Short Communication
Human Papillomavirus Capsid Antibody Response to
Natural Infection and Risk of Subsequent
HPV Infection in HIV-Positive and
HIV-Negative Women
Raphael P. Viscidi,
1
Brad Snyder,
3
Susan Cu-Uvin,
4
Joseph W. Hogan,
3
Barbara Clayman,
1
Robert S. Klein,
5
Jack Sobel,
6
and Keerti V. Shah
2
1
Johns Hopkins University School of Medicine and
2
School of Public Health, Baltimore, Maryland;
3
Center for Statistical Sciences,
Department of Community Health and
4
The Miriam Hospital, Brown University, Providence, Rhode Island;
5
Montefiore Medical Center
and Albert Einstein College of Medicine, Bronx, New York; and
6
Harper Hospital, Detroit, Michigan
Abstract
The association between seropositivity to virus-like particles
(VLP) of human papillomavirus (HPV) types 16, 18, 31, 35, or
45 and subsequent cervical HPV infection was examined in
829 women with HIV and 413 risk-matched HIV-negative
women. We found no statistically significant differences
between HPV-seropositive and HPV-seronegative women in
the risk of a new infection with the homologous HPV type,
with the exception of a reduced risk of HPV 45 infections 4.5
years beyond the baseline serology measurement in HIV-
positive women [hazard ratio, 0.21; 95% confidence interval
(CI), 0.05-0.89]. Among HIV-negative women, HPV seropo-
sitivity was not associated with a statistically significant
reduced risk of infections with related viruses in the HPV 16,
HPV 18, or ‘‘other’’ HPV groups. Among HIV-positive
women, HPV seropositivity was associated with a slightly
increased risk of infection with group-related viruses, but
the differences were only statistically significant for infec-
tion with HPV 16 group viruses (hazard ratio, 1.6; 95% CI,
1.1-2.3) in HPV 18-seropositive women and for infections
with ‘‘other’’ HPV group viruses in HPV 31-seropositive
women (hazard ratio, 1.45; 95% CI, 1.0-2.0). The lack of a
protective immune effect from natural infection is most
likely due to the low level of antibody elicited by natural
HPV infection and/or the potential for reactivation of HPV,
especially in HIV-positive women. (Cancer Epidemiol Bio-
markers Prev 2005;14(1):283 – 8)
Introduction
Human papillomavirus (HPV) is the most common sexually
transmitted viral infection in the world. An estimated 60% of
sexually active women will become infected with a genital
HPV in their lifetime (1– 3). In the majority of women, the
infection is asymptomatic and cleared within weeks to months
(4, 5). More than 40 HPV types infect the genital tract.
Whether the antibody response to one type of HPV confers
protection against subsequent infection with the same or
related types is unknown. For many viruses, the presence of
serum neutralizing antibodies is a correlate of immune
protection (6). HPV cannot be cultivated in tissue culture;
therefore, true neutralization assays are not available. Surro-
gate neutralization assays with the use infectious pseudovi-
rions have been developed but these methods are insensitive
and inefficient for large-scale epidemiologic studies (7).
Capsid proteins of HPV produced in insect cells self-assemble
into virus-like particles (VLP; ref. 8). VLPs have many
immunologic features of native virions including display of
type-specific, surface-exposed neutralizing epitopes (8), and
are suitable reagents for use in enzyme immunoassays (9).
Among recipients of an HPV 16 L1 VLP vaccine, for example,
the serum antibody titer measured by VLP-based enzyme
immunoassay was highly correlated with the neutralizing
antibody titer, thereby indicating the VLP-based enzyme
immunoassay can serve as a surrogate marker for neutralizing
antibodies (10).
Compared with HIV-negative women, HIV-infected women
have a higher prevalence of cervical HPV infection (11) and are
at increased risk of acquiring new HPV infections (12).
Whether prior HPV type-specific immune status influences
the risk of HPV infection in HIV-positive women is unknown.
The HIV Epidemiology Research Study (HERS) is a
large prospective cohort study of HIV-positive and risk-
matched HIV-negative women recruited at multiple sites
around the United States (13). The women in HERS have had
HPV DNA measurements at approximately 6-month intervals
for up to 6 years, providing a wealth of data on detection of
type-specific HPV infection.
To assess whether anti-VLP antibodies are a marker of
immune protection, we examined measures of baseline serum
antibodies to VLPs of HPV types 16, 18, 31, 35, and 45 in 829
HIV-positive and 413 HIV-negative women enrolled in HERS
and analyzed the association of seropositivity with risk of
detection of HPV DNA during follow-up.
Methods
Study Population. The study population was drawn from
HERS. These women were recruited at four sites: Baltimore,
MD; Bronx, NY; Detroit, MI; and Providence, RI. The cohort
characteristics, recruitment methods, and protocols of the
Received 3/30/04; revised 7/16/04; accepted 8/6/04.
Grant support: NIH grants AI-42058 (R.P. Viscidi) and R01-AI-50505 (J.W. Hogan), the
Lifespan/Tufts/Brown Center for AIDS Research (NIH grant P30-AI-42853), and Centers for
Disease Control and Prevention (contracts U64/CCU106795, U64/CCU206798, U64/
CCU306802, and U64/CCU506831).
The costs of publication of this article were defrayed in part by the payment of page charges.
This article must therefore be hereby marked advertisement in accordance with 18 U.S.C.
Section 1734 solely to indicate this fact.
Requests for reprints: Raphael P. Viscidi, Johns Hopkins Hospital, Blalock Room 1105, 600
North Wolfe Street, Baltimore, MD 21287. Phone: 410-614-1494; Fax: 410-955-3723. E-mail:
rviscid1@jhem.jhmi.edu
Copyright D 2005 American Association for Cancer Research.
283
Cancer Epidemiol Biomarkers Prev 2005;14(1). January 2005
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