AIDS Behav DOI 10.1007/s10461-014-0791-2
ORIGINAL PAPER
Chlamydia Prevalence and Associated Behaviours Among Female Sex Workers in Vanuatu: Results from an Integrated Bio-behavioural Survey, 2011 Caroline van Gemert • Mark Stoove • Tamara Kwarteng • Siula Bulu Isabel Bergeri • Ian Wanyeki • Steve Badman • Jayline Malverus • Alyce Vella • Len Tarivonda • Lisa Grazina Johnston
•
Ó Springer Science+Business Media New York 2014
Abstract There is insufficient data on sexually transmitted infections (STI) and related behaviours among key populations, including female sex workers (FSW), in the Pacific region. Using respondent driven sampling, we conducted an integrated bio-behavioural survey with FSW in Vanuatu (aged C18 years) to investigate risk behaviours associations with Chlamydia trachomatis (CT). Weighted population estimates and correlates of CT infection were calculated. Among 149 FSW, prevalence of CT was 36 % (95 % CI 26–48 %). Few FSW reported consistent condom use with recent transactional sex partners (TSP) (8 %; 95 % CI 2–13 %). CT infection was positively associated with increasing number of TSP (adjusted odds ratio [AOR] 1.1; 95 % CI 1.0–1.2) and group sex (AOR 2.9; 95 % CI 1.1–8.2). CT was negatively associated with increasing age of first sex (AOR 0.6; 95 % CI 0.5–0.9) and previous STI treatment (AOR 0.1; 95 % CI 0.0–0.4). A comprehensive public health strategy for prevention and treatment of STI among FSW, incorporating community empowerment strategies, FSW-targeted health services and periodic presumptive treatment, is urgently needed in Vanuatu. C. van Gemert (&) M. Stoove I. Bergeri A. Vella Centre for Population Health, Burnet Institute, GPO Box 2284, Melbourne, VIC 3001, Australia e-mail: [email protected] T. Kwarteng Centre for International Health, Burnet Institute, Melbourne, VIC, Australia
Keywords Integrated bio-behavioural survey Female sex workers Chlamydia Pacific Risk behaviours
Introduction The prevalence of sexually transmitted infections (STI), particularly Chlamydia trachomatis (CT), are among the highest globally in the 22 Pacific Island Countries and Territories (PICT) [1]. Surveillance data from women attending antenatal care services in Fiji, Kiribati, Samoa, Solomon Islands, Tonga and Vanuatu between 2004 and 2005 found an overall CT prevalence of 18 %; prevalence was higher among women aged B24 years (26 %) [2]. Prevalence studies and routine testing data support these findings, with CT positivity as high as 29 % among women attending antenatal care services [1]. In Vanuatu (2009 population 234,023 [3]), routine annual testing data shows CT positivity ranging between 19 and 22 % [4]. In comparison, World Health Organization estimates of CT prevalence among women in 2008 were 2.6 % in the African Region, 7.6 % in the Region of the Americas and S. Badman Kirby Institute, University of New South Wales, Sydney, NSW, Australia L. Tarivonda Department of Public Health, Ministry of Health, Port Vila, Vanuatu
S. Bulu J. Malverus Wan Smolbag Theatre, Port Vila, Vanuatu
L. G. Johnston School of International Public Health and Tropical Medicine, Tulane University, New Orleans, LA, USA
I. Wanyeki Secretariat of the Pacific Community, Noumea, New Caledonia, France
L. G. Johnston Global Health Sciences, University of California, San Francisco, San Francisco, USA
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1.1 % in the South-East Asia Region [5]. Adverse outcomes of untreated CT include cervicitis, endometriosis and infertility and 10–40 % of women with untreated CT infection develop symptomatic pelvic inflammatory disease; [6, 7] therefore, timely detection, treatment and prevention of onward transmission is paramount. Despite endemic levels of STI across the region, passive surveillance data suggest HIV prevalence is low in all PICT excluding Papua New Guinea (PNG); however, HIV prevalence is likely underestimated due to low testing rates [8–10]. Limited testing may be a result of fear of HIVrelated stigma and discrimination, concerns regarding confidentiality of test results in smaller countries and communities, as well as lack of access to, and uptake of, HIV testing and counselling, particularly in rural or geographically isolated areas and among key populations at increased risk of HIV and other STI [10, 11]. Further, epidemiological surveillance systems are lacking in the region to monitor HIV and STI among key populations; as a result, limited data exist on key populations, including female sex workers (FSW) [9]. PICT are therefore unable to determine who is at risk of HIV infection and how to target appropriate prevention strategies. In the absence of quality surveillance data, targeted Integrated Bio-Behavioural Surveys (IBBS) among key populations are needed to assess burden of disease, monitor risky behaviours, and identify populations for targeted interventions. IBBS link HIV and other STI testing data to behavioural data collected through a structured questionnaire that explores risky behaviours and practices. A 2012 IBBS in Fiji among FSW is the only recent IBBS conducted among FSW in the region; this study reported an overall CT prevalence of 22 %; however socio-demographic and behavioural variables significantly associated with CT infection were not presented and reported findings therefore have limited utility to monitor risky behaviours and practices and inform prevention initiatives [12]. In Vanuatu, data for FSW are limited to a 2007 behavioural surveillance survey (BSS) and a 2011 qualitative study; both reported inconsistent condom use with paying and non-paying partners and low HIV testing rates [8, 13]. To date, there are no recent studies presenting STI prevalence alongside behavioural correlates of infection among FSW in Vanuatu or other PICT. In 2011, the Burnet Institute, in partnership with the non-governmental organisation, Wan Smolbag, and the Vanuatu Ministry of Health, conducted an IBBS among FSW in Port Vila, the capital of Vanuatu (2009 population: 44,040 [3] ), to measure HIV and other STI prevalence and identify risk factors. This paper presents the prevalence of CT and other STI and associated socio-demographic and behavioural predictors of CT infection among FSW.
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Methods Study Design, Sampling and Recruitment This cross-sectional study was guided by surveillance tools developed by Family Health International, WHO and UNAIDS [14, 15]. Participants were recruited between September and November 2011 using respondent driven sampling (RDS), a link-tracing sampling technique whereby participants recruit new participants from their peer network [16]. RDS allows for the anonymous and confidential recruitment of hidden and socially networked populations [14, 17]. In RDS, participants provide information on their social network size to establish relative probabilities of recruitment and RDS analysis techniques mitigate common biases found in link tracing sampling methods [16]. Eligible FSW included females exchanging sex (vaginal, anal or oral) for money, goods or favours (defined as transactional sex) in the previous year, C18 years, and living in or near Port Vila. The sample size was calculated for 244 respondents based on an estimated HIV prevalence of 3 %, a population correction fraction (FSW population size estimated as 1,000), confidence of 95 %, power of 80 %, a non-response rate of 0.2 and a design effect of 2.0. The final estimated sample size was rounded up to 250. Sampling began with seven seeds (initial recruits), identified through key contacts. Seeds were selected purposively for their close links with the study population and for diversity of individual attributes (such as age, marital status, type of sex work, geographical location). Seeds were given three recruitment coupons to recruit the first wave of participants. Subsequent participants received three recruitment coupons. Participants received the equivalent of AUD$15 for participating in the survey, AUD$5 for each peer recruited (a maximum of three peers could be recruited), and AUD$5 for returning to receive test results. Data Collection Three trained female field researchers assessed eligibility and obtained informed written consent. Intervieweradministered interviews were conducted at Wan Smolbag in Bislama (an official language of Vanuatu), consisting of a questionnaire incorporating items about socio-demographic characteristics and sexual risk behaviours. The questionnaire was piloted with FSW and modified for clarity based on field researchers and pilot participants feedback. For RDS analysis, FSW were asked about their social network size including the number of FSW they know and who know them, seen in the previous month and who meet study eligibility. Following pre-test counselling, a trained nurse at Kam Pussum Hed (KPH) Clinic, a reproductive
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health clinic managed by Wan Smolbag, collected a total of 20 ml of venous blood for HIV and syphilis testing and vaginal swabs for CT and Neisseria gonorrhoea (NG) testing. Vaginal swabs were tested for CT and NG with BD ProbeTec nucleic acid amplification testing. Active syphilis was detected with an RPR screening test and confirmation of reactive samples by DetermineTM Syphilis TP. HIV was detected using the recommended HIV testing algorithm validated for PICT [18] (a rapid screening test [Determine] with confirmation of reactive samples by two additional rapid tests [Insti and Unigold]). All testing was conducted at the Port Vila Central Hospital; the national laboratory is the only place with staff currently trained to provide HIV point of care tests and also conducts all diagnostic testing for the KPH Clinic. FSW were asked to return to receive post-test counselling and test results within four weeks following participation; positive cases received treatment and/or were referred for further management through the public primary health care system. To facilitate confidentiality, coupons, questionnaires, specimens, and test results were linked using a unique study identification number. Measures This analysis explores several socio-demographic and sexual behaviour measures and associations with CT infection among FSW [19]. The majority of measures included in this analysis are dichotomous (yes/no, or two-category age groups or time periods) or categorical. Consistent condom use defined as always using a condom with transactional sex partners (TSP) or non-TSP during the previous month. Multiple responses were permitted to describe the reason why a condom was not used at last sex with a TSP or non-TSP and genital symptoms experienced in the last 12 months (including genital discharge, genital ulcer or sore, burning or sharp pain on urination, and rash or general itching); these were then re-categorised as a binary variable. Open ended responses were used to collect information on goods or favours received at last transactional sex; these were then categorised as clothing, food, drugs or alcohol, or other. Additional measures are numerical; the median age, duration or number and interquartile range (IQR) were calculated as appropriate for several measures, including age of first sex, age of first transactional sex, duration of transactional sex work (calculated as current age–age of first transactional sex), unique number of TSP in the previous week and unique number of non-TSP during the previous year. Data Analysis Population estimates (%) and 95 % confidence intervals (CI) were calculated with RDS-Analyst version 9.0 (www.
