• 1

    Shimbo S, Watanabe T, Nakatsuka H, Matsuda-Inoguchi N, Ko YS, Kim ES, Higashikawa K, Ikeda M, 2001. Prevalence of hepatitis B and C virus infection among women in Jeju Island, Republic of Korea. Southeast Asian J Trop Med Public Health 32 :362–368.

    • Search Google Scholar
    • Export Citation
  • 2

    Shin HR, Kim JY, Ohno T, Cao K, Mizokami M, Risch H, Kim SR, 2000. Prevalence and risk factors of hepatitis C virus infection among Koreans in rural area of Korea. Hepatol Res 17 :185–196.

    • Search Google Scholar
    • Export Citation
  • 3

    Shin HR, Kim JY, Kim JI, Lee DH, Yoo KY, Lee DS, Franceschi S, 2002. Hepatitis B and C virus prevalence in a rural area of South Korea: the role of acupuncture. Br J Cancer 87 :314–318.

    • Search Google Scholar
    • Export Citation
  • 4

    Memon MI, Memon MA, 2002. Hepatitis C: an epidemiological review. J Viral Hepat 9 :84–100.

  • 5

    Ding X, Park YN, Taltavull TC, Thung SN, Jin X, Jin Y, Trung NS, Edamoto Y, Sata T, Abe K, 2003. Geographic characterization of hepatitis virus infections, genotyping of hepatitis B virus, and p53 mutation in hepatocellular carcinoma analyzed by in situ detection of viral genomes from carcinoma tissues: comparison among six different countries. Jpn J Infect Dis 56 :12–18.

    • Search Google Scholar
    • Export Citation
  • 6

    Terrault NA, 2002. Sexual activity as a risk factor for hepatitis C. Hepatology 36 :S99–105.

  • 7

    Corona R, Prignano G, Mele A, Gentili G, Caprilli F, Franco E, Ferrigno L, Giglio A, Titti F, Bruno C, 1991. Heterosexual and homosexual transmission of hepatitis C virus: relation with hepatitis B virus and human immunodeficiency virus type 1. Epidemiol Infect 107 :667–672.

    • Search Google Scholar
    • Export Citation
  • 8

    Page-Shafer KA, Cahoon-Young B, Klausner JD, Morrow S, Molitor F, Ruiz J, McFarland W, 2002. Hepatitis C virus infection in young, low-income women: the role of sexually transmitted infection as a potential cofactor for HCV infection. Am J Public Health 92 :670–676.

    • Search Google Scholar
    • Export Citation
  • 9

    Yee LJ, Weiss HL, Langner RG, Herrera J, Kaslow RA, van Leeuwen DJ, 2001. Risk factors for acquisition of hepatitis C virus infection: a case series and potential implications for disease surveillance. BMC Infect Dis 1 :8.

    • Search Google Scholar
    • Export Citation
  • 10

    Mertens TE, Hayes RJ, Smith PG, 1990. Epidemiological methods to study the interaction between HIV infection and other sexually transmitted diseases. AIDS 4 :57–65.

    • Search Google Scholar
    • Export Citation
  • 11

    Kim O, Kim SS, Park MS, Suh SD, Lee MW, Kim KS, Yoon JD, Lee JS, 2003. Seroprevalence of sexually transmitted viruses in Korean populations including HIV-seropositive individuals. Int J STD AIDS 14 :46–49.

    • Search Google Scholar
    • Export Citation
  • 12

    Terrault NA, 2005. Sex and hepatitis C. Am J Gastroenterol 100 :825–826.

  • 13

    Laurent C, Henzel D, Mulanga-Kabeya C, Maertens G, Larouze B, Delaporte E, 2001. Seroepidemiological survey of hepatitis C virus among commercial sex workers and pregnant women in Kinshasa, Democratic Republic of Congo. Int J Epidemiol 30 :872–877.

    • Search Google Scholar
    • Export Citation
  • 14

    Ishi K, Suzuku F, Saito A, Yoshimoto S, Kubota T, 2001. Prevalence of human immunodeficiency virus, hepatitis B and hepatitis C virus antibodies and hepatitis B antigen among commercial sex workers in Japan. Infect Dis Obstet Gynecol 9 :215–219.

    • Search Google Scholar
    • Export Citation
  • 15

    Miyazaki M, Takagi S, Kato M, Une H, 2002. Prevalences of and risk factors for sexually transmitted diseases among Japanese female commercial sex workers in middle- and high-class soap-lands in Japan. Int J STD AIDS 13 :833–838.

    • Search Google Scholar
    • Export Citation
  • 16

    Kim YS, Pai CH, Chi HS, Kim DW, Min YI, Ahn YO, 1992. Prevalence of hepatitis C virus antibody among Korean adults. J Korean Med Sci 7 :333–336.

    • Search Google Scholar
    • Export Citation
  • 17

    Estcourt CS, Marks C, Rohrsheim R, Johnson AM, Donovan B, Mindel A, 2000. HIV, sexually transmitted infections, and risk behaviours in male commercial sex workers in Sydney. Sex Transm Infect 76 :294–298.

    • Search Google Scholar
    • Export Citation
  • 18

    Russi JC, Serra M, Vinoles J, Perez MT, Ruchansky D, Alonso G, Sanchez JL, Russell KL, Montano SM, Negrete M, Weissenbacher M, 2003. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite comercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 68 :716–720.

    • Search Google Scholar
    • Export Citation
  • 19

    Montella M, Crispo A, Grimaldi M, Angeletti C, Amore A, Ronga D, Sabbatini M, Pisani A, Spiteri D, Serraino D, 2005. Prevalence of hepatitis C virus infection in different population groups in southern Italy. Infection 33 :9–12.

