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Temporal changes in HCV genotype distribution in three different high risk populations in San Francisco, California
© Dias et al; licensee BioMed Central Ltd. 2011
Received: 27 January 2011
Accepted: 2 August 2011
Published: 2 August 2011
Hepatitis C virus (HCV) genotype (GT) has become an important measure in the diagnosis and monitoring of HCV infection treatment. In the United States (U.S.) HCV GT 1 is reported as the most common infecting GT among chronically infected patients. In Europe, however, recent studies have suggested that the epidemiology of HCV GTs is changing.
We assessed HCV GT distribution in 460 patients from three HCV-infected high risk populations in San Francisco, and examined patterns by birth cohort to assess temporal trends. Multiple logistic regression was used to assess factors independently associated with GT 1 infection compared to other GTs (2, 3, and 4).
Overall, GT 1 was predominant (72.4%), however younger injection drug users (IDU) had a lower proportion of GT 1 infections (54.7%) compared to older IDU and HIV-infected patients (80.5% and 76.6%, respectively). Analysis by birth cohort showed increasing proportions of non-GT 1 infections associated with year of birth: birth before 1970 was independently associated with higher adjusted odds of GT 1: AOR 2.03 (95% CI: 1.23, 3.34). African-Americans as compared to whites also had higher adjusted odds of GT 1 infection (AOR: 3.37; 95% CI: 1.89, 5.99).
Although, HCV GT 1 remains the most prevalent GT, especially among older groups, changes in GT distribution could have significant implications for how HCV might be controlled on a population level and treated on an individual level.
Hepatitis C virus (HCV), first identified in 1990, is a single strand RNA virus in the family Flaviviridae. It is prone to high rates of genetic mutation, resulting in evolution to divergent forms and six major genotypes . Each genotype (GT) is further divided into subtypes, based on genetic sequence variability. There are notable clinical differences in responsiveness to interferon-based therapy for treatment of chronic infection by GT, with GTs 1 and 4 being less responsive and requiring longer exposure time to treatment than types 2 and 3 [2–5]. GT has been associated with different patterns in HCV viremia during interferon treatment , and antiviral resistance [7, 8]. Although some clinical conditions have been noted to differ by HCV GT, including insulin resistance , HIV and HIV disease progression , little is known regarding how different HCV GTs differ in virulence or pathogenicity . African Americans infected with GT 1 are significantly less likely to respond to HCV treatment than Asian and Caucasian patients with GT 1 [12, 13]. Patients infected with GT 1 who carry a genetic variant allele near IL28B gene are more likely to respond to combination therapy (pegylated interferon-alpha-2a or -2b and ribavirin)  and clear spontaneously . As this polymorphism varies by race , it partially explains differences in these outcomes. Finally, GT heterogeneity may hinder the development of a vaccine .
In the U.S. HCV GT 1 has been the most common infecting subtype; over 70% of patients with chronic infection are GT 1 [17–19]. In Europe, however, recent studies have reported more variation in the extent and diversity of HCV GTs, and have shown associations between HCV GT and risk exposure, age, and clinical group [20–24]. In the U.S., race/ethnicity have been found to be independently associated with GT in the NHANES general population sample  and in other samples , but none have examined temporal changes in circulating infecting GTs.
The objective of this study was to examine the distribution of prevalent HCV GTs in various high risk populations in San Francisco by birth cohort and other demographic factors.
Selected characteristics of participants in three studies of HCV infection in San Francisco (N = 460)
Total all studies
Age (in years)#
28.0 - 48.0
Years of recruitment
HCV Genotypes* ¶
< High School
>= High school
In all studies anti-HCV and HCV viremia were assessing using Ortho EIA 3.0, with confirmation by RIBA 3.0, Chiron, Corp, and a discriminatory HCV transcription-mediated amplification (dHCV TMA) assay component of the Procleix HIV-1/HCV assay (Novartis Diagnostics, Emeryville, CA, USA), respectively. HCV GT was determined by the LiPA Line Probe Assay (Bayer Diagnostics, Tarrytown, NY, USA). Indeterminate GTs and co-infected cases were not included in the final analysis of the study.
