Journal of Minimal Access Surgery

REVIEW ARTICLE
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Year : 2008  |  Volume : 4  |  Issue : 3  |  Page : 63--70

Changing role of laparoscopy in the management of patients with cirrhosis

AO Adisa1, RK Mishra2,  
1 Laparoscopic Surgery Unit, Department of Surgery, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife, Nigeria
2 Laparoscopy Hospital, New Delhi, India

Correspondence Address:
A O Adisa
Laparoscopic General Surgery Unit, Department of Surgery, Obafemi Awolowo University Teaching Hospitals Complex, Ile-Ife
Nigeria

Abstract

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.



How to cite this article:
Adisa A O, Mishra R K. Changing role of laparoscopy in the management of patients with cirrhosis.J Min Access Surg 2008;4:63-70


How to cite this URL:
Adisa A O, Mishra R K. Changing role of laparoscopy in the management of patients with cirrhosis. J Min Access Surg [serial online] 2008 [cited 2019 Dec 14 ];4:63-70
Available from: http://www.journalofmas.com/text.asp?2008/4/3/63/43089


Full Text

 Introduction



Cirrhosis is a chronic, diffuse and progressive condition characterised by fibrosis and conversion of normal liver architecture into structurally abnormal nodules. [1] 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],[3],[4],[5]

Open surgical procedures in cirrhotic patients are associated with high morbidity and mortality. [6],[7],[8],[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],[11],[12],[13]

 Aim



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, andSafety and efficacy of laparoscopy in the treatment of various surgical conditions in cirrhotic patients.

 Materials and Methods



A literature search was performed using the following search engines: HINARI, Google, High Wire Press, Pubmed and the online Springerlink MetaPress Library available at the Laparoscopy hospital, New 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.

 General Considerations



Pathophysiology of liver cirrhosis [14],[15]

Liver cirrhosis may be caused by Hepatitis C or B infection, alcoholic liver disease, non-alcoholic fatty liver among others. The central histological finding in cirrhosis is the development of hepatic fibrosis with an alteration in the normally balanced processes of extracellular matrix production and degradation. The extracellular matrix which is composed of collagens, glycoproteins, and proteoglycans depends on the activities of stellate cells, which in cirrhosis may become activated into collagen-forming cells by a variety of paracrine factors. Such factors may be released by hepatocytes, Kupffer cells, and sinusoidal endothelium following liver injury. With disease progression, there is increased collagen deposition in the space between hepatocytes and sinusoids (the space of Disse) and diminution of the size of endothelial fenestrae leading to the capillarisation of sinusoids. The capillarisation along with constriction of sinusoids by stellate cells, contribute to the development of portal hypertension in cirrhosis.

Several indices have been proposed for the estimation of the surgical risk in a patient with cirrhosis. [16],[17],[18],[19],[20] Of these, the Child's classification and the modification proposed by Pugh et al , (1973) remain the most widely acceptable. [18],[21],[22] As will be shown later, the outcome of both open and laparoscopic procedures in cirrhotic patients is influenced by the preoperative Child's class.

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. [23],[24],[25] Theoretically, pneumoperitoneum was initially 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 one hour after desufflation. [26] 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 SGOT and SGPT as well as an impairment of the functions of the Kupffer cells within the liver. [27],[28] 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. [29],[30],[31] The levels usually return to normal within 72h 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. [32] In their study, three of the 24 cirrhotic patients who had laparoscopic cholecystectomy were converted to open and two 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. [33]

Preoperative preparation: Preoperative preparation of the patients in elective cases is important. This will include correction of coagulopathy with parenteral Vitamin K administration and or transfusion with fresh frozen plasma, lowering of portal hypertension with medications, attainment of 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. [34]

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 CO 2 insufflation after a head-down tilt will lead to an increase in portal venous blood flow while a head-up tilt before CO 2 insufflation decreases both the portal venous and the hepatic arterial blood flow. [35] 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. [32] 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. [36]

A major safety consideration in the operative technique of patient with cirrhosis is the risk of transmission of Hepatitis B or Hepatitis C virus from the patient to the members of the operating team as these viruses are well known aetiological factors in cirrhosis. Precautions for safe passage and disposal of all sharp objects used intraoperatively are to be strictly adhered to.

