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Oral Sex and HIV Transmission

David A Reznik, D.D.S. Chief, Dental Service Grady Health System Atlanta, GA

Case Reports and Observations on Oral Transmission

Sabatini et al. 1984 Possible transmission by female to female sexual contact. Marmor et al. 1986 2 female patients, one of whom appeared to transmit HIV to the other through orogenital contact. Mayer and Degruttola 1987 1 of 8 seroconversions among 290 seronegative men attributable to oral contact (no anal sex since 1982; 3 negative tests before conversion) Perry et al. 1989 Male partial transsexual who became infected in a monogamous relationship with an HIV+ women having only orogenital contact. Murray et al. 1991 1 man acquired both gonorrhea and HIV from receptive oral sex. Lane et al. 1991 1 man acquired HIV after deep kissing, receptive oral sex without ejaculation, and receptive anal intercourse with a condom.

Case Reports and Observations on Oral Transmission

Keet et al. 1992 9 men among 102 seroconverters (out of 757 followed) had only orogenital exposure confirmed by reinterview. Vidmar et al. 1996 1 older man exposed to bite from terminal AIDS patient whom he was assisting during a grand mal seizure. Berry and Shea 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 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.

Oral Transmission of HIV: A Review of the Evidence

Rothenberg R , Scarlett M, del Rio C, Reznik DA, ODaniels CM AIDS 1998, 12:2095-2105

Epidemiologic studies measuring oral risk for HIV transmission.


Jaffe et al. 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. 1984 20 cases, 40 controls (MSM); ROI RR=1.5 (p=0.01) RR=1.9 (p=0.003) with swallowing semen. Oral exposure not an independent risk factor Goedert et al. 1984 cohort of 66 men (MSM) adjusted results: Oral exposure not an independent risk factor Newell et al. 1985 31 cases, 29 controls (MSM) no difference in ROI or IOI; Oral exposure not an independent risk factor Moss et al. 1987 187 MSM HIV+; 135 community controls and 137 clinic controls. Oral exposure not an independent risk factor Kingsley et al. 1987 2507 MSM cohort; 95 conversions. Oral exposure is not a risk factor McCusker et al. 1988 cohort of 290 men (MSM). Oral exposure not an independent risk factor

Epidemiologic studies measuring oral risk for HIV transmission.


Osmond et al. 1988 117 MSM contacts to AIDS cases. Oral exposure not an independent risk factor; Possible seroconversion by oral contact in 2 instances. Coates et al. 1988 cases: 246 MSM seroconverters ROI: 1.26 (0.44-3.60) No association could be made with orogenital contact. Raiteri et al. 1994 18 discordant lesbian couples practicing high risk behavior observed for 3 months; no seroconversions. Nonexistent risk of transmission in this setting. Faruque et al. 1996 2323 persons, inner city, 18-29yo Oral exposure associated independently with HIV, especially among those with oral sores. Wallace et al. 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. 1997 345 MSM HIV+; 345 MSM HIV- in MSM with no or little RAI: Oral exposure significantly associated with HIV seroconversion.

Oral Transmission of HIV: A Review of the Evidence

Rothenberg R , Scarlett M, del Rio C, Reznik DA, ODaniels CM AIDS 1998, 12:2095-2105

Questions:

What has the evidence revealed since 1998?

Is receptive oral intercourse considered safe or safer sex? Is transmission of HIV possible through oral intercourse? If so, why are there few cases? What is the theoretical and documented risk of HIV transmission during oral sex? What is the frequency of condom use during oral intercourse?

Is receptive oral intercourse considered safe sex?

Oral intercourse, particularly unprotected receptive fellatio with ejaculation, should be considered as a potential risk behavior for HIV transmission.* Oral intercourse is considered less risky for the insertive partner than the receptive partner.*

*Scully C, Porter S. HIV Topic update: oro-genital transmission of HIV. Oral Dis. 2000 Mar;6(2):92-8

Is receptive oral intercourse considered safe sex?

The likelihood of becoming infected with HIV from performing oral sex on male partners is quite low, though not impossible. Within published medical literature, there have been approximately 38 cases in which individuals report that they became infected with HIV through oral sex. This is a very low number, especially when you consider the number of individuals who have attributed their HIV infection to other riskbehaviors. However, the number is not zero.

