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Toxin Reviews

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Toxic metals in agricultural soils near theindustrial areas of Bangladesh: ecological andhuman 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 industrialareas 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 andMahfuzur Rahmanh

aDepartment of Emergency Management, Patuakhali Science and Technology University, Dumki, Bangladesh; bInstitute of MountainHazards and Environment, Chinese Academy of Sciences, Chengdu, China; cDepartment of Soil Science, Patuakhali Science andTechnology University, Dumki, Bangladesh; dDepartment of Applied Biological Chemistry, Graduate School of Agricultural and LifeSciences, The University of Tokyo, Tokyo, Japan; eGraduate School of Environment and Information Sciences, Yokohama NationalUniversity, Yokohama, Japan; fFaculty of Agricultural Engineering and Technology, Sylhet Agricultural University, Sylhet, Bangladesh;gDepartment of Environmental Science, Bangladesh Agricultural University, Mymensingh, Bangladesh; hFaculty of Agriculture,Patuakhali Science and Technology University, Dumki, Bangladesh

ABSTRACTThis study was conducted to assess the potential ecological and human health risk of toxic met-als in agricultural soils near the industrial areas of Bangladesh. In this study, six toxic metals(chromium, nickel, copper, arsenic, cadmium, and lead) were assessed in 58 soil samples of fivedifferent sampling sites around the industrial areas of Jhenaidah and Kushtia districts inBangladesh. Toxic metals were measured using inductively coupled plasma mass spectrometer.Potential ecological and human health risk were assessed through enrichment factor (EF), con-tamination factor (Cf

i), geoaccumulation index (Igeo), pollution load index (PLI), toxic unit analysis,chronic daily intake through exposure pathway, hazard quotient, and hazard index. The meanconcentrations of Cr, Ni, Cu, As, Cd, and Pb were found to be 5.78, 21.0, 31.8, 8.05, 1.20, and19.2mg/kg, respectively. Metals concentrations were found below the recommended value setby 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 industrialsector. The mean values of EF, Igeo, Cf

i, PLI, and toxic units were found safe level for all metalsexcept Cd. In the view of potential ecological risk (PER), soils from all sampling sites indicatedmoderate 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 <10�6 indicating low noncarcinogenic and can-cer risk for adult and children.

ARTICLE HISTORYReceived 16 June 2019Revised 27 July 2019Accepted 28 July 2019

KEYWORDSAgricultural soils; toxicmetals; PCA; ecological risk;health risk; Bangladesh

Introduction

Soil is a vital element for human life to survive theplanet which is assumed as prime receiver of persist-ent pollutants such as toxic metals (Karim et al. 2014,Islam et al. 2015a, Proshad et al. 2018a). Soil contamin-ation by toxic metals is a substantial environmentalproblem worldwide (Alloway 1995, due to their widesources, toxicity, and nonbiodegradable nature (Yuanet al. 2011, Zhao et al. 2014, Islam et al. 2015b,Bhuyan et al. 2017, Islam et al. 2018). According to theUS Environment Protection Agency (EPA), toxic metalssuch as chromium, nickel, copper, arsenic, cadmium,and lead have been considered as the most toxic met-als in the environment (Lei et al. 2010, Proshad et al.2017). In recent decades, contamination of soils occurs

due to various toxic metals from rapid industrializationand development and it has become more severe fordeveloping countries like Bangladesh due to its indis-criminate growing industries without any proper plan-ning (Sun et al. 2010, Chen et al. 2010, Shi et al. 2011,Ahmed et al. 2015). Heavy metals may originate insoils around the industrial areas from numerous sour-ces but industrial activities such as generation ofpower, manufacturing, burning of fossil fuel, and dis-posal of waste are the most important contributors ofsoil pollution (Karim et al. 2014, Rodr�ıguez Mart�ınet al. 2014, Islam et al. 2016). Almost all industrial unitsare discharging their untreated wastes in the surfacedrains and spread over agricultural fields. Toxic ele-ments toxicity changes agricultural soil bionetworks

CONTACT Ram Proshad ramproshadpstu03470@gmail.com 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

� 2019 Informa UK Limited, trading as Taylor & Francis Group

TOXIN REVIEWShttps://doi.org/10.1080/15569543.2019.1650777

that have a significant negative consequence on theproductivity of land (Khan et al. 2010, Yuanet al. 2014).

The contaminations of soil quality by toxic metalshave exerted long-term ecological and health risks.Agricultural crops which are being cultivated in thecontaminated agricultural soils may cause serious car-cinogenic and noncarcinogenic risks to the humanbody (Man et al. 2010, Proshad et al. 2018b). In theindustrial areas, toxic metals polluted soil can posesignificant human health risks due to soil ingestion,inhalation, and dermal contact (Siciliano et al. 2009,Luo et al. 2011, Li et al. 2011). Toxic metals can bevery harmful to the human body even in low concen-trations as there is no effective excretion mechanism(Ghosh et al. 2012). The common public (especiallychildren and adult citizens) are most vulnerable to thetoxic metals from soil (Luo et al. 2012). Therefore,exposure to toxic metal pollutants is of utmost con-cern for children in their primary developmental yearsand also for the adult (Lee et al. 2013, Rachwał et al.2017). Various indexes have been widely used todetermine environmental risks of toxic elements insoils such as contamination factor (CF), enrichmentfactor (EF) and geoaccumulation index (Igeo) (Rashed2010, Liu et al. 2014). The contamination factor, EF,and geoaccumulation index of individual toxic metalin soil are calculated using its total content and soilquality guideline value (Zhang et al. 2013). For deter-mination of multiple risk of toxic metals in soil, pollu-tion load index (PLI) and potential ecological riskindex (PER) have also been developed (Huang et al.2013). The PLI compares the metal concentrationswith baseline values, which helps in assessing theenrichment of toxic metals in soil (Yang et al. 2009,Islam et al. 2018). The chronic daily intake (CDI) esti-mation, target hazard quotient (THQ), and hazardindex (HI) methods have also been developed toassess the carcinogenic and noncarcinogenic healthrisk through several exposure pathways such as inges-tion, inhalation, and dermal contact. Therefore,research on potential ecological and health risk assess-ment due to toxic metals pollution in soils near theindustrial area is very essential.

Jhenaidah and Kushtia are two industrialized dis-tricts of Bangladesh that are supposed to be highlycontaminated by toxic metals. These two districts arewell-known for agricultural production and it pro-vides a large portion of agricultural products all overthe country. Although several studies have conductedfor assessing ecological and human health risk dueto toxic metal contamination from soil in the urban

and industrial regions of the world as well asBangladesh (Luo et al. 2007, Man et al. 2010, Islamet al. 2016, Proshad et al. 2017, but there is very lim-ited research has been conducted so far on toxicmetals in soils and its adverse effects on the environ-ment as well as human health, especially the indus-trial areas of Jhenaidah and Kushtia districts.Therefore, the purposes of this study were (1) todetermine the physiochemical properties and concen-trations of toxic metals (Cr, Ni, Cu, As, Cd, and Pb) inagricultural soils; (2) to identify the potential sourcesof toxic metals in agricultural soils; and (3) to assessthe potential ecological and health risk oftoxic metals.

