Household Cleaning Activities as Noningestion Exposure

Article pubs.acs.org/est

Household Cleaning Activities as Noningestion Exposure Determinants of Urinary Trihalomethanes P. Charisiadis,†,¶ S. S. Andra,†,‡,¶ K. C. Makris,*,† M. Christodoulou,† C. A. Christophi,† S. Kargaki,§ and E. G. Stephanou§ †

Cyprus International Institute for Environmental and Public Health in association with Harvard School of Public Health, Cyprus University of Technology, Irenes 95, Limassol, 3041, Cyprus ‡ Harvard-Cyprus Program, Department of Environmental Health, Harvard School of Public Health, Boston, Massachusetts 02115, United States § Environmental Chemical Processes Laboratory, Department of Chemistry, University of Crete, Heraklion, Crete 71003, Greece S Supporting Information *

ABSTRACT: Previous epidemiological studies linking drinking water total trihalomethanes (THM) with pregnancy disorders or bladder cancer have not accounted for specific household cleaning activities that could enhance THM exposures. We examined the relation between household cleaning activities (washing dishes/clothes, mopping, toilet cleaning, and washing windows/surfaces) and urinary THM concentrations accounting for water sources, uses, and demographics. A cross-sectional study (n = 326) was conducted during the summer in Nicosia, Cyprus, linking household addresses to the geocoded public water pipe network, individual household tap water, and urinary THM measurements. Household tap water THM concentrations ranged between 3−129 μg L−1, while the median (Q1, Q3) creatinine-adjusted urinary THM concentration in females (669 ng g−1 (353, 1377)) was significantly (p < 0.001) higher than that in males (399 ng g−1, (256, 681)). Exposure assessment, based on THM exposure equivalency units, showed that hand dishwashing, mopping, and toilet cleaning significantly (p < 0.001) increased urinary THM levels. The effect of dishwashing by females ≥36 y of age remained significant, even after adjusting for potential confounders. No significant (p > 0.05) association was observed between ingestion-based THM exposure equivalency units and urinary THM. Noningestion routes of THM exposures during performance of routine household cleaning activities were shown for the first time to exert a major influence on urinary THM levels. It is warranted that future pregnancy−birth cohorts include monitoring of noningestion household THM exposures in their study design.

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INTRODUCTION

External exposures to THM are estimated from reported tap water levels,13 reconstructed water consumption patterns,7 indoor air quality,14 and water use patterns (showering, bathing, indoor swimming),15 while assessment of internal THM exposures relies upon measurements of blood16 or urine17 biomarkers of exposure. Spatial variability of DBP in urban drinking water distribution systems is wide, hindering our progress in accurately assigning DBP doses to disease processes.12,18 Data on water THM concentrations is predominantly taken from regulatory compliance monitoring schemes19 and not directly from participants’ residences. Commonly used bleach and chlorine-containing household cleaning products have been part of our lives for decades, but

The general population is routinely exposed to disinfectants and disinfection byproducts (DBP) on any typical day from various sources and activities at home and at work.1 For example, natural organic matter in water may react with added chlorine (a disinfectant) resulting in the formation of more than 600 DBP.2 Trihalomethanes (THM) is a frequently occurring class of DBP in tap water. Notable health effects of THM are adverse pregnancy outcomes,3 congenital anomalies,4 birth defects,5 respiratory symptoms,6 and bladder cancer,7 but findings are often inconsistent. Several pregnancy−birth cohorts examined the association between water THM exposures and adverse health effects observed in mother− child pairs, including, low birth weight and small size for gestational age,8,9 preterm delivery and low birth weight,10 and fetal growth restriction and preterm birth,11 just to name a few.12 © 2013 American Chemical Society

Received: Revised: Accepted: Published: 770

September 22, 2013 November 19, 2013 November 22, 2013 November 22, 2013 dx.doi.org/10.1021/es404220z | Environ. Sci. Technol. 2014, 48, 770−780

