Oral Manifestations
 

  

Oral Transmission of HIV: A Review of the Evidence
 
 

Oral Transmission of HIV: A Review of the Evidence
Rothenberg R , Scarlett M, del Rio C, Reznik DA, O’Daniels CM
AIDS 1998, 12:2095-2105
Requests for reprints of the entire article should be forwarded to Richard Rothenberg, Department of Family and Preventive Medicine, Emory University School of Medicine, 69 Butler Street SE, Atlanta, GA 30303, USA

Introduction

Early in the AIDS epidemic, there was substantial concern over so-called "casual," or non-sexual transmission, of HIV, much of it centered on contact with saliva (sharing an eating utensil or toothbrush)[1,2] Several epidemiologic studies and national AIDS case surveillance data demonstrated that the transmission of HIV depended on contact with infected body fluids, primarily blood and semen.[3,4] Studies of household transmission of HIV, involving family members who shared commonplace activities, could not demonstrate passage of the virus.[5][6] As the epidemic unfolded, concerns about casual contact abated and widespread major risk factors— such as needle-sharing, anal sexual contact, and transfusion--became the primary epidemiologic focus.

Another realignment of emphasis may now be taking place. After about 2 decades, the transmission of HIV in industrialized nations shows some signs of amelioration. Recent surveillance data in the United States and Europe demonstrate a declining acceleration in the reporting of new incident cases of AIDS.[7-9] Over the past two years, there has been a substantial decline in AIDS deaths,[7] attributed largely to new therapeutic developments, and continuing reports of declines in risk taking.[10][11] A number of continuing concerns remain, however. Younger homosexual men may still be evidencing sexual behaviors that place them at risk,[12] and the burden of HIV infection in women is growing.[9]

Despite continuing concerns about the major risks, overall moderating of the epidemic pace offers an opportunity to reconsider several epidemiologic features whose importance may be modified by the changing epidemiologic picture. Though casual contact with saliva remains an insignificant factor, oral sexual contact may now be of increasing importance in the transmission of HIV. Oral sex may be less efficient than needle sharing or anal intercourse for the transmission of HIV[13], but its increased use by men who have sex with men (MSM)[14][15], and its prominence in the sexual activity of crack smokers,[16][17] may increase its contribution to HIV transmission. In this review, we assess the epidemiologic and anecdotal evidence for oral HIV transmission, review current laboratory investigations of the oral ecology of HIV, and suggest a classification scheme and an epidemiologic approach for further delineation of the role of oral sexual activity.

Table 1. Epidemiologic studies measuring oral risk for HIV transmission.

Study

Year

Findings

Risk Assessment
Jaffe et al.[76]

1983

 50 cases; 120 controls (MSM);

ROI: 98%(cases) vs.

99-100% (controls)

 No difference in orogenital contact for cases and controls
Marmor et al. [77]

1984

 20 cases, 40 controls (MSM);

ROI (Univariate):

RR=1.5 (p=0.01)

RR=1.9 (p=0.003) with

swollowing semen

ROI (adjusted): NS

 Oral exposure not an independent risk factor
Goedert et al.[78]

1984

 cohort of 66 men (MSM)

adjusted results:

ROI ?2=0.42 (p=0.5)

IOI ?2=2.36 (p=0.1)

 Oral exposure not an independent risk factor
Newell et al.[79]

1985

 31 cases, 29 controls (MSM)

no difference in ROI or IOI

(data not provided)

 Oral exposure not an independent risk factor
Lyman et al.[80]

1986

 cohort of 1035 men

Prevalence of HIV infection:

no partners in past 2y: 3/15 (20%)

OI only in past 2y: 11/56 (19.6%)

 No difference in infection in those with only OI suggests it is not an important mode of transmission.
Moss et al.[81]

1987

 187 MSM HIV+; 135 community controls and 137 clinic controls.

RR for IOI (adj for # of partners):

0.5--cases vs. HIV- comm, NS

0.8--cases vs. HIV- clinic,NS

2.0--HIV+ vs HIV-, comm,NS

1.6--HIV+ vs. HIV-. clinic,NS

RR for ROI (adj for # of partners):

