J Hepatobiliary Pancreat Surg (2005) 12:38–43 DOI 10.1007/s00534-004-0949-9
How I do it: assessment of hepatic functional reserve for indication of hepatic resection Sung-Gyu Lee and Shin Hwang Division of Hepatobiliary Surgery and Liver Transplantation, Department of Surgery, Asan Medical Center, University of Ulsan College of Medicine, 388-1 Poongnap-dong, Songpa-gu, Seoul 138-736, Korea
Abstract Liver resection of up to 75% of the total liver volume (TLV) has been regarded as safe in normal livers, but this concept was challenged by the results of living donor hepatectomies. In normal livers or livers with resolved jaundice, hepatectomy of 65% of TLV may be safe, except for patients with an indocyanine green retention rate at 15 min (ICG R15) of over 15%, excessive hepatic steatosis, and age of over 70 years. However, the permissible extent of hepatectomy has been much restricted in cirrhotic livers because most post-hepatectomy liver failure (PHLF) has occurred in cirrhotic livers. Our routine protocols for the assessment of functional hepatic reserve (FHR) include biochemical liver function tests, ICG R15, Doppler ultrasonography, and triphasic liver computed tomogram (CT) with volumetry. Blood cell count and gastroesophageal endoscopic findings are taken into consideration for cirrhotic livers, as well as age, diabetes, cardiopulmonary function, and general performance. Preoperative portal vein embolization has been used for safe hepatectomy even in cirrhotic livers. We think that any cirrhotic liver showing optimal FHR should have a remnant liver of 40% of TLV to prevent PHLF. ICG R15 and triphasic CT with volumetry have been the most useful methods for assessment of FHR and determination of hepatecomy extent in our institution. Key words Liver resection · Liver cirrhsosis · Hepatic failure · Portal vein embolization
Introduction The liver has unique regenerative capability for coping with partial resection. Hepatectomy of up to 75% of the total liver volume (TLV) has been regarded as safe if the liver is normal. This concept of the permissible extent of liver resection has been challenged since the introduction of living-donor liver transplantation (LDLT) using a right lobe (RL) graft. Most LDLT cenOffprint request to: S.-G. Lee Received: April 1, 2004 / Accepted: September 1, 2004
ters have set the upper limit of safe donor hepatectomy as 65% or 70% of TLV. Unfortunately, a few living donors themselves had to undergo liver transplantation, or died due to post-hepatectomy liver failure (PHLF).1–4 On the other hand, a considerable proportion of recipients whose partial liver graft was equivalent to near 30% of the standard liver volume (SLV) have survived uneventfully.5 These latest experiences with LDLT may have influenced the conventional concepts of preoperative risk evaluation for non-transplant liver resection. There are many kinds of hepatobiliary diseases requiring liver resection and the background status of the liver parenchyma in hepatobiliary disease can be roughly classified as normal, icteric, or cirrhotic. As these different natures of the liver parenchyma may have different degrees of regenerating power or functional reserve, we have to manage them in different fashions. Recent advances in radiological imaging have enabled us to accurately assess the parenchymal hepatic resection rate (PHRR), as well as to predict the extent of outflow disturbance before certain types of hepatectomy.6,7 Furthermore, preoperative portal vein embolization (PPVE) is now more commonly used than before, by which interlobar shifting of some liver volume and a tolerance to the elevated portal pressure can be expected.8–10 We herein describe our evaluation and management processes that have been applied before, during, and after liver resections for various hepatobiliary diseases.