hpmrg.org) using the successive sampling estimator with apriori mid-range population size estimate set at 1,390 [20, 21]. Univariate and multivariate logistic regression identified statistically significant (p \ 0.1) correlates of CT infection using RDS-Analyst-generated survey weights, also using the successive sampling estimator. Multivariate logistic regression using reverse stepwise selection procedures were used whereby non-significant candidate predictors were removed sequentially until only significant predictors (p \ 0.1) remained. Age, age of first sex, age first transacted sex and the number of TSP and non-TSP in the previous week were treated as continuous variables; the remainder were categorised as above. Missing data were included as a category as appropriate in logistic regressions; OR and AOR are not presented for these. Weighted statistical analyses were conducted using STATA version 11 (Stata Statistical Software: Release 11, StataCorp LP, TX, College Station, 2009). Ethical Approval The Ministry of Health, Government of the Republic of Vanuatu Ethics Committee and Alfred Hospital Ethics Committee approved this study.
Results Data were analysed from 149 FSW, after excluding two nonproductive seeds and two ineligible participants; ineligible participants included one participant who identified as male and one who had not transacted sex in the previous 12 months. The maximum recruitment chain was six waves. Almost half (47.1 %; 95 % CI 35.7–58.4 %) were aged 20–29 years (median age = 24 years, IQR = 22–26 years) and most reported completing secondary education (59.5 %; 95 % CI 50.0–69.0 %), never being married (68.8 %; 95 % CI 60.8–76.8 %), and having additional sources of income (75.8 %; 95 % CI 66.8–84.7 %). The most commonly reported setting for additional income was at a shop or market stall (62.2 %; 95 % CI 51.2–73.0 %, Table 1). Vaginal swab results for CT and NG testing were available for 137 participants. Of the 12 FSW for whom results were not available, four FSW did not provide specimens and eight results were missing. Blood test results for HIV and syphilis were available for 118 participants. Of the 31 FSW for whom blood test results were not available, 18 did not provide samples and 13 were missing. CT positivity among FSW was 36.7 % (95 % CI 25.6–47.9 %), NG 17.1 % (95 % CI 10.2–23.9 %), and syphilis 3.7 % (95 % CI 0.3–7.1 %, and 11.1 % (95 % CI 3.3–18.9 %) were CT and NG co-infected (Table 2). HIV seropositivity was not detected among FSW.
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Three-quarters of all FSW (76.0 %; 95 % CI 67.6–84.4 %) reported genital STI symptoms in the previous year, however less than half (38.7 %; 95 % CI 29.2–48.3 %) sought treatment. Among those who sought treatment, most (56.7 %; 95 % CI 33.0–80.3 %) attended the public hospital and one-third (34.5 %; 95 % CI 9.7–59.3 %) attended the KPH clinic. Almost half of FSW who did not seek treatment (44.7 %; 95 % CI 30.0–59.4 %) reported being too scared to seek treatment.
Table 1 Weighted population estimates and confidence intervals (CI) for demographic variables among female sex workers (n = 149), Vanuatu, 2011
Agea 18–19 years 20–29 years
n (median)
Population estimate % (IQRf)
(24) 30
(22–26) 26.2
72
47.1
95 % CI
35.7, 58.4
31
17.1
9.6, 24.5
40? years
14
9.7
3.3, 16.1
Highest level of education Some or all primary
2
1.6
0.1, 3.2
Secondary
86
59.5
50.0, 69.0
61
38.8
Table 2 Weighted population estimates and confidence intervals (CI) for STI history, symptoms and prevalence among female sex workers (n = 149), Vanuatu, 2011 n
13.8, 38.6
30–39 years
Higher
The majority of FSW reported their age of first sex as \18 years (68.3 %; 95 % CI 58.1–78.4 %; median = 16, IQR = 16–17), age of first transactional sex [18 years (61.3 %; 95 % CI 50.3–72.1 %; median = 19, IQR = 18–19) and duration of transactional sex work [one year (80.9 %, 95 % CI 72.4–89.4 %; median = 4, IQR = 3–5) (Table 3). Nearly all (87.4 %; 95 % CI 80.7–94.1 %) transacted sex in the previous week; most (70.5 %; 95 % CI 59.0–82.0 %) reported receiving both money and goods, 22.7 % (95 % CI 11.5–34.0 %) received money only and 6.8 % (95 % CI 1.4–12.1 %) received goods only. Among FSW that reported TSP during the previous week, the median total number of unique TSP was three (IQR 3–4). The most common goods received during
30.0, 48.0
100
Currently or previously married
49
68.8 31.2
60.8, 76.8 23.2, 39.2
Has other income in addition to sex work Yes
Chlamydiaa Gonorrheaa
Setting of additional income Shop or market stallb
a
36.7 17.1
25.6, 47.9 10.2, 23.9
4
3.7
0.3, 7.1
HIVa
0
–
–
Co-infectionsa Chlamydia and gonorrhoea
15
11.1
3.3, 18.9
Gonorrhoea and syphilis
1
1.8
-0.5, 4.1
Chlamydia and syphilis
1
0.4
0.2, 0.5
No
81
59.7
50.8, 68.6
Yes
68
40.3
31.4, 49.2
Prior STI
Had genital symptom/s in previous yearb Yes
116
76.0
67.6, 84.4
Had treatment for genital symptom/s in previous year No
60
61.3
50.5, 72.1
Yes 56 Place where treatment was soughta
38.7
29.2, 48.3
27
56.7
33.0, 80.3
22
34.5
9.7, 59.3
6
8.8
0.1, 17.5
75.8
66.8, 84.7
68
62.2
51.2, 73.0
Hospital KPH clinic Otherb
Otherc
26
22.2,
10.9, 33.4
Informald
14
6.5
1.9, 11.2
Too scared
27
44.7
30.0, 59.4
Hospitalitye
7
9.0
2.0, 16.1
Other
18
26.9
13.0, 40.8
Too busy
4
10.7
1.7, 19.6
Too public
8
12.7
-0.6, 26.0
Too expensive
3
5.1
-0.6, 10.8
Reason why treatment was not sought
Missing values: Age (n = 2)
b
Shop or market stall includes shop assistant, selling food/produce at market, selling handicrafts
c
47 24
Syphilisa
115 b
95 % CI
STI prevalencea
Marital status Never been married
Population estimate (%)
Other income includes office work, peer education, hairstylist
d
Informal income includes massage, house girl, gardener, laundry services, car wash, and sewing
e
Hospitality income includes bartending, hostessing, working at a kava bar, hotel or guesthouse f Interquartile range
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a
Missing responses: Chlamydia and gonorrhoea test result (n = 8, 4 additional specimens not provided); HIV and syphilis test result (n = 13,18 additional specimens not provided); location where treatment was sought (n = 1) b
Other includes Vanuatu Family Health Association Clinic, private doctor, pharmacy or chemist, traditional healer
AIDS Behav Table 3 Weighted population estimates and confidence intervals (CI) for sexual risk behaviours with transactional and non-TSP among female sex workers (n = 149), Vanuatu, 2011
Age of first sex
N (median)
Population estimate % (IQRd)
(16)
(16–17)
95 % CI
\18 years
99
68.3
58.1, 78.4
18? years
50
31.7
21.6, 41.9
Age first sold/transacted sexa
(19)
(18–19)
\18 years
50
38.7
27.9, 49.7
18? years
98
61.3
50.3, 72.1
(4) 26
(3–5) 19.1
10.6, 27.6
121
80.9
72.4, 89.4
No
20
12.6
5.9, 19.3
Yes
129
87.4
80.7, 94.1
Duration of sex work/transactional sexa \1 year More than 1 year Had transactional sex partner (TSP) in previous week
Money and/or goods received during previous week Received both money and goods
94
70.5
59.0, 82.0
Received money only
28
22.7
11.5, 34.0
Received goods only
7
6.8
1.4, 12.1
Number of TSP from whom money was received
(2)
(2–2)
–
Number of TSP from whom goods were received
