Preoperative Risk Assessment of Hepatic Resection for Malignant ...

World J. Surg. 21, 396 – 401, 1997

WORLD Journal of

SURGERY © 1997 by the Socie´te´ Internationale de Chirurgie

Preoperative Risk Assessment of Hepatic Resection for Malignant Disease T.U. Cohnert, M.D.,1 H.G. Rau, M.D.,1 E. Buttler, M.D.,1 T. Hernandez-Richter, M.D.,1 G. Sauter, M.D.,2 C. Reuter, M.D.,1 F.W. Schildberg, M.D.1 1

Department of Surgery, Klinikum Grosshadern, Ludwig Maximilians University, Marchioninistrasse 15, D 81377 Munich, Germany Department of Medicine II, Klinikum Grosshadern, Ludwig Maximilians University, Marchioninistrasse 15, D 81377 Munich, Germany

2

Abstract. Clinical, laboratory, functional, and volumetric data of 340 consecutive patients undergoing hepatic resection for malignant disease between November 1990 and June 1995 were analyzed. The operative mortality was 3.3% (8/244 patients). Among 178 patients with liver metastases and 66 with primary hepatobiliary tumors the hospital mortality was 4.1% (10/244 patients) and morbidity 22.0% (54/244 patients). Survival after hepatectomy was strongly influenced by the extent of resection quantified by the parenchymal hepatic resection rate. The prediction of fatal postoperative complications can be improved for patients with hepatic metastases by calculating the liver resection index (sensitivity 75%, specificity 83%).

Liver resection has become an important therapy with curative intention for primary neoplasms of the liver and hepatic metastases. To improve patient survival and decrease the risk of fatal postoperative liver failure a preoperative risk assessment can improve patient selection for primary resection or interventional pretreatment as chemoembolization. The aim of the study was to quantify the postoperative risk of death after partial hepatectomy for a single patient by using only preoperatively available data to minimize the risk of the operation and to select patients for pretreatment by chemotherapy or chemoembolization prior to resection.

Hepatic resections were performed by six experienced surgeons trained at our institution by the same surgical principles. Three standard methods of dissection— blunt dissection, ultrasonic aspirator (CUSA), and jet cutter—were used. Liver hilus clamping was applied individually depending on the intraoperative surgical situation. Neither total vascular exclusion of the liver nor hypothermia or cold infusion of the liver was instituted. Drainage of the abdominal cavity was performed in all patients. Hepatic function tests (transaminases, prothrombin time, activated partial thromboplastin time, pseudocholinesterase, alkaline phosphatase, serum bilirubin) were routinely monitored postoperatively. Results were expressed as mean values (6 SD). Univariate analysis of single clinical and laboratory values was performed using the Mann-Whitney U-test. Differences between patient groups were analyzed by the Kruskal-Wallis test for independent samples as appropriate. A p value below 0.01 was considered significant. To determine safe limits for the extent of a planned hepatic resection, a multivariate analysis using BMDP software as a stepwise logistic regression was performed to identify factors significant for survival after hepatectomy. Combining patient- and organ-specific data, the liver resection index (LRI) was developed and its prognostic value in a prospective study investigated [3]. The LRI was defined as follows.

Methods Between November 1990 and June 1995 a total of 340 consecutive patients underwent hepatic resection for malignant hepatic lesions in our institution. Data collection was retrospective through March 1994 (n 5 179 patients) and prospective since April 1994 (n 5 65). Clinical and laboratory data were analyzed pre-, intra-, and postoperatively. In addition, a preoperative 14C-aminopyrine breath test (ABT) to assess liver function was performed [1]. Using a preoperative computed tomography (CT) scan of the abdomen, the parenchymal hepatic resection rate (PHRR) was calculated according to Okamoto’s formula [2] as

resected volume 2 tumor volume liver volume 2 tumor volume Correspondence to: T.U. Cohnert

LRI 5

ABT ~%! 3 100 PHRR 3 age ~years! 3 ~tumor volume/liver volume!

