Article

A population assessment of mercury exposure from two cities of Pakistan with respect to freshwater and marine fish consumption

Toxicology and Industrial Health 1–9 © The Author(s) 2014 Reprints and permissions: sagepub.co.uk/journalsPermissions.nav DOI: 10.1177/0748233714545503 tih.sagepub.com

Abdul Qadir Shah1, Tasneem Gul Kazi1, Hassan Imran Afridi1 and Mohammad Balal Arain2 Abstract In this study, we aimed to estimate the level of mercury (Hg) in scalp hair samples of human subjects and its association with consumption of sea- and freshwater fish species. The scalp hairs were collected from both genders (male and female) aged between 15 and 50 years (n ¼ 200), living in coastal areas of Karachi, who mostly consumed sea fish species, referred to as exposed subjects. For comparison purposes, scalp hair samples of both genders (n ¼ 160) were collected from the inhabitants of Karachi and Hyderabad cities who consumed freshwater fish species termed as referent subjects. The frequently consumed fresh and marine fish species were also collected. The level of Hg was determined in fish and scalp hair samples by cold vapor atomic absorption spectrometry, prior to ultrasonic-assisted acid digestion in a mixture of nitric acid and hydrogen peroxide. The validity of methodology was checked by certified reference material (CRM) BCR 397 (human hair) and DORM-2. The concentrations of Hg in sea- and freshwater fish were found in the range of 1.47–2.09 and 0.402–0.676 g/g, respectively. The exposed subjects had significantly elevated levels of Hg in scalp hair samples (1.8–4.3 g/g) as compared to referent subjects (0.87–1.95 g/g) (p < 0.001). A significant positive correlation was obtained between the concentration of Hg in hair and age of study population. Exposed and referent female subjects had higher levels of Hg in scalp hair than that in males of both study groups (p ¼ 0.02–0.031). Keywords Mercury, scalp hair, sea fish, gender, cold vapor atomic absorption spectrophotometry

Introduction Mercury (Hg) is a widely dispersed environmental pollutant with well-known toxic effects. It has systematic acute and chronic effects on different systems of the human body (Pizzichini et al., 2002; Thronhill and Pemberton, 2003). High exposure to Hg damages the central nervous system, causing paresthesia, dysarthria, and ataxia (Olivero et al., 2002; Sari and Tuzen, 2009). Impairment of hearing, constriction of the visual field, and limb tremor are also common symptoms of severe Hg poisoning (Thronhill and Pemberton, 2003; Pizzichini et al., 2002). In the general population, there are two main sources of Hg exposure, namely occupational as well as consumption of food including fish and other seafood (Agah et al., 2007; McDowell et al., 2004; Ramirez et al., 2000). Therefore, many studies have

reported that Hg concentrations in blood and hair have been widely used as biomarkers for humans in studies related to fish consumption and are also employed in risk assessment (Bjornberg et al., 2005; Ip et al., 2004). Hg in fish is easily absorbed by the gastrointestinal tract and rapidly enters the blood stream. It is distributed throughout the body within 3–4 days. It is estimated that 5% of dietary Hg is found in the blood and 10% in the brain, with a half-life ranging 1

Centre of Excellence in Analytical Chemistry, University of Sindh, Jamshoro, Pakistan 2 University of Science and Technology Bannu, Pakistan Corresponding author: Tasneem Gul Kazi, Centre of Excellence in Analytical Chemistry, University of Sindh, Jamshoro 76080, Pakistan. Email: [email protected]

