marsupialization External drainage Omentoplasty
240 73 3 8 18 44 167 138 29 214 75 87 52
tients and multiple in 158 (one lobe in 85, both lobes in 73). A total of 417 cysts were classified as deep: 314 were sited in the right lobe, 72 in the left lobe, and 31 in both lobes. Fifty-six cysts were clear (sterile cysts), and 639 were multivesicular. Migration of daughter cysts into the common bile duct was documented in 71 patients. A conservative approach was adopted in 214 patients (319 cysts), whereas 240 patients (376 cysts) were treated with radical procedures (Table 3). No differences were found in age and gender between these groups. The local complication rates and hospital stays were significantly superior in patients who underwent conservative procedures. No main differences in general complications, with the exception of pleural effusion, were observed in patients treated with conservative or radical procedures. Operation time was significantly shorter for conservative treatment, which, moreover, required fewer blood transfu-
Table 4
Associated procedures
Associated Procedure
Radical Treatment
Conservative Treatment
Cholecystectomy Cholecystectomy ⫹ papillotomy Cholecystectomy ⫹ T-tube Papillotomy Choledochotomy ⫹ T-tube Endoscopic sphincterotomy
45 17 9 3 2 3
38 19 17 5 4 2
sions. Operative mortality was not significantly different between conservative (6.5%) and radical (9.2%) procedures (Table 4). The number and type of surgical associated procedures were similar in the 2 groups (Table 5). The presence of daughter cysts outside the cystic wall was observed on histology in 67 of the 376 specimens (17.8%) from radical procedures. The incidence of recurrence was 30.4% in patients who underwent conservative surgery and 1.2% in patients treated with radical procedures (Table 4). No recurrence was observed in patients with clear cysts. Table 6 shows a comparison between the 2 subgroup time periods. Local complication and recurrence rates decreased from 62% to 32% and from 15% to 8%, respectively, between the 2 time periods.
Comments The desired goals for the treatment of LHD include complete elimination of the parasite and prevention of recurrent disease with minimum mortality.7 However, selec-
Outcomes of radical and conservative procedures
Outcome
Radical Procedures (n ⫽ 240)
Conservative Procedures (n ⫽ 214)
P
Local operative complications Biliary leaks Residual cavity infection Residual cavity hematoma General complications Pleural effusion Pulmonary embolism Cardiac failure Respiratory failure Renal Failure Hepatic failure Hospital stay (d) Recurrences Operation time (min) Blood transfusion (L) Operative mortality
39 11 11 17 18 3 2 5 2 0 6 13.8 3 281 3.53 22
171 65 80 26 29 17 1 4 6 1 0 33.7 48 200 r1.35 14
⬍.001 ⬍.001 ⬍.001 .065 .034 ⬍.001 .630 .870 .111 .289 .019 ⬍.001 ⬍.001 ⬍.001 ⬍.001 .301
(16.2%) (4.6%) (4.6%) (7.1%) (7.5%) (1.2%) (.8%) (2.1%) (.8%) (2.5%) (1.2%) (240–420) (2–6) (9.2%)
(79.9%) (30.4%) (37.4%) (12.1%) (13.6%) (7.9%) (.5%) (1.9%) (2.8%) (.5%) (30.4%)* (110–261) (0–4) (6.5%)
(NS) (NS) (NS) (NS) (NS)
(NS)
Data are expressed as number (percentage) or as mean (range). *Fifty-six of 214 patients treated with conservative procedures had solitary clear cysts. The rate of recurrence was calculated in 158 patients with multivesicular cysts.
S. Tagliacozzo et al. Table 6
Surgical treatment of hepatic hydatidosis
801
Comparison of surgical procedures and main outcomes between the 2 subgroups
Variable Procedure Conservative procedures External drainage Marsupialization Omentoplasty Radical procedures Hepatic resections Pericystectomy Outcomes Local operative complications General complications Recurrences Operative mortality
Group A (1980–1992) (n ⫽ 213)
Group B (1993–2005) (n ⫽ 241)
151 (70.9%) 71 44 36 62 (29.1%) 37 25
63 (26.1%) 16 31 16 178 (73.9%) 36 142
132 24 32 17
(61.9%) (11.3%) (15%) (8%)
tion of the most appropriate treatment to achieve these goals remains the subject of debate, and 3 main approaches are used to date: systemic chemotherapy, percutaneous procedures, and surgical treatment. Systemic chemotherapy is presently based on benzimidazole carbamate compounds. However, the clinical efficacy of these treatments is not clear; complete regression of cysts has never been reported, whereas persistence of living parasite within the cysts has been documented in ⬎50% of the patients being treated preoperatively with benzimidazole compounds.8 –11 Therefore, the World Health Organization has suggested restricting the use of medical treatment for disseminated systemic disease, cases that are not amenable to surgery, and in which known intra-abdominal spillage of hydatid fluid has occurred, and combined with surgery to prevent postoperative recurrence.9 Percutaneous procedures have been proposed more recently.12–14 The main shortcomings of these techniques are incomplete evacuation of the cyst content, difficulty in achieving adequate scolicidal concentration, doubt about the right exposure time, and sclerosing cholangitis in case of cystobiliary communication.15–18 The use of percutaneous treatment seems to represent an alternative treatment in patients who cannot undergo or refuse surgery. Surgery thus remains the first-line treatment for LHD. However, there is considerable disagreement about the optimal surgical technique.16,19 –22 The major issue is whether complete removal of the pericyst is necessary for the proper care of the disease. Proposed surgical procedures can be divided into 2 groups: conservative procedures and radical procedures. Conservative procedures have been defined as those limited to evacuation of cyst content with part or all the pericyst remaining in situ. These techniques, as suggested, should be preferred to radical procedures because they are safer and easier to perform.20,23,24 However, nonnegligible drawbacks have been reported to affect the outcomes of conservative procedures. The main immediate postoperative complications are biliary leakage and fistulas, along with septic complications of the residual cavity leading to prolonged
