Clinical characteristics and risk factors of COVID-19 patients with chronic hepatitis B: a multi-center retrospective cohort study

doi:10.1007/s11684-021-0854-5

Frontiers of Medicine

2022, Vol. 16

Issue (1): 111-125 https://doi.org/10.1007/s11684-021-0854-5

本期目录

Clinical characteristics and risk factors of COVID-19 patients with chronic hepatitis B: a multi-center retrospective cohort study

Jing Wang¹, Zequn Lu², Meng Jin³, Ying Wang⁴, Kunming Tian^5,⁶, Jun Xiao¹, Yimin Cai², Yanan Wang¹, Xu Zhang⁷, Tao Chen⁸, Zhi Yao⁹, Chunguang Yang¹, Renli Deng¹⁰, Qiang Zhong¹¹, Xiongbo Deng¹², Xin Chen¹³, Xiang-ping Yang¹⁴, Gonghong Wei¹⁵, Zhihua Wang¹(

), Jianbo Tian²(

), Xiao-ping Chen¹⁶(

)

¹. Department of Urology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
². Department of Epidemiology and Biostatistics, Key Laboratory for Environment and Health, School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
³. Department of Respiratory and Critical Care Medicine, Renmin Hospital of Wuhan University, Wuhan 430060, China
⁴. Department of Virology, Wuhan Centers for Disease Prevention and Control, Wuhan 430024, China
⁵. Institute of Reproductive Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
⁶. School of Nursing, Zunyi Medical University, Zunyi 563099, China
⁷. Key Laboratory of Environment and Health, Ministry of Education & Ministry of Environmental Protection, and State Key Laboratory of Environmental Health (Incubating), School of Public Health, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
⁸. Department and Institute of Infectious Disease, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
⁹. Department of Respirology and Tuberculosis Specialty, Wuhan Pulmonary Hospital, Wuhan 430030, China
¹⁰. The Fifth Affiliated (Zhuhai) Hospital of Zunyi Medical University, Zhuhai 519199, China
¹¹. Department of Critical Care Medicine, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
¹². Department of Radiology, Wuhan Jinyintan Hospital, Wuhan 430048, China
¹³. Department of Oncology, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
¹⁴. Department of Immunology, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China
¹⁵. Biocenter Oulu, Faculty of Biochemistry and Molecular Medicine, University of Oulu, Oulu 90014, Finland
¹⁶. Hepatic Surgery Center, Tongji Hospital, Tongji Medical College, Huazhong University of Science and Technology, Wuhan 430030, China

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Abstract：

The coronavirus disease 2019 (COVID-19) has spread globally. Although mixed liver impairment has been reported in COVID-19 patients, the association of liver injury caused by specific subtype especially chronic hepatitis B (CHB) with COVID-19 has not been elucidated. In this multi-center, retrospective, and observational cohort study, 109 CHB and 327 non-CHB patients with COVID-19 were propensity score matched at an approximate ratio of 3:1 on the basis of age, sex, and comorbidities. Demographic characteristics, laboratory examinations, disease severity, and clinical outcomes were compared. Furthermore, univariable and multivariable logistic and Cox regression models were used to explore the risk factors for disease severity and mortality, respectively. A higher proportion of CHB patients (30 of 109 (27.52%)) developed into severe status than non-CHB patients (17 of 327 (5.20%)). In addition to previously reported liver impairment markers, such as alanine aminotransferase, aspartate aminotransferase, alkaline phosphatase, and total bilirubin, we identified several novel risk factors including elevated lactate dehydrogenase (≥245 U/L, hazard ratio (HR) = 8.639, 95% confidence interval (CI) = 2.528–29.523; P <0.001) and coagulation-related biomarker D-dimer (≥0.5 μg/mL, HR= 4.321, 95% CI= 1.443–12.939; P = 0.009) and decreased albumin (<35 g/L, HR= 0.131, 95% CI= 0.048–0.361; P <0.001) and albumin/globulin ratio (<1.5, HR= 0.123, 95% CI= 0.017–0.918; P = 0.041). In conclusion, COVID-19 patients with CHB were more likely to develop into severe illness and die. The risk factors that we identified may be helpful for early clinical surveillance of critical progression.

