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Relationship between personal care products usage and triclosan exposure: the second Korean National Environmental Health Survey (KoNEHS 2012–2014)

Relationship between personal care products usage and triclosan exposure: the second Korean... Background: We aimed to find the exposure level of triclosan (TCS), a known endocrine disruptor, related to the use of personal care products using a nationally representative data of the general population in Korea. Methods: This study included data of 6288 adults aged 19 years and older (2692 men, 3596 women), based on the Second Korean National Environmental Health Survey (KoNEHS 2012–2014). The data were divided according to gender. The frequency and proportion of each variable were determined by dividing participants into two groups based on the top 75th percentile concentration of urinary TCS (male: 1.096 μg/g creatinine, female: 1.329 μg/g creatinine). Odds ratios (ORs) were calculated using logistic regression analysis for the high TCS exposure and low TCS exposure groups. Results: Overall, the proportion of participants using personal care products was higher in women than in men. There was a significantly higher proportion of participants in the high TCS exposure group with younger age, higher education and income levels and with more frequent use of fragrance products, hair care products, body cleansers, cosmetics, and antimicrobial agents. In both men and women, ORs tended to increase with increased frequency of use of hair care products, body cleansers, and cosmetics before and after adjustment. Conclusions: Our findings demonstrate that as the frequency of use of personal care products increases, urine TCS concentration increases. Because TCS is a well-known endocrine disruptor, further studies are needed and explore other health effects with exposure to TCS in general population in Korea. Keywords: Triclosan, Personal care products, Korean National Environmental Health Survey Background TCS is absorbed into the body through the mouth and Triclosan (TCS), chemical name 5-chloro-2-(2,4-dichlor- skin [2]. TCS is absorbed at a rate of nearly 100% in the ophenoxy)phenol, is a synthetic antimicrobial and anti- oral cavity, with a half-life of 10–20 h; less than 10% is fungal agent, which is widely used throughout the world. absorbed via the transdermal route, with a half-life of TCS is used mainly as a disinfectant in soaps, detergents, 1.4–2.1 days. Absorbed TCS is detected mainly in toothpaste, mouthwash, fabrics, deodorant, shampoo, plasma, urine, and breast milk [3]; it is mostly excreted and plastic additives, and it is used in many personal in the urine [4]. According to a pharmacokinetic study, care products, animal products, and industry and house- after oral administration of 4 mg TCS, most was ex- hold products [1]. creted in the urine within the first 24 h and levels had recovered to baseline within 8 days after administration [5]. These results demonstrate that urinary TCS concen- * Correspondence: drforest@hanmail.net trations can be used as a biomarker of TCS exposure Department of Occupational and Environmental Medicine, Kyung Hee [6]. There have been several studies indicating that University Medical Center, Seoul, South Korea Department of Occupational and Environmental Medicine, School of Medicine Kyung Hee University, Seoul, Korea © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 2 of 8 urinary TCS concentrations are associated with the use Variables of personal care products containing TCS [6–8]. Variables of interest TCS is known to be an endocrine disruptor that is To determine the association between TCS exposure structurally similar to polychlorinated biphenyls, bisphe- and frequency of personal care products use, the fre- nol A, dioxins, and thyroid hormones [9]. TCS increases quency of use was classified as used rarely, less than estradiol (E2) and progesterone secretion [10], has a once a week, and more than once a week. Personal care similar effect as estrogen [11], and can induce hypothyr- products were classified as hair care products, body oxinemia [12]. Moreover, in experiments with mice, rats, cleansers, make-up products, nail care products, antibac- and hamsters, TCS has been associated with liver tumors terial agents, and fragrance products. Hair care products [4]. Contact dermatitis, photosensitivity, contact derma- referred to products such as waxes, gels, and sprays. titis, skin irritation, and other conditions have also been Body cleansers included foam cleansers, body wash, and reported in association with TCS [13, 14]. shampoo, but not soap. Make-up products included Because of these health problems, various regulations cosmetic products other than basic cosmetics, such as have recently been established in relation to TCS in skin care products and lotions; sun block products were many countries. Various studies on TCS exposure levels also included. Antimicrobial agents refer to liquid-type have also been carried out. However, studies on TCS antibacterial or sterilizing products [17]. levels in Korea and related factors have not yet been Sociodemographic variables and health behavior-re- conducted. In this study, we used a nationally represen- lated variables of participants were analyzed as follows. tative data for the general population in Korea to analyze Age and body mass index (BMI) were averaged as socio- the level of TCS exposure in the general population demographic variables. Education level was classified as according to the frequency of use of personal care prod- below a middle school graduate level, high school gradu- ucts, which are the main exposure source of TCS. ate level, or college graduate and above. Marital status was classified as unmarried, married, or other (divorced, widowed, separated), and socioeconomic status was Material and methods classified into quartiles according to household income. Study participants Participants were classified as never, former or current This study was based on data of the Second Korean smokers and alcohol drinkers. Participants were also National Environmental Health Survey (KoNEHS 2012– categorized according to physical activity level as 2014). According to Article 14 of the Environmental regularly performing no exercise, moderate exercise, or Health Act, the KoNEHS is conducted every 3 years to vigorous exercise. investigate the human exposure levels of harmful envir- onmental factors in the Korean population, explore the influencing factors, and continuously investigate the Urinary triclosan spatial and temporal distribution and change in these Urinary TCS concentration was measured using ultra factors [15]. performance liquid chromatography – tandem mass The survey area consisted of 16 cities and provinces spectrometry (UPLC–MS/MS) with the Xevo TQ-S nationwide. For the survey sample, the enumeration (Waters Corporation, Milford, MA, USA) using a spot districts of the National Population and Housing Census urine sample [18]. After hydrolyzing each urine sample 2010 were used for the sample population with the with ß-glucuronidase/arylsulfatase-degrading enzyme, initial stratification classified by local administration. the metabolites of TCS were extracted with ethyl ether Secondary stratification was according to socioeconomic and measured. The measuring principle of TCS concen- factors, using stratified multistage cluster sampling tration was to apply a calibration curve prepared by the applied with proportional allocation of the square root standard addition method with using standard solution of the population to extract 400 sample enumeration to the sample. For the precision control in the whole districts [16]. Approximately 15 people from each analysis process, relative standard deviation (RSD) of sample enumeration district were surveyed, targeting a two samples of low dose of standard solution should be total of 6478 Koreans aged 19 years and older. The sur- less than 15% for within batch and 20% for between vey consisted of an environmental exposure-related batch. Quality control (QC) sample was used for the questionnaire, clinical testing, and analysis of harmful accuracy control in the analysis process. The concentra- environmental substances in biological samples [15]. tions less than the method detection limit (MDL, In this study, after excluding 190 participants with 0.500 μg/L) were substituted with values of MDL divided missing urinary TCS concentration data, 6288 partici- by the square root of 2. The final TCS concentration for pants (2692 men, 3596 women) were included from statistical analysis was calculated after adjusting urinary among a total of 6478 participants. creatinine concentration. Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 3 of 8 Statistical analysis group. Additionally, more women in the high TCS The frequency and proportion of each variable were pre- exposure group reported more frequent use of nail care sented after stratification by gender to determine the products. general characteristics of participants. First, participants Logistic regression analysis was applied to determine were divided into a high TCS exposure group and low the degree of association between the frequency of TCS exposure group, based on the top 75th percentile personal care products use and urinary TCS concentra- concentration of urinary TCS (male: 1.096 μg/g creatin- tion according to low TCS and high TCS exposure ine, female: 1.329 μg/g creatinine). The frequency and groups (Table 3). In the case of men, fragrance products, proportion of each variable were then determined by hair care products, body cleansers, and cosmetics gender. Chi-square tests were performed to analyze the showed significantly higher ORs for use more than once difference in the distribution of each variable. Odds ra- a week versus rarely use: 1.52 (95% CI 1.16–1.98), 1.50 tios (ORs) and 95% confidence intervals (CIs) were cal- (95% CI 1.19–1.87), 1.67 (95% CI 1.33–2.08), and 1.60 culated using logistic regression for the high TCS (95% CI 1.19–2.15), respectively. In the case of women, exposure and low TCS exposure groups. Unadjusted hair care products, body cleansers, and cosmetics models are presented and a multivariate adjusted model showed significantly higher ORs for use more than once was adjusted for age, BMI, socioeconomic variables, and a week versus rarely use of these products: 1.20 (95% CI health behavior-related variables. IBM SPSS version 19 1.01–1.42), 1.28 (95% CI 1.04–1.58), and 1.33 (95% CI for Windows (SPSS Inc., Chicago, IL, USA) was used for 1.08–1.65), respectively. Interestingly, ORs were higher statistical analysis and the statistical significance level in men than in women. was set at p < 0.05. Discussion Results In this study, general characteristics for high urinary The distribution of the independent variables in the TCS concentration were younger age, higher educational present study was as follows (Table 1). A total 2692 level, higher household income level, drinkers, and (42.8%) participants were male, and 3596 (57.2%) were vigorous exercise group. In a previous study in Canada, female. A greater percentage of men than women were higher urinary TCS concentrations were found among college graduates or higher, and more men than women women with higher education and income levels, with were current drinkers and smokers. In terms of fra- higher TCS exposure levels in those over 25 years of age grance products, hair care products, nail care products, than in those under age 25 years [19]. In the United antimicrobial agents, and air fresheners usage, more States (US), a study among the general population than half of men and women responded that they rarely showed that the higher the income, the higher the con- used these products. More than half of men said they centration of urinary TCS, in relation to age, with the rarely used cosmetics and body cleansers, whereas more highest concentrations among participants in their 30s; than half of women reported using these products once concentrations then gradually decreased with age [2]. a week. On the other hand, according to a study conducted in Urine TCS concentration was determined according to Korea in 2009, older age and lower income levels were high and low TCS exposure groups, based on the upper associated with higher urinary TCS concentration with 75th percentile concentration; the distribution of inde- no significant difference [20]. Explanations for the differ- pendent variables is presented in Table 2. The average ing results among studies may be owing to differences in age in the high TCS exposure group was significantly lifestyles, such as different frequency of use of TCS-con- lower than that in the low exposure group. Furthermore, taining consumer products; additional research is needed the urinary TCS concentration tended to decrease as age to clarify these differences in study findings [20]. There increased (See Additional file 1: Table S1). For both has been no confirmation of the common trend found genders, the proportions of college graduates and partic- among studies regarding characteristics of drinking, ipants with household income in the third quartile or smoking, exercise, and BMI of participants. The high higher, were significantly greater in the high TCS TCS exposure among young adults aged 20–30 years is exposure group than in the low exposure group; the pro- important in that it can be associated with pregnancy portions of current drinkers and participants who vigor- and childbirth. TCS is an endocrine disruptor and sev- ously exercised were also higher in the high TCS eral animal studies have found that it can affect thyroid exposure group. Distribution by frequency of use of hormone homeostasis [1]. Because thyroid hormones are personal care products showed that for both genders, essential for development of the fetal nervous system perfumes, hair care products, body cleansers, cosmetics, and differentiation of the brain, deficiency of thyroid and antimicrobial agents were used more frequently in hormones can cause fetal neurodevelopmental problems the high TCS exposure group than in the low exposure [21–23]. Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 4 of 8 Table 1 Basic characteristics according to sociodemographic factors and several exposure factros to triclosan in study population Category Total (n = 6288) Male (n = 2692) Female (n = 3596) Triclosan level (μg/L) 0.35 (0.35–1.21) 0.35 (0.35–1.09) 0.35 (0.35–1.33) Age (years) 51.6 (15.1) 51.7 (15.5) 51.4 (14.8) BMI (kg/m ) 24.3 (3.4) 24.6 (3.2) 24.1 (3.5) Education ≤ Middle school 2207 (35.1) 762 (28.3) 1445 (40.2) High school 1901 (30.2) 822 (30.5) 1079 (30.0) ≥ College 2180 (34.7) 1108 (41.2) 1072 (29.8) Marital status Single 632 (10.0) 346 (12.9) 286 (7.9) Married 4992 (79.4) 2213 (82.2) 2779 (77.3) Others 664 (10.6) 133 (4.9) 531 (14.8) Household income 1st quartile 1767 (28.1) 769 (28.6) 998 (27.8) 2nd quartile 2900 (46.1) 1261 (46.8) 1639 (45.6) 3rd quartile 1563 (24.9) 634 (23.6) 929 (25.8) 4th quartile 58 (0.9) 28 (1.0) 30 (0.8) Smoking None 4147 (66.0) 742 (27.6) 3405 (94.7) Ex-smoker 1028 (16.3) 964 (35.8) 64 (1.8) Current-smoker 1013 (17.7) 986 (36.6) 127 (3.5) Alcohol None 2153 (34.2) 429 (15.9) 1724 (47.9) Ex 412 (6.6) 274 (10.2) 138 (3.9) Current 3723 (59.2) 1989 (73.9) 1734 (48.2) Exercise No 3307 (52.6) 1309 (48.6) 1998 (55.6) Moderate 709 (11.3) 284 (10.6) 425 (11.8) Vigorous 2272 (36.1) 1099 (40.8) 1173 (32.6) Fragrance products Rarely 5023 (79.9) 2269 (84.3) 2754 (76.6) < Once a week 403 (6.4) 122 (4.5) 281 (7.8) ≥ Once a week 862 (13.7) 301 (11.2) 561 (15.6) Hair care products Rarely 3838 (61.1) 1948 (72.4) 1890 (52.5) < Once a week 732 (11.6) 251 (9.3) 481 (13.4) ≥ Once a week 1718 (27.3) 493 (18.3) 1225 (34.1) Body cleansers Rarely 2958 (47.0) 1902 (70.7) 1056 (29.4) < Once a week 110 (1.8) 46 (1.7) 64 (1.8) ≥ Once a week 3220 (51.2) 744 (27.6) 2476 (68.8) Cosmetics Rarely 3154 (50.2) 2381 (88.5) 773 (21.5) < Once a week 252 (4.0) 81 (3.0) 171 (4.8) ≥ Once a week 2882 (45.8) 230 (8.5) 2652 (73.7) Nail care products Rarely 5325 (84.7) 2681 (99.6) 2644 (73.5) < Once a week 678 (10.8) 8 (0.3) 670 (18.6) ≥ Once a week 285 (4.5) 3 (0.1) 282 (7.9) Antimicrobial agents Rarely 5234 (83.2) 2320 (86.2) 2914 (81.0) < Once a week 213 (3.4) 57 (2.1) 156 (4.4) ≥ Once a week 841 (13.4) 315 (11.7) 526 (14.6) Air freshener Rarely 4673 (74.3) 2017 (74.9) 2656 (73.9) < Once a week 231 (3.7) 73 (2.7) 158 (4.4) ≥ Once a week 1384 (22.0) 602 (22.4) 782 (21.7) Data are mean (standard deviation), median (interquartile range), or number (%) Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 5 of 8 Table 2 Basic characteristics of study population in both high (the top 75th percentile) and low urinary concentration of triclosan group by gender Male Female Category Low (n = 2016) High (n = 676) p value Low (n = 2696) High (n = 900) p value Age (years) 52.6 (15.3) 49.0 (15.9) < 0.0001 52.3 (14.7) 48.8 (14.7) < 0.0001 BMI (kg/m ) 24.5 (3.1) 24.7 (3.3) 0.219 24.1 (3.5) 23.9 (3.5) 0.034 Education ≤ Middle school 618 (30.6) 144 (21.3) < 0.0001 1162 (43.1) 283 (31.4) < 0.0001 High school 633 (31.4) 189 (28.0) 783 (29.0) 296 (32.9) ≥ College 765 (38.0) 343 (50.7) 751 (27.9) 321 (35.7) Marital status Single 234 (11.6) 112 (16.6) 0.003 187 (6.9) 99 (11.0) < 0.0001 Married 1678 (83.2) 535 (79.1) 2088 (77.5) 691 (76.8) Others 104 (5.2) 29 (4.3) 421 (15.6) 110 (12.2) Household income 1st quartile 598 (29.6) 171 (29.3) 0.039 790 (29.3) 208 (23.1) < 0.0001 2nd quartile 947 (47.0) 314 (46.4) 1223 (45.4) 416 (46.2) 3rd quartile 451 (22.4) 183 (27.1) 663 (24.6) 266 (29.6) 4th quartile 20 (1.0) 8 (1.2) 20 (0.7) 10 (1.1) Smoking None 552 (27.4) 190 (28.2) 0.898 2551 (94.6) 854 (94.9) 