Included in the LRI were the preoperative ABT value as a quantification of the hepatic functional capacity, the patient’s age, and two volumetric parameters. 1. The amount of remaining liver parenchyma was estimated by the PHRR according to Okamoto et al. [2]. To reach safe margins for a curative resection, especially with anatomic resections for small tumors, the PHRR can reach more than 60% of the functioning liver parenchyma. 2. The tumor volume was expressed in relation to liver volume, giving the extent of malignant disease involving the liver. For calculation of sensitivity and specificity, a value for LRI of 0.15 or less was considered a prognostic indicator for postoperative fatal liver failure.

Cohnert et al.: Risk with Hepatic Resection

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Table 1. Diagnoses in 244 patients with hepatic resection for malignant disease. Tumor Primary hepatobiliary tumors Hepatocellular carcinoma Gallbladder carcinoma Cholangiocellular carcinoma Hemangiosarcoma Total Metastatic lesions from Colorectal cancer Hypernephroma Intra-abdominal leiomyosarcoma Gastric cancer Breast cancer Pancreatic cancer Soft tissue sarcoma Adrenal carcinoma Bronchial carcinoma Miscellaneous Total

No.

Table 2. Operations in 244 patients with hepatic resection for malignant disease (combined procedures possible). %

47 10 8 1 66

19.3 4.1 3.3 0.4 27.1

136 7 6 5 4 4 3 3 2 8 178

55.7 2.9 2.5 2.0 1.6 1.6 1.2 1.2 0.8 3.3 72.8

Results Included in the study were 149 men (61.1%) and 95 women (38.9%) with a mean age of 60.4 6 11.5 years (range 27– 85 years) who underwent consecutive hepatic resections in our institution between November 1990 and June 1995. Most of these patients had liver metastases (178/244, 73.0%), and primary hepatobiliary tumors were seen less frequently (66/244, 27.0%). The predominant primary tumor in patients with metastases was colorectal carcinoma (136/178, 76.4%); 42 patients had primary tumors of 14 different origins including hypernephroma, breast cancer, pancreatic and gastric cancer, and various sarcomas. In 66 patients with hepatobiliary malignomas the main histologic type was hepatocellular carcinoma in 47 patients followed by gallbladder carcinoma and cholangiocellular carcinoma (Table 1). Major concomitant disease at the time of surgery was present in 72 of 340 patients (21.2%). Here cardiovascular disorders were predominant (33/340, 9.7%). The incidence of diabetes mellitus (17/244, 7.0%) and liver cirrhosis (13/244, 5.3%) were unexpectedly low in our patient group. These factors did not have a significant influence on the perioperative risk. In 92 of 244 (37.7%) patients with malignant disease major resections involving more than two anatomic segments were performed, as shown in Table 2. The total number of resections exceeds 244 because of combined procedures, such as segmentectomy plus atypical resection. Simultaneous intraabdominal procedures such as colonic resections were performed in 36 patients (14.8%). The overall operating time was 200 6 76 minutes (range 30 – 450 minutes). Liver hilus clamping was applied in 164 patients (67.2%) with a mean duration of 29.2 6 17.9 minutes (range 5– 85 minutes). In 80 patients (32.8%) liver hilus clamping was not used. Mean blood loss for the 244 patients was 1813 6 1539 ml (range 300 –12,000 ml) requiring transfusions in 129 patients (52.9%) (Table 3). Operative mortality was 3.3% for all patients with liver resection for malignant disease (8/244) with 4.5% in patients with liver tumors (3/66) and 2.8% (5/178) in patients with metastases. Hospital mortality was 6.1% among patients with primary liver

Operation

No. of procedures

%

Right hemihepatectomy Extended right hemihepatectomy Left hemihepatectomy Left lobectomy Bisegmentectomy Segmentectomy Atypical resection

