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  • 标题:Tattooing and risk of hepatitis B: a systematic review and meta-analysis.
  • 作者:Jafari, Siavash ; Buxton, Jane A. ; Afshar, Kourosh
  • 期刊名称:Canadian Journal of Public Health
  • 印刷版ISSN:0008-4263
  • 出版年度:2012
  • 期号:May
  • 语种:English
  • 出版社:Canadian Public Health Association
  • 摘要:In North America, most cases of hepatitis B infection occur via blood or sexual contact. (4) Acute hepatitis B infection causes chronic infection in 6-10% of adolescents and adults; chronic infection can lead to liver cirrhosis and to cancer. (5) Thus, cases of hepatitis B infection due to tattooing have important clinical and public health implications. Results from epidemiologic studies regarding the risk of hepatitis among tattooed individuals are conflicting; (3,6) therefore, we conducted a review of the current literature in order to quantify, in a systematic fashion and by using appropriate meta-analytical techniques, the risk of transmission of hepatitis B infection.
  • 关键词:Health promotion;Hepatitis B;Hepatitis B vaccine;Hepatitis B vaccines;Infection;Medical research;Medicine, Experimental;Prisons;Tattooing

Tattooing and risk of hepatitis B: a systematic review and meta-analysis.


Jafari, Siavash ; Buxton, Jane A. ; Afshar, Kourosh 等


Tattooing and body arts have become more prevalent in recent years, their popularity increasing among young adults. A population-based study revealed that one third of people younger than 30 years old in the United States have at least one tattoo. (1) Canadian data indicate that around 8% of high school students have at least one tattoo (2,3) and that 21% of those who did not have a tattoo were eager to have one. Tattooing requires injection of pigments into the dermal layer of skin by repeated puncture of the skin. Such close contact of the tattoo instruments with blood and bodily fluids may cause transmission of viral and bacterial infections if the instruments are used on more than one person without being sterilized.

In North America, most cases of hepatitis B infection occur via blood or sexual contact. (4) Acute hepatitis B infection causes chronic infection in 6-10% of adolescents and adults; chronic infection can lead to liver cirrhosis and to cancer. (5) Thus, cases of hepatitis B infection due to tattooing have important clinical and public health implications. Results from epidemiologic studies regarding the risk of hepatitis among tattooed individuals are conflicting; (3,6) therefore, we conducted a review of the current literature in order to quantify, in a systematic fashion and by using appropriate meta-analytical techniques, the risk of transmission of hepatitis B infection.

METHODS

Search strategy

MEDLINE (1966-March 2011), EMBASE (1980-March 2011), Database of Abstracts of Reviews of Effects (1991-March 2011), and ACP Journal Club (1991-March 2011), International Pharmaceutical Index (1970-March 2011), BIOSIS Previews (1969-March 2011) and Web of Science (1961-March 2011) were searched to identify the relevant studies and abstracts. The initial search strategy was developed from the MeSH subject headings "hepatitis" and "tattoo" in MEDLINE. We reviewed the titles for their relevance to this study, and then examined subject headings and abstracts. We searched the proceedings and conference abstracts through the databases PapersFirst (1993) and ProceedingsFirst (1993) up to March 2011. Authors' names and year of publication from key papers were entered into the cited reference search in the Web of Science. References of the retrieved studies and review articles were screened for any potentially missed articles. We also hand searched the reference lists of retrieved studies as well as journals related to "hepatitis", "hepatology", "transfusion", "blood", "infection", "epidemiology", "gastroenterology", and abstracts and books related to hepatitis. We did not have any language restrictions. Details of the search strategy are available upon request from the authors.

Selection criteria

Observational studies that assessed the association between tattooing and hepatitis B were included if they clearly defined: 1) hepatitis B as either primary or secondary outcome based on serology test, and 2) tattoos as either primary or secondary exposure; and presented relative risks or odds ratios (ORs) and their corresponding 95% confidence intervals (95% CI) or provided sufficient data to compute these parameters. If a study was published in different phases or data were duplicated in more than one publication, we only included the most recent. Two authors (SJ and SB) scanned the titles of abstracts identified through our search strategy and excluded articles that did not meet the selection criteria, such as those on basic sciences, review articles, letters to editor, and commentaries.

Data extraction

We created a spreadsheet and recorded study characteristics, including authors' names, publication year, country of study, study design, sample size, study population, mean age and/or range, gender of participants, type of risk factors or confounders adjusted for, outcome of interest (hepatitis B), and the adjusted OR and 95% CI. Included articles were reviewed in full by two independent reviewers (SJ and SB). All discrepancies were resolved after reviewing the source papers and further discussion among two reviewers. Studies were included only after full consensus was achieved. For studies that provided several levels of exposure, each exposure was categorized and analyzed in the designated subgroup.