78 23 19 19
(32.4%) (9.5%) (7.9%) (7.9%)
P ⬍.001
⬍.001
⬍.001 .547 (NS) .016 .969 (NS)
hospital stays.10,21,25 Most of these complications may be ascribed to the pericyst lining the residual cavity. A pericyst left in situ, especially if thick and calcified, represents an obstacle to liver regeneration filling the residual cavity, thus leading to serum and blood accumulation or liver abscess formation. Furthermore, the persistence of the pericyst hides possible biliary communication in the residual cavity, considered the main reason for biliary leakage, which occurs in up to 50% of patients after conservative procedures.26 However, it should be stressed that even when biliary communications are identified, their closure within a stiff, calcified pericyst wall would not be easy or effective. The incidence of biliary leaks and residual cavity infection in patients of our series treated with conservative procedures was 30.4% and 37.4%, respectively. These data, consistent with those of other authors, confirm conservative surgery as a significant determinant of high complication rates and prolonged hospital stays.27–30 Furthermore, infection, biliary fistula, and slow reduction of the cyst cavity may lead to more serious complications, such as obstruction of main hepatic ducts or the portal vein.31,32 In these cases, reoperation is quite complex, with high mortality due to the technical difficulties related to distorted liver anatomy, deteriorated liver function, and poor general conditions.22 Radical procedures include CP and hepatic resection. Hepatic resection has seldom been considered the principal technique to adopt when treating LHD. The notable development of liver resection surgery in more recent years has not changed this trend, so the rate of hepatic resections rarely exceeds 10% in different series.15,19,22,25 In our series, the rate of hepatic resections was much higher because many patients referred from general hospitals to our tertiary referral center had extremely large or multiple localized cysts responsible for diffuse parenchymal damage. Resections were adopted in these cases because entire sectors, lobes, or hemilivers were destroyed by the cysts, and interruption of main bile ducts would have made their repair questionable because of an extremely high risk for serious cholerrhagia. With the exception of these particular cases,
802 our policy has been to avoid liver resection to spare as much healthy hepatic parenchyma as possible at the first surgery. This trend has led us to use CP more frequently. The purpose of CP is the complete removal of the cyst along with its pericyst (CP) without opening the cavity; this avoids contamination of peritoneum and the risk for leaving behind daughter cysts within the pericyst in the hepatic parenchyma.15,19,22,30,33,34 CP may be performed either as a closed or open procedure. The closed procedure was used mainly in patients with superficial cysts or single-lobe deep cysts. Open CP was performed every time there was a risk for breaking the cyst wall, in case of cysts of the hepatic dome, strictly adherent to the hepatic veins and vena cava, and in case of deep intraparenchymal cysts with an interportocaval location. Both in open and closed procedures, the hepatic lobes were fully mobilized to control the confluence of the hepatic veins and inferior vena cava as well as the retrohepatic segment of the vena cava and vascular and biliary elements of the hepatic hilum. In the open method, after evacuation of its content, the cavity is stubbed with swabs soaked in sterilizing substances. The cyst wall is then sectioned and dissection is carried out by molding with the left hand the residual pericyst to enhance the visual control of its relationship with the surrounding parenchyma and afferent vessels and biliary duct (Fig. 3). For the deep, interportocaval location, the access to the cyst is greatly favored by opening the median fissure, which increases the extension of the cystic wall (Fig. 4). Completion of the detachment of the residual, deep pericyst from the hepatic parenchyma may be further eased by dividing it into segments and performing the separate dissection of each segment after it has been refolded on itself (Fig. 5). In case of hard, calcified pericysts strongly adherent to main vessels,
Figure 3 Open pericystectomy. The cyst has been opened and its contents evacuated. The visual control of the relationship between the cystic wall and hepatic parenchyma are in this way enhanced.
The American Journal of Surgery, Vol 201, No 6, June 2011
Figure 4 Deep interportocaval cysts. The access to the cyst is effectively eased by opening the sagittal fissure.
especially to the vena cava, it is advisable to stop dissection just before the vascular plane and to leave behind a small part of the cystic wall (partial CP) (Fig. 6). Overall postoperative complications and hospital stays associated with radical procedures in our series were strikingly lower compared with those after conservative procedures. Complete removal of the pericyst allows the exact
Figure 5 Dissection of the pericyst is eased by dividing the deepest part of it into segments that are refolded and separately dissected.
