C M Lowndes1,2, L Mukenge-Tshibaka1, C A B
Gnintoungbé3, E Bédard1, N Geraldo4, P
Jossou5, E Lafia6, F Bernier7, É
Baganizi3,8, J R Joly9, E Frost10 and S
Unité de recherche en santé des populations, Centre hospitalier affilié
universitaire de Québec, Québec, Canada 2 HIV and STI Division, PHLS Communicable Disease
Surveillance Centre, London, UK 3 Projet SIDA 3-Bénin, Cotonou, Bénin 4 Dispensaire MST, Centre de Santé de Circonscription Urbaine
Cotonou 1, Bénin 5 Faculté des sciences de la santé, Université Nationale du
Bénin 6 Programme national de lutte contre le Sida et les MST (PNLS),
Bénin 7 Héma Québec, Montréal, Canada 8 Centers for Disease Control and Prevention, Atlanta, GA,
USA 9 Laboratoire de santé publique du Québec,
Sainte-Anne-de-Bellevue, Canada 10 Département de Microbiologie, Université de Sherbrooke,
Michel Alary, MD, Unité de recherche en santé des populations, Centre
hospitalier affilié universitaire de Québec,1050, chemin Sainte-Foy,
Québec, G1S 4L8, Canada;
publication 24 March 2003
Objectives: (1) To assess risk factors for urethral infectionswith Chlamydia trachomatis, Neisseria gonorrhoeae,
and Trichomonasvaginalis among male clients of female
sex workers (FSWs) inBenin; (2) to study the validity of LED
testing of male urinesamples compared to a highly sensitive
gold standard (PCR) forthe diagnosis of urethral infections
with the organisms citedabove.
Male clients of FSWs (n=404) were recruited on siteat
prostitution venues in Cotonou, Benin, between 28 May and18
August 1998. A urine sample was obtained from each participantjust before he visited the FSW, and tested immediately usinga leucocyte esterase dipstick (LED) test. It was then testedfor HIV using the Calypte EIA with western blot confirmation,and for C trachomatis, N gonorrhoeae, and T vaginalis
by PCR.After leaving the FSW’s room, participants were
interviewedabout demographics, sexual behaviour, STI history
and currentsymptoms and signs, and were examined for
urethral discharge,genital ulcers, and inguinal
STI prevalences were: C trachomatis, 2.7%; N gonorrhoeae,5.4%; either chlamydia or gonorrhoea 7.7%; T vaginalis
2.7%;HIV, 8.4%. Lack of condom use with FSWs and a history
of STIwere independently associated with C trachomatis
and/or N gonorrhoeaeinfection. Over 80% of these
infections were in asymptomaticsubjects. The overall
sensitivity, specificity, positive andnegative predictive
values of the LED test for detection ofeither C
trachomatis or N gonorrhoeae were 48.4%, 94.9%, 44.1%,and 95.7%, respectively. In symptomatic participants (n=22),all these parameters were 100% while they were 47.4%, 94.7%,37.5%, and 96.4% in asymptomatic men (n=304).
Since most STIs are asymptomatic in this population,case
finding programmes for gonorrhoea and chlamydia could be
useful. The performance characteristics of the LED test in thisstudy suggest that it could be useful to detect asymptomaticinfection by either C trachomatis or N gonorrhoeae
in high riskmen.
male clients; female sex workers; STIs; HIV; risk factors; leucocyte
In developing countries, preventive
interventions for HIV andsexually transmitted infections (STIs)
directed at high riskpopulations often target female sex
workers (FSWs), even thoughthe male clients of these women
also represent a significantsource of STIs and HIV, as well
as acting as a bridge for diseasetransmission between FSWs
and women in the general population.In fact, reports from
sub-Saharan Africa have shown high prevalenceof HIV in
clients of FSWs
and in populations of men frequentlyusing prostitution
services, ranging from 8.4% to 56%.Despite these dramatic figures, these men are rarely specifictargets for intervention because they are considered very hardto reach.
A better understanding of
sociodemographic and behavioural characteristicsassociated
with STIs and HIV in male clients of FSWs in Africacould aid
in the formulation of effective interventions fortheir
prevention. STI control and HIV prevention strategiesin men
should also focus on the diagnosis and treatment of curable
STIs. Such a combined strategy, including promotion of condom
use as well as detection and treatment of STIs, has been shownto reduce the prevalence of these diseases and of HIV infectionamong FSWs in sub-Saharan Africa.