We assessed differences between the study groups and between GT 1 versus other GTs with respect to sociodemographic and clinical variables using standard methods. Differences in proportions were compared using Pearson Chi-Square tests. Differences in variables with continuous data were assessed by comparing medians and distributions using the Kruskal-Wallis test. We examined HCV GT distribution by birth cohort to assess trends by 10-year birth intervals using the Mantel-Haenszel Chi-Square test for trend. Multiple logistic regression was used to assess factors independently associated with GT 1 infection compared to other GTs (2, 3, and 4); adjusted odds ratios (AOR) and 95% Confidence Intervals (CI) were calculated. Models were constructed in an iterative backwards stepwise manner. All variables with a p-value <= 0.05 at the bivariate level were entered into the model and removed one by one. Variables with a p-value of <= 0.10 were retained in the final model. All analyses were conducted using SPSS for Windows statistical software package (version 13).
All of the research from participating studies in this project was conducted under protocols reviewed and approved by the University of California San Francisco Human Subjects Research Committee, and conformed to the Helsinki Declaration and local regulations. All study subjects gave informed consent for participation.
Bivariate and multivariate associations between selected demographic characteristics and infection with HCV genotype 1 vs. non-1 (genotypes 2, 3, 4)
% with genotype 1 HCV infection
1.22 (0.78, 1.90)
4.65 (2.75, 7.86)
3.37 (1.89, 5.99)
1.77 (0.71, 4.45)
1.57 (0.61, 3.98)
1.16 (0.59, 2.30)
1.85 (0.59, 2.37)
Born before 1970
2.97 (1.20, 4.59)
2.03 (1.23, 3.34)
Born 1971 or later
3.33 (2.04, 5.45)
2.92 (1.68, 5.06)
These results suggest that in San Francisco, within the ongoing HCV epidemic, the epidemiology of infecting HCV viruses has changed over time. Among younger IDU, who are also more likely to have more recent infection, non-GT 1 is increasingly prevalent. Historically, few studies have been published describing GTs in San Francisco patients. In 1999, Gish et al,  described GTs (using restriction fragment length polymorphism analysis) in 186 patients with chronic HCV (the majority presumptively IDU); 76% were type 1 (1a, 41%; 1b, 35%), 13% were type 2 (2a, 3%; 2b, 10%) and 11% were type 3a. In that sample, HCV GT was not associated with age, gender, ethnic origin, or presumptive mode of transmission. In two small groups (n = 8 each) of chronically HCV infected, active and former IDU recruited from two urban San Francisco Hospitals, 75% of active IDU (median age 47 years) and all of the former IDU (median age 49) were type 1. As patients in these studies were more heterogeneous with respect to routes of exposure, and were likely to have been infected some years before clinical assessment, these data are consistent with the suggestion that type 1 GTs were more prevalent in San Francisco IDU in the 1990's.
In Europe, Simmonds et al  showed an association between HCV GT and age, and attributed it primarily to risk exposure differences. In Germany, Schroter et al  also showed increases in GTs 3a in younger groups, including IDU and non-IDU, leading these authors to hypothesize that the introduction of new subtypes in a high risk group may rapidly impact lower risk groups. Others have shown differences in HCV GT distribution by route of exposure, with GT 3a associated with injection exposures, and GT 1b associated with acquisition through blood transfusion [21, 22, 30, 31]. In a multicentre study of HCV infection in 183 HIV-infected IDU sampled between 1984 and 2001, Van Asten et al , using phylogenetic analyses, found that subtypes 3a and 1a were most prevalent (38.3%, and 36%, respectively) and extensively dispersed throughout the countries.
