Bioresource Technology 101 (2010) 5043–5053

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Bioresource Technology

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Review

Biosorption of heavy metal ions using wheat based biosorbents – A reviewof the recent literature

Umar Farooq a,b,*, Janusz A. Kozinski a, Misbahul Ain Khan b,c, Makshoof Athar c

a College of Engineering, University of Saskatchewan, SK, Canada S7N 5A9b Department of Chemistry, The Islamia University of Bahawalpur, Bahawalpur, Pakistanc Institute of Chemistry, University of the Punjab, Lahore, Pakistan

a r t i c l e i n f o a b s t r a c t

Article history:Received 16 September 2009Received in revised form 3 February 2010Accepted 7 February 2010Available online 12 March 2010

Keywords:Triticum aestivumStrawBranBiosorptionMetal ions

0960-8524/$ - see front matter � 2010 Elsevier Ltd. Adoi:10.1016/j.biortech.2010.02.030

* Corresponding author. Address: College of Engineewan, SK, Canada S7N 5A9.

E-mail address: umar.farooq@usask.ca (U. Farooq)

Conventional technologies for the removal/remediation of toxic metal ions from wastewaters are provingexpensive due to non-regenerable materials used and high costs. Biosorption is emerging as a techniqueoffering the use of economical alternate biological materials for the purpose. Functional groups like car-boxyl, hydroxyl, sulphydryl and amido present in these biomaterials, make it possible for them to attachmetal ions from waters.

Every year, large amounts of straw and bran from Triticum aestivum (wheat), a major food crop of theworld, are produced as by-products/waste materials. The purpose of this article is to review rather scat-tered information on the utilization of straw and bran for the removal/minimization of metal ions fromwaters. High efficiency, high biosorption capacity, cost-effectiveness and renewability are the importantparameters making these materials as economical alternatives for metal removal and waste remediation.Applications of available adsorption and kinetic models as well as influences of change in temperatureand pH of medium on metal biosorption by wheat straw and wheat bran are reviewed. The biosorptionmechanism has been found to be quite complex. It comprises a number of phenomena including adsorp-tion, surface precipitation, ion-exchange and complexation.

� 2010 Elsevier Ltd. All rights reserved.

1. Introduction

Heavy metal ions have lethal effects on all forms of life and theseenter the food chain through the disposal of wastes in water chan-nels. From among various metal ions, lead, mercury, cadmium andchromium(VI) are at the top on the toxicity list (Volesky, 1994). Dueto non-biodegradability, metal ions accumulate and their amountsare increased along the food chain. Hence, their toxic effects aremore pronounced in the animals at higher trophic levels. Sourcesand toxicity of certain metal ions are listed in Table 1.

Owing to the toxic effects, the industries are advised that thewaste waters be treated systematically to remove/minimize themetal contents in their wastes. A number of methods are alreadyat operation and Table 2 compares selective techniques used forthe purpose. Adsorption by activated carbon is the most efficientclassical way as it removes more than 99% of certain metal ionsbut the cost of its production is prohibitive and it can not be regen-erated and recycled. Generally, the materials employed in thesemethods are highly expensive and capital costs are much too highto be economical. These methods mostly treat the metal ions as a

ll rights reserved.

ering, University of Saskatch-

.

‘waste’ only and eliminate recycling of materials. Some of themethods (e.g., precipitation and coagulation) produce concen-trated and further toxic wastes, creating yet another disposal prob-lem. Moreover, there are concentration limits to which thesemethods are economical and become ineffective or too expensiveto treat wastes having metal ions in concentrations of 100 mg/Lor below (Ceribasi and Yetis, 2001). Hence, there is a constant needto search for an optimal technology while considering its cost,materials employed and its efficiency.

2. Biosorption – an alternative solution

Biosorption is the removal of materials (compounds, metal ions,etc.) by inactive, non-living biomass (materials of biological origin)due to ‘‘high attractive forces” present between the two (Voleskyand Holan, 1995).

Living as well as dead (metabolically inactive) biological mate-rials have been sought to remove metal ions. It was found that var-ious functional groups present on their cell wall offer certain forcesof attractions for the metal ions and provide a high efficiency fortheir removal (Ashkenazy et al., 1997; Kuyucak and Volesky,1988). The mechanisms of uptake by living materials (bioaccumu-lation) and removal by dead ones (biosorption) are entirelydifferent. Use of dead materials has several advantages because

Table 1Sources and toxic effects of heavy metals on human beings.

Metal Source Toxic effect References

Lead Electroplating, manufacturing of batteries,pigments, ammunition

Anaemia, brain damage, anorexia, malaise, loss ofappetite, diminishing IQ

Gaballah and Kilbertus (1998), Low et al.(2000), Volesky (1993)

Cadmium Electroplating, smelting, alloy manufacturing,pigments, plastic, mining, refining

Carcinogenic, renal disturbances, lung insufficiency,bone lesions, cancer, hypertension, Itai–Itai disease,weight loss

Chen and Hao (1998), Godt et al. (2006), Lowet al. (2000), Sharma (1995), Singh et al. (2006)

Mercury Weathering of mercuriferous areas, volcaniceruptions, naturally-caused forest fires,biogenic emissions, battery production, fossilfuel burning, mining and metallurgicalprocesses, paint and chloralkali industries

Neurological and renal disturbances, impairment ofpulmonary function, corrosive to skin, eyes, muscles,dermatitis, kidney damage

Boening (2000), Manohar et al. (2002), Morelet al. (1998)

Chromium(VI)

Electroplating, leather tanning, textile, dyeing,electroplating, metal processing, woodpreservatives, paints and pigments, steelfabrication and canning industry

Carcinogenic, mutagenic, teratogenic, epigastric painnausea, vomiting, severe diarrhoea, producing lungtumors