S. Tagliacozzo et al.
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vative treatment, calculated by removing the results of the 56 patients with clear cysts, grew in our series from 22.4% to 30.4%. In conclusion, the use of radical procedures for treating LHD have been confirmed by the results in our series. These techniques should be considered safe and effective, especially at high-flow hepatic surgery centers, because they are associated with an excellent morbidity and mortality rates and because the recurrence rate is reduced almost to zero. CP should be preferred to hepatic resection whenever possible because it avoids the undue sacrifice of healthy liver parenchyma. Alternative treatments and conservative surgical procedures should be restricted to clear cysts, severely ill patients, and situations in which the pericyst tissue strongly adheres to main vessels.
References Figure 6 Partial pericystectomy. Dissection of the cystic wall has been stopped and a plug of the calcified pericyst left in situ adherent to the vena cava.
detection and safe direct suture in healthy hepatic parenchyma of biliary and vascular breaches and thus minimizes the risk for biliary leaks and blood collection. Furthermore, the easy approach of the smooth parenchymal limbs promotes the spontaneous reduction of the residual cavity brought about by natural liver regeneration. Local recurrence represents a major concern in the treatment of LHD.35–37 The cause of local recurrence is failure to remove or kill all viable cysts and protoscolices at the time of surgery. Better understanding of certain aspects related to the survival of infectious agents, mainly exogenous vesiculation, has shed new light on this argument. Exogenous vesiculation, detected in 20.2% of specimens of our series derived from radical surgery, suggests that this would have been the rate of recurrence if conservative procedures had been performed in these patients. This rate, evocatively similar to the 22.4% recurrence rate observed in all the patients of our series treated with conservative surgery, corresponds to the mean rate of recurrences reported in literature.28,36 The cyst content, which may change from clear, that is, sterile cysts, to multivesicular with daughter cysts, makes it necessary to consider these 2 kinds of cysts as different pathologic entities. The absence of the germinal layer excludes clear cysts from the risk for vesiculation, that is, recurrences. In our series, the rate of recurrences in 56 treated clear cysts by conservative procedures was nil. Conservative procedures should then, quite rightly, be considered an adequate treatment for clear cysts. Mixing the results of conservative treatment of clear and multivesicular cysts inevitably would introduce, and has introduced in the literature, a bias that decreases the true rate of immediate and long-term failures of conservative treatment of multivesicular cysts. The local recurrence rate following conser-
1. Richards KS. Biology of Echinococcus and diagnosis of hydatid disease. In Morris DL, Richards KS, eds. Hydatid disease: current medical and surgical management. Oxford, UK: Butterworth Heinemann; 1992:1–24. 2. Gemmel MA. Australasian contributions to an understanding of the epidemiology and control of hydatid disease caused by Echinococcus granulosus—past, present and future. Int J Parasitol 1990;20:431–56. 3. Eckert J, Gemmel MA, Matyas Z, et al. Guidelines for surveillance, prevention and control of Echinococcosis/hydatidosis. Geneva, Switzerland: World Health Organization; 1984:1–5. 4. Richards KS, Morris DL. Evidence for the development of human hydatid daughter cysts for protoscolices. Parasitol Res 1989;75:333– 4. 5. Tagliacozzo S. Chirurgia della idatidosi epatica. EMSI 1997. 6. Bourgeon R, Isman H, Brisard M. Le perikyste et la perikystectomie au cours du kyste hydatique du foie: a propos de 178 observations. J Chir (Paris) 1979;116:693– 8. 7. Gokskoy E, Saklal M, Saribeyoglu K, et al. Surgery for Echinococcus cysts of the liver. Chirurg 2008;79:729 –37. 8. Schantz PM. Effective medical treatment for hydatid disease? JAMA 1985;253:2095–7. 9. Davis A, Pawlowski ZS, Dixon H. Multicentre clinical trials of benzimidazole carbamates in human echinococcosis. Bull World Health Organ 1986;64:383– 8. 10. Falagas M, Bliozotis I. Albendazole for the treatment of human echinococcosis: a review of comparative clinical trials. Am J Med Sci 2007;334:171–9. 11. Monterola M, Monsilla JA, Fonseca F. Preoperative albendazole and scolices viability in patients with hepatic echinococcosis. World J Surg 2005;29:750 –3. 12. Mueller PR, Dawson SL, Ferrucci JT Jr, et al. Hepatic echinococcal cyst: successful percutaneous drainage. Radiology 1985;155:627– 8. 13. Akhan O, Ozmen MN. Percutaneous treatment of liver hydatid cysts. Eur J Radiol 1999;32:76 – 85. 14. Saremi F, McNamara TO. Hydatid cysts of the liver: long-term results of percutaneous treatment using a cutting instrument. AJR Am J Roentgenol 1995;165:1163–7. 15. Sayek I, Onat D. Diagnosis and treatment of uncomplicated hydatid cyst of the liver. World J Surg 2001;25:21–7. 16. Dawson JL, Stamatakis JD, Stringer MD, et al. Surgical treatment of hepatic disease. Br J Surg 1988;75:946 –50. 17. Belghiti J, Benhamau JP, Perniceri T, et al. Sclerosing cholangitis. A complication of surgical treatment of hydatid disease of the liver. Arch Surg 1986;121:1162–5. 18. Polo JR, Garcia SL. Sclerosing cholangitis associated with hydatid liver disease. Arch Surg 1987;124:637.