 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. [37],[38] 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],[39],[40],[41],[42],[43] In some cases, macronodular cirrhosis is erroneously diagnosed as metastatic disease on ultrasound leading to confusion, repeated biopsies and inappropriate treatment. [44]

With improved expertise and increased use, diagnostic laparoscopy and biopsy are 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. [45] This advantage has been highlighted in many studies comparing laparoscopic biopsy to blind and ultrasound guided percutaneous biopsy in cirrhosis. [46],[47],[48] No study has however compared laparoscopic liver biopsies to transjugular biopsy method while 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. [Table 1] [49],[50],[51],[52] 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%. [53],[54],[55]

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). [38],[48],[55],[56]

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 3) which routinely contraindicate blind percutaneous biopsy. [57]

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. [58] Haydon and Hayes, (1997) also advocated that physicians in the United Kingdom should be the ones performing diagnostic laparoscopy. [59]

 Therapeutic Role of Laparoscopy in Cirrhosis



Laparoscopic cholecystectomy in cirrhotic patients

Post-mortem examinations have revealed an incidence of gallstones twice as high in cirrhotic patients as in the general population. [60],[61],[62] This is commonly attributed to accelerated pigment stone formation. Small size, friable bilirubin stones are the most common type seen in cirrhosis. [63],[64] 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. [49],[50],[56],[57] These poor outcomes have led to the development of many multifactorial indices to more accurately estimate the surgical risk in cirrhosis. [18],[19],[20],[65] 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. [66],[67] 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. [Table 2] [12],[13],[68],[69],[70],[71] 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. [71]

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. [72]

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. [68]

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. [10] 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 porto-systemic venous communication. [75] 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. [76] In the report, the authors used dual mesh prosthesis and advocated meticulous sterile fashion of mesh insertion and fixation. This is important since ascitic 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. [75]

Laparoscopic management of ascites

The pathogenesis of ascites in cirrhosis is multifactorial. [77] Mild to moderate ascites is commonly treated medically, however in refractory ascites, surgical procedures may be required. Laparoscopic assisted peritoneo-venous shunt insertion has been advocated especially when peritoneal biopsy and or abdominal exploration are required for a definitive diagnosis. [78] Similarly, laparoscopic placement of peritoneal dialysis catheters may be done in refractory ascites with renal impairment. [79]

Other laparoscopic procedures in cirrhotic patients

Cobb et al (2004) reported 52 laparoscopic procedures performed on 50 cirrhotic patients. [11] 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. [80] They reported fewer rates of wound infection and wound bleeding in the laparoscopic group. Many other laparoscopic procedures including laparoscopic liver resections for hepatocellular carcinomas [81],[82] and laparoscopic ultrasound with radiofrequency ablation [83],[84] are now routinely done in cirrhotic patients in some centres.

 Conclusion



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 basic and advanced laparoscopic procedures are associated with fewer postoperative complications when compared with 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. We advocate further research into the effects of prolonged pneumoperitoneum on the hepatic function in cirrhotic patients.

