Toxin Reviews

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Toxic metals in agricultural soils near the industrial areas of : ecological and human health risk assessment

Tapos Kormoker, Ram Proshad, Saiful Islam, Saad Ahmed, Krishno Chandra, Minhaz Uddin & Mahfuzur Rahman

To cite this article: Tapos Kormoker, Ram Proshad, Saiful Islam, Saad Ahmed, Krishno Chandra, Minhaz Uddin & Mahfuzur Rahman (2019): Toxic metals in agricultural soils near the industrial areas of Bangladesh: ecological and human health risk assessment, Toxin Reviews, DOI: 10.1080/15569543.2019.1650777 To link to this article: https://doi.org/10.1080/15569543.2019.1650777

Published online: 07 Aug 2019.

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RESEARCH ARTICLE Toxic metals in agricultural soils near the industrial areas of Bangladesh: ecological and human health risk assessment

Tapos Kormokera, Ram Proshadb,c , Saiful Islamc,d,e, Saad Ahmedc, Krishno Chandraf, Minhaz Udding and Mahfuzur Rahmanh aDepartment of Emergency Management, Patuakhali Science and Technology University, Dumki, Bangladesh; bInstitute of Mountain Hazards and Environment, Chinese Academy of Sciences, Chengdu, China; cDepartment of Soil Science, Patuakhali Science and Technology University, Dumki, Bangladesh; dDepartment of Applied Biological Chemistry, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan; eGraduate School of Environment and Information Sciences, Yokohama National University, Yokohama, Japan; fFaculty of Agricultural Engineering and Technology, Agricultural University, Sylhet, Bangladesh; gDepartment of Environmental Science, Bangladesh Agricultural University, , Bangladesh; hFaculty of Agriculture, Patuakhali Science and Technology University, Dumki, Bangladesh

ABSTRACT ARTICLE HISTORY This study was conducted to assess the potential ecological and human health risk of toxic met- Received 16 June 2019 als in agricultural soils near the industrial areas of Bangladesh. In this study, six toxic metals Revised 27 July 2019 (chromium, nickel, copper, arsenic, cadmium, and lead) were assessed in 58 soil samples of five Accepted 28 July 2019 different sampling sites around the industrial areas of and districts in KEYWORDS Bangladesh. Toxic metals were measured using inductively coupled plasma mass spectrometer. Agricultural soils; toxic Potential ecological and human health risk were assessed through enrichment factor (EF), con- i metals; PCA; ecological risk; tamination factor (Cf ), geoaccumulation index (Igeo), pollution load index (PLI), toxic unit analysis, health risk; Bangladesh chronic daily intake through exposure pathway, hazard quotient, and hazard index. The mean concentrations of Cr, Ni, Cu, As, Cd, and Pb were found to be 5.78, 21.0, 31.8, 8.05, 1.20, and 19.2 mg/kg, respectively. Metals concentrations were found below the recommended value set by Dutch standard, Canadian guidelines, and Australian guidelines except Cd. Principal compo- nent analysis indicates that most of the metals in agricultural soils are coming from industrial i sector. The mean values of EF, Igeo, Cf , PLI, and toxic units were found safe level for all metals except Cd. In the view of potential ecological risk (PER), soils from all sampling sites indicated moderate to very high PER. Total target hazard quotients for all the studied metals in total sam- pling sites were <1 and cancer risk values were <106 indicating low noncarcinogenic and can- cer risk for adult and children.

Introduction due to various toxic metals from rapid industrialization Soil is a vital element for human life to survive the and development and it has become more severe for planet which is assumed as prime receiver of persist- developing countries like Bangladesh due to its indis- ent pollutants such as toxic metals (Karim et al. 2014, criminate growing industries without any proper plan- Islam et al. 2015a, Proshad et al. 2018a). Soil contamin- ning (Sun et al. 2010, Chen et al. 2010, Shi et al. 2011, ation by toxic metals is a substantial environmental Ahmed et al. 2015). Heavy metals may originate in problem worldwide (Alloway 1995, due to their wide soils around the industrial areas from numerous sour- sources, toxicity, and nonbiodegradable nature (Yuan ces but industrial activities such as generation of et al. 2011, Zhao et al. 2014, Islam et al. 2015b, power, manufacturing, burning of fossil fuel, and dis- Bhuyan et al. 2017, Islam et al. 2018). According to the posal of waste are the most important contributors of US Environment Protection Agency (EPA), toxic metals soil pollution (Karim et al. 2014, Rodrıguez Martın such as chromium, nickel, copper, arsenic, cadmium, et al. 2014, Islam et al. 2016). Almost all industrial units and lead have been considered as the most toxic met- are discharging their untreated wastes in the surface als in the environment (Lei et al. 2010, Proshad et al. drains and spread over agricultural fields. Toxic ele- 2017). In recent decades, contamination of soils occurs ments toxicity changes agricultural soil bionetworks

CONTACT Ram Proshad [email protected] Chinese Academy of Sciences, Institute of Mountain Hazards and Environment, Chengdu, 610041, China; Department of Soil Science, Patuakhali Science and Technology University, Dumki, 8602, Bangladesh ß 2019 Informa UK Limited, trading as Taylor & Francis Group 2 T. KORMOKER ET AL. that have a significant negative consequence on the and industrial regions of the world as well as productivity of land (Khan et al. 2010, Yuan Bangladesh (Luo et al. 2007,Manet al. 2010, Islam et al. 2014). et al. 2016, Proshad et al. 2017, but there is very lim- The contaminations of soil quality by toxic metals ited research has been conducted so far on toxic have exerted long-term ecological and health risks. metals in soils and its adverse effects on the environ- Agricultural crops which are being cultivated in the ment as well as human health, especially the indus- contaminated agricultural soils may cause serious car- trial areas of Jhenaidah and Kushtia districts. cinogenic and noncarcinogenic risks to the human Therefore, the purposes of this study were (1) to body (Man et al. 2010, Proshad et al. 2018b). In the determine the physiochemical properties and concen- industrial areas, toxic metals polluted soil can pose trations of toxic metals (Cr, Ni, Cu, As, Cd, and Pb) in significant human health risks due to soil ingestion, agricultural soils; (2) to identify the potential sources inhalation, and dermal contact (Siciliano et al. 2009, of toxic metals in agricultural soils; and (3) to assess Luo et al. 2011,Liet al. 2011). Toxic metals can be the potential ecological and health risk of very harmful to the human body even in low concen- toxic metals. trations as there is no effective excretion mechanism (Ghosh et al. 2012). The common public (especially children and adult citizens) are most vulnerable to the Materials and methods toxic metals from soil (Luo et al. 2012). Therefore, exposure to toxic metal pollutants is of utmost con- Study area and sampling cern for children in their primary developmental years The soil samples were collected from industrial ł and also for the adult (Lee et al. 2013, Rachwa et al. areas of Jhenaidah and Kushtia districts, Bangladesh 2017). Various indexes have been widely used to (Figure 1). Jhenaidah and Kushtia districts are two determine environmental risks of toxic elements in industrial growing sites of Bangladesh. There are sev- soils such as contamination factor (CF), enrichment eral types of industrial units including tobacco indus- factor (EF) and geoaccumulation index (I ) (Rashed geo tries, garments, tannery industries, packaging industry, 2010, Liu et al. 2014). The contamination factor, EF, dyeing, brick kiln, metal workshops, battery manufac- and geoaccumulation index of individual toxic metal turing industries, textile industries, pesticide, and fertil- in soil are calculated using its total content and soil izer industries, different food processing industries, quality guideline value (Zhang et al. 2013). For deter- and other industrial areas produce huge volumes of mination of multiple risk of toxic metals in soil, pollu- effluents that contain toxic metals. The untreated tion load index (PLI) and potential ecological risk wastes and effluents from these industries are dis- index (PER) have also been developed (Huang et al. charged randomly to river and canals. Then that 2013). The PLI compares the metal concentrations wastes are mixed with soils and the soil is continu- with baseline values, which helps in assessing the ously polluted by toxic metals. Soil samples were col- enrichment of toxic metals in soil (Yang et al. 2009, – Islam et al. 2018). The chronic daily intake (CDI) esti- lected during March April, 2016. Five agricultural soil mation, target hazard quotient (THQ), and hazard sampling sites (Porahati, Udoipur, Lokhikol, Dhanharia, index (HI) methods have also been developed to and Chourhas) and (58 sampling locations) were assess the carcinogenic and noncarcinogenic health selected near the industrial areas of Jhenaidah and risk through several exposure pathways such as inges- Kushtia districts, Bangladesh. Agricultural surface soils – tion, inhalation, and dermal contact. Therefore, (0 10 cm depth) were collected in the form of three research on potential ecological and health risk assess- subsamples. These subsamples were thoroughly mixed ment due to toxic metals pollution in soils near the to form a composite sample. Samples were air-dried at industrial area is very essential. room temperature for two weeks, then ground and Jhenaidah and Kushtia are two industrialized dis- homogenized. For metal analysis, soil was taken by tricts of Bangladesh that are supposed to be highly means of a percussion hammer corer (50–80 cm in contaminated by toxic metals. These two districts are length) as pre-industrial sample (Schottler and well-known for agricultural production and it pro- Engstrom 2006). The dried soil samples were crumbled vides a large portion of agricultural products all over with a porcelain mortar and pestle and sieved through the country. Although several studies have conducted 2 mm nylon sieve and stored in an airtight clean for assessing ecological and human health risk due Ziploc bag and kept frozen until chemical analysis to toxic metal contamination from soil in the urban (Oliveira et al. 2012, Arenas-Lago et al. 2013, 2014). TOXIN REVIEWS 3

Figure 1. Map showing the study area of Jhenaidah and Kushtia districts, Bangladesh.

