Vaccine 33 (2015) 28082812

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Vaccine
journal homepage: www.elsevier.com/locate/vaccine

Hepatitis A and B among young persons who inject

drugsVaccination, past, and present infection
Melissa G. Collier a, , Jan Drobeniuc a , Jazmine Cuevas-Mota b , Richard S. Garfein b ,
Saleem Kamili a , Eyasu H. Teshale a
a
Centers for Disease Control and Prevention, National Center for HIV, Hepatitis, STD, and TB Prevention, Division of Viral Hepatitis, Atlanta, GA, United States
b
Division of Global Public Health, School of Medicine, University of California, San Diego, CA, United States

a r t i c l e i n f o a b s t r a c t

Article history: Background: Our study aims were to assess hepatitis A virus (HAV) and hepatitis B virus (HBV) suscep-
Received 3 February 2015 tibility and infection among young persons who inject drugs (PWID) who may have been vaccinated as
Received in revised form 3 April 2015 children and to evaluate self-report of HAV and HBV vaccination.
Accepted 6 April 2015
Methods: We recruited PWID aged 1840 years-old in San Diego during 2009 and 2010 and collected
Available online 15 April 2015
demographic, socioeconomic, health, and behavioral factors. Participants were asked if they had been
vaccinated against HAV and HBV, and serum samples were collected for HAV and HBV serologic testing.
Keywords:
Results: Of 519 participants, 365 (72%) were male, 252 (49%) were white non-Hispanic, 38 (7%) were
Hepatitis C virus
Persons who inject drugs
Black non-Hispanic, 138 (27%) were White Hispanic, and 22 (4%) were born outside the U. S. Of the
Self-report total participants, 245 (47%) had surface hepatitis B antibody (anti-HBs) titers <10 mIU/ml (i.e., HBV
susceptible) and 325 (63%) had no detectable HAV antibodies (HAV susceptible). Hepatitis B surface
antigen was detected in 7 (1%) of total participants; and 135 (26%) were anti-HCV-antibody positive.
Compared to serologic findings, self-report of HBV and HAV vaccination was 71% and 41% sensitive, and
58% and 73% specific, respectively.
Conclusion: HAV and HBV antibodies in half or more of this young PWID population did not have levels
indicative of protection, and about a quarter had HCV infection, putting them at risk for complications
resulting from co-infection with HAV or HBV. Programs serving this population should vaccinate PWIDs
against HAV and HBV and not rely on self-report of vaccination.
Published by Elsevier Ltd.

1. Background ACIP first recommended universal infant vaccination in 1991 and

Persons who inject drugs (PWID) are at risk for hepatitis B and
C virus (HBV and HCV) infection due to parenteral exposure, par-
ticularly when sharing needle and other injection equipment [1].
Chronic infection with both viruses is a major cause of morbidity
and mortality due to liver cirrhosis and liver cancer. PWID are also
at increased risk for contact with hepatitis A virus (HAV) putatively
due to poor hygiene during shared injections [26]. Infection or co-
infection with HAV or HBV increases the risk of acute liver failure
causing death or requiring liver transplant [710]. Safe and effective
vaccines are available for both hepatitis A and B. A plasma-derived
HBV vaccine was licensed in 1981, but uptake was poor and was
removed from the U.S. market in 1992 after two recombinant hep-
atitis B vaccines became licensed by the FDA in 1986 and 1989. The
Corresponding author. Tel.: +1 404 718 8661; fax: +1 404 718-8585.
E-mail address: mgcollier@cdc.gov (M.G. Collier).
adolescent vaccination in 1996 [11]. Two inactivated whole-virus
hepatitis A vaccines became licensed by FDA in 1995 and 1996,
and the Advisory Committee on Immunization Practices (ACIP) rec-
ommended vaccination for high risk groups in 1996 [12], updated
recommendations in 1999 to include universal infant vaccination in
select U.S. states [13], with an expansion of the universal infant vac-
cination recommendations to all states in 2006 [14]. There is also
clear evidence that immune response after HAV and HBV vaccine is
impaired once chronic HCV infection or HIV infection has occurred
[15], making vaccination of those at risk before they acquire HIV
or HCV infection imperative. CDC recommends vaccination of all
PWID as part of a comprehensive plan to improve the health of this
population [16]. However, knowing which individuals to vaccinate
is complicated by the possibility that they could have already been
vaccinated for both hepatitis A and B, either during infancy or child-
hood depending on their U.S. state of residence and date of birth,
or due to their risk behaviors [1114]. One way to determine vac-
cination status of individual PWID is to ask them if theyve been

http://dx.doi.org/10.1016/j.vaccine.2015.04.019
0264-410X/Published by Elsevier Ltd.