(2)
(2–2)
–
Total number of TSP
(3)
(3–4)
–
Number of TSP during the previous week, by goods/money received
Description of goods or favours received at last transactional sex among FSW that received goods during the previous weekb Clothing Food
58 24
62.6 18.6
50.6, 74.7 8.6, 28.5
Drugs or alcohol
21
18.3
10.3, 26.3
Other
14
11.1
4.8, 17.4
13
7.5
2.4, 12.5
No
79
55.9
45.6, 66.0
Yes
69
44.2
33.4, 55.0
Consistency of condom use with TSP during previous monthc Consistent Condom use at last sex with TSP
a
Reason for not using a condom at last sex with TSPb Client objected
55
65.1
52.4, 77.8
Used other contraceptive
16
17.2
7.6, 26.5
Not available
11
22.9
9.9, 3.6
Don’t like them
7
18.1
5.3, 30.9
Didn’t think of it
5
10.1
2.0, 18.1
Trusted partner
4
1.7
0.8, 2.6
Afraid Client paid more not to use
4 2
7.6 1.1
-1.0, 16.1 0.1, 2.1
Client looked healthy
1
0.8
-0.2, 1.9
Too drunk/high
1
0.4
-0.1, 0.1
Didn’t think it necessary
1
0.2
-0.0, 0.4
Had regular partners in the previous year
149
–
–
Number of regular non-TSP in the previous year
(4)
(3–4)
Had casual partners in the previous year
117
76.4
Number of casual non-TSP in the previous year
(3)
(2–3)
Total number of non-TSP in the previous year
(6)
(5–6)
Sexual risk behaviours with non-TSP
68.2, 84.5
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AIDS Behav Table 3 continued N (median)
Population estimate % (IQRd)
95 % CI
Used a condom at last sex with non-TSPa
43
37.5
19.6, 55.4
Consistent condom use with non-TSP during previous yeara
10
7.2
3.1, 11.4
Had group sex in previous yeara Used a condom during last group sex
59 27
37.6 55.3
26.6, 48.6 34.4, 76.2
Has ever been forced to have sexa
101
69.5
60.7, 78.4
Has had anal sex in the previous yeara
44
28.2
18.6, 37.9
Condom use at last anal sex
17
40.0
23.3, 56.6
a
Missing responses: Age first sold/transacted sex (n = 1); Duration of sex work/transactional sex (n = 2); Condom use at last sex with TSP (n = 1); Number of regular partners in previous year (n = 3), Number of casual partners in previous year (n = 1), Condom use with non-TSP— last sex and consistent condom use (n = 32), Had group sex in previous year (n = 2), Ever been forced to have sex (n = 1), Has had anal sex in the previous year (n = 7) b
Multiple responses permitted
c
Consistent condom use defined as always using a condom with TSP and non-TSP during the previous month
d
Interquartile range
Table 4 Predictors of chlamydial or gonorrhoeal infection among FSW with available Chlamydia test results (n = 137) in Vanuatu, 2011: Odds ratios (OR) and adjusted OR (AOR) with 95 % confidence intervals (CI) Chlamydia infection ORa
95 % CI
p value
0.9
0.9, 1.0
0.02
AORb
95 % CI
p value
0.6
0.5, 0.9
\0.01
1.1
1.0, 1.2
0.06
Demographic variables Age For each additional year Education level (reference group some or all primary) Secondary
1.3
0.5, 3.5
Higher than secondary
1.6
0.1, 27.9
0.5
0.2, 1.5
Married before (reference group no) Yes
Has other income in addition to sex work (reference group no) Yes
0.8
0.3, 2.4
0.7
0.5, 0.9
\0.01
0.9
0.8, 1.0
0.04
0.6
0.2, 2.0
6.9
0.8, 59.8
0.08
For each TSP from whom money was received
1.3
1.0, 1.8
0.08
For each TSP from whom goods were received
1.2
0.8, 1.7
For each TSP (total number)
1.2
1.0, 1.4
Sexual risk characteristics Age of first sex For each additional year Age first sold/transacted sex For each additional year Duration of sex work/transactional sex (ref. 1.11 year) More than one year Had TSP in the previous week (ref. no) Yes Number of TSP in previous week
Consistency of condom use with TSP during previous month (ref. inconsistent) Consistent
0.3
0.1, 1.5
1.1
0.4, 3.1
Condom use at last sex with TSP (ref. no) Yes
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0.06
AIDS Behav Table 4 continued Chlamydia infection ORa
95 % CI
p value
1.2
1.0, 1.4
0.05
AORb
95 % CI
p value
2.9
1.1, 8.2
0.04
0.1
0.0, 0.4
\0.01
Number of non-TSP in previous year For each regular non-TSP For each casual non-TSP
1.2
1.0, 1.5
0.02
For each non-TSP (total number)
1.1
1.0., 1.3
0.01
Consistency of condom use with non-TSP during previous month (ref. inconsistent) Consistent
0.9
0.2, 4.4
3.0
1.1, 7.6
1.4
0.3, 6.0
2.3
0.9, 6.4
1.2
0.4, 3.5
0.1
0.0, 0.9
0.4
0.1, 1.2
1.0
0.3, 3.3
0.2
0.1, 0.6
Group sex in previous year (ref. no) Yes
0.03
Used a condom during last group sex (ref. no) Yes Ever been forced to have sex (ref. no) Yes Anal sex in the previous year (ref. no) Yes Condom use at last anal sex (ref. no) Yes
0.03
Previous sexual health Ever had an STI (self-reported) (ref. no) Yes Had genital symptoms in previous year* (ref. no) Yes Had treatment for previous STI (ref. no) * Yes a
Odds ratio
b
Adjusted odds ratio
the previous week was clothing (62.6 %; 95 % CI 50.6–74.7 %). Consistent condom use with TSP during the previous month was low (7.5 %; 95 % CI 2.4–12.5 %). Fewer than half (44.2 %; 95 % CI 33.4–55.0 %) used a condom at last transactional sex; among FSW that did not use a condom at last transactional sex, the most common reason was client objection (65.1 %; 95 % CI 26.1–48.1 %). Nearly all FSW (n = 132, 90.2 %) reported their most recent TSP as being ni-Vanuatu (that is, from Vanuatu; not in table). The median total number of nonTSP during the previous year was six (IQR = 5–6). Consistent condom use with non-TSP during the previous year was low (7.2 %; 95 % CI 3.1–11.4 %). Over one-third (37.6 %; 95 % CI 26.6–48.6 %) of FSW reported having group sex in the previous year, of whom half (55.3 %; 95 % CI 34.4–76.2 %) reported using a condom during last group sex. Over two-thirds (69.7 %; 95 % CI 60.7–78.4 %) reported ever being forced to have sex. Over one-quarter (28.2 %; 95 % CI 18.6–37.9 %) reported anal sex in the previous year; less than half (40.0 %; 95 % CI 23.3–56.6 %) reported using a condom during last anal sex.
\0.01
In bivariate analysis (Table 4), the likelihood of CT was significantly greater among FSW reporting TSP in the previous week (OR 6.9; 95 % CI 0.8–59.8, p = 0.08) and group sex during the previous year (OR 3.0; 95 % CI 1.1–7.6, p = 0.03), and for each additional TSP from whom either money or goods were received (OR 1.2; 95 % CI 1.0–1.4, p = 0.06) and non-TSP (OR 1.1; 95 % CI 1.0–1.3, p = 0.01) during the previous year. The likelihood of CT infection reduced as age increased (OR 0.9 for each year; 95 % CI 0.9–1.0, p = 0.02), as age of first sex increased (OR 0.7 for each year; 95 % CI 0.5–0.9, p = 0.04), and as age of first transactional sex increased (OR 0.9 for each year; 95 % CI 0.8–1.0, p = 0.04), for condom use at last anal sex (OR 0.1; 95 % CI 0.0–0.9, p = 0.03) and treatment for a previous STI (OR 0.2; 95 % CI 0.1–0.6, p \ 0.01). In multivariate analysis, FSW had significantly increased odds of CT with increasing numbers of TSP during the previous week (OR 1.1 for each additional TSP; 95 % CI 1.0–1.2, p = 0.06) and among those reporting group sex during the previous year (OR 2.9; 95 % CI
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1.1–8.2, p = 0.04), whilst the odds of CT decreased as age of first sex increased (OR 0.6 for each year; 95 % CI 0.5–0.9, p \ 0.01) and for treatment for a previous STI (OR 0.1; 96 % CI 0.1–0.4, p \ 0.01).
