Journal of Viral Hepatitis, 2014
doi:10.1111/jvh.12353
Decreasing prevalence of HCV coinfection in all risk groups for HIV infection between 2004 and 2011 in Spain S. Serrano-Villar,1 P. Sobrino-Vegas,2 S. Monge,2 F. Dronda,1 A. Hernando,3 M. Montero,4 P. Viciana,5 B. Clotet,6 J. A. Pineda,7 J. del Amo,2 and S. Moreno1 on behalf of CoRIS† 1
Department of Infectious Diseases, Hospital Universitario Ramon y Cajal and IRYCIS, Madrid, Spain; 2National Center of Epidemiology, Instituto de
Salud Carlos III, Madrid, Spain; 3HIV Unit, Hospital Universitario Doce de Octubre and Universidad Europea, Madrid, Spain; 4Infectious Diseases Unit, Hospital La Fe, Valencia, Spain; 5Clinical Infectious Diseases Unit, Hospital Virgen del Rocıo, Sevilla, Spain; 6HIV Unit, Hospital Germans Trias i Pujol, Barcelona, Spain; and 7Infectious Diseases Unit, Hospital Universitario de Valme, Sevilla, Spain Received August 2014; accepted for publication September 2014
SUMMARY. While hepatitis C virus (HCV) infection seems
to be expanding among HIV-infected men who have sex with men (MSM), the rate of coinfection in intravenous drug users (IDU) is assumed to remain constant. We evaluated the serial prevalence of HIV/HCV coinfection across all risk groups for HIV infection in Spain. We used data from 7045 subjects included in the multicentre, prospective Spanish Cohort of Adult HIV-infected Patients (CoRIS) between 2004 and 2011. We analysed risk factors for HIV/HCV coinfection by logistic regression analyses. The prevalence of HIV/HCV coinfection decreased from 25.3% (95% CI, 23.1–27.5) in 2004– 2005 to 8.2% (95% CI, 6.9–9.5) in 2010–2011. This trend was consistently observed from 2004 to 2011
INTRODUCTION While antiretroviral therapy (ART) represents an outstanding breakthrough in the natural history of HIV infection, the intersection among human immunodeficiency virus (HIV) and hepatitis C virus (HCV) epidemics still poses a major challenge to both patients and healthcare providers. As end-stage liver disease-related deaths increased steadily during the last decade in the general population [1], the burden of HCV-associated disease has dramatically risen among HIV-infected persons and end-stage liver disease has become a leading cause of death among people living with HIV on ART [2–6].
Abbreviations: ART, antiretroviral therapy; HCV, hepatitis C virus; IDU, intravenous drug users; MSM, men who have sex with men. Correspondence: Sergio Serrano-Villar, MD, PhD, Department of Infectious Diseases, University Hospital Ram on y Cajal, Carretera de Colmenar Viejo, Km 9.100, Madrid 28034, Spain. E-mail: [email protected] † Spanish AIDS Research Network Cohort.
© 2014 John Wiley & Sons Ltd
among all risk groups: IDU, 92.4% to 81.4%; MSM, 4.7% to 2.6%; heterosexual men, 13.0–8.9%; and heterosexual women, 14.5–4.0% (all P < 0.05). Strongest risk factors for HIV/HCV coinfection were IDU (OR, 54.9; 95% CI, 39.4–76.4), birth decade 1961–1970 (OR, 2.1; 95% CI, 1.1–3.7) and low educational level (OR, 2.4; 95% CI, 1.6–3.5). Hence, the prevalence of HIV/HCV coinfection decreased in Spain between 2004 and 2011. This decline was observed across all risk groups and is likely to be explained by a declining burden of HCV in the general population. Keywords: coinfection, HCV, HIV, injection drug use, men who have sex with men, prevalence.
Although HIV and HCV share common routes of transmission, the efficiency of HCV transmission by percutaneous exposure is much higher than that of HIV, and much lower by sexual contact. Consequently, HIV/HCV coinfection has essentially been associated to injection drug users (IDU), who become typically infected with HCV before HIV [7,8]. Importantly, several studies have determined a decline in the incidence of HCV infection both in the general population [9,10] and in people living with HIV, likely related in the latter group to a decrease in the incidence of HCV infection among IDU [11–13]. In contrast, since 2000, there is increasing awareness of an ongoing epidemic of acute HCV infection in HIV-infected MSM [14,15]. While HIV infection continues to expand in most countries among men who have sex with men (MSM) [16– 19], outbreaks of acute HCV infection in HIV-infected MSM have been reported in cities of Europe and North America [17,20,21]. Whether these outbreaks of acute HCV infection are the tip of the iceberg of an underlying real increase of HCV transmission among HIV-infected MSM or instead merely reflect microepidemics within confined groups remains debated [17,22].
2
S. Serrano-Villar et al.
We hypothesized that the serial prevalence of HIV/HCV coinfection might have stabilized or even be in ascent in MSM, and we assessed changes in serial prevalence of HIV/HCV coinfection in the three main HIV transmission groups (IDU, MSM and heterosexuals) in an ongoing prospective multicentre cohort (CoRIS) in Spain from 2004 to 2011.
