Abstract
Abstract
Background:
The laparoscopic approach to liver resective surgery is slowly spreading to specialized centers. Little is known about factors influencing the immediate postoperative outcome.
Study Design:
The purpose of the study was to evaluate the immediate outcome of laparoscopic liver resection (LLR), with particular emphasis on intraoperative bleeding and conversion. A retrospective analysis of demographic, clinical, and surgical data, including conversion, morbidity/mortality, and hospital stay, of the first 100 patients at our institution undergoing LLR from February 1997 through March 2007 was performed.
Results:
Indication for LLR was benign lesion in 28 patients, malignancy in 33, and living donation in 39. Seventy-five resections involved two or more segments. Mean blood loss was 120±127.6 mL. One patient (1%) required transfusion. Mean operative time was 253±91.6 minutes. No patient died. Postoperative complications occurred in 21 patients. The conversion rate was 17%. Variables related to conversion were American Society of Anesthesiologists Class II, body mass index, cirrhosis, necessity for the Pringle maneuver, and intraoperative blood loss. Conversion did not influence the operative time. Patients with conversion had more complications and a longer hospital stay.
Conclusions:
Liver resection by laparoscopy is feasible and safe, implying low intraoperative blood loss. Not perfect physical conditions, cirrhosis, high body mass index, and, intraoperatively, blood loss and the necessity of a Pringle maneuver should be considered risk factors for conversion. A meticulous dissection by bipolar coagulation, Harmonic® (Ethicon) scalpel, and ultrasound dissector, other than the attitude not to delay conversion in difficult cases, may allow for low blood loss without prolongation of operative time, with a possible, slight increase of the conversion rate.
Introduction
Despite the initial concerns regarding the laparoscopic management of the intrinsic difficulties of liver surgery and its possible complications, several studies have confirmed the feasibility and safety of this approach in selected patients.5–10 In particular, considering intraoperative hemorrhage, which is traditionally the main concern of liver surgeons, laparoscopic liver surgery was reported to be associated with less bleeding and a shorter operative time than traditional surgery.11–14
Nevertheless, most of the published laparoscopic liver resection series have shown bleeding as the main cause of conversion.6,7,10,15–17 Even though not considered a complication in itself, conversion inevitably reduces the supposed advantages of a mini-invasive approach. Such a sequence of adverse events may be supposed to prolong operative time and postoperative hospital stay and to increase the morbidity of the procedure.
We present the results of laparoscopic liver resection (LLR) in the first 100 consecutive patients treated with a totally laparoscopic approach at our institution. Because we traditionally have a blood-sparing attitude in liver resective surgery, regardless of the adopted approach (traditional or laparoscopic), we decided to analyze our results with special emphasis on intraoperative bleeding, conversion, and their consequences on the immediate postoperative outcome.
Moreover, in order to improve the selection of patients to undergo LLR, we tried to identify pre- and intraoperative criteria related to conversion, by comparing patients undergoing converted procedures and those successfully treated laparoscopically.
Subjects and Methods
A retrospective analysis of prospectively collected demographic, clinical, and surgical data of 100 consecutive patients undergoing LLR from February 1997 to March 2007 at our institution was performed. Personal demographic and clinical data included sex, age, weight, body mass index (BMI), American Society of Anesthesiologists (ASA) physical status score, presence (and etiology) of cirrhosis, and previous abdominal surgery.
Patients' selection and laparoscopic procedures
Tumor liver resection
Patients referred for benign or malignant liver lesions were routinely considered for laparoscopic hepatectomy. The indication for surgery was not modified by the use of the laparoscopic approach, especially for benign lesions, which were resected only in the presence of symptoms or uncertain diagnosis at biopsy. Resection of metastases was undertaken only in the absence of peritoneal carcinomatosis and/or unresectable extrahepatic disease. In patients with compensated cirrhosis, resection of hepatocellular carcinoma (HCC) was considered.