Discussion This study is one of the first IBBS conducted with key populations in PICT and the first in Vanuatu. The overall CT prevalence is among the highest documented in PICT [2] and globally among FSW [22]. PICT are commonly underrepresented in global discussion on STI epidemiology despite evidence of alarmingly high levels of STI. Indeed, evidence that STI facilitate transmission of HIV [6] coupled with high STI rates highlight the potential for increased HIV cases in PICT. This study clearly demonstrates the need for increased focus and investment in STI prevention activities in PICT, particularly those targeting FSW. Comparison of the CT prevalence among FSW reported in this study to other studies with FSW in the Pacific region reveals variation in prevalence; the CT prevalence reported here is 50 % higher than recently reported in Fiji (22 %) [12] and in PNG in 1998–1999 (31 %) [23]. Direct comparison with PNG data is limited given marked differences in HIV epidemiology, time lapse and sampling strategies, whilst the 2012 Fiji IBBS used similar methodology and calculated weighted population estimates. Several interrelated factors may explain the difference in CT prevalence between Fiji and Vanuatu. First, the nature of sex work in Fiji is direct (that is, solicitation of clients in settings such as the street or brothels with the primary purpose to exchange sex for money) [24–26] whilst in Vanuatu it is mostly indirect (that is, informal and commonly an additional source of income and/or involving the transaction of goods/services) [13, 25, 26]. There is evidence that indirect sex work increases HIV and STI risk, particularly when sex is exchanged for survival, basic necessities, additional income and alcohol and/or drugs [25]. Our findings demonstrate the ubiquity of exchanging sex for alcohol and/or drugs among FSW and previous studies have reported the central role of sex work in Vanuatu to provide supplementary income [13]. Second, vastly different levels of condom use with TSP were reported in the two studies. Fewer than half of all FSW in Vanuatu reported using a condom with their last TSP; lower than reported in the 2012 Fiji IBBS (93 %), [12] and lower than reported in the 2007 Vanuatu BSS (71.4 %) [8]. The role of FSW community empowerment in Fiji as opposed to Vanuatu may explain differences in rates of condom use between these two countries, [27, 28] as WHO recommendations identify community empowerment as a necessary component of
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FSW interventions [29]. For example, qualitative research among FSW in Fiji noted the role of FSW networks, peer education and support organisations, underpinned by a ‘‘culture of cooperation and sharing’’, as being central to condom access and use and facilitation of access to clinical services [24]. In comparison, community empowerment strategies such as these are lacking in Vanuatu. These data suggest a need to develop a comprehensive prevention and treatment program for FSW in Vanuatu incorporating community empowerment and accessible and acceptable health services. In light of the indirect nature of sex work, such a strategy must acknowledge that many FSW may not self-identify as such [25, 26] when designing approaches to reach and engage this population. Additional prevention and treatment strategies with FSW should also be considered in Vanuatu, including periodic asymptomatic screening (following exposure or at regular intervals) and periodic presumptive treatment (PPT, whereby treatment is provided to individuals based on increased risk of exposure) for asymptomatic STI [29]. These strategies are pertinent given that CT infections are commonly asymptomatic among women, [6] that the majority of STI are undiagnosed among FSW and that FSW do not seek treatment even when symptoms are present. A systematic review of interventions for HIV prevention and treatment among FSW identified nine screening programs reporting either an initial or long-term decrease in CT infection among FSW; however such programs require use of point-of-care tests for CT that are sophisticated and expensive, and many are not available in low- and medium-income countries [29]. Given this limitation, PPT is potentially a more appropriate strategy to implement in PICT. PPT has been used for STI control interventions and demonstrated utility through mathematical modelling and in field settings [30], especially where STI prevalence is high. The aforementioned systematic review reported a CT prevalence decrease associated with PPT in 11 of 12 studies [29]. To date, PPT has not been used as a prevention or treatment strategy among FSW in PICT, but potentially offers an effective and appropriate strategy as part of a broader comprehensive prevention and treatment package for FSW. This study revealed the high frequency of group sex and anal sex among FSW in Vanuatu, and that group sex was independently associated with CT infection. There is evidence for increased risk of HIV and other STI associated with group sex [31] and heterosexual anal sex [32], and some studies have identified increased risky behaviours among FSW reporting anal sex [32]. The multivariate association with group sex and bivariate association with condom use at last anal sex highlight the need to further investigate their role in STI epidemiology in Vanuatu. It may also be warranted for future studies with FSW to
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collect anal swabs to assess the contribution of anal sex on CT transmission. Given low levels of consistent condom use with TSP and non-TSP and low levels of condom use at last anal sex and group sex it is paramount that strategies to facilitate condom access and use by FSW and the broader community be urgently improved, potentially through the development of a national condom strategy. This study was subject to several limitations. First, the analysis revealed design effects for some variables above two which may indicate that the sample size should have been slightly larger. We were unable to attain the desired sample size as a result of the small population size of Vanuatu and limited social networks between FSW in Vanuatu; nonetheless, we sampled 11 % of the estimated FSW population size in Port Vila (calculated using capturerecapture methods) [21] and approximately 1 % of the total female population (aged 20–54) in Port Vila (n = 11,073). Whilst estimates are not available for PICT, Vandepitte et al. [26] estimated in 2006 that FSW comprised between 0.2 and 2.6 % of the female population in Asia, and our estimate falls within this range. It is possible that additional adjusted predictors of CT infection would be identified with a larger sample size. Second, sample chains reached a maximum of six waves and may not have been sufficient to eliminate bias from the non-randomly selected seeds. Third, the multivariate analysis utilised exported weights for the dependent variable (i.e. CT infection) which may have resulted in biased results. There is currently no agreement among statisticians on how to perform multivariate analyses for network data. Forth, two seeds were excluded from analysis as they did not recruit any participants; this does not impact the analysis as the seeds need at least one recruit in order to be included in the estimator. Fifth, laboratory results for 12 participants were not included in the analysis; however, the FSW for whom results were not available had the same median number of total TSP during the previous week (median = 3, range 2–5; median = 3, range = 3–4 respectively) and similar number of total non-TSP during the previous 12 months (median = 5.5, range 4–8; median = 5–6 respectively), potentially limiting bias in relation to CT prevalence estimates. Finally, we used interviewer-administered surveys which may have introduced social desirability bias; however we note that the questionnaire was piloted for acceptability with FSW before implementation.
Conclusion This study provides much-needed evidence for the scale of the STI epidemic in Vanuatu and the need for urgent initiatives to address the high rates of CT among FSW. In particular, a comprehensive public health strategy for
prevention and treatment of STI among FSW, including community empowerment strategies, FSW-targeted health services and periodic presumptive treatment, is urgently needed. Acknowledgments We wish to thank the Vanuatu Ministry of Health for their ongoing support and for laboratory testing; NRL (Melbourne, Australia) for laboratory testing; Wan Smolbag for coordinating data collection and entry and management of the field researchers; WHO Western Pacific Regional Office and the Pacific UNAIDS Coordinator for their technical support in project implementation. Caroline van Gemert received a Travel Grant from the Ian Potter Foundation to receive training in Respondent Driven Sampling from Lisa G Johnston of Tulane University and University of California, San Francisco in USA. We thank the Pacific Island HIV and STI Response Fund Grant, a collaborative funding mechanism by the Australia and New Zealand governments and managed by the Secretariat of the Pacific Community for funding this project. Laboratory testing of specimens at the Port Vila Central Hospital was provided by the Global Fund Round 7 Grant through the Vanuatu Ministry of Health. Finally, we thank all participants of the study for their valuable input. Conflict of interest
None.
