Bioresource Technology 162 (2014) 308–315

Contents lists available at ScienceDirect

Bioresource Technology

journal homepage: www.elsevier .com/locate /bior tech

Risk analysis of pyrolyzed biochar made from paper mill effluenttreatment plant sludge for bioavailability and eco-toxicity of heavymetals

http://dx.doi.org/10.1016/j.biortech.2014.03.0930960-8524/� 2014 Elsevier Ltd. All rights reserved.

⇑ Corresponding author. Tel.: +91 1126591032; fax: +91 1126581020.E-mail address: aksaroha@chemical.iitd.ac.in (A.K. Saroha).

Parmila Devi, Anil K. Saroha ⇑Department of Chemical Engineering, Indian Institute of Technology, Delhi, Hauz Khas, New Delhi 110016, India

h i g h l i g h t s

� Disposal of toxic sludge containingheavy metals poses an environmentalrisk.� Pyrolysis of sludge was performed to

explore the potential of biochar forreuse.� The effect of pyrolysis temperature on

partitioning of heavy metals wasstudied.� Fractionation and bioavailability of

heavy metals in sludge and biocharwas analyzed.� The leachability and ecotoxicity of

heavy metals in biochar weredetermined.

g r a p h i c a l a b s t r a c t

a r t i c l e i n f o

Article history:Received 6 February 2014Received in revised form 13 March 2014Accepted 18 March 2014Available online 27 March 2014

Keywords:SludgeBiocharPyrolysisHeavy metalLeaching

a b s t r a c t

The risk analysis was performed to study the bioavailability and eco-toxicity of heavy metals in biocharobtained from pyrolysis of sludge of pulp and paper mill effluent treatment plant. The sludge was pyro-lyzed at different temperatures (200–700 �C) and the resultant biochar were analyzed for fractionation ofheavy metals by sequential extraction procedure. It was observed that all the heavy metals get enrichedin biochar matrix after pyrolysis, but the bioavailability and eco-toxicity of the heavy metals in biocharwere significantly reduced as the mobile and bioavailable heavy metal fractions were transformed intothe relatively stable fractions. Moreover, it was observed that the leaching potential of heavy metalsdecreased after pyrolysis and the best results were obtained for biochar pyrolyzed at 700 �C.

� 2014 Elsevier Ltd. All rights reserved.

1. Introduction contaminants in the food chain, which can cause an indirect risk

Sludge handling and disposal is a universal problem as it con-tains significant amount of heavy metals, organic toxins and path-ogenic microorganisms (Fang et al., 2012; Ren et al., 2012; Azeezet al., 2011). The contaminated sludge can have direct toxic effectson aquatic ecosystem, and through the bioaccumulation of toxic

to the humans (Nzihou and Stanmore, 2013). Accumulation andbioavailability of heavy metals is the limiting factor for disposaland utilization of sludge. The recycling of sludge is only possibleif the toxic dioxins and heavy metals are removed or stabilized,thus allowing the treated sludge to recycle into the materials cycle.

In order to reduce the toxicity of heavy metals in the sludge,two main approaches can be applied, i.e. removal of heavy metalsfrom the sludge or heavy metal immobilization inside the sludge(Shi et al., 2013). Various methods like chemical extraction (Silva

P. Devi, A.K. Saroha / Bioresource Technology 162 (2014) 308–315 309

et al., 2005), bioleaching (Pathak et al., 2008), and bioremediation(Gaur et al., 2014) are used for heavy metal removal from thesludge. But these methods are time consuming and it is very diffi-cult to control the heavy metal removal efficiency. Heavy metalimmobilization is widely used in sludge remediation due to itssimplicity and cost effective management. Pyrolysis is an effectivetechnique to immobilize the heavy metals in the pyrolysis residue(biochar). Immobilization of heavy metals decreases the direct tox-icity or leachable fraction of heavy metals, resulting in significantreduction in the environmental risks. Various studies have beenreported in the literature on the mobility of heavy metals in thebiochar produced from sewage sludge. Kistler and Widmer(1987) studied the behavior of heavy metals Cr, Ni, Cu, Zn, Cd,Pb, and Hg during the pyrolysis of sewage sludge and found thatthe heavy metals were highly immobile in the char due to its alka-line properties. Debela et al. (2012) tested the optimum combina-tion of high heating temperature (HHT) and heating time toeffectively immobilize heavy metals in the biochar. Similar reduc-tions in metal leaching from dredged sediments after pyrolysishave been reported by Zhang et al. (2009b).

