How safe is Kissing?

Many newspapers have reported on this story without including many of the important facts described in the report below. This report contains no "new" information about the risk of transmission through kissing. It merely reports on a case that might be an example of this type of transmission. HIV is not transmissible through saliva, but bleeding gums and discharge from periodontal disease do contain sufficient white blood cells to transmit HIV. Note also that this a case of repeated exposures over many years with the same HIV infected partner resulting in an accumulated level of risk.

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MORBIDITY AND MORTALITY WEEKLY REPORT
Centers for Disease Control and Prevention
July 11, 1997 Vol. 46, No. 27

Transmission of HIV Possibly Associated with Exposure of Mucous Membrane to Contaminated Blood

In February 1996, transmission of human immunodeficiency virus
(HIV) by an unknown route involving an HIV-infected man and his
previously uninfected female sex partner was reported to CDC.
This report summarizes the epidemiologic investigation of this
transmission, which suggests that the woman was infected through
mucous membrane exposure to contaminated blood.*

In 1992, after obtaining informed consent from the HIV-infected
man and his uninfected female sex partner, they were enrolled in
a study in which couples with one HIV-infected partner and one
non-HIV-infected partner were extensively counseled, administered
questionnaires, and tested periodically for HIV infection. Blood
drawn from the woman on July 19, 1994, was HIV-negative by both
enzyme immunoassay (EIA) and polymerase chain reaction (PCR).
However, serum specimens obtained from the woman on July 24,
1995, and September 11, 1995, were positive by both EIA and
immunofluorescent assay. During the interval from the month
before her last HIV-negative test (June 1994) to the month of her
first HIV-positive test (July 1995), the woman denied known risk
exposures for HIV (i.e., other sex partners; noninjecting- or
injecting-drug use; sexually transmitted diseases; blood
transfusion; artificial insemination; occupational exposure to
HIV; or acupuncture, tattoos, body piercing, or other
percutaneous injections).

The sources of information obtained separately from each partner
by two independent interviewers during this investigation and by
interview records obtained during the study before the couple was
aware of the HIV transmission were consistent about the couple's
sex practices during June 1994-July 1995. During this period, the
woman and her partner reported having vaginal intercourse an
average of six times per month but never during menses. The
couple reported always using latex condoms (for men) during sex,
most times with the spermicide nonoxynol-9. The couple denied
having had anal sex during this period. Although the couple
reported a condom breakage that occurred in January 1994, both
independently denied awareness of condom breakage or slippage
during June 1994-July 1995 and believed that the condom remained
in place each time while the penis was withdrawn. The couple
engaged in "deep kissing" (open-mouth to open-mouth) several
times per month. The man indicated that his gums frequently bled
after he brushed and flossed his teeth and that the couple
generally engaged in sexual intercourse and "deep kissing" at
night after he brushed his teeth. Occasional instances of oral
sex between the couple reportedly did not involve the exchange of
semen or blood. In addition, the woman recalled using the man's
toothbrush and razor, both without visible blood, on one occasion
each, but she was unable to specify whether these events occurred
during the putativ einfection period of June 1994-July 1995.

The man had been HIV-infected since 1988 as the result of
injecting-drug use, and he reported longstanding poor dentition
and occasional sores in his mouth. On August 29, 1994, the man
had a normal platelet count and a CD4+ T-lymphocyte count of 110
cells/uL. On September 6, 1994, he sought medical care at a
clinic because of a cough, stress, and intermittent weight loss;
small vesicles were noted in his throat. At a follow-up visit in
April 1995, canker sores, halitosis, and gingivitis were noted.
In May 1995, at his first dental visit since 1988, gingivitis and
oral hairy leukoplakia were diagnosed. The man had never received
antiretroviral medications or prophylaxis against Pneumocystis
carinii pneumonia although they had been recommended to him.

Because of a 4-month history of increasing dental sensitivity to
hot and cold, on August 8, 1994, the woman underwent a dental
evaluation followed by endodontic therapy (a "root canal"). Her
dental records noted poor condition of gums, 2-mm to 6-mm pockets
(indicating periodontitis), poor personal dental hygiene
practices, and a recommendation for periodontal therapy. No
complications or excessive bleeding from the endodontic therapy
were reported by the woman or noted by the dentist. The dentist
had been tested for HIV in May 1996 and was negative by EIA.


On August 26, 1994, the woman had onset of a syndrome of 7-10
days' duration characterized by fever of 102 F (39 C), headache,
swollen lymph nodes, sore neck and back, and muscle aches in her
legs. On September 2, she sought medical care from her primary-
are physician, who noted erythema and inflammation of the
gingiva. The physician diagnosed a viral process with concomitant
gum infection and prescribed erythromycin for treatment. The
woman reported no other clinically important illness from June
1994 to July 1995.

Blood samples were obtained from both HIV-infected partners in
April 1996. A nested PCR was used to amplify proviral HIV DNA
sequences from peripheral blood mononuclear cells (PBMCs), and
viral RNA sequences from serum were amplified using a nested
reverse transcriptase PCR. Analysis of a 345-nucleotide segment
of the C2V3 region of the env gene revealed a 4% nucleotide
difference between the man and woman's PBMC proviral sequences
and a 9% difference between the viral strains in the man and
woman's serum. Sequence analysis of the complete p17 region of
the gag gene from the PBMC proviral DNA from each partner
indicated only a 1.6% nucleotide difference between the proviral
sequences of the man and woman. Phylogenetic analysis of the C2V3
sequences grouped all HIV strains from the couple's PBMCs and
serum as a monophyletic clade distinct from sequences from other
HIV-infected persons in the United States, with a bootstrap
support of 87% (1). These laboratory results indicate a high
degree of relatedness between the viruses infecting the man and
woman, supporting the conclusion that HIV was transmitted from
one to the other. Testing of stored PBMCs obtained from each
partner in 1995 produced similar results.