Materials and methods

Study area and sampling

The soil samples were collected from industrialareas of Jhenaidah and Kushtia districts, Bangladesh(Figure 1). Jhenaidah and Kushtia districts are twoindustrial growing sites of Bangladesh. There are sev-eral types of industrial units including tobacco indus-tries, garments, tannery industries, packaging industry,dyeing, brick kiln, metal workshops, battery manufac-turing industries, textile industries, pesticide, and fertil-izer industries, different food processing industries,and other industrial areas produce huge volumes ofeffluents that contain toxic metals. The untreatedwastes and effluents from these industries are dis-charged randomly to river and canals. Then thatwastes are mixed with soils and the soil is continu-ously polluted by toxic metals. Soil samples were col-lected during March–April, 2016. Five agricultural soilsampling sites (Porahati, Udoipur, Lokhikol, Dhanharia,and Chourhas) and (58 sampling locations) wereselected near the industrial areas of Jhenaidah andKushtia districts, Bangladesh. Agricultural surface soils(0–10 cm depth) were collected in the form of threesubsamples. These subsamples were thoroughly mixedto form a composite sample. Samples were air-dried atroom temperature for two weeks, then ground andhomogenized. For metal analysis, soil was taken bymeans of a percussion hammer corer (50–80 cm inlength) as pre-industrial sample (Schottler andEngstrom 2006). The dried soil samples were crumbledwith a porcelain mortar and pestle and sieved through2mm nylon sieve and stored in an airtight cleanZiploc bag and kept frozen until chemical analysis(Oliveira et al. 2012, Arenas-Lago et al. 2013, 2014).

2 T. KORMOKER ET AL.

Physicochemical parameters analysis

Soil pH was determined by using a glass electrode pHmeter (WTW pH 522; Germany). For EC determination,5.0 g of soil was taken in 50ml polypropylene tubesand 30ml of Milli-Q water was added to the tube. Thelid was closed properly and was shaken for 5min.After that, EC was measured using an EC meter (WTWLF 521; Germany). For organic carbon, 1.0 g of soil wasplaced at the bottom of a dry 500ml conical flask(Corning/Pyrex). Then 10ml of 1 N K2Cr2O7 was addedinto the conical flask and swirled a little. The flask waskept on asbestos sheet. Then 20ml of concentratedH2SO4 was added into the conical flask and swirledagain 2–3 times. The flask was allowed to stand for30min and thereafter 200ml of distilled water wasadded. After incorporation of 5.0ml of phosphoricacid and 35 drops of diphenylamine indicator, thecontents were titrated against ferrous ammonium sul-fate solution till the color flashes blue-violet to green.Simultaneously, a blank titration was run without soil.Particle size was determined using the hydrometermethod. The textural classes for different soil sampleswere then determined by plotting the results on a

triangular diagram designed by Marshall followedUSDA system. The percentage of sand, silt, and claywere calculated as follows:

% siltþ clayð Þ ¼corrected hydrometer reading at 40 s=ð

oven dry weight of soil�100 (1)

% clayð Þ ¼corrected hydrometer reading after 2 h=ð

oven dry weight of soil�100 (2)

Sand %ð Þ ¼ 100�% siltþ clayð Þ (3)

Silt %ð Þ ¼ % siltþ clayð Þ�%clay (4)

Toxic metal analysis

All chemicals were analytical grade. Milli-Q water (ElixUV5 and MilliQ, Millipore, Boston, MA) was used forthe preparation of solutions. The Teflon vessel andpolypropylene containers were cleaned, soaked in 5%HNO3 for more than 24 h, then rinsed with Milli-Qwater and dried. For metal analysis, 0.3–0.5 g of thesoil sample was treated with 6ml 69% HNO3 (Kanto

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

TOXIN REVIEWS 3

Chemical Co, Tokyo, Japan) and 2ml 30% H2O2 (WakoChemical Co, Tokyo, Japan) in a closed Teflon vesseland was digested in a Microwave Digestion System(Berghof speedwave, Eningen, Germany). The digestedsamples were then transferred into a Teflon beaker,and total volume was made up to 50ml with Milli-Qwater. The digested solution was then filtered byusing syringe filter (DISMIC1–25HP PTFE, pore size ¼0.45mm; Toyo Roshi Kaisha, Ltd., Tokyo, Japan) andstored in 50ml polypropylene tubes (Nalgene, NewYork, NY). After that, the digestion tubes were thencleaned using blank digestion procedure following thesame procedure of samples. For toxic metals, sampleswere analyzed using inductively coupled plasma massspectrometer (ICP-MS, Agilent 7700 series, Santa Clara,CA). Instrument operating conditions and parametersfor metal analysis were done. The detection limits ofICP-MS for the studied metals were 0.7, 0.6, 0.8, 0.4,0.06, and 0.09 ng/L for Cr, Ni, Cu, As, Cd, and Pb,respectively. Multi-element Standard XSTC-13 (SpexCertiPrepVR , Metuchen, NJ) solutions were used to pre-pare calibration curves. Multi-element solution (pur-chased from Agilent Technologies, Japan) was used astuning solution covering a wide range of masses ofelements. All test batches were evaluated using aninternal quality approach and validated if they satis-fied the defined internal quality controls (IQCs). Beforestarting the analysis sequence, relative standard devi-ation (RSD, <5%) was checked using the tuning solu-tion purchased from Agilent Technologies. Thecertified reference materials INCT-CF-3 (corn flour)bought from the National Research Council (Canada)were analyzed to confirm analytical performance andgood precision (relative standard deviation below20%) of the applied method.

Ecological risk assessment for soil pollution

Enrichment factor

EF is considered as an effective tool to evaluate themagnitude of contaminants in the environment(Franco-Uria et al. 2009). The EF for each element wascalculated to evaluate anthropogenic influences onheavy metals in soils using the following formula(Selvaraj et al. 2004):

EF ¼ CM=CAlð Þsample= CM=CAlð Þbackground (5)

where (CM/CAl)sample is the ratio of concentration ofheavy metal (CM) to that of aluminum (CAl) in the soilsample, and (CM/CAl)background is the same referenceratio in the background sample (Islam et al. 2015a).Generally, an EF value of about 1 suggests that a

given metal may be entirely from crustal materials ornatural weathering processes (Zhang and Liu 2002).Samples having EF >1.5 was considered indicative ofhuman influence and (arbitrarily) an EF of 1.5–3, 3–5,5–10, and >10 is considered the evidence of minor,moderate, severe, and very severe modification,respectively (Birch and Olmos 2008).

Contamination factor (Cfi)

The contamination factor means the proportion of theheavy metal concentration in the soil to that of base-line or background value:

Cfi ¼ Cheavy metal=Cbackground (6)

The contamination factor divided into four classesbased on their intensities on a scale ranging from 1 to6: low degree (Cf

i<1), moderate degree (1� Cfi<3),

considerable degree (3� Cfi<6), and very high degree

(Cfi � 6) (Islam et al. 2015c). This approach has been

used by other researchers (Proshad et al. 2017).

Geoaccumulation index (Igeo)

The degree of contamination from the trace metalscould be assessed by determining the geoaccumula-tion index (Igeo) proposed by Muller (1969). The indexof geoaccumulation (Igeo) has been widely applied tothe assessment of soil contamination (Santos et al.2003). To characterize the level of pollution in the soil,geoaccumulation index (Igeo) values were calculatedusing the equation:

Igeo ¼ log 2 Cn=1:5Bnð Þ (7)

where Cn is the measured concentration of metal n inthe soil and Bn is the geochemical background valueof element n in the background sample (Turekian andWedepohl 1961, Rudnick and Gao 2003). The factor1.5 is introduced to minimize the possible variations inthe background values which may be attributed tolithogenic effects (Nikolaidis et al. 2010).Geoaccumulation index (Igeo) values were interpretedas follows: Igeo�0, practically uncontaminated;0� Igeo�1, uncontaminated to moderately contami-nated; 1� Igeo�2, moderately contaminated;2� Igeo�3, moderately to heavily contaminated;3� Igeo�4, heavily contaminated; 4� Igeo�5, heavilyto extremely contaminated; and 5< Igeo, extremelycontaminated.