Methods Experience of overall hepatectomies at the Asan Medical Center and outcomes focused on post-hepatectomy liver failure We have performed more than 3000 liver resections since 1989 for the treatment of hepatocellular carci-
S.-G. Lee and S. Hwang: Assessment of functional hepatic reserve
noma (HCC; n ⫽ 1670), hepatolithiasis (n ⫽ 650), gallbladder cancers (n ⫽ 150), hilar bile duct cancer (n ⫽ 210), peripheral cholangiocarcinoma (n ⫽ 60), metastatic liver cancer (n ⫽ 100), and other miscellaneous diseases (n ⫽ 200).11 We have also performed almost 900 living-donor hepatectomies to date.12 Apart from patients with complicating episodes of postoperative bleeding leading to multiorgan failure, 15 patients have died directly of PHLF in our institution. Nearly all of these deceased patients had cirrhotic livers.10,11 We have not experienced purely PHLF-induced mortality in 1000 consecutive hepatectomies for various hepatobiliary diseases performed during the past 3 years, and there has been no mortality of living donors. We think that our recent results justify the processes we use to assess the functional hepatic reserve (FHR) and to determine the extent of liver resection. Preoperative assessment of functional hepatic reserve and intra- and post-operative management Our routine protocols to assess FHR for non-transplant liver resection include serum biochemical liver function tests, indocyanine green retention rate at 15 min (ICG R15), Doppler untrasonography (DUS), and triphasic liver computed tomogram (CT). DUS and CT give information on the status of the liver parenchyma and the size of the spleen. Risk factors such as degree of hepatic steatosis (more than mild degree), age (more than 70 years), diabetes, cardiopulmonary diseases, and general performance are additionally taken into consideration for determination of hepatectomy extent and operation design. The permissible limit of liver resection in our institution is 65% of TLV for patients with normal livers and absence of significant risk factors.12 The PHRR has been applied for livers with an intrahepatic mass and can be calculated as follows: PHRR (%) ⫽ (resected liver volume — tumor volume)/(TLV — tumor volume)) ⫻ 100. The SLV has also been used for large hepatic tumors, instead of the TLV, because tumor volume is often included in the TLV; SLV is calculated according to our own formula as follows: SLV (ml) ⫽ 691 ⫻ body surface area (m2) ⫹ 95.12 In patients with PPVE, we usually wait for more than 2 weeks for compensatory hypertrophy of the remaining liver lobe or segment, and then a routine FHR assessment is repeated. We think that CT volumetry should be carried out by experienced hepatobiliary surgeons or radiologists to achieve acceptable reliability, because deviation of the transection plane by 1 cm can induce a volume difference of more than 5% of TLV. Recently, in our institution, specialized software (VoxelPlus; Mevisys, Daejeon, Korea), enabling real-time three-dimensional reconstruction, has served as an effective tool to delineate the extent of liver resection, as well as to evaluate
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the complex intrahepatic venous anatomy. On the day before operation, or on the morning of the operation day, we have occasionally initiated the infusion of gabexate mesilate solution to induce a cytoprotective effect against ischemia-reperfusion injury.13 During hepatectomy, the quality and size of the liver are evaluated to match with the preoperatively determined extent of hepatectomy. We have also adopted intraportal infusion of glucose-insulin-potassium solution for highrisk or diabetic patients, in whom a thin catheter was inserted into the side branch of the inferior mesenteric vein.14 Confirmation of total absence of bleeding at the operation site is one of the most important procedures to reduce operative risk, so we often use a method of spraying 2–4 ml of fibrin glue solution thinly over the liver cut surface, inferior vena cava, and right adrenal gland, by which even minor pin-point venous bleeding can be identified definitely. Another reliable method to detect insidious bleeding points is to just wait for over 10 min after gauze packing at the dissection surface. After hepatectomy, in our institution, nearly all patients are moved to the surgical intensive care unit. We have usually used intravenous hyperalimentation (IVH) during the postoperative fasting period, and it is tapered on the initiation of oral food intake. The arterial ketone body ratio (AKBR) is monitored daily and used for adjustment of the glucose concentration in the IVH solution. We usually carry out triphasic CT weekly after hepatectomy, to detect concealed or latent lesions, as well as analysis of regeneration. Abnormal fluid collection is often evacuated, with radiological guidance, so as not to serve as an infection focus. Assessment of functional hepatic reserve for patients with normal livers In the normal liver, as in patients with metastatic colon cancer, nearly all items of the routine FHR assessment may show normal values. Normal liver usually reveals an ICG R15 of less than 10%: On occasion, we found that the value exceeded 15%, but this was often proven to be a sampling error on repeated examination. We do not think that all untimely sampling would be screened during the process of calculation of the ICG R15. When there are no significant risk factors, the maximal extent of safe liver resection is set as leaving a remnant liver volume (RLV) that is equivalent to at least 35% of the TLV or SLV. If the tumor size is small, the PHRR can reach 65%. However, the PHRR is not accurate for huge infiltrating tumors, because a considerable portion of the liver parenchyma has already been infiltrated and there remains only a small volume of functional parenchyma. Instead, the concept of SLV can be used, as it is in LDLT. If RLV is calculated as less than 35% of TLV, or if there are some risk factors, we usually perform
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S.-G. Lee and S. Hwang: Assessment of functional hepatic reserve
PPVE. For right or left trisegmentectomy, all of the inflow portal branches of the resected segments should be occluded.15 In PPVE of the right portal vein, we simply predict that 10% of TLV will be shifted from the right lobe to the left lobe. Briefly speaking, we think that nearly all hepatectomies leaving an RLV equivalent to 35% of TLV or SLV will be permissible if the liver parenchyma is normal and not more steatotic than mild grade and the patient’s age is not greater than 70 years. Hepatic steatosis may make the liver parenchyma vulnerable to ischemic injury.16–18 Age of over 70 years itself may not serve as a significant risk factor for liver regeneration, but, at this age, there is a definite increase in patient morbidity, such as incidental cardiovascular or cerebrovascular accidents.19,20 The outcome of this assessment policy has been proven in our recent review of 400 consecutive cases of living-donor hepatectomies (January 2002– March 2004), in which the extent of liver resection near or over 65% of TLV was the only significant risk factor. We emphasize that any bleeding episode after major hepatectomy can worsen the post-hepatectomy consequences, by which a catastrophic outcome cannot be completely preventable even if all of the FHR items are optimal.20 Assessment of functional hepatic reserve for patients with icteric livers In cholestatic livers, the preoperative decompression of obstructive jaundice is the first procedure for surgical treatment. If the jaundice cannot be controlled by endoscopic nasobiliary drainage (ENBD), percutaneous transhepatic biliary drainage (PTBD) should be done immediately. Our policy for biliary decompression is not to leave major missing ducts. In a review of 50 consecutive patients with hilar bile duct cancer in our institution, there were 25 single PTBDs, 23 double PTBDs, and only 2 ENBDs. As the ICG R15 is directly influenced by the degree of jaundice, due to excretory competition with bilirubin, its result is not reliable until the total bilirubin level falls below 2–5 mg/dl (Fig. 1). In this group of 50 patients, the mean level of serum total bilirubin on admission was 10.4 mg/dl, and it decreased to 1.7 mg/dl after 37 days, just before operation. Our guidelines for the timing of PPVE and liver resection during biliary decompression are serum total bilirubin levels of 5 mg/dl and 2 mg/dl, respectively. We compared the regeneration rates of the remnant livers after right lobectomy in 30 patients with normal livers and resolved icteric livers, and there was no significant difference in the remnant liver regeneration during the first 7 days. Therefore, completely decompressed liver may have the same, or at least not significantly different, FHR compared with the normal liver. We also think
Fig. 1. The interrelationship between serum total bilirubin and indocyanine green retention rate at 15 min (ICG R15). Open circles, gray circles, and black ovals indicate the results of ICG R15 on admission, at mid-term, and before operation, respectively, in 30 patients with hilar bile duct cancer. There was a close correlation between serum total bilirubin and ICG R15