The relative differences in HCV GT seen in these San Francisco patients may be due to various factors, including temporal changes in the dominant circulating virus, or potentially separate epidemics marked by differential social mixing. All three populations were sampled in San Francisco and were at high risk of HCV due to parenteral exposure, but younger patients had significantly lower odds of being infected with GT 1. African-Americans represented 62% of older IDU, only 1.9% of younger IDU, and 41.6% of HIV co-infected patients, but controlling for birth year and other factors, still had significantly higher odds of subtype 1 HCV infection compared to Caucasian patients. This differential GT distribution by racial group may be due to various factors including temporal, social (mixing), differential access to prevention, and/or possibly genetic explanations. The prevalence of IDU has decreased among younger age groups and among African-American populations in the U.S., and drug injector networks and associated risks may influence the spread of HCV GTs [34, 35] as seen with other diseases . Risk groups, in particular IDU compared to non-IDU populations, may have differential access to prevention methods by age, race or other factors that might result in differences in HCV transmission patterns or detection [37–39]. The genetic polymorphism recently associated with treatment and spontaneous clearance of HCV [14, 40] occurs with less frequency in African populations, and may account for some of the relative differences seen in HCV GTs prevalence in African Americans and possibly other racial/ethnic groups .
To our knowledge no studies have examined GT distribution patterns over several age groups (or by birth cohort) and risk group. In Spain, Serra et al (40), found that GTs varied by risk group: IDU were less likely to be infected with GT 1b and more likely to be infected with GTs 1a and 3, compared to transfusion recipients and blood donors, and GT prevalence varied over time in all groups . Our results are also consistent with others who have shown that African-Americans are more likely to be infected with HCV GT 1 [18, 19]. Significantly, a very recent report analyzing over 22,000 samples from HCV infected patients at a national reference laboratory in the U.S., found that patients infected with GT 3 were significantly younger (P<0.0001) than those with non-GT 3 (1, 2, or 4). the frequency of HCV GT 3 ranged from just 4.3% in subjects over age 70 to 20.6% in those age 21 to 30 . Our results are consistent with these new findings, and among the first to suggest that the relative prevalence of GT 3 may be increasing as younger groups are more likely to have been recently infected.
This study has some limitations that should be acknowledged. Genotyping was performed by reverse hybridization, and viruses were not sequenced; misclassification could have occurred . Patients may also be infected with multiple GTs, especially IDU who have frequent opportunities for exposure , and the assay would have only identified the dominant virus . The groups here are selected from studies of high risk populations in San Francisco, so results may not be generalizable to other risk groups. Finally, two groups (UHS and SCOPE) predominantly represent chronically infected patients, and samples were genotyped only if HCV RNA was present. If there is differential spontaneous clearance in association with HCV GT , these results would not reflect the circulating infecting GTs in acutely infected patients, but only those in chronically infected groups.
IDU are the population most at risk for HCV in the U.S. and younger IDU are most likely to present with more recently acquired infection. Although GT 1 remains the most prevalent GT, especially among older groups, changes in GT distribution coupled with changes in the demography of injection drug use  could have important implications for the HCV epidemic. From a public health perspective, these findings might have significant implications for how blood borne virus infections could be controlled on a population level and how they are treated on an individual level.
The following sources of funding supported the investigators and studies participating in this project: U.S. National Institutes for Health (NIH) (R01-DA016017-03A1, U19-AI40034-13, K01-DA023365, UL1-RR024131, P30-AI27763, R01-DA09532, R01-DA12109, R01-DA13245, R01-DA021550, N01-CO-12400); the Substance Abuse and Mental Health Services Administration (H79-TI12103); and the San Francisco Department of Public Health (POHC99001316). Dr. Telles was supported by NIDA Invest Fellowship linked to 2 R01 DA016017-03A1. We also acknowledge the UCSF Liver Center NIH P30 DK026743.