    • Search Google Scholar
    • Export Citation
  • 20

    Ahn Y, 1999. Recent changes in HBV carrier rate among Koreans. JAMA SEA 14 :382–383.

  • 21

    UNAIDS/UNICEF/WHO, 2004. Republic of Korea, 2004 Update. Epidemiological Fact Sheets on HIV/AIDS and Sexually Transmitted Infections. Geneva: World Health Organization.

  • 22

    Kim JM, Cho GJ, Hong SK, Chang KH, Chung JS, Choi YH, Song YG, Huh A, Yeom JS, Lee KS, Choi JY, 2003. Epidemiology and clinical features of HIV infection/AIDS in Korea. Yonsei Med J 44 :363–370.

    • Search Google Scholar
    • Export Citation
  • 23

    Kim YS, Ahn YO, Kim DW, 1996. A case-control study on the risk factors of hepatitis C virus infection among Koreans. J Korean Med Sci 11 :38–43.

    • Search Google Scholar
    • Export Citation
  • 24

    Chen TZ, Wu JC, Yen FS, Sheng WY, Hwang SJ, Huo TI, Lee SD, 1995. Injection with nondisposable needles as an important route for transmission of acute community-acquired hepatitis C virus infection in Taiwan. J Med Virol 46 :247–251.

    • Search Google Scholar
    • Export Citation
  • 25

    Shimoyama R, Sekiguchi S, Suga M, Sakamoto S, Yachi A, 1993. The epidemiology and infection route of asymptomatic HCV carriers detected through blood donations. Gastroenterol Jpn 28 (Suppl 5):1–5.

    • Search Google Scholar
    • Export Citation
  • 26

    Walsh B, Maguire H, Carrington D, 1999. Outbreak of hepatitis B in an acupuncture clinic. Commun Dis Public Health 2 :137–140.

  • 27

    Israeli E, 1995. Harefuah 128 :769–770.

  • 28

    Hirose K, Tajima K, Fujihira N, Hasegawa S, Fujioka M, 1995. Nippon Koshu Eisei Zasshi 42 :269–279.

  • 29

    Wiwanitkit V, 2003. HIV infection after Chinese traditional acupuncture treatment. Complement Ther Med 11 :272.

  • 30

    Mehta SH, Brancati FL, Strathdee SA, Pankow JS, Netski D, Coresh J, Szklo M, Thomas DL, 2003. Hepatitis C virus infection and incident type 2 diabetes. Hepatology 38 :50–56.

    • Search Google Scholar
    • Export Citation
  • 31

    Mehta SH, Brancati FL, Sulkowski MS, Strathdee SA, Szklo M, Thomas DL, 2000. Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Ann Intern Med 133 :592–599.

    • Search Google Scholar
    • Export Citation
  • 32

    Bahtiyar G, Shin JJ, Aytaman A, Sowers JR, McFarlane SI, 2004. Association of diabetes and hepatitis C infection: epidemiologic evidence and pathophysiologic insights. Curr Diab Rep 4 :194–198.

    • Search Google Scholar
    • Export Citation
  • 33

    Sotiropoulos A, Peppas TA, Skliros E, Apostolou O, Kotsini V, Pappas SI, 1999. Low prevalence of hepatitis C virus infection in Greek diabetic patients. Diabet Med 16 :250–252.

    • Search Google Scholar
    • Export Citation
  • 34

    Kanesaki T, Kinoshita S, Tsujino G, Yoshioka K, Ikegami N, 1993. Hepatitis C virus infection in children with hemophilia: characterization of antibody response to four different antigens and relationship of antibody response, viremia, and hepatic dysfunction. J Pediatr 123 :381–387.

    • Search Google Scholar
    • Export Citation
  • 35

    Eyster ME, Diamondstone LS, Lien JM, Ehmann WC, Quan S, Goedert JJ, 1993. Natural history of hepatitis C virus infection in multitransfused hemophiliacs: effect of coinfection with human immunodeficiency virus. The Multicenter Hemophilia Cohort Study. J Acquir Immune Defic Syndr 6 :602–610.

    • Search Google Scholar
    • Export Citation
  • 36

    Makris M, Preston FE, Triger DR, Underwood JC, Choo QL, Kuo G, Houghton M, 1990. Hepatitis C antibody and chronic liver disease in haemophilia. Lancet 335 :1117–1119.

    • Search Google Scholar
    • Export Citation
  • 37

    Tokars JI, Frank M, Alter MJ, Arduino MJ, 2002. National surveillance of dialysis-associated diseases in the United States, 2000. Semin Dial 15 :162–171.

    • Search Google Scholar
    • Export Citation
  • 38

    Fabrizi F, Bunnapradist S, Lunghi G, Martin P, 2003. Kinetics of hepatitis C virus load during hemodialysis: novel perspectives. J Nephrol 16 :467–475.

    • Search Google Scholar
    • Export Citation

 

 

 

 

SEROPREVALENCE AND RISK FACTORS FOR HEPATITIS C VIRUS INFECTION AMONG FEMALE COMMERCIAL SEX WORKERS IN SOUTH KOREA WHO ARE NOT INTRAVENOUS DRUG USERS

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  • 1 Department of Preventive Medicine, Seonam University College of Medicine, Namwon, Jeonbuk, South Korea; Microbiology Division, Jeollanam-do Institute of Health and Environment, Gwangju, South Korea; Department of Preventive Medicine, Chonnam National University College of Medicine, Chonnam National University Research Center of Medical Sciences, Gwangju, South Korea

Several previous studies have reported a high prevalence of hepatitis C virus (HCV) infection among commercial sex workers (CSWs), but the situation is often compounded by coexisting factors, such as intravenous drug use. We conducted a seroepidemiologic study of 1,527 female CSWs in South Korea. All participants tested negative for human immunodeficiency virus and were not illicit intravenous drug users (IDUs). Twenty-one participants (1.4%) were positive for antibodies to HCV. According to the multivariate logistic regression analysis, a history of acupuncture and diabetes mellitus were associated with the seroprevalence of HCV, whereas time spent as a CSW showed only borderline significance. Sexual activity was not an independent predictor of increased risk for HCV infection in female CSWs who had never been illicit IDUs.

