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Prevalence and factors associated with hepatitis B and D virus infections among migrant sex workers in Chiangmai, Thailand: A cross-sectional study in 2019

Open AccessPublished:September 05, 2020DOI:https://doi.org/10.1016/j.ijid.2020.09.004

      Highlights

      • The prevalence of hepatitis B surface antigen (HBsAg) among migrant sex workers in Chiangmai, Thailand was 11.4%.
      • HBsAg prevalence was higher in males (14.7%) than in females (8.1%).
      • One-third of this young population were still susceptible to HBV infection.
      • No HBsAg-positive participants had anti-hepatitis delta virus antibodies.
      • Several factors related to HBsAg positivity are described.

      Abstract

      Objectives

      To determine the prevalence of hepatitis B surface antigen (HBsAg) and antibody to hepatitis delta virus (anti-HDV) and associated factors among migrant sex workers in Chiangmai, Thailand.

      Methods

      This cross-sectional study was conducted at various sexual entertainment venues in Chiangmai, Thailand, in 2019. Consenting participants were interviewed using a questionnaire, and plasma was tested for hepatitis B virus (HBV) markers (DiaSorin, Italy) and anti-HDV antibody (DIA.PRO Diagnostic Bioprobes, Italy), if HBsAg-positive. Associations between HBsAg positivity or HDV antibody and potential factors were examined using univariable and multivariable logistic regression analysis.

      Results

      A total of 396 migrant sex workers, half of them female, were recruited between February and September 2019. Their median age was 25 years (interquartile range 22–30 years) and 95% were Burmese. Overall, HBsAg prevalence was 11.4%; 8.1% in females and 14.7% in males (Chi-square, p = 0.040). One-third were still susceptible to HBV. No HBsAg-positive participants had anti-HDV antibodies. HBsAg positivity was associated with being male (adjusted odds ratio (aOR) 3.01, 95% confidence interval (CI) 1.25–7.68, p = 0.014), having attended school (aOR 4.50, 95% CI 1.26–15.98, p = 0.020), being separated/divorced/widowed (aOR 5.77, 95% CI 1.48–22.52, p = 0.012), and having unprotected sex (aOR 3.38, 95% CI 1.31–8.71, p = 0.012).

      Conclusions

      In this young population, higher HBsAg prevalence in males may be related to sexual transmission, indicating the need for HBV screening programs linked with HBV prevention and care.

      Keywords

      Introduction

      Hepatitis B virus (HBV) is a major cause of chronic viral hepatitis, severe liver diseases, and liver cancer. Approximately 250 million people worldwide are chronically infected with HBV and it is estimated that one million people die annually, mostly from cirrhosis and hepatocellular carcinoma (). About 5% of chronic HBV carriers are co-infected with hepatitis delta virus (HDV) (), which is a defective RNA virus that requires hepatitis B surface antigen (HBsAg) for its replication (
      • Taylor J.M.
      Replication of human hepatitis delta virus: recent developments.
      ). Individuals with chronic hepatitis B develops a more severe hepatitis disease when they are superinfected with HDV (
      • Gupta P.
      • Biswas D.
      • Shukla I.
      • Bal A.
      Need for routine screening of HBV and HDV in patients with cirrhosis of the liver.
      ). The main routes of transmission of these two viruses include perinatal transmission and parenteral or sexual contact with infected blood or body fluids.
      Sex workers are considered as a high-risk group for the acquisition and transmission of HIV, as well as other sexually transmitted infections (STIs), due to the nature of their work and their sexual practices, e.g. high number of sexual partners, high frequency of unprotected sex. Furthermore, migrant sex workers are a more vulnerable population due to their legal status and have been shown to be at a greater risk of STIs and blood-borne infections than non-migrant sex workers, in both low-income and high-income countries (
      • Platt L.
      • Grenfell P.
      • Fletcher A.
      • Sorhaindo A.
      • Jolley E.
      • Rhodes T.
      • et al.
      Systematic review examining differences in HIV, sexually transmitted infections and health-related harms between migrant and non-migrant female sex workers.
      ).
      Chiangmai province is in the North of Thailand and is the second-largest province of the country. It shares a border with Myanmar. Chiangmai city is the economic and tourist hub of the northern region and one of the most important tourist destinations in Thailand. In 2015, the Foreign Workers Administration Office of Thailand estimated that about 102,000 migrants were legal workers in Chiangmai; most of them were Tai-Yai, Shan, and Karen. The number of illegal migrant workers is unknown, and due to legal or language barriers, they are often employed in the informal sectors such as childcare and sex work (
      • Barmania S.
      Thailand’s migrant sex workers struggle to access health care.
      ). Moreover, most migrant sex workers do not have an identification card, leading to problems in accessing health services. Many migrant sex workers come from neighboring countries where universal hepatitis B vaccine policies were implemented in the early 2000s and are still highly endemic for chronic hepatitis B. Most have limited knowledge of HBV infection and its clinical consequences, and are unaware of their hepatitis B status. Moreover, most investigations in sex workers in Thailand have focused on the prevalence of and factors associated with HIV infection and other STIs such as syphilis, chlamydia, gonorrhea (
      • Celentano D.D.
      • Akarasewi P.
      • Sussman L.
      • Suprasert S.
      • Matanasarawoot A.
      • Wright N.H.
      • et al.
      HIV-1 infection among lower class commercial sex workers in Chiang Mai, Thailand.
      ,
      • Chemnasiri T.
      • Netwong T.
      • Visarutratana S.
      • Varangrat A.
      • Li A.
      • Phanuphak P.
      • et al.
      Inconsistent condom use among young men who have sex with men, male sex workers, and transgenders in Thailand.
      ,
      • Kilmarx P.H.
      • Palanuvej T.
      • Limpakarnjanarat K.
      • Chitvarakorn A.
      • St Louis M.E.
      • Mastro T.D.
      Seroprevalence of HIV among female sex workers in Bangkok: evidence of ongoing infection risk after the “100% condom program” was implemented.
      ,
      • Kunawararak P.
      • Beyrer C.
      • Natpratan C.
      • Feng W.
      • Celentano D.D.
      • de Boer M.
      • et al.
      The epidemiology of HIV and syphilis among male commercial sex workers in northern Thailand.
      ,
      • Limpakarnjanarat K.
      • Mastro T.D.
      • Saisorn S.
      • Uthaivoravit W.
      • Kaewkungwal J.
      • Korattana S.
      • et al.
      HIV-1 and other sexually transmitted infections in a cohort of female sex workers in Chiang Rai, Thailand.
      ,
      • Manopaiboon C.
      • Prybylski D.
      • Subhachaturas W.
      • Tanpradech S.
      • Suksripanich O.
      • Siangphoe U.
      • et al.
      Unexpectedly high HIV prevalence among female sex workers in Bangkok, Thailand in a respondent-driven sampling survey.
      ,
      • van Griensven G.J.
      • Limanonda B.
      • Chongwatana N.
      • Tirasawat P.
      • Coutinho R.A.
      Socio-economic and demographic characteristics and HIV-1 infection among female commercial sex workers in Thailand.
      ). Data on HBV and HDV prevalence are more limited.
      This study was performed to analyze the prevalence of and factors associated with HBV and HDV infections among a population of migrant sex workers in Chiangmai, Thailand.