- Simmonds P, Bukh J, Combet C, Deleage G, Enomoto N, Feinstone S, Halfon P, Inchauspe G, Kuiken C, Maertens G, Mizokami M, Murphy DG, Okamoto H, Pawlotsky JM, Penin F, Sablon E, Shin IT, Stuyver LJ, Thiel HJ, Viazov S, Weiner AJ, Widell A: Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology. 2005, 42 (4): 962-973. 10.1002/hep.20819.View ArticlePubMedGoogle Scholar
- Fried MW, Shiffman ML, Reddy KR, Smith C, Marinos G, Goncales FL, Haussinger D, Diago M, Carosi G, Dhumeaux D, Craxi A, Lin A, Hoffman J, Yu J: Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection. N Engl J Med. 2002, 347 (13): 975-982. 10.1056/NEJMoa020047.View ArticlePubMedGoogle Scholar
- Manns MP, McHutchison JG, Gordon SC, Rustgi VK, Shiffman M, Reindollar R, Goodman ZD, Koury K, Ling M, Albrecht JK: Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial. Lancet. 2001, 358 (9286): 958-965. 10.1016/S0140-6736(01)06102-5.View ArticlePubMedGoogle Scholar
- Muir AJ, Bornstein JD, Killenberg PG: Peginterferon alfa-2b and ribavirin for the treatment of chronic hepatitis C in blacks and non-Hispanic whites. N Engl J Med. 2004, 350 (22): 2265-2271. 10.1056/NEJMoa032502.View ArticlePubMedGoogle Scholar
- McHutchison JG, Gordon SC, Schiff ER, Shiffman ML, Lee WM, Rustgi VK, Goodman ZD, Ling MH, Cort S, Albrecht JK: Interferon alfa-2b alone or in combination with ribavirin as initial treatment for chronic hepatitis C. Hepatitis Interventional Therapy Group [see comments]. N Engl J Med. 1998, 339 (21): 1485-1492. 10.1056/NEJM199811193392101.View ArticlePubMedGoogle Scholar
- Tobler LH, Bahrami SH, Kaidarova Z, Pitina L, Winkelman VK, Vanderpool SK, Guiltinan AM, Cooper S, Busch MP, Murphy EL: A case-control study of factors associated with resolution of hepatitis C viremia in former blood donors (CME). Transfusion. 50 (7): 1513-1523.Google Scholar
- Thomas DL, Astemborski J, Rai RM, Anania FA, Schaeffer M, galai N, Nolt K, Nelson KE, Strathdee SA, Johnson L, Laeyendecker O, Boitnott J, Wilson LE, Vlahov D: The natural history of hepatitis C virus infection. Journal of the American Medical Association. 2000, 284 (4): 450-456. 10.1001/jama.284.4.450.PubMedGoogle Scholar
- Schito ML, D'Souza MP, Owen SM, Busch MP: Challenges for rapid molecular HIV diagnostics. J Infect Dis. 201 (Suppl 1): S1-6.Google Scholar
- Moucari R, Asselah T, Cazals-Hatem D, Voitot H, Boyer N, Ripault MP, Sobesky R, Martinot-Peignoux M, Maylin S, Nicolas-Chanoine MH, Paradis V, Vidaud M, Valla D, Bedossa P, Marcellin P: Insulin resistance in chronic hepatitis C: association with genotypes 1 and 4, serum HCV RNA level, and liver fibrosis. Gastroenterology. 2008, 134 (2): 416-423. 10.1053/j.gastro.2007.11.010.View ArticlePubMedGoogle Scholar
- Yoo TW, Donfield S, Lail A, Lynn HS, Daar ES: Effect of hepatitis C virus (HCV) genotype on HCV and HIV-1 disease. J Infect Dis. 2005, 191 (1): 4-10. 10.1086/426513.View ArticlePubMedGoogle Scholar
- Farci P, Purcell RH: Clinical significance of hepatitis C virus genotypes and quasispecies. Semin Liver Dis. 2000, 20 (1): 103-126.PubMedGoogle Scholar
- Hepburn MJ, Hepburn LM, Cantu NS, Lapeer MG, Lawitz EJ: Differences in treatment outcome for hepatitis C among ethnic groups. Am J Med. 2004, 117 (3): 163-168. 10.1016/j.amjmed.2004.02.043.View ArticlePubMedGoogle Scholar
