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Cervical human papillomavirus infection among female sex workers in southern Vietnam

Cervical human papillomavirus infection among female sex workers in southern Vietnam Background: Cervical cancer is the most frequently diagnosed malignancy among women in southern Vietnam where its incidence is one of the highest observed worldwide. Results: Cervical HPV DNA infection was measured in a cross-sectional sample of 282 female sex workers (FSW) in Soc Trang province in southern Vietnam. HPV DNA was detected in 85% of FSW and prevalence did not vary by age. Thirty-five HPV genotypes were detected; HPV 52 was the most common type. Half of HPV-positive women were infected with oncogenic types and 37% were infected with multiple genotypes. The prevalence of oncogenic HPV infection was lower among FSW with more formal education (adj. prevalence ratio = 0.63, 95% CI 0.42–0.93), those servicing 25 or more clients per month (adj. PR = 0.66 95% CI 0.48–0.92), and those engaging in withdrawal prior to ejaculation (adj. PR = 0.68, 95% CI 0.53–0.87). Oncogenic HPV prevalence was higher among FSW with regular male partners who had other female partners (adj. PR = 1.75, 95% CI 1.34–2.28) and FSW who were HIV+ (adj. PR = 1.42, 95% CI 1.08–1.88). Conclusion: Our results demonstrate that although cervical HPV infection is extremely common among FSW in southern Vietnam, prevalence varies by education level, sexual activity, habits of regular partners, and HIV status. Background lence of HPV infection among female sex workers (FSW) Cervical cancer is the most frequently diagnosed malig- in southern Vietnam–a group presumably at particularly nancy among women in southern Vietnam where its inci- high risk for HPV and other sexually transmitted infec- dence is one of the highest observed worldwide [1,2]. tions. There is considerable variation in the incidence of cervical cancer within Vietnam with rates in southern regions Results (age-standardized rate 26 per 100,000) four times higher Between April and August of 2003, 406 women were than that observed in northern provinces (6.1 per recruited. Of these women, interviews, physical exams, 100,000) [1]. These differences correspond to regional and cervical specimen collection were completed for 395. differences in the prevalence of HPV, the principal cause Following chlamydia and gonorrhea testing on 395 cervi- of cervical cancer [3], which is substantially higher in cal DNA specimens, 300 specimens remained and were southern compared to northern Vietnam [4]. This cross- sent to the HPV testing lab. DNA was sufficient for 282 of sectional study examined the genotype-specific preva- the 300 specimens. Sexually transmitted infections other Page 1 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 than HPV were evaluated in a recent report. (Nguyen TV, Twenty-two percent of HPV-positive specimens were not Khuu NV, Le TT, Nguyen AP, Cao V, Tham DC, Detels R. positive for any of the 37 types covered in the assay. Submitted.) The mean age of FSW was 25 years (range 16–47). The HPV DNA was detected in 85% (239/282) of women. majority of FSW was of Kinh ethnicity and over half lived HPV prevalence varied little by age and exceeded 80% for within the local province. Overall, 52% of women were all age groups (Figure 1). Thirty-five different HPV geno- single, 10% were married, 14% were cohabitating, 23% types were identified. Half (119/239) of HPV-positive were divorced/separated, and 1% were widowed. Fifty- women were infected with oncogenic types and 37% (88/ four percent of women had a current relationship with a 239) were infected with multiple genotypes. Oncogenic regular male partner outside of their commercial sex HPV 52 was the most common type observing comprising work. Sixty-three percent of women had no more than a 11.4% of all genotypes detected (Table 1). HPV 16, 58, 62, primary school education. Sixty-three percent of women 51, and 18 were also among the most common types. had been a sex worker for less than 3 years. FSW were dis- tinguished by the venues for selling sex. Forty-eight per- cent of women engaged in sex work from "direct" venues Table 1: Genotypes detected in cervical HPV-positive sex including the streets, parks, bus stops, boats, ferry piers, workers, Soc Trang province, Vietnam. brothels, small cafés, and guesthouses; 52% worked out of "indirect" venues, that is, hotels, restaurants, massage par- HPV genotype Frequency % lors, karaoke lounges, bars, and barbershops. The mean number of clients seen per month was 18 (range 1–81). 52 50 11.4 All women engaged in vaginal intercourse. Condom use 16 29 6.6 58 19 4.3 with regular and irregular clients was reported by 84% and 62 19 4.3 85% of FSW, respectively. Prevalence of sexually transmit- 51 18 4.1 ted infections other than HPV ranged from 2% for HIV to 18 17 3.9 43% for chlamydia. 59 13 3.0 11 12 2.7 2 When adjusted for age alone, none of the variables were 39 11 2.5 significant for any HPV infection, oncogenic HPV, or mul- 84 11 2.5 56 10 2.3 tiple HPV infection. Variables were then evaluated in 70 10 2.3 models containing all 26 variables (Table 2). Variables 66 92.1 significant in one or more full models included the fol- 68 92.1 lowing: education level (no formal schooling, primary 54 8 1.8 school, secondary/high school), number of clients serv- 55 8 1.8 iced per month (<10, 10–25, >25), engaging in with- 61 8 1.8 71 8 1.8 drawal prior to ejaculation (ever/never), engaging in anal 67 1.6 intercourse (ever/never), use of intrauterine device (IUD) 33 61.4 (ever/never), age of regular male partner (<30, ≥30), rela- 53 61.4 tionship with a regular partner with other female partners 72 6 1.4 (yes/no), and HIV infection (positive/negative). 81 6 1.4 26 51.1 2 Final models were developed consisting of these 8 varia- 73 51.1 CP6108 5 1.1 bles in addition to age (continuous) (Table 3). FSW with 45 40.9 a secondary or high school education were less likely to be 83 4 0.9 positive for oncogenic or multiple HPV types than women 40 3 0.7 with a primary school education or no formal schooling. 