0.135 Ex-smoker 721 (35.8) 243 (35.9) 43 (1.6) 21 (2.3) Current smoker 743 (36.8) 243 (35.9) 102 (3.8) 25 (2.8) Alcohol None 333 (16.5) 96 (14.2) < 0.0001 1323 (49.1) 401 (44.5) 0.036 Ex 227 (11.3) 47 (6.9) 96 (3.6) 42 (4.7) Current 1456 (72.2) 533 (78.9) 1277 (47.3) 457 (50.8) Exercise No 1007 (49.9) 302 (44.7) 0.029 1538 (57.0) 460 (51.1) 0.005 Moderate 215 (10.7) 69 (10.2) 300 (11.1) 125 (13.9) Vigorous 794 (39.4) 305 (45.1) 858 (31.9) 315 (35.0) Fragrance products Rarely 1740 (86.3) 529 (78.3) < 0.0001 2106 (78.1) 648 (72.0) < 0.0001 < Once a week 83 (4.1) 39 (5.8) 192 (7.1) 89 (9.9) ≥ Once a week 193 (9.6) 108 (15.9) 398 (14.8) 163 (18.1) Hair care products Rarely 1510 (74.9) 438 (64.8) < 0.0001 1442 (53.5) 448 (49.8) 0.113 < Once a week 179 (8.9) 72 (10.6) 360 (13.3) 121 (13.4) ≥ Once a week 327 (16.2) 166 (24.6) 894 (33.2) 331 (36.8) Body cleansers Rarely 1496 (74.2) 406 (60.1) < 0.0001 858 (31.8) 198 (22.0) < 0.0001 < Once a week 13 (1.6) 13 (1.9) 49 (1.8) 15 (1.7) ≥ Once a week 487 (24.2) 257 (38.0) 1789 (66.4) 687 (76.3) Cosmetics Rarely 1814 (90.0) 567 (83.9) < 0.0001 629 (23.3) 144 (16.0) < 0.0001 < Once a week 56 (2.8) 25 (3.7) 136 (5.0) 35 (3.9) ≥ Once a week 146 (7.2) 84 (12.4) 1931 (71.6) 721 (80.1) Nail care products Rarely 2007 (99.5) 674 (99.7) 0.604 2024 (75.1) 620 (68.9) 0.001 < Once a week 6 (0.3) 2 (0.3) 469 (17.4) 201 (22.3) ≥ Once a week 3 (0.2) 0 (0.0) 203 (7.5) 79 (8.8) Antimicrobial agents Rarely 1763 (87.4) 557 (82.4) 0.004 2215 (82.2) 699 (77.7) 0.008 < Once a week 38 (1.9) 19 (2.8) 114 (4.2) 42 (4.7) ≥ Once a week 215 (10.7) 100 (14.8) 367 (13.6) 159 (17.6) Air fresheners Rarely 1517 (75.3) 500 (73.9) 0.55 2014 (74.7) 642 (71.3) 0.13 < Once a week 57 (2.8) 16 (2.4) 113 (4.2) 45 (5.0) ≥ Once a week 442 (21.9) 160 (23.7) 569 (21.1) 213 (23.7) Male:≥ 1.096 μg/g creatinine, female: ≥1.329 μg/g creatinine, data are mean (standard deviation), or number (%) Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 6 of 8 Table 3 Odds ratios (OR) and 95% confidence intervals (CI) relating personal care products usage of high urinary concentration of triclosan (male: ≥ 1.096 μg/g creatinine, female: ≥1.329 μg/g creatinine) compared to low urinary concentration of triclosan Male Female Category Unadjusted Multivariate adjusted model Unadjusted Multivariate adjusted model Fragrance products Rarely 1.00 1.00 1.00 1.00 < Once a week 1.55 (1.04–2.29) 1.39 (0.93–2.07) 1.51 (1.15–1.97) 1.27 (0.97–1.67) ≥ Once a week 1.84 (1.43–2.38) 1.52 (1.16–1.98) 1.33 (1.09–1.63) 1.05 (0.84–1.30) Hair care products Rarely 1.00 1.00 1.00 1.00 < Once a week 1.39 (1.03–1.86) 1.39 (1.03–1.87) 1.08 (0.86–1.36) 1.21 (0.96–1.54) ≥ Once a week 1.75 (1.41–2.17) 1.50 (1.19–1.87) 1.19 (1.01–1.41) 1.20 (1.01–1.42) Body cleansers Rarely 1.00 1.00 1.00 1.00 < Once a week 1.45 (0.76–2.78) 1.20 (0.62–2.32) 1.33 (0.73–2.41) 1.20 (0.66–2.20) ≥ Once a week 1.95 (1.61–2.34) 1.67 (1.33–2.08) 1.66 (1.39–1.99) 1.28 (1.04–1.58) Cosmetics Rarely 1.00 1.00 1.00 1.00 < Once a week 1.43 (0.88–2.31) 1.21 (0.74–1.98) 1.12 (0.74–1.70) 1.04 (0.68–1.58) ≥ Once a week 1.84 (1.39–2.45) 1.60 (1.19–2.15) 1.63 (1.33–1.99) 1.33 (1.08–1.65) Nail care products Rarely 1.00 1.00 1.00 1.00 < Once a week 0.99 (0.20–4.93) 1.06 (0.21–5.30) 1.40 (1.16–1.69) 1.26 (1.04–1.53) ≥ Once a week –– 1.27 (0.97–1.67) 1.13 (0.85–1.50) Antimicrobial agents Rarely 1.00 1.00 1.00 1.00 < Once a week 1.58 (0.91–2.77) 1.43 (0.81–2.52) 1.17 (0.81–1.68) 0.98 (0.67–1.42) ≥ Once a week 1.47 (1.14–1.90) 1.27 (0.98–1.65) 1.37 (1.12–1.69) 1.17 (0.95–1.44) Air fresheners Rarely 1.00 1.00 1.00 1.00 < Once a week 0.85 (0.49–1.50) 0.82 (0.47–1.46) 1.25 (0.87–1.79) 1.20 (0.84–1.72) ≥ Once a week 1.10 (0.89–1.35) 0.96 (0.78–1.20) 1.17 (0.98–1.41) 1.03 (0.85–1.24) Multivariate adjusted model: adjusted with age, BMI, education, marital status, household income, alcohol intake, exercise, and smoking According to analysis of the relationship between the showed higher ORs than women. Men tend to use less frequency of use of personal care products and urinary personal care products compared to women, which may TCS concentration, we found that the frequency of use be the cause of the larger differences between used and of hair care products, body cleansers, and cosmetics unused groups. These results suggest that personal care were consistently related to urinary TCS concentration products are a major source of TCS exposure. in both men and women. In the upper 75th percentile of As a result of analyzing a list of the raw materials of urinary TCS concentration, the proportion of more cosmetics reported to the Korea Food & Drug Adminis- frequent products use was higher than among partici- tration (KFDA) by domestic manufacturers in 2015, 127 pants with rarely products use and ORs were higher in of the 100,190 (0.13%) cosmetics products manufactured participants who used these products more often. Simi- in Korea were found to have used TCS [24]. It has been lar results were found in a study of breastfeeding found that TCS is mainly used in products that are mothers in Sweden. Mothers who used personal care rinsed off after use, such as body cleansers and foam products containing TCS showed significantly higher cleansers [24]. According to US data in 2010, 28 of 3359 breast milk and plasma TCS concentrations than those eye make-up products, 10 of 4345 facial make-up prod- who did not use these products [8]. In addition, men ucts, 226 of 3070 body cleansing products, 3 of 5242 Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 7 of 8 hair care products, and 42 of 2842 fragrance products toxic substances as they have rapid rates of body contained TCS [25]. TCS is mainly found in body organ development and their processes of detoxifica- cleansing products and it is thought that exposure via tion of toxic substances are less developed [27]. these products is high. A smaller number of cosmetics Therefore, additional research is needed to determine and hair care products contain TCS, but these can result whether current levels of regulation are appropriate in direct exposure and TCS-containing cleansing prod- for these susceptible population. ucts are often used to remove cosmetics. Therefore, The limitations of this study are as follows. First, we urine TCS concentrations may be high depending on the did not identify the usage amount of personal care prod- use frequency of cosmetics and hair care products. ucts, only the frequency of use. Second, we did not According to the results of previous studies both on consider the simultaneous use of other personal care TCS toxicity in humans and use of personal care prod- products, use of other personal care products not in- ucts as the main exposure source of TCS, regulations on cluded in the survey, and other TCS exposure factors the use of TCS for personal care products have been apart from personal care products. Third, in about 60% established in many countries. In Korea, KFDA launched of participants, urinary TCS concentration was mea- a new regulation with TCS concentration in personal sured below the detection limit. However, it did not care products, such as, body cleansing products that are affect the statistical analysis of this study. Fourth, the rinsed off after use, deodorants (excluding spray prod- health effects of increased urinary TCS concentration ucts), face powder, and foundation like concealer, that were not analyzed. Despite these limitations, this study the concentration limit of TCS in personal care products suggested the exposure level of TCS and the relationship was 0.3%; moreover, TCS could not be used in tooth- with use of personal care products, which are major paste and mouthwash in 2015 [24]. In Europe, the exposure sources of TCS using a representative data in concentration limit of TCS in mouthwash was 0.2% and Korean population. that in other personal hygiene products was 0.3%. In the Regulation of TCS was initiated in Korea in 2015 and case of Japan, the concentration limit of TCS in all prod- it is expected that the effect of reduction of TCS expos- ucts 0.1% [24]. Although TCS regulation has started in ure by the regulation will be confirmed through the ana- many countries, some cosmetics and human body lysis of third KoNEHS data, which was conducted in cleansing products still contain TCS and these products 2015–2017 and not publically released yet. Furthermore, still can be purchased in countries with no regulations children over three years old were included in the study in place. Regulatory concentrations are set at levels that population in the third KoNEHS, therefore, the TCS are harmless to the human body [24]; however, women exposure level and health effects could be studied in the of childbearing age, children, and adolescents should susceptible population. Based on future studies, it could select products that do not contain TCS or should rinse confirm the effect