Liver resections were defined according to Couinaud's classification of liver segments. Hepatic resection was considered anatomic when at least one segment was removed entirely; all other resections were defined as nonanatomic or atypical. Among anatomic resections, hepatectomies were defined as “major” whenever more than two Couinaud's segments were resected, whereas they were defined “minor” (or segmental) when resection involved one or two segments. Owing to intrinsic technical difficulties due to left vessels/biliary duct dissection and parenchymal section, according to the technique we previously described, 18 left lobectomy performed for transplantation from a living donor was considered a major hepatectomy, although involving only two hepatic segments. The indications for laparoscopic segmental and atypical resections were tumors smaller than 4 cm located in the inferior or anterior segments of the liver (segments III, IV, V, and VI) or in left segment I. Tumors invading or adjacent to the portal pedicle or hepatic veins were not considered suitable for laparoscopy.
Major hepatectomies for liver diseases (three or more Couinaud's segments) were performed for either larger tumors or localized Caroli's or polycystic disease. Vascular control (of the portal vessels and hepatic vein) and ligation of the portal pedicle were carried out before the parenchymal transection whenever possible (anatomic resections with prior vascular control). This procedure was typically sought for right hepatectomy (segments V, VI, VII, and VIII), left hepatectomy (segments II, III, and IV), and left lateral lobectomy (segments II and III), including living donor's resections. Other resections including bisegmental, segmental, and nonanatomic resections were performed without prior vascular control.
Laparoscopy was carried out under carbon dioxide pneumoperitoneum, with the abdominal pressure maintained between 11 and 13 mm Hg. The initial step was visual and ultrasonographic exploration of the liver. Once the decision had been made to proceed with resection, a tape was placed around the hepatic pedicle in case a Pringle maneuver became necessary. For major hepatectomy, the portal pedicle was dissected outside the liver parenchyma with an intrafascial dissection. Arterial branches were clipped and divided. The portal branch was divided with a linear stapler. The common bile duct was dissected as high as possible without any duct section. The hilar plate was divided and clipped above the biliary convergence. The inferior vena cava was dissected from bottom to top. The omolateral hepatic vein was dissected free but not divided before parenchymal division. Hepatic transection was initiated according to the line of demarcation visualized on Glisson's capsule, directed to the axis of the inferior vena cava. The resected specimen was placed in a plastic bag and withdrawn through a suprapubic incision. Abdominal drainage was usually omitted, and the pneumoperitoneum was vented with the trocars in place in patients with malignant tumors.
Living donor's resection
LLR in living donors for transplantation in children was included in the series. The liver graft included the left lateral section (i.e., segments II and III), the left branch of the hepatic artery and left portal branch, the left bile duct, and the left hepatic vein. No clamping was used during parenchyma transection. The technique of laparoscopic left lateral sectionectomy in living donors is described in a previous publication. 18
Perioperative assessment
Collected intraoperative data included purpose of the procedure (tumor resection, liver donor left lobectomy), nature of the lesion (neoplastic or benign), type of procedure, need for a Pringle maneuver, blood loss, and operative time. The following postoperative data were also recorded: mortality/morbidity, hospital stay, and intensive care hospitalization. All complications were prospectively monitored in all cases. Surgical complications included biliary fistula, hemorrhage, and wound hematoma. A biliary fistula was defined by bilious drainage from intraoperatively placed drains or bile collection requiring drainage. Medical complications included pulmonary conditions related to the surgery, ascitis, jaundice, urinary infections, etc.
Statistical analysis
Data analyses were performed using SPSS® software (SPSS, Chicago, IL), using a two-tailed chi-square test, Fisher's exact test, and a Student's t test. Values of P<.05 were considered significant.
