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Prevalence survey of sexually transmitted infections among female sex workers and truck drivers in China, 1999-2000

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TABLE OF CONTENTS

Executive Summary Acknowledgements Introduction Methods Results Discussion Reference

1 2

3 7

10 15

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ABBREVIATIONS AND ACRONYMS

ELIZA

enzyme-linked immuno-sorbent assay injecting drug users polymerase chain reaction pelvic inflammatory disease rapid plasma reagin sexually transmitted infection treponema pallidum haemagglutination assay

IDU

peR PID

RPR STI

TPHA

EXECUTIVE SUMMARY A cross-sectional sexually transmitted infection (STI) prevalence survey was conducted by the National Center for STD and Leprosy Control, China, in conjunction with the Kunming Institute of Dermatology, Yunnan Province, and the Tongling Institute of Dermatology, Anhui Province, China. A total of 505 female sex workers, recruited in Kunming from November 1999 to May 2000, and 550 male truck drivers, recruited in Tongling from February to May 2000, participated in the survey. All eligible partiCipants gave written informed consent. Demographic, behavioural and clinical information of the participants was gathered by direct interviews. Tampon swabs and blood samples were collected from the women. Urine and blood samples were collected from the men. Tampon swabs were tested using the polymerase chain reaction (PCR) technique for Chlamydia trachomatis, Nesseria gonorriloeae and Trichomonas vaginalis. Urine was tested with PCR for C. trachomatis and N. gonorriloeae. Blood was tested for syphilis using rapid plasma reagin (RPR) serology as the screening test, and Treponema pallidum haemagglutination assay (TPHA) as a confirmatory test. HIV testing was carried out using enzyme-linked immuno-sorbent assay (ELISA) and, if positive, Western blot for confirmation. Free treatment was provided to study participants diagnosed with an STI. Among female sex workers, the most prevalent STI was Chlamydia trachomatis (58.6%), followed by Trichomonas vaginalis (43.2%) and Neisseria gonorriloeae (37.8%). Twenty-five per cent had co-infection with both gonorrhoea and chlamydiosis; 10% were positive for HIV infection, all injecting drug users (IDUs); and 9.5% had treponemal seropositivity. The highest prevalence of chlamydial infection or gonorrhoea was observed among the 15-19 and the 19-24 age groups.

Prevalence Survey of STI - China

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Among truck drivers, no positive HIV infection was found. The most prevalent STI was chlamydiosis (10.2%), followed by gonorrhoea (7.8%). Treponemal seropositivity was low (0.7%). Two per cent had co-infection with both gonorrhoea and chlamydiosis. A high prevalence of STI was observed among sex workers and men at higher risk of infection. Sentinel surveillance and passive casereporting need to be complemented by further STI surveys among specific populations. Policies and prevention strategies for STIIHIV need to focus on high-risk sub-populations, such as IDUs, sex workers (particularly sex workers who inject drugs) and clients.

ACKNOWLEDGEMENTS The study team would like to thank the following individuals for their assistance in supporting and conducting the STI prevalence surveys in Kunming and Tongling: Dr Shen Jie, Dr. Xia Gang and Dr Cui Haixia, Ministry of Health, China; Dr Zhu Cheng bing and Ms Yu Jin, National Center for STD and Leprosy Control; Dr Cui Ming and Ms Shu Chengxia, Kunming Institute of Dermatology; Dr Oi Oingshang, Mr Wu Shouqiang, Mr Ma Lin, Ms Bi Xiufang and Ms Zhu Min, Tongling Institute of Dermatology; Dr Elizabeth Sullivan, University of New South Wales, Australia; Dr Sepehr Tabrizi, Royal Women's Hospital, Australia; and Dr Gilles Poumerol and Dr Nguyen Thi Thanh Thuy, World Health Organization, Regional Office for the Western Pacific.