Robust methods were used to estimate the confidence intervals, assuming correlation among subjects recruited within each centre and independence among subjects from different centres. The adjusted model was included those variables which in the univariate analyses showed a level of statistical significance 50 85 (13.5) Year of inclusion (N,%) 2004–2005 399 (25.3) 2006–2007 308 (17.6) 2008–2009 251 (12.6) 2010–2011 141 (8.2) CD4+ T-cell count at cohort entry (N,%) < 200 cells/lL 396 (21.1) 200–350 cells/lL 256 (17.0) >350 cells/lL 431 (12.0) HIV RNA at cohort entry (N,%) 5 log/mL 349 (15.6)
HCV N = 5946 4904 (85.5) 1042 (79.7) 3911 (81.4) 2019 (90.1) 1819 (74.8) 1981 (90.0) 1435 (95.8) 97 3605 2030 214
(13.1) (96.9) (89.1) (74.8)
828 1529 2353 1236
(79.8) (83.8) (89.1) (95.4)
2134 2222 1046 544
(92.9) (82.8) (72.8) (86.5)
1177 1438 1747 1584
(74.7) (82.4) (81.4) (91.8)
1485 (78.9) 1248 (83.0) 3172 (88.0) 1391 (82.6) 2643 (85.6) 1885 (84.4)
Data expressed as no. (%). IDU, injection drug user; MSM, men who have sex with men; HTX, heterosexual. Univariate associations and independent risk factors for HIV/HCV coinfection after multivariate analyses are represented in Fig. 3. In the multivariate analysis, factors independently associated with the prevalence of HIV/HCV coinfection at cohort entry during the whole period were transmission category (IDU vs heterosexual; OR, 54.9; 95% CI, 39.4–76.4), birth decade (1961–1970 vs >1981; OR, 2.1; 95% CI, 1.1–3.7), age at cohort entry (41–50 years vs ≤30; OR, 1.8; 95% CI, 1.1–2.9), earlier © 2014 John Wiley & Sons Ltd
Fig. 1 Changes in patterns of risk behaviors for acquisition of HIV infection. Between 2004–05 and 2010–11, significant decreases in IDU category from 19.2% to 5.6% and in the heterosexual category, from 36.4% to 21.9% were observed. The category of MSM significantly increased from 40.6% in 2004–05 to 68.6% in 2010–11 (all trend P values
doi:10.1111/jvh.12353
Decreasing prevalence of HCV coinfection in all risk groups for HIV infection between 2004 and 2011 in Spain S. Serrano-Villar,1 P. Sobrino-Vegas,2 S. Monge,2 F. Dronda,1 A. Hernando,3 M. Montero,4 P. Viciana,5 B. Clotet,6 J. A. Pineda,7 J. del Amo,2 and S. Moreno1 on behalf of CoRIS† 1
Department of Infectious Diseases, Hospital Universitario Ramon y Cajal and IRYCIS, Madrid, Spain; 2National Center of Epidemiology, Instituto de
Salud Carlos III, Madrid, Spain; 3HIV Unit, Hospital Universitario Doce de Octubre and Universidad Europea, Madrid, Spain; 4Infectious Diseases Unit, Hospital La Fe, Valencia, Spain; 5Clinical Infectious Diseases Unit, Hospital Virgen del Rocıo, Sevilla, Spain; 6HIV Unit, Hospital Germans Trias i Pujol, Barcelona, Spain; and 7Infectious Diseases Unit, Hospital Universitario de Valme, Sevilla, Spain Received August 2014; accepted for publication September 2014
SUMMARY. While hepatitis C virus (HCV) infection seems
to be expanding among HIV-infected men who have sex with men (MSM), the rate of coinfection in intravenous drug users (IDU) is assumed to remain constant. We evaluated the serial prevalence of HIV/HCV coinfection across all risk groups for HIV infection in Spain. We used data from 7045 subjects included in the multicentre, prospective Spanish Cohort of Adult HIV-infected Patients (CoRIS) between 2004 and 2011. We analysed risk factors for HIV/HCV coinfection by logistic regression analyses. The prevalence of HIV/HCV coinfection decreased from 25.3% (95% CI, 23.1–27.5) in 2004– 2005 to 8.2% (95% CI, 6.9–9.5) in 2010–2011. This trend was consistently observed from 2004 to 2011
INTRODUCTION While antiretroviral therapy (ART) represents an outstanding breakthrough in the natural history of HIV infection, the intersection among human immunodeficiency virus (HIV) and hepatitis C virus (HCV) epidemics still poses a major challenge to both patients and healthcare providers. As end-stage liver disease-related deaths increased steadily during the last decade in the general population [1], the burden of HCV-associated disease has dramatically risen among HIV-infected persons and end-stage liver disease has become a leading cause of death among people living with HIV on ART [2–6].