Physicochemical parameters analysis triangular diagram designed by Marshall followed USDA system. The percentage of sand, silt, and clay Soil pH was determined by using a glass electrode pH were calculated as follows: meter (WTW pH 522; Germany). For EC determination, 5.0 g of soil was taken in 50 ml polypropylene tubes %ðÞsilt þ clay ¼ and 30 ml of Milli-Q water was added to the tube. The ðcorrected hydrometer reading at 40 s= lid was closed properly and was shaken for 5 min. oven dry weight of soilÞ100 (1) After that, EC was measured using an EC meter (WTW %ðÞclay ¼ LF 521; Germany). For organic carbon, 1.0 g of soil was = placed at the bottom of a dry 500 ml conical flask ðcorrected hydrometer reading after 2 h

(Corning/Pyrex). Then 10 ml of 1 N K2Cr2O7 was added oven dry weight of soilÞ100 (2) into the conical flask and swirled a little. The flask was Sand ðÞ% ¼ 100%ðÞsilt þ clay (3) kept on asbestos sheet. Then 20 ml of concentrated Silt ðÞ% ¼ %ðÞsilt þ clay %clay (4) H2SO4 was added into the conical flask and swirled again 2–3 times. The flask was allowed to stand for 30 min and thereafter 200 ml of distilled water was Toxic metal analysis added. After incorporation of 5.0 ml of phosphoric acid and 35 drops of diphenylamine indicator, the All chemicals were analytical grade. Milli-Q water (Elix contents were titrated against ferrous ammonium sul- UV5 and MilliQ, Millipore, Boston, MA) was used for fate solution till the color flashes blue-violet to green. the preparation of solutions. The Teflon vessel and Simultaneously, a blank titration was run without soil. polypropylene containers were cleaned, soaked in 5% Particle size was determined using the hydrometer HNO3 for more than 24 h, then rinsed with Milli-Q method. The textural classes for different soil samples water and dried. For metal analysis, 0.3–0.5 g of the were then determined by plotting the results on a soil sample was treated with 6 ml 69% HNO3 (Kanto 4 T. KORMOKER ET AL.

Chemical Co, Tokyo, Japan) and 2 ml 30% H2O2 (Wako given metal may be entirely from crustal materials or Chemical Co, Tokyo, Japan) in a closed Teflon vessel natural weathering processes (Zhang and Liu 2002). and was digested in a Microwave Digestion System Samples having EF >1.5 was considered indicative of (Berghof speedwave, Eningen, Germany). The digested human influence and (arbitrarily) an EF of 1.5–3, 3–5, samples were then transferred into a Teflon beaker, 5–10, and >10 is considered the evidence of minor, and total volume was made up to 50 ml with Milli-Q moderate, severe, and very severe modification, water. The digested solution was then filtered by respectively (Birch and Olmos 2008). using syringe filter (DISMIC1–25HP PTFE, pore size ¼ i 0.45 mm; Toyo Roshi Kaisha, Ltd., Tokyo, Japan) and Contamination factor (Cf ) stored in 50 ml polypropylene tubes (Nalgene, New The contamination factor means the proportion of the York, NY). After that, the digestion tubes were then heavy metal concentration in the soil to that of base- cleaned using blank digestion procedure following the line or background value: same procedure of samples. For toxic metals, samples f = were analyzed using inductively coupled plasma mass Ci ¼ Cheavy metal Cbackground (6) spectrometer (ICP-MS, Agilent 7700 series, Santa Clara, The contamination factor divided into four classes CA). Instrument operating conditions and parameters based on their intensities on a scale ranging from 1 to for metal analysis were done. The detection limits of 6: low degree (C i<1), moderate degree (1 C i<3), ICP-MS for the studied metals were 0.7, 0.6, 0.8, 0.4, f f considerable degree (3 C i<6), and very high degree 0.06, and 0.09 ng/L for Cr, Ni, Cu, As, Cd, and Pb, f (C i 6) (Islam et al. 2015c). This approach has been respectively. Multi-element Standard XSTC-13 (Spex f used by other researchers (Proshad et al. 2017). CertiPrepVR , Metuchen, NJ) solutions were used to pre- pare calibration curves. Multi-element solution (pur- Geoaccumulation index (I ) chased from Agilent Technologies, Japan) was used as geo tuning solution covering a wide range of masses of The degree of contamination from the trace metals elements. All test batches were evaluated using an could be assessed by determining the geoaccumula- internal quality approach and validated if they satis- tion index (Igeo) proposed by Muller (1969). The index fied the defined internal quality controls (IQCs). Before of geoaccumulation (Igeo) has been widely applied to starting the analysis sequence, relative standard devi- the assessment of soil contamination (Santos et al. ation (RSD, <5%) was checked using the tuning solu- 2003). To characterize the level of pollution in the soil, tion purchased from Agilent Technologies. The geoaccumulation index (Igeo) values were calculated certified reference materials INCT-CF-3 (corn flour) using the equation: bought from the National Research Council (Canada) Igeo ¼ log 2ðÞCn=1:5Bn (7) were analyzed to confirm analytical performance and good precision (relative standard deviation below where Cn is the measured concentration of metal n in 20%) of the applied method. the soil and Bn is the geochemical background value of element n in the background sample (Turekian and Wedepohl 1961, Rudnick and Gao 2003). The factor Ecological risk assessment for soil pollution 1.5 is introduced to minimize the possible variations in Enrichment factor the background values which may be attributed to lithogenic effects (Nikolaidis et al. 2010). EF is considered as an effective tool to evaluate the Geoaccumulation index (Igeo) values were interpreted magnitude of contaminants in the environment as follows: Igeo0, practically uncontaminated; (Franco-Uria et al. 2009). The EF for each element was 0 Igeo1, uncontaminated to moderately contami- calculated to evaluate anthropogenic influences on nated; 1 Igeo2, moderately contaminated; heavy metals in soils using the following formula 2 Igeo3, moderately to heavily contaminated; (Selvaraj et al. 2004): 3 Igeo4, heavily contaminated; 4 Igeo5, heavily = = = EF ¼ ðÞCM CAl sample ðÞCM CAl background (5) to extremely contaminated; and 5 < Igeo, extremely contaminated. where (CM/CAl)sample is the ratio of concentration of heavy metal (C ) to that of aluminum (C ) in the soil M Al Pollution load index sample, and (CM/CAl)background is the same reference ratio in the background sample (Islam et al. 2015a). To assess the quality of soil in terms of metal contam- Generally, an EF value of about 1 suggests that a ination, an integrated approach of PLI of the six TOXIN REVIEWS 5 metals was calculated according to Rashed (2010). The Health risk assessment from polluted soil PLI is defined as the nth root of the multiplications of Daily intake of heavy metals through exposure the contamination factor (C i) of metals (Bhuiyan et al. f pathway from soil 2011). Ingestion and dermal absorption of heavy metals from = i i i i 1 n polluted agricultural soils have great importance in PLI ¼ C f1 C f2 C f3 ... C fn (8) potential exposure pathways (Fryer et al. 2006, Qu et al. 2012). Out of several exposure pathways, The PLI gave an assessment of the overall toxicity ingestion of metals from soil is the most common status of the sample and also it is a result of the con- exposure pathway for Cr, Ni, Cu, As, Cd, and Pb tribution of the six metals. (Ordonez~ et al. 2011). CDI (mg/kg/day) of metals was determined from ingestion (CDI ) and dermal Potential ecological risk ingest-soil contact (CDIdermal-soil) in this study for both adult and The degrees of hazardous elements contamination in children were estimated using the following formulas: agricultural soils are determined by PER index. CSIRSEFED Ingestion from soil : CDI ¼ CF Guo et al. (2010) and Luo et al. (2007) proposed equa- ingestsoil BWAT tions which were used to calculate PER and are as (11) follows: Dermal contact from soil : CDIdermal-soil ¼ CS SA AF ABS IRS EF ED Xn CF (12) Ci BW AT Ci ¼ ; C ¼ Ci (9) f Ci d f Inhalation from soil : CDI n i¼1 inhalationsoil ¼ CS InhR EF ED CF (13) Xm BW AT i i i; i Er ¼ Tr Cf PER ¼ Er (10) where CDI¼chronic daily intake; CS¼exposure-point i¼1 concentration, mg/kg; IRS¼ingestion rate, 100 and 200mg d1 for adult and children (USEPA 2011); where Ci is the single element contamination factor, f EF¼exposure frequency, 350 d/a (USEPA 2011); Ci is the content of the element in samples, and Ci is n ED¼exposure duration, 30years for adult and 6years the background value of the element. The background for children (USEPA 2011); CF¼units conversion factor, value of Cr, Ni, Cu, As, Cd, and Pb in soils were 90, 68, 106kg mg1 (USEPA 2002); SA¼exposure skin area, 45, 13, 0.3, and 20 mg/kg, respectively (preindustrial 5700 and 1600cm2 for adult and children (USEPA samples of the study area) (Turekian and Wedepohl 2 2011); AF¼adherence factor, 0.07 and 0.02mg cm 1961). The sum of Ci for all metals represent the inte- f for adult and children (USEPA 2011); ABS¼dermal i grated pollution degree (Cd) of the environment. Er is absorption fraction, 0.01 for adult and 0.001 for chil- i the PER index and Tr is the biological toxic factor of dren (USEPA 2011); BW¼body weight, 70kg for adult an individual element. The toxic-response factors for male, 65kg for adult female, and 15kg for children Cr, Ni, Cu, As, Cd, and Pb were 2, 6, 5, 10, 30, and 5, (USEPA 2001); AT¼averaging time for noncarcinogens, respectively (Håkanson 1980, Gong et al. 2008, 365 ED (USEPA 2002); InhR¼inhalation rate 20 m3/d Wu et al. 2010, Guo et al. 2010, Jintao et al. 2011, for both adult and child (USEPA 1997). Amuno 2013). PER is the comprehensive PER index, i: which is the sum of Er Hazard quotient (HQ)

