Rapid Syphilis Testing Uptake for Female Sex Workers at

Sex Venues in Southern China: Implications for

Expanding Syphilis Screening
Xiang-Sheng Chen
1
*, Yue-Ping Yin
1
, Crystal Shen
1,2
, Guo-Gu Liu
3
, Zheng-Jun Zhu
4
, Wan-Hui Wei
1
, Hong-
Chun Wang
1
, Shui-Jie Huang
4
, Jing Li
1
, Joseph D. Tucker
5
, David C. Mabey
6
, Rosanna W. Peeling
6
1National Center for Sexually Translated Disease (STD) Control and Chinese Academy of Medical Sciences Institute of Dermatology, Nanjing, China, 2Mayo Medical
School, Rochester, New York, United States of America, 3Health Bureau of Liuzhou City, Liuzhou, China, 4Jiangmen Center for STD Control, Jiangmen, China, 5University
of North Carolina School of Medicine, Chapel Hill, North Carolina, United States of America, 6London School of Hygiene and Tropical Medicine, London, United Kingdom
Abstract
Background: Accessibility of syphilis testing services is critical in syphilis control programs for female sex workers (FSWs),
but few FSWs attend public STI clinics or other testing sites. Introduction of free rapid syphilis testing (RST) into outreach
programs for FSWs will help improve test uptake.
Methods: Commercial sex venues were identified in two cities in South China. In cooperation with health advocacy
organizations, health outreach teams from local public health or medical facilities approached all types of sex venues in
study areas to offer free RST. Acceptability and uptake of RST among FSWs were evaluated.
Results: A total of 2812 FSWs were offered RST and 2670 (95.0%) accepted syphilis testing. 182 (6.8%) FSWs had a positive
RST result among whom 136 (74.7%) were willing to attend an STD clinic for confirmatory testing and treatment. More than
half (89, 66.4%) of those with syphilis were not willing to notify their sex partners. Multivariate logistic analysis showed that
syphilis test uptake was associated with residing in Jiangmen (AOR, 1.78; 95% CI, 1.152.77), older age (AOR, 2.11, 95% CI,
1.173.79 for age of 31 years or above), and not working at a service venue (AOR, 1.60; 95% CI, 1.102.34).
Conclusions: RST at sex venues is well accepted by FSWs when it is integrated into ongoing outreach services. Such
programs provide excellent opportunities for expanding syphilis screening efforts among specific subgroups of FSW who
are difficult to reach through clinic-based programs.
Citation: Chen X-S, Yin Y-P, Shen C, Liu G-G, Zhu Z-J, et al. (2012) Rapid Syphilis Testing Uptake for Female Sex Workers at Sex Venues in Southern China:
Implications for Expanding Syphilis Screening. PLoS ONE 7(12): e52579. doi:10.1371/journal.pone.0052579
Editor: Michelle Louise Gatton, The Queensland Institute of Medical Research, Australia
Received August 29, 2012; Accepted November 20, 2012; Published December 27, 2012
Copyright: 2012 Chen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by a grant to principal investigator XS Chen from the Rapid Syphilis Test Introduction Project (UNICEF/UNDP/World Bank/
WHO Special Programme for Research and Training in Tropical Diseases A70577 through a grant from the Bill and Melinda Gates Foundation), the UNC Fogarty
AIDS International Research and Training Program (NIH FIC D43 TW01039), and the UNC Center for AIDS Research. The funders had no role in study design, data
collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: [email protected]
Introduction
Female sex workers (FSWs) in South China have a high
prevalence of syphilis and an increasing burden of sexually
transmitted HIV infection [14]. A multi-site survey in China
indicates an overall syphilis prevalence of 5.0% among female sex
workers (FSWs) but the rates vary significantly among women
from different sex work venues [5]. Chinas most recent national
HIV report revealed that HIV cases are increasing among several
subgroups of FSWs [6]. Now more than half of all new HIV
infections in China are sexually transmitted [7], which has been
supported by several molecular epidemiology studies [810].
Expanding routine STD/HIV testing among Chinas six million
FSWs is an important public health priority [11], but implement-
ing clinic-based STD/HIV screening among FSWs has been
challenging [12]. Most FSWs do not attend public STD clinics, or
the voluntary testing and counseling (VCT) sites where they can
receive free syphilis and HIV testing [13,14]. FSWs in China may
not be aware of their risk of syphilis infection because there are not
any specific syphilis screening programs for this population,
mistrust of local public health STD clinics about confidentiality
and privacy protection, or fear of social stigma and condemnation
[15].
