Transmission of Nonviral Sexually Transmitted Infections and

372
Transmission of Nonviral Sexually Transmitted Infections and
Oral Sex
jsm_2515
372..384
Andrea Ballini, BSc,* Stefania Cantore, DDS, MSc,* Laura Fatone, DDS,*
Valentina Montenegro, DDS,* Danila De Vito, MD,* Francesco Pettini, DDS,* Vito Crincoli, DDS, MSc,*
Annarita Antelmi, MD,† Paolo Romita, MD,† Biagio Rapone, DDS,* Giovanni Miniello, MD,‡
Letizia Perillo, MD, DMD,§ Felice Roberto Grassi, MD, DMD, PhD,*‡ and Caterina Foti, MD†
*Department of Dental Sciences and Surgery University of Bari “Aldo Moro,” Bari, Italy; †Department of Internal
Medicine, Immunology and Infectious Diseases, Dermatology Clinic University of Bari “Aldo Moro,” Bari, Italy;
‡
Department of Gynecology, Obstetrics, and Neonatology, University of Bari “Aldo Moro,” Bari, Italy; §Department of Oral
Sciences, Second University of Naples, Naples, Italy
DOI: 10.1111/j.1743-6109.2011.02515.x
ABSTRACT
Introduction. Oral sex is usually considered a lower-risk sexual activity when compared with sex, but it is frequently
the cause of sexually transmitted infections (STI). In particular, STI transferred through oral sex might have no
visible symptoms, depending on the type of infection.
Aims. The aim of this study is to review the literature about the role of oral sex in the transmission of nonviral STI.
Main Outcome Measures. State-of-the-art information in the area of STI in relation to sexual function and
self–care, this last important for development of STI prevention products such as vaginal microbicides. Sexual
behaviors assessed focusing on receiving oral sex and giving oral sex.
Methods. A search of the main electronic databases including registers of clinical controlled trials was performed in
addition to a hand search of the most relevant Journals. The following electronic databases were searched: PubMed,
Embase, Google Scholar, literature review of research articles, and public health department Internet Web sites, for
the period of 1945–2011. In addition to searching the Clinical Trials Registry at the US National Institutes of Health,
we also used the meta Register of Controlled Trials and the Cochrane Central Register of Controlled Trials.
Results. STI affect the mucous membranes both directly and indirectly producing characteristic diagnostic signs and
lesions. Daily dental clinical activity needs an appropriate knowledge of any kind of oral lesions-related STI. The
reader is offered a practical approach with clinically relevant recommendations that may prove useful in his/her daily
practice when dealing with STI.
Conclusions. These data provide a foundation for understanding diverse STI. We advise physicians to be receptive
to discuss sexuality issues and provide patients with adequate therapy. Ballini A, Cantore S, Fatone L, Montenegro
V, De Vito D, Pettini F, Crincoli V, Antelmi A, Romita P, Rapone B, Miniello G, Perillo L, Grassi FR, and
Foti C. Transmission of nonviral sexually transmitted infections and oral sex. J Sex Med 2012;9:372–384.
Key Words. Oral Sex; Genital Intercourse; Nonviral-sexually Transmissible Infections; Orogenital Sexual Activity;
Sexual Health; Sexual Behavior
Introduction
D
aily dental clinical activity needs an appropriate knowledge of any kind of oral lesions
related to nonviral sexually transmitted infections
(STI).
Oral sex is a common sexual practice between
both heterosexual and homosexual couples of
various age [1]. That orogenital practices are
J Sex Med 2012;9:372–384
in common use is clear from the reports
of Kinsey et al. [1], who stated that nearly
60% of all American men had had such contact, while women seemed somewhat less
interested.
Oral sex refers to sexual activities related to the
stimulation of the genitalia by the use of mouth,
tongue, teeth, or throat and includes both oro-anal
and orogenital practices.
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Nonviral STI and Oral Sex
There are different types of oral sex activities,
such as fellatio, cunnilingus (orogenital sex), and
analingus (oro-anal sex), which are correlated to the
different origin of infection, even if the most
common sexual practice still remains vaginal sex
[2].
Johnson et al. [3] reported that 72.9% of men
and 66.2% of women refer to have experienced
cunnilingus, instead 69.4% of men and 64% of
women declare to have practiced fellatio. Previous
studies, among adolescents, report contrasting
findings regarding the sequence of sexual initiation: a study, among female adolescents, reports
that lots of them practiced orogenital stimulation
before than the traditional vaginal intercourse [4].
On the other hand, data from the 2002 National
Survey of Family Growth among 15- to 19-yearolds indicate vaginal sex as initial type of sexual
intercourse even if these conclusions should be
correlated to racial/ethnic group and socioeconomic status [5].
The majority of patients practice unprotected
orogenital contact: oral sex is often performed
without a condom or any form of barrier protection because people are not scared about
pregnancy.
