Prevalence
of Hepatitis C Among Injection
Drug
Users in England and Wales:
Is Harm Reduction Working?
American
Journal of Public Health 39
January 2001,
Vol. 91, No.1
American Journal of
Public Health 39
Abstract
Objectives:
This study sought to establish the prevalence of hepatitis
C antibodies (anti-Hepatitis C Virus) and hepatitis B antibodies (anti-HBc)
among injection drug users in England and Wales.
Methods:
A voluntary cross-sectional survey collected oral fluid
samples and behavioral information; 2203 injectors were
recruited through drug agencies, and 758 were recruited in the
community.
Results:
Prevalence was 30% for anti-Hepatitis C Virus, 21% for anti-HBc), and 0.9%
for HIV antibodies, Anti-Hepatitis C Virus prevalence rates were
significantly greater among those with longer injecting
careers, those in older age groups, those residing in London,
those recruited in drug agencies, those positive for anti-HBc,
and those with a previous voluntary HIV test.
Conclusions:
Anti-Hepatitis C Virus prevalence rates among injectors in England and
Wales, where comprehensive harm reduction programs exist, are
lower than rates in other industrialized countries.
(Am J Public Health.
2001; 91: 38-42)
Vivian D. Hope,
PhD, MMedSc, Ali Judd, MSc, Matthew Hickman, MPH,
MFPHM(Hon),
Theresa Lamagni, MSc, Gillian Hunter; MSc,
Gerry J: Stimson, PhD,
MFPHM(Hon), Steve Jones, EA, Linda Donovan, BSc,
John J: Parry, PhD, and 0.
Noel Gill, ME, FFPHM
We conducted a large national cross- sectional
study to establish the prevalence of antibodies to Hepatitis C Virus (anti-Hepatitis C Virus)
in current injection drug users In the industrialized world, most trans- mission of hepatitis C virus (Hepatitis C Virus)
occurs through injection drug use, with prevalence typically
above 60% among injection drug users.I-5 In England
and Wales, local studies of injectors receiving drug treatment
in the mid-1990s revealed Hepatitis C Virus prevalence of 59% to 67%.6--8
Estimates of Hepatitis C Virus incidence among injection drug users in other
industrialized countries are also high, typically ranging from
10% to 20% per annum.1 For many, infection may be acquired
rapidly after initiation of in- jecting9; high
prevalence has been found
among those with short injecting careers ( e.g., in Baltimore, 65% of
those injecting for 1 year or less).10
There is evidence that harm
reduction interventions, which include a range of specialized
treatment services offering prescription and nonprescription
programs as well as needle exchange, have been effective in
reducing transmission of HIV among injection drug users.14-17
Areas that introduced comprehensive harm
reduction interventions for injection drug users a decade ago
currently have either a low and stable HIV prevalence, as in
Australia and the United Kingdom,I4-17 or a falling
prevalence, as in Geneva, Switzerland.18 Transmission of
hepatitis B virus (HBV) has also declined in these areas. 17,!8
There has, however, been little direct evidence indicating
that these measures reduce transmission of Hepatitis C Virus 19,20
Methods
Complementary voluntary unlinked- anonymous
surveys of drug users who had injected in the previous 4 weeks
were con- ducted at drug agencies (organizations, both public
and private, that provide services such as treatment, needle
exchange, and ad- vice to drug users) and in the community.
Those agreeing to participate provided an oral fluid specimen
and completed a brief questionnaire.
As part of an HIV prevalence monitoring
program, all injectors in contact with 47 representative drug
agencies in England and Wales during 1998 were eligible for
inclusion. The methodology has been described elsewhere. 17
Briefly, agency staff offered participation to all of their
injecting clients during the year; those who had not injected
in the previous 4 weeks were excluded from the present
analysis.
A community survey of injection drug users not receiving specialized
treatment for their drug use was conducted in 7 English cities
between October 1997 and June 1998 as part of a study of
injecting risk behavior!1 Participants were
eligible for the study if they had both injected and not
received specialized treatment or had contact with a drug
worker in the previous 4 weeks. Recruitment and interviews
occurred in a variety of sites, including street locations,
social venues, and participants , homes.
Comparable data collected included age, sex,
age at first injection, previous voluntary confidential HIV
test history, area of recruitment, frequency of sharing
injecting equipment ("During the last 4 weeks, how often
have you shared injecting equipment?"), and number of
sharing partners. The Injecting Risk Questionnaire22
was used in collecting sharing data.