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 M.G. Collier et al. / Vaccine 33 (2015) 28082812
vaccinated; however, studies on self-report of hepatitis B vaccina-
tion in PWID show poor prediction of actual serologic status, either
because their memory of what vaccines they received in childhood
is poor and they lack documentation of childhood vaccinations
or their titers waned over time [17]. Limited studies examining
self-report of hepatitis A vaccine among PWID are available. State
vaccination registries exist in many states and could potentially
be utilized to accurately identify individuals who received vaccine
doses. The objectives of this study were to determine susceptibility
to HAV and HBV infections among young PWID, assess self-report
of HAV and HBV vaccination compared to serologic testing, and
analyze risk factors for susceptibility to both vaccine-preventable
illnesses.
2. Methods
PWID between ages 1840 years-old in San Diego, California
were recruited to participate in the Study to Assess Hepatitis C
Risk (STAHR) between March 2009 and June 2010 [18]. Sociode-
mographic, drug use, behavioral, and access to care factors were
assessed using audio computer assisted self-interviewing (ACASI)
technology. All participants who agreed to blood testing for viral
hepatitis and HIV were tested for IgM antibodies to HAV (IgM
anti-HAV), total antibodies to HAV (total anti-HAV), antibodies to
HBV surface antigen (anti-HBs), total antibodies to HBV core anti-
gen (total anti-HBc), IgM antibodies to HBV core antigen (anti-HBc
IgM), and HBV surface antigen (HBsAg) using a chemiluminescent
immunoassay (VITROS ECi, Ortho Clinical Diagnostics, Rochester,
NY, www.orthoclinical.com). All participants with a positive total
anti-HBc test result were considered previously infected with
HBV. Antibodies to HCV (anti-HCV) were tested using Abbott
Axsym microparticle enzyme immunoassay (Abbott Laboratories,
Chicago, IL, www.abbott.com). Participants who tested positive for
anti-HCV were older than participants who tested negative for
anti-HCV [19].
Patients were asked, Have you ever received shots to prevent
hepatitis B? and Have you ever received shots to prevent hepatitis
A? to determine self-reported vaccination status. We calculated
the sensitivity and specificity of self-reported hepatitis A and B
vaccination by comparing participant responses to their antibody
testing results. We did not use a state vaccine registry to confirm
documentation of hepatitis A and B vaccine doses.
We performed separate analyses to identify factors associ-
ated with hepatitis B and hepatitis A susceptibility. Participants
with anti-HBs titers 10 mIU/ml but anti-HBc and HBsAg negative
results were considered to be immune to HBV through vaccination
[20]; those with anti-HBs titers 10 mIU/ml and HBsAg negative,
but anti-HBc positive, were considered immune to HBV through
natural infection. Participants with negative results for all three
markers (anti-HBs, HBsAg, and anti-HBc) were considered suscep-
tible to HBV infection. We defined susceptibility to hepatitis A as
testing negative for total anti-HAV. We analyzed differences in
selected covariates by comparing participants with antibody test-
ing results confirming susceptibility to those not susceptible for
HAV and HBV infections separately. Additionally, we determined
covariates associated with past or present hepatitis B infection
by comparing participants testing positive for anti-HBc to those
who tested negative. Odds ratios and 95% CIs were calculated. Fac-
tors significantly associated with positive antibody testing results
at a level of p < 0.1 during bivariate analysis were included in a
multivariate logistic regression analysis. Factors with p < 0.05 were
retained in the final model. We used SAS 9.3 (SAS Institute, Cary,
NC). This study was approved by the institutional review board of