Pollution load index

To assess the quality of soil in terms of metal contam-ination, an integrated approach of PLI of the six

4 T. KORMOKER ET AL.

metals was calculated according to Rashed (2010). ThePLI is defined as the nth root of the multiplications ofthe contamination factor (Cf

i) of metals (Bhuiyan et al.2011).

PLI ¼ Cif1 � Ci

f2 � Cif3 � � � � . . .� Ci

fn

� �1=n(8)

The PLI gave an assessment of the overall toxicitystatus of the sample and also it is a result of the con-tribution of the six metals.

Potential ecological risk

The degrees of hazardous elements contamination inagricultural soils are determined by PER index.Guo et al. (2010) and Luo et al. (2007) proposed equa-tions which were used to calculate PER and are asfollows:

Cif ¼

Ci

Cin; Cd ¼

Xn

i¼1

Cif (9)

Eir ¼ T ir � Cif; PER ¼

Xm

i¼1

Eir (10)

where Cif is the single element contamination factor,

Ci is the content of the element in samples, and Cin is

the background value of the element. The backgroundvalue of Cr, Ni, Cu, As, Cd, and Pb in soils were 90, 68,45, 13, 0.3, and 20mg/kg, respectively (preindustrialsamples of the study area) (Turekian and Wedepohl1961). The sum of Ci

f for all metals represent the inte-grated pollution degree (Cd) of the environment. Eir isthe PER index and T ir is the biological toxic factor ofan individual element. The toxic-response factors forCr, Ni, Cu, As, Cd, and Pb were 2, 6, 5, 10, 30, and 5,respectively (Håkanson 1980, Gong et al. 2008,Wu et al. 2010, Guo et al. 2010, Jintao et al. 2011,Amuno 2013). PER is the comprehensive PER index,which is the sum of Eir:

Toxic unit analysis

The sum of toxic units (RTUs) is considered as poten-tial acute toxicity of hazardous elements in agriculturalsoil samples. Toxic unit analysis is stated as the ratioof the assessed concentration of hazardous elementsin soil to probable effect level (PELs) (Zheng et al.2008). A moderate to serious toxicity of hazardous ele-ments remain in soil when the sum of toxic units forall soil samples is more than 4 (Bai et al. 2011).

Health risk assessment from polluted soil

Daily intake of heavy metals through exposurepathway from soil

Ingestion and dermal absorption of heavy metals frompolluted agricultural soils have great importance inpotential exposure pathways (Fryer et al. 2006,Qu et al. 2012). Out of several exposure pathways,ingestion of metals from soil is the most commonexposure pathway for Cr, Ni, Cu, As, Cd, and Pb(Ord�o~nez et al. 2011). CDI (mg/kg/day) of metals wasdetermined from ingestion (CDIingest-soil) and dermalcontact (CDIdermal-soil) in this study for both adult andchildren were estimated using the following formulas:

Ingestion from soil :CDIingest�soil ¼CS�IRS�EF�EDBW�AT

�CF

(11)Dermal contact from soil :CDIdermal-soil ¼

CS�SA�AF�ABS� IRS�EF�EDBW�AT

�CF (12)

Inhalation from soil :CDIinhalation�soil ¼CS� InhR�EF�ED

BW�AT�CF (13)

where CDI¼chronic daily intake; CS¼exposure-pointconcentration, mg/kg; IRS¼ ingestion rate, 100 and200mg d�1 for adult and children (USEPA 2011);EF¼exposure frequency, 350 d/a (USEPA 2011);ED¼exposure duration, 30years for adult and 6yearsfor children (USEPA 2011); CF¼units conversion factor,10�6kg mg�1 (USEPA 2002); SA¼exposure skin area,5700 and 1600cm2 for adult and children (USEPA2011); AF¼adherence factor, 0.07 and 0.02mg cm�2

for adult and children (USEPA 2011); ABS¼dermalabsorption fraction, 0.01 for adult and 0.001 for chil-dren (USEPA 2011); BW¼body weight, 70kg for adultmale, 65kg for adult female, and 15kg for children(USEPA 2001); AT¼averaging time for noncarcinogens,365� ED (USEPA 2002); InhR¼ inhalation rate 20 m3/dfor both adult and child (USEPA 1997).

Hazard quotient (HQ)

The noncarcinogenic risks for each individual heavymetal (Cr, Ni, Cu, As, Cd, and Pb) through ingestion,dermal, and inhalation were assessed by the THQ(USEPA 1989). The methodology for the estimation ofnon-carcinogenic risks was applied in accordance withthat provided by the U.S. Environmental ProtectionAgency (USEPA) Region III’s risk-based concentrationtable (USEPA 2011). Hazard quotient (HQ) was deter-mined on the basis of CDI from ingestion (CDIingest),dermal (CDIdermal), and inhalation (CDIinhalation), it was

TOXIN REVIEWS 5

calculated by dividing the average daily dose to a spe-cific reference dose (RfD) (USEPA 1989). The equationused for estimating the THQ is as follows:

HQingest ¼ CDIingestð Þ=RfD (14)

HQdermal ¼ CDIdermalð Þ=RfD (15)

HQinhalation ¼ CDIinhalationð Þ=RfD (16)

where THQ is the target hazard quotient, CDI is thechronic daily intake of heavy metal (mg/kg), and RfDis the reference dose (mg/kg/day). The RfD for Cr, Ni,Cu, As, Cd, and Pb were 0.003, 0.02, 0.04, 0.0003,0.0005, and 0.0035mg/kg/day, respectively (USEPA2002, USDOE 2011). The reference dose (RfD) (mg/kg/day) is an estimation of maximum permissible risk onhuman population through daily exposure, taking intoconsideration sensitive group (children) during the life-time. If the CDI is higher than RfD (HQ > 1), there willbe a severe health hazard to human, whereas CDI isless than RfD (HQ � 1), there will be no severe humanhealth effects (USEPA 1989, 2001). The health riskguidelines determination of chemical mixtures definedthat “simultaneous sub-threshold exposures to severalchemicals may result in an adverse health effect” and“the magnitude of the adverse effect will be propor-tional to the sum of the ratios of the sub-thresholdexposures to acceptable exposures” (USEPA 1986).Again, HI can be generated from the HQ to calculatethe combined risk of individual heavy metals in theform of mix contaminates (USEPA 1989).

Hazard index (HI)

To assess the overall potential for noncarcinogeniceffects from more than one heavy metal, a HI hasbeen formulated based on the guidelines for healthrisk assessment of chemical mixtures (USEPA 1999).The HI from THQs is expressed as the sum of the HQs(USEPA 2011). The equation used for estimating the HIis as follows:

HI ¼ RTHQn

(17)

¼ THQelement 1 þ THQelement 2 þ . . . . . . . . . . . . :þTHQelements n (18)

HI ¼ RTHQ ¼ HQingest þ HQdermal þ HQinhalation (19)

The guidelines also state that any single metal withan exposure level greater than the toxicity value willcause the HI to exceed unity; for multiple metal expo-sures, the HI can also exceed unity even if no singlemetal exposure exceeds its RfD.

Carcinogenic risk

Carcinogenic risk is considered as the probability of anindividual developing any type of cancer in the wholelifetime due to exposure to carcinogenic hazards(Li et al. 2014). Carcinogenic risk expressed as the totalcancer risk (Eq. 23).