Even if infrequently investigated, oral sex can
transmit oral, respiratory, genito-urinary, and
enteric pathogens. It is plausible that performing
oral sex may increase the risk of oral disease,
either through the introduction of microbes and
mechanical trauma to the oral cavity [6]. Oral status
is strictly correlated with the transmission of infections: wounds and abrasions in mouth, bleeding
gums, unhealthy periodontal status (gingivitis and
periodontitis), and lip sores increase chances of
acquiring infection by getting the systemic circulation. Otherwise, injuries because of fellatio must be
considered as an etiological factor to hemorrhagic
changes of the oral mucosa: erythema, petechiae,
ecchymoses, dilated blood vessels, vesicles, and
submucosal hemorrhage [7] could be secondary to
intraoral trauma [8]. The responsible mechanism of
these injuries are postulated to be combined muscular actions initiated reflexively through tactile
stimulation, and the negative pressure in the posterior oropharynx created through fellatio, both
acting simultaneously on the mucosa of the soft
palate.
There are various vehicles likely responsible of
infections: saliva, precum, sperm, vaginal secretions, and menstrual blood. The intact mucosal
membrane, the diluent function of saliva, and the
antimicrobial action of salivary enzymes constitute
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a defensive barrier to infection by pathogenic
microbes.
Sexually transmitted diseases affect the mucous
membranes both directly and indirectly producing
characteristic diagnostic signs and lesions. The
aim of this work is to review the scientific literature about the oral transmission of nonviral STI.
Search Strategy
A search of the main electronic databases including registers of clinical controlled trials was performed in addition to a hand search of the most
relevant journals. For the identification of studies,
detailed search strategies were developed for each
database searched. Selected articles were reviewed
for data extraction.
The bibliographies of relevant clinical trials and
relevant articles were checked for identifying
studies outside the hand searched journals. The
following electronic databases were searched:
PubMed, Embase, Google Scholar, literature
review of research articles, and public health
department Internet Web sites, for the period of
1945–2011. In addition to searching the Clinical
Trials Registry at the US National Institutes of
Health, we also used the meta Register of Controlled Trials and the Cochrane Central Register
of Controlled Trials. No language restriction was
placed. The last electronic search was conducted
on 14 March 2011.
Disagreements were resolved by discussion. All
studies meeting the inclusion criteria underwent
validity assessment and data extraction. All studies
rejected at this or subsequent stages, and reasons
for exclusion, were recorded.
Syphilis
Syphilis, like other STI, is a sociologic marker that
reflects the sexual behaviors of individuals belonging to this society. In the past decade, the prevalence of infective syphilis in the developed world
increased significantly [9]. Since 1980s, the evolution of STI has been characterized by the
resurgence, and since 2000 by a significant recrudescence of syphilis, the appearance of resistance
of gonococcus to fluoroquinolones and the emergence of lymphogranuloma venereum [10]. This
phenomenon could be attributable to human
immunodeficiency virus (HIV) immunodepression
and iatrogenic immunosuppression.
Syphilis is an STI caused by an anaerobic filamentous spirochete, the bacterium Treponema palJ Sex Med 2012;9:372–384
374
lidum. Syphilis is transmitted from person to
person through direct contact with a syphilis sore.
This ulcer, commonly called chancre, appears on
the external genitals, vagina, anus, or in the
rectum, on the lips, and in the mouth. This bacterium can be transmitted during vaginal, anal, or
oral sex (analingus, cunnilingus, and fellatio).
Pregnant women with syphilis may also transmit it
transplacentally or during birth to the fetus [11],
leading to malformations of the skin, mucous
membranes, skeletal, eye, liver, kidney, and central
nervous system. The congenital disease gives rise
to Hutchinson’s triad dental abnormalities, deafness, and eye damage, as well as bone, skin, and
neurological anomalies of the face [11].
This venereal disease is a prototypic STI with
oral signs and manifestations. Although oral manifestations of syphilis are frequently observed
during secondary disease, oral lesions may be
present during every stage of the disease.
The mouth is rarely the site of primary syphilis
and, above all, because of its transient nature, the
oral ulceration of primary syphilis often goes
unnoticed by the patient or by any unsuspicious
clinician [12].
Primary syphilis is usually the consequence of
orogenital or oro-anal contact with an infectious
lesion. Kissing may, rarely, cause transmission [13];
indeed, it has been suggested that intrafamilial oral
acquisition of syphilis in a child may have occurred
in this way, although more usually oral syphilis in
a child is indicative of sexual abuse [14].
Primary syphilis is represented by a lesion
(chancre or syphiloma), that is an indolent nodule,
round or oval form, red-brown color, with very
sharp and regular margins, edges slope gently
down to the bottom. It appears at the point of
penetration of the bacterium and solitary ulcer
is often on the lip or tongue: the upper lip is
more commonly affected than the lower in males
while the opposite occurs in females—probably
reflecting the anatomy involved with fellatio and
cunnilingus [15].
