Open Access

Sero-prevalence and associated risk factors for hepatitis C virus infection among voluntary counseling testing and anti retroviral treatment clinic attendants in Adwa hospital, northern Ethiopia

  • Ataklti Hailu Atsbaha2,
  • Tsehaye Asmelash Dejen1,
  • Rashmi Belodu1,
  • Konjit Getachew1,
  • Muthupandian Saravanan1 and
  • Araya Gebreyesus Wasihun1Email author
BMC Research Notes20169:121

https://doi.org/10.1186/s13104-016-1936-3

Received: 1 June 2015

Accepted: 12 February 2016

Published: 23 February 2016

Abstract

Background

Hepatitis C virus (HCV) is a major health concern where about 3 % of the world’s population is infected globally. In Ethiopia the prevalence ranges from 0.9 to 1.3 % in the general populations. Human immune deficiency virus (HIV) patients due to their weak immune response are heavily affected by the virus. There is no data on magnitude and associated risk factors for HCV infection among voluntary counseling, testing center and anti retroviral treatment clinic Attendants in the study area. Therefore, the aim of this study was to determine the sero-prevalence and associated risk factors for HCV infection among voluntary counseling testing and anti retroviral treatment clinic attendants Adwa general hospital.

Methods

Cross sectional study was carried out among 302 participants (151 HIV-negative from VCT and 151 HIV-positive from ART follow up) clinics of Adwa hospital from September to December, 2014. About 5 ml of venous blood samples were collected from study participants for anti HCV antibody tests. Univariate analyses were used to identify associated variables with anti HCV positivity. Variables having p < 0.05 were considered as statistically significant association.

Results

Out of the total 302 participants, 52.6 % of them were females and 47.4 % males. The mean age of the participants was 34.1 year (SD ± 10.5). The overall sero-prevalence of HCV in this study was 4.3 %. The prevalence HCV (6.6 %) was higher among the ART clinic attendants than the VCT (2 %) clinic attendants. History of hospitalization (p = 0.001), tooth extraction (p = 0.018) and blood transfusion (p = 0.041) showed statistically significant association with anti-HCV antibody.

Conclusion

HCV sero-prevalence in this study was high. The prevalence was three fold higher among HIV positive patients than their counter parts. Thus, screening of HCV should be done among HIV patients for close monitoring and better management in HIV patients.

Keywords

HCV Sero-prevalence Risk factors VCT clinic ART clinic Adwa hospital

Background

Infection with hepatitis C virus (HCV) is a major cause of chronic hepatitis, cirrhosis, and hepato cellular carcinoma around the world [1]. About 3 % of the world’s population have HCV with 170 million chronic carriers at risk of developing liver cirrhosis, and annual new infection rate of four million [2]. The prevalence of HCV is higher in developing nation like the sub-Saharan Africa [3].

Above 80 % of the HCV exposed individuals become chronically carriers, and 30 % of them develop chronic liver disease [4]. High-risk groups who have exposure with blood or blood products, like intravenous drug use, patients with pediatric hematologic malignancies, long term haemo-dialysis, with organ transplantation, infants born to HCV positive mothers and un-protective sex are highly infected with HCV [5].

Due to the similar routes of transmissions and exposure, HIV patients are highly infected with HCV; as a result there are about four to five million HIV/HCV co-infection globally [4]. As HIV virus declines the immune response of the patients to HCV, this results in lower viral clearance of HCV infection, increased levels of HCV RNA in the blood, rapid progression to HCV-related end stage liver disease and increased risk of antiretroviral associated liver toxicity [6]. These HCV related complication in HIV patients highlights the importance of timely and appropriate diagnosis and treatment to prevent further spread of HCV infections and improve their quality of life [7].

Hence, magnitude of HCV infections in patient populations in different areas and risk factors for the transmission should be investigated to take measures for reduction of such transmission in the populations. In Ethiopia there are few studies done on prevalence of hepatitis infections [815] and HCV/HIV co-infection [1619].