On-site syphilis screening using rapid syphilis tests (RSTs) is a
potential solution since such simple, rapid, and reliable tests are
commercially available [16]. RSTs have been used among FSWs
in a number of clinical settings [16,17], but few studies have
reported the use of RST among FSWs at sex venues [18]. Since
many FSWs in China do not attend standardized clinics where
syphilis testing is available, on-site testing assumes greater potential
importance for a community-based approach to testing. The
primary goal of this study was to determine RST uptake among
FSWs at sex venues in South China.
PLOS ONE | www.plosone.org 1 December 2012 | Volume 7 | Issue 12 | e52579
Methods
Study sites
A cross-sectional study was conducted with integration into
FSW outreach services at sex work venues in two cities in Southern
China provinces (Jiangmen in Guangdong and Liuzhou in
Guangxi) during AprilAugust 2009. These two cities were
selected to serve as a pilot based on local capacity and the
availability of ongoing public health outreach programs focused on
FSWs. Prior to this study, the local public health unit identified
sex-work venues in each study site. The venues were mapped and
selected for recruiting a convenience sample of FSWs for a survey.
Study participants
FSWs, aged sixteen and older, who were willing to provide
verbal informed consent were eligible to participate in the study.
For the purposes of this study, only women who had sold sex in the
past six months were eligible. Sex-work venues where FSWs
solicited clients were categorized into three types, i.e., entertain-
ment venues including karaoke bars, and hotels; service venues
including hair salons or barber shops, massage parlors, foot
bathing shops, roadside shops, guesthouses, or roadside restau-
rants; and street-walking venues including streets or public
outdoor places.
Survey design
The survey consisted of a structured questionnaire interview
and on-site testing with RST. The questionnaire survey contained
24 items related to socio-demographics, sexual behaviors, willing-
ness to be tested for syphilis, willingness to follow-up at an STD
clinic, and willingness to engage in partner notification. The
survey was developed in collaboration with a World Health
Organization (WHO)-supported project based on discussions with
local STD physicians, outreach workers, policy makers, and
national syphilis experts.
Study implementation
Each of the two cities has an FSW outreach team composed of
medical professionals (nurses and/or physicians), and public health
staff. FSW outreach programs include regular visits to FSW
settings to conduct condom promotion, sexual health education,
and risk reduction counseling developed according to the national
guidelines. Free RST was integrated into these routine outreach
services for this pilot study. A total of 218 and 101 venues
including walking stands on the streets were reached in Liuzhou
and Jiangmen, respectively. Most of the accessed venues accepted
the services. As part of this pilot project, the free syphilis testing
was offered to all FSWs at sex venues visited by the public health
outreach programs. Data regarding sex venues unwilling to
participate in the outreach services programs were not collected
as part of this investigation. During public health services, eligible
participants were taken to a separate, enclosed room to conduct a
questionnaire interview and discuss syphilis testing following
informed consent. Those who were willing to be tested had whole
blood or finger prick blood collected for on-site RST.
Laboratory testing, clinical diagnosis and treatment
procedures
The commercially available treponemal tests (Wantai anti-TP
Antibody Rapid Test, Wantai Biological Pharmaceutical Co., Ltd,
Beijing, China) were applied as the RST. Using a standard
treponemal test (Treponema pallidum particle agglutination, TPPA)
as reference standard, the sensitivity and specificity of the RST
were 95.1% and 95.8%, respectively (Yin YP, unpublished data).
The outreach team members were responsible for conducting
tests, interpreting the test results, and informing the FSWs of test
results on site. Confidentiality of testing results was ensured when
the FSWs were informed of their results. All FSWs with positive
RST were referred by an outreach team member to designated
STD clinics for further diagnosis and treatment according to the
national guidelines. In addition, health education and counseling,
condom promotion, and partner notification services were
provided in the STD clinics. All of the positive specimens and
10% of the negative specimens were sent back to the National
Center for Sexually Transmitted Disease Control (NCSTD) in
Nanjing for quality control assurance.
Statistical analyses
The primary outcome of this study was the uptake of syphilis
screening, defined by participating in the RST and having the
testing result. The secondary outcomes included testing prefer-
ences, , willingness to follow up at clinic for confirmatory testing
and treatment, and willingness to notify sex partners. To
determine univariate relationships, chi-squared (x
2
) values and
unadjusted odds ratio (ORs) with 95% confidence intervals (CIs)
were calculated. The variables associated with p,0.10 in
univariate analysis were included in the multivariate logistic
regression analysis. The final model included variables at level of
p#0.05. Adjusted odds ratios (AOR), with 95% CIs, were
calculated. All statistical analyses were performed using SPSS
(version 13.0, Chicago, IL) software.