Reported by:

N Padian, PhD, S Glass, Univ of California at San Francisco. HIV
Laboratory Investigations Br, Div of AIDS, STD, and TB Laboratory
Research, National Center for Infectious Diseases; Epidemiology
Br, Div of HIV/AIDS Prevention, National Center for HIV, STD, and
TB Prevention, CDC.




Editorial Note:

The findings in this report suggest that the woman probably
became infected with HIV during June 1994-July 1995, possibly
during the weeks before the onset of her symptoms on August 26,
1994; these symptoms were consistent with acute retroviral
syndrome (2). In addition, during June 1994-July 1995, the man's
CD4+ T-lymphocyte count was low, which may be associated with
increased infectivity and risk for transmission (3). Results of
the DNA sequencing and phylogenetic analysis support the
epidemiologic findings that the woman's infection was acquired
from her infected male partner.

Although the exact route of transmission in this report cannot
be determined, the most likely possibility is that the woman
became infected through mucous membrane exposure to the man's
saliva that was contaminated by blood from his bleeding gums or
exudate from undetected oral lesions. Such exposure may have
occurred during "deep kissing"; the woman's inflamed gingival
mucosa, as indicated by her dental and medical records, might
have been a contributing factor. Exposure to saliva
uncontaminated with blood is considered to be a rare mode of HIV
transmission for at least five reasons: 1) saliva inhibits HIV-1
infectivity (4 ); 2) HIV is infrequently isolated from saliva
(5); 3) none of the approximately 500,000 cases of AIDS reported
to CDC have been attributed to exposure to saliva; 4) levels of
HIV are low in the saliva of HIV-infected persons, even in the
presence of periodontal disease (6); and 5) transmission of HIV
in association with kissing has not been documented in studies of
nonsexual household contacts of HIV-infected persons (7).
However, rare bite-related instances of HIV transmission from
exposure to saliva contaminated with HIV-infected blood have been
reported (8,9).

Other exposures of the woman to the man's blood or semen cannot
be excluded. Although occasional instances of oral sex did not
reportedly involve the exchange of semen or blood between the
persons in this report, these routes of transmission cannot
definitively be excluded. Sexual exposure through vaginal
intercourse is a plausible mechanism of transmission for the case
described in this report; however, other studies of couples in
which one partner is HIV-infected and the other is not indicate
that HIV transmission is rare when heterosexual couples use
condoms consistently during vaginal intercourse (10). If a condom
is not used correctly, it may slip off or break, thereby reducing
its effectiveness as a barrier to HIV. However, for this case,
both partners could not recall any instances of condom slippage
or breakage during the time infection was likely to have
occurred. In addition, although the shared use of a toothbrush or
razor are theoretically plausible routes of transmission, the
woman recalled that each event occurred only once, and she could
not specify whether either event occurred during the period when
transmission most likely occurred.

The findings of this investigation underscore the multiple routes
by which exposure to infectious body fluids can occur among
sexually intimate persons. Uninfected persons considering
intimate relationships with persons known to be infected with HIV
should be educated about the rare possibility of HIV transmission
through mucous membrane exposures. Persons choosing to have sex
with HIV-infected persons or persons with unknown HIV serostatus
should correctly use latex condoms (for men) during each act of
intercourse and should avoid any other exposure to potentially
infectious body fluids, including blood, semen, or any other body
fluid visibly contaminated with blood.


References

1. Robbins KE, Bandea CI, Levin A, et al. Genetic variability of
human immunodeficiency virus type 1 in rural northwest Tanzania.
AIDS Res Human Retroviruses 1996;12:1389-91.

2. Schacker T, Collier AC, Hughes J, Shea T, Corey L. Clinical
and epidemiologic features of primary HIV infection. Ann Intern
Med 1996;125:257-64.

3. Laga M, Taelman H, Van der Stuyft P, Bonneux L, Vercauteren G,
Piot P. Advanced immuno-deficiency as a risk factor for
heterosexual transmission of HIV. AIDS 1989;3:361-6.

4. Yeh CK, Handelman B, Fox PC, Baum BJ. Further studies of
salivary inhibition of HIV-1 infectivity. J Acquir Immune Defic
Syndr 1992;5:898-903.

5. Ho DD, Byington RE, Schooley RT, Flynn T, Rota TR, Hirsch MS.
Infrequency of isolation of HTLV-III virus from saliva in AIDS. N
Engl J Med 1985;313:1606.

6. Yeung SC, Kazazi F, Randle CG, et al. Patients infected with
human immunodeficiency virus type 1 have low levels of virus in
saliva even in the presence of periodontal disease. J Infect Dis
1993;167:803-9.

7. Rogers MF, White CR, Sanders R, et al. Lack of transmission of
human immunodeficiency virus from infected children to their
household contacts. Pediatrics 1990;85:210-4.

8. Vidmar L, Poljak M, Tomazic J, Seme K, Klavs I. Transmission
of HIV-1 by human bite. Lancet 1996;347:1762-3.

9. Anonymous. Notes and news: transmission of HIV by human bite.
Lancet 1987;2:522.

10. Saracco A, Musicco M, Nicolosi A, et al. Man-to-woman sexual
transmission of HIV: longitudinal study of 343 steady partners of
infected men. J Acquir Immune Defic Syndr 1993; 6:497-502.

* Single copies of this report will be available until July 11,
1998, from the CDC National AIDS Clearinghouse, P.O. Box 6003,
Rockville, MD 20849-6003; telephone (800) 458-5231 or (301)
217-0023.

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