DR A. O. ADISA. MBChB, DMAS
Department of Surgery Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Nigeria Member, World Association of Laparoscopic Surgeons (WALS) Member, West African Society of Gastroenterologists (WASOG)
Project submitted towards completion of Combined Course of Fellowship and Diploma in Minimal Access Surgery, World Laparoscopy Hospital, India 110018
Cirrhosis was previously a contraindication to laparoscopic surgery. The associated coagulation defects, portal hypertension and nutritional disorders were seen as risk factors for high morbidity and mortality. Open surgery in cirrhotic patients over the years have witnessed poor outcome. However, as experience with laparoscopic surgery continues to grow, several studies have described the use of laparoscopy for the diagnosis of cirrhosis as well as the treatment of various surgical conditions among cirrhotic patients. This article reviews the effect of laparoscopy on the cirrhotic patient and describes the increasing role of laparoscopy in management of cirrhosis as well as its proven benefits
: Liver cirrhosis, laparoscopic procedures
Cirrhosis is a chronic, diffuse and progressive condition characterised by fibrosis and conversion of normal liver architecture into structurally abnormal nodules . It induces various physiological and metabolic changes in the body which may worsen with disease progression. These changes, including fluid retention, coagulation defects and poor resistance to infections, can increase the peri-operative morbidity and mortality in cirrhotic patients. This observation led to various recommendations advocating the use of non-invasive procedures for the diagnosis and treatment of patients with cirrhosis. Earlier studies however show that different imaging techniques have varying specificity in the diagnosis and staging of liver cirrhosis [2-5].
Open surgical procedures in cirrhotic patients are associated with high morbidity and mortality [6-9]. At the onset of laparoscopic surgery, liver cirrhosis was either an absolute or a relative contraindication; however current literature has increasingly shown that the use of laparoscopy in the diagnosis of cirrhosis and treatment of various disease specific and non-specific surgical conditions in cirrhotic patients is safe and offers many advantages [10-13].
This study aims to evaluate the role of laparoscopy in the management of patients with liver cirrhosis over the years with emphasis on the increasing use of laparoscopy in the diagnosis and treatment of specific and non-specific surgical conditions in cirrhotic patients. This will include a review of:
- The risk of laparoscopy and laparoscopic surgery in cirrhotic patients,
- Previous role and current trends in the use of laparoscopy in the diagnosis of liver cirrhosis, and
- Safety and efficacy of laparoscopy in the treatment of various surgical conditions in cirrhotic patients.
MATERIALS AND METHOD
A literature search was performed using the following search engines: HINARI, Google, High Wire Press and the online Springer link MetaPress Library available at the World Laparoscopy Hospital, Gurugram, NCR Delhi India, where this study was carried out. The following terms were used for the search: “Laparoscopy in Liver cirrhosis”; “Liver cirrhosis, diagnosis”; “Laparoscopic surgery in cirrhosis”; “Surgery and Cirrhosis” and “Surgical procedures in cirrhosis”. A review of the articles that matched the search criteria was then carried out.
Physiological effects of pneumoperitoneum on patients with liver cirrhosis
A major difference of open and laparoscopic procedures is the creation of pneumoperitoneum for visualisation of the abdominal cavity. Studies have shown that along with other effects, there is decreased cardiac output, splanchnic blood flow and portal venous flow following pneumoperitoneum [14, 15, 16]. Theoretically, pneumoperitoneum is considered unsafe in cirrhotic patients since they already have varying degrees of alterations in hepatic blood flow and general haemodynamics. Tsubio et al (2002) studied the effect of carbon dioxide pneumoperitoneum on the haemodynamics of cirrhotic rats and observed a marked decrease in splanchnic organ blood flow (particularly hepatic blood flow), which persisted up to 1hour after desufflation . This suggests that impaired hepatic arterial buffer response may play a role in the decreased hepatic blood flow in cirrhosis. Other studies have shown that the resulting relative ischemia leads to some immediate hepatocyte damage with consequent elevation of various hepatic enzymes such as serum glutamic oxaloacetic transaminase (SGOT), serum glutamic pyruvic transaminase (SGPT), as well as an impairment of the functions of the Kupffer cells within the liver [18,19]. The implication of this in the clinical setting is a possibility of hepatic failure intraoperatively or in the early postoperative period. Few clinical studies have also showed transient increased levels of alanine aminotransferase, aspartate aminotransferase, alcohol dehydrogenase and glutathione S-transferase in patients undergoing laparoscopy. [20, 21, 22]. The levels usually return to normal within 72hours after surgery. These changes, though not very rare, are usually subclinical in human. Within the limits of our literature search, no report of hepatic failure attributable to laparoscopy alone in a cirrhotic patient was found. This may indicate that more factors may be involved in the response of cirrhotic patients to the effect of pneumoperitoneum and should be a subject for further research.