INTRODUCTION

Previous community-based studies have shown that the prevalence of hepatitis C virus (HCV) varied between 1.6% and 11% of the populations studied,13 but there is a lack of information on the nationwide prevalence of HCV and its risk factors in South Korea. The prevalence of HCV infection differs according to geographic area and among the general population,4 patients with hepatocellular carcinoma (HCC),5 and specific risk groups such as commercial sex workers (CSWs).4,6 Percutaneous exposure to HCV, such as through blood transfusion, intravenous drug use, and surgery, is a well-established risk factor for HCV infection, but the causal relationship between sexual contact and HCV infection has not been extensively studied. There are conflicting reports on the sexual transmission of HCV,79 and investigation of the potential for sexual transmission of HCV is hampered by the confounding effects of concomitant sexually transmitted diseases (STDs) and intravenous drug use.10 The prevalence of HCV in CSWs in South Korea has not been extensively reported. One study of the Korean population suggested that the prevalence of HCV may be higher in CSWs than in the general population.11 However, this study was limited and presented prevalence data for one small group of CSWs in one region of South Korea.

In previous studies of CSWs, sexual transmission of HCV was proposed to play an important role in infection, and, although it has not been evaluated in CSWs who are not intravenous drug users (IDUs), evidence suggested that sexual transmission may be the second most common risk factor for HCV infection.12 However, whether sexual transmission is an independent risk factor for HCV transmission is debatable because of the frequently confounding effect of concomitant intravenous drug use, which is one of the most important risk factors for HCV infection.6,12

We performed a cross-sectional seroepidemiologic study to estimate the prevalence of HCV infection and its potential risk factors among female CSWs who were not IDUs and who were seronegative for human immunodeficiency virus (HIV). We also evaluated the independent contribution of sexual activity to HCV transmission.

MATERIALS AND METHODS

Study participants.

A cross-sectional survey was performed in Jeollanam-do Province, South Korea, from January to July 2004. Potential participants were recruited from registered CSWs in five cities, three located in seaside areas and two located in inland areas. We used the public health center’s administrative lists of female CSWs to identify potential participants, who were required to be more than 19 years of age, the legal adult age in South Korea, and had been trading sex for money. The five target cities had an estimated 2,234 registered female CSWs who were of eligible age between January and July 2004. All registered CSWs must visit the public health center for monthly STD screening tests to maintain the test certificate required for their jobs. Tests for syphilis were conducted in all eligible female CSWs at each public health center laboratory. Among the 2,234 eligible female CSWs who had undergone STD screening in public health centers during the study period, 1,527 (68.4%) agreed to participate in the study, gave written informed consent, and completed a self-administered questionnaire without omitting any essential variables, such as age and prior or current status of intravenous drug use. Approval for the study was obtained from the Ethical Committee of Jeollanam-do Institute of Health and Environment before conducting the survey.

Serologic testing.

Blood samples were collected into jelly vacuum tubes under aseptic conditions and were subsequently tested for syphilis and HIV at each health center laboratory. The tubes were sent to the Central Laboratory, Jeollanam-do Institute of Health and Environment on the same day. Sera were isolated by centrifugation and stored at −70°C. The sera were tested for HCV and hepatitis B virus (HBV) in the same laboratory. Third-generation enzyme-linked immunosorbent assays (ELISAs) were performed to detect antibodies to HCV (Genedia HCV ELISA 3.0; Green Cross Sang-A Corp., Chungcheongbuk-do, South Korea) and hepatitis B virus surface antigen (Genedia hepatitis B surface antigen [HBsAg] ELISA 3.0; Green Cross Sang-A Corp.) using an ELISA plate processor (Behring ELISA Processor III; Dade Behring, Marburg, Germany). Third-generation tests for antibodies to HCV contain antigens from HCV core protein and non-structural (NS) 3, NS4, and NS5 gene proteins. Previous infection with HIV was determined by ELISA (Genedia HIV 1/2 ELISA 3.0; Green Cross Sang-A Corp.) using an ELISA plate processor (Plato 3300; Rosys, Hombrechtikon, Switzerland) and confirmed by Western blotting (HIV blot 2.2; Genelabs Diagnostics, Singapore). Syphilis serologic status was screened by the rapid plasmid reagin (RPR) test or the Venereal Disease Research Laboratory (VDRL) test and was confirmed by the Treponema pallidum hemagglutination assay (TPHA).

Definitions.

To determine the serologic status of syphilis and HIV, we traced the laboratory data of each public health center and the registered data of the National Communicable Diseases Surveillance System in Korea, 2002–2004. Subjects with reactive TPHA and previous positive VDRL or RPR test results were defined as syphilis seropositive. The presence of diabetes mellitus was confirmed by a self-report that the subject was taking anti-hyperglycemic medication because almost none of the study subjects had been fasting. Subjects who had been exposed to potential risk factors, such as acupuncture, on more than one occasion were considered positive for that risk factor. A family history of hepatitis C was defined as the presence of HCV in an immediate family member (e.g., parent or full siblings). A non-paying sexual partner was defined as a spouse or male cohabitant.

