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Correlation of arsenic exposure through drinking groundwater and urinary arsenic excretion among adults in Pakistan.

Introduction

Arsenic is a ubiquitous element occurring naturally in the environment in both organic and inorganic forms. Inorganic arsenic is more toxic to humans and more prevalent in groundwater either naturally through geochemical and weathering processes or by anthropogenic activities such as agriculture, industry, and mining (National Research Council, 2001).

Arsenic has been identified as a potent human carcinogen by the International Agency for Research on Cancer (2004). Millions of people are exposed to arsenic through drinking groundwater with arsenic concentrations above the World Health Organization (WHO) guideline value of 10 [micro]g/L in many parts of the world, including parts of the U.S., Canada, Argentina, Chile, Mexico, Hungary, and various countries of Southeast Asia, including Bangladesh, West Bengal India, Nepal, China, Myanmar, Thailand, Taiwan, Vietnam, Cambodia, Laos, and Pakistan (Caussy, 2005; Rahman et al., 2001).

Long-term human exposure to arsenic through drinking water containing arsenic above 10 [micro]g/L is associated with the following:

* characteristic skin lesions, melanosis (darkening of skin) and keratosis (thickening of the skin of palms and soles) (Kadono et al., 2002);

* increased blood pressure (Lee et al., 2005);

* decreased lung function (Pervez et al., 2008);

* cardiovascular disease (Chen, Chiou, Chiang, Lin, & Tai, 1996);

* diabetes (Rahman, Todel, Ahmed, & Axelson, 1998; Tseng et al., 2000);

* adverse reproductive outcomes (Ihrig, Shalat, & Baynes, 1998);

* stillbirth (Cherry, Shaikh, McDonald, & Chowdhury, 2008);

* cancers of lung and bladder (Michaud et al., 2004; Morales, Ryan, Kuo, Wu, & Chen, 2000; Mukherjee et al., 2003); and

* decreased intellectual functions and peripheral neuropathy (Wasserman et al., 2004).

Arsenic has a short half-life in the body; it is readily excreted in urine in 1-3 days (Calderon, Hudgens, Le, Schreinemachers, & Thomas, 1999; Chen, Amarasiriwardena, Hsueh, & Christiani, 2002; Karagas et al., 2001). Interindividual variability in arsenic excretion in urine at similar levels of arsenic exposure was also reported (Del Razo, Aguilar, Sierra-Santoyo, & Cebrian, 1999).

Accurate estimation of arsenic exposure is required for risk assessment of arsenic's adverse health effects and for making mitigation decisions. Most of the previous epidemiologic studies have measured arsenic in the available drinking water to estimate individual exposure (Rahman et al., 2006; Yu, Sun, & Zheng, 2006). In our study, human exposure to arsenic through drinking water was measured by determining the concentration of arsenic excreted in urine, testing it as a biomarker of current arsenic exposure. Many of the correlation studies of arsenic in water and urine have showed positive correlation. Those studies, however, were based on selective sampling in a few towns or communities with high arsenic exposure with a limited number of water and urine samples; for instance, 167 subjects were recruited for water (n = 164) and urine (n = 176) sample analysis (Ahsan et al., 2000); 96 subjects gave water and urine samples (Calderon et al., 1999); 43 subjects gave water (n = 35) and urine (n = 43) samples (Mera, Kopplin, Burgess, & Gandolfi, 2004); and 346 subjects gave urine and water (n = 86) samples (Wata nabe et al., 2001).

Ours is the first study from Pakistan based on arsenic exposure estimates through urinary arsenic excretion in a population that is chronically exposed to arsenic from drinking groundwater. Our study was part of a larger investigation in which the prevalence of arsenicosis (melanosis or keratosis) was evaluated in a population chronically exposed to arsenic through drinking water (Fatmi et al., 2009). The objective of the present study was to assess the relationship between arsenic concentration in the drinking water and total arsenic excretion in urine among the adult population of one of the arsenic-affected districts (Khairpur) of Pakistan.

Materials and Methods

Study Site

Khairpur district is located in the northern part of Sindh province along the river Indus. It is a dry and hot climate area; average annual precipitation is 78 mm, relative humidity in summer is 48%, and humidity in winter is 61%. Wind speed in summer is 10 kilometers per hours (kph) and in winter it is 5 kph. The maximum monthly average temperature in June is 44[degrees]C and in January it is 23[degrees]C (Pakistan meteorological department). The district has an area of 15,910 [km.sup.2] and a population of 1,546,587, of which 76% is rural (Population Census Organization, Ministry of Economic Affairs and Statistics, Government of Pakistan, 2006). The district is divided administratively into eight talukas (subdistricts), i.e., Khairpur, Faiz Gunj, Thari Mirwah, Kot Diji, Gambat, Kingri, Sobho Dero, and Nara. The residents are primarily involved in agriculture and groundwater is utilized for drinking purposes. Khairpur district was identified as one of the arsenic-affected districts of Sindh province in a national arsenic survey in 2001 (Ahmed, Kahlown, Tahir, & Rashid, 2004).