Safety considerations in cirrhotic patients undergoing laparoscopic procedures
The Surgeon: Schiff et al (2005), while concluding that laparoscopic cholecystectomy is safe in cirrhotic patients, stated that “… tremendous amount of patience is necessary (in the procedure) because conversion (to open surgery) does not help to control coagulopathy . In their study, 3 of the 24 cirrhotic patients who had laparoscopic cholecystectomy were converted to open and 2 of these were due to surgeons’ inexperience. This and other findings in the literature suggest a role of the experience of the surgeon in the success of the procedure in this group of patients.
Anaesthetic Techniques in Cirrhotic Patients: As previously noted, hepato-splanchnic perfusion may be impaired in cirrhotic patients. This implies that adequate circulation must be maintained in the patients throughout the period of anaesthesia. In addition, some anaesthetic drugs may have specific effects on liver circulation. While isoflurane increases hepatic regional blood flow, halothane is noted to increase hepatic arterial resistance. Fentanyl, Vencuronium and Pancuronium do not significantly affect hepatic blood flow and may be preferable in cirrhotic patients .
Preoperative Preparation: Preoperative preparation of the patients in elective cases is important. This will include correction of coagulopathy, lowering of portal hypertension, fluid and electrolyte balance as well as control of infection where present. Garrison et al (1984) had identified absolute serum albumin concentration, presence of infection or contamination and number of seconds partial thromboplastin time is deviated from its control value as the three main preoperative variables that predict surgical outcome in cirrhotic patients .
Operative Techniques: Some authors have advocated a number of operative techniques to help minimise the morbidity associated with surgery in cirrhotic patients undergoing laparoscopic procedures. Klopfenstein et al (1998) demonstrated in anaesthetised pigs that CO2 insufflation after a head-down tilt will lead to an increase in portal venous blood flow while a head-up tilt before CO2 insufflation decreases both the portal venous and the hepatic arterial blood flow. This has not been sufficiently studied in humans and the beneficial effects of positioning on the hepatic circulation in cirrhotic patients need to be further studied.
Friel et al (1999) advocated the use of open technique using Hassan’s trocar for access to prevent inadvertent puncture of an umbilical varix or placement of the trocar in the right paramedian position when umbilical varix is already present . Other techniques advocated include subtotal cholecystectomy in cases of severe inflammation leaving the back wall of the gallbladder on the liver bed. The use of mechanical compression from introduced surgical sponges to achieve haemostasis with additional haemostatic modalities such as oxidized cellulose, topical haemostatic agents, application of ultrasonic energy via a harmonic scalpel and the use of argon beam coagulator which can be inserted through an operative port have also been described .
ROLE OF LAPAROSCOPY IN DIAGNOSIS OF LIVER CIRRHOSIS
The diagnosis of liver cirrhosis is important in the evaluation and management of the patients. Histopathology of a liver biopsy specimen is the gold standard for diagnosis but the invasive procedure required as well as the associated complications encountered by initial researchers led to the preference for imaging and biochemical studies [28, 29]. However, the accuracy of liver ultrasonography which is the most commonly used imaging modality in the diagnosis of cirrhosis has been the subject of much debate. While features of portal hypertension and marked architectural distortions in late stage disease can be easily identified on ultrasound, many studies have reported low specificity and sensitivity of ultrasound findings when correlated with histopathological reports especially in early cirrhosis. Other studies have however shown that high resolution ultrasound analysis of the liver is of high accuracy in diagnosing cirrhosis [3, 4, 30-34]. In some cases, macronodular cirrhosis is erroneously diagnosed as metastatic disease on ultrasound leading to confusion, repeated biopsies and inappropriate treatment .