the University of California San Diego. Participants received mon-
etary compensation for participating in the study.
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2809
3. Results
A total of 519 participants had specimens available for anti-HBc
testing. Fifty-one (10%) of 519 tested positive, indicating current
or past infection. Because inclusion criteria included only PWID
1840 years of age, this cohort is younger and thus had been inject-
ing less time than other PWID cohorts in the past [18]. Despite the
proximity of the Mexican border to the recruitment area, 96% of
participants were born in the U.S. HBsAg was positive in 7 (1%) par-
ticipants, indicative of chronic active infection with HBV, and no
one tested positive for anti-HBc IgM, indicative of acute infection.
Participants positive for total anti-HBc were older (median age 32,
IQR 2937 years) than those with anti-HBs only (median age 24,
IQR 2128 years, p < 0.001). Eight (16%) of 51 total anti-HBc posi-
tive participants were negative for HBsAg and had anti-HBs titers
<10 mIU/ml (isolated core); the remaining 32 were positive for
both total anti-HBc and anti-HBs and negative for HBsAg.
A total of 520 participants had specimens available for total
anti-HAV testing; 325 (63%) participants tested negative, indicat-
ing susceptibility to HAV infection. Anti-HCV was detected in 135
(26%) of 520 participants, indicating either active HCV infection or
past exposure to HCV; 56 of 135 (41%) were susceptible to HAV and
54 (40%) were susceptible to HBV. No HAV and HIV or HBV and HIV
co-infections were identified, but 2 participants were co-infected
with HBV and HCV.
3.1. HBV susceptibility
Of 519 participants with specimens for anti-HBc testing, we
excluded 47 participants who were not subsequently tested for
anti-HBs because of inadequate specimen volume, leaving 472 par-
ticipants for the HBV susceptibility analysis (Fig. 1); 245 (52%)
were total anti-HBc negative and had anti-HBs levels <10 mIU/ml,
indicating susceptibility to HBV infection, either because they
were never vaccinated, they were vaccinated but did not mount
an antibody response, or they were vaccinated but their anti-
body titers waned over time (Table 1). One hundred seventy-six
(37%) participants had evidence of immunity to HBV from vac-
cination and another 51 participants had evidence of immunity
to HBV due to natural infection. Bivariate analysis showed that
HBV susceptible participants were older, more likely male, more
likely homeless, less likely ever tested for HIV and HCV, and
more likely to be HAV susceptible than participants immune to
HBV from vaccination or natural infection. Multivariate analy-
sis demonstrated that older age, ever tested for HCV, and HAV
susceptibility was independently associated with HBV suscep-
tibility (Table 3). One hundred fifty-one participants reported
never having HBV vaccination; of these, 41 had anti-HBs titers
10 IU/ml. One hundred eighty-two participants reported hav-
ing HBV vaccination; of these, 81 had anti-HBs titers <10 IU/ml.
Compared to serologic testing, self-reported history of hepatitis
B vaccination had a sensitivity and specificity of 71% and 58%,
respectively.
3.2. HAV susceptibility
Of 520 tested for anti-HAV, 325 (63%) had no detectable total
anti-HAV antibodies (susceptible, never infected or vaccinated);
no one (0%) tested positive for anti-HAV IgM, indicative of acute
infection. Bivariate analysis showed that HAV susceptible partic-
ipants were more likely to be white, have higher income levels,
report ever using a syringe exchange program (SEP), and suscep-
tible to HBV (Table 2). They were less likely to have been born
outside the U.S. and ever diagnosed with an STI in the past. Multi-
variate analysis showed that being born outside the U.S., ever used
SEP, and HBV susceptibility were independently associated with
2810 M.G. Collier et al. / Vaccine 33 (2015) 28082812