Oral fluid specimens were
obtained with the EpiScreen device (Epitope, Inc, Beaverton,
Ore) and tested for antibodies to HIV (anti-HIV), to HBV core
antigen (anti-HBc), and to Hepatitis C Virus Details on laboratory methods
have been published elsewhere23; specimens that
were re- active on initial testing were subjected to
confirmatory testing via alternative methods.
Associations between antibody prevalence and
covariates were explored in univariate analyses and,
subsequently, in a multivariable logistic regression model. In
this model, significance was assessed with the likelihood
ratio statistic; Stata 6.0 (Stata Corp, College Station, Tex)
was used in these analyses.
Incidence rates were estimated among those who
had been injecting for less than 2 years. Among those who had
been injecting for up to I year, the average injecting career
was assumed to be 0.5 years; similarly, for those who had been
injecting between I and 2 years, the average injecting career
was assumed to be 1.5 years. Those who were anti- Hepatitis C Virus positive
were assumed to have been infected at 0.25 and 0.75 years of
injecting, respectively.
Results
A total of 2961 participants provided oral
fluid samples and completed questionnaires. Of these
individuals, 2203 were recruited through drug agencies, and
758 were recruited in the community.
The agency- and community-recruited participants had
similar distributions of age and years injecting (Table 1)
Overall, 29% were younger than 25 years, and 46% had injected
for less than 6 ~. Agency-recruited injectors were less likely
to be female or to have been recruited in London {Table I ).
Similar proportions in the agency and community groups
reported sharing injecting equipment in the previous month and
having had a voluntary confidential HIV test {Table I ).
The
prevalence of anti-Hepatitis C Virus was 30% {895/2943), and the prevalence
of anti-HBc was 21% {616/2955). Table 2 shows the prevalence
of anti-Hepatitis C Virus and anti-HBc by different risk factors. Further
analysis of risk factors for HIV infection was precluded by
the low prevalence of anti-HIV {less than 1%).
Anti-Hepatitis C Virus prevalence increased from 7% among
those injecting for less than 3 years to 62% for those who had
been injecting for 15 years or more. In comparison with those
who had injected for less than 3 years, the adjusted odds
ratios of having anti-Hepatitis C Virus were just over 3 for those who had
injected for 6 to 8 years and above 7 for those who had
injected for 15 or more years (X2s= 120.8, P< .001;
Table 2).
The association between age and anti- Hepatitis C Virus
prevalence was weaker but still statistically significant,
with an odds ratio above 2 for anti-Hepatitis C Virus in those 30 years or
older relative to those younger than 20 years (X26= 15.6,
P< .02). Anti-Hepatitis C Virus prevalence was elevated in
participants who had undergone a previous voluntary
confidential HIV test, in those recruited in London, and in
those recruited at drug agencies (Table 2).
Prevalence of anti-HBc increased from 5% in
those injecting for less than 3 years to 52% in those
injecting for 15 or more years. In comparison with those
injecting for less than 3 years, the adjusted odds ratios for
the presence of anti-HBc were 6.5 among those injecting for 15
or more years and above 2 among those injecting 6 to 8 years
(X2s= 103.8, P< .00 I; see Table 2). Anti-HBc
prevalence in- creased with increasing age; the odds ratio for
anti-HBc was above 2 in those 40 years and older in comparison
with those younger than 20 years (X26 = 32.7 , P<
.00 1 ). Having undergone a previous voluntary
confidential HIV test was positively associated with anti-HBc,
but area and site of recruitment were not.
Previous HBV infection was associated with Hepatitis C Virus
infection (Table 2); 59% (363/612) of those with anti-HBc also
had anti-Hepatitis C Virus; compared with only 23% of those without anti-
HBc (X21 = 50.1, P< .00 1 ). Frequency of sharing
injecting equipment in the 4 weeks before participation (42%)
was not associated with either anti-Hepatitis C Virus or anti-HBc
prevalence.