Results
From February 1997 through March 2007, 100 liver resections were performed by laparoscopy. Overall, they represented 10.9% of the hepatic resective procedures performed at our Unit during that period. The resections included 47 women and 53 men, with a mean age of 42.5±13.5 years (range, 19–79 years). Sixty-seven patients were graded as being ASA Class I, 32 as ASA II, and 1 as ASA III. Mean BMI was 24.1±4.3 kg/m2 (range, 15.4–39.8 kg/m2). Forty-eight patients had undergone abdominal surgery previously, including 31 appendectomies, 9 cesarean (Pfannenstiel's) sections, 6 cholecystectomies, and 4 colorectal resections (2 patients had more than one procedure).
Indication for surgery/types of procedures
The indications of hepatectomy were malignant tumors in 34 patients, benign lesions in 27 patients, and pediatric living donor liver transplantations in 39 patients. Malignant tumors were mainly HCC (Table 1).
Among the 27 HCC patients undergoing laparoscopic liver resection, 23 had cirrhosis (22 Child–Pugh A and 1 Child–Pugh B), 1 had hepatitis C virus infection without cirrhosis, 1 had steatosis, and 2 had normal livers. Etiologies of cirrhosis were alcohol in 12 patients, hepatitis C virus in 8 patients, and virus B hepatitis in 3 patients. Eighteen patients had single nodules, 6 had two nodules, and 1 had three nodules, with a median diameter of 4.5 cm (range, 1–10 cm). One of the patients had undergone preoperative radiofrequency ablation.
The types of liver resection are detailed in Table 2. Seventy-three resections involved two or more segments. Excluding cholecystectomy during a major resection, 14 associated surgical procedures were performed during the same operation: 2 colorectal resections, 7 cholecystectomies, 3 radiofrequency ablations, 1 atypical gastrectomy, and 1 hepatic pedicle lymphadenectomy.
Outcome
The mean operative time was 253±91.6 minutes (range, 60–540 minutes). The mean operative blood loss was 120±127.6 mL (range, 10–1,000 mL). Overall, 1 patient (1%) received blood transfusion (after a converted procedure).
There was no mortality. Twenty-one patients (21%) experienced 26 postoperative complications (Table 3). Two patients required reoperation for biliary leak, in both cases by laparoscopy (drainage of biliary collection and treatment of the biliary fistula). One patient presenting a biliary collection was treated by percutaneous drainage. The last patient with biliary leak was managed conservatively, and the biliary fistula spontaneously closed 19 days postoperatively. One cirrhotic patient (Child A) who underwent bisegmentectomy for HCC had transient hepatic failure and prolonged intensive care hospitalization. Among the 20 cirrhotic patients, 6 developed ascites, and 3 had jaundice. There was no postoperative bleeding. The mean hospital stay was 8.9±9 days (range, 3–55 days). For liver donor left lateral lobectomy, the mean hospital stay was 6.1±2.3 (range, 3–14 days).
Conversion
The procedure was completed laparoscopically in 83 patients (83%). Reasons for conversion to laparotomy of the remaining 17 (17%) patients were as follows: slow progression of liver transection associated with diffused parenchymal bleeding in 6 patients (living donor in 4), difficult exposure/uncertain localization of tumor margins in 6 patients (HCC in cirrhotic liver in 5 cases and voluminous left lobe angioma in 1), location of the tumor in 2 (VII segment in one case, at the hepatic hilum in the other), size of the tumor in 2, tight adhesions in 1, and intraoperative ultrasound diagnosis of a second tumor (undetected preoperatively) in 1 case (the patient underwent a bisegmentectomy [IV and V] by laparotomy). The indications for liver resections in converted cases were HCC (n=10), liver donor transplantation (n=4), colorectal metastases (n=1), hemangioma (n=1), and biliary cystoadenoma (n=1). Among the converted cases, 9 patients (53%) were cirrhotic, and 3 (18%) had portal hypertension with esophageal varices. In none of these cases was the decision to proceed to conversion taken in an emergency situation or because of life-threatening bleeding.
The results for the 17 converted cases were compared with those for 83 without conversion (Table 4). The factors related significantly with conversion were ASA classification, cirrhosis, BMI, intraoperative blood loss, necessity for a Pringle maneuver, morbidity, hospital stay, and intensive care hospitalization (Table 4).