Fig. 1. Hepatitis B serology testing algorithm. * An anti-HBs result of 10 IU/ml suggests immunity from hepatitis B. An anti-HBs result of <10 IU/ml suggests no immunity
from hepatitis B.

HAV susceptibility (see Table 3). Two hundred fifty-five participants
reported never having HAV vaccination; of these, 83 tested posi-
tive for anti-HAV. One hundred twenty-four participants reported
having HAV vaccination; of these, 65 tested negative for anti-HAV.
Compared to serologic testing, self-reported history of hepatitis
A vaccination had a sensitivity and specificity of 41% and 73%,
respectively.
4. Discussion
This study showed that self-reported history of hepatitis A
and B vaccination by young PWID is poorly predictive of serologic
evidence of immunity, that many are already infected with HCV,
and that many remain susceptible and need to be vaccinated
against HAV and HBV infection. Even though hepatitis A and B

Table 2
Table 1
Bivariate analysis of factors associated with HAV susceptibility among 1840 year
Bivariate analysis of factors associated with HBV susceptibility among 1840 year
old persons who inject drugs.
old persons who inject drugs.
Characteristic Anti-HAV Anti-HAV Odds ratio
Characteristic Anti-HBs Anti-HBs Odds ratio (95%CI)
positive negative (95%CI)
positive negative
(N = 195) (N = 325)
(N = 227) (N = 245)
Median age (years, IQR) 28 (2433) 28 (2433) 1.01 (0.981.04)
Median age (years, IQR) 26 (2230) 29 (2635) 1.10 (1.061.14)
Median years injecting 6 (211) 6 (212) 0.99 (0.961.02)
Median years injecting 5 (210) 6 (212) 1.02 (0.991.05)
(years, IQR)
(years, IQR)
Male sex 138 (73) 228 (72) 0.99 (0.661.48)
Male sex 150 (69) 184 (77) 1.49 (0.982.25)
Race
Race
White 74 (38) 177 (55) Ref
White 105 (46) 125 (51) Ref
Black 18 (9) 20 (6) 0.47 (0.230.93)
Black 19 (8) 16 (6) 0.71 (0.351.44)
Hispanic 63 (32) 76 (23) 0.50 (0.330.78)
Hispanic 55 (24) 66 (27) 1.01 (0.651.57)
Other 40 (21) 52 (16) 0.54 (0.330.89)
Other 48 (21) 38 (16) 0.67 (0.401.10)
Born outside U. S. 14 (7) 9 (3) 0.38 (0.160.88)
Born outside U.S. 9 (4) 13 (5) 1.35 (0.573.22)
Travel Mexico 120 (64) 205 (68) 1.17 (0.801.71)
Travel Mexico 142 (67) 153 (67) 0.98 (0.661.46)
Spanish speaking 43 (22) 62 (19) 0.83 (0.541.29)
Spanish speaking 43 (19) 48 (20) 1.04 (0.661.65)
Education Education
Less than high school 62 (28) 62 (26) Ref Less than high school 54 (28) 81 (26) Ref
diploma/GED diploma/GED
High school 91 (41) 93 (39) 1.02 (0.651.61) High school 71 (37) 129 (41) 1.2 (0.771.90)
diploma/GED only diploma/GED only
More than high school 68 (31) 85 (35) 1.25 (0.772.10) More than high school 68 (35) 106 (34) 1.0 (0.661.65)
diploma/GED diploma/GED

Income level Income level

No income 53 (24) 67 (28) Ref No income 65 (34) 69 (22) Ref
$19999 122 (55) 122 (51) 0.79 (0.511.23) $19999 96 (50) 175 (56) 1.72 (1.132.62)
>$10,000 46 (21) 50 (21) 0.86 (0.501.47) >$10,000 32 (17) 70 (22) 2.06 (1.203.53)
Homeless 151 (63) 115 (52) 1.60 (1.102.32) Homeless 108 (56) 189 (60) 1.19 (0.831.71)
Ever incarcerated 169 (76) 180 (75) 0.93 (0.611.44) Ever incarcerated 149 (77) 240 (76) 0.95 (0.621.45)
Ever used SEP 103 (48) 96 (41) 0.76 (0.521.11) Ever used SEP 70 (37) 152 (50) 1.68 (1.162.43)
Ever HIV test 165 (78) 156 (68) 0.60 (0.390.92) Ever HIV test 138 (77) 218 (71) 0.75 (0.491.14)
Ever diagnosed STI 41 (19) 36 (16) 0.78 (0.471.27) Ever diagnosed STI 45 (24) 50 (16) 0.63 (0.400.99)
Ever HCV tested 112 (57) 100 (45) 0.62 (0.420.92) Ever HCV tested 88 (52) 144 (49) 0.87 (0.611.31)
Anti-HCV positive 61 (27) 54 (22) 0.76 (0.501.16) Anti-HCV positive 56 (29) 79 (25) 0.80 (0.541.20)
HAV susceptible 126 (42) 174 (58) 1.95 (1.332.85) HBV susceptible 71 (41) 174 (58) 1.95 (1.332.85)

