B

TCa

b

h

•

•

•

•

•

a

ARRAA

KCNsbh

TT

h0

Journal of Hazardous Materials 274 (2014) 229–236

Contents lists available at ScienceDirect

Journal of Hazardous Materials

j o ur nal ho me pa ge: www.elsev ier .com/ locate / jhazmat

lack water sludge reuse in agriculture: Are heavy metals a problem?

aina Tervahautaa,b,∗, Sonia Rania, Lucía Hernández Leala,ees J.N. Buismana,b, Grietje Zeemanb

Wetsus, Centre of Excellence for Sustainable Water Technology, Oostergoweg 7, 8911MA Leeuwarden, The NetherlandsSub-department Environmental Technology, Wageningen University, P.O. Box 17, 6700AA Wageningen, The Netherlands

i g h l i g h t s

Based on mass balance, black waterdoes not contain external sources ofheavy metals.Black water should be differentiatedfrom sewage in sludge reuse regula-tion.Heavy metals in black water aremainly human originated (feces andurine).Heavy metals in feces and urine areprimarily from dietary sources.Heavy metal input to agriculture canbe reduced by promoting black watersludge reuse.

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

r t i c l e i n f o

rticle history:eceived 18 February 2014eceived in revised form 11 April 2014ccepted 12 April 2014vailable online 23 April 2014

eywords:arbon recovery

a b s t r a c t

Heavy metal content of sewage sludge is currently the most significant factor limiting its reuse in agricul-ture within the European Union. In the Netherlands most of the produced sewage sludge is incinerated,mineralizing the organic carbon into the atmosphere rather than returning it back to the soil. Source-separation of black water (toilet water) excludes external heavy metal inputs, such as industrial effluentsand surface run-offs, producing sludge with reduced heavy metal content that is a more favorable sourcefor resource recovery. The results presented in this paper show that feces is the main contributor tothe heavy metal loading of vacuum collected black water (52–84%), while in sewage the contribution of

utrient recoveryludge reuselack watereavy metals

feces is less than 10%. To distinguish black water from sewage in the sludge reuse regulation, a controlparameter should be implemented, such as the Hg and Pb content that is significantly higher in sewagesludge compared to black water sludge (from 50- to 200-fold). The heavy metals in feces and urine areprimarily from dietary sources, and promotion of the soil application of black water sludge over livestockmanure and artificial fertilizers could further reduce the heavy metal content in the soil/food cycle.

© 2014 Elsevier B.V. All rights reserved.

∗ Corresponding author at: Wetsus, Centre of Excellence for Sustainable Waterechnology, Oostergoweg 7, 8911MA Leeuwarden, The Netherlands.el.: +31 058 284 30 00; fax: +31 058 284 30 01.

E-mail address: taina.tervahauta@wetsus.nl (T. Tervahauta).

ttp://dx.doi.org/10.1016/j.jhazmat.2014.04.018304-3894/© 2014 Elsevier B.V. All rights reserved.

1. Introduction

Soil is an important carbon storage and can hold three timesthe amount of carbon present in the atmospheric carbon pool [29].

Even a minute change in soil carbon reserve could therefore resultin a significant change in the atmospheric CO2 concentration [13].The carbon sink capacity of soil impacts significantly not only theglobal climate change but also the world food security [30]. Soil

230 T. Tervahauta et al. / Journal of Hazardo

Nomenclature

BW black waterDW dry weightDM dry matterQ heavy metal loadingC heavy metal concentrationP production rateUASB up-flow anaerobic sludge blanketDESAR decentralized sanitation and reuseICP-AES inductively coupled plasma optical emission spec-

trometryICP-MS inductively coupled plasma mass spectrometry

eufpm

mgmcuUtfctrpmdten[

nrrwbhmrtHwtb

ocemdshtos

phosphate granules were formed in the sludge bed. Five differ-

rosion and microbial mineralization of organic carbon due to landse change and soil cultivation are suggested as the major routesor soil organic carbon loss [14]. To restore the soil organic carbonool, reuse of crop residues and bio-solids, such as compost andanure, in agriculture is promoted [29].Soil application of sewage sludge is considered as one of the

ost desired disposal methods to utilize its rich organic and inor-anic plant nutrient content, but the presence of potentially toxicetals often restricts its use [49]. Reuse of sewage sludge in agri-

ulture therefore divides opinions and the legislation regulating itsse is highly diverse in different regions [43]. Within the Europeannion (EU) the soil application of sewage sludge is regulated under

he Directive 86/278/EEC that sets the minimum quality standardsor the soil and sludge used in agriculture in terms of heavy metaloncentration and load [17]. However, several member states ofhe EU define national limit values apart from the EU standards,esulting in a great variety of sewage sludge treatment and disposalractices [23]. The Netherlands, being among the most rigid of theember states, sets the limit values below the common EU stan-

ards, prohibiting the soil application of sewage sludge [6]. Instead,he most common disposal route is incineration that not only min-ralizes the organic carbon into CO2 and destroy the plant nutrientsitrogen and phosphorus, but also requires additional energy input19].

Source-separation of black water (toilet water) excludes exter-al heavy metal inputs, such as industrial effluents and surfaceun-offs, and is therefore a more favorable source for resourceecovery compared to sewage [71]. Vacuum collection of blackater and sub-sequent treatment in an up-flow anaerobic sludge

lanket (UASB) reactor produces sludge with minimum input ofeavy metals from household chemicals [74]. Although the heavyetal content is significantly lower compared to sewage sludge, the

euse of black water sludge is prohibited in the Netherlands underhe Dutch guidelines due to elevated Cu and Zn concentrations [15].owever, as the characteristics of sewage and concentrated blackater are different, leading to different origin of heavy metals in

hese streams, the use of the same guidelines on both streams cane argued.

There is a need to work towards a more targeted regulationf the soil application of wastewater sludge that is based on theharacteristics and the origin of heavy metals in the sludge. Sev-ral studies have been conducted to determine the origin of heavyetals in municipal sewage [36,12,25,50,46] and source-separated

omestic wastewater (black water/ feces and urine, grey water andolid bio-waste [64,41,66]. No studies, however, have drawn the fulleavy metal mass balance of black water including the fractions of

oilet paper and toilet detergent, and investigate the primary originf heavy metals in the black water components. Furthermore, notudies have compared the heavy metal content of black water and

us Materials 274 (2014) 229–236

sewage sludge, and critically evaluated the applicability of currentsludge reuse regulation on these different streams.