Environmental Science & Technology

Article

(ii) very low urinary creatinine values with a mean (SD) of 0.33 (0.44) g L−1 (6 participants); (iii) incomplete questionnaire (one participant); and (iv) forty one children (0.00−0.75 >0.75 0.00 >0.00−1.75 >1.75 3.14 5825 10.5

200 126 167 159 79 167 80 137 134 54 44 253 7 19 103 133 81 72 204 44 34 54 195 90 156 79 119 128 79 102 143 80 81 167 78 81 164 81 81 165 80

61 39 51 49 24 51 25 42 41 17 14 78 2 6 32 42 26 23 64 14 12 19 69 28 48 24 37 39 24 31 44 25 25 51 24 25 50 25 25 51 25

a

Three classes of quartiles used in this study were 75th percentile). bTwo areas with contrasting drinking water distribution network characteristics were selected (Table S1, Supporting Information). cPer capita water consumption in Cyprus (Mediterranean region) includes water use not only for plain consumption (PW) but also predominantly in the form of cold (CB) and hot beverages (HB).48,49 dPC and PET stands for polycarbonate and polyethylene terephthalate.

Spearman’s correlation coefficient, was used for the remaining cases. Multivariable linear regression was utilized to identify the significant predictors of urinary TTHM and assess their impact on urinary TTHM after adjusting for other covariates.

(Supporting Information, text). Urinary creatinine was determined by the picric acid-based spectrophotometric method (Jaffe method).30 Statistical Analyses. The sum of bromine-containing THM, viz., BDCM, DBCM, and TBM, is hereby considered as brominated THM, while the sum of all four THM was denoted as total THM (TTHM). Samples with analyte level < LOD were assigned half of their respective values. The distributions of creatinine-adjusted and unadjusted urinary total THM concentrations were right-skewed and, thus, were log-transformed. Associations between normally distributed continuous variables were assessed using the Pearson’s correlation coefficient, and the nonparametric alternative, the

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RESULTS Selected Population Characteristics. Participants were primarily Greek-Cypriots and ranged in age from 18 to 87 y with a mean ± SD of 50 ± 17 y and BMI of 16 to 51 kg m−2 (17% obese) (Table 1). The majority of them were females (60%), married (78%) with either primary and/or secondary education level. About 64% of them were nonsmokers, while only 23% reported that were currently smoking (Table 1). 772

dx.doi.org/10.1021/es404220z | Environ. Sci. Technol. 2014, 48, 770−780


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Table 2. Distribution of THM Concentration Classes in Tap Water (n = 193) and Participants’ Urine Samples (n = 326) percentile medium −1 b

1

water (μg L )

2

creatinine-unadjusted urinary concentration (ng L−1)c

3 4

urinary creatinine (g L−1) creatinine-adjusted urinary concentration (ng g−1)

trihalomethane

mean (standard deviation)a

min.

10th

25th

median

75th

90th

max.

16 (7) 21 (8) 22 (9) 7 (3) 50 (19) 67 (25) 332 (3) 73 (2) 54 (1) 23 (1) 161 (2) 560 (2) 1.2 (0.8) 336 (3) 73 (3) 54 (2) 23 (2) 162 (2) 565 (2)

1 1 1 1 2 3 47d 23d 47e 20d 90 137 0.1 12 6 12 5 24 45

8 11 8 2 21 29 47d 23d 47e 20d 90 182 0.3 55 26 21 9 58 186

12 17 18 5 42 55 311 68e 47e 20d 135 480 0.6 178 37 29 13 87 309

16 22 24 7 53 69 456 68e 47e 20d 135 625 1.1 380 67 47 22 152 552

21 25 27 9 60 80 601 68e 47e 20d 188 797 1.8 731 123 86 36 261 989

25 30 31 11 71 95 783 165 117 60e 283 1001 2.3 1488 251 166 69 486 1893

38 39 46 17 98 129 3008 1934 195 60e 2156 5163 3.9 5351 2648 802 395 2951 7278

chloroform bromodichloromethane dibromochloromethane bromoform brominated THM total THM chloroform bromodichloromethane dibromochloromethane bromoform brominated THM total THM chloroform bromodichloromethane dibromochloromethane bromoform brominated THM total THM