References

1Anthony 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.
2Sandford 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.
3Ong TZ, Tan HJ. Ultrasonography is not reliable in diagnosing liver cirrhosis in clinical practice. Singapore Med J 2003;44:293-5.
4Di Lelio A, Cestari C, Lomazzi A, Berretta L. Cirrhosis: Diagnosis with sonographic study of the liver surface. Radiology 1989;172:389-92.
5Ladenheim JA, Luba DG, Yao F, Gregory PB, Jeffrey RB, Garcia G. Limitations of liver surface US in the diagnosis of cirrhosis. Radiology 1992;17:74-8.
6Lindenmuth WW, Eisenberg MM. The surgical risk in cirrhosis of the liver. Arch Surg 1963;86:77-84.
7Doberneck RC, Sterling WA, Allison DC. Morbidity and mortality after operation in non-bleeding cirrhotic patients. Am J Surg 1983;146:306-9.
8Schwartz SI. Biliary tract surgery and cirrhosis: A critical combination. Surgery 1981;90:577-83.
9Wirthlin LS, Urk HV, Malt RB. Predictors of surgical mortality in patients with cirrhosis and non-variceal gastroduodenal bleeding. Surg Gynecol Obstet 1974;139:65-8.
10Belli G, D'Agostino A, Fantini C, Cioffi L, Belli A, Russolillo N, et al . Laparoscopic incisional and umbilical hernia repair in cirrhotic patients. Surg Lap Endosc Percut Tech 2006;16:330-3.
11Cobb WS, Heniford BT, Burns JT, Carbonell AM, Matthews BD, Kercher KW. Cirrhosis is not a contraindication to laparoscopic surgery. Surg Endosc 2005;19:418-23.
12Leone N, Garino M, De Paolis P, Pellicano R, Fronda GR, Rizzetto M. Laparoscopic cholecystectomy in cirrhotic patients. Dig Surg 2001;18:449-52.
13Rasic Z, Bakula B, Zoricic I, Bevanda M, Kozomara D, Brekalo Z. Laparoscopic cholecystectomy in cirrhotic patients. Acta Clin Croat 2002;41:229-31.
14Williams EJ, Iredale JP. Liver cirrhosis. Postgrad Med J 1998;74:193-202.
15Gines P, Cardenas A, Arroyo V, Rodes J. Management of cirrhosis and ascites. N Engl J Med 2004;350:1646-54.
16Cayer D, Sohmer MF. Surgery in patients with cirrhosis. AMA Arch Surg 1955;71:828-38.
17Doberneck RC, Sterling WA Jr, Allison DC. Morbidity and mortality after operation in non-bleeding cirrhotic patients. Am J Surg 1983;146:306-9.
18Child CG, Turcotte JF. The liver and portal hypertension. Philadelphia: WB Saunders; 1964.
19Linton RR. The selection of patients for portacaval shunts. Ann Surg 1951;134:433-43.
20McDermott WV Jr. The double portacaval shunt in the treatment of chronic ascites. Surg Gynaecol Obstet 1960;110:457-69.
21Stone HH. Preoperative and postoperative care. Surg Clin North Am 1977;57:407-19.
22Pugh RN, Murray-Lyon IM, Dawson JL, Pietroni MC, Williams R. Transection of the oesophagus for bleeding oesophageal varices. Br J Surg 1973;60:646-9.
23Shuto K, Kitano S, Yoshida T, Bandoh T, Mitarai Y, Kobayashi M. Haemodynamics and arterial blood gas changes during carbon dioxide and helium pneumoperitoneum in pigs. Surg Endosc 1995;9:1173-8.
24Jakimovicz J, Stultiens G, Smulders F. Laparoscopic insufflation of the abdomen reduces portal venous flow. Surg Endosc 1998;12:129-32.
25Sharma KC, Brandstetter RD, Brensilver JM, Jung LD. Cardiopulmonary physiology and pathophysiology as a consequence of laparoscopic surgery. Chest 1996;110:810-5.
26Tsubio S, Kitano S, Yoshida T, Bandoh T, Ninomiya K, Baatar D. Effects of carbon dioxide pneumoperitoneum on haemodynamics in cirrhotic rats. Surg Endosc 2002;16:1220-5.
27Toens C, Schachtrupp A, Hoer J, Junge K, Klosterhalfen B, Schumpelick V. A porcine model of the abdominal compartment syndrome. Shock 2002;18:316-21.
28Gutt 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;137:1408-12.
29Tan M, Xu FF, Peng JS, Li DM, Chen LH, Lv BJ, et al . Changes in the level of serum liver enzymes after laparoscopic surgery. World J Gastroenterol 2003;9:364-7.
30Saber 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.