Although screening based on antibody detection could markedly reduce the risk of HCV infection [20], little emphasis is given for viral hepatitis co-infections in HIV patients in Ethiopia and recent ART guidelines don’t recommend routine screening tests for HCV [21], rather recommends only for alanine amino transferase (ALT) levels test to determine liver related complications among HIV patients. The magnitude of HCV among HIV positive and negative participants and its associated risk factors isn’t known in the study area. Therefore this study was aimed to fill the existing knowledge gap on HCV prevalence in the study area.

Methods

Study design, study period and sample size determination

Prospective cross-sectional study was conducted from September to December, 2014 at Adwa hospital which is located in Central Zone of Tigray regional state, northern Ethiopia. Three hundred two study participants (151 HIV-negative from VCT and 151 HIV-positive subjects in ART follow up) were enrolled in the study. Adwa town is located at longitude and latitude of 14°15′N and 38°54′E at an elevation of 1907 meters above sea level. It is 1006 km north of Addis Ababa (the capital city of Ethiopia) and 223 km far from North–West of Mekelle, the capital city of Tigray national regional state. Adwa General hospital covers four catchment Woredas and serves for an estimated population of more than 970,644. Adwa general hospital is the main center for ART and VCT center in the zone.

Sample size determination

The sample size was calculated using a double proportion formula by considering the seroprevalence of HCV in HIV positive (p1) and HIV negative study participants (p2) which is 9.2 and 1.58 %, respectively Hadush et al. 2013 [18]. Using the following formula:
$${\text{n}}1 = {\text{n}}2 = \frac{{\left( {{\text{Z}}\upalpha/2 \sqrt {\left( {1 + \frac{1}{\text{r}}} \right)} \overline{\text{pq}} + {\text{Z}}\beta \sqrt {{\text{p}}1{\text{q}}1 + \frac{{{\text{p}}2{\text{q}}2}}{\text{r}}} } \right)^{2} }}{{\left( {{\text{p}}1 - {\text{p}}2} \right)^{2} }}$$
\({\bar{\text{p}}} = \frac{{{\text{p}}1 + {\text{p}}2}}{2}\) average proportion, \({\bar{\text{q}}} = 1 - {\bar{\text{p}}}\)r = Ratio of HIV positive to HIV negative individuals = n1/n2 = 1 for equal sample size.

P1 = Prevalence of HCV among HIV positive individuals.

P2 = Prevalence of HCV among HIV negative individuals.

\({\text{Z}}\upalpha/2\) = The z-score corresponding to the probability with which it is desirable to be able to conclude that an observed difference of size (p1 − p2) of variables between HIV positive and HIV negative individuals will not occur by chance = 1.96.

Zβ = the score corresponding to the degree of confidence with which it is desired to certain of detecting a difference size (p1 − p2) between variables of that actively present = 0.84.
$${\bar{\text{p}}} = \frac{{{\text{p}}1 + {\text{p}}2}}{2} = \frac{0.092 + 0.0158}{2} = 0.0539$$
$${\bar{\text{q}}} = 1 - {\bar{\text{p}}} = 1 - 0.0539 = 0.9461$$
p1 = 0.092 and q1 = 0.908
p2 = 0.0158 and q2 = 9842
$${\text{n}}1 = {\text{n}}2 = \frac{{\left( {1.96\sqrt {1 + \frac{1}{1}} \left( {0.0539 \times 0.9461} \right) + 0.84\sqrt {\left( {0.092 \times 0.908} \right) + \left( {\frac{0.0158 \times 0.9842}{1}} \right)} } \right)^{2} }}{{\left( {0.092 - 0.0158} \right)^{2} }}$$
\({\text{n}}1 = {\text{n}}2 = \frac{0.79273}{0.005806} = 137\) from each group with a total of 274 participants. However, to increase the power of the study we added 10 % contingency, \(137 \, \times \frac{10}{100} = \sim14\), and 14 + 137 = 151 in each group with a total of 302 participants.