Toxic unit analysis The noncarcinogenic risks for each individual heavy metal (Cr, Ni, Cu, As, Cd, and Pb) through ingestion, The sum of toxic units (RTUs) is considered as poten- dermal, and inhalation were assessed by the THQ tial acute toxicity of hazardous elements in agricultural (USEPA 1989). The methodology for the estimation of soil samples. Toxic unit analysis is stated as the ratio non-carcinogenic risks was applied in accordance with of the assessed concentration of hazardous elements that provided by the U.S. Environmental Protection in soil to probable effect level (PELs) (Zheng et al. Agency (USEPA) Region III’s risk-based concentration 2008). A moderate to serious toxicity of hazardous ele- table (USEPA 2011). Hazard quotient (HQ) was deter- ments remain in soil when the sum of toxic units for mined on the basis of CDI from ingestion (CDIingest), all soil samples is more than 4 (Bai et al. 2011). dermal (CDIdermal), and inhalation (CDIinhalation), it was 6 T. KORMOKER ET AL. calculated by dividing the average daily dose to a spe- Carcinogenic risk cific reference dose (RfD) (USEPA 1989). The equation Carcinogenic risk is considered as the probability of an used for estimating the THQ is as follows: individual developing any type of cancer in the whole HQingest ¼ ðÞCDIingest =RfD (14) lifetime due to exposure to carcinogenic hazards (Li et al. 2014). Carcinogenic risk expressed as the total HQdermal ¼ ðÞCDIdermal =RfD (15) cancer risk (Eq. 23). HQinhalation ¼ ðÞCDIinhalation =RfD (16) CRingest-soil ¼ ðÞCS AF IngR EF ED =ðÞBW AT where THQ is the target hazard quotient, CDI is the CF CSFingest (20) chronic daily intake of heavy metal (mg/kg), and RfD CRdermal-soil ¼ ðÞCS SA AF ABSd EF ED = is the reference dose (mg/kg/day). The RfD for Cr, Ni, ðÞBW AT gCF CSF ABS (21) Cu, As, Cd, and Pb were 0.003, 0.02, 0.04, 0.0003, ingest GI 0.0005, and 0.0035 mg/kg/day, respectively (USEPA CRinhalationsoil ¼ ðÞCS ET EF ED = 2002, USDOE 2011). The reference dose (RfD) (mg/kg/ ðÞPEF 24 AT gIUR 103 (22) day) is an estimation of maximum permissible risk on Total cancer risk ¼ Riskingestion þ Riskdermal þ Riskinhalation human population through daily exposure, taking into (23) consideration sensitive group (children) during the life- where CR is the cancer risk of metals from time. If the CDI is higher than RfD (HQ > 1), there will ingest-soil ingestion of soil; CR , the cancer risk of metals be a severe health hazard to human, whereas CDI is dermal-soil from dermal contact of soil; CS, the heavy metal con- less than RfD (HQ 1), there will be no severe human centration in soil, mg/kg; AF, soil-to-skin adherence health effects (USEPA 1989, 2001). The health risk factor, 0.7 mg/cm2 for adult and 0.2 mg/cm2 for chil- guidelines determination of chemical mixtures defined dren (USEPA 2011); IngR, ingestion rate of soil, 100 that “simultaneous sub-threshold exposures to several and 200 mg d1 for adult and children, respectively ” chemicals may result in an adverse health effect and (USEPA 2011); EF, exposure frequency, 350 days/year “ the magnitude of the adverse effect will be propor- (USEPA 2011); ED, exposure duration, 30 years for adult tional to the sum of the ratios of the sub-threshold and 6 years for children (USEPA 2011); BW, body ” exposures to acceptable exposures (USEPA 1986). weight, 70 kg for adult male, 65 kg for adult female, Again, HI can be generated from the HQ to calculate and 15 kg for children; AT, averaging time for noncar- the combined risk of individual heavy metals in the cinogens, 365 ED (USEPA 2011); CF, units conversion 6 form of mix contaminates (USEPA 1989). factor, 10 kg/mg (USEPA 2002); CSFingest, chronic oral slope factor, 1.5 for As and 8.5 103 for Pb (USEPA Hazard index (HI) 2011, USDOE 2011); SA, exposure skin surface area 2 2 To assess the overall potential for noncarcinogenic available for contact, 5700 cm for adult and 1600 cm for children (USEPA 2011); ABS , dermal absorption effects from more than one heavy metal, a HI has d fraction, 0.01 for adult and 0.001 for children (USEPA been formulated based on the guidelines for health 2011); ET, exposure time, 1 for residents for the site risk assessment of chemical mixtures (USEPA 1999). specific (USDOE 2011); ABS , gastrointestinal absorp- The HI from THQs is expressed as the sum of the HQs GI tion factor, 0.41 and 1 for As and Pb, respectively (USEPA 2011). The equation used for estimating the HI (USEPA 2011); PEF, particle emission factor, 1.36 109 is as follows: (USDOE 2011, USEPA 2011); IUR, chronic inhalation 3 5 HI ¼ RTHQn unit risk, 4.30 10 for As, 1.20 10 for adult (17) (USDOE 2011). In this study, we calculated carcinogenic risk for ¼ THQelement 1 þ THQelement 2 þ ...... :þ arsenic and lead as they are classified as probably car- THQelements n (18) cinogenic to humans (ATSDR 2007, 2012). The excess 6 HI ¼ RTHQ ¼ HQingest þ HQdermal þ HQinhalation (19) cancer risks lower than 10 (a probability of 1 chance in 1,000,000 of an individual developing cancer) are The guidelines also state that any single metal with considered to be negligible, cancer risks above 104 an exposure level greater than the toxicity value will are considered unacceptable by most international cause the HI to exceed unity; for multiple metal expo- regulatory agencies (USEPA 1989, Guney et al. 2010), sures, the HI can also exceed unity even if no single and risks lying between 106 and 104 are generally metal exposure exceeds its RfD. considered an acceptable range, depending on the TOXIN REVIEWS 7 situation and circumstances of exposure (Hu et al. alkaline conditions and low pH also may lead to met- 2012). The value 106 is also considered the carcino- als becoming unavailable to plants and therefore, less genic target risk by USEPA (2011). likely to be incorporated in plant tissues (Loska et al. 2005). According to Soil Resources Development Statistical analysis Institute (SRDI) soil salinity class, electrical conductivity (EC) value of the studied soil was nonsaline The data were statistically analyzed using the statis- (0–2 dS/m) for all sampling sites which mean the salin- tical package, SPSS 20.0 (SPSS, USA). The means of the ity effect is negligible. The percentage of organic car- hazardous element concentrations in soils were calcu- bon in soils ranged from 0.17 to 5.41, 0.67 to 3.89, lated. Multivariate methods in terms of principal com- 0.52 to 1.55, and 0.55 to 4.59 at Porahati, Udoipur, ponent analysis (PCA) were used to interpret the Lokhikol, and Dhanharia sites of , potential sources of toxic metals in soil (Liang et al. respectively, and 0.21 to 4.55 at Chourhas site of 2015). A Pearson bivariate correlation was used to (Table 1). The highest mean percent- evaluate the interelement relationship in soil. Other age value of organic carbon was observed in soil that calculations were performed by Microsoft Excel 2013. collected from the Porahati site (1.87) and the lowest value observed in the Lokhikol site (1.22). High organic Results and discussion carbon content is an indication that metals are more likely to be bound to organic matter to form metal che- Physiochemical properties of soil late complexes, and this would also result in less avail- The physicochemical properties of soil in the study ability of metals to plants (Yap et al. 2009,Islamet al. sites are presented in Table 1. The mean values of soil 2014). According to the USDA soil texture classification, pH were obtained 7.41, 7.69, 8.45, 8.01, and 8.04 at the textural analysis revealed that the studied soil silt Porahati, Udoipur, Lokhikol, Dhanharia, and Chourhas, and silty loam among the sites of the study area. respectively. The studied soils were slightly acidic to alkaline in nature which can be due to the decompos- Toxic metal concentration in soil samples ition of organic matter and subsequent formation of carbonic acid (Islam et al. 2014). Higher soil acidity The concentration of total toxic metals (Cr, Ni, Cu, As, (lower pH values) favors the availability of cations in Cd, and Pb) in soil samples are presented in (Table 2). soil. Many metal complexes are insoluble under The mean concentration of Cr, Ni, Cu, As, Cd, and Pb