Statistical methods.

Continuous variables, such as age and years spent as a CSW, were grouped and treated as categorical variables. Comparisons for the associations of HCV status were conducted using the chi-square test, Student’s t-test, or Fisher’s exact test as appropriate. The analysis of risk factors was conducted using multivariate logistic regression. Previously identified risk factors that were significant at the P < 0.1 level in an unadjusted model (age group, acupuncture, diabetes, time spent as a CSW, and history of hemodialysis) were included in the model. Data processing and statistical analyses were performed with SPSS version 11.5 (SPSS Inc., Chicago, IL).

RESULTS

Characteristics of the subjects.

There were no significant differences in age or seropositivity for syphilis between participants and non-participants. The mean ± SD age and seropositivity for syphilis were 27 ± 6.1 years and 2.7%, respectively, for CSWs who participated in the study and 27.9 ± 6.2 years and 2.2%, respectively, for non participating CSWs. The sociodemographic characteristics of the study subjects are shown in Table 1. No cases of HIV or intravenous drug use were found and approximately 75% of the subjects were < 30 years of age (range = 19–54 years, median = 25 years). Most subjects (91.2%) had worked as a CSW for ≤ 5 years, and the remaining 8.8% had been CSWs for > 5 years; 966 subjects (63.3%) worked in seaside cities and 561 (36.7%) worked in inland cities. Most of the subjects (86.6%) reported a history of sexual contact with non-paying partners (husband or cohabitant). A family history of HCV or HBV was infrequent and was reported by only 21 (1.4%) or 45 (2.9%) of the subjects, respectively.

Prevalence of antibodies to HCV according to demographic and potential risk factors.

Twenty-one (1.4%) subjects were positive for antibodies to HCV, 102 (6.7%) were carriers of HBsAg, and none were co-infected with HCV and HBV. Table 2 shows the sociodemographic factors and potential risk factors according to serologic status for antibodies to HCV. Univariate analysis showed that age (or age group), history of hemodialysis, use of acupuncture, and diabetes mellitus were associated with increased risk of being positive antibodies to HCV. Other potential risk factors, such as a family history of HCV, prior surgery, prior blood transfusion, HBsAg serology, and HBV vaccination were not associated with a risk of having antibodies to HCV.

Prevalence of antibodies to HCV according to sexual activity.

There were no cases of HIV among the study subjects, and 41 (2.7%) were seropositive for syphilis. Univariate analysis showed that subjects who had been a CSW for > 3 years had a significantly (P < 0.05) higher rate of antibodies to HCV. This positive statistical association with antibodies to HCV was not seen with other variables indicative of sexual activity, such as syphilis serology, presence of a non-paying sexual partner, and HCV history of non-paying sexual partners.

Independent risk factors for HCV infection.

Using a multivariate logistic regression model, we analyzed all factors associated at the P < 0.1 level with HCV serologic status. There were too few subjects with some of the traditional risk factors, such as blood transfusion and HBsAg carrier status, to perform a multivariate analysis for those factors. In the multivariate logistic model, HCV was significantly associated with diabetes (odds ratio [OR] = 11.2, 95% confidence interval [CI] = 2.63–47.8, P = 0.001) and acupuncture (OR = 3.30; 95% CI = 1.16–9.34, P = 0.024), whereas time spent as a CSW (≥ 3 years) did not reach statistical significance (OR = 2.21, 95% CI = 0.90–5.41, P = 0.08). A history of hemodialysis and age (≥ 30 years) were not associated with HCV serologic status (Table 3).

DISCUSSION

In previous studies of CSWs, sexual transmission of HCV was believed to play an important role in HCV infection; however, these studies did not exclude CSWs who were IDUs. Thus, although evidence indicates that sexual transmission is the second most common risk factor for HCV acquisition,12 it is debatable whether sexual contact is an independent risk factor for HCV transmission because of the confounding effect of frequently coexisting intravenous drug use, which is important in HCV transmission.6,12 In the present study, which did not have this confounding effect, we estimated HCV seroprevalence and risk factors in female CSWs in South Korea. The participation rate in the study was 68.4%, which compares favorably with that of previous community-based epidemiologic studies. In addition, there were no differences in age or syphilis serologic status between participating and non-participating CSWs.

Women who work in the commercial sex industry differ from the general population in their increased vulnerability to infection and their potential for increased rates of STDs and blood-borne virus infections, including HCV. CSWs play a specific role as a bridge population between reservoirs of infectious disease and the general populations; therefore, they require intensive health care. Several studies have reported a high prevalence of HCV infection in CSWs. Kim and others reported that HCV prevalence in CSWs in South Korea was 10.3%, and this rate was three times higher than that of voluntary recipients for STD testing in public health centers.11 Despite a small sample size and selection bias, these findings suggest the possibility of sexual transmission of HCV in South Korea. Terraut estimated the average seroprevalence of antibodies to HCV among female sex workers to be at 6% in the United States;6 Laurent and others reported a seroprevalence of 6.6% in the Congo,13 and Ishi and others reported a seroprevalence of 3.2% in Japan.14 The HCV seroprevalence of 1.4% in female CSWs in our study is lower than that in most previous reports except another for a report from Japan,15 and is lower than that in the general female population in South Korea.16 In addition, CSWs in other countries show a higher seroprevalence than in our study,8,13,17 despite some differences in the study designs. We suggest that this difference in HCV seroprevalence is attributable to differences in the pattern of intravenous drug use in the study populations. Illicit intravenous drug use in CWSs ranged form 3%18 to 9.1%17 in previous studies and was 4.4% in low-income, young American women.8 Our sample consisted of a large number of female CSWs, but none were current or prior IDUs. IDUs are very rare in South Korea even among CSWs because illicit drug use is strictly banned in South Korea. Montella and others suggested that illicit intravenous drug use is a major transmission route for HCV infection in younger people and that iatrogenic transmission via non-sterile syringes is a major route of transmission in older age groups.19 Given that three of four of our study subjects were less than 30 years of age, it is likely that the absence of IDUs accounts for the lower HCV seroprevalence in our study compared with that in other studies.