804 19. Cirenei A, Bertoldi I. Evolution of surgery for liver hydatidosis from 1950 to today: analysis of personal experience. World J Surg 2001; 25:87–92. 20. Safioleas MC, Misiakos EP, Kouvaraki M, et al. Hydatid disease of the liver. A continuing surgical problem. Arch Surg 2006;141:1101– 8. 21. Chadli D, Haouet K, Fingerhut A. Treatment of hydatid cyst of the liver: where is the evidence? World J Surg 2004;28:731– 6. 22. Gonzales ME, Selas PR, Martinez B, et al. Result of surgical treatment of hepatic hydatidosis: current therapeutic modification. World J Surg 1991;15:254 – 63. 23. Langer JC, Rose DB, Keystone JS, et al. Diagnosis and management of hydatid disease of the liver. A 15-year North America experience. Ann Surg 1984;199:412–7. 24. Safioleas M, Misiakos EP, Kakisis J, et al. Surgical treatment of human echinococcosis. Int Surg 2000;85:358 – 65. 25. Kayaalp C, Sengul N, Akoglu M. Importance of cyst content in hydatid liver surgery. Arch Surg 2002;137:159 – 63. 26. Association Universitaire de Recherche en Chirurgie, Association de Recherche Chirurgie, Association de Chirurgiens de l’Assistance Publique pour les Evaluations Medicales, Chipponi J, Huguier M. Les kystes hydatiques du foie operes en France: epidemiologie, attitudes diagnostiques et therapeutique: etude de 306 cas. Gastroenterol Clin Biol 1986;10:419 –23. 27. Ag˘aog˘lu N, Türkyilmaz S, Arslan MK. Surgical treatment of hydatid cysts of the liver. Br J Surg 2003;90:1536 – 41.
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Clinical Science
Surgical treatment of hydatid disease of the liver: 25 years of experience Sandro Tagliacozzo, M.D., Michelangelo Miccini, Ph.D., Stefano Amore Bonapasta, M.D., Matteo Gregori, M.D., Adriano Tocchi, M.D.* Division of Gastroenterologic and Hepato-Bilio Pancreatic Surgery, First Department of Surgery, Sapienza University Medical School, Rome, Italy KEYWORDS: Liver hydatid disease; Cystopericystectomy; Hepatic resection
Abstract BACKGROUND: The aim of this study was to evaluate the results of conservative and radical treatment of liver hydatid disease. METHODS: Records of patients who underwent surgery for liver hydatid disease between 1980 and 2005 were reviewed. Outcomes measured were operative morbidity and mortality, hospital stay, and recurrence. RESULTS: Two hundred fourteen patients underwent conservative treatment (external drainage, marsupialization, omentoplasty), and 240 had radical surgery (hepatic resection, cystopericystectomy). Operative morbidity was 79.9% and 16.2% for conservative and radical procedures, respectively (P ⬍ .001). Operative mortality was 6.5% for conservative procedures and 9.2% for radical procedures (P ⫽ .3). The recurrence rate was 30.4% in patients having conservative surgery and 1.2% in patients undergoing radical surgery (P ⬍ .001). No recurrences occurred in patients with clear cysts after conservative surgery. CONCLUSIONS: Cystopericystectomy was a safe and effective procedure that achieved excellent immediate and long-term results. Hepatic resection should be considered only in exceptional cases, because it involves the unnecessary sacrifice of healthy hepatic parenchyma. Conservative surgery and alternative procedures should be restricted to the treatment of clear cysts and to patients who cannot undergo radical surgery. © 2011 Elsevier Inc. All rights reserved.