Secondary syphilis is characterized by nonspecific oral lesion, pharyngitis, glistening patch, oral
ulcers, lingual fissures, but the most wellrecognized manifestations are the mucous patch,
an irregular, often ulcerated plaque of about 1 cm
diameter, covered by a gray with necrotic membrane surrounded by an erythematous border [16]
and the maculopapular lesions on the hard palate.
The mucous patches may coalesce to give rise to,
or de novo as, serpiginous lesions, sometimes
termed snail track ulcers [17–19]. Papular syphJ Sex Med 2012;9:372–384
Ballini et al.
ilides are rare. They manifest as red round nodules
with a gray center that may ulcerate on the buccal
mucosa or commissures.
After a latent phase, tertiary syphilis manifests
itself with serious systemic diseases, with neurosyphilis, with gummas, that are destructive granulomas and with glossitis or mucosal atrophy,
syphilitic leukoplakia, which may transform into
oral squamous cell carcinoma.
Untreated syphilis can eventually cause brain
damage, heart disease, blindness, and death. Open
syphilis sores or chancres provide also an easy
entry and exit for HIV and increase viral load. In
effect, oral syphilitic lesions disrupt the protective
epithelial barrier and recruit HIV target cells,
increasing the risk for HIV transmission [20].
Gonorrhea
Gonorrhea is an STI caused by bacteria, Neisseria
gonorrhoeae also called Gonococcus. It is a species
of Gram-negative coffee-bean shaped bacteria.
The incubation period is 2–30 days with most
symptoms rising between 4 and 6 days after infection, even if a small number of people could be
asymptomatic.
As a sexually transmitted disease, the genital
tract is its reservoir [21]. Women are more susceptible to infection than men: the transmission probability during a single contact is estimated to be
0.5–0.7 from male to female and 0.2–0.3 vice versa.
Despite it, gonorrhea rates of symptomatic disease
in men are higher than women.
N. gonorrhoeae infections are associated with
infertility, pelvic inflammatory disease, and ectopic
pregnancy in women and epididymitis, prostatitis,
and infertility in men. Furthermore, Chlamydia
and gonorrhea have been associated with increased
risk of transmission and acquisition of HIV infection [22].
The most common symptoms reported by men
are urethral discharge and dysuria, while women
usually complain about cervical or vaginal discharge; therefore, the routine examination for
gonorrhea is designed to the demonstration of the
bacterium in the secretion from the genital organs
directly implicated in sexual intercourse [23].
Anyhow, a considerable portion of N. gonorrhoeae
infections occurs at nongenital anatomic sites
among men who have sex with men (MSM) [24].
It is well established that N. gonorrhoeae can be
transmitted through unprotected vaginal and anal
sex and through oral sex from the male urethra to
the oropharynx [23]. Hence, gonococci may be
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Nonviral STI and Oral Sex
transferred from the genitalia to the mouth by
cunnilingus and/or fellatio.
Osborne and Grubin [25] pointed out fellatio as
the culprit of gonococcal colonization of the
pharynx of patients affected by gonorrhea;
nevertheless, the authors did not exclude cunnilingus, autoinoculation, or even ordinary kissing as
possible modalities of transmission of N. gonorrhoeae. This statement needed further scrutiny [25].
In 1980, the British Co-operative Clinical
Group demonstrated that also cunnilingus predisposed to gonorrhea: it was stated that 14% of men
practicing cunnilingus with presumed affected
women were positive to pharyngeal gonorrhea vs.
3% among men with pharyngeal infection who
denied this practice [26].
Patients with oral gonococcal infection may be
asymptomatic (79%) or show severe oral symptoms such as a painful pharyngitis (15%), purulent
tonsillitis (5%), or lymphadenopathy [27]. The
lesions related to gonorrhea are not pathognomonic and may be confused with several oral
diseases.
The clinical signs and symptoms of pharyngeal
gonorrhea do not suggest the presence of gonococci at this site because the condition is largely
asymptomatic. Any symptom would be indistinguishable from those of common oral infections
[22].
Nowadays, diagnosis of pharynx infection
requires a swab specimen to demonstrate the presence of the gonococcus, even if this pose several
methodical issue [23].
Neisseria Meningitidis
Orogenital sex is implicated as a route of transmission also for Neisseria meningitides, a gram-negative,
aerobic, encapsulated, coffee-bean shaped diplococcus that can parasitize the nasopharynx of
healthy individuals as a harmless saprophyte.
The natural habitat and reservoir for meningococci are the mucosal surfaces of the human
nasopharynx and, to a lesser extent, the urogenital
tract and anal canal [28].
It is well known that this bacterium is frequently present in the pharynx of healthy people
and that during orogenital intercourse it can be
directly inoculated in the genital mucosa. As a
matter of fact, N. meningitidis remains the leading
worldwide cause of meningitis and fatal sepsis
[29].