Key words： COVID-19 chronic hepatitis B liver injury coagulation dysfunction

收稿日期: 2020-11-22 出版日期: 2022-03-28

Corresponding Author(s): Zhihua Wang,Jianbo Tian,Xiao-ping Chen

引用本文:

. [J]. Frontiers of Medicine, 2022, 16(1): 111-125.
Jing Wang, Zequn Lu, Meng Jin, Ying Wang, Kunming Tian, Jun Xiao, Yimin Cai, Yanan Wang, Xu Zhang, Tao Chen, Zhi Yao, Chunguang Yang, Renli Deng, Qiang Zhong, Xiongbo Deng, Xin Chen, Xiang-ping Yang, Gonghong Wei, Zhihua Wang, Jianbo Tian, Xiao-ping Chen. Clinical characteristics and risk factors of COVID-19 patients with chronic hepatitis B: a multi-center retrospective cohort study. Front. Med., 2022, 16(1): 111-125.

链接本文:

https://academic.hep.com.cn/fmd/CN/10.1007/s11684-021-0854-5
https://academic.hep.com.cn/fmd/CN/Y2022/V16/I1/111

Fig.1

Variables	Total	CHB		Non-CHB		P value
Variables	N = 436	N = 109		N = 327		P value
Characteristics	N = 436		N = 109		N = 327
Age, year, M (IQR)	57.00 (43.00–66.00)	N = 109	55.00 (44.00–64.50)	N = 327	57.00 (43.00–66.00)	0.669
Sex, n (%)						0.144
Male	258 (59.17)		71 (65.14)		187 (57.19)
Female	178 (40.83)		38 (34.86)		140 (42.81)
Comorbidities, n (%)	N = 436		N = 109		N = 327
Hypertension	89 (20.41)		19 (17.43)		70 (21.41)	0.373
Diabetes	56 (12.84)		13 (11.93)		43 (13.15)	0.741
Coronary heart disease	30 (6.88)		7 (6.42)		23 (7.03)	0.827
Cerebral infarction	10 (2.29)		4 (3.67)		6 (1.83)	0.276^a
Pulmonary tuberculosis	6 (1.38)		1 (0.92)		5 (1.53)	1.000^a
Laboratory examinations
Blood routine, M (IQR)
Leukocytes, # (N = 434), × 10⁹/L	5.46 (4.28–7.22)	N = 107	6.15 (4.75–8.63)	N = 327	5.24 (4.23–6.67)	<0.001*
Erythrocytes, # (N = 434), × 10¹²/L	4.10 (3.71–4.50)	N = 107	4.10 (3.62–4.55)	N = 327	4.10 (3.71–4.48)	0.768
Monocytes, # (N = 429), × 10⁹/L	0.47 (0.36–0.62)	N = 102	0.48 (0.35–0.70)	N = 327	0.47 (0.36–0.62)	0.423
Neutrophils, # (N = 434), × 10⁹/L	3.40 (2.41–4.81)	N = 107	4.26 (2.92–7.98)	N = 327	3.25 (2.31–4.24)	<0.001*