38 3 51 13 43 58 102

15.6 1.2 20.9 5.3 17.6 23.8 41.8

tumors (4/66) and 3.9% (6/178) among those with metastases, resulting in an overall hospital mortality for malignant disease of 4.1% (10/244). The main cause of death was multiple organ failure induced by liver failure in five patients and by septic complications in two. Two patients with concomitant coronary artery disease died of postoperative myocardial infarction (Table 4). The hospital mortality was 5.6% (10/179) during the retrospective study period. During the prospective study period no patient deaths occurred. Pretreatment by chemoembolization with epirubicin and Lipiodol was instituted in four patients (Table 5), by which the mean PHRR could be reduced from 49.6% to 20.7% and the mean LRI increased from 0.50 to 1.14. In two of these four patients the pathologist could no longer find vital tumor cells in the resected specimen. In addition to these patients, alternative treatment without resection was performed in 16 patients because the risk evaluation showed that the extent of the planned resection put the patient at high risk for developing postoperative fatal complications. Reoperations were required in 12 patients (4.9%) mainly for bleeding or septic problems. Overall morbidity was 27.0% (66/244) (Table 6). The mean hospital stay was 16.6 6 15.6 days (maximum 118 days). Altogether 121 patients underwent a preoperative ABT. The results show that there was no significant difference in prognostic relevance (Table 7). Calculation of PHRR was possible in 84 patients and of the LRI in 67 patients (Table 8). For all patients with malignant disease the mean PHRR for survivors was 17.6 6 18.7% compared to 40.7 6 17.5% for the nonsurvivors (p 5 0.0009). The LRI was 5.32 6 7.48 for survivors in contrast to 0.17 6 0.21 for nonsurvivors (p 5 0.0005). Excluding the patients with postoperative myocardial infarctions, the mean PHRR of nonsurvivors was 42.3 6 18.0% and the LRI 0.12 6 0.10. In these patients the sensitivity of LRI for a fatal postoperative course was 75% with a specificity of 83%. Although PHRR showed a significant difference for survivors and nonsurvivors, a preoperative prognosis based on the calculation of PHRR did not have major value because of the large number of patients with sufficient liver function who survived extensive resections. PHRR reached a sensitivity of 60% with a specificity of 79% for a PHRR of more than 35%. Among patients with liver metastases the values of nonsurvivors differed significantly from those of the nonsurvivors. The mean PHRR for survivors was 14.0% with a mean LRI of 8.6. Among the nonsurvivors after hepatic resection for metastases the mean PHRR was 44.5% with a mean LRI of 0.1 (p , 0.01) (Table 8).

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Table 3. Blood loss and amount of blood transfusions in patients with hepatic resection for malignant disease. Blood loss

Transfusions Primary liver tumors

Metastases

Patients

Metastases No.

Loss (ml)

No.

Loss (ml)

No.

Units

No.

Units

Survivors Nonsurvivors

140 6

1662 6 1498 2841 6 1172

48 4

1990 6 1549 3300 6 1671

111 6

2.9 6 3.2 5.5 6 2.1

35 4

3.7 6 3.4 4.0 6 1.6

«

«

p , 0.05

Primary liver tumors

« p , 0.01

NS

« NS

Significance (p) was determined by the Mann-Whitney U-test. Table 4. Clinical, preoperative, and intraoperative data for 10 nonsurvivors after hepatic resection (hospital mortality). Patients Gender/age (years)

Diagnosis

Operation

Blood loss (ml)

Survival (days)

M/54 M/75 F/76

Meta. bronchial cancer Gallbladder cancer Meta. colon cancer

Cause of death

PHRR

LRI

Right hemihepatectomy Resection, segment 4 Right hemihepatectomy, right hemicolectomy Right hemihepatectomy Right hemihepatectomy Left hemihepatectomy

1800 3700 3000

2 48 3

Myocardial infarction Myocardial infarction Bleeding

44.5 27.8 71.0

0.01 0.72 0.02

M/55 M/62 M/70

Meta. rectal cancer Meta. colon cancer Meta. renal cancer

5000 1850 2500

18 7 41

22.2 62.2 25.9

0.05 0.02 0.15

Right hemihepatectomy, anterior rectal resection Right hemihepatectomy Left lobectomy Right hemihepatectomy

2900

16

41.2

0.19

5500 2000 2000

3 10 24

MOF after liver failure MOF after liver failure MOF after intra-abdominal abscess MOF after anastomotic insufficiency and peritonitis MOF after liver failure MOF after liver failure MOF after liver failure