As confirmed by literature, gonorrhea of the
genitourinary tract is occasionally caused by oro1052
genital sexual practice. Hagman et al. described
the cases [30] of three patients who harbored meningococci in the genitourinary tract with the same
serogroup/serotyope of the pharyngeal meningococci of their sexual partners.
Urra et al. [31] presented a story of urethritis
caused by N. meningitidis, serogroup C. The
microorganism was isolated from the nasopharynx and endocervix of the patient’s sexual partner
and such evidence was confirmed by genotyping
techniques. The similarity of the urethral and
nasopharyngeal isolates’ electrophoretic patterns,
using pulsed-field gel electrophoresis, attested
the transmission via orogenital contact: the identical strain was isolated from the patient’s urethral exudates and from his sexual partner’s
pharyngeal exudates.
Another case report [32] confirms the transmission of N. meningitidis group A by fellatio, in a
young heterosexual couple, which caused an acute
purulent urethritis in the 18-year-old boyfriend;
N. meningitidis was present in the urethra of the
man and in the throat of his girlfriend.
Fiorito et al. [33] described an unusual primary
neonatal conjunctivitis acquired at delivery from
the mother’s endocervical infection. The microorganism was isolated from the cervix, the neonate
conjunctive, and the oropharynx of the mother’s
male partner, showing the same serotype and
genotype.
Quarto et al. [34] described a case of acute urethritis in a heterosexual man caused by N. meningitidis, serogroup Y. The symptoms began 6 days
after a single episode of fellatio with an occasional
female partner.
Kanemitsu et al. presented a similar case of
acute urethritis in a 48-year-old heterosexual man
[35]. The symptoms appeared 1 day after a fellatio
performed by a prostitute; N. meningitidis was isolated in the urethral discharge.
Vaginal Infections
Vulvovaginal Candidiasis
The vulvovaginal candidiasis is a common
inflammatory disease caused by yeast in female
population of childbearing age.
Candida albicans is the etiologic agent responsible for 30% of all vaginitis and 85% of mycotic
vulvovaginitis, probably because of the high capacity of the yeast to adhere to vaginal epithelial cells,
especially at certain times of the menstrual cycle
[36]. Other species include C. glabrata and C.
tropicalis [37].
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Oral contraceptives, sexual activity, antimicrobial use, and many other possible risk factors have
been associated with vulvovaginal candidiasis in
anecdotal reports and occasionally in clinic-based
studies, but none of these associations has been
conclusive [38].
The real incidence of vulvovaginitis is
unknown, but apparently about 75% of women
experience at least one episode of yeast vulvovaginitis during their reproductive years [37]
and 40–50% of them suffer from recurrent episodes [39]. Recurrent vulvovaginal candidosis is
not a chronic infection but a disease with recurrent
episodes (from three to four attacks during the
year) [40] and the cause of recurrences is still
unknown in the majority of the cases.
It is possible that intestinal colonization by
Candida spp. is responsible of the reinoculation of
the yeast in the vagina so the “intestinal reservoir”
might be responsible for a large number of recurrent infections without the classic predisposing
factors [36,41].
The classic symptoms of vaginal candidiasis are
represented by itching, burning, dyspareunia
accompanied by vaginal discharge (leukorrhea)
of different intensity, and cervico–vaginal
erythematosus-ulcerated lesions [36]. The signs
and symptoms of yeast vulvovaginitis are not diriment, so clinicians need laboratory tests to confirm
diagnosis [37].
Vulvovaginal candidiasis is not usually defined
as an STI even if it is suggested that oral contact
with genitalia (cunnilingus) may predispose to the
recurrent form [42]. Moreover, it is reported that
candida is present in up to 50% of the mouth of
healthy patients, likely because of oral–genital
contacts [43].
Despite of this, in 1993, Evans et al. did not find
any evidence that either vaginal candidosis (acute
form) or bacterial vaginosis (BV) was sexually
transmitted [44]. According Mårdh, the oral cavity
has been assumed to be the main reservoir for
recolonization of the genital tract of women with
recurrent episodes of genital candidosis, even if
more researches are required [40,45].
Markos et al. in 1992 analyzed the possible correlation between recurrent vulvovaginal candidiasis and the practice of oral sex (fellatio/
cunnilingus), considering the practice as the
possible vehicle for transmission of C. albicans.
Performing oral sex might contribute to the
recolonization of the vagina from the oral cavity so
predisposing to the recurrent vulvovaginal candidiasis. The use of the sheath and/or abandoning
J Sex Med 2012;9:372–384
Ballini et al.
Figure 1 Adhered streptococci to a buccal epithelial cell.
the practice of oral sex was associated with a
decrease in incidence of recurrences [46].
Rylander et al. in 2004 noticed a significant
association between orogenital sex and candidiasis:
Candida was present in 42% of sexually active
women undergoing a genital examination at an
adolescent health center [39].
