Scoring criteria for determining the safety of liver resection for malignant liver tumors

Table 1 Clinical demographics of the patients who underwent liver resection for malignant tumors in the no liver dysfunction group (n = 78) and liver dysfunction group (n = 8)

Clinical variables / characteristics	Total values (n = 86)	No liver dysfunction (n = 78)	Liver dysfunction (n = 8)	P-values
Age (yr)	67.0 ± 10.3	66.8 ± 10.5	68.7 ± 9.3	NS
BSA (cm2)	1.61 ± 0.18	1.60 ± 0.18	1.65 ± 0.18	NS
Albumin (g/dL)	4.0 ± 0.4	4.0 ± 0.4	3.8 ± 0.4	NS
Bilirubin (mg/dL)	0.7 ± 0.3	0.6 ± 0.3	0.8 ± 0.4	NS
PT (%)	93.4 ± 11.9	93.9 ± 12.1	88.4 ± 9.7	NS
ICGR15 (%)	9.0 ± 4.6	8.4 ± 4.3	14.9 ± 2.5	< 0.001
HH15	0.578 ± 0.079	0.575 ± 0.078	0.617 ± 0.010	NS
LHL15	0.940 ± 0.027	0.940 ± 0.028	0.935 ± 0.024	NS
ATIII (%)	94.9 ± 17.2	96.0 ± 17.3	83.9 ± 13.4	0.036
Intraoperative bleeding (mL)	481.2 ± 468.5	455.8 ± 472.4	675.0 ± 430.0	NS
Operative time (min)	404.5 ± 135.2	390.8 ± 129.3	525.9 ± 140.9	0.014
Sex (male:female)	49:37	44:34	5:3	NS
Background (HCC: meta or CCC)	57:29	49:29	8:0	0.047
Hr (0/S:1:2/3)	53:17:16	49:16:13	4:1:3	NS
Sapporo score	13.2 ± 2.4	13.4 ± 2.5	11.0 ± 3.2	0.037
MELD score	7.6 ± 1.6	7.6 ± 1.7	7.8 ± 0.7	0.103
Child-Pugh score	3.2 ± 0.4	3.2 ± 0.4	3.4 ± 0.5	0.119
Total liver volume (cc)	1137.8 ± 222.9	1136.2 ± 228.5	1153.5 ± 221.4	NS
Reduction in liver volume (%)	19.0 ± 13.0	17.6 ± 12.1	32.8 ± 15.0	0.006
Residual liver volume (%)	85.1 ± 14.4	86.0 ± 13.7	75.4 ± 17.9	0.039

Continuous variables are expressed as the mean and standard deviation. BSA: Body surface area; PT-INR: Prothrombin time-international normalized ratio; ICG15: Indocyanine green retention rate at 15 min; ATIII: Serum anti-thrombin III level; HCC: Hepatocellular carcinoma; meta: Metastatic tumor; CCC: Cholangiocellular carcinoma; Hr: Hepatic resection; HH15: Uptake ratio of the heart at 15 min to that seen at 3 min on 99m Tc-galactosyl human serum albumin scintigraphy (GSA); LHL15: The uptake ratio of the liver to the liver plus heart at 15 min on GSA; MELD: Model For End-Stage Liver Disease; NS: Not significant.

Table 2 Sapporo scores for liver resection of malignant tumors

Factors	Scores
	4	3	2	1
ICGR15 (%)	≤ 10	10-19	20-29	≥ 30
ATIII (%)	≥ 90	80-89	70-79	≤ 69
HH15	≤ 0.55	0.56-0.59	0.60-0.64	≥ 0.65
LHL15	≥ 0.95	0.90-0.94	0.85-0.89	≤ 0.84

The total number of points was calculated as the sum of the scores for the ICGR15, serum ATIII level, HH15, and LHL15. Hr 2 or Hr 3: 16 points, Hr: 1 ≥ 12 points, Hr S: ≥ 8 points, Hr 0: ≤ 7 points. ICG15: Indocyanine green retention rate at 15 min; ATIII: Serum anti-thrombin III level; HH15: Uptake ratio of the heart at 15 min to that seen at 3 min on 99m Tc-galactosyl human serum albumin scintigraphy (GSA); LHL15: The uptake ratio of the liver to the liver plus heart at 15 min on GSA.

