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RESEARCH ARTICLE

Co-Infection Burden of Hepatitis C Virus and Human Immunodeficiency Virus among Injecting Heroin Users at the Kenyan Coast Ruth S. Mwatelah1,2,3, Raphael M. Lwembe4, Saida Osman4, Bernhards R. Ogutu1,5,6, Rashid Aman1,6,7, Rose C. Kitawi1,2,3, Laura N. Wangai3, Florence A. Oloo1,8, Gilbert O. Kokwaro6, Washingtone Ochieng1,4,6* 1 Centre for Research in Therapeutic Sciences, Strathmore University, Nairobi, Kenya, 2 Institute of Tropical Medicine and Infectious Diseases, Nairobi, Kenya, 3 Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya, 4 Centre for Virus Research, Kenya Medical Research Institute, Nairobi, Kenya, 5 Centre for Clinical Research, Kenya Medical Research Institute, Nairobi, Kenya, 6 Institute of Healthcare Management, Strathmore University, Nairobi, Kenya, 7 African Center for Clinical Trials, Nairobi, Kenya, 8 Technical University of Kenya, Nairobi, Kenya * [email protected]

OPEN ACCESS Citation: Mwatelah RS, Lwembe RM, Osman S, Ogutu BR, Aman R, Kitawi RC, et al. (2015) CoInfection Burden of Hepatitis C Virus and Human Immunodeficiency Virus among Injecting Heroin Users at the Kenyan Coast. PLoS ONE 10(7): e0132287. doi:10.1371/journal.pone.0132287 Editor: Anil Kumar, University of Missouri-Kansas City, UNITED STATES Received: March 21, 2015 Accepted: June 11, 2015 Published: July 24, 2015 Copyright: © 2015 Mwatelah et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper. Funding: This study was funded partly by the Consortium for National Health Research (CNHR; www.cnhrkenya.org), Grant# RCDG-2012-005 awarded to WO and partly by Internal Research Grant from the Kenya medical Research Institute (KEMRI; www.kemri.org), Grant# IRG51/2 awarded to RML. Competing Interests: The authors have declared that no competing interests exist.

Abstract Background Injection drug use is steadily rising in Kenya. We assessed the prevalence of both human immunodeficiency virus type 1 (HIV-1) and hepatitis C virus (HCV) infections among injecting heroin users (IHUs) at the Kenyan Coast.

Methods A total of 186 IHUs (mean age, 33 years) from the Omari rehabilitation center program in Malindi were consented and screened for HIV-1 and HCV by serology and PCR and their CD4 T-cells enumerated by FACS.

Results Prevalence of HIV-1 was 87.5%, that of HCV was 16.4%, co-infection was 17.9% and 18/ 152 (11.8%) were uninfected. Only 5.26% of the HIV-1 negative injectors were HCV positive. Co-infection was higher among injectors aged 30 to 40 years (20.7%) and among males (22.1%) than comparable groups. About 35% of the injectors were receiving antiretroviral treatment (ART). Co-infection was highest among injectors receiving D4T (75%) compared to those receiving AZT (21.6%) or TDF (10.5%) or those not on ART (10.5%). Mean CD4 T-cells were 404 (95% CI, 365 - 443) cells/mm3 overall, significantly lower for co-infected (mean, 146; 95% CI 114 – 179 cells/mm3) than HIV mono infected (mean, 437, 95% CI 386 – 487 cells/mm3, p40 years. By genders, 18/95 (18.9%) and 77/95 (81.1%) males and 7/57 (12.3%) and 98.2% females were HCV and HIV positive respectively. Nine of 53 HIV positive injectors aged 30 years and below were also positive for HCV, constituting 17% prevalence of dual infection in this age group. Dual infection was 20.7% for injectors aged 31–40 years, 13.6% for injectors above 40 years old, 22.1% among males and 14.3% among females. Assessed differently, HIV infection was 96% among the 25 HCV positive injectors and Table 1. Baseline demographic and infection characteristics of subjects. Number, N; %N

Number, N; %N

HCV+

HCV-

N, %T

HIV+

HIV-

N, %T

< = 30 years

9; 15

51; 85

60; 39.5

64; 84.2

12; 15.8

76; 40.9

31–40 years

13; 19.4

54; 80.6

67; 44.1

68; 86.1

11; 13.9

79; 42.5

>40 years

3; 12

22; 88

25; 16.4

27; 87.1

4; 12.9

31; 16.7

AZT+3TC+NVP/EFV

11; 21.6

40; 78.4

51; 33.6

52; 100

0; 0

52; 28

D4T+3TC+NVP/EFV

3; 75

1; 25

4; 2.6

7; 100

0; 0

7; 3.8

TDF+3TC+NVP/EFV

0; 0

4; 100

4; 2.6

6; 100

0; 0

6; 3.2

Cotrimoxazole

4; 15.4

22; 84.6

26; 17.1

44; 100

0; 0

44; 23.7

No ART

1; 5.3

18; 94.7

19; 12.5

0; 0

27; 100

27; 14.5

ART unknown

6; 14.3

36; 85.7

42; 27.6

43; 100

0; 0

43; 23.1

Sub-optimal ART

0; 0

6; 100

6; 3.9

7; 100

0; 0

7; 3.8

Male

18; 18.9

77; 81.1

95; 62.5

90; 77.6

26; 22.4

116; 62.4

Female

7; 12.3

50; 87.7

57; 37.5

69; 98.6

1; 1.4

70; 37.6

Total, T

25; 16.4

127; 83.6

152; 100

159; 85.5

27; 14.5

186; 100

Age

Treatment arm

Gender

Antiretroviral treatment arms: AZT, Zidovudine; D4T, Stavudine; TDF, Tenofovir; 3TC, Lamivudine; NVP, nevirapine; EFV, efavirenz. IHUs in the suboptimal ART arm were actively taking one or both NVP or EFV instead of the standard 3-drug ART regimen. doi:10.1371/journal.pone.0132287.t001