CRingest-soil ¼ CS� AF� IngR� EF� EDð Þ= BW� ATð Þ� �

�CF� CSFingest (20)

CRdermal-soil ¼ CS� SA� AF� ABSd � EF� EDð Þ=�

BW� ATð Þg�CF� CSFingest � ABSGI (21)

CRinhalation�soil ¼ CS� ET� EF� EDð Þ=�

PEF� 24� ATð Þg�IUR� 103 (22)

Total cancer risk ¼ Riskingestion þ Riskdermal þ Riskinhalation(23)

where CRingest-soil is the cancer risk of metals fromingestion of soil; CRdermal-soil, the cancer risk of metalsfrom dermal contact of soil; CS, the heavy metal con-centration in soil, mg/kg; AF, soil-to-skin adherencefactor, 0.7mg/cm2 for adult and 0.2mg/cm2 for chil-dren (USEPA 2011); IngR, ingestion rate of soil, 100and 200mg d�1 for adult and children, respectively(USEPA 2011); EF, exposure frequency, 350 days/year(USEPA 2011); ED, exposure duration, 30 years for adultand 6 years for children (USEPA 2011); BW, bodyweight, 70 kg for adult male, 65 kg for adult female,and 15 kg for children; AT, averaging time for noncar-cinogens, 365� ED (USEPA 2011); CF, units conversionfactor, 10�6 kg/mg (USEPA 2002); CSFingest, chronic oralslope factor, 1.5 for As and 8.5� 10�3 for Pb (USEPA2011, USDOE 2011); SA, exposure skin surface areaavailable for contact, 5700 cm2 for adult and 1600 cm2

for children (USEPA 2011); ABSd, dermal absorptionfraction, 0.01 for adult and 0.001 for children (USEPA2011); ET, exposure time, 1 for residents for the sitespecific (USDOE 2011); ABSGI, gastrointestinal absorp-tion factor, 0.41 and 1 for As and Pb, respectively(USEPA 2011); PEF, particle emission factor, 1.36� 109

(USDOE 2011, USEPA 2011); IUR, chronic inhalationunit risk, 4.30� 10�3 for As, 1.20� 10�5 for adult(USDOE 2011).

In this study, we calculated carcinogenic risk forarsenic and lead as they are classified as probably car-cinogenic to humans (ATSDR 2007, 2012). The excesscancer risks lower than 10�6 (a probability of 1 chancein 1,000,000 of an individual developing cancer) areconsidered to be negligible, cancer risks above 10�4

are considered unacceptable by most internationalregulatory agencies (USEPA 1989, Guney et al. 2010),and risks lying between 10�6 and 10�4 are generallyconsidered an acceptable range, depending on the

6 T. KORMOKER ET AL.

situation and circumstances of exposure (Hu et al.2012). The value 10�6 is also considered the carcino-genic target risk by USEPA (2011).

Statistical analysis

The data were statistically analyzed using the statis-tical package, SPSS 20.0 (SPSS, USA). The means of thehazardous element concentrations in soils were calcu-lated. Multivariate methods in terms of principal com-ponent analysis (PCA) were used to interpret thepotential sources of toxic metals in soil (Liang et al.2015). A Pearson bivariate correlation was used toevaluate the interelement relationship in soil. Othercalculations were performed by Microsoft Excel 2013.

Results and discussion

Physiochemical properties of soil

The physicochemical properties of soil in the studysites are presented in Table 1. The mean values of soilpH were obtained 7.41, 7.69, 8.45, 8.01, and 8.04 atPorahati, Udoipur, Lokhikol, Dhanharia, and Chourhas,respectively. The studied soils were slightly acidic toalkaline in nature which can be due to the decompos-ition of organic matter and subsequent formation ofcarbonic acid (Islam et al. 2014). Higher soil acidity(lower pH values) favors the availability of cations insoil. Many metal complexes are insoluble under

alkaline conditions and low pH also may lead to met-als becoming unavailable to plants and therefore, lesslikely to be incorporated in plant tissues (Loska et al.2005). According to Soil Resources DevelopmentInstitute (SRDI) soil salinity class, electrical conductivity(EC) value of the studied soil was nonsaline(0–2 dS/m) for all sampling sites which mean the salin-ity effect is negligible. The percentage of organic car-bon in soils ranged from 0.17 to 5.41, 0.67 to 3.89,0.52 to 1.55, and 0.55 to 4.59 at Porahati, Udoipur,Lokhikol, and Dhanharia sites of Jhenaidah district,respectively, and 0.21 to 4.55 at Chourhas site ofKushtia district (Table 1). The highest mean percent-age value of organic carbon was observed in soil thatcollected from the Porahati site (1.87) and the lowestvalue observed in the Lokhikol site (1.22). High organiccarbon content is an indication that metals are morelikely to be bound to organic matter to form metal che-late complexes, and this would also result in less avail-ability of metals to plants (Yap et al. 2009, Islam et al.2014). According to the USDA soil texture classification,the textural analysis revealed that the studied soil siltand silty loam among the sites of the study area.

Toxic metal concentration in soil samples

The concentration of total toxic metals (Cr, Ni, Cu, As,Cd, and Pb) in soil samples are presented in (Table 2).The mean concentration of Cr, Ni, Cu, As, Cd, and Pb

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 (n¼ 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 ± 3.26Range 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 (n¼ 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 ± 22.01Range 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 (n¼ 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 ± 30.57Range 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 (n¼ 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 ± 10.38Range 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 (n¼ 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 ± 7.20Range 0.24–1.66 1.02–54.46 0.99–64.19 1.47–12.49 0.13–1.65 1.86–24.41

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 (n¼ 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 loamRange 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 (n¼ 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 SiltRange 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 (n¼ 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 loamRange 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 (n¼ 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 loamRange 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 (n¼ 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 loamRange 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

TOXIN REVIEWS 7

in soils at different sampling sites were found 5.78,21.0, 31.8, 8.05, 1.20, and 19.2mg/kg, respectively.

Chromium is a toxic heavy metal is dischargedfrom several industries into the agricultural landaround industrial areas and pollutes agricultural soils(Nriagu 1988). The concentration of Cr in agriculturalsoils varies up to values as high as 350mg kg�1

(Branca et al. 1990). The toxicity of Cr has negativeimpacts on the growth of plants that interfere withsome important metabolic processes (Shaker et al.2009, Hasnine et al. 2017). In this study, the highestmean concentration of Cr (18.88mg/kg) was observedat Porahati site. Chromium concentration was found inthe study areas may be disposed of untreated tannerywaste to agricultural fields since chromium salt usedin tannery industries (Srinivasa et al. 2010). The meanconcentration of Cr was found 5.78mg/kg in thisstudy which was lower than the Dutch Soil QualityStandard (VROM 2000), Canadian EnvironmentalQuality Guidelines (CCME 2003), and AustralianGuideline for Soil Quality (DEP 2003). Chromium con-centration in soils of this study were also compared toother study conducted in Bangladesh and other coun-tries and found that Cr concentration in this studywas lower than the other studies (Tokalıoglu and

Kartal 2006, Ahmad and Goni 2010, Acosta et al. 2011,Bhagure and Mirgane 2011, Luo et al. 2011, Rahmanet al. 2012, Islam et al. 2014, Proshad et al. 2018b)(Table 3).