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23. Mgone CS, Passey ME, Anang J, Peter W, Lupiwa T, Russell DM, et al. Human immunodeficiency virus and other sexually transmitted infections among female sex workers in two major cities in Papua New Guinea. Sex Transm Dis. 2002;29(5):265–70. 24. McMillan K, Worth H. Risky business: sex work and HIV prevention in Fiji. Sydney: International HIV Research Group; 2010. 25. Harcourt C, Donovan B. The many faces of sex work. Sex Transm Infect. 2005;81(3):201–6. 26. Vandepitte J, Lyerla R, Dallabetta G, Crabbe F, Alary M, Buve A (2006) Estimates of the number of female sex workers in different regions of the world. Sex Transm Infect 82(Suppl 3):iii18–25. PubMed PMID: 16735288. Pubmed Central PMCID: 2576726. 27. Baral S, Beyrer C, Muessig K, Poteat T, Wirtz AL, Decker MR, et al. Burden of HIV among female sex workers in low-income and middle-income countries: a systematic review and metaanalysis. Lancet Infect Dis. 2012;12(7):538–49. 28. Kerrigan D, Fonner V, Stromdahl S, Kennedy C. Community empowerment among female sex workers is an effective HIV prevention intervention: a systematic review of the peer-reviewed evidence from low- and middle-income countries. AIDS Behav. 2013;17(6):1926–40 (English). 29. World Health Organization. Prevention and treatment of HIV and other sexually transmitted infections for sex workers in low- and middle-income countries: recommendations for a public health approach. Geneva: WHO; 2012. 30. WHO. Periodic presumptive treatment for sexually transmitted infections, experience from the field and recommendations for research. Geneva: WHO Library Cataloguing-in-Publication Data. 2008. 31. Friedman SR, Bolyard M, Khan M, Maslow C, Sandoval M, Mateu-Gelabert P, et al. Group sex events and HIV/STI risk in an urban network. J Acquir Immune Defic Syndr. 2008;1(49):440–6. 32. Baggaley RF, Dimitrov D, Owen BN, Pickles M, Butler AR, Masse B, et al. Heterosexual anal intercourse: a neglected risk factor for HIV? Am J Reprod Immunol. 2013;69:95–105.
ORIGINAL PAPER
Chlamydia Prevalence and Associated Behaviours Among Female Sex Workers in Vanuatu: Results from an Integrated Bio-behavioural Survey, 2011 Caroline van Gemert • Mark Stoove • Tamara Kwarteng • Siula Bulu Isabel Bergeri • Ian Wanyeki • Steve Badman • Jayline Malverus • Alyce Vella • Len Tarivonda • Lisa Grazina Johnston
•
Ó Springer Science+Business Media New York 2014
Abstract There is insufficient data on sexually transmitted infections (STI) and related behaviours among key populations, including female sex workers (FSW), in the Pacific region. Using respondent driven sampling, we conducted an integrated bio-behavioural survey with FSW in Vanuatu (aged C18 years) to investigate risk behaviours associations with Chlamydia trachomatis (CT). Weighted population estimates and correlates of CT infection were calculated. Among 149 FSW, prevalence of CT was 36 % (95 % CI 26–48 %). Few FSW reported consistent condom use with recent transactional sex partners (TSP) (8 %; 95 % CI 2–13 %). CT infection was positively associated with increasing number of TSP (adjusted odds ratio [AOR] 1.1; 95 % CI 1.0–1.2) and group sex (AOR 2.9; 95 % CI 1.1–8.2). CT was negatively associated with increasing age of first sex (AOR 0.6; 95 % CI 0.5–0.9) and previous STI treatment (AOR 0.1; 95 % CI 0.0–0.4). A comprehensive public health strategy for prevention and treatment of STI among FSW, incorporating community empowerment strategies, FSW-targeted health services and periodic presumptive treatment, is urgently needed in Vanuatu. C. van Gemert (&) M. Stoove I. Bergeri A. Vella Centre for Population Health, Burnet Institute, GPO Box 2284, Melbourne, VIC 3001, Australia e-mail: [email protected] T. Kwarteng Centre for International Health, Burnet Institute, Melbourne, VIC, Australia
Keywords Integrated bio-behavioural survey Female sex workers Chlamydia Pacific Risk behaviours
Introduction The prevalence of sexually transmitted infections (STI), particularly Chlamydia trachomatis (CT), are among the highest globally in the 22 Pacific Island Countries and Territories (PICT) [1]. Surveillance data from women attending antenatal care services in Fiji, Kiribati, Samoa, Solomon Islands, Tonga and Vanuatu between 2004 and 2005 found an overall CT prevalence of 18 %; prevalence was higher among women aged B24 years (26 %) [2]. Prevalence studies and routine testing data support these findings, with CT positivity as high as 29 % among women attending antenatal care services [1]. In Vanuatu (2009 population 234,023 [3]), routine annual testing data shows CT positivity ranging between 19 and 22 % [4]. In comparison, World Health Organization estimates of CT prevalence among women in 2008 were 2.6 % in the African Region, 7.6 % in the Region of the Americas and S. Badman Kirby Institute, University of New South Wales, Sydney, NSW, Australia L. Tarivonda Department of Public Health, Ministry of Health, Port Vila, Vanuatu
S. Bulu J. Malverus Wan Smolbag Theatre, Port Vila, Vanuatu
L. G. Johnston School of International Public Health and Tropical Medicine, Tulane University, New Orleans, LA, USA
I. Wanyeki Secretariat of the Pacific Community, Noumea, New Caledonia, France
L. G. Johnston Global Health Sciences, University of California, San Francisco, San Francisco, USA
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1.1 % in the South-East Asia Region [5]. Adverse outcomes of untreated CT include cervicitis, endometriosis and infertility and 10–40 % of women with untreated CT infection develop symptomatic pelvic inflammatory disease; [6, 7] therefore, timely detection, treatment and prevention of onward transmission is paramount. Despite endemic levels of STI across the region, passive surveillance data suggest HIV prevalence is low in all PICT excluding Papua New Guinea (PNG); however, HIV prevalence is likely underestimated due to low testing rates [8–10]. Limited testing may be a result of fear of HIVrelated stigma and discrimination, concerns regarding confidentiality of test results in smaller countries and communities, as well as lack of access to, and uptake of, HIV testing and counselling, particularly in rural or geographically isolated areas and among key populations at increased risk of HIV and other STI [10, 11]. Further, epidemiological surveillance systems are lacking in the region to monitor HIV and STI among key populations; as a result, limited data exist on key populations, including female sex workers (FSW) [9]. PICT are therefore unable to determine who is at risk of HIV infection and how to target appropriate prevention strategies. In the absence of quality surveillance data, targeted Integrated Bio-Behavioural Surveys (IBBS) among key populations are needed to assess burden of disease, monitor risky behaviours, and identify populations for targeted interventions. IBBS link HIV and other STI testing data to behavioural data collected through a structured questionnaire that explores risky behaviours and practices. A 2012 IBBS in Fiji among FSW is the only recent IBBS conducted among FSW in the region; this study reported an overall CT prevalence of 22 %; however socio-demographic and behavioural variables significantly associated with CT infection were not presented and reported findings therefore have limited utility to monitor risky behaviours and practices and inform prevention initiatives [12]. In Vanuatu, data for FSW are limited to a 2007 behavioural surveillance survey (BSS) and a 2011 qualitative study; both reported inconsistent condom use with paying and non-paying partners and low HIV testing rates [8, 13]. To date, there are no recent studies presenting STI prevalence alongside behavioural correlates of infection among FSW in Vanuatu or other PICT. In 2011, the Burnet Institute, in partnership with the non-governmental organisation, Wan Smolbag, and the Vanuatu Ministry of Health, conducted an IBBS among FSW in Port Vila, the capital of Vanuatu (2009 population: 44,040 [3] ), to measure HIV and other STI prevalence and identify risk factors. This paper presents the prevalence of CT and other STI and associated socio-demographic and behavioural predictors of CT infection among FSW.