Dupont and Guillon (2003), Granados-Correaand Serrano-Gómez (2009), Kobya (2004),Singh et al. (2009)

Arsenic Smelting, mining, energy production fromfossil fuels, rock sediments

Gastrointestinal symptoms, disturbances ofcardiovascular and nervous system functions, bonemarrow depression, haemolysis, hepatomegaly,melanosis, polyneuropathy and encephalopathy, livertumor

Chilvers and Peterson (1987), Dudka andMarkert (1992), Robertson (1989)

Copper Printed circuit board manufacturing,electronics plating, plating, wire drawing,copper polishing, paint manufacturing, woodpreservatives and printing operations

Reproductive and developmental toxicity,neurotoxicity, and acute toxicity, dizziness, diarrhoea

Chuah et al. (2005), Papandreou et al. (2007),Yu et al. (2000)

Zinc Mining and manufacturing processes Causes short term ‘‘metal-fume fever”,gastrointestinal distress, nausea and diarrhoea

WHO (2001)

Nickel Non-ferrous metal, mineral processing, paintformulation, electroplating, porcelainenameling, copper sulphate manufacture andsteam-electric power plants

Chronic bronchitis, reduced lung function, lungcancer

Akhtar et al. (2004), Ozturk (2007)

Table 2Some methods to remove metal ions from Wastewaters.

Method Advantages Disadvantages

Chemical Precipitation � Simple� Inexpensive� Most of metals can be removed

� Large amounts of sludge produced� Disposal problems

Chemical coagulation � Sludge settling� Dewatering

� High cost� Large consumption of chemicals

Ion-exchange � High regeneration of materials� Metal selective

� High cost� Less number of metal ions removed

Electrochemical methods � Metal selective� No consumption of chemicals� Pure metals can be achieved

� High capital cost� High running cost� Initial solution pH and Current density

AdsorptionUsing activated carbon � Most of metals can be removed

� High efficiency (>99%)� Cost of activated carbon� No regeneration� Performance depends upon adsorbent

Using natural zeolite � Most of metals can be removed� Relatively less costly materials

� Low efficiency

Membrane process and ultrafilteration � Less solid waste produced� Less chemical consumption� High efficiency (>95% for single metal)

� High initial and running cost� Low flow rates� Removal (%) decreases with the presence of other metals

Source: (O’Connell et al. 2008).

5044 U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053

there is no need of growing, no growth media is required and thesematerials are available as wastes or by-products. Biomass from al-gae (Hamdy, 2000; Seki and Suzuki, 1998), fungi (Guibal et al.,1992; Kapoor et al., 1999), bacteria (Ozturk, 2007; Pumpel et al.,1999), sea-weeds (Elangovan et al., 2008; Murphy et al., 2008),some higher plants (Joshi et al., 2003; Rahman et al., 2005), all ofthese have been effectively and successfully utilized in metal re-moval studies.

Volesky has shared his views about the biosorption process inhis recent review (Volesky, 2007). He stated that currently ‘biosorp-tion of metals’ is only the ‘tip of the ice-berg’ and in future, it mustfocus on utilization for purification and recovery of high valued pro-teins, steroids and drugs, that cost in thousands of dollars per gram.

He termed this form to be ‘‘the best biosorption”. Apart from Vole-sky’s groups, a number of review articles have been published byseveral researchers. Recently, Sud et al. (2008) reviewed the useof certain cellulosic agricultural waste materials for the removalof heavy metal ions. Ahluwalia and Goyal (2007) have collectedthe dispersed information, covering from 1981 to 2006, about theuse of microbial and certain plants derived biomass types. Simi-larly, use of Saccharomyces cerevisiae was compiled by Wang andChen (2006). A number of other reviews are available in the litera-ture (Davis et al., 2003; Lodiero et al., 2006; Nurchi and Villaescusa,2008; Romera et al., 2006; Shukla et al., 2002).

Research in biosorption suggests the following advantages overother techniques (Modak and Natarajan, 1995).

U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053 5045

� The materials can be found easily as wastes or by-products andat almost no cost.

� There is no need of costly growth media.� The process is independent of physiological constraints of living

cells.� Process is very rapid, as non-living material behaves as an ion-

exchange resin, metal loading is very high.� The conditions of the process are not limited by the living bio-

mass, no aseptic conditions required.� Process is reversible and metal can be desorbed easily thus recy-

cling of the materials is quite possible.� Chemical or biological sludge is minimized.

However, there are certain disadvantages as well;

� Irrespective of the value of the metal, it needs to be desorbedfrom the material to be further re-employed.

� The characteristics of the biosorbents can not be biologicallycontrolled.

3. Wheat based materials – new biosorbents

Among biological materials, agricultural materials usually playan important role due to being widely and easily produced. Foodcrops are being cultivated all over the world (e.g., sugar cane, rice,corn, wheat, etc.) and the parts other than fruit, grain, juice etc. areavailable for biosorption experimentation. In 2007, world wheatproduction was 610.6 million tonnes including a share of 23.3 mil-lion tonnes from Pakistan and 20.1 million tonnes from Canada(Annual Report, 2009). The straw and bran of wheat, Triticum aes-tivum, are two main ‘wastes’ produced in large amounts. Its strawhas found use as fodder and in paper industry to produce low qual-ity boards or packing materials. The stems are burnt directly insome parts of the world for energy purposes, adding seriously toatmospheric pollution and wastage of resources.