Is transmission of HIV possible through oral intercourse?

The actual risk of HIV transmission through oral intercourse is difficult to assess since research subjects may underreport sexual activities that are of higher risk.

Potential Co-Factors for HIV Transmission During Oral Intercourse


Saliva that does not contain blood presents no potential for transmission. In general, the mouth and throat are well defended against HIV: the oral mucosal lining contains few of the cells that are the most susceptible to HIV.* Other research notes that saliva contains several HIV inhibitors, such as peroxidases and thrombospondin-1, and that the hypotonicity of saliva disrupts the transmission of infected leukocytes (white blood cells).**

*Reucroft S, Swain J. Saliva thwarts HIV. New Scientist 1998;157(2117):23. **Baron S. Oral transmission of HIV, a rarity: emerging hypotheses. J Dent Res 2001;80(7):1602-4.

Potential Co-Factors for HIV Transmission During Oral Intercourse

Case reports identify factors potentially associated with increased risk of HIV transmission through oral sex:

oral trauma sores inflammation secondary to poor oral health concomitant sexually transmitted infections ejaculation in the mouth systemic immune suppression.*

*Robinson EK, Evans BG. Oral sex and HIV transmission. AIDS 1999; 13(6):737-8

Potential Co-Factors for HIV Transmission During Oral Intercourse

In a 1996 cross-sectional study of crack cocaine smokers, oral lesions were associated with HIV infection among persons who reported receptive oral sex. Of the eight MSM in the Options Project in San Francisco in 2000 who may have acquired their HIV infection through receptive oral intercourse, three reported oral problems, including occasional bleeding gums.**

**Dillon B, Hecht FM, Swanson M et al. Primary HIV infections associated with oral transmission. 7th Conference on Retroviruses and Opportunistic Infections, San Francisco, January 30th-February 2nd, 2000 (abstract 473).

Meth Mouth

The key ingredients in meth-- lithium, muriatic and sulfuric acids, lye-they are all corrosive. Xerostomia Bruxism Poor diet

Oral Defense

Oral tissues are naturally resistant to HIV infection, unlike anorectal and genital tissues. Mechanisms involved are not completely understood. The innate immune response is a key defense against HIV-1 particularly at mucosal surfaces. Mucosal epithelium provides a physical barrier to infection and also produces anti-HIV-1 peptides and proteins that serves as key effector molecules.

Jana NK, Gray LR, Shugars DC HIV-1 Stimulates the Expression and Production of Secretory Leukocyte Protease Inhibitor (SLPI) in Oral Epithelial Cells: a Role for SLPI in Innate Mucosal Immunity. J Virology; 2005:6432-6440

Oral Defense

Oral antimicrobial factors having anti-HIV activity include secretory leukocyte protease inhibitor (SLPI), human beta defensins (hBDs), salivary agglutinin, thrombospondin 1, and mucins. SLPI participates in mucosal defense by reducing inflammation, blocking the growth of selected bacteria, fungi, and non-HIV-1 viruses, HIV-1 and enhancing wound healing.

Jana NK, Gray LR, Shugars DC HIV-1 Stimulates the Expression and Production of Secretory Leukocyte Protease Inhibitor (SLPI) in Oral Epithelial Cells: a Role for SLPI in Innate Mucosal Immunity. J Virology; 2005:6432-6440

Secretory Leukocyte Protease Inhibitor (SLPI)

Brief exposure of cells to HIV-1 leads to a significant increase in SLPI mRNA and protein secretion, which occurs rapidly after contact with the virus. The time frame, as little as 5 minutes, has biological relevance in that it mirrors the brief duration that oral epithelial cells are likely to be exposed to virus in vivo during receptive oral sex.

Secretory Leukocyte Protease Inhibitor (SLPI)

Given the anti-inflammatory and antiviral properties of SLPI, the induction of SLPI in virus-stimulated cells represents a tug-of-war between the virus and the host immune response, as the virus attempts to stimulate the local inflammatory response while the inhibitor tries to dampen the response and/or protect neighboring cells against infection. An imbalance between the opposing responses may dictate whether virus exposure ultimately results in productive infection or protection.