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Methods Study Design, Sampling and Recruitment This cross-sectional study was guided by surveillance tools developed by Family Health International, WHO and UNAIDS [14, 15]. Participants were recruited between September and November 2011 using respondent driven sampling (RDS), a link-tracing sampling technique whereby participants recruit new participants from their peer network [16]. RDS allows for the anonymous and confidential recruitment of hidden and socially networked populations [14, 17]. In RDS, participants provide information on their social network size to establish relative probabilities of recruitment and RDS analysis techniques mitigate common biases found in link tracing sampling methods [16]. Eligible FSW included females exchanging sex (vaginal, anal or oral) for money, goods or favours (defined as transactional sex) in the previous year, C18 years, and living in or near Port Vila. The sample size was calculated for 244 respondents based on an estimated HIV prevalence of 3 %, a population correction fraction (FSW population size estimated as 1,000), confidence of 95 %, power of 80 %, a non-response rate of 0.2 and a design effect of 2.0. The final estimated sample size was rounded up to 250. Sampling began with seven seeds (initial recruits), identified through key contacts. Seeds were selected purposively for their close links with the study population and for diversity of individual attributes (such as age, marital status, type of sex work, geographical location). Seeds were given three recruitment coupons to recruit the first wave of participants. Subsequent participants received three recruitment coupons. Participants received the equivalent of AUD$15 for participating in the survey, AUD$5 for each peer recruited (a maximum of three peers could be recruited), and AUD$5 for returning to receive test results. Data Collection Three trained female field researchers assessed eligibility and obtained informed written consent. Intervieweradministered interviews were conducted at Wan Smolbag in Bislama (an official language of Vanuatu), consisting of a questionnaire incorporating items about socio-demographic characteristics and sexual risk behaviours. The questionnaire was piloted with FSW and modified for clarity based on field researchers and pilot participants feedback. For RDS analysis, FSW were asked about their social network size including the number of FSW they know and who know them, seen in the previous month and who meet study eligibility. Following pre-test counselling, a trained nurse at Kam Pussum Hed (KPH) Clinic, a reproductive
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health clinic managed by Wan Smolbag, collected a total of 20 ml of venous blood for HIV and syphilis testing and vaginal swabs for CT and Neisseria gonorrhoea (NG) testing. Vaginal swabs were tested for CT and NG with BD ProbeTec nucleic acid amplification testing. Active syphilis was detected with an RPR screening test and confirmation of reactive samples by DetermineTM Syphilis TP. HIV was detected using the recommended HIV testing algorithm validated for PICT [18] (a rapid screening test [Determine] with confirmation of reactive samples by two additional rapid tests [Insti and Unigold]). All testing was conducted at the Port Vila Central Hospital; the national laboratory is the only place with staff currently trained to provide HIV point of care tests and also conducts all diagnostic testing for the KPH Clinic. FSW were asked to return to receive post-test counselling and test results within four weeks following participation; positive cases received treatment and/or were referred for further management through the public primary health care system. To facilitate confidentiality, coupons, questionnaires, specimens, and test results were linked using a unique study identification number. Measures This analysis explores several socio-demographic and sexual behaviour measures and associations with CT infection among FSW [19]. The majority of measures included in this analysis are dichotomous (yes/no, or two-category age groups or time periods) or categorical. Consistent condom use defined as always using a condom with transactional sex partners (TSP) or non-TSP during the previous month. Multiple responses were permitted to describe the reason why a condom was not used at last sex with a TSP or non-TSP and genital symptoms experienced in the last 12 months (including genital discharge, genital ulcer or sore, burning or sharp pain on urination, and rash or general itching); these were then re-categorised as a binary variable. Open ended responses were used to collect information on goods or favours received at last transactional sex; these were then categorised as clothing, food, drugs or alcohol, or other. Additional measures are numerical; the median age, duration or number and interquartile range (IQR) were calculated as appropriate for several measures, including age of first sex, age of first transactional sex, duration of transactional sex work (calculated as current age–age of first transactional sex), unique number of TSP in the previous week and unique number of non-TSP during the previous year. Data Analysis Population estimates (%) and 95 % confidence intervals (CI) were calculated with RDS-Analyst version 9.0 (www.
hpmrg.org) using the successive sampling estimator with apriori mid-range population size estimate set at 1,390 [20, 21]. Univariate and multivariate logistic regression identified statistically significant (p \ 0.1) correlates of CT infection using RDS-Analyst-generated survey weights, also using the successive sampling estimator. Multivariate logistic regression using reverse stepwise selection procedures were used whereby non-significant candidate predictors were removed sequentially until only significant predictors (p \ 0.1) remained. Age, age of first sex, age first transacted sex and the number of TSP and non-TSP in the previous week were treated as continuous variables; the remainder were categorised as above. Missing data were included as a category as appropriate in logistic regressions; OR and AOR are not presented for these. Weighted statistical analyses were conducted using STATA version 11 (Stata Statistical Software: Release 11, StataCorp LP, TX, College Station, 2009). Ethical Approval The Ministry of Health, Government of the Republic of Vanuatu Ethics Committee and Alfred Hospital Ethics Committee approved this study.
Results Data were analysed from 149 FSW, after excluding two nonproductive seeds and two ineligible participants; ineligible participants included one participant who identified as male and one who had not transacted sex in the previous 12 months. The maximum recruitment chain was six waves. Almost half (47.1 %; 95 % CI 35.7–58.4 %) were aged 20–29 years (median age = 24 years, IQR = 22–26 years) and most reported completing secondary education (59.5 %; 95 % CI 50.0–69.0 %), never being married (68.8 %; 95 % CI 60.8–76.8 %), and having additional sources of income (75.8 %; 95 % CI 66.8–84.7 %). The most commonly reported setting for additional income was at a shop or market stall (62.2 %; 95 % CI 51.2–73.0 %, Table 1). Vaginal swab results for CT and NG testing were available for 137 participants. Of the 12 FSW for whom results were not available, four FSW did not provide specimens and eight results were missing. Blood test results for HIV and syphilis were available for 118 participants. Of the 31 FSW for whom blood test results were not available, 18 did not provide samples and 13 were missing. CT positivity among FSW was 36.7 % (95 % CI 25.6–47.9 %), NG 17.1 % (95 % CI 10.2–23.9 %), and syphilis 3.7 % (95 % CI 0.3–7.1 %, and 11.1 % (95 % CI 3.3–18.9 %) were CT and NG co-infected (Table 2). HIV seropositivity was not detected among FSW.
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Three-quarters of all FSW (76.0 %; 95 % CI 67.6–84.4 %) reported genital STI symptoms in the previous year, however less than half (38.7 %; 95 % CI 29.2–48.3 %) sought treatment. Among those who sought treatment, most (56.7 %; 95 % CI 33.0–80.3 %) attended the public hospital and one-third (34.5 %; 95 % CI 9.7–59.3 %) attended the KPH clinic. Almost half of FSW who did not seek treatment (44.7 %; 95 % CI 30.0–59.4 %) reported being too scared to seek treatment.
Table 1 Weighted population estimates and confidence intervals (CI) for demographic variables among female sex workers (n = 149), Vanuatu, 2011
Agea 18–19 years 20–29 years
n (median)
Population estimate % (IQRf)
(24) 30
(22–26) 26.2
72
47.1
95 % CI
35.7, 58.4
31
17.1
9.6, 24.5
40? years
14
9.7
3.3, 16.1
Highest level of education Some or all primary
2
1.6
0.1, 3.2
Secondary
86
59.5
50.0, 69.0
61
38.8
Table 2 Weighted population estimates and confidence intervals (CI) for STI history, symptoms and prevalence among female sex workers (n = 149), Vanuatu, 2011 n
13.8, 38.6
30–39 years
Higher