Ali et al. (1991) and Lawther et al. (1995) are among theresearchers who have been investigating the composition andstructure of wheat straw. The main components found, are cellu-lose (37–39%), hemicellulose (30–35%), lignin (�14%) and sugarsas well as other compounds carrying different functional groupslike carboxyl, hydroxyl, sulphydryl, amide, amine etc. The percent-age composition of different substances varies in different parts ofthe world, although the substances are almost similar. Cellulose isa proven adsorbent and has been employed previously for adsorp-tion chromatographic studies (Acemioglu and Alma, 2001; Grover,1974; Peterson and Sober, 1956). The scanning electron micro-graph (SEM) of wheat straw (figure not shown) reveals that thesurface is porous and thus suitable for adsorption of metal ions.Presence of different functional groups, large amounts of celluloseand the porosity of surface demand that such a material should beused for biosorption studies.

Table 3Use of straw from Triticum aestivum for the removal of metal ions in a batch system.

Metal ion Optimum time (min) pH Removal (%

Cd(II) 210 6 –60 5 –

Pb(II) 15 6 >85Cu(II) 210 6 –Cr(III) 10–20 5 –Ni(II)a – – –Zn(II)a – – –

a Using continuous flow reactor.

Determining metal uptake by a biosorbent is required in orderto express its quality. Different research groups have used two dif-ferent scales i.e., percent removal (R%) and ‘q’ or ‘qe’ (mg/g) value.

Rð%Þ ¼ C0 � Ce

C0� 100 ð1Þ

and

qðqeÞ ¼C0 � Ce

m� v ð2Þ

where C0 and Ce are initial and equilibrium metal ion concentrations(mg/L), v is the volume (L), m is dry weight of biomass used (g) andq (or qe) is the mount of metal ions sorbed per gram of biomass (mg/g). Between the two, q value is considered a better tool to expressand compare the capacities of different biomass types. Units of q de-pend upon the purpose of exercise. Engineers use ‘mg per gram ofdry sorbent’ and chemists use ‘mmol per gram’ or ‘meq per gram’for stoichiometric purposes, but there is no definitive rule. Percent-age removal gives no information about the amount of biomassused and, sometimes, can be misleading while comparing differentbiomaterials (Volesky and Holan, 1995).

This article offers a review of the use of bran and straw fromTriticum aestivum for the removal/minimization of metal ions.

4. Applications of wheat straw (WS) in metal removal

Straw from wheat has successfully been used to study its bio-sorptive behaviour from aqueous solution of single metal ions (Ta-ble 3). Chojnacka (2006) studied the feasibility of using groundstraw to remove less toxic metal Cr(III) ions. The process was quitefast and equilibrium reached in less than 20 min (Chojnacka et al.2005). Farooq et al. (2007) reported a study for the removal ofPb(II) ions using ground straw. More than 85% of metal ions pres-ent were removed in just 15 min. The mechanism proposed wasbased on adsorption along with a strong contribution from Hydro-gen ion-exchange mechanism. Doan et al. (2008) observed thesorptive removal of Zn(II) and Ni(II) ions in a fixed bed of wheatstraw using single metal as well as bi-metal solutions. They ob-served that Zn(II) ions caused the biosorption of Ni(II) to decreaseup to 14% when a bi-metal solution was used. Tan and Xiao (2009)as well as Dang et al. (2009), independently, studied the sorption ofCd(II) ions. The process was, again, found to be a quick removal ofmost of the metal contents in less than 20 min, although equilib-rium was attained after a longer time (2–4 h). The amount of metalsorbed was almost comparable in both of the results. Dang et al.(2009) also studied the sorption of Cu(II) ions. They were able toremove 11.4 mg of copper per gram of WS. They further stated thatWS capacity for Cd(II) was 27% higher than that of Cu(II). The sorp-tion of different metal ions by straw shows promising results andneeds for further investigation.

) Amount of metal sorbed (mg/g) References

14.56 Dang et al. (2009)11.60 Tan and Xiao (2009)– Farooq et al. (2007)11.43 Dang et al. (2009)21.0 (36 �C) Chojnacka (2006)– Doan et al. (2008)– Doan et al. (2008)

Table 4Use of bran from Triticum aestivum for the removal of metal ions.

Metal ion Optimum time (min) pH Removal (%) Amount of metal sorbed (mg/g) References

Cd(II) 110 8.6 87.15 (20 �C) – Singh et al. (2006)b 60 5 – 51.58 Nouri and Hamdaoui (2007)

25 5 – 15.71 (20 �C) Nouri et al. (2007)20 5 – 21.0 Farajzadeh and Monji (2004)

Pb(II) 60 4–7 – 87.0 (60 �C) Bulut and Baysal (2006)20 5 – 62.0 Farajzadeh and Monji (2004)

Cr(VI)c 24 ha >4 – 35 Dupont and Guillon (2003)12 ha 1 – 40.8 Wang et al. (2008)110 2 – 310.58 Singh et al. (2009)60 2 87.8 0.942 Nameni et al. (2008)

Cr(III) 20 5 – 93.0 Farajzadeh and Monji (2004)

Cu(II)c 24 ha 4.5 12.7 Dupont et al. (2005)3 ha 6 – 17.42 (60 �C) Aydın et al. (2008)120 5 – 8.34 Basci et al. (2004)60 5 – 6.85 Wang et al. (2009)

d 30 5 – 51.5 (60 �C) Ozer et al. (2004)20 5 – 15.0 Farajzadeh and Monji (2004)

Zn(II)c 24 ha 6.5 16.4 Dupont et al. (2005)

Ni(II) 20 5 12.0 Farajzadeh and Monji (2004)

Hg(II) 20 5 70 Farajzadeh and Monji (2004)

a Time in hours.b Using ultrasounds and stirring simultaneously.c Using lignocellulosic substrate from wheat bran.d Using dehydrated wheat bran.