With improved expertise and increased use, diagnostic laparoscopy and biopsy is now commonly employed in cirrhosis. Laparoscopy enables direct visualisation of the liver surfaces, usually both liver lobes, which can vary in their degree of nodularity with disease progression . This advantage has been highlighted in many studies comparing laparoscopic biopsy to blind and ultrasound guided percutaneous biopsy in cirrhosis [37-39]. Different studies have affirmed that the sensitivity and specificity of pathological features identified at laparoscopy are close to 100% since laparoscopic biopsies are directed at macroscopically identified targets [40-43]. (Table 1) This is in contrast to percutaneous biopsy where the specimen may be too small or fragmented and therefore inadequate for definitive confirmation of cirrhosis. False negative findings with blind biopsies in cirrhosis have been estimated to be up to 10-15% [44-46].
Table1: Sensitivity and specificity of pathological features identified at laparoscopy
|Pathological feature||Sensitivity (%)||Specificity (%)|
Adapted from Jalan et al. (1995).
In large patient population studies, Orlando et al (1990) and Henning et al, (1994) have reported complication rates from diagnostic laparotomies for liver biopsies that are similar to those reported for percutaneous biopsies in previous studies by Linder (1967) and Piccinino et al (1986) [29,39,46,47].
Laparoscopy also allows application of direct pressure or a heater probe to attain haemostasis in the event of bleeding from a biopsy site and may hence be carried out safely despite haematological abnormalities (e.g. PTR>1.3; Platelet <80,000/mm3) which routinely contraindicate blind percutaneous biopsy .
The use of diagnostic laparoscopy has therefore expanded in liver cirrhosis so much that Vargas et al, (1995) recommended that diagnostic laparoscopy should be incorporated into the training programmes for gastroenterologists in America . Haydon and Hayes, (1997) also advocated that physicians in the United Kingdom should be the ones performing diagnostic laparoscopy .
THERAPEUTIC ROLE OF LAPAROSCOPY IN CIRRHOSIS
Laparoscopic Cholecystectomy in Cirrhotic Patients
Postmortem examinations have revealed an incidence of gallstones twice as high in cirrhotic patients as in the general population [51, 52, and 53]. This is commonly attributed to accelerated pigment stone formation. Small size, friable bilirubin stones are the most common type seen in cirrhosis [54, 55]. With the increased incidence, symptoms of gallstones and its complications are also frequently seen in cirrhotic patients thus indicating cholecystectomy and hence cholecystectomy may be the commonest laparoscopic procedure performed in cirrhotic patients.
Open cholecystectomy (OC) in cirrhotic patients is associated with poor outcome. Many studies have reported high rates of morbidity (5-30%) and mortality (7-25%) compared to 0.5-1% mortality in non-cirrhotics [40, 41, 47, and 48]. These poor outcomes have led to the development of many multifactorial indices to more accurately estimate the surgical risk in cirrhosis [56-59]. However across the various stages of the disease, open procedure still has a high rate of complications.
At the inception of laparoscopic surgery, cirrhosis was listed either as an absolute or a relative contraindication [60, 61]. However with increased experience with laparoscopy, several studies across the world have demonstrated that laparoscopic cholecystectomy (LC) is safe and effective with fewer complications compared to OC [12, 13, 62-65]. (Table2) Specifically, LC is associated with less intraoperative bleeding and shorter duration of hospital stay and fewer postoperative complications. Visualisation is much better than with open cholecystectomy and the small vessels that may not be seen at open surgery appear larger during laparoscopy allowing for better haemostasis. It is also particularly useful in liver transplant candidates since it is associated with fewer postoperative adhesions 
Certain problems may be encountered during laparoscopic cholecystectomy with a cirrhotic liver. There may be difficulty with traction of the liver, inadequate exposure of the hilum, adhesions around the gallbladder and the hilum with difficulty in identifying anatomical landmarks as well as increased vascularity of the gallbladder bed. The use of additional ports as well as performance of retrograde cholecystectomy or modified subtotal cholecystectomy in selected cases can be helpful .