Statistical analysis

We pooled the OR and 95% CI of all studies to calculate the overall risk. If a study provided more than one OR, we used the OR that was representative of all participants to calculate the overall pooled OR and 95% CI of all studies included in the meta-analysis. If the overall OR (95% CI) for all participants was not provided in a study, we calculated the pooled OR of that study and then used it for the purpose of calculation of overall OR (95% CI) of our meta-analysis. We performed several subgroup analyses to investigate the association between tattooing and risk of hepatitis B among different populations. We conducted subgroup analyses based on the study population and study design (case control, cohort, and cross-sectional). We grouped the studies on tattoos and hepatitis B into four main groups: 1) community sample (e.g., blood donors, students, and pregnant women), 2) hospital samples, 3) prisoners and 4) high-risk populations (street youth, persons with HIV, people who use drugs, those whose tattoos were done with reused tattoo needles, and those tattooed in non-professional tattoo parlours). Because only three studies in our review [W5,W18,W31] * were reporting samples derived from blood donors, we did not create a subgroup for this group; however, those studies are included in the pooled analysis. We calculated pooled OR (95% CI) from one study [W9] that provided data on both tattoos performed in non-professional parlours and tattoos done with reused needles, and used it in the subgroup of high-risk subjects.

For all analyses, we weighted the study-specific adjusted log ORs by the inverse of their variances. A random effects model was used to estimate the pooled adjusted OR. Statistical heterogeneity between studies was evaluated with Higgins I2 statistic. (7) Sensitivity analysis was carried out to assess the influence of individual studies and then repeating the analysis by excluding the studies with the largest weights.

[FIGURE 1 OMITTED]

RESULTS

Figure 1 shows the results of our search strategy and step-by-step inclusion and exclusion of the retrieved papers. We identified a total of 516 citations related to risk factors of hepatitis. After excluding 273 duplicates, 243 titles were reviewed, of which 64 were selected for abstract review; of these, 59 studies were selected for full-text review. The review process resulted in 31 studies (19 cross-sectional, 9 case-control, 3 cohort), with a total of 665,169 participants from 19 countries, being included in the meta-analysis. All studies identified were in English. Characteristics of the 31 studies included in the meta-analysis are presented in Table 1.

We found a statistically significant association (pooled OR=1.48, 95% CI: 1.30-1.68; [I.sup.2]=47%) between tattooing and risk of trans mission of hepatitis B infection. In subgroup analysis, we found the strongest association between tattooing and risk of hepatitis B for samples derived from high-risk groups (OR=1.64, 95% CI: 1.32-2.03; [I.sup.2]=0%), followed by community samples (OR=1.47, 95% CI: 1.12-1.92; [I.sup.2]=58%), hospital samples (OR=1.45, 95% CI: 1.07-1.97; [I.sup.2]=30%), and prison samples (OR=1.30, 95% CI: 1.01-1.66; [I.sup.2]=56%). Figure 2 shows the results of our meta-analysis for association between tattooing and risk of hepatitis B for four main subgroups of samples derived from community, hospital, prison inmates, and high-risk groups.

We conducted a subgroup analysis to investigate the effect of the study design on the association of tattooing and the risk of hepatitis B. The association between tattooing and risk of hepatitis B was the strongest among case-control studies (OR=1.97, 95% CI: 1.45-2.69; [I.sup.2]=46%), followed by cohort (OR=2.01, 95% CI: 1.522.67; [I.sup.2]=0%) and cross-sectional (OR=1.34, 95% CI: 1.16-1.54; [I.sup.2]=43%) studies. We also conducted sensitivity analysis to review the effect of three studies with wide confidence intervals [W2,W12,W31] on overall pooled OR (95% CI). The analysis was conducted multiple times; first, all three studies were removed from the analysis, and then one study at a time was removed. We did not find a significant difference in OR (95% CI) when all three studies were removed from the analysis (OR=1.44, 95% CI: 1.20-2.08; [I.sup.2]=38%). We also found no significant difference between the pooled pre-sensitivity effect size (OR=1.48, 95% CI: 1.30-1.68; [I.sup.2]=47%) and post-sensitivity effect size after removing any of these studies (OR=1.46, 95% CI: 1.29-1.65; [I.sup.2]=41%) [W2], (OR=1.45, 95% CI: 1.29-1.64; [I.sup.2]=41%) [W12], (OR=1.48, 95% CI: 1.30-1.68; [I.sup.2]=46%) [W31] from the analysis.