a

Arithmetic mean and standard deviation in parentheses were presented for normally distributed data such as concentrations of trihalomethanes in water and urinary creatinine. Geometric mean (geometric standard deviation) was presented for skewed data such as creatinine-unadjusted and adjusted urinary trihalomethanes. bThe limit of detection, LOD (and limit of quantification, LOQ), for the water samples analyses were 0.13 (0.39) μg L−1, 0.11 (0.32) μg L−1, 0.13 (0.38) μg L−1, and 0.11 (0.34) μg L−1 for the TCM, BDCM, DBCM, and TBM, respectively. Since the concentrations of all the analytes in water samples were above LOD and LOQ, no corrections were made and data was presented as is. cThe LODs (and LOQ) for the urine samples analysis were 94 (282) ng L−1, 46 (136) ng L−1, 31 (94) ng L−1, and 40 (120) ng L−1 for the TCM, BDCM, DBCM, and TBM, respectively. Since the concentrations of the analytes in certain urine samples were below LOD and LOQ, an adjustment was made for statistical purposes and are shown beside. dUrinary concentrations below the LOD for an analyte were assigned a respective half-LOD value. This corresponds to 47 ng L−1, 23 ng L−1, 16 ng L−1, and 20 ng L−1 for the TCM, BDCM, DBCM, and TBM, respectively. eUrinary concentrations below LOQ and above LOD were assigned a half-LOQ value. This corresponds to 141 ng L−1, 68 ng L−1, 47 ng L−1, and 60 ng L−1 for the TCM, BDCM, DBCM, and TBM, respectively.

occurrence for the brominated THM in urine (bromodichloromethane, dibromochloromethane, and tribromomethane) were lower (Table 2). Median concentrations of urinary creatinineadjusted chloroform and brominated THM were 380 ng g−1 (Q1, Q3: 178, 731) and 152 ng g−1 (Q1, Q3: 87, 261), respectively (Table 2). Median creatinine-adjusted urinary TTHM concentration in females and males was 669 ng g−1 (Q1, Q3: 353, 1377) and 399 ng g−1 (Q1, Q3: 256, 681), respectively. Urinary chloroform measured in other studies was of comparable magnitude, varying from as low as 1−1005 ng L−1 to as high as 250−9800 ng L−1.31,32 A significant correlation was observed between chloroform and brominated THM in urine samples (Spearman r = 0.52, p < 0.0001) (Table S3, Supporting Information). Participants’ Characteristics and Daily Activities Related to Trihalomethanes Exposures. Using the EEU concept, women as compared to men and participants ≥36 y compared to their younger counterparts were shown to engage at a substantially (p < 0.001) higher frequency of domestic cleaning activities (hand dishwashing, mopping, and toilet cleaning) (Table S4, Supporting Information). Water-contact noningestion activities like shower, bathtub, and swimming in pools were only influenced by age, where elderly (>63 y) spent less EEU than those ≤63 y. Noningestion-based activities EEU summing both cleaning activities and water-contact activities (all noningestion-based), and total EEU (all ingestion-based and noningestion-based) were all higher in females (Table S4, Supporting Information). Logarithmically transformed urinary

About 90% of tap water originated from surface water in dams, while the rest was desalinated. Tap water was consumed either plain or used to prepare cold and/or hot beverages at and away from home by 72% of participants, while 28% reported no tap water consumption (Table 1). Trihalomethanes were quantified in all tap water samples (one sample per household) (n = 193) (Table 2). A median value of 69 μg L−1 total THM in tap water samples was observed, ranging between 3 and 129 μg L−1 (Table 2). Bottled water (either PC- or PET-based) consumption at and away from home was reported by 63% of the participants, while 37% of them did not consume bottled water. In a collection of samples from 20 different bottled water brands, bottled water THM levels were consistently LOD (LOD: 94 ng L−1) (Table 2). The frequencies of 773