This study presents the full heavy metal mass balance of blackwater based on literature data with additional control samples ana-lyzed within this study. The contribution of different black watercomponents to the total heavy metal loading of black water is deter-mined and compared with the heavy metal loading of sewage. Toargue for targeted sludge reuse regulation, a control parameter issuggested to distinguish black water from sewage. To further pro-mote soil application of black water sludge, the primary origin ofheavy metals in the black water components is investigated, and theimpact of current agricultural practices on the heavy metal contentin the soil/food cycle is discussed.

2. Materials and methods

2.1. Heavy metal loading calculations

Heavy metal loading (mg/cap/day) was used as a parameter todraw the heavy metal mass balance of black water, to calculate thecontribution of different black water components, and to determinethe dietary excretion of heavy metals from the human body. Theheavy metal loading of black water components and black waterwas calculated according to Eq. (1)

Q = C ∗ DW ∗ P (1)

where Q is the heavy metal loading (mg/cap/day), C is the heavymetal concentration (mg/gDW), DW is the dry weight of the sam-ple (g/L), and P is the production rate of the sample (L/cap/day orgDM/cap/day) presented in Appendix (Table A1).

2.2. Literature data

Extensive literature study was done to acquire data on theheavy metal concentrations of different black water componentsand black water, and the heavy metal loading of food (diet). Thedata was collected from studies conducted in 11 different countrieswithin Europe during the last 30 years. The location, sample sizeand reference of literature data on feces, urine, flush water andblack water is presented in Appendix (Table A2). In this study flushwater is considered to be tap water. The location, type of studyand reference of literature data on food is presented in Appendix(Table A3). Three different types of studies were included: dupli-cate diet study, total diet study and direct analysis. In duplicate dietstudy an ordinary diet is consumed from which a duplicate portionis prepared for analysis. Total diet study, also known as marketbasket analysis, determines the level of contaminants in variousfood products and estimates the dietary intake of a population. Indirect analysis, randomly selected food products are analysed andthe dietary intake is determined.

2.3. Sample collection

To cross-check the literature data on the heavy metal con-centration of black water components and black water, sampleswere collected at three different locations in the Netherlands allusing vacuum toilets (Table A4). Additionally, toilet paper and toi-let detergent were sampled and analyzed to complete the heavymetal mass balance of black water. Black water sludge was sampledwithin the study of Tervahauta et al. [56] during the first 500 daysof operation of a black water UASB reactor. After 500 days calcium

ent toilet papers were analyzed: two regular, two 100% recycledand one ecological toilet paper made 100% from an agricultural by-product of wheat straw. Three different brands of toilet rim blocks

zardo

ws

2

gdflwaatmpaamhwwHCEacdawtfTc

2

ptswblatHtdn

3

3

wb(co

iisl

T. Tervahauta et al. / Journal of Ha

ere analyzed as toilet detergent. The wastewater samples weretored at 4 ◦C prior to analysis.

.4. Sample preparation and analysis

The heavy metal concentration of feces, toilet paper, toilet deter-ent, black water, and black water sludge was determined from thery matter fraction, and the heavy metal concentration of urine andush water was determined from the unfiltered sample. The dryeight was determined by drying the sample at 105 ◦C overnight

nd by recording the weight. The dry matter fraction was thencid digested using Ethos 1 Advanced Microwave digestion sys-em of Milestone. The dried sample (0.5 g) was placed in a special

icrowave vessel with 10 mL of nitric acid (68%). To ensure a com-lete destruction of the sample, a mixture of nitric acid (2.5 mL)nd hydrochloric acid (37%) (7.5 mL) was used for toilet paper,nd a mixture of nitric acid (6 mL), sulfuric acid (96%) (2 mL) andilliQ water (1 mL) was used for toilet detergent. The samples were

eated in the microwave at 180 ◦C for 25 min. The acid digestionas done in duplicate and the relative standard deviation (%RSD)as controlled within 20%. Heavy metals (As, Zn, Cu, Ni, Cd, Pb,g and Cr) were then analyzed from the digestate with Inductivelyoupled Plasma Optical Emission Spectrometry (ICP-AES) (Perkinlmer Optima 5300174 DV). Urine and flush water were directlynalyzed with ICP-AES after addition of nitric acid to reach acidoncentration of 1% to retain heavy metals in solution. The limit ofetection (LOD) for ICP-AES was 25 ppb for Cu, Cd, Cr, Zn and Ni,nd 250 ppb for As and Pb. The heavy metals below these limitsere analyzed with Inductively Coupled Plasma Mass Spectrome-

ry (ICP-MS) in an external lab with LOD of 0.02 ppb for Hg, 0.1 ppbor Cd, 1 ppb for As, Cr, Pb and Ni, 5 ppb for Cu, and 10 ppb for Zn.he ICP-AES/MS analysis was done in duplicate and the %RSD wasontrolled within 5% and for toilet paper within 7%.

.5. Statistical analysis

Statistical analysis using Statdisk software was used to com-are the contribution of different black water components to theotal heavy metal loading of black water. Hypothesis test using theample size, average heavy metal loading and standard deviationas used to evaluate the confidence interval at which a certain

lack water component is the major contributor in the heavy metaloading of black water. The normality of the data sets was definedccording to Hair et al. [22], and was confirmed normally dis-ributed at a confidence interval of 99% for feces and 95% for urine.owever, it should be noted that the normality was calculated using

he average values from the literature studies, and the size of theata sets was therefore limited. Furthermore, due to this reason theormality of the flush water data set was not possible to confirm.

. Results

.1. Heavy metal mass balance of black water

Tables 1–3 present the heavy metal loading of feces, urine, flushater, toilet paper, toilet detergent and black water according to

oth literature and experimental data, calculated according to Eq.1). The calculated total heavy metal loading of the black wateromponents is compared with the measured heavy metal loadingf black water.