The content and mobility of heavy metals in the biochar matrixshould be determined to assess the risk to the environment by therecycling of biochar. The total heavy metal concentration is a usefulpollution indicator, but it provides no information on the mobility ofheavy metals, which depends on their chemical form (Su and Wong,2003). Chemical speciation or sequential extraction of heavy metalsfrom the sludge is a useful technique for determining the chemicalforms in which the heavy metals are present in the sludge and thebiochar. Such information is valuable for determining the mobility,bioavailability and leaching potential of heavy metals in the sludgeand the biochar (Flyhammar, 1998). Therefore, the evaluation ofsludge toxicity by chemical fractionation is important in decidingthe suitability as well as the optimum use rate of sludge in recycling.

Pulp and paper industry is capital-intensive with high consump-tion of raw materials, chemicals and utilities. Huge amount of efflu-ent (20–250 cubic meters per metric ton (m3/t) of air dried pulp) isgenerated and the disposal of waste (liquid, solid and suspendedmatter) generated (10–400 kg/ton of paper produced) during thepaper manufacturing process contributes to a very high impact onthe environment (Pokhrel and Viraraghavan, 2004). To the best ofour knowledge, there is no study reported in the literature investi-gating the bioavailability and eco-toxicity of the sludge generatedfrom the effluent treatment plant in the pulp and paper mill. The lackof the information limits the use of the sludge in various applica-tions. Therefore, efforts have been made in the present study toimmobilize the heavy metals present in the sludge using pyrolysisto explore the potential of reutilization of the biochar in agriculturaland other purposes like brick formation, use as low-cost adsorbentsetc. The pyrolysis of the sludge leads to the production of biogas, bio-oil and biochar and the heavy metals present in the sludge can par-tition in any of the products depending on the pyrolysis tempera-ture. The effect of pyrolysis temperature on partitioning andmobility of the six heavy metals (Cr, Cu, Ni, Zn, Pb, and Cd) was stud-ied. The speciation and fractionation of the heavy metals in thesludge and biochar was analyzed. The toxicity and bioavailabilityof the heavy metals in the sludge and biochar was examined. Theleachability of the heavy metals and the effect of solution pH onthe leachability of the heavy metals were investigated.

2. Methods

2.1. Pyrolysis of paper mill sludge

Paper mill sludge (PMS), collected from the effluent treatmentplant of a pulp and paper mill, and was used as a raw material

for biochar production. The PMS was characterized and resultsare given in Table S1 (Supplementary materials). Pyrolysis ofPMS was carried out according to the procedure reported else-where (Devi and Saroha, 2013). The pyrolysis was performed inthe temperature range 200–700 �C and the resultant biochar sam-ples were assigned codes BC200, BC300, BC 400, BC500, BC600 andBC700 depending on their pyrolysis temperature. The producedbiochars were stored in air-tight containers for further use.

2.2. Acid digestion

Heavy metal concentration in PMS, biochar and bio-oil weredetermined by acid digestion method (Ramteke and Moghe,1988; Rodriguez et al., 2009). Initially, 1 g of the solid sample (bio-char or PMS; 1 mL in case of bio-oil) was added in 25 mL of HNO3–HClO4 (3:1) and was heated gently for 4 h. A colorless solution wasobtained which was evaporated to near dryness. After completionof the digestion and adequate cooling of residues, solutions weremade up to 25 mL by adding 0.04 N HNO3.

2.3. Sequential extraction

The PMS and biochar samples were sequentially extracted asper the procedure shown in Fig. 1. The procedure categorizes theheavy metals in five fractions (F1, F2, F3, F4 and F5), according totheir nature and mode of occurrence. Similar procedure forsequential extraction has been reported by Poykio et al. (2006).

After each extraction, the supernatant was collected by centri-fugation at 5000 rpm for 10 min in a centrifuge and filteredthrough a 0.45-lm nylon filter. The resultant filtrate was dilutedto the desired volume (25 mL) by adding 2% HNO3. All the extract-ants were analyzed using atomic absorption spectrophotometer(AAS) for the six heavy metals.

The heavy metal concentration was determined using the fol-lowing Eq. (1):

HM concentrationmgkg

� �

¼HM concentration mg

L

� �� total volume makeup ðmLÞ

weight of solid sample ðgÞ ð1Þ

2.4. Leaching tests

Leaching behavior of the heavy metals was analyzed using thetoxicity characteristic leaching procedures (TCLP). The US EPA TCLPprocedure involves adding 10 g powder sample in 100 mL of 0.1 Macetic acid with a liquid/solid ratio of 10:1 and shaking for 18 h in arotary incubator shaker at 32 rpm. The resultant mixture was fil-tered through a 0.45 lm nylon filter and the concentration of theheavy metals in the leachate was determined using AAS. The leach-ing potential of a heavy metal was determined by dividing its con-centration in the leachate with its initial concentration in the solid.