Ethical review
This study was approved by the Medical Ethics Committee of
the Chinese Academy of Medical Sciences Institute of Dermatol-
ogy and the NCSTD in Nanjing. A verbal informed consent was
obtained from all subjects who agreed to participate in the study.
Results
A total of 2812 women enrolled in this study. Most FSWs were
younger than 29 years old, had less than or equal to five sex
partners in the previous week, and had no history of prior syphilis
infection. Our sample of FSWs included women employed in a
variety of sex venues, including 1495 (53.2%), 1156 (41.1%) and
161 (5.7%) from entertainment, service and street-walking venues,
respectively. Among 2536 women who responded to question
about history of syphilis, 58 (2.3%) had previous syphilis infection.
Among those who responded to question of treatment history,
87.4% had the infection treated.
Of the 2812 female sex workers who were offered on-site RST,
2670 accepted testing, giving an overall test uptake rate of 95.0%
(95% CI, 94.195.7%). Among 2689 FSWs who were willing to
get a syphilis testing, 2670 (99.3%, 95% CI 98.999.5%) finally got
the test. Univariate analysis identified the factors positively
correlated with RST uptake, including residing in Jiangmen
(OR, 1.97; 95% CI, 1.312.97), age of 31 years old or above (OR,
1.79; 95% CI, 1.113.15), and not working in a service venue
(OR, 1.55; 95% CI, 1.102.19). There were not significant
differences between women who took test and who were willing
but did not take in terms of age, and types of venues. As shown in
Table 1, multivariate analysis showed the following factors
associated with RST uptake: residing in Jiangmen (AOR, 1.78;
95% CI, 1.152.76; P=0.01), being age of 31 years old or above
(AOR, 1.90; 95% CI, 1.023.52; P =0.04), and not working at a
service venue (AOR, 1.53; 95% CI, 1.042.26; P=0.03). The
following factors were associated with preference of verbal
Rapid Syphilis Testing among Female Sex Workers
PLOS ONE | www.plosone.org 2 December 2012 | Volume 7 | Issue 12 | e52579
notification of RST results: residing in Liuzhou (AOR, 4.87; 95%
CI, 3.826.19; P,0.001), working on the street (AOR, 4.14; 95%
CI, 2.437.06, p,0.001) or at a service venue (AOR, 2.01; 95%
CI, 1.552.59, p,0.001), and willingness to get RST results
immediately on site (AOR, 132.80; 95% CI, 18.34961.48,
P,0.001) The following factors were associated with preference
of finger prick blood collection: residing in Jiangmen (AOR, 3.37;
95% CI, 2.714.18, P,0.001).
A total of 2689 (95.6%) women reported willingness to receive a
syphilis test (Table 2). The finger prick method of collecting blood
for testing was preferred compared to the standard venous blood
draws. Nearly 60% of women reported pain as the reason for not
wanting finger-prick blood collection. Most participants preferred
being verbally notified of their test results at either the sex venue
site (52.5%) or via cell phone (47.0%).
Of the FSWs who were tested for syphilis with an on-site RST,
182 (6.8%) had a positive result. Of those with positive RST
results, 136 (74.7%) were willing to attend an STD clinic for
further confirmatory testing and treatment (Table 3). However,
most FSWs (66.4%) with positive RST results were not willing to
notify their sexual partners. Among those participants, not being
in contact with their sex partner was the most frequent reason
provided for their unwillingness to contact their partner (Table 3).
Discussion
Syphilis control programs among FSWs in China are crucial
because they have a higher incidence of syphilis and are one of the
most-at-risk populations for acquisition and transmission of
syphilis and HIV. However, reaching the FSW population,
especially certain subgroups, presents various challenges including
structural barriers hindering access to care as well as patients
distrust of public clinics [13,14]. Venue-based introduction of RST
can expand testing among these difficult-to-reach FSW subgroups.
To our knowledge, this is the first study in China to examine the
feasibility of introducing community-based RST among sex
workers. A highlight of this study is its diversity of venues,
particularly its ability to reach marginalized FSW venues. This
study reached women in vulnerable subsets of FSW that are not
often included in the current intervention programs for FSWs,
such as street-based FSWs or those at massage, sauna and other
services venues.