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Table 3. Association between Exposure Equivalency Units and Urinary Trihalomethanes Levels among the Study Participants (ln) urinary TCM (ng g−1) category A Ingestion Exposuresd 1 tap water (at home, PW+CB+HB)e

2

total ingestion (tap water, at and away from home, PW+CB+HB)e

B Noningestion Exposures 1 hand dishwashing

2

mopping

3

toilet cleaning

4

other cleaning

5

all cleaning activities

6

shower

7

swim in pool

8

all water-contact activities

9

total noningestion (all noningestion sources)

C Total Exposure 10 cumulative ingestion (tap water at and away from home) and noningestion sources

exposure equivalency unita and quartileb

n

0.00 >0.00−0.57 >0.57 0.00 >0.00−0.63 >0.63

(ln) urinary brominated-THM (ng g−1)

(ln) urinary TTHM (ng g−1)

mean (SD)

diffc

mean (SD)

diffc

mean (SD)

diffc

110 135 81 91 155 80

5.79 5.88 5.75 5.78 5.87 5.75

(1.06) (1.24) (1.31) (1.08) (1.21) (1.31)

ns

5.01 5.21 5.00 4.96 5.21 5.01

(0.76) (0.86) (0.86) (0.74) (0.86) (0.86)

ns

6.29 6.44 6.23 6.26 6.43 6.24

(0.80) (0.92) (1.04) (0.83) (0.89) (1.04)

ns

0.00 >0.00−1.00 >1.00 0.00 >0.00−1.00 >1.00 0.00 >0.00−0.67 >0.67 0.00 >0.00 0.00 >0.00−2.85 >2.85 ≤2.00 >2.00−3.63 >3.63 0.00 >0.00 ≤2.00 >2.00−4.29 >4.29 ≤2.76 >2.76−7.43 >7.43

138 120 68 139 113 74 159 135 32 274 52 118 127 81 140 105 81 284 42 121 129 76 81 165 80

5.53 5.94 6.17 5.52 6.09 5.95 5.58 6.01 6.15 5.71 6.37 5.56 5.85 6.15 5.76 5.82 5.91 5.82 5.78 5.77 5.84 5.84 5.63 5.74 6.16

(1.12) (1.20) (1.23) (1.08) (1.22) (1.28) (1.12) (1.29) (0.97) (1.20) (1.02) (1.11) (1.25) (1.16) (1.14) (1.32) (1.15) (1.23) (1.00) (1.15) (1.32) (1.05) (1.16) (1.24) (1.10)

B A A B A A B A A B A B AB A ns

(0.82) (0.81) (0.76) (0.82) (0.80) (0.79) (0.82) (0.82) (0.71) (0.83) (0.84) (0.84) (0.83) (0.73) (0.79) (0.93) (0.75) (0.84) (0.78) (0.78) (0.73) (0.73) (0.87) (0.84) (0.78)

6.06 6.48 6.64 6.06 6.59 6.46 6.12 6.53 6.58 6.26 6.73 6.07 6.43 6.58 6.26 6.40 6.38 6.35 6.22 6.28 6.41 6.31 6.19 6.30 6.55

(0.84) (0.88) (0.97) (0.81) (0.92) (0.97) (0.83) (0.99) (0.76) (0.90) (0.88) (0.86) (0.91) (0.91) (0.86) (1.00) (0.89) (0.93) (0.78) (0.87) (1.02) (0.79) (0.87) (0.93) (0.89)

B A A B A A B A A B A B A A ns

B B A

4.83 5.23 5.38 4.83 5.33 5.20 4.87 5.31 5.22 5.04 5.34 4.82 5.23 5.26 4.98 5.22 5.11 5.12 4.89 5.01 5.21 5.02 4.95 5.11 5.19

≤3.10 >3.10−7.92 >7.92

82 163 81

5.60 (1.18) 5.78 (1.23) 6.11 (1.12)