In studies of tattooing and hepatitis B, a moderate heterogeneity was detected ([I.sup.2]=47%) in this review. Using Jackknife method, (8) six studies [W1,W2,W3,W10,W12,W13] were identified to be the source of heterogeneity. Removing these studies from the analysis resulted in elimination of the heterogeneity from pooled and subgroup analysis. However, pre- and post-sensitivity overall pooled OR (95% CI) (pre-sensitivity OR=1.48, 95% CI: 1.30-1.68, [I.sup.2]=47%; post-sensitivity OR=1.58, 95% CI: 1.44-1.74, [I.sup.2]=0%), and pre-/post-sensitivity OR (95% CI) in community samples (pre-sensitivity OR=1.47, 95% CI: 1.12-1.92, [I.sup.2]=58%; post-sensitivity OR=1.51, 95% CI: 1.25-1.84, [I.sup.2]=0%) and prisoners (pre-sensitivity OR=1.30, 95% CI: 1.01-1.66, [I.sup.2]=56%; post-sensitivity OR=1.62, 95% CI: 1.33-1.96, [I.sup.2]=0%) increased, whereas for hospital samples (pre-sensitivity OR=1.45, 95% CI: 1.07-1.97, [I.sup.2]=16%; post-sensitivity OR=1.35, 95% CI: 1.07-1.72, [I.sup.2]=0%), these diminished. Differences in the study populations, time and place that the studies were conducted and the study methodology would potentially contribute to the heterogeneity in this study. To further examine the effect of adjustment done in some studies, we removed studies with non-adjusted OR from all subgroups. We did not find any significant change in pooled OR (95% CI) (pre-sensitivity OR=1.48, 95% CI: 1.30-1.68, [I.sup.2]=47%; post-sensitivity OR=1.48, 95% CI: 1.24-1.77, [I.sup.2]=30%). We did not conduct such a sensitivity for subgroups because exclusion of studies with unadjusted OR resulted in a small number of studies in each subgroup.

DISCUSSION

Results of our systematic review indicate an increased risk of hepatitis B infection among those who receive tattoos. The risk is persistent among all population subgroups. Not surprisingly, the strongest association is observed among samples from the high-risk populations: injection drug users, sex workers, street youth, HIV patients, those whose tattoos were done with reused tattoo needles, and those tattooed in non-professional tattoo parlours.

A major strength of our review is the large number of studies and the multinational nature of the study sample. We found an association between tattooing and hepatitis B in all subgroups and across all study designs. Our findings are consistent with the literature which documents an association between tattooing and risk of transmission of other infections (including HIV, (9) leprosy, (10) tetanus, (9) and Methicillin Resistant Staphylococcus Aureus (11)) and with a systematic review of hepatitis C. (12) Several studies have indicated a dose-response relationship between tattooing and the risk of transmission of hepatitis C. (13-15) In fact, the risk of transmission of hepatitis C infection increases with the increase in the surface area covered by a tattoo as well as the number of tattoos received by an individual. Taking into account that the infectivity and inocula differ between HBV and HCV and considering that such dose-response associations between tattooing and risk of transmission of hepatitis B were not reported in the included studies, this topic requires further study.

The risk from tattooing may depend on the background prevalence of hepatitis B infection and immunization uptake in the subgroups of a population. Tattooing among prisoners is an area of concern due to the high prevalence of hepatitis B infection among incarcerated individuals; the background rates of hepatitis B infection are 10 to 20 times higher among prisoners (16-18) than among the general public. Reusing and sharing tattoo needles are reported to be common practice among almost 45% of prisoners. (19) However, our results indicate that the association between tattooing and the risk of transmission of hepatitis B among prisoners is minimally lower compared with other subgroups. This may be because of variations in study design and sampling method among included studies or immunization programs within correctional facilities. The results of this study support the recommendations of experts, (19) advocating the need for prison programs that provide safer tattooing practices to inmates. Such programs may also prevent the transmission of other blood-borne infections among the prison population.

Given that hepatitis can spread through percutaneous or mucous membrane exposure to blood, (20) needlestick injury, (21) and tattooing using unsterile equipment, (22) several measures can be implemented to prevent the transmission of hepatitis B among tattoo recipients. Educational programs for tattoo parlour owners and tattoo artists which reinforce the guidelines and emphasize the importance of appropriate infection control measures should be implemented. These measures include the use of single-use sterile tattoo needles, proper functioning of autoclaves, use of appropriate disinfectants and keeping records of sterilization techniques. Regular and unscheduled inspection of tattoo parlours conducted by health protection units of the local health authorities may improve adherence to the current guidelines. Insufficient follow-up can cause public panic and has resulted in lawsuits against health authorities and business owners in Canada and the United States in recent years. (23)

Tattoo parlours should be required to keep records of their clients and to report any adverse event related to tattooing to local health authorities. (12,22) Tattoo recipients should be provided with written handouts informing them about the risks related to tattooing and the signs and symptoms of common infections that can be transmitted through tattooing. Last, tattoo artists and clients should be aware of the availability of an effective vaccine for the prevention of hepatitis B infection.