As confirmed by literature, there is a correlation
between oral sex and recurrent vaginal candidiasis
but not between oral sex and general (acute) forms
of vaginal candidiasis. Edwards et al. assumed as an
explanation that the antimicrobial substances (i.e.,
lysozyme, NO, thiocyanate, etc.) in saliva might
kill bacteria on genitalia but not Candida spores
letting them to survive and give a recurrence [43].
Furthermore, Rylander et al. proposed that saliva
may promote the growth of candida by moistening
or irritating the vulvar mucosa or modifying the
local immunological state [39].
Candida cytopathy (Figures 1 and 2) is characterized by cytoplasmic tunnels and holes with a
sharply condensed border.
Chlamydia Trachomatis
Chlamydia trachomatis is a Gram-negative obligate
intracellular parasite belonging to the Chlamydiaceae family. It can be transmitted through vaginal
anal or oral intercourse but also from mother to
fetus.
C. trachomatis infections are the most common
bacterial STI found in adolescents. Young women
are more susceptible to STI than older women
because of their not yet completed cervical
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Nonviral STI and Oral Sex
Figure 2 Duplicating adhered short bacilli to a buccal epithelial cell.
anatomic development, sexual behavior, and
health care behavior [47]. STI caused by C. trachomatis bacteria affect women more than men.
Chlamydia is known as a “silent” disease
because the majority of infected people have no
symptoms. If symptoms do occur, they usually
appear within 1–3 weeks after exposure. Common
symptoms include pain and burning sensation
when urinating, smelly vaginal or penile discharge,
spotting after intercourse. Most infections are
asymptomatic and, therefore, untreated. In
extreme cases, cervical chlamydial infections may
cause severe damage to women’s reproductive
system, including pelvic inflammatory diseases and
permanent infertility.
Urogenital infection with C. trachomatis is well
recognized, but there are few data about pharyngeal colonization [48]. As a matter of fact, Chlamydia can be also found in the throats of women and
men who recently performed unprotected active
oral sex with an infected partner [49].
Positive pharyngeal specimens for C. trachomatis have been isolated from patients who had orogenital contact with infected heterosexual females
and from homosexual man with a history of orogenital contact with infected partner. None of
these patients had any symptoms of pharyngitis.
Diagnosis of pharyngeal C. trachomatis infection
requires a posterior pharynx swab or mouthwash
oral–throat rinses [50].
In particular, C. trachomatis has been isolated
from the throat of a patient affected by TRIC
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ocular disease, likely secondary to infection or
contamination of the throat by the nasolacrimal
secretions [51]. TR- stands for trachoma and the
-IC for inclusion conjunctivitis [52].
Six cases of prolonged and recurrent tonsillitis
associated with C. trachomatis have been reported
in the literature. The bacteria have been found in
tonsillar crypts of all the patients, and in the urogenital swabs in five patients, and in three sexual
partners [53]. Pharyngeal infection apparently
resulted from direct inoculation. The available
data suggest that tonsillitis, the most common
problem in otorhinolaryngology, may be caused by
C. trachomatis more often than suspected [54].
However, the isolation of C. trachomatis in the
pharynx is not common, despite of the presence of
a genital infection and a history of active oral sex
[55]. The use of Polymerase Chain Reaction
(PCR), in a population at high risk of sexually
transmitted disease, showed that the prevalence of
C. trachomatis. in the pharynx was very low. This
means that transmission of C. trachomatis to the
oropharynx does not pose a serious health risk.
Hence, the screening of patients for oropharyngeal C. trachomatis is not useful [48].
BV
BV was reported for the first time in 1995 by
Gardner and Dukes, who described its unique
clinical signs, symptoms, and distinctive nature of
the vaginal discharge. BV is currently the most
prevalent cause of infectious vaginitis among
women attending for genitourinary diseases.
BV is characterized by important changes in the
vaginal ecosystem: saprophyte flora is absent or
greatly reduced and replaced with a mixed, predominantly anaerobic flora. Lactobacillus populations, which are usually dominant in healthy
women, are substituted by a polymicrobial group
of organisms that includes Gardnerella vaginalis
and anaerobic Gram-negative rods such as Prevotella, Bacteroides, Fusobacterium, Porphyromonas and
Peptostreptococcus species, Mycoplasma hominis,
Ureaplasma urealyticum, and often Mobiluncus
species [56–59].
BV is the most prevalent form of vaginal disturbances in reproductive age women even if more
than 50% of all women with BV are asymptomatic.
Common clinical symptoms of BV are related with
anaerobic bacteria production of enzymes (aminopeptidases) that degrade protein and decarboxylases that convert amino acids and other
compounds to amines raising the vaginal pH.
Symptomatic women usually complaint malodorJ Sex Med 2012;9:372–384
378
ous (like rotten fish), whitish and foamy vaginal
discharge. BV has been associated with many
gynecological and obstetric complications such as
cervicitis, salpingitis, endometritis, postoperative
infections, urinary tract infections, pelvic inflammatory disease, mild abnormal Pap smear results.
