Correlation of hepatitis B surface antigen expression with clinicopathological and biochemical parameters in liver biopsies: A comprehensive study

doi:10.4254/wjh.v14.i1.260

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World Journal of Hepatology

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World J Hepatol. Jan 27, 2022; 14(1): 260-273
Published online Jan 27, 2022. doi: 10.4254/wjh.v14.i1.260

Table 1 Basic clinical, histopathological and immunohistochemical findings according to hepatitis B e antigen status

Parameters	Total	HBeAg positive	HBeAg negative
n	140	86	54
Age (yr)	42.75 ± 11.53	40.30 ± 11.03	46.74 ± 11.29^a
Gender
Male	78	48 (61.5)	30 (38.5)
Female	62	38 (61.3)	24 (38.7)
HBV DNA (log₁₀IU/mL)	7.27 ± 2.17	7.67 ± 2.39	6.65 ± 1.58^a
HBsAg (log₁₀IU/mL)	3.85 ± 1.04	4.01 ± 1.07	3.61 ± 0.94^b
ALT IU/L	7.27 ± 2.17	155.80 ± 114.32	134.54 ± 98.71
ALT < 200 IU/L	91	52 (51.7)	39 (42.9)
ALT ≥ 200 IU/L	49	34 (69.4)	15 (30.6)
INR	1.08 ± 0.21	1.04 ± 0.14	1.15 ± 0.27^b
Platelets (× 10³/μL)	226.4 ± 73.43	224.54 ± 70.67	227.59 ± 75.53
HAI score ≥ 9	61	38 (62.3)	23 (37.7)
HAI score < 9	79	48 (60.8)	31 (39.2)
Fibrosis ≥ 4	53	33 (62.3)	20 (37.7)
Fibrosis < 4	87	53 (60.9)	34 (39.1)
p-HBsAg	41.05 ± 22.78	47.2 ± 13.98	31.26 ± 13.98^a
HBsAg SP1
A	33	17 (51.5)	16 (48.5)
B	24	10 (41.7)	14 (58.3)
C	21	16 (76.2)	5 (23.8)
D	16	10 (62.5)	6 (37.5)
E	46	33 (71.7)	13 (28.3)
HBsAg SP2
Diffuse	59	29 (49.2)	30 (50.8)
Globular	34	24 (70.6)	10 (29.4)
Submembranous	47	33 (70.2)	14 (29.8)
Membranous expression
Present	53	33 (63.3)	20 (37.7)
Absent	87	53 (60.9)	34 (39.1)

Data are presented as mean ± SD, number (%).

^aP < 0.05.

^bP < 0.01.

p-HbsAg: Percentage of hepatitis B surface antigen expression; SP: Staining pattern; ALT: Alanine aminotransferase; INR: International normalized ratio, HAI: Histologic activity index; HBsAg: Hepatitis B surface antigen; HBV: Hepatitis B virus.

Table 2 The correlation of clinicopathologic factors and hepatitis B surface antigen expression patterns with viral replication in hepatitis B e antigen positive cases