In the developing world, diagnosis
and treatment of STIs aregenerally based on the syndromic
approach, a strategy that hasbeen shown to be effective for
However,results from several studies suggest that a
significant proportionof men with positive laboratory tests
for Chlamydia trachomatisor Neisseria gonorrhoeae
in their urethra are asymptomatic.Trichomonasvaginalis has also been shown to be an important cause of
urethralinfection in some African settings, including in
The leucocyte esterase dipstick (LED) test has beenproposed
as a cheap non-specific test that could allow the detection
of polymorphonuclear cells in asymptomatic men and also be usedto confirm symptomatic urethritis.
However, moststudies evaluating the LED test were performed
in the era precedingthe wider use of nucleic acid
amplification tests (NAAT) andshowed sensitivities varying
from 50% to 100% and specificitiesbetween 50% and 80%.
With such results, in most instances,LED was not recommended
as a screening test because of its lowpositive predictive
value, nor was it considered particularlyuseful in
symptomatic patients. More recently, Bowden carriedout a
study in Australia on the validity of the LED comparedto
NAAT (in this case, polymerase chain reaction, PCR) for the
detection of C trachomatis or N gonorrhoeae in urine among
apopulation of largely asymptomatic men.
He used a cut-offvalue of trace for the LED test to maximise
the negative predictivevalue with the objective of selecting
men for whom it wouldbe useful to perform the PCR assay. The
use of this cut offyielded a sensitivity and specificity of
77.8% and 80.8%, respectively.From the detailed results of
the study, it can be observed thata 1+ cut off for the LED
test would result in a sensitivityof 50% and a specificity
of 93.6%, this latter figure beinghigher than any previously
The objectives of this study were:
(1) to evaluate risk factorsfor urethral infections by C
trachomatis, N gonorrhoeae, andT vaginalis
among male clients of FSWs in Benin; (2) to studythe
validity of LED testing of male urine samples compared toa
highly sensitive gold standard (PCR) for the diagnosis of
urethral infections caused by the agents cited above.
This study was undertaken within a larger project whose overallaim was to document the STI/HIV epidemiological situation amongclients of FSWs in Cotonou, Benin, the sociodemographic
characteristicsof these men and their sexual behaviour with
FSWs and otherfemale partners.1
Health seeking behaviour for STIs was alsoinvestigated, as
was the feasibility of interventions targetingthese men. The
study was conducted in Cotonou, the largest cityof Benin
with approximately 800 000 inhabitants. In this city,an
ongoing (started in 1993) HIV/STI intervention project funded
by the Canadian International Development Agency targets FSWs
for HIV and STI prevention. The project strategies involve promotionof correct condom use and free STI treatment according to localsyndromic approach guidelines, including a screening algorithmfor FSWs.
Study population and study
The data collection period for this study was between 28 May
and 18 August 1998. The study population consisted of male clientsof FSWs recruited directly at 13 different prostitution sites(not selected randomly, but chosen to ensure a diversity oftypes of prostitution venues and adequate geographical
distributionin the city) between 8 pm and 1 am. The study
was proposed tothe men by a field worker in collaboration
with the FSWs themselvesand the bar and brothel owners. The
study was entirely anonymousand there was no payment made
for participation. However, freecondoms were given to
participants and, in case of STI symptomsor signs or when
the LED test was positive (see below for procedures),STI
treatment was provided at no charge. The study procedures
were performed on site in a room or a curtained off space outsideprovided by the bar or brothel owner. After verbal informedconsent, a first void urine sample was obtained from each
participantjust before he went into a room with the FSW to
have sex. Afterthe client came out of the FSW’s room, he was
interviewedfor a duration of 15–30 minutes on demographics,
sexualbehaviour, STI history, and current symptoms as well
as on healthseeking behaviour for STIs. Thereafter, the
genital area wasexamined for the presence of urethral
discharge, ulcers, andinguinal lymphadenopathies. Ethical
approval for this studywas given by the ethics committee of
the Centre hospitalieraffilié universitaire de Québec and by
the Ministryof Health, Benin.
A LED (Chemstrip 10A, Boehringer Mannheim, Québec, Canada)
test was performed on the urine sample immediately after collectionon site and aliquots were stored at 4°C for HIV testing
and at -20°C for PCR testing for STIs. HIV testing was performedlocally in Cotonou and in Montreal, Canada, with the CalypteEIA (Calypte Biomedical Corporation, Berkeley, CA, USA) followedby western blot confirmation (Cambridge Biotech/Calypte BiomedicalCorporation).