Table 2: Recent reports on laparoscopic cholecystectomy in patients with liver cirrhosis
|Reference||No||Child-Pugh Classification A B C||Morbidity||Mortality|
The safety of LC is however more documented for patients with Child-Pugh’s class A and B. The experience of Yeh et al (2002) with LC in 226 cirrhotic patients represents the largest series published so far. However no patient with Child-Pugh’s class C was operated upon. This is similar to the patient population in most of the studies as shown in Table 2. Curro et al (2005) compared 4 Child-Pugh’s class C patients who had LC with 38 Child-Pugh’s A and B patients in the same centre and found a morbidity rate of 75% in the Child-Pugh’s C patients compared with 26% in the A and B group. The authors further advised that surgery in Child-Pugh’s C patients should be avoided except in acute emergencies where conservative procedures such as gallbladder aspiration and partial cholecystectomies may be considered. A meta-analysis of LC in cirrhotic patients, (Puggioni and Wong, 2003) was inconclusive in either recommending LC for patients with Child-Pugh’s class C cirrhosis or not due to inconclusive data in most of the studies reviewed. It is not clear whether many surgeons consider the risks of morbidity and mortality to be so high as to withhold even emergency surgeries in these patients or that the data on this group of patients are not included in the different publications. It would seem that indications for surgery in these patients should be limited to emergencies such as cholecystectomy for acute cholecystitis. Even in such instances, percutaneous drainage of the gallbladder and other conservative procedures may suffice .
Laparoscopic hernia repair in cirrhosis
In a report of 14 cirrhotic patients who underwent laparoscopic incisional and umbilical hernia repair, Giulio et al (2006) observed that though open repair in cirrhotic patients has significant recurrence rates and frequent wound infections, laparoscopic repair yields less morbidity and fewer recurrences . The study further highlighted that the preservation of the anterior abdominal wall in laparoscopic repair avoids the interruption of collateral veins which are not infrequently distended in cirrhotic patients.
McAlister (2003), in an editorial titled “Management of umbilical hernia in patients with advanced liver disease” observed that the tendency for umbilical hernia to develop in patients with chronic liver disease is high and opined that in addition to the abdominal distension and abdominal muscle weakness which may predispose to hernias generally in them, umbilical hernia may be commoner due to transmission of additional pressure to the umbilicus via the portosystemic venous communication . He noted that previous attempts at umbilical hernia repair in cirrhotic patients were followed by different complications. The suture era witnessed a high rate of recurrences while the era of prosthetic mesh had fewer recurrences but a greater rate of wound complications. Laparoscopic umbilical hernia repair in cirrhotic patients appears to offer advantages over the open methods. He further proposed an algorithm for the management of umbilical hernia in these patients. Emergency repair is necessitated when there are associated complications such as incarceration, bowel obstruction or impending rupture. Elective repair is to be considered in other patients after controlling coagulopathy and ascites. In liver transplant candidates, elective repair should be delayed for a formal repair with transplantation.
Successful laparoscopic repair of recurrent incarcerated umbilical hernia in a cirrhotic patient with refractory ascites has also been reported . In the report, the authors used dual mesh prosthesis and advocated meticulous sterile fashion of mesh insertion and fixation. This is important since ascetic fluid infection, which may occur after surgery may affect the hernia mesh repair. The possibility of mesh migration due to the ascitic fluid can be reduced by placing the mesh in a preperitoneal space .
Laparoscopic management of ascites
The pathogenesis of ascites in cirrhosis is multifactorial . Mild to moderate ascites is commonly treated medically, however in refractory ascites, surgical procedures may be required. Laparoscopic assisted vetriculo-peritoneal shunt insertion has been advocated especially when peritoneal biopsy and or abdominal exploration is required for a definitive diagnosis . Similarly, laparoscopic placement of peritoneal dialysis catheters may be done in refractory ascites with renal impairment .