M/68

Meta. rectal cancer

M/80 F/71 M/57

HCC HCC HCC

37.3 26.4 52.4

0.12 0.30 0.09

Meta.: metastasis; HCC: hepatocellular carcinoma; MOF: multiple organ failure; PHRR: parenchymal hepatic resection rate; LRI: liver resection index. Table 5. Data from four patients chemoembolization pretreatment.

with

hepatic

Patient

Gender/ age (years) Diagnosis

No. of CEs

Duration of CE (months)

A.H. H.K.

M/57 M/42

6 3

M.T. A.R.

M/64 M/62

3 5

HCC Pancreatic cancer HCC HCC

resection

PHRR (%)

after

PreCE

PostCE

Change PHRR (%)

10 6

27.7 83.8

9.8 39.6

17.9 44.2

5 9

— 36.9

— 12.7

— 24.2

CE: chemoembolization; PHRR: parenchymal hepatic resection rate; HCC: hepatocellular carcinoma.

Table 6. Postoperative complications in 244 patients with hepatic resection for malignant disease. Complication Perihepatic abscess Liver failure Bile fistula Pleural effusion Postoperative bleeding Anastomotic insufficiency Peritonitis Pancreatitis Pneumonia

No. of patients

Reoperations (no. of patients)

14 11 7 7 4

2 — 1 — 4

4

2

3 3 1

3 — —

Discussion With the therapeutic advances for liver tumors, detailed preoperative diagnostic measures such as contrast-enhanced spiral CT [4], refined operative techniques for dissection [5], and improved modalities for control of intraoperative blood loss [6 – 8], the resectability of liver tumors has increased [9]. Mortality is decreasing and has been reported to be as low as 0.9% [10] to 2.9% [9] for hepatocellular carcinoma, 6% for cholangiocellular carcinoma [11], and 0% [12], 2.4% [13], or 4.4% [14] for liver metastases. Nevertheless, a considerable risk of postoperative morbidity has been reported: 16% [15] to 19% [9] and up to 62% [16]. Temporary or definite hepatic failure has been a problem in patients with impaired or normal liver function [7, 17]. Yamanaka et al. developed a prediction system for a large number of patients, including 705 patients with liver cirrhosis, by calculating volumetric and functional data [18]. During their 10-year experi-

Table 7. Preoperative 14C-aminopyrine breath test values in 121 patients with malignant liver lesions. Survivors

Nonsurvivors

Lesion

No.

ABT

No.

ABT

MannWhitney U-test

Metastases

73

0.368 6 0.348

6

0.402 6 0.259

NS


38

0.361 6 0.244

4

0.467 6 0.208

NS

ABT:

14

C-aminopyrine breath test.

ence [19] they used the indocyanine green retention test, which is currently not available at our institution. Hepatic function in our series was estimated by the ABT, which had shown predictive value in a pilot study [3]. These results could


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Table 8. Parenchymal hepatic resection rates in 84 patients and liver resection index values in 67 patients prior to hepatic resection. PHRR (%)

LRI

Metastases


Patients

No. pts.

PHRR (%)

Survivors Nonsurvivors

55 6

14.0 6 16.6 44.5 6 19.3

« p , 0.01

Metastases


No. pts.

PHRR (%)

No. pts.

LRI

No. pts.