      Materials and methods

      Study population and inclusion criteria

      This cross-sectional survey was conducted among migrant sex workers in Chiangmai, Thailand, between February and September 2019. Eligible participants were individuals of both sexes (male and female), who were non-Thai citizens, aged 18 years or more, and who had traded sex for money in the past year. Participants were recruited from various sexual entertainment venues (e.g., karaoke, bars, clubs, massage parlors, and restaurants).
      The study was approved by the Human Experimentation Committee of the Research Institute for Health Sciences, Chiang Mai University (Number 19/61). Potential participants were informed about the study and signed a consent form. Their participation in the study was kept confidential. Participants were identified with a code (no names) that was used to link each participant with the questionnaire, blood samples, and test results.

      Data collection methods

      Participants were administered a face-to-face standard questionnaire by trained interviewers speaking the same language. The interviews were conducted in their workplaces, where participants felt comfortable and safe. Data were collected using a structured questionnaire with seven sections covering socio-demographic characteristics, health behavior, sexual behavior, quality of life, rating scale for depression, HIV knowledge, and HBV and hepatitis C virus (HCV) knowledge. For this sub-study, only socio-demographic information, medical history, health behaviors, risk behaviors, and sexual behaviors data were included.

      Blood processing and laboratory testing for HBV markers and anti-HDV

      After the interview, 6 ml of peripheral blood was collected from each participant and transferred to the laboratory for processing. Plasma was separated and kept frozen at −70 °C until testing for HBV markers and anti-HDV antibody. Plasma samples were first tested for HBsAg using MUREX® HBsAg version 3 (DiaSorin, Saluggia-Vercelli, Italy) (97% sensitivity and 98% specificity). Samples negative for HBsAg were then tested for antibody to hepatitis B surface antigen (anti-HBs) levels using ETI-AB-AUK-3 anti-HBs (99.1% sensitivity and 98.2% specificity) and antibody to hepatitis B core antigen (anti-HBc) using MUREX® anti-HBc total (100% sensitivity and 99.7% specificity), according to the manufacturer’s protocols (DiaSorin, Saluggia-Vercelli, Italy). Participants with an anti-HBs antibody level >10 IU/mL were considered as having protective immunity against HBV.
      HBsAg-negative participants were categorized into four groups according to their anti-HBs and anti-HBc serology results: (1) resolved HBV infection if anti-HBc and anti-HBs were positive; (2) exposed to HBV if only anti-HBc was positive; (3) HB vaccinated if only anti-HBs was positive; (4) susceptible to HBV infection if both anti-HBc and anti-HBs were negative.
      Participants testing HBsAg-positive were tested for anti-HDV antibody using the HDV antibody test (98% sensitivity and 98% specificity) according to the manufacturer’s protocol (DIA.PRO; Diagnostic Bioprobes, Milan, Italy).
      The results of laboratory tests were delivered to participants on presentation of their card number in private places. Participants who tested positive for HBsAg received information about the prevention and management of HBV and HDV infection and were encouraged to attend the health center of their choice for clinical care.

      Data analysis

      Categorical variables are presented as frequencies and percentages and continuous variables are described using the median with interquartile range (IQR). Continuous variables were dichotomized using common cutoff values. The prevalence of HBV markers and anti-HDV are reported with the 95% confidence interval (95% CI).
      The variables analyzed for association with HBsAg positivity were socio-demographic data (i.e., sex, age, race, education, workplace, marital status), health behaviors (i.e., smoking, alcohol consumption, drug use), medical history (i.e., surgery or blood transfusion, STIs), risk behaviors (i.e., sharing sharp personal equipment, piercing/tattoos, visiting a barber, circumcision), and sexual behaviors (i.e., sexual identity, age at first sexual activity, number of sexual partners, sexual behavior, and condom use).
      Univariable analyses were performed using logistic regression to identify factors potentially associated with HBV infection. Variables with a p-value lower than 0.250 in the univariable analysis were entered into a multivariable analysis, and a backward elimination procedure was used to identify factors independently associated with HBsAg positivity. All data analyses were performed using Stata version 14.0 software (StataCorp, College Station, TX, USA). Differences were considered statistically significant if the p-value was ≤0.05.

