Objective
Human herpesvirus 8 (HHV-8) infection is common among children in areas where Kaposi sarcoma is endemic. Human herpesvirus 8 is uncommon in children but prevalent in adults at risk for human immunodeficiency virus (HIV) infection in the United States, including men who have sex with men (MSM) and women who engage in high-risk sexual behavior. We examined the prevalence and predictors of HHV-8 infection among adolescents with or at high risk for acquiring HIV infection.
Design
Cross-sectional analysis.
Setting
National study of HIV infection among adolescents in primary care.
Participants
A total of 537 young adults practicing high-risk sexual behavior, of which 403 were women and 134 were men; among the 134 men, 75% were MSM.
Interventions
Detailed questionnaires and testing for serum antibodies to HHV-8.
Outcome Measure
Detection of serum antibodies to HHV-8.
Results
Sixty (11.2%) of 537 young adults were HHV-8 seropositive, including 20 MSM (19.6%), 2 male heterosexuals (6.5%), and 27 female heterosexuals (8.2%). The prevalence of HHV-8 in HIV-positive MSM (17/74 [23.0%]) was twice as high as that in HIV-negative MSM (3/28 [10.7%]) (P = .18), but no characteristic predicted HHV-8 infection among MSM. In multivariate analysis, history of gonorrhea (odds ratio [OR], 2.8; 95% confidence interval [CI], 1.4-5.7; P<.01), history of having sex with women (OR, 2.4; 95% CI, 1.1-5.3; P = .03), and African American race (OR, 3.4; 95% CI, 1.1-10.0; P = .03) were associated with HHV-8 infection among women.
Conclusions
Human herpesvirus 8 is common among US adolescents practicing high-risk sexual behaviors. Sexual identity, race, and sexual behavior may influence the risk of infection with HHV-8 in women.
Human herpesvirus 8 (HHV-8) (also known as Kaposi sarcoma [KS]–associated herpesvirus) was first identified in 1994.1 In the United States and western Europe, the virus is likely acquired through sexual contact and is largely restricted to men who have sex with men (MSM)2 and women at high risk for sexually transmitted or parenteral infections.3 Infection is rare among US children4 but ranges from 30% to 100% in African children, who typically acquire HHV-8 before the onset of puberty but after the perinatal period.5-7 In many parts of Africa, KS is a tumor endemic among children with and without human immunodeficiency virus (HIV) infection,8-10 but most HHV-8 infections worldwide are asymptomatic.
Human herpesvirus 8 is shed frequently in the oropharynx.11 Contact with saliva during sex is associated with incident HHV-8 infection in adult MSM,11-14 whereas household contact with saliva may be a mode of HHV-8 transmission in African children.15 Children contract other HHV infections through contact with saliva, including herpes simplex virus type 1 (HSV-1),16 cytomegalovirus,17 and Epstein-Barr virus,18 which are all ubiquitous worldwide. If some or all HHV-8 transmission is explained by contact with saliva, it remains unclear why HHV-8 infection is not more prevalent in most parts of the developed world.
We hypothesized that HIV-positive adolescents and young adults and those practicing high-risk sexual behavior may be at substantial risk of HHV-8 infection because of homosexual contact and multiple sex partners. We therefore examined the seroprevalence and predictors of HHV-8 infection among such individuals.
The REACH (Reaching for Excellence in Adolescent Care and Health) project recruited adolescents aged 13 to 18 years from 15 clinical sites in 13 US cities to evaluate the biomedical and behavioral characteristics of HIV infection.19 Eligible adolescents either had acquired HIV sexually or parenterally or were HIV negative but with similar age and risk behaviors. Participants or their guardians provided informed consent, as approved by each site's institutional review board and human experimentation guidelines of the US Department of Health and Human Services. Subjects underwent physical examination, questionnaire collection, and phlebotomy at 3-month intervals for HIV-positive and at 6-month intervals for HIV-negative persons.