PLOS ONE | DOI:10.1371/journal.pone.0132287 July 24, 2015

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HIV and HCV Co-Infection of Injecting Drug Users in Malindi

Table 2. Prevalence of HIV-1 and HCV mono and dual infections among heroin injectors. HIV-1 status: N, % Positive (+) Category < = 30 years

Negative (-)

Total, %

HCV status +

9, 17

0, 0

9, 15

-

44, 83

7, 100

51, 85

31–40 years

+

12, 20.7

1, 11.1

13, 19.4

-

46, 79.3

8, 88.9

54, 80.6

>40 years

+

3, 13.6

0, 0

3, 12

-

19, 86.4

3, 100

22, 88

33.17

32.95

33.14

+

17, 22.1

1, 5.6

18, 18.9

-

60, 77.9

17, 94.4

77, 81.1

+

7, 12.5

0, 0

7, 12.3

-

49, 87.5

1, 100

50, 87.3

+

14, 23.3

0, 0

14, 23.3

-

45, 76.3

0, 0

45, 76.3

+

4, 15.4

0, 0

4, 15.4

-

22, 84.6

0, 0

22, 84.6

+

0, 0

1, 5.3

1, 5.3

-

0, 0

18, 94.7

18, 94.7

+

6, 14.3

0, 0

6, 14.3

-

36, 85.7

0, 0

36, 85.7

+

0, 0

0, 0

0, 0

-

6, 100

0, 0

6, 100

+

24, 18

1, 5.3

25, 16.4

-

109, 82

18, 94.7

127, 83.5

Total, N, %

133, 100

19, 100

152, 100

33.17

32.95

33.14

Mean age, years Males Females Receiving ART* Cotrimoxazole No ART ART unknown Sub-optimal ART Overall

Mean age, years

*ART recipients had initiated first-line AZT, D4T or TDF triple regimen arms that included 3TC and either NVP or EFV. doi:10.1371/journal.pone.0132287.t002

85.8% (109/127) for HCV negative injectors. When the 152 injectors screened for HCV were grouped by ART regimen arm, 11 of 51 (21.6%) receiving AZT, 3 of 4 (75%) receiving D4T, none (0/4) receiving TDF and 10/93 (10.5%) with no or unknown ART statuses were coinfected by both HIV and HCV. Taken together, majority of IHUs in the Omari cohort were HIV positive. The prevalence of HCV infection was comparable across all age groups, but slightly high among those older than 30 years who were also HIV positive and higher among male than female injectors. A Chi square analysis was modeled to assess associations between infection status and either age or gender. Using this approach, the proportion of males that were HIV/HCV dual infected, HIV mono-infected and uninfected was 18.1%, 63.8% and 18.1% respectively. That of female IHUs was 12.3%, 86% and 1.8% respectively. Pearson’s χ2 revealed a significant association between infection status and gender (p = 0.004), suggesting that the IHUs have an increased likelihood (risk) of being infected by either viruses than not being infected. This analysis yielded no significant association comparing infection status with age group (data not shown). A χ2 test comparing treatment arms with infection status was not meaningful since IHUs in the ‘No ART’ arm were also all ‘Not infected’.

PLOS ONE | DOI:10.1371/journal.pone.0132287 July 24, 2015

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HIV and HCV Co-Infection of Injecting Drug Users in Malindi

Table 3. CD4 T-cell counts compared by various categories of heroin injectors who were screened for both HIV and HCV. Infection Status:- Mean counts; number N, 95% CI of mean HIV/HCV dual

HIV mono

Not infected

Total

Age in yr < = 30

100; 9, 48–153

479; 44, 387–570

622; 7, 542–703

439; 60, 361–516

31–40

172; 12, 127–216

396; 46, 327–465

572; 8, 426–718

376; 66, 319–434

>40

181; 3, -23–386

439; 19, 319–559

732; 3, 560–904

443; 25, 337–550

Males

140; 17, 104–176

454; 60, 374–534

619; 17, 545–692

427; 94, 366–487

Females

160; 7, 72–249

416; 49, 359–473

610; 1b

388; 57, 333–443

205; 11, 166–243

548; 40, 435–661

0a, b

474; 51, 377–570

Gender

ART arm AZT

b

a, b

D4T

54; 3, 28–80

150; 1

0

78; 4, 0.4–156

TDF

0a

607; 4, 196–1018

0a, b

607; 4, 196–1018

Cotrimoxazole

156; 4, 102–209

367; 22, 293–441

0a, b

334; 26, 265–404

No ART

0a, b

0a, b

618; 18, 549–687

618; 18, 549–687

ARTunknown

79; 6, 34–123

369; 36, 323–415

0a, b

328; 42, 277–379

293; 6, 74–512

0a, b

293; 6, 74–512

437; 109, 386–487

618; 18, 549–687

412; 151, 370–455

a, b

suboptimalART

0

Total

146; 24, 114–179

p-value†