Open Access

HBV and HCV seroprevalence and their correlation with CD4 cells and liver enzymes among HIV positive individuals at University of Gondar Teaching Hospital, Northwest Ethiopia

  • Yitayih Wondimeneh1Email author,
  • Meseret Alem1,
  • Fanaye Asfaw1 and
  • Yeshambel Belyhun1, 2
Virology Journal201310:171

https://doi.org/10.1186/1743-422X-10-171

Received: 23 September 2012

Accepted: 29 May 2013

Published: 30 May 2013

Abstract

Background

The co-existence of viral hepatitis caused by HBV and HCV become common causes of severe liver complication and immunological impairment among HIV infected individuals. The aim of this study was to assess the seroprevalence of HBV and HCV and their correlation with CD4 and liver enzyme levels among HAART naïve HIV positive individuals.

Method

A Cross-sectional study was conducted from March-May, 2011 at University of Gondar Teaching Hospital, Northwest Ethiopia. HBV and HCV serological tests and liver enzymes as well as CD4 T cell level determination were assessed following the standard procedures. Socio-demographic data was collected by using structured questionnaire. The data was entered and analyzed by using SPSS version 20.0 statistical software and p < 0.05 was considered as statistically significant.

Result

Among 400 study participants, the overall prevalence of HIV-viral hepatitis co-infection was 42(11.7%). The prevalence of HIV-HBV, HIV-HCV and HIV-HBV-HCV co-infections were 20(5.6%), 18(5.0%) and 4(1.1%) respectively. Study participants who had HIV-HBV, HIV-HCV and HIV-HBV-HCV co-infection have relatively raised mean liver enzyme levels (ALT, AST and ALP) than HIV mono-infected once. Individuals with HIV-HBV, HIV-HCV and HIV-HBV-HCV co-infection also had a lower mean CD4 levels than HIV mono-infected study participants. The mean CD4 value in males was lower than females.

Conclusion

The prevalence of HBV and HCV was higher than reports from general population of the country. Raised levels of liver enzymes and lowered mean CD4 counts were seen in HIV-HBV, HIV-HCV and HIV-HBV-HCV co-infections. These findings underscore the importance of screening all HIV positive individuals before initiating antiretroviral treatment.

Keywords

HBVHCVHIVCD4 T cellsLiver enzymes

Introduction

Hepatitis B Virus (HBV) and Hepatitis C Virus (HCV) are the most common cause of chronic liver diseases worldwide. The infection continues to have a severe and invasive impact on the health of millions of people around the world and the infection is often asymptomatic [14]. Due to similar routes of viral transmission [5], co-infection of HIV with HBV and/or HCV is common. The co-infection pattern of these viruses showed that 10.0% of the HIV-infected population estimated to have chronic HBV infection and around a third estimated to have chronic HCV infection worldwide [2, 5]. However, studies reported [69] that the rates of co-infection of HIV with either HCV or HBV vary from region to region, study population and risk factors for HIV acquisition. A systematic review in 18 sub Saharan African countries also showed that the prevalence of HBV and HCV in HIV-infected individuals ranged from 3.9-7.3% and 6.9%, respectively [10].

Despite the effective decline of the mortality and morbidity rate from HIV/AIDS as the result of highly active antiretroviral therapy (HAART), liver diseases due to chronic HBV and HCV infections become a leading cause of death. Although the direct impact of HCV upon HIV disease progression remains controversial in many reports [8, 1115], the complex interactions between HIV-HBV/HCV co-infection and HAART are increasingly apparent in HIV disease progression [16].

In HIV-HBV co-infections, HIV infection causes increased rates of persistent HBV infection, increased cirrhosis and liver-related mortality and increased risk of hepatocellular carcinoma at lower CD4T cell counts [17]. Similarly in HIV-HCV co-infections, there is a more rapid progress to cirrhosis, end-stage liver disease and hepatocellular carcinoma [18].

The impact of HBV and HCV could not limited in causing liver hepatotoxicity but also results in failure in immunological recovery in HIV positive patients. For example, a study in Tanzania reported slow rate of immunologic recovery after initiation of HAART treatment and higher risk of hepatotoxicity among HIV/HBV and HIV/HCV co-infected patients [19]. Thus the management of HBV and HCV in HIV infection is complicated and bring high burden in particular where HIV is rampant. As the result, globally HIV, HBV and HCV become the major public health concerns [20, 21]. In some countries, screening of HIV-infected individuals for HBV and HCV is highly recommended before initiation of antiviral treatment [22].

In Ethiopia, the seroprevalence of HBV and HCV among HIV positive individuals is scarce except few reports among blood donors and infection prone groups [2325]. In addition, there is no report about liver enzyme levels and CD4 count determination among HIV-HBV and/or HIV-HCV co-infected patients. Therefore, the aim of this study was to assess the seroprevalence of HBV and HCV and CD4 cells as well as liver enzyme levels among HIV positive individuals at University of Gondar Teaching Hospital, Northwest Ethiopia.

Materials and methods

Study design, area, and period

A cross-sectional study was conducted from March to May, 2011 at University of Gondar Teaching Hospital, which is found in Gondar town, Northwest Ethiopia.