The solubility of nickel in soils increases with itsacidity and if the acidity increases it results higher Niin soils (Baralkiewicz and Siepak 1999). Nickel cancause dermatitis, lung fibrosis, cardiovascular, and kid-ney diseases and cancer of the respiratory tract in thehuman body (Hasnine et al. 2017). In this study, Niconcentrations ranged between 1.02 and 77.32mg/kgin the study area. The highest concentration(77.32mg/kg) was found at Udoipur and the lowestvalue (1.02mg/kg) at Chourhas (Table 2). The elevatedlevels of Ni were found in this study which resultsfrom localized additions or accidental spillages of Nicontaining materials (Govil et al. 1998, Krishna andGovil 2007). The mean concentration of Ni was found21.0mg/kg in this study which was lower than theDutch Soil Quality Standard (VROM 2000), CanadianEnvironmental Quality Guidelines (CCME 2003), andAustralian Guideline for Soil Quality (DEP 2003). Nickelconcentration in soils of this study were also com-pared to the other study conducted in Bangladeshand other countries and found that Ni concentration

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 andKushtia,Bangladesh

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

Tangail(Bangladesh)

8.31 16.49 20.64 5.06 2.2 16.9 Proshadet al. 2018b

Dhaka(Bangladesh)

384 (158–1160) 192 (104–443) 311 (157–519) 64 (41–93) 7.1 (3.9–13) 199 (84–574) Islam et al. 2014

Noakhali(Bangladesh)

29 (18–46) 64 (37–93) 22 (13–63) 3.3 (1.5–9.2) 0.07 (0.03–0.2) 13 (8–22) Rahmanet al. 2012

Dhaka(Bangladesh)

54 (34–68) 58 (36–74) 39 (31–45) NA 11 (6–16) 50 (44–52) Ahmad andGoni 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. 2011Maharashtra

(India)164 (66–279) 171 (69–465) 155 (52–373) 2.8 (NA–11.2) 30 (22–39) 42 (36–49) Bhagure and

Mirgane 2011Murcia (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. 2011Kayseri (Turkey) 29 (17–81) 45 (16–217) 37 (12–144) NA 2.5 (0.98–15) 75 (28–312) Tokalıo�glu and

Kartal 2006Dutch soil quality

standard(target value)

100 35 36 29 0.8 85 VROM 2000

Dutch soil qualitystandard(interventionvalue)

380 210 190 55 12 530 VROM 2000

Canadianenvironmentalqualityguidelines

64 50 63 12 1.4 70 CCME 2003

Department ofEnvironmentalProtection,Australia

50 60 60 20 3 300 DEP 2003

8 T. KORMOKER ET AL.

in this study was higher than the other studies (Luoet al. 2011, Acosta et al. 2011, Proshad et al. 2018b)(Table 3).

Soluble soil Cu can be toxic to plants since Cu-enriched liquid dairy waste used in agricultural land asirrigation water (White and Brown 2010). Excessive Cuconcentrations are harmful to plants and highly toxicto some microorganisms (Hasnine et al. 2017). In thisstudy, the value of Cu ranged between 0.99 and122.9mg/kg (Table 2). The elevated concentration ofCu was observed in soil at Lokhikol site which can bedue to the emission of Cu from the uncontrolledindustrial and waste burning activities (Srinivasa et al.2010, Luo et al. 2011). The mean concentration of Cuwas found 31.8mg/kg in this study which was lowerthan the Dutch Soil Quality Standard (VROM 2000),Canadian Environmental Quality Guidelines (CCME2003), and Australian Guideline for Soil Quality (DEP2003) indicating lower contamination of Cu in soil(Table 3). Yu et al. (2008) found 17.10mg/kg Cu in aridagricultural soil in central Gansu Province, China. Thethreshold value for Cu is �60mg/kg for arid agricul-tural soils in China (NEPA 1995). Hasnine et al. (2017)reported average Cu concentration in the surface agri-cultural soil at DEPZA was found to be91.06 ± 152.70mg/kg.

Arsenic is called “slow poison” or death metalbecause it kills people slowly whenever it enters intothe human body (Nawab et al. 2017). In this study,the concentration of As ranged from 1.28 to23.38mg/kg (Table 2). The highest concentration of As(13.58mg/kg) was observed at Lokhikol site. In gen-eral, the arsenic in agricultural soils can be derivedfrom both natural and anthropogenic sources, espe-cially use of arsenic contaminated groundwater for irri-gation and uncontrolled application of As enrichedfertilizers and pesticides (Renner 2004, Neumann et al.2011). Moreover, emission and waste from brick fields

and incineration activities might contribute to thehigh concentration of As in agricultural soil (Olawoyinet al. 2012). The mean concentration of As was found8.05mg/kg in this study which was lower than theDutch Soil Quality Standard (VROM 2000), CanadianEnvironmental Quality Guidelines (CCME 2003), andAustralian Guideline for Soil Quality (DEP 2003).Arsenic concentration in soils of this study were alsocompared to other study conducted in Bangladeshand other countries and found that As concentrationin this study was higher than the other studies(Bhagure and Mirgane 2011, Rahman et al. 2012,Proshad et al. 2018b) (Table 3). Frank et al. (1976) esti-mated 6.21 ± 2.67mg/kg As in agricultural soils ofOntario while Yu et al. (2008) recorded 8.80mg/kg Asin arid agricultural soil in central Gansu Province,China. The threshold value for As is �20mg/kg forarid agricultural soils in China (NEPA 1995).

Cadmium concentrations were ranged from 0.13 to7.51mg/kg (Table 2). The highest concentration of Cd(2.40mg/kg) was observed at Lokhikol site. Higher Cdconcentration in soils might be related to industrialactivity, metal processing, atmospheric emission, andCd plated items (Proshad et al. 2019). The mean con-centration of Cd was found 1.20mg/kg in this studywhich was higher than The Dutch Soil QualityStandard (VROM 2000) and lower than CanadianEnvironmental Quality Guidelines (CCME 2003) andAustralian Guideline for Soil Quality (DEP 2003). TheDutch soil quality standard is considered the mostsuitable guideline indicating all possible exposurepathways for protecting humans, plants, and animals(Proshad et al. 2017). The soil is considered clean ifany heavy metal concentration in soil is below itsrespective Dutch Target Value. The soil is regarded tobe slightly to moderately contaminated if the concen-tration level lies between the target values and inter-vention values. In contrast, if the value is above the

Table 4. Correlation coefficient matrix for physiochemical properties and toxic metals in soils collected from Kushtia andJhenaidah districts, Bangladesh.

pH EC Sand Silt Clay OM Cr Ni Cu As Cd Pb

pH 1EC �0.057 1Sand �0.110 0.622�� 1Silt 0.695�� 0.098 0.785�� 1Clay �0.641�� �0.872�� �0.047 0.030 1OM 0.130 0.009 �0.215 �0.052 0.142 1Cr �0.116 �0.102 0.123 �0.140 �0.129 �0.194 1Ni 0.082 �0.103 �0.250 �0.043 �0.110 �0.174 0.026 1Cu 0.174 0.079 0.040 0.052 0.134 �0.097 0.443�� 0.166 1AS 0.123 0.160 0.244 0.116 0.173 0.002 0.018 0.016 �0.248 1Cd �0.023 0.001 0.069 0.071 �0.082 �0.199 0.176 0.723�� 0.161 0.015 1Pb 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).

TOXIN REVIEWS 9

Dutch Intervention Value, the soil is considered detri-mental to humans, plants, and animals. About 80% ofthe studied soil samples exceeded the Dutch targetvalue assuming that Cd in soil might pose a severerisk to the surrounding ecosystems.

