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101
© Rapid Science Publishers ISSN 0269-9370
Introduction
Heterosexual intercourse is the major route of transmis-
sion of HIV in sub-Saharan Africa [1,2] and accounts
for at least 75% of HIV infections among adults in that
part of the world [3,4].
Although epidemiological studies have demonstrated
that ulcerative and non-ulcerative sexually transmitted
diseases (STD) are risk factors for HIV heterosexual
transmission [5–8], the role of other factors that may
have an impact on the genital tract remains unknown.
There is some evidence that frequent vaginal douching,
through modification of vaginal flora, may increase a
woman’s susceptibility to sexually transmitted agents.
Previous studies have suggested that vaginal douching
may increase the risk of cervical infections [9,10] and
predispose women to pelvic inflammatory disease
[11–13]. Cervical infections, in turn, have been identi-
fied as a risk factor for HIV infection [5,6]. These find-
ings suggest that vaginal douching may play a role in
the heterosexual transmission of HIV.
Preliminary reports have described the use of intravagi-
HIV infection and vaginal douching in Central Africa
Gérard Gresenguet*†, Joan K. Kreiss*‡, Michael K. Chapko§,
Sharon L. Hillier¶and Noel S. Weiss*
Objective: To determine whether vaginal douching is associated with HIV infection.
Methods: A total of 397 female patients who attended the referral clinic for sexually
transmitted diseases in Bangui, Central African Republic, from August 1994 to
February 1995, were interviewed regarding sexual behavior, sexual history, and
vaginal douching during the previous 3 years. Pelvic examinations were conducted
and vaginal and cervical fluids evaluated for genital infections. Blood was drawn for
HIV and syphilis serologic testing.
Results: The seroprevalence of HIV infection in the study population was 34%.
Twenty-one per cent of the 115 HIV-seropositive women had a consistent practice
of douching with commercial antiseptics versus 35% of the 223 HIV-seronegative
women [odds ratio (OR), 0.6; 95% confidence interval (CI), 0.4–0.9; after adjusting
for lifetime number of sexual partners, marital status, and condom use]. In contrast,
a higher percentage of HIV-seropositive than HIV-seronegative women had a
consistent practice of douching with a non-commercial preparation (14.8 versus
6.7%; adjusted OR, 1.7; 95% CI, 1.0–3.0).
Conclusion: Our results suggest that vaginal douching with non-commercial
preparations is associated with an increased prevalence of HIV, whereas douching
with commercial antiseptic preparations was associated with a lower prevalence of
HIV. The findings from this cross-sectional survey require confirmation in
prospective studies.
AIDS 1997, 11:101–106
Keywords: HIV infection, antiseptic douching, vaginal douching
From the *Department of Epidemiology, University of Washington, Seattle, Washington, USA, the †National Reference Centre
for Sexually Transmitted Diseases and AIDS, Ministry of Public Health and Population, Bangui, Central African Republic, the
‡Department of Medicine, University of Washington, the §Center for Cooperation Studies in Health Services, Seattle Veterans
Affairs Medical Center and Department of Health Services, University of Washington, Seattle, Washington and the
¶Department of Obstetrics, Gynecology and Reproductive Sciences, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.
Sponsorship: G.G. was a scholar in the International AIDS Research and Training Program, supported by a grant from the
Fogarty International Center, National Institutes of Health (grant no. D43-TW00007).
Request for reprints to: G.Gresenguet, National Reference Centre for Sexually Transmitted Diseases and AIDS, B.P. 2229,
Bangui, République Centrafricaine.
Date of receipt: 23 May 1996; revised: 7 October 1996; accepted: 15 October 1996.
AIDS 1997, Vol 11 No 1
102
nal substances as being common practice in some areas
in Central and Southern Africa. In Zimbabwe, 87% of
women reported using herbs or other intravaginal sub-
stances regularly prior to sexual intercourse [14]. In
Zaïre, a study of 50 women using irritant intravaginal
substances suggested that these substances cause inflam-
matory lesions of the vagina and the cervix [15]. More
recently, in Malawian pregnant women, Dallabetta et
al. [16] reported a small positive association between
HIV seropositivity and use of intravaginal agents for
treatment of vaginal discharge. Little is known about
the relationship between douching using commercial
products and HIV seropositivity.
This study was undertaken to assess the association
between vaginal douching and HIV infection, with
particular attention to the type of product used for
douching.
