Br. J. Surg. 1992, Vol. 79, March,
224--226
T. Ezaki*, Y. Seo, H.Tomoda, M. Furusawa, T. Kanematsu* and K. Sugimachi* Department of Gastroenterological Surgery, bJational Kyushu Cancer Center and *Department of Surgery I!, Kyushu University Hospital, Fukuoka, Japan Correspondence to: Dr T. Ezaki, Second Department of Surgery, School of Medicine, University of Occupational and Environmental Health, Yahatanishi-ku, Kitakyushu 807, Japan
Partia I hepatic resection under intermittent hepatic inflow occlusion in patients with chronic liver disease A partial hepatic resection was performed in 13 patients with chronic liver disease using intermittent hepatic inflow occlusion. Eleven patients had liver cirrhosis and two had chronic hepatitis. Seven patients were classiJied as Child’s grade A and six as Child’s grade B before operation. Dissection of the hepatic parenchyma was performed during intermittent injow occlusion. The time of clamping and declamping was 10-20 min and 5-8 min, respectively. Postoperative data on liver function showed recovery to preoperative levels by about 10 days after operation. There were no life-threatening complications. These results indicate that intermittent hepatic inflow occlusion can be achieved easily and safely to allow non-anatomical resection inpatients with chronic liver disease.
The accepted and standardized resectional procedures in liver surgery have been a lobar or segmental resection. Resection in those with chronic liver disease, particularly cirrhosis, has been considered dangerous because of poor regeneration of the residual liver. Non-anatomical resection may be advocated to: ( 1 ) leave as much of a liver remnant as possible; ( 2 ) minimize intraoperative blood loss; and (3 ) shorten the liver ischaemic time. The Pringle manoeuvre’ reduces blood loss but the ischaemic time must be monitored, particularly in patients with chronic liver disease. The best method for liver resection would be surgery performed under intermittent hepatic inflow occlusion. This study investigated the postoperative damage following partial hepatic resection in patients with chronic liver disease using intermittent hepatic inflow occlusion. This was not a comparative study.
Table 1 Preoperative liverfunction of patients with chronic liver diseuse undergoing hepatic resection Liver cirrhosis ( n = 11) Child’s grade A B Blood biochemistry Albumin (g/dl) Bilirubin (mg/dl) SGOT (units/l) SGPT (unitsil)
5 6
3.5( 0.4 ) 0.7(0.2 ) 49( 19) 54(25)
Chronic hepatitis ( n = 2) -
2 0
3.9(0.1 ) 0.6(0.0) 48(18) 72(23)
Values are mean(s.d. ). SGOT, serum glutamic oxaloacetic transaminase (normal range 11 -37 units/l); SGPT, serum glutamic pyruvic transaminase (normal range 7-30 units/!)
Patients and methods During the past 2 years partial resection of the liver of less than one lobe was carried out using intermittent hepatic inflow occlusion in 13 patients with chronic liver disease. There were 11 men and two women with a mean age of 60 (range 49-70) years. Eleven patients had hepatocellular carcinoma, one had intrahepatic cholangiocarcinoma and one had a regenerating liver nodule. Eleven patients had cirrhosis and two had chronic hepatitis. Seven patients were classified as Child’s grade A and six as Child’s grade B before operation’. Results of preoperative liver function tests are shown in Table I . The eight segments of the liver are as described by Couinaud3.
(Alcon, Humacao, Puerto Rico) or Oxycel (Becton-Dickinson, New Jersey, USA) cotton were used with suture ligation of the bleeding vessels during declamping. The tumour-free margin was examined repeatedly using intraoperative ultrasonography. Clamping and declamping were repeated until the liver lesion had been completely resected.