5046 U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053

5. Applications of wheat bran (WB) in metal removal

Bran is another by-product obtained from wheat crops that hasbeen studied to explore its biosorption properties towards metalions in single metal solutions. There is more literature available onthe use of WB than WS (Tables 3 and 4). Bulut and Baysal (2006) re-ported the use of WB against Pb(II) ions having capacity of 87 mg/g,in almost 60 min. Removal of cadmium ions has been studied by dif-ferent groups (Nouri et al., 2007; Nouri and Hamdaoui, 2007; Singhet al., 2006). The sorption capacity was found to be different in eachcase. Nouri and Hamdaoui (2007) reported the use of ultrasonics(40 kHz, 9.5 W) in Cd-biosorption, with and without stirring thecontents of biosorption system. It was observed that ultrasoundshad no effects on the equilibrium time and optimum pH but causeda drastic change in the activation energy of Cd-WB physiosorptionfrom +11.19 to �14.71 kJ/mol. As a result, the monolayer sorptioncapacity (maximum amount of metal sorbed) increased from22.78 to 51.81 mg/g. Chromium (VI) ions were also removed usingWB by different research groups (Dupont and Guillon, 2003; Nameniet al., 2008; Singh et al., 2009; Wang et al., 2008). The capacity of WBwas reported to be different in each case. This variation in metalcapacities corresponds to variation in the structure of WB used indifferent studies, along with other parameters. The differences inthe origin, area, soil and kind of wheat from where WB was obtained,may explain such a variation in results.

Biosorption of Cu(II) ions using WB was reported by severalauthors (Aydın et al., 2008; Basci et al., 2004; Dupont et al.,2005; Farajzadeh and Monji, 2004; Ozer et al., 2004; Wang et al.,2009). A variation in the biosorption capacity can be seen in Ta-ble 4. It can be explained in a similar way as discussed above, incase of Cr(VI) ions. Ozer et al. (2004) reported that dehydratingthe WB caused an increase in the copper sorption capacity. Dupontet al. (2005) studied sorption of Cu(II) and Zn(II) on a lignocellu-losic substrate extracted from WB and found that it exhibited com-parable affinity for the metal ions. Farajzadeh and Monji (2004)reported the use of WB for a number of metal ions from their aque-ous solutions. The results were very promising. The comparatively

fast process and encouraging results urge the use of WB for furtherinvestigations.

The equilibrium times for metal biosorption by both WS andWB have been found to be relatively shorter than widely utilizedalgae, sea-weeds (Dönmez et al., 1999; Suzuki et al., 2005; Vald-man and Leite, 2000).

6. Equilibrium models

The equilibrium models are extensively used to investigate theamounts of metal ions sorbed by a certain biomass. The distributionof metal ions between solution and biomass is a measure of the po-sition of equilibrium and can be expressed by one or more isotherms.Lanmguir model, Freundlich model, Tempkin model and Dubinin–Radushkevich (D–R) model are some examples and among thesemost common are the monolayer adsorption developed by Lang-muir and the muilti-layer adsorption Freundlich models.

According to Langmuir, the sorption occurs at the surface of thesorbent in a homogeneous way and the atoms/ions form a mono-layer, having no mutual interactions, on the sorbent surface.Although it gives no information about the mechanism, it is stillused to obtain the uptake capacities of the sorbents. It is shown as

qe ¼qmaxbCe

1þ bCeð3Þ

where ‘qe’ is the amount of metal sorbed at equilibrium (mg/g),‘qmax’ is the monolayer sorption capacity (mg/g), ‘b’ is Langmuirconstant, ‘Ce’ is concentration of metal ions in solution at equilib-rium. The linear form is

Ce

qe¼ Ce

qmaxþ 1

bqmaxð4Þ

There must be a straight line with slope of (1/qmax) and an interceptof (1/b qmax) when a plot of (Ce/qe) versus Ce is drawn. Langmuirmodel can be further used to calculate the specific surface area‘SL’ (m2/g) for the monolayer coverage of certain metal ion on a

U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053 5047

specific biosorbent (Ho et al. 2002). For ‘qmax’ being the biosorptioncapacity (mg/g), ‘N’ the Avogadro number (6.022 � 1023), ‘A’ thecross sectional area of metal ion (ÅA

02) and ‘M’ the molecular mass

of metal ion, it can be calculated as follows

S ¼ qmaxNAM

ð5Þ

Freundlich isotherm model considers the non-ideal sorption onheterogeneous surfaces in a multilayer way. It is shown as

qe ¼ Kf C1=ne ð6Þ

where Kf and 1/n are Freundlich constants. The linear form is asunder

ln qe ¼ ln Kf þ1n

ln Ce ð7Þ

A plot of ‘ln qe’ versus ‘ln Ce’ should yield a straight line with ‘1/n’ asslope and ‘ln Kf’ as intercept.

Equilibrium models followed by metal-WS and metal-WB sys-tems are listed in Tables 5 and 6. It can be observed that in mostof the cases, Langmuir model was successfully applied pointingto the most metal ions sorbed in monolayer fashion and thatadsorption played an important role in the mechanism of biosorp-tion. The feasibility of Langmuir isotherm can be expressed by adimensionless constant separation factor or the equilibriumparameter RL defined as

RL ¼1

1þ bC0ð8Þ

‘b’ being the Langmuir constant and C0 the initial concentration ofmetal (mg/L). It indicates the shape as well as the feasibility ofthe isotherm (McKay et al., 1982). The value of RL indicates the typeof isotherm to be unfavourable (RL > 1), linear (RL = 1), irreversible

Table 5Isotherm, kinetic and thermodynamic data for the use of straw from Triticum aestivum for

Metal ion Equilibrium model Kinetic model

Cd(II) Langmuir Pseudo second orderLangmuir Pseudo second order

Pb(II) Freundlich –Cu(II) Langmuir Pseudo second orderCr(III) Freundlich Pseudo second order

Table 6Isotherm, kinetic and thermodynamic data for the use of bran from Triticum aestivum for

Metal ion Equilibrium model Kinetic model

Cd(II) Langmuir First ordera Lanmuir Pseudo second order

Langmuir Pseudo second orderPb(II) Langmuir Pseudo second orderCr(VI) Langmuir Pseudo second order

Langmuir Pseudo second orderFreundlich –

b Langmuir –Cr(III)Cu(II) Langmuir Pseudo second orderc Langmuir Pseudo second order

Langmuir Pseudo second orderb Langmuir –Zn(II)b Langmuir –

a Using ultrasounds and stirring simultaneously.b Using lignocellulosic substrate from wheat bran.c Using dehydrated wheat bran.