Study Design and Subjects

A cross-sectional survey was conducted from January to May 2006. Multistage cluster sampling was performed. Out of a total of 1,858 villages in Khairpur, 216 villages were randomly selected for a primary prevalence study. From each selected village, 10 households were identified for the survey In each selected household, one male and one female who had been living there for at least the previous six months and who were at least 15 years old were recruited for the interview. Drinking water samples from all participants were taken for arsenic content determination. Urine samples were taken on the spot from one male participant (in household three) and from one female participant (in household seven) in each visited village. In addition, urine samples were also collected from those participants who had arsenic skin lesions (melanosis or keratosis). During the survey, a total of 505 spot urine samples were collected. Out of those, 40 urine samples were excluded from analysis because of unavailability of corresponding arsenic water results due to spillage of samples during transportation. Therefore, 465 spot urine samples were included in the analysis.

Exposure Assessment

An exposure assessment questionnaire was filled out by each individual in the study. Individuals were excluded who had eaten seafood (fish) during the past three days. Demographic information was also taken (age, sex, education, and occupation). Individuals were asked to estimate their average daily water consumption in order to determine their exposure. Other sources of arsenic exposure (environmental, occupational, and use of herbal medicines) were also assessed. Cigarette smoking and nutritional status (body mass index [BMI]) were evaluated. Drinking water and spot urine samples from study individuals were sent for laboratory analysis of arsenic concentration.

Daily Arsenic Intake Estimation

Daily arsenic intake was calculated directly by multiplying the arsenic concentration in drinking water by the amount of water consumed per day (based on recall) per body weight of the study individuals. Arsenic estimates were not calculated for solid food.

Water and Urine Sample Collection and Processing

The current drinking water source (home hand pump) and spot urine from our study subjects were sampled. Water samples were collected in 0.5-L (500 mL) and urine samples in 0.1-L (100 mL) polyethylene containers. Before sample collection, these containers were washed with nitric acid and then rinsed with deionized water. For water sampling, after discarding the initial water (10 pumps for one minute) from the hand pump, the water was collected in the container. For urine samples, a container was provided to the study subject for a urine sample at the time of the interview. People who had eaten fish or prawns (seafood) within three days of the interview were excluded from the analysis.

To preserve the samples, 1 mL of 1% nitric acid (HN[O.sub.3]) was added to the water sample, and 2-3 drops (0.5 mL) of 3% HN[O.sub.3] were added to the urine samples. The containers were capped and sealed with cloth tape and stored at room temperature. Stored samples were dispatched within one week to the Pakistan Council for Research in Water Resources (PCRWR) laboratory, Islamabad, for total arsenic analysis.

Total arsenic in water and urine samples was analyzed through hydride generation-atomic absorption spectrometry (HG-AAS) at the PCRWR laboratory, Islamabad. The minimum detection limit for arsenic was 0.1 [micro]g/L. Calibration standards for arsenic with concentrations 0, 10, 20, 30, 40, and 50 [micro]g/L were prepared by dilution of a certified standard solution (1,000 mg/L) from Fluka Kamica. Analytical performance

was monitored by analysis of standard reference materials and internal water quality control samples.

Statistical Analysis

Descriptive analysis was performed, including frequency distribution of demographic variables (age, sex, and education), calculation of central tendency (mean/median), variability (percentiles), and arsenic concentration in water and urine. The association between the unspeciated arsenic in drinking water and the concentration of arsenic excreted in urine were evaluated graphically (scatter plot) and by calculating Spearman's rank correlation coefficient. Multivariate regression analysis was performed for adjusting potential confounders (age, sex, smoking, and BMI) of the outcome variable (arsenic in urine). All statistical analyses were computed by using SPSS v. 16.0.

Ethical Approval

The study protocol was reviewed and approved by the ethics review committee of Aga Khan University. All study participants signed an informed consent form.