Data are mean±SD values or number (%) as indicated.
ASA, American Society of Anesthesiologists; BMI, body mass index.
Discussion
Our study confirms that LLR surgery is feasible and safe. Moreover, it shows that a policy of not delaying conversion in the case of difficult procedures, together with a meticulous, blood-sparing technique of liver transection, may allow for minimal blood loss without prolonging the operative time.
In recent years, the results of open liver surgery have improved. The mortality rate of patients undergoing hepatic resective surgery with no underlying liver disease is approaching 1% in specialized centers, and the morbidity rate as well as the rate of patients needing transfusion is falling below 30%.19–21 Modern hepatic surgery is based on the respect of old principles and the introduction of new technical/technological advances. The systematic encircling of the hepatic pedicle and the preference for anatomical resections, 22 associated with the meticulous parenchymal transection allowed nowadays by new surgical tools, such as the ultrasonic dissector6,23 and intraoperative ultrasound, may be credited for such a reduction of intraoperative bleeding and perioperative complications.19–22
After Azagra et al. 4 first showed that liver resection may be achieved laparoscopically, several studies showed that patients undergoing liver surgery may benefit from the typical advantages of a laparoscopic approach: less postoperative pain,24,25 shorter hospital stay,11,12,24,26–28 and fewer postoperative peritoneal adhesions. 29
Patients affected by hepatic diseases may be assumed to benefit from additional advantages of a mini-invasive approach. In cirrhotic patients, limited incisions and less mobilization/manipulation of the liver reduce surgical trauma, thus allowing for the preservation of abdominal collateral venous circulation, which may be related with less postoperative ascites.30,31 The non-exposure of abdominal viscera reduces fluid requirements and decreases electrolytic and protein losses. Moreover, decreasing intraoperative bleeding, as is reported during laparoscopy relative to open procedures,11–14 may be assumed to reduce the mortality of surgery because this latter is related to blood loss.30–33 Finally, fewer pulmonary complications have been described after laparoscopy, 29 as lesser postoperative pain and prompter patients' mobilization may be assumed to allow improving diaphragm kinetics in the immediate postoperative period, thus preventing pulmonary complications.
Despite the recent improvement in results of liver surgery, nevertheless, bleeding still represents a major concern to hepatic surgeons, regardless of the approach adopted. Other than potentially life-threatening complications, excessive blood loss has been reported to be associated with worse results of surgery, in terms of both immediate outcome and long-term survival.11–14 Moreover, in the case of a laparoscopic approach, a massive liver hemorrhage may have severe15,34 or fatal 35 consequences and may oblige surgeons to finally convert the procedure, thus losing the potential advantages of a mini-invasive approach. In the case of LLR surgery, as for other procedures, it is often difficult to set the right time for conversion in the case of hard-to-perform procedures. Theoretically, delaying a conversion may be assumed to prolong the operative time and to increase blood loss. In contrast, a prompt conversion may allow reducing the procedure's risks, operative time, and blood loss to a minimum, as an open approach may probably allow for a faster and more effective management of difficult procedures and complications. Because at our institution we always had a blood-saving, low-risk attitude in liver surgery, we thought to verify the results of such a policy in the laparoscopic era.
From 1997, we started to perform increasingly difficult liver procedures laparoscopically by applying the same principles learned in many years of open liver surgery and by taking advantage of the most recently introduced tools. From a technical point of view, the use of an ultrasound dissector clearly allowed for the careful isolation of small vessels and bile ducts one by one and for a clear skeletonization of the portal structures and hepatic veins, thus increasing the safety of liver transection and reducing the risk of major hemorrhages.6,23 Similar to our practice in open liver surgery, hemostasis and biliostasis were achieved by the meticulous use of bipolar coagulation, in the case of diffuse parenchyma bleeding, or bolt clips, whenever small vessels/biliary ducts were identifiable. We never used “en masse” or blind stapling of liver parenchyma. Like in open procedures, intermittent clamping of the hepatic pedicle was also used during laparoscopy, whenever needed. Laparoscopic ultrasound was routinely used for both neoplastic and benign lesions, in order to perform a complete staging and to define adequate resection margins as well as to identify anatomical repairs and location of vessels.