2.5. Effect of pH on heavy metal leaching

Experiments were conducted to study the effect of pH of thesolution (pH 3–13) on heavy metals leaching from PMS and bio-char samples. The solid sample (5 g) was mixed with 50 mL of dis-tilled water and the pH of the solution was adjusted to the desiredvalue by addition of 0.1 N HCl/NaOH solutions. The solution waskept for 24 h and was filtered using 0.45 lm nylon filter. The resul-tant filtrate was analyzed for heavy metals using AAS.

The reproducibility of the experimental results was checkedand the error in the experimental results was found to be ±2%.

Fig. 1. Sequential extraction procedure of the heavy metals in PMS and biochar.

Fig. 2. Partitioning of the heavy metals in biochar pyrolyzed at differenttemperatures.

Table 1Enrichment of heavy metals in biochar pyrolyzed at different temperatures.

Temperature(�C)

Enrichment factor (Ef)

Chromium(Cr)

Copper(Cu)

Nickel(Ni)

Zinc(Zn)

Lead(Pb)

Cadmium(Cd)

200 1.18 1.09 1.55 1.04 1.28 0.77300 1.23 1.14 1.481 1.14 1.53 1.07400 1.24 1.17 1.32 1.19 1.90 0.73500 1.26 1.44 1.14 1.26 2.01 0.71600 1.28 1.55 1.01 1.49 2.09 0.59700 1.29 1.75 0.87 1.72 2.22 0.53

310 P. Devi, A.K. Saroha / Bioresource Technology 162 (2014) 308–315

3. Results and discussion

In the present study, pyrolysis of the sludge collected from theeffluent treatment plant of a pulp and paper mill was carried out toexplore the potential of reutilization of the biochar. The effect ofpyrolysis temperature on the partitioning and mobility of theheavy metals was investigated.

3.1. Effect of pyrolysis temperature on heavy metal partitioning

The partitioning of heavy metals in the pyrolysis products wasstudied by performing the pyrolysis of PMS in the temperaturerange 200–700 �C and the results are shown in Fig. 2. It can beobserved that Zn and Cu were present in significant quantities inthe PMS compared to other heavy metals and their concentrationwas found to be 193.48 and 83.98 mg/kg respectively. The heavymetals partitioned into the solid (biochar), liquid (bio-oil) and gas-eous products (biogas) on pyrolysis, depending upon the pyrolysistemperature and speciation of the heavy metals. It can be noticedfrom Fig. 2 that the major amount of the heavy metals were parti-tioned in the biochar, and the heavy metals concentration (massbasis, mg of heavy metal/kg of the sample) was not significant inthe bio-oil and biogas samples (Table S2; Supplementary materi-als). The concentrations of the heavy metals in the PMS and thebiochar was found in the order Zn > Cu > Pb > Ni > Cr > Cd.

The concentration of the heavy metals in the biochar was foundto be higher compared to their concentration in the PMS except forCd. This is due to the fact that decomposition of the organic matterpresent in the sludge causes the release of heavy metals bound tothe organic matter. The heavy metals precipitated in the biocharmatrix and resulted in the partitioning of large fraction of heavymetals into the biochar (Bo et al., 2009). Further, there was a lossin the weight of the sludge due to the decomposition of the organic

Fig. 3. Fractionation and bioavailability of the heavy metals in PMS and biochar (a) Cr; (b) Cu; (c) Ni; (d) Zn; (e) Pb; (f) Cd. F1 = water soluble fraction; F2 = exchangeablefraction; F3 = reducible fraction; F4 = oxidizable fraction; and F5 = residual fraction.

P. Devi, A.K. Saroha / Bioresource Technology 162 (2014) 308–315 311

matter during pyrolysis. But the loss in the weight of the heavymetals was lower compared to the loss in weight of the organicmatter during pyrolysis, resulting in the enrichment of heavy met-als in the biochar matrix (Yeiwei et al., 2008). The concentration ofCd in biochar was found to be lower as it may have volatilized intothe biogas during pyrolysis (Shi et al., 2013). The partitioning of theheavy metals in biochar was quantified in terms of enrichment fac-tor (Ef) which is defined as the ratio of heavy metal concentrationin the biochar to its concentration in the PMS (Yeiwei et al., 2008).