Source population and study participants

The source populations were all HIV positive individuals who had access to be served at University of Gondar Teaching Hospital. The study participants were all HAART naïve HIV positive adult individuals who had visited ART clinics at Gondar University Hospital during the study period. A total of 403 study participants were enrolled by considering 95% confidence interval, 5% margin of error, 50% proportion (since there is no previous estimation of HBV and HCV among HIV infected individuals in the area) and 5% contingency. However, 2(0.5%) of them had refused to participate and the other 1(0.2%) were excluded due to chronic alcoholism and 400(99.3%) HIV positive individuals were used for the final analysis.

Inclusion and exclusion criteria

All ART naïve adult HIV positive individuals who visited ART clinic for CD4 and liver enzyme level determinations for their pre-ART follow up during the study period were included. But individuals who were on ART follow up and those ART naïve but who refused to give informed consent were excluded from the study. Individuals who have been vaccinated against HBV and those who visited ART clinic and requested for laboratory investigation for the second and consequent follow up at the time of the study period were also excluded from the study to avoid duplication. Patients who had TB, malaria, leishmaniasis, opportunistic infections (OIs), drug induced hepatotoxicity and chronic alcoholism were assessed and excluded as per the HIV management guidelines of Ethiopia [26].

Data collection procedures

Socio-demographic information and other relevant possible risk factors of the study participants were collected using structured and pre tested questionnaire by trained nurses and physicians. Ten milliliter (10 ml) of veinous blood was aseptically collected using plain and EDTA vacutainer tube (5 ml in each tube) for the determination of HBV and HCV seroprevalence and CD4 and liver enzyme levels from each study participants. The blood specimen in the plain tube was centrifuged at 3000 RPM for 5 minutes to separate the serum and used for determination of liver enzyme levels within one hour of separation. The remaining serum kept in deep refrigerator (−40°C) until detection of HBV and HCV. The second tube that contains whole blood was used for the CD4 levels determination.

The collected sera were checked for the presence of HBsAg using TULIP’S INSTANT (TULIP DIAGNOSTICS (P) LTD. 88/89, Phase II C, Verna Ind. Est., Verna, Goa-403 722, INDIA) which have sensitivity and specificity of 100%. Anti-HCV antibody was detected using Flavicheck-HCV WB (TULIP DIAGNOSTICS (P) LTD. 88/89, Phase II C, Verna Ind. Est., Verna, Goa-403 722, INDIA) following the manufacturer’s instructions. The catalytic activities of the liver enzyme levels were analyzed by using clinical chemistry analyzer (Humastar 80) and the CD4 count was done by BD FACS count flow cytometry machine.

Quality control

The standard operational procedures were strictly followed for the quality control issues. Both hepatitis B and C kits were checked by using known HBsAg and anti-HCV antibody positive and negative control samples. Similarly the quality of both CD4 and liver enzyme reagents were regularly monitored by running control materials in each morning before the actual work was done.

Data analysis

The data was entered and analyzed using SPSS Version 20.0 statistical software and the differences in proportions was evaluated by Pearson’s Chi-square test (x2 test) and P-value of less than 0.05 was considered as statistical significant. Mean plus standard deviation with 95% confidence interval (CI) was also used for continuous variables and the difference in means was compared with independent-sample t-test.

Ethical consideration

The study was conducted after obtaining ethical clearance from ethical committee of Department of Medical Microbiology, Immunology and Parasitology, University of Gondar (University of Gondar, College of Medicine and Health Sciences, Ref. No: V/D06/07/2011). Informed consent was also obtained from each study participants.

Result

Socio-demographic characteristics

Among 400 study participants, 122(30.5%) were males (mean age: 37 ± 9 years) and 278(69.5%) were females (mean age: 32 ±9 years) with male to female ratio of 0.4:1. The lowest and the highest age of the study participants were 18 and 70 years respectively. The median age of the study participants was 32 years. Majority 167 (41.8%) of the study participants were in the age group of 30–39 years old. Among the study groups, 151 (37.7%) were illiterate (Table 1).
Table 1

Socio-demographic characteristics of HIV positive study participants at University of Gondar Teaching Hospital, Northwest Ethiopia, 2011

Characteristics

Male N (%)

Female N (%)

Total N (%)

Age group

   

18-29

21(16.4)

107(83.6)

128(32.0)

30-39

50(29.9)

117(70.1)

167(41.8)

40-49

40(51.3)

38(48.7)

78(19.5)

≥50

11(40.7)

16(59.3)

27(6.8)

Marital status

   

Single

27(36.0)

48(64.0)

75(18.8)

Married

76(38.0)

124(62.0)

200(50.0)

Divorced

17(20.7)

65(79.3)

82(20.5)

Widowed

2(4.7)

41(95.3)

43(10.7)

Religion

   

Christian

111(30.2)

256(69.8)

367(91.8)

Muslim

11(33.3)

22(66.7)

33(8.2)

Education

   

Illiterate

34(22.5)

117(77.5)

151(37.7)

Elementary

31(32.3)

65(67.7)

96(24.0)

High school

37(33.3)

74(66.7)

111(27.8)

Certificate and above

20(47.6)

22(52.4)

42(10.5)

Residence

   

Urban

103(30.7)

232(69.3)

335(83.7)

Rural

19(29.2)

46(70.8)

65(16.3)

Occupation

   

Civil servant

33(56.9)

25(43.1)

58(14.5)

Merchant

18(42.9)

24(57.1)

42(10.5)

Daily laborer

21(52.5)

39(97.5)

60(10.0)

Farmer

15(60.0)

10(40.0)

25(6.3)

House wife

 

114(100)

114(28.5)

Student

3(42.9)

4(57.1)

7(1.8)

Driver

8(80.0)

2(20.0)

10(2.5)

Commercial sex worker

 

5(100.0)

5(1.3)

No work

7(14.6)

41(85.4)

48(12.0)

Other

17(54.8)

16(51.6)

31(7.7)

Seroprevalence of HBVand HCV

The overall prevalence of viral hepatitis (HBV and HCV) was 42(11.7%). The seroprevalence of HBV and HCV were 20(5.6%) and 18(5.0%), respectively. Only 4(1.1%) of HIV positive individuals showed triple (HIV-HBV-HCV) infections.