42 3 0.7 FSW servicing 25 or more clients per month were less 67 3 0.7 likely to have any or oncogenic HPV infection compared 31 20.5 2 to those with fewer clients. The prevalence of any, onco- 35 20.5 82 20.5 genic, and multiple HPV infection was significantly lower 64 1 0.2 among FSW engaging in withdrawal prior to ejaculation. Untyped 99 22.6 FSW using IUDs were less likely to be infected with multi- ple HPV types. The prevalence of HPV (any, oncogenic, Total 438 100 and multiple infection) was significantly greater among HIV+ women. Apart from their commercial sex work, FSW 239 HPV+ sex workers; 88 HPV+ for 2 or more genotypes with regular male partners who had other female partners Oncogenic/probable oncogenic genotypes Page 2 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 <20 20-24 25-29 30-34 35-39 40+ age group (years) Preval Figure 1 ence of cervical HPV in sex workers by age, Soctrang province, Vietnam Prevalence of cervical HPV in sex workers by age, Soctrang province, Vietnam. were more likely to have all 3 HPV outcomes while those Cambodia. Sex workers commonly traverse between the 2 with male partners ages 30 years and older were more countries through these areas. It is possible that these likely to have any infection. highly transient sex workers are at particularly high risk for HPV. The substantial proportions of multiple infec- Discussion tions and untyped specimens are consistent with a high- Our results demonstrate that cervical HPV infection is risk population with exposure to many different partners. extremely common among southern Vietnamese sex workers with an overall prevalence nearly twice that of Oncogenic HPV 52 was more common than HPV 16 in chlamydia. HPV prevalence in the present study was much this population of sex workers. HPV 52 is one of the most higher than that observed in a population-based preva- common types found among women in southeast Asia as lence study of HPV in Vietnam [4]. In Ho Chi Minh City, well as eastern Asia including women with normal cervi- the major city of southern Vietnam, 10.9% of women cal cytology as well as those with SIL and carcinoma [6]. were positive for cervical HPV DNA compared to 2.0% of HPV 16 is estimated to be responsible for the majority of women in Hanoi, the major city of northern Vietnam [4]. invasive cervical cancers. It is not known whether the pro- The prevalence of HIV among sex workers in Vietnam portion of cervical cancers attributed to HPV 16 in south- shown similar geographic disparities with rates in the ern Vietnam, which has among the highest rates of southern border higher than that in the north and central cervical cancer in the world [1,2], is different from other regions [5]. parts of the world. The basis for these differences in the prevalence of HPV The lack of variation of HPV prevalence with age among and other sexually transmitted infections by geographic these sex workers is contrary to what has been observed in region is not completely understood. It may reflect differ- North American, European, and some Asian populations. ences in sexual practices including the pervasiveness of The flat age curve in this population of sex workers is sim- prostitution by region. Soc Trang province, where nearly ilar to that observed in high-risk populations in India and 1/3 of the population is Khmer, is proximate to Kien Nigeria characterized by high cervical cancer incidence Giang, An Giang and Dong Thap provinces which border and mortality [7]. Page 3 of 9 (page number not for citation purposes) HPV preval ence (%) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 Table 2: Cervical HPV infection and characteristics of sex workers, Soc Trang province, Vietnam 1 1 1 No. (%) Any HPV Adj. PR (95% CI) Oncogenic HPV Adj. PR (95% CI) Multiple HPV Adj. PR (95% CI) Age (yrs.) <20 45 (16%) 1.00 1.00 1.00 20–29 175 (62%) 0.83 (0.62–1.10) 0.72 (0.48–1.09) 0.72 (0.41–1.25) 30+ 62 (22%) 0.78 (0.53–1.16) 0.79 (0.33–1.87) 0.88 (0.37–2.10) p trend = 0.35 p trend = 0.12 p trend = 0.07 Ethnicity Kinh 230 (82%) 1.00 1.00 1.00 Other 52 (18%) 1.14 (0.92–1.41) 1.10 (0.73–1.64) 1.02 (0.60–1.73) Marital Status Not Single 136 (48%) 1.00 1.00 1.00 Single 146 (52%) 1.02 (0.83–1.27) 1.29 (0.83–1.98) 1.68 (0.83–6.79) Education None 43 (15%) 1.00 1.00 1.00 Primary School 136 (48%) 0.94 (0.73–1.22) 0.78 (0.48–1.25) 0.63 (0.37–1.08) Secondary-high school 103 (37%) 0.80 (0.59–1.10) 0.57 (0.32–1.04) 0.43 (0.23–0.79) Age of regular partner (yrs.) <30 72 (47%) 1.00 1.00 1.00 30+ 81 (53%) 1.39 (1.09–1.76) 1.60 (1.13–2.27) 1.78 (1.14–2.78) Regular partner has other female 2,3 partners No 54 (36%) 1.00 1.00 1.00 Yes 97 (64%) 1.27 (1.04–1.54) 2.01 (1.34–3.00) 2.17 (1.30–3.62) Age at first sex 15 yrs 11 (4%) 1.00 1.00 1.00 >15 yrs 270 (96%) 0.84 (0.58–1.20) 1.09 (0.54–2.19) 0.77 (0.35–1.69) Duration of commercial sex work <1 year 54 (19%) 1.00 1.00 1.00 1 – 3 years 125 (44%) 1.11 (0.79–1.57) 0.88 (0.61–1.27) 0.97 (0.65–1.45) > 3 years 103 (37%) 1.16 (0.78–1.72) 0.96 (0.62–1.49) 1.20 (0.76–1.88) p trend = 0.11 p trend = 0.02 p trend = 0.03 Venue for sex work Indirect venues 148 (52%) 1.00 1.00 1.00 Direct venues 134 (48%) 1.03 (0.87–1.22) 1.11 (0.77–1.59) 0.99 (0.68–1.44) No. of clients per month (average) <10 97 (34%) 1.00 1.00 1.00 10–25 85 (30%) 1.00 (0.88–1.15) 1.08 (0.79–1.46) 1.27 (0.75–2.13) >25 100 (36%) 0.64 (0.49–0.83) 0.43 (0.27–0.70) 0.52 (0.29–0.94) p trend = 0.16 p trend = 0.85 p trend = 0.69 Oral-penile contact Never 239 (85%) 1.00 1.00 1.00 Ever 43 (15%) 1.29 (0.94–1.78) 1.45 (0.74–2.82) 1.51 (0.70–6.55) Anal-penile contact Never 272 (96%) 1.00 1.00 1.00 Ever 10 (4%) 0.72 (0.40–1.34) 0.36 (0.14–0.92) 0.26 (0.10–0.69) Condom use with regular clients Not always 37 (16%) 1.00 1.00 1.00 Always 190 (84%) 1.13 (0.88–1.44) 1.58 (0.98–2.55) 1.68 (0.84–3.36) Page 4 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 Table 2: Cervical HPV infection and characteristics of sex workers, Soc Trang province, Vietnam (Continued) Condom use with irregular clients Not always 29 (13% 1.00 1.00 1.00 Always 189 (87%) 0.96 (0.70–1.30) 0.95 (0.69–1.30) 0.94 (0.60–1.49) Oral contraceptives Never 261 (93%) 1.00 1.00 1.00 Ever 20 (7%) 1.06 (0.81–1.40) 1.32 (0.84–2.07) 1.41 (0.75–2.64) Intrauterine device Never 218 (78%) 1.00 1.00 1.00 Ever 63 (22%) 0.89 (0.69–1.13) 0.63 (0.33–1.20 0.52 (0.28–0.99) Withdrawal Never 198 (70%) 1.00 1.00 1.00 Ever 83 (30%) 0.80 (0.67–0.96) 0.62 (0.42–0.89 0.58 (0.30–1.12) Illegal drugs Never 255 (91%) 1.00 1.00 1.00 Ever 26 (9%) 0.76 (0.54–1.06) 0.61 (0.33–1.13) 1.42 (0.80–2.52) Pregnant Never 144 (51%) 1.00 1.00 1.00 Ever 138 (49%) 1.00 (0.81–1.24 0.95 (0.61–1.46) 1.06 (0.59–1.92) Current STI status Trichomonas Negative 258 (92%) 1.00 1.00 1.00 Positive 23 (8%) 1.04 (0.78–1.39) 1.30 (0.84–2.02) 1.51 (0.76–3.00) Bacterial vaginosis Negative 200 (71%) 1.00 1.00 1.00 Positive 81 (29%) 1.10 (0.93–1.31) 1.07 (0.75–1.52) 1.30 (0.58–2.00) Yeast Negative 253 (90%) 1.00 1.00 1.00 Positive 28 (10%) 1.20 (0.97–1.49) 0.80 (0.51–1.25) 0.81 (0.39–1.69) Syphilis Negative 270 (96%) 1.00 1.00 1.00 Positive 11 (4%) 1.34 (0.84–2.16) 1.38 (0.65–2.93) 1.05 (0.42–2.67) HIV Negative 276 (98%) 1.00 1.00 1.00 Positive 5 (2%) 1.57 (0.98–2.51) 3.01 (1.01–9.00) 2.87 (0.69–12.00) Gonorrhea Negative 253 (90%) 1.00 1.00 1.00 Positive 28 (10%) 1.06 (0.91–1.24) 0.92 (0.89–1.45) 0.98 (0.68–2.86) Chlamydia Negative 161 (57%) 1.00 1.00 1.00 Positive 120 (43%) 0.99 (0.76–1.28) 0.95 (0.66–1.37) 0.98 (0.64–1.50) Prevalence ratio, adjusted for all variables 153 FSW had a regular male partner Responses missing from 2 subjects Response missing from 1 subject Direct venues include streets, parks, bus stops, boats, ferry piers, brothels, small cafés, and guesthouses; indirect venues include hotels, restaurants, massage parlors, karaoke lounges, bars, and barbershops. 