Assessment of hepatitis E seropositivity among HIV-infected patients in Bulgaria

Golkocheva-Markova, Elitsa; Kevorkyan, Ani; Raycheva, Ralitsa; Ismailova, Chiydem; Yoncheva, Viliana; Tenev, Tencho; Emilova, Radoslava; Grigorova, Lyubomira; Baltadzhiev, Ivan; Komitova, Radka

doi:10.1016/j.bjid.2022.102329

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Original Article • Braz. j. infect. dis 26 (01) • 2022 • https://doi.org/10.1016/j.bjid.2022.102329 copy

Assessment of hepatitis E seropositivity among HIV-infected patients in Bulgaria

Authorship SCIMAGO INSTITUTIONS RANKINGS

Abstract

It is debatable whether HIV-infected patients are at greater risk for hepatitis E virus (HEV) infection compared with healthy subjects. The reported anti-HEV seroprevalence among different groups in Bulgaria varied from 9.04% to 25.9%, but the information regarding the HIV population is still missing. The aim of the present study was to evaluate hepatitis E seroprevalence among HIV-infected patients in Bulgaria and to analyze demographic and immunological factors associated with HEV infection. Serum samples of 312 HIV-infected patients were analyzed retrospectively. Age, sex, residence and laboratory markers for HEV, HBV, HCV and HIV infection, and lymphocytes subpopulations were collected for all patients. None of the tested samples were positive for HEV RNA. HEV seroprevalence among HIV-infected patients was 10.9%. Males were more affected with the highest prevalence of positivity in the age group > 30 to ≤ 40 years. The documented HIV transmission routes in HIV/HEV co-infected group were heterosexual, homosexual, intravenous drug use (IDU), and vertical with predominace of the heterosexual route (z = 0.2; p = 0.804). There was a statistically significant trend of HIV mixed infection with routes of HIV transmission other than homosexual - heterosexual in HIV/HEV group and injection drug use in HIV/HBV/HCV co-infected group. The route of HIV transmission, in contexts of patients’ behavior, was associated with HEV prevalence among HIV-infected patients.

Keywords
Hepatitis E virus; HIV infection; HEV seropositivity; HIV/HEV co-infection

	HIV patients (N=312)	HIV-mono (N=210)	HIV/HBV/HCV (N=68)	HIV/HEV (N=34)
Variables
Age; median (25^th - 75^th percentiles)	35.0 30.0 – 42.0	34.0 29.0 - 42.2	37.0 33.0 - 43.0	35.5 27.5 - 40.3
Sex; m:f	5:1	6:1	7:1	7:2
Duration HIV seropositivity [years]
Median (25^th - 75^th percentiles)	< 1.0 < 1.0 - 3.5	< 1.0 < 1.0 - 2.0	1.0 < 1.0 - 6.0	< 1.0 < 1.0 - 7.0
CD AC [cells/µl]; median (25^th - 75^th percentiles)
CD45	1875 (1395 – 2333)	1875 (1468 – 2309)	1762 (1762 – 2303)	2044 (1443 – 2522)
CD3	1385 (1021 – 1843)	1389 (1044 – 1850)	1310 (894 – 1685)	1486 (1109 – 2007)
CD4	419 (223 – 606)	435 (225 – 622)	332 (155 – 554)	441 (259 – 737)
CD8	844 (587 – 1182)	846 (601 – 1202)	831 (525 – 1133)	881 (581 – 1270)
Hepatitis co-infection; n (%)
HBV	38 (12.2%)	—	—	5 (14.7%)
HCV	48 (15.4%)	—	—	6 (17.6%)