Inclusion and exclusion criteria

All HAART naive adult HIV positive study participants who visited ART clinic for their pre ART follow up and other laboratory investigation during the study period were included in the study. Individuals who visited VCT clinic and sero negative for HIV testing regardless of other risk factors during the study period were included in the study. Children, and individuals who refused and unable to give informed consent were excluded from the study.

Data collection procedure

Socio-demographic data and risk factors such as, drug injection, dental procedure, surgery, blood transfusion, hospitalization, history of tattooing, scarification, multiple sexual partners, abortion, STI and visiting traditional healers were collected using standard questioner by clinical nurses working in the hospital.

Blood sample collection and processing

Approximately 5 ml of venous blood was collected using vacationer tube and then serum was separated by centrifugation at 3000 rpm for 10 min. Clear non-hemolysed serum specimens were tested for HCV by Anti-HCV Rapid Test kits (Zhejiang Orient Gene Biotech Co.LTD, China) according to the manufacturer’s instruction. The presence of antibodies to HIV for the VCT attendants was determined using the standard methods available to determine the test in the hospital.

Quality control and data analysis

The Quality of the study was maintained by strictly following standard operational procedures during laboratory investigation. Internal quality control was done using known anti-HCV-antibody positive and anti-HCV-antibody negative samples. The data was entered and analyzed using SPSS version 20.0 statistical software. Chi square test (χ2) was used to see the association with HCV and p value of less than 0.05 was considered as statistically significant.

Ethical consideration

Ethical clearance was obtained from the Ethical Review committee of the College of Health Science, Mekelle University (Ref. no: ERC 0459/2014). Official letter of permission was obtained from Tigray Regional Health Bureau and Adwa General Hospital. Written consent was obtained from all study participants. Confidentiality was kept and participants who were found to be positive for HCV were communicated by the health care workers for further management.

Results

Socio-demographic and sero-prevalence of HCV among participants

Among the total 302 study participants of VCT and ART clinics (response rate 100 %), 52.6 % of them were females and 47.4 % were males. The mean age of participants was 34.1 years (SD ± 10.5). One hundred and nineteen (39.4 %) of the participants were in the age range of 18–29 years. Fifty percent of the study participants were single, and 47.0 % of them have attained secondary school or above.

The overall seroprevalence of anti-HCV antibody in this current study was 13 (4.3). HCV prevalence was relatively higher in the age group of 40–49 years and in male, but not statistically significant (p > 0.5). Similarly higher sero-prevalence was seen among divorced, farmers and illiterate participants but not statistically significant (Table 1). In this study, HCV infection was higher in HIV positive patients 10 (6.6 % than the negative 3 (2 %) patients (Table 2).
Table 1

Seroprevalence of HCV by socio-demographic variables among VCT and ART clinic attendants in Adwa general hospital from September to December, 2014

Variables

HCV-antibody

χ2

p value

Positive no (%)

Negative no (%)

Total no (%)

Age group

 18–29

4 (3.4)

115 (96.6)

119 (39.4)

0.975

0.807

 30–39

4 (4.3)

58 (93.5)

62 (20.5)

  

 40–49

4 (6.5)

26 (96.3)

27 (8.9)

  

 ≥50

1 (3.7)

90 (95.7)

119 (39.4)

  

Sex

 Male

7 (4.9)

136 (95.1)

143 (47.4)

0.038

0.845

 Female

6 (3.8)

153 (96.2)

159 (52.6)

  

Marital status

 Married

3 (2.9)

99 (97.1)

102 (33.8)

  

 Single

7 (4.6)

145 (95.4)

152 (50.3)

  

 Divorced

2 (6.9)

27 (93.1)

29 (9.6)

1.009

0.799

 Widowed

1 (5.0)

18 (94.7)

19 (6.3)

  

Educational status

 Illiterate

4 (7.4)

50 (92.6)

54 (17.9)

  

 Elementary school

5 (4.7)

101 (95.3)

106 (35.1)