Hydatid disease (HD) is a zoonotic disease caused by the larval form of Echinococcus. The most common form is E granulosus, which gives rise to cysts, primarily in the liver. HD has a worldwide distribution and is endemic in many countries in the Mediterranean region, the Middle East and Far East, and South Africa.1 Because of increasing immigration, the disease is becoming more frequent outside endemic areas. In recent years, knowledge of its etiology and * Corresponding author. Tel.: 39-6-4462127; fax: 39-6-4959357. E-mail address: [email protected] Manuscript received December 2, 2009; revised manuscript February 8, 2010
0002-9610/$ - see front matter © 2011 Elsevier Inc. All rights reserved. doi:10.1016/j.amjsurg.2010.02.011
pathogenesis has largely contributed to improved prevention and reduced the incidence of HD.2,3 Clarifying some aspects of the biology of the parasite and of its interaction with the human host represents the scientific basis for a more rational approach to surgery of liver HD (LHD).4 – 6
Pathophysiologic basis of surgical management The adult tape worm consists of a head (scolex) and 3 following segments (proglottides). The scolex has 4 suckers and a prominent rostellum armed with a double row of 30 to 36 hooks. Sexual, mature organs and countless eggs are contained in the more distal of the 3 proglottides. Each egg
798 consists of a shell containing 6 hook-armed embryo hexacanth (6 hooks), as shown in Figure 1. The adult tapeworm lives in the small bowel of its most common definitive host, the dog, attached to the mucosa by its hooklets. Infected eggs pass out with dog feces and contaminate soil, water, and plants. Humans become infected via accidental ingestion of eggs. Once inside the human intestine, the eggs open, and the embryo hexacanth attaches to and then crosses the intestinal mucosa and via the portal system migrates to the liver, where the parasite develops into the larval stage, which is the hydatid cyst. The growth of the cyst leads to the formation of a connective lamina in the surrounding parenchyma (ectocyst or pericyst). The parasite-derived endocyst may consist of either 1 or 2 layers. The outer one, the laminated layer, is a totally acellular membrane permeable to water and electrolytes, which protects the cyst from host enzymes, bile, and bacteria. The inner layer, the germinal layer, is the living element of the parasite (Fig. 2). Cysts with the sole laminated layer are sterile cysts, also called univesicular or clear cysts, whereas cysts provided with both laminated and germinal layers are fertile or multivesicular cysts. Invaginations of the germinal layer form brood capsules, each containing 5 to 10 protoscolices. When brood capsules open, protoscolices are released into the cystic fluid, giving rise to daughter cysts, a process called endogenic vesiculation. The process of vesiculation occurs not only inside but also outside the cyst within the pericyst (exogenous vesiculation). We have retrospectively reviewed and analyzed the changes in the approach and results of surgical treatment of
The American Journal of Surgery, Vol 201, No 6, June 2011
Figure 2 Schematic drawing of a liver hydatid cyst. BC ⫽ brood capsule; DC ⫽ daughter cyst; GL ⫽ germinal layer; L ⫽ liver; LL ⫽ laminated layer; P ⫽ pericyst; S ⫽ protoscolex.
LHD according to our evolving, personal knowledge of the pathophysiology of the parasite.
Methods Patients
Figure 1 Echinococcus granulosus. Adult form of tapeworm. E ⫽ egg; H ⫽ hook; P ⫽ proglottides; S ⫽ head or scolex; SO ⫽ sexual organs.
Patients were identified by a computer-based indexing system containing data on all patients admitted for LHD at the First Department of Surgery of the University of Rome “La Sapienza” Medical School between January 1, 1980, and January 1, 2005. The overall study group was divided into 2 subgroups: group A (1980 –1992) and group B (1993–2005). Criteria for exclusion from this study were previous medical or surgical treatment for HD, concomitant extrahepatic HD, and the presence of a bronchobiliary fistula. No laparoscopic procedure was performed in the current series. Suitable records of all patients were extracted from the computer database and retrospectively analyzed. Variables considered for analysis were age, gender, length of clinical history, number of hepatic cysts, and site. According to their location, cysts were divided into superficial and deep or vasculobiliary cysts. Cysts extrinsic to the hepatic parenchyma, however distant from main intrahepatic vessels and vena cava, were defined as superficial cysts. Cysts deeply located in the hepatic parenchyma, near the pedicles and stems of the main intrahepatic vessels and vena cava, were defined as vasculobiliary cysts. Further-
S. Tagliacozzo et al. Table 1
Surgical treatment of hepatic hydatidosis
Clinical and demographic data
Variable Age (y) Gender Male Female Clinical presentation Abdominal pain History of jaundice Abdominal mass History of fever Nausea and vomiting Asymptomatic Duration of symptoms (mo) Comorbidity Obesity* Cardiovascular disease Lung disease Diabetes mellitus Neurologic disease
Value 51 (15–77) 152 (33.5%) 302 (66.5%) 328 315 281 124 106 43 16
(72.2%) (69.3%) (61.8%) (27.3%) (23.3%) (9.4%) (2–72)
32 28 11 10 7
(7.0%) (6.1%) (2.4%) (2.2%) (1.5%)
Data are expressed as mean (range) or as number (percentage). *Body mass index ⱖ30 kg/m2.
more, cysts were classified according to their content as clear or sterile cysts and multivesicular or fertile cysts. Comorbidity, surgical procedures used, operative morbidity and mortality, length of postoperative hospital stay, and recurrence were other variables considered.