The literature and experimental data on the heavy metal load-

ng of feces are similar, and the relatively low standard deviationsndicate consistent feces composition, also realized in regions out-ide Europe [36,47]. The As content of feces is below the detectionimits, and Hg is only detected in the literature data. The differences

us Materials 274 (2014) 229–236 231

between the literature and experimental data on Hg is possibly dueto different local conditions and demographic aspects [50].

The literature and experimental data on the heavy metal loadingof urine are similar for As, Pb, Cu and Zn. Possibly due to the differentlocations and sample sizes, Cd, Cr, Ni and Hg are only detected inthe literature data. The high standard deviations indicate highlyvariable urine composition. In the study of Kuntke [28], the amountof organic compounds in urine was shown to strongly correlatewith the dilution of urine. However, as the inorganic compounds inurine did not show as strong correlation with the dilution, the highstandard deviations for heavy metals in urine cannot be explainedby it. Instead, the highly variable composition of tap water used fordrinking could influence the variation in the urine composition.

The type of water source, the regional geological conditions andthe piping materials influence the changes in tap water compo-sition [25]. The heavy metal loading of tap water in the regionalpumping station providing water to the DESAR demonstration sitein Sneek (NL) (Cu and Zn ≤0.03 and Ni ≤0.006 mg/cap/day in Span-nenburg pumping station [67]) is significantly lower compared tothe loading of tap water at the demonstration site (Cu 1.35, Zn 1.47and Ni 0.81 mg/cap/day), indicating an input of heavy metals to tapwater from the distribution network. The strong influence of pip-ing materials on the Cd, Cu, Zn and Pb loading in tap water has alsobeen shown in other studies [12,25].

Due to the lack of recent literature data, only experimental dataare presented for toilet paper and toilet detergent. Toilet paper con-tains mostly Zn and Cu, and small amounts of Pb, Cd and Ni. SimilarCd and Pb content of recycled toilet paper is presented in the studyof Storr-Hansen and Rastogi [52], while no Hg is detected in toi-let paper in this study, and might be due to the overall decreasein Hg levels in the environment [66]. The Cu and Zn loading fromthe wheat straw toilet paper (Cu 0.09 and Zn 0.22 mg/cap/day)is slightly lower compared to the wood derived toilet paper (Cu0.11 and Zn 0.25 mg/cap/day). However, the Cd, Pb and Ni load-ing from the wheat straw toilet paper (Cd 0.002, Pb 0.03 and Ni0.02 mg/cap/day) is around 10-fold higher compared to the woodderived toilet paper (Cd 0.0003, Pb 0.007 and Ni 0.005 mg/cap/day),and has an additional Cr loading of 0.04 mg/cap/day. The use ofwheat straw toilet paper is therefore not considered in this study.Only small amount of Zn is detected in toilet detergent, contribut-ing less than 0.0005% to the calculated total heavy metal loadingof black water. Similarly, the heavy metal content of most house-hold detergents is found to be low [12]. The low standard deviationsindicate consistent composition of toilet paper and toilet detergent.

The measured heavy metal loading of black water is either loweror similar to the calculated total heavy metal loading of black watercomponents, indicating absence of external heavy metal input totoilets such as household chemicals. However, the measured Cr andNi loading of black water according to experimental data is highercompared to the calculated loading, and could be explained by atemporary input of household chemicals to the toilets. The highstandard deviations of Cr and Ni in the experimental data could berelated to the use of Cr and Ni in metal finishing processes for stain-less steel used in pipes, pumps and fittings, and the wearing off ofthe metal coating over time [46]. The overall high standard devia-tions of the measured heavy metal loadings of black water indicatehighly variable black water composition that can originate fromregional and seasonal changes in the household activities. Nev-ertheless, the heavy metal mass balance of black water is closedwith the exception of As that is correlating with local geochemicalconditions [68].

3.2. Heavy metal contribution from black water components

Based on the literature data on average heavy metal loadings ofblack water (Tables 1–3), feces contributes major part to the Pb, Cd,

232 T. Tervahauta et al. / Journal of Hazardous Materials 274 (2014) 229–236

Table 1Heavy metal loading of feces, urine, flush water, toilet paper, toilet detergent and black water according to literature and experimental data (As, Pb, Cd) (unit mg/cap/day).

Sample As Pb Cd

Lit. Exp. Lit. Exp. Lit. Exp.

Avg Std Avg Std Avg Std Avg Std Avg Std Avg Std

Feces nd nd nd – 0.041 0.030 0.023 – 0.010 0.005 0.010 –Urine 0.030 0.023 0.037 – 0.011 0.018 0.008 – 0.001 0.001 nd –Flush water 0.034 0.024 nd nd 0.020 0.019 nd nd 0.001 0.000 nd ndToilet paper – – nd nd – – 0.007 – – – 0.0003 –Toilet detergent – – nd nd – – nd nd – – nd nd

BW calculated 0.063 0.047 0.037 – 0.072 0.066 0.039 – 0.012 0.006 0.010 –BW measured nd nd 0.015 0.006 0.076 0.083 0.068 0.034 0.007 0.006 0.009 0.004

Lit., literature data; Exp., experimental data; Avg, average; Std, standard deviation; nd, not detected; –, not determined.

Table 2Heavy metal loading of feces, urine, flush water, toilet paper, toilet detergent and black water according to literature and experimental data (Cu, Zn, Cr) (unit mg/cap/day).

Sample Cu Zn Cr

Lit. Exp. Lit. Exp. Lit. Exp.

Avg Std Avg Std Avg Std Avg Std Avg Std Avg Std

Feces 1.23 0.233 1.68 – 10.5 0.395 8.53 – 0.020 0.000 0.059 –Urine 0.054 0.048 0.064 – 0.360 0.503 0.266 – 0.005 0.005 nd –Flush water 0.559 0.743 1.35 1.11 1.97 1.90 1.47 0.891 0.003 0.000 nd ndToilet paper – – 0.107 0.013 – – 0.247 0.069 – – nd ndToilet detergent – – nd nd – – 2.1 × 10−5 1.2 × 10−6 – – nd nd

BW calculated 1.84 1.02 3.20 1.12 12.8 2.80 10.5 0.960 0.028 0.005 0.059 –BW measured 1.26 0.443 4.68 2.51 5.36 2.00 14.1 4.21 0.058 0.050 3.82 4.04

Lit., literature data; Exp., experimental data; Avg, average; Std, standard deviation; nd, not detected; –, not determined.