2.069

0.355

 High school and above

4 (2.8)

138 (97.2)

142 (47.0)

  

Occupational category

 Unemployed

4 (4.2)

91 (95.8)

95 (31.5)

  

 Private employee

5 (4.7)

102 (95.3)

107 (35.4)

  

 Government

1 (2.6)

38 (97.4)

39 (12.9)

0.382

0.996

 Farmer

1 (5.0)

19 (95.0)

20 (6.6)

  

 House wife

1 (4.8)

20 (95.2)

21 (7.0)

  

 Sex worker

1 (5.0)

19 (95.0)

20 (6.6)

  
Table 2

Comparison of HIV/HCV coinfection between VCT and ART clinics at Adwa hospital (September to December, 2014.)

HIV status

HCV-antibody

χ2

p value

Positive N (%)

Negative N (%)

Total no (%)

Positive

10 (6.6)

141 (93.4)

151 (50)

4.146

0.085

Negative

3 (2.0)

148 (98.0)

151 (50)

Total

13 (4.3)

289 (96.7)

302 (100)

Associated risk factors and HCV sero-prevalence

In this study, previous history of hospitalization (χ2 = 15.635, p = 0.001), tooth extraction (χ2 = 5.569, p = 0.018) and blood transfusion (χ2 = 4.349, p = 0.041) have shown a statistically significant association with sero-prevalence of HCV. Dental procedure, surgery, multiple sexual partners, history of abortion, STI and visiting traditional healers however; showed no statistically significant association with HCV infection (p > 0.05) (Table 3).
Table 3

Univariate analysis of HCV sero-prevalence by risk factors among VCT and ART clinic attendants in Adwa general hospital from September to December, 2014

Risk factors

HCV-antibody

χ2

p value

Positive N (%)

Negative N (%)

Total N (%)

Tattooing/scarification

 Yes

3 (10.0)

27 (90.0)

30 (9.9)

2.018

0.128

 No

10 (3.7)

262 (96.3)

272 (90.1)

  

Unsafe injection

 Yes

2 (12.5)

14 (87.5)

16 (5.3)

1.908

0.146

 No

11 (3.8)

275 (96.2)

286 (94.7)

  

Visiting traditional healers

 Yes

2 (7.7)

24 (92.3)

26 (8.6)

0.662

0.310

 No

11 (4.0)

265 (96.0)

276 (91.4)

  

Hospitalization

 Yes

10 (12.8)

68 (87.2)

78 (25.8)

15.635

0.001

 No

3 (1.3)

221 (98.7)

224 (74.2)

  

Tooth extraction

 Yes

4 (15.4)

22 (84.6)

26 (8.6)

5.569

0.018

 No

9 (3.3)

267 (96.7)

276 (91.4)

  

Surgical operation

 Yes

2 (8.7)

21 (91.3)

23 (7.6)

0.931

0.259

 No

11 (3.9)

268 (96.1)

279 (92.4)

  

Blood transfusion

 Yes

2 (25.0)

6 (75.0)

8 (2.6)

4.349

0.041

 No

11 (3.7)

283 (96.3)

294 (97.4)

  

Occupational exposure to blood

 Yes

1 (8.3)

11 (91.7)

12 (4.0)

0.395

0.416

 No

12 (4.1)

278 (95.9)

290 (96.0)

  

Multiple sexual partners

 Yes

4 (6.6)

57 (93.4)

61 (20.2)

0.850

0.305

 No

9 (3.7)

232 (96.3)

241 (79.8)

  

STI

 Yes

3 (9.4)

29 (90.6)

32 (10.6)

1.761

0.148

 No

10 (3.7)

260 (96.3)

270 (89.4)

  

Abortion

 Yes

2 (6.9)

27 (93.1)

29 (9.6)

0.815

0.301

 No

4 (3.1)

126 (96.9)

130 (90.4)

  

Discussion

Sero-prevalence of HCV among HIV negative and HIV positive in this study was (4.3 %, with prevalence rate of 2 and 6.6 % in HIV negative and HIV positive participants respectively. The overall sero-prevalence of HCV in this study (4.3 %) was comparable with results from Burkina Faso 5.4 % [22], Malawi 4.5 % [23] and Ghana 3.6 % [24], however, it was higher than reports from Addis Ababa, 0.9 % [17] and Debretabor, South Gondar 1.3 % [12]. Higher value of prevalence than our result was reported from other parts of Ethiopia, Mekelle, 6 % [18] and South Gondar 7.5 % [8].