The annual incidence of Hepatitis C Virus infection was
estimated to be 4.6% in those who had injected for less than 2
years (23 infections in 502.8 years of exposure ), among whom
the anti-Hepatitis C Virus prevalence was 4.~/o(23/471). The equivalent
annual incidence for HBV infection was 3.6%, with an anti-HBc
prevalence in this group of3.8%.
|
TABLE
1-Characteristics of Agency- and Community-Recruited
Injection Drug Users: England and Wales, 1997-1998
|
|
|
Agency-
Recruited,
No. (%) (n=2203)
|
Community-
Recruited. No. (%)
(n= 758)
|
X2
|
p
|
|
Age,
y
<25
25-29
30-34
>35
Total
Gender
Female
Male
Total
Number
of years injecting
0-2
3-5
6-8
9-11
12-14
>
15
Total
Shared
injecting equipment in previous month
No
Yes
Total
Previous
voluntary confidential HIV test
No
Yes
Total
Area
of recruitment
London
Elsewhere
Total
|
633
558
503
509
2203
476
1716
2192
557
444
293
224
204
423
2145
1148
833
1981
1016
1092
2108
356
1847
2203
|
(29) (25) (23) (23)
(22) (78)
(26) (21) (14) (10) (10) (20)
|
232
194
160
171
757
220
535
755
198
131
109
82
72
145
737
426
328
754
361
395
756
244
514
758
|
(31)
(26)
(21)
(23)
(29)
(71)
(27)
(18)
(15)
(11)
(10)
(20)
(56)
(44)
(48)
(52)
(32)
(68)
|
1.5
17.2
3.3
0.5
0.0
89.7
|
.679
<.001
.653
.492
.833
<.001
|
| |
|
|
|
|
|
|
Discussion
At 30%, the prevalence of anti-Hepatitis C Virus found in this study was much lower
than that found in previous studies. Among those who had been
injecting for less than 3 years, the prevalence was 7.4%, and
the estimated annual incidence in those who had begun
injecting in the previous 2 years was below 5%. These results
differ from other evidence suggesting that Hepatitis C Virus infection in
injection drug users is Hepatitis C Virus infection in injection drug users
is difficult to prevent and that infection is acquired rapidly
after initiation into injecting.9-10
The reliability of the oral fluid tests used is important in assessing
our study's results. Ongoing assessment suggests sensitivity
and specificity rates of 80% and 99%, respectively, for anti-Hepatitis C Virus
and 82%
and 99%, respectively, for anti-HBc.23 An evaluation of a
similar technique in Scotland showed that anti-Hepatitis C Virus was present
in the oral fluid of 85% of 115 injection drug users with
serum antibodies to Hepatitis C Virus.24 Adjusting for a test
sensitivity of 80% would increase the overall anti-Hepatitis C Virus
prevalence to 38% and result in an estimated incidence among
recent initiates of 5.7%, but these figures are still lower
than what would be expected on the basis of previous studies.
Such an adjustment for low test sensitivity would leave
unchanged the relative differences in anti-Hepatitis C Virus prevalence
according to duration of injection and age.
The illegality of injection drug
use, its rarity in the population overall, and the
marginalization of injection drug users combine to make
monitoring of blood-borne virus trans- mission in this group
difficult. Although injectors can be recruited and followed up
while receiving treatment25 such interventions are
completed by only a subset of participants who tend to be
older and to have longer injection drug use careers, which in
turn may make their infection incidence rates
unrepresentative. The most useful and
"representative" data from which inferences about
transmission trends can be drawn are probably those provided
by large voluntary, unlinked-anonymous cross-sectional surveys
of injectors recruited concurrently from drug services and
community sites, as we have described here.
Two other studies provide
further evidence of a low anti-Hepatitis C Virus prevalence among injectors
in England and Wales. First, a 1997-1998 survey of prison
inmates reported an anti-Hepatitis C Virus prevalence of 30% among
more than 800 prisoners who reported ever injecting drugs.26
Second, an unlinked-anonymous survey involving syphilis
serology specimens from more than 1300 injection drug users
attending genitourinary medicine clinics during 1995- 1996
revealed an anti-Hepatitis C Virus prevalence rate of 37% (K. Balogun,
written communication, August 1999). Once adjusted for test
sensitivity, the results of the oral fluid surveys were the
same as in this serum survey.
Moreover, the anti-HIV and anti-HBc prevalence in our survey was
consistent with earlier data from surveys of injectors
recruited drug service and community settings.15-17
Previous studies in England and Wales may have led to
overestimation of the overall prevalence of anti-Hepatitis C Virus because
they recruited individuals receiving diagnostic tests while
at- tending drug treatment agencies, and these respondents
tended to be older and to have had long injecting careers.