Materials and methods
The study was conducted at the National Reference
Center for Sexually Transmitted Diseases and AIDS in
Bangui, the central public referral clinic for treatment
and diagnosis of STD in the Central African Republic,
from August 1994 through February 1995.
Non-pregnant women aged 15–45 years who attended
the STD clinic during the study period for a routine
check-up or for an investigation related to genital
symptoms were eligible for enrollment. The purpose of
the study was explained to each woman and pretest
counseling for HIV testing was provided.
After informed consent, women underwent an inter-
view concerning demographic data, gynecologic and
obstetric history, sexual history including age of first
sexual experience, lifetime number of sexual partners,
and prior STD, and use of contraceptives. A portion of
the interview was devoted to the practice of vaginal
douching, including age of first douching, type of
product usually used, reason for douching, duration of
use, use in relation to sexual intercourse, and frequency
of douching. In order to minimize the influence of
current HIV serostatus on the results, questions were
asked concerning any changes in douching during the
previous 3 years. All interviews were conducted by one
female medical practitioner (who spoke the national
language) in a face-to-face interview. A physical exami-
nation, including pelvic examination, was performed.
Specimens were obtained from the lateral vaginal wall
for Gram stain and the posterior fornix for wet-mount
microscopy and Candida culture. Swab specimens of
the endocervix were obtained for detection of cervical
infections. Ten milliliters of blood were drawn for
serological testing of HIV and syphilis.
Neisseria gonorrhoeae was isolated on modified
Thayer–Martin medium and identified on the basis of
typical colony morphology, oxidase reaction, and sugar
utilization patterns. Chlamydiae trachomatis antigen was
detected by enzyme immunoassay using the Syva
Microtrack (Syva Co., Palo Alto, California, USA).
Bacterial vaginosis was diagnosed by microscopic
examination of Gram-stained vaginal smears, using the
standardized scoring method of Nugent et al. [17].
Trichomonas vaginalis was identified by wet-mount
microscopy, and vaginal yeast was identified by culture
on Sabouraud medium.
The presence of HIV antibodies was assessed by an
enzyme-linked immunosorbent assay (ELISA) using
two tests with different principles (Genelavia Mixt
HIV1/HIV2, Pasteur Diagnostic, Marnes-la-
Cocquette, France; and Wellcozyme HIV1, Murex
Diagnostics Ltd, Dartford, UK). HIV infection was
defined by positive results on these two ELISA assays.
In the case of discordant results, a third ELISA
(Wellcozyme HIV1/HIV2, Murex Diagnostics) was
performed. The serologic diagnosis of syphilis was
made using rapid plasma reagin and Treponema pallidum
hemagglutination assays.
Statistical analysis was performed using the Statistical
Package for Social Sciences for Windows version 6.0
(SPSS Inc., Chicago, Illinois, USA). A x2test was used
for comparison of proportions and Kruskal–Wallis test
for comparison of medians. Odds ratios (OR) and 95%
confidence intervals (CI), calculated by Epi Info
(World Health Organization, Geneva, Switzerland),
were used to estimate the relative risk of HIV infection
according to douching practice. Logistic regression
analyses were performed to adjust associations for
potentially confounding factors.
Results
Between August 1994 and February 1995, 462 eligible
women attended the STD clinic, of whom 410 were
enrolled in the study. Fifty-two women refused partici-
pation, mainly because of lack of time or reluctance to
answer personal questions. Thirteen patients were
excluded because of incomplete data. Thus, 397
women were included in the current analysis. Ninety
per cent of women came to the clinic because of vagi-
nal symptoms. Of the 397 women, 135 (34%) had HIV
antibodies.
Demographic characteristics, sexual behavior, and med-
ical history of HIV-1-seropositive and -seronegative
women are compared in Table 1. There was no associ-
ation between age and HIV serostatus. Prevalence
of HIV infection was significantly higher among
HIV infection and vaginal douching Gresenguet
et al.
103
women not married at the time of the interview.
Neither the level of education nor employment status
was associated with HIV infection. Although age at first
sexual intercourse was unrelated to HIV infection,
HIV-seropositive women had a significantly greater
lifetime number of sexual partners. Twenty-five per
cent of HIV-seropositive and 13% of HIV-seronegative
women reported a history of genital ulcer disease.