The value of the enrichment factor of the heavy metals in biocharfor different pyrolysis temperatures is shown in Table 1. It can benoticed from Table 1 that the enrichment factor was found toincrease with an increase in the pyrolysis temperature for Cu, Znand Pb. No significant effect of pyrolysis temperature on theenrichment factor for Cr was observed. The enrichment factor forNi and Cd were found to decrease with an increase in the pyrolysistemperature since Ni and Cd may have volatilized to the gasstream at higher temperatures (Shi et al., 2013).

312 P. Devi, A.K. Saroha / Bioresource Technology 162 (2014) 308–315

3.2. Fractionation and bioavailability of heavy metals

Heavy metals can be divided into three categories on the basisof their bioavailability: (a) bioavailable (Cbio), (b) potentially bio-available (Cpbio), and (c) non-bioavailable heavy metals (Cnon-bio).Bio-available category includes the water soluble (F1) andexchangeable (F2) fraction of the heavy metals, which are easilyprone to leaching. Potentially bioavailable category includes reduc-ible (F3) and oxidizable (F4) fractions which undergo degradationand leaching under very rigorous conditions (highly acidic condi-tions and oxidizing atmosphere). Non-bioavailable categoryincludes residual (F5) fraction, which is not prone to leachingand degradation. The fractionation of the heavy metals in thePMS and biochar was analyzed using sequential extraction proce-dure and the results are shown in Fig. 3a–f. It was observed thatpyrolysis could immobilize heavy metals by converting a part ofunstable fractions (F1, F2, F3 and F4) into stable fraction (F5).

The total heavy metals concentration obtained by sequentialextraction procedure (i.e. sum of all the five fractions) must beequal to the heavy metals concentration determined by acid diges-tion method. The comparison between the two heavy metal con-centrations obtained by sequential extraction procedure and aciddigestion method highlights the complete sequential extractionof the heavy metal from the solid and the agreement is reportedin terms of Recovery. The result for the evaluation of the proce-dures is shown in Table 2 and a good agreement (±4%) betweenthe two heavy metals concentrations can be noticed. A deviationof ±1–8% has been reported in the literature (Filgueiras et al.,2002).

The fractionations of Cr in PMS and biochar are shown in Fig. 3a.It can be noticed that the concentration of Cr in the water solubleand exchangeable fractions was reduced from 20% in PMS to13.57% in biochar after pyrolysis at 700 �C (BC700). In contrast,the concentration of Cr in the residual fraction was found toincrease from 30.81% in PMS to 47.51% in biochar BC700. Thiscould be due to the formation of free CaO during pyrolysis whichcan immobilize Cr by forming a stable complex (Hu et al., 2013).The XRD analysis of the PMS showed the presence of CaCO3 in sig-nificant quantity (Devi and Saroha, 2013). The chemical speciationof Cu changed significantly when PMS was pyrolyzed at differenttemperatures (Fig. 3b). The major amount of the Cu existed inthe potentially bioavailable form (Cpbio ’ 60%), in the PMS and bio-char. The bioavailable fraction (F1 + F2) of the Cu decreased signif-icantly from 22.02% (PMS) to 1.70% (BC700) after the pyrolysis. Thelarge fraction of the Ni (70%) existed in non-bioavailable categoryin the PMS and biochar and the fraction of Ni in bioavailable cate-gory was not significant (Fig. 3c). The Ni content in the residualphase was found to increase with an increase in the pyrolysistemperature.

The Zn content in the bioavailable category in PMS was found tobe 22.02% which was reduced to 0.89% in BC700 after pyrolysis(Fig. 3d). The Zn content in the non-bioavailable category, 18.36%in the PMS was found to increase to 45.32% in biochar BC700 after

Table 2Percentage recovery of heavy metals calculated by comparison of analyticalprocedures.