Variables	HIV-mono(N=210)			HIV/HBV/HCV(N=68)			HIV/HEV(N=34)		p-value
Variables	N		%	N	%		N	%	p-value
Sex:									0.822
male	177		84.29	59	86.76		28	82.35
female	33		15.71	9	13.24		6	17.65
Years [age decades]									0.054
≤20	6		2.86	0	0.00		1	2.94
>20 ≤30	60		28.57	8	11.76		10	29.41
>30 ≤40	80		38.10	38	55.88		15	44.12
>40 ≤50	44		20.95	19	27.94		7	20.59
>50 ≤60	17		8.10	2	2.94		0	0.00
≥60	3		1.43	1	1.47		1	2.94
Residence (population)									0.599
< 50 000	18	8.57		6		8.82	3	8.82
≥ 50 000 < 100 000	39	18.57		9		13.24	9	26.47
≥ 100 000	153	72.86		53		77.94	22	64.71
Route of HIV transmission									0.000
MSM^a a Data were missing for route of HIV transmission in HIV-mono (N = 204), and in HIV/HBV/HCV (N = 64)	112	54.90		13	20.00		12	35.29
Hetero	86	42.16		21	32.31		13	38.24
IDUs	5	2.45		31	47.69		8	23.53
Vertical^§ § transmission from mother to child. CD 45 AC [cells/µl] min-aver-max values [1000-1800-2800] CD3 AC [cells/µl] min-aver-max values [700-1200-2500]; CD4 AC [cells/µl] min-aver-max values [400-700-1600]; CD 8 AC [cells/µl] min-aver-max values [200-400-1100].	1	0.49		0	0.00		1	2.94
Duration HIV seropositivity									0.002
< 1	125	59.52		21	30.88		16	47.06
≥ 1 < 5	49	23.33		23	33.82		7	20.59
≥ 5 < 10	20	9.52		16	23.53		7	20.59
≥ 10	16	7.62		8	11.76		4	11.76
HIV VL Log [copies/ml]
<1.3/1.6	59	28.10		21	31.34		8	23.53	0.132
≥1.3 to <3	20	9.52		13	19.40		5	14.71
≥3	131	62.38		33	49.25		21	61.76
CD45 AC [cells/µl]									0.636
< min [1000]	29	13.81		11	16.18		3	8.82
≥min <max [1800]	155	73.81		47	69.12		24	70.59
≥max [2800]	26	12.38		10	14.71		7	20.59
CD3 AC [cells/µl]									0.436
< min [700]	23	10.95		10	14.71		2	5.88
≥min <max [1200]	172	81.90		50	73.53		28	82.35
≥max [2500]	15	7.14		8	11.76		4	11.76
CD4 AC [cells/µl]									0.213
< min [400]	94	44.76		38	55.88		11	32.35
≥min <max [700]	115	54.76		30	44.12		23	67.65
≥max [1600]	1	0.48		0	0.00		0	0.00
CD8 AC [cells/µl]									0.623
< min [200]	7	3.33		1	1.47		0	0.00
≥min <max [400]	141	67.14		47	69.12		21	61.76
≥max [1100]	62	29.52		20	29.41		13	38.24

Variables	Number	OR	95% CI for OR		ANOVA	p-value
Variables	Number	OR	Lower	Upper	ANOVA	p-value
Sex
Males	264	1.03	0.88	1.21	0.15^* * x2 test; OR = odds ratio; CI = confidence interval	0.698
Females	48	0.86	0.39	1.86
Years [age decades]
≤20	7	0.68	0.03	14.03	0.64	0.673
>20 ≤30	78	0.59	0.06	5.81
>30 ≤40	133	0.51	0.05	4.85
>40 ≤50	70	0.44	0.04	4.55
>50 ≤60	19	0.00	0.00	0.00
≥60	5	0.67	0.03	14.03
Duration of HIV seropositivity
< 1	162	0.66	0.20	2.14	4.03	0.008
≥ 1 <5	79	0.58	0.16	2.17
≥5 <10	43	1.17	0.31	4.43
≥10 yrs.	28	0.00	0.00	0.00
Route of HIV transmission
MSM	137	0.10	0.01	1.63	18.40	0.000
Hetero	120	0.10	0.01	2.06
IDUs	44	0.20	0.01	3.94
vertical	2	0.00	0.00	0.00

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[1] *Corresponding author at: Virology, National Center of Infectious and Parasitic Diseases, 44A Gen. Stoletov, blvd, 1233 Sofia, Bulgaria. E-mail address: elmarkova2007@gmail.com (E. Golkocheva-Markova).