History of sexual intercourse during menses was not
associated with HIV seropositivity. Use of condoms
was reported by fewer than 10% of women and was
unrelated to HIV infection.
Table 1. Demographic and behavioral characteristics of HIV-
seropositive and HIV-seronegative women.
HIV+ HIV–
(n = 135) (n = 262)
P
Median age (years) 27 26 0.4
Median years of education 6 6 0.6
Marital status
Married 65 (48) 149 (57)
Never married 55 (41) 101 (38) 0.03
Divorced or widowed 15 (11) 12 (5)
Occupation
Housewife 73 (54) 127 (48)
Student or worker 31 (23) 76 (29) 0.4
Self-employed 31 (23) 59 (23)
Age at first sexual intercourse
10–14 years 24 (18) 37 (14)
15–17 years 80 (59) 153 (58) 0.5
>17 years 31 (23) 72 (28)
Lifetime no. sexual partners
1–2 29 (22) 91 (35)
3–5 53 (39) 107 (41) 0.01
>5 53 (39) 64 (24)
History of genital ulcer disease 34 (25) 35 (13) 0.01
Vaginal sex during menses 20 (15) 42 (16) 0.75
Condom use 11 ( 8) 24 ( 9) 0.74
Data are expressed as numbers (%) of women, unless otherwise
indicated.
Of the 397 women, 195 (49%) had douched at some
time. Among women with history of douching, reasons
included hygiene in 60%, treatment of vaginal dis-
charge in 30%, treatment of infertility in 6%, and to
produce a vaginal tightening effect in 4%. The median
age at first douching was 20 years (range, 12–47 years).
Thirty-six per cent of women reported that they had
learned douching practices from a health worker, 29%
from a relative, and 25% by self-training. The mean
weekly frequency of douching was seven (range, 1–21).
Forty-three per cent of women reported regular
douching before and after sexual intercourse, 34%
reported douching before intercourse only, and 8%
after only. For the remaining 15%, timing of douching
was independent of sexual intercourse. Eighty-two per
cent of women reported use of a douche bag, 15% use
of fingers, and 3% use of a douche bulb. Of the 194
patients who reported routine douching at the time of
the interview, 140 (72%) used a commercial antiseptic,
48 (25%) used a non-commercial preparation, and
seven (3%) used water alone. Mercurobutol (Mercryl
Lauryle, Menarini Laboratoire, Rungis, France) and
trichlocarban (Solubacter, Boots Healthcare
Laboratories, Courbevoie, France) were the commer-
cial products most frequently used (by 40 and 30% of
women, respectively). Povidone-iodine (Betadine solu-
tion gynecologique, Laboratoires Sarget, Merignac,
France) and glycocolle (Gyn Hydralin, Soekami
Lefrancq Laboratoire, Saint-Ouen, France) were used
by 17 and 13% of women, respectively. Mercurobutol
and trichlocarban have antiseptic properties and are
used as a 1 : 10 dilution for gynecological purposes or
undiluted in medical practice (e.g., to disinfect
wounds). A vaginal solution of povidone-iodine or gly-
cocolle is recommended by the manufacturers to treat
vaginal discharge and to disinfect the genital tract.
Among the 48 women who used non-commercial
preparations, 22 (46%) used herbs or medicinal plants,
and 26 (54%) used solutions they prepared themselves
at home, such as mixtures of water and crystals of
potassium permanganate (six women) or traditional
powder (10 women). Of all women who ever
douched, 55 (28%) had changed their douching habits
at some time during the previous 3 years.
Table 2. Comparison of demographic and behavioral characteris-
tics of women according to douching practice.
Ever douched* (%)
Commercial Non-commercial
Never douched (%) antiseptics preparations
(n = 202) (n = 104) (n = 32)
Median age (years) 25 26 30‡
Median years of
education 6 8†2
Marital status
Married 55 53 59
Never married 39 45 28
Divorced or widowed 6 2†13
Occupation
Housewife 56 49 53
Student or worker 20 39†12
Self-employee 24 12†35
Age at first sexual
intercourse
10–14 years 18 9†19
15–17 years 58 61 62
>17 years 24 31 19
Lifetime number of
sexual partners
1–2 partners 36 29† 12‡
3–5 partners 37 44 41
>5 partners 27 27 47‡
History of genital
ulcer disease 17 16 28
Vaginal sex during
menses 17 13 25
Condom use 6 13†13
*Restricted to women whose douching practices did not change
during the 3 years prior to interview. †
P
<0.05 versus never
douched. ‡
P
<0.05 versus never douched.