B AB A

4.91 (0.88) 5.15 (0.85) 5.15 (0.74)

ns

ns ns

ns

B A A B A A B A AB B A B A A ns

ns ns

ns

ns

6.17 (0.88) 6.34 (0.93) 6.51 (0.89)

ns

ns ns

B AB A B AB A

An exposure equivalency unit is equal to 1 L day−1 tap water consumption; 15-min day−1 dish washing, mopping, toilet, or other cleaning activities; 5-min day−1 shower or bathtub time; and 5-min day−1 swim in pool time. bThree classes of quartiles used in this study were 75th percentile). cStatistical difference between the means of the quartiles was calculated by using Tukey’s HSD and Student’s t test (in case of two groups).Treatment means denoted with different alphabetical letters differ significantly (p < 0.05). “ns” denotes a nonsignificant difference in treatment means for a given category. d50% and 70% reduction in exposure was applied in case of filter use and hot beverage consumption, respectively. ePer capita water consumption in Cyprus (Mediterranean region) includes water use not only for plain consumption (PW) but also predominantly in the form of cold (CB) and hot beverages (HB).48,49 a

Similarly, those who consumed tap water and/or bottled water and/or mobile station water both at and away from home for all purposes (plain, cold and hot beverages) constituted slightly over 70% of the population and had a significantly higher ingestion EEU compared to those who did not consume tap water. Those households with >83 μg L−1 (75th percentile) water total THM concentrations had significantly (p < 0.001) lower water-contact, noningestion and total EEU than those residing in households with water THM 63 y), nonsmokers, those with primary education, and those residing in households being above the 75th percentile of distance from both chlorination tank and nearest water pipe (Table S4, Supporting Information). The majority of participants (67%) do not flush at all the tap water prior to its use, preventing flushing to initiate THM losses from running water; the same faucet showed a decrease of water THM concentrations up to 30% within 1 min of flushing (data not shown). About 95% of the study participants used tap water for cooking and thereby had a significantly higher ingestion EEU when compared with the rest (p < 0.01). 774



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Table 4. Multiple Linear Regression Coefficients for the Study Variables with a Unit Change in Log-Transformed and Creatinine (i) Unadjusted and (ii) Adjusted Urinary Total Trihalomethanes #

covariate

(ln) creatinine unadjusted urinary TTHM (ng L−1)

(ln) creatinine adjusted urinary TTHM (ng g−1)

β (SE)

1 2 3 4 5 6 7 8 a

age (y) gender (female) BMI (kg m−2) residence proximity to the water chlorination tank (km) residence proximity to the nearest water distribution pipe (m) tap water TTHM (μg L−1) hand dishwashing, exposure equivalency unit mopping, exposure equivalency unit

R2 = 0.13 p < 0.0001 −0.001 (0.002) −0.03 (0.04) −0.01 (0.01)a 0.11 (0.03)c 0.002 (0.002)

R2 = 0.25 p < 0.0001 0.02 (0.002)c 0.24 (0.06)c −0.02 (0.01) 0.12 (0.04)b 0.005 (0.002)a

−0.01 (0.001)c 0.05 (0.04) 0.01 (0.05)

−0.01 (0.002)b 0.14 (0.07)a −0.11 (0.08)

p < 0.05. bp < 0.01. cp < 0.001.