	HBV DNA		HAI		Fibrosis
Parameters	< 7.67	≥ 7.67	< 9	≥ 9	< 4	≥ 4
n	32	54	48	38	53	33
Age (yr)	48.28 ± 9.6	35.57 ± 8.93^b	37.79 ± 10.83	43.47 ± 10.59^a	36.06 ± 9.39	47.12 ± 10.11^b
Gender
Male	23 (71.9)	25 (46.3)^a	23 (47.9)	25 (65.8)	27 (50.9)	21 (63.6)
Female	9 (28.1)	29 (53.7)	25 (52.1)	13 (34.2)	26 (49.1)	12 (36.4)
HBV DNA (log₁₀IU/mL)	-	-	8.36 ± 2.26	6.79 ± 2.30^a	8.15 ± 2.32	6.89 ± 2.34
HBsAg (log₁₀IU/mL)	3.02 ± 0.91	4.59 ± 0.64^b	4.28 ± 0.91	3.66 ± 1.61^a	4.19 ± 1.01	3.07 ± 1.10^a
ALT IU/L	106.97 ± 73.55	184.74 ± 124.85^a	148.97 ± 61.46	121.46 ± 50.84	167.74 ± 72.1	136.64 ± 56.2
ALT< 200 IU/L	26 (81.2)	26 (48.1)^a	34 (70.8)	18 (47.4)^a	32 (60.4)	20 (60.6)
ALT ≥ 200 IU/L	6 (18.8)	28 (51.9)	14 (29.2)	20 (52.6)	21 (39.6)	13 (39.4)
INR	1.03 ± 0.08	1.05 ± 0.16	1.03 ± 0.10	1.06 ± 0.17	1.04 ± 0.16	1.04 ± 0.09
Platelets (× 10³/μL)	217.59 ± 66.85	233.98 ± 80.60	226 ± 74.74	228 ± 77.51	224.53 ± 74.72	232.61 ± 77.82
HAI score ≥ 9	22 (68.8)	16 (29.6)^b	-	-	17 (32.1)	21 (63.6)^b
HAI score < 9	10 (31.2)	38 (70.4)	-	-	36 (67.9)	12 (36.4)
Fibrosis ≥ 4	19 (59.4)	14 (25.9)^a	12 (25)	21 (55.3)^b	-	-
Fibrosis < 4	13 (40.6)	40 (74.1)	36 (75)	17 (44.7)	-	-
p-HBsAg	29.92 ± 10.84	57.44 ± 25.50^b	53.53 ± 25.12	39.21 ± 22.85^a	54.49 ± 26.02	35.49 ± 18.34^b
HBsAg SP1
A	2 (6.2)	15 (27.8)^a	11 (22.9	6 (15.8)^a	17 (32.1)	0^b
B	4 (12.5)	6 (11.1)	1 (2.1)	9 (23.7)	6 (11.3)	4 (12.1)
C	6 (18.8)	10 (18.5)	12 (25)	4 (10.5)	14 (26.4)	2 (6.1)
D	4 (12.5)	6 (11.1)	7 (14.6)	3 (7.9)	8 (15.1)	2 (6.1)
E	16 (50)	17 (31.5)	17 (35.4)	16 (42.1)	8 (15.1)	25 (75.8)
HBsAg SP2
Diffuse	8 (25)	21 (38.9)	12 (25)	17 (44.7)^a	23 (43.4)	6 (18.2)^b
Globular	8 (25)	16 (29.6)	19 (39.6)	5 (13.1)	22 (41.5)	2 (6.1)
Submembranous	16 (50)	17 (31.5)	17 (35.4)	16 (42.1)	8 (15.1)	25 (75.8)
Membranous expression
Present	5 (15.6)	28 (51.9)^b	21 (43.8)	12 (31.6)	29 (54.7)	4 (12.1)^b
Absent	27 (84.4)	26 (48.1)	27 (56.3)	26 (68.4)	24 (45.3)	29 (87.9)

Data are presented as mean ± SD, number (%).

^aP < 0.05.

^bP < 0.01.

p-HbsAg: Percentage of hepatitis B surface antigen expression; SP: Staining pattern; ALT: Alanine aminotransferase; INR: International normalized ratio; HAI: Histologic activity index; HBsAg: Hepatitis B surface antigen; HBV: Hepatitis B virus.

Table 3 The correlation of clinicopathologic factors and hepatitis B surface antigen expression patterns with viral replication in hepatitis B e antigen negative cases

	HBV DNA		HAI		Fibrosis
Parameters	< 6.65	≥ 6.65	< 9	≥ 9	< 4	≥ 4
n	23	31	31	23	34	20
Age (yr)	48.13 ± 10.34	45.71 ± 12.02	46.52 ± 11.73	47.04 ± 10.92	45.82 ± 11.63	48.30 ± 10.81
Gender
Male	10 (43.5)	20 (64.5)	19 (61.3)	11 (47.8)	23 (67.6)	7 (35)^a
Female	13 (56.5)	11 (35.5)	12 (38.7)	12 (52.2)	11 (32.4)	13 (65)
HBV DNA (log₁₀IU/mL)	-	-	4.97 ± 1.49	7.56 ± 1.21^a	4.16 ± 0.97	3.98 ± 0.93
HBsAg (log₁₀IU/mL)	3.19 ± 0.84	3.92 ± 0.90	3.30 ± 0.8	3.86 ± 0.91^a	3.46 ± 0.95	4.03 ± 0.98
ALT IU/L	96.09 ± 33.55	163.06 ± 50.85^a	102.55 ± 41.36	177.65 ± 80.65	126.18 ± 64.87	148.75 ± 58.6
ALT < 200 IU/L	21 (91.3)	18 (58.1)^b	26 (83.9)	13 (56.5)^a	25 (73.5)	14 (70)
ALT ≥ 200 IU/L	2 (8.7)	13 (41.9)	5 (16.1)	10 (43.5)	9 (26.5)	6 (30)
INR	1.13 ± 0.27	1.17 ± 0.28	1.15 ± 0.3	1.16 ± 0.24	1.22 ± 0.32	1.04 ± 0.10^b
Platelets (× 10³/μL)	234.91 ± 80.6	216.31 ± 61.29	237.67 ± 73.34	206.64 ± 73.34	218.21 ± 71.85	236.5 ± 68.79
HAI score ≥ 9	2 (8.7)	21 (67.7)^b	-	-	14 (26.5)	9 (70)^b
HAI score < 9	21 (91.3)	10 (32.3)	-	-	20 (73.5)	11 (30)
Fibrosis ≥ 4	4 (17.4)	16 (51.6)^a	6 (19.4)	14 (60.9)^b	-	-
Fibrosis < 4	19 (82.6)	15 (48.4)	25 (80.6)	9 (39.1)	-	-
p-HBsAg	30.39 ± 14.18	31.91 ± 14.04	28.68 ± 11.16	34.75 ± 16.71	33.21 ± 15.32	27.96 ± 10.93
HBsAg SP1
A	6 (26.1)	10 (32.3)	13 (41.9)	3 (13)^a	13 (38.2)	3 (15)
B	5 (21.7)	9 (29)	5 (16.1)	9 (39.1)	7 (20.6)	7 (35)
C	4 (17.4)	1 (3.2)	4 (12.9)	1 (4.3)	5 (14.7)	0
D	5 (21.7)	1 (3.2)	5 (16.1)	1 (4.3)	3 (8.8)	3 (15)
E	3 (13)	10 (32.3)	4 (12.9)	9 (39.1)	6 (17.6)	7 (35)
HBsAg SP2
Diffuse	11(47.8)	19 (61.3)^b	18 (58.1)	12 (52.2)^a	20 (58.8)	10 (50)
Globular	9 (39.1)	2 (3.2)	9 (29)	1 (4.3)	7 (20.6)	3 (15)
Submembranous	3 (13.1)	10 (31.5)	4 (12.9)	10 (43.5)	7 (20.6)	7 (35)
Membranous expression
Present	7 (30.4)	13 (41.9)	10 (32.3)	10 (43.5)	14 (41.2)	6 (30)
Absent	16 (69.6)	18 (58.1)	21 (67.7)	13 (56.5)	20 (58.8)	14 (70)