Samples % Recovery

Cr Cu Ni Zn Pb Cd

Sludge 97.82 97.86 99.55 98.50 92.64 101.16BC 200 98.83 100.0 98.73 99.19 98.72 101.01BC 300 98.78 100.0 99.42 98.02 97.92 101.01BC 400 99.82 100.0 98.33 99.63 98.53 99.76BC 500 98.37 99.65 101.01 99.46 102.36 99.55BC 600 98.41 97.15 97.02 101.41 104.51 98.23BC 700 99.60 99.95 99.49 98.83 102.71 100.82

the pyrolysis. This may be due to the fact that CaCO3, which is pres-ent in significant amount in PMS, may act as a strong adsorbent forZn and could lead to the formation of complex salts like CaCO3-

�ZnCO3 during precipitation of Zn (Banerjee, 2003).The major content of Pb was found in the reducible (F3) and

oxidizable (F4) fractions in PMS. The Pb content in water soluble(F1) and exchangeable (F2) fractions were not significant and werefound to decrease in the biochar after pyrolysis (Fig. 3e). The Pbcontent in residual fraction (F5) in PMS was found to increase sig-nificantly in the biochar after pyrolysis. This may be due to the factthat at higher temperature biochar formed is alkaline in nature(Hossain et al., 2011), which leads to the formation of lead hydrox-ide. The lead hydroxide eventually results in the formation of insol-uble PbO during precipitation, which eventually gets fixed asresidual fraction in the biochar matrix (Song et al., 2013).

The speciation behavior of Cd is slightly different compared toother five heavy metals (Fig. 3f). It can be noticed from Fig. 3f thatabout 30% of the Cd in PMS is present in bioavailable form (Cbio),which is easily prone to leaching. This may be due to the presenceof Cd as their chlorides or as free metal (Abanades et al., 2002).Itcan be further noticed from Fig. 3f that Cd is mainly associatedwith the oxidizable fraction in the biochar. Similar results havereported in the literature for other types of sludge (Jamali et al.,2007; He et al., 2010).

It can be concluded from the Fig. 3a–f that the distribution pat-tern in the five fractions (F1–F5) differs with each heavy metal. Thebioavailable fractions (F1 and F2) of the heavy metals were foundto decrease on pyrolysis of PMS to biochar whereas the non-bio-available fractions (F5) for the heavy metals were found to increasesignificantly on pyrolysis. Since the residual fraction is the moststable form of the heavy metals, the pyrolysis temperature is adecisive factor for immobilization of heavy metals in the biochar.

3.3. Leaching studies

The heavy metals present in the sludge are major restrictive fac-tor for reutilization of PMS and PMS derived biochar. The environ-mental behavior of heavy metals depends strongly on their specificchemical fractions or binding characteristics in PMS and biochar.The leaching characteristics of PMS and biochar were studied byperforming the experiments as per toxicity characteristic leachingprocedure (TCLP) recommended by USEPA. The effect of the pH ofthe solution on the leaching behavior of the heavy metals was alsostudied.

Fig. 4. Leaching potential of the heavy metals.

P. Devi, A.K. Saroha / Bioresource Technology 162 (2014) 308–315 313

The results of the TCLP test for the six heavy metals in the PMSand biochar are shown in the Fig. 4. In case of PMS, the leachingpotential of the six heavy metals followed the following sequence:Zn > Cu > Cd > Cr > Ni > Pb. The leaching potential of the heavymetals in the biochar was found to be lower compared with thatin the PMS and decreased with an increase in the pyrolysis temper-ature from 200 �C to 700 �C. The result is in agreement with thefractionation pattern of the heavy metals where the bioavailablefraction (F1 + F2) was found to be lower in biochar and decreasedwith an increase in the pyrolysis temperature. The leaching poten-tial of the heavy metals in BC700 was found to follow the sequenceZn > Cr > Cd > Ni > Cu > Pb.

It was observed that the leaching of the heavy metals in the bio-char was within the limits as their concentrations in the leachate ofTCLP test were lower than the statuary limits prescribed by IndianStandards for Industrial and Sewage Effluents Discharge (inlandsurface water) (Ramteke and Moghe, 1988) Table 3.

3.4. Effect of solution pH on heavy metals leaching

The solution pH is an important parameter affecting the leach-ability of the heavy metals. Experiments were carried out at differ-ent solution pH (3–13) to study the effect of solution pH on theleaching potential of the heavy metals from the PMS and biochar(BC700) and the results are shown in Fig. 5. It can be noticed thatall the heavy metals present in the PMS and biochar showed max-imum leaching potential at pH 3 as low pH conditions generallyenhance the metal dissolution. The leaching of the heavy metalswas found to decrease with an increase in solution pH from 3 to7. Further increase in the solution pH from 7 to 13 resulted in anincrease in the leaching of the heavy metals. The leaching potentialwas significant in case of Cr and Cd. It can be further noticed that

Table 3Concentration of different heavy metals (mg/L) in leachate (TCLP).