A combined whole-virus enzyme immunoassay with immunofluorescence assay detected serum HHV-8 antibodies from the last study visit available.20 Antigens derived from purified viral lysate (Advanced Biotechnologies Inc, Columbia, Md) are plated on 96-well plates. After application of human serum, bound antibodies are detected by horseradish peroxidase–conjugated goat anti–human IgG Fc (Chemicon, Temecula, Calif) and TMB (3,3′,5,5′-tetramethylbenzidine) substrate (KPL Inc, Gaithersburg, Md). Optical densities are determined in a standard enzyme-linked immunosorbent assay plate reader. Samples with intermediate enzyme immunoassay values are rerun with a standard immunofluorescence assay for antibodies to latent and lytic antigens in body cavity–based B-cell lymphoma 1 cells. This testing strategy was found to be 88% sensitive and 97% specific for the identification of HHV-8 infection.
Laboratory tests for gonorrhea, chlamydia, and syphilis were performed biannually. For HIV-positive participants, the AIDS Clinical Trials Group laboratories determined T-cell lymphocyte counts by flow cytometry, and HIV plasma RNA levels were quantified by nucleic acid sequence-based amplification (Organon Technika, Westchester, Pa).
For each potential predictor of HHV-8 infection, we selected data from the period closest to the date of HHV-8 antibody assessment, with the exception of some characteristics collected only at baseline.
The analysis was restricted to participants previously identified as having a high HHV-8 prevalence among adults, that is, MSM (defined by self-identification as being homosexual or bisexual or reporting any history of anal receptive sex) and all women (who by inclusion in the cohort were at risk for or had HIV infection). Men reporting exclusively heterosexual partners and behaviors were excluded.
Statistical analysis was performed using SAS for Windows Version 8.2 software (SAS Institute Inc, Cary, NC). Associations with HHV-8 status were evaluated using univariate and multivariate logistic regression. Multivariate model selection proceeded by including all factors univariately associated with HHV-8 at P<.1 and eliminating factors until all remaining predictors were significant at P≤.05.
Demographic characteristics of study participants
Of the 550 adolescents enrolled in the REACH project, 537 (97.6%) had serum samples available for HHV-8 testing. Participants had a median follow-up time of 33 months (range, 0-57 months) prior to the HHV-8 serologic assessment. Of the 537 participants, 134 (25.0%) were men and 403 (75.0%) were women. Among the 134 men, 102 (76.1%) were classified as MSM.
The median age of participants at the time of HHV-8 serologic assessment was 19 years (range, 18-21 years), with most (71.1%) identifying themselves as African American (Table 1). A greater proportion of women study participants were African American when compared with MSM (75.4% of women vs 53.9% of MSM; P<.001).
Risk behavior of study cohort
Most (82.1%) of the women identified themselves as heterosexual (Table 1), whereas 47.8% of the men identified themselves as homosexual. Men who have sex with men were more likely to report a history of sex with a commercial sex worker (20.6% of MSM vs 7.9% of women [P<.01]) but had similar exposure to HIV-positive sex partners (24.5% of MSM vs 19.6% of women [P = .34]). Anal sex was common among both MSM and women. At the time of HHV-8 serologic testing, 12.7% of women and 8.8% of MSM had a concurrent diagnosis of chlamydia; 5.2% of women and 3.9% of MSM, of gonorrhea; and 2.2% of women and 3.9% of MSM, of syphilis. Intravenous drug use was uncommon among the study youth, reported by 0.5% of women and 6.9% of MSM.
At the time of enrollment, 64.3% of women and 70.6% of MSM were HIV-positive, and an additional 2 MSM acquired HIV during the study. The median CD4 count was 601 cells/μL (interquartile range, 398-839 cells/μL), and the median HIV plasma RNA level was 3.9 log copies/mL. Only 7 participants reported having an AIDS-defining illness21 and no participant had KS.