HIV-HBV and HIV-HCV co-infection and sociodemographic characteristics

Significantly higher prevalence of HIV-HBV co-infection was observed in males 11(9.4%) compared to females 9(3.4%) (X2 = 5.714, P = 0.017). Although statistically non-significant, higher 6(8.3%) (X2 = 3.083, P = 0.379) prevalence of HIV-HBV co-infection was observed in the age group between 40–49 years. Individuals who were widowed 4(9.8%) (X2 =3.681, P = 0.298) and those who had better educational status (certificate, diploma and above) 4(10.3%) (X2 = 2.602, P = 0.457) showed non-significantly higher HIV-HBV positive rate. The prevalence of HIV-HBV co-infection in urban and rural residences were 17(5.3%) and 3 (5.0%) respectively. Non-statistically significant higher prevalence of HIV-HCV co-infection was also observed in females 15(5.6%), in the age group of 40–49 years 5(7.0%), in rural residence 4(6.6%), in married 12(6.3%) and in the housewives 8(7.2%). The co-existence of both HBV and HCV in males and females were 2(1.8%) and 2(0.8%) (X2 = 0.786, P = 0.375) respectively (Table 2).
Table 2

Sociodemographic characteristics and their association with HIV-HBV and HIV-HCV co-infections at University of Gondar Teaching Hospital, Northwest Ethiopia, 2011

Variables

HIV-HBV

 

HIV- HCV

 

HIV-HBV-HCV

 
 

Negative N (%)

Positive N (%)

Sign

Negative N (%)

Positive N (%)

Sign

Negative N (%)

Positive N (%)

Sign

Age

         

18-29

118(95.9)

5(4.1)

X2 = 3.083

118(96.7)

4(3.3)

X2 = 1.461

118(99.2)

1(0.8)

X2 = 12.169

30-39

150(94.3)

9(5.7)

P = 0.379

150(94.9)

8(5.1)

P = 0.691

150(100.0)

0(0.0)

P = 0.007

40-49

66(91.7)

6(8.3)

66(93.0)

5(7.0)

66(98.5)

1(1.5)

≥50

24(100)

0(0)

24(96.0)

1(4.0)

24(92.3)

2(7.7)

Sex

         

Male

106 (90.6)

11(9.4)

X2 = 5.714

106(97.2)

3(2.8)

X2 = 1.395

106(98.2)

2(1.8)

X2 = 0.786

Female

252(96.6)

9(3.4)

P = 0.017

252(94.4)

15(5.6)

P = 0.238

252(99.2)

2(0.8)

P = 0.375

Residence

         

Urban

301(94.7)

17(5.3)

X2 = 0.12

301(95.6)

14(4.4)

X2 = 0.501

301(99.0)

3(1.0)

X2 = 0.242

Rural

57(95.0)

3(5.0)

P = 0.913

57(93.4)

4(6.6)

P = 0.479

57(98.3)

1(1.7)

P = 0.623

Marital status

         

Single

72(96.0)

3(4.0)

X2 = 3.681

72(100.0)

0(0.0)

X2 = 4.653

72(100.0)

0(0.0)

X2 = 1.777

Married

178(96.2)

7(3.8)

P = 0.298

178(93.7)

12(6.3)

P = 0.199

178(98.3)

3(1.7)

P = 0.620

Divorced

71(92.2)

6(7.8)

71(94.7)

4(5.3)

71(98.6)

1(1.4)

Widowed

37(90.2)

4(9.8)

37(94.9)

2(5.1)

37(100.0)

0(0.0)

Religion

         

Christian

327(94.5)

19(5.5)

X2 = 0.327

327(94.8)

18(5.2)

X2 = 1.699

327(99.1)

3(0.9)

X2 = 1.311

Muslim

31(96.9)

1(3.1)

P = 0.567

31(100.0)

0(0.0)

P = 0.192

31(96.9)

1(3.1)

P = 0.252

Education

         

Illiterate

133(94.3)

8(5.7)

X2 = 2.602

133(95.0)

7(5.0)

X2 = 0.672

133(97.8)

3(2.2)

X2 = 4.553

Elementary

89(95.7)

4(4.3)

P = 0.457

89(96.7)

3(3.3)

P = 0.880

89(100.0)

0(0.0)

P = 0.208

High school

101(96.2)

4(3.8)

101(94.4)

6(5.6)

101(100.0)

0(0.0)

Certificate & above

35(89.7)

4(10.3)

35(94.6)

2(5.4)

35(97.2)

1(2.8)

Occupation

         

Civil servant

49(89.1)

6(10.9)

X2 = 12.352

49(96.1)

2(3.9)