Table 1. Physicochemical properties of soil collected from industrial areas of Jhenaidah and Kushtia districts, Bangladesh. Sampling sites pH EC (dS/m) OC (%) OM (%) Sand (%) Silt (%) Clay (%) Textural class Porahati, Jhenaidah (n ¼ 9) Mean ± SD 7.41 ± 0.69 0.23 ± 0.14 1.87 ± 1.76 3.23 ± 3.04 39.88 ± 10.53 42.16 ± 8.82 18.00 ± 5.52 Silty loam Range 5.80–8.06 0.11–0.48 0.17–5.41 0.29–9.35 24.20–61.00 26.60–54.10 12.40–26.70 Udoipur, Jhenaidah (n ¼ 13) Mean ± SD 7.69 ± 0.36 0.14 ± 0.05 1.59 ± 1.11 2.75 ± 1.92 25.56 ± 3.89 55.80 ± 2.60 18.64 ± 2.84 Silt Range 7.11–8.15 0.08–0.24 0.67–3.89 1.15–6.72 19.20–33.50 51.60–59.10 12.40–24.20 Lokhikol, Jhenaidah (n ¼ 9) Mean ± SD 8.45 ± 0.14 0.26 ± 0.13 1.22 ± 0.36 2.11 ± 0.62 31.83 ± 10.49 47.72 ± 8.75 20.44 ± 8.37 Silty loam Range 8.28–8.65 0.16–0.51 0.52–1.55 0.89–2.68 16.90–48.50 39.10–64.10 12.40–41.60 Dhanharia, Jhenaidah (n ¼ 13) Mean ± SD 8.01 ± 0.37 0.24 ± 0.06 1.56 ± 1.23 2.69 ± 2.12 27.82 ± 4.87 52.97 ± 4.90 18.65 ± 3.45 Silty loam Range 7.04–8.40 0.15–0.35 0.55–4.59 0.95–7.94 17.60–34.40 41.90–61.60 12.40–26.70 Chourhas, Kushtia (n ¼ 14) Mean ± SD 8.04 ± 0.30 0.29 ± 0.18 1.59 ± 1.18 2.75 ± 2.04 38.49 ± 13.68 43.76 ± 11.06 17.79 ± 4.73 Silty loam Range 7.60–8.50 0.14–0.85 0.21–4.55 0.36–7.87 25.50–64.50 21.60–56.60 11.50–25.80

Table 2. Concentration of toxic metals in soils (mg/kg dw) collected from industrial areas of Jhenaidah and Kushtia dis- tricts, Bangladesh. Sampling sites Cr Ni Cu As Cd Pb Porahati, Jhenaidah (n ¼ 9) Mean ± SD 18.88 ± 4.30 9.22 ± 5.67 18.50 ± 16.99 8.01 ± 6.93 1.00 ± 0.76 4.43 ± 3.26 Range 9.32–23.03 3.78–19.55 2.00–52.54 1.78–21.89 0.41–2.88 1.15–9.56 Udoipur, Jhenaidah (n ¼ 13) Mean ± SD 1.94 ± 1.68 31.21 ± 24.64 27.75 ± 25.79 5.45 ± 4.91 1.11 ± 1.15 18.66 ± 22.01 Range 0.08–6.05 2.66–77.32 4.72–98.19 1.28–16.20 0.13–3.39 1.22–70.11 Lokhikol, Jhenaidah (n ¼ 9) Mean ± SD 6.39 ± 3.89 38.12 ± 24.38 66.91 ± 28.35 13.58 ± 6.20 2.40 ± 2.31 36.70 ± 30.57 Range 2.34–14.85 9.07–72.85 24.84–101.9 4.80–21.54 0.49–7.51 14.31–114.7 Dhanharia, Jhenaidah (n ¼ 13) Mean ± SD 5.12 ± 4.47 16.91 ± 10.08 38.05 ± 41.62 10.20 ± 5.70 1.24 ± 0.81 24.57 ± 10.38 Range 1.22–17.53 3.49–34.24 4.64–122.9 1.52–23.38 0.22–2.85 8.01–52.16 Chourhas, Kushtia (n ¼ 14) Mean ± SD 1.13 ± 0.48 11.82 ± 14.61 15.70 ± 21.07 4.92 ± 3.35 0.60 ± 0.49 13.13 ± 7.20 Range 0.24–1.66 1.02–54.46 0.99–64.19 1.47–12.49 0.13–1.65 1.86–24.41 8 T. KORMOKER ET AL.

Table 3. Comparison of metal concentration (mg/kg) [mean (range)] in soils of this study with other studies and guide- line values. District (country) Cr Ni Cu As Cd Pb References Jhenaidah and 5.78 (0.08–23.0) 21.0 (1.02–77.3) 31.8 (0.99–123) 8.05 (1.28–23.4) 1.20 (0.13–7.5) 19.2 (1.15–115) This study Kushtia, Bangladesh Tangail 8.31 16.49 20.64 5.06 2.2 16.9 Proshad (Bangladesh) et al. 2018b 384 (158–1160) 192 (104–443) 311 (157–519) 64 (41–93) 7.1 (3.9–13) 199 (84–574) Islam et al. 2014 (Bangladesh) Noakhali 29 (18–46) 64 (37–93) 22 (13–63) 3.3 (1.5–9.2) 0.07 (0.03–0.2) 13 (8–22) Rahman (Bangladesh) et al. 2012 Dhaka 54 (34–68) 58 (36–74) 39 (31–45) NA 11 (6–16) 50 (44–52) Ahmad and (Bangladesh) Goni 2010 Guandong (China) 12.3 (9.66–19) 8.83 (7.04–10.3) 324 (210–450) NA 0.9 (0.26–1.17) 96 (73–134) Luo et al. 2011 Maharashtra 164 (66–279) 171 (69–465) 155 (52–373) 2.8 (NA–11.2) 30 (22–39) 42 (36–49) Bhagure and (India) Mirgane 2011 Murcia (Spain) 18 (10–60) 14 (5.1–31) 11 (3.8–65) NA 0.22 (0.06–1.1) 49 (11–674) Acosta et al. 2011 Kayseri (Turkey) 29 (17–81) 45 (16–217) 37 (12–144) NA 2.5 (0.98–15) 75 (28–312) Tokalıoglu and Kartal 2006 Dutch soil quality 100 35 36 29 0.8 85 VROM 2000 standard (target value) Dutch soil quality 380 210 190 55 12 530 VROM 2000 standard (intervention value) Canadian 64 50 63 12 1.4 70 CCME 2003 environmental quality guidelines Department of 50 60 60 20 3 300 DEP 2003 Environmental Protection, Australia