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between 45 and 70 days (Castoldi et al., 2003). Ingested Hg readily crosses the placenta and blood– brain barriers (Ramirez et al., 2000). The severity of the symptoms correlates with the duration and rate of ingestion of Hg-contaminated food (Tuzen and Soylak, 2005; Tuzen et al., 2009a). In recent decades, the high concentration of Hg in the environment is due to the use of hard and brown coals as well as other fossil fuels (Falandysz et al., 2000). The increasing level of Hg found in the food chain caused disasters like Minamata and other tragedies in Japan, Iraq, Quebec, Canada, Brazil, and many other areas of the world (Michael, 2003). The severity of the symptoms correlates with the duration and rate of ingestion of Hg-contaminated food (Grandjean et al., 2002). Different studies have shown that fish consumption may also constitute an important source of inorganic Hg exposure (Dakeishi et al., 2005; Diez et al., 2008; Nahum et al., 2000; Ohno et al., 2007). To assess human exposure to Hg, body fluids such as blood and urine and tissues such as hair and nail have been analyzed (Agusa et al., 2007; Akagi et al., 1995; Mortada et al., 2002; Johnsson et al., 2004). Hair is a suitable indicator for biomonitoring of human exposure to Hg that can reflect body burden of Hg as well as dietary intake (Agusa et al., 2005; Barbosa et al., 2008; Grandjean et al., 1994). The potential risk of health hazards to human by Hg exposure has been estimated by using its content in hair, nail, blood, and other body tissues (Apostoli et al., 2002; Minoia et al., 2007). Among them, however, hair Hg seems to be the best indicator and widely used matrix for investigating Hg exposure of an individual (Xiaojie et al., 2008), which has been suggested by many researchers due to easy collection, low cost, and storage (Bjornberg et al., 2003; Harakeh et al., 2002; Tuzen et al., 2009b; Yasutake et al., 2004; Zahir et al., 2005). In analytical chemistry, ultrasound radiation is of great help in the pretreatment of solid samples, as it facilitates and accelerates operations such as the extraction of organic and inorganic compounds (Afridi et al., 2006). The effects of extremely high temperature and pressure at the interface of sonicated solution and solid matrix along with the oxidative power of strong acids result in high extractive power (Suslick, 1994). The use of ultrasonic devices is a good alternative to minimize the disadvantages of conventional extraction procedures in number of analytical steps, time, extraction efficiency, and reagent consumption (Kazi et al., 2009).

Nowadays, the most widespread method for Hg determination is cold vapor atomic absorption spectrometry (CV AAS) (Shah et al., 2009; Tuzen et al., 2009). This technique is based on the chemical reduction of Hg, usually by tin (Sn2þ) or tetrahydroborate (BH4) ions, to elemental Hg which is swept from the solution by a carrier gas to a quartz cell placed in the optical path of an atomic absorption spectrophotometer, where the absorption of Hg is measured. The purpose of the present study was to determine the Hg level in the scalp hair samples of local population of Karachi residing in coastal areas (mostly fishermen), who most frequently consume sea fish and are predicted as exposed population. For comparative purposes, the scalp hair of residents of Karachi and Hyderabad cities consuming freshwater fish species are termed as referents or nonexposed subjects. The fresh- and seawater fish, consumed frequently by population of both cities of Pakistan, were also collected simultaneously. The level of Hg was determined by CV AAS. The correlation of Hg levels in scalp hair and different fish species related to gender and age of the study population was studied. The selected study subjects do not have any occupational and industrial exposure or even amalgam fillings. The resulted data are compared with the literature reported data (Hg levels in hair and in consumed fish species).

Materials and methods Instrumentation The ultrasonic-assisted extractions were carried out with an ultrasonic bath Sonicor, Model No. SC121TH, Sonicor Instrument Corporation (Copiague, New York, USA) with technical specifications; programmable for temperature ranging from 0 to 90 C, time 0–30 min, 220 V, 50–60 Hz, intensification frequency of 35 kHz for the ultrasound energy was used to induce the acid digestion process. For comparative purposes, microwave-assisted acid digestion method was also used. The Hg in samples and standard solutions was determined using an atomic absorption spectrometer, Analyst 700 (Perkin-Elmer, Norwalk, Connecticut, USA) using MHS-15 chemical vapor generation system (Perkin-Elmer, Waltham, Massachusetts, USA). A Hg hollow cathode lamp operated at 5 mA was utilized as the radiation source. Measurements were carried out in the integrated absorbance (peak area) mode at 253.7 nm, using a spectral band width of 2.6 nm. Argon of 99.99% purity was used as the carrier gas.