HCV/HIV coinfection rate in this study, 6.6 % was comparable with the studies done in Gonder, 5.0 % [25], Mekelle, 8.6 % [18], Nigeria, 8.2 % [26] and Malawi, 5.7 % [27]. Our result was however; higher than reports from other parts of Ethiopia like Debretabor Hospital, South Gondar, 1.3 % [12], Bahir Dar, 5.5 % [15], Northwest Ethiopia, 1.7 % [13], and Burkina Faso, 4.8 % [22], Malawi, 4.5 % [23], Zimbabwe, 0.8 % [28], Zambia, 2.2 % [29], Rwanda 4.9 % [30], Ghana, 3.6 % [24], SouthAfrica, 1 % [31], Gambia, 0.6 % [32], Zambia, 1.2 % [33], Senegal, 1.6 % [34], Uganda, 3.3 % [35] and Cote D’voir, 1.2 % [36].

Higher HCV/HIV coinfection was documented from Hawassa, South Ethiopia, 9.2 % [19] and Addis Ababa, 11.6 % [17], Cameroon, 8.6 % [37] and Kenya, 10.3 % [38].

These variations could be due to differences in geographic regions, types of risk exposure and methodology used [39, 40]. The higher HCV co-infection rate in HIV patients in this study and other places could be due to the shared modes of transmission of both viruses in the study patients [17, 41]. Hence investigation of HCV in HIV-positive patients is crucial to prevent them from further infections and complications [42].

HCV prevalence among VCT clinic attendants in this current study (2 %) was comparable with results from Mekelle, Ethiopia, 1.65 % [18]; but lower than that of Addis Ababa (5 %) [16].

There was no statistically significant association between sero-prevalence rate of HCV and marital status, educational status and occupational status of the participants (p > 0.05). This was in line with finding by of other researchers from Zambia [33] and Gonder [25].

However, hospitalization, tooth extraction and blood transfusion showed statistically significant association with HCV infection (p < 0.05). This was supported by other reports from Ethiopia [12, 18]. On the other hand, these variables were not significantly associated with HCV infection in the study conducted in Hawassa [19] and Addis Ababa [17]. None of the HCV antibody positive study participants had history of intravenous drug use. This might be due to the fact that it is uncommon practice in the study area.

Limitation

Rapid test kit was used to detect anti HCV prevalence, hence may not detect early HCV infections like what the ELISA and PRC tests do.

Conclusion

The overall sero prevalence of HCV in this study was high; hospitalization, tooth extraction and blood transfusion were significantly associated with HCV infection. The prevalence was three times higher among HIV positive than their counter parts. Therefore, routine screening programme of HCV infection in HIV-infected patients is should be in place for the better management of the patients and prevent them from further complications. Implementation of more effective public health education and counseling on the risk factors should be given to reduce the burden of HIV/HCV co-infection.

Declarations

Authors’ contributions

AH: conceived, designed and proposed the research idea, data collection, data entry, clearance, analysis and interpretation of the findings and drafting the manuscript. TA, designed the methodology, analyzed data and prepared the initial version of the manuscript, RB and KG: designed the methodology and analyzed data. AG and SM: designed the methodology, prepared the initial and final version of the manuscript for publication. All authors read and approved the final manuscript.