227 FSW serviced regular clients 218 FSW serviced irregular clients Page 5 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 Table 3: Factors associated with cervical HPV infection in sex workers, Soc Trang province, Vietnam 1 1 1 Any HPV Adj. PR (95% CI) Oncogenic HPV Adj. PR (95% CI) Multiple HPV Adj. PR (95% CI) Education None 1.00 1.00 1.00 Primary School 0.92 (0.73–1.15) 0.80 (0.58–1.11) 0.82 (0.56–1.21) Secondary-high school 0.80 (0.61–1.04) 0.63 (0.42–0.93) 0.61 (0.38–0.99) No. of clients per month (average) <10 1.00 1.00 1.00 10–25 1.03 (0.92–1.16) 1.06 (0.87–1.30) 1.14 (0.83–1.57) >25 0.78 (0.65–0.94) 0.66 (0.48–0.92) 0.70 (0.47–1.06) p trend = 0.93 p trend = 0.43 p trend = 0.49 2,3 Regular partner has other female partners No 1.00 1.00 1.00 Yes 1.22 (1.03–1.44) 1.75 (1.34–2.28) 1.91 (1.41–2.60) Intrauterine device Never 1.00 1.00 1.00 Ever 0.85 (0.68–1.06) 0.58 (0.31–1.08) 0.53 (0.29–0.99) Withdrawal Never 1.00 1.00 1.00 Ever 0.84 (0.73–0.97) 0.68 (0.53–0.87) 0.60 (0.43–0.83) HIV Negative 1.00 1.00 1.00 Positive 1.20 (1.01–1.42) 1.42 (1.08–1.88) 1.45 (1.01–2.10) Age of regular partner (yrs.) <30 1.00 1.00 1.00 30+ 1.21 (1.03–1.44) 1.16 (0.92–1.46) 1.22 (0.86–1.73) Adjusted for all variables listed in addition to age, condom use with regular clients, gonorrhea, sex work venue 153 FSW had a regular male partner Responses missing from 2 subjects Response missing from 1 subject The observed association of education level with onco- infections. Consistent with this theory, compared to more genic and multiple-type HPV infection is consistent with experienced sex workers in Mexico City, an increased risk studies in other countries demonstrating an inverse asso- of HPV infection was observed among women involved in ciation of socioeconomic status and HPV [8,9]. Education prostitution for less than 1 year [13]. and other indicators of socioeconomic status may reflect differences in sexual practices, partner characteristics, and The lower prevalence of HPV among FSW engaging in other factors that influence exposure to the virus. withdrawal during intercourse is difficult to explain. Semen is not a major site of HPV infection in males com- Interestingly, HPV infection (any and oncogenic types) pared to the external genitals [14]. Furthermore, use of were less prevalent among FSW servicing the most clients. withdrawal is likely correlated with lack of use of con- Risk of cervical HPV infection has been consistently doms and other contraceptive methods. We also observed observed to increase with number of recent partners [10] a lower prevalence of multiple HPV infection among IUD and partners over the lifetime [11]. In contrast to the gen- users. Previous studies have demonstrated a protective eral female population, however, sex workers are likely to effect of IUD use with abnormal cervical cytology and cer- have consistent and repeated exposure to HPV with each vical adenocarcinoma [15,16]. new partner. It has been suggested that persistent, repeti- tive exposure to HPV antigen increases the development The prevalence of oncogenic and multiple HPV was and persistence of local immune responses [12]. Accord- higher among the limited number of HIV-positive women ingly, those sex workers with the largest number of clients in this population. This is consistent with studies of cervi- may be most protected from acquisition of new HPV cal HPV and HIV in other populations [17,18] and may Page 6 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 reflect the increased susceptibility to viral acquisition and/ Vietnam where the incidence of cervical cancer is one of or to viral persistence with HIV-induced immune suppres- the highest observed worldwide. Effective measures to sion. reduce the incidence of invasive cervical cancer in the pop- ulation will ideally incorporate both primary and second- Our results demonstrate that even among a high-risk pop- ary prevention efforts, including HPV vaccination and ulation such as commercial sex workers, the behavior of cervical screening. regular partners, including spouses and cohabitating part- ners, plays an important role in HPV acquisition. Sex Methods workers with regular male partners who engaged in sexual Study Recruitment relationships with other females were at increased risk of The study was approved by the Pasteur Institute, Ho Chi any, oncogenic, and multiple HPV infection. While other Minh City and the Standing Bureau for HIV/AIDS in Soc studies have demonstrated that the important role of men Trang province (currently known as the Soc Trang Center who are serviced by prostitutes in transmission of HPV to for HIV/AIDS Control and Prevention). their wives [11,19], the present study demonstrates that even for high-risk females, the behavior of their regular Initially, a mapping process to identify local sites where male partners are key to the acquisition of the virus. This FSW could be found and the numbers of FSW in each hot may indicate that HPV transmission is most efficient with spot was conducted by meeting with various local provin- repeated exposure to the same source relative to one-time cial and district sector officials, including health workers, or periodic exposures. police, the women's union, the Department of Labor, Invalid and Social Affairs, and peer educators. Interestingly, the relationship of partner's age and HPV prevalence contrasts with other sexually transmitted infec- Using the information from mapping, 406 FSW in Soc tions. A previous study of sex workers in Vietnam found Trang province were identified and invited to participate that age of partners was inversely associated with risk of in a cross-sectional study between May and August 2003. gonorrhea and chlamydia [20]. It is possible that HPV is a Because no lists of FSW were available, it was impossible more persistent infection in older men such that older to do systematic random sampling to recruit subjects in partners are more likely to transmit infections. each hot spot. After obtaining agreement from the owners of establishments and FSW, subjects were recruited by Observations of the role of condoms in HPV infection are convenience sampling. The number of refusals (FSW who inconsistent and conflicting [11,21,22]. The large major- avoided meeting with the interviewers) was not known. ity of sex workers reported 100% use of condom with reg- Verbal informed consent was obtained from all study sub- ular clients. However, information on condom use with jects. regular partners was not collected. It is possible that con- doms were less likely to be used with regular partners Specimen collection thereby increasing the risk of acquiring sexually transmit- Blood specimens were obtained for serological measure- ted infections from those partners who had other sexual ment