that the same extent of volume shifting can be expected in resolved icteric livers and normal livers after PPVE. When patients persistently showed serum total bilirubin levels of more than 5 mg/dl despite prolonged biliary decompression, we found that there was a high possibility of far-advanced tumor not permitting resection, due to peritoneal seeding or distant metastasis. Prolonged obstructive jaundice and repeated cholangitis may induce diffuse shrinkage of the hepatic parenchyma, which is accompanied by prominent ductal dilatation. In such patients, we have occasionally found a significant rise of ICG R15. In patients with hilar bile-duct cancer and advanced gallbladder cancer, the caudate lobe has been routinely resected and the parenchymal transection plane was often found to have encroached on the plane of the MHV. These surgical features can result in a small RLV or increased PHRR, because of which patients with such cancers have been more often indicated for PPVE than those with normal livers. Once the serum total bilirubin level drops below 2 mg/dl, we think that there is no need to classify the liver as icteric or cholestatic, because nearly all of the liver functions may be restored already. Therefore, the same extent of liver resection will be permissible for resolved icteric livers as for normal livers. However, special attention should be paid to livers in patients with an ICG R15 higher than 15%. We found that such livers often showed diffuse parenchymal shrinkage and occurred in old age, without evidence of liver cirrhosis. If the ICG R15 was in the range of 15%–20%, we often restricted PHRR to less than 50% of TLV, in which the resection of one or two sectors (left lobectomy, central bisegmentectomy, anterior segmentectomy, or medial
S.-G. Lee and S. Hwang: Assessment of functional hepatic reserve
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Table 1. Summary of a case-controlled study to evaluate the effects of preoperative portal vein embolization (PPVE) in 63 patients with hepatocellular carcinoma from January 1994 to November 199610 PPVE (⫹)
PPVE (⫺)
Group
Cirrhotic
Noncirrhotic
Cirrhotic
Noncirrhotic
No. of cases HBsAg(⫹) ICG R15 (%) Size of tumor (cm) Pre-PPVE volume (ml) Right lobea Left lobe⫹S1 Post-PPVE volume (ml) Right lobea Left lobe⫹S1 In-hospital mortality Hepatic decompensation at 3 months
19 19 7.5 ⫾ 2.9 4.8 ⫾ 3.2
11 10 8.8 ⫾ 7.6 5.8 ⫾ 3.3
22 21 8.6 ⫾ 4.9 6.7 ⫾ 3.0
11 9 7.5 ⫾ 4.9 8.2 ⫾ 3.8
762 ⫾ 316 434 ⫾ 63
680 ⫾ 160 435 ⫾ 99
768 ⫾ 148 454 ⫾ 95
947 ⫾ 341 484 ⫾ 95
651 ⫾ 273 462 ⫾ 94 0 2 (10.5%)
627 ⫾ 131 515 ⫾ 107 0 1 (9.1%)
5 (22.7%) 4 (18.2%)
0 1 (9.1%)
S1, caudate lobe a Without tumor volume
segmentectomy) was preferred. For patients with ICG R15 exceeding 20%, more restricted parenchymapreserving operations, such as central partial hepatectomy or isolated caudate lobectomy should be considered.21–23 If the liver appears diffusely atrophied or there are huge space-occupying lesions, it is better to use the concept of SLV rather than TLV for calculation of the liver resection rate. When doing hepatopancreatoduodenectomy (HPD), the risk of PHLF is increased.24 Although our series revealed that liver generation after right lobectomy was not altered by combined pancreatoduodenectomy (pancreatic resection rate up to 40%), when doing HPD, we set the minimal RLV as definitely more than 35% of TLV to prevent PHLF.25 Assessment of functional hepatic reserve for patients with cirrhotic livers The assessment of FHR has been mainly focused on parenchymal liver diseases such as viral hepatitis B or C. Livers in patients with these diseases can be in a precirrhotic or an overtly cirrhotic state. Child-Pugh (CP) or Child-Turcotte-Pugh (CTP) scores are initially used to delineate FHR. Profiles of complete blood count and gastroesophageal endoscopic findings of varices should be considered. In livers with a precirrhotic background, such as chronic persistent hepatitis B, the CTP score and ICG R15 usually do not become abnormally high. These parameters often remain normal even in the livers of Child A class patients. However, the post-hepatectomy consequences in patients with livers of different parenchymal backgrounds are not the same at all, because many of the currently available items for FHR assessment cannot discern between narrow degrees of cirrhotic changes.