The highest concentration of Pb (41.60) mg/kg) wasobserved at Lokhikol site. The higher level of Pb con-centration present in soils due to metal processingfactories release Pb into the open environment andseveral anthropogenic factors (Karim et al. 2008,Nziguheba and Smolders 2008). In this study, Lokhikolsite showed the elevated concentrations of Pb whichcan be due to the release of Pb contaminated wastefrom this area (Srinivasa et al. 2010). The mean con-centration of Pb was found 19.20mg/kg in this studywhich was lower than the Dutch Soil Quality Standard(VROM 2000), Canadian Environmental QualityGuidelines (CCME 2003), and Australian Guideline forSoil Quality (DEP 2003) indicating lower contaminationof Pb in soil (Table 3). Lead concentration in soils ofthis study were also compared to other study con-ducted in Bangladesh and other countries and foundthat Pb concentration in this study was lower than theother studies (Tokalıoglu and Kartal 2006, Ahmad andGoni 2010, Acosta et al. 2011, Bhagure and Mirgane2011, Luo et al. 2011, Islam et al. 2014) and higherthan Rahman et al. (2012) and Proshad et al. (2018b)(Table 3).

Source analysis of toxic metals

Pearson’s correlation coefficients for the investigatedmetals are depicted in Table 4. Intermetal interactionsillustrate the sources and pathways of the metals pre-sent in soil. The results highlighted close associationamong correlation coefficient matrix for physiochem-ical properties and heavy metals in soils collected

from industrial vicinity of Jheanaidah and Kushtia dis-tricts. The value of pH showed significant positive cor-relation with silt (r¼ 0.695��) and significant negativecorrelation with clay (r¼�0.641��). Similarly, ECshowed significant positive correlation with sand(r¼ 0.622��) and Pb (r¼ 0.555��) and significant nega-tive correlation with clay (r¼�0.872��). Sand showedsignificant positive correlation with Pb (r¼ 0.476��)and significant negative correlation with silt(r¼�0.785��). Silt showed significant positive correl-ation with Pb (r¼ 0.597��). Clay showed significantpositive correlation with Pb (r¼ 0.548��). Organic mat-ter showed significant positive correlation with Pb(r¼ 0.478��). Cr showed significant positive correlationwith Cu (r¼ 0.443��), Ni showed significant positivecorrelation with Cd (r¼ 0.723��). On the other hand,considering the relationship between the combina-tions showed positive significant relationship whichindicates the parameters were interrelated with eachother and may be originated from the same source tothe study area. Other relationships among the constit-uents of soil were not significant.

PCA has commonly been used for investigatingmetal sources, anthropogenic activities, or soil parentmaterials (Bai et al. 2011, Anju and Banerjee 2012,Cai et al. 2012). Three principal components wereobtained (Table 5 and Figure 2), and those accountedfor 83.4% total variation. In the PCA analysis, first threecomponents were computed and the variancesexplained by them were 51.7%, 21.1%, and 10.7% forsoil. Overall, PCA revealed three major groups of themetals for soil. One group comprised of Ni and Pb insoil which were predominantly contributed byanthropogenic activities. Second group showedmutual association of As, Cd, and Cu in soil whichwere mostly contributed by industrial emissions in thevicinity of the sampling sites (Manzoor et al. 2006).

Table 5. Total variance explained and component matrices for the toxic metals in soils collected from Jhenaidah and Kushtiadistricts, 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 40.12 1.3 21.1 72.7 1.3 21.1 72.7 1.6 26.1 66.23 0.64 10.7 83.4 0.64 10.7 83.4 1.0 17.2 83.44 0.48 8.1 91.55 0.36 6.0 97.56 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 0.479Ni 0.76 �0.326 0.22 0.76 �0.33 0.22Cu 0.86 0.169 �0.31 0.86 0.17 �0.31As 0.83 0.39 �0.153 0.83 0.387 �0.153Cd 0.84 0.09 �0.10 0.84 0.09 �0.10Pb 0.63 �0.46 0.486 0.63 �0.46 0.49

10 T. KORMOKER ET AL.

Third group revealed similar loadings of Cr in soil indi-cated that these were mostly contributed by litho-genic sources. The depositions of atmosphericparticulates released by automobile emissions werebelieved to contribute these metals in the urban areasfrom where the soil samples were collected (Cui et al.2004, Manzoor et al. 2006, Pandey et al. 2012). PCAanalysis revealed that the apportionment of same kindof toxic metals in soil were not similar, which mightbe due to the emission behavior of toxic metals fromthe source to environment.

Ecological risk assessment

Ecological risk assessment for heavy metals contamin-ation in soil was performed following the method-ology developed by Håkanson (1980). In this study, EF,contamination factor (CF), degree of contaminations(Cd), PLI, PER, and toxic units analysis have beenapplied to assess the contamination of toxic metals inagricultural soils near the industrial areas of Jhenaidahand Kushtia districts, Bangladesh.

The EF is a normalization technique that is beingwidely used to categorize the metal fractions that isassociated with soils (Proshad et al. 2019). The calcu-lated values of EF of toxic metals are presented inTable 6. The highest EF value was found in Cd (2.69)and the lowest EF value was found in Cr (0.018).Among the sites, the descending order of EFs was asLokhikol>Udoipur>Dhanharia> Porahati>Chourhas.As a whole, the EF of all the studied metals for allsampling sites were in the descending order ofCd>Cu>As> Pb>Ni>Cr. The higher EF of Cd in

soils indicated higher strong human influence fromindustrial pollution (Rashed 2010).

The contamination factor (Cfi), degree of contamin-

ation (Cd), ecological risk (Eir), and risk index (RI)classes are shown in Table 7. The contamination factor(CF) for individual metal and degree of contamination(Cd) are presented in Table 8. Porahati and Lokhikolsites showed higher contamination of Cr and Ni.Lokhikol site also showed higher contamination of Cu,As, Cd, and Pb. Among the sampling sites, about mostof the samples showed very high contamination forCd concentration in soil, indicating that this metalmight pose a potential risk to the surrounding ecosys-tems (Rashed 2010) which ultimately would degradethe ecological balance. Overall, the Cf

i for all metalswere in the descending order ofCd>As>Cu> Pb>Ni>Cr. The assessment of theoverall contamination of soil was based on the degreeof contamination (Cd). The degree of contamination oftoxic metals were 4.92, 6.14, 12.98, and 7.31 inPorahati, Udoipur, Lokhikol, and Dhanharia in

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

Table 6. Enrichment factor (EF) of toxic metals in soils col-lected from Jhenaidah and Kushtia districts, Bangladesh.Sampling location Cr Ni Cu As Cd Pb

Porahati, Jhenaidah Mean 0.235 0.132 0.314 0.473 0.589 0.092SD 0.053 0.081 0.288 0.409 0.447 0.067

Udoipur, Jhenaidah Mean 0.058 1.067 1.109 0.791 1.379 0.808SD 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 1.695SD 0.129 0.772 0.924 0.621 2.333 1.772

Dhanharia, Jhenaidah Mean 0.055 0.210 0.583 0.521 0.647 0.440SD 0.047 0.134 0.701 0.341 0.540 0.173

Chourhas, Kushtia Mean 0.018 0.206 0.315 0.388 0.481 0.366SD 0.010 0.225 0.408 0.319 0.431 0.247

TOXIN REVIEWS 11

Jhenaidah district, respectively, and 3.59 in Chourhasin Kushtia district. The degree of contaminationshowed low to considerable level of contamination.