1.5--cases vs. HIV- comm,NS

1.0--cases vs. HIV- clinic,NS

3.2--HIV+ vs HIV-, comm,NS

1.0--HIV+ vs. HIV-. clinic,NS

similar results for RRs by number of partners

 Oral exposure not an independent risk factor
Winkelstein et al.[82]

1987

 171 MSM with or without OI.

OI: adj RR 1.01 (0.47-2.18)

 Oral exposure not an independent risk factor
van Griensven et al.[83]

1987

 741 MSM;

increase in probability of being seropositive (.28-.40) with number of partners (0-20); not significant in regression analysis

Oral exposure not an independent risk factor
Fischl et al.[84]

1987

 26+ and 19- spouses to HTLVIII+s:

ROI (females) 11+, 1-

no multivariate assessment

 Oral exposure may be important in transmission; role of oral sex alone could not be determined
Darrow et al. [85]

1987

 cohort of 492 MSM;

Univariate RR (steady ptnrs)

IOI 2.9 (0.6-13.0)

ROI 2.1 (0.1-33.9)

Univariate RR (nonsteady)

IOI 2.0 (0.3-14.7)

ROI 3.1 (0.5-18.7)

 Oral exposure not an independent risk factor
Kingsley et al.[86]

1987

 2507 MSM cohort; 95 conversions

147 MSM, ROI ³1 partner, no RAI or ROI---0 serconversions

 Oral exposure is not a risk factor.
McCusker et al. [87]

1988

 cohort of 290 men (MSM)

Univariate RRs (³1/month)

ROI 6.33 (0.82-48.88)

IOI 5.92 (0.77-45.81)

Adjusted RRs

ROI 1.07 (0.75-1.53)

IOI 1.19 (0.82-1.73)

 Oral exposure not an independent risk factor
Peterman et al. [88]

1988

 80 spouses of HIV+s;

Frequency of ROI and IOI greater in (-) spouses

 Oral exposure not an independent risk factor
Osmond et al. [89]

1988

 117 MSM contacts to AIDS cases

ROI with case: adj RR 0.9 (0.4-2.4)

ROI with partners:

adj RR 2.1 (0.8-5.6)

 Oral exposure not an independent risk factor;

Possible seroconversion by oral contact in 2 instances.
Coates et al.[90]

1988

 cases: 246 MSM seroconverters

ROI: 1.26 (0.44-3.60)

 No association could be made with orogenital contact
 

Burcham et al.[91]

1989

 cases--55 MSM seroconverters; controls--588 nonseroconverter

ROI: unadj RR 0.9 (0.3-2.4)

IOI: unadj RR 1.5 (0.6-3.7)

 Oral exposure not an independent risk factor
Evans et al.[92]

1989

 cases: 272 MSM HIV+

controls: 778 MSM HIV-

data collected on OI, not significant, not reported

 Oral exposure not an independent risk factor
Kuiken et al.[93]

1990

 cases--84 MSM seroconverters; controls--168 MSM HIV-.

ROI: unadj RR 1.12 (0.59-2.12)

IOI: unadj RR 1.50 (0.81-2.78)

 Oral exposure not an independent risk factor
Samuel et al.[21]

1993

 cases--83 MSM seroconverters; controls--249 MSM HIV-.

ROI: unadj RR 5.3 (2.0-19)

IOI: unadj RR 3.6 (1.4-13);

ROI (no RAI): RR 3.0 (1.1-12)

IOI (no RAI): RR 1.7 (0.8-4.1);

ROI: adj RR 3.2 (0.76-14)

IOI: adj RR 1.7 (0.37-7.4)

 Oral exposure not an independent risk factor
Raiteri et al.[94]

1994

 18 discordant lesbian couples practicing high risk behavior observed for 3 months; no seroconversions Nonexistent risk of transmission in this setting
Ostrow et al.[22]

1995

 cases: 76 MSM seroconverters

controls: 389 MSM HIV-

ROI: adj RR 0.95 (0.89-1.01)

 Oral exposure not an independent risk factor , but data at the limits of detection.
Faruque et al.[16]

1996

 2323 persons, inner city, 18-29yo

ROI: unadj POR 2.2 (1.6-3.0)

adj POR 1.5 (1.0-2.1)

oral sores and ROI:

adj POR 1.9 (1.0-3.6)

 Oral exposure associated independently with HIV, especially among those with oral sores
Wallace et al.[24]

1996

 3073 prostitutes.