The 6.2% prevalence of HBsAg carriers among female CSWs in our study is higher than that reported in previous studies of female CSWs in Japan,14 Uruguay,18 and South Korea,11 and in male CSWs in Australia.17 It is also higher than that in the general female population of South Korea,1,3,20 in which prevalence ranges from 1.4% to 5%. This may be because South Korea is endemic for HBV and sexual transmission of HBV is well established, unlike that of HCV. The HBV vaccination coverage rate in our study subjects was low, which may be related to the relatively high fee that must be paid by an applicant in the Korean vaccination system.

HIV was not detected in our study subjects. The total number of patients with HIV/acquired immunodeficiency syndrome (AIDS) in South Korea at the end of 2003 was approximately estimated 8,300, according to the World Health Organization,21 HIV/AIDS occurred predominantly in men,22 and the prevalence rate in CSWs was 1.75 per 10,000 person. Therefore, HIV was not likely to be detected in a study of our size.

Our results suggest that acupuncture is an important risk factor for HCV infection, as reported in previous studies in Asia.2325 Acupuncture is a common health practice in South Korea, as reflected in our study subjects. Despite the frequent use of acupuncture, it is conducted in non-medical areas and commonly by unqualified persons with non-sterile equipment. Therefore, acupuncture should be considered a mode of HCV transmission in South Korea3,23 and the rest of the world.24,2629 Shin and others reported that 55% of female HCV transmission is attributable to acupuncture and suggested that safer acupuncture practices should be a priority for HCV prevention in South Korea.3 Shimoyama and others reported that acupuncture accounts for ≤ 20% of HCV cases in Japan.25 Of the 21 subjects positive for antibodies to HCV in the present study, only eight reported a prior surgery or hemodialysis, and their only other likely risk factor for HCV transmission, apart from being CSWs, was the use of acupuncture. In addition, a strong association between the presence of antibodies to HCV and acupuncture remained in our regression model after adjusting for other factors. These results suggest that acupuncture plays a major role in HCV transmission among female CSWs who are not IDUs in South Korea, as in other Asian countries.

None of the variables associated with sexual activity, such as time spent as a CSW, syphilis, or HBV serologies, and non-paying sexual contact with HCV-positive partners, that were analyzed in the present study were associated with the presence of antibodies to HCV. Time spent as a CSW was shown to be strongly associated with the presence of antibodies to HCV by univariate analysis, but it did not remain significantly associated by multivariate analysis. Only 2 of 21 subjects positive for antibodies to HCV were free from potential risk factor exposures except those related to sexual activity. Together with the relatively low prevalence of antibodies to HCV previously described, these results indicate that HCV was transmitted mainly by the more common route, such as acupuncture, rather than by sexual transmission, which appears to play a minor role even in CSWs. However, the possibility of sexual transmission is not ruled out by our study because indicators that may more directly gauge sexual activity, such as condom use or number of daily sexual partners, were not analyzed. Although sexual activity seems to have a minimal effect on HCV transmission, the frequency of sexual activity in most adults necessitates further consideration of the potential for sexual transmission of HCV.

An interesting finding in our study was the positive association between diabetes and positivity for antibodies to HCV, which is consistent with the findings of most studies of general populations30,31 and of patients with diabetes or HCV,32 with the exception of one study from Greece.33 However, advanced liver disease, such as cirrhosis and HCC, has been shown to cause glucose intolerance and insulin resistance, so it is still not clear whether mild or severe HCV infection is actually associated with diabetes. In the present study, diabetes was the factor most strongly associated with HCV positivity. Furthermore, none of the subjects positive for antibodies to HCV in our study had been clinically diagnosed with liver disease including cirrhosis and HCC. Thus, despite the small number of subjects with diabetes and the possibility of an inaccurate definition of diabetes, diabetes may still be a risk factor for HCV infection. In addition, none of the persons with diabetes had used needles for insulin injection.

The transfusion of blood or blood products carries an extremely high risk of HCV infection worldwide. Therefore, patients with hemophilia have a very high incidence of HCV infection (46–90%).3436 Hemodialysis is also an effective transmission route for HCV. Recent epidemiologic data show that the risk of HCV infection among patients undergoing dialysis and staff at dialysis units has increased.37,38 However, in our study, there were too few subjects with a history of transfusion or hemodialysis to establish an association with the presence of antibodies to HCV.

Our study has some limitations. First, direct indicators of sexual activities, such as condom use and daily numbers of sex partners, and some potential risk factors, such as intranasal drug use, tattooing, and body piercing, were not used in the analysis because of insufficient data. Second, CSWs can be classified into two groups that show differences in behaviors and sexual activities: 1) direct CSWs who live in brothels in red-light areas, and 2) indirect CSWs who are non–brothel-based. However, it was not possible to classify our study subjects into these two groups. Third, the subjects recruited for this study may not have been representative of the female CSWs in the target area; unregistered CSWs who were not recruited may be direct CSWs with more risky behavior than registered CSWs. However, it is expected that there were only a small number of unregistered direct CSWs and that these CSWs would soon need to become registered to remain CSWs. Therefore, we believe that the effects of this selection bias and its implications could be ignored. Fourth, a misclassification bias concerning the definition of diabetes and under-reporting of intravenous drug use may have occurred. Lastly, our study has low statistical power because of the small number of positive results for antibodies to HCV, diabetes, and syphilis serologic status.