X2 = 4.427

49(98.0)

1(2.0)

X2 = 5.695

Merchant

37(90.2)

4(9.8)

P = 0.194

37(97.4)

1(2.6)

P = 0.881

37(100.0)

0(0.0)

P = 0.770

Daily laborer

54(91.5)

5(8.5)

54(98.2)

1(1.8)

54(100.0)

0(0.0)

Farmer

22(95.7)

1(4.3)

22(95.7)

1(4.3)

22(95.7)

1(4.3)

House wife

103(99.0)

1(1.0)

103(92.8)

8(7.2)

103(99.00)

1(1.0)

Student

7(100.0)

0(0.0)

7(100.0)

0(0.0)

7(100.0)

0(0.0)

Driver

9(90.0)

1(10.0)

9(100.0)

0(0.0)

9(100.0)

0(0.0)

Com. sex worker

4(100.0)

0(0.0)

4(100.0)

0(0.0)

4(100.0)

0(0.0)

No work

44(97.8)

1(2.2)

44(93.6)

3(6.4)

44(100.0)

0(0.0)

Other

29(96.7)

1(3.3)

 

29(93.5)

2(6.5)

 

22(95.7)

1(4.3)

 

Liver enzyme levels and mean CD4 count in HIV/HBV, HIV/HCV and HBV/HCV/HIV co-infection

The mean serum levels; ALT, AST, and ALP in HIV mono-infected study participants were 25 international units (IU), 27 IU and 243 IU respectively. However, in HIV-HBV co-infected study participants, the levels of ALT, AST and ALP were non-significantly raised (29 IU, 31 IU and 262 IU, respectively). Similarly, in HIV-HCV co-infected study participants, the mean levels of ALT, AST and ALP were 27 IU, 32 IU, and 290 IU respectively. Statistically non-significant raised mean serum ALT, AST and ALP were found in HIV-HBV-HCV triple infected study participants (Table 3).
Table 3

Mean CD4 and liver enzyme levels and their association with HBV and HCV co-infection at University of Gondar Teaching Hospital, Northwest Ethiopia, 2011

Immunological and liver biomarkers

HIV alone

HIV/HBV

P-value

HIV alone

HIV/HCV

P-value

HIV alone

HIV/HBV/HCV

P-value

CD4 mean ± SD

288 ± 190

250

0.375

288 ± 190

274 ± 138

0.754

288 ± 190

125 ± 96

0.087

Normal value

500-1300

500-1300

 

500-1300

500-1300

 

500-1300

500-1300

 

ALT mean ± SD

25 ± 21

29 ± 18

0.356

25 ± 21

27 ± 17

0.472

25 ± 21

39 ± 6

0.170

Normal value

0-37

0-37

 

0-37

0-37

 

0-37

0-37

 

Abnormal High (%)

12.3%

20%

 

12.3%

22.2%

 

12.3%

50%

 

AST mean ± SD

27 ± 19

31 ± 18

0.419

27 ± 19

32 ± 17

0.339

27 ± 19

33 ± 15

0.587

Normal value

0-34

0-34

 

0-34

0-34

 

0-34

0-34

 

Abnormal High (%)

20.1%

25%

 

20.1%

27.8%

 

20.1%

50%

 

ALP mean ± SD

243 ± 130

262 ± 118

0.515

243 ± 130

290 ± 127

0.135

243 ± 130

332 ± 228

0.176

Normal value

72-306

72-306

 

72-306

72-306

 

72-306

72-306

 

Abnormal High (%)

19.6%

15%

 

19.6%

33.3%

 

19.6%

50%

 
The mean CD4 count of HIV mono-infection was 288cells/mm3. However, in HIV-HBV, HIV-HCV and HIV-HBV-HCV co-infections, the mean CD4 count were 250 cells/mm3, 274 cells/mm3 and 125 cells/mm3 respectively. However, the difference was not statistically significant (Table 3). The CD4 value in females was higher than males (299 ± 197 vs 249 ± 152). Males study participants who had both HBV and HCV have the lowest mean CD4 count. The highest and lowest mean CD4 values were observed in the age groups of 18–29 and ≥50 years respectively (Table 4).
Table 4

Mean CD4 values in relation to gender and different age categories at University of Gondar Teaching Hospital, Northwest Ethiopia, 2011

Variables

Mean CD4 count

 

HIV alone

HIV-HBV

HIV-HCV

HIV-HBV-HCV

Over all

Gender

     

Male

256 ±155

197 ± 113

334 ± 133

75 ± 30

249 ± 152

Female

302 ± 201

314 ± 188

262 ± 140

176 ± 129

299 ± 197

Age categories

     

18-29

338 ± 223

383 ± 201

328 + 151

84 ± 0

337 ± 219

30-39

261 ± 151

169 ± 108

241 + 128

 

255 ± 149

40-49

292 ± 203

260 ± 121

286 + 173

53 ± 0

286 ± 196

≥50

203 ± 135

 

260 +0

182 ± 121

204 ± 129

Discussion

This study investigated the seroprevalence of HBV and HCV among HIV positive study participants and tried to assess levels of liver enzymes and CD4 count for HIV mono infected, HIV-HBV and HIV-HCV co-infected and HIV-HBV-HCV triple infected individuals. The overall prevalence (11.7%) of hepatitis (both HBV and HCV) among the study participants was very high. In this study, HIV-HBV co-infection rate was 5.6% which is more or less comparable with 7.1% prevalence [24] among blood donors in the same hospital. However, the present prevalence was lower as compared to studies reported in Nigeria (9.2%) [27], Ethiopia (10.9%) [23] and Malawi (20.4%) [28]. In the present study, the prevalence of HIV-HBV co-infection was higher in males than females (9.4%% vs 3.4%) which are in line with some other reports [2931]. Generally, as several studies reported and anticipated in different parts of the world, such co-infection differences could be due to differences in geographic regions, types of risk groups and the means of exposures involved [26, 27, 3235].