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Prevalence Surveys of STI - China

INTRODUCTION Sexually transmitted infections (STls) are a major public health concern in the developing world. It has been estimated that more than 35 million new STI cases occurred in the Western Pacific Region in the 1990s. STls have consistently ranked among the five most important causes of adults seeking health care and of healthy productive lives lost 1. In recent years, epidemiological studies have shown that persons with ulcerative and non-ulcerative STls are more susceptible to HIV. People with HIV and non-ulcerative STls have increased shedding of HIV-infected cells and greater effiCiency in transmitting the virus·2 The association between STls and HIV is strongest for those infections that cause genital ulceration, 3-5 but has also been demonstrated for infections such as gonorrhoea, chlamydiosis and trichomoniasis. Prevention and treatment of STls are efficient and cost-effective ways to contain the HIV epidemic. In order to formulate STI and HIV control strategies and programmes, it is usefUl to understand the epidemiology of STls and to estimate the prevalence of the various etiological agents responsible for STls in the local community, particularly among high-risk populations. China covers an area of 9.6 million square kilometres and extends about 4000 kilometres from north to south and 4800 from east to west. Land frontiers extend for 20 000 km and are shared with Afghanistan, Bhutan, the Democratic People's Republic of Korea, India, Kazakhstan, Kyrgyzstan, the Lao People's Democratic Republic, Mongolia, Nepal, Pakistan, the Russian Federation, Tajikistan and Vietnam. The country had an estimated population of 1.22 billion in 1996, of which about 70% lived in rural areas. In 1996, the crude birth rate was 17 per 1000 population, the death rate was 6.6 and the growth rate was 10.4. The epidemiology of STls in China is not well defined, with only a few prevalence ·surveys,6-8 in which small size samples were investigated with non-standardized protocols, having been conducted. Based on the National STI Surveillance System, more than 600 000 to 800 000 new infections have been reported annually in recent years and there was an almost fourfold increase in reported STls from 1990 to 1998 (from 14 to 51 cases per 100 000 persons).9 The most commonly reported STI is gonorrhoea (40.7 % of the 837 357 reported STls in 1999).10

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It is estimated that about 600 000 people in China were living with HIV infection in 2000. Surveillance of STI and HIV infections concentrates on passive case-reporting and sentinel site surveillance. It is acknowledged that reported STI and HIV infections make up only a small portion of the real number and that there is a need to strengthen STI and HIV surveillance and information systems. One strategy to improve surveillance is to conduct periodic baseline prevalence studies of selected STls. This report details the findings of the STI prevalence survey conducted during 1999-2000 among female sex workers in Kunming City, Yunnan Province, and long-distance truck drivers in Tongling City, Anhui Province. The majority of the female sex workers were recruited from among those arrested because of their illegal commercial sex activities. All truck drivers in the Tongling local transportation company were recruited. Although caution should be used in extrapolation of these results to similar population groups in China, the findings of the survey can be used in refining STI prevention and control measures and revising disease prevalence estimates among high-risk populations.

STUDY INVESTIGATORS

The study was supported by the World Health Organization Regional Office for the Western Pacific, coordinated by the Ministry of Health and implemented by the National Center for STD and Leprosy Control with the assistance of the Kunming Institute of Dermatology and Tongling Institute of Dermatology. The principal investigators were Drs Zhang Guocheng, Liang Guojun and Yin Yueping. The study team comprised staff members from the National Center for STD and Leprosy Control, Nanjing, Jiangsu Province, the Kunming Institute of Dermatology, Yunnan Province, and Tongling Institute of Dermatology, Anhui Province (see Table 1).