AIDS 1997, Vol 11 No 1
104
The following analyses are restricted to those women
who reported consistent use (at least once per week) of
either commercial antiseptics or non-commercial
preparations during the previous 3 years. Because of
small numbers, women using water alone were exclud-
ed. The correlates of particular douching methods are
presented in Table 2. A total of 104 women used a
commercial antiseptic during the previous 3 years.
Compared with women who never douched, douching
with a commercial antiseptic was associated with
greater education, more frequent employment outside
the home as a student or worker, less frequent self-
employment status, older age at first intercourse, greater
lifetime number of sexual partners, and greater condom
use. The 32 women who used non-commercial prepa-
rations were older and had a higher lifetime number of
sexual partners than women who never douched.
A significant inverse association between douching
with commercial antiseptics and HIV seropositivity was
observed (Table 3). Twenty-five (21.7%) out of 115
HIV-seropositive women reported use of commercial
antiseptics compared with 79 (35.4%) out of 223 HIV-
seronegative women (OR, 0.6; 95% CI, 0.3–1.0). In
contrast, douching with non-commercial preparation
was positively associated with HIV serostatus (OR, 2.0;
95% CI, 0.9–4.5). Use of non-commercial preparation
was reported by 17 (14.8%) out of 115 HIV-seroposi-
tive and 15 (6.8%) out of 223 HIV-seropositive
women.
Table 3 presents data about the relationship between
vaginal douching and HIV infection according to the
duration, reason for use, frequency, and timing in rela-
tion to sexual intercourse. The negative association
between HIV infection and douching with a commer-
cial antiseptic was restricted to women who douched
more than three times per week and who did not do so
to treat vaginal discharge. In addition, the negative
association was seen only when women douched after
sexual intercourse or at times unrelated to intercourse.
The positive association between douching with a non-
commercial preparation and HIV infection was limited
to women who had a history of douching for more
than 5 years.
The relationship between current genital infections and
vaginal douching was assessed after adjustment for vari-
ables which were associated with douching practice.
There was no association between douching using a
non-commercial preparation and the presence of geni-
tal infections at the time of the interview (data not
shown). Table 4 shows data concerning the risk of gen-
ital infections among women who used a commercial
antiseptic for vaginal douching compared with women
who did not douche. An increased presence of vaginal
yeast was found among women who used commercial
antiseptics (adjusted OR, 1.4; 95% CI, 1.3–3.0). There
was no association between douching practice and bac-
terial vaginosis, nor with cervical infections due to N.
gonorrhoeae or C. trachomatis.
Table 3. Vaginal douching* and HIV infection according to the
duration, frequency, reasons for use, and timing in relation to sexu-
al intercourse.
HIV+ HIV–
(n = 115) (n = 223) OR (95% CI)
Never douched 73 129 1.0
Douched using a
commercial antiseptic 25 79 0.6 (0.3–1.0)
Duration
<1 year 3 16 0.4 (0.1–1.3)
1–5 years 11 37 0.6 (0.3–1.1)
>5 years 11 26 0.8 (0.4–1.7)
Frequency
Once per week 5 7 1.3 (0.3–4.6)
2 or 3 times per week 4 6 1.2 (0.3–4.9)
>3 times/week 16 66 0.5 (0.2–0.8)
Reasons
Treat vaginal discharge 11 20 1.0 (0.4–2.3)
Other 14 59 0.5 (0.2–0.8)
Timing in relation to sexual intercourse
Only before 2 1 3.6 (0.3–99.8)
Always after 6 20 0.6 (0.2–1.5)
Not related to
intercourse 17 58 0.6 (0.3–1.0)
Douched using a non-commercial
preparation 17 15 2.0 (0.9–4.5)
Duration
<1 year 2 5 0.7 (0.1–4.2)
1–5 years 4 3 2.4 (0.4–13.5)
>5 years 11 7 2.8 (1.0–8.2)
Frequency
Once per week 1 4 0.5 (0.1–4.3)
2 or 3 times per week 5 2 4.4 (0.7–33.4)
>3 times per week 11 9 2.2 (0.8–5.9)
Reasons
Treat vaginal discharge 5 6 1.5 (0.4–5.6)
Other 12 9 2.4 (0.9–6.3)
Use in relation to sexual intercourse
Only before 6 6 1.8 (0.5–6.5)
Always after 6 5 2.2 (0.6–8.4)
Not related to
intercourse 5 4 2.3 (0.5–10.1)
*Restricted to women whose douching practices did not change
during 3 years prior to interview. OR, Odds ratio; CI, confidence
interval.