Acknowledgements

We would like to thank Mekelle University, College of Health Science for the financial support. We are also grateful to Mr. Teklit Gebremeskel for his technical support in the blood bank during data collection. 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 Adwa General Hospital laboratory personnel for their consistent support with reagents and other materials during data collection.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Medical Microbiology and Immunology, Institute of Biomedical Science, College of Health Sciences, Mekelle University
(2)
Tigray Regional Health and Research Laboratory

References

  1. Maheshwari A, Thulvath PJ, Ray S. Acute hepatitis C virus. Lancet. 2008;372:321–32.View ArticlePubMedGoogle Scholar
  2. Chen SL, Morgan TR. The natural history of hepatitis C virus (HCV) infection. Int J Med Sci. 2006;3:47–52.PubMed CentralView ArticlePubMedGoogle Scholar
  3. Thomas DL, Leoutsakas D, Zabransky T, et al. Hepatitis C in HIV-infected individuals: cure and control, right now. Int AIDS Soc. 2011;14:22. doi:https://doi.org/10.1186/1758-2652-14-22.View ArticleGoogle Scholar
  4. Sultan MT, Rahman MM, Begum S. Epidemiology of hepatitis C virus (HCV) infection. J Bangladesh Coll Phy Surg. 2009;27:160–2.Google Scholar
  5. Murray KF, Richardson LP, Morishima C, et al. Prevalence of hepatitis C virus infection and risk factors in an incarcerated juvenile population: a pilot study. Pediatrics. 2003;111:153–7.View ArticlePubMedGoogle Scholar
  6. Madhava V, Burgess C, Drucker E. Epidemiology of chronic hepatitis C virus infection in sub-Saharan Africa. Lancet Infect Dis. 2002;2:293–302.View ArticlePubMedGoogle Scholar
  7. Perz JF, Armstrong GL, Farrington LA, Hutin JF, Bell BP. The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol. 2006;45:529–38.View ArticlePubMedGoogle Scholar
  8. Balew M, Moges F, Yismaw G, Unakal C. Assessment of hepatitis B virus and hepatitis C virus infections and associated risk factors in HIV infected patients at Debretabor hospital, South Gondar, Northwest Ethiopia. Asian Pac J Trop Dis. 2014;4(1):1–7.PubMed CentralView ArticleGoogle Scholar
  9. Shimelis T, Torben W, Medhin G, Tebeje M, Andualm A, Demessie F, et al. Hepatitis B virus infection among attendants of VCT and ART clinic of St Paul’s General Specialized Hospital, Addis Ababa, Ethiopia. Sex Transm Infect. 2007;84:37–41.View ArticlePubMedGoogle Scholar
  10. Negero A, Sisay Z, Medhin G. Prevalence of Hepatitis B surface antigen (HBsAg) among visitors of Shashemene General Hospital voluntary counseling and testing center. BMC Res Notes. 2011;4:35.PubMed CentralView ArticlePubMedGoogle Scholar
  11. Moges F, Kebede Y, Kassu A, Mulu A, Tiruneh M, Degu G, et al. Prevalence of HIV, hepatitis B infections and syphilis among street dwellers in Gondar city, northwest Ethiopia. Ethop J Health Dev. 2006;20:160–5.Google Scholar
  12. Balew M, Moges F, Yismaw G, Unakal C. Assessment of hepatitis B virus and hepatitis C virus infections and associated risk factors in HIV infected patients at Debretabor hospital, South Gondar, northwest Ethiopia. Asian Pac J Trop Dis. 2014;4(1):1–7.PubMed CentralView ArticleGoogle Scholar
  13. Gelaw B, Mengistu Y. The prevalence of HBV, HCV& malaria parasites among blood donors in Amhara and Tigray regional states. Ethiop J Health Dev. 2007;22:3–7.Google Scholar