Jana NK, Gray LR, Shugars DC HIV-1 Stimulates the Expression and Production of Secretory Leukocyte Protease Inhibitor (SLPI) in Oral Epithelial Cells: a Role for SLPI in Innate Mucosal Immunity. J Virology; 2005:6432-6440

Theoretical and Documented Risk of HIV Transmission

Theoretical and Documented Risk of HIV Transmission During Oral-Penile Contact

Theoretical

In fellatio, there is a theoretical risk of transmission for the receptive partner because infected pre-ejaculate fluid or semen can get into the mouth. For the insertive partner, there is a theoretical risk of infection because infected blood from a partner's bleeding gums or an open sore could come in contact with a scratch, cut, or sore on the penis.

Theoretical and Documented Risk of HIV Transmission During Oral-Penile Contact

Documented Risk

Although the risk is many times smaller than anal or vaginal sex, HIV has been transmitted to receptive partners through fellatio, even in cases when insertive partners didn't ejaculate.

Centers For Disease Control Factsheet, "Preventing the Sexual Transmission of HIV, the Virus that Causes AIDS: What You Should Know about Oral Sex" (December 2000)

Theoretical and Documented Risk of HIV Transmission During Oral-Vaginal Contact

Theoretical Risk

Cunnilingus carries a theoretical risk of HIV transmission for the insertive partner because infected vaginal fluids and blood can get into the mouth. (This includes, but is not limited to, menstrual blood.) Likewise, there is a theoretical risk of HIV transmission during cunnilingus for the receptive partner if infected blood from oral sores or bleeding gums comes into contact with vulvar or vaginal cuts or sores.

Theoretical and Documented Risk of HIV Transmission During Oral-Vaginal Contact

Documented Risk

The risk of HIV transmission during cunnilingus is extremely low compared to vaginal and anal sex. However, there have been a few cases of HIV transmission most likely resulting from oral-vaginal sex.
Centers For Disease Control Factsheet, "Preventing the Sexual Transmission of HIV, the Virus that Causes AIDS: What You Should Know about Oral Sex" (December 2000)

Theoretical and Documented Risk of HIV Transmission During Oral-Anal Contact

Theoretical Risk

Anilingus carries a theoretical risk of transmission for the insertive partner if there is exposure to infected blood, either through bloody fecal matter (bodily waste) or cuts/sores in the anal area. Anilingus carries a theoretical risk to the receptive partner if infected blood in saliva comes in contact with anal/rectal lining.

Theoretical and Documented Risk of HIV Transmission During Oral-Anal Contact

Documented Risk

There has been one published case of HIV transmission associated with oral-anal sexual contact.

Other STDs Can Also Be Transmitted Through Oral Sex

Researchers have documented a number of other sexually transmitted diseases that have also been transmitted through oral sex.

Herpes, syphilis, gonorrhea, genital warts (HPV), intestinal parasites (amebiasis), and hepatitis A are examples of STDs which can be transmitted during oral sex with an infected partner.

Risk of transmission

The risk of HIV transmission through unprotected anal and vaginal intercourse is well known. Estimates of the probability of per-sexact (receptive penile-anal intercourse with ejaculation) HIV transmission among homosexual men in the USA range from 0.005 to 0.03 during the asymptomatic phase of infection* to as high as 0.1-0.3 during primary HIV infection.**

* DeGruttola V, Seage GR III, Mayer KH, Horsburgh CR. Infectiousness of HIV between male homosexual partners. J Clin Epidemiol 1989;42(9):849-56. ** Jacquez JA, Koopman JS, Simon CP, Longini IM Jr . Role of the primary infection in epidemics of HIV infection in gay cohorts. J Acquir Immune Defic Syndr 1994;7(11):1169-84.

Oral Sex between MSM Epidemiological Overview

Several epidemiological studies have examined the risk of HIV infection through unprotected receptive oral intercourse (receptive fellatio):

In a 1996-1999 study of MSM with a recent diagnosis of HIV infection, it was found that 7.8% of subjects (eight of 102) were probably infected through receptive oral sex.

Dillon B, Hecht FM, Swanson M et al. Primary HIV infections associated with oral transmission. 7th Conference on Retroviruses and Opportunistic Infections, San Francisco, January 30thFebruary 2nd, 2000 (abstract 473).