Abbreviations: ART, antiretroviral therapy; HCV, hepatitis C virus; IDU, intravenous drug users; MSM, men who have sex with men. Correspondence: Sergio Serrano-Villar, MD, PhD, Department of Infectious Diseases, University Hospital Ram on y Cajal, Carretera de Colmenar Viejo, Km 9.100, Madrid 28034, Spain. E-mail: [email protected] † Spanish AIDS Research Network Cohort.
© 2014 John Wiley & Sons Ltd
among all risk groups: IDU, 92.4% to 81.4%; MSM, 4.7% to 2.6%; heterosexual men, 13.0–8.9%; and heterosexual women, 14.5–4.0% (all P < 0.05). Strongest risk factors for HIV/HCV coinfection were IDU (OR, 54.9; 95% CI, 39.4–76.4), birth decade 1961–1970 (OR, 2.1; 95% CI, 1.1–3.7) and low educational level (OR, 2.4; 95% CI, 1.6–3.5). Hence, the prevalence of HIV/HCV coinfection decreased in Spain between 2004 and 2011. This decline was observed across all risk groups and is likely to be explained by a declining burden of HCV in the general population. Keywords: coinfection, HCV, HIV, injection drug use, men who have sex with men, prevalence.
Although HIV and HCV share common routes of transmission, the efficiency of HCV transmission by percutaneous exposure is much higher than that of HIV, and much lower by sexual contact. Consequently, HIV/HCV coinfection has essentially been associated to injection drug users (IDU), who become typically infected with HCV before HIV [7,8]. Importantly, several studies have determined a decline in the incidence of HCV infection both in the general population [9,10] and in people living with HIV, likely related in the latter group to a decrease in the incidence of HCV infection among IDU [11–13]. In contrast, since 2000, there is increasing awareness of an ongoing epidemic of acute HCV infection in HIV-infected MSM [14,15]. While HIV infection continues to expand in most countries among men who have sex with men (MSM) [16– 19], outbreaks of acute HCV infection in HIV-infected MSM have been reported in cities of Europe and North America [17,20,21]. Whether these outbreaks of acute HCV infection are the tip of the iceberg of an underlying real increase of HCV transmission among HIV-infected MSM or instead merely reflect microepidemics within confined groups remains debated [17,22].
2
S. Serrano-Villar et al.
We hypothesized that the serial prevalence of HIV/HCV coinfection might have stabilized or even be in ascent in MSM, and we assessed changes in serial prevalence of HIV/HCV coinfection in the three main HIV transmission groups (IDU, MSM and heterosexuals) in an ongoing prospective multicentre cohort (CoRIS) in Spain from 2004 to 2011.
Robust methods were used to estimate the confidence intervals, assuming correlation among subjects recruited within each centre and independence among subjects from different centres. The adjusted model was included those variables which in the univariate analyses showed a level of statistical significance 50 85 (13.5) Year of inclusion (N,%) 2004–2005 399 (25.3) 2006–2007 308 (17.6) 2008–2009 251 (12.6) 2010–2011 141 (8.2) CD4+ T-cell count at cohort entry (N,%) < 200 cells/lL 396 (21.1) 200–350 cells/lL 256 (17.0) >350 cells/lL 431 (12.0) HIV RNA at cohort entry (N,%) 5 log/mL 349 (15.6)
HCV N = 5946 4904 (85.5) 1042 (79.7) 3911 (81.4) 2019 (90.1) 1819 (74.8) 1981 (90.0) 1435 (95.8) 97 3605 2030 214
(13.1) (96.9) (89.1) (74.8)
828 1529 2353 1236
(79.8) (83.8) (89.1) (95.4)
2134 2222 1046 544
(92.9) (82.8) (72.8) (86.5)
1177 1438 1747 1584
(74.7) (82.4) (81.4) (91.8)
1485 (78.9) 1248 (83.0) 3172 (88.0) 1391 (82.6) 2643 (85.6) 1885 (84.4)
Data expressed as no. (%). IDU, injection drug user; MSM, men who have sex with men; HTX, heterosexual. Univariate associations and independent risk factors for HIV/HCV coinfection after multivariate analyses are represented in Fig. 3. In the multivariate analysis, factors independently associated with the prevalence of HIV/HCV coinfection at cohort entry during the whole period were transmission category (IDU vs heterosexual; OR, 54.9; 95% CI, 39.4–76.4), birth decade (1961–1970 vs >1981; OR, 2.1; 95% CI, 1.1–3.7), age at cohort entry (41–50 years vs ≤30; OR, 1.8; 95% CI, 1.1–2.9), earlier © 2014 John Wiley & Sons Ltd
Fig. 1 Changes in patterns of risk behaviors for acquisition of HIV infection. Between 2004–05 and 2010–11, significant decreases in IDU category from 19.2% to 5.6% and in the heterosexual category, from 36.4% to 21.9% were observed. The category of MSM significantly increased from 40.6% in 2004–05 to 68.6% in 2010–11 (all trend P values