      Results

      Study population characteristics

      A total of 396 sex workers were recruited. Their characteristics are described in Table 1. Fifty percent of participants were female. The median age of the participants was 25 years (IQR 22–30 years). Almost all were Shan/Tai-Yai (91.7%) and had been born in Myanmar (92.9%). A large majority (70.2%) had received an education either in their country of origin or in Thailand. The median duration of living in Thailand was 9 years (IQR 4–16 years). More than half were single and one-third had children. The median monthly income was 10,000 Baht ($320).
      Table 1Socio-demographic, behavioral, and medical history characteristics of migrant sex workers in Chiangmai, Thailand, 2019.
      Total (n = 396)

      n (%) or value
      Female (n = 198)

      n (%) or value
      Male (n = 198)

      n (%) or value
      Socio-demographic information
      Age (years), median (IQR)25 (22–30)27 (23–31)24 (22–28)
      Age (years)
       ≤2040 (10.0)14 (7.1)26 (13.1)
       21–30277 (70.0)129 (65.1)148 (74.8)
       >3079 (20.0)55 (27.8)24 (12.1)
      Country of birth
       Myanmar368 (92.9)186 (94.0)182 (91.9)
       Laos4 (1.0)3 (1.5)1 (0.5)
       Thailand24 (6.1)9 (4.5)15 (7.6)
      Race/ethnicity, n = 372
       Shan/Tai-Yai341 (91.7)171 (90.5)170 (93.0)
       Burmese12 (3.2)3 (1.6)9 (4.9)
       Laotian4 (1.1)3 (1.6)1 (0.5)
       Other15 (4.0)12 (6.3)3 (1.6)
      Education278 (70.2)130 (65.7)148 (74.7)
      Median duration, years (IQR)6 (4–10)6 (3–10)6 (5–10)
      Education duration (years)
       0–3 years (non-primary)62 (22.3)36 (27.7)26 (17.5)
       4–9 years (primary)143 (51.4)59 (45.4)84 (56.8)
       >9 years (secondary or higher)73 (26.3)35 (26.9)38 (25.7)
      Religion: Buddhism375 (94.7)185 (93.4)190 (96.0)
      Current workplace (>1 answer can be chosen)
       Karaoke208 (52.5)167 (84.3)41 (20.7)
       Traditional massage52 (13.1)17 (8.6)35 (17.7)
       Spa and sauna2 (0.5)02 (1.0)
       Restaurants23 (5.8)2 (1.0)21 (10.6)
       Rural roadside bar25 (6.3)1 (0.5)24 (12.1)
       Pub/bar80 (20.2)2 (1.0)78 (39.4)
       Massage parlor21 (5.3)18 (9.1)3 (1.5)
       Other
      Other: labor, housemaid, officer, handicraft maker, factory worker, online business, salesman.
      26 (6.6)6 (3.0)20 (10.1)
      Median duration of stay in Thailand, years (IQR)9 (4–16)12 (4–20)8 (5–12)
      Marital status
       Single221 (55.8)94 (47.5)127 (64.1)
       Has a partner135 (34.1)70 (35.4)65 (32.8)
       Separated/divorced/widowed40 (10.1)34 (17.1)6 (3.0)
      Has children131 (33.1)99 (50.0)32 (16.2)
      Median monthly income, Baht (IQR)10 000 (9000–17 000)15 000 (10 000–20 000)10 000 (9000–12 000)
      Health behavior information
      Smoking (past 3 months)135 (34.1)27 (13.6)108 (54.5)
      Drinking alcohol (past 3 months)358 (90.4)180 (90.9)178 (89.9)
      Drugs use (past 3 months)18 (4.5)5 (2.5)13 (6.6)
      Drug injection3 (0.8)03 (1.5)
      Medical history
      The answer “I don’t know” was considered as missing data.
      Ever had a surgery or blood transfusion74/393 (18.8)62/197 (31.5)12/196 (6.1)
      Ever had HB vaccination31/344 (9.0)27/160 (16.9)4/184 (2.2)
      Ever been diagnosed with STIs
      Sexually transmitted infections (STIs): gonorrhea, non-gonorrhea, syphilis, HIV, HBV, HCV, or genital herpes.
      106/240 (44.2)42/145 (29.0)64/95 (67.4)
      Risk behavior
      The answer “I don’t know” was considered as missing data.
      Ever had needle-stick injury16/391 (4.1)8/197 (4.1)8/194 (4.1)
      Ever shared sharp personal care items with others195/396 (49.2)137/198 (69.2)58/198 (29.3)
      Ever had tattoo or piercing on any part of body357/396 (90.2)188/198 (95.0)169/198 (85.4)
      Ever visited a community barber for shaving (males)78/198 (39.4)78/198 (39.4)
      Ever had circumcision (males)11/198 (5.6)11/198 (5.6)
      Sexual behavior
      Sexual identity
       Heterosexual208 (52.5)188 (95.0)20 (10.1)
       Homosexual7 (1.8)1 (0.5)6 (3.0)
       Bisexual181 (45.7)9 (4.5)172 (86.9)
      Median age at first sexual activity, years (IQR)17 (16–18)17 (16–18)17 (16–18)
      Total number of sexual partners (lifetime)
       <10 persons66 (16.7)37 (18.7)29 (14.7)
       10–49 persons125 (31.6)56 (28.3)69 (34.8)
       50–99 persons106 (26.8)39 (19.7)67 (33.8)
       100–149 persons44 (11.1)31 (15.7)13 (6.6)
       150–199 persons9 (2.2)7 (3.5)2 (1.0)
       ≥200 persons46 (11.6)28 (14.1)18 (9.1)
      Number of sexual partners per day (past 3 months)
       <1 person64 (16.2)20 (10.1)44 (22.2)
       1–2 persons217 (54.8)129 (65.1)88 (44.4)
       3–4 persons93 (23.5)36 (18.2)57 (28.8)
       ≥5 persons22 (5.5)13 (6.6)9 (4.5)
      Vaginal sex383 (96.7)197 (99.5)186 (93.9)
      Anal sex177 (44.7)1 (0.5)176 (88.9)
      Ever been forced to have sexual intercourse25 (6.3)13 (6.6)12 (6.1)
      In the past months, have had sex with husband/wife/lover265 (66.9)126 (63.6)139 (70.2)
       Always used condoms45 (17.0)25 (19.8)20 (14.4)
       Occasionally used condoms65 (24.5)18 (14.3)47 (33.8)
       Never used condoms155 (58.5)83 (65.9)72 (51.8)
      In the past months, have had sex with casual partners (including sex workers)321 (81.1)152 (76.8)169 (85.4)
       Always used condoms282 (87.9)143 (94.0)139 (82.2)
       Occasionally used condoms37 (11.5)8 (5.3)29 (17.2)
       Never used condoms2 (0.6)1 (0.7)1 (0.6)
      HB, hepatitis B; IQR, interquartile range; STI, sexually transmitted infection.
      a Other: labor, housemaid, officer, handicraft maker, factory worker, online business, salesman.
      b The answer “I don’t know” was considered as missing data.
      c Sexually transmitted infections (STIs): gonorrhea, non-gonorrhea, syphilis, HIV, HBV, HCV, or genital herpes.
      During the past 3 months, most participants (90.4%) reported having consumed alcohol, 34.1% reported smoking, and 4.5% reported experiencing drug abuse. Three participants (0.8%) reported a history of injecting drugs. In the past 12 months, 44.2% of them had been diagnosed with STIs. Almost all had tattoos or ear–nose–body piercings (90.2%). The median age at first sexual activity was 17 years (IQR 16–18 years). Half (54.8%) had one to two sexual partners per day. The majority always used condoms while having sex with casual partners other than their husband or wife.