having > 83 μg L−1 tap water THM levels were significantly (p < 0.001) decreased (Table S4, Supporting Information). Household Cleaning Activities and Urinary Total Trihalomethanes. All four cleaning activities monitored in this study, viz., hand dishwashing, mopping, toilet cleaning, and other (window glass, furniture, garden), were associated with urinary TTHM (Table 3). Urinary THM levels of those study participants who reported any form of household cleaning activity were significantly (p < 0.001) higher than those who did not perform any cleaning activity (Interquartile vs Quartile 1) (Table 3 and Figure S4, Supporting Information). None of the exposures from individual or cumulative water-contact activities (showering, indoor swimming, and bathtub) was significantly associated with urinary TTHM (Table 3). A significant (p < 0.001) difference in urinary TTHM levels was observed only between the third and first quartile of total EEU (sum of both ingestion-, and noningestion-based exposures), highlighting the need for detailed questionnaire structure (Table 3). The fact that the magnitude of noningestion-based EEU was close to total EEU coupled with the linearly increasing trend of EEU quartiles illustrated the importance of noningestion-based exposures in dictating urinary TTHM levels. Because of their lipophilic nature and higher occurrence in tap water from the study area (Table 2), brominated THM were significantly higher in urine samples of participants reporting higher frequency of cleaning activities (such as dishwashing), where dermal uptake and inhalation are the predominant routes of exposure (Table 3). In a linear multivariate regression model, age, gender, BMI, residence proximity to chlorination tank and pipe, tap water THM, hand dishwashing EEU, and mopping EEU were included as predictors of urinary TTHM (Table 4). Creatinine-adjusted urinary total THM was 1.27 times higher in females compared to males, and 1.15 times higher per unit increase in hand dishwashing EEU in the study participants (Table 4). Residence proximity to the chlorination tank and to the nearest water main pipe and the water THM concentration in each household were significant predictors of urinary TTHM even after adjusting for several covariates (Table 4). This finding corroborates engineering trends linking higher water residence time into pipes with enhanced THM formation potential.26,33,34 The significant (p = 0.01) negative influence of water THM concentrations on urinary TTHM levels was driven by water THM concentrations being >75th percentile

(>83 μg L−1). No associations were observed between per capita water consumption rates and urinary TTHM for those participants using: (i) only tap (n = 21, 6%) (rS = −0.14, p = 0.54), (ii) water sources other than tap (bottled water and mobile station water) (n = 90, 28%) (rS = −0.11, p = 0.29), and (iii) both tap and other water sources (n = 214, 66%) (rS = 0.13, p = 0.06) (Figure S5, Supporting Information). After adjusting for potential confounders, we reported an R2 of 0.20, 0.23, and 0.25 for the models of creatinine-adjusted log-urinary TCM, brominated-THM, and TTHM, respectively. In a multivariate regression model for blood TCM, (i) the reported partial R2 for log-TCM in air was 0.38 (p < 0.001), while the R2 of other variables, such as for the use of chlorine-based cleaning products, was less by an order of magnitude,16 and (ii) neither ingestion nor noningestion exposure metrics significantly predicted blood THM levels.13 As part of a sensitivity analysis, the model in Table 4 was rerun after excluding 1% of the sample in both ends of the distribution of studentized residuals to consider outlier influence (Table S5, Supporting Information). We also reran the same model by including only 50% of the sample after generating a uniform random number (Table S6, Supporting Information). Results suggested that the regression coefficients of study variables retained the direction, significance, and model R2. Evaluation of contribution of the two noningestion exposure routes in this study, viz., all house cleaning and all water-contact activities, was performed by classifying the study participants into four groups based on a dichotomous EEU classifier (low vs high based on < or ≥ median EEU). Differences in mean urinary TTHM levels between the groups were compared using a Student’s t test (Figure S4, Supporting Information). In addition, contribution of ingestion and noningestion exposure toward urinary TTHM in females was assessed to understand gender differences (Figure S6, Supporting Information). To further explore the relationships of frequency of activity (number of times per week) and duration of activity (minutes per time) of both hand dishwashing and other household cleaning activities, we regressed the reference group and three quartiles of each variable on log-transformed and creatinineadjusted urinary THM components (Figure 1). Linear associations were observed between quartiles and urinary total THM for both characteristics, but the trend was much clearer when frequency of the hand dishwashing or total cleaning activity was used (Figure 1). A clear monotonic 775



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Figure 1. Changes in β coefficient log-creatinine adjusted urinary THM stratified by cleaning activity characteristics. Comparison with reference group for (a) chloroform, (b) brominated THM, and (c) total THM. R = reference group (Q3). Number of activities per day and duration per activity per day were modeled as a continuous variable for calculating “p for trend”.