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Prevalence Surveys of STI - China

Table 1: Study Team and Technical Support Group for STI Prevalence Survey

National Center for SID and Leprosy Control Dr Liang Guo-jun Dr Yin Vue-ping Dr Chen Xiang-sheng Dr Gong Xiang-dong Dr Li Hua-sheng Dr Zhang We-ying Mrs Shi Mei-qin Mrs Yu Yan-hua Mr Wei Cong Mr Wu Shouqiang National Center for s'm and Leprosy Control National Center for STD and Leprosy Control National Center for SID and Leprosy Control National Center for STD and Leprosy Control Kunrning Institute of Dennatology, Kunrning, Yunnan Province Tongling Institute ofDerrnatology, Tongling, Anhui Province National Center for SID and Leprosy Control National Center for SID and Leprosy Control Kunming Institute ofDennatology, Kunrning, Yunnan Province Tongling Institute of Dennatology, Tongling, Anhui Province

Principal Investigator I Executive Director-General Co-Principal Investigator / Head of Surveillance Unit Co- Principal Investigator / Head

of Referral Laboratory Study coordinator / epidemiologist Clinician Director of the Institute Organization on Kunming site Director of the Institute Organization on Tongling site Referral Laboratory Referral Laboratory Chief Technician Chief Technician

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OBJECTIVES

(1) to provide baseline data to monitor trends and impacts of STI prevention and control programmes: • to determine the baseline prevalence rates of gonorrhoea, chlamydiosis, treponemal seropositivity and HIV infection among a group of female sex workers and male truck drivers in China; and to determine the prevalence rate of trichomoniasis among female sex workers;

(2) to analyse demographic and behavioural factors related to the STI infections in specific populations; (3) to strengthen the capacity for epidemiological assessment and surveillance for STls in China; and (4) to strengthen the technical capacity of epidemiological, laboratory, and clinical based study investigators. Sexually transmitted infections included:

Chlamydia Neisseria gonorrhoeae (gonorrhoea), vaginalis trachomatis (chlamydiosis) Trichomonas (trichomoniasis); Syphilis: as reflected seropositivity; and by prevalence of treponemal

Human immunodeficiency virus (HIV).

The STls were included in the prevalence survey becautoe they are curable, and are primarily sexually transmitted. In addition, chlamydiosis and trichomoniasis are often asymptomatic in men and women.

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Prevalence Surveys of STI - China

METHODS

STUDY POPULATION AND STUDY PROCEDURE

A cross-sectional study was undertaken to determine by laboratory confirmation the prevalence of the selected STls. A total of 505 female sex workers, arrested by public security forces in Kunming, Yunnan Province, were recruited from November 1999 to May 2000. A sample of 550 male truck drivers attending their annual routine physical examination in Tongling, Anhui Province, partiCipated in the surveys from February to May 2000. The protocol of the study was reviewed and approval granted by the ethics committee for each participating institution, i.e. the National Center for STD and Leprosy Control, the Kunming Institute of Dermatology and the Tongling Institute of Dermatology. Participation in the study was voluntary and informed consent was obtained from all eligible participants prior to data and sample collection. PartiCipants completed a confidential interview administered by trained interviewers to obtain demographic, behavioural and other information. Vaginal swabs and blood specimens were also taken. The STI prevalence surveys in the field were organized by the study team in cooperation with the local government.

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SPECIMEN COLLECTION, TRANSPORTATION AND PREPARATION

After a routine clinical examination for STI signs and symptoms, a 5ml blood sample was obtained from each participant. Sera were separated by centrifugation at 3000 rpm for 10 minutes. A vaginal swab was taken from each female sex worker, with a tampon inserted and immediately withdrawn and placed in 15ml of transport medium (0.14 M NaCl, 3 mM KCI, 10 mM Na2HPO", 2 mM KH 2 PO,,). 11 All samples were coded with a number corresponding to the number in the questionnaire, and then stored at 4°C in the local laboratory until transportation to the Reference Laboratory of the National Center for STD and Leprosy Control, Nanjing. Specimen collection, preparation, storage and shipping were supervised by the chief technician at the local laboratory. Shipments were completed within one day.