      Prevalence of HBsAg positivity and serological status

      Of the 396 participating migrant sex workers, 56.1% (111 of 198) of females and 61.6% (122 of 198) of males presented markers of current or past HBV infection (Table 2). Of the 351 who were HBsAg-negative, 138 (39.3%) were considered as having resolved their HBV infection, 50 (14.2%) as having been previously exposed to HBV, 15 (4.3%) as vaccinated, and 148 (42.2%) as susceptible to HBV infection.
      Table 2HBV serological status of migrant sex workers in Chiangmai, Thailand.
      HBV serological status
      HBV-infected: HBsAg-positive. Resolved HBV infection: HBsAg-negative, anti-HBc-positive, anti-HBs-positive. Exposure to HBV: HBsAg-negative, anti-HBc-positive, anti-HBs-negative. HB vaccinated: HBsAg-negative, anti-HBc-negative, anti-HBs-positive. Susceptible to HBV infection: HBsAg-negative, anti-HBc-negative, anti-HBs-negative.
      TotalFemalesMales
      Nn% (95% CI)Nn% (95% CI)Nn% (95% CI)
      HBV-infected3964511.4 (8.6–14.9)198168.1 (5.0–12.8)1982914.7 (10.3–20.3)
      Resolved HBV infection35113839.3 (34.3–44.6)1826435.2 (28.5–42.4)1697443.8 (36.5–51.4)
      Exposure to HBV3515014.2 (10.9–18.3)1823117.0 (12.2–23.2)1691911.2 (7.3–17.0)
      HB vaccinated351154.3 (2.6–7.0)182116.0 (3.4–10.6)16942.4 (0.9–6.2)
      Susceptible to HBV infection35114842.2 (37.1–47.4)1827641.8 (34.8–49.1)1697242.6 (35.3–50.2)
      Anti-HBc, antibody to hepatitis B core antigen; anti-HBs, antibody to hepatitis B surface antigen; CI, confidence interval; HB, hepatitis B; HBsAg, hepatitis B surface antigen; HBV, hepatitis B virus.
      a HBV-infected: HBsAg-positive. Resolved HBV infection: HBsAg-negative, anti-HBc-positive, anti-HBs-positive. Exposure to HBV: HBsAg-negative, anti-HBc-positive, anti-HBs-negative. HB vaccinated: HBsAg-negative, anti-HBc-negative, anti-HBs-positive. Susceptible to HBV infection: HBsAg-negative, anti-HBc-negative, anti-HBs-negative.
      The overall prevalence of HBsAg positivity was 11.4% (95% CI 8.6–14.9%) (Table 3); the prevalence was 8.1% (95% CI 5.0–12.8% ) in females and 14.7% (95% CI 10.3–20.3%) in males (Chi-square, p = 0.040). The prevalence of HBsAg positivity tended to increase with age. Among migrant sex workers aged 21–30 years, the overall prevalence of HBsAg positivity was 11.2%, and it was higher in males than in females (16.2% vs 5.4%; Chi-square, p = 0.004). The prevalence of HBsAg positivity according to sex and other variables is described in Table 3.
      Table 3Prevalence of HBsAg positivity among migrant sex workers in Chiangmai, Thailand, 2019.
      TotalFemaleMale
      Nn% (95% CI)Nn% (95% CI)Nn% (95% CI)
      HBsAg positivity3964511.4 (8.6–14.9)198168.1 (5.0–12.8)1982914.7 (10.3–20.3)
      Socio-demographic information
      Age (years)≤204037.5 (2.4–21.1)14214.3 (3.4–44.3)2613.8 (0.5–23.7)
      21–302773111.2 (8.0–15.5)12975.4 (2.6–11.0)1482416.2 (11.1–23.1)
      >30791114.0 (7.8–23.5)55712.7 (6.1–24.6)24416.7 (6.2–37.6)
      Country of birthMyanmar3684010.9 (8.1–14.5)186137.0 (4.1–11.7)1822714.8 (10.3–20.8)
      Laos4125.0 (2.4–82.1)3133.3 (2.5–90.6)100 (N/A)
      Thailand24416.7 (6.2–37.5)9222.2 (5.1–60.5)15213.3 (3.2–42.0)
      Race/ethnicityShan/Tai-Yai3413710.9 (8.0–14.6)171116.4 (3.6–11.3)1702615.3 (10.6–21.6)
      Burmese1218.3 (1.1–43.7)300 (N/A)9111.1 (1.3–53.5)
      Laotian4125.0 (2.4–82.1)3133.3 (2.5–90.6)100 (N/A)
      Other15213.3 (3.2–41.9)12216.7 (3.9–49.7)300 (N/A)
      School attendingNo118108.5 (4.6–15.1)6834.4 (1.4–13.0)50714.0 (6.7–26.8)
      Yes2783512.6 (9.2–17.1)1301310.0 (5.9–16.5)1482214.9 (10.0–21.6)
      Current workplaceKaraoke208209.6 (6.3–14.5)167148.4 (5.0–13.7)41614.6 (6.6–29.3)
      Traditional massage52815.4 (7.8–28.1)17317.6 (5.6–43.9)35514.3 (6.0–30.5)
      Spa and sauna200 (N/A)000200 (N/A)
      Restaurants23417.4 (6.5–38.9)2150.0 (1.9–98.1)21314.3 (4.5–37.0)
      Rural roadside bar25312.0 (3.8–31.9)111002428.3 (2.0–28.7)
      Pub/bar801215.0 (8.7–24.7)200 (N/A)781215.4 (8.9–25.3)
      Massage parlor2100 (N/A)1800 (N/A)300 (N/A)
      Other
      Other: labor, housemaid, officer, handicraft maker, factory worker, online business, salesman.
      26311.5 (3.7–30.9)6116.7 (1.8–68.1)20210.0 (2.4–33.4)
      Marital statusSingle221188.1 (5.2–12.6)9444.3 (1.6–10.9)1271411.0 (6.6–17.8)
      Has a partner1351914.1 (9.1–21.1)7057.1 (3.0–16.2)651421.5 (13.1–33.3)
      Separated/divorced/ widowed40820.0 (10.2–35.5)34720.6 (10.0–37.7)6116.7 (1.8–68.1)