Moreover, BV is likely linked with cervical
intraepithelial neoplasia, preterm delivery, premature rupture of the membranes, chorioamnionitis,
and postpartum endometritis [57,60–62].
Diagnosis of BV is established by Amsel’s criteria: presence of homogeneous discharge; vaginal
fluid pH > 4.5; positive amine test; microscopic
analysis of Gram-stained smear of vaginal discharge where “clue” cells (epithelial vaginal cells
covered with mass of adherent bacteria, mostly
coccobacilli) should be detected [61,63].
BV risk factors are as follows: multiple partners,
exposure to semen, prior trichomoniasis, intrauterine device usage, smoking, indigent population,
and frequent use of scented soap [61].
The role of sexual transmission in BV remains
unclear: some studies show similar risk behavior in
groups with BV and other STI but others refute
this [44,60,64].
Among heterosexual women, noncoital sexual
behaviors, such as receptive oral sex, receptive anal
sex and nonpenetrative digito-genital contact,
have also been identified to confer an increased
risk of BV acquisition [65]. According with Schwebke et al. history of BV, a greater number of partners, and more frequent episodes of receptive oral
sex, are associated with unstable vaginal flora.
Women reporting more frequent episodes of oral
sex had a corresponding increase in the number of
episodes reported in their diary. Strictly similarities exist between the anaerobic bacteria associated
with gingivitis and those associated with BV [66].
In a prospective cohort study (including 256
heterosexual female patients) Nandwani et al.
found a highly significant difference in the rate of
BV among women who reported receptive oral sex
in the previous 4 weeks and women who did not
experience cunnilingus in the past 4 weeks [67].
An attempt to explain the unconfirmed association of BV in lesbians, and between BV and receptive cunnilingus in women, was done by
Tchamouroff. According to him, the evidence
associating BV with oral sex is too strong to be
ignored. In a parallel prospective study of 256 heterosexual female patients attending the same
department, 55 (21%) were diagnosed as having
BV. Forty-one (37%) out of 111 women, who
practiced receptive cunnilingus in the previous 4
J Sex Med 2012;9:372–384
Ballini et al.
weeks, had BV. Fourteen (10%) out of 145 women,
who did not have oral sex, had BV. Six (67%) out of
nine lesbians, who practiced receptive cunnilingus
in the previous 4 weeks, had BV. In both heterosexual and homosexual female groups there was a
strong association between BV and receptive cunnilingus (P < 0.001). A possible explanation could
be that the mouth is full of Gram-positive and
Gram-negative organisms including Bacteroides
oralis and, although in much smaller quantities,
lactobacilli [60,68].
Even if lactobacilli are part of normal oral flora,
it is not clear if they are saprophyte into the vagina.
Lactobacillus phages may be directly inoculated into
the vagina from the male (or female) partner.
Blackwell hypothesized that a sexually transmitted
lactobacillus phage may specifically destroy the
endogenous healthy lactobacillus vaginal flora.
Moreover, the overgrowth of endogenous anaerobic bacteria and G. vaginalis may explain why
anaerobic vaginosis behaves epidemiologically as a
sexually transmitted agent [59].
Mechanical transfer of infectious agents in
lesbian couples is most likely to occur via cunnilingus, a common practice among lesbians [69].
According to Berger, lesbians in monogamous
relationships usually have concordant vaginal
secretions that probably reflect the sexual transmission of BV between them [69,70].
Microscopy of the wet mount should be considered the most powerful diagnostic tool for the
presence of clue cells (Figure 3), epithelial cells
covered by tiny bacteria (pleomorphic bacteria).
Pregnancy and Oral Sex
Pregnancy appears to be usually accompanied by a
decrease in sexual desire, coital frequency, and
orgasm. Sexual behavior in pregnancy has been
traditionally restricted and is currently poorly
defined. Abortion is only rarely caused by coitus,
even if a clear relationship between coitus and
orgasm to prematurity, distress of the fetus, and
newborn has not been established. Air embolism in
pregnancy associated with cunnilingus and vaginal
insufflations have been reported as an infrequent
cause of deaths of the mother and the fetus within
minutes because air passes beneath the fetal membranes and into the circulation of the subplacental
sinuses [71,72].
The BV complex of microbes, compared with a
normal vaginal microflora dominated by facultative lactobacilli, is associated with significantly
increased risks for preterm labor, preterm prema1055
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Nonviral STI and Oral Sex
Figure 3 Short bacilli, adhered to a buccal epithelial cell by
their extremity.
ture rupture of membranes, and other perinatal
infectious complications. Pathogenic mechanisms
include an ascending route of infection and/or
inflammatory process because of microbial products and maternal and/or fetal response(s) with
production of prostaglandins and cytokines [73].
As above mentioned, oral sex may play a role in
the pathogenesis of BV: cunnilingus practiced
during the pregnancy could be the responsible of
the transmission of BV pathogens, increasing the
risk of preterm birth.