Our findings suggest that the prevalence of Hepatitis C Virus infection among injection
drug users in England and Wales is lower than that in other
industrialized countries.1
They also suggest that transmission of Hepatitis C Virus among
injection drug users in England and Wales may have been
reduced in recent years. We may be observing an "aging
cohort" effect in the age-specific prevalence of anti-Hepatitis C Virus
similar to that observed for anti-HBc following the large
decrease in hepatitis B transmission in the mid-1980s27
The possibility of a similar decline in Hepatitis C Virus transmission among
injection drug users in Geneva, Switzerland18;
Victoria, Australia28; and Scotland29-albeit
against a background prevalence in excess of 50%---has been
suggested.
Cross-sectional
surveys such as ours, however, cannot provide proof that
prevalence and estimated incidence have decreased, establish
when such a decrease occurred, or monitor whether the decline
is continuing. It is essential, therefore, that prevalence and
incidence of anti-Hepatitis C Virus in injectors with short injecting
careers be monitored for a number of years.
Cohort studies of the effects on Hepatitis C Virus incidence of individual harm
reduction activities, such as needle exchange programs, have
produced inconclusive findings;30-32 but these
evaluations of individual prevention measures would not have
revealed possible synergistic benefits from large-scale
programs consisting of a variety of harm reduction activities.
In the United Kingdom, an extensive program that includes
widespread access to drug treatment services has existed for
many years. An estimated 25 million syringes were distributed
in the United Kingdom in 1997, a total that may be higher than
that for the United States (J Parsons, verbal communication,
August 1999).
The public health success in England and Wales with regard to controlling
HIV in injection drug users may have engendered complacency,
and opportunities to control Hepatitis C Virus transmission through
intensifying harm reduction possibly are being missed.
Evidence from HIV researchl2 suggests that
increased investment in comprehensive provision of harm
reduction interventions may be rewarded with a decrease in Hepatitis C Virus
transmission.
References
1)
MacDonald M, Crofts N, Kaldor 1. Transmission of
hepatitis C virus: rates, routes, and co- factors. Epidemiol
Rev. 1996;18:137-148.
2)
2. Donahue 1G, Nelson KE, Munoz A, et al. Anti- body to
hepatitis C virus among cardiac surgery patients, homosexual
men, and intravenous drug users in Baltimore, Maryland. Am
J Epidemiol. 1991;134:1206-1211.
3)
Coppola RC,
Manconi PE, Piro R, DiMartino ML, Masia G. Hepatitis C Virus; HIV; HBV and
HDV infections in intravenous drug addicts. Eur J Epi-
demiol.1994;10:279-283.
4)
Van Ameijden El, Van den Hock 1A, Mientjes GH, Coutinho
RA. A longitudinal study on the incidence and transmission
patterns of HIV; HBV and Hepatitis C Virus infection among drug users in
Amsterdam. Eur J Epidemiol. 1993;9:255-262.
5)
van Beek I, Buckley R, Stewart M, MacDonald M, Kaldor
1. Risk factors for hepatitis C virus infection among
injecting drug users in Sydney. Genitourin Med. 1994;70:321-324.
6)
MajidA, Holmes R, Desselberger U, Simmonds P, McKee TA.
Molecular epidemiology of hepatitis C virus infection amongst
intravenous drug users in rural communities. J Med Virol. 1995;
46:48-51.
7)
Lamden KH, Kennedy N, Beeching N1, et al. Hepatitis B
and hepatitis C virus infections: risk factors among drug
users in the Northwest of England. J Infect. 1998;37:260-269.
8)
Serfaty MA, Lawrie A, Smith B, et al. Risk factors and
medical follow-up of drug users tested for hepatitis C~an the
risk of transmission be reduced? Drug Alcohol Rev. 1997;16:339-347.
9)
Di Bisceglie AM. Hepatitis C. Lancet. 1998;
351:351-355.
10)
Garfein RS, Vlahov D, Galai N, Doherty MC,
11)
Nelson KE. Viral infections in short tenn in- jecting
drug users: the prevalence of hepatitis C, hepatitis B, human
immunodeficiency and human T-Iymphotropic viruses. Am J
Public Health. 1996;86:655-661.
12)
Hurley SF, Jolley Dl, Kaldor JM. Effectiveness of
needle exchange programmes for prevention of HIV infection. Lancet.
1997;349:1797-1800.
13)
Stimson GV Has the United Kingdom averted an epidemic
of HIV-I infection among drug injectors? Addiction. 1996;91:
1085-1088.