Eosinophils, # (N = 429), × 10⁹/L	0.06 (0.02–0.13)	N = 102	0.08 (0.02–0.21)	N = 327	0.06 (0.01–0.11)	0.003*
Basophils, # (N = 429), × 10⁹/L	0.01 (0.01–0.03)	N = 102	0.02 (0.01–0.03)	N = 327	0.01 (0.01–0.03)	0.087
Immune cell subsets, M (IQR)
Lymphocytes, # (N = 436), × 10⁹/L	1.35 (0.97–1.81)	N = 109	1.24 (0.80–1.56)	N = 327	1.42 (1.00–1.84)	<0.001*
CD3⁺CD19^- T cells, # (N = 112), /μL	846.67 (617.07–1279.75)	N = 35	552.80 (309.48–718.07)	N = 77	1112.00 (781.50–1352.00)	<0.001*
CD4⁺ T cells, # (N = 112), /μL	483.00 (350.03–806.50)	N = 35	481.00 (236.00–644.87)	N = 77	564.00 (353.97–946.00)	0.001*
CD8⁺ T cells, # (N = 112), /μL	352.50 (231.75–471.25)	N = 35	345.00 (135.29–492.90)	N = 77	353.00 (258.00–456.00)	0.366
CD3^-CD19⁺ B cells, # (N = 97), /μL	181.00 (124.00–284.50)	N = 20	129.50 (83.75–173.25)	N = 77	207.00 (127.00–301.00)	0.001*
CD3^-CD16⁺CD56⁺ NK cells, # (N = 97), /μL	174.00 (115.00–274.00)	N = 20	150.50 (90.25–221.75)	N = 77	181.00 (122.00–276.00)	0.256
T cells+ B cells+ NK cells, # (N = 97), /μL	1386.00 (936.50–1902.00)	N = 20	792.04 (652.17–1103.02)	N = 77	1580.00 (1161.50–1958.00)	<0.001*
Inflammatory cytokines and biomarkers, M (IQR)
IL-6 (N = 352), pg/mL	3.59 (1.50–11.36)	N = 69	9.92 (2.83–25.60)	N = 283	3.08 (1.50–7.93)	<0.001*
IL-10 (N = 337), pg/mL	5.20 (5.00–7.50)	N = 58	5.00 (5.00–6.88)	N = 279	5.30 (5.00–7.50)	0.373
IL-8 (N = 337), pg/mL	12.40 (6.50–24.10)	N = 58	12.80 (7.15–25.68)	N = 279	12.20 (6.40–23.90)	0.292
TNF-α (N = 342), pg/mL	7.30 (5.30–9.33)	N = 58	9.15 (7.30–13.08)	N = 284	7.00 (5.03–8.98)	<0.001*
IL-1β (N = 337), pg/mL	5.00 (5.00–5.00)	N = 58	5.00 (5.00–5.53)	N = 279	5.00 (5.00–5.00)	0.075
IL-2R (N = 334), U/mL	497.00 (351.00–673.25)	N = 58	509.00 (334.50–776.50)	N = 276	495.50 (354.25–657.50)	0.401
Ferritin (N = 225), μg/L	368.90 (181.00–609.70)	N = 44	470.05 (173.05–1162.50)	N = 181	349.80 (183.10–582.50)	0.051