- Kinzie JL, Naylor PH, Nathani MG, Peleman RR, Ehrinpreis MN, Lybik M, Turner JR, Janisse JJ, Massanari M, Mutchnick MG: African Americans with genotype 1 treated with interferon for chronic hepatitis C have a lower end of treatment response than Caucasians. J Viral Hepat. 2001, 8 (4): 264-269. 10.1046/j.1365-2893.2001.00292.x.View ArticlePubMedGoogle Scholar
- Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, Heinzen EL, Qiu P, Bertelsen AH, Muir AJ, Sulkowski M, McHutchison JG, Goldstein DB: Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance. Nature. 2009, 461 (7262): 399-401. 10.1038/nature08309.View ArticlePubMedGoogle Scholar
- Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, Kidd J, Kidd K, Khakoo SI, Alexander G, Goedert JJ, Kirk GD, Donfield SM, Rosen HR, Tobler LH, Busch MP, McHutchison JG, Goldstein DB, Carrington M: Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature. 2009, 461 (7265): 798-801. 10.1038/nature08463.View ArticlePubMedPubMed CentralGoogle Scholar
- Strickland GT, El-Kamary SS, Klenerman P, Nicosia A: Hepatitis C vaccine: supply and demand. Lancet Infect Dis. 2008, 8 (6): 379-386. 10.1016/S1473-3099(08)70126-9.View ArticlePubMedGoogle Scholar
- Alter MJ: Hepatitis C virus infection in the United States. J Hepatol. 1999, 31 (Suppl 1): 88-91.View ArticlePubMedGoogle Scholar
- Blatt LM, Mutchnick MG, Tong MJ, Klion FM, Lebovics E, Freilich B, Bach N, Smith C, Herrera J, Tobias H, Conrad A, Schmid P, McHutchison JG: Assessment of hepatitis C virus RNA and genotype from 6807 patients with chronic hepatitis C in the United States. J Viral Hepat. 2000, 7 (3): 196-202. 10.1046/j.1365-2893.2000.00221.x.View ArticlePubMedGoogle Scholar
- Nainan OV, Alter MJ, Kruszon-Moran D, Gao FX, Xia G, McQuillan G, Margolis HS: Hepatitis C virus genotypes and viral concentrations in participants of a general population survey in the United States. Gastroenterology. 2006, 131 (2): 478-484. 10.1053/j.gastro.2006.06.007.View ArticlePubMedGoogle Scholar
- Payan C, Roudot-Thoraval F, Marcellin P, Bled N, Duverlie G, Fouchard-Hubert I, Trimoulet P, Couzigou P, Cointe D, Chaput C, Henquell C, Abergel A, Pawlotsky JM, Hezode C, Coude M, Blanchi A, Alain S, Loustaud-Ratti V, Chevallier P, Trepo C, Gerolami V, Portal I, Halfon P, Bourliere M, Bogard M, Plouvier E, Laffont C, Agius G, Silvain C, Brodard V, et al: Changing of hepatitis C virus genotype patterns in France at the beginning of the third millenium: The GEMHEP GenoCII Study. J Viral Hepat. 2005, 12 (4): 405-413. 10.1111/j.1365-2893.2005.00605.x.View ArticlePubMedGoogle Scholar
- Chlabicz S, Flisiak R, Kowalczuk O, Grzeszczuk A, Pytel-Krolczuk B, Prokopowicz D, Chyczewski L: Changing HCV genotypes distribution in Poland--relation to source and time of infection. J Clin Virol. 2008, 42 (2): 156-159. 10.1016/j.jcv.2008.02.001.View ArticlePubMedGoogle Scholar
- Bourliere M, Barberin JM, Rotily M, Guagliardo V, Portal I, Lecomte L, Benali S, Boustiere C, Perrier H, Jullien M, Lambot G, Loyer R, LeBars O, Daniel R, Khiri H, Halfon P: Epidemiological changes in hepatitis C virus genotypes in France: evidence in intravenous drug users. J Viral Hepat. 2002, 9 (1): 62-70. 10.1046/j.1365-2893.2002.00319.x.View ArticlePubMedGoogle Scholar