      Has childrenNo2652910.9 (7.7–15.3)9977.1 (3.4–14.2)1662213.3 (8.9–19.4)
      Yes1311612.2 (7.6–19.1)9999.1 (4.8–16.7)32721.9 (10.6–39.7)
      Health behavior
      Smoking (past 3 months)No2612710.3 (7.2–14.7)171148.2 (4.9–13.4)901314.4 (8.5–23.4)
      Yes1351813.3 (8.5–20.2)2727.4 (1.8–25.9)1081614.8 (9.2–22.9)
      Drinking alcohol (past 3 months)No38821.1 (10.8–37.1)18316.7 (5.3–41.9)20525.0 (10.5–48.7)
      Yes3583710.3 (7.6–14.0)180137.2 (4.2–12.1)1782413.5 (9.2–19.4)
      Drug user (past 3 months)No3784211.1 (8.3–14.7)193168.3 (5.1–13.2)1852614.1 (9.7–20.0)
      Yes18316.7 (5.3–41.8)500 (N/A)13323.1 (7.2–53.7)
      Drug injectionNo3934511.5 (8.7–15.0)198168.1 (5.0–12.8)1952914.9 (10.5–20.6)
      Yes300 (N/A)000300 (N/A)
      Medical history
      Ever had a surgery or blood transfusionNo3193811.9 (8.8–16.0)135128.9 (5.1–15.1)1842614.1 (9.8–20.0)
      Yes7479.4 (4.5–18.6)6246.4 (2.4–16.2)12325.0 (7.8–56.8)
      Ever had an HBV vaccinationNo3133711.8 (8.7–15.9)133107.5 (4.1–13.5)1802715.0 (10.5–21.1)
      Yes31516.1 (6.8–33.8)27414.8 (5.5–34.1)4125.0 (2.3–82.2)
      Ever been diagnosed with STI
      Sexually transmitted infections (STIs): gonorrhea, non-gonorrhea, syphilis, HIV, HBV, HCV, or genital herpes.
      No134129.0 (5.1–15.2)10365.8 (2.6–12.5)31619.4 (8.8–37.5)
      Yes1061413.2 (7.9–21.2)42614.3 (6.5–28.7)64812.5 (6.3–23.2)
      Risk behavior
      Ever shared sharp personal care items with othersNo2012211.0 (6.9–22.1)6123.3 (0.8–12.4)1402014.3 (9.4–21.2)
      Yes1952311.8 (8.0–15.0)1371410.2 (6.1–16.6)58915.5 (8.2–27.4)
      Ever had tattoo or piercing on any part of bodyNo39718.0 (8.7–33.4)1000 (N/A)29724.1 (11.8–43.2)
      Yes3573810.6 (7.8–14.3)188168.5 (5.2–13.5)1692213.0 (8.7–19.0)
      Ever visited a community barber for shaving (males)No120119.2 (5.1–15.9)120119.2 (5.1–15.9)
      Yes781823.1 (15.0–33.8)781823.1 (15.0–33.8)
      Ever had a circumcision (males)No1872613.9 (9.6–19.7)1872613.9 (9.6–19.7)
      Yes11327.3 (8.5–60.3)11327.3 (8.5–60.3)
      Sexual behavior
      Sexual identityHeterosexual208188.7 (5.5–13.4)188168.5 (5.3–13.5)20210.0 (2.4–33.4)
      Homosexual700 (N/A)100 (N/A)600 (N/A)
      Bisexual1812714.9 (10.4–20.9)900 (N/A)1722715.7 (11.0–22.0)
      Age at first sexual activity (years)<1544613.6 (6.2–27.4)14214.3 (3.4–44.3)30413.3 (5.0–31.1)
      15–192963511.8 (8.6–16.1)153138.5 (5.0–14.1)1432215.4 (10.3–22.3)
      20–245135.9 (1.9–16.9)2713.7 (0.5–23.0)2428.3 (2.0–28.7)
      ≥255120.0 (2.1–74.5)400 (N/A)11100.0
      Total number of sexual partners, lifetime (persons)<1066710.6 (5.1–20.8)37410.8 (4.0–25.9)29310.3 (3.3–28.2)
      10–49125129.6 (5.5–16.2)5647.1 (2.7–17.8)69811.6 (5.9–21.7)
      50–991061716.0 (10.2–24.4)39512.8 (5.3–27.7)671217.9 (10.4–29.1)
      100–14944511.4 (4.8–24.8)3126.5 (1.6–23.0)13323.1 (7.2–53.7)
      150–199900 (N/A)700 (N/A)200 (N/A)
      ≥2004648.7 (3.3–21.2)2813.6 (0.5–22.3)18316.7 (5.3–41.9)
      Number of sexual partners per day, past 3 months (persons)<1641015.6 (8.6–26.8)20420.0 (7.5–43.7)44613.6 (6.2–27.5)
      1–22172210.1 (6.8–15.0)12986.2 (3.1–12.0)881415.9 (9.6–25.2)
      3–4931212.9 (7.4–21.5)3638.3 (2.6–23.3)57915.8 (8.3–27.9)
      ≥52214.6 (0.6–27.2)1317.7 (1.0–41.4)900 (N/A)
      Vaginal sexNo1300 (N/A)100 (N/A)1200 (N/A)
      Yes3834511.8 (8.9–15.4)197168.1 (5.0–12.9)1862915.6 (11.0–21.6)
      Anal sexNo219188.2 (5.2–12.7)197168.1 (5.0–12.9)2229.1 (2.2–30.9)
      Yes1772715.3 (10.7–21.4)100 (N/A)1762715.3 (10.7–21.5)
      Frequency of condom use while having sex with husband/wife/loverAll the time4536.7 (2.1–19.0)2514.0 (0.5–24.7)20210.0 (2.4–33.5)
      Occasionally6546.2 (2.3–15.4)1800 (N/A)4748.5 (3.2–20.9)
      Never1552314.8 (10.0–21.4)83910.8 (5.7–19.7)721419.4 (11.8–30.4)
      Frequency of condom use while having sex with casual sexual partner (including sex worker)All the time2823512.4 (9.0–16.8)143139.1 (5.3–15.1)1392215.8 (10.6–23.0)
      Occasionally37410.8 (4.1–25.8)800 (N/A)29413.8 (5.1–32.1)
      Never200 (N/A)100 (N/A)100 (N/A)
      CI, confidence interval; HBsAg, hepatitis B surface antigen; HBV, hepatitis B virus; N/A, not applicable; STI, sexually transmitted infection.
      a Other: labor, housemaid, officer, handicraft maker, factory worker, online business, salesman.
      b Sexually transmitted infections (STIs): gonorrhea, non-gonorrhea, syphilis, HIV, HBV, HCV, or genital herpes.