In the presence of periodontal disease, oral
opportunistic pathogens and/or their inflammatory products also may play a role in prematurity
via a hematogenous route [74].
Fusobacterium nucleatum and Capnocytophaga
species are common oral pathogens and infrequent
causes of systemic infection in patients with compromised immunity or disrupted mucosal integrity. The isolation of both organisms from a
clinical specimen suggests an oral source of infection [75].
F. nucleatum is a common oral species that can
be found both in healthy and diseased subgingival
sites and is the most frequently isolated species
from amniotic fluid cultures among women with
preterm labor and intact membranes. Furthermore, the species and subspecies of fusobacteria
identified from amniotic fluid are F. nucleatum subspecies vincentii and F. nucleatum subspecies
nucleatum. These fusobacteria could be acquired
1056
both by oral-hematogenous route and cunnilingus
from a partner [73].
A case report described the occurrence of
chorioamnionitis, fever, fetal tachycardia, and
uterine tenderness in a 23-year-old woman at the
24th week of gestation in preterm labor. After bacteriological studies an placental cultures, F. nucleatum and Capnocytophaga species were found.
Reviewing the patient’s history, it was established a
temporal relation between orogenital contact and
the onset of amniotic infection. At the intraoral
examination, the patient did not show any odontogenic focus, but the positive history of periodontal disease in her partner suggests that
chorioamnionitis may have been due to an ascending infection after orogenital contact [75].
Another case presented a case of Streptococcus
viridans intra-amniotic infection occurred at the
25th week of gestation. History revealed a clear
temporal relationship between the onset of symptoms and cunnilingus. A history of recent cunnilingus may be associated with the presence of
Streptococcus viridans in the amniotic fluid including
all species displaying alpha hemolysis (i.e., S. salivarius, S. mitis, S. mutans, and S. sanguis species)
that are normal saprophytes in the human upper
respiratory tract [76].
Alanen described a case of intra-amniotic infection caused by Capnocytophaga sputigena, frequently
found in the normal bacterial flora of the oral
cavity but not in the vagina. Oral sex during pregnancy was the most probable source of the infection. The aborted fetus showed signs of
pneumonia upon histological examination. The
bacterial species was identified using broad PCR
directly from the amniotic fluid and after bacterial
culture [77].
Enteric Infections
A great number of bowel bacterial pathogens (Salmonella, Shigella, Campylobacter) or intestinal parasites (Amoeba, Giardia, and Cryptosporidia) are
transmitted through sexual practices. Furthermore,
because feces can contain multiple pathogens,
polymicrobial infections may result from a single
sexual exposure causing diarrhea, rectal bleeding,
anal itching, fever, nausea, and abdominal pain or
stomach cramps, increasing gas, bloating [2].
Direct oral-anal sexual contact (analingus) is a
common practice among MSM and is implicated in
the transmission of various enteric pathogens [78].
Because of their larger numbers of sexual partners,
promiscuity and prevalent mode of sexual practices
J Sex Med 2012;9:372–384
380
such as analingus and anal intercourse, homosexual
men commonly acquire giardiasis, amebiasis,
shigellosis, and campylobacteriosis [79].
On the other hand, the incidence of these infections in heterosexuals is lower, maybe because of
different sexual behaviors.
Homosexuality and oral-anal sex were the most
important risk factors in Entamoeba histolytica,
G. lamblia, and helminthic infections. Three
factors make “hyperendemic” enteric protozoan
infection in homosexual men: the original endemic
level in the general population; the prevalence of
sexual acts that facilitate transmission; the frequency of exposure to an infected person [80].
Outbreaks of shigellosis among MSM have
occurred because of direct or indirect oral-anal
contact but usually are caused by Shigella flexneri
[81].
In the past, shigellosis in Seattle-King County
has been primarily a disease of children, their
parents, and foreign travelers. During July 1975,
an outbreak of shigellosis in Seattle’s community
of MSM (nearly 30% of all cases of shigellosis)
involved both S. flexneri and S. sonnei. Fellatio
and/or oral-anal contact were declared by 90% of
the infected homosexual men. It was reported the
finding of S. flexneri, a previously unusual organism in Seattle [82].
Approximately 40,000–100,000 people die
yearly from amebiasis, the second leading cause of
death from parasitic diseases.
In the United States, the majority of the
reported cases are in immigrants or in travelers to
endemic areas such as Mexico, Central America,
and South America. A prevalence rate of 20–30%
has been documented in selected populations of
homosexuals of North America and Europe.
Although E. histolytica may be isolated from
stool specimens in 20–30% of selected homosexual
populations, reports of severe disease are rare.
Despite of this, a case reported the death of a
35-year-old MSM secondary to fulminant amebic
colitis leading to perforation [83].
In a controlled study, 67.5% of 200 homosexual
men and 16% of 100 heterosexual men were found
to be infected with intestinal parasites. E. histolytica
was isolated from 27% of the homosexual and 1%
of the heterosexual men; Giardia lamblia was isolated from 13% of the homosexual and 3% of the
heterosexual men.