of syphilis (rapid plasma regain; Bio-Rad) and HIV relationships. (SFD HIV 1/2 PA, Bio-Rad). Positive sera were first stored at -20°C, then batched and sent to the Pasteur Institute in Given the transient nature of most HPV infections, this Ho Chi Minh City every two weeks for confirmation with cross-sectional study offers a limited perspective of the two ELISA tests for HIV (Murex HIV 1.2.0, Abbott; Gen- natural history of HPV in this high-risk population. The screen HIV 1/2 V.2, Bio-Rad) and the Treponema pallidum minority of sex workers who were negative for HPV in the hemagglutination assay (Bio-Rad) for syphilis. present study were likely infected in the past and subse- quently cleared these HPV infections. The HPV-positive Vaginal fluid specimens were obtained for microscopic sex workers observed in this study may disproportionately and clinical identification of trichomoniasis and candi- include those with persistent infections. The ability to dis- diasis. Bacterial vaginosis was defined by Amsel criteria. tinguish factors associated with any, oncogenic, and mul- Cervical secretions were collected and temporarily stored tiple infection was limited as many women were positive at -20 degrees C prior to transport to the Pasteur Institute for multiple HPV types including concurrent oncogenic in Ho Chi Minh City where they were stored at -70 degrees and non-oncogenic types. C. DNA was extracted from cervical specimens and used for PCR-based testing of chlamydia, gonorrhea, and HPV. Conclusion The dynamics of HPV transmission are not well under- Interview stood. Our study demonstrates that sex workers may be Study subjects were interviewed by trained interviewers important reservoirs of HPV infection within southern using a structured questionnaire. Social and demographic Page 7 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 information and behavioral and sexual characteristics Acknowledgements This project was supported by Service laique de Cooperation au Develop- were queried. ment, Belgium (SLCD) and the Centers of Biomedical Research Excellence (COBRE) Program award P20 RR018727 from the National Center for HPV DNA testing, genotyping, and variant analysis Research Resources (NCRR), National Institutes of Health. Its contents are Frozen cervical DNA was sent to the Cancer Research solely the responsibility of the authors and do not necessarily represent the Center of Hawaii in Hawaii, U.S.A. for HPV DNA testing official views of NIH. The authors have no commercial or other association and genotyping. The PCR reaction utilized PGMY09/ that might pose a conflict of interest. PGMY11 primers [23] to amplify a 450 base pair region of the L1 HPV genome (nt 6582–7033). The authors would like to acknowledge the following individuals for their contributions to this study: Dr. Tien Kim Thi Nguyen of the Ministry of Health; Dr. Nghia Van Khuu, Dr. Lien Xuan Thi Truong, Dr. Van Cao, Ms. HPV-positive specimens were subsequently genotyped Phuong Kim Thi Tran, and Mr. Phuc Duy Nguyen of the Pasteur Institute using a reverse line blot detection method [24] (Roche Ho Chi Minh City; Dr. Phong Hoai Truong, Dr.Anh Phuong Nguyen of the Molecular Systems) for 37 different HPV types including Soc Trang Health Department, Dr.An Ngoc Tran & Dr. The (Soc Trang oncogenic/probable oncogenic types (HPV 16, 18, 26, 31, Center for Social Diseases), Dr. Thuc Van Nguyen, Dr. Truc TT.Le, (Hos- 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 68, 73, 82, IS39), pital for Dermato-Venereology of Ho Chi Minh City) ; Mrs. Marie Claire non-oncogenic types (HPV 6, 11, 40, 42, 54, 61, 70, 72, Rabier of the SLCD; Dr. Xuemei Zhu of the Cancer Research Center of 81, CP6108), and types with undetermined risk status Hawaii; and Dr. Richard Yanagihara of the John A. 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Dr. dom use, and human papillomavirus: pooled analysis of the IARC human papillomavirus prevalence surveys. Cancer Epi- Nguyen was responsible for the overall design and con- demiol Biomarkers Prev 2006, 15:326-33. duct of the study in Vietnam including staff training, study 12. Laurence J: Repetitive and consistent cervicovaginal exposure recruitment, data collection, laboratory testing, and data to certain viral pathogens appears to protect against their sexual acquisition in some women: potential mechanisms. J management. Dr. Hernandez was responsible for HPV Reprod Immunol 2003, 58:79-91. testing and genotyping. Dr. Nguyen and Hernandez were 13. Juárez-Figueroa LA, Wheeler CM, Uribe-Salas FJ, Conde-Glez CJ, Zampilpa-Mejía LG, García-Cisneros S, Hernández-Avila M: Human both responsible for the statistical analysis of data and the papillomavirus: a highly prevalent sexually transmitted dis- authorship of this manuscript. 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Thomas DB, Ray RM, Kuypers J, Kiviat N, Koetsawang A, Ashley RL, Qin Q, Koetsawang S: Human papillomaviruses and cervical cancer in Bangkok. III. The role of husbands and commercial sex workers. Am J Epidemiol 2001, 153:740-48. 20. Nguyen VT, Nguyen TL, Nguyen DH, Le TT, Vo TT, Cao TB, O'Far- rell N: Sexually transmitted infections in female sex workers in five border provinces of Vietnam. Sexually Transmitted Dis- eases 2005, 32:550-556. 21. Manhart LE, Koutsky LA: Do condoms prevent genital HPV infection, external genital warts, or cervical neoplasia? A meta-analysis. Sex Transm Dis 2002, 29:725-35. 22. Winer RL, Hughes JP, Feng Q, O'Reilly S, Kiviat NB, Holmes KK, Koutsky LA: Condom use and the risk of genital human papil- lomavirus infection in young women. N Engl J Med 2006, 354:2645-54. 23. Gravitt PE, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hild- esheim A, et al.: Improved amplification of genital human pap- illomaviruses. J Clin Microbiol 2000, 38:357-61. 24. 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BMC Med Res Publish with Bio Med Central and every Methodol 2003, 20;3:21. scientist can read your work free of charge "BioMed Central will be the most significant development for disseminating the results of biomedical researc h in our lifetime." Sir Paul Nurse, Cancer Research UK Your research papers will be: available free of charge to the entire biomedical community peer reviewed and published immediately upon acceptance cited in PubMed and archived on PubMed Central yours — you keep the copyright BioMedcentral Submit your manuscript here: http://www.biomedcentral.com/info/publishing_adv.asp Page 9 of 9 (page number not for citation purposes) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Infectious Agents and Cancer Springer Journals

Cervical human papillomavirus infection among female sex workers in southern Vietnam

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Springer Journals
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Copyright © 2008 by Hernandez and Vu Nguyen; licensee BioMed Central Ltd.