      Prevalence of anti-HDV positivity

      None of the 45 participants who were positive for HBsAg were found to be positive for anti-HDV (0%, 95% CI 0–7.9%).

      Factors associated with HBsAg positivity

      Univariable analysis showed that HBsAg positivity was associated with being male, having separated/divorced/widowed, having visited a community barber for shaving, having anal sex, and having unprotected sex (p < 0.05) (Table 4).
      Table 4Factors associated with HBV infection among migrant sex workers in Chiangmai, Thailand, 2019.
      CharacteristicsUnivariableMultivariableMultivariable
      This analysis was adjusted for sex (anal sex was omitted from this analysis).
      OR (95% CI)p-ValueaOR (95% CI)p-ValueaOR (95% CI)p-Value
      Socio-demographic information
      SexFemale1.00
      Male1.95 (1.02–3.72)0.0423.10 (1.25–7.68)0.014
      School attendanceNo1.00
      Yes1.56 (0.74–3.26)0.2414.80 (1.34–17.22)0.0164.50 (1.26–15.98)0.020
      Marital statusSingle1.00
      Has a partner1.85 (0.93–3.66)0.0791.80 (0.70–4.61)0.2191.90 (0.75–4.82)0.178
      Separated/divorced/ widowed2.82 (1.13–7.02)0.0265.40 (1.42–20.61)0.0135.77 (1.48–22.52)0.012
      Health behavior
      Drinking alcohol (past 3 months)No1.00
      Yes0.43 (0.18–1.01)0.053
      Risk behavior
      Ever had tattoo or piercing on any part of bodyNo1.00
      Yes0.54 (0.22–1.32)0.178
      Ever visited a community barber for shaving (males)No1.00
      Yes2.97 (1.32–6.71)0.009
      Ever had a circumcision (males)No1.00
      Yes2.32 (0.58–9.32)0.235
      Sexual behavior
      Sexual identityHeterosexual1.00
      Bisexual1.85 (0.98–3.49)0.057
      Number of sexual partners per day, past 3 months (persons)<11.00
      1–20.61 (0.27–1.36)0.228
      3–40.8 (0.32–1.98)0.63
      ≥50.26 (0.31–2.13)0.209
      Anal sexNo1.00
      Yes2.01 (1.07–3.78)0.0313.63 (1.51–8.75)0.004
      Frequency of condom use while having sex with husband/wife/ loverAll the time or occasionally1.00
      Never2.58 (1.07–6.26)0.0353.68 (1.40–9.65)0.0083.38 (1.31–8.71)0.012
      aOR, adjusted odds ratio; CI, confidence interval; OR, odds ratio.
      a This analysis was adjusted for sex (anal sex was omitted from this analysis).
      Multivariable analysis (Table 4) showed that HBsAg positivity was independently associated with having attended school (adjusted odds ratio (aOR) 4.80, 95% CI 1.34–17.22, p = 0.016), having separated/divorced/widowed (aOR 5.40, 95% CI 1.42–20.61, p = 0.013), having anal sex (aOR 3.63, 95% CI 1.51–8.75, p = 0.004), and having unprotected sex (aOR 3.68, 95% CI 1.40–9.65, p = 0.008). The other factors are described in Supplementary Material Table S1.
      After adjusting for sex (anal sex, closely associated with sex, was omitted from this analysis) (Table 4), HBsAg positivity was associated with being male (aOR 3.10, 95% CI 1.25–7.68, p = 0.014), having attended school (aOR 4.50, 95% CI 1.26–15.98, p = 0.020), having separated/divorced/widowed (aOR 5.77, 95% CI 1.48–22.52, p = 0.012), and having unprotected sex (aOR 3.38, 95% CI 1.31–8.71, p = 0.012).