Results
Operative procedures After mobilization of the liver, cholecystectomy and intraoperative ultrasonography were performed. The main hepatic pedicle was encircled with tape, as were the right and left branches of the inflow vessels. An ATOM (polyvinyl chloride; ATOM Medical, Tokyo, Japan) tube of 2.75 mm diameter was used for the snares. For hemihepatic inflow occlusion a smaller tube was used (2.0 or 2.35 rnm in diameter). When the tumour was located in the posterior segment of the right lobe (segments VI and VII) or the left lateral segment of the left lobe (I1 and H I ) , hepatic resection was carried out by clamping the right or left branch of the inflow vessels. When the tumour was located in the anterior segment of the right lobe (segments V and VIII) or the medial segment of the left lobe (IV), an occlusion of the total hepatic pedicle was sometimes needed because these regions receive blood from the opposite lobe. The time of clamping and declamping was usually 10-20 min and 5-8 min, respectively, depending on the adequacy of preoperative liver function. During clamping, dissection of the liver was carried out using an ultrasonic surgical aspirator. Haemostasis was achieved with electrocautery. Haemostatic agents such as Avitene
Patient details are shown in Table 2. All patients had cirrhosis except numbers 1 and 6. Two patients (numbers 3 and 7 ) underwent a right hepatic lobectomy leaving a small volume of segment VIII. Other patients underwent a partial hepatectomy of less than one segment or two subsegments. One patient (number 1 ) had a small liver cancer of 3 5 cm in diameter situated in the bifurcation between the anterior and posterior branches of the right portal vein; this patient underwent a partial hepatic resection. Details of the occlusion times for each operation are shown in Table 2. Estimated blood loss during surgeryrangedfrom 150to2700ml(mean(s.d.) 1153(784)ml). Patient number 10 (2700 ml loss) underwent resection in two different regions (segments 111 and VII) and had undergone a gastrectomy. Mean(s.d.) operative time was 4.8( 1.2) h in patients with cirrhosis and 4.611.9) h in those with chronic hepatitis. No instances of haemorrhagic shock occurred. One patient (number 1) had a postoperative intraperitoneal abscess, and another (patient number 5 ) had a right pleural effusion which required pleural paracentesis. Two patients (numbers 7 and 12) suffered right ulnar nerve palsy after
224
0007-1323/92/030224-03
0 1992 Butterworth-Heinemann Ltd
Intermittent hepatic inflow occlusion and liver resection: T. Ezaki et al.
Table 2 Details of patients undergoing hepatic resection Tumour Patient no.
(years)
Child‘s grade
Liver tumour
Localization (segment )
54
A
HCC
V
Age
1
Diameter (cm)
3.5
Type of resection
Type of occlusion
Partial
Total Right
2
55
B
HCC
V
3.5
Partial
3
49
A
4
59
B
CC Haemangioma RN
V VIII VIII
3.0 2.0 2.0
Right lobectomy Partial
5
67
B
HCC
VIII
4.0
Partial
6
56
A
HCC
VlII
3.0
7
68
A
HCC
V VII
1.5
8
58
A
HCC
9
59
HCC
10
63
B B
VI Vlll
HCC
111
10.0 2.2 2.0 3.5 4.0
Partial Right lokctomy Partial
1.5
Total Right Total Right Total Right
Duration of occlusion time (min x frequency ) 10 x 4
to
x
5
15 x 1 17 x 1
5
Total Right Total
10 x 2 15 x 2
5
15 x 3
5
Total Right
10 x 5 10 x 2 20 x 2 10 x 2
Total
Partial Partial Partial
Total Total
Partial
Total Left
II
70
A
HCC
VII IV
12
60
A
HCC
VII
3.5
Partial
Total Right
13
56
B
HCC
VI
1.4
Partial
Total Right
to
1 1
220
5
10 x 4
2200 490
1700 150
I700
5
I650 600 2700
8
5 5
x 5
10 x 1 10 x 2
5
10 x 2
5
20 x 8
Intraoperative bleeding (ml)
730
5
3 10 x 2 10 x 2
}
Revascularization time (min)
700 950
1200
5 ~
HCC, hepatocellular carcinoma; CC, cholangiocarcinoma; RN, regenerating nodule
OT
a
i
t ’
I
1
3
s 7 Time (days)
L i v e r resection
I
I
I
t ’
14
b
I
I
1
I
3
5
7
14
Time (days)
L i v e r resection
T
500
-3;-
1 400
-
.-c
VI
c,
C
V
C
Y
300
c .-
-
300
v)
J
k
400
C
200
200
100
100
0
2
I
t ‘ Liver resection
I
I
3
5
I
7 Time (days)
C
I
0
t ’
14
d
L i v e r resection
3
5
7
14
Time (days)
Figure 1 Serial changes in a serum albumin level, b serum concentraiions of toial bilirubin, c serum activities of glutamic oxaloacetic transaminuse ( S G O T ; normal range 11-37 unitsll) and d serum activities of glutamic pyruvic transaminase (SGPT; normal range 7-30 unitsll) after hepatic resection. Values are mean(s.d.1
Br. J. Surg., Vol. 79, No. 3, March 1992
225
Intermittent hepatic inflow occlusion and liver resection: T. Ezaki et al.