In reality, the risk of PHLF is highly associated with the degree of cirrhosis and the liver resection rate. In other words, assessment of FHR in cirrhotic livers is made regarding the level of liver parenchymal function and how much the partially functioning parenchyma should remain. In Korea, the main indication for the resection of cirrhotic livers is hepatocellular carcinoma (HCC). Professor Makuuchi proposed modifying the surgical approach in patients with HCC and liver cirrhosis, and we also observe his guidelines.26 We summarized the outcomes of a classical case-controlled study to evaluate the risk of PHLF following right lobectomy in 63 consecutive HCC patients (Table 1).10 In the cirrhotic non-PPVE patient group, 13.6% of patients died of PHLF, with a PHRR of 62.8%, and an additional 9.1% died due to multiorgan failure triggered by postoperative bleeding. However, in the other three groups (noncirrhotic livers with and without PPVE and cirrhotic livers with PPVE), there was no in-hospital mortality, with PHRR values of 54.9%–66.2%. These data suggested that resection of cirrhotic livers equivalent to a PHRR over 60% is no longer safe, even when the current assessment of FHR, using the ICG R15 and some other parameters, seems to be adequate.27 Subsequently, in livers with cirrhotic features, we had to adjust the permissible extent of hepatectomy to a PHRR of less than 60%, by which the incidence of pure PHLF has been significantly lowered to nearly zero. PPVE often reduces PHRR to less than 60% in livers with small HCC. When a cirrhotic liver shows ICG R15 values between 15% and 20%, we try to make PHRR not exceed 50% and to make PLV definitely over 40% of the SLV or over 50% of the TLV. This guideline has often been applied to patients with right lobectomy with
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S.-G. Lee and S. Hwang: Assessment of functional hepatic reserve
a 5-cm-sized HCC lesion and a small volume of functional liver parenchyma. This range of ICG R15 may be the upper limit of PPVE for right lobectomy in cirrhotic livers.28 If the ICG R15 exceeds 20%, liver resection should be considered prudently, on a case-by-case basis, and the permissible extent of liver resection should be reduced to segmentectomy or nonanatomical hepatectomy.26 If the ICG R15 is over 30%, we think that it is better not to attempt any type of surgical resection, because radiofrequency (RF) ablation is much less invasive. In comparisons of cirrhotic and normal livers, the effects of PPVE of the right portal vein were different, as follows. Atrophy of the right lobe side was usually less prominent in cirrhotic livers, and the amount of volume shifting was reduced to 5% of the TLV or less. The change in portal pressure between before and after PPVE was more prominent in cirrhotic livers, and this served as a buffer before the further elevation of portal vein pressure after right lobectomy.9,10 We have experienced two patients with cirrhotic livers who revealed marked deterioration of liver function after PPVE of the right portal vein. We waited for 1 month until recovery of liver function and then carried out right lobectomy, but both patients had to stay in the intensive care unit for 3 weeks due to unstable liver function. They also revealed overt features of hepatic decompensation for more than 6 months. We do not regard patients who have barely tolerated the insult of PPVE as indication for major liver resection any longer. Interestingly, we have reported the control of intractable posthepatectomy ascites, using a transjugular intrahepatic portosystemic shunt.29 As cirrhotic livers are known to be vulnerable to ischemic injury, parenchymal transection without intermittent inflow interruption seems to be beneficial. As the inflow of the liver on the resection side can be totally clamped, unlike in living-donor hepatectomy, the parenchymal transection can be done easily, without the use of Cavitron ultrasonic surgical aspirator. However, in a case-controlled series of this method (selective inflow occlusion) applied to 100 hepatectomies of cirrhotic and noncirrhotic livers, we did not find any significant differences in intraoperative blood loss and postoperative peak levels of liver enzymes between the group with Pringle’s maneuver and the group with continuous perfusion. A similar outcome in living-donor hepatectomy was also reported with this method.30
Conclusion In normal livers or livers with resolved obstructive jaundice, hepatectomy leaving an RLV equivalent to 35% of the TLV or SLV may be quite safe, except for patients
with an ICG R15 of greater than 15%, excessive hepatic steatosis, and age of over 70 years. However, the permissible extent of hepatectomy is often restricted in cirrhotic livers. We think that any cirrhotic liver showing optimal FHR should have an RLV equivalent to 40% of the TLV or SLV for secure prevention of PHLF. We have found that ICG R15 and triphasic liver CT with volumetry have been the most useful methods for the assessment of FHR and determination of hepatectomy extent.
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