      Discussion

      In this study, 58.8% (233 of 396) of migrant sex workers had markers of exposure to HBV, of whom 45 individuals were positive for HBsAg, giving a prevalence of 11.4% in the total population studied. This prevalence is higher than that in the general population of Thailand (4%) and Myanmar (6.5%) (
      • Chongsrisawat V.
      • Yoocharoen P.
      • Theamboonlers A.
      • Tharmaphornpilas P.
      • Warinsathien P.
      • Sinlaparatsamee S.
      • et al.
      Hepatitis B seroprevalence in Thailand: 12 years after hepatitis B vaccine integration into the national expanded programme on immunization.
      ,
      • Ministry of Health and Sports of Myanmar
      Myanmar National Strategic Plan on Viral Hepatitis 2016-2020.
      ). Most of the migrant sex workers came from Myanmar and had been born before the hepatitis B vaccine was integrated into the Expanded Program on Immunization in 2003 and before the birth dose vaccination initiated in 2010 (
      • Ministry of Health and Sports of Myanmar
      Myanmar National Strategic Plan on Viral Hepatitis 2016-2020.
      ). The high prevalence of HBsAg positivity among the population studied may reflect the situation of chronic HBV infection in Myanmar before 2003 and may have resulted mainly from perinatal transmission of HBV, a common route of infection in these settings. However, sexual transmission, in particular among the male population, may also have contributed to this high prevalence. Indeed, the risk of HBsAg positivity was more than three times higher among participants having unprotected sex (aOR 3.38, 95% CI 1.31–8.71, p = 0.012). In a study conducted among female commercial sex workers in Chiangmai, the prevalence of HBsAg positivity was 11% and factors associated with HBV infection were blood transfusion and sexually transmitted diseases, indicating that HBV can be transmitted readily by either blood or sexual contact (
      • Taketa K.
      • Ikeda S.
      • Suganuma N.
      • Phornphutkul K.
      • Peerakome S.
      • Sitvacharanum K.
      • et al.
      Differential seroprevalences of hepatitis C virus, hepatitis B virus and human immunodeficiency virus among intravenous drug users, commercial sex workers and patients with sexually transmitted diseases in Chiang Mai, Thailand.
      ).
      In the present study, the prevalence of HBsAg positivity was higher among male migrant sex workers than among females (14.7% vs 8.1%, p = 0.040), with a risk of HBsAg positivity triple the risk in females (aOR 3.10, 95% CI 1.25–7.68, p = 0.014). The reason for this increased risk in males is unclear. Most of the participants had not been vaccinated, so this difference in risk was not related to the response to hepatitis B (HB) vaccine. Also, it is still unclear whether this difference could have been due to a higher risk of perinatal transmission of HBV in males. Some studies have reported that the male sex was associated with a higher risk of perinatal transmission of HBV (
      • Li Z.
      • Xie Z.
      • Ni H.
      • Zhang Q.
      • Lu W.
      • Yin J.
      • et al.
      Mother-to-child transmission of hepatitis B virus: evolution of hepatocellular carcinoma-related viral mutations in the post-immunization era.
      ,
      • Siakwa M.
      • Kpikpitse D.
      • Hansen-Owoo E.
      • Azanu W.
      • Awuku Y.A.
      • Boye A.
      • et al.
      Perinatal transmission ofthe hepatitis b virus: the ghanaian situation.
      ), while other studies have found no difference in HBV transmission between the sexes in infants (
      • Agbede O.
      • Iseniyi J.
      • Kolawole O.
      • Ojuawo A.
      Risk factors and seroprevalence of hepatitis B surface antigenemia in mothers and their preschool age children in Ilorin, Nigeria.
      ,
      • Chen F.
      • Li X.
      • Yuan T.
      • Chen J.
      • Yu W.
      • Yu G.
      Perinatal factors influencing mother-to-child HBV transmission.
      ,
      • Zhang L.
      • Gui X.
      • Wang B.
      • Ji H.
      • Yisilafu R.
      • Li F.
      • et al.
      A study of immunoprophylaxis failure and risk factors of hepatitis B virus mother-to-infant transmission.
      ). Sexual HBV transmission is a plausible explanation for the higher risk of HBsAg among males, since most of the male participants reported practicing anal sex, which has also been associated with HBsAg positivity (
      • Lange W.R.
      • Cone E.J.
      • Snyder F.R.
      The association of hepatitis delta virus and hepatitis B virus in parenteral drug abusers. 1971 to 1972 and 1986 to 1987.
      ).
      The risk of being HBsAg-positive was almost five times higher in participants who had attended school for education (aOR 4.50, 95% CI 1.26–15.98, p = 0.020). A previous investigation suggested that the transmission from an HBV-infected student to a teacher in an elementary school setting can occur without a reported overt percutaneous or permucosal exposure to blood or infectious body fluids (