Many countries have introduced a universal infant and/or adolescent hepatitis B immunization program; therefore those who undergo tattooing at a young age are now likely to be immunized. In Canada, all unimmunized individuals who are at increased risk of hepatitis B infection (i.e., IDU, persons with high-risk sexual behaviour) are recommended to receive hepatitis B vaccine. However, this strategy has several limitations. Risk factors cannot be identified for about 25% of acute hepatitis B infections, (24) and there is poor compliance with the hepatitis B vaccine schedule in risk groups. (25) Therefore, it is important to ensure that individuals have been fully immunized--including those who move between jurisdictions which may have different immunization schedules--and to concentrate on immunization of high-risk and prison populations.

Over time, there has been a shift in the demographics of the people who acquire tattoos. Tattoos are no longer popular just among people with high-risk behaviour, but are becoming common among younger adults with a more conservative lifestyle. This increased prevalence of tattooing warrants the need for prevention programs that target young adults. (26)

Our study is subject to several limitations due to the observational nature of the studies included in the review. Information on the past history of tattooing may not reflect the current population risk of hepatitis infection. Second, recall bias and social desirability bias may affect the validity of the information collected in observational studies. Finally, it is important to note that background prevalence of hepatitis B infection and hepatitis B vaccinations vary in different settings and countries. We did not have specific geographic data on the transmission of hepatitis B. Further studies to determine the pre-tattoo hepatitis B serostatus and the prevalence of other high-risk behaviours are needed to fully assess the association between tattooing and hepatitis B transmission.

The results of this systematic review are consistent with an increase in all population groups in the risk of contracting hepatitis B through tattooing. Immunization of susceptible individuals with hepatitis B vaccine, unscheduled inspection and enforcement of infection control guidelines in tattoo parlours, and provision of safe tattoo programs to inmates can play an important role in the interruption of transmission.

Conflict of Interest: None to declare.

Received: September 20, 2011

Accepted: January 21, 2012

REFERENCES

(1.) Laumann AE, Derick AJ. Tattoos and body piercing in the United States: A national data set. J Am Acad Dermatol 2006;55:413-21.

(2.) Deschesnes M, Demers S, Fines P. Prevalence and characteristics of body piercing and tattooing among high school students. Can J Public Health 2006;97(4):325-29.

(3.) Health Canada. Special Report on Youth, Piercing, Tattooing and Hepatitis C TrendScan Findings, Health Canada, March 2001. Available at: http://www.phac-aspc.gc.ca/hepc/pubs/ youthpt-jeunessept/pdf/youth_piercings.pdf (Accessed August 12, 2009).

(4.) Glasgow KW, Schabas R, Williams DC, Wallace E, Nalezyty LA. A population-based hepatitis B seroprevalence and risk factor study in a Northern Ontario town. Can J Public Health 1997;88(2):87-90.

(5.) Mast E, Mahoney F, Kane M, Margolis HS. Hepatitis B vaccine. In: Plotkin SA, Orenstein WA (Eds.), Vaccines, 4th ed. Philadelphia, PA: WB Saunders, 2004.

(6.) Brooks EA, Lacey LF, Payne SL, Miller DW. Economic evaluation of lamivudine compared with interferon-alpha in the treatment of chronic hepatitis B in the United States. Am J Manag Care 2001;7(7):677-82.

(7.) Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002;21:1539-58.

(8.) Efron B. Nonparametric estimates of standard error: The jackknife, the bootstrap and other methods. Biometrika 1981;68:589-99.

(9.) Nishioka S de A, Gyorkos TW. Tattoos as risk factors for transfusion-transmitted diseases. Int J Infect Dis 2001;5(1):27-34.

(10.) Ghorpade A. Inoculation (tattoo) leprosy: A report of 31 cases. J Eur Acad Dermatol Venereol 2002;16:494-99.

(11.) United States Centers for Disease Control and Prevention (CDC). Methicillin-resistant Staphylococcus aureus skin infections among tattoo recipients--Ohio, Kentucky, and Vermont, 2004-2005. MMWR 2006;55(24):677-69.

(12.) Jafari S, Copes R, Baharlou S, Etminan M, Buxton J. Tattooing and risk of transmission of hepatitis C: A systematic review and meta-analysis. Int J Infect Dis 2010;14(11):e928-40.

(13.) Roy E, Haley N, Leclerc P, Boivin JF, Cedras L, Vincelette J. Risk factors for hepatitis C virus infection among street youths. CMAJ 2001;165:557-60.