(RL = 0) or favourable (0 > RL > 1) (Hall et al., 1966). A plot of RL vs.C0 will show the type of isotherm. RL values further indicate the or-der of preference or selectivity for biosorption of certain metal ionsby some specific biosorbent (Ho et al. 2002). This may be helpful indesigning the study (experiments) for multi-metal ion systems.

The physical or chemical nature of adsorption can be deter-mined by calculating the mean free energy of adsorption ‘E’ usingthe following equation

E ¼ 1ffiffiffiffiffiffiffiffiffiffiffiffiffi2 � b

p ð9Þ

The value of ‘b’ can be determined from Dubinin–Radushkevich (D–R) model as follows,

qe ¼ qmax expð�be2Þ ð10Þ

where ‘b’ is a coefficient related to the mean free energy of adsorp-tion (mol2/J) and ‘e’ is Polanyi potential (J/mol) that can be writtenas

e ¼ RT ln 1þ 1Ce

� �ð11Þ

Linear form of D–R model can be written as

ln qe ¼ ln qmax � be2 ð12AÞ

or

ln qe ¼ ln qmax � b � RT ln 1þ 1Ce

� �� �2

ð12BÞ

The slope of the plot of ‘ln qe’ vs ‘e2’ will give the value of ‘b’. Thevalue of E will decide the nature of adsorption. The adsorption pro-cess will be a physical adsorption for E < 8 kJ/mol and it will be achemical adsorption or chemisorption for 8 < E < 16 kJ/mol. This

the removal of metal ions.

Thermodynamic parameters References

DH (kJ/mol) DS (J/mol K)

– – Tan and Xiao (2009)– – Dang et al. (2009)– – Farooq et al. (2007)– – Dang et al. (2009)– – Chojnacka (2006)

the removal of metal ions.

Thermodynamic parameters References

DH (kJ/mol) DS (J/mol K)

�38.535 �115.585 Singh et al. (2006)– – Nouri and Hamdaoui (2007)22.17 �141.3 Nouri et al. (2007)11.55 60 Bulut and Baysal (2006)22.514 �79.452 Singh et al. (2009)– – Nameni et al. (2008)143.105 451.395 Wang et al. (2008)– – Dupont and Guillon (2003)

10.60 108.02 Wang et al. (2009)2.85 95.44 Ozer et al. (2004)

Basci et al. (2004)18.791 105 Aydın et al. (2008)– – Dupont et al. (2005)– – Dupont et al. (2005)

Table 7Specific surface area values of some commonly used materials in comparison with WS.

Material Particle size (�10�6 m) Average pore diameter (�10�10 m) Specific surface area (m2/g) References

Granular activated carbon (Filtrasorb 400) – – 1100 Ozacar and Sengil (2002)Activated carbon from pine wood 120–200 33.2 902 Tseng et al. (2003)Yellow passion-fruit shell (Brazil) <500 – 40 Jacques et al. (2007)Wheat straw 100–200 127.8 8.17 Unpublished dataSargassum sp. – 34.76 8.13 Sheng et al. (2008)Wood – – 3.8–6.4 Poots et al. (1976)Moringa oleifera 105 – 4.01 Kumari et al. (2006)Lamarck seedsSpirogyra sp. 60–90 – 1.31 Gupta and Rastogia (2008)Waste pomace of olive oil factory 150–250 – 1.24 Nuhoglu and Malkoc (2009)Soy meal shell <125 – 0.76 Arami et al. (2006)Rubber tree leaves <500 154.6 0.48 Ngah and Hanafiah (2008)Rice bran 150–425 320 � 104 0.46 Montanher et al. (2005)

5048 U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053

will help understanding the mechanism of biosorption (Dang et al.,2009).

An important key factor that helps in explaining the metal bio-sorption is the ‘‘available surface area” of biosorbent. The surfacearea is calculated by employing Brunauer–Emett–Teller (BET)adsorption isotherm using nitrogen as the adsorbate (Brunaueret al., 1938).

1v ½ðP0=PÞ � 1� ¼

c � 1vmc

PP0

� �þ 1

vmcð13Þ

where P and P0 are the equilibrium and saturation pressure of nitro-gen at temperature of adsorption respectively, v is adsorbed gasquantity, vm is monolayer adsorbed quantity and c is BET constant.The values of vm ¼ 1

AþI

� �and c ¼ 1þ A

I

� �are determined from the

slope ‘A’ and intercept ‘I’ of BET plot. Total (SBET Total) and specificsurface areas (SBET) are calculated as

SBET;Total ¼vmNs

Vð14Þ

and

SBET ¼SBET;Total

að15Þ

where N is Avogadro’s number, s is adsorption cross section area(0.16 nm2 for nitrogen at 77 K), V is molar volume of nitrogen anda is the molar mass of nitrogen.