Table 3Heavy metal loading of feces, urine, flush water, toilet paper, toilet detergent and black water according to literature and experimental data (Ni, Hg) (unit mg/cap/day).

Sample Ni Hg

Lit. Exp. Lit. Exp.

Avg Std Avg Std Avg Std Avg Std

Feces 0.116 0.073 0.146 – 0.013 0.006 nd –Urine 0.016 0.017 nd – 0.006 0.005 nd –Flush water 0.019 0.033 0.814 0.359 nd nd nd ndToilet paper – – 0.005 – – – nd ndToilet detergent – – nd nd – – nd nd

BW calculated 0.150 0.122 0.965 0.359 0.018 0.012 nd nd

L nd, no

C7ttbtcbtliaflcb

oofea

BW measured 0.119 0.071 2.28

it., literature data; Exp., experimental data; Avg, average; Std, standard deviation;

u, Zn, Cr, Ni and Hg loading of black water (52%, 84%, 63%, 80%, 72%,5% and 69%, respectively). Flush water has a high contribution tohe Pb (25%) and Cu (29%) content of black water, and can be relatedo the use of Pb and Cu piping materials [12,25]. The As loading oflack water originates from flush water (53%) and urine (47%), andhe Hg loading originates from feces (69%) and urine (31%). Theontribution of toilet paper to the Pb, Cu, Zn, Cd and Ni content oflack water stays within 10%. According to the statistical analysis,he contribution of urine to the As loading of black water is eitherower or equal to the contribution of flush water at a confidencenterval of 95%. The contribution of feces to the Pb, Cd, Cu, Zn, Crnd Ni loading of black water is higher than the contribution ofush water at a confidence interval of 95%. Feces can be thereforeonsidered as the main contributor to the heavy metal loading oflack water with the exception of As.

In the study of Koch and Rotard [25], tap water is found to bene of the most significant contributors to the heavy metal loading

f municipal sewage, in particular Cu and Zn, while feces accountsor less than 10% of the heavy metal loading and urine is consid-red to be a negligible source. As concentrated black water contains

significantly smaller fraction of tap water compared to sewage,

2.33 0.005 nd 0.0003 0.0002

t detected; –, not determined.

the contribution of heavy metals from tap water decreases, whileincreasing the heavy metal contribution from feces and urine. Thevacuum collection of black water therefore creates a wastewa-ter stream characterized by human originated content (feces andurine) rather than infrastructure originated content (tap water).

3.3. Origin of heavy metals in feces and urine

The absorption and excretion of heavy metals in the human bodycan be defined by the exposure media, major uptake pathways,transport and distribution, and major excretory pathways [1]. Theexposure media can be divided to air, water, food and medicine,the major uptake pathways can be divided to skin, respiratorytract and gastrointestinal tract, the transport and distribution isdone via blood and organs (in particular liver and kidney), andthe major excretory pathways can be divided to sweat, hair, urine

and feces. To investigate the correlation between the major heavymetal uptake and excretory pathways, the average heavy metalloading of food, feces and urine according to literature data areused to compare the calculated and theoretical dietary excretion of

T. Tervahauta et al. / Journal of Hazardous Materials 274 (2014) 229–236 233

Table 4Literature data on the average heavy metal loading of food (mg/cap/day) and dietaryexcretion of heavy metals from the human body (%).

Element Fooda Dietary excretion (%)

Avg Std Calculated Theoretical

As 0.106 0.175 28 70b

Pb 0.034 0.029 153 90c

Cd 0.014 0.006 78 95d

Cu 1.25 0.179 103 25–45e

Zn 11.3 2.35 96 60–80f

Cr 0.128 0.118 19 98g

Ni 0.168 0.090 79 99h

Hg 0.005 0.003 405 5–85i

Avg, average; Std, standard deviation.a References presented in Table A3.b Rossman [45].c Cohen and Roe [11].d WHO [69].e Tapiero et al. [55].f Tapiero and Tew [54].g Offenbacher et al. [39].

he

D

w(s(

etZhtoCeodITtcatieme

gmd6ttcpmco

Table 5Heavy metal content of black water sludge, sewage sludge, cow manure and phos-phate fertilizer (unit mg/kg P).

Element BW sludgea Sewage sludgeb Cow manurec P-fertilizerd

As 12 300 nd 33Cd 13 39 33 91Cr 731 1268 1145 1245Cu 3720 12701 14397 207Hg 0.12 23 nd 0.7Ni 466 1025 1472 202Pb 69 3519 695 154Zn 13919 31166 25947 1923

nd, not detected.a Measured in this study.b CBS [9].c van Dooren et al. [62].

[38]. For the sludge reuse regulation to reflect more the application

h Grandjean et al. [21].i Miettinen [34].

eavy metals from the human body (Table 4). The calculated dietaryxcretion (%) was determined according to Eq. (2)

ietary excretion = Qfeces + Qurine

Qfood× 100% (2)

here Qfeces and Qurine are the average heavy metal loadingsmg/cap/day) of feces and urine according to literature data pre-ented in Tables 1–3, and Qfood is the average heavy metal loadingmg/cap/day) of food presented in Table 4.