ROI: most prevalent act-35.4%+

not most prevalent-24.2%+

(p< 0.0001) (unadjusted)

 Oral exposure associated with HIV+ , especially with crack use
Page-Shafer et al.[23]

1997

 345 MSM HIV+; 345 MSM HIV-

in MSM with no or little RAI:

ROI (per partner):

adj RR 1.05 (1.00-1.11)

ROI (³ 10 partners; vs. all):

adj RR 1.93 (1.18-3.14)

ROI (³ 10 partners; vs. no RAI)

adj RR 5.06 (1.66-15.4)

Oral exposure significantly associated with HIV seroconversion.

A number of major epidemiologic studies of AIDS transmission did not report information about oral transmission, nor provide even nonsignificant odds ratios.[95-100]

Table 2. Case Reports and Observations on oral transmission

Source

Year

Finding
Sabatini et al.[101] 1984 Possible transmission by female to female sexual contact.
Marmor et al.[102] 1986 2 female patients, one of whom appeared to transmit HIV to the other through orogenital contact
Mayer and Degruttola[103] 1987 1 of 8 seroconversions among 290 seronegative men attributable to oral contact (no anal sex since 1982; 3 negative tests before conversion)
Monzon and Capellan[104] 1987 1 woman with exclusive female-to-female orogenital contact and no other risk factors
Rozenbaum et al.[105] 1988 5 men seroconverted with oral sex as the only risk factor for 3 months or more before seroconversion
Goldberg et al.[106] 1988 1 man with exclusive orogenital sexual contact; exposure to HIV+ male 2 years prior to documentation of seroconversion
Perry et al.[107] 1989 Male partial transsexual who became infected in a monogamous relationship with an HIV+ women having only orogenital contact.
Detels et al.[108] 1989 1 possible seroconversion related to orogenital contact among 232 (8%) converters out of 2915 men followed for 9,.330 person-intervals
Spitzer and Weiner[109] 1989 1 man (with subcortical dementia at age 60) with history of oral sex with one extramarital female partner (a prostitute)
Quarto et al.[110] 1990 1 man (age 25) with steady female partner and one other insertive orogenital contact with a female one month prior to probable acute AIDS syndrome.
Lifson et al.[111] 1990 2 men who seroconverted after receptive oral sex with ejaculation
Murray et al.[112] 1991 1 man acquired both gonorrhea and HIV from receptive oral sex
Lane et al.[113] 1991 1 man acquired HIV after deep kissing, receptive oral sex without ejaculation, and receptive anal intercourse with a condom
Keet et al.[114] 1992 9 men among 102 seroconverters (out of 757 followed) had only orogenital exposure confirmed by reinterview.
Rich et al.[115] 1993 1 women with orogential contact to an HIV+ positive women and no other risk factors.
Vidmar et al.[116] 1996 1 older man exposed to bite from terminal AIDS patient whom he was assisting during a grand mal seizure.
Schacker et al.[117] 1996 4 patients (out of 46 seroconverted) reported only unprotected orogenital contact prior to critical exposure leading to HIV infection; confirmed by partners of 2 out of the 4
Berry and Shea[118] 1997 1 man with receptive orogenital contact with 20 partners, 2 of whom were known to the patient to be HIV positive
Padian and Glass[119] 1997 Discordant couple; female partner became infected in association with oral exposure with good epidemiologic and virologic data for the likelihood of contact with contaminated salivary secretions as the route of transmission.
Bratt et al.[120] 1997 2 patients; one pair had concordant histories and an HIV strain genetically similar to that of the infected partner was passed via orogenital contact to the uninfected partner; in the second case, transmission may have been facilitated by penile skin damage
Senterfitt et al.[121] 1998 4 persons; among 30 newly infected persons, these four had a risk context that suggested transmission from receptive oral sex

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