operation. There were no complications relating to the liver and no deaths related to surgery. The serial changes in the levels of albumin, total bilirubin, serum glutamic oxaloacetic transaminase (SGOT ) and serum glutamic pyruvic transaminase ( S G P T ) of the patients are shown in Figure 1 . Most parameters attained the preoperative levels by about 10 days after operation.
Discussion Recently liver resection has become safer and more widely practised, sometimes even without blood transfusion4. Bleeding must be kept to a minimum because it often leads to postoperative hepatic failure, particularly in those with cirrhosis'. Various methods have been described to reduce bleeding" - 9 but the total ischaemic time of the liver remnant must be kept t o a minimum. Delva et a!." reported that vascular occlusion was well tolerated ( u p to 60 min) in a normal liver. Makuuchi et a/.' reported occlusion of the inflow vessels for up to 30 min using hemihepatic vascular occlusion in a cirrhotic liver. Ten to 20 min of ischaemia may be considered safe and there is a direct correlation between the levels of tissue adenosine triphosphate and the status of the hepatic blood supply'0. It takes longer to perform hepatectomy under intermittent inflow occlusion but this may save the cirrhotic liver remnant by allowing a shorter overall ischaemic time. In the bloodless operative field which can be obtained during intermittent inflow occlusion, the surgeon can perform hepatic resection much more safely and easily by accurately confirming and managing the intrahepatic vessels. A reduced blood loss may be obtained
226
during hepatic resection, particularly when dissecting the upper parts of the liver, if respiration is controlled to decrease the intrathoracic pressure and thereby the hepatic venous backflow.
References 1. 2. 3.
4. 5. 6. 7.
8. 9. 10.
Pringle JH. Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg 1908; 48: 541-9. Child CG, Turcotte JG. Surgery in portal hypertension. In: Child CG, ed. Major Problems in Clinical Surgery. The Liver und Porrul Hypertension. Philadelphia: WB Saunders, 1964: 1-85. Couinaud C . Le Foie, Eludes Anatomiques et Chirurgicales. Paris: Masson et Cie, 1957: 9-12. Ryan J, Faulkner J. Liver resection without blood transfusion. Am J Surg 1989; 157: 412-5. Nagorney DM, van Heerden JA, Ilstrup DM, Adson MA. Primary hepatic malignancy: surgical management and determinants of survival. Surgery 1989; 106: 740-9. Delva E, Camus Y, Nordlinger B et a/. Vascular occlusions for liver resections. Operative management and tolerance to hepatic ischemia: 142 cases. Ann Surg 1989; 209: 211-18. Makuuchi M, Mori T, Gunven P, Yamazaki S, Hasegawa H. Safety of hemihepatic vascular occlusion during resection of the liver. Sury Gynecol Obstet 1987; 164: 155-8. Nagasue N, Yukaya H, Ogawa Y, Hirose S, Okita M. Segmental and subsegmental resections of the cirrhotic liver under hepatic inflow and outflow occlusion. Br J Surg 1985; 72: 565-8. Schwartz SI. What's new in general surgery. Hepatic resection. Ann Surg 1990; 211: 1-8. Kanematsu T, Higashi K , Takenaka K, Maehara K , Sugimachi K . Bioenergy status of human liver during and after warm ischemia. Hepatogastroenterolog~1990; 37: 160-2.