of the regulation and suggest another them off thoroughly after use. It is especially important more powerful policy to minimize TCS exposure in to be careful when purchasing mouthwash in some Korean population. foreign countries because nearly 100% of TCS can be absorbed in the oral cavity [3]. Conclusion In the present study, similar to those of other coun- This study found out the association of the use of tries, we found a tendency for urinary TCS concentra- personal care products and the concentration of urin- tion to increase in younger age, higher income level and ary TCS in general population in Korea. According to education level. The present study findings also con- this study, the levels of urinary TCS were higher in firmed that personal care products represent the main female, younger people, and higher-income people. cause of TCS exposure. People with higher levels of Because TCS is a well-known endocrine disruptor and income and education tend to have greater interest in several health problems related with exposure to TCS personal hygiene and tend to purchase personal care have suggested, further studies are needed to monitor products, which may lead to increased exposure to the trend of urinary TCS level and explore other chemicals such as TCS. Likewise, young people in health effects with exposure to TCS in general popu- their 20s and 30s are more concerned about personal lation in Korea using a representative data for general care than children, adolescents, and elderly adults; population. therefore, this young population is more exposed to TCS through greater use of personal care products. Additional file TCS in women of childbearing age can be a potential neurotoxic agent for the fetus during pregnancy [26] Additional file 1: Medians (interquartile range) of Urinary TCS concentration according to age. The urinary TCS concentration tended to decrease as age and can be delivered to infants through breast milk. increased. (XLSX 11 kb) Infants and young children are highly susceptible to Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 8 of 8 Abbreviations 12. Helbing CC, van Aggelen G, Veldhoen N. Triclosan affects thyroid hormone- BMI: Body mass index; CI: Confidence interval; KoNEHS: Korean National dependent metamorphosis in anurans. Toxicol Sci. 2011;119(2):417–8 Environmental Health Survey; OR: Odds ratio; TCS: Triclosan author reply 9-22. 13. Durbize E, Vigan M, Puzenat E, Girardin P, Adessi B, Desprez PH, et al. Spectrum of cross-photosensitization in 18 consecutive patients with Acknowledgements contact photoallergy to ketoprofen: associated photoallergies to non- There is no conflict of interest or financial support to declare. benzophenone-containing molecules. Contact Dermatitis. 2003;48(3):144–9. 14. Storer E, Koh KJ, Warren L. Severe contact dermatitis as a result of an Funding antiseptic bath oil. Australas J Dermatol. 2004;45(1):73–5. Not applicable. 15. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Survey overview. Guidelines for using raw materials for Korean National Environmental Health Survey - the second Availability of data and materials stage ('12-'14). Incheon: Korean national institute of environmental research; The data of the KoNEHS is opened to the public, therefore, any researcher 2017. p. 1–5. can be obtained after request from the website http://meta.narastat.kr/ 16. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Sample design. Guidelines for using metasvc/svc/SvcMetaDcDtaPopup.do?confmNo=106027&inputYear=2012. raw materials for Korean National Environmental Health Survey - the second stage (‘12∼‘14). Incheon: Korean national institute of environmental research; Authors’ contributions 2017. p. 6–15. MP designed this study and wrote a draft of this manuscript. SK, YK, and DJN 17. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Survey Items. Guidelines for using raw analyzed the data. JR provided technical support. SL performed critical revision materials for Korean National Environmental Health Survey - the second of the manuscript. All authors read and approved the final manuscript. stage (‘12∼‘14). Incheon: Korean national institute of environmental research; 2017. p. 28–9. 18. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Analysis manual of environmental Ethics approval and consent to participate noxious materials. Guidelines for using raw materials for Korean National Not applicable. Environmental Health Survey - the second stage ('12-'14). Incheon: Korean national institute of environmental research; 2017. p. 54–67. Consent for publication 19. Arbuckle TE, Marro L, Davis K, Fisher M, Ayotte P, Belanger P, et al. Exposure Not applicable. to free and conjugated forms of bisphenol a and triclosan among pregnant women in the MIREC cohort. Environ Health Perspect. 2015;123(4):277–84. Competing interests 20. Kim K, Park H, Yang W, Lee JH. Urinary concentrations of bisphenol a and The authors declare that they have no competing interests. triclosan and associations with demographic factors in the Korean population. Environ Res. 2011;111(8):1280–5. 21. Boas M, Feldt-Rasmussen U, Main KM. Thyroid effects of endocrine Publisher’sNote disrupting chemicals. Mol Cell Endocrinol. 2012;355(2):240–8. Springer Nature remains neutral with regard to jurisdictional claims in 22. Krassas GE, Poppe K, Glinoer D. Thyroid function and human reproductive published maps and institutional affiliations. health. Endocr Rev. 2010;31(5):702–55. 23. Zoeller TR, Dowling AL, Herzig CT, Iannacone EA, Gauger KJ, Bansal R. Received: 31 August 2018 Accepted: 22 January 2019 Thyroid hormone, brain development, and the environment. Environ Health Perspect. 2002;110(Suppl 3):355–61. 24. Cosmetics Research Team. Risk assessment of cosmetics. Cheongju-si: The References National Institute of Food and Drug Safety Evaluation, Ministry of Food and 1. Dann AB, Hontela A. Triclosan: environmental exposure, toxicity and Drug Safety; 2017. p. 151–72. mechanisms of action. J Appl Toxicol. 2011;31(4):285–311. 25. Cosmetic Ingredient Review Expert P. Final safety assessment of triclosan. 2. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Urinary concentrations Washington, DC: The cosmetic ingredient review; 2010. p.33–7. of triclosan in the U.S. population: 2003-2004. Environ Health Perspect. 2008; 26. Yueh MF, Tukey RH. Triclosan: a widespread environmental toxicant with 116(3):303–7. many biological effects. Annu Rev Pharmacol Toxicol. 2016;56:251–72. 3. Cullinan MP, Palmer JE, Carle AD, West MJ, Westerman B, Seymour GJ. The 27. Goldman LR. Children-unique and vulnerable. Environmental risks facing influence of a triclosan toothpaste on adverse events in patients with children and recommendations for response. Environ Health Perspect. cardiovascular disease over 5-years. Sci Total Environ. 2015;508:546–52. 1995;103(Suppl 6):13–8. 4. Rodricks JV, Swenberg JA, Borzelleca JF, Maronpot RR, Shipp AM. Triclosan: a critical review of the experimental data and development of margins of safety for consumer products. Crit Rev Toxicol. 2010;40(5):422–84. 5. Sandborgh-Englund G, Adolfsson-Erici M, Odham G, Ekstrand J. Pharmacokinetics of triclosan following oral ingestion in humans. J Toxicol Environ Health A. 2006;69(20):1861–73. 6. Den Hond E, Paulussen M, Geens T, Bruckers L, Baeyens W, David F, et al. Biomarkers of human exposure to personal care products: results from the Flemish Environment and Health Study (FLEHS 2007-2011). Sci Total Environ. 2013;463-464:102–10. 7. Allmyr M, Harden F, Toms LM, Mueller JF, McLachlan MS, Adolfsson-Erici M, et al. The influence of age and gender on triclosan concentrations in Australian human blood serum. Sci Total Environ. 2008;393(1):162–7. 8. Allmyr M, Adolfsson-Erici M, McLachlan MS, Sandborgh-Englund G. Triclosan in plasma and milk from Swedish nursing mothers and their exposure via personal care products. Sci Total Environ. 2006;372(1):87–93. 9. Crofton KM, Paul KB, Devito MJ, Hedge JM. Short-term in vivo exposure to the water contaminant triclosan: evidence for disruption of thyroxine. Environ Toxicol Pharmacol. 2007;24(2):194–7. 10. Gee RH, Charles A, Taylor N, Darbre PD. Oestrogenic and androgenic activity of triclosan in breast cancer cells. J Appl Toxicol. 2008;28(1):78–91. 11. Henry ND, Fair PA. Comparison of in vitro cytotoxicity, estrogenicity and anti-estrogenicity of triclosan, perfluorooctane sulfonate and perfluorooctanoic acid. J Appl Toxicol. 2013;33(4):265–72. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Annals of Occupational and Environmental Medicine Springer Journals

Relationship between personal care products usage and triclosan exposure: the second Korean National Environmental Health Survey (KoNEHS 2012–2014)

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Springer Journals
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Copyright © 2019 by The Author(s).