Frequency and predictors of hhv-8 infection
Overall, 60 (11.2%) of 537 participants were HHV-8 seropositive, including 20 (19.6%) of 102 MSM, 2 (6.5%) of 31 heterosexual men (data not shown), and 38 (9.4%) of 403 women (χ2 test, P<.01). The Figure depicts the prevalence of HHV-8 infection by demographic group and HIV status (26 [10.0%] of 259 HIV-positive women vs 12 [8.3%] of 144 HIV-negative women; odds ratio [OR], 1.2; 95% confidence interval [CI], 0.6-2.5; P = .58; 1 [7.1%] of 14 vs 1 [5.9%] of 17 heterosexual males; OR, 1.2; 95% CI, 0.1-23.8; P = .89; 17 [23.0%] of 74 vs 3 [10.7%] of 28 MSM; OR, 2.5; 95% CI, 0.7-9.4; P = .18). There was no significant difference in the prevalence of HHV-8 infection among HIV-negative women and HIV-negative MSM (8.3% vs 10.7%, P = .68). In a univariate analysis, only 3 factors were significantly associated with an increased risk of HHV-8 infection among women, including a history of gonorrhea (OR, 2.8; 95% CI, 1.4-5.7; P = .002) and sex with other women (WSW) (OR, 2.4; 95% CI, 1.1-5.3; P = .03) (Table 2). In a multivariate model restricted to female participants, these factors remained significantly associated with an elevated risk of HHV-8 infection. No factors were significantly associated with HHV-8 infection among MSM.
In subset analyses of 331 HIV-positive subjects separated by sex, neither HIV RNA level (modeled continuously, OR, 1.4; 95% CI, 0.9-2.1; P = .12 among women, and OR, 0.8; 95% CI, 0.4-1.4; P = .40 among MSM) nor highly active antiretroviral treatment (HAART) use (OR, 0.5; 95% CI, 0.1-1.2; P = .15 among women, and OR, 1.5; 95% CI, 0.5-4.8; P = .46 among MSM) was associated with HHV-8 infection.
A decade after the initial identification of HHV-8, many questions still remain about its epidemiology.22 The restriction of HHV-8 infection to specific geographic and demographic “pockets” is perplexing given the evidence for the transmission of HHV-8 through saliva and the comparative ubiquity of other HHVs.12 We found antibodies to HHV-8 in 11.2% of adolescents with HIV infection and/or high-risk sexual and substance use behavior. Our results provide several important insights into the epidemiology of HHV-8 in adolescents.
In the United States and western Europe, 2% to 10% of the general population have serum antibodies to HHV-8,23 but little is known about the timing of HHV-8 acquisition. One previous study24 found a low rate of infection among MSM aged 16 to 22 years in the United States, which was comparable to the rate in a matched population of young heterosexual males and females.
We found the highest rates of HHV-8 infection in HIV-positive adolescent MSM, but this rate is lower than the 30% to 75% prevalence previously observed in populations of adult HIV-positive MSM.14,25 In a cross-sectional study, the relationship between the timing of HHV-8 and HIV infection could not be assessed. The lower prevalence of HHV-8 in HIV-positive adolescent MSM compared with adult MSM suggests that they acquire HIV prior to HHV-8. This may be clinically relevant because the incidence of KS appears to be higher among MSM who acquire HHV-8 after HIV infection compared with those first infected with HHV-8.26
The rarity of KS among women in the pre-HAART era led many to speculate that HHV-8 infection was uncommon among women.27 Recent data, however, suggest rates that are 2 to 4 times higher than the rate among the general population of the United States and similar to that among HIV-negative MSM.3,28,29 We identified 2 novel risk factors for HHV-8 infection among young women.