in soils at different sampling sites were found 5.78, Kartal 2006, Ahmad and Goni 2010, Acosta et al. 2011, 21.0, 31.8, 8.05, 1.20, and 19.2 mg/kg, respectively. Bhagure and Mirgane 2011, Luo et al. 2011, Rahman Chromium is a toxic heavy metal is discharged et al. 2012, Islam et al. 2014, Proshad et al. 2018b) from several industries into the agricultural land (Table 3). around industrial areas and pollutes agricultural soils The solubility of nickel in soils increases with its (Nriagu 1988). The concentration of Cr in agricultural acidity and if the acidity increases it results higher Ni soils varies up to values as high as 350 mg kg1 in soils (Baralkiewicz and Siepak 1999). Nickel can (Branca et al. 1990). The toxicity of Cr has negative cause dermatitis, lung fibrosis, cardiovascular, and kid- impacts on the growth of plants that interfere with ney diseases and cancer of the respiratory tract in the some important metabolic processes (Shaker et al. human body (Hasnine et al. 2017). In this study, Ni 2009, Hasnine et al. 2017). In this study, the highest concentrations ranged between 1.02 and 77.32 mg/kg mean concentration of Cr (18.88 mg/kg) was observed in the study area. The highest concentration at Porahati site. Chromium concentration was found in (77.32 mg/kg) was found at Udoipur and the lowest the study areas may be disposed of untreated tannery value (1.02 mg/kg) at Chourhas (Table 2). The elevated waste to agricultural fields since chromium salt used levels of Ni were found in this study which results in tannery industries (Srinivasa et al. 2010). The mean from localized additions or accidental spillages of Ni concentration of Cr was found 5.78 mg/kg in this containing materials (Govil et al. 1998, Krishna and study which was lower than the Dutch Soil Quality Govil 2007). The mean concentration of Ni was found Standard (VROM 2000), Canadian Environmental 21.0 mg/kg in this study which was lower than the Quality Guidelines (CCME 2003), and Australian Dutch Soil Quality Standard (VROM 2000), Canadian Guideline for Soil Quality (DEP 2003). Chromium con- Environmental Quality Guidelines (CCME 2003), and centration in soils of this study were also compared to Australian Guideline for Soil Quality (DEP 2003). Nickel other study conducted in Bangladesh and other coun- concentration in soils of this study were also com- tries and found that Cr concentration in this study pared to the other study conducted in Bangladesh was lower than the other studies (Tokalıoglu and and other countries and found that Ni concentration TOXIN REVIEWS 9

Table 4. Correlation coefficient matrix for physiochemical properties and toxic metals in soils collected from Kushtia and Jhenaidah districts, Bangladesh. pH EC Sand Silt Clay OM Cr Ni Cu As Cd Pb pH 1 EC 0.057 1 Sand 0.110 0.622 1 Silt 0.695 0.098 0.785 1 Clay 0.641 0.872 0.047 0.030 1 OM 0.130 0.009 0.215 0.052 0.142 1 Cr 0.116 0.102 0.123 0.140 0.129 0.194 1 Ni 0.082 0.103 0.250 0.043 0.110 0.174 0.026 1 Cu 0.174 0.079 0.040 0.052 0.134 0.097 0.443 0.166 1 AS 0.123 0.160 0.244 0.116 0.173 0.002 0.018 0.016 0.248 1 Cd 0.023 0.001 0.069 0.071 0.082 0.199 0.176 0.723 0.161 0.015 1 Pb 0.185 0.555 0.476 0.597 0.548 0.478 0.052 0.004 0.209 0.087 0.013 1 Correlation is significant at the 0.05 level (two-tailed). Correlation is significant at the 0.01 level (two-tailed). in this study was higher than the other studies (Luo and incineration activities might contribute to the et al. 2011, Acosta et al. 2011, Proshad et al. 2018b) high concentration of As in agricultural soil (Olawoyin (Table 3). et al. 2012). The mean concentration of As was found Soluble soil Cu can be toxic to plants since Cu- 8.05 mg/kg in this study which was lower than the enriched liquid dairy waste used in agricultural land as Dutch Soil Quality Standard (VROM 2000), Canadian irrigation water (White and Brown 2010). Excessive Cu Environmental Quality Guidelines (CCME 2003), and concentrations are harmful to plants and highly toxic Australian Guideline for Soil Quality (DEP 2003). to some microorganisms (Hasnine et al. 2017). In this Arsenic concentration in soils of this study were also study, the value of Cu ranged between 0.99 and compared to other study conducted in Bangladesh 122.9 mg/kg (Table 2). The elevated concentration of and other countries and found that As concentration Cu was observed in soil at Lokhikol site which can be in this study was higher than the other studies due to the emission of Cu from the uncontrolled (Bhagure and Mirgane 2011, Rahman et al. 2012, industrial and waste burning activities (Srinivasa et al. Proshad et al. 2018b)(Table 3). Frank et al.(1976) esti- 2010, Luo et al. 2011). The mean concentration of Cu mated 6.21 ± 2.67 mg/kg As in agricultural soils of was found 31.8 mg/kg in this study which was lower Ontario while Yu et al. (2008) recorded 8.80 mg/kg As than the Dutch Soil Quality Standard (VROM 2000), in arid agricultural soil in central Gansu Province, Canadian Environmental Quality Guidelines (CCME China. The threshold value for As is 20 mg/kg for 2003), and Australian Guideline for Soil Quality (DEP arid agricultural soils in China (NEPA 1995). 2003) indicating lower contamination of Cu in soil Cadmium concentrations were ranged from 0.13 to (Table 3). Yu et al. (2008) found 17.10 mg/kg Cu in arid 7.51 mg/kg (Table 2). The highest concentration of Cd agricultural soil in central Gansu Province, China. The (2.40 mg/kg) was observed at Lokhikol site. Higher Cd threshold value for Cu is 60 mg/kg for arid agricul- concentration in soils might be related to industrial tural soils in China (NEPA 1995). Hasnine et al.(2017) activity, metal processing, atmospheric emission, and reported average Cu concentration in the surface agri- Cd plated items (Proshad et al. 2019). The mean con- cultural soil at DEPZA was found to be centration of Cd was found 1.20 mg/kg in this study 91.06 ± 152.70 mg/kg. which was higher than The Dutch Soil Quality Arsenic is called “slow poison” or death metal Standard (VROM 2000) and lower than Canadian because it kills people slowly whenever it enters into Environmental Quality Guidelines (CCME 2003) and the human body (Nawab et al. 2017). In this study, Australian Guideline for Soil Quality (DEP 2003). The the concentration of As ranged from 1.28 to Dutch soil quality standard is considered the most 23.38 mg/kg (Table 2). The highest concentration of As suitable guideline indicating all possible exposure (13.58 mg/kg) was observed at Lokhikol site. In gen- pathways for protecting humans, plants, and animals eral, the arsenic in agricultural soils can be derived (Proshad et al. 2017). The soil is considered clean if from both natural and anthropogenic sources, espe- any heavy metal concentration in soil is below its cially use of arsenic contaminated groundwater for irri- respective Dutch Target Value. The soil is regarded to gation and uncontrolled application of As enriched be slightly to moderately contaminated if the concen- fertilizers and pesticides (Renner 2004, Neumann et al. tration level lies between the target values and inter- 2011). Moreover, emission and waste from brick fields vention values. In contrast, if the value is above the 10 T. KORMOKER ET AL.

Table 5. Total variance explained and component matrices for the toxic metals in soils collected from Jhenaidah and Kushtia districts, Bangladesh. Initial eigenvalues Extraction sums of squared loadings Rotation sums of squared loadings Component Total % of variance Cumulative % Total % of variance Cumulative % Total % of variance Cumulative % 1 3.1 51.7 51.7 3.1 51.6 51.7 2.4 40.1 40.1 2 1.3 21.1 72.7 1.3 21.1 72.7 1.6 26.1 66.2 3 0.64 10.7 83.4 0.64 10.7 83.4 1.0 17.2 83.4 4 0.48 8.1 91.5 5 0.36 6.0 97.5 6 0.15 2.5 100 Component matrix Rotated component matrix Elements PC1 PC2 PC3 PC1 PC2 PC3 Cr 0.007 0.871 0.479 0.01 0.87 0.479 Ni 0.76 0.326 0.22 0.76 0.33 0.22 Cu 0.86 0.169 0.31 0.86 0.17 0.31 As 0.83 0.39 0.153 0.83 0.387 0.153 Cd 0.84 0.09 0.10 0.84 0.09 0.10 Pb 0.63 0.46 0.486 0.63 0.46 0.49