Our findings suggest that the prevalence of antibodies to HCV in female CSWs without HIV or a history of intravenous drug use was no higher than that in the general population of South Korea or that previously reported from other countries. The higher prevalence rates reported in other studies may be related to the prevalence of intravenous drug use in study populations. Although we cannot rule out the role of sexual activity as an independent risk factor for HCV infection, we suggest that sexual activity is less of a risk factor than are acupuncture or diabetes in female CSWs who are not IDUs. This remains to be quantified in a prospective study.

Table 1

Distribution of sociodemographic characteristics and potential risk factors among the 1,527 study subjects*

CharacteristicDistribution
* CSW = commercial sex worker; HCV = hepatitis C virus; HBSAg = hepatitis B surface antigen.
Mean age ± SD (range, median), years27 ± 6.1 (19–54, 25)
Age groups, no. (%), years
    < 301,175 (76.9)
    30–39279 (18.3)
    ≥ 4073 (4.7)
Time as CSW, no. (%), years
    < 1464 (30.4)
    1–2533 (34.9)
    3–5396 (25.9)
    6–9114 (7.5)
    ≥ 1020 (1.3)
Workplace location, no. (%)
    Seaside966 (63.3)
    Inland561 (36.7)
Non-paying sexual partners, no. (%)
    Never204 (13.4)
    Previous or current1,323 (86.6)
Antibodies to HCV, no. (%)
    Negative1,506 (98.6)
    Positive21 (1.4)
HBsAg carrier, no. (%)
    No1,425 (93.3)
    Yes102 (6.7)
Syphilis seropositive, no. (%)
    No1,486 (97.3)
    Yes41 (2.7)
Table 2

Seroprevalence of HCV among 1,527 study subjects according to demographic and potential risk factors*

CharacteristicHCV antibody positive (n = 21)HCV antibody negative (n = 1,506)P
* HCV = hepatitis C virus; HBSAg = hepatitis B surface antigen; HBV = hepatitis B virus; CSW = commercial sex worker.
† By t-test, chi-square test, or Fisher’s exact test.
Mean age (± SD), years30.1 (5.7)26.9 (6.1)0.019
Age groups (years)0.030
    < 3012 (1.0)1,163 (99)
    ≥ 309 (2.6)343 (97.4)
Workplace location0.897
    Seaside13 (1.3)953 (98.7)
    Inland8 (1.4)553 (98.6)
Family history of HCV1.000
    No21 (1.4)1,485 (98.6)
    Yes0 (0)21 (100)
Surgical history0.565
    No13 (1.5)836 (98.5)
    Yes8 (1.2)667 (98.8)
Blood transfusion history0.621
    No21 (1.5)1,429 (98.6)
    Yes0 (0)77 (100)
Hemodialysis history0.067
    No20 (1.3)1,502 (98.7)
    Yes1 (20)4 (80)
Acupuncture history0.004
    No5 (0.6)835 (99.4)
    Yes16 (2.3)671 (98.2)
Diabetes mellitus0.002
    No18 (1.2)1,489 (98.8)
    Yes3 (15.8)16 (84.2)
HBsAg carrier0.393
    No21 (1.5)1,404 (98.5)
    Yes0 (0)102 (100)
Vaccination against HBV0.547
    Yes10 (1.6)619 (98.4)
    No11 (1.2)887 (98.8)
Time as a CSW, years0.031
    ≤ 39 (0.9)985 (99.1)
    > 312 (2.3)521 (97.7)
Syphilis seropositive0.438
    No20 (1.3)1,466 (98.7)
    Yes1 (2.4)40 (97.6)
Non-paying partners with HCV1.000
    No15 (1.4)1,032 (98.6)
    Yes0 (0)6 (100)
Table 3

Results of the multivariate logistic regression analysis of variables associated with a positive reaction for antibodies to HCV*

VariablesOR95% CIP
* HCV = hepatitis C virus; OR = odds ratio; CI = confidence interval; CSW = commercial sex worker.
Age (≥ 30 years)1.870.75–4.680.179
>3 years as CSW2.210.90–5.410.08
Acupuncture3.31.16–9.340.024
Diabetes mellitus11.22.63–47.80.001
Hemodialysis5.220.37–73.70.221

*

Address correspondence to Sun-Seog Kweon, Department of Preventive Medicine, Seonam University College of Medicine, 720, Gwanchi-dong, Namwon, Jeonbuk 590-711, South Korea. E-mail: sskweonx@netian.com

Authors’ addresses: Sun-Seog Kweon and Min-Ho Shin, Department of Preventive Medicine, Seonam University College of Medicine, 720, Gwanchi-dong, Namwon, Jeonbuk 590-711, South Korea, Telephone: 82-63-620-0373, Fax: 82-63-620-0375, E-mails: sskweonx@netian.com and mhshinx@orgio.net. Hyeon-Je Song and Doo-Young Jeon, Microbiology Division, Jeollanam-do Institute of Health and Environment, 291-1, Nongsung-dong, Gwangju 502-200, South Korea, Telephone: 82-62-360-5338, Fax: 82-62-366-7413, E-mails: songha1@dreamwiz.com and jeondy@hanmail.net. Jin-Su Choi, Department of Preventive Medicine, Chonnam National University College of Medicine, Chonnam National University Research Center of Medical Sciences, 5, Hak-dong, Dong-gu, Gwangju 501-746, South Korea, Telephone: 82-62-220-4172, Fax: 82-62-233-0305, E-mail: jschoix@chonnam.ac.kr.