The different dietary excretion fractions are due to the differ-nt functions of heavy metals in the human body, and depends onhe form and solubility of the metal compound ingested. Cu andn are essential trace elements, therefore, their excretion from theuman body is generally lower compared to As, Pb, Cd, Cr, Ni, Hghat either have no significant function in the metabolic systemr are toxic already at low levels. The calculated excretion of Pb,u, Zn and Hg is higher compared to the theoretical excretion, andxternal sources are therefore considered to contribute to the loadf these heavy metals in feces and urine. External sources can berinking water, medicine, mineral supplements and air pollution.

n addition, Hg is known to originate from dental amalgam [20,50].he calculated excretion of As, Cd, Cr and Ni is lower comparedo the theoretical excretion, and no external sources are thereforeonsidered to contribute to the load of these heavy metals in fecesnd urine. The differences in geochemical conditions and agricul-ural practices in different regions further influence the variationn the heavy metal load in food, and thus the calculated dietaryxcretion of heavy metals. The data in Table 4 show that the heavyetals in feces and urine primarily originate from dietary sources,

xcept for Hg.In the study of Rose et al. [44], the contribution of different food

roups to the dietary exposure of heavy metals is determined. Theain contributors to the Pb, Cd, Cu, Cr, Ni and Hg loading of the

iet are bread, cereals, fruits, potatoes and vegetables (57%, 73%,1%, 46%, 41%, and 29%, respectively). Meat and dairy products con-ribute the largest part to the Zn loading (56%) and fish contributeshe largest part to the As loading (88%) of the diet. Other food groupsontributing to the heavy metal loading of the diet are sugars andreserves (1–16%), and beverages (2–21%). As majority of the heavy

etals in the diet originate from agricultural products (bread and

ereals, fruit and vegetables, meat and dairy), the dietary exposuref heavy metals can be linked to agricultural practices.

d Remy and Ruhland [42].

4. Discussion

4.1. Closing the agricultural heavy metal cycle

According to Nicholson et al. [37], the main sources of heavymetals entering agricultural soil in England and Wales can beascribed to atmospheric deposition, livestock manures, sewagesludge and inorganic fertilizers. The heavy metal input rates(g/ha/year) from the different sources are compared by assuming anapplication rate equivalent to 250 kg N/ha/year for sewage sludgeand livestock manures. Based on this comparison, the soil appli-cation of sewage sludge generates the highest input rates of allheavy metals to agricultural soil. Major part of the Pb and Hg inputis further contributed by atmospheric deposition, originating fromindustrial activities such as energy production, mining and wasteincineration. Heavy metals in livestock manures originate from thediets, drinking water and housing of the livestock, and contributemajor part to the Zn and Cu input. Among the inorganic fertilizers,phosphate fertilizer has a significant heavy metal content that ori-ginates from phosphate rock, and contributes major part to the Cdand Cr input.

Although the soil application of sewage sludge promotes clos-ing of the carbon and nutrient cycle, the high input rates of heavymetals to agricultural soil poses a serious threat to the soil qual-ity. Major part of the heavy metals in sewage sludge originatesfrom industrial effluents and surface run-offs, and yet many sourcesare unknown [25,50]. Given the new developments in waste man-agement and sanitation, a new sludge reuse regulation is requiredfollowing a source-oriented approach to allow feces and urine toreturn to the soil/food cycle without external heavy metal inputs.As black water sludge is predominantly human originated (fecesand urine), it should be differentiated from sewage sludge in thesludge reuse regulation to promote carbon and nutrient recoverywhile improving the soil quality. This could be done by defininga control parameter, such as the Hg and Pb content that is signif-icantly higher in sewage sludge compared to black water sludge(from 50- to 200-fold) (Table 5), to distinguish these two streamsin the sludge reuse regulation.

To decrease the amount of heavy metals in feces and urine,external sources of heavy metals entering agricultural soil and sub-sequently the food products need to be reduced. Including manureand artificial fertilizers in the sludge reuse regulation is thereforerecommended. One of these examples is the ongoing plan to regu-late the Cd content of phosphate fertilizers in the European market

rate of inorganic and organic fertilizers, the maximum permissibleheavy metal content should be based on the phosphorus contentof these products. As black water sludge has a significantly lower

2 zardo

hCpmvsigadtmtpFiee

4

ttmNto[oUpmttoIwsc

5

•

•

•

•

A

mcyW

Appendix A.

Table A1Production rate of feces, urine, flush water, toilet paper, toilet detergent and con-centrated black water.

Sample Unit Production rate

Feces gDM/cap/day 30a

Urine L/cap/day 1b

Flush water L/cap/day 6b

Toilet paper gDM/cap/day 14c

Toilet detergent gDM/cap/day 1d

Concentrated black water L/cap/day 7.5b

DM, dry matter.a Kujawa-Roeleveld and Zeeman [27].b Kujawa [26] (based on vacuum toilet).c van der Wijst and Groot-Marcus [61].d Assumed based on consumption of 1 toilet rim, block/cap/month.

Table A2Location, sample size and reference of literature data on feces, urine, flush waterand black water.

Sample Location Samplesize

Reference

Feces UK 23 Bunker et al. [8]Belgium 25 Claeys-Thoreau et al. [10]Sweden 27 Claeys-Thoreau et al. [10]Sweden 15 Vahter et al. [58]Sweden 20 Vahter et al. [60]Sweden nd Vinnerås [65]Sweden 15 Vahter et al. [59]Croatia 17 Vahter et al. [59]LU 40 Benetto et al. [3]

Urine UK 23 Bunker et al. [8]Italy nd Minoia et al. [35]Sweden 20 Srikumar et al. [51]Sweden 13 Kirchmann and Pettersson [24]Germany 14 Schramel et al. [48]Germany 4000 Koch and Rotard [25]LU 40 Benetto et al. [3]

Flush water Germany 5100 Koch and Rotard [25]Italy 36 Tamasi and Cini [53]

Black water Sweden 3 Palmquist and Hanæus [41]NL nd Kujawa [26]

Table A3Location, type of study and reference of literature data on food (diet)

Location Type of study Reference

Belgium Duplicate diet study Buchet et al. [7]NL Total diet study Dokkum et al. [16]France Direct analysis Biego et al. [4]France Total diet study Leblanc et al. [32]UK Total diet study Ysart et al.[72]UK Total diet study Rose et al.[44]

34 T. Tervahauta et al. / Journal of Ha

eavy metal content compared to cow manure, and a lower As,d, Cr, Hg and Pb content compared to phosphate fertilizers per kghosphorus (Table 5), black water sludge should replace part of theanure and phosphate fertilizers applied in agricultural land, pro-

ided that the bio-availability of phosphate in black water sludge isufficient. Zeeman [73] calculates that at full recovery phosphorusn black water and kitchen refuse can replace 25% of the presentlobal artificial phosphate fertilizer need. As manure represents

significant stream of carbon and nutrients, alternative ways toecrease the heavy metal content, such as heavy metal regula-ion of the livestock feed, should be ultimately implemented for

anure to be utilized in agriculture. To minimize the risk relatedo pathogens when applying wastewater sludge in agricultural soil,asteurization of the sludge at 70 ◦C should be performed [70].or this reason a hyper-thermophilic treatment of sludge could bemplemented [33]. Hyper-thermophilic treatment can be appliednergy efficiently on black water that is collected with highly waterfficient toilets [73].