14)
Des Jarlais DC, Hagan H, Friedman SR, et al Maintaining
low HIV seroprevalence in Populations of injecting drug users.
JAMA. 1995;274. 1226-1231.
15)
van Beek
1, Dwyer R, Dore GJ, Luo K, Kaldor JM. Infection with HIV and
hepatitis C virus among injecting drug users in a prevention
set- ting: retrospective cohort study. BMJ 1998;317'
433--437.
16)
Stimson GV; Hunter GM, Donoghoe MC, Rhodes T, Parry Jv;
Chalmers CP. HIV-I prevalence in community-wide samples of
injecting drug users in London, 1990-1993. AIDS. 1996;
10.657-666.
17)
Judd A, Hunter GM, Maconochie N, et al HIV prevalence
and risk behaviour among female injecting drug users in
London, 1990 to 1996. AIDS. 1999;13:833-837.
18)
Unlinked Anonymous HIV Surveys Steering Group. Prevalence
of HIV in the United Kingdom: 1998. London, England: Dept
of Health, Public Health Laboratory Service; 1999.
19)
Broers B, Junet C, Bourquin M, Deglon 11, Per- rin L,
Hirschel B. Prevalence and incidence rate of HIV; hepatitis B
and C among drug users on methadone maintenance treatment in
Geneva between 1988 and 1995. AIDS. 1998;12: 2059-2066.
20)
Coutinho RA. HIV and hepatitis C among in- jecting drug
users-success in preventing HIV has not been mirrored for
hepatitis C. BMJ. 1998;317:425--426.
21)
Judd A, Hickrnan M, Renton A, Stimson GV Hepatitis C
virus infection among injecting drug users: has harm reduction
worked? Addict Res. 1999;7'1-6.
22)
Hunter GM,
Stimson GV; Judd A, Jones S, Hick- man M. Measuring injecting
risk behaviour in the second decade of harm reduction. a
survey of injecting drug users in England. Addiction. 2000;95:1351-1361.
23)
Stimson GV; Jones S, Chalmers C, Sullivan D. A short
questionnaire (IRQ) to assess injecting risk behaviour. Addiction.
1998;93:337-347.
24)
Allwright S, Bradley F, Long J, Barry J, Thom- ton L,
Parry N Prevalence of antibodies to hepatitis B,
hepatitis C and HIV in Irish prisoners. results of a national
cross sectional survey. BMJ. 2000;321:78-82.
25)
Cameron SO, Wilson KS, Good T, et al Detec- tion of
antibodies against hepatitis C virus in saliva. a marker of
viral replication. J Viral Hepat. 1999;6:141-144.
26)
Gossop M, Marsden J, Stewart D. NTORS at One Year:
The National Treatment Outcome Re- search Study. London,
England: Dept of Health; 1998.
27)
Weild AR, Gill ON, Bennett D, Livingstone SJM, Parry
J\.; Curran L. Prevalence of HIV; hepatitis B, and hepatitis C
antibodies in prisoners in England and Wales. a national
survey. Commun Dis Public Health. 2000;3;121-126.
28)
Balogun MA, Ram say ME, Fairley CK, Collins M,
Heptonstall J. Acute hepatitis B infection in England and
Wales; 1985-96. Epidemiol
. 1999;122;125-13J.
29)
Crofts N, Aitken CK. Incidence of bloodbome virus
infection and risk behaviours in a cohort of
28)
injecting drug users in Victoria, 199(}-1995. Med
JAust. 1997;167:17-20.
29)
Goldberg D, Cameron S, McMenamin J. Hepatitis C virus
antibody prevalence among in- jecting drug users in Glasgow
has fallen but re- mains high. Commun Dis Public Health. 1998;
1:95-97.
30)
Hagan H, Des Jarlais DC, Friedman SR, Purchase D, Alter
MJ. Reduced risk of hepatitis C among injection drug users in
the Tacoma syringe exchange program.
Am J Public Health 1995; 85:1531-1537
31)
Hagan H, McGrough JP, Thiede H, Weiss NS, Hopkins S,
Alexander ER. Syringe
exchange and risk of infection with hepatitis B and C viruses.
Am J Epidermiol.
1999;149:203-213
32)
Crofts N, Nigro L, Oman K, Stevenson E, Sherman H.
Methadone maintenance and hepatitis C virus infection among
drug users. Addiction.
1997; 92:999-1005