hs-CRP (N = 416), mg/L	4.50 (1.10–29.88)	N = 94	19.25 (2.18–62.73)	N = 322	3.70 (1.00–15.10)	<0.001*
Organ damage indexes, M (IQR)
ALT (N = 435), U/L	19.00 (14.00–30.00)	N = 108	31.00 (19.00–72.25)	N = 327	18.00 (13.00–25.00)	<0.001*
AST (N = 435), U/L	22.00 (18.00–33.00)	N = 108	35.50 (21.25–64.25)	N = 327	21.00 (17.00–28.00)	<0.001*
TBIL (N = 435), μmol/L	8.70 (6.50–12.10)	N = 108	10.25 (7.65–15.63)	N = 327	8.20 (6.30–11.30)	<0.001*
DBIL (N = 431), μmol/L	3.40 (2.60–4.40)	N = 104	3.60 (2.90–5.93)	N = 327	3.30 (2.60–4.30)	0.003*
ALB (N = 433), g/L	38.50 (34.95–41.75)	N = 106	33.95 (29.28–38.55)	N = 327	39.40 (36.70–42.20)	<0.001*
GLO (N = 433), g/L	29.10 (25.70–31.60)	N = 106	27.55 (24.68–30.33)	N = 327	29.40 (26.10–31.90)	0.002*
TP (N = 433), g/L	67.80 (63.50–71.70)	N = 106	61.55 (55.88–65.63)	N = 327	69.30 (65.90–72.70)	<0.001*
ALB/GLO (N = 433)	1.33 (1.15–1.57)	N = 106	1.23 (1.03–1.50)	N = 327	1.35 (1.19–1.57)	<0.001*
LDH (N = 400), U/L	217.00 (180.00–265.50)	N = 105	238.00 (175.00–319.00)	N = 295	211.00 (180.00–251.00)	0.019*
ALP (N = 400), U/L	64.00 (48.00–87.00)	N = 104	68.00 (53.25–88.50)	N = 296	62.50 (46.00–84.75)	0.049*
CK-MB (N = 303), U/L	0.70 (0.40–1.20)	N = 72	1.10 (0.58–9.15)	N = 231	0.70 (0.40–1.00)	<0.001*
PT (N = 432), s	13.60 (13.10–14.20)	N = 105	14.40 (13.55–16.50)	N = 327	13.50 (13.00–14.00)	<0.001*
APTT (N = 428), s	37.90 (35.60–40.30)	N = 101	38.10 (34.70–41.40)	N = 327	37.90 (35.70–40.00)	0.512
D-dimer (N = 431), μg/mL	0.42 (0.24–0.90)	N = 104	0.95 (0.32–2.64)	N = 327	0.36 (0.23–0.62)	<0.001*
Complication, n (%)	N = 436		N = 109		N = 327	0.026*^,a
DIC	8 (1.83)		5 (4.59)		3 (0.92)
Non-DIC	428 (98.17)		104 (95.41)		324 (99.08)
Severity, n (%)	N = 436		N = 109		N = 327	<0.001*
Severe	72 (16.51)		30 (27.52)		42 (12.84)
Non-severe	364 (83.49)		79 (72.48)		285 (87.16)
Outcomes, n (%)	N = 436		N = 109		N = 327	<0.001*
Survivor	415 (95.18)		96 (88.07)		319 (97.55)
Non-survivor	21 (4.82)		13 (11.93)		8 (2.45)