LRI

29 4

22.9 6 20.6 36.0 6 12.0

34 6

8.6 6 8.6 0.1 6 0.1

23 4

1.1 6 1.5 0.3 6 0.3

« NS

not be confirmed in the prospective study with a larger series. The ABT values were subnormal for most of our patients in comparison with the normal values of 0.6 to 1.0 reported by Miotti et al. [20]. From the present data we cannot recommend use of the ABT to calculate the risk of postoperative liver failure. Improved operative technique and equipment and postoperative intensive care has resulted in additional indications for hepatic resection of primary liver tumors and liver metastases. To determine safe limits for the extent of hepatic resection, clinical [21–23], volumetric [2, 18, 19], and functional [24] studies have been undertaken to estimate hepatic functional reserve. They have shown that multiple preoperative and perioperative factors influence morbidity and mortality after hepatic resection. We analyzed parameters that can be determined preoperative to develop the LRI as a predictor for survival because the influence of intraoperative and early postoperative factors, such as the amount of blood loss [25, 26], blood transfusions [27], warm ischemia time especially in patients with impaired liver function [28], and operating time [29], demonstrated previously, does not help to distinguish patients at risk preoperatively. For these patients such pretreatment as cytoreduction and sequential resection [30] or alternative treatments such as liver transplantation [31], percutaneous ethanol injection, portal embolization [32], transcatheter arterial embolization, or hepatic arterial chemoinfusion, depending on the primary disease, should be discussed [33]. The extent of the resection should be estimated quantitatively prior to the operation by computer-assisted CT scan or MRI tomography. Pretreatment can reduce tumor size [34] and enhance the growth of the portion of the liver remaining after a planned resection [35]. Various models have been introduced to select patients prior to hepatic resection. Nagino et al. [36] showed the possibility of estimating risk for resection in a subgroup of patients with carcinoma of the biliary tract. In our study we included patients without discrimination of the lesions because it was the aim of our study to find a preoperative predictor with applicability and predictive value for every type of hepatic resection. Preexisting disease did not have a significant influence on survival in our patient group, similar to the results of Yanaga [37], who found no increased mortality in patients with preexistent diabetes mellitus. Although the importance of the extent of hepatic resection in regard to mortality and morbidity is generally accepted, most authors [15, 21, 38] have not analyzed their resection data quantitatively. We could not confirm Sitzmann and Greene’s results [38] that preoperative bilirubin was the only preoperative predictor after hepatic resection. In our patient population the preoperative

« p , 0.01

« NS

serum bilirubin showed no significant difference between survivors and nonsurvivors. The data for the LRI cannot be correlated with the equations of the Japanese authors because of the use of a different function test to estimate hepatic functional reserve. In patients with primary liver tumors neither the PHRR nor the LRI reached significance levels, but the number of patients in this group is also limited. For those with liver metastases the extent of hepatic resection is a major determinant of postoperative survival. The prediction can be improved by calculating the LRI as a combination of preoperatively available clinical, functional, and volumetric data. Inclusion of the ABT value in the LRI limits the prognosis of postoperative liver function tests. It should be replaced by a more reliable liver function test, although one is not yet available because of the complexity of hepatic function. In conclusion, as a result of better patient selection by preoperative volumetric evaluation and pretreatment of patients identified to be at risk for the development of postoperative liver failure, morbidity and mortality were reduced during the course of this study. Re´sume´ On a analyse´ les donneés cliniques, fonctionnelles et volume´triques chez 340 patients conse ćutifs ayant eu une re ´section he´patique pour maladie maligne entre Novembre 1990 et Juin 1995 avec une mortalite´ ope´ratoire de 3.3% (8/244 patients). Chez 178 patients ayant des me´tastases he ´patiques et chez 66 patients ayant une tumeur he´patobiliaire primitive, la mortalite´ hospitalie`re a éte´ de 4.1% (10/244) et la morbidite´ de 22% (54/244). La survie apre`s he´patectomie était fortement influence é par l’e´tendue de la re´section selon le taux de la re´section he ´patique parenchymateuse, la «Parenchymal Hepatic Resection Rate». On peut ame´liorer la pre ´diction des complications postope´ratoires chez les patients ayant des me´tastases he ´patique en calculant l’Index de Re´section He ´patique qui a une sensibilite´ de 75% et une spećificite ´ de 83%. Resumen Se analizo ´ la informacio ń clıńica de laboratorio, funcional y volume´trica en 350 pacientes consecutivos que fueron sometidos a resecciones hepa´ticas por neoplasia maligna con una mortalidad operatoria de 3.3% (8/244 pacientes), entre noviembre de 1990 y junio de 1995. En 178 pacientes con meta´stasis hepa´ticas y en 66 pacientes con tumores hepatobiliares primarios, la mortalidad hospitalaria fue 4.1% (10/244) y la morbilidad 22% (54/244). La