Table 4. Association between current genital infections and douch-
ing with commercial antiseptic.
n (%)
Douched using
Never commercial
douched antiseptic
(n = 202) (n = 104) OR* (95% CI)
Bacterial vaginosis 111 (55) 53 (51) 0.9 (0.7–1.1)
Vaginal yeast 33 (16) 32 (31) 1.4 (1.1–1.9)
Trichomonas vaginalis
15 (7) 9 (9) 1.1 (0.7–1.8)
Neisseria gonorrhoeae
7 (4) 3 (3) 0.9 (0.4–1.9)
Chlamydiae trachomatis
9 (6) 6 (6) 1.2 (0.7–2.2)
Genital ulcer disease 5 (3) 4 (4) 1.3 (0.6–2.6)
TPHA-positive 19 (9) 5 (5) 1.3 (0.7–2.2)
*Odds ratios (OR) adjusted for years of education, marital status,
occupation, age at first sexual intercourse, lifetime number of sexu-
al partners, and condom use. TPHA,
Treponema pallidum
hemag-
glutination assay; CI, confidence interval.
HIV infection and vaginal douching Gresenguet
et al.
105
A multivariate analysis was performed to evaluate the
independent effects of variables that were significantly
associated with both HIV serostatus and vaginal douch-
ing. Condom use was also included in the model
because of its strong association with douching with a
commercial antiseptic. The negative association
between HIV infection and use of commercial antisep-
tic for douching (OR, 0.6; 95% CI, 0.4–0.9) and the
positive association with use of a non-commercial
preparation (OR, 1.7; 95% CI, 1.0–3.0) persisted after
adjustment for marital status, lifetime number of sexual
partners and condom use (Table 5). The association
between HIV and douching persisted after excluding
from the analysis women who were douching for vagi-
nal discharge. The negative association with HIV infec-
tion was similar for each of the two primary
commercial products used for douching (data not
shown).
Table 5. Multivariate analysis of the association between HIV
infection and vaginal douching.
Adjusted OR* (95% CI)
P
Douching practice
Never douched 1.0
Douched using a
commercial antiseptic 0.6 (0.4–0.9) 0.01
Douched using a
non-commercial preparation 1.7 (1.0–3.0) 0.04
Marital status
Married 1.0
Unmarried 1.2 (0.9–1.5) 0.2
Lifetime number of sexual partners
1–2 partners 1.0
3–5 partners 1.0 (0.7–1.3) 0.8
>5 partners 1.5 (1.1–2.2) 0.02
*Odds ratios (OR) adjusted for douching practice, lifetime sexual
partners, marital status, and condom use. CI, Confidence interval.
Discussion
The main objective of this study was to assess the rela-
tionship between vaginal douching and seroprevalence
of HIV with an emphasis on the type of product used
for vaginal douching.
The use of various products for vaginal douching has
been previously described by many authors. In the
United States, the practice of douching has appeared to
be relatively more common among black women than
among white and Hispanic women. These women
reported douching primarily for hygienic reasons, using
commercial products or home preparations (mostly a
mixture of vinegar and water) [18,19]. According to
studies conducted in Central and Southern Africa, tra-
ditional agents used intravaginally have included herbs
and dry leaves. These are used for treatment of vaginal
infection or for a ‘tightening effect’ (to achieve ‘dry
sex’) [14–16]. In our study, the majority of women
with a history of douching used a commercial antiseptic
and the most common reason for douching was per-
sonal hygiene. A smaller number of women reported
use of home preparations.
Our data suggest that women who use non-commer-
cial douche preparations are more likely to be infected
by HIV than women who never douched, whereas
women who used commercial antiseptics for vaginal
douching appeared to have a reduced risk. The limi-
tations of the study must be recognized and taken into
consideration prior to the interpretation of the results.