Dutch Intervention Value, the soil is considered detri- from industrial vicinity of Jheanaidah and Kushtia dis- mental to humans, plants, and animals. About 80% of tricts. The value of pH showed significant positive cor- the studied soil samples exceeded the Dutch target relation with silt (r ¼ 0.695) and significant negative value assuming that Cd in soil might pose a severe correlation with clay (r¼0.641). Similarly, EC risk to the surrounding ecosystems. showed significant positive correlation with sand The highest concentration of Pb (41.60) mg/kg) was (r ¼ 0.622) and Pb (r ¼ 0.555) and significant nega- observed at Lokhikol site. The higher level of Pb con- tive correlation with clay (r¼0.872). Sand showed centration present in soils due to metal processing significant positive correlation with Pb (r ¼ 0.476) factories release Pb into the open environment and and significant negative correlation with silt several anthropogenic factors (Karim et al. 2008, (r¼0.785). Silt showed significant positive correl- Nziguheba and Smolders 2008). In this study, Lokhikol ation with Pb (r ¼ 0.597). Clay showed significant site showed the elevated concentrations of Pb which positive correlation with Pb (r ¼ 0.548). Organic mat- can be due to the release of Pb contaminated waste ter showed significant positive correlation with Pb from this area (Srinivasa et al. 2010). The mean con- (r ¼ 0.478). Cr showed significant positive correlation centration of Pb was found 19.20 mg/kg in this study with Cu (r ¼ 0.443), Ni showed significant positive which was lower than the Dutch Soil Quality Standard correlation with Cd (r ¼ 0.723). On the other hand, (VROM 2000), Canadian Environmental Quality considering the relationship between the combina- Guidelines (CCME 2003), and Australian Guideline for tions showed positive significant relationship which Soil Quality (DEP 2003) indicating lower contamination indicates the parameters were interrelated with each of Pb in soil (Table 3). Lead concentration in soils of other and may be originated from the same source to this study were also compared to other study con- the study area. Other relationships among the constit- ducted in Bangladesh and other countries and found uents of soil were not significant. that Pb concentration in this study was lower than the PCA has commonly been used for investigating other studies (Tokalıoglu and Kartal 2006, Ahmad and metal sources, anthropogenic activities, or soil parent Goni 2010, Acosta et al. 2011, Bhagure and Mirgane materials (Bai et al. 2011, Anju and Banerjee 2012, 2011, Luo et al. 2011, Islam et al. 2014) and higher Cai et al. 2012). Three principal components were than Rahman et al. (2012) and Proshad et al. (2018b) obtained (Table 5 and Figure 2), and those accounted (Table 3). for 83.4% total variation. In the PCA analysis, first three components were computed and the variances explained by them were 51.7%, 21.1%, and 10.7% for Source analysis of toxic metals soil. Overall, PCA revealed three major groups of the Pearson’s correlation coefficients for the investigated metals for soil. One group comprised of Ni and Pb in metals are depicted in Table 4. Intermetal interactions soil which were predominantly contributed by illustrate the sources and pathways of the metals pre- anthropogenic activities. Second group showed sent in soil. The results highlighted close association mutual association of As, Cd, and Cu in soil which among correlation coefficient matrix for physiochem- were mostly contributed by industrial emissions in the ical properties and heavy metals in soils collected vicinity of the sampling sites (Manzoor et al. 2006). TOXIN REVIEWS 11

Figure 2. Principal component analysis (PCA) of toxic metals in soils collected from different agricultural fields of Jhenaidah and Kushtia districts, Bangladesh.

Third group revealed similar loadings of Cr in soil indi- Table 6. Enrichment factor (EF) of toxic metals in soils col- cated that these were mostly contributed by litho- lected from Jhenaidah and Kushtia districts, Bangladesh. genic sources. The depositions of atmospheric Sampling location Cr Ni Cu As Cd Pb particulates released by automobile emissions were Porahati, Jhenaidah Mean 0.235 0.132 0.314 0.473 0.589 0.092 SD 0.053 0.081 0.288 0.409 0.447 0.067 believed to contribute these metals in the urban areas Udoipur, Jhenaidah Mean 0.058 1.067 1.109 0.791 1.379 0.808 from where the soil samples were collected (Cui et al. SD 0.076 1.229 1.516 0.995 1.750 0.979 Lokhikol, Jhenaidah Mean 0.166 1.140 2.251 1.559 2.698 1.695 2004, Manzoor et al. 2006, Pandey et al. 2012). PCA SD 0.129 0.772 0.924 0.621 2.333 1.772 analysis revealed that the apportionment of same kind Dhanharia, Jhenaidah Mean 0.055 0.210 0.583 0.521 0.647 0.440 SD 0.047 0.134 0.701 0.341 0.540 0.173 of toxic metals in soil were not similar, which might Chourhas, Kushtia Mean 0.018 0.206 0.315 0.388 0.481 0.366 be due to the emission behavior of toxic metals from SD 0.010 0.225 0.408 0.319 0.431 0.247 the source to environment.

soils indicated higher strong human influence from Ecological risk assessment industrial pollution (Rashed 2010). i Ecological risk assessment for heavy metals contamin- The contamination factor (Cf ), degree of contamin- i ation in soil was performed following the method- ation (Cd), ecological risk (E r), and risk index (RI) ology developed by Håkanson (1980). In this study, EF, classes are shown in Table 7. The contamination factor contamination factor (CF), degree of contaminations (CF) for individual metal and degree of contamination

(Cd), PLI, PER, and toxic units analysis have been (Cd) are presented in Table 8. Porahati and Lokhikol applied to assess the contamination of toxic metals in sites showed higher contamination of Cr and Ni. agricultural soils near the industrial areas of Jhenaidah Lokhikol site also showed higher contamination of Cu, and Kushtia districts, Bangladesh. As, Cd, and Pb. Among the sampling sites, about most The EF is a normalization technique that is being of the samples showed very high contamination for widely used to categorize the metal fractions that is Cd concentration in soil, indicating that this metal associated with soils (Proshad et al. 2019). The calcu- might pose a potential risk to the surrounding ecosys- lated values of EF of toxic metals are presented in tems (Rashed 2010) which ultimately would degrade i Table 6. The highest EF value was found in Cd (2.69) the ecological balance. Overall, the Cf for all metals and the lowest EF value was found in Cr (0.018). were in the descending order of Among the sites, the descending order of EFs was as Cd > As > Cu > Pb > Ni > Cr. The assessment of the Lokhikol > Udoipur > Dhanharia > Porahati > Chourhas. overall contamination of soil was based on the degree As a whole, the EF of all the studied metals for all of contamination (Cd). The degree of contamination of sampling sites were in the descending order of toxic metals were 4.92, 6.14, 12.98, and 7.31 in Cd > Cu > As > Pb > Ni > Cr. The higher EF of Cd in Porahati, Udoipur, Lokhikol, and Dhanharia in 12 T. KORMOKER ET AL.

Table 7. Indices and grades of potential ecological risk of toxic metal pollution (Luo et al. 2007). Contamination Contamination Grade of Contamination degree of Degree of degree of the ecological risk of Ci Ei factor ( f ) individual metal contamination (Cd) environment r individual metal Risk index (PER) Ci< < Ei< < f 1 Low Cd 5 Low contamination r 40 Low risk RI 65 Low risk Ci< < Ei< < 1 f 3 Moderate 5Cd 10 Moderate 40 r 80 Moderate risk 65 RI 130 Moderate risk contamination Ci< < Ei< < 3 f 6 Considerable 10Cd 20 Considerable 80 r 160 Considerable risk 130 RI 260 Considerable risk contamination Ci Ei< f 6 High Cd20 High 160 r 320 High risk RI 260 Very high risk contamination Ei r320 Very high risk

Table 8. Contamination factor, degree of contamination, and contamination level of toxic metals in soils collected from Jhenaidah and Kushtia districts, Bangladesh. Contamination factor (CF) Sampling sites Cr Ni Cu As Cd Pb Degree of contamination Contamination level Porahati, Jhenaidah 0.21 0.14 0.41 0.62 3.33 0.22 4.92 Low Udoipur, Jhenaidah 0.02 0.46 0.62 0.42 3.69 0.93 6.14 Moderate Lokhikol, Jhenaidah 0.07 0.56 1.49 1.04 7.98 1.84 12.98 Considerable Dhanharia, Jhenaidah 0.06 0.25 0.85 0.78 4.15 1.23 7.31 Moderate Chourhas, Kustia 0.01 0.17 0.35 0.38 2.02 0.66 3.59 Low

Table 9. Geoaccumulation index (Igeo) of toxic metals in soils collected from different areas of Jhenaidah and Kushtia dis- tricts, Bangladesh. Porahati, Jhenaidah Udoipur, Jhenaidah Lokhikol, Jhenaidah Dhanharia, Jhenaidah Chourhas, Kushtia Cr 2.84 6.12 4.40 4.72 6.90 Ni 2.93 1.18 0.89 2.06 2.58 Cu 1.18 0.60 0.67 0.14 1.42 As 0.09 0.46 0.86 0.44 0.61 Cd 2.89 3.03 4.15 3.20 2.16 Pb 2.52 0.45 0.53 0.05 0.96

Jhenaidah district, respectively, and 3.59 in Chourhas Figure 3. The PLI values were found 0.42, 0.45, 0.98, in Kushtia district. The degree of contamination 0.60, and 0.27, respectively, for Porahati, Udoipur, showed low to considerable level of contamination. Lokhikol, Dhanharia, and Chourhas sites. It was shown