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Medicine & Public Health; Public Health; Occupational Medicine/Industrial Medicine
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2052-4374
DOI
10.1186/s40557-019-0283-y
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Abstract

Background: We aimed to find the exposure level of triclosan (TCS), a known endocrine disruptor, related to the use of personal care products using a nationally representative data of the general population in Korea. Methods: This study included data of 6288 adults aged 19 years and older (2692 men, 3596 women), based on the Second Korean National Environmental Health Survey (KoNEHS 2012–2014). The data were divided according to gender. The frequency and proportion of each variable were determined by dividing participants into two groups based on the top 75th percentile concentration of urinary TCS (male: 1.096 μg/g creatinine, female: 1.329 μg/g creatinine). Odds ratios (ORs) were calculated using logistic regression analysis for the high TCS exposure and low TCS exposure groups. Results: Overall, the proportion of participants using personal care products was higher in women than in men. There was a significantly higher proportion of participants in the high TCS exposure group with younger age, higher education and income levels and with more frequent use of fragrance products, hair care products, body cleansers, cosmetics, and antimicrobial agents. In both men and women, ORs tended to increase with increased frequency of use of hair care products, body cleansers, and cosmetics before and after adjustment. Conclusions: Our findings demonstrate that as the frequency of use of personal care products increases, urine TCS concentration increases. Because TCS is a well-known endocrine disruptor, further studies are needed and explore other health effects with exposure to TCS in general population in Korea. Keywords: Triclosan, Personal care products, Korean National Environmental Health Survey Background TCS is absorbed into the body through the mouth and Triclosan (TCS), chemical name 5-chloro-2-(2,4-dichlor- skin [2]. TCS is absorbed at a rate of nearly 100% in the ophenoxy)phenol, is a synthetic antimicrobial and anti- oral cavity, with a half-life of 10–20 h; less than 10% is fungal agent, which is widely used throughout the world. absorbed via the transdermal route, with a half-life of TCS is used mainly as a disinfectant in soaps, detergents, 1.4–2.1 days. Absorbed TCS is detected mainly in toothpaste, mouthwash, fabrics, deodorant, shampoo, plasma, urine, and breast milk [3]; it is mostly excreted and plastic additives, and it is used in many personal in the urine [4]. According to a pharmacokinetic study, care products, animal products, and industry and house- after oral administration of 4 mg TCS, most was ex- hold products [1]. creted in the urine within the first 24 h and levels had recovered to baseline within 8 days after administration [5]. These results demonstrate that urinary TCS concen- * Correspondence: drforest@hanmail.net trations can be used as a biomarker of TCS exposure Department of Occupational and Environmental Medicine, Kyung Hee [6]. There have been several studies indicating that University Medical Center, Seoul, South Korea Department of Occupational and Environmental Medicine, School of Medicine Kyung Hee University, Seoul, Korea © The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 2 of 8 urinary TCS concentrations are associated with the use Variables of personal care products containing TCS [6–8]. Variables of interest TCS is known to be an endocrine disruptor that is To determine the association between TCS exposure structurally similar to polychlorinated biphenyls, bisphe- and frequency of personal care products use, the fre- nol A, dioxins, and thyroid hormones [9]. TCS increases quency of use was classified as used rarely, less than estradiol (E2) and progesterone secretion [10], has a once a week, and more than once a week. Personal care similar effect as estrogen [11], and can induce hypothyr- products were classified as hair care products, body oxinemia [12]. Moreover, in experiments with mice, rats, cleansers, make-up products, nail care products, antibac- and hamsters, TCS has been associated with liver tumors terial agents, and fragrance products. Hair care products [4]. Contact dermatitis, photosensitivity, contact derma- referred to products such as waxes, gels, and sprays. titis, skin irritation, and other conditions have also been Body cleansers included foam cleansers, body wash, and reported in association with TCS [13, 14]. shampoo, but not soap. Make-up products included Because of these health problems, various regulations cosmetic products other than basic cosmetics, such as have recently been established in relation to TCS in skin care products and lotions; sun block products were many countries. Various studies on TCS exposure levels also included. Antimicrobial agents refer to liquid-type have also been carried out. However, studies on TCS antibacterial or sterilizing products [17]. levels in Korea and related factors have not yet been Sociodemographic variables and health behavior-re- conducted. In this study, we used a nationally represen- lated variables of participants were analyzed as follows. tative data for the general population in Korea to analyze Age and body mass index (BMI) were averaged as socio- the level of TCS exposure in the general population demographic variables. Education level was classified as according to the frequency of use of personal care prod- below a middle school graduate level, high school gradu- ucts, which are the main exposure source of TCS. ate level, or college graduate and above. Marital status was classified as unmarried, married, or other (divorced, widowed, separated), and socioeconomic status was Material and methods classified into quartiles according to household income. Study participants Participants were classified as never, former or current This study was based on data of the Second Korean smokers and alcohol drinkers. Participants were also National Environmental Health Survey (KoNEHS 2012– categorized according to physical activity level as 2014). According to Article 14 of the Environmental regularly performing no exercise, moderate exercise, or Health Act, the KoNEHS is conducted every 3 years to vigorous exercise. investigate the human exposure levels of harmful envir- onmental factors in the Korean population, explore the influencing factors, and continuously investigate the Urinary triclosan spatial and temporal distribution and change in these Urinary TCS concentration was measured using ultra factors [15]. performance liquid chromatography – tandem mass The survey area consisted of 16 cities and provinces spectrometry (UPLC–MS/MS) with the Xevo TQ-S nationwide. For the survey sample, the enumeration (Waters Corporation, Milford, MA, USA) using a spot districts of the National Population and Housing Census urine sample [18]. After hydrolyzing each urine sample 2010 were used for the sample population with the with ß-glucuronidase/arylsulfatase-degrading enzyme, initial stratification classified by local administration. the metabolites of TCS were extracted with ethyl ether Secondary stratification was according to socioeconomic and measured. The measuring principle of TCS concen- factors, using stratified multistage cluster sampling tration was to apply a calibration curve prepared by the applied with proportional allocation of the square root standard addition method with using standard solution of the population to extract 400 sample enumeration to the sample. For the precision control in the whole districts [16]. Approximately 15 people from each analysis process, relative standard deviation (RSD) of sample enumeration district were surveyed, targeting a two samples of low dose of standard solution should be total of 6478 Koreans aged 19 years and older. The sur- less than 15% for within batch and 20% for between vey consisted of an environmental exposure-related batch. Quality control (QC) sample was used for the questionnaire, clinical testing, and analysis of harmful accuracy control in the analysis process. The concentra- environmental substances in biological samples [15]. tions less than the method detection limit (MDL, In this study, after excluding 190 participants with 0.500 μg/L) were substituted with values of MDL divided missing urinary TCS concentration data, 6288 partici- by the square root of 2. The final TCS concentration for pants (2692 men, 3596 women) were included from statistical analysis was calculated after adjusting urinary among a total of 6478 participants. creatinine concentration. Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 3 of 8 Statistical analysis group. Additionally, more women in the high TCS The frequency and proportion of each variable were pre- exposure group reported more frequent use of nail care sented after stratification by gender to determine the products. general characteristics of participants. First, participants Logistic regression analysis was applied to determine were divided into a high TCS exposure group and low the degree of association between the frequency of TCS exposure group, based on the top 75th percentile personal care products use and urinary TCS concentra- concentration of urinary TCS (male: 1.096 μg/g creatin- tion according to low TCS and high TCS exposure ine, female: 1.329 μg/g creatinine). The frequency and groups (Table 3). In the case of men, fragrance products, proportion of each variable were then determined by hair care products, body cleansers, and cosmetics gender. Chi-square tests were performed to analyze the showed significantly higher ORs for use more than once difference in the distribution of each variable. Odds ra- a week versus rarely use: 1.52 (95% CI 1.16–1.98), 1.50 tios (ORs) and 95% confidence intervals (CIs) were cal- (95% CI 1.19–1.87), 1.67 (95% CI 1.33–2.08), and 1.60 culated using logistic regression for the high TCS (95% CI 1.19–2.15), respectively. In the case of women, exposure and low TCS exposure groups. Unadjusted hair care products, body cleansers, and cosmetics models are presented and a multivariate adjusted model showed significantly higher ORs for use more than once was adjusted for age, BMI, socioeconomic variables, and a week versus rarely use of these products: 1.20 (95% CI health behavior-related variables. IBM SPSS version 19 1.01–1.42), 1.28 (95% CI 1.04–1.58), and 1.33 (95% CI for Windows (SPSS Inc., Chicago, IL, USA) was used for 1.08–1.65), respectively. Interestingly, ORs were higher statistical analysis and the statistical significance level in men than in women. was set at p < 0.05. Discussion Results In this study, general characteristics for high urinary The distribution of the independent variables in the TCS concentration were younger age, higher educational present study was as follows (Table 1). A total 2692 level, higher household income level, drinkers, and (42.8%) participants were male, and 3596 (57.2%) were vigorous exercise group. In a previous study in Canada, female. A greater percentage of men than women were higher urinary TCS concentrations were found among college graduates or higher, and more men than women women with higher education and income levels, with were current drinkers and smokers. In terms of fra- higher TCS exposure levels in those over 25 years of age grance products, hair care products, nail care products, than in those under age 25 years [19]. In the United antimicrobial agents, and air fresheners usage, more States (US), a study among the general population than half of men and women responded that they rarely showed that the higher the income, the higher the con- used these products. More than half of men said they centration of urinary TCS, in relation to age, with the rarely used cosmetics and body cleansers, whereas more highest concentrations among participants in their 30s; than half of women reported using these products once concentrations then gradually decreased with age [2]. a week. On the other hand, according to a study conducted in Urine TCS concentration was determined according to Korea in 2009, older age and lower income levels were high and low TCS exposure groups, based on the upper associated with higher urinary TCS concentration with 75th percentile concentration; the distribution of inde- no significant difference [20]. Explanations for the differ- pendent variables is presented in Table 2. The average ing results among studies may be owing to differences in age in the high TCS exposure group was significantly lifestyles, such as different frequency of use of TCS-con- lower than that in the low exposure group. Furthermore, taining consumer products; additional research is needed the urinary TCS concentration tended to decrease as age to clarify these differences in study findings [20]. There increased (See Additional file 1: Table S1). For both has been no confirmation of the common trend found genders, the proportions of college graduates and partic- among studies regarding characteristics of drinking, ipants with household income in the third quartile or smoking, exercise, and BMI of participants. The high higher, were significantly greater in the high TCS TCS exposure among young adults aged 20–30 years is exposure group than in the low exposure group; the pro- important in that it can be associated with pregnancy portions of current drinkers and participants who vigor- and childbirth. TCS is an endocrine disruptor and sev- ously exercised were also higher in the high TCS eral animal studies have found that it can affect thyroid exposure group. Distribution by frequency of use of hormone homeostasis [1]. Because thyroid hormones are personal care products showed that for both genders, essential for development of the fetal nervous system perfumes, hair care products, body cleansers, cosmetics, and differentiation of the brain, deficiency of thyroid and antimicrobial agents were used more frequently in hormones can cause fetal neurodevelopmental problems the high TCS exposure group than in the low exposure [21–23]. Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 4 of 8 Table 1 Basic characteristics according to sociodemographic factors and several exposure factros to triclosan in study population Category Total (n = 6288) Male (n = 2692) Female (n = 3596) Triclosan level (μg/L) 0.35 (0.35–1.21) 0.35 (0.35–1.09) 0.35 (0.35–1.33) Age (years) 51.6 (15.1) 51.7 (15.5) 51.4 (14.8) BMI (kg/m ) 24.3 (3.4) 24.6 (3.2) 24.1 (3.5) Education ≤ Middle school 2207 (35.1) 762 (28.3) 1445 (40.2) High school 1901 (30.2) 822 (30.5) 1079 (30.0) ≥ College 2180 (34.7) 1108 (41.2) 1072 (29.8) Marital status Single 632 (10.0) 346 (12.9) 286 (7.9) Married 4992 (79.4) 2213 (82.2) 2779 (77.3) Others 664 (10.6) 133 (4.9) 531 (14.8) Household income 1st quartile 1767 (28.1) 769 (28.6) 998 (27.8) 2nd quartile 2900 (46.1) 1261 (46.8) 1639 (45.6) 3rd quartile 1563 (24.9) 634 (23.6) 929 (25.8) 4th quartile 58 (0.9) 28 (1.0) 30 (0.8) Smoking None 4147 (66.0) 742 (27.6) 3405 (94.7) Ex-smoker 1028 (16.3) 964 (35.8) 64 (1.8) Current-smoker 1013 (17.7) 986 (36.6) 127 (3.5) Alcohol None 2153 (34.2) 429 (15.9) 1724 (47.9) Ex 412 (6.6) 274 (10.2) 138 (3.9) Current 3723 (59.2) 1989 (73.9) 1734 (48.2) Exercise No 3307 (52.6) 1309 (48.6) 1998 (55.6) Moderate 709 (11.3) 284 (10.6) 425 (11.8) Vigorous 2272 (36.1) 1099 (40.8) 1173 (32.6) Fragrance products Rarely 5023 (79.9) 2269 (84.3) 2754 (76.6) < Once a week 403 (6.4) 122 (4.5) 281 (7.8) ≥ Once a week 862 (13.7) 301 (11.2) 561 (15.6) Hair care products Rarely 3838 (61.1) 1948 (72.4) 1890 (52.5) < Once a week 732 (11.6) 251 (9.3) 481 (13.4) ≥ Once a week 1718 (27.3) 493 (18.3) 1225 (34.1) Body cleansers Rarely 2958 (47.0) 1902 (70.7) 1056 (29.4) < Once a week 110 (1.8) 46 (1.7) 64 (1.8) ≥ Once a week 3220 (51.2) 744 (27.6) 2476 (68.8) Cosmetics Rarely 3154 (50.2) 2381 (88.5) 773 (21.5) < Once a week 252 (4.0) 81 (3.0) 171 (4.8) ≥ Once a week 2882 (45.8) 230 (8.5) 2652 (73.7) Nail care products Rarely 5325 (84.7) 2681 (99.6) 2644 (73.5) < Once a week 678 (10.8) 8 (0.3) 670 (18.6) ≥ Once a week 285 (4.5) 3 (0.1) 282 (7.9) Antimicrobial agents Rarely 5234 (83.2) 2320 (86.2) 2914 (81.0) < Once a week 213 (3.4) 57 (2.1) 156 (4.4) ≥ Once a week 841 (13.4) 315 (11.7) 526 (14.6) Air freshener Rarely 4673 (74.3) 2017 (74.9) 