The Amplicor CT/NG detection kit from RocheDiagnostics was
performed in Montreal for detection of chlamydialand
gonococcal infections. Finally, an in-house PCR for Trichomonasvaginalis targeting the 650 base pair repetitive sequence wasperformed in the Department of Microbiology of the Universitéde Sherbrooke, using an adaptation
of the procedure of Shaioand collaborators.
The data were analysed using Epi-Info (Center for Diseases Controland Prevention, USA, World Health Organization, Geneva,
Switzerland)and SAS (SAS Institute, Cary, NC, USA). For the
analysis ofSTI risk factors, the prevalence odds ratio (POR)
was used asthe measure of association. The 2and
Fisher’s exact testswere used for univariate analysis
whereas logistic regressionwas used for multivariate
analysis. We calculated the sensitivityand specificity (with
95% confidence intervals) as well as thepositive and
negative predictive values of the LED test, usinga cut off
of 1+, meaning that samples with a result greaterthan trace
were considered LED positive (the possible valuesfor the
test were: negative, trace, 1+, and 2+), in comparisonwith a
gold standard based on PCR results.
A total of 404 male clients of FSWs provided a urine sample
over 47 nights of data collection between 28 May and 18 August,1998. From 17 June to 18 August, the numbers of clients refusingto participate in the study were recorded. Of 486 clients
approached,329 (67.7%) accepted and 157 (32.3%) declined
participation.Of the 404 subjects who provided a urine
sample, 330 (81.7%)answered the questionnaire and 298
(73.8%) had a physical examination.Among those answering the
questionnaire, median age was 25.5years (range 17–53).
Overall, 34 (8.4%) of the participantswere infected with
HIV; 22 (5.4%) with N gonorrhoeae; 11 (2.7%)with C
trachomatis; 11 (2.7%) with T vaginalis; 31 (7.7%) witheither N gonorrhoeae or C trachomatis; and 41
(10.1%) with anyof the latter three pathogens.
Among the 326 men who provided
information on STI symptoms,seven (2.1%) reported urethral
discharge while 17 (5.2%) complainedof dysuria. Physical
examination revealed that six clients outof 298 (2.0%) had
genital ulcers while presence of urethraldischarge was
confirmed in three men (1.0%). Overall, 22 menreported
either dysuria or urethral discharge or had dischargeupon
clinical examination. Table 1
shows the association betweensymptoms/signs of urethritis
Table 1 Univariate analysis of clinical signs/symptoms and risk
factors for N gonorrhoeae, C trachomatis, and T
vaginalis infection among male clients of FSWs in Cotonou, Benin
Symptoms/signs or risk factor
No (%) with NG* or CT
Prevalence odds ratio
No (%) with TV
Prevalence odds ratio
Current symptoms and/or signs¶
Price paid to FSW
> 1US $
Condom use with FSW just seen
Condom use with FSW in general
*N gonorrhoeae; C
otherwise specified; Trichomonas
vaginalis; ¶reported urethral discharge or dysuria or
urethral discharge on physical examination; **2for
Table 1also shows the risk factors other than symptoms/signs
associated with the different STIs studied. Factors that did
not show any significant association with STIs include age,
ethnicity, country of origin, city of residence, marital status,and frequency of visits to FSWs. Whereas price paid to FSW,STI history, and current urethritis signs/symptoms were
significantlyassociated with infection by either N
gonorrhoeae or C trachomatis(all p <0.05), none
of these variables were significantlyrelated to T
vaginalis infection. Even though current urethritis
signs/symptoms were associated with gonococcal or chlamydial
infection, the majority of the men infected with either pathogen(81.3%) were asymptomatic.
For the multivariate analysis (table
we entered all thevariables identified as risk factors in
the univariate analysisin a multiple logistic regression
model (for condom use, sincethere was a strong correlation
between the two condom use variablesshown in table 1,
we chose to enter in the model only the variableon condom
use with FSWs in general). In this analysis, historyof
previous STI and condom use were significantly associated
with chlamydial or gonococcal infection, whereas urethritis
signs/symptoms were only of borderline significance.
Table 2 Multivariate analysis of risk factors for
infection by either N gonorrhoeae or C trachomatis among
male clients of FSWs in Cotonou, Benin
Condom use with FSW in general
Current urethritis symptoms/signs
*Prevalence odds ratio; test
The LED test was positive in 34 of the 404 subjects (8.4%).
The overall sensitivity, specificity, positive and negative
predictive values of the LED test, in comparison with the goldstandard PCR results, for the detection of either C trachomatisor N gonorrhoeae, are shown in table 3.