Samples Sludge BC200 BC300 BC400 BC500 BC600 BC700 Permissiblelimits

Cr 1.71 2.75 2.72 2.59 2.39 2.11 1.80 2.0Cu 23.03 16.67 3.72 2.71 4.00 3.41 1.97 3.0Ni 1.77 1.21 1.81 1.20 0.88 0.69 0.54 3.0Zn 28.05 16.20 7.98 4.18 3.05 2.71 1.42 5.0Pb 0.84 0.76 0.72 0.80 0.74 0.57 0.20 0.1Cd 0.32 0.22 0.25 0.13 0.11 0.11 0.14 2.0

Fig. 5. Effect of pH on leachability of heavy metals from PMS

except for Cr, the leaching potential of the heavy metals in the bio-char was lower compared to that in the PMS. This may be due tothe fact that the biochar obtained after pyrolysis at elevated tem-peratures is relatively alkaline in nature compared to the PMS.The decomposition of carbonate form of alkaline earth metals atthe higher temperature leads to the formation of metal oxideswhich are not prone to leaching (Zhang et al., 2009a,b). In case ofCr, the availability of CaO after the decomposition of carbonatesleads to the formation of leachable CaCrO4 (Zheng et al., 2010).

3.5. Ecological risk assessment

Potential ecological risk index (RI) was used to assess the degreeof potential risk of heavy metal pollution in PMS and biochar usingthe Eqs. (2)–(4) proposed by Hakanson (1980).

Cf ¼ Ci=Cn ð2Þ

Er ¼ TrCf ð3Þ

RI ¼X

Er ð4Þ

where, Cf is the contamination factor; Ci and Cn are the mobile andstable fractions of the heavy metals respectively, Er is the potentialecological index for individual heavy metal; Tr is toxic factor of theindividual heavy metal; and RI is the potential ecological risk index.The Tr values used for calculation of potential ecological index forindividual metal are Cr (2), Cu (5), Ni (6), Zn (1), Pb (5) and Cd(30) (Hakanson, 1980; Chabukdhara and Nema, 2012).

Contamination factor (Cf) of a heavy metal is the ratio of thesum of the concentrations of the heavy metal extracted in the firstfour fractions of the sequential extraction (F1 + F2 + F3 + F4) to theconcentration of the heavy metal in the residual fraction (F5)(Jamali et al., 2007). The value of the contamination factor of aheavy metal is inversely proportional to the leaching potential ofthe heavy metal. The potential ecological index of a heavy metal(Er) is obtained by multiplying the contamination factor of theheavy metal with the toxic factor (Tr) of the heavy metal. Thepotential ecological risk index (RI) of the solid (PMS/biochar) isobtained by adding the potential ecological index of each heavymetal present in the solid. The significance of the Cf, Er and RI alongwith their risk potential is shown in Table 4.

The values of Cf, Er and RI were determined to find out the risklevel of the heavy metals in the PMS and biochar (BC700) and are

and biochar (S = PMS; BC = Biochar pyrolyzed at 700 �C).

Table 4Indices for the ecological risk assessment.

Cf Metal contamination Er Potential ecological risk RI Sludge/biochar contamination

Cf < 1 Clean Er < 40 Low RI 6 50 Low1 < Cf < 3 Low 40 6 Er < 80 Moderate 50 < RI 6 100 Moderate3 < Cf < 6 Moderate 80 6 Er < 160 Considerable 100 < RI 6 200 Considerable6 < Cf < 9 Considerable 160 6 Er < 320 High RI > 200 HighCf > 9 High Er P 320 Very high

Table 5Ecological risk assessment of the heavy metals in sludge and biochar.

Heavy metal Tr Contamination factor (Cf) Potential ecological risk index (Er)

Sludge BC200 BC300 BC400 BC500 BC600 BC700 Sludge BC200 BC300 BC400 BC500 BC600 BC700

Cr 2 1.11 1.11 1.06 1.02 0.99 0.99 0.99 2.22 2.22 2.12 2.04 1.98 1.98 1.98Cu 5 2.02 2.03 1.91 1.73 1.58 1.58 1.58 10.14 10.15 9.55 8.65 7.9 7.9 7.91Ni 6 0.66 0.61 0.56 0.42 0.39 0.31 0.27 3.96 3.66 3.36 2.52 2.34 1.86 1.67Zn 1 3.31 13.19 13.24 13.17 1.29 1.27 1.17 3.31 13.19 13.24 13.17 1.29 1.27 1.17Pb 5 13.19 3.39 3.28 1.13 1.05 1.03 0.77 65.95 16.95 16.4 5.65 5.25 5.15 3.85Cd 30 18.22 15.17 15.15 12.38 3.59 2.48 1.62 546.67 455.1 454.5 371.4 107.7 74.4 48.59Potential ecological risk index (RI) 632.25 501.27 499.17 403.43 126.46 92.56 65.17