Data are presented as mean ± SD, number (%).

^aP < 0.05.

^bP < 0.01.

Table 4 The relationship between clinicopathological factors and hepatitis B surface antigen expression patterns with viral response and serological response

	HBeAg positive				HBeAg negative
	VR		SR		VR
Parameters	Absent	Present	Absent	Present	Present
Age (yr)
< Mean	11 (34.4)	39 (72.2)^b	19 (48.7)	31 (66)^b	24 (44.4)
≥ Mean	21 (65.6)	15 (27.8)	20 (51.43)	16 (34)	30 (55.6)
Gender
Male	21 (34.4)	27 (50)	24 (61.5)	24 (48.9)	30 (55.6)
Female	11 (34.4)	27 (50)	15 (38.5)	23 (51.1)	24 (44.4)
HBV DNA
Low	17 (53.1)	39 (72.2)^a	16 (41)	16 (34)	23 (42.6)
High	15 (45.9)	15 (27.8)	23 (59)	31 (66)	31 (57.4)
HBsAg
Low	21 (65.6)	15 (27.8)^a	21 (53.8)	15 (31.9)^b	30 (55.6)
High	11 (34.4)	39 (72.2)	18 (46.2)	32 (68.1)	24 (44.4)
ALT
< 200 IU/L	23 (71.9)	29 (53.7)	29 (74.4)	23 (48.9)^a	39 (72.2)
≥ 200 IU/L	9 (28.1)	25 (46.3)	10 (25.6)	24 (51.1)	15 (27.8)
INR
Low	15 (46.9)	26 (48.1)	19 (48.7)	22 (46.8)	39 (72.2)
High	17 (53.1)	28 (51.9)	20 (51.3)	25 (53.2)	15 (27.8)
Platelets
Low	15 (46.9)	31 (57.4)	20 (51.3)	26 (55.3)	31 (57.4)
High	17 (53.1	23 (42.6)	19 (48.7)	21 (44.7)	23 (42.6)
HAI score ≥ 9	13 (40.6)	25 (46.3)	11 (25)	28 (59.6)^a	23 (42.6)
HAI score < 9	19 (59.4)	29 (53.7)	28 (75)	19 (40.4)	31 (57.4)
Fibrosis ≥ 4	17 (53.1)	16 (29.6)^a	17 (43.6)	16 (34)	20 (37)
Fibrosis < 4	15 (46.9)	10 (70.4)	22 (56.4)	31 (66)	34 (63)
p-HbsAg
Low	26 (81.3)	25 (46.3)^b	29 (74.4)	24 (51.1)^b	21 (38.9)
High	6 (18.8)	29 (53.7)	10 (25.6)	23 (48.9)	33 (61.1)
HBsAg SP1
A	1 (3.1)	16 (29.6)^b	2 (5.1)	15 (31.9)^b	16 (29.6)
B	0	10 (18.5)	0	10 (21.3)	14 (25.9)
C	6 (18.8)	10 (18.5)	11 (28.2)	5 (10.6)	5 (9.3)
D	6 (18.8)	4 (7.4)	6 (15.4)	4 (8.5)	6 (11.1)
E	19 (59.4)	14 (25.9)	20 (51.3)	13 (27.7)	13 (24.1)
HBsAg SP2
Diffuse	1 (3.1)	28 (58.1)^b	2 (5.1)	2 (57.4)^b	30 (55.6)
Globular	12 (37.5)	12 (22.2)	17 (43.6)	7 (14.9)	10 (18.5)
Submembranous	19 (59.4)	14 (25.9)	20 (51.3)	13 (27.7)	14 (25.9)
Membranous expression
Absent	27 (84.4)	26 (48.1)^b	29 (74.4)	24 (51.1)^b	21 (38.9)
Present	5 (15.6)	28 (51.9)	10 (25.6)	23 (48.9)	33 (61.1)