Per-contact risk of HIV transmission between MSM

One study calculated the per-sex-act probability of HIV transmission in a cohort of MSM and determined that for unprotected receptive anal intercourse with a HIV+ partner, the probability was 0.82% per act; for unprotected insertive anal intercourse with a HIV+/? partner 0.06%; and for unprotected receptive oral intercourse with ejaculation with a partner of unknown status 0.04% (4/10,000 occurrences).* Of note, the risk of HIV transmission per 1,000 was higher for protected receptive anal intercourse with a person of unknown HIV status (1.8%) when compared to receptive unprotected oral intercourse with ejaculation with a person of unknown status (0.04%)

* Vittinghoff E, Douglas J, Judson F, McKirnan D, MacQueen K, Buchbinder SP. Per-contact risk of human immunodeficiency virus transmission between male sexual partners. Am J Epidemiol 1999, 150:306311.

Del Romero et al., Evaluating the Risk of HIV transmission through Unprotected Orogential Contact. J AIDS 2002

In June 2002, a study conducted amongst 135 sexually active serodiscordant Spanish heterosexuals couples, reported that over 19,000 instances of unprotected oral sex had not led to a single case of HIV transmission.

Del Romero et al., Evaluating the Risk of HIV transmission through Unprotected Orogential Contact. J AIDS 2002

The study also looked at contributing factors that could effect the potential transmission of HIV through oral sex.

They monitored viral load, CD4 count, whether ejaculation in the mouth occurred, and oral health status. Amongst HIV-positive men, 34 per cent had ejaculated into the mouths of their partners. Viral load levels were available for 60 people in the study, 10 per cent of whom had levels over 10,000 copies. Nearly 16 per cent of the HIV-positive people had CD4 counts below 200. The study was conducted over a 10 year period between 1990 and 2000.

Evaluating risk

Various scientific studies have been performed around the world to try and document and study instances of HIV transmission through oral sex. A programme in San Francisco studied 198 people, nearly all gay or bisexual men. The subjects stated that they had only had oral sex for a year, from six months preceding the six-month study to its end. 20% of the study participants, 39 people, reported performing oral sex on partners they knew to be HIV+. 35 of those did not use a condom and 16 reported swallowing ejaculate. No one became HIV positive during the study.

Accessed on 07/26/06 from Avert.org: Oral Sex and the Risk of HIV Transmission

Primary HIV Infection Associated with Oral Transmission - The Options Study

Abstract 473, presented at CROI in early 2000, Primary HIV infections associated with oral transmission, garnered a significant amount of media attention. In May of 2003, the CDC released a fact sheet addressing this topic. Of note, the last review of this fact sheet took place on 07/21/06 The fact sheet can be located at http://www.cdc.gov/hiv/resources/factsheets/or alsexqa.htm

What was the study about?

This study, one component of a primary and recent HIV infection study called the Options Project, is funded by the Centers for Disease Control and Prevention (CDC) at the University of California, San Francisco. The purpose of this particular study was to ascertain the extent of HIV transmitted by oral sex among MSM who were identified with HIV within 12 months of seroconversion.

Findings

The risk of becoming infected with HIV through unprotected oral sex is lower than that of unprotected anal or vaginal sex. However, even a lower risk activity can become an important way people get infected if it is done often enough. The Options Project found that 7.8% (8 of 102) of recently infected men who have sex with men in San Francisco were probably infected through oral sex.

What are the exact ways that HIV was transmitted in this study?

Nearly half (3 of 8) of these cases reported oral problems, including occasional bleeding gums. Almost all (7 of 8) of these men reported to have had oral contact with pre-semen or semen.

Was this a surprise finding?

Yes and No. The percentage of recently infected men enrolled in this study who were probably infected through oral sex (8%) was higher than many researchers had thought likely or found in other studies. More media attention appeared to be placed on this particular study, probably because of the higher number of study participants. There appears to be evidence that higher risk activities (anal sex) among men who have sex with men is decreasing while lower risk activities (oral sex) among these men is increasing. Oral sex has always been considered a lower risk activity but is certainly not risk free.

Accessed from the CDC website on 07/29/06

What can be done to prevent HIV?