POLYMERASE CHAIN REACTION

(peR)

Upon arrival at the National Center for STD and Leprosy Control, Nanjing, cells were dislodged from tampons by manual ringing and squeezing, and were pelleted by centrifugation. DNA was extracted from 20111 aliquots of tampon cell pellet using a QIAamp DNA Purification Kit (Qiagen Inc., Valencia, CA, USA) as per the manufacturer's instructions Overall, three amplification reactions were performed on DNA extracted from each tampon specimen: (1) combined amplification of C. trachomatis and N. gonormoeae sequences using PE 9600 (Perkin Elmer Geneamp PCR 9600 Thermalcycler, PE Corporation, USA); (2) amplification of T. vaginalis sequences and; (3) amplification of Bglobin gene sequences as positive internal control

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Prevalence Surveys of STI - China

PCR reaction for detection of C. trachomatis and N. gono/Thoeae by PE 9600 thermalcycler mixing of 25!J.1 of extracted tampon DNA and 25~1 of Specimen Diluent (Roche Diagnostics), followed by a 10-minute room temperature incubation prior to amplification and detection of C. trachomatis and N. gono/Thoeas. PCR detection of T. vaginalis and B-globin gene sequences were performed using PCR ELISA DNA detection assay (Roche Biochemicals). Amplification was performed in capillaries with a volume of 50!J.I, conSisting of a 20!J.I aliquot of extracted DNA and 30!J.I of mastermix reactions (obtaining from Royal Women's Hospital, Melbourne). The samples were heated at 95°C for nine minutes and cycled 35 times using parameters of 94°C for one minute, 47°C for one minute and 670C for one minute.

ANTIBODY TESTING OF SERA

The survey provided the prevalence rates of treponemal seropositivity, not the prevalence of syphilis (active infection). Accurate diagnosis of infectious syphilis and latent syphilis require the recording of serial rapid plasma reagin (RPR) titres and treatment details. A significant proportion of high-level titres would support a high background prevalence of active infection. Each serum sample was tested by RPR (Shanghai, China) according to manufacturer's instructions. All positive RPR sera were re-tested using Treponema pallidum haemagglutination assay (TPHA, Fuji Corporation, Japan) for confirmation of positives. HIV tests were done on an unlinked aliquot of serum using the enzyme-linked immuno-sorbent assay (ELISA) technique (Vironostika'IP HIV Uni-Form II Plus O;Organon Teknika). Positive serum samples were then confirmed by a reference laboratory using Western blot (Genelabs Diagnostics·, HIV Blot 2.2, Singapore).

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STI SYNDROMIC CASE MANAGEMENT

During the survey, participants received counselling on STI and HIV prevention. STI Syndromic case management was provided at the time of examination, based on clinical findings, according to the standard syndromic approach protocol.

NOTIFICATION OF RESULTS

The results were notified to the Principal Investigator and kept with the maximum level of confidentiality. The HIV results were unlinked and were reported on a population basis.

DATA ANALYSIS

Data were entered using Epi-Info software (version 6.0; Centers for Disease Control and Prevention, Atlanta, GA, USA) and analysed using SPSS (version 8.0 for Windows; SPSS Inc., Chicago. IL), in the National Center for STD and Leprosy Control. Outcome variables include prevalence rates of study STls, of any STI (at least one infection), and their 95% confidence intervals.

RESULTS CHARACTERISTICS OF THE STUDY POPULATIONS (TABLE 2)

Of tHe 505 eligible female sex workers, more than half (54.3%) were aged under 25 years; their mean age was 24.7 years (SO: ±5.0, range: 15-39). The majority had an educational level of secondary school or lower; 75% were unmarried, divorced or cohabiting. One third came from outside the local area, but from within the study province, and one third came from other provinces.