Table 1. Multivariate Model Predicting Rapid Syphilis Test (RST) Uptake and Preferences Regarding RST Among FSWs.
Variable
RST uptake
Preference of verbal
notification of RST results
Preference of finger prick
blood collection
AOR (95% CI) P value AOR (95% CI) P value AOR (95% CI) P value
Site city
Liuzhou Reference 4.87 (3.826.19) ,0.001 Reference
Jiangmen 1.78 (1.152.76) 0.01 Reference 3.37 (2.714.18) ,0.001
Age group (years old)
20 or below Reference
2125 1.05 (0.701.58) 0.82
2630 1.59 (0.912.78) 0.10
31 or above 1.90 (1.023.52) 0.04
Type of sex work venue
Street venue 3.10 (0.7213.36) 0.13 4.14 (2.437.06) ,0.001
Service venue Reference 2.01 (1.552.59) ,0.001
Entertainment venue 1.53 (1.042.26) 0.03 Reference
Willingness to get RST results now (on site)
Yes 132.80 (18.34
961.48)
,0.001 17.95 (10.16
31.69)
,0.001
No Reference Reference
FSWs: female sex workers; AOR: adjusted odds ratio; CI: confidence interval.
doi:10.1371/journal.pone.0052579.t001
Table 2. Preferences Regarding Rapid Syphilis Testing
Among FSWs.
Variable Number (%)
Reports willing to receive syphilis test (n =2805)
Yes 2689 (95.6)
No 116 (4.1)
RST Collection Preference (n =2689)
Prefer finger prick 1859 (66.1)
Prefer blood draw 830 (29.5)
Reason unwilling to finger prick (n =326)
More pain 188 (57.7)
Afraid of infection 61 (18.7)
Affect work 73 (22.4)
Concern of inaccuracy 4 (1.2)
Preferred method of RST result notification (n =1651)
Verbal Onsite (sex work venue) 866 (52.5%)
Cellphone 776 (47.0%)
Clinic and Others 9 (0.05%)
FSWs: female sex workers.
doi:10.1371/journal.pone.0052579.t002
Rapid Syphilis Testing among Female Sex Workers
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In this study, FSWs had a high overall RST uptake rate (95.1%),
which is higher than 57.1% among FSWs in a previous RST study
in India [17], or 81.6% among patients at STD clinics a previous
study in China [19]. The high up-take rate in our study population
is mainly because the RST screening service was integrated into
the pre-existing routine FSW outreach services, especially at
entertainment venues. Uptake was relatively consistent across
venues (and greater than 90%), which reveals the benefit of RST
in expanding the reach of testing into those street-walking venues
which are usually less covered by the current STD/HIV
intervention programs in China. The uptake was also excellent
across age ranges, particularly in the older age range who engage
in riskier behaviors [2], which is also encouraging as an
implication for using RST to expand access to testing.
Correlates of test uptake included delivering RSTs in Jiangmen,
older age and not working service venue types. Difference in RST
uptake between the two study sites may result from their difference
in outreach providers which were the STD clinic outreach teams
in Jiangmen but reproductive health hospital or center for disease
control outreach teams in Liuzhou. Older FSWs of age 31 years
old or above were more than two times as likely to undergo testing.
This is consistent with a study of FSWs in China that showed older
age associated with increased rates of HIV testing [20]. Older
FSWs may have a better perception of risk of infection due to
longer history of working as sex workers. FSWs from entertain-
ment or street venues were nearly twice as likely to undergo testing
(OR: 1.53, 95% CI: 1.042.26). This finding is also consistent with
a study of FSWs in China that showed higher tier FSW venues
with increased rates of HIV testing [20]. The difference in RST
uptake between the FSWs from entertainment- and service-based
venues may be related to the higher education background among
those in entertainment settings [21]. However, those FSWs who
solicited clients on streets are usually poor and marginalized by
society and intervention programs. Compared with distribution of
health education materials and promotion of condoms, health
services including syphilis testing and other reproductive health
services are usually more welcome by this population. The relative
low-uptake among FSWs in service venues may be due to the lack
of trust between these FSWs and the outreach teams. FSWs from
service venues typically have decreased opportunities and funds to
seek health care, thus may be more likely to utilize an opportunity
for free healthcare at their venue.