First, the short study period and the restriction of
enrollment to women who were attending the STD
clinic limited the number of study subjects. This led to
some statistical imprecision of the associations observed
with the different types of douching agents. Second, of
all the variables we collected, only the lifetime number
of sexual partners and marital status were potential con-
founders in the association between previous douching
and HIV infection. Although we adjusted for these two
variables, it is possible that some unknown factor may
have acted to confound this association. For example,
we were unable to measure the presence or degree of
exposure to HIV infection in these patients. Third, and
most importantly, the cross-sectional study design did
not allow us to determine the temporal relationship
between douching practice and HIV infection, nor to
investigate the impact of genital infections on douching
practice.
In Malawi, Dallabeta et al. [16] previously found a
weak positive association between HIV infection and
the use of vaginal agents for self-treatment of discharge
and itching. However, the interpretation of their results
is uncertain, since it is not possible to determine
whether the use of the agents or the underlying condi-
tion was responsible for the association. In women with
no vaginal symptoms, the use of vaginal agents was not
associated with HIV infection. In our study, women
who used non-commercial preparations for vaginal
douching were more likely to be HIV-seropositive
than those who did not douche or who used commer-
cial antiseptics.
Our finding of an increased prevalence of HIV infec-
tion among women who used non-commercial
medicines for vaginal douching suggests that some
intravaginal agents may enhance the heterosexual
transmission of HIV. There are two potential mecha-
nisms whereby transmission could be enhanced. First,
these intravaginal substances may irritate vaginal
mucosa, and thus may promote the proliferation of
lymphocytes which are target cells for HIV [20,21].
Second, if ‘dry sex’ is the desired effect of using
traditional intravaginal medicines, the use of these
AIDS 1997, Vol 11 No 1
106
agents may lead to dehydration of the vaginal mucosa,
rendering the vaginal epithelium more vulnerable to
local trauma [22].
The negative association between the use of a commer-
cial antiseptic for douching and HIV infection suggests
that douching with a commercial antiseptic may
decrease the risk of acquiring HIV. Previous studies
have demonstrated that douching may modify the vagi-
nal pH [23] and it has been established that HIV infec-
tivity is reduced in an acidic environment. For
example, Ongradi et al. [24], found that cell-free HIV-
1 particles lose infectivity gradually between a pH of
7.4 and 6.0 and that this process is not reversible at a
pH below 6.0 [25]. In our series, the commercial prod-
ucts primarily used were mercurobutol (an organic
mercurial compound with a pH of 6.7) and triclocar-
ban (a carbinilide with a pH of 5.5). According to the
manufacturers’ guidelines, mercurobutol and trichlocar-
ban have antifungal and bacteriostatic activities. The
use of these antiseptic solutions immediately after sexu-
al intercourse may reduce the inoculum of sexually
transmitted agents, HIV included, through a flushing
mechanism. Alternatively, if these commercial agents,
through their antimicrobial activities, reduced the fre-
quency of STD that serve as cofactors to enhance HIV
transmission, then a protective effect on HIV acquisi-
tion might ensue. However, we documented no effect
of douching with antiseptic preparations on prevalent
genital infection, with the exception of an increased
frequency of Candida colonization.
Clearly our results must be viewed as preliminary, but
we believe these relationships warrant testing in other
populations. Our data are consistent with previous
results that suggest that use of traditional preparations
for douching may be associated with increased risk of
HIV infection. In developing countries, particularly in
those areas of sub-Saharan Africa where this practice is
highly prevalent, prevention campaigns for AIDS could
include the recommendation that traditional medicines
for vaginal douching be avoided. The negative associ-
ation we observed between HIV infection and the use
of commercial antiseptics for douching requires confir-
mation in prospective observational studies.
Acknowledgement
We thank the study participants and the Ministry of
Public Health and Population for their active collabora-
tion, the European Communities (DGVIII) for support-
ing the Centre National de Référence MST/SIDA, and
A. Samory and A. Tete for valuable technical assistance.
References
1. Merson MH: Slowing the spread of HIV: agenda for the 1990s.
Science
1993, 260:1266–1268.
2. Global Programme on AIDS:
Current and Future Dimensions of
the HIV/AIDS Pandemic: A Capsule Summary.
Geneva: World
Health Organization; January 1992.
3. Piot P, Tezzo R: The epidemiology of HIV and other sexually
transmitted infections in the developing world.
Scand J Infect
Dis
1990, 69 (suppl):89–97.
4. Quinn TC: The epidemiology of the acquired immunodeficiency
syndrome in the 1990s.