(14.) Haley RW, Fischer RP. Commercial tattooing as a potentially important source of hepatitis C infection: Clinical epidemiology of 626 consecutive patients unaware of their hepatitis C serologic status. Medicine 2001;80:134-51.

(15.) Kim YS, Ahn YO, Lee HS. Risk factors for hepatitis C virus infection among Koreans according to the hepatitis C virus genotype. J Korean Med Sci 2002;17:187-92.

(16.) Weild AR, Gill ON, Bennett D, Livingstone SJM, Parry JV, Curry L. Prevalence of HIV, hepatitis B, and hepatitis C antibodies in prisoners in England and Wales: A national survey. Commun Dis Public Health 2000;3:121-26.

(17.) Khan AJ, Simard EP, Bower WA, Wurtzel HL, Khristova M, Wagner KD, et al. Ongoing transmission of hepatitis B virus infection among inmates at a state correctional facility. Am J Public Health 2005;95:1793-99.

(18.) Canada Dept of Health and Welfare. Seroepidemiologic study of hepatitis B and C viruses in federal correctional institutions in British Columbia. Can Dis Wkly Rep 1990;52:265-66.

(19.) Crofts N, Stewart T, Hearne P, Ping XY, Breschkin AM, Locarnini SA. Spread of blood borne viruses among Australian prison entrants. BMJ1995;310:285 88.

(20.) Gerberding JL. Incidence and prevalence of human immunodeficiency virus, hepatitis B virus, hepatitis C virus, and cytomegalovirus among health care personnel at risk for blood exposure: Final report from a longitudinal study. J Infect Dis 1994;170:1410-17.

(21.) Sartori M, La Terra G, Aglietta M, Manzin A, Navino C, Verzetti G. Transmission of hepatitis C via blood splash into conjunctiva. (Letter) Scand J Infect Dis 1993;25:270-7l.

(22.) Kiyosawa K, Sodeyama T, Tanaka E, Nakano Y, Furuta S, Nishioka K, et al. Hepatitis C in hospital employees with needle stick injuries. Ann Intern Med 1991;115:367-69.

(23.) City TV. Tattoo Parlour, Peel Sued Over Possible HIV, Hepatitis Exposure. March 19, 2009. Available at: http://www.citytv.com/toronto/citynews/news/ local/article/9477--tattoo-parlour-peel-sued- over-possible-hiv-hepatitis-exposure (Accessed August 19, 2011).

(24.) Boulos D, Goedhuis NJ, Wu J, Baptiste B, Poliquin D, Furseth J, et al. Enhanced surveillance for acute and likely acute hepatitis B in Canada: 1999 to 2002. Can J Infect Dis Med Microbiol 2005;16:275-81.

(25.) Sellors J, Zimic-Vincetic M, Howard M, Chernesky MA. Lack of compliance with hepatitis B vaccination among Canadian STD clinic patients: Candidates for an accelerated immunization schedule? Can J Public Health 1997;88:210 11.

(26.) Public Health Agency of Canada. Special Report on Youth, Piercing, Tattooing and Hepatitis C Trendscan Findings. Available at: http://www.phacaspc.gc.ca/hepc/pubs/youthpt- jeunessept/pdf/youth_piercings.pdf (Accessed August 26, 2011).

Siavash Jafari, MD, MHSc, [1] Jane A. Buxton, MBBS, FRCPC, [1] Kourosh Afshar, MD, MHSc, FRCPC FAAP, [2] Ray Copes, MD, MSc, [2] Souzan Baharlou, MD [3]

Author Affiliations

[1.] School of Population and Public Health, Faculty of Medicine, University of British Columbia, Vancouver, BC

[2.] Division of Pediatric Urology, BC Children's Hospital, Vancouver, BC

[3.] Director, Environmental and Occupational Health, Ontario Agency for Health Protection and Promotion, Toronto, ON

Correspondence: Dr. Jane A. Buxton, Epidemiologist and Harm Reduction Lead, BC Centre for Disease Control, 655 West 12th Avenue, Vancouver, BC V5Z 4R4, Tel: 604-707-2573, Fax: 604-707-2516, E-mail: jane.buxton@ubc.ca

* See Table 1 for a list of the 31 studies (W1 through W31).
Table 1. Characteristics of Studies Included in Both Systematic Review
and Meta-analysis

Study   Author            Year   Location     Sample Size
ID                                            (case/control)

W1      Anda              1985   USA          619

W2      Auamnoy           2003   Thailand     92 (46/46)