.2. Toxicity of heavy metals

The regulations on heavy metals entering agricultural soil needo take into account the greatly varying toxicity of the metals andhe characteristics of the soil. As, Cu and Zn are essential trace ele-

ents, they become toxic only at high levels of exposure, whilei, Cr, Cd, Pb and Hg have no essential role in the metabolic sys-

em and are toxic already at low concentrations (Cd, Pb and Hg),r can be tolerated at medium to high concentrations (Ni and Cr)40,63]. Within the EU the maximum permissible concentrationsf Zn and Pb in the soil are the same (300 mg/kgDW), while in the.S. the permissible concentration of Pb is significantly lower com-ared to Zn (150 mgPb/kgDW and 1400 mgZn/kgDW), reflectingore the different toxicity of the heavy metals [43]. The EU Direc-

ive 86/278/EEC is currently under revision and a study is launchedo examine the environmental, economic, social and health impactsf present sewage sludge reuse practices in agricultural soil [18].n order to protect the soil quality, a new heavy metal regulation

ithin the EU is needed that differentiates black water sludge fromewage sludge, promoting the reuse of black water sludge in agri-ulture.

. Conclusions

According to the heavy metal mass balance, black water does notcontain external heavy metal sources, such as household chemi-cals.Feces is the main contributor to the heavy metal loading ofvacuum collected black water (52–84%), while in sewage the con-tribution of feces is less than 10%.To distinguish black water from sewage in the sludge reuse reg-ulation, a control parameter should be implemented, such as theHg and Pb content that is significantly higher in sewage sludgecompared to black water sludge (from 50- to 200-fold).The heavy metals in feces and urine are primarily from dietarysources, and promotion of the soil application of black watersludge over livestock manure and artificial fertilizers could fur-ther reduce the heavy metal content in the soil/food cycle.

cknowledgements

The authors thank Katja Grolle, Andrii Butkovskyi, Brendo Meul-

an and Willem van Smeden for their contribution in the sample

ollection, and Luewton Lemos for the help in the statistical anal-sis. This work was performed in the cooperation framework ofetsus, centre of excellence for sustainable water technology

us Materials 274 (2014) 229–236

(www.wetsus.nl). Wetsus is co-funded by the Dutch Ministry ofEconomic Affairs and Ministry of Infrastructure and Environment,the European Union Regional Development Fund, the Provinceof Fryslân, and the Northern Netherlands Provinces. The authorslike to thank the participants of the research theme Source Sep-arated Sanitation for the fruitful discussions and their financialsupport.

Denmark Direct analysis Larsen et al. [31]Spain Direct analysis Bocio et al. [5]Italy Total diet study Turconi et al. [57]Sweden Total diet study Becker et al. [2]

T. Tervahauta et al. / Journal of Hazardo

Table A4Location and sample size of collected samples of black water components, blackwater, and black water sludge in the Netherlands.

Sample Location Sample size

Feces WUR (NL) 20 (collective sample)Urine Wetsus (NL) 2 (collective sample)Flush water DESAR (NL) 3Toilet paper NL 5Toilet detergent NL 3Black water DESAR (NL) 7Black water sludge Wetsus (NL) 3

NiS

R

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

[

L – the Netherlands; WUR – Wageningen University; DESAR – Decentralized San-tation and Reuse demonstration site, Sneek; Wetsus – Centre of Excellence forustainable Water Technology, Leeuwarden.

eferences

[1] P. Apostoli, Elements in environmental and occupational medicine, J. Chro-matogr. B 778 (1) (2002) 63–97.

[2] W. Becker, L. Jorhem, B. Sundström, K.P. Grawé, Contents of mineral elementsin swedish market basket diets, J. Food Composit. Anal. 24 (2) (2011) 279–287.

[3] E. Benetto, D. Nguyen, T. Lohmann, B. Schmitt, P. Schosseler, Life cycle assess-ment of ecological sanitation system for small-scale wastewater treatment, Sci.Total Environ. 407 (5) (2009) 1506–1516.

[4] G.H. Biego, M. Joyeux, P. Hartemann, G. Debry, Daily intake of essential mineralsand metallic micropollutants from foods in France, Sci. Total Environ. 217 (1–2)(1998) 27–36.

[5] A. Bocio, M. Nadal, J.L. Domingo, Human exposure to metals through the dietin Tarragona, Spain, Biol. Trace Elem. Res. 104 (3) (2005) 193–201.

[6] BOOM, Manual of Environmental Policy, 2008, http://www.eu-milieubeleid.nl/ch05s10.html(in dutch).

[7] J.P. Buchet, R. Lauwerys, A. Vandevoorde, J.M. Pycke, Oral daily intake of cad-mium, lead, manganese, copper, chromium, mercury, calcium, zinc and arsenicin Belgium: a duplicate meal study, Food Chem. Toxicol. 21 (1) (1983) 19–24.

[8] V.W. Bunker, M.S. Lawson, H.T. Delves, B.E. Clayton, The intake and excretionof lead and cadmium by the elderly, Am. J. Clin. Nutr. 39 (5) (1984) 803–808.

[9] CBS, Urban Wastewater Treatment per Province and River Basin District, 2011www.cbs.nl

10] F. Claeys-Thoreau, L. Thiessen, P. Bruaux, G. Ducoffre, G. Verduyn, Assessmentand comparison of human exposure to lead between Belgium, Malta, Mexicoand Sweden, Int. Arch. Occup. Environ. Health 59 (1) (1987) 31–41.

11] A.J. Cohen, F.J.C. Roe, Review of lead toxicology relevant to the safety assessmentof lead acetate as a hair colouring, Food Chem. Toxicol. 29 (7) (1991) 485–507.

12] S.D.W. Comber, A.M. Gunn, Heavy metals entering sewage-treatment worksfrom domestic sources, Water Environ. J. 10 (2) (1996) 137–142.