Emerg Med Clin North Am
1995,
13:1–25.
5. Laga M, Manoka A, Kivuvu M,
et al.
: Non-ulcerative sexually
transmitted diseases as risk factors for HIV-1 transmission in
women: results from a cohort study.
AIDS
1993, 7:95–102.
6. Plummer FA, Simonsen JN, Cameron DW,
et al.
: Cofactors in
male to female sexual transmission of human immunodeficien-
cy virus type 1.
J Infect Dis
1991, 163:233–239.
7. Kreiss JK, Koech D, Plummer FA,
et al.
:AIDS virus infection in
Nairobi prostitutes. Spread of the epidemic to East Africa.
N
Engl J Med
1986, 314:414–418.
8. Martin PMV, Gresenguet G, Massanga M, Georges AJ, Testa J:
Association between HIV1 infection and sexually transmitted
diseases among men in Central Africa.
Res Virol
1992,
143:205–209.
9. Stergachis A, Scholes D, Heidrich FE, Sherer DM, Holmes KK,
Stamm WE: Selective screening for
Chlamydiae trachomatis
infection in a primary care population of women.
Am J
Epidemiol
1993, 138:143–153.
10. Hoegsberg B, Abulafia O, Sedlis A,
et al.
: Sexually transmitted
diseases and human immunodeficiency virus infection among
women with pelvic inflammatory disease.
Am J Obstet Gynecol
1990, 163:1135–1139.
11. Scholes D, Daling JR, Stergachis A, Weiss NS, Wang SP,
Grayston JT: Vaginal douching as a risk factor for acute pelvic
inflammatory disease.
Obstet Gynecol
1993, 81:601–606.
12. Wolner Hanssen P, Eschenbach DA, Paavonen J,
et al.
:
Association between vaginal douching and acute pelvic inflam-
matory disease.
JAMA
1990, 263:1936–1941.
13. Forrest KA, Washington AE, Daling JR, Sweet RL: Vaginal douch-
ing as a possible risk factor for pelvic inflammatory disease.
J
Natl Med Assoc
1989, 81:159–165.
14. Runganga A, Pitts M, McMaster J: The use of herbal and other
agents to enhance sexual experience.
Soc Sci Med
1992,
35:1037–1042.
15. Brown RC, Brown JE, Ayowa OB: The use and physical effects
of intravaginal substances in Zairian women.
Sex Transm Dis
1993, 20:96–99.
16. Dallabeta GA, Miotti PG, Chiphangwi JD, Liomba G, Canner JK,
Saah AJ: Traditional vaginal agents: use and association with
HIV infection in Malawian women.
AIDS
1995, 9:293–297.
17. Nugent RP, Krohn MA, Hillier SL: Reliability of diagnosing bac-
terial vaginosis is improved by a standardized method of Gram
stain interpretation.
J Clin Microbiol
1991, 29:297–301.
18. Rosenberg MJ, Phillips RS, Holmes MD: Vaginal douching. Who
and why?
J Reprod Med
1991, 36:753–758.
19. Aral SO, Mosher WD, Cates W: Vaginal douching among
women of reproductive age in the United States: 1988.
Am J
Public Health
1992, 82:210–214.
20. Peterman TA: Facilitators of HIV transmission during sexual
contact. In
Heterosexual Transmission of AIDS.
Edited by
Alexander NJ, Gabelnick HL, Spieler JM. New York: Alan R. Liss;
1990.
21. Alexander NJ: Sexual transmission of human immunodeficiency
virus: virus entry into male and female genital tract.
Fertil Steril
1990, 54:1–18.
22. Irwin K, Mibandumba N, Mbuyi K, Ryder R, Sequeira D: More
on vaginal inflammation in Africa [letter].
N Engl J Med
1993,
328:888–889.
23. Kaminsky M, Willigan DA: pH and potential irritancy of douche
formulations to the vaginal mucosa of albino rabbit and rat.
Food Chem Toxicol
1982, 20:193–196.
24. Ongradi J, Ceccherini-Nelli L, Pistello M, Specter S, Bendinelli
M: Acid sensitivity of cell-free and cell associated HIV-1: clini-
cal implications.
AIDS Res Hum Retroviruses
1990,
6:1433–1436.
25. Voeller B, Anderson DJ: Heterosexual transmission of HIV.
JAMA
1992, 267:1917–1919.