The specific surface areas of activated carbons and some biosor-bents are given in Table 7 in comparison with that of WS. Gener-ally, the greater the surface area of a specific biosorbent, thegreater the metal biosorption is, provided that all other parametersinfluencing the process are kept constant. Activated carbon hasmuch higher specific surface area than any biosorbent (Table 7)but the cost-effectiveness and re-usability of biosorbents make itpossible for them to compete activate carbons in remediation ofmetal-contaminated waters.

7. Biosorption kinetics

Kinetic data are often used for the scale-up of biosorption sys-tems. Elovich model is the simplest model, initially applied to de-scribe the biosorption kinetics. It is shown as

qt ¼lnða� bÞ

bþ lnðt þ t0Þ

bð16Þ

where a, b and t0 are constant and qt represents the quantity of ad-sorbed species at a given time t. a gives an idea of reaction rate con-stant whereas b represents the rate of adsorption at zero coverage.

Pseudo first and pseudo second order kinetic models originallyappeared as an alternative to the Elovich model to describe adsorp-

tion kinetics of gas on solids. Pseudo first order model can be ex-pressed as

dqt

dt¼ k1ðqe � qtÞ ð17Þ

where qe and qt are the amounts of metal sorbed at equilibrium anda given time t respectively, k1 is the first order rate constant. Thelinear form is

lnðqe � qtÞ ¼ ln qe � k1t ð18Þ

A plot of ‘ln (qe � qt)’ vs. ‘t’ should generate a straight line withintercept of ‘ln qe’ and slope of ‘�k1’. Value of ‘qe’ can be calculatedand compared with that experimental.

Pseudo second order model can be shown as

dqt

dt¼ k2ðqe � qtÞ

2 ð19Þ

where k2 is second order rate constant. The linear form is

tqt¼ 1

k2ðq2e Þþ t

qeð20Þ

A plot of (t/qt) vs. t should generate a straight line with intercept of1/k2 q2

e and slope of 1/qe. Value of qe can be calculated and comparedwith that obtained via experiment.

The shape of graph and comparison of experimental and calcu-lated qe values can help deciding which kinetic model is followedby biosorption. Another, very important, factor that influencessuch a decision is coefficient of determination R2. Its value indi-cates the correlation of the two quantities and a value ofR2 > 0.98 shows that the model is suitable for describing the kinet-ics (Al-Garni, 2005).

Most of the literature available for wheat-metal biosorption to-day shows the use of pseudo first- and second order models. Tables5 and 6 show the kinetic models followed by wheat-metal biosorp-tion systems and it is clear that mostly pseudo second order modelis followed. The great advantage of this model is its great accuracyin describing the whole kinetic experimental data.

According to Dang et al. (2009), the required amount of biomassmD to treat a finite volume of metal-contaminated solution vD inbatch studies can be estimated as follows,

mD ¼ðC0 � CeÞvD

qð21Þ

8. Effect of temperature – thermodynamic control

Temperature is found to be an important parameter for thesorption of metal ions dealing with the thermodynamics of the bio-sorption process. It is directly related to the kinetic energy of the

U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053 5049

metal ions. Thus, it can account for the diffusion process. An in-crease or decrease in temperature should cause a change in theamount of metal removed or sorbed by the biomass. As the bio-mass is porous in nature, possibilities of diffusion along withadsorption cannot be ruled out as a mechanism for metal removal.

The change in temperature causes a change in thermodynamicparameters like DG�, DH� and DS�. These parameters contribute tohelp understand the sorption mechanism. Temperature data areused to determine these parameters (Horsfall and Spiff, 2005; Saw-alha et al., 2006).

DG� ¼ �RT ln KD ð22Þ

where DG� is standard free energy change, R is universal gas con-stant, T temperature in Kelvin and KD is the equilibrium constantand it is calculated from

KD ¼qe

Ceð23Þ

Values of DH� and DS� can be determined from the followingequation;

ln KD ¼DS�

R� DH�

RTð24Þ

A plot of ln KD versus 1/T gives the straight line and DS� and DH�can be determined. On rearranging the equation

�RT ln KD ¼ DH� � TDS� ð25Þ

DG� ¼ DH� � TDS� ð26Þ

A plot of DG� versus T also yields a straight line and the values ofDS� and DH� can be easily determined.

Parameters like DG�, DS� and DH� provide valuable informationabout the sorption process. DG� addresses the possibility and fea-sibility of a certain reaction. The negative value of DG� shows theprocess is feasible and spontaneous. The increase in DG� value,on a negative scale, with temperature shows the increased proba-bility of the sorption process. DH� shows the route of energy in thesystem. A positive value shows an endothermic process and a neg-ative value indicates an exothermic process. This also contributesto deciding whether a certain biomass can be used for the removalof metal ions at elevated temperature or not. Tables 5 and 6 showthe thermodynamic parameters of certain wheat-metal biosorp-tion systems.

The studies performed using WS have not accounted for the val-ues of thermodynamic parameters, yet they describe the role oftemperature as causing an increase in the metal biosorption. Theprocess was found to be endothermic. On the other hand, theseparameters were determined in WB studies. Almost all the studiesshowed the endothermic nature of the sorption process. DG� val-ues were negative and showed the spontaneity of the process. Neg-ative values of DS� showed a decreased randomness or increasedorderness at the metal–biomass interface. The positive valueshowed a change in biomass structure during the sorption process,causing an increase in the disorderness of the system (Ajmal et al.,2003).

Singh et al. (2009) determined that in the process of Cd(II)-WBsorption, all above-mentioned three thermodynamic parameterswere negative. On one hand, this indicated the feasibility and spon-taniety of the process, and on the other, the process was exother-mic and increase in temperature caused a decrease in thesorption capacity. They further calculated the heat of adsorption(DH) for the process as;

ln b ¼ ln b0 � DH=RT ð27Þ

where ‘b’ is Langmuir constant related to energy of adsorption, b0 isa constant and R and T are the gas constant and temperature (in Kel-

vin). The value of DH was calculated from ln b versus 1/T plot andwas found to be �8.267 k cal/mol. This confirmed that Cd(II) bio-sorption by WB, under studied conditions, was exothermic.