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Reagents The ultrapure water obtained from ELGA lab water system (Bucks, UK) was used throughout. Concentrated nitric acid (HNO3) and hydrogen peroxide (H2O2) were of analytical reagent grade obtained from Merck (Germany) and were checked for possible trace contamination. Working standard solutions were prepared by appropriate dilution of the certified stock solution of Hg (1000 g/l) obtained from Fluka Kamica (Bushs, Switzerland). The method was validated by CRM, BCR 397 (human hair). A solution of sodium tetrahydroborate (Acros Organics New Jersey, USA) was prepared by dissolving in 0.05 M KOH. All glassware and polyethylene bottles were thoroughly washed and then soaked overnight in 5 M HNO3, thoroughly rinsed with distilled and deionized water before use.

Study population The survey on fish consumption was conducted in two cities (Hyderabad and Karachi) of Pakistan. The population of Karachi and especially Hyderabad generally consume freshwater fish, termed as nonexposed/referent subjects, while in coastal areas of Karachi, people (mostly fishermen) consumed sea fish, termed as exposed subjects. Karachi is located near the Arabian Sea, while Hyderabad is about 60 kilometers away from Karachi. The coastal area of Karachi is polluted due to untreated waste water sewage of industries as well as oil spills from ships and fishing trawlers during transiting the port (Pakistan National Environmental Action Plan, 1991). Hair samples were collected from 360 individuals living in two cities of Pakistan. Each participant was interviewed using the questionnaire, containing information such as age, gender, race, weight, height, fish consumption (the quantity and frequencies of consumption), type of their favorite fish, and number of amalgam dental fillings (if they had any). The exposed subjects informed that there is no favorite type of fish, as they usually eat what is readily available from their daily catch. Fishing was the major economic activities for exposed population, while referents were mostly office workers and laborers. People exposed to Hg by other sources (working in chemical or pesticide industries) were not included in this study. None of exposed and control subjects had any amalgam dental fillings. It was observed that following sea fish species are frequently consumed by exposed subjects of Karachi,

Pakistan in their diet: Scombermorus (Surmai), Arius spp. (Khagga), Otolithes (Mushka), and Pampus argenteus (Poplet), while referent subjects mostly eat freshwater fish species, Labeo calbasu, Cirrhinus mrigala, Cirrhinus reba, and Mystus gullio. The estimated average daily consumption of fish per capita was about 100–200 g for adults of coastal areas, while nonexposed population may consume about 100–200 g/week. All the participants informed that they cooked fish in home. In present study, the fish consumption was expressed as g/day and not as number of meals per period thereby avoiding local differences in the size of the meals (average each standard meal 100 g).

Sampling Four types of marine and freshwater fish species (n ¼ 10 of each) were collected from the shops of areas understudy or directly acquired from local fishermen (only sea fish). The fish samples were delivered in an ice box filled with ice and brought to the laboratory for further treatment. In first step, muscles were separated from the bones. The muscle tissues were freeze-dried for 20 h at a chamber pressure of 0.225 torr. The lyophilized samples were crushed and homogenized to a fine powder in an agate ball mill. The resulting powder was stored in polyethylene bottles at 4 C till further preparation and analysis. Hair samples (about 2 cm) were taken from the nape of the head as near as possible to the scalp with a pair of stainless steel scissors. The hair treatments (e.g. bleaching, dyeing, and artificial waving) may influence the Hg content of hair, so only untreated hair was selected for the study. Hair specimens were packed in polyethylene bags and stored at room temperature until analysis. The scalp hair samples were first washed with ultrapure water, then three times with acetone and finally washed with ultrapure distilled water. The samples were then oven-dried at 60 C. The study protocol for hair sampling was approved by the institutional review Board of National centre of excellence, Sindh University working under higher education commission.