We found a high HHV-8 prevalence among WSW but did not specifically ask about their behaviors. Previous studies offer potential explanations for the higher prevalence in this group. First, WSW in this study infrequently reported exclusively female sex partners, and WSW are more likely to have sex with bisexual males.30-32 Second, some WSW practice riskier sexual behavior, including concurrent substance abuse with sex.32 Third, exposure of the oral cavity to genital or oral secretions during sex is nearly universal among WSW33 and the use of protective barriers is uncommon.34 Human herpesvirus 8 infects epithelial cells, which may be the site of primary infection.11,35 Limited studies in women find HHV-8 in oral and genital secretions.36-39 Whether HHV-8 shed in saliva is transmissible through other mucosal sites, such as the genital epithelium, has yet to be determined. Taken together, it is possible that sexual mixing between WSW and other demographic groups with high HHV-8 prevalence may allow transmission to female partners during oro-oral or orogenital sex.
The association between HHV-8 and gonorrhea has been reported in both men40,41 and women,42 but the small number of participants in our study infected with both HHV-8 and gonorrhea precluded a comprehensive analysis. Sexual networks could also help explain the relationship between HHV-8 prevalence and gonorrhea in women because previous studies43 have found that persons infected with Neisseria gonorrhoeae have larger, more demographically discordant sexual networks.
Our observed association between African American race and HHV-8 infection has been corroborated by 2 other cohorts of adult women3,28 and, to our knowledge, has not been described in men.44 Studies of sexual networks among African American adolescents show that most report their typical sex partner to be older and sex with these partners to be often unprotected.45 This “disassortive mixing” by age increases the risk of sexually transmitted infections in adolescents46 and of HSV-2 infection in adults.47
The findings of this study must be taken in the context of the included study population. Specifically, the relatively small number of MSM limits the ability to detect predictors of HHV-8 infection among this group. Conversely, the overrepresentation of female or African American youths may have allowed us to identify previously uncharacterized risks for HHV-8 in these groups. Finally, the lack of information on behaviors specifically associated with the exchange of saliva is a limitation of previous studies and our current investigation.
In sum, we found HHV-8 infection to be common among US adolescents practicing high-risk sexual behavior and identified novel risk factors for HHV-8 infection in females. The incidence of KS in the United States and western Europe has declined dramatically in the HAART era,48 with little change in the prevalence of HHV-8 infection.49 The long-term sequelae of infection with HHV-8, a known oncogenic virus, are still undetermined, and specific therapy for HHV-8 infection is lacking. Consequently, prevention of HHV-8 infection remains important, and future studies should examine the mode of HHV-8 transmission and acquisition.
Correspondence: Corey Casper, MD, MPH, Program in Infectious Diseases, Fred Hutchinson Cancer Research Center, 1100 Fairview Ave N, Mail Stop D3-100, Seattle, WA 98109 (ccasper@u.washington.edu).
Accepted for Publication: April 27, 2006.
Author Contributions:Study concept and design: Casper, Wald, Corey, and Moscicki. Acquisition of data: Morrow and Moscicki. Analysis and interpretation of data: Casper, Meier, Wald, Corey, and Moscicki. Drafting of the manuscript: Casper, Meier, and Moscicki. Critical revision of the manuscript for important intellectual content: Meier, Wald, Morrow, Corey, and Moscicki. Statistical analysis: Casper and Meier. Obtained funding: Corey and Moscicki. Administrative, technical, and material support: Casper, Morrow, Corey, and Moscicki. Study supervision: Wald, Morrow, and Corey.
Funding/Support: This study was supported in part by National Institutes of Health (NIH) grant U01-HD32830 from the National Institute of Child Health and Human Development with cofunding from the National Institutes on Drug Abuse, of Allergy and Infectious Diseases, and of Mental Health; NIH grants K23 AI54162 and U19 AI31448 from the National Institute of Allergy and Infectious Diseases; and a Clinical Scientist Development Award from the Doris Duke Charitable Foundation.