The results of LLR for hepatic diseases were so encouraging, in terms of improved postoperative outcome, feasibility, and safety, that from the very beginning we decided to adopt such an approach to liver resections for living donors because we thought that a minimally invasive procedure may reduce the aggressiveness of a major hepatectomy in “healthy patients” (liver donors). This procedure constitutes roughly 40% of the present series.
In our series of selected patients, we had no mortality and a 21% morbidity rate. These latter data are consistent with the 15%–41% morbidity rate reported in the literature.15,34,35–37 Overall morbidity was mostly due to minor complications, such as transient ascitis or pneumonia. All the patients, including the 4 developing a biliary leak, completely recovered with no permanent sequelae.
Blood loss in our series (120 mL) was lower than traditionally reported during open liver resective surgery. These data are in accordance with recent articles, where a lesser degree of hemorrhaging is reported during LLR surgery.11–14 Several reasons may explain such a feature. As we 38 and others 39 have shown that relative hypovolemia may allow limiting hemorrhage (by reducing blood backflow) and avoiding clamping in open hepatectomies, we believe that, additionally, the supine, 30° anti-Trendelenburg position during laparoscopic hepatic procedures may contribute to decrease retrohepatic vena cava pressure, thus reducing liver venous backflow. Moreover, a more effective hemostasis, as is allowed by the laparoscope-enhanced vision, and the effect of the pneumoperitoneum pressure (“cut surface”) may also be credited for lower blood losses during LLR. 15 In our experience, the “cut surface” effect of the pneumoperitoneum seems to be particularly useful in reducing diffused parenchymal bleeding and may also be improved, as we are used to doing in difficult-to-manage situations, by increasing the pneumoperitoneum pressure from 12 to 16 mm Hg.
Indeed, blood loss in our series (120 mL) was also lower than that reported by the vast majority of authors during laparoscopic liver procedures, accounting for a mean (or median) of 200–625 mL,11,15,24,27,34,36,37 but also exceeding 2000 mL in sporadic cases.13,15 This comparison may be biased by several factors, including a different percentage of major (or right-sided) hepatectomies, which may be assumed to imply more blood loss than minor (or left-sided) procedures, or a different percentage of cirrhotic patients in the cited series. Nevertheless, in our opinion, it is worth noting that in our series, which includes a relevant number of major hepatectomies, only 1 patient out of 100 (1%) needed blood transfusions, and no postoperative bleeding occurred. Also, this value is lower than that reported in the majority of published articles, where a 5.6%–32% transfusion rate is observed.11,15,25,35,37,40 Possibly, our blood-saving attitude, including a systematic and meticulous use of bipolar coagulation and an ultrasound dissector, the intermittent clamping of the hepatic pedicle when needed, and the tendency not to postpone conversion in the case of difficulty, may be credited for such low blood loss. It is interesting that the few other articles reporting a low intraoperative blood loss (64–150 mL13,14,41) and a low transfusion rate (4%) 41 describe a meticulous technique of parenchymal transection very similar to ours, implying the use of bipolar coagulation, Harmonic® (Ethicon) scalpel, and ultrasound dissector13,41 or radiofrequency sealer. 14
Our conversion rate was 17%, which is slightly higher than the 6.6%–12.4% reported in the literature.7,15,25,34,35,40 In our opinion, these data reflect our attitude not to indefinitely postpone conversion to open surgery in the case of difficult or long-lasting procedures. Such a tendency of not delaying conversion is confirmed by the absence of a significant difference in the operative time needed to accomplish converted and non-converted procedures (Table 4).