Paper accepted 17 October 1991
Br. J. Surg., Vol. 79, No. 3, March 1992
224--226
T. Ezaki*, Y. Seo, H.Tomoda, M. Furusawa, T. Kanematsu* and K. Sugimachi* Department of Gastroenterological Surgery, bJational Kyushu Cancer Center and *Department of Surgery I!, Kyushu University Hospital, Fukuoka, Japan Correspondence to: Dr T. Ezaki, Second Department of Surgery, School of Medicine, University of Occupational and Environmental Health, Yahatanishi-ku, Kitakyushu 807, Japan
Partia I hepatic resection under intermittent hepatic inflow occlusion in patients with chronic liver disease A partial hepatic resection was performed in 13 patients with chronic liver disease using intermittent hepatic inflow occlusion. Eleven patients had liver cirrhosis and two had chronic hepatitis. Seven patients were classiJied as Child’s grade A and six as Child’s grade B before operation. Dissection of the hepatic parenchyma was performed during intermittent injow occlusion. The time of clamping and declamping was 10-20 min and 5-8 min, respectively. Postoperative data on liver function showed recovery to preoperative levels by about 10 days after operation. There were no life-threatening complications. These results indicate that intermittent hepatic inflow occlusion can be achieved easily and safely to allow non-anatomical resection inpatients with chronic liver disease.
The accepted and standardized resectional procedures in liver surgery have been a lobar or segmental resection. Resection in those with chronic liver disease, particularly cirrhosis, has been considered dangerous because of poor regeneration of the residual liver. Non-anatomical resection may be advocated to: ( 1 ) leave as much of a liver remnant as possible; ( 2 ) minimize intraoperative blood loss; and (3 ) shorten the liver ischaemic time. The Pringle manoeuvre’ reduces blood loss but the ischaemic time must be monitored, particularly in patients with chronic liver disease. The best method for liver resection would be surgery performed under intermittent hepatic inflow occlusion. This study investigated the postoperative damage following partial hepatic resection in patients with chronic liver disease using intermittent hepatic inflow occlusion. This was not a comparative study.
Table 1 Preoperative liverfunction of patients with chronic liver diseuse undergoing hepatic resection Liver cirrhosis ( n = 11) Child’s grade A B Blood biochemistry Albumin (g/dl) Bilirubin (mg/dl) SGOT (units/l) SGPT (unitsil)
5 6
3.5( 0.4 ) 0.7(0.2 ) 49( 19) 54(25)
Chronic hepatitis ( n = 2) -
2 0
3.9(0.1 ) 0.6(0.0) 48(18) 72(23)
Values are mean(s.d. ). SGOT, serum glutamic oxaloacetic transaminase (normal range 11 -37 units/l); SGPT, serum glutamic pyruvic transaminase (normal range 7-30 units/!)
Patients and methods During the past 2 years partial resection of the liver of less than one lobe was carried out using intermittent hepatic inflow occlusion in 13 patients with chronic liver disease. There were 11 men and two women with a mean age of 60 (range 49-70) years. Eleven patients had hepatocellular carcinoma, one had intrahepatic cholangiocarcinoma and one had a regenerating liver nodule. Eleven patients had cirrhosis and two had chronic hepatitis. Seven patients were classified as Child’s grade A and six as Child’s grade B before operation’. Results of preoperative liver function tests are shown in Table I . The eight segments of the liver are as described by Couinaud3.
(Alcon, Humacao, Puerto Rico) or Oxycel (Becton-Dickinson, New Jersey, USA) cotton were used with suture ligation of the bleeding vessels during declamping. The tumour-free margin was examined repeatedly using intraoperative ultrasonography. Clamping and declamping were repeated until the liver lesion had been completely resected.