Acknowledgment: We thank the investigators and staff of the Adolescent Medicine HIV/AIDS Research Network (1994-2001) (listed in the Journal of Adolescent Health [2001;29(suppl):5-60]), and the adolescents and young adults who participated in the REACH project, for their valuable contributions.
1.Chang
YCesarman
EPessin
MS
et al. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma
Science 1994;2661865- 1869
PubMedGoogle ScholarCrossref 2.Martin
JNGanem
DEOsmond
DHPage-Shafer
KAMacrae
DKedes
DH Sexual transmission and the natural history of human herpesvirus 8 infection
N Engl J Med 1998;338948- 954
PubMedGoogle ScholarCrossref 3.Cannon
MJDollard
SCSmith
DK
et al. HIV Epidemiology Research Study Group, Blood-borne and sexual transmission of human herpesvirus 8 in women with or at risk for human immunodeficiency virus infection
N Engl J Med 2001;344637- 643
PubMedGoogle ScholarCrossref 4.Martro
EBulterys
MStewart
JA
et al. Comparison of human herpesvirus 8 and Epstein-Barr virus seropositivity among children in areas endemic and non-endemic for Kaposi's sarcoma
J Med Virol 2004;72126- 131
PubMedGoogle ScholarCrossref 5.Mayama
SCuevas
LESheldon
J
et al. Prevalence and transmission of Kaposi's sarcoma–associated herpesvirus (human herpesvirus 8) in Ugandan children and adolescents
Int J Cancer 1998;77817- 820
PubMedGoogle ScholarCrossref 6.Gessain
AMauclere
Pvan Beveren
M
et al. Human herpesvirus 8 primary infection occurs during childhood in Cameroon, Central Africa
Int J Cancer 1999;81189- 192
PubMedGoogle ScholarCrossref 7.Brayfield
BPPhiri
SKankasa
C
et al. Postnatal human herpesvirus 8 and human immunodeficiency virus type 1 infection in mothers and infants from Zambia
J Infect Dis 2003;187559- 568
PubMedGoogle ScholarCrossref 8.Taylor
JFTempleton
ACVogel
CLZiegler
JLKyalwazi
SK Kaposi's sarcoma in Uganda: a clinico-pathological study
Int J Cancer 1971;8122- 135
PubMedGoogle ScholarCrossref 10.Wabinga
HRParkin
DMWabwire-Mangen
FNambooze
S Trends in cancer incidence in Kyadondo County, Uganda, 1960-1997
Br J Cancer 2000;821585- 1592
PubMedGoogle ScholarCrossref 12.Corey
LBrodie
SHuang
MLKoelle
DMWald
A HHV-8 infection: a model for reactivation and transmission
Rev Med Virol 2002;1247- 63
PubMedGoogle ScholarCrossref 13.Casper
CWald
APauk
JTabet
SRCorey
LCelum
CL Correlates of prevalent and incident Kaposi's sarcoma–associated herpesvirus infection in men who have sex with men
J Infect Dis 2002;185990- 993
PubMedGoogle ScholarCrossref 14.Casper
CRedman
MHuang
ML
et al. HIV infection and human herpesvirus-8 oral shedding among men who have sex with men
J Acquir Immune Defic Syndr 2004;35233- 238
PubMedGoogle ScholarCrossref 15.Plancoulaine
SAbel
Lvan Beveren
M
et al. Human herpesvirus 8 transmission from mother to child and between siblings in an endemic population
Lancet 2000;3561062- 1065
PubMedGoogle ScholarCrossref 16.Stanberry
LRosenthal
S The epidemiology of herpes simplex virus infections in adolescents
Herpes 1999;612- 15
Google Scholar 17.Adler
SP Molecular epidemiology of cytomegalovirus: viral transmission among children attending a day care center, their parents, and caretakers
J Pediatr 1988;112366- 372
PubMedGoogle ScholarCrossref 18.Fleisher