Methodology Ultrasound-assisted acid digestion Triplicate tissue samples of each fish species, scalp hair samples of study population, and six replicate

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Table 1. Validation of the proposed method for determination of Hg in CRMs (g/g). Certified values (g/g) Ultrasonic-assisted acid extraction Microwave-assisted acid digestion Paired t-testb (texperimental) DORM-2 4.64 + 0.26 BCR 397 (human hair) 12.3 + 0.5

4.62 + 0.211 (99.9)a

4.629 + 0.234 (99.7)a

0.0845

12.2 + 0.21 (99.1)a

11.9 + 0.23 (96.7)a

0.146

Hg: mercury; CRM: certified reference material. a

% Recovery ¼

½certified value  100: ½found values

b

Paired t-test between certified/found values, at degree of freedom (n  1) ¼ 5, tcritical at 95% confidence limit ¼ 2.57.

samples of CRM (200 mg) were placed in flasks (25 ml in capacity). Then, 2 ml of a mixture of concentrated (65%) HNO3 and 30% H2O2 in (2:1 ratio) were added and the flask was kept at room temperature for 10 min. The flasks were placed inside the ultrasonic water bath and subjected to ultrasonic energy at 35 kHz for different time intervals at a fixed temperature of 80 C. After sonication for different time intervals, the resulting extracted solution was diluted with 5 ml of ultrapure water and centrifuged at 3000 r/min for 5 min. The supernatant solutions were collected in a polyethylene flask for the determinations of Hg by CV AAS. Blank extractions were carried out through the complete procedure. Blanks and standard solutions were prepared in a similar acid matrix. To evaluate the efficiency of the process, the results obtained with the ultrasoundassisted acid digestion were compared with those obtained from microwave-assisted acid digestion (MAD), using a domestic microwave oven on same CRM and real samples.

Microwave-assisted acid digestion A MAD procedure was carried out to obtain Hg in samples for comparative purpose. Six replicates of CRM and duplicate samples of fish tissue of each species and scalp hair were directly weighed into polytetrafluoroethylene (PTFE) tubes. Then, 2 mL of a freshly prepared mixture of concentrated HNO3 and H2O2 (2:1, v/v) was added to each tube and kept for 10 min at room temperature; then the tubes were closed and placed in a covered PTFE container. It was then heated following a one-stage digestion programmed at 80% of total power (900 W), 4–5 min for complete dissolution. The digestion tubes were cooled, and the resulting solution was diluted up to 10 mL with ultrapure water and stored in Teflon

flasks as master sample solutions. The Hg determination was carried out by CV AAS, using sodium tetrahydroborate as the reducing agent and hydrochloric acid as carrier solution.

Statistics The comparisons between the exposed and referent groups according to consumption of sea- and freshwater fish were analyzed by Kruskal–Wallis test and Wilcoxon’s rank sum test. In the univariate analysis of the data, the Mann-Whitney was used for assessing the differences between under study groups. p Values less than 0.05 were considered statistically significant. The relationship between Hg level and age of residents was determined by Pearson’s correlation coefficient.

Analytical figure of merit The method was assured by the analysis of triplicate samples, reagent blank, and standard reference material. The linear calibration graph of Hg was obtained from the quantification limit up to 5.0 g/l, while the coefficient of correlation was 0.999. The limits of detection (LOD) and quantitation (LOQ) were calculated as, LOD ¼ 3  ms and LOQ ¼ 10  ms , respectively, where ‘s’ is the standard deviation of 10 measurements of reagent blanks and ‘m’ is the slope of the calibration graph. The calculated LOD was 0.133 g/l and LOQ was 0.445 g/l. The precision of the methods, expressed as the relative standard deviation (%RSD) of 8 independent analyses of the same sample, provided values are less than 10% for the determination of total Hg. The accuracy of analytical method was determined with CRMs, DORM 2, and BCR 397 (human hair) (Table 1).

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Table 2. Estimation of Hg in fish muscles of freshwater and marine fish species by ultrasonic acid extraction method (g/g) dried weight basis (n ¼ 30 each). Sea fish species

Freshwater species

Scientific and common names

Total Hg

Scombermorus commersoni (Surmai) Arius spp. (Khagga) Otolithes ruber (Mushka) Pampus argenteus (Poplet)

a

1.861 2.09 1.47 1.74

Scientific and common names a

+ 0.58 + 0.44 + 0.38 + 0.27

Mystus gullio (Gullio) Catla catla (Thaila) Mystus seenghara (Senghara) Labeo rohita (Rahu)

Total Hg 0.546 + 0.676 + 0.583 + 0.402 +

0.062 0.084 0.074 0.089

Hg: mercury. a Common name of fish in parentheses.