Financial support: This work was supported by the Jeollanam-do Institute of Health and Environment and the Korean Center for Disease Control and Prevention.

REFERENCES

  • 1

    Shimbo S, Watanabe T, Nakatsuka H, Matsuda-Inoguchi N, Ko YS, Kim ES, Higashikawa K, Ikeda M, 2001. Prevalence of hepatitis B and C virus infection among women in Jeju Island, Republic of Korea. Southeast Asian J Trop Med Public Health 32 :362–368.

    • Search Google Scholar
    • Export Citation
  • 2

    Shin HR, Kim JY, Ohno T, Cao K, Mizokami M, Risch H, Kim SR, 2000. Prevalence and risk factors of hepatitis C virus infection among Koreans in rural area of Korea. Hepatol Res 17 :185–196.

    • Search Google Scholar
    • Export Citation
  • 3

    Shin HR, Kim JY, Kim JI, Lee DH, Yoo KY, Lee DS, Franceschi S, 2002. Hepatitis B and C virus prevalence in a rural area of South Korea: the role of acupuncture. Br J Cancer 87 :314–318.

    • Search Google Scholar
    • Export Citation
  • 4

    Memon MI, Memon MA, 2002. Hepatitis C: an epidemiological review. J Viral Hepat 9 :84–100.

  • 5

    Ding X, Park YN, Taltavull TC, Thung SN, Jin X, Jin Y, Trung NS, Edamoto Y, Sata T, Abe K, 2003. Geographic characterization of hepatitis virus infections, genotyping of hepatitis B virus, and p53 mutation in hepatocellular carcinoma analyzed by in situ detection of viral genomes from carcinoma tissues: comparison among six different countries. Jpn J Infect Dis 56 :12–18.

    • Search Google Scholar
    • Export Citation
  • 6

    Terrault NA, 2002. Sexual activity as a risk factor for hepatitis C. Hepatology 36 :S99–105.

  • 7

    Corona R, Prignano G, Mele A, Gentili G, Caprilli F, Franco E, Ferrigno L, Giglio A, Titti F, Bruno C, 1991. Heterosexual and homosexual transmission of hepatitis C virus: relation with hepatitis B virus and human immunodeficiency virus type 1. Epidemiol Infect 107 :667–672.

    • Search Google Scholar
    • Export Citation
  • 8

    Page-Shafer KA, Cahoon-Young B, Klausner JD, Morrow S, Molitor F, Ruiz J, McFarland W, 2002. Hepatitis C virus infection in young, low-income women: the role of sexually transmitted infection as a potential cofactor for HCV infection. Am J Public Health 92 :670–676.

    • Search Google Scholar
    • Export Citation
  • 9

    Yee LJ, Weiss HL, Langner RG, Herrera J, Kaslow RA, van Leeuwen DJ, 2001. Risk factors for acquisition of hepatitis C virus infection: a case series and potential implications for disease surveillance. BMC Infect Dis 1 :8.

    • Search Google Scholar
    • Export Citation
  • 10

    Mertens TE, Hayes RJ, Smith PG, 1990. Epidemiological methods to study the interaction between HIV infection and other sexually transmitted diseases. AIDS 4 :57–65.

    • Search Google Scholar
    • Export Citation
  • 11

    Kim O, Kim SS, Park MS, Suh SD, Lee MW, Kim KS, Yoon JD, Lee JS, 2003. Seroprevalence of sexually transmitted viruses in Korean populations including HIV-seropositive individuals. Int J STD AIDS 14 :46–49.

    • Search Google Scholar
    • Export Citation
  • 12

    Terrault NA, 2005. Sex and hepatitis C. Am J Gastroenterol 100 :825–826.

  • 13

    Laurent C, Henzel D, Mulanga-Kabeya C, Maertens G, Larouze B, Delaporte E, 2001. Seroepidemiological survey of hepatitis C virus among commercial sex workers and pregnant women in Kinshasa, Democratic Republic of Congo. Int J Epidemiol 30 :872–877.

    • Search Google Scholar
    • Export Citation
  • 14

    Ishi K, Suzuku F, Saito A, Yoshimoto S, Kubota T, 2001. Prevalence of human immunodeficiency virus, hepatitis B and hepatitis C virus antibodies and hepatitis B antigen among commercial sex workers in Japan. Infect Dis Obstet Gynecol 9 :215–219.

    • Search Google Scholar
    • Export Citation
  • 15

    Miyazaki M, Takagi S, Kato M, Une H, 2002. Prevalences of and risk factors for sexually transmitted diseases among Japanese female commercial sex workers in middle- and high-class soap-lands in Japan. Int J STD AIDS 13 :833–838.

    • Search Google Scholar
    • Export Citation
  • 16

    Kim YS, Pai CH, Chi HS, Kim DW, Min YI, Ahn YO, 1992. Prevalence of hepatitis C virus antibody among Korean adults. J Korean Med Sci 7 :333–336.

    • Search Google Scholar
    • Export Citation
  • 17

    Estcourt CS, Marks C, Rohrsheim R, Johnson AM, Donovan B, Mindel A, 2000. HIV, sexually transmitted infections, and risk behaviours in male commercial sex workers in Sydney. Sex Transm Infect 76 :294–298.