The geoaccumulation index (Igeo) values of thestudied metals are presented in Table 9. Among thestudied metals, the Igeo values showed the decreasingorder of Cd>As>Cu> Pb>Cr>Ni at Porahati site;Cd>As> Pb>Cu>Ni>Cr at Dhanharia andChourhas sites; Cd> Pb>As>Cu>Ni>Cr at Udoipursite; and Cd>As>Cu> Pb>Ni>Cr at Lokhikol site. Itwas showed in the table that Cd was heavily contami-nated to extremely contaminated among the threesites. The highest values of Cd might be due to contri-butions from atmospheric emission, leachates fromdefuzed batteries, and Cd-plated items (Islam et al.2015c, Proshad et al. 2019). Others toxic metals wereuncontaminated.

PLI value equal to zero indicates perfection; a valueof one indicates the presence of only baseline level ofpollutants and values above one indicate progressivedeterioration of soil in terms of contamination of thetoxic metals (Tomilson et al. 1980, Rashed 2010, Islamet al. 2015a). The PLI of soils in industrial vicinity ofJhenaidah and Kushtia district are presented in

Figure 3. The PLI values were found 0.42, 0.45, 0.98,0.60, and 0.27, respectively, for Porahati, Udoipur,Lokhikol, Dhanharia, and Chourhas sites. It was shownin the above figure that the contamination of PLI waslow but with the increasing number of industries inthe industrial areas may cause progressive deterior-ation of soils and PLI value will be increased (Bhuiyanet al. 2010).

PER represents the sensitivity of the biological com-munity to the toxic substance and illustrates the PERcaused by the overall contamination (Proshad et al.2019). Combining the PER index of individual metals(Eir) and the PER index of the environment (PER) withtheir grade classifications (Table 7) (Luo et al. 2007),soils from industrial vicinity were classified consider-able to very high PER with Cd and low PER with Cr,Ni, Cu, As, and Pb (Table 10). Cd contributes signifi-cantly to the PER index of the environment (PER)which can be due to the effect from anthropogenicactivities such as application of phosphate fertilizersand industrial activities (ATSDR 2008, Islam et al.2015c). The order of Eir in soils was in the followingdescending order of Cd>As> Pb>Cu>Ni>Cr.The PER of the different sampling sites can be ranked

Table 7. Indices and grades of potential ecological risk of toxic metal pollution (Luo et al. 2007).

Contaminationfactor (Cif )

Contaminationdegree of

individual metalDegree of

contamination (Cd)

Contaminationdegree of theenvironment Eir

Grade ofecological risk ofindividual metal Risk index (PER)

Cif<1 Low Cd<5 Low contamination Eir<40 Low risk RI < 65 Low risk1�Cif<3 Moderate 5�Cd<10 Moderate

contamination40�Eir<80 Moderate risk 65� RI<130 Moderate risk

3�Cif<6 Considerable 10�Cd<20 Considerablecontamination

80�Eir<160 Considerable risk 130� RI<260 Considerable risk

Cif�6 High Cd�20 Highcontamination

160�Eir<320 High risk RI � 260 Very high risk

Eir�320 Very high risk

Table 8. Contamination factor, degree of contamination, and contamination level of toxic metals in soils collected fromJhenaidah and Kushtia districts, Bangladesh.

Sampling sites

Contamination factor (CF)

Degree of contamination Contamination levelCr Ni Cu As Cd Pb

Porahati, Jhenaidah 0.21 0.14 0.41 0.62 3.33 0.22 4.92 LowUdoipur, Jhenaidah 0.02 0.46 0.62 0.42 3.69 0.93 6.14 ModerateLokhikol, Jhenaidah 0.07 0.56 1.49 1.04 7.98 1.84 12.98 ConsiderableDhanharia, Jhenaidah 0.06 0.25 0.85 0.78 4.15 1.23 7.31 ModerateChourhas, 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 �6.90Ni �2.93 �1.18 �0.89 �2.06 �2.58Cu �1.18 �0.60 0.67 �0.14 �1.42As 0.09 �0.46 0.86 0.44 �0.61Cd 2.89 3.03 4.15 3.20 2.16Pb �2.52 �0.45 0.53 �0.05 �0.96

12 T. KORMOKER ET AL.

in the following order:Lokhikol>Dhanharia>Uoipur> Porahati>Chourhas.In Lokhikol site, potential risk value was 270 and thedegree of pollution was very high. In Porahati,Udoipur, and Chourhas sites, PER values were 110,125, and 70, respectively, and degree of pollution wasmoderate. In Dhanharia, potential risk value was 144and the degree of pollution was considerable.

Potential acute toxicity of hazardous elements insoil samples can be estimated as the sum of toxicunits (RTUs), defined as the ratio of the determinedconcentration of metal in soil to probable effect levels(PELs) (Zheng et al. 2008, Islam et al. 2015c). The sumtoxic units for toxic metals in different soil samplingsites are presented in Figure 4. In Porahati, Udoipur,

Lokhikol, Dhanharia, and Chourhas sites, the toxicunits were 1.364, 1.871, 3.356, 1.945, and 1.026,respectively. The sum of toxic units for all the sam-pling sites was <4, indicating low toxicity of metals.

Health risk assessment

Heavy metals present in soils may have an impact onhuman health (Okorie et al. 2011). In the industrialareas, the risks of toxic elements in industrial, wasteburning sites, waste thronging sites and brick fieldsare important for the exposure through ingestion, der-mal contact, and inhalation (Zheng et al. 2008).According to the risk assessment approach, noncarci-nogenic risks of toxic metals through three exposure

0

0.2

0.4

0.6

0.8

1

1.2

Porahati Udoipur Lokhikol Dhanharia ChourhasP

ollu

tion

load

inde

x va

lue

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 andKushtia districts, Bangladesh.

Sampling sites

Potential ecological risk factor (Eir)

Potential risk (PER) Pollution degreeCr Ni Cu As Cd Pb

Porahati, Jhenaidah (n¼ 9) 0.42 0.81 2.1 6.2 99.8 1.1 110 ModerateUdoipur, Jhenaidah (n¼ 13) 0.04 2.8 3.1 4.2 110.6 4.7 125 ModerateLokhikol, Jhenaidah (n¼ 9) 0.14 3.4 7.4 10.4 239.5 9.2 270 Very highDhanharia, Jhenaidah (n¼ 13) 0.11 1.5 4.2 7.8 124.4 6.1 144 ConsiderableChourhas, Kustia (n¼ 14) 0.03 1.04 1.74 3.8 60.5 3.3 70 Moderate

0

0.5

1

1.5

2

2.5

3

3.5

4

Porahati Udoipur Lokhikol Dhanharia Chourhas

Toxi

c un

it v

alue

s

Sampling sites

Cr Ni Cu As Cd Pb

Figure 4. Toxic unit (TU) analysis of toxic metals in soils collected from Jhenaidah and Kushtia districts, Bangladesh.