Table 3. The total Hg concentration in scalp hair of exposed and nonexposed subjects (g/g). Exposed subjectsa Age group 15–30 30–50

Male a

1.91 + 0.16 (2.80 + 0.16)

Nonexposedb Female

Male

Female

2.19 + 0.03 (3.14 + 0.31)

1.06 + 0.04 (1.23 + 0.13)

1.13 + 0.12 (1.58 + 0.26)

Hg: mercury. a Consumed marine fish species. b Consumed freshwater fish species.

Results and discussion Hg levels in fish species and scalp hair samples The moisture contents in fish muscle tissues were found in the range of 74–78%. The mean values with standard deviation of Hg in freshwater and marine fish species are shown in Table 2. The levels of Hg in freshwater fish were significantly lower than in marine fish species (p < 0.001). Freshwater fish species collected from Indus river, considered to be unpolluted (without any anthropogenic Hg point source input), usually have >1 g/g. The concentration of Hg in sea fish species collected from the coastal area of Karachi was found to be in the range of 1.47–2.09 g/g, whereas Hg content in fish species of freshwater was observed in the range of 0.402– 0.676 g/g. These values were used to correlate with the concentration of Hg in scalp hair of both understudy populations.

Hg concentration in scalp hair of exposed and referent populations The concentrations of Hg in scalp hair of exposed and nonexposed males were found in the range of 1.2–3.4 and 0.7–1.8 g/g, respectively, while the levels of Hg in scalp hair of exposed and referent females were

observed in the range of 1.8–4.3 and 0.87–1.95 g/ g, respectively (Table 3). The high levels of Hg in scalp hair of exposed population are above the normal value of Hg in scalp hair (2. 0 g/g) recommended by World Health Organization (WHO) and International Program on Chemical Safety (IPCS, 1990). The levels of Hg in scalp hair samples of exposed female were significantly higher than those of corresponding exposed males (p < 0.05). Previous studies also indicated that sex is unlikely to be an important factor determining Hg accumulation in hair (Kosatsky et al., 2000; Olivero et al., 2002). Batista et al. (1996) had reported that girls exhibited higher Hg levels in their hair than boys, whereas another study reported that Hg concentration in the hair of males was higher than that of females (Diez et al., 2008). At present, the reason for explaining the gender difference is not yet clear. Fish consumption is one of the major factors of Hg intake for humans (Al-Majed and Preston, 2000; Harada et al., 2001; Olivero et al., 2002; Santos et al., 2000; Yasutake et al., 2004). The use of hair analysis for evaluating Hg intoxication of the human body is a useful bioindicator, which is also suggested by other investigators (Abe et al., 1995; Dumont et al., 1998; Malm et al., 1995; Oskarsson et al., 1994). The correlation of Hg contents in different fish species and scalp hair of humans was compared with the

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Table 4. Comparison of the mean/ranges of Hg concentrations in fish species and scalp hair samples with the literature. Countries Brazil Rabat, Morocco South western Ghana Seychelles Islands Sweden Spain, Madeira Our study

Hg in fish (g/g) 0.69 0.05–0.137 0.01–2.50 0.3 0.7

1.47–2.09 (marine fish) 0.739–1.47 (freshwater fish)

Hg in scalp hair (g/g)

References

25 0.22–9.56 0.06–28.3 0.5–27 0.9 Females ¼ 38.9 g/g; male ¼ 10.4 g/g Male ¼ 1.91–2.80 g/g; female ¼ 2.19–3.14 g/g Male ¼ 1.06–1.23 g/g; female ¼ 1.13–1.58 g/g

Malm et al., 1995 Hecham et al., 2007 Adimado and Baah, 2002 Myers et al., 2003 Al-Majed and Preston, 2000 Renzoni et al., 1998 This work

Hg: mercury.

literature reported data (Table 4). It was observed that in present study the concentrations of Hg in understudied fish species and scalp hair were high, as compared to the literature reported values of Hg concentration in fishes and scalp hair (Adimado and Baah, 2002; Al-Majed and Preston, 2000; Hecham et al., 2007; Myers et al., 2003), except the concentration of Hg in scalp hair reported by Hecham et al., 2007 and Renzoni et al., 1998.