    • Search Google Scholar
    • Export Citation
  • 18

    Russi JC, Serra M, Vinoles J, Perez MT, Ruchansky D, Alonso G, Sanchez JL, Russell KL, Montano SM, Negrete M, Weissenbacher M, 2003. Sexual transmission of hepatitis B virus, hepatitis C virus, and human immunodeficiency virus type 1 infections among male transvestite comercial sex workers in Montevideo, Uruguay. Am J Trop Med Hyg 68 :716–720.

    • Search Google Scholar
    • Export Citation
  • 19

    Montella M, Crispo A, Grimaldi M, Angeletti C, Amore A, Ronga D, Sabbatini M, Pisani A, Spiteri D, Serraino D, 2005. Prevalence of hepatitis C virus infection in different population groups in southern Italy. Infection 33 :9–12.

    • Search Google Scholar
    • Export Citation
  • 20

    Ahn Y, 1999. Recent changes in HBV carrier rate among Koreans. JAMA SEA 14 :382–383.

  • 21

    UNAIDS/UNICEF/WHO, 2004. Republic of Korea, 2004 Update. Epidemiological Fact Sheets on HIV/AIDS and Sexually Transmitted Infections. Geneva: World Health Organization.

  • 22

    Kim JM, Cho GJ, Hong SK, Chang KH, Chung JS, Choi YH, Song YG, Huh A, Yeom JS, Lee KS, Choi JY, 2003. Epidemiology and clinical features of HIV infection/AIDS in Korea. Yonsei Med J 44 :363–370.

    • Search Google Scholar
    • Export Citation
  • 23

    Kim YS, Ahn YO, Kim DW, 1996. A case-control study on the risk factors of hepatitis C virus infection among Koreans. J Korean Med Sci 11 :38–43.

    • Search Google Scholar
    • Export Citation
  • 24

    Chen TZ, Wu JC, Yen FS, Sheng WY, Hwang SJ, Huo TI, Lee SD, 1995. Injection with nondisposable needles as an important route for transmission of acute community-acquired hepatitis C virus infection in Taiwan. J Med Virol 46 :247–251.

    • Search Google Scholar
    • Export Citation
  • 25

    Shimoyama R, Sekiguchi S, Suga M, Sakamoto S, Yachi A, 1993. The epidemiology and infection route of asymptomatic HCV carriers detected through blood donations. Gastroenterol Jpn 28 (Suppl 5):1–5.

    • Search Google Scholar
    • Export Citation
  • 26

    Walsh B, Maguire H, Carrington D, 1999. Outbreak of hepatitis B in an acupuncture clinic. Commun Dis Public Health 2 :137–140.

  • 27

    Israeli E, 1995. Harefuah 128 :769–770.

  • 28

    Hirose K, Tajima K, Fujihira N, Hasegawa S, Fujioka M, 1995. Nippon Koshu Eisei Zasshi 42 :269–279.

  • 29

    Wiwanitkit V, 2003. HIV infection after Chinese traditional acupuncture treatment. Complement Ther Med 11 :272.

  • 30

    Mehta SH, Brancati FL, Strathdee SA, Pankow JS, Netski D, Coresh J, Szklo M, Thomas DL, 2003. Hepatitis C virus infection and incident type 2 diabetes. Hepatology 38 :50–56.

    • Search Google Scholar
    • Export Citation
  • 31

    Mehta SH, Brancati FL, Sulkowski MS, Strathdee SA, Szklo M, Thomas DL, 2000. Prevalence of type 2 diabetes mellitus among persons with hepatitis C virus infection in the United States. Ann Intern Med 133 :592–599.

    • Search Google Scholar
    • Export Citation
  • 32

    Bahtiyar G, Shin JJ, Aytaman A, Sowers JR, McFarlane SI, 2004. Association of diabetes and hepatitis C infection: epidemiologic evidence and pathophysiologic insights. Curr Diab Rep 4 :194–198.

    • Search Google Scholar
    • Export Citation
  • 33

    Sotiropoulos A, Peppas TA, Skliros E, Apostolou O, Kotsini V, Pappas SI, 1999. Low prevalence of hepatitis C virus infection in Greek diabetic patients. Diabet Med 16 :250–252.

    • Search Google Scholar
    • Export Citation
  • 34

    Kanesaki T, Kinoshita S, Tsujino G, Yoshioka K, Ikegami N, 1993. Hepatitis C virus infection in children with hemophilia: characterization of antibody response to four different antigens and relationship of antibody response, viremia, and hepatic dysfunction. J Pediatr 123 :381–387.

    • Search Google Scholar
    • Export Citation
  • 35

    Eyster ME, Diamondstone LS, Lien JM, Ehmann WC, Quan S, Goedert JJ, 1993. Natural history of hepatitis C virus infection in multitransfused hemophiliacs: effect of coinfection with human immunodeficiency virus. The Multicenter Hemophilia Cohort Study. J Acquir Immune Defic Syndr 6 :602–610.

    • Search Google Scholar
    • Export Citation
  • 36

    Makris M, Preston FE, Triger DR, Underwood JC, Choo QL, Kuo G, Houghton M, 1990. Hepatitis C antibody and chronic liver disease in haemophilia. Lancet 335 :1117–1119.

    • Search Google Scholar
    • Export Citation
  • 37

    Tokars JI, Frank M, Alter MJ, Arduino MJ, 2002. National surveillance of dialysis-associated diseases in the United States, 2000. Semin Dial 15 :162–171.

    • Search Google Scholar
    • Export Citation
  • 38

    Fabrizi F, Bunnapradist S, Lunghi G, Martin P, 2003. Kinetics of hepatitis C virus load during hemodialysis: novel perspectives. J Nephrol 16 :467–475.

    • Search Google Scholar
    • Export Citation
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