314 P. Devi, A.K. Saroha / Bioresource Technology 162 (2014) 308–315

tabulated in Table 5. It can be noticed that the values of Cf for Pband Cd in the PMS are13.19 and 18.22 respectively indicating ahigh metal contamination. The values of Cf for Pb and Cd in the bio-char (BC700) are 0.77 and 1.62 respectively, indicating a significantreduction in the metal contamination after pyrolysis. Similarly, thevalue of RI of PMS was found to be 632.26 indicating a high degreeof contamination by the heavy metals. The value of RI for the bio-char (BC700) was 65.19 indicating a significant reduction in thedegree of potential risk of heavy metal pollution.

4. Conclusions

The risk analysis of pyrolyzed biochar made from pulp andpaper mill effluent treatment plant sludge was carried out for bio-availability and eco-toxicity of heavy metals. Most of the heavymetals were found to exist in the residual form in the biochar pyro-lyzed at 700 �C. It was found that the pyrolysis is a promisingsludge treatment method for heavy metals immobilization result-ing in significant reduction in the bioavailability and leachingpotential of the heavy metals in the biochar. The eco-toxicity ofthe heavy metals reduced significantly after the pyrolysis, resultingin a decrease in the environmental risk of biochar utilization.

Acknowledgement

The authors wish to acknowledge the funding received for theproject from CSIR, New Delhi (India).

Appendix A. Supplementary data

Supplementary data associated with this article can be found, inthe online version, at http://dx.doi.org/10.1016/j.biortech.2014.03.093.

References

Abanades, S., Flamant, G., Gagnepain, B., Gauthier, D., 2002. Fate of heavy metalsduring municipal solid waste incineration. Waste Manage. Res. 20, 55–68.

Azeez, A.M., Meier, D., Odermatt, J., 2011. Temperature dependence of fast pyrolysisvolatile products from European and African biomasses. J. Anal. Appl. Pyrolysis90, 81–92.

Banerjee, A.D.K., 2003. Heavy metal levels and solid phase speciation in street dustsof Delhi, India. Environ. Pollut. 123, 95–105.

Bo, D., Zhang, F.S., Zhao, L., 2009. Influence of supercritical water treatment onheavy metals in medical waste incinerator fly ash. J. Hazard. Mater. 170, 66–71.

Chabukdhara, M., Nema, A.K., 2012. Heavy metals in water, sediments, andaquatic macrophytes: river Hindon, India. J. Hazard. Toxic Radioact. Waste 16,273–281.

Debela, F., Thring, R.W., Arocena, J.M., 2012. Immobilization of heavy metals by co-pyrolysis of contaminated soil with woody biomass. Water Air Soil Pollut. 223,1161–1170.

Devi, P., Saroha, A.K., 2013. Effect of temperature on biochar properties during papermill sludge pyrolysis. Int. J. ChemTech Res. 5, 682–687.

Fang, L., Yuan, N., Wu, Y., Zhao, X., Sun, H., 2012. Evolution of heavy metalsleachability and speciation in residues of sewage sludge treated by microwaveassisted pyrolysis. Appl. Mech. Mater. 178–181, 833–837.

Filgueiras, A.V., Lavilla, I., Bendicho, C., 2002. Chemical sequential extraction forheavy metal partitioning in environmental solid samples. J. Environ. Monit. 4,823–857.

Flyhammar, P., 1998. Use of sequential extraction on anaerobically degradedmunicipal solid waste. Sci. Total Environ. 212, 203–215.

Gaur, N., Flora, G., Yadav, M., Tiwari, A., 2014. A review with recent advancementson bioremediation-based abolition of heavy metals. Environ. Sci.: Process.Impacts 16, 180–193.

Hakanson, L., 1980. An ecological risk index for aquatic pollution control: asedimentological approach. Water Res. 14, 975–1001.

He, Y.D., Zhai, Y.B., Li, C.T., Yang, F., Chen, L., Fan, X.P., Peng, W.F., Fu, Z.M., 2010. Thefate of Cu, Zn, Pb and Cd during the pyrolysis of sewage sludge at differenttemperatures. Environ. Technol. 31, 567–574.