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 M.G. Collier et al. / Vaccine 33 (2015) 28082812
Table 3
Multivariate analysis of factors associated with HAV and HBV susceptibility among
1840 year old persons who inject drugs.
Variable Adjusted odds 95% Confidence
ratio interval
HAV susceptibility analysis
U.S. born 3.57 1.399.09
Ever used SEP 1.96 1.302.95
HBV susceptible 2.03 1.363.04
HBV susceptibility analysis
Age 1.10 1.071.15
Ever tested for HCV 0.50 0.330.76
HAV susceptible 1.76 1.152.69
vaccination of PWID has been recommended by ACIP since 1996
[12], almost half of STAHR participants had inadequate anti-HBs
titers and more than half did not have anti-HAV titers. Importantly,
nearly half of PWID infected with HCV did not have adequate
anti-HBs titers or anti-HAV titers to suggest protection despite
their increased risk for fulminant liver failure should they become
infected with either virus.
The association of HBV susceptibility with increasing age is often
due to the well documented loss of anti-HBs over time in persons
vaccinated before 1 year of age; however, this does not necessar-
ily mean that protection has been lost [21]. Other explanations
would be either waning immunity over time or decreased likeli-
hood for older PWID to have received catch-up HBV vaccination
during childhood and adolescence [11]. The association of HBV
susceptibility with lower likelihood of HCV testing suggests that
opportunities for HCV testing and HBV vaccination were related;
perhaps missed opportunities for both are due to lack of access to
health care or integrated delivery of care [16]. HAV susceptibility
was associated with HBV susceptibility likely for the same reasons.
Unlike for HBV, there is no serologic test to distinguish immu-
nity induced by HAV vaccine from natural infection. Because of this,
specifically white, U. S. born, higher socioeconomic status partic-
ipants were less likely to be exposed to HAV, in addition to not
having been vaccinated, and therefore more likely to be suscepti-
ble [22]. As the opportunity to be vaccinated would be theoretically
the same for both infections because both are recommended for
the PWID risk group [16], even though the opportunity would be
practically different for individuals depending on when and where
they were born [1114], participants with increased HAV suscep-
tibility (unvaccinated and unexposed) were also more likely to be
susceptible to HBV.
We encountered limitations during this study. All risk behav-
iors were self-reported, although we attempted to minimize recall
bias for the drug use questions by using a short recall period
(3 months) for injection behaviors and substance use. The cross-
sectional design of the study makes it impossible to establish
temporal relationships. The study sample came from a narrow pop-
ulation (PWID in San Diego from 2009 to 2010 using three different
recruitment methods [18]) which might affect the ability to gen-
eralize our findings. Also, the utility of anti-HBs as a surrogate to
determine protection against hepatitis B virus might be limited
because of the fact that anti-HBs tends to disappear in persons vac-
cinated at less than one year of age despite no loss of protection
against the virus [21].
PWID are at increased risk for hepatitis A, B, and C infections
compared to the general population. If acquired alone or in combi-
nation, these viruses increase morbidity and mortality from acute
and chronic liver disease compared to mono infection. Therefore,
it is important to vaccinate all PWID for HAV and HBV, despite
the difficulties in reaching this population for preventive health
services, even when resources are available. Many STAHR partic-
ipants were susceptible to hepatitis A and B, indicating that they
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2811
either had never been exposed to either virus, they had no oppor-
tunity to be vaccinated, they were vaccinated but did not develop
adequate antibody titers, they were vaccinated and their antibody
titers waned over time, or they were protected but were anti-HBs
negative. PWID should be screened for HBsAg because they are at
risk for chronic infection, and if this is being done, it is an oppor-
tunity to test for anti-HBs and anti-HBc to identify those who are
susceptible to HBV. However, if no blood draw is available, vaccina-
tion should still occur [23]. One strategy for community outreach
programs and providers to decrease unnecessary hepatitis A and B
vaccine doses is to check individual names in a state vaccination
registry. If no doses were documented, then the hepatitis A and B
vaccination series is given and documented in the state vaccination
registry. This would be a low-cost and reliable way to assure docu-
mentation of vaccine doses, and would not delay giving the vaccine
to susceptible PWID who might not return for follow-up. Despite
the inherent difficulties of caring for this vulnerable population,
increasing the number of participants who are not susceptible to
i.e. vaccinated against HAV and HBV infections would have a
major beneficial public health impact.
CDC disclaimer
The findings and conclusions in this report are those of the
authors and do not necessarily represent the official position of
the Centers for Disease Control and Prevention.
Conflict of interest
None of the authors have any conflicts of interest to report.
Acknowledgement
This study was funded by the Centers for Disease Control and
Prevention grant number 200 2007 21016.
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