13] E.A. Davidson, I.A. Janssens, Temperature sensitivity of soil carbon decomposi-tion and feedbacks to climate change, Nature 440 (7081) (2006) 165–173.

14] J.J. Dawson, P. Smith, Carbon losses from soil and its consequences for land-usemanagement, Sci. Total Environ. 382 (2–3) (2007) 165–190.

15] M.S. de Graaff, Resource Recovery from Black Water, Wageningen University,2010 (Ph.D. thesis).

16] W.V. Dokkum, R.H. De Vos, T.H. Muys, J.A. Wesstra, Minerals and trace elementsin total diets in the Netherlands, Br. J. Nutr. 61 (01) (1989) 7–15.

17] European Commission, Council directive 86/278/EEC on the protection of theenvironment, and in particular of the soil, when sewage sludge is used in agri-culture, 1986 http://ec.europa.eu/environment/waste/sludge/index.htm

18] European Commission, Sewage sludge, 2012 http://ec.europa.eu/environment/waste/sludge/index.htm

19] J. Frijns, M. Mulder, J. Roorda, Op weg naar een klimaatneutrale waterketen.Utrecht, The Netherlands, 2008 (in dutch).

20] D. Gompertz, C. Courage, P. Illing, M. Taylor, IEH report on factors affecting theabsorption of toxic metals from the diet. Leicester, England, 1998.

21] P. Grandjean, O. Andersen, G. Nielsen, Biological Indicators for the Assessmentof Human Exposure to Industrial Chemicals, Commission of the European Com-munities, 1988.

22] J.F. Hair, R.E. Anderson, R.L. Tatham, W.C. Black, Multivariate analysis, PrenticeHall International, Englewood, 1998.

23] A. Kelessidis, A.S. Stasinakis, Comparative study of the methods used for treat-ment and final disposal of sewage sludge in European countries, Waste Manage.32 (6) (2012) 1186–1195.

24] H. Kirchmann, S. Pettersson, Human urine-chemical composition and fertilizeruse efficiency, Fertil. Res. 40 (2) (1994) 149–154.

25] M. Koch, W. Rotard, On the contribution of background sources to the heavymetal content of municipal sewage sludge, Water Sci. Technol. 43 (2) (2001)67–74.

26] K. Kujawa, Anaerobic Treatment of Concentrated Wastewater in DESAR Con-cepts, STOWA, 2005.

27] K. Kujawa-Roeleveld, G. Zeeman, Anaerobic treatment in decentralised andsource-separation-based sanitation concepts, Rev. Environ. Sci. Biotechnol. 5(1) (2006) 115–139.

28] P. Kuntke, Nutrient and Energy Recovery From Urine, Wageningen University,2013 (Ph.D. thesis).

[

us Materials 274 (2014) 229–236 235

29] R. Lal, Soil carbon sequestration to mitigate climate change, Geoderma 123(1–2) (2004) 1–22.

30] R. Lal, R.F. Follett, B.A. Stewart, J.M. Kimble, Soil carbon sequestration to mitigateclimate change and advance food security, Soil Sci. 172 (12) (2007) 943–956.

31] E.H. Larsen, N.L. Andersen, A. Møller, A. Petersen, G.K. Mortensen, J. Petersen,Monitoring the content and intake of trace elements from food in Denmark,Food Addit. Contam. 19 (1) (2002) 33–46.

32] J.-C. Leblanc, T. Guérin, L. Noël, G. Calamassi-Tran, J.-L. volatier, P. Verger,Dietary exposure estimates of 18 elements from the 1st French total diet study,Food Addit. Contam. 22 (7) (2005) 624–641.

33] J. Lu, H.N. Gavala, I.V. Skiadas, Z. Mladenovska, B.K. Ahring, Improving anaerobicsewage sludge digestion by implementation of a hyper-thermophilic prehy-drolysis step, J. Environ. Manage. 88 (4) (2008) 881–889.

34] J.K. Miettinen, Absorption and elimination of dietary mercury (Hg2+) andmethylmercury in man, in: M.W. Miller, T.W. Clarkson (Eds.), Mercury, Mer-curials and Mercaptans, Charles C Thomas, Springfield, IL, 1973, pp. 233–243.

35] C. Minoia, E. Sabbioni, P. Apostoli, R. Pietra, L. Pozzoli, M. Gallorini, G. Nicolaou,L. Alessio, E. Capodaglio, Trace element reference values in tissues from inha-bitants of the European community. I. A study of 46 elements in urine bloodand serum of Italian subjects, Sci. Total Environ. 95 (1990) 89–105.

36] K. Moriyama, T. Mori, H. Arayashiki, H. Saito, M. Chino, The amount of heavymetals derived from domestic wastewater, Water Sci. Technol. 21 (1989)1913–1916.

37] F. Nicholson, S. Smith, B. Alloway, C. Carlton-Smith, B. Chambers, An inventoryof heavy metals inputs to agricultural soils in England and Wales, Sci. TotalEnviron. 311 (1–3) (2003) 205–219.

38] G. Nziguheba, E. Smolders, Inputs of trace elements in agricultural soils viaphosphate fertilizers in European countries, Sci. Total Environ. 390 (1) (2008)53–57.

39] E.G. Offenbacher, H. Spencer, H.J. Dowling, F.X. Pi-Sunyer, Metabolic chromiumbalances in men, Am. J. Clin. Nutr. 44 (1) (1986) 77–82.

40] M. Ottaviani, A. Santarsiero, S. De Fulvio, Heavy metals in sewage sludge utilizedin agriculture, Ann. Ist. Super. Sanita 25 (3) (1989) 525–530.

41] H. Palmquist, J. Hanæus, Hazardous substances in separately collected grey- andblackwater from ordinary Swedish households, Sci. Total Environ. 348 (1–3)(2005) 151–163.

42] D.-I.C. Remy, I.A. Ruhland, Ecological assessment of alternative sanitationconcepts with life cycle assessment, Technical University Berlin 55, Berlin,Germany, 2006.

43] R. Renner, Sewage sludge, pros & cons, Environ. Sci. Technol. 34 (19) (2000)430A–435A.