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Prevalence Surveys of STI - China

Table 2 - Demographic characteristics of 505 female sex workers in Kunming, and 550 truck drivers in Tongling, China, 2000

Age group (years) 15-19 20-24 25-29 30-34 35-39 ~40

70 204

13.9 40.4 28.5 11.9 5.3 0.0

0 55 143 158 III 83

0.0 \0.0 26.0 28.7 20.2 15.1

144 60 27 0

Education Illiteracy Primary school Secondary school High school or higher Marital status Married Unmarried Divorced Cohabiting Residence Local area Other area in province Other province 162 152 191 32.1 30.1 37.8 498 46 6 90.5 8.4 l.l

34 142 234 95

6.7 28.1 46.3 18.8

3 18 277 252

0.5 3.3 50.4 45.8

126 282 54 43

25.0 55.8 \0.7 8.5

395 145 3 4

71.8 26.4 0.9 0.7

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PREVALENCE OF SEXUALLY TRANSMITTED INFECTIONS (TABLES 3 AND 4)

Among the female sex workers, the prevalence rate for Chlamydia trachomatis was 58.6%, for Trichomonas vaginalis 43.2% and for Neisseria gonorrhoeae 37.8%. One quarter had co-infection with both gonorrhoea and chlamydiosis. The prevalence of HIV infection was 10.3% and all HIV-positive cases were injecting drug users (IDUs). Treponemal seropositivity was about 10 %. Of the 505 female sex workers, 433 (85.7%) had at least one infection, 179 (35.4%) had two concurrent infections, 80 (15.8%) had three concurrent infections and 11 (2.2%) had four infections. The highest prevalences of chlamydial infection and of gonorrhoea were observed among the 15-19 and 1924 year-old age groups (Chi square test for trend, P<0.05 and <0.01, respectively; data not shown). Among the truck drivers, treponemal seropositivity was 0.7%, gonorrhoea 7.8%, chlamydial infection 10.2%, and co-infection with gonorrhoea and chlamydiosis 2.0%. Of the 550 truck drivers, 92 (16.7%) had at least one infection and 11 (2.0%) had two concurrent infections. No HIV infection was diagnosed.

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Prevalence Surveys of STI - China

Table 3: Prevalence of sexually transmitted infections, seroprevalence of treponemal antibodies, and HIV infection among 505 female sex workers in Kunming, and 550 truck drivers in Tongling, China, 2000

Neisseria gonorrhoeae Chlamydia trachomatis Chlamydia trachomatis and Neisseria gonorrhoeae Chlamydia trachomatis or Neisseria gonorrhoeae Treponemal antibody seroreacti vity HIV

37.8 58.6

33.6-42.0 54.3-62.9

7.8 10.2

5.6-10.0 7.7-12.7

24.6

20.8-28.4

2.0

0.8-3.2

71.9

68.0---75.8

16.0

12.9-19.1

9.5 10.3

6.9-12.1 7.6-13.0

0.7 0.0

0.0---1.4

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Table 4: HIV and any STI infection by demographic and behavioural factors among 505 female sex workers in Kunming, and 550 truck drivers in Tongling, China, 2000

<25 yrs. ::::25 yrs. 15-19 20-24 25-29 30-34 35-39 2:40* 4.3 9.8

87.6 70.4

16.4 16.8

13.2 10.0 14.8

$

Primary

2: Secondary

5.1 13.2 11.1 10.0

86.4 85.4 84.9 86.0

4.8 17.2

Married

16.2 18.1

Other

Local area Other Condom use < 50% of sex 2: 50% of sex Regular Irregular

19. I 6.1

87.7 84.8

17. I 13.5

11.7 7.1 9.4 11.0

85.6 85.7 84.5 87.2

Yes

17.8 0

87.3 83.4

Rate: % any among the number of study subjects in each row. .. No study! participants in this group

'------------_.. 14

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HIGH -RISK BEHAVIOUR

A high frequency of risky behaviours was noted among the female sex workers in the study. Only 30% (n=154) reported using condoms for ~ 50% of sexual acts. About 44 % (n=219 out of 496 responses) reported having irregular sex partners, including irregular clients and casual boyfriends, and 58.1% (n=292 out of 503 responses) reported using drugs.