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Biomedicine; Cancer Research; Infectious Diseases; Oncology
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1750-9378
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10.1186/1750-9378-3-7
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18433504
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Abstract

Background: Cervical cancer is the most frequently diagnosed malignancy among women in southern Vietnam where its incidence is one of the highest observed worldwide. Results: Cervical HPV DNA infection was measured in a cross-sectional sample of 282 female sex workers (FSW) in Soc Trang province in southern Vietnam. HPV DNA was detected in 85% of FSW and prevalence did not vary by age. Thirty-five HPV genotypes were detected; HPV 52 was the most common type. Half of HPV-positive women were infected with oncogenic types and 37% were infected with multiple genotypes. The prevalence of oncogenic HPV infection was lower among FSW with more formal education (adj. prevalence ratio = 0.63, 95% CI 0.42–0.93), those servicing 25 or more clients per month (adj. PR = 0.66 95% CI 0.48–0.92), and those engaging in withdrawal prior to ejaculation (adj. PR = 0.68, 95% CI 0.53–0.87). Oncogenic HPV prevalence was higher among FSW with regular male partners who had other female partners (adj. PR = 1.75, 95% CI 1.34–2.28) and FSW who were HIV+ (adj. PR = 1.42, 95% CI 1.08–1.88). Conclusion: Our results demonstrate that although cervical HPV infection is extremely common among FSW in southern Vietnam, prevalence varies by education level, sexual activity, habits of regular partners, and HIV status. Background lence of HPV infection among female sex workers (FSW) Cervical cancer is the most frequently diagnosed malig- in southern Vietnam–a group presumably at particularly nancy among women in southern Vietnam where its inci- high risk for HPV and other sexually transmitted infec- dence is one of the highest observed worldwide [1,2]. tions. There is considerable variation in the incidence of cervical cancer within Vietnam with rates in southern regions Results (age-standardized rate 26 per 100,000) four times higher Between April and August of 2003, 406 women were than that observed in northern provinces (6.1 per recruited. Of these women, interviews, physical exams, 100,000) [1]. These differences correspond to regional and cervical specimen collection were completed for 395. differences in the prevalence of HPV, the principal cause Following chlamydia and gonorrhea testing on 395 cervi- of cervical cancer [3], which is substantially higher in cal DNA specimens, 300 specimens remained and were southern compared to northern Vietnam [4]. This cross- sent to the HPV testing lab. DNA was sufficient for 282 of sectional study examined the genotype-specific preva- the 300 specimens. Sexually transmitted infections other Page 1 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 than HPV were evaluated in a recent report. (Nguyen TV, Twenty-two percent of HPV-positive specimens were not Khuu NV, Le TT, Nguyen AP, Cao V, Tham DC, Detels R. positive for any of the 37 types covered in the assay. Submitted.) The mean age of FSW was 25 years (range 16–47). The HPV DNA was detected in 85% (239/282) of women. majority of FSW was of Kinh ethnicity and over half lived HPV prevalence varied little by age and exceeded 80% for within the local province. Overall, 52% of women were all age groups (Figure 1). Thirty-five different HPV geno- single, 10% were married, 14% were cohabitating, 23% types were identified. Half (119/239) of HPV-positive were divorced/separated, and 1% were widowed. Fifty- women were infected with oncogenic types and 37% (88/ four percent of women had a current relationship with a 239) were infected with multiple genotypes. Oncogenic regular male partner outside of their commercial sex HPV 52 was the most common type observing comprising work. Sixty-three percent of women had no more than a 11.4% of all genotypes detected (Table 1). HPV 16, 58, 62, primary school education. Sixty-three percent of women 51, and 18 were also among the most common types. had been a sex worker for less than 3 years. FSW were dis- tinguished by the venues for selling sex. Forty-eight per- cent of women engaged in sex work from "direct" venues Table 1: Genotypes detected in cervical HPV-positive sex including the streets, parks, bus stops, boats, ferry piers, workers, Soc Trang province, Vietnam. brothels, small cafés, and guesthouses; 52% worked out of "indirect" venues, that is, hotels, restaurants, massage par- HPV genotype Frequency % lors, karaoke lounges, bars, and barbershops. The mean number of clients seen per month was 18 (range 1–81). 52 50 11.4 All women engaged in vaginal intercourse. Condom use 16 29 6.6 58 19 4.3 with regular and irregular clients was reported by 84% and 62 19 4.3 85% of FSW, respectively. Prevalence of sexually transmit- 51 18 4.1 ted infections other than HPV ranged from 2% for HIV to 18 17 3.9 43% for chlamydia. 59 13 3.0 11 12 2.7 2 When adjusted for age alone, none of the variables were 39 11 2.5 significant for any HPV infection, oncogenic HPV, or mul- 84 11 2.5 56 10 2.3 tiple HPV infection. Variables were then evaluated in 70 10 2.3 models containing all 26 variables (Table 2). Variables 66 92.1 significant in one or more full models included the fol- 68 92.1 lowing: education level (no formal schooling, primary 54 8 1.8 school, secondary/high school), number of clients serv- 55 8 1.8 iced per month (<10, 10–25, >25), engaging in with- 61 8 1.8 71 8 1.8 drawal prior to ejaculation (ever/never), engaging in anal 67 1.6 intercourse (ever/never), use of intrauterine device (IUD) 33 61.4 (ever/never), age of regular male partner (<30, ≥30), rela- 53 61.4 tionship with a regular partner with other female partners 72 6 1.4 (yes/no), and HIV infection (positive/negative). 81 6 1.4 26 51.1 2 Final models were developed consisting of these 8 varia- 73 51.1 CP6108 5 1.1 bles in addition to age (continuous) (Table 3). FSW with 45 40.9 a secondary or high school education were less likely to be 83 4 0.9 positive for oncogenic or multiple HPV types than women 40 3 0.7 with a primary school education or no formal schooling. 