Whereas among symptomaticmen the concordance between LED and
PCR results was perfect,among asymptomatic men the
sensitivity was just under 50% andthe specificity
approximately 95%, resulting in a positive predictivevalue
of 37.5%. In contrast with the very strong association
between LED positivity and an infection with either N gonorrhoeaeor C trachomatis (p<0.0001), there was no significant
associationbetween a positive LED test and the presence of
T vaginalis(p=0.24), irrespective of symptoms. The
performance of the LEDtest to detect T vaginalis was
thus very poor, with a sensitivityof 18.2% (95% CI: 2.8 to
51.8), a specificity of 91.9% (95%CI: 88.7 to 94.4), a
positive predictive value of 5.9%, anda negative predictive
value of 97.6%.
Table 3 Performance of the LED test in the diagnosis of
C trachomatis and/or N gonorrhoeae among male clients of FSWs
in Cotonou, Benin
Our data show that about 8% of male clients of FSWs in Cotonouwere infected with either N gonorrhoeae or C trachomatis.
Similarresults were found by Steen and colleagues, who
reported a prevalenceof 10.9% for N gonorrhoeae or
C trachomatis among male clientsof FSWs in South Africa.
The prevalence of T vaginalis infectionwas relatively
low in our study population and was not associatedwith known
STI risk factors in our data. In studies carriedout in Kenya
T vaginalis was much more frequentthan either N
gonorrhoeae or C trachomatis in truck driversand
men in the general population, respectively, independentlyof
the presence of symptoms. In a study on aetiology of urethritisin five west African countries, the prevalence of T vaginalisvaried considerably from one country to the other, from 2.5%in Côte d’Ivoire to 24.5% in Senegal.
In the latterstudy, the prevalence of T vaginalis
among men consulting forurethral discharge in Benin was
8.1%. These results are compatiblewith ours for the subgroup
of symptomatic men (prevalence of9.1%, table 1),
and suggest important geographical variationsin the
prevalence of T vaginalis.
Among symptomatic subjects, the
prevalence of gonorrhoea orchlamydial infection was low at
only 22.7%. One reason for thiscould be that we did not
screen the participants for Mycoplasmagenitalium.
This organism was found to be the most common causeof non-gonococcal
urethritis in a study by Morency and colleaguesin Bangui,
Central African Republic,
and one important aetiologicalagent of urethral discharge in
Furthermore, studieson symptomatic men such as those
generallyenrol subjects consulting spontaneously at health
centres fortheir symptoms. In our study, enrolment was not
based on spontaneouscomplaints, but symptoms were rather
actively elicited fromall participants. This could well lead
to an overestimationof the frequency of symptoms and,
consequently, to a lower STIprevalence than that observed in
studies on men with spontaneouscomplaints of dysuria or
urethral discharge. This is very likelygiven that urethral
discharge was confirmed in only three menon clinical
examination. Finally, PCR on urine samples is lesssensitive
than on urethral swabs,
although it is still consideredan acceptable screening test,
whereas the use of PCR on femaleurine samples can be much
more problematic with reported sensitivitiesas low as 54%.
In Cotonou, a study carried out
among FSWs, at the same timeas this one, demonstrated high
prevalence of N gonorrhoeae orC trachomatis
among these women (24.5%).
Similar results werereported from the study by Steen et
al (24.9% among FSWs).The observed difference in STI prevalence among FSWs and theirmale clients may be attributed to the fact that duration ofinfection is generally longer in women than in men (women beingmore often asymptomatic than men) and that women are more
susceptiblethan men to acquiring these infections, as well
as much morefrequently exposed to STIs. In fact, while the
median numberof visits to FSWs by the clients was 24 per
year in this study,the corresponding figure for FSWs was 17 male clients per week.
In multivariate analysis, gonorrhoea
or chlamydial infectionwas associated with lack of condom
use with FSW and STI history.Lower price paid to the FSW, as
well as lower educational level,which were also associated
with these infections in univariateanalysis, did not remain
significantly associated in the finalmultivariate model,
probably because they were found to be predictorsof condom
use in this population.