Surgery Surgical access consisted of laparotomy (median or subcostal incision) and, mostly in the first period, thoracophrenolaparotomy. Surgical procedures were classified as radical or conservative. Liver resection, cystopericystectomy (CP), and subtotal pericystectomy were grouped as radical procedures and partial cystectomy with tube drainage, omentoplasty, or “capitonage” as conservative approaches. All clear cysts were treated with conservative procedures. Radical and conservative procedures were never done together. Intraoperative cholangiography was always associated with both types of procedures. Cholecystectomy and either surgical papillotomy or T-tube biliary drainage were associated when cystobiliary communication or elevated pressure in the biliary tract were detected by intraoperative cholangiography and in case lesions of the intrahepatic biliary system were determined during the course of surgery. More recently, in case of preoperative diagnosis of cystobiliary communication, the biliary tract has been cleared preoperatively by endoscopy. All surgical procedures were performed by 2 of the authors (S.T., A.T.).
Outcomes The early outcome was determined from the medical records. Postoperative complications were classified as lo-
799
cal when they occurred at the site of surgery or as general complications otherwise. After discharge, patients were followed periodically in the 3rd, 5th, and 12th postoperative months during the first year and thereafter every year. The follow-up procedures included physical examination, serologic tests, plain abdominal radiography, and ultrasound and computed tomography after these diagnostic procedures became available. The median follow-up period was 87 months (range, 36 –190 months). The last control was performed in January 2009. Reappearance of live cysts at the site of a previously treated cyst was defined as local recurrence.
Histology Histology of the cystic wall and pericyst was performed in all specimens from radical procedures.
Statistical analysis Comparisons of the continuous variable were performed using Student’s t test, and categorical variables were compared using Pearson’s 2 test. Statistical analyses were performed with Statistica 5’97 (StatSoft, Inc, Tulsa, OK). P values ⬍.05 were regarded as statistically significant.
Results The present study included 454 patients. Table 1 lists their demographic and clinical characteristics. Results of serologic tests (hemagglutination, complement fixation) were positive in 69% of 454 patients. A total of 695 hepatic cysts were treated. Table 2 shows the characteristics of the cysts and their distribution. Cysts were solitary in 296 pa-
Table 2
Characteristics of cysts
Variable
Value
Total number Type Multivesicular Clear Size (cm) Number of cysts per patient 1 2 3 ⬎3 Location Right lobe Deep Left lobe Deep Bilobar Deep
695 639 (87.7%) 56 (12.3%) 19 (3–41) 296 103 34 21
(65.1%) (22.6%) (7.4%) (4.6%)
458 314 203 72 34 31
(65.8%) (68.5%) (29.2%) (35.4%) (4.8%) (91.1%)
Data are expressed as number (percentage) or as mean (range).
800 Table 3
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Treatment
Table 5 Number of Patients
Radical treatment Hepatic resection Right extended Right Left Sectoriectomy CP Total Subtotal Conservative treatment Marsupialization External drainage Omentoplasty
240 73 3 8 18 44 167 138 29 214 75 87 52
tients and multiple in 158 (one lobe in 85, both lobes in 73). A total of 417 cysts were classified as deep: 314 were sited in the right lobe, 72 in the left lobe, and 31 in both lobes. Fifty-six cysts were clear (sterile cysts), and 639 were multivesicular. Migration of daughter cysts into the common bile duct was documented in 71 patients. A conservative approach was adopted in 214 patients (319 cysts), whereas 240 patients (376 cysts) were treated with radical procedures (Table 3). No differences were found in age and gender between these groups. The local complication rates and hospital stays were significantly superior in patients who underwent conservative procedures. No main differences in general complications, with the exception of pleural effusion, were observed in patients treated with conservative or radical procedures. Operation time was significantly shorter for conservative treatment, which, moreover, required fewer blood transfu-
Table 4
Associated procedures
Associated Procedure
Radical Treatment
Conservative Treatment
Cholecystectomy Cholecystectomy ⫹ papillotomy Cholecystectomy ⫹ T-tube Papillotomy Choledochotomy ⫹ T-tube Endoscopic sphincterotomy
45 17 9 3 2 3
38 19 17 5 4 2
sions. Operative mortality was not significantly different between conservative (6.5%) and radical (9.2%) procedures (Table 4). The number and type of surgical associated procedures were similar in the 2 groups (Table 5). The presence of daughter cysts outside the cystic wall was observed on histology in 67 of the 376 specimens (17.8%) from radical procedures. The incidence of recurrence was 30.4% in patients who underwent conservative surgery and 1.2% in patients treated with radical procedures (Table 4). No recurrence was observed in patients with clear cysts. Table 6 shows a comparison between the 2 subgroup time periods. Local complication and recurrence rates decreased from 62% to 32% and from 15% to 8%, respectively, between the 2 time periods.