42 3 0.7 FSW servicing 25 or more clients per month were less 67 3 0.7 likely to have any or oncogenic HPV infection compared 31 20.5 2 to those with fewer clients. The prevalence of any, onco- 35 20.5 82 20.5 genic, and multiple HPV infection was significantly lower 64 1 0.2 among FSW engaging in withdrawal prior to ejaculation. Untyped 99 22.6 FSW using IUDs were less likely to be infected with multi- ple HPV types. The prevalence of HPV (any, oncogenic, Total 438 100 and multiple infection) was significantly greater among HIV+ women. Apart from their commercial sex work, FSW 239 HPV+ sex workers; 88 HPV+ for 2 or more genotypes with regular male partners who had other female partners Oncogenic/probable oncogenic genotypes Page 2 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 <20 20-24 25-29 30-34 35-39 40+ age group (years) Preval Figure 1 ence of cervical HPV in sex workers by age, Soctrang province, Vietnam Prevalence of cervical HPV in sex workers by age, Soctrang province, Vietnam. were more likely to have all 3 HPV outcomes while those Cambodia. Sex workers commonly traverse between the 2 with male partners ages 30 years and older were more countries through these areas. It is possible that these likely to have any infection. highly transient sex workers are at particularly high risk for HPV. The substantial proportions of multiple infec- Discussion tions and untyped specimens are consistent with a high- Our results demonstrate that cervical HPV infection is risk population with exposure to many different partners. extremely common among southern Vietnamese sex workers with an overall prevalence nearly twice that of Oncogenic HPV 52 was more common than HPV 16 in chlamydia. HPV prevalence in the present study was much this population of sex workers. HPV 52 is one of the most higher than that observed in a population-based preva- common types found among women in southeast Asia as lence study of HPV in Vietnam [4]. In Ho Chi Minh City, well as eastern Asia including women with normal cervi- the major city of southern Vietnam, 10.9% of women cal cytology as well as those with SIL and carcinoma [6]. were positive for cervical HPV DNA compared to 2.0% of HPV 16 is estimated to be responsible for the majority of women in Hanoi, the major city of northern Vietnam [4]. invasive cervical cancers. It is not known whether the pro- The prevalence of HIV among sex workers in Vietnam portion of cervical cancers attributed to HPV 16 in south- shown similar geographic disparities with rates in the ern Vietnam, which has among the highest rates of southern border higher than that in the north and central cervical cancer in the world [1,2], is different from other regions [5]. parts of the world. The basis for these differences in the prevalence of HPV The lack of variation of HPV prevalence with age among and other sexually transmitted infections by geographic these sex workers is contrary to what has been observed in region is not completely understood. It may reflect differ- North American, European, and some Asian populations. ences in sexual practices including the pervasiveness of The flat age curve in this population of sex workers is sim- prostitution by region. Soc Trang province, where nearly ilar to that observed in high-risk populations in India and 1/3 of the population is Khmer, is proximate to Kien Nigeria characterized by high cervical cancer incidence Giang, An Giang and Dong Thap provinces which border and mortality [7]. Page 3 of 9 (page number not for citation purposes) HPV preval ence (%) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 Table 2: Cervical HPV infection and characteristics of sex workers, Soc Trang province, Vietnam 1 1 1 No. (%) Any HPV Adj. PR (95% CI) Oncogenic HPV Adj. PR (95% CI) Multiple HPV Adj. PR (95% CI) Age (yrs.) <20 45 (16%) 1.00 1.00 1.00 20–29 175 (62%) 0.83 (0.62–1.10) 0.72 (0.48–1.09) 0.72 (0.41–1.25) 30+ 62 (22%) 0.78 (0.53–1.16) 0.79 (0.33–1.87) 0.88 (0.37–2.10) p trend = 0.35 p trend = 0.12 p trend = 0.07 Ethnicity Kinh 230 (82%) 1.00 1.00 1.00 Other 52 (18%) 1.14 (0.92–1.41) 1.10 (0.73–1.64) 1.02 (0.60–1.73) Marital Status Not Single 136 (48%) 1.00 1.00 1.00 Single 146 (52%) 1.02 (0.83–1.27) 1.29 (0.83–1.98) 1.68 (0.83–6.79) Education None 43 (15%) 1.00 1.00 1.00 Primary School 136 (48%) 0.94 (0.73–1.22) 0.78 (0.48–1.25) 0.63 (0.37–1.08) Secondary-high school 103 (37%) 0.80 (0.59–1.10) 0.57 (0.32–1.04) 0.43 (0.23–0.79) Age of regular partner (yrs.) <30 72 (47%) 1.00 1.00 1.00 30+ 81 (53%) 1.39 (1.09–1.76) 1.60 (1.13–2.27) 1.78 (1.14–2.78) Regular partner has other female 2,3 partners No 54 (36%) 1.00 1.00 1.00 Yes 97 (64%) 1.27 (1.04–1.54) 2.01 (1.34–3.00) 2.17 (1.30–3.62) Age at first sex 15 yrs 11 (4%) 1.00 1.00 1.00 >15 yrs 270 (96%) 0.84 (0.58–1.20) 1.09 (0.54–2.19) 0.77 (0.35–1.69) Duration of commercial sex work <1 year 54 (19%) 1.00 1.00 1.00 1 – 3 years 125 (44%) 1.11 (0.79–1.57) 0.88 (0.61–1.27) 0.97 (0.65–1.45) > 3 years 103 (37%) 1.16 (0.78–1.72) 0.96 (0.62–1.49) 1.20 (0.76–1.88) p trend = 0.11 p trend = 0.02 p trend = 0.03 Venue for sex work Indirect venues 148 (52%) 1.00 1.00 1.00 Direct venues 134 (48%) 1.03 (0.87–1.22) 1.11 (0.77–1.59) 0.99 (0.68–1.44) No. of clients per month (average) <10 97 (34%) 1.00 1.00 1.00 10–25 85 (30%) 1.00 (0.88–1.15) 1.08 (0.79–1.46) 1.27 (0.75–2.13) >25 100 (36%) 0.64 (0.49–0.83) 0.43 (0.27–0.70) 0.52 (0.29–0.94) p trend = 0.16 p trend = 0.85 p trend = 0.69 Oral-penile contact Never 239 (85%) 1.00 1.00 1.00 Ever 43 (15%) 1.29 (0.94–1.78) 1.45 (0.74–2.82) 1.51 (0.70–6.55) Anal-penile contact Never 272 (96%) 1.00 1.00 1.00 Ever 10 (4%) 0.72 (0.40–1.34) 0.36 (0.14–0.92) 0.26 (0.10–0.69) Condom use with regular clients Not always 37 (16%) 1.00 1.00 1.00 Always 190 (84%) 1.13 (0.88–1.44) 1.58 (0.98–2.55) 1.68 (0.84–3.36) Page 4 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 Table 2: Cervical HPV infection and characteristics of sex workers, Soc Trang province, Vietnam (Continued) Condom use with irregular clients Not always 29 (13% 1.00 1.00 1.00 Always 189 (87%) 0.96 (0.70–1.30) 0.95 (0.69–1.30) 0.94 (0.60–1.49) Oral contraceptives Never 261 (93%) 1.00 1.00 1.00 Ever 20 (7%) 1.06 (0.81–1.40) 1.32 (0.84–2.07) 1.41 (0.75–2.64) Intrauterine device Never 218 (78%) 1.00 1.00 1.00 Ever 63 (22%) 0.89 (0.69–1.13) 0.63 (0.33–1.20 0.52 (0.28–0.99) Withdrawal Never 198 (70%) 1.00 1.00 1.00 Ever 83 (30%) 0.80 (0.67–0.96) 0.62 (0.42–0.89 0.58 (0.30–1.12) Illegal drugs Never 255 (91%) 1.00 1.00 1.00 Ever 26 (9%) 0.76 (0.54–1.06) 0.61 (0.33–1.13) 