The study results emphasize that any type of sexual activity with an infected person is a risk of HIV transmission. Oral sex with someone who is infected with HIV is certainly not risk free. Prevention of HIV is more important than ever. Some persons have indicated that they are less concerned about HIV because of new treatments and are being less careful. This study presents a wake-up call to everyone that HIV is far from over and remains a serious, lifelong disease that is best to prevent. The surest way to avoid transmission of sexually transmitted diseases is to abstain from sexual intercourse, or to be in a long-term mutually monogamous relationship with a partner who has been tested and you know is uninfected. For persons whose sexual behaviors place them at risk for STDs, correct and consistent use of the male latex condom can reduce the risk of STD transmission. However, no protective method is 100 percent effective, and condom use cannot guarantee absolute protection against any STD. http://www.cdc.gov/hiv/resources/factsheets/oralsexqa.htm

The HIV Oral Transmission (HOT) Study

Risk of HIV infection attributable to oral sex among men who have sex with men and in the population of men who have sex with men.

AIDS 2002, Vol 16 No 17

Kimberly Page-Shafer, Caroline H. Shiboski, Dennis H. Osmond, James Dilley, Willi McFarland, Steve C. Shiboski, Jeffrey D. Klausner , Joyce Ballsa, Deborah Greenspan and John S. Greenspan

Page-Shafer et al. 1997 345 MSM HIV+; 345 MSM HIV- in MSM with no or little RAI: Oral exposure significantly associated with HIV seroconversion.

The HOT Study: Populationattributable risk percentage

This study attempted to calculate the populationattributable risk percentage (PAR%) for HIV prevalence associated with fellatio. PAR% refers to the incidence of a disease (in this case, HIV) in a population that can be attributed to a certain risk behavior (in this case, fellatio). The study focused on MSM and found that the PAR% was 0.18% for MSM who had had one partner in the previous six months, 0.25% for two partners, and 0.31% for three partners. Among 239 MSM who exclusively practiced fellatio in the past 6 months, 50% had three partners, 98% unprotected; and 28% had an HIV-positive partner; no HIV was detected.

HOT Study conclusions

These data confirm that the risk of HIV infection attributable to fellatio among MSM and in the MSM population is especially low. It is important that health professionals, including HIV counselors have valid information to impart to their sexually active clients. If individuals believe that the risk of HIV from fellatio is high or on a par with well-documented high-risk exposures such as anogenital sex, they may not feel that sexual behavior choices make a difference. Acquiring HIV through fellatio is significantly less risky than from anal sex, and therefore ones choice of sexual practices do matter.

Questions

Are people using barrier protection when engaging in oral sex?

Reducing the Risk of HIV Transmission Through Oral Sex

The already low risk of becoming infected with HIV from oral sex can be reduced still further by using latex condoms. For cunnilingus or anilingus, plastic food wrap, a condom cut open, or a dental dam can serve as a physical barrier to prevent transmission of HIV and many other STDs.

Centers For Disease Control Factsheet, "Preventing the Sexual Transmission of HIV, the Virus that Causes AIDS: What You Should Know about Oral Sex" (December 2000)

Condom utilization during oral sex

In a study of female street youth involved in prostitution in Montreal, researchers found that condom use was extremely low during oral sex. Only 5% of girls involved in prostitution and 4% of girls not involved in prostitution used condoms while performing fellatio.

Weber AE, Boivin JF, Blais L et al. HIV risk profile and prostitution among female street youths. J Urban Health 2002;79(4):525-35.

Oral Sex and Condom Use Among Young People in the United Kingdom
Perspectives on Sexual and Reproductive Health Vol 38, 1, March 2006

Methods

Results

Between 2003 and 2005, a sample of 1,373 students ages 16 18 completed questionnaires about their knowledge, attitudes and experiences related to sexual health and behavior 56% had experienced fellatio or cunnilingus including 22% that had not yet engaged in penetrative intercourse Among those who had experienced fellatio only once, 17% used a condom Among those who had experienced fellatio more than once only 2% used a condom Reduced pleasure and lack of motivation, desire and forethought were reasons given for not using a condom during fellatio. Hygiene, avoidance of the dilemma of whether to spit or swallow ejaculate, and taste were commonly cited as triggers for use.

Oral Sex and Condom Use Among Young People in the United Kingdom
Perspectives on Sexual and Reproductive Health Vol 38, 1, March 2006

Conclusions

Greater efforts are needed to publicize the risk of exposure to STDs that many young people face because of unprotected noncoital sexual activities before, as well as after, they enter into relationships involving intercourse.

Discussion

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