2656 (73.9) < Once a week 231 (3.7) 73 (2.7) 158 (4.4) ≥ Once a week 1384 (22.0) 602 (22.4) 782 (21.7) Data are mean (standard deviation), median (interquartile range), or number (%) Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 5 of 8 Table 2 Basic characteristics of study population in both high (the top 75th percentile) and low urinary concentration of triclosan group by gender Male Female Category Low (n = 2016) High (n = 676) p value Low (n = 2696) High (n = 900) p value Age (years) 52.6 (15.3) 49.0 (15.9) < 0.0001 52.3 (14.7) 48.8 (14.7) < 0.0001 BMI (kg/m ) 24.5 (3.1) 24.7 (3.3) 0.219 24.1 (3.5) 23.9 (3.5) 0.034 Education ≤ Middle school 618 (30.6) 144 (21.3) < 0.0001 1162 (43.1) 283 (31.4) < 0.0001 High school 633 (31.4) 189 (28.0) 783 (29.0) 296 (32.9) ≥ College 765 (38.0) 343 (50.7) 751 (27.9) 321 (35.7) Marital status Single 234 (11.6) 112 (16.6) 0.003 187 (6.9) 99 (11.0) < 0.0001 Married 1678 (83.2) 535 (79.1) 2088 (77.5) 691 (76.8) Others 104 (5.2) 29 (4.3) 421 (15.6) 110 (12.2) Household income 1st quartile 598 (29.6) 171 (29.3) 0.039 790 (29.3) 208 (23.1) < 0.0001 2nd quartile 947 (47.0) 314 (46.4) 1223 (45.4) 416 (46.2) 3rd quartile 451 (22.4) 183 (27.1) 663 (24.6) 266 (29.6) 4th quartile 20 (1.0) 8 (1.2) 20 (0.7) 10 (1.1) Smoking None 552 (27.4) 190 (28.2) 0.898 2551 (94.6) 854 (94.9) 0.135 Ex-smoker 721 (35.8) 243 (35.9) 43 (1.6) 21 (2.3) Current smoker 743 (36.8) 243 (35.9) 102 (3.8) 25 (2.8) Alcohol None 333 (16.5) 96 (14.2) < 0.0001 1323 (49.1) 401 (44.5) 0.036 Ex 227 (11.3) 47 (6.9) 96 (3.6) 42 (4.7) Current 1456 (72.2) 533 (78.9) 1277 (47.3) 457 (50.8) Exercise No 1007 (49.9) 302 (44.7) 0.029 1538 (57.0) 460 (51.1) 0.005 Moderate 215 (10.7) 69 (10.2) 300 (11.1) 125 (13.9) Vigorous 794 (39.4) 305 (45.1) 858 (31.9) 315 (35.0) Fragrance products Rarely 1740 (86.3) 529 (78.3) < 0.0001 2106 (78.1) 648 (72.0) < 0.0001 < Once a week 83 (4.1) 39 (5.8) 192 (7.1) 89 (9.9) ≥ Once a week 193 (9.6) 108 (15.9) 398 (14.8) 163 (18.1) Hair care products Rarely 1510 (74.9) 438 (64.8) < 0.0001 1442 (53.5) 448 (49.8) 0.113 < Once a week 179 (8.9) 72 (10.6) 360 (13.3) 121 (13.4) ≥ Once a week 327 (16.2) 166 (24.6) 894 (33.2) 331 (36.8) Body cleansers Rarely 1496 (74.2) 406 (60.1) < 0.0001 858 (31.8) 198 (22.0) < 0.0001 < Once a week 13 (1.6) 13 (1.9) 49 (1.8) 15 (1.7) ≥ Once a week 487 (24.2) 257 (38.0) 1789 (66.4) 687 (76.3) Cosmetics Rarely 1814 (90.0) 567 (83.9) < 0.0001 629 (23.3) 144 (16.0) < 0.0001 < Once a week 56 (2.8) 25 (3.7) 136 (5.0) 35 (3.9) ≥ Once a week 146 (7.2) 84 (12.4) 1931 (71.6) 721 (80.1) Nail care products Rarely 2007 (99.5) 674 (99.7) 0.604 2024 (75.1) 620 (68.9) 0.001 < Once a week 6 (0.3) 2 (0.3) 469 (17.4) 201 (22.3) ≥ Once a week 3 (0.2) 0 (0.0) 203 (7.5) 79 (8.8) Antimicrobial agents Rarely 1763 (87.4) 557 (82.4) 0.004 2215 (82.2) 699 (77.7) 0.008 < Once a week 38 (1.9) 19 (2.8) 114 (4.2) 42 (4.7) ≥ Once a week 215 (10.7) 100 (14.8) 367 (13.6) 159 (17.6) Air fresheners Rarely 1517 (75.3) 500 (73.9) 0.55 2014 (74.7) 642 (71.3) 0.13 < Once a week 57 (2.8) 16 (2.4) 113 (4.2) 45 (5.0) ≥ Once a week 442 (21.9) 160 (23.7) 569 (21.1) 213 (23.7) Male:≥ 1.096 μg/g creatinine, female: ≥1.329 μg/g creatinine, data are mean (standard deviation), or number (%) Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 6 of 8 Table 3 Odds ratios (OR) and 95% confidence intervals (CI) relating personal care products usage of high urinary concentration of triclosan (male: ≥ 1.096 μg/g creatinine, female: ≥1.329 μg/g creatinine) compared to low urinary concentration of triclosan Male Female Category Unadjusted Multivariate adjusted model Unadjusted Multivariate adjusted model Fragrance products Rarely 1.00 1.00 1.00 1.00 < Once a week 1.55 (1.04–2.29) 1.39 (0.93–2.07) 1.51 (1.15–1.97) 1.27 (0.97–1.67) ≥ Once a week 1.84 (1.43–2.38) 1.52 (1.16–1.98) 1.33 (1.09–1.63) 1.05 (0.84–1.30) Hair care products Rarely 1.00 1.00 1.00 1.00 < Once a week 1.39 (1.03–1.86) 1.39 (1.03–1.87) 1.08 (0.86–1.36) 1.21 (0.96–1.54) ≥ Once a week 1.75 (1.41–2.17) 1.50 (1.19–1.87) 1.19 (1.01–1.41) 1.20 (1.01–1.42) Body cleansers Rarely 1.00 1.00 1.00 1.00 < Once a week 1.45 (0.76–2.78) 1.20 (0.62–2.32) 1.33 (0.73–2.41) 1.20 (0.66–2.20) ≥ Once a week 1.95 (1.61–2.34) 1.67 (1.33–2.08) 1.66 (1.39–1.99) 1.28 (1.04–1.58) Cosmetics Rarely 1.00 1.00 1.00 1.00 < Once a week 1.43 (0.88–2.31) 1.21 (0.74–1.98) 1.12 (0.74–1.70) 1.04 (0.68–1.58) ≥ Once a week 1.84 (1.39–2.45) 1.60 (1.19–2.15) 1.63 (1.33–1.99) 1.33 (1.08–1.65) Nail care products Rarely 1.00 1.00 1.00 1.00 < Once a week 0.99 (0.20–4.93) 1.06 (0.21–5.30) 1.40 (1.16–1.69) 1.26 (1.04–1.53) ≥ Once a week –– 1.27 (0.97–1.67) 1.13 (0.85–1.50) Antimicrobial agents Rarely 1.00 1.00 1.00 1.00 < Once a week 1.58 (0.91–2.77) 1.43 (0.81–2.52) 1.17 (0.81–1.68) 0.98 (0.67–1.42) ≥ Once a week 1.47 (1.14–1.90) 1.27 (0.98–1.65) 1.37 (1.12–1.69) 1.17 (0.95–1.44) Air fresheners Rarely 1.00 1.00 1.00 1.00 < Once a week 0.85 (0.49–1.50) 0.82 (0.47–1.46) 1.25 (0.87–1.79) 1.20 (0.84–1.72) ≥ Once a week 1.10 (0.89–1.35) 0.96 (0.78–1.20) 1.17 (0.98–1.41) 1.03 (0.85–1.24) Multivariate adjusted model: adjusted with age, BMI, education, marital status, household income, alcohol intake, exercise, and smoking According to analysis of the relationship between the showed higher ORs than women. Men tend to use less frequency of use of personal care products and urinary personal care products compared to women, which may TCS concentration, we found that the frequency of use be the cause of the larger differences between used and of hair care products, body cleansers, and cosmetics unused groups. These results suggest that personal care were consistently related to urinary TCS concentration products are a major source of TCS exposure. in both men and women. In the upper 75th percentile of As a result of analyzing a list of the raw materials of urinary TCS concentration, the proportion of more cosmetics reported to the Korea Food & Drug Adminis- frequent products use was higher than among partici- tration (KFDA) by domestic manufacturers in 2015, 127 pants with rarely products use and ORs were higher in of the 100,190 (0.13%) cosmetics products manufactured participants who used these products more often. Simi- in Korea were found to have used TCS [24]. It has been lar results were found in a study of breastfeeding found that TCS is mainly used in products that are mothers in Sweden. Mothers who used personal care rinsed off after use, such as body cleansers and foam products containing TCS showed significantly higher cleansers [24]. According to US data in 2010, 28 of 3359 breast milk and plasma TCS concentrations than those eye make-up products, 10 of 4345 facial make-up prod- who did not use these products [8]. In addition, men ucts, 226 of 3070 body cleansing products, 3 of 5242 Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 7 of 8 hair care products, and 42 of 2842 fragrance products toxic substances as they have rapid rates of body contained TCS [25]. TCS is mainly found in body organ development and their processes of detoxifica- cleansing products and it is thought that exposure via tion of toxic substances are less developed [27]. these products is high. A smaller number of cosmetics Therefore, additional research is needed to determine and hair care products contain TCS, but these can result whether current levels of regulation are appropriate in direct exposure and TCS-containing cleansing prod- for these susceptible population. ucts are often used to remove cosmetics. Therefore, The limitations of this study are as follows. First, we urine TCS concentrations may be high depending on the did not identify the usage amount of personal care prod- use frequency of cosmetics and hair care products. ucts, only the frequency of use. Second, we did not According to the results of previous studies both on consider the simultaneous use of other personal care TCS toxicity in humans and use of personal care prod- products, use of other personal care products not in- ucts as the main exposure source of TCS, regulations on cluded in the survey, and other TCS exposure factors the use of TCS for personal care products have been apart from personal care products. Third, in about 60% established in many