- Katsoulidou A, Sypsa V, Tassopoulos NC, Boletis J, Karafoulidou A, Ketikoglou I, Tsantoulas D, Vafiadi I, Hatzis G, Skoutelis A, Akriviadis E, Vasiliadis T, Kitis G, Magiorkinis G, Hatzakis A: Molecular epidemiology of hepatitis C virus (HCV) in Greece: temporal trends in HCV genotype-specific incidence and molecular characterization of genotype 4 isolates. J Viral Hepat. 2006, 13 (1): 19-27. 10.1111/j.1365-2893.2005.00649.x.View ArticlePubMedGoogle Scholar
- Schroter M, Zollner B, Schafer P, Reimer A, Muller M, Laufs R, Feucht HH: Epidemiological dynamics of hepatitis C virus among 747 German individuals: new subtypes on the advance. J Clin Microbiol. 2002, 40 (5): 1866-1868. 10.1128/JCM.40.5.1866-1868.2002.View ArticlePubMedPubMed CentralGoogle Scholar
- Lorvick J, Kral AH, Seal K, Gee L, Edlin BR: Prevalence and duration of hepatitis C among injection drug users in San Francisco, Calif. Am J Public Health. 2001, 91 (1): 46-47.View ArticlePubMedPubMed CentralGoogle Scholar
- Page K, Hahn JA, Evans J, Shiboski S, Lum P, Delwart E, Tobler L, Andrews W, Avanesyan L, Cooper S, Busch MP: Acute hepatitis C virus infection in young adult injection drug users: a prospective study of incident infection, resolution, and reinfection. J Infect Dis. 2009, 200 (8): 1216-1226. 10.1086/605947.View ArticlePubMedPubMed CentralGoogle Scholar
- Hunt PW, Brenchley J, Sinclair E, McCune JM, Roland M, Page-Shafer K, Hsue P, Emu B, Krone M, Lampiris H, Douek D, Martin JN, Deeks SG: Relationship between T Cell Activation and CD4(+) T Cell Count in HIV-Seropositive Individuals with Undetectable Plasma HIV RNA Levels in the Absence of Therapy. J Infect Dis. 2008, 197 (1): 126-133. 10.1086/524143.View ArticlePubMedPubMed CentralGoogle Scholar
- Gish RG, Qian K, Brooks L, Leung J, Xu Y, Pike I, Lau JY: Characterization of anti-hepatitis C virus-positive sera not genotyped by restriction fragment length polymorphism or serology. J Gastroenterol Hepatol. 1999, 14 (4): 339-344.View ArticlePubMedGoogle Scholar
- Simmonds P, Mellor J, Craxi A, Sanchez-Tapias JM, Alberti A, Prieto J, Colombo M, Rumi MG, Lo Iacano O, Ampurdanes-Mingall S, Forns-Bernhardt X, Chemello L, Civeira MP, Frost C, Dusheiko G: Epidemiological, clinical and therapeutic associations of hepatitis C types in western European patients. J Hepatol. 1996, 24 (5): 517-524. 10.1016/S0168-8278(96)80135-8.View ArticlePubMedGoogle Scholar
- Dal Molin G, Ansaldi F, Biagi C, D'Agaro P, Comar M, Croce L, Tiribelli C, Campello C: Changing molecular epidemiology of hepatitis C virus infection in Northeast Italy. J Med Virol. 2002, 68 (3): 352-356. 10.1002/jmv.10210.View ArticlePubMedGoogle Scholar
- Mathei C, Wollants E, Verbeeck J, Van Ranst M, Robaeys G, Van Damme P, Buntinx F: Molecular epidemiology of hepatitis C among drug users in Flanders, Belgium: association of genotype with clinical parameters and with sex- and drug-related risk behaviours. Eur J Clin Microbiol Infect Dis. 2005, 24 (8): 514-522. 10.1007/s10096-005-1376-9.View ArticlePubMedGoogle Scholar
- van Asten L, Verhaest I, Lamzira S, Hernandez-Aguado I, Zangerle R, Boufassa F, Rezza G, Broers B, Robertson JR, Brettle RP, McMenamin J, Prins M, Cochrane A, Simmonds P, Coutinho RA, Bruisten S: Spread of hepatitis C virus among European injection drug users infected with HIV: a phylogenetic analysis. J Infect Dis. 2004, 189 (2): 292-302. 10.1086/380821.View ArticlePubMedGoogle Scholar
- Armstrong GL: Injection drug users in the United States, 1979-2002: an aging population. Arch Intern Med. 2007, 167 (2): 166-173. 10.1001/archinte.167.2.166.View ArticlePubMedGoogle Scholar