Although condom use ratesby clients with the FSW just seen
were suboptimal at 56%,
ourdata nevertheless provide further evidence for the
protectiveeffect of condom use on STIs. The association with
a historyof STI, however, underlines the need for intensive
preventivecounselling of men when an STI is diagnosed. The
recurrenceof STIs in these men indicates that this
opportunity is beinglost in current clinical practice in
The fact that the vast majority
(>80%) of infections withN gonorrhoeae or C
trachomatis were asymptomatic in this populationsuggests
that case finding programmes in this high risk male
population could be very useful. Such programmes could includeregular sessions of LED testing at prostitution venues, inspiredfrom the methodology used in this study, as well as the
developmentand promotion of specific clinical services for
high risk menwhere LED testing would be available.
of the clients of female sex workers inCotonou, Benin,
had a urethral infection caused by Neisseria
gonorrhoeae, Chlamydia trachomatis, or Trichomonas
Lackof condom use and previous history of STI were associated
withinfection by N gonorrhoeae or C
trachomatis, whereas no specificfactor was
associated with T vaginalis.
leucocyte esterasedipstick (LED) test performed
relatively well for the detectionof N gonorrhoeae
and C trachomatis, but not for the detectionof
finding among high risk men in developingcountries is
a priority and the LED test could be useful forthis
In our study, the performance of the
LED test was very similarto that derived from the data
presented by Bowden,
with asensitivity of around 50% and a specificity of around
95%. Inanother recent study, comparing LED to ligase chain
reaction(LCR) for chlamydial infection only, the results
were even better,with a sensitivity of 87.5% and a
specificity of 92.4%.
Theseresults suggest that the LED test has a much better
specificity(and thus higher positive predictive value) than
when previouslyevaluated in comparison with non-NAAT
technologies.Although schistosomiasis has been associated with a positiveLED test
and could have resulted in a poor specificityin studies
carried out in east Africa where the prevalence ofthis
parasitic infection is relatively high, it could not have
affected results of studies conducted in developed countrieswhere poor specificity of the LED test has also been reported.It thus appears that some true cases were detected by the LEDtest but not by non-NAAT technologies, resulting in an apparentlack of specificity of the former.
Such results suggest that LED could
be a useful case findingtool in high risk men in developing
countries. Indeed, in ourstudy, the positive predictive
value of the LED test among asymptomaticmen was 37.5%, a
figure which, although lower than is generallyfound for the
syndromic approach in the management of men presentingwith
symptoms of urethral discharge, is much higher than thatof
another standard of care for STI management in developing
countries, the syndromic approach for the diagnosis of cervicalinfections among symptomatic women.
In addition, the factthat the LED test is rapid and
inexpensive and can be administeredat the point of care
makes it a particularly useful test ina context where high
rates of non-attendance for return visitsoccur, as shown for
example in FSWs in Cotonou.
It has beenshown that even in the industrialised world,
non-attendancefor follow up visits can have a negative
impact on STI treatmentrates.
In our study, the LED test had
perfect performance parametersin symptomatic men. However,
these findings are based on a verysmall number of men and
need to be confirmed by other studies.
In conclusion, the performance of
the LED test in our studysuggests that it could be a useful
case finding tool for STIsin high risk asymptomatic men in
developing countries. Giventhe fact that the prevalence of
STIs in clients of FSWs wasfound to be much higher than that
of the general populationof men in Cotonou (1% for
gonorrhoea and 2% for chlamydial infection),and that these men constitute a bridge between FSWs and thegeneral population of women in terms of STI and HIV transmission,interventions targeted towards this population, involving bothSTI screening and treatment and outreach prevention activities,are urgently needed.
The study was funded in part by the project "Appui à lalutte
contre le sida en Afrique de l’ouest" executed byCCISD Inc
and funded by CIDA Canada. HIV-1 urine EIA and westernblot
diagnostic kits were donated by Calypte Biomedical Corporation,USA. We appreciate the help from our field workers MargueriteKpikpitse and Ibrahim Camara. We thank female sex workers fortheir collaboration and bar/brothel owners for accepting uson site and for assistance in recruitment. Finally, we acknowledgethe contribution of Sylvie Deslandes for laboratory analyses.
MA was a co-principal investigator, was responsiblefor the
data analyses related to this article and was the mainwriter
of the manuscript; CML was a co-principal investigatorand
contributed to data analysis and to the writing of the manuscript;LMT contributed to data analysis and to the writing of the
manuscript;CABG was responsible for data collection in the
field and contributedto data analyses; EB, NG, and PJ
contributed to the data collection;EF was responsible for
the laboratory tests carried out in Cotonou;FB and JRJ were
responsible for the laboratory tests for chlamydialand
gonococcal infections; EF was responsible for the PCR testing
for trichomonas. EB and SA were the local co-investigators andcontributed to the organisation and implementation of the study.All authors contributed to the interpretation of the data andreviewed and commented the manuscript.
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