(minutes) of household cleaning activities (Figure S7, Supporting Information).

relationship was observed for frequency rather than duration of the activity (either hand dishwashing or total domestic cleaning). We further stratified the study participants into four combination groups based on a dichotomous classification (low or high frequency and duration) (Figure S7, Supporting Information). We noticed that an increased significance of a change in urinary THM between the stratified study groups compared to the reference group was primarily influenced by an increase in frequency (number of times) rather than duration

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DISCUSSION This cross-sectional study is the first of its kind focusing on determinants of THM exposures using urinary THM as the biomarker of exposure. The majority of participants (>95%) reported the use of more than a single source of potable water, complicating estimates of ingestion-based THM exposures. Tap water was the only source with detectable THM concen776



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trichloroacetic acid in 611 pregnant women. Moreover, our study sample size is larger or comparable to the size of other population-based studies that measured blood THM levels (n = 401 men reported by Zeng et al.,42 153 women by RiveraNúñez et al.,13 100 volunteers by Silva et al.,43 99 participants by Backer et al.,16 50 mothers by Lynberg et al.,44 and 46 women by Zhang et al).45 A limitation of our study was the collection of a single first morning void urine sample something that we are currently addressing by taking additional measurements. Another study limitation was the potential for measurement errors in THM content of drinking water sources and daily intake estimates of water THM and the potential for bias in participant recall of cumulative frequency of exposure to household cleaning activities. Also, the use of EEU conversion factors was based on chamber-based THM studies that may not exactly match environmental conditions encountered in this study’s households.

trations, while bottled water and mobile station water did not contain THM. However, the most popular source of potable water was the THM free mobile station water source, suggesting that at higher water consumption rates THM mass intake may get diluted and concomitantly reflected into decreasing urinary THM levels. Thus, no significant (p > 0.05) association was observed between ingestion-based EEU and urinary THM levels, while a negative association was observed between water and urine THM levels. No association was observed between water-contact activities like showering, bathing, and indoor swimming with urinary THM levels, even though the literature suggests otherwise.14 This study was characterized by a very high percentage (90%) of participants reporting some sort of ventilation during showering, which could increase air exchange rates and decrease exposures to volatile THM. About 70% of the participants took a shower with cold or mild temperature water (85%) did not use a swimming pool or bath tub. Specific household cleaning activities like dishwashing, mopping, and laundry were associated with higher urinary TTHM levels, especially for females. Detailed cleaning activities have never been assessed before in THM epidemiological studies, particularly in pregnancy−birth cohorts where maternal exposures to environmental chemicals are of importance. Noningestion-based THM exposures have been occasionally studied, such as, inhalation and dermal absorption of THM during showering or bathing16 and swimming in chlorinated pools.37 Nuckols et al.14 reported an average of 2-fold increase in total THM levels in exhaled breath and corresponding increase in blood levels of study participants who performed hand dishwashing. One of our laboratory studies suggested that mixing commercial chlorine with tap water increased water chloroform concentrations by an order of magnitude of that found in tap water (unpublished results). Indoor air chloroform concentrations increased by 10−50 times higher during and half an hour after cleaning the bathroom, kitchen, and floors.22 Constituents of cosmetics and personal care products that come in contact with free chlorine could also react to form DBP.38 Reports on triclosan, a widely used antimicrobial agent, illustrate the generation of chloroform and chlorinated volatile organics upon reaction with residual chlorine in water or soap,39 enhancing chloroform formation by up to 40%.40 Chlorine may persist in bleached fabrics (clothes) for several months,41 which could act as a reservoir for chloroform generation when in contact with household products. This study combined both external (chlorinated tap water) and internal exposure measurements (urinary THM) that better characterized the magnitude and variability of human exposures to THM. Sampling tap water from the residence’s main faucet enabled us to match individual exposures to point of use sources of THM within the household: chlorinated water used for drinking, preparing soap solutions, preparing mopping floor cleaning solutions, etc. Each residence was imprinted on a GIS map showing distances from the main chlorination tank. Detailed water consumption survey questions allowed for recording all three major water sources used by participants along with individual consumption rates. This study is the second largest population studied to date (n = 326) on biomonitoring of THM exposures using urine as the biomarker of exposure, second to Costet et al.11 who monitored urinary