The seroprevalence rates of HIV-HCV co-infection in this study was 5.0% which is almost comparable with the studies which were done in Nigeria (5.8%), Malawi (5.0%), Burkina Faso (4.8%) and Senegal (8.0%) [27, 28, 36, 37]. However, the epidemiological survey of HCV in Ethiopia showed variation from 2-3% in the general population in early 1990s [3840] and recently, the co-infection rates of HIV-HCV ranges from 3.6-13.3% in different reports [24, 25, 4145]. The reasons for the HCV variation both in HIV infected individuals and the general population could share the factors responsible HBV prevalence variations discussed above.

The seroprevalence of HIV-HBV-HCV triple infection in this study was 1.1%, which is more or less comparable to reports from Senegal (0.5%), Kenya (0.26%), Nigeria (1.5%) and Egypt (0.44%) [37, 46, 47]. However, higher prevalence of HCV-HBV-HIV triple co-infection was reported in Argentina (9.5%) and Iran (9.2%) [48, 49]. For such variations, risk factors which accounts for HBV and HIV prevalence difference might work for the triple infection.

Despite absence of statistical significance difference in the mean levels of the liver enzymes between HIV-mono-infected and HIV-viral hepatitis co-infected individuals, raised ALT, AST and ALP were found in HIV-HBV, HIV-HCV and HIV-HBV-HCV co-infected individuals. However, in a study which was conducted in South Africa, 70% of HIV-HBV and HIV-HCV co-infected study participants had significantly elevated AST and ALT, 56% of them had elevated ALP [35]. Similarly, significantly raised ALT was found in 14% of HIV/HBV co-infections and 20% in HIV-HCV co-infected patients in India [50]. These liver enzyme levels difference between different studies may be due to difference in study design, duration of the viral hepatitis infection as well as the patient’s condition like having chronic alcoholism or other drug induced hepatotoxicity. In addition, HIV can also infect the hepatic or kupffer cells [51] that may farther contributes for the development of liver fibrosis and raised liver enzyme levels. However, the magnitude of the complication of the liver may be worse if the HIV positive patients co-infected with HBV and HCV as indicated in the above.

In the present study, there is no statistically significant CD4 count mean difference between HIV mono-infected, HIV-HBV and HIV- HCV co-infected study participants. However, study participants who had HIV-HBV co-infection in this study have the mean CD4 count (250 cells/mm3) which was incomparable with mean CD4 count of 141.6 cells/mm3 and 121 cells/mm3 in the studies which were conducted in South Africa and Nigeria respectively [35, 46]. These controversial results may be due to the differences in the immune status of the individual who have been participated in the study or it may be due to the viral hepatitis. In individuals who have both HIV and HBV infections, there may be high HIV and HBV viral replication that may farther contribute for the impairment of the immune system of the patients.

In this study, the mean CD4 count (274 cells/mm3) was found in HIV-HCV co-infected study participants which is comparable with a mean CD4 count of 260 cells/mm3 and 288.6 cells/mm3 that were reported in Nigerian and Indian studies respectively [46, 50]. Such high values of mean CD4 count in HIV-HCV co-infected study participants than study participants who had HIV-HBV co-infections were unclear. However, HIV-HCV co-infected study participants have relatively lower mean CD4 values than HIV mono-infected study participants. This low CD4 count in HIV-HCV co-infected may be associated with an increased HIV and HCV replication, reflecting the immunosuppressed state.

Among HIV-HBV-HCV infected individuals, the mean CD4 count was 125cells/mm3. This CD4 levels is comparable with the mean CD4 count of 116/mm3 which was reported in India [50]. Similarly in a study which was done in Nigeria, HIV-HBV-HCV infected individuals had the mean CD4 count of 106 cells/mm3[46]. However, all of these results showed the mean CD4 count of less than 200 cells/mm3. This could be due to the fact that the presence of both HBV and HCV in HIV positive individuals may highly contribute for the impairment of the immune system of an individual that may also further lead the person for the development of advanced HIV diseases. In addition, there is also inverse relationship between CD4 values and HIV diseases progression. However, the impact of viral hepatitis on the immune system and liver enzymes needs farther studies in both on HAART and HAART naïve HIV positive patients.

In the present study, there was also difference on the mean CD4 values in relation to gender. The mean CD4 value in the males was lower than females (249 cells/mm3 vs 299 cells/mm3). Similar findings were reported in studies which have been conducted in Nigeria [52] and Uganda [53]. Male study participants who had both HBV and HCV had also the lowest mean CD4 values. This lower CD4 count in males may be associated with their daily activities. In addition, males are mostly more muscular and may not be ready to accept their HIV, HBV and/or HCV results and they may develop mental stress that farther contribute for the impairment of their immune system or lower CD4 count. Farther more, males may spend most of their time with hard works for a long period of time and this may contribute for lower CD4 count. We have also analyzed the mean CD4 values in different age categories and the lowest mean CD4 values was observed in the age groups of 50 years and above. As age increases, there may be impairment of the immune system of the individuals specially HIV positive patients and older age groups may have severed HIV diseases progression than younger once.