      • Williams I.
      • Smith M.G.
      • Sinha D.
      • Kernan D.
      • Minor-Babin G.
      • Garcia E.
      • et al.
      Hepatitis B virus transmission in an elementary school setting.
      ). Also, when going to school, children are in contact with many other children who may be infected with HBV, so the risk of exposure to HBV may be higher in schools than in households.
      The risk of HBsAg positivity in participants who were separated/divorced/widowed was five times higher when compared to those who were single (aOR 5.77, 95% CI 1.48–22.52, p = 0.012). This is consistent with the study of Mutagoma et al., which demonstrated an increase in HBsAg prevalence among female sex workers with married status in Rwanda (
      • Mutagoma M.
      • Nyirazinyoye L.
      • Sebuhoro D.
      • Riedel D.J.
      • Ntaganira J.
      Syphilis and HIV prevalence and associated factors to their co-infection, hepatitis B and hepatitis C viruses prevalence among female sex workers in Rwanda.
      ). The explanation behind this higher HBsAg prevalence is unclear, since the population in the present study was sex workers, who may differ in their sexual behavior from a general population.
      Among the HBsAg-positive individuals, none were found to be positive for anti-HDV, consistent with the very low prevalence among the general Thai population reported in a systematic review of HDV prevalence (0%, 95% CI 0–9.41%) (
      • Chen H.Y.
      • Shen D.T.
      • Ji D.Z.
      • Han P.C.
      • Zhang W.M.
      • Ma J.F.
      • et al.
      Prevalence and burden of hepatitis D virus infection in the global population: a systematic review and meta-analysis.
      ). However, a high seroprevalence of anti-HDV has been reported in some specific populations in Thailand: 21.8% in intravenous drug users (IVDUs) (
      • Theamboonlers A.
      • Hansurabhanon T.
      • Verachai V.
      • Chongsrisawat V.
      • Poovorawan Y.
      Hepatitis D virus infection in Thailand: HDV genotyping by RT-PCR, RFLP and direct sequencing.
      ), 11.1% in chronic hepatitis patients, and 8.3% in cirrhotic patients (
      • Louisirirotchanakul S.
      • Wasi C.
      • Uneklabh C.
      • Phutiprawan T.
      • Suwanagool S.
      • Chainuvati T.
      • et al.
      High prevalence of delta virus infection in Thai intravenous drug abusers.
      ).
      This study has some limitations. All data were reported through an interview and answers could not be fully confirmed. For example, 31 participants reported a history of HB vaccination, but anti-HBs antibody was found in only 15 participants.
      In conclusion, more than one-third of this young population of migrant sex workers were still susceptible to HBV infection and 11% were positive for HBsAg. These results indicate that HBV screening programs targeting migrant sex workers are needed to identify individuals with high-risk behaviors who will benefit from HB vaccine and to link those with chronic hepatitis B infection to care. These interventions will contribute to the control of HBV and reaching the sustainable development goals to combat hepatitis (SDG 3).

      Funding

      This study was supported by Chiang Mai University, Chiangmai, Thailand.

      Ethical approval

      The study was approved by the Human Experimentation Committee of the Research Institute for Health Sciences, Chiang Mai University (Number 19/61), Chiangmai, Thailand.

      Conflict of interest

      The authors declare that they have no conflict of interest.

      CRediT authorship contribution statement

      Sayamon Hongjaisee: Conceptualization, Resources, Project administration, Methodology, Investigation, Data curation, Formal analysis, Validation, Visualization, Writing - original draft, Writing - review & editing. Woottichai Khamduang: Methodology, Investigation, Data curation, Formal analysis, Validation, Visualization, Writing - original draft, Writing - review & editing. Patumrat Sripan: Methodology, Investigation, Data curation, Formal analysis, Validation, Visualization, Writing - review & editing. Sirinath Choyrum: Methodology, Writing - review & editing. Viraporn Thepbundit: Methodology, Writing - review & editing. Nicole Ngo-Giang-Huong: Investigation, Data curation, Formal analysis, Validation, Visualization, Writing - review & editing, Supervision. Arunrat Tangmunkongvorakul: Conceptualization, Resources, Writing - review & editing, Supervision.

      Acknowledgements

      The authors would like to express their gratitude to all participants in this study and to the local teams that carried out the fieldwork. We are also grateful for the support of the Perfect Life Organization, M Plus Clinic, Office of Disease Prevention and Control 1 Chiangmai, and Chiangmai Provincial Public Health Office.

      Appendix A. Supplementary data

      The following is Supplementary data to this article:

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