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sobrevida luego de hepatectomıá aparecio ´ fuertemente influenciada por la magnitud de la reseccio ń cuantificada por el Parenchymal Hepatic Resection Rate. La prediccio ń de complicaciones postoperatorias letales puede ser mejorada en los pacientes con meta´stasis hepa ´ticas mediante el ca´lculo del Indice de Reseccio ń Hepa´tica, con una sensibilidad de 75% y una especificidad de 83%. References 1. Gill, R.A., Goodman, M.W., Golfus, G.R., Onstad, G.R., Bubrick, M.P.: Aminopyrine breath test predicts surgical risk for patients with liver disease. Ann. Surg. 198:701, 1983 2. Okamoto, E., Kyo, A., Yamanaka, N., Tanaka, N., Kuwata K.: Prediction of the safe limits of hepatectomy by combined volumetric and functional measurements in patients with impaired hepatic function. Surgery 95:586, 1984 3. Hofmann, T.U., Rau, H.G., Sauter, G., Hernandez-Richter, T., Lauterjung, K.L., Schildberg, F.W.: Liver resection index for prognosis of death after hepatectomy. Br. J. Surg. 81(Suppl. 1):87, 1994 4. Yoshimi, F., Hasegawa, H., Amemiya, R., Koizumi, S., Kobayashi, H., Matsueda, K.: Application of three-dimensional spiral computed tomographic angiography prior to hepatectomy for hepatocellular carcinoma. Surg. Today 25:37, 1995 5. Rau, H.G., Schardey, H.M., Buttler, E., Reuter, C., Cohnert, T.U., Schildberg, F.W.: A comparison of different techniques for liver resection: blunt dissection, ultrasonic aspirator and jet-cutter. Eur. J. Surg. Oncol. 21:183, 1995 6. Huguet, C., Nordlinger, B., Galopin, J.J., Bloch, P., Gallot, D.: Normothermic hepatic vascular exclusion for extensive hepatectomy. Surg. Gynecol. Obstet. 147:689, 1978 7. Belghiti, J., DiCarlo, I., Sauvanet, A., Uribe, M., Fekete, F.: A ten-year experience with hepatic resection in 338 patients: evolutions in indications and of operative mortality. Eur. J. Surg. 160:277, 1994 8. Cunningham, J.D., Fong, Y., Shriver, C., Melendez, J., Marx, W.L., Blumgart, L.H.: One hundred consecutive hepatic resections. Arch. Surg. 129:1050, 1994 9. Bismuth, H., Chiche, L., Castaing, D.: Surgical treatment of hepatocellular carcinomas in noncirrhotic liver: experience with 68 liver resections. World. J. Surg. 19:35, 1995 10. Kawasaki, S., Makuuchi, M., Miyagawa, S., Kakazu, T., Hayashi, K., Kasai, H., Miwa, S., Hui, A-M., Nishimaki, K.: Results of hepatic resection for hepatocellular carcinoma. World J. Surg 19:31, 1995 11. Pichlmayr, R., Lamesch, P., Weimann, A., Tusch, G., Ringe, B.: Surgical treatment of cholangiocellular carcinoma. World J. Surg. 19:83, 1995 12. Gayowski, T.J., Iwatsuki, S., Madariaga, J.R., Selby, R., Todo, S., Irish, W., Starzl, T.E.: Experience in hepatic resection for metastatic colorectal cancer: analysis of clinical and pathologic risk factors. Surgery 116:703, 1994 13. Schildberg, F.W., Meyer, G., Piltz, S., Koebe, H.G.: Surgical treatment of tumor metastases: general considerations and results. Surg. Today 25:1, 1995 14. Scheele, J., Stang, R., Altendorf-Hofmann, A., Paul, M.: Resection of colorectal liver metastases. World J. Surg. 19:59, 1995 15. Tsao, J.I., Loftus, J.P., Nagorney, D.M., Adson, M.A., Ilstrup, D.M.: Trends in morbidity and mortality of hepatic resection for malignancy. Ann. Surg. 220:199, 1994 16. Vetto, J.T., Hughes, K.S., Rosenstein, R., Sugarbaker, P.H.: Morbidity and mortality of hepatic resection for metastatic colorectal carcinoma. Dis. Colon Rectum 33:408, 1990 17. Lehnert, T., Otto, G., Herfarth, C.: Therapeutic modalities and prognostic factors for primary and secondary liver tumors. World J. Surg. 19:252, 1995