Table 3 Formulae for the calculation of standard liver volume based on height and weight

	Authors	Journals	Formulae	ICC
Height and weight	Ogiu et al[22]	Health Phys, 1997	LV = 576.9 × H + 8.9 × BW – 159.7 (males); LV = 674.3 × H + 6.5 × BW – 214.5 (females)	0.73
	Lin et al[23]	Hepatogastroenterology, 1998	LV = 133 × H + 12 × BW – 1530	0.78
	Yu et al[24]	Liver Transpl, 2004	LV = 21.585 × BW0.7322 × H0.225	0.77
	Chandramohan et al[25]	Indian J Gastroenterol, 2007	LV = 18.51 × BW + 191.80	0.77
	Fu-Gui et al[26]	Transplant Proc, 2009	LV = 11.508 × BW + 334.024	0.71
	Poovathumkadavil et al[27]	Transplant Proc, 2010	LV = 12.26 × BW + 555.65	0.72
	Herden et al[28]	Transpl Int, 2013	LV = −143.062973 + 4.274603051 × H + 14.78817631 × BW (Age: 0-1); LV = −20.2472281 + 3.339056437 × H + 13.11312561 × BW (Age: 1-16)	0.76

ICC: Intraclass correlation coefficient; LV: Liver volume; BW: Body weight; H: Height.

Table 4 Formulae for the calculation of standard liver volume based on body surface area

	Authors	Journals	Formulae	ICC
BSA	DeLand et al[29]	Radiology, 1968	LV = 1020 × BSA – 220	0.77
	Urata et al[30]	Hepatology, 1995	LV = 706.2 × BSA + 2.4	0.71
	Murry et al[31]	Drug Metab Dispos, 1995	LV = 710 × BSA	0.71
	Heinemann et al[32]	Liver Transpl Surg, 1999	LV = 1072.8 × BSA – 345.7	0.78
	Vauthey et al[33]	Liver Transpl, 2002	LV = 1267.28 × BSA – 794.41	0.78
	Yoshizumi et al[34]	Transplant Proc, 2003	LV = 772 × BSA	0.74
	Yu et al[24]	Liver Transpl, 2004	LV = 1145.4 × BSA − 506.1 (adults)	0.78
	Hashimoto et al[35]	J Gastroenterol Hepatol, 2006	LV = 961.3 × BSA – 404.8	0.77
	Chandramohan et al[25]	Indian J Gastroenterol, 2007	LV = 1267.28 × BSA – 794.41	0.78
	Saeki et al[36]	Pediatr Transplant, 2012	LV = 689.9 × BSA − 24.7	0.70
	Our study		LV = 822.7 × BSA – 183.2	0.74

ICC: Intraclass correlation coefficient; LV: Liver volume; BSA: Body surface area.

Table 5 Formulae for the calculation of standard liver volume based on age, gender, or radiological findings

	Authors	Journals	Formulae	ICC
Others	Takahashi et al[37]	Clin Pharmacol Ther, 2000	LV = 15 × (4.6 × Age + 19.8), Age: 1-18; LV = 15 × (0.31 × Age + 97.8), Age: 30-40; LV = 15 × (–0.91 × Age + 149), Age: ≥ 41	0.39
	Kanamori et al[38]	Int J Clin Pharmacol Ther, 2002	LV = 67.3 × Age + 229.8	−0.39
	Choukèr et al[39]	Liver Transpl, 2004	LV=452 + 16.34 × BW + 11.85 × Age – 166 × Gender (Age: 16–50, M: 0, F: 1); LV=1390 + 15.94 × BW – 12.86 × Age (Age: 51–70)	0.79
	Chan et al[40]	World J Gastroenterol, 2006	LV = 218 + BW × 12.3 + Gender × 51 (F: 0, M: 1)	0.74
	Yuan et al[41]	Transplant Proc, 2008	LV = 949.7 × BSA − 48.3 × Age − 247.4 (Age: 1: < 40, 2: 41–60, 3: > 60)	0.77
	Kokudo et al[42]	J Hepatol, 2015	LV = 203.3 − 3.61 × Age + 58.7 × Thoracic width − 463.7 × Race (Asian: 1, Caucasian: 0)	0.66
	Ma et al[43]	Liver Transpl, 2017	LV = (2 × Depth) + (10 × BW) + 190	0.75

ICC: Intraclass correlation coefficient; LV: Liver volume; BSA: Body surface area; BW: Body weight; F: Female; M: Male.