Comments The desired goals for the treatment of LHD include complete elimination of the parasite and prevention of recurrent disease with minimum mortality.7 However, selec-
Outcomes of radical and conservative procedures
Outcome
Radical Procedures (n ⫽ 240)
Conservative Procedures (n ⫽ 214)
P
Local operative complications Biliary leaks Residual cavity infection Residual cavity hematoma General complications Pleural effusion Pulmonary embolism Cardiac failure Respiratory failure Renal Failure Hepatic failure Hospital stay (d) Recurrences Operation time (min) Blood transfusion (L) Operative mortality
39 11 11 17 18 3 2 5 2 0 6 13.8 3 281 3.53 22
171 65 80 26 29 17 1 4 6 1 0 33.7 48 200 r1.35 14
⬍.001 ⬍.001 ⬍.001 .065 .034 ⬍.001 .630 .870 .111 .289 .019 ⬍.001 ⬍.001 ⬍.001 ⬍.001 .301
(16.2%) (4.6%) (4.6%) (7.1%) (7.5%) (1.2%) (.8%) (2.1%) (.8%) (2.5%) (1.2%) (240–420) (2–6) (9.2%)
(79.9%) (30.4%) (37.4%) (12.1%) (13.6%) (7.9%) (.5%) (1.9%) (2.8%) (.5%) (30.4%)* (110–261) (0–4) (6.5%)
(NS) (NS) (NS) (NS) (NS)
(NS)
Data are expressed as number (percentage) or as mean (range). *Fifty-six of 214 patients treated with conservative procedures had solitary clear cysts. The rate of recurrence was calculated in 158 patients with multivesicular cysts.
S. Tagliacozzo et al. Table 6
Surgical treatment of hepatic hydatidosis
801
Comparison of surgical procedures and main outcomes between the 2 subgroups
Variable Procedure Conservative procedures External drainage Marsupialization Omentoplasty Radical procedures Hepatic resections Pericystectomy Outcomes Local operative complications General complications Recurrences Operative mortality
Group A (1980–1992) (n ⫽ 213)
Group B (1993–2005) (n ⫽ 241)
151 (70.9%) 71 44 36 62 (29.1%) 37 25
63 (26.1%) 16 31 16 178 (73.9%) 36 142
132 24 32 17
(61.9%) (11.3%) (15%) (8%)
tion of the most appropriate treatment to achieve these goals remains the subject of debate, and 3 main approaches are used to date: systemic chemotherapy, percutaneous procedures, and surgical treatment. Systemic chemotherapy is presently based on benzimidazole carbamate compounds. However, the clinical efficacy of these treatments is not clear; complete regression of cysts has never been reported, whereas persistence of living parasite within the cysts has been documented in ⬎50% of the patients being treated preoperatively with benzimidazole compounds.8 –11 Therefore, the World Health Organization has suggested restricting the use of medical treatment for disseminated systemic disease, cases that are not amenable to surgery, and in which known intra-abdominal spillage of hydatid fluid has occurred, and combined with surgery to prevent postoperative recurrence.9 Percutaneous procedures have been proposed more recently.12–14 The main shortcomings of these techniques are incomplete evacuation of the cyst content, difficulty in achieving adequate scolicidal concentration, doubt about the right exposure time, and sclerosing cholangitis in case of cystobiliary communication.15–18 The use of percutaneous treatment seems to represent an alternative treatment in patients who cannot undergo or refuse surgery. Surgery thus remains the first-line treatment for LHD. However, there is considerable disagreement about the optimal surgical technique.16,19 –22 The major issue is whether complete removal of the pericyst is necessary for the proper care of the disease. Proposed surgical procedures can be divided into 2 groups: conservative procedures and radical procedures. Conservative procedures have been defined as those limited to evacuation of cyst content with part or all the pericyst remaining in situ. These techniques, as suggested, should be preferred to radical procedures because they are safer and easier to perform.20,23,24 However, nonnegligible drawbacks have been reported to affect the outcomes of conservative procedures. The main immediate postoperative complications are biliary leakage and fistulas, along with septic complications of the residual cavity leading to prolonged
78 23 19 19
(32.4%) (9.5%) (7.9%) (7.9%)
P ⬍.001
⬍.001
⬍.001 .547 (NS) .016 .969 (NS)
hospital stays.10,21,25 Most of these complications may be ascribed to the pericyst lining the residual cavity. A pericyst left in situ, especially if thick and calcified, represents an obstacle to liver regeneration filling the residual cavity, thus leading to serum and blood accumulation or liver abscess formation. Furthermore, the persistence of the pericyst hides possible biliary communication in the residual cavity, considered the main reason for biliary leakage, which occurs in up to 50% of patients after conservative procedures.26 However, it should be stressed that even when biliary communications are identified, their closure within a stiff, calcified pericyst wall would not be easy or effective. The incidence of biliary leaks and residual cavity infection in patients of our series treated with conservative procedures was 30.4% and 37.4%, respectively. These data, consistent with those of other authors, confirm conservative surgery as a significant determinant of high complication rates and prolonged hospital stays.27–30 Furthermore, infection, biliary fistula, and slow reduction of the cyst cavity may lead to more serious complications, such as obstruction of main hepatic ducts or the portal vein.31,32 In these cases, reoperation is quite complex, with high mortality due to the technical difficulties related to distorted liver anatomy, deteriorated liver function, and poor general conditions.22 Radical procedures include CP and hepatic resection. Hepatic resection has seldom been considered the principal technique to adopt when treating LHD. The notable development of liver resection surgery in more recent years has not changed this trend, so the rate of hepatic resections rarely exceeds 10% in different series.15,19,22,25 In our series, the rate of hepatic resections was much higher because many patients referred from general hospitals to our tertiary referral center had extremely large or multiple localized cysts responsible for diffuse parenchymal damage. Resections were adopted in these cases because entire sectors, lobes, or hemilivers were destroyed by the cysts, and interruption of main bile ducts would have made their repair questionable because of an extremely high risk for serious cholerrhagia. With the exception of these particular cases,