Although blood loss observed during converted procedures is low (mean, 306 mL), nevertheless, we found a significant relationship between bleeding and conversion, as converted procedures implied a more significant blood loss (306 versus 82 mL, P=.001). These data may concomitantly explain also the more frequent necessity of performing the Pringle maneuver because difficult liver resections are more likely to imply significant blood loss (regardless of the cause of difficulty experienced by the surgeon), to need to control the bleeding, and finally to require conversion. It is interesting that no patient was converted for massive bleeding due to a major vessel's injury, and only roughly one-third of the patients (6 of 17) were converted because of slow progression associated with diffused parenchymal bleeding. Moreover, it should be considered that, in four of the six cases, conversion occurred during a living donor's left lobectomy, which we consider a conversion-prone procedure. Owing to obvious reasons, in fact, the necessity to accomplish an effective, short-lasting procedure, to preserve both remnant liver and specimen in excellent conditions, to achieve a perfect hemostasis at both sides of liver transection, and to avoid any procedure-related complication to the donor (such as perioperative transfusion) may be supposed to play a role in deciding to convert laparoscopy. These considerations may gain importance if we consider that bleeding, in contrast, is the main cause of conversion in other studies.6,7,10,15–17
Moreover, if we compare the mean blood loss in the 17 converted procedures of our series (306 mL) with the finding (625 mL) of the only other study reporting such data, 34 it may be deduced that a different attitude to conversion with respect to intraoperative bleeding actually exists. Consistent with such a different approach, those authors reported a lower conversion rate (9.6% versus 17%), a higher transfusion rate (5.6% versus 1%), and a significant difference in accomplishing non-converted and converted procedures, these latter lasting 1 hour longer (240 versus 180 minutes). 34 It seems that our prompt-conversion attitude may allow avoiding the sequence that a difficult procedure or a non-bleeding complication finally becomes a bleeding complication, implying a significant blood loss (and possibly transfusion), finally often requiring conversion and longer operative time. In accordance with such a policy, in our daily practice, we consider now a blood loss of 200 mL as a “threshold of conversion.”
Considering the other variables related to conversion in our series, cirrhosis and BMI are well-recognized factors increasing the difficulty of surgery. The alterations associated with cirrhosis (portal hypertension, coagulation deficit, abnormal liver anatomy, etc.) together with intrinsic limitations of laparoscopy (impossibility of palpating masses, difficulty in dealing with sudden bleeding, etc.) may explain why cirrhotic patients have an increased conversion rate. BMI, in our opinion, may also be considered a factor increasing the difficulty of surgery in general and laparoscopy in particular because a fatty, deep abdomen and a thick abdominal wall may be supposed to be related to more difficult exposure of the liver transection line and accomplishment of hepatectomy during laparoscopy.
Although the minimal blood loss and operative time of our prompt-conversion policy encourage us in persevering in such an attitude, nevertheless, it should be remarked that those advantages should be balanced with the drawbacks of converted procedures. According to our findings, patients undergoing conversion have more complications, require more frequently a hospitalization in the intensive care unit, and need a significantly longer postoperative hospital stay (roughly 1 week longer [15 days versus 8 days]) than those undergoing a laparoscopically accomplished procedure. These data were noted and are now considered in the perioperative management of patients undergoing laparoscopic liver surgery.
In conclusion, this study confirms that liver resection by laparoscopy, if performed with the same technical principles as open liver surgeries, is feasible and safe. The presence of cirrhosis and a high BMI are related to an increased risk of conversion, which is associated to higher morbidity, longer hospital stay, and more frequent need for intensive care hospitalization. Our approach to laparoscopic liver surgery, implying a meticulous dissection of hepatic parenchyma by means of old and newly introduced tools (bipolar coagulation, Harmonic scalpel, ultrasound dissector), other than our attitude not to delay conversion in difficult cases, may allow for a significant reduction of blood loss without prolongation of operative time, with a possible, slight increase of the conversion rate.
Footnotes
Disclosure Statement
No competing financial interests exist.