  14. Tiruneh M. Seroprevalence of multiple sexually transmitted infections among antenatal clinic attendees in Gondar Health Center, northwest Ethiopia. Ethiop Med J. 2008;46(4):359–66.PubMedGoogle Scholar
  15. Abera B, Zenebe Y, Mulu W, Kibret M, Kahsu G. Seroprevalence of hepatitis B and C iruses and risk factors in HIV infected children at the Felgehiwot referral hospital, Ethiopia. BMC Res Notes. 2014;25(7):838. doi:https://doi.org/10.1186/1756-0500-7-838.View ArticleGoogle Scholar
  16. Tessema B, Yismaw G, Kassu A, Amsalu A, Mulu A, Emmrich F, Sack U. Seroprevalence of HIV, HBV, HCV and syphilis infections among blood donors at Gondar University Teaching Hospital, Northwest Ethiopia: declining trends over a period of five years. BMC Infect Dis. 2010;10:111.PubMed CentralView ArticlePubMedGoogle Scholar
  17. Ayele W, Nokes DJ, Abebe A, et al. Higher prevalence of anti-HCV antibodies among HIV positive compared to HIV-negative inhabitants of Addis Ababa, Ethiopia. J Med Virol. 2002;68:12–7.View ArticlePubMedGoogle Scholar
  18. Hadush H, Gebreslassie S, Mihret A. Hepatitis C virus and Human immunodeficiency virus (HIV) co-infection among attendants of voluntary counseling and testing (VCT) and ART follow up clinic at Mekelle hospital. Pan Afr med J. 2013;14:107.PubMed CentralView ArticlePubMedGoogle Scholar
  19. 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 Res Notes. 2011;4:193. doi:https://doi.org/10.1186/1756-0500-4-193.PubMed CentralView ArticlePubMedGoogle Scholar
  20. Lauer GM, Walker BD. Hepatitis C virus infection. N Engl J Med. 2001;345:41–52.View ArticlePubMedGoogle Scholar
  21. Federal Ministry of Health. Guidelines for management of opportunistic infections and anti retroviral treatment in adolescents and adults in Ethiopia. Federal ministry of Health; 2007.Google Scholar
  22. Simpore J, Savadogo A, Ilboudo D, Nadambega C, Esposito M, Yara J, et al. Toxoplasma gondii, HCV and HBV seroprevalence and co-infection among HIV positive and negative pregnant women in Burkina Faso. J Med Virol. 2006;78:730–3.View ArticlePubMedGoogle Scholar
  23. Nyirenda M, Beadsworth M, Stephany P, Hart C, Hart I, Munthali C, et al. Prevalence of infection with hepatitis B and C virus and co-infection with HIV in medical inpatients in Malawi. J Infect Dis. 2008;57:72–7.Google Scholar
  24. Sagoe KW, Agyei AA, Ziga F, Lartey M, Adiku TK, Seshi M. Prevalence and impact of hepatitis B and C virus co-infections in antiretroviral treatment naive patients with HIV infection at a major treatment center in Ghana. J Med Virol. 2012;84:6–10.View ArticlePubMedGoogle Scholar
  25. Wondimeneh Y, Alem M, Asfaw F, Belyhun Y. 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. Virol J. 2013;10:171.PubMed CentralView ArticlePubMedGoogle Scholar
  26. Agwale SM, Tanimoto L, Womack C, et al. Prevalence of HCV coinfection in HIV infected individuals in Nigeria and characterization of HCV genotypes. J Clin Virol. 2004;31:S3–6.View ArticlePubMedGoogle Scholar
  27. Moore E, Beadsworth MB, Chaponda M, Mhango B, Faragher B, Njala J, Hofland HW, Davies J, Hart IJ, Beeching NJ, Zijlstra EE, van Oosterhout JJ. Favourable one-year ART outcomes in adult Malawians with hepatitis B and C co-infection. J Infect. 2010;61(2):155–63.View ArticlePubMedGoogle Scholar