Tab.1

Variables	Total	Severe		Non-severe		P value
Variables	N = 109	N = 30		N = 79
Characteristics	N = 109		N = 30		N = 79
Age, year, M (IQR)	55.00 (44.00–64.50)	N = 30	58.50 (49.25–62.75)	N = 79	54.00 (42.00–65.00)	0.461
Sex, n (%)						0.269
Male	71 (65.14)		22 (73.33)		49 (62.03)
Female	38 (34.86)		8 (26.67)		30 (37.97)
Comorbidities, n (%)	N = 109		N = 30		N = 79
Hypertension	19 (17.43)		5 (16.67)		14 (17.72)	0.897
Diabetes	13 (11.93)		7 (23.33)		6 (7.59)	0.042*^{, a}
Coronary heart disease	7 (6.42)		3 (10.00)		4 (5.06)	0.391^a
Cerebral infarction	4 (3.67)		1 (3.33)		3 (3.80)	1.000^a
Pulmonary tuberculosis	1 (0.92)		1 (3.33)		0 (0.00)	0.275^a
Laboratory examinations
Blood routine, M (IQR)
Leukocytes, # (N = 107), × 10⁹/L	6.15 (4.75–8.63)	N = 28	7.48 (5.09–8.97)	N = 79	6.09 (4.72–8.46)	0.436
Erythrocytes, # (N = 107), × 10¹²/L	4.10 (3.62–4.55)	N = 28	4.02 (2.74–4.31)	N = 79	4.15 (3.80–4.55)	0.085
Monocytes, # (N = 102), × 10⁹/L	0.48 (0.35–0.70)	N = 25	0.58 (0.40–0.71)	N = 77	0.46 (0.35–0.63)	0.581
Neutrophils, # (N = 107), × 10⁹/L	4.26 (2.92–7.98)	N = 28	6.18 (4.08–11.37)	N = 79	4.01 (2.66–6.67)	0.001*
Eosinophils, # (N = 102), × 10⁹/L	0.08 (0.02–0.21)	N = 25	0.07 (0.00–0.24)	N = 77	0.09 (0.03–0.18)	0.183
Basophils, # (N = 102), × 10⁹/L	0.02 (0.01–0.03)	N = 25	0.02 (0.01–0.04)	N = 77	0.02 (0.01–0.03)	0.235
Immune cell subsets, M (IQR)
Lymphocytes, # (N = 109), × 10⁹/L	1.24 (0.80–1.56)	N = 30	1.02 (0.55–1.33)	N = 79	1.28 (0.90–1.65)	0.006*
CD3⁺CD19^- T cells, # (N = 35), /μL	552.80 (309.48–718.07)	N = 10	340.25 (165.13–467.28)	N = 25	582.45 (361.59–799.46)	0.014*
CD4⁺ T cells, # (N = 35), /μL	481.00 (236.00–644.87)	N = 10	271.11 (124.73–411.50)	N = 25	508.00 (291.38–721.17)	0.024*
CD8⁺ T cells, # (N = 35), /μL	345.00 (135.29–492.90)	N = 10	295.08 (130.25–564.75)	N = 25	345.00 (175.08–454.00)	0.927
CD3^-CD19⁺ B cells, # (N = 20), /μL	129.50 (83.75–173.25)	N = 8	91.50 (60.00–124.50)	N = 12	161.50 (131.00–177.25)	0.012*
CD3^-CD16⁺CD56⁺ NK cells, # (N = 20), /μL	150.50 (90.25–221.75)	N = 8	142.00 (73.75–234.75)	N = 12	158.00 (129.50–219.50)	0.440
T cells+ B cells+ NK cells, # (N = 20), /μL	792.04 (652.17–1103.02)	N = 8	677.08 (358.04–797.06)	N = 12	1000.33 (773.49–1145.04)	0.021*
Inflammatory cytokines and biomarkers, M (IQR)
IL-6 (N = 69), pg/mL	9.92 (2.83–25.60)	N = 21	32.00 (10.92–119.47)	N = 48	6.69 (2.44–14.92)	<0.001*
IL-10 (N = 58), pg/mL	5.00 (5.00–6.58)	N = 15	5.00 (5.00–10.00)	N = 43	5.00 (5.00–6.25)	0.776
IL-8 (N = 58), pg/mL	12.80 (7.15–25.68)	N = 15	13.10 (8.10–45.00)	N = 43	12.40 (6.70–21.80)	0.248
TNF-α (N = 58), pg/mL	9.15 (7.30–13.08)	N = 15	13.00 (9.40–17.90)	N = 43	8.70 (6.40–11.30)	0.001*
IL-1β (N = 58), pg/mL	5.00 (5.00–5.53)	N = 15	5.00 (5.00–5.00)	N = 43	5.00 (5.00–6.30)	0.074