Results
Operative procedures After mobilization of the liver, cholecystectomy and intraoperative ultrasonography were performed. The main hepatic pedicle was encircled with tape, as were the right and left branches of the inflow vessels. An ATOM (polyvinyl chloride; ATOM Medical, Tokyo, Japan) tube of 2.75 mm diameter was used for the snares. For hemihepatic inflow occlusion a smaller tube was used (2.0 or 2.35 rnm in diameter). When the tumour was located in the posterior segment of the right lobe (segments VI and VII) or the left lateral segment of the left lobe (I1 and H I ) , hepatic resection was carried out by clamping the right or left branch of the inflow vessels. When the tumour was located in the anterior segment of the right lobe (segments V and VIII) or the medial segment of the left lobe (IV), an occlusion of the total hepatic pedicle was sometimes needed because these regions receive blood from the opposite lobe. The time of clamping and declamping was usually 10-20 min and 5-8 min, respectively, depending on the adequacy of preoperative liver function. During clamping, dissection of the liver was carried out using an ultrasonic surgical aspirator. Haemostasis was achieved with electrocautery. Haemostatic agents such as Avitene
Patient details are shown in Table 2. All patients had cirrhosis except numbers 1 and 6. Two patients (numbers 3 and 7 ) underwent a right hepatic lobectomy leaving a small volume of segment VIII. Other patients underwent a partial hepatectomy of less than one segment or two subsegments. One patient (number 1 ) had a small liver cancer of 3 5 cm in diameter situated in the bifurcation between the anterior and posterior branches of the right portal vein; this patient underwent a partial hepatic resection. Details of the occlusion times for each operation are shown in Table 2. Estimated blood loss during surgeryrangedfrom 150to2700ml(mean(s.d.) 1153(784)ml). Patient number 10 (2700 ml loss) underwent resection in two different regions (segments 111 and VII) and had undergone a gastrectomy. Mean(s.d.) operative time was 4.8( 1.2) h in patients with cirrhosis and 4.611.9) h in those with chronic hepatitis. No instances of haemorrhagic shock occurred. One patient (number 1) had a postoperative intraperitoneal abscess, and another (patient number 5 ) had a right pleural effusion which required pleural paracentesis. Two patients (numbers 7 and 12) suffered right ulnar nerve palsy after
224
0007-1323/92/030224-03
0 1992 Butterworth-Heinemann Ltd
Intermittent hepatic inflow occlusion and liver resection: T. Ezaki et al.
Table 2 Details of patients undergoing hepatic resection Tumour Patient no.
(years)
Child‘s grade
Liver tumour
Localization (segment )
54
A
HCC
V
Age
1
Diameter (cm)
3.5
Type of resection
Type of occlusion
Partial
Total Right
2
55
B
HCC
V
3.5
Partial
3
49
A
4
59
B
CC Haemangioma RN
V VIII VIII
3.0 2.0 2.0
Right lobectomy Partial
5
67
B
HCC
VIII
4.0
Partial
6
56
A
HCC
VlII
3.0
7
68
A
HCC
V VII
1.5
8
58
A
HCC
9
59
HCC
10
63
B B
VI Vlll
HCC
111
10.0 2.2 2.0 3.5 4.0
Partial Right lokctomy Partial
1.5
Total Right Total Right Total Right
Duration of occlusion time (min x frequency ) 10 x 4
to
x
5
15 x 1 17 x 1
5
Total Right Total
10 x 2 15 x 2
5
15 x 3
5
Total Right
10 x 5 10 x 2 20 x 2 10 x 2
Total
Partial Partial Partial
Total Total
Partial
Total Left
II
70
A
HCC
VII IV
12
60
A
HCC
VII
3.5
Partial
Total Right
13
56
B
HCC
VI
1.4
Partial
Total Right
to
1 1
220
5
10 x 4
2200 490
1700 150
I700
5
I650 600 2700
8
5 5
x 5
10 x 1 10 x 2
5
10 x 2
5
20 x 8
Intraoperative bleeding (ml)
730
5
3 10 x 2 10 x 2
}
Revascularization time (min)
700 950
1200
5 ~
HCC, hepatocellular carcinoma; CC, cholangiocarcinoma; RN, regenerating nodule
OT
a
i
t ’
I
1
3
s 7 Time (days)
L i v e r resection
I
I
I
t ’
14
b
I
I
1
I
3
5
7
14
Time (days)
L i v e r resection
T
500
-3;-
1 400
-
.-c
VI
c,
C
V
C
Y
300
c .-
-
300
v)
J
k
400
C
200
200
100
100
0
2
I
t ‘ Liver resection
I
I
3
5
I
7 Time (days)
C
I
0
t ’
14
d
L i v e r resection
3
5
7
14
Time (days)
Figure 1 Serial changes in a serum albumin level, b serum concentraiions of toial bilirubin, c serum activities of glutamic oxaloacetic transaminuse ( S G O T ; normal range 11-37 unitsll) and d serum activities of glutamic pyruvic transaminase (SGPT; normal range 7-30 unitsll) after hepatic resection. Values are mean(s.d.1
Br. J. Surg., Vol. 79, No. 3, March 1992
225
Intermittent hepatic inflow occlusion and liver resection: T. Ezaki et al.