^aP < 0.05.

^bP < 0.01.

VR: Viral response; SR: Serological response; p-HbsAg: Percentage of hepatitis B surface antigen expression; SP: Staining pattern; ALT: Alanine aminotransferase; INR: International normalized ratio; HAI: Histologic activity index; HBsAg: Hepatitis B surface antigen; HBeAg: Hepatitis B e antigen; HBV: Hepatitis B virus.

Table 5 The association of clinicopathological factors and hepatitis B surface antigen expression patterns with viral response and serological response

	HBeAg positive (n = 86)							HBeAg negative (n = 54)
Parameters	VR			SR				VR
	HR (95%CI)	P value¹	P value²		HR (95%CI)	P value¹	P value²	HR (95%CI)	P value²
Age (yr)	0.685 (0.228-2.055)	0.001	0.449		0.892 (0.301-2.644)	0.007	0.837	0.936 (0.460-1.904)	0.855
Gender: male vs female	0.581 (0.301-1.121)	0.72	0.105		0.516 (0.251-1.062)	0.79	0.072	2.410 (0.986-5.985)	0.054
HBV DNA (log₁₀IU/mL)	0.782 (0.275-2.224)	0.003	0.645		0.707 (0.246-2.029)	0.40	0.519	0.620 (0.255-1.508)	0.292
HBsAg (log₁₀IU/mL)	1.931 (0.757-4.923)	0.001	0.168		2.252 (0.878-5.773)	0.001	0.091	0.700 (0.294-1.669)	0.422
ALT ≥ 200 IU/L vs < 200 IU/L	0.992 (0.476-2.068)	0.90	0.982		1.037 (0.436-2.471)	0.018	0.934	0.854 (0.372-1.962)	0.710
INR	0.539 (0.271-1.072)	0.751	0.078		0.493 (0.222-1.092)	0.901	0.081	1.815 (0.791-4.161)	0.159
Platelets (× 10³/μL)	0.619 (0.309-1.240)	0.194	0.176		0.538 (0.243-1.189)	0.389	0.125	0.925 (0.452-1.892)	0.831
HAI score ≥ 9 vs < 9	1.566 (0.692-3.546)	0.282	0.282		2.881 (1.170-7.094)	0.132	0.021	6.876 (2.219-21.309)	0.001
Fibrosis ≥ 4 vs < 4	1.245 (0.517-2.999)	0.021	0.625		1.079 (0.427-2.730)	0.092	0.872	0.833 (0.326-2.125)	0.702
p-HBsAg	3.178 (1.582-6.387)	0.001	0.001		3.990 (1.843-8.638)	0.001	0.001	1.089 (0.575-2.063)	0.793
SP1	0.899 (0.495-1.634)	0.001	0.727		3.760 (1.742-7.861)	0.001	0.531	0.959 (0.443-2.167)	0.990
SP2	0.727 (0.240-2.200)	0.001	0.573		0.721 (0.216-2.410)	0.001	0.595	0.996 (0.552-1.798)	0.990
Membranous expression	1.085 (0.513-2.294)	0.001	0.831		1.082 (0.472-2.482)	0.001	0.952	0.692 (0.246-1.944)	0.485

¹Univariate analysis.

²Cox regression analysis.

VR: Viral response; SR: Serological response; HR: Hazard ratio; CI: Confidence interval; p-HbsAg: Percentage of hepatitis B surface antigen expression; SP: Staining pattern; ALT: Alanine aminotransferase; INR: International normalized ratio; HAI: histologic activity index; HBsAg: Hepatitis B surface antigen; HBeAg: Hepatitis B e antigen.

Citation: Alpsoy A, Adanir H, Bayramoglu Z, Elpek GO. Correlation of hepatitis B surface antigen expression with clinicopathological and biochemical parameters in liver biopsies: A comprehensive study. World J Hepatol 2022; 14(1): 260-273
URL: https://www.wjgnet.com/1948-5182/full/v14/i1/260.htm
DOI: https://dx.doi.org/10.4254/wjh.v14.i1.260