In conclusion, the prevalence of viral hepatitis (HBV, HCV) among HIV positive individuals was higher than the prevalence of the respective viruses in the general population. Thus screening of HBV and HCV before initiation of antiretroviral treatment is mandatory for strict monitoring and a regular evaluation of liver enzyme levels and CD4 status in order to minimize the complication of the liver and for effective HIV treatment.

Declarations

Acknowledgements

We would like to thank the University of Gondar and Emeritus Prof. Fusao Ota’s Scholarship for funding the project, facilitating and following the progresses of the study. Our special thanks and appreciation also goes to all the study participants who voluntarily participated in this study. Last but not least, we also thank University of Gondar Teaching Hospital ART laboratory personnel for their consistent support with some reagents and other materials during the project work.

Authors’ Affiliations

(1)
School of Biomedical and Laboratory Sciences, College of Medicine and Health Sciences, University of Gondar
(2)
Institute of Virology, Faculty of Medicine, University of Leipzig

References

  1. Chen LS, Morgan RT: The natural history of Hepatitis C Virus (HCV) infection. Int J Med Sci 2006,3(2):48-59.Google Scholar
  2. Fenton K: The changing global epidemiology of HBV and HCV. Frontiers in Drug Development for Viral Hepatitis 2007, 3: 3-4.Google Scholar
  3. Alberti A, Clumeck N, Collins S, Gerlich W, Lundgren J, Palù G: Short statement of the first European consensus conference on the treatment of chronic hepatitis B and C in HIV co-infected patients. J Hepatol 2005,42(5):615-624. 10.1016/j.jhep.2005.03.003PubMedView ArticleGoogle Scholar
  4. Volf V, Marx D, Pliscova L, Sumega L, Celko A: A survey of hepatitis B and C prevalence among the homeless community of parague. Eur J Public Health 2008, 18: 44-47. 10.1093/eurpub/ckm072PubMedView ArticleGoogle Scholar
  5. Soriano V, Barreiro P, Nunez M: Management of chronic hepatitis B and C in HIV-coinfected patients. J Antimicrob Chemother 2006, 57: 815-818. 10.1093/jac/dkl068PubMedView ArticleGoogle Scholar
  6. Sharifi-Mood B, Metanat M: HIV/AIDs and hepatitis C Co-infection. Int J Virol 2006,2(1):63-66.View ArticleGoogle Scholar
  7. Koziel M, Peters M: Viral hepatitis in HIV infection. New England Medical Journal 2007,356(14):1445-1454. 10.1056/NEJMra065142View ArticleGoogle Scholar
  8. Konopnicki D, Mocroft A, de Wit S, Antunes F, Ledergerber B, Katlama C: Hepatitis B and HIV Prevalence, AIDS progression, response to highly active antiretroviral therapy and increased mortality in the EuroSIDA cohort. AIDS 2005, 19: 593-601. 10.1097/01.aids.0000163936.99401.fePubMedView ArticleGoogle Scholar
  9. Amin J, Kaye M, Skidmore S, Pillay D, Cooper DA, Dore GJ: HIV and hepatitis C co infection within the CAESAR study. HIV Med 2004, 5: 174-179. 10.1111/j.1468-1293.2004.00207.xPubMedView ArticleGoogle Scholar
  10. Barth E, Quirine H, Jantjie T, Hoepelman I: Hepatitis B/C and HIV in sub-Saharan Africa. Int J Infect Dis 2010,14(12):1024-1031. 10.1016/j.ijid.2010.06.013View ArticleGoogle Scholar
  11. Sulkowski M: Viral hepatitis and HIV co-infection. Journal of Hepathology 2008,48(2):353-367. 10.1002/hep.22407View ArticleGoogle Scholar
  12. Petrovic L: HIV/HCV co-infection, histopathologic findings, natural history, fibrosis, and impact of antiretroviral treatment. Liver Int 2007, 27: 598-606. 10.1111/j.1478-3231.2007.01478.xPubMedView ArticleGoogle Scholar
  13. Lincoln D, Petoumenos K, Dore G: HIV/HBV and HIV/HCV co-infection and outcomes following highly active antiretroviral therapy. HIV Med 2003, 4: 241-249. 10.1046/j.1468-1293.2003.00152.xPubMedView ArticleGoogle Scholar
  14. Sullivan PS, Hanson D, Teshale E, Wotring L, Brooks J: Effect of hepatitis C infection on progression of HIV disease and early response to initial antiretroviral therapy. AIDS 2006, 20: 1171-1179. 10.1097/01.aids.0000226958.87471.48PubMedView ArticleGoogle Scholar
  15. Sulkowski M, Moore R, Mehta S, Chaisson R, Thomas D: Hepatitis C and progression of HIV disease. J Am Med Assoc 2002, 288: 199-206. 10.1001/jama.288.2.199View ArticleGoogle Scholar
  16. Mallet V, Vallet-Pichard A, Pol S: The impact of human immunodeficiency virus on viral hepatitis. Liver Int 2011,31(1):135-139.PubMedView ArticleGoogle Scholar