operation. There were no complications relating to the liver and no deaths related to surgery. The serial changes in the levels of albumin, total bilirubin, serum glutamic oxaloacetic transaminase (SGOT ) and serum glutamic pyruvic transaminase ( S G P T ) of the patients are shown in Figure 1 . Most parameters attained the preoperative levels by about 10 days after operation.
Discussion Recently liver resection has become safer and more widely practised, sometimes even without blood transfusion4. Bleeding must be kept to a minimum because it often leads to postoperative hepatic failure, particularly in those with cirrhosis'. Various methods have been described to reduce bleeding" - 9 but the total ischaemic time of the liver remnant must be kept t o a minimum. Delva et a!." reported that vascular occlusion was well tolerated ( u p to 60 min) in a normal liver. Makuuchi et a/.' reported occlusion of the inflow vessels for up to 30 min using hemihepatic vascular occlusion in a cirrhotic liver. Ten to 20 min of ischaemia may be considered safe and there is a direct correlation between the levels of tissue adenosine triphosphate and the status of the hepatic blood supply'0. It takes longer to perform hepatectomy under intermittent inflow occlusion but this may save the cirrhotic liver remnant by allowing a shorter overall ischaemic time. In the bloodless operative field which can be obtained during intermittent inflow occlusion, the surgeon can perform hepatic resection much more safely and easily by accurately confirming and managing the intrahepatic vessels. A reduced blood loss may be obtained
226
during hepatic resection, particularly when dissecting the upper parts of the liver, if respiration is controlled to decrease the intrathoracic pressure and thereby the hepatic venous backflow.
References 1. 2. 3.
4. 5. 6. 7.
8. 9. 10.
Pringle JH. Notes on the arrest of hepatic hemorrhage due to trauma. Ann Surg 1908; 48: 541-9. Child CG, Turcotte JG. Surgery in portal hypertension. In: Child CG, ed. Major Problems in Clinical Surgery. The Liver und Porrul Hypertension. Philadelphia: WB Saunders, 1964: 1-85. Couinaud C . Le Foie, Eludes Anatomiques et Chirurgicales. Paris: Masson et Cie, 1957: 9-12. Ryan J, Faulkner J. Liver resection without blood transfusion. Am J Surg 1989; 157: 412-5. Nagorney DM, van Heerden JA, Ilstrup DM, Adson MA. Primary hepatic malignancy: surgical management and determinants of survival. Surgery 1989; 106: 740-9. Delva E, Camus Y, Nordlinger B et a/. Vascular occlusions for liver resections. Operative management and tolerance to hepatic ischemia: 142 cases. Ann Surg 1989; 209: 211-18. Makuuchi M, Mori T, Gunven P, Yamazaki S, Hasegawa H. Safety of hemihepatic vascular occlusion during resection of the liver. Sury Gynecol Obstet 1987; 164: 155-8. Nagasue N, Yukaya H, Ogawa Y, Hirose S, Okita M. Segmental and subsegmental resections of the cirrhotic liver under hepatic inflow and outflow occlusion. Br J Surg 1985; 72: 565-8. Schwartz SI. What's new in general surgery. Hepatic resection. Ann Surg 1990; 211: 1-8. Kanematsu T, Higashi K , Takenaka K, Maehara K , Sugimachi K . Bioenergy status of human liver during and after warm ischemia. Hepatogastroenterolog~1990; 37: 160-2.
Paper accepted 17 October 1991
Br. J. Surg., Vol. 79, No. 3, March 1992
