Lower Genitourinary Tract Sources of Seminal HIV
Robert W. Coombs, MD, PhD,*† David Lockhart, MSc,‡ Susan O. Ross, RN,§ Leslie Deutsch, RN,§
Joan Dragavon, BSc, MLM,* Kurt Diem, BSc,* Thomas M. Hooton, MD,† Ann C. Collier, MD,†
Lawrence Corey, MD,*† and John N. Krieger, MD§
Objective: To investigate genital tract sources of HIV-1, we conducted
extensive genitourinary sampling of 23 seropositive men without
urethritis who shed HIV in their seminal plasma.
Design: Semen was collected, then samples were obtained for HIV
RNA in blood plasma, urethral fluid, preYprostate massage fluid/urine
(PMF/U) and post-PMF/U, and expressed prostatic secretions. System-
atic transrectal ultrasound-guided prostate biopsies obtained from
multiple prostate areas were evaluated for HIV RNA and DNA.
Results: Seminal HIV RNA levels correlated with HIV RNA levels in
urethral fluid and post-PMF/U and with prostate biopsies HIV DNA, but
not with expressed prostatic secretions HIV RNA. However, only the
HIV RNA level in post-PMF/U independently predicted that in semen
(2.77-fold change in semen for each 10-fold change in post-PMF/U;
95% confidence interval, 1.0Y7.7) accounting for one third of the
seminal HIV RNA level variation, irrespective of adjustment for
antiretroviral therapy.
Conclusions: These data indicate that distal genitourinary sources
other than the prostate appear to be the major source of seminal HIV in
men without clinical urethritis or prostatitis. Because the HIV RNA
level in blood plasma is not reliable as an independent clinical predictor
of virus levels in seminal plasma, these findings also extend the concept
that the male genital tract is a distinct virological compartment from
blood.
Key Words: AIDS, HIV, RNA, DNA, semen, prostate gland,
compartmentalization, urethra, sexual transmission, male
(J Acquir Immune Defic Syndr 2006;41:430Y438)
S
emen is well established as a primary vehicle for sexual
transmission of HIV-1. Surprisingly, the anatomic sites
and sources of seminal HIV are largely unknown. Based on
earlier studies showing that seminal shedding of HIV RNA
and HIV DNA continued after vasectomy, we and others
deduced that distal genitourinary anatomic sites are likely
important sources of seminal HIV.
1Y4
We report a pilot study
to test the hypotheses that the urethra and prostate are critical
viral sources and that these sites remain reservoirs of genital
virus in men who continue to shed seminal HIV while on
antiretroviral therapy (ART). We localized and quantified
HIV viral burdens in specimens systematically obtained from
various genitourinary sites by using systematic anatomic
sampling of genital fluids and prostate biopsies (Pbx).
METHODS
Study Design
Our clinical population of HIV-seropositive men was
screened between April 1999 and January 2003 to identify
men either on no ART or on stable regimens (for at least
3 months) and who had more than 200 HIV RNA copies/mL
of blood and seminal plasma. Following written informed
consent, each participant agreed to provide 3 separate
samples of semen and blood before collecting urethral fluid
(UrF; both a urethral swab and/or a less invasive wick), ex-
pressed prostate secretions (EPSs), and 6 Pbx. All nonsemi-
nal genitourinary specimens were collected during a single
clinic visit. The initial study design included only UrF and
the prostate biopsy procedure (since we obtained multiple
biopsies). However, we modified the protocol to also include
preYprostate massage fluid collected in urine (PMF/U) and
post-PMF/U when we noted a low rate of HIV detection in
biopsies from the initial participants.
Each subject had a standardized history and physical
examination by the same examiner to exclude potential sub-
jects with symptoms or signs of active urethritis, prostatitis,
or other active genitourinary tract problems. Semen samples
were collected at each subject’s home and transported by taxi
to the urology laboratory.
5
After semen analysis and staining,
the specimen was sent to the retrovirus laboratory by our
courier service. The semen analysis studies were accom-
plished within 2 hours, and viral studies were initiated within
4 hours of sample collection.
6
Blood Specimens
Peripheral blood was collected into EDTA-containing
tubes (Becton Dickinson, Franklin Lakes, NJ), separated
within 8 hours of collection into plasma and peripheral blood
mononuclear cells by Ficoll-Hypaque gradient centrifugation,
then frozen at
j
70-C. All specimens were tested in batch for
CLINICAL SCIENCE
430 J Acquir Immune Defic Syndr & Volume 41, Number 4, April 1, 2006
Received for publication August 8, 2005; accepted November 16, 2005.
From the Departments of *Laboratory Medicine, †Medicine, ‡Biostatistics, and
§Urology, University of Washington, Seattle, WA.
Informed consent was obtained from all subjects following human experimen-
tation guidelines of the United States Department of Health and Human
Services and the University of Washington.
The authors have no commercial associations that might pose a conflict of
interest.
Presented in part at the 11th Conference on Retroviruses and Opportunistic
Infections; February 8 to 11, 2004; San Francisco, CA (abstract 420).
Funding sources: DK-49477; Centers for AIDS Research AI-27757; AIDS
Clinical Trials Group AI-27664 and AI-38858, AI-41535, and HD-40540.
Reprints: Robert W. Coombs, MD, PhD, Harborview Medical Center, Research
& Training Building, Room 706, 325-9th Avenue, Seattle, WA 98104-2499
(e-mail: bcoombs@u.washington.edu).
Copyright * 2006 by Lippincott Williams & Wilkins
Copyr ight © Lippincott Williams & Wilkins. Unauthor iz ed reproduction of this article is prohibited.