9. Effect of pH

Among all other parameters, pH of solution has been found tobe the most important one. It not only influences the speciationof metal ions but also the charges on the sorption sites of biomasstype (Gao and Wang, 2007; Lee et al., 1998; Marques et al., 2000).So, it is very important to consider the ionic states of the functionalgroups of the biosorbent as well as the metal solution chemistry atdifferent pH values.

Biosorbents, in general, and specifically WS and WB, are consid-ered to contain various functional groups like hydroxyl, carboxyl,sulphydryl etc. (Lawther et al., 1995; Wang, 2002). With thechange in pH of solution, the behaviour of each of these functionalgroup changes. For example, the ionization constants of variouscarboxyl groups have been reported to be around 3–4 (Eccles andHunt, 1986). In highly acidic pHs, these are protonated and act aspositively charged species (Gardea-Torresdey et al., 1990). Depro-tonation of these functional groups occur on increasing pH andthese behave as negatively charged moieties. It starts attractingthe positively charged metal ions and there is a competition be-tween hydrogen ions and positively charged metal ions and the‘winner’ can be estimated through the amount of metal sorbed ata certain pH value. As the pH is increased from highly acidic toslightly acidic region, the positive character of biomass is con-verted to negative one.

To assess the ideal pH for metal biosorption, it would be veryhelpful to determine the point of zero charge pH of the biosorbent.Point of zero charge pH (pHpzc) is a pH of the solution at which theoverall observed charge on the surface of the biomass type is zero.When biomass is kept in a solution having pH less than pHpzc of bio-mass, the protonation of certain functional groups occur and thebiomass behaves as a positively charged polymatrix (Ofomaja andHo, 2007; Suksabye et al., 2007). This attracts the negativelycharged ions, present in the solution. Usually metal ions are posi-tively charged except the oxyanions of certain metals like chro-mate, arsenate etc. which are negatively charged. At this stage,the biomass type attracts these negative ions. This explains and jus-tifies the removal of chromate ions and less or no removal of posi-tively charged ions in highly acidic conditions (Dupont and Guillon,2003; Nameni et al., 2008; Singh et al., 2009; Wang et al., 2008). Anincrease in pH above this point makes the functional groups on thebiomass type deprotonate and act as negative species and thus itbinds the positive metal ions. This can be shown as

BH BBH2below pHpzc above pHpzc

where –BH represents the biomass type bearing zero charge. More-over it can be concluded that sorbed positive metal ions can be re-moved by decreasing the pH of the system and the biosorbent canbe regenerated, re-used and thus, pH contributes directly to theeconomics of the biosorption process. In most sorption processes,pHpzc gives the lower pH limit.

Certain functional groups such as amino, contain lone pairs ofelectrons and thus can contribute towards the formation of coordi-nate bond with the metal ions. The complexation process is highlypH dependent and occurs only at some specific pH. Thus, a changein pH can affect the complex formation and can cause a change inbiosorption efficiency of the biomass.

The solution chemistry is also influenced by pH. In acidic pHs,metal ions are generally positively charged and are attracted bynegatively charged biomass. When the pH is increased, the amount

Fig. 1. Lead species as a function of pH (Giraldo and Moreno-Pirajan, 2008).

5050 U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053

of OH- ions is increased in the solution. Metal ions react with theseOH� ions and are precipitated as metal hydroxide at some pH va-lue, depending upon the Ksp values of the metal hydroxides. In gen-eral, metal ions are precipitated out in alkaline pH range and do notcontribute towards the biosorption. This gives the upper limit ofpH to be studied. Moreover, the chemical speciation of metal isdecided by solution pH. For example, lead is present as Pb2+ asdominant species at pHs < 5.5, as PbðOHÞ2�4 at pHs above 12.5and as Pb(OH)2 at 5.5 < pH < 12.5 as shown by Fig. 1. Similarly, cad-mium is present as free Cd2+ species along the whole acid pHrange. Above pH 7.5, it starts to precipitate as Cd(OH)2 and thus,no more ‘available’ for biosorption (Basualto et al., 2006). ThuspH has a direct influence on the mechanism and uptake of metalby biosorbent (Giraldo and Moreno-Pirajan, 2008).

Fig. 2. Mechanism of biosor

Generally, when the pH of solution exceeds 8, metal ions areprecipitated out. It gives the upper limit of pH range to be studied.Most of the studies performed for positively charged metal ion (asis clear also from Tables 3 and 4) are carried out in this pH range.

There is an interesting case associated with change in pH. Dur-ing the removal of Cr(VI) by WB (Singh et al., 2009), it was ob-served that some Cr(VI) reduced to Cr(III) in highly acidic pHfollowing the route

Cr2O2�7 þ 6e� þ 14Hþ ! 2Cr3þ þ 7H2O E0 ¼ 1:33 V

Cr(III) is present as a positive ion whereas Cr(VI) is an oxyanion.In the highly acidic pH studied, the biomass (WB) was consideredas positive species and offers forces of attraction to the oxyanion ofCr(VI) whereas Cr(III) are being repelled by protonated functionalgroups. Thus, only Cr(VI) should be removed under these condi-tions. A greenish layer was observed to be present on the surfaceof WB, indicating the simultaneous adsorption of Cr(III). Although,it is possible that Cr(VI) ions are reduced into Cr(III) ions at low pH,Gupta and Rastogia (2008) and Kumari et al. (2006) reported thatthe amount of total Cr and Cr(VI) at low pH is approximately same.This indicates that the presence of Cr(III) in the final solution ofCr(VI) is insignificant. This indicates that although pH is a veryimportant and influencing factor, yet it is not solely responsiblefor the biosorption mechanism. A number of mechanisms are beingcurrently considered and the actual mechanism is a mixture of allsuch processes.