  17. Thio CL: Hepatitis B and human immunodeficiency virus coinfection. Hepathology 2009,49(5):138-145.View ArticleGoogle Scholar
  18. Romeo R, Rumi M, Donato M, Cargne P, Vigano M, Mondelli B: Hepatitis C is more severe in drug users with human immunodeficiency virus infection. Journal of Viral Hepathology 2000, 7: 297-301. 10.1046/j.1365-2893.2000.00230.xView ArticleGoogle Scholar
  19. Christian B, Okuma J, Claudia H, Chalamilla G, Spiegelman D, Nagu T: Prevalence of hepatitis B and C Co-infection and response to antiretroviral therapy among HIV-infected patients in an urban setting in Tanzania. California: 17th Conference on Retroviruses & Opportunistic Infections in San Francisco; 2010.Google Scholar
  20. Leeratanapetch N, Suseangrut W: Hepatitis B virus and hepatitis C virus Co-infection with HIV patients at khon kaen hospital. Khon Kaen Hospital Medical Journal 2008, 32: 229-238.Google Scholar
  21. Modi A, Feld J: Viral hepatitis and HIV in Africa. AIDS Review 2007, 9: 25-39.Google Scholar
  22. Chung R: Hepatitis C and B viruses: the new opportunists in HIV infection. Tropical HIV Medicine 2006,14(2):78-83.Google Scholar
  23. Moges F, Kebede Y, Kassu A, Mulu A, Tiruneh M, Degu G: Seroprevalence of HIV, hepatitis B infections and syphilis among street dwellers in Gondar city, Northwest Ethiopia. Ethiop J Heal Dev 2006,20(3):5.Google Scholar
  24. Tessema B, Yismaw G, Kassu A, Amsalu A, Mulu A, Emmrich F: Seroprevalence of HIV, HBV, HCV and syphilis infections among blood donors at Gondar University teaching hospital Northwest Ethiopia. BMC Infect Dis 2010,10(111):4-5.Google Scholar
  25. Diro E, Alemu S, Alemu S, G/Yohannes A: Blood safety & prevalence of transfusion transmissible viral infections among donors at the Red cross blood bank in Gondar University hospital. Ethiop Med J 2008,46(1):7-13.PubMedGoogle Scholar
  26. Ethiopian Federal Ministry of Health: Guidelines for management of opportunistic infections and anti-retroviral treatment in adolescents and adults in Ethiopia. Addis Ababa Ethiopia: Federal HIV/AIDS Prevention and Control Office Federal Ministry of Health; 2008.Google Scholar
  27. Lesi O, Kehinde M, Oguh D, Amira C: Hepatitis B and C virus infection in Nigerian patients with HIV/AIDS. Niger Postgrad Med J 2007, 14: 129-133.PubMedGoogle Scholar
  28. Nyirenda M, Beadsworth M, Stephany P, Hart C, Hart I, Munthali C: Prevalence of infection with hepatitis B and C virus and co-infection with HIV in medical inpatients in Malawi. J Infect Dis 2008, 57: 72-77.Google Scholar
  29. Hussain T, Kulshreshtha KK, Sinha S, Yadav VS, Katoch VM: HIV, HBV, HCV, and syphilis co-infections among patients attending the STD clinics of district hospitals in Northern India. Int J Infect Dis 2006,10(5):358-363. 10.1016/j.ijid.2005.09.005PubMedView ArticleGoogle Scholar
  30. Otegbayo JA, Taiwo BO, Akingbola TS, Odaibo GN, Adedapo KS, Penugonda S, Adewole IF, Olaleye DO, Murphy R, Kanki P: Prevalence of hepatitis B and C seropositivity in a Nigerian cohort of HIV-infected patients. Ann Hepatol 2008,7(2):152-156.PubMedGoogle Scholar
  31. Omosigho OP, Inyinbor HE, Emumwen GE, Mohammed SK, Ledogo G, Njab J, Oladejo OP, Omueti EA: Hepatitis C virus Co-infection in human immuno deficiency virus positive population in bida, north central Nigeria. The Internet Journal of Infectious Diseases 2011, 9: 2.Google Scholar
  32. Alter M: Epidemiology of viral hepatitis and HIV co-infection. Journal of Hepathology 2006, 44: 6-9. 10.1002/hep.21269View ArticleGoogle Scholar
  33. Sherman K, Rouster S, Chung R, Rajicic N: Hepatitis C virus prevalence among patients infected with human immunodeficiency virus. Clin Infect Dis 2002, 34: 831-837. 10.1086/339042PubMedView ArticleGoogle Scholar
  34. Rockstroh J, Mocroft A, Soriano V, Tural C, Losso MH, Horban A: Influence of hepatitis C virus infection on HIV-1 disease progression and response to highly antiretroviral therapy. J Infect Dis 2005, 192: 992-1002. 10.1086/432762PubMedView ArticleGoogle Scholar
  35. Lodenyo H, Schoub B, Ally R, Kairu S, Segal I: Hepatitis B and C virus infections and liver function in AIDS patients at Chrishanibaragwanath hospital Johannesburg. East African Medical January 2000,77(1):13-15.Google Scholar