1.42 (0.80–2.52) Pregnant Never 144 (51%) 1.00 1.00 1.00 Ever 138 (49%) 1.00 (0.81–1.24 0.95 (0.61–1.46) 1.06 (0.59–1.92) Current STI status Trichomonas Negative 258 (92%) 1.00 1.00 1.00 Positive 23 (8%) 1.04 (0.78–1.39) 1.30 (0.84–2.02) 1.51 (0.76–3.00) Bacterial vaginosis Negative 200 (71%) 1.00 1.00 1.00 Positive 81 (29%) 1.10 (0.93–1.31) 1.07 (0.75–1.52) 1.30 (0.58–2.00) Yeast Negative 253 (90%) 1.00 1.00 1.00 Positive 28 (10%) 1.20 (0.97–1.49) 0.80 (0.51–1.25) 0.81 (0.39–1.69) Syphilis Negative 270 (96%) 1.00 1.00 1.00 Positive 11 (4%) 1.34 (0.84–2.16) 1.38 (0.65–2.93) 1.05 (0.42–2.67) HIV Negative 276 (98%) 1.00 1.00 1.00 Positive 5 (2%) 1.57 (0.98–2.51) 3.01 (1.01–9.00) 2.87 (0.69–12.00) Gonorrhea Negative 253 (90%) 1.00 1.00 1.00 Positive 28 (10%) 1.06 (0.91–1.24) 0.92 (0.89–1.45) 0.98 (0.68–2.86) Chlamydia Negative 161 (57%) 1.00 1.00 1.00 Positive 120 (43%) 0.99 (0.76–1.28) 0.95 (0.66–1.37) 0.98 (0.64–1.50) Prevalence ratio, adjusted for all variables 153 FSW had a regular male partner Responses missing from 2 subjects Response missing from 1 subject Direct venues include streets, parks, bus stops, boats, ferry piers, brothels, small cafés, and guesthouses; indirect venues include hotels, restaurants, massage parlors, karaoke lounges, bars, and barbershops. 227 FSW serviced regular clients 218 FSW serviced irregular clients Page 5 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 Table 3: Factors associated with cervical HPV infection in sex workers, Soc Trang province, Vietnam 1 1 1 Any HPV Adj. PR (95% CI) Oncogenic HPV Adj. PR (95% CI) Multiple HPV Adj. PR (95% CI) Education None 1.00 1.00 1.00 Primary School 0.92 (0.73–1.15) 0.80 (0.58–1.11) 0.82 (0.56–1.21) Secondary-high school 0.80 (0.61–1.04) 0.63 (0.42–0.93) 0.61 (0.38–0.99) No. of clients per month (average) <10 1.00 1.00 1.00 10–25 1.03 (0.92–1.16) 1.06 (0.87–1.30) 1.14 (0.83–1.57) >25 0.78 (0.65–0.94) 0.66 (0.48–0.92) 0.70 (0.47–1.06) p trend = 0.93 p trend = 0.43 p trend = 0.49 2,3 Regular partner has other female partners No 1.00 1.00 1.00 Yes 1.22 (1.03–1.44) 1.75 (1.34–2.28) 1.91 (1.41–2.60) Intrauterine device Never 1.00 1.00 1.00 Ever 0.85 (0.68–1.06) 0.58 (0.31–1.08) 0.53 (0.29–0.99) Withdrawal Never 1.00 1.00 1.00 Ever 0.84 (0.73–0.97) 0.68 (0.53–0.87) 0.60 (0.43–0.83) HIV Negative 1.00 1.00 1.00 Positive 1.20 (1.01–1.42) 1.42 (1.08–1.88) 1.45 (1.01–2.10) Age of regular partner (yrs.) <30 1.00 1.00 1.00 30+ 1.21 (1.03–1.44) 1.16 (0.92–1.46) 1.22 (0.86–1.73) Adjusted for all variables listed in addition to age, condom use with regular clients, gonorrhea, sex work venue 153 FSW had a regular male partner Responses missing from 2 subjects Response missing from 1 subject The observed association of education level with onco- infections. Consistent with this theory, compared to more genic and multiple-type HPV infection is consistent with experienced sex workers in Mexico City, an increased risk studies in other countries demonstrating an inverse asso- of HPV infection was observed among women involved in ciation of socioeconomic status and HPV [8,9]. Education prostitution for less than 1 year [13]. and other indicators of socioeconomic status may reflect differences in sexual practices, partner characteristics, and The lower prevalence of HPV among FSW engaging in other factors that influence exposure to the virus. withdrawal during intercourse is difficult to explain. Semen is not a major site of HPV infection in males com- Interestingly, HPV infection (any and oncogenic types) pared to the external genitals [14]. Furthermore, use of were less prevalent among FSW servicing the most clients. withdrawal is likely correlated with lack of use of con- Risk of cervical HPV infection has been consistently doms and other contraceptive methods. We also observed observed to increase with number of recent partners [10] a lower prevalence of multiple HPV infection among IUD and partners over the lifetime [11]. In contrast to the gen- users. Previous studies have demonstrated a protective eral female population, however, sex workers are likely to effect of IUD use with abnormal cervical cytology and cer- have consistent and repeated exposure to HPV with each vical adenocarcinoma [15,16]. new partner. It has been suggested that persistent, repeti- tive exposure to HPV antigen increases the development The prevalence of oncogenic and multiple HPV was and persistence of local immune responses [12]. Accord- higher among the limited number of HIV-positive women ingly, those sex workers with the largest number of clients in this population. This is consistent with studies of cervi- may be most protected from acquisition of new HPV cal HPV and HIV in other populations [17,18] and may Page 6 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 reflect the increased susceptibility to viral acquisition and/ Vietnam where the incidence of cervical cancer is one of or to viral persistence with HIV-induced immune suppres- the highest observed worldwide. Effective measures to sion. reduce the incidence of invasive cervical cancer in the pop- ulation will ideally incorporate both primary and second- Our results demonstrate that even among a high-risk pop- ary prevention efforts, including HPV vaccination and ulation such as commercial sex workers, the behavior of cervical screening. regular partners, including spouses and cohabitating part- ners, plays an important role in HPV acquisition. Sex Methods workers with regular male partners who engaged in sexual Study Recruitment relationships with other females were at increased risk of The study was approved by the Pasteur Institute, Ho Chi any, oncogenic, and multiple HPV infection. While other Minh City and the Standing Bureau for HIV/AIDS in Soc studies have demonstrated that the important role of men Trang province (currently known as the Soc Trang Center who are serviced by prostitutes in transmission of HPV to for HIV/AIDS Control and Prevention). their wives [11,19], the present study demonstrates that even for high-risk females, the behavior of their regular Initially, a mapping process to identify local sites where male partners are key to the acquisition of the virus. This FSW could be found and the numbers of FSW in each hot may indicate that HPV transmission is most efficient with spot was conducted by meeting with various local provin- repeated exposure to the same source relative to one-time