The majority of FSW reported their age of first sex as \18 years (68.3 %; 95 % CI 58.1–78.4 %; median = 16, IQR = 16–17), age of first transactional sex [18 years (61.3 %; 95 % CI 50.3–72.1 %; median = 19, IQR = 18–19) and duration of transactional sex work [one year (80.9 %, 95 % CI 72.4–89.4 %; median = 4, IQR = 3–5) (Table 3). Nearly all (87.4 %; 95 % CI 80.7–94.1 %) transacted sex in the previous week; most (70.5 %; 95 % CI 59.0–82.0 %) reported receiving both money and goods, 22.7 % (95 % CI 11.5–34.0 %) received money only and 6.8 % (95 % CI 1.4–12.1 %) received goods only. Among FSW that reported TSP during the previous week, the median total number of unique TSP was three (IQR 3–4). The most common goods received during
30.0, 48.0
100
Currently or previously married
49
68.8 31.2
60.8, 76.8 23.2, 39.2
Has other income in addition to sex work Yes
Chlamydiaa Gonorrheaa
Setting of additional income Shop or market stallb
a
36.7 17.1
25.6, 47.9 10.2, 23.9
4
3.7
0.3, 7.1
HIVa
0
–
–
Co-infectionsa Chlamydia and gonorrhoea
15
11.1
3.3, 18.9
Gonorrhoea and syphilis
1
1.8
-0.5, 4.1
Chlamydia and syphilis
1
0.4
0.2, 0.5
No
81
59.7
50.8, 68.6
Yes
68
40.3
31.4, 49.2
Prior STI
Had genital symptom/s in previous yearb Yes
116
76.0
67.6, 84.4
Had treatment for genital symptom/s in previous year No
60
61.3
50.5, 72.1
Yes 56 Place where treatment was soughta
38.7
29.2, 48.3
27
56.7
33.0, 80.3
22
34.5
9.7, 59.3
6
8.8
0.1, 17.5
75.8
66.8, 84.7
68
62.2
51.2, 73.0
Hospital KPH clinic Otherb
Otherc
26
22.2,
10.9, 33.4
Informald
14
6.5
1.9, 11.2
Too scared
27
44.7
30.0, 59.4
Hospitalitye
7
9.0
2.0, 16.1
Other
18
26.9
13.0, 40.8
Too busy
4
10.7
1.7, 19.6
Too public
8
12.7
-0.6, 26.0
Too expensive
3
5.1
-0.6, 10.8
Reason why treatment was not sought
Missing values: Age (n = 2)
b
Shop or market stall includes shop assistant, selling food/produce at market, selling handicrafts
c
47 24
Syphilisa
115 b
95 % CI
STI prevalencea
Marital status Never been married
Population estimate (%)
Other income includes office work, peer education, hairstylist
d
Informal income includes massage, house girl, gardener, laundry services, car wash, and sewing
e
Hospitality income includes bartending, hostessing, working at a kava bar, hotel or guesthouse f Interquartile range
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a
Missing responses: Chlamydia and gonorrhoea test result (n = 8, 4 additional specimens not provided); HIV and syphilis test result (n = 13,18 additional specimens not provided); location where treatment was sought (n = 1) b
Other includes Vanuatu Family Health Association Clinic, private doctor, pharmacy or chemist, traditional healer
AIDS Behav Table 3 Weighted population estimates and confidence intervals (CI) for sexual risk behaviours with transactional and non-TSP among female sex workers (n = 149), Vanuatu, 2011
Age of first sex
N (median)
Population estimate % (IQRd)
(16)
(16–17)
95 % CI
\18 years
99
68.3
58.1, 78.4
18? years
50
31.7
21.6, 41.9
Age first sold/transacted sexa
(19)
(18–19)
\18 years
50
38.7
27.9, 49.7
18? years
98
61.3
50.3, 72.1
(4) 26
(3–5) 19.1
10.6, 27.6
121
80.9
72.4, 89.4
No
20
12.6
5.9, 19.3
Yes
129
87.4
80.7, 94.1
Duration of sex work/transactional sexa \1 year More than 1 year Had transactional sex partner (TSP) in previous week
Money and/or goods received during previous week Received both money and goods
94
70.5
59.0, 82.0
Received money only
28
22.7
11.5, 34.0
Received goods only
7
6.8
1.4, 12.1
Number of TSP from whom money was received
(2)
(2–2)
–
Number of TSP from whom goods were received
(2)
(2–2)
–
Total number of TSP
(3)
(3–4)
–
Number of TSP during the previous week, by goods/money received
Description of goods or favours received at last transactional sex among FSW that received goods during the previous weekb Clothing Food
58 24
62.6 18.6
50.6, 74.7 8.6, 28.5
Drugs or alcohol
21
18.3
10.3, 26.3
Other
14
11.1
4.8, 17.4
13
7.5
2.4, 12.5
No
79
55.9
45.6, 66.0
Yes
69
44.2
33.4, 55.0
Consistency of condom use with TSP during previous monthc Consistent Condom use at last sex with TSP
a
Reason for not using a condom at last sex with TSPb Client objected
55
65.1
52.4, 77.8
Used other contraceptive
16
17.2
7.6, 26.5
Not available
11
22.9
9.9, 3.6
Don’t like them
7
18.1
5.3, 30.9
Didn’t think of it
5
10.1
2.0, 18.1
Trusted partner
4
1.7
0.8, 2.6
Afraid Client paid more not to use
4 2
7.6 1.1
-1.0, 16.1 0.1, 2.1
Client looked healthy
1
0.8
-0.2, 1.9
Too drunk/high
1
0.4
-0.1, 0.1
Didn’t think it necessary
1
0.2
-0.0, 0.4
Had regular partners in the previous year
149
–
–
Number of regular non-TSP in the previous year
(4)
(3–4)
Had casual partners in the previous year
117
76.4
Number of casual non-TSP in the previous year
(3)
(2–3)
Total number of non-TSP in the previous year
(6)
(5–6)
Sexual risk behaviours with non-TSP
68.2, 84.5
123
AIDS Behav Table 3 continued N (median)
Population estimate % (IQRd)
95 % CI
Used a condom at last sex with non-TSPa
43
37.5
19.6, 55.4
Consistent condom use with non-TSP during previous yeara
10
7.2
3.1, 11.4
Had group sex in previous yeara Used a condom during last group sex
59 27
37.6 55.3
26.6, 48.6 34.4, 76.2
Has ever been forced to have sexa
101
69.5
60.7, 78.4
Has had anal sex in the previous yeara
44
28.2
18.6, 37.9
Condom use at last anal sex
17
40.0
23.3, 56.6
a
Missing responses: Age first sold/transacted sex (n = 1); Duration of sex work/transactional sex (n = 2); Condom use at last sex with TSP (n = 1); Number of regular partners in previous year (n = 3), Number of casual partners in previous year (n = 1), Condom use with non-TSP— last sex and consistent condom use (n = 32), Had group sex in previous year (n = 2), Ever been forced to have sex (n = 1), Has had anal sex in the previous year (n = 7) b
Multiple responses permitted
c
Consistent condom use defined as always using a condom with TSP and non-TSP during the previous month
d
Interquartile range
Table 4 Predictors of chlamydial or gonorrhoeal infection among FSW with available Chlamydia test results (n = 137) in Vanuatu, 2011: Odds ratios (OR) and adjusted OR (AOR) with 95 % confidence intervals (CI) Chlamydia infection ORa
95 % CI
p value
0.9
0.9, 1.0
0.02
AORb
95 % CI
p value
0.6
0.5, 0.9
\0.01
1.1
1.0, 1.2
0.06
Demographic variables Age For each additional year Education level (reference group some or all primary) Secondary
1.3
0.5, 3.5
Higher than secondary
1.6
0.1, 27.9
0.5
0.2, 1.5
Married before (reference group no) Yes
Has other income in addition to sex work (reference group no) Yes
0.8
0.3, 2.4
0.7
0.5, 0.9
\0.01
0.9
0.8, 1.0
0.04
0.6
0.2, 2.0
6.9
0.8, 59.8
0.08
For each TSP from whom money was received
1.3
1.0, 1.8
0.08
For each TSP from whom goods were received
1.2
0.8, 1.7
For each TSP (total number)
1.2
1.0, 1.4
Sexual risk characteristics Age of first sex For each additional year Age first sold/transacted sex For each additional year Duration of sex work/transactional sex (ref. 1.11 year) More than one year Had TSP in the previous week (ref. no) Yes Number of TSP in previous week
Consistency of condom use with TSP during previous month (ref. inconsistent) Consistent
0.3
0.1, 1.5
1.1
0.4, 3.1
Condom use at last sex with TSP (ref. no) Yes
123
0.06
AIDS Behav Table 4 continued Chlamydia infection ORa
95 % CI
p value
1.2
1.0, 1.4
0.05
AORb
95 % CI
p value
2.9
1.1, 8.2
0.04
0.1
0.0, 0.4
\0.01
Number of non-TSP in previous year For each regular non-TSP For each casual non-TSP
1.2
1.0, 1.5
0.02
For each non-TSP (total number)
1.1
1.0., 1.3
0.01
Consistency of condom use with non-TSP during previous month (ref. inconsistent) Consistent
0.9
0.2, 4.4
3.0
1.1, 7.6
1.4
0.3, 6.0
2.3
0.9, 6.4
1.2
0.4, 3.5
0.1
0.0, 0.9
0.4
0.1, 1.2
1.0
0.3, 3.3
0.2
0.1, 0.6
Group sex in previous year (ref. no) Yes
0.03
Used a condom during last group sex (ref. no) Yes Ever been forced to have sex (ref. no) Yes Anal sex in the previous year (ref. no) Yes Condom use at last anal sex (ref. no) Yes
0.03
Previous sexual health Ever had an STI (self-reported) (ref. no) Yes Had genital symptoms in previous year* (ref. no) Yes Had treatment for previous STI (ref. no) * Yes a
Odds ratio
b
Adjusted odds ratio
the previous week was clothing (62.6 %; 95 % CI 50.6–74.7 %). Consistent condom use with TSP during the previous month was low (7.5 %; 95 % CI 2.4–12.5 %). Fewer than half (44.2 %; 95 % CI 33.4–55.0 %) used a condom at last transactional sex; among FSW that did not use a condom at last transactional sex, the most common reason was client objection (65.1 %; 95 % CI 26.1–48.1 %). Nearly all FSW (n = 132, 90.2 %) reported their most recent TSP as being ni-Vanuatu (that is, from Vanuatu; not in table). The median total number of nonTSP during the previous year was six (IQR = 5–6). Consistent condom use with non-TSP during the previous year was low (7.2 %; 95 % CI 3.1–11.4 %). Over one-third (37.6 %; 95 % CI 26.6–48.6 %) of FSW reported having group sex in the previous year, of whom half (55.3 %; 95 % CI 34.4–76.2 %) reported using a condom during last group sex. Over two-thirds (69.7 %; 95 % CI 60.7–78.4 %) reported ever being forced to have sex. Over one-quarter (28.2 %; 95 % CI 18.6–37.9 %) reported anal sex in the previous year; less than half (40.0 %; 95 % CI 23.3–56.6 %) reported using a condom during last anal sex.