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18. Yamanaka, N., Okamoto, E., Toyosaka, A., Mitunobu, M., Fujihara, S., Kato, T., Fujimoto, J., Oriyama, T., Furukawa, K., Kawamura, E.: Prognostic factors after hepatectomy for hepatocellular carcinomas. Cancer 65:1104, 1990 19. Yamanaka, N., Okamoto, E., Oriyama, T., Fujimoto, J., Furukawa, K., Kawamura, E., Tanaka, T., Tomoda, F.: A prediction scoring system to select the surgical treatment of liver cancer. Ann. Surg. 219:342, 1994 20. Miotti, T., Bircher, J., Preisig, R.: The 30-minute aminopyrine breath test: optimization of sampling times after intravenous administration of 14C-aminopyrine. Digestion 39:241, 1988 21. Didolkar, M.S., Fitzpatrick, J.L., Elias, E.G., Whitley, N., Keramati, B., Suter, C.M., Brown, S.: Risk factors before hepatectomy, hepatic function after hepatectomy and computed tomographic changes as indicators of mortality from hepatic failure. Surg. Gynecol. Obstet. 169:17, 1989 22. Farid, H., O’Connell, T.: Hepatic resections: changing mortality and morbidity. Am. Surg. 60:748, 1994 23. Lai, E.C.S., Fam, S.T., Lo, C.M., Chu, K.M., Liu, C.L., Wong, J.: Hepatic resection for hepatocellular carcinoma. Ann. Surg. 221:291, 1995 24. Yasui, M., Harada, A., Torii, A., Nakao, A., Nonami, T., Takagi, H.: Impaired liver function and long-term prognosis after hepatectomy for hepatocellular carcinoma. World J. Surg. 19:439, 1995 25. Shimada, M., Matsumata, T., Akazawa, K., Kamakura, T., Itasaka, H., Sugimachi, K., Nose, Y.: Estimation of risk of major complications after hepatic resection. Am. J. Surg. 167:399, 1994 26. Nagasue, N., Uchida, M., Kubota, H., Takafumi, H., Kohno, H., Nakamura, T.: Cirrhotic livers can tolerate 30 minutes ischemia at normal environmental temperature. Eur. J. Surg. 161:181, 1995 27. Habib, N.A., Koh, M.K., Zografos, G., Awad, R.W., Bottino, G.: Elective hepatic resection for benign and malignant disease: early results. Br. J. Surg. 80:1039, 1993 28. Huguet, C., Gavelli, A., Bona, S.: Hepatic resection with ischemia of the liver exceeding one hour. J. Am. Coll. Surg. 178:454, 1994 29. Miyagawa, S., Makuuchi, M., Kawasaki, S., Kakazu, T.: Criteria for safe hepatic resection. Am. J. Surg. 169:589, 1995 30. Tang, Z.Y., Yu, Y.Q., Zhou, Z.D., Ma, Z.C., Yang, B.H., Lin, Z.Y., Lu, J.Z., Liu, K.D., Fan, Z., Zeng, Z.C.: Treatment of unresectable primary liver cancer: with reference to cytoreduction and sequential resection. World J. Surg. 19:47, 1995 31. Selby, R., Kadry, Z., Carr, B., Tzakis, A., Madariaga, J.R., Iwatsuki, S.: Liver transplantation for hepatocellular carcinoma. World J. Surg. 19:53, 1995 32. Makuuchi, M., LeThai, B., Takayasu, K., Takayama, T., Kosuge, T., Gunven, P., Yamazaki, S., Hasegawa, H., Ozaki, H.: Preoperative portal embolization to increase safety of major hepatectomy for hilar bile duct carcinoma: a preliminary report. Surgery 107:521, 1990 33. Ohto, M., Yoshikawa, M., Saisho, H., Ebara, M., Sugiura, N.: Nonsurgical treatment of hepatocellular carcinoma in cirrhotic patients. World J. Surg. 19:42, 1995 34. Yu, Y.Q., Xu, D.B., Zhou, S.D., Lu, J.Z., Tang, Z.Y., Mack, P.: Experience with liver resection after hepatic arterial chemoembolization for hepatocellular carcinoma. Cancer 71:62, 1993 35. DeBaere, T., Roche, A., Vavassuer, D., Therasse, E., Indushekar, S., Elias, D., Bognel, C.: Portal vein embolization: utility for inducing left hepatic lobe hypertrophy before surgery. Radiology 188:73, 1993 36. Nagino, M., Nimura, Y., Hayakawa, N., Kamiya, J., Kondo, S., Sasaki, R., Hamajima, N.: Logistic regression and discriminant analysis of hepatic failure after liver resection for carcinoma of the biliary tract. World J. Surg. 17:250, 1993 37. Yanaga, K., Matsumata, T., Hayashi, H., Shimada, M., Urata, K., Suehiro, T., Sugimachi, K.: Effect of diabetes mellitus on hepatic resection. Arch. Surg. 128:445, 1993 38. Sitzmann, J.V., Greene, P.S.: Perioperative predictors of morbidity following hepatic resection for neoplasm. Ann. Surg. 219:13, 1994