W3      Babudieri         2005   Italy        973

W4      Butler            2007   Australia    612

W5      Christensen       2000   Denmark      325

W6      Christensen       2001   Denmark      10,862

W7      Coppola           2007   Italy        3579

W8      Hull              1985   USA          455

W9      Hwang             2006   USA          7960

        Hwang             2006   USA          7960

        Hwang             2006   USA          7960

        Hwang             2006   USA          7960

        Hwang             2006   USA          7960

        Hwang             2006   USA          7960

        Hwang             2006   USA          7960

W10     Hymas             1989   Sudan        851

W11     Khan              2005   USA          1124

W12     Ko                1990   Taiwan       90/180

W13     Lai               2007   Taiwan       286

W14     Liao              2006   Taiwan       298

W15     Luksamijarulkul   2008   Thailand     354

W16     Mariano           2004   Italy        2964/7221

W17     Mele              1995   Italy        5241 (363/4879)

W18     Nishioka          2003   Brazil       345

W19     Nurgalieva        2007   Kazakhstan   290

W20     Pallas            1999   Spain        1215

W21     Pereira           2006   Brazil       1025

W22     Phoon             1988   Singapore    6328

W23     Pourahmad         2007   Iran         1431 (497/934)

W24     Roy               1999   Canada       437

W25     Sali              2005   Iran         (500/434)

W26     Samuel            2001   USA          2898

        Samuel            2001   USA          2898

W27     Sebastian         1992   Brunei       (187/187)

W28     Shi               2007   Taiwan       (476/1421)

W29     Tawk              2005   Australia    2120

W30     Vahid             2005   Iran         454/428

W31     Wada              1999   Japan        95

        Wada              1999   Japan        95

Study   Study           Sample               Age, Range,
ID      Design          Derived From         Mean (SD)

W1      CS *            Prison               Mean (24.8-28.2)

W2      CC ([dagger])   Hospital             22.88 [+ or -] 1.41

W3      CS              Prison               30-44 (36.9)

W4      CS              Prison               All ages

W5      CO ([double     Prison               All ages
        dagger])

W6      CS              Blood donors         Median=48

W7      CS              Healthy subjects     33.19 (12.18)

W8      CS              Prison               18-71

W9      CS              Students; all        >18; median age:
                                             21.62

        CS              1-2 tattoo(s)        Not reported

        CS              >3 tattoos           Not reported

        CS              Professional         Not reported
                        tattoo parlour

        CS              Non-professional     Not reported
                        tattoo parlour

        CS              New or autoclaved    Not reported
                        needle

        CS              Reused needle        Not reported

W10     CS              Community            1-89 (24.6)

W11     CS              Prison               18-72

W12     CC              Healthy adults       Not reported

W13     CS              Prison               Not reported

W14     CS              Prison               Not reported

W15     CS              Public cleaners      39.5 (7.7)

W16     CC              IVDU & blood         15-55
                        transfusion

W17     CC              Community            Not reported

W18     CS              Blood donors         18-62

W19     CS              Community            10-65

W20     CS              Prison               30.6 (9.9)

W21     CS              HIV patients         17-77

W22     CS              Hospital             35-65

W23     CC              Prison               25-60

W24     CO              Street youth         19.5

W25     CC              Hospital             37.6 (15.1)

W26     CO              IDU, tattooed        >15
                        in prison

        CO              IDU, tattooed in     >17
                        community

W27     CC              Hospital             20-70

W28     CC              Military             All 20 years old

W29     CS              Hospital             52.3

W30     CC              Blood donors         HBsAg+ 36.69 (0.82);
                                             HBsAg- 30.88 (0.80)

W31     CS              Hospital             24.4 (6.1)

        CS              Hospital             24.4 (6.1)

Study   Gender   OR/     95% CI        Adjustment
ID               RR

W1      M        0.53    0.31-0.92     IVDU; IVDU and previous
                                       imprisonment; prior hepatitis
                                       or jaundice; race; age

W2      M/F      15.9    1.97-128.16   No

W3      M/F      1.14    0.89-1.47     Age; gender; area of origin;
                                       exposure category; unprotected
                                       sex; transfusions;
                                       imprisonment

W4      M/F      1.66    1.01-2.74     No

W5      M        1.00    0.30-2.90     Age, times in prison, duration
                                       of IDU, sexual risk index, IDU
                                       in prison

W6      M/F      2.89    1.51-5.50     No

W7      M/F      1.85    1.18-2.90     No

W8      M        1.30    0.40-2.60     No

W9      M/F      0.96    0.73-1.25     No

        M/F      0.99    0.74-1.32     No

        M/F      0.87    0.50-1.50     No

        M/F      0.93    0.70-1.23     No

        M/F      1.24    0.69-2.23     No

        M/F      0.87    0.65-1.18     No

        M/F      1.91    1.11-3.30     No

W10     M/F      1.58    1.04-2.39     No

W11     M        1.46    1.04-2.06     Age, race, history of IDU/
                                       STI, lifetime number of female
                                       partners, incarcerated more
                                       than 14 years, tattoo during
                                       incarceration