31Kotake Y, Takeda J, Matsumoto M, Tagawa M, Kikuchi H. Subclinical hepatic dysfunction in laparoscopic cholecystectomy and laparoscopic colectomy. Br J Anaesth 2001;87:774-7.
32Schiff J, Misra M, Rendon G, Rothschild J, Schwaitzberg S. Laparoscopic cholecystectomy in cirrhotic patients. Surg Endosc 2005;19:1278-81.
33Gelman S, Dillard E, Bradley EL. Hepatic circulation during surgical stress and anesthesia with halothane, isoflurane, or fentanyl. Anesth Analg 1987;66:936-43.
34Garrison RN, Cryer HM, Howard DA, Polk HC Jr. Clarification of the risk factors for abdominal operations in patients with hepatic cirrhosis. Ann Surg 1984;199:648-55.
35Klopfenstein CE, Morel DR, Clergue F, Pastor CM. Effects of abdominal CO 2 insufflation and changes of position on hepatic blood flow in anesthetized pigs. Am J Physiol 1998;275:H900-5.
36Friel CM, Stack J, Forse RA, Babineau TJ. Laparoscopic cholecystectomy in patients with hepatic cirrhosis: A Five-Year Experience. J Gastrointest Surg 1999;3:286-91.
37Mahal AS, Knauer C, Gregory PB. Bleeding after liver biopsy. West J Med 1981;134:11-4.
38Piccinino 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.
39Gaiani S, Gramantieri L, Venturoli N, Piscaglia F, Siringo S, D'Errico A, et al . What is the criterion for differentiating chronic hepatitis from compensated cirrhosis? A prospective study comparing ultrasonography and percutaneous liver biopsy. J Hepatol 1997;27:979-85.
40Ferral H, Male R, Cardiel M, Munoz L, Ferrari F. Cirrhosis: diagnosis by liver surface analysis with high frequency ultrasound. Gastrointest Radiol 1992;17:74-8.
41Simonovsky V. The diagnosis of cirrhosis by high resolution ultrasound of the liver surface. Br J Radiol 1999;72:29-34.
42Colli 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.
43Needleman 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 Am J Roentgenol 1986;146:1011-5.
44Leuschner M, Leuschner U. Diagnostic laparoscopy in focal parenchymal disease of the liver. Endoscopy 1992;24:689-92.
45Jeffers LJ, Findor A, Thung SN. Minimizing sampling error with laparoscopic guided liver biopsy of the right and left lobes. Gastrointest Endosc 1991;37:A266
46Terry R. Risks of needle biopsy of the liver. Br Med J 1952;1:1102-5.
47Thaler H. Uber vorteil und risiko der leberbiopsiemethode nach Menghini. Wien Kin Woschenschr 1964;76:533-8.
48Linder H. Grenzen und gefahren der perkutanen leberbiopsie mit der Menghini nadel. Erfahrungen bei 80,000 leberbiopsien. Dtsch med Wochenschr 1967;39:1751-7.
49Boyce HW, Henning H. Diagnostic laparoscopy in1992: Time for a new look. Endoscopy 1992;24:671-3.
50Jalan RJ, Hayes PC. Laparoscopy in the diagnosis of chronic liver disease. Br J Hosp Med 1995;53:81-6.
51Helmreich-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.
52Jalan RJ, Harrison DJ, Dillon JF, Elton RA, Finlayson ND, Hayes PC. Laparoscopy and histology in the diagnosis of chronic liver disease. Q J Med 1995;88:559-64.
53Menghini G. One-second needle biopsy of the liver. Gastroenterology 1958;35:190-9.
54Lindner H. Grenzen und Gefahren der percutanen Leberbiopsie mit der Menghini Nadel. Dtsch Med Wochenschr 1967;92:1751.
55Henning H, Lightdale CJ, Look D. Color atlas of diagnostic laparoscopy. New York: Thieme Medical Publishers; 1994. p. 23-8.
56Orlando R, Lirrusi F, Okolicsanyi 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.
57Dillon JF, Simpson KJ, Hayes PC. Liver biopsy bleeding time: An unpredictable event. J Gastroenterol Hepatol 1994;9:269-71.
58Vargas C, Jeffers LJ, Bernstein D, Reddy KR, Munnangi S, Behar S, et al . Diagnostic laparoscopy: A 5 year experience in a hepatology training program. Am J Gastroenterol 1995;8:1258-62.
59Haydon GH, Hayes PC. Diagnostic laparoscopy by physicians: We should do it. Q J Med 1997;90:297-304.
60Nicholas P, Rinaudo P, Conn HO. Increased incidence of cholelithiasis in Laennec's cirrhosis: A post-mortem evaluation of pathogenesis. Gastrenterology 1972;63:112-21.