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IMPLICATIONS

Our findings suggest that habitual individual characteristics, such as household cleaning activities, dominate THM exposures, indicating that ingestion of tap water may not be the primary route of THM exposures. In addition, our results highlighted the higher exposure susceptibility of females who perform domestic cleaning activities several times in short bursts, even within the same day. The significant association between specific household cleaning activities and internal exposure THM concentrations could be implicated with adverse health risk scenarios of indoor environmental quality. The importance of this may be exacerbated in cases where energy efficiency measures could adversely impact household ventilation rates. Within-household air quality with respect to indoor contaminants is of utmost importance since, on average, urban dwellers spend >80% of their time indoors (home or work).46 In addition to toxic chemicals being present in indoor construction materials, equipment, and installations, indoor human activities of cleaning and hygiene, such as those discussed in this study, supplemented with the extensive and repetitive use of household cleaning and personal care products, including smoking and air fresheners, actively contribute to a resident’s body burden of chemicals. Thus, it is of utmost importance to promote and sustain a healthy indoor environment during home energy retrofits.47 Millions of Europeans will have to comply with the tighter energy requirements and the near-future EU-wide implementation of energy performance certificates (EU 31/2010 and EU/244/ 2012). Cost-effective options of improved indoor energy use should not come at the expense of indoor environmental quality, undermining residents’ health. Instead, energy efficiency measures should go hand in hand with interventions that decrease residents’ indoor body burden of chemicals, like THM. We anticipate that future studies, maybe within existing pregnancy birth cohorts, will include detailed exposure assessment of THM in maternal households and specific cleaning activities with either chlorine or antimicrobial containing formulations or alternative cleaning commercial products. Such exposures have not yet been examined in relation with adverse pregnancy outcomes or cancer. 777



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ASSOCIATED CONTENT

S Supporting Information *

(1) Details about GIS analysis and (2) water and urine sampling and analytical methodology, (3) drinking water distribution system characteristics for the two water district areas, (4) frequency distribution of the trihalomethanes ingestion and noningestion exposure characteristics of the study participants, (5) correlations and (6) variability between study characteristics and urinary trihalomethanes, (7) sensitivity analyses, (8) study location map, (9) GIS maps showing individual household characteristics in relation to urban drinking water distribution network features, (10) dichotomous analysis of cleaning and water-contact activities EEU with respect to urinary TTHM, (11) per capita water consumption from various sources and urinary TTHM, (12) female-based analysis of ingestion versus noningestion effects on urinary TTHM concentrations, and (13) dichotomous analysis of frequency and duration of cleaning activities with respect to urinary TTHM. This information is available free of charge via the Internet at http://pubs.acs.org/

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AUTHOR INFORMATION

Corresponding Author

*Fax: +357-25002676; tel: +357-25002398; e-mail: [email protected]. Author Contributions ¶

P. Charisiadis and S.S. Andra contributed equally to this manuscript.

Notes

The observations and speculations in this Article represent those of the authors and do not necessarily reflect the views of the participating organizations, viz., Cyprus University of Technology, Limassol, Cyprus; University of Crete, Heraklion, Greece; and Water Board of Nicosia, Nicosia, Cyprus. The authors declare no competing financial interest.

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ACKNOWLEDGMENTS The authors would like to thank the Cyprus Research Promotion Foundation for funding this study (AEIFORIA/ ASTI/0311(BIE)/20) with Structural Funds of the European Commission awarded to the corresponding author, Dr. Makris. We also appreciate help from Dr. D. Skarlatos and Mr. V. Vamvakousis with GIS analyses (Department of Civil Engineering and Geomatics, Cyprus University of Technology). We sincerely thank the Water Board of Nicosia for sharing water network data with us.

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ABBREVIATIONS EEU exposure equivalency unit DBP disinfection byproducts THM trihalomethanes TCM chloroform BDCM bromodichloromethane DBCM dibromochloromethane TBM bromoform

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REFERENCES

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Household Cleaning Activities as Noningestion Exposure

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