GRPasquariello
PSWarren
WS
et al. Intrafamilial transmission of Epstein-Barr virus infections
J Pediatr 1981;9816- 19
PubMedGoogle ScholarCrossref 19.Wilson
CMHouser
JPartlow
CRudy
BJFutterman
DCFriedman
LB The REACH (Reaching for Excellence in Adolescent Care and Health) project: study design, methods, and population profile
J Adolesc Health 2001;29(3 suppl)8- 18
PubMedGoogle ScholarCrossref 20.Casper
CKrantz
ETaylor
H
et al. Assessment of a combined testing strategy for detection of antibodies to human herpesvirus 8 (HHV-8) in persons with Kaposi's sarcoma, persons with asymptomatic HHV-8 Infection, and persons at low risk for HHV-8 infection
J Clin Microbiol 2002;403822- 3825
PubMedGoogle ScholarCrossref 21. 1993 Revised classification system for HIV infection and expanded surveillance case definition for AIDS among adolescents and adults
MMWR Recomm Rep 1992;41(RR-17)1- 19
PubMedGoogle Scholar 24.Diamond
CThiede
HPerdue
TMacKellar
DValleroy
LACorey
L Seroepidemiology of human herpesvirus 8 among young men who have sex with men
Sex Transm Dis 2001;28176- 183
PubMedGoogle ScholarCrossref 25.Schulz
TF Epidemiology of Kaposi's sarcoma–associated herpesvirus/human herpesvirus 8
Adv Cancer Res 1999;76121- 160
PubMedGoogle Scholar 26.Renwick
NHalaby
TWeverling
GJ
et al. Seroconversion for human herpesvirus 8 during HIV infection is highly predictive of Kaposi's sarcoma
AIDS 1998;122481- 2488
PubMedGoogle ScholarCrossref 27.Kedes
DHGanem
DAmeli
NBacchetti
PGreenblatt
R The prevalence of serum antibody to human herpesvirus 8 (Kaposi sarcoma–associated herpesvirus) among HIV-seropositive and high-risk HIV-seronegative women
JAMA 1997;277478- 481
PubMedGoogle ScholarCrossref 28.Greenblatt
RMJacobson
LPLevine
AM
et al. Human herpesvirus 8 infection and Kaposi's sarcoma among human immunodeficiency virus-infected and -uninfected women
J Infect Dis 2001;1831130- 1134
PubMedGoogle ScholarCrossref 29.de Sanjose
SMarshall
VSola
J
et al. Prevalence of Kaposi's sarcoma–associated herpesvirus infection in sex workers and women from the general population in Spain
Int J Cancer 2002;98155- 158
PubMedGoogle ScholarCrossref 30.Scheer
SPeterson
IPage-Shafer
K
et al. Sexual and drug use behavior among women who have sex with both women and men: results of a population-based survey
Am J Public Health 2002;921110- 1112
PubMedGoogle ScholarCrossref 31.Bauer
GRWelles
SL Beyond assumptions of negligible risk: sexually transmitted diseases and women who have sex with women
Am J Public Health 2001;911282- 1286
PubMedGoogle ScholarCrossref 32.Koh
ASGomez
CAShade
SRowley
E Sexual risk factors among self-identified lesbians, bisexual women, and heterosexual women accessing primary care settings
Sex Transm Dis 2005;32563- 569
PubMedGoogle ScholarCrossref 33.Marrazzo
JMKoutsky
LAStine
KL
et al. Genital human papillomavirus infection in women who have sex with women
J Infect Dis 1998;1781604- 1609
PubMedGoogle ScholarCrossref 34.Kennedy
MMoore
JSchuman
P
et al. Sexual behavior of HIV-infected women reporting recent sexual contact with women
JAMA 1998;28029- 30
PubMedGoogle ScholarCrossref 35.Duus
KMLentchitsky
VWagenaar
TGrose
CWebster-Cyriaque