- Bluthenthal RN, Do DP, Finch B, Martinez A, Edlin BR, Kral AH: Community characteristics associated with HIV risk among injection drug users in the San Francisco Bay Area: a multilevel analysis. J Urban Health. 2007, 84 (5): 653-666. 10.1007/s11524-007-9213-3.View ArticlePubMedPubMed CentralGoogle Scholar
- Johnson RA, Gerstein DR, Pach A, Cerbone FG, Brown J: HIV risk behaviors in African-American drug injector networks: implications of injection-partner mixing and partnership characteristics. Addiction. 2002, 97 (8): 1011-1024. 10.1046/j.1360-0443.2002.00165.x.View ArticlePubMedGoogle Scholar
- Friedman SR, Lieb S, Tempalski B, Cooper H, Keem M, Friedman R, Flom PL: HIV among injection drug users in large US metropolitan areas, 1998. J Urban Health. 2005, 82 (3): 434-445.View ArticlePubMedPubMed CentralGoogle Scholar
- Cooper HL, Bossak BH, Tempalski B, Friedman SR, Des Jarlais DC: Temporal trends in spatial access to pharmacies that sell over-the-counter syringes in New York City health districts: relationship to local racial/ethnic composition and need. J Urban Health. 2009, 86 (6): 929-945. 10.1007/s11524-009-9399-7.View ArticlePubMedPubMed CentralGoogle Scholar
- Heinzerling KG, Kral AH, Flynn NM, Anderson RL, Scott A, Gilbert ML, Asch SM, Bluthenthal RN: Human immunodeficiency virus and hepatitis C virus testing services at syringe exchange programs: availability and outcomes. J Subst Abuse Treat. 2007, 32 (4): 423-429. 10.1016/j.jsat.2006.11.002.View ArticlePubMedGoogle Scholar
- Stopka TJ, Garfein RS, Ross A, Truax SR: Increasing syringe access and HIV prevention in California: findings from a survey of local health jurisdiction key personnel. J Urban Health. 2007, 84 (1): 116-125. 10.1007/s11524-006-9122-x.View ArticlePubMedGoogle Scholar
- Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, Kidd J, Kidd K, Khakoo SI, Alexander G, Goedert JJ, Kirk GD, Donfield SM, Rosen HR, Tobler LH, Busch MP, McHutchison JG, Goldstein DB, Carrington M: Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature. 2009Google Scholar
- Serra MA, Rodriguez F, del Olmo JA, Escudero A, Rodrigo JM: Influence of age and date of infection on distribution of hepatitis C virus genotypes and fibrosis stage. J Viral Hepat. 2003, 10 (3): 183-188. 10.1046/j.1365-2893.2003.00372.x.View ArticlePubMedGoogle Scholar
- Germer JJ, Mandrekar JN, Bendel JL, Mitchell PS, Yao JD: Hepatitis C Virus Genotypes in Clinical Specimens Tested at a National Reference Testing Laboratory in the United States. J Clin Microbiol. 2011Google Scholar
- Nadarajah R, Khan GY, Miller SA, Brooks GF: Evaluation of a new-generation line-probe assay that detects 5' untranslated and core regions to genotype and subtype hepatitis C virus. Am J Clin Pathol. 2007, 128 (2): 300-304. 10.1309/RBAAC0HJFWRJB1HD.View ArticlePubMedGoogle Scholar
- Herring BL, Page-Shafer K, Tobler LH, Delwart EL: Frequent hepatitis C virus superinfection in injection drug users. J Infect Dis. 2004, 190 (8): 1396-1403. 10.1086/424491.View ArticlePubMedGoogle Scholar
- Schroter M, Feucht HH, Zollner B, Schafer P, Laufs R: Multiple infections with different HCV genotypes: prevalence and clinical impact. J Clin Virol. 2003, 27 (2): 200-204. 10.1016/S1386-6532(02)00264-0.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2334/11/208/prepub
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