Results

A total of 465 individuals were recruited to participate in the study from 216 villages of Khairpur district. Females numbered 246 (53%). The mean age of the study participants was 38 [+ or -] 15.1 years. Among participants, 61% had no formal education, 17% were smokers, and 14% had low BMI (<18.5) (Table 1). Drinking water samples (465) were collected from household water sources and analyzed for total arsenic concentration. The arsenic concentrations in drinking water samples ranged from 0.1 to 350 [micro]g/L and the median was calculated as 2.1 [micro]g/L. Approximately 147 (32%) drinking water samples had arsenic above the WHO guideline value of 10 [micro]g/L and 42 (9%) samples were above the Pakistan guideline value of 50 [micro]g/L.

A total of 465 spot urine samples were analyzed for total arsenic. Urinary arsenic concentrations ranged from 0.1 to 848 [micro]g/L and the median was 28.5 [micro]g/L.

In the study population the average water consumption volume was 2.8 [+ or -] 0.9 L per day (range: 0.75-5.75 L/day). Median arsenic concentration intake through drinking water was 5.7 [micro]g/day (range: 0.1-742 [micro]g/ day), per body weight daily arsenic intake ranged from 0.1 to 14.7 [micro]g/kg/day, and the median was 0.10 [micro]g/kg/day. Considering oral reference dose (RfD) of daily arsenic intake is 0.30 [micro]g/kg/day (U.S. Environmental Protection Agency, 1998), then approximately 175 (37.6%) of the study individuals had been exposed to arsenic above RfD.

Spearman's rank correlation coefficient was calculated between total arsenic in drinking water and the total arsenic excreted in urine of the study individuals. We found a moderate degree of positive correlation (r = .52, p < .01), indicating a linear relationship between total arsenic in drinking water and total arsenic excreted in urine (Figure 1). Similar positive correlation was also found when daily arsenic intake ([micro]g/ day) through drinking water was compared with the total arsenic excreted in urine (r = 0.52, p < .01) (Figure 2). Potential confounders (age, sex, smoking, and BMI) were adjusted by using multivariate linear regression and the arsenic in drinking water was found more associated with urinary arsenic (B coefficient = 1.672; p < .001).

Discussion

Our study provides information on arsenic exposure to humans through drinking groundwater. This was established by using the urine samples of exposed individuals as a biomarker of arsenic exposure. People in the study district (Khairpur) have continuously ingested unsafe levels of arsenic (above 10 [micro]g/L) through drinking groundwater for a long time. No alternate safe water options exist, and people have been developing arsenic-induced skin lesions, melanosis and keratosis (Fatmi et al., 2009). Our study consolidated the evidence of arsenic exposure in the chronically exposed population solely through drinking groundwater after adjusting independent predictor variables (age, sex, smoking, and BMI) of the outcome variable (arsenic in urine) by using multivariate regression analysis.

Study drinking water samples (n = 465) were screened for arsenic concentration using the "gold standard" laboratory method (HG-AAS). Hence reliability of the water arsenic test results was not compromised. Previous studies performed arsenic screening for only limited commonly shared water sources (Calderon et al., 1999; Mera et al., 2004) and through using a less sensitive arsenic field test kits method (Rahman et al., 2006).

Spot urine specimens, instead of morning urine samples, were utilized for the study to determine the arsenic concentration in urine of the study population who were exposed to arsenic through drinking groundwater. Studies have reported that concentration of arsenic in urine remains stable throughout the day and over a period of five consecutive days (Calderon et al., 1999). The stability of arsenic concentration in urine suggests that the exposed population was at steady state in terms of exposure to arsenic.

Limitations of our study were that only total arsenic concentration was detected in drinking water and urine samples and we did not perform arsenic speciation due to limited laboratory capacity and financial constraints. Arsenic levels in urine were determined only through weight by volume without adjustment of urinary creatinine levels (weight/weight). Another limitation of our study was related to the methods of estimation of arsenic intake. In our study, the estimation of individual arsenic intake was calculated only from drinking water of the household water source, supposed as a main source of drinking water and a stable source of arsenic exposure; other sources of drinking water such as the workplace were not considered. Dietary (solid food) sources of arsenic were also not considered. A previous study reported that the average contribution to the total arsenic intake from solid food was 11% (Ohno et al., 2007).

Median arsenic concentration in drinking water was reported as 2.1 [micro]g/L (right-skewed data distribution), which lies within the normal limit of WHO's guideline value. Still, nearly one-third of the study population was exposed to arsenic through drinking water above 10 [micro]g/L at higher percentiles (Table 2).

In the study population, average daily water intake was reported high (2.8 L) possibly because of the hot climate of the area (maximum monthly average temperature in summer was 42[degrees]C); therefore body water demand increased and consequently an increased amount of arsenic was ingested. Considering this fact only from a single household drinking water source, daily arsenic exposure per body weight was above RfD in more than one-third of the study population.