The real problem is that undiagnosed and
untreated infections, frequently asymptomatic,
add to the reservoir of infection in the homosexual
community [84].
J Sex Med 2012;9:372–384
Ballini et al.
Conclusions
The first comprehensive study that examined
the prevalence of the oral sex was published in the
Time magazine [85]. A report, performed by the
National Center for Health Statistics and based on
a computer-administered survey over 12,000
Americans between 15 and 44 years old, stated that
over half of the questioned teenagers have had oral
sex. This report provided evidence that oral sex
among teenagers is “on the rise.”
In a recent study, Herbenick et al. [86] analyzed
the most recent partnered sexual event reported by
3990 adults (ages 18–59) in United States.
However, oral sex (giving and receiving) was frequently a part of participants’ most recent sexual
event, particularly for men ages 25–49 and women
ages 18–39.
The same authors conducts a similar study
among the black and Hispanic populations in the
United States [87], in Americans men and women
over age 50 [88] and in men and women ages
14–94 in the United States [89].
Nevertheless, if STI status is unknown for partners, condoms or dental dams is recommended
when performing or receiving oral intercourse.
The plastic wrap may also be used as a barrier
during oral intercourse, but many find that the
thickness of the plastic dulls sensation [90].
Public health programs among youths and
minorities may underlie higher condom use rates
among these groups. Condom use may be further
improved by continuing such programs and also
expanding outreach to older persons and whites,
suggesting prolonging use as relationships
develop, and highlighting that condom use does
not necessarily interfere with the sexual experience
[91,92].
Two recent cases [93,94] supported the prophylactic use of chlorhexidine rinse to reduce the retrograde entry of bacteria from oral cavity to the
urethra. This approach will be a new, easy, attractive, and effective method for the prevention of
nongonococcal urethritis, prostatitis, and epididymitis following insertive oral intercourse.
Chlorhexidine is poorly absorbed from skin,
mucosa, and gastrointestinal tract indicating a systemic safety.
Self-care may be important for development of
STI prevention products such as vaginal microbicides [95].
Furthermore, it does not cause any bacterial
resistance and suprainfection. Is important cytological diagnosis to proceed with a correct therapy
1057
381
Nonviral STI and Oral Sex
As reported from Sadeghi-Nejad et al. [97],
there is a need for state-of-the-art information in
the area of STI in relation to sexual function.
Early and late recurrences of the infection and
related pathologies are frequent. They may have a
very different impact from the psychosexual point
of view, according to the severity of lesions,
aggressiveness of related treatments and their side
effects, frequency of recurrences and their severity,
and quality of psychosexual support from relatives
and health care providers [98].
We advise physicians to be receptive to discuss
sexuality issues and provide patients with adequate
therapy.
Figure 4 “Side-to-side” adhered short bacilli to a buccal
epithelial cell.
Figure 5 Pleomorphic-adhered bacteria to a buccal epithelial cell (clue cell).
[96]. In sample’s preparation of the a phase contrast or direct microscopy are required. A spatula is
used to collect the cells from the buccal mucosa.
The spatula is immediately dabbed (not rubbed) in
a drop of sterile saline solution, previously applied
on a microscope slide. Soon after, the specimen is
mounted with a coverslip and the sample is thus
ready to be examined under the pH microscope,
without any fixation or staining.
In bacterial cytoadhesion, the adhesion of bacteria to cells (Figure 4–6) is a necessary prerequisite to bacterial duplication, colonization,
interbacterial coaggregation, and subsequent
infection. Interbacterial coaggregation (Figure 7)
is indispensable for the formation of pilus and consequent transfer of bacterial virulence factors by
means of plasmids.
1058
Figure 6 Cytoplasmic tunnel with sharply condensed
border in a buccal epithelial cell.
Figure 7 Cytoplasmic holes with sharply condensed border
in a buccal epithelial.
J Sex Med 2012;9:372–384
382
Corresponding Author: Andrea Ballini, BSc, Department of Dental Sciences and Surgery University of Bari
“Aldo Moro,” Bari 70124, Italy. Fax: +39 (080) 5478043;
E-mail: andrea.ballini@medgene.uniba.it
Conflict of Interest: None.
Statement of Authorship
Category 1
(a) Conception and Design
Andrea Ballini; Stefania Cantore
(b) Acquisition of Data
Laura Fatone; Valentina Montenegro
(c) Analysis and Interpretation of Data
Francesco Pettini; Paolo Romita; Giovanni
Miniello; Annarita Antelmi; Biagio Rapone
Category 2
(a) Drafting the Article
Laura Fatone; Andrea Ballini; Valentina Montenegro; Stefania Cantore
(b) Revising It for Intellectual Content
Felice Roberto Grassi; Caterina Foti
Category 3
(a) Final Approval of the Completed Article
Vito Crincoli; Danila De Vito; Letizia Perillo
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