Table 6 Characteristics of the patients and simple standard liver volume formulae based on a mean body surface area of 1.61

Authors	Mean age ± SD (range)	BSA	Simple formulae (tentative mean BSA = 1.61)	ICC	Clusters
DeLand et al[29]	ND	ND	LV = 883 × BSA	0.75	B
Urata et al[30]	11.1 ± 8.8	1.078 ± 0.528 (0.248–1.935)	LV = 707 × BSA	0.71	A
Murry et al[31]	9.7 (3.3–18.8)	Median: 1.37 (0.57–2.0)	LV = 710 × BSA	0.71	A
Heinemann et al[32]	50.6±18.9	ND	LV = 858 × BSA	0.75	B
Vauthey et al[33]	Mean: 54, Median: 56 (14-90)	Median: 1.82 (1.32–2.90)	LV = 770 × BSA	0.74	B
Yoshizumi et al[34]	38.6 ± 20.6 (0–87) for males; 47.0 ± 19.7 (0–85) for females	1.86 ± 0.36 (0.24-2.88); 1.68 ± 0.28 (0.28-2.38)	LV = 772 × BSA	0.74	B
Yu et al[24]	42.4 ± 16.5	1.65 ± 0.26	LV = 831 × BSA	0.74	B
Hashimoto et al[35]	(17-66)	1.67 ± 0.18 (1.25-2.56)	LV = 710 × BSA	0.71	A
Chandramohan et al[25]	46.5 (10-70)	Median: 1.60 (0.88-2.25)	LV = 774 × BSA	0.73	B
Saeki et al[36]	5.8 (0 d-15)	ND	LV = 675 × BSA	0.70	A
Our study	67.0 ± 10.3	1.61 ± 0.18	LV = 709 × BSA	0.71	A

ICC: Intraclass correlation coefficient; BSA: Body surface area; ND: Not describe; LV: Liver volume.

Table 7 Minimum residual liver volume based on various functional assessments

Authors	Publications	Functional assessments	Minimum residual LV			Mortality
			NL	CH, liver injury	LC
Shirabe et al[49]	J Am Coll Surg, 1999	Pathology (HCC, HB, or HC)	250 mL/m2 (40%)			8.8% (180 d)
Shoup et al[50]	J Gastrointest Surg, 2003	Pathology (NL, CRC metastasis alone)	25%	-	-	ND
Schindl et al[51]	Gut, 2005	Pathology (NL, 99% metastasis)	26.6%	-	-	ND
Ferrero et al[17]	World J Surg, 2007	Pathology (NL, liver injury)	26.5%	31%	-	0.8% (60 d)
van den Esschert et al[52]	J Gastrointest Surg, 2009	Pathology (CH, LC)	-	40%	50%	ND
Kishi et al[53]	Ann Surg, 2009	Pathology (NL)	20%	-	-	2.0% (30 d) 4.7% (60 d) 6.0% (90 d)
Suda et al[54]	Am J Surg, 2009	Pathology (NL, HCCa, GBCa, ICCa)	40%	-	-	8.1% (ND)
Vauthey et al[55]	HPB, 2010	Pathology (NL, liver injury, LC)	20%	30%	40%	ND
Gulielmi et al[56]	Dig Surg, 2012	Pathology (NL, steatosis, LC)	20%	30%	40%	ND
Hwang et al[16]	J Gastrointest Surg, 2015	Pathology (CH, LC)	-	35%	30%	0.8% (90 d)
Ribero et al[57]	J Am Coll Surg, 2016	Pathology (NL, HCCa alone)	30%	-	-	11% (90 d)
Our series	Hepatogastroenterolo-gy (in press)	ATIII, ICG15, GSA	35%-95%			2.3% (90 d)

LV: Liver volume; NL: Normal liver; CH: Chronic hepatitis; LC: Liver cirrhosis; HCC: Hepatocellular carcinoma; GBCa: Gallbladder cancer; ICCa: Intrahepatic cholangiocellular carcinoma; HCCa: Hilar cholangiocellular carcinoma; ATIII: Anti-thrombin III; ICG15: Indocyanine green retention rate at 15 min; GSA: 99m Tc-galactosyl human serum albumin scintigraphy; ND: Not describe.