Moderate correlation was reported between arsenic exposure through drinking water and urinary arsenic excretion. Considerable variability is found, however, between the level of arsenic exposure through drinking water and urinary arsenic excretion; for instance, variability observed at the median level is 14 times higher and at the 75th percentile level it is 3-4 times higher for urinary arsenic excretion (Table 2).

Our study could not find an age-related difference in arsenic excretion in urine (Table 3). Similar results were reported in a study conducted in a northern Argentina population chronically exposed to arsenic through drinking water (Concha, Nermell, & Vahter, 1998). When correlating with gender, no significant difference was found in urinary arsenic excretion in either males or females. This finding is in contrast with the finding reported in earlier studies in which distinct gender-related differences have been reported in the excretion of arsenic in urine (Del Razo et al., 1994; 1997).

In conclusion, a moderate correlation exists between the concentration of arsenic in drinking water and the concentration of arsenic excreted in urine. This suggests that over the range of exposure, drinking water was the predominant source of arsenic exposure. Hence arsenic in urine came out as a good predictor of arsenic exposure to humans through drinking water.

Conclusion

A moderate positive correlation exists between arsenic exposure through drinking water and the concentration of arsenic in urinary excretion. This would suggest that if the arsenic content in drinking water is higher then the arsenic excretion in urine would be higher. Thus arsenic excretion in urine can be used as a good indicator of arsenic exposure.

Acknowledgments: We would like to acknowledge the donor agency UNICEF for providing financial support, PCRWR for doing laboratory analysis, and local government Sindh for facilitating the study. We would also like to thank our field staff who made it possible to conduct this survey. Lastly we thank the people of Khairpur for their hospitality and participation in the survey.

Corresponding Author: Mubashir Ahmed, Research Coordinator, Department of Community Health Sciences, Aga Khan University, Stadium Road, PO. Box 3500, Karachi, Pakistan.

E-mail: mubashir.ahmed71@yahoo.com.

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Mubashir Ahmed, MBBS, MSc

Zafar Fatmi, MBBS, FCPS

Department of Community Health Sciences

Aga Khan University

Arif Ali, MSc

Department of Research

Dow University of Health Sciences

TABLE 1

Demographics Details of the Study Population of Khairpur District
(N = 465)

Characteristics                               #        %

Age (years)

15-29                                        153      32.9
30-44                                        163      35.1
45-59                                        102      21.9
[greater than                                 47      10.1
  or equal to]60
Mean (SE) (a)                              38 (0.7)    --

Gender

Male                                         219      47.1
Female                                       246      52.9

Education level

College                                       49      10.5
Secondary                                     63      13.5
Primary                                       71      15.3
No formal education                          282      60.6

Smoking status

Never smoked                                 384      82.6
Ever smoked                                   81      17.4

BMI (kg/[m.sup.2])

Low (<18.5)                                   64      13.8
Normal ([greater than or equal to]18.5)      401      86.2
Mean (SE)                                  23 (0.2)    --

(a) SE = standard error of mean.

TABLE 2

Arsenic Concentrations in Drinking Water, Daily Intake,
and Urine of Study Population of Khairpur District (N = 465)

Characteristics   Drinking Water    Daily Intake       Urine
                   ([micro]g/L)    ([micro]g/day)   ([micro]g/L)

Maximum                350              742            848.5
90th percentile        46.5            128.9           171.1
75th percentile        15.8             41.4            67.7
Median                 2.1              5.7             28.5
25th percentile        0.9              2.5             11.2
10th percentile        0.4              1.1             3.0
Minimum                0.1              0.1             0.1
# of cases             465              465             465

TABLE 3

Age-Related Difference in Arsenic Concentration in Urine in Study
Population of Khairpur District (N = 465)

Characteristics   Age Groups (Years)

                  15-29   30-44   45-59   [greater than or
                                            equal to] 60

Mean              72.6    60.9    56.0          55.2
Median            27.7    29.7    29.6          26.0
Minimum            0.1     0.0     0.4          1.2
Maximum            848    700.8    309         722.4
25th percentile   10.8     9.6    13.6          12.5
75th percentile   74.8    67.6    67.9          55.5
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Title Annotation:INTERNATIONAL PERSPECTIVES
Author:Ahmed, Mubashir; Fatmi, Zafar; Ali, Arif
Publication:Journal of Environmental Health
Article Type:Report
Geographic Code:9PAKI
Date:Jan 1, 2014
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