  36. Simpore J, Savadogo A, Ilboudo D, Nadambega C, Esposito M, Yara J: Toxoplasma gondii , HCV, and HBV seroprevalence and Co-infection among HIV positive and negative pregnant women in Burkina Faso. J Med Virol 2006, 78: 730-733. 10.1002/jmv.20615PubMedView ArticleGoogle Scholar
  37. Diop-Ndiaye H, Toure’-Kane C, Etard JF, Loˆ G, Diaw PA, Ngom-Gueye NF: Hepatitis B, C seroprevalence and delta viruses in HIV-1 Senegalese patients at HAART initiation (retrospective study). J Med Virol 2008, 80: 1332-1336. 10.1002/jmv.21236PubMedView ArticleGoogle Scholar
  38. Flatau E, Segol O, Shneour A, Tabenkin H, Raz R: Prevalence of markers of infection with hepatitis B and C viruses in immigrants of operation Solomon, 1991. Isr J Med Sci 1993,29(6–7):387-389.PubMedGoogle Scholar
  39. Frommel D, Tekle-Haimanot R, Berhe N, Aussel L, Verdier M, Preux PM, Denis F: A survey of antibodies to HCV in Ethiopia. AmJTrop Med Hyg 1993,49(4):435-439.Google Scholar
  40. Tsegaye E, Nordenfelt E, Hansson BG: Hepatitis C virus infection and chronic liver disease in Ethiopia where hepatitis B infection is hyperendemic. Trans R Soc Trop Med Hyg 1995,89(2):171-174. 10.1016/0035-9203(95)90482-4View ArticleGoogle Scholar
  41. Ayele W, Nokes J, Abebe A, Messele T, Dejene A, Enquselassie F: Higher prevalence of anti-HCV antibodies among HIV-positive compared to HIV-negative inhabitants of Addis Ababa, Ethiopia. J Med Virol 2002, 68: 12-17. 10.1002/jmv.10164PubMedView ArticleGoogle Scholar
  42. Dessie A, Abera B, Wale F: Seroprevalence of major blood-borne infections among blood donors at Felege Hiwot referral hospital, northwest Ethiopia. Ethiop J Health Dev 2007,21(1):68-69.Google Scholar
  43. Ayele Ayele W, Nokes DJ, Abebe A, Messele T, Dejene A, Enquselassie F, Rinke de Wit FT, Fontanet LA: Higher prevalence of anti HCV antibodies among HIV positive compared to HIV negative inhabitants of Addis Ababa Ethiopia. J Med Virol 2002, 68: 12-17. 10.1002/jmv.10164PubMedView ArticleGoogle Scholar
  44. Abreha T, Woldeamanuel Y, Pietsch C, Maier M, Asrat D, Abebe A, Hailegiorgis B, Aseffa A, Liebert UG: Genotypes and viral load of HCV among persons attending a VCT center in Ethiopia. J Med Virol 10.1002/jmv.21788Google Scholar
  45. Alemayehu A, Tassachew Y, Sisay Z, Shimelis T: Prevalence and risk factors of hepatitis C among individuals presenting to HIV testing centers, hawassa city southern Ethiopia. BMC Research Notes 2011, 4: 193. 10.1186/1756-0500-4-193PubMedPubMed CentralView ArticleGoogle Scholar
  46. Olufemi A, Emmanuel A, Zaccheus A, Ibrahim W, Funmilayo E, Patience A: Hepatitis B and C virus co-infection in Nigerian patients with HIV infection. Journal of Infectious DevCtries 2009,3(5):369-375.Google Scholar
  47. Kazem S, Asl H, Avijgan M, Mohamadnejad M: High prevalence of HBV, HCV, and HIV infections in gypsy population residing in Shahr-E-Kord. Arch Iranian Medicine 2004,7(1):20-22.Google Scholar
  48. Fuse V, Cornelio C, Meraldi N: Prevalence of HCV and HBV in HIV positive patients attending a general hospital in Buenos Aires. International Conference of AIDS: Argentina; 2004.Google Scholar
  49. Ataei B, Tayeri K, Kassaian N: Hepatitis B and C among patients infected with human immunodeficiency virus in Isfahan, Iran: seroprevalence and associated factors. Hepatitis Monthly summer 2010,10(3):188-192.Google Scholar
  50. Tripathi A, Khanna M, Gupta N, Chandra M: Low prevalence of hepatitis B virus and hepatitis C virus Co-infection in patients with human immunodeficiency virus in northern India. Indian Journal of Physicians Association 2007, 55: 430.Google Scholar
  51. Cao YZ, Dieterich D, Thomas PA, Huang YX, Mirabile M, Ho DD: Identification and quantitation of HIV-1 in the liver of patients with AIDS. AIDS 1992, 6: 65-70. 10.1097/00002030-199201000-00008PubMedView ArticleGoogle Scholar
  52. Akinsegun A, Adedoyin D, Adewumi A, Sarah A, Olajumoke Oshinaike KW: CD4 Count pattern and demographic distribution of treatment-Na¨ıve HIV patients in Lagos, Nigeria. AIDS Research and Treatment 2012, 2012: 1-6.Google Scholar
  53. Tugume SB, Piwowar EM, Lutalo T, Mugyenyi PN, Grant RM, Mangeni FW: Hematological reference ranges among healthy Ugandans. Clin Diagn Lab Immunol 1995,2(2):233-235.PubMedPubMed CentralGoogle Scholar

Copyright

© Wondimeneh et al.; licensee BioMed Central Ltd. 2013

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.