Age and gender dependent accumulation of Hg in scalp hair In the current study, exposed and referent subjects were also classified according to age, ranging from 15 to 30 years and 31 to 50 years of both genders. The Hg concentrations in scalp hair samples of exposed subjects with lower age groups were found in the range of 1.2–3.1 g/g, while in older groups the levels of Hg in scalp hair were significantly higher (1.8–4.3 g/g), p < 0.01 (Table 3). The relationships between Hg concentrations and age were tested by one-way analysis of variance (ANOVA). Spearman’s correlation coefficient showed that a positive correlation was observed between the level of Hg in scalp hair and age groups of both genders (r ¼ 0.629–0.724, p < 0.01). Our results are consistent with other studies, who reported a positive relation between Hg levels in scalp hair and age (Al-Majed and Preston, 2000).

Risk assessment of Hg exposure via fish consumption The toxicity of Hg derived from fish consumption is a potential threat to public health. The present study gave an insight that fish consumption is a significant

route of Hg exposure for the coastal communities. Analysis of Hg in hair of the exposed population helps to establish the risk of Hg intake due to consumption of contaminated sea fish (USEPA, 2001). Estimated daily intake of Hg by exposed population based on the consumption of 100–200 g fresh fish muscles per day ranges from 0.62 to 0.87 and 1.22 to 1.74 g/kg body weight/day for two age groups, which is significantly higher than Food and Agriculture Organization/WHO recommended tolerable daily intake of 0.22 g/person/day of Hg (p < 0.001) (WHO FAO, 1989), while the consumption of the same amount of freshwater fish species by two age groups corresponds to 0.167–0.281 and 0.335–0.563, which are greater than or equal to the tolerable limit. It was reported that high intakes of fish can be traced by the high Hg concentrations in hair (Al-Majed and Preston, 2000; Olivero et al., 2002; Santos et al., 2000; Scerbo et al., 2005; Yasutake et al., 2004). It was noted that more than 50% of exposed subjects complained of headache, back pain, irritability, and reduction in hearing, while neurological problems were not studied presently. Guallar et al. (2002) reported that about 0.34–2.03 g/g Hg in scalp hair was associated with increased risk of myocardial infarction and may diminish the cardio protective effect of fish intake. The US Environmental Protection Agency defines a reference dose of 0.1 g Hg/kg of body weight per day, which corresponds to a level of 1.0 g/g in hair (USEPA, 2005). Our results support the findings of earlier studies and indicated that the concentration of Hg found in hair of adult respondents with no occupational exposure is mainly dependent on dietary intake (Bjornberg et al., 2005; Lee et al., 2000; Johnsson et al., 2004; Olsen and Secher, 2002).

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Conclusion According to the results of the present study, Hg exposure was higher in individuals who consumed sea fish species, indicated by the higher levels of Hg in scalp hair samples of both genders, than those who consumed freshwater fish species with lower levels of Hg. So, sea fish consumption is the most important route of Hg exposure to common people, especially the poor fishermen who do not have a diverse choice of diet other than sea fish. This is the first published study on the exposure of Pakistani population of two areas to Hg through fish consumption. The establishment of baseline levels for the study areas enables future monitoring to be carried out with the aim of detecting changes in Hg exposure, especially in relation to the impact of industrial and other human activities on the marine ecosystem. In the coastal area of Karachi, the price of sea fish is less than other cities of Pakistan and different types of fish species are easily available throughout the year. The Hg monitoring and neurological studies should be conducted to assess the impact of Hg intake by fish consumption on the health of people, especially on &&&childbearing women. Funding This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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A population assessment of mercury exposure from two cities of Pakistan with respect to freshwater and marine fish consumption.

In this study, we aimed to estimate the level of mercury (Hg) in scalp hair samples of human subjects and its association with consumption of sea- and...
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