Invited Commentary J. Alvarez F. Represa, M.D. Department of Surgery, Complutense University, San Carlos Hospital, Madrid, Spain

When surgeons are faced with any hepatic resection, they should try to preserve sufficient liver parenchyma to maintain adequate hepatocellular function. This point is particularly important in patients with cirrhosis. For many years, one of the main goals of surgeons has been to predict the operative risk of patients who are going to have a liver tumor operation and to evaluate the patient’s survival probabilities. For this purpose, many data have been used, such as the presence of other liver diseases, several liver function tests, the morphologic characteristics of the tumor, and its microscopic special features. However, most of this information is obtained after having performed the operation. Cohnert et al., in their excellent paper, seek to quantify the postoperative risk by using only preoperatively available data. They study the PHRR using volumetric parameters, as well as the LRI in which they use, in addition to the volumetric parameters, other data such as the age of the patients, and the ABT value, which evaluates the hepatic functional capacity of the patients. The authors studied 244 patients. As they highlight, the incidence of cirrhosis was unexpectedly low (5.3%), especially when these figures are compared with the ones obtained in eastern

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Asian countries. Furthermore, simultaneous intraabdominal procedures were carried out in 14.8% of these patients, and it would have been helpful if we had been told what sort of procedures were performed. The mean blood loss of 1,813 ml should be noted. The main cause of hospital mortality was multiple organ failure. Several studies have addressed prediction of posthepatectomy liver failure, but no reliable tests are available that are simple and easy to perform and that can clearly classify the patient who may or may not tolerate hepatic resection. Nevertheless, the paper of Naguino, which is cited by the authors, could distinguish the patients with posthepatectomy liver failure from those without with 86.9% accuracy, 96.0% sensitivity, and 83.1% specificity by means of his own discriminant formula, using five variables: linear pattern of oral glucose tolerance test, presence of cholangitis, presence of pancreatoduodenectomy, indocyanine green disappearance rate, and liver resection rate. The results obtained in the chemoembolization cases, by reducing the PHHR from 49.6% to 20.7% and by increasing the LRI from 0.50 to 1.4 are remarkable. The figures of PHRR and LRI for the survivors and nonsurvivors are noteworthy and highly conclusive. I agree with the authors that inclusion of the ABT value in the LRI curbs the use of this index; however, for the moment, there is no other reliable test of hepatic function available. In the near future we hope that we will be able to accurately assess these patients using new diagnostic techniques, such as positron emission tomography, which analyzes functions of the organs under consideration.