Hossain, M.K., Strezov, V., Chan, K.Y., Ziolkowski, A., Nelson, P.F., 2011. Influence ofpyrolysis temperature on production and nutrient properties of wastewatersludge biochar. J. Environ. Manage. 92, 223–228.

Hu, H.Y., Liu, H., Shen, W.Q., Luo, G.Q., Li, A.J., Lu, Z.L., Yao, H., 2013. Comparison ofCaO’s effect on the fate of heavy metals during thermal treatment of two typicaltypes of MSWI fly ashes in China. Chemosphere 93, 590–596.

Jamali, M.K., Kazi, T.G., Afridi, H.I., Arain, M.B., Jalbani, N., Memon, A.R., 2007.Speciation of heavy metals in untreated domestic wastewater sludge by timesaving BCR sequential extraction method. J. Environ. Sci. Health A 42, 649–659.

Kistler, R.C., Widmer, F., 1987. Behaviour of chromium, nickel, copper, zinc,cadmium, mercury, and lead during the pyrolysis of sewage sludge. Environ.Sci. Technol. 21, 704–708.

Nzihou, A., Stanmore, B., 2013. The fate of heavy metals during combustion andgasification of contaminated biomass—A brief review. J. Hazard. Mater. 256–257, 56–66.

Pathak, A., Dastidar, M.G., Sreekrishnan, T.R., 2008. Bioleaching of heavy metalsfrom anaerobically digested sewage sludge. J. Environ. Sci. Health A: Tox.Hazard Subst. Environ. Eng. 43, 402–411.

Pokhrel, D., Viraraghavan, T., 2004. Treatment of pulp and paper mill wastewater – areview. Sci. Total Environ. 333, 37–58.

Poykio, R., Nurmesniemi, H., Kuokkanen, T., Peramaki, P., 2006. The use ofsequential leaching procedure for assessing the heavy metal leachability inlime waste from the lime kiln at a caustizicing process of a pulp mill.Chemosphere 65, 2122–2129.

Ramteke, D.S., Moghe, C.A., 1988. Manual on Water and Wastewater Analysis.National Environmental Engineering Research Institute (NEERI), Nagpur, India.

Ren, X., Liang, B., Liu, M., Xu, X., Cui, M., 2012. Effects of pyrolysis temperature, timeand leaf litter and powder coal ash addition on sludge-derived adsorbents fornitrogen oxide. Bioresour. Technol. 125, 300–304.

Rodriguez, L., Ruiz, E., Azcarate, J.A., Rincon, J., 2009. Heavy metal distribution andchemical speciation in tailings and soils around a Pb–Zn mine in Spain. J.Environ. Manage. 90, 1106–1116.

P. Devi, A.K. Saroha / Bioresource Technology 162 (2014) 308–315 315

Shi, W., Liy, C., Ding, D., Lei, Z., Yang, Y., Feng, C., Zhang, Z., 2013. Immobilization ofheavy metals in sewage sludge by using subcritical water technology.Bioresour. Technol. 137, 18–24.

Silva, J.E., Paiva, A.P., Soares, D., Labrincha, A., Castro, F., 2005. Solvent extractionapplied to the recovery of heavy metals from galvanic sludge. J. Hazard. Mater.B120, 113–118.

Song, F., Gu, L., Zhu, N., Yuan, H., 2013. Leaching behavior of heavy metals fromsewage sludge solidified by cement-based binders. Chemosphere 92, 344–350.

Su, D.C., Wong, J.W.C., 2003. Chemical speciation and phytoavailability of Zn, Cu, Niand Cd in soil amended with fly ash-stabilized sewage sludge. Environ. Int. 29,895–900.

Yeiwei, C., Guijian, L., Lei, W., Yu, K., Jianli, Y., 2008. Occurrence and fate of sometrace elements during pyrolysis of yima coal, China. Energ. Fuel. 22, 3877–3882.

Zhang, D., He, S., Dai, L., Xie, Y., Wu, D., Bu, G., Peng, K., Kong, H., 2009a. Impact ofpyrolysis process on the chromium behavior of COPR. J. Hazard. Mater. 172,1597–1601.

Zhang, D., Kong, H., Wu, D., He, S., Hu, Z., Dai, L., 2009b. Impact of pyrolysistreatment on heavy metals in sediment. Soil Sediment Contam. 18, 754–765.

Zheng, L., Wang, W., Shi, Y.C., 2010. The effects of alkaline dosage and Si/Al ratio onthe immobilization of heavy metals in municipal solid waste incineration flyash-based geopolymer. Chemosphere 79, 665–671.