W12     M        8.10    1.90-34.8     No

W13              0.66    0.32-1.39     No

W14              1.49    0.78-2.84     No

W15     M/F      1.17    0.69-1.99     No

W16     M/F      1.70    1.00-3.10     Sex, age, education,
                                       geographical area, surgical
                                       intervention, dental therapy,
                                       number of sexual partners,
                                       households or sexual partners
                                       of HBsAg/HCV chronic carrier

W17     M/F      2.12    1.10-4.09     Age, sex, education level,
                                       geographic area, surgical
                                       interventions, dental therapy,
                                       sexual exposure

W18     M/F      1.90    0.94-3.83     Syphilis, Chagas' disease, HIV
                                       infection, at least one marker
                                       for HBV, HCV, or HIV

W19     M/F      1.26    0.51-3.12     No

W20     M/F      1.70    0.80-3.5      Age, sex, educational level,
                                       number of sexual partners

W21     M/F      1.60    1.10-2.40     Age, gender, number of sexual
                                       partners

W22     M        1.16    0.75-1.79     Age

W23     M        1.85    1.00-3.43     No

W24     M/F      1.60    0.60-4.20     Age, IDU, number of sexual
                                       partners, body piercing

W25     M/F      1.40    0.85-2.29     No

W26     M/F      2.30    1.40-3.8      Age, study site, race, share
                                       injection equipment, use of
                                       heroin, years of injection

        M/F      1.60    1.10-2.50     No

W27     M        2.01    1.05-3.95     Matched case-control

W28     M        1.37    0.98-1.93     No

W29     M/F      1.33    0.88-2.02     No

W30     M/F      4.60    1.50-13.9     No

W31     M/F      1.60    0.00-24.00    No

        M/F      1.40    0.37-4.99     No

* CS = Cross-sectional; ([dagger]) CC = Case-control; [double dagger])
CO = Cohort; M = Male; F = Female

Figure 2. Forest plot of meta-analysis of tattooing and risk of
transmission of hepatitis B

                            log
Study or Subgroup       [Odds Ratio]     SE     Weight

1.4.1 Tattoo and Hepatitis-B, Community sample

Coppola, 2007                 0.615     0.23      4.2%
Hwang, 2006                   -0.04    0.136      6.4%
Hymas, 1989                   0.455    0.213      4.5%
Ko, 1990                      2.092    0.741      0.7%
Luksamijarulkul, 2008         0.157     0.27      3.5%
Mele, 1995                   0.7514    0.335      2.6%
Nurgalieva, 2007             0.2311    0.462      1.6%
Shi, 2007                    0.3148    0.174      5.4%
Subtotal (95% CI)                                29.0%

Heterogeneity: [Tau.sup.2] = 0.08; [Chi.sup.2] = 16.55, df = 7
(P = 0.02); [I.sup.2] = 58%

Test for overall effect: Z = 2.77 (P = 0.006)

1.4.3 Tattoo and Hepatitis-B, Hospital samples

Auamnoy, 2003                2.7663    1.0648     0.4%
Phoon, 1988                  0.1484     0.22      4.4%
Sali, 2005                   0.3365     0.25      3.8%
Sebastian, 1992              0.6981    0.345      2.5%
Tawk, 2005                   0.2582    0.228      4.2%
Wada, 1999                    0.355     0.59      1.1%
Subtotal (95% CI)                                16.4%

Heterogeneity: [Tau.sup.2] = 0.04; [Chi.sup.2] = 7.16, df = 5
(P = 0.21); [I.sup.2] = 30%

Test for overall effect: Z = 2.38 (P = 0.02)

1.4.4 Tattoo and Hepatitis-B, Prisoners

Anda, 1985                  -0.6349     0.28      3.3%
Babudieri, 2005                0.13     0.13      6.6%
Butler, 2004-b                0.505    0.256      3.7%
Christensen, 2001             0.001    0.543      1.2%
Hull, 1985                   0.2624    0.353      2.4%
Khan, 2005                   0.3784    0.175      5.4%
Lai, 2007                   -0.4155    0.379      2.2%
Liao, 2006(2)                0.3988    0.329      2.7%
Pallas, 1999                  0.528     0.37      2.3%
Pourahmad, 2007              0.6152    0.315      2.9%
Samuel, 2001                 0.8329    0.256      3.7%
Subtotal (95% CI)                                36.4%

Heterogeneity: [Tau.sup.2] = 0.09; [Chi.sup.2] = 22.96, df = 10
(P = 0.01); [I.sup.2] = 56%

Test for overall effect: Z = 2.07 (P = 0.04)