DISCUSSION Very high prevalence rates of bacterial STls were found among the female sex workers studied in Kunming (58.6% chlamydiosis, 37.8% gonorrhoea and 43.2% trichomoniasis). About 35 % were diagnosed with two concurrent infections and 16% with three concurrent infections. The prevalence of gonorrhoea approximates to results of other studies among similar populations in China, ranging from 29% to 35%12-15. However, the prevalence of chlamydial infection is much higher than previously reported for female sex workers in China 16, probably because a more sensitive diagnostic technique (PCR-based test) was used in the study. Chlamydial infection has been associated with pelvic inflammatory disease (PI D) and infertility, while trichomoniasis has been implicated in atypical PIO in infertile women. A hyperendemic level of T. vaginalis was detected among the female sex workers in the study. T. vaginalis is associated with premature rupture of membranes and premature labour 17 and may increase the transmission of HIV18 . Prevalence of HIV infection (10.3%) was much higher than that had been reported in previous studies in some areas in the country 19-21. Two factors that could explain the high HIV infection rate in the study group are the high STI prevalence rates (which can facilitate HIV infection) and the high proportion (58.1%) of drug users in among the participants. Because most female sex workers were from the re-education centres and had recently been arrested by the police, and more than 50% were drug users, caution should be used in extrapolation of the HIV prevalence to the general sex worker population of China. The high rates of STls among the female sex workers in the study would justify STI screening and treatment in that population. In a previous survey of the high-risk population in Yunnan

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Province, the HIV prevalence rate among underground prostitutes not using drugs was found to be 2.2%. It was projected that the rate would increase to over 5% by 200322 • The low prevalence of HIV among prostitutes not using drugs of this survey perhaps is due to the small number. The prevalence rates of chlamydial infection and gonorrhoea in the truck drivers participating in the study were 10.2% and 7.8%, substantially higher than observed in the general population sample (5.6% and 1.9%, respectively) 23, 16 and also higher than those of previous studies reported among similar populations 24-26 in China. The study suggests that underreporting of STI cases is common in China. The main reason is that many people with a mild or subclinical STI are not identified, particularly in areas with limited diagnostic capacity. In addition, a significant proportion of STI patients seek care from other sources than public health settings, and many health care providers do not report cases because of their heavy workload 27. Current surveillance of STls in China could be improved to facilitate better policy development, measurement of the disease burden and potential risks, and evaluation of STI programmes. Sentinel surveillance and passive case-reporting could be complemented by similar well-targeted STI surveys among specific population groups. STIIHIV and prevention programmes (Le. health promotion and risk reduction programmes that promote safer sex, including condom use, health information programmes to raise community awareness of STIIHIV and implementation of syndrome management programmes) should focus on high-risk sub-populations, such as IDUs, sex workers (particularly sex workers who inject drugs) and clients. However, surveillance of female sex workers who are not drug users is also important.

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21. Qu S et al. HIV sentinel surveillance in China in 1997. Chinese journal of STOIAIOS prevention and control, 1998,4:178-185. 22. Cheng HH et a/. Analysis and prediction on the trends of the HIV infection epidemic in Yunnan Province. Chinese journal of STOIAIDS prevention and control, 2000, 6:257. 23. Jin HM et al. Infections with gonorrhoea in pregnant women. Chinese journal of dennatovenereology, 1995, 9:200-201. 24. Han F et a/. The STD surveillance report of 3629 drivers. Chinese journal of STOIAIDS prevention and control, 1997, 3: 101. 25. Meng Q, Tan M, Zhang Z. Report of STO survey in 4376 drivers in Mengcheng County, Anhui Province. Chinese journal of STOIAIDS prevention and control, 1996,2:9. 26. Chen F et a/. An investigation on the HIV-infected cases in 1190 truckers in a certain county, Yunnan Province. Chinese journal of STOIAIOS prevention and control, 1997,3:147. 27. Shao C, Xu W, Ye G. China. In: Brown T et a/. Sexually transmitted diseases in Asia and the Pacific. Armidale, NSW,Australia, Venreology Publishing Inc., 1998, pp.72-85.

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