J Wild-type Kaposi's sarcoma–associated herpesvirus isolated from the oropharynx of immune-competent individuals has tropism for cultured oral epithelial cells
J Virol 2004;784074- 4084
PubMedGoogle ScholarCrossref 36.Lampinen
TMKulasingam
SMin
J
et al. Detection of Kaposi's sarcoma–associated herpesvirus in oral and genital secretions of Zimbabwean women
J Infect Dis 2000;1811785- 1790
PubMedGoogle ScholarCrossref 37.Calabro
MLFiore
JRFavero
A
et al. Detection of human herpesvirus 8 in cervicovaginal secretions and seroprevalence in human immunodeficiency virus type 1–seropositive and –seronegative women
J Infect Dis 1999;1791534- 1537
PubMedGoogle ScholarCrossref 38.Monini
PHoward
MRRimessi
Pde Lellis
LSchulz
TFCassai
E Human herpesvirus DNA in prostate and semen from HIV-negative individuals in Italy [letter]
AIDS 1997;111530- 1532
PubMedGoogle Scholar 39.Taylor
MMChohan
BLavreys
L
et al. Shedding of human herpesvirus 8 in oral and genital secretions from HIV-1-seropositive and -seronegative Kenyan women
J Infect Dis 2004;190484- 488
PubMedGoogle ScholarCrossref 40.Armenian
HKHoover
DRRubb
S
et al. Composite risk score for Kaposi's sarcoma based on a case-control and longitudinal study in the Multicenter AIDS Cohort Study (MACS) population
Am J Epidemiol 1993;138256- 265
PubMedGoogle Scholar 41.Jacobson
LPMunoz
AFox
R
et al. Multicenter AIDS Cohort Study Group, Incidence of Kaposi's sarcoma in a cohort of homosexual men infected with the human immunodeficiency virus type 1
J Acquir Immune Defic Syndr 1990;3(suppl 1)S24- S31
PubMedGoogle Scholar 42.Lavreys
LChohan
BAshley
R
et al. Human herpesvirus 8: seroprevalence and correlates in prostitutes in Mombasa, Kenya
J Infect Dis 2003;187359- 363
PubMedGoogle ScholarCrossref 43.Stoner
BPWhittington
WLHughes
JPAral
SOHolmes
KK Comparative epidemiology of heterosexual gonococcal and chlamydial networks: implications for transmission patterns
Sex Transm Dis 2000;27215- 223
PubMedGoogle ScholarCrossref 44.Crum
NFWallace
MRStephan
K
et al. Correlates of human herpesvirus-8 seropositivity among U.S. military members recently infected with human immunodeficiency virus
Sex Transm Dis 2003;30713- 718
PubMedGoogle ScholarCrossref 45.Doherty
IAPadian
NSMarlow
CAral
SO Determinants and consequences of sexual networks as they affect the spread of sexually transmitted infections
J Infect Dis 2005;191(suppl 1)S42- S54
PubMedGoogle ScholarCrossref 46.Lee
JKJennings
JMEllen
JM Discordant sexual partnering: a study of high-risk adolescents in San Francisco
Sex Transm Dis 2003;30234- 240
PubMedGoogle ScholarCrossref 47.Catania
JABinson
DStone
V Relationship of sexual mixing across age and ethnic groups to herpes simplex virus-2 among unmarried heterosexual adults with multiple sexual partners
Health Psychol 1996;15362- 370
PubMedGoogle ScholarCrossref 48.Eltom
MAJemal
AMbulaiteye
SMDevesa
SSBiggar
RJ Trends in Kaposi's sarcoma and non-Hodgkin's lymphoma incidence in the United States from 1973 through 1998
J Natl Cancer Inst 2002;941204- 1210
PubMedGoogle ScholarCrossref 49.Osmond
DHBuchbinder
SCheng
A
et al. Prevalence of Kaposi sarcoma–associated herpesvirus infection in homosexual men at beginning of and during the HIV epidemic
JAMA 2002;287221- 225
PubMedGoogle ScholarCrossref