1.4.5 Tattoo and Hepatitis-B, Highr risk group and IDUs

Hwang, 2006                   0.523    0.195      4.9%
Mariano, 2004                0.5306    0.307      3.0%
Pereira, 2006                  0.47    0.206      4.7%
Roy, 1999                      0.47    0.492      1.4%
Samuel, 2001                  0.473    0.227      4.2%
Subtotal (95% CI)                                18.3%

Heterogeneity: [Tau.sup.2] = 0.00; [Chi.sup.2] = 0.06, df = 4
(P = 1.00); [I.sup.2] = 0%

Test for overall effect: Z = 4.54 (P < 0.00001)

Total (95% CI)                                  100.0%

Heterogeneity: [Tau.sup.2] = 0.05; [Chi.sup.2] = 50.42, df = 29
(P = 0.008); [I.sup.2] = 42%

Test for overall effect: Z = 5.45 (P < 0.00001)

Test for subgroup differences: [Chi.sup.2] = 2.04, df = 3 (P = 0.56),
[I.sup.2] = 0%

                             Odds Ratio
Study or Subgroup        IV, Random, 95% CI

1.4.1 Tattoo and Hepatitis-B, Community sample

Coppola, 2007              1.85 [1.18, 2.90]
Hwang, 2006                0.96 [0.74, 1.25]
Hymas, 1989                1.58 [1.04, 2.39]
Ko, 1990                  8.10 [1.90, 34.62]
Luksamijarulkul, 2008      1.17 [0.69, 1.99]
Mele, 1995                 2.12 [1.10, 4.09]
Nurgalieva, 2007           1.26 [0.51, 3.12]
Shi, 2007                  1.37 [0.97, 1.93]
Subtotal (95% CI)          1.47 [1.12, 1.92]

Heterogeneity: [Tau.sup.2] = 0.08; [Chi.sup.2] = 16.55, df = 7
(P = 0.02); [I.sup.2] = 58%

Test for overall effect: Z = 2.77 (P = 0.006)

1.4.3 Tattoo and Hepatitis-B, Hospital samples

Auamnoy, 2003           15.90 [1.97, 128.16]
Phoon, 1988                1.16 [0.75, 1.79]
Sali, 2005                 1.40 [0.86, 2.29]
Sebastian, 1992            2.01 [1.02, 3.95]
Tawk, 2005                 1.29 [0.83, 2.02]
Wada, 1999                 1.43 [0.45, 4.53]
Subtotal (95% CI)           1.45 n.07, 1.971

Heterogeneity: [Tau.sup.2] = 0.04; [Chi.sup.2] = 7.16, df = 5
(P = 0.21); [I.sup.2] = 30%

Test for overall effect: Z = 2.38 (P = 0.02)

1.4.4 Tattoo and Hepatitis-B, Prisoners

Anda, 1985                 0.53 [0.31, 0.92]
Babudieri, 2005            1.14 [0.88, 1.47]
Butler, 2004-b             1.66 [1.00, 2.74]
Christensen, 2001          1.00 [0.35, 2.90]
Hull, 1985                 1.30 [0.65, 2.60]
Khan, 2005                 1.46 [1.04, 2.06]
Lai, 2007                  0.66 [0.31, 1.39]
Liao, 2006(2)              1.49 [0.78, 2.84]
Pallas, 1999               1.70 [0.82, 3.50]
Pourahmad, 2007            1.85 [1.00, 3.43]
Samuel, 2001               2.30 [1.39, 3.80]
Subtotal (95% CI)          1.30 [1.01, 1.66]

Heterogeneity: [Tau.sup.2] = 0.09; [Chi.sup.2] = 22.96, df = 10
(P = 0.01); [I.sup.2] = 56%

Test for overall effect: Z = 2.07 (P = 0.04)

1.4.5 Tattoo and Hepatitis-B, Highr risk group and IDUs

Hwang, 2006                1.69 [1.15, 2.47]
Mariano, 2004              1.70 [0.93, 3.10]
Pereira, 2006              1.60 [1.07, 2.40]
Roy, 1999                    1.60(0.61,4.20]
Samuel, 2001               1.60 [1.03, 2.50]
Subtotal (95% CI)          1.64 [1.32, 2.03]

Heterogeneity: [Tau.sup.2] = 0.00; [Chi.sup.2] = 0.06, df = 4
(P = 1.00); [I.sup.2] = 0%

Test for overall effect: Z = 4.54 (P < 0.00001)

Total (95% CI)             1.42 [1.25, 1.61]

Heterogeneity: [Tau.sup.2] = 0.05; [Chi.sup.2] = 50.42, df = 29
(P = 0.008); [I.sup.2] = 42%

Test for overall effect: Z = 5.45 (P < 0.00001)

Test for subgroup differences: [Chi.sup.2] = 2.04, df = 3 (P = 0.56),
[I.sup.2] = 0%
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