802 our policy has been to avoid liver resection to spare as much healthy hepatic parenchyma as possible at the first surgery. This trend has led us to use CP more frequently. The purpose of CP is the complete removal of the cyst along with its pericyst (CP) without opening the cavity; this avoids contamination of peritoneum and the risk for leaving behind daughter cysts within the pericyst in the hepatic parenchyma.15,19,22,30,33,34 CP may be performed either as a closed or open procedure. The closed procedure was used mainly in patients with superficial cysts or single-lobe deep cysts. Open CP was performed every time there was a risk for breaking the cyst wall, in case of cysts of the hepatic dome, strictly adherent to the hepatic veins and vena cava, and in case of deep intraparenchymal cysts with an interportocaval location. Both in open and closed procedures, the hepatic lobes were fully mobilized to control the confluence of the hepatic veins and inferior vena cava as well as the retrohepatic segment of the vena cava and vascular and biliary elements of the hepatic hilum. In the open method, after evacuation of its content, the cavity is stubbed with swabs soaked in sterilizing substances. The cyst wall is then sectioned and dissection is carried out by molding with the left hand the residual pericyst to enhance the visual control of its relationship with the surrounding parenchyma and afferent vessels and biliary duct (Fig. 3). For the deep, interportocaval location, the access to the cyst is greatly favored by opening the median fissure, which increases the extension of the cystic wall (Fig. 4). Completion of the detachment of the residual, deep pericyst from the hepatic parenchyma may be further eased by dividing it into segments and performing the separate dissection of each segment after it has been refolded on itself (Fig. 5). In case of hard, calcified pericysts strongly adherent to main vessels,
Figure 3 Open pericystectomy. The cyst has been opened and its contents evacuated. The visual control of the relationship between the cystic wall and hepatic parenchyma are in this way enhanced.
The American Journal of Surgery, Vol 201, No 6, June 2011
Figure 4 Deep interportocaval cysts. The access to the cyst is effectively eased by opening the sagittal fissure.
especially to the vena cava, it is advisable to stop dissection just before the vascular plane and to leave behind a small part of the cystic wall (partial CP) (Fig. 6). Overall postoperative complications and hospital stays associated with radical procedures in our series were strikingly lower compared with those after conservative procedures. Complete removal of the pericyst allows the exact
Figure 5 Dissection of the pericyst is eased by dividing the deepest part of it into segments that are refolded and separately dissected.
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vative treatment, calculated by removing the results of the 56 patients with clear cysts, grew in our series from 22.4% to 30.4%. In conclusion, the use of radical procedures for treating LHD have been confirmed by the results in our series. These techniques should be considered safe and effective, especially at high-flow hepatic surgery centers, because they are associated with an excellent morbidity and mortality rates and because the recurrence rate is reduced almost to zero. CP should be preferred to hepatic resection whenever possible because it avoids the undue sacrifice of healthy liver parenchyma. Alternative treatments and conservative surgical procedures should be restricted to clear cysts, severely ill patients, and situations in which the pericyst tissue strongly adheres to main vessels.
References Figure 6 Partial pericystectomy. Dissection of the cystic wall has been stopped and a plug of the calcified pericyst left in situ adherent to the vena cava.
detection and safe direct suture in healthy hepatic parenchyma of biliary and vascular breaches and thus minimizes the risk for biliary leaks and blood collection. Furthermore, the easy approach of the smooth parenchymal limbs promotes the spontaneous reduction of the residual cavity brought about by natural liver regeneration. Local recurrence represents a major concern in the treatment of LHD.35–37 The cause of local recurrence is failure to remove or kill all viable cysts and protoscolices at the time of surgery. Better understanding of certain aspects related to the survival of infectious agents, mainly exogenous vesiculation, has shed new light on this argument. Exogenous vesiculation, detected in 20.2% of specimens of our series derived from radical surgery, suggests that this would have been the rate of recurrence if conservative procedures had been performed in these patients. This rate, evocatively similar to the 22.4% recurrence rate observed in all the patients of our series treated with conservative surgery, corresponds to the mean rate of recurrences reported in literature.28,36 The cyst content, which may change from clear, that is, sterile cysts, to multivesicular with daughter cysts, makes it necessary to consider these 2 kinds of cysts as different pathologic entities. The absence of the germinal layer excludes clear cysts from the risk for vesiculation, that is, recurrences. In our series, the rate of recurrences in 56 treated clear cysts by conservative procedures was nil. Conservative procedures should then, quite rightly, be considered an adequate treatment for clear cysts. Mixing the results of conservative treatment of clear and multivesicular cysts inevitably would introduce, and has introduced in the literature, a bias that decreases the true rate of immediate and long-term failures of conservative treatment of multivesicular cysts. The local recurrence rate following conser-
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