Other laparoscopic procedures in Cirrhotic Patients
Cobb et al (2004) reported 52 laparoscopic procedures performed on 50 cirrhotic patients  These procedures, including cholecystectomies, splenectomies, colectomies, diagnostic laparoscopies, ventral hernia repairs , Nissen fundoplication, Heller’s myotomy, gastric bypass and radical nephrectomy had a morbidity rate of 16% but no mortality. Tsugawa et al, (2001) had earlier compared open and laparoscopic appendicectomies among patients with liver cirrhosis . They reported fewer complications in the laparoscopic procedures. Many other studies have also affirmed the feasibility and safety as well as different benefits of laparoscopic surgeries for various diagnostic and therapeutic procedures in cirrhotic patients as the experience with the procedures increase
This review has shown that the risk of laparoscopy, though real, is not significant enough to contraindicate the procedure in cirrhotic patients. Laparoscopy is being used increasingly in the diagnosis and treatment of these patients. Many studies have also shown that laparoscopy is not only safe in carefully selected cirrhotic patients but also has many advantages over the various open procedures. However, its safety in Child-Pugh’s class C patients is not yet proven hence surgery in such patients may be limited to conservative procedures in emergency cases.
1. Anthony PP, Ishak KG, Nayak NC, Poulsen HE, Scheuer PJ, Sobin LH. The morphology of cirrhosis. Recommendations on definition, nomenclature and classification by a working group sponsored by the World Health Organization. J Clin Pathol 1978;31:395-414
2. Sandford NL, Walsh P, Matis C, Baddeley H, Powell LW. Is ultrasonography useful n the assessment of diffuse parenchymal liver disease? Gastroenterology. 1985; 89:186-91.
3. Ong TZ, Tan HJ. Ultrasonography is not reliable in diagnosing liver cirrhosis in clinical practice. SingaporeMed J. 2003;44(6):293-295.
4. Di Lelio A, Cestari C, Lomazzi A, Berretta L. Cirrhosis: Diagnosis with sonographic study of the liver surface. Radiology 1989; 172:389-392.
5. Ladenheim JA, Luba DG, Yao F, Gregory PB, Jeffrey RB, Garcia G. Limitations of liver surface US in the diagnosis of cirrhosis. Radiology. 1992;17:74-78.
6. Lindenmuth WW, Eisenberg MM. The surgical risk in cirrhosis of the liver. Arch Surg 1963; 86:77-84.
7. Doberneck RC, Sterling WA, Allison DC. Morbidity and mortality after operation in non-bleeding cirrhotic patients. Am J Surg 1983; 146:306-309.
8. Schwartz SI. Biliary tract surgery and cirrhosis: a critical combination. Surgery 1981; 90:577-583.
9. Wirthlin LS, Urk HV, Malt RB. Predictors of surgical mortality in patients with cirrhosis and non-variceal gastroduodenal bleeding. Surg Gynecol Obstet 1974; 139:65-68.
10. Guilio B, Alberto D, Corrado F, Luigi C, Andrea B, Nadia R, Serena L. Laparoscopic incisional and umbilical hernia repair in cirrhotic patients. Surg Lap Endosc Percut Tech. 2006 16(5):330-333.
11. Cobb WS, Heniford BT, Burns JT, Carbonell AM, Matthews BD, Kercher KW. Cirrhosis is not a contraindication to laparoscopic surgery. Surg Endosc (2005) 19: 418–423.
12. Leone N, Garino M, Paolis PD, Pellicano R, Fronda GR, Rizzetto M. Laparoscopic Cholecystectomy in Cirrhotic Patients. Dig Surg 2001;18:449-452.
13. Rasic Z, Bakula B, Zoricic I, Bevanda M, Kozomara D, Brekalo Z. Laparoscopic cholecystectomy in cirrhotic patients. Acta Clin Croat. 2002; 41:229-231.