  28. Kallestrup P, Zinyama R, Gomo E, Dickmeiss E, Platz P, Gerstoft J, Ullum H. Low prevalence of hepatitis C virus antibodies in HIV-endemic area of Zimbabwe support sexual transmission as the major route of HIV transmission in Africa. AIDS. 2003;17(9):1400–2.View ArticlePubMedGoogle Scholar
  29. Kapembwa KC, Goldman JD, Lakhi S, Banda Y, Bowa K, Vermund SH, Mulenga J, Chama D, Chi BH. HIV, hepatitis B, and hepatitis C in Zambia. J Global Infect Dis. 2011;3:269–74.View ArticleGoogle Scholar
  30. Pirillo MF, Bassani L, Germinario EA, Mancini MG, Vyankandondera J, Okong P, Vella S, Giuliano M. Seroprevalence of hepatitis B and C viruses among HIV-infected pregnant women in Uganda and Rwanda. J Med Virol. 2007;79(12):1797–801.View ArticlePubMedGoogle Scholar
  31. Otedo AE. HBV, HIV co-infection at Kisumu district hospital, Kenya. East Afr Med J. 2004;81(12):626–30.PubMedGoogle Scholar
  32. Mboto CI, Fielder M, Russell A, Jewell AP. Prevalence of HIV-1, HIV-2, hepatitis C and co-infection in the Gambia. West Afr J Med. 2009;28:306–9.Google Scholar
  33. Kapembwa KC, Goldman JD, Lakhi S, Banda Y, Bowa K, Vermund SH. HIV, hepatitis B and hepatitis C in Zambia. J Global Infect Dis. 2011;3(3):269–74.View ArticleGoogle Scholar
  34. Diop-Ndiaye H, Touré-Kane C, Etard JF, Lô G, Diaw P, Ngom-Gueye NF, Gueye PM, Ba-Fall K, Ndiaye I, Sow PS, Delaporte E, Mboup S. Hepatitis B, C seroprevalence and delta viruses in HIV-1 Senegalese patients at HAART initiation. J Med Virol. 2008;80(8):1332–6.View ArticlePubMedGoogle Scholar
  35. Walusansa V, Kagimu M. Screening for hepatitis C among HIV positive patients at Mulago Hospital in Uganda. J Afr Health Sci. 2009;9:143–6.Google Scholar
  36. Rouet F, Chaix ML, Inwoley A, Msellati P, Viho I, Combe P, Leroy V, Dabis F, Rouzioux C. ANRS 1236 DITRAME-B&C study group. HBV and HCV prevalence and viraemia in HIV-positive and HIV-negative pregnant women in Abidjan, Côte d’Ivoire: the ANRS 1236 study. J Med Virol. 2004;74(1):34–40.View ArticlePubMedGoogle Scholar
  37. Kim S, Hu J, Gautom R, et al. HIV and Hepatitis C virus coinfection, Cameroon. Emerg Infect Dis. 2007;13:248–60.View ArticleGoogle Scholar
  38. Muriuki MB, Gicheru MM, Wachira D, Nyamache KA, Khamadi AS. Prevalence of hepatitis B and C viral co-infections among HIV-1 infected individuals in Nairobi. Kenya. BMC Res Notes. 2013;6:363.View ArticlePubMedGoogle Scholar
  39. 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 Afr Med J. 2000;77(1):13–5.PubMedGoogle Scholar
  40. Verucchi G, Calza L, Manfredi R, et al. HIV and HCV coinfection epidemiology, natural history, therapeutic options, and clinical management. Infection. 2004;32:33–46.View ArticlePubMedGoogle Scholar
  41. Frommel D, Tekle-Haimanot R, Berhe N, Aussel L, Verdier M, Preux PM, et al. A survey of antibodies to hepatitis C virus in Ethiopia. Am J Trop Med Hyg. 1993;49:435–9.PubMedGoogle Scholar
  42. Mohammadi M, Talei G, Sheikhian A, Ebrahimzade F, Pournia Y, Ghasemi E. Survey of both hepatitis B virus (HBsAg) and hepatitis C virus (HCV-Abs) co-infection among HIV patients. Virol J. 2009;6:202. doi:https://doi.org/10.1186/1743-422X-6-202.PubMed CentralView ArticlePubMedGoogle Scholar

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