The geoaccumulation index (Igeo) values of the in the above figure that the contamination of PLI was studied metals are presented in Table 9. Among the low but with the increasing number of industries in studied metals, the Igeo values showed the decreasing the industrial areas may cause progressive deterior- order of Cd > As > Cu > Pb > Cr > Ni at Porahati site; ation of soils and PLI value will be increased (Bhuiyan Cd > As > Pb > Cu > Ni > Cr at Dhanharia and et al. 2010). Chourhas sites; Cd > Pb > As > Cu > Ni > Cr at Udoipur PER represents the sensitivity of the biological com- site; and Cd > As > Cu > Pb > Ni > Cr at Lokhikol site. It munity to the toxic substance and illustrates the PER was showed in the table that Cd was heavily contami- caused by the overall contamination (Proshad et al. nated to extremely contaminated among the three 2019). Combining the PER index of individual metals i sites. The highest values of Cd might be due to contri- (E r) and the PER index of the environment (PER) with butions from atmospheric emission, leachates from their grade classifications (Table 7) (Luo et al. 2007), defuzed batteries, and Cd-plated items (Islam et al. soils from industrial vicinity were classified consider- 2015c, Proshad et al. 2019). Others toxic metals were able to very high PER with Cd and low PER with Cr, uncontaminated. Ni, Cu, As, and Pb (Table 10). Cd contributes signifi- PLI value equal to zero indicates perfection; a value cantly to the PER index of the environment (PER) of one indicates the presence of only baseline level of which can be due to the effect from anthropogenic pollutants and values above one indicate progressive activities such as application of phosphate fertilizers deterioration of soil in terms of contamination of the and industrial activities (ATSDR 2008, Islam et al. i toxic metals (Tomilson et al. 1980, Rashed 2010, Islam 2015c). The order of E r in soils was in the following et al. 2015a). The PLI of soils in industrial vicinity of descending order of Cd > As > Pb > Cu > Ni > Cr. Jhenaidah and Kushtia district are presented in The PER of the different sampling sites can be ranked TOXIN REVIEWS 13

1.2

1

0.8

0.6

0.4

0.2

Pollution load index value 0 Porahati Udoipur Lokhikol Dhanharia Chourhas Sampling location Figure 3. Pollution load index (PLI) of toxic metals in soils collected from Jhenaidah and Kushtia districts, Bangladesh.

Table 10. Potential ecological risk factor, risk index, and pollution degree of toxic metals in soils collected from Jhenaidah and Kushtia districts, Bangladesh. Ei Potential ecological risk factor ( r) Sampling sites Cr Ni Cu As Cd Pb Potential risk (PER) Pollution degree Porahati, Jhenaidah (n ¼ 9) 0.42 0.81 2.1 6.2 99.8 1.1 110 Moderate Udoipur, Jhenaidah (n ¼ 13) 0.04 2.8 3.1 4.2 110.6 4.7 125 Moderate Lokhikol, Jhenaidah (n ¼ 9) 0.14 3.4 7.4 10.4 239.5 9.2 270 Very high Dhanharia, Jhenaidah (n ¼ 13) 0.11 1.5 4.2 7.8 124.4 6.1 144 Considerable Chourhas, Kustia (n ¼ 14) 0.03 1.04 1.74 3.8 60.5 3.3 70 Moderate

4 Cr Ni Cu As Cd Pb 3.5

3

2.5

2

1.5

1 Toxic unit values Toxic 0.5

0 Porahati Udoipur Lokhikol Dhanharia Chourhas Sampling sites Figure 4. Toxic unit (TU) analysis of toxic metals in soils collected from Jhenaidah and Kushtia districts, Bangladesh. in the following order: Lokhikol, Dhanharia, and Chourhas sites, the toxic Lokhikol > Dhanharia > Uoipur > Porahati > Chourhas. units were 1.364, 1.871, 3.356, 1.945, and 1.026, In Lokhikol site, potential risk value was 270 and the respectively. The sum of toxic units for all the sam- degree of pollution was very high. In Porahati, pling sites was <4, indicating low toxicity of metals. Udoipur, and Chourhas sites, PER values were 110, 125, and 70, respectively, and degree of pollution was Health risk assessment moderate. In Dhanharia, potential risk value was 144 and the degree of pollution was considerable. Heavy metals present in soils may have an impact on Potential acute toxicity of hazardous elements in human health (Okorie et al. 2011). In the industrial soil samples can be estimated as the sum of toxic areas, the risks of toxic elements in industrial, waste units (RTUs), defined as the ratio of the determined burning sites, waste thronging sites and brick fields concentration of metal in soil to probable effect levels are important for the exposure through ingestion, der- (PELs) (Zheng et al. 2008, Islam et al. 2015c). The sum mal contact, and inhalation (Zheng et al. 2008). toxic units for toxic metals in different soil sampling According to the risk assessment approach, noncarci- sites are presented in Figure 4. In Porahati, Udoipur, nogenic risks of toxic metals through three exposure 14 .KROE TAL. ET KORMOKER T.

Table 11. Chronic daily intake (CDI) (mg/kg) of toxic metals due to ingestion, dermal contact, and inhalation of contaminated soils. Cr Ni Cu As Cd Pb

Adult Adult Adult Adult Adult Adult Sampling sites Adult male female Children Adult male female Children Adult male female Children Adult male female Children Adult male female Children Adult male female Children Chronic daily intake of toxic metals due to ingestion Porahati, Jhenaidah 2.59E 08 2.79E 08 2.41E 07 1.26E 08 1.36E 08 1.18E 07 2.53E 08 2.73E 08 2.37E 07 1.1E 08 1.18E 08 1.02E 07 1.37E 09 1.48E 09 1.28E 08 6.07E 09 6.54E 09 5.66E 08 Udoipur, Jhenaidah 2.66E 09 2.86E 09 2.48E 08 4.28E 08 4.6E 08 3.99E 07 3.8E 08 4.09E 08 3.55E 07 7.47E 09 8.04E 09 6.97E 08 1.52E 09 1.64E 09 1.42E 08 2.56E 08 2.75E 08 2.39E 07 Lokhikol, Jhenaidah 8.75E 09 9.43E 09 8.17E 08 5.22E 08 5.62E 08 4.87E 07 9.17E 08 9.87E 08 8.55E 07 1.86E 08 2.0E 08 1.74E 07 3.29E 09 3.54E 09 3.07E 08 5.03E 08 5.41E 08 4.69E 07 Dhanharia, Jhenaidah 7.01E 09 7.55E 09 6.55E 08 2.32E 08 2.49E 08 2.16E 07 5.21E 08 5.61E 08 4.86E 07 1.4E 08 1.5E 08 1.3E 07 1.7E 09 1.83E 09 1.59E 08 3.37E 08 3.62E 08 3.14E 07 Chourhas, Kustia 1.55E 09 1.67E 09 1.44E 08 1.62E 08 1.74E 08 1.51E 07 2.15E 08 2.32E 08 2.01E 07 6.74E 09 7.26E 09 6.29E 08 8.22E 10 8.85E 10 7.67E 09 1.8E 08 1.94E 08 1.68E 07 Total CDI 4.59E 08 4.94E 08 4.27E 07 1.47E 07 1.58E 07 1.37E 06 2.29E 07 2.46E 07 2.13E 06 5.78E 08 6.21E 08 5.39E 07 8.70E 09 9.38E 09 8.13E 08 1.34E 07 1.44E 07 1.25E 06 RfD 0.003 0.02 0.04 0.0003 0.0005 0.0035 Contamination of concern No No No No No No Chronic daily intake of heavy metals due to dermal contact Porahati, Jhenaidah 1.03E 07 1.11E 07 7.72E 09 5.04E 08 5.43E 08 3.77E 09 1.01E 07 1.09E 07 7.57E 09 4.38E 08 4.71E 08 3.28E 09 5.47E 09 5.89E 09 4.09E 10 2.42E 08 2.61E 08 1.81E 09 Udoipur, Jhenaidah 1.06E 08 1.14E 08 7.94E 10 1.71E 07 1.84E 07 1.28E 08 1.52E 07 1.63E 07 1.14E 08 2.98E 08 3.21E 08 2.23E 09 6.07E 09 6.53E 09 4.54E 10 1.02E 07 1.10E 07 7.63E 09 Lokhikol, Jhenaidah 3.49E 08 3.76E 08 2.61E 09 2.08E 07 2.24E 07 1.56E 08 3.66E 07 3.94E 07 2.74E 08 7.42E 08 7.99E 08 5.56E 09 1.31E 08 1.41E 08 9.82E 10 2.01E 07 2.16E 07 1.50E 08 Dhanharia, Jhenaidah 2.80E 08 3.01E 08 2.09E 09 9.24E 08 9.95E 08 6.92E 09 2.08E 07 2.24E 07 1.56E 08 5.58E 08 6.00E 08 4.17E 09 6.78E 09 7.30E 09 5.07E 10 1.34E 07 1.45E 07 1.01E 08 Chourhas, Kustia 6.18E 09 6.65E 09 4.62E 10 6.46E 08 6.96E 08 4.84E 09 8.58E 08 9.24E 08 6.42E 09 2.69E 08 2.90E 08 2.01E 09 3.28E 09 3.53E 09 2.45E 10 7.18E 08 7.73E 08 5.37E 09 Total CDI 1.83E 07 1.97E 07 1.37E 08 5.86E 07 6.31E 07 4.39E 08 9.13E 07 9.82E 07 6.84E 08 2.31E 07 2.48E 07 1.73E 08 3.47E 08 3.74E 08 2.60E 09 5.33E 07 5.74E 07 3.99E 08 RfD 0.003 0.02 0.04 0.0003 0.0005 0.0035 Contamination of concern No No No No No No Chronic daily intake of toxic metals due to inhalation Porahati, Jhenaidah 5.17E 06 5.57E 06 1.81E 05 2.53E 06 2.72E 06 8.84E 06 5.07E 06 5.46E 06 1.77E 05 2.19E 06 2.36E 06 7.68E 06 2.74E 07 2.95E 07 9.59E 07 1.21E 06 1.31E 06 4.25E 06 Udoipur, Jhenaidah 5.32E 07 5.72E 07 1.86E 06 8.55E 06 9.21E 06 2.99E 05 7.60E 06 8.19E 06 2.66E 05 1.49E 06 1.61E 06 5.23E 06 3.04E 07 3.28E 07 1.06E 06 5.11E 06 5.51E 06 1.79E 05 Lokhikol, Jhenaidah 1.75E 06 1.89E 06 6.13E 06 1.04E 05 1.12E 05 3.66E 05 1.83E 05 1.97E 05 6.42E 05 3.72E 06 4.01E 06 1.30E 05 6.58E 07 7.08E 07 2.30E 06 1.01E 05 1.08E 05 3.52E 05 Dhanharia, Jhenaidah 1.40E 06 1.51E 06 4.91E 06 4.63E 06 4.99E 06 1.62E 05 1.04E 05 1.12E 05 3.65E 05 2.79E 06 3.01E 06 9.78E 06 3.40E 07 3.66E 07 1.19E 06 6.73E 06 7.25E 06 2.36E 05 Chourhas, Kustia 3.10E 07 3.33E 07 1.08E 06 3.24E 06 3.49E 06 1.13E 05 4.30E 06 4.63E 06 1.51E 05 1.35E 06 1.45E 06 4.72E 06 1.64E 07 1.77E 07 5.75E 07 3.60E 06 3.87E 06 1.26E 05 Total CDI 9.16E 06 9.88E 06 3.21E 05 2.94E 05 3.16E 05 1.03E 04 4.57E 05 4.92E 05 1.60E 04 1.15E 05 1.24E 05 4.04E 05 1.74E 06 1.87E 06 6.08E 06 2.68E 05 2.87E 05 9.36E 05 RfD 0.003 0.02 0.04 0.0003 0.0005 0.0035 Contamination of concern No No No No No No TOXIN REVIEWS 15