\0.01
In bivariate analysis (Table 4), the likelihood of CT was significantly greater among FSW reporting TSP in the previous week (OR 6.9; 95 % CI 0.8–59.8, p = 0.08) and group sex during the previous year (OR 3.0; 95 % CI 1.1–7.6, p = 0.03), and for each additional TSP from whom either money or goods were received (OR 1.2; 95 % CI 1.0–1.4, p = 0.06) and non-TSP (OR 1.1; 95 % CI 1.0–1.3, p = 0.01) during the previous year. The likelihood of CT infection reduced as age increased (OR 0.9 for each year; 95 % CI 0.9–1.0, p = 0.02), as age of first sex increased (OR 0.7 for each year; 95 % CI 0.5–0.9, p = 0.04), and as age of first transactional sex increased (OR 0.9 for each year; 95 % CI 0.8–1.0, p = 0.04), for condom use at last anal sex (OR 0.1; 95 % CI 0.0–0.9, p = 0.03) and treatment for a previous STI (OR 0.2; 95 % CI 0.1–0.6, p \ 0.01). In multivariate analysis, FSW had significantly increased odds of CT with increasing numbers of TSP during the previous week (OR 1.1 for each additional TSP; 95 % CI 1.0–1.2, p = 0.06) and among those reporting group sex during the previous year (OR 2.9; 95 % CI
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AIDS Behav
1.1–8.2, p = 0.04), whilst the odds of CT decreased as age of first sex increased (OR 0.6 for each year; 95 % CI 0.5–0.9, p \ 0.01) and for treatment for a previous STI (OR 0.1; 96 % CI 0.1–0.4, p \ 0.01).
Discussion This study is one of the first IBBS conducted with key populations in PICT and the first in Vanuatu. The overall CT prevalence is among the highest documented in PICT [2] and globally among FSW [22]. PICT are commonly underrepresented in global discussion on STI epidemiology despite evidence of alarmingly high levels of STI. Indeed, evidence that STI facilitate transmission of HIV [6] coupled with high STI rates highlight the potential for increased HIV cases in PICT. This study clearly demonstrates the need for increased focus and investment in STI prevention activities in PICT, particularly those targeting FSW. Comparison of the CT prevalence among FSW reported in this study to other studies with FSW in the Pacific region reveals variation in prevalence; the CT prevalence reported here is 50 % higher than recently reported in Fiji (22 %) [12] and in PNG in 1998–1999 (31 %) [23]. Direct comparison with PNG data is limited given marked differences in HIV epidemiology, time lapse and sampling strategies, whilst the 2012 Fiji IBBS used similar methodology and calculated weighted population estimates. Several interrelated factors may explain the difference in CT prevalence between Fiji and Vanuatu. First, the nature of sex work in Fiji is direct (that is, solicitation of clients in settings such as the street or brothels with the primary purpose to exchange sex for money) [24–26] whilst in Vanuatu it is mostly indirect (that is, informal and commonly an additional source of income and/or involving the transaction of goods/services) [13, 25, 26]. There is evidence that indirect sex work increases HIV and STI risk, particularly when sex is exchanged for survival, basic necessities, additional income and alcohol and/or drugs [25]. Our findings demonstrate the ubiquity of exchanging sex for alcohol and/or drugs among FSW and previous studies have reported the central role of sex work in Vanuatu to provide supplementary income [13]. Second, vastly different levels of condom use with TSP were reported in the two studies. Fewer than half of all FSW in Vanuatu reported using a condom with their last TSP; lower than reported in the 2012 Fiji IBBS (93 %), [12] and lower than reported in the 2007 Vanuatu BSS (71.4 %) [8]. The role of FSW community empowerment in Fiji as opposed to Vanuatu may explain differences in rates of condom use between these two countries, [27, 28] as WHO recommendations identify community empowerment as a necessary component of
123
FSW interventions [29]. For example, qualitative research among FSW in Fiji noted the role of FSW networks, peer education and support organisations, underpinned by a ‘‘culture of cooperation and sharing’’, as being central to condom access and use and facilitation of access to clinical services [24]. In comparison, community empowerment strategies such as these are lacking in Vanuatu. These data suggest a need to develop a comprehensive prevention and treatment program for FSW in Vanuatu incorporating community empowerment and accessible and acceptable health services. In light of the indirect nature of sex work, such a strategy must acknowledge that many FSW may not self-identify as such [25, 26] when designing approaches to reach and engage this population. Additional prevention and treatment strategies with FSW should also be considered in Vanuatu, including periodic asymptomatic screening (following exposure or at regular intervals) and periodic presumptive treatment (PPT, whereby treatment is provided to individuals based on increased risk of exposure) for asymptomatic STI [29]. These strategies are pertinent given that CT infections are commonly asymptomatic among women, [6] that the majority of STI are undiagnosed among FSW and that FSW do not seek treatment even when symptoms are present. A systematic review of interventions for HIV prevention and treatment among FSW identified nine screening programs reporting either an initial or long-term decrease in CT infection among FSW; however such programs require use of point-of-care tests for CT that are sophisticated and expensive, and many are not available in low- and medium-income countries [29]. Given this limitation, PPT is potentially a more appropriate strategy to implement in PICT. PPT has been used for STI control interventions and demonstrated utility through mathematical modelling and in field settings [30], especially where STI prevalence is high. The aforementioned systematic review reported a CT prevalence decrease associated with PPT in 11 of 12 studies [29]. To date, PPT has not been used as a prevention or treatment strategy among FSW in PICT, but potentially offers an effective and appropriate strategy as part of a broader comprehensive prevention and treatment package for FSW. This study revealed the high frequency of group sex and anal sex among FSW in Vanuatu, and that group sex was independently associated with CT infection. There is evidence for increased risk of HIV and other STI associated with group sex [31] and heterosexual anal sex [32], and some studies have identified increased risky behaviours among FSW reporting anal sex [32]. The multivariate association with group sex and bivariate association with condom use at last anal sex highlight the need to further investigate their role in STI epidemiology in Vanuatu. It may also be warranted for future studies with FSW to
AIDS Behav
collect anal swabs to assess the contribution of anal sex on CT transmission. Given low levels of consistent condom use with TSP and non-TSP and low levels of condom use at last anal sex and group sex it is paramount that strategies to facilitate condom access and use by FSW and the broader community be urgently improved, potentially through the development of a national condom strategy. This study was subject to several limitations. First, the analysis revealed design effects for some variables above two which may indicate that the sample size should have been slightly larger. We were unable to attain the desired sample size as a result of the small population size of Vanuatu and limited social networks between FSW in Vanuatu; nonetheless, we sampled 11 % of the estimated FSW population size in Port Vila (calculated using capturerecapture methods) [21] and approximately 1 % of the total female population (aged 20–54) in Port Vila (n = 11,073). Whilst estimates are not available for PICT, Vandepitte et al. [26] estimated in 2006 that FSW comprised between 0.2 and 2.6 % of the female population in Asia, and our estimate falls within this range. It is possible that additional adjusted predictors of CT infection would be identified with a larger sample size. Second, sample chains reached a maximum of six waves and may not have been sufficient to eliminate bias from the non-randomly selected seeds. Third, the multivariate analysis utilised exported weights for the dependent variable (i.e. CT infection) which may have resulted in biased results. There is currently no agreement among statisticians on how to perform multivariate analyses for network data. Forth, two seeds were excluded from analysis as they did not recruit any participants; this does not impact the analysis as the seeds need at least one recruit in order to be included in the estimator. Fifth, laboratory results for 12 participants were not included in the analysis; however, the FSW for whom results were not available had the same median number of total TSP during the previous week (median = 3, range 2–5; median = 3, range = 3–4 respectively) and similar number of total non-TSP during the previous 12 months (median = 5.5, range 4–8; median = 5–6 respectively), potentially limiting bias in relation to CT prevalence estimates. Finally, we used interviewer-administered surveys which may have introduced social desirability bias; however we note that the questionnaire was piloted for acceptability with FSW before implementation.
Conclusion This study provides much-needed evidence for the scale of the STI epidemic in Vanuatu and the need for urgent initiatives to address the high rates of CT among FSW. In particular, a comprehensive public health strategy for
prevention and treatment of STI among FSW, including community empowerment strategies, FSW-targeted health services and periodic presumptive treatment, is urgently needed. Acknowledgments We wish to thank the Vanuatu Ministry of Health for their ongoing support and for laboratory testing; NRL (Melbourne, Australia) for laboratory testing; Wan Smolbag for coordinating data collection and entry and management of the field researchers; WHO Western Pacific Regional Office and the Pacific UNAIDS Coordinator for their technical support in project implementation. Caroline van Gemert received a Travel Grant from the Ian Potter Foundation to receive training in Respondent Driven Sampling from Lisa G Johnston of Tulane University and University of California, San Francisco in USA. We thank the Pacific Island HIV and STI Response Fund Grant, a collaborative funding mechanism by the Australia and New Zealand governments and managed by the Secretariat of the Pacific Community for funding this project. Laboratory testing of specimens at the Port Vila Central Hospital was provided by the Global Fund Round 7 Grant through the Vanuatu Ministry of Health. Finally, we thank all participants of the study for their valuable input. Conflict of interest
None.
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