10. Mechanisms proposed

Metal biosorption is the removal of metal ions by inactive, non-living biomass due to highly attractive forces present between thetwo (Volesky and Holan, 1995). Particularly, it is due to the pres-ence of certain functional groups, such as amine, carboxyl, hydro-xyl, phosphate, sulfhydryl etc., on the cell wall of the biomass(Wang, 2002). The process involves a solid phase (biomass) and aliquid phase containing metal ions (solution of metal ions/waste-

ption (Sud et al., 2008).

Table 8Sorption efficiencies of some commonly utilized biomaterials for metal biosorption.

Biomass Metal Amount of metal sorbed (mg/g) References

Algal Fucus vesiculosus Pb 270–371 Holan and Volesky (1995)Ascophyllum nodosum Cd 215 Holan et al. (1993)Spirogyra sp. Pb 140 Gupta and Rastogia (2008)Apanothece halophutica Zn 133 Incharoensakdi and Kitjaharn (2002)Sargassum sp. Zn 118 Valdman and Leite (2000)

Bacterial Bacillus firmus Cu 381 Salehzadeh and Shojasadati (2003)Saccharomyces cerevisiae Pb 270.3 Ozer and Ozer (2003)Streptomyces rimosus Pb 135 Selatnia et al. (2004)Thiobacillus ferooxidans Zn 82 Baillet et al. (1998)

Fungal Phanerochaete chrysosporium Pb 69.77 Say et al. (2001)Penicillium chrysogenum Pb 116 Niu et al. (1993)Pleurotus sapidus Cd 127 Yalcinkaya et al. (2002)Rhizopus nigricans Pb 166 Fourest and Roux (1992)

U. Farooq et al. / Bioresource Technology 101 (2010) 5043–5053 5051

water). Metal ions are attracted and bound to the biomass by acomplex process that comprises of a number of mechanisms likeadsorption on the surface and pores, ion-exchange, surface precip-itation, complexation and chelation and entrapment in capillariesand spaces of polysaccharide network, due to the concentrationcausing diffusion through the cell wall and membrane (Chojnackaet al., 2005; Crist et al., 1981; Kuyucak and Volesky, 1989; Miretzkyet al., 2006; Muraleedharan and Venkobachar, 1990; Murphy et al.,2009; Tsezos and Mattar, 1996; Veglio and Beolchini, 1997; Yangand Volesky, 1999). The complex nature of the mechanism isshown in Fig. 2.

To study the mechanism, it is necessary to have the exact infor-mation about the cell wall structure of the biomass as well as thesolution chemistry. Biomass types from agricultural origin arecomposed of lignin, cellulose, hemicellulose, extractives, lipids,proteins, sugars, water and many more compounds having a vari-ety of functional groups. The cell walls of the different biomasses,fungi, algae, plants, sea-weeds for instance, differ significantly fromone another. Thus the groups present, type and size of pores,chains of polysaccharides etc. are ever-varying naturally in thedead material and the structure of cell walls of these materials isquite a complex one.

An emerging area of research being developed is the investiga-tion of the role of different functional groups. Volesky (2007) haslisted major functional groups that contribute towards biosorptionthrough ion-exchange, adsorption, complexation etc. He has classi-fied them using hard and soft acid base concept, the pKa values andthe electron pair donor atom. A study by Tan and Xiao (2009)shows the contribution of carboxyl groups in the sorption of cad-mium. When carboxyl groups were esterified, there was a decreasein the metal biosorption capacity. This was due to minimization ofthe number of carboxyl groups. After the material was hydrolyzedagain, an increase in the biosorption was observed. The structuralchanges were also studied using spectroscopic techniques likeFT-IR, XPS etc. The role of different groups can be illustrated usingconventional techniques such as titration (Fourest et al. 1996) ormore advanced instrumental analyses such as FT-IR, Ramanmicroscopy, EDS, XPS, XRD, EPR, etc. (Nakbanpote et al. 2007). Eachone can reveal certain information and thus can contribute to ex-plain the actual mechanism of biosorption.

11. Comparison of capacities with other biosorbents

Direct comparison of WS and WB with other sorbent materialsis difficult, since experimental conditions applied are different.Hence, WS and WB have been compared with other sorbents basedon their maximum sorption capacities (qmax, mg g�1). The sorptioncapacities of WS and WB are relatively smaller than some otherbiomaterials like fungi and algae (Table 8). Unlike fungi, algae

etc., one needs not to grow wheat especially to obtain WS andWB for such a purpose. This cuts short the initial cost and henceWS and WB find their significantly important place in the list ofcost-effective and economical materials used for metalsequestering.

12. Conclusions

The use of inexpensive and efficient materials, wheat straw andwheat bran, for metal biosorption has been reviewed. Relativelyshorter contact time, endothermic nature of biosorption process(in most cases), acidic pH range and high affinity for metal ionswas found. The use of WS needs further investigation as more lit-erature is available for the use of WB. Biosorption requires investi-gation in structural studies of biosorbents, multi-metal studies,mechanistic modeling, recovery of metal ions, enhancement of bio-sorption capacity through modification of biosorbents and contin-uous flow studies. At present, information on these materials isinadequate for process scale-up and design-perfection.

Acknowledgement

One of the authors (U. Farooq) would like to thank Higher Edu-cation Commission of Pakistan for awarding an indigenous Ph.D.scholarship as well as assistance for travel and research under-taken at the University of Saskatchewan.

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