A high overall willingness to test was stated by FSWs, revealing
widespread desire for testing. Of the 6.8% of tested FSWs with
positive rapid test results, the majority were willing to go to a STD
clinic for confirmation of infection and treatment. The 74.7% rate
is slightly higher than a general willingness to attend clinic rate
from a previous FSW study in Northern China [13]. Rapid tests
can improve clinic attendance due to reaching more FSWs
through community-based testing leading to increased subsequent
clinic follow-up as FSWs realize the need for care.
FSWs with syphilis were largely unwilling to notify partners.
Lack of contact is the most often stated reason, likely due to the
often transient nature of client interactions leading to decreased
ability for further contact. Although studies have been performed
on partner notification in developing countries and China [22
24], there is little research on partner notification with FSWs [24].
The 33.6% partner notification willingness rate is consistent with
operational studies of partner notification rates in China [22].
However, there are likely differences between the stated willing-
ness for notification and actual notification rate. Developing
effective partner notification strategies to overcome these contact
challenges could help reduce syphilis transmission.
This study has several limitations. As both study sites are in
South China, generalizations to other regions should be made with
caution. However, Guangdong Province attracts migrant workers
from all over China, and there is much demographic diversity in
the study area. The study recruited a convenience sample of
FSWs, likely resulting in the sample bias. Also, the rapid syphilis
tests have certain limitations as a screening method, particularly
among populations with a high prevalence of previous syphilis
infection. Hence a positive rapid test result requires a clinic visit for
confirmation of syphilis infection. This aspect can be inconvenient
and create a barrier for patients [25]. Also, lower sensitivity has
been reported with use of point of care rapid syphilis tests [17,18].
However, the rapid syphilis test has shown overall benefit in
improved detection of syphilis, especially in hardto-reach
populations that have not been previously tested and treated
[17,18]. Difficulties may also arise from large-scale implementa-
tion of venue-based testing. Evening testing is optimal for reaching
many FSWs, but finding outreach workers willing to perform
testing during atypical times can be challenging. Despite these
limitations, RST has potential as a tool to reach FSWs. A large
seven-country study found high acceptability and feasibility for
RST among pregnant women in a range of low and middle
income settings [26].
Improved rapid syphilis tests are showing promise. A novel
point-of-care (POC) syphilis test for the dual detection of
nontreponemal and treponemal antibodies has been developed
[27]. Screening and confirmatory diagnosis would occur through
the same test, reducing the need for clinic visits for confirmatory
diagnosis and likely increasing treatment rates. A laboratory-based
evaluation of the dual POC has been conducted in multiple sites in
China and shown a good performance in sensitivity and specificity
Table 3. Follow Up Preferences Among FSWs with RST
Positive Results.
Variable
Overall n
(%)
RST result (n =2670)
Negative 2488 (93.2)
Positive 182 (6.8)
Willing to STD clinic for confirm & treatment (n =182)
Yes 136 (74.7)
No 46 (25.3)
Preferred time to attend STI clinic (n =138)
Today 38 (27.5)
Tomorrow 26 (18.8)
Two days later 10 (7.3)
One week later 2 (1.5)
When have time 62 (44.9)
Willing to notify sex partner (n =134)
Yes 45 (33.6)
No 89 (66.4)
Reason for not willing to notify sex partner (n =55)
Fear of his response 8 (14.6)
Not in contact 25 (45.5)
Separated/divorced 4 (7.3)
Trust him 12 (21.8)
Other 6 (10.9)
doi:10.1371/journal.pone.0052579.t003
Rapid Syphilis Testing among Female Sex Workers
PLOS ONE | www.plosone.org 4 December 2012 | Volume 7 | Issue 12 | e52579
as compared with TPPA and TRUST, particularly among
specimens with high titer of TRUST [28]. As diagnostic
technology continues to advance, the potential for improving
syphilis control through rapid syphilis testing continues to grow.
In conclusion, rapid syphilis tests showed high uptake among
FSWs in South China. Implementing rapid syphilis testing in sex
venues would expand testing among this high risk population,
including the subgroup of FSWs on the streets that are more
difficult to reach. Rapid syphilis testing would be one important
method of improving access to testing and to care within these
subgroups, and could play an important role in syphilis control in
this high-risk population.
Acknowledgments
The authors would like to thank the staff who worked in the study sites for
their recruiting the participants, conducting the rapid syphilis testing, and
collecting study data. We are also very grateful to all FSWs participating in
this study for their cooperation.
Author Contributions
Conceived and designed the experiments: XSC YPY DCM RWP.
Performed the experiments: XSC YPY GGL ZJZ WHW HCW SJH.
Analyzed the data: XSC CS JL. Wrote the paper: XSC CS JDT.
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