IL-2R (N = 58), U/mL	509.00 (334.50–776.50)	N = 15	696.00 (404.50–1042.50)	N = 43	502.00 (315.50–697.50)	0.153
Ferritin (N = 44), μg/L	470.05 (173.05–1162.50)	N = 13	511.78 (235.10–1787.00)	N = 31	417.60 (156.00–949.25)	0.286
hs-CRP (N = 94), mg/L	19.25 (2.18–62.73)	N = 25	30.90 (14.25–93.85)	N = 69	13.34 (1.40–47.43)	0.015*
Organ damage indexes, M (IQR)
ALT (N = 108), U/L	31.00 (19.00–72.25)	N = 30	71.50 (25.50–177.25)	N = 78	27.50 (17.00–52.25)	0.001*
AST (N = 108), U/L	35.50 (21.25–64.25)	N = 30	52.50 (30.50–121.00)	N = 78	27.50 (20.00–47.25)	0.003*
TBIL (N = 108), μmol/L	10.25 (7.65–15.63)	N = 30	18.50 (10.80–33.60)	N = 78	9.10 (6.60–12.05)	<0.001*
DBIL (N = 104), μmol/L	3.60 (2.90–5.93)	N = 26	5.65 (3.23–13.63)	N = 78	3.49 (2.70–4.50)	0.008*
ALB (N = 106), g/L	33.95 (29.28–38.55)	N = 28	28.20 (22.95–33.33)	N = 78	35.30 (30.88–39.63)	<0.001*
GLO (N = 106), g/L	27.55 (24.68–30.33)	N = 28	25.70 (22.45–29.28)	N = 78	27.85 (25.45–30.68)	0.013*
TP (N = 106), g/L	61.55 (55.88–65.63)	N = 28	58.00 (50.40–61.35)	N = 78	63.20 (58.20–66.60)	<0.001*
ALB/GLO (N = 106)	1.23 (1.03–1.50)	N = 28	1.12 (0.90–1.23)	N = 78	1.30 (1.08–1.60)	0.001*
LDH (N = 105), U/L	238.00 (175.00–319.00)	N = 28	282.00 (186.75–427.50)	N = 77	224.00 (175.00–286.00)	0.025*
ALP (N = 104), U/L	68.00 (53.25–88.50)	N = 26	76.50 (65.75–116.75)	N = 78	64.00 (49.75–84.00)	0.012*
CK-MB (N = 72), U/L	1.10 (0.58–9.15)	N = 18	1.50 (0.50–11.78)	N = 54	0.95 (0.60–7.30)	0.658
PT (N = 105), s	14.40 (13.55–16.50)	N = 28	16.65 (15.65–17.95)	N = 77	14.10 (13.50–14.80)	<0.001*
APTT (N = 101), s	38.10 (34.70–41.40)	N = 26	41.15 (35.20–59.08)	N = 75	37.30 (34.75–40.15)	0.017*
D-dimer (N = 104), μg/mL	0.95 (0.32–2.64)	N = 28	2.02 (1.02–11.46)	N = 76	0.60 (0.22–2.13)	<0.001*
Complication, n (%)	N = 109		N = 30		N = 79	0.020*^{, a}
DIC	5 (4.59)		4 (13.33)		1 (1.27)
Non-DIC	104 (95.41)		26 (86.67)		78 (98.73)
Hepatitis B virus serological markers, n (%)	N = 109		N = 30		N = 79	0.020*^,a
HBsAg⁺	102 (93.58)		28 (93.33)		74 (93.67)	1.000 ^a
HBsAb⁺	8 (7.34)		1 (3.33)		7 (8.86)	0.441 ^a
HBeAg⁺	11 (10.09)		11 (36.67)		0	<0.001*
HBeAb⁺	92 (84.40)		18 (60.00)		74 (93.67)	<0.001*
HBcAb⁺	106 (97.25)		29 (96.67)		77 (97.47)	0.819
HBV DNA, # (N = 84), × 10⁵/L	2.35 (0.73–5.68)	N = 23	2.70 (0.94–4.40)	N = 61	1.90 (0.69–6.40)	0.964
Anti-hepatitis therapies, n (%)	N = 109		N = 30		N = 79
Past anti-HBV therapy^b	74 (67.89)		22 (73.33)		52 (65.82)	0.453
Liver protective therapy^c	86 (78.90)		27 (90.00)		59 (74.68)	0.080
Outcomes, n (%)	N = 109		N = 30		N = 79	0.042*^,a
Survivor	96 (88.07)		23 (76.67)		73 (92.41)
Non-survivor	13 (11.93)		7 (23.33)		6 (7.59)

Tab.2

Tab.3

Tab.4

Fig.2

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