14. Shuto K, Kitano S, Yoshida T, Bandoh T, Mitarai Y, Kobayashi M. (1995) Haemodynamics and arterial blood gas changes during carbon dioxide and helium pneumoperitoneum in pigs. Surg Endosc. 9:1173-1178.
15. Jakimovicz J, Stultiens G, Smulders F. (1998). Laparoscopic insufflation of the abdomen reduces portal venous flow. Surg Endosc. 12:129-132.
16. Kailash CS, Robert DB, Jeffrey MB, Lance DJ. (1996). Cardiopulmonary physiology and pathophysiology as a consequence of laparoscopic surgery. Chest 110:810-815.
17. Tsubio S, Kitano S, Yoshida T, Bandoh T, Ninomiya K, Baatar D. Effects of carbon dioxide pneumoperitoneum on haemodynamics in cirrhotic rats. (2002). Surg Endosc. 16:1220-1225.
18. Toens C, Schachtrupp A, Hoer J, Junge K, Klosterhalfen B, Schumpelick V. A porcine model of the abdominal compartment syndrome. Shock 2002;18:316–321.
19. Gutt CN, Kim ZG, Schemmer P, Krahenbuhl L, Schmedt CG. Impact of laparoscopic and conventional surgery on Kupffer cells, tumor associated CD44 expression, and intrahepatic tumor spread. Arch Surg 2002;137:1408–1412.
20. Tan M, Xu FF, Peng JS, Li DM, Chen LH, Lv BJ, Zhao ZX, Huang C, Zheng CX. Changes in the level of serum liver enzymes after laparoscopic surgery. World J Gastroenterol 2003;9:364–367.
21. Saber AA, Laraja RD, Nalbandian HI, Pablos-Mendez A, Hanna K: Changes in liver function tests after laparoscopic cholecystectomy: Not so rare, not always ominous. Am. Surg 2000;66:699–702.
22. Kotake Y, Takeda J, Matsumoto M, Tagawa M, Kikuchi H: Subclinical hepatic dysfunction in laparoscopic cholecystectomy and laparoscopic colectomy. Br J Anaesth 2001;87:774–777.
23. Schiff J, Misra M, Rendon G, Rothschild J, Schwaitzberg S. Laparoscopic cholecystectomy in cirrhotic patients. Surg Endosc (2005) 19: 1278–1281
24. Gelman S, Dillard E, Bradley EL. Hepatic circulation during surgical stress and anesthesia with halothane, isoflurane, or fentanyl. Anesth Analg 1987;66:936–43.
25. Garrison RN, Cryer HM, Howard DA, Polk HC. Clarification of the risk factors for abdominal operations in patients with hepatic cirrhosis. Ann Surg. 1984; 199:648-655.
26. Klopfenstein CE, Morel D.R, Clergue F, Pastor CM. Effects of abdominal CO2 insufflation and changes of position on hepatic blood flow in anesthetized pigs. Am J Physiol 1998;275:H900–H905
27. Friel CM, Stack J, Forse RA, Babineau TJ. Laparoscopic Cholecystectomy in Patients with Hepatic Cirrhosis: A Five-Year Experience. J Gastrointest Surg 1999;3:286-291.