countries. In Korea, KFDA launched of participants, urinary TCS concentration was mea- a new regulation with TCS concentration in personal sured below the detection limit. However, it did not care products, such as, body cleansing products that are affect the statistical analysis of this study. Fourth, the rinsed off after use, deodorants (excluding spray prod- health effects of increased urinary TCS concentration ucts), face powder, and foundation like concealer, that were not analyzed. Despite these limitations, this study the concentration limit of TCS in personal care products suggested the exposure level of TCS and the relationship was 0.3%; moreover, TCS could not be used in tooth- with use of personal care products, which are major paste and mouthwash in 2015 [24]. In Europe, the exposure sources of TCS using a representative data in concentration limit of TCS in mouthwash was 0.2% and Korean population. that in other personal hygiene products was 0.3%. In the Regulation of TCS was initiated in Korea in 2015 and case of Japan, the concentration limit of TCS in all prod- it is expected that the effect of reduction of TCS expos- ucts 0.1% [24]. Although TCS regulation has started in ure by the regulation will be confirmed through the ana- many countries, some cosmetics and human body lysis of third KoNEHS data, which was conducted in cleansing products still contain TCS and these products 2015–2017 and not publically released yet. Furthermore, still can be purchased in countries with no regulations children over three years old were included in the study in place. Regulatory concentrations are set at levels that population in the third KoNEHS, therefore, the TCS are harmless to the human body [24]; however, women exposure level and health effects could be studied in the of childbearing age, children, and adolescents should susceptible population. Based on future studies, it could select products that do not contain TCS or should rinse confirm the effect of the regulation and suggest another them off thoroughly after use. It is especially important more powerful policy to minimize TCS exposure in to be careful when purchasing mouthwash in some Korean population. foreign countries because nearly 100% of TCS can be absorbed in the oral cavity [3]. Conclusion In the present study, similar to those of other coun- This study found out the association of the use of tries, we found a tendency for urinary TCS concentra- personal care products and the concentration of urin- tion to increase in younger age, higher income level and ary TCS in general population in Korea. According to education level. The present study findings also con- this study, the levels of urinary TCS were higher in firmed that personal care products represent the main female, younger people, and higher-income people. cause of TCS exposure. People with higher levels of Because TCS is a well-known endocrine disruptor and income and education tend to have greater interest in several health problems related with exposure to TCS personal hygiene and tend to purchase personal care have suggested, further studies are needed to monitor products, which may lead to increased exposure to the trend of urinary TCS level and explore other chemicals such as TCS. Likewise, young people in health effects with exposure to TCS in general popu- their 20s and 30s are more concerned about personal lation in Korea using a representative data for general care than children, adolescents, and elderly adults; population. therefore, this young population is more exposed to TCS through greater use of personal care products. Additional file TCS in women of childbearing age can be a potential neurotoxic agent for the fetus during pregnancy [26] Additional file 1: Medians (interquartile range) of Urinary TCS concentration according to age. The urinary TCS concentration tended to decrease as age and can be delivered to infants through breast milk. increased. (XLSX 11 kb) Infants and young children are highly susceptible to Park et al. Annals of Occupational and Environmental Medicine (2019) 31:2 Page 8 of 8 Abbreviations 12. Helbing CC, van Aggelen G, Veldhoen N. Triclosan affects thyroid hormone- BMI: Body mass index; CI: Confidence interval; KoNEHS: Korean National dependent metamorphosis in anurans. Toxicol Sci. 2011;119(2):417–8 Environmental Health Survey; OR: Odds ratio; TCS: Triclosan author reply 9-22. 13. Durbize E, Vigan M, Puzenat E, Girardin P, Adessi B, Desprez PH, et al. Spectrum of cross-photosensitization in 18 consecutive patients with Acknowledgements contact photoallergy to ketoprofen: associated photoallergies to non- There is no conflict of interest or financial support to declare. benzophenone-containing molecules. Contact Dermatitis. 2003;48(3):144–9. 14. Storer E, Koh KJ, Warren L. Severe contact dermatitis as a result of an Funding antiseptic bath oil. Australas J Dermatol. 2004;45(1):73–5. Not applicable. 15. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Survey overview. Guidelines for using raw materials for Korean National Environmental Health Survey - the second Availability of data and materials stage ('12-'14). Incheon: Korean national institute of environmental research; The data of the KoNEHS is opened to the public, therefore, any researcher 2017. p. 1–5. can be obtained after request from the website http://meta.narastat.kr/ 16. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Sample design. Guidelines for using metasvc/svc/SvcMetaDcDtaPopup.do?confmNo=106027&inputYear=2012. raw materials for Korean National Environmental Health Survey - the second stage (‘12∼‘14). Incheon: Korean national institute of environmental research; Authors’ contributions 2017. p. 6–15. MP designed this study and wrote a draft of this manuscript. SK, YK, and DJN 17. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Survey Items. Guidelines for using raw analyzed the data. JR provided technical support. SL performed critical revision materials for Korean National Environmental Health Survey - the second of the manuscript. All authors read and approved the final manuscript. stage (‘12∼‘14). Incheon: Korean national institute of environmental research; 2017. p. 28–9. 18. Yoo J, Choi W, Jeon H, Joo Y, Lee C. Analysis manual of environmental Ethics approval and consent to participate noxious materials. Guidelines for using raw materials for Korean National Not applicable. Environmental Health Survey - the second stage ('12-'14). Incheon: Korean national institute of environmental research; 2017. p. 54–67. Consent for publication 19. Arbuckle TE, Marro L, Davis K, Fisher M, Ayotte P, Belanger P, et al. Exposure Not applicable. to free and conjugated forms of bisphenol a and triclosan among pregnant women in the MIREC cohort. Environ Health Perspect. 2015;123(4):277–84. Competing interests 20. Kim K, Park H, Yang W, Lee JH. Urinary concentrations of bisphenol a and The authors declare that they have no competing interests. triclosan and associations with demographic factors in the Korean population. Environ Res. 2011;111(8):1280–5. 21. Boas M, Feldt-Rasmussen U, Main KM. Thyroid effects of endocrine Publisher’sNote disrupting chemicals. Mol Cell Endocrinol. 2012;355(2):240–8. Springer Nature remains neutral with regard to jurisdictional claims in 22. Krassas GE, Poppe K, Glinoer D. Thyroid function and human reproductive published maps and institutional affiliations. health. Endocr Rev. 2010;31(5):702–55. 23. Zoeller TR, Dowling AL, Herzig CT, Iannacone EA, Gauger KJ, Bansal R. Received: 31 August 2018 Accepted: 22 January 2019 Thyroid hormone, brain development, and the environment. Environ Health Perspect. 2002;110(Suppl 3):355–61. 24. Cosmetics Research Team. Risk assessment of cosmetics. Cheongju-si: The References National Institute of Food and Drug Safety Evaluation, Ministry of Food and 1. Dann AB, Hontela A. Triclosan: environmental exposure, toxicity and Drug Safety; 2017. p. 151–72. mechanisms of action. J Appl Toxicol. 2011;31(4):285–311. 25. Cosmetic Ingredient Review Expert P. Final safety assessment of triclosan. 2. 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Published: Jan 28, 2019

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