TOXIN REVIEWS 13

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CrNi

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CdPb

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Adult

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2.59E�08

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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

Udo

ipur,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

Dhanh

aria,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

Chou

rhas,K

ustia

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

TotalC

DI

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

Contam

inationof

concern

No

No

No

No

No

No

Chronicdaily

intake

ofheavymetalsdu

eto

derm

alcontact

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

Udo

ipur,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

Dhanh

aria,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

Chou

rhas,K

ustia

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

TotalC

DI

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

Contam

inationof

concern

No

No

No

No

No

No

Chronicdaily

intake

oftoxicmetalsdu

eto

inhalatio

nPorahati,

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

Udo

ipur,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

Dhanh

aria,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

Chou

rhas,K

ustia

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

TotalC

DI

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

Contam

inationof

concern

No

No

No

No

No

No

14 T. KORMOKER ET AL.

pathways were characterized in this study. To evaluatethe risk, the CDIs, HQs, HI, and carcinogenic risk of thestudied metals were estimated for adult male, adultfemale, and children and the results are presented inthis 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 wasused to determine CDI of heavy metals from ingestion(CDI). We assume long-term exposure for 30 years foradult male and adult female and 6 years for childrenas the worst-case default assumption. The estimatedCDI values for all studied toxic metals were remaininglower than the standard guideline values. On the basisof ingestion daily exposure, there is low chance topose public health effect concerns for both adult andchildren from soil ingestion. Again, CDI for ingestionwas found highest in children than adult male andadult female. This may be the result of lower bodyweight of children than the adult. The dermal contactof toxic metals from soil is considered another import-ant pathway of exposure. There may be several waysto expose metals due to dermal contact from soil likeworking, wading, playing, etc. The estimated CDI fromdermal contact for all studied toxic metals wereremaining lower than the standard guideline values.Due to inhalation, the CDI of metals was negligible inthis study.

The potential noncarcinogenic toxic effects posedby toxic metals are usually characterized by calculatingHQ. The HQs of individual metal are presented inTable 12. If the HQ value is higher than one thenthere will be adverse health effects associated withover exposure (USEPA 1989, 2001, Zabin et al. 2008,Qu et al. 2012, Genthe et al. 2013). The noncancerhealth risks related to individual element exposurethrough soil ingestion, dermal contact, and inhalationwas low for all the investigated metals resulted in aHQ < 1, indicating low risk for both adultsand children.

The combined effects of exposed metals and metal-loids were calculated as HI and the data indicated thatthe HI values were also lower than one (Figure 5).However, when considering the total exposure HI ofingestion, dermal contact, and inhalation, there waslower chance of having noncancer risk for adults andchildren health at all the studied sites. The hazard riskindex values for children were higher adult inhabi-tants, indicating children may pose noncancer risk inthe future. The total target hazard quotients (TTHQ)for children was higher due to touching and mouthingof dust contaminated particles, direct ingestion byTa

ble12.Target

hazard

quotient

(THQ)of

toxicmetalsthroug

hingestion,

derm

al,and

inhalatio

nof

contam

inated

soils.

CrNi

CuAs

CdPb

Samplingsites

Adultmale

Adult

female

Children

Adultmale

Adult

female

Children

Adultmale

Adult

female

Children

Adultmale

Adult

female

Children

Adultmale

Adult

female

Children

Adultmale

Adult

female

Children

Porahati,

Jhenaidah

0.0018

0.0019

0.0061

0.0001

0.0001

0.0004

0.0001

0.0001

0.0004

0.0075

0.0081

0.0260

0.0006

0.0006

0.0019

0.0004

0.0004

0.0012

Udo

ipur,Jhenaidah

0.0002

0.0002

0.0006

0.0004

0.0005

0.0015

0.0002

0.0002

0.0007

0.0051

0.0055

0.0177

0.0006

0.0007

0.0022

0.0015

0.0016

0.0052

Lokhikol,Jhenaidah

0.0006

0.0006

0.0021

0.0005

0.0006

0.0019

0.0005

0.0005

0.0016

0.0127

0.0137

0.0440

0.0013

0.0015

0.0047

0.0029

0.0032

0.0102

Dhanh

aria,Jhenaidah

0.0005

0.0005

0.0017

0.0002

0.0003

0.0008

0.0003

0.0003

0.0009

0.0095

0.0103

0.0331

0.0007

0.0007

0.0024

0.0020

0.0021

0.0068

Chou

rhas,K

ustia

0.0001

0.0001

0.0004

0.0002

0.0002

0.0006

0.0001

0.0001

0.0004

0.0046

0.0050

0.0159

0.0003

0.0004

0.0012

0.0011

0.0011

0.0036

TOXIN REVIEWS 15

hand to mouth activities, and play behavior (Mielkeet al. 1999). The ingestion of greater amounts of smallparticles may have greater impact on children becauseof their small body weight than adult.

The carcinogenic risk of As and Pb for adults arepresented in Table 13. The carcinogenic risks from Asand Pb at all sites via ingestion, dermal contact, andinhalation were in acceptable ranges. The total cancerrisk of As and Pb was 1.43E� 05 and 4.54E� 07 foradult male; 1.54E� 05 and 4.54E� 07 for adult female;6.97E� 07 and 4.55E� 07 for children. The carcino-genic risks of As and Pb due to exposure from studiedsoil via ingestion, dermal contact, and inhalation path-ways can be negligible in the industrial areas ofJhenaidah and Kushtia districts, Bangladesh. Amongthe three exposure pathways, the ingestion of soilseems to be the major pathway of exposure to haz-ardous elements followed by dermal contact andinhalation. Hazardous elements could be accumulatedin human for a long time and especially noncanceradverse effects of these toxic metals to the tissues of

adult population can become more serious. Accordingto the result of this study, health risk for adult andchildren due to toxic metal exposure through soilcould not be overlooked.

Conclusions

Contamination of six toxic metals (Cr, Ni, Cu, As, Cd,and Pb) were investigated near the industrial areas ofJhenaidah and Kushtia districts, Bangladesh. The majorfindings of the study revealed that Cd concentrationsin some sampling sites exceeded the Dutch standardand Canadian quality guidelines values, representingthat the studied soils were heavily contaminated byCd. The EF, geoaccumulation index, contamination fac-tor, PLI, and toxic unit analysis values were found safefor all metals except Cd. PER showed moderate tovery high degree of contamination. It is necessary tofurther study to find out the main reasons for thehigher PER mainly caused by Cd in the study area.The noncancer risks related to individual elementexposure through soil ingestion, dermal contact, andinhalation showed low risk for both adults and chil-dren. The carcinogenic risks from As and Pb at all siteswere in acceptable ranges. But concern is that long-term exposure of these metals can pose cancer risksfor both adults and children.

Acknowledgments

The authors thank the authority of Patuakhali Science andTechnology University (PSTU), Bangladesh and YokohamaNational University, Japan for providing laboratory facilitiesto complete this study. Furthermore, the authors are thank-ful for the kind help from the members Patuakhali Science

0

0.01

0.02

0.03

0.04

0.05

0.06

0.07

Porahati Udoipur Lokhikol Dhanharia Chourhas

Haz

ard

inde

x va

lue

Sampling location

Adult male Adult female Children

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, andchildren due to ingestion, dermal contact, and inhalation ofarsenic and lead in soils.

Exposure pathways Arsenic (As) Lead (Pb)

Adult male Ingestion 6.06E� 08 7.95E� 10Dermal contact 1.42E� 05 4.53E� 07Inhalation 5.33E� 09 3.44E� 11

Adult female Ingestion 6.53E� 08 8.56E� 10Dermal contact 1.53E� 05 4.53E� 07Inhalation 5.33E� 09 3.44E� 11

Children Ingestion 1.62E� 07 2.12E� 09Dermal contact 5.30E� 07 4.53E� 07Inhalation 5.33E� 09 3.44E� 11

Total risk (adult male) 1.43E� 05 4.54E� 07Total risk (adult female) 1.54E� 05 4.54E� 07Total risk (children) 6.97E� 07 4.55E� 07

16 T. KORMOKER ET AL.

and Technology University, Bangladesh during thefield sampling.

Disclosure statement

The authors declare that there are no conflicts of interest.

ORCID

Ram Proshad http://orcid.org/0000-0002-4878-9616

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