28. Mahal A, Knauer C, Gregory P. Bleeding after liver biopsy. West J Med 1981; 134:11-14
29. Piccinino F, Sagnelli E, Pasquale G, Giusti G. Complications following percutaneous liver biopsy: multicenter retrospective study on 68,276 biopsies. J Hepatol 1986;2:165-73
30. Gaiani S, Gramantieri L, Venturoli N. What is the criterion for differentiating chronic hepatitis from compensated cirrhosis? A prospective study comparing ultrasonography and percutaneous liver biopsy. J Hepatol1997; 27: 979–985
31. Ferral H, Male R, Cardiel M, Munoz L, Ferrari FQ. Cirrhosis: diagnosis by liver surface analysis with high frequency ultrasound. Gastrointest Radiol. 1992; 17:74-8
32. Simonovski V. The diagnosis of cirrhosis by high resolution ultrasound of the liver surface. Br J Radiol.1999; 72:29-34
33. Colli A, Fraquelli M, Andreoletti M, Marino B, Zuccoli E, Conte D. Severe liver fibrosis or cirrhosis: Accuracy of US for detection- Analysis of 300 cases. Radiology 2003; 227:89-94
34. Needleman L, Kurtz AB, Rifkin MD, Cooper HS, Pasto ME, Goldberg BB. Sonography of diffuse benign liver disease: accuracy of pattern of recognition and grading. AJR 1986; 146:1011-5
35. Leuschner M, Leuschner U. Diagnostic laparoscopy in focal parenchymal disease of the liver. Endoscopy. 1992; 24:682-6
36. Jeffers LJ, Findor A, Thung SN et al. Minimizing sampling error with laparoscopic guided liver biopsy of the right and left lobes. Gastroin-test Endosc 1991; 37: A266
37. Terry R. Risks of needle biopsy of the liver. Br Med J 1952; 1:1102-1105
38. Thaler H. Uber vorteil und risiko der leberbiopsiemethode nach Menghini. Wien Kin Woschenschr1964.;76:533-538
39. Linder H. Grenzen und gefahren der perkutanen leberbiopsie mit der Menghini nadel. Erfahrungen bei 80,000 leberbiopsien. Dtsch med Wochenschr. 1967;39:1751-1757
40. Boyce HW, Henning H. Diagnostic laparoscopy in1992: Time for a new look. Endoscopy 1992; 24:671-3
41. Jalan RJ, Hayes PC. Laparoscopy in the diagnosis of chronic liver disease. Br J Hosp Med 1995; 53:81-6
42. Helmreich-Becker I, Schirmacher P, Denzer U, Hensel A, Meyer zum Buschenfelde KH, Lohse AW. Minilaparoscopy in the Diagnosis of Cirrhosis: Superiority in Patients with Child–Pugh A and Macronodular Disease. Endoscopy.2003; 35: 55–60
43. Jalan RJ, Harrison DJ, Dillon JF, Elton RA, Finlayson NDC, Hayes PC. Laparoscopy and histology in the diagnosis of chronic liver disease. Q J Med. 1995; 88:559-64
44. Menghini G. One-second needle biopsy of the liver. Gastroenterology 1958; 35:190
45. Lindner H. Grenzen und Gefahren der percutanen Leberbiopsie mit der Menghini Nadel. Dtsch Med Wochenschr 1967;92: 1751
46. Henning H, Lightdale CJ, Look D. Color atlas of diagnostic laparoscopy. New York. Thieme Medical Publishers. 1994: 23-8
47. Orlando R, Lirrusi F, Oklicsanyl L. Laparoscopy and liver Biopsy: further evidence that the two procedures improve the diagnosis of liver cirrhosis- a retrospective study of 1003 consecutive examinations. J Clin Gastroenterol 1990; 12:47-52
48. Dillon JF, Simpson KJ, Hayes PC. Liver biopsy bleeding time: An unpredictable event. J Gastroenterol Hepatol. 1994; 9:269-71
49. Vargas C, Jeffers LJ, Bernstein D, Reddy R, Munnangi S, Behar S, Scott C, Parker T, Schiff ER. Diagnostic laparoscopy: A 5 year experience in a hepatology training program. Am J Gastroenterol 1995; 8:1258-61
50. Haydon GH, Hayes PC. Diagnostic laparoscopy by physicians: we should do it. Q J Med 1997; 90:297-304
51. Nicholas P, Rinaudo P, Conn H. Increased incidence of cholelithiasis in Laennec’s cirrhosis. A post-mortem evaluation of pathogenesis. Gastrenterology. 1972; 63:112-21
52. Bouchier I. Postmortem study of the frequency of gallstones in patients with cirrhosis of the liver. Gut 1969;10:705–710.
53. Maggi A, Solenghi D, Panzeri A. Prevalence and incidence of cholelithiasis in patients with liver cirrhosis. Ital J Gastroenterol.1991; 86:1629-32
54. Dunnington G, Alfrey E, Sampliner R, Kogan F, Putnam C. Natural history of cholelithiasis in patients with alcoholic cirrhosis. Ann. Surg. 1987; 205: 226–9.