61Bouchier IA. Postmortem study of the frequency of gallstones in patients with cirrhosis of the liver. Gut 1969;10:705-10.
62Maggi A, Solenghi D, Panzeri A, Borroni G, Cazzaniga M, Sangiovanni A, et al . Prevalence and incidence of cholelithiasis in patients with liver cirrhosis. Ital J Gastroenterol Hepatol 1997;29:330-5.
63Dunnington G, Alfrey E, Sampliner R, Kogan F, Putnam C. Natural history of cholelithiasis in patients with alcoholic cirrhosis. Ann Surg 1987;205:226-9.
64Schwesinger WH, Kurtin WE, Levine BA, Page CP. Cirrhosis and alcoholism as pathogenetic factors in pigment gallstone disease. Ann Surg 1985;210:319-22.
65Befeler AS, Palmer DE, Hoffman M, Longo W, Solomon H, Di Bisceglie AM. The safety of intraabdominal surgery in patients with cirrhosis. Arch Surg 2005;140:650-4.
66Gadacz TR, Talamini MA. Traditional versus laparoscopic cholecystectomy. Am J Surg 1991;161:336-8.
67Cuschieri A, Dubios F, Mouiel J, Mouret P, Becker H, Buess G, et al . The European experience with laparoscopic cholecystectomy. Am J Surg 1991;161:385-7.
68Curro G, Baccarani U, Adani G, Cucinotta E. Laparoscopic cholecystectomy in patients with mild cirrhosis and symptomatic cholelithiasis. Transplant Proc 2007;39:1471-3.
69Morino M, Cavuoti G, Miglietta C, Giraudo G, Simone P. Laparoscopic cholecystectomy in cirrhosis: Contraindication or privileged indication? Surg Laparosc Endosc Percutan Tech 2000;10:360-3.
70Cucinotta E, Lazzara S, Melita G. Laparoscopic cholecystectomy in cirrhotic patients. Surg Endosc 2003;17:1958-60.
71Fernandes NF, Schwesinger WH, Hilsenbeck SG, Gross GW, Bay MK, Sirinek KR, et al . Laparoscopic cholecystectomy and cirrhosis: A case-control study of outcomes. Liver Transpl 2000;6:340-4.
72Palanivelu C. Atlas of laparoscopic surgery. New Delhi: Jaypees Medical Publishers; 2000. p. 53-8.
73Clark JR, Wills VL, Hunt DR. Cirrhosis and laparoscopic cholecystectomy. Surg Laparosc Endosc Percutan Tech 2001;11:165-9.
74Yeh CN, Chen MF, Jan YY. Laparoscopic cholecystectomy in 226 cirrhotic patients: Experience of a single centre in Taiwan. Surg Endosc 2002;16:1583-7.
75McAlister V. Management of umbilical hernia in patients with advanced liver disease. Liver Transpl 2003;9:623-5.
76Sarit C, Eliezer A, Mizrahi S. Minimally invasive repair of recurrent strangulated umbilical hernia in cirrhotic patient with refractory ascites. Liver Transpl 2003;9:621-2.
77Arroyo V. Pathophysiiology, diagnosis and treatment of ascites in cirrhosis. Ann Hepatol 2002;1:72-9.
78Renzo 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;14:222-5.
79Lessin MS, Luks FI. Primary laparoscopic placement of peritoneal dialysis catheter in children and young adults. Surg Endosc 1999;13:1165-7.
80Tsugawa K, Koyanagi N, Hashizume M, Tomikawa M, Ayukawa K, Akahoshi K, et al . A comparison of open and laparoscopic appendectomy for patients with liver cirrhosis. Surg Laparosc Endosc Percutan Tech 2001;11:189-94.
81Belli G, Fantini C, D'Agostino A, Belli A, Russolillo N. Laparoscopic liver resections for hepatocellular carcinoma (HCC) in cirrhotic patients. HPB (Oxford) 2004;6:236-46.
82Laurent A, Cherqui D, Lesurtel M, Brunetti F, Tayar C, Fagniez P. Laparoscopic liver resection for subcapsular hepatocellular carcinoma complicating chronic liver disease. Arch Surg 2003;138:763-9.
83Podnos YD, Henry G, Ortiz JA, Ji P, Cooke J, Cao S, et al . Laparoscopic ultrasound with radiofrequency ablation in cirrhotic patients with hepatocellular carcinoma: Technique and technical considerations. Am Surg 2001;67:1181-4.
84Santambrogio R, Podda M, Zuin M, Bertolini E, Bruno S, Cornalba GP, et al. Safety and efficacy of laparoscopic radiofrequency ablation of hepatocellular carcinoma in patients with liver cirrhosis. Surg Endosc 2003;17:1826-32.