pathways were characterized in this study. To evaluate the risk, the CDIs, HQs, HI, and carcinogenic risk of the studied metals were estimated for adult male, adult female, and children and the results are presented in Adult female Children this study. CDI of heavy metals through ingestion, dermal con- tact, and inhalation for adult and children are pre- sented in Table 11. Metal specific information was used to determine CDI of heavy metals from ingestion (CDI). We assume long-term exposure for 30 years for adult male and adult female and 6 years for children as the worst-case default assumption. The estimated Adult female Children Adult male CDI values for all studied toxic metals were remaining lower than the standard guideline values. On the basis of ingestion daily exposure, there is low chance to pose public health effect concerns for both adult and children from soil ingestion. Again, CDI for ingestion was found highest in children than adult male and adult female. This may be the result of lower body

Adult female Children Adult male weight of children than the adult. The dermal contact of toxic metals from soil is considered another import- ant pathway of exposure. There may be several ways to expose metals due to dermal contact from soil like working, wading, playing, etc. The estimated CDI from dermal contact for all studied toxic metals were remaining lower than the standard guideline values. Due to inhalation, the CDI of metals was negligible in

Adult female Children Adult male this study. The potential noncarcinogenic toxic effects posed by toxic metals are usually characterized by calculating HQ. The HQs of individual metal are presented in Table 12. If the HQ value is higher than one then there will be adverse health effects associated with over exposure (USEPA 1989, 2001, Zabin et al. 2008, Qu et al. 2012, Genthe et al. 2013). The noncancer Adult female Children Adult male health risks related to individual element exposure through soil ingestion, dermal contact, and inhalation was low for all the investigated metals resulted in a HQ < 1, indicating low risk for both adults and children. The combined effects of exposed metals and metal- loids were calculated as HI and the data indicated that

Cr Nithe Cu HI values were also As lower than one (Figure Cd 5). Pb Adult female Children Adult male However, when considering the total exposure HI of ingestion, dermal contact, and inhalation, there was lower chance of having noncancer risk for adults and children health at all the studied sites. The hazard risk index values for children were higher adult inhabi-

Target hazard quotient (THQ) of toxic metals through ingestion, dermal, and inhalation of contaminated soils. tants, indicating children may pose noncancer risk in the future. The total target hazard quotients (TTHQ) for children was higher due to touching and mouthing Sampling sites Adult male Porahati, JhenaidahUdoipur, JhenaidahLokhikol, Jhenaidah 0.0018Dhanharia, Jhenaidah 0.0002Chourhas, 0.0019 Kustia 0.0006 0.0005 0.0002 0.0061 0.0006 0.0006 0.0005 0.0001 0.0021 0.0017 0.0001 0.0004 0.0001 0.0005 0.0001 0.0002 0.0005 0.0004 0.0004 0.0006 0.0015 0.0003 0.0001 0.0019 0.0008 0.0002 0.0002 0.0001 0.0005 0.0002 0.0003 0.0002 0.0004 0.0006 0.0005 0.0007 0.0003 0.0075 0.0016 0.0009 0.0001 0.0051 0.0081 0.0127 0.0001 0.0095 0.0055 0.0260 0.0004 0.0137 0.0177 0.0103 0.0006 0.0440 0.0331 0.0046 0.0006 0.0006 0.0013 0.0050 0.0007 0.0007 0.0019 0.0159 0.0015 0.0022 0.0007 0.0004 0.0047 0.0024 0.0003 0.0015 0.0004 0.0029 0.0004 0.0020 0.0016 0.0012 0.0012 0.0032 0.0052 0.0021 0.0102 0.0068 0.0011 0.0011 0.0036 Table 12. of dust contaminated particles, direct ingestion by 16 T. KORMOKER ET AL.

0.07 Adult male Adult female Children 0.06

0.05

0.04

0.03 Hazard index value 0.02

0.01

0 Porahati Udoipur Lokhikol Dhanharia Chourhas Sampling location Figure 5. Hazard index (HI) of toxic metals in soils collected from Jhenaidah and Kushtia districts, Bangladesh.

Table 13. Carcinogenic risk of adult male, adult female, and adult population can become more serious. According children due to ingestion, dermal contact, and inhalation of to the result of this study, health risk for adult and arsenic and lead in soils. children due to toxic metal exposure through soil Exposure pathways Arsenic (As) Lead (Pb) could not be overlooked. Adult male Ingestion 6.06E 08 7.95E 10 Dermal contact 1.42E 05 4.53E 07 Inhalation 5.33E 09 3.44E 11 Adult female Ingestion 6.53E 08 8.56E 10 Conclusions Dermal contact 1.53E 05 4.53E 07 Inhalation 5.33E 09 3.44E 11 Contamination of six toxic metals (Cr, Ni, Cu, As, Cd, Children Ingestion 1.62E 07 2.12E 09 and Pb) were investigated near the industrial areas of Dermal contact 5.30E 07 4.53E 07 Inhalation 5.33E 09 3.44E 11 Jhenaidah and Kushtia districts, Bangladesh. The major Total risk (adult male) 1.43E 05 4.54E 07 findings of the study revealed that Cd concentrations Total risk (adult female) 1.54E 05 4.54E 07 Total risk (children) 6.97E 07 4.55E 07 in some sampling sites exceeded the Dutch standard and Canadian quality guidelines values, representing hand to mouth activities, and play behavior (Mielke that the studied soils were heavily contaminated by et al. 1999). The ingestion of greater amounts of small Cd. The EF, geoaccumulation index, contamination fac- particles may have greater impact on children because tor, PLI, and toxic unit analysis values were found safe of their small body weight than adult. for all metals except Cd. PER showed moderate to The carcinogenic risk of As and Pb for adults are very high degree of contamination. It is necessary to presented in Table 13. The carcinogenic risks from As further study to find out the main reasons for the and Pb at all sites via ingestion, dermal contact, and higher PER mainly caused by Cd in the study area. inhalation were in acceptable ranges. The total cancer The noncancer risks related to individual element risk of As and Pb was 1.43E 05 and 4.54E 07 for exposure through soil ingestion, dermal contact, and adult male; 1.54E 05 and 4.54E 07 for adult female; inhalation showed low risk for both adults and chil- 6.97E 07 and 4.55E 07 for children. The carcino- dren. The carcinogenic risks from As and Pb at all sites genic risks of As and Pb due to exposure from studied were in acceptable ranges. But concern is that long- soil via ingestion, dermal contact, and inhalation path- term exposure of these metals can pose cancer risks ways can be negligible in the industrial areas of for both adults and children. Jhenaidah and Kushtia districts, Bangladesh. 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