55. Schwesinger WH, Kurtin WE, Levine BA, Page CP. Cirrhosis and alcoholism as pathogenetic factors in pigment gallstone disease. Ann Surg 1985;210:319-322.
56. Befeler AS, Palmer DE, Hoffman M, Longo W, Solomon H, Di Bisceglie AM. The safety of intraabdominal Surgery in patients with cirrhosis. Arch Surg 2005; 140:650-654
57. Child CG, Turcotte JF. The Liver and Portal Hypertension. Philadelphia: Saunders, WB 1964.
58. Linton RR. The selection of patients for portacaval shunts. Ann Surg 1951; 134:433-443.
59. McDermott W. The double portacaval shunt in the treatment of chronic ascites. Surg Gynaecol Obstet. 1960; 110:457-469.
60. Gadacz TR, Talamini MA: Traditional versus laparoscopic cholecystectomy. Am J Surg.1991;161:336–338
61. Cushieri A, Dubios F, Mouiel J, Mouret P, Becker H, Buess G, Trede M, Troidl H. The European experience with laparoscopic cholecystectomy. Am J Surg 1991; 161:385-387
62. Curro G, Baccarani U, Adani G, Cucinotta E. Laparoscopic cholecystectomy in patients with mild cirrhosis and symptomatic cholelithiasis. Transplant Proc. 2007 ;39:1471-1473
63. Morino M, Cavuoti G, Miglietta C, Giraudo G, Simone P. Laparoscopic cholecystectomy in cirrhosis: contraindication or privileged indication? Surg Laparosc Endosc Percutan Tech. 2000 Dec;10:360-363
64. Cucinotta E, Lazzara S, Melita G. Laparoscopic cholecystectomy in cirrhotic patients. Surg Endosc. 2003 ;17:1958-1960
65. Fernandes FN, Schwesinger WH, Hilsenbeck SG, Gross GW, Bay MK, Sirinek KR, Schenker S. Laparoscopic Cholecystectomy and Cirrhosis: A Case-Control Study of Outcomes. Liver transplantation. 2000; 6:340-344
66. Palanivelu C. Atlas of laparoscopic surgery. 2000. Jaypees Medical Publishers. New Delhi: 53-58
67. Clark JR, Wills VL, Hunt DR. Cirrhosis and laparoscopic cholecystectomy. Surg Laparosc Endosc Percutan Tech. 2001; 11:165-169.
68. Yeh CN, Chen MF, Jan YY. Laparoscopic cholecystectomy in 226 cirrhotic patients: experience of a single centre in Taiwan. Surg Endosc. 2002; 16:1583-1587
69. McAlister V. Management of Umbilical Hernia in Patients With Advanced Liver Disease. LiverTransplantation. 2003 ;9:623-625
70. Sarit C, Eliezer A, Mizrahi S. Minimally invasive repair of recurrent strangulated umbilical hernia in cirrhotic patient with refractory ascites. Liver transplantation. 2003; 9: 621-622.
71. Arroyo V. Pathophysiiology, diagnosis and treatment of ascites in cirrhosis. Annals of hepatology 2002; 1:72-79
72. Renzo C, Dorico R, Massimiliano B, Silvia C, Maria Antonella R, Claudio Z. Role of Different Techniques for the Placement of Denver Peritoneovenous Shunt (PVS) in Malignant Ascites. Surg Laparosc Endosc Percutan Tech. 2004;14:222-225
73. Lessin MS,LuksFI. Primary laparoscopic placement of peritoneal dialysis cathters in children and young adults. Surg Endosc. 1999; 13:1165-1167.
74. Tsugawa K, Koyanagi N, Hashizume M, Tomikawa M, Ayukawa K, Akahoshi, K, Sugimachi K. A comparison of an open and laparoscopic appendectomy for patients with liver cirrhosis. Surg Laparosc Endosc Percutan Tech. 2001; 11:189-194