cial and district sector officials, including health workers, or periodic exposures. police, the women's union, the Department of Labor, Invalid and Social Affairs, and peer educators. Interestingly, the relationship of partner's age and HPV prevalence contrasts with other sexually transmitted infec- Using the information from mapping, 406 FSW in Soc tions. A previous study of sex workers in Vietnam found Trang province were identified and invited to participate that age of partners was inversely associated with risk of in a cross-sectional study between May and August 2003. gonorrhea and chlamydia [20]. It is possible that HPV is a Because no lists of FSW were available, it was impossible more persistent infection in older men such that older to do systematic random sampling to recruit subjects in partners are more likely to transmit infections. each hot spot. After obtaining agreement from the owners of establishments and FSW, subjects were recruited by Observations of the role of condoms in HPV infection are convenience sampling. The number of refusals (FSW who inconsistent and conflicting [11,21,22]. The large major- avoided meeting with the interviewers) was not known. ity of sex workers reported 100% use of condom with reg- Verbal informed consent was obtained from all study sub- ular clients. However, information on condom use with jects. regular partners was not collected. It is possible that con- doms were less likely to be used with regular partners Specimen collection thereby increasing the risk of acquiring sexually transmit- Blood specimens were obtained for serological measure- ted infections from those partners who had other sexual ment of syphilis (rapid plasma regain; Bio-Rad) and HIV relationships. (SFD HIV 1/2 PA, Bio-Rad). Positive sera were first stored at -20°C, then batched and sent to the Pasteur Institute in Given the transient nature of most HPV infections, this Ho Chi Minh City every two weeks for confirmation with cross-sectional study offers a limited perspective of the two ELISA tests for HIV (Murex HIV 1.2.0, Abbott; Gen- natural history of HPV in this high-risk population. The screen HIV 1/2 V.2, Bio-Rad) and the Treponema pallidum minority of sex workers who were negative for HPV in the hemagglutination assay (Bio-Rad) for syphilis. present study were likely infected in the past and subse- quently cleared these HPV infections. The HPV-positive Vaginal fluid specimens were obtained for microscopic sex workers observed in this study may disproportionately and clinical identification of trichomoniasis and candi- include those with persistent infections. The ability to dis- diasis. Bacterial vaginosis was defined by Amsel criteria. tinguish factors associated with any, oncogenic, and mul- Cervical secretions were collected and temporarily stored tiple infection was limited as many women were positive at -20 degrees C prior to transport to the Pasteur Institute for multiple HPV types including concurrent oncogenic in Ho Chi Minh City where they were stored at -70 degrees and non-oncogenic types. C. DNA was extracted from cervical specimens and used for PCR-based testing of chlamydia, gonorrhea, and HPV. Conclusion The dynamics of HPV transmission are not well under- Interview stood. Our study demonstrates that sex workers may be Study subjects were interviewed by trained interviewers important reservoirs of HPV infection within southern using a structured questionnaire. Social and demographic Page 7 of 9 (page number not for citation purposes) Infectious Agents and Cancer 2008, 3:7 http://www.infectagentscancer.com/content/3/1/7 information and behavioral and sexual characteristics Acknowledgements This project was supported by Service laique de Cooperation au Develop- were queried. ment, Belgium (SLCD) and the Centers of Biomedical Research Excellence (COBRE) Program award P20 RR018727 from the National Center for HPV DNA testing, genotyping, and variant analysis Research Resources (NCRR), National Institutes of Health. Its contents are Frozen cervical DNA was sent to the Cancer Research solely the responsibility of the authors and do not necessarily represent the Center of Hawaii in Hawaii, U.S.A. for HPV DNA testing official views of NIH. The authors have no commercial or other association and genotyping. The PCR reaction utilized PGMY09/ that might pose a conflict of interest. PGMY11 primers [23] to amplify a 450 base pair region of the L1 HPV genome (nt 6582–7033). The authors would like to acknowledge the following individuals for their contributions to this study: Dr. Tien Kim Thi Nguyen of the Ministry of Health; Dr. Nghia Van Khuu, Dr. Lien Xuan Thi Truong, Dr. Van Cao, Ms. HPV-positive specimens were subsequently genotyped Phuong Kim Thi Tran, and Mr. Phuc Duy Nguyen of the Pasteur Institute using a reverse line blot detection method [24] (Roche Ho Chi Minh City; Dr. Phong Hoai Truong, Dr.Anh Phuong Nguyen of the Molecular Systems) for 37 different HPV types including Soc Trang Health Department, Dr.An Ngoc Tran & Dr. The (Soc Trang oncogenic/probable oncogenic types (HPV 16, 18, 26, 31, Center for Social Diseases), Dr. Thuc Van Nguyen, Dr. Truc TT.Le, (Hos- 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 68, 73, 82, IS39), pital for Dermato-Venereology of Ho Chi Minh City) ; Mrs. Marie Claire non-oncogenic types (HPV 6, 11, 40, 42, 54, 61, 70, 72, Rabier of the SLCD; Dr. Xuemei Zhu of the Cancer Research Center of 81, CP6108), and types with undetermined risk status Hawaii; and Dr. Richard Yanagihara of the John A. Burns School of Medi- cine, University of Hawaii. (HPV 55, 62, 64, 67, 69, 71, 83, 84) [25,26]. HPV-positive specimens that were subsequently found to be negative in References the genotyping assay were considered to be untyped HPV- 1. Quoc NM, Hung NC, Parkin DM: Cancer incidence in Ho Chi positive specimens. The HPV testing and genotyping pro- Minh City Viet Nam, 1995–1996. Int J Cancer 1998, 76:472-79. cedure has been detailed previously [27]. 2. Bray F, Parkin DM: Chapter 2: The burden of HPV-related can- cers. Vaccine 2006, 24(Suppl 3):S11-25. 3. Bosch FX, de SS: Chapter 1: Human papillomavirus and cervi- All specimens were also tested using GH20 and PC04 cal cancer–burden and assessment of causality. J Natl Cancer primers to amplify a 268 base pair region of the human Inst Monogr 2003, 31:3-13. 4. 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