44] M. Rose, M. Baxter, N. Brereton, C. Baskaran, Dietary exposure to metals andother elements in the 2006 UK total diet study and some trends over the last30 years, Food Addit. Contam. A 27 (10) (2010) 1380–1404.

45] T. Rossman, Arsenic, in: W. Rom, S. Markowitz (Eds.), Environmental and Occu-pational Medicine, 4th ed., Lippincott Williams & Wilkins, Hagerstown, MD,2007, pp. 1006–1017.

46] K. Rule, S. Comber, D. Ross, A. Thornton, C. Makropoulos, R. Rautiu, Diffusesources of heavy metals entering an urban wastewater catchment, Chemo-sphere 63 (1) (2006) 64–72.

47] N. Schouw, S. Danteravanich, H. Mosbaek, J. Tjell, Composition of human excreta– a case study from southern Thailand, Sci. Total Environ. 286 (2002) 155–166.

48] P. Schramel, I. Wendler, J. Angerer, The determination of metals (antimony,bismuth, lead, cadmium, mercury, palladium, platinum, tellurium, thallium,tin and tungsten) in urine samples by inductively coupled plasma-mass spec-trometry, Int. Arch. Occup. Environ. Health 69 (3) (1997) 219–223.

49] R. Singh, M. Agrawal, Potential benefits and risks of land application of sewagesludge, Waste Manage. 28 (2) (2008) 347–358.

50] L. Sörme, R. Lagerkvist, Sources of heavy metals in urban wastewater in Stock-holm, Sci. Total Environ. 298 (1) (2002) 131–145.

51] T.S. Srikumar, G.K. Johansson, P. Öckerman, J.A. Gustafsson, B. Akesson, Traceelement status in healthy subjects switching from a mixed to a lactovegetariandiet for 12 mo1−3, Am. J. Clin. Nutr. 55 (4) (1992) 885–890.

52] E. Storr-Hansen, S.C. Rastogi, Polychlorinated biphenyls and heavy metal lev-els in recycled paper for household use, Bull. Environ. Contam. Toxicol. 40 (3)(1988) 451–456.

53] G. Tamasi, R. Cini, Heavy metals in drinking waters from mount Amiata (Tus-cany, Italy). possible risks from arsenic for public health in the province of Siena,Sci. Total Environ. 327 (1–3) (2004) 41–51.

54] H. Tapiero, K.D. Tew, Trace elements in human physiology and pathology: zincand metallothioneins, Biomed. Pharmacother. 57 (9) (2003) 399–411.

55] H. Tapiero, D. Townsend, K. Tew, Trace elements in human physiology andpathology. Copper, Biomed. Pharmacother. 57 (9) (2003) 386–398.

56] T. Tervahauta, R.D. van der Weijden, R.L. Flemming, L. Hernández Leal, G. Zee-man, C.J. Buisman, Calcium phosphate granulation in anaerobic treatment ofblack water: a new approach to phosphorus recovery, Water Res. 48 (2014)632–642.

57] G. Turconi, C. Minoia, A. Ronchi, C. Roggi, Dietary exposure estimates of twenty-one trace elements from a total diet study carried out in Pavia, northern Italy,Br. J. Nutr. 101 (08) (2008) 1200.

58] M. Vahter, M. Berglund, B. Lind, L. Jorhem, S. Slorach, L. Friberg, Personal moni-

toring of lead and cadmium exposure – a Swedish study with special referenceto methodological aspects, Scand. J. Work Environ. Health 17 (1) (1991) 65–74.

59] M. Vahter, M. Berglund, S. Slorach, L. Friberg, M. Saric, X. Zheng, M. Fujita, Meth-ods for integrated exposure monitoring of lead and cadmium, Environ. Res. 56(1) (1991) 78–89.

2 zardo

[

[

[

[

[

[

[

[

[

[

[

[

[

36 T. Tervahauta et al. / Journal of Ha

60] M. Vahter, G. Johansson, A. Akesson, B. Rahnster, Faecal elimination of lead andcadmium in subjects on a mixed and a lactovegetarian diet, Food Chem. Toxicol.30 (4) (1992) 281–287.

61] M. van der Wijst, A.P. Groot-Marcus, Huishoudelijk afvalwater: Berekening vande zuurstofvraag, Wageningen Landbouuniversiteit, 1998.

62] H.J.C. van Dooren, M.C. Hanegraaf, K. Blanken, Emission and compost quality ofon farm composted dairy slurry. PraktijkRapport rundvee 68, Animal SciencesGroup, 2005.

63] M. Vargová, O. Ondrasovicová, N. Sasáková, M. Ondrasovic, K. Culenová, S.Smirjáková, Heavy metals in sewage sludge and pig slurry solids and the healthand environmental risk associated with their application to agricultural soil,Folia Veterinaria 49 (3) (2005) 28–30.

64] A. Veeken, B. Hamelers, Sources of cd, cu, pb and zn in biowaste, Sci. TotalEnviron. 300 (1) (2002) 87–98.

65] B. Vinnerås, Possibilities for Sustainable Nutrient Recycling by Faecal Sep-

aration Combined with Urine, Swedish University of Agricultural Sciences,Uppsala, Sweden, 2002 (Ph.D. thesis).

66] B. Vinnerås, H. Palmquist, P. Balmér, H. Jönsson, The characteristics of house-hold wastewater and biodegradable solid waste – a proposal for new Swedishdesign values, Urban Water J. 3 (1) (2006) 3–11.

[

[

us Materials 274 (2014) 229–236

67] Vitens, Drinking Water Quality in Friesland (NL). Vitens, 2013http://www.vitens.nl/

68] WHO, Arsenic (International Programme on Chemical Safety, Environmen-tal Health Criteria, 18), World Health Organization, Geneva, Switzerland,1981.

69] WHO, Cadmium (International Programme on Chemical Safety, EnvironmentalHealth Criteria, 134), World Health Organization, Geneva, Switzerland, 1992.

70] WHO, Guidelines for the Safe Reuse of Wastewater, Excreta and Greywater,vols. 1–4, World Health Organization, Geneva, Switzerland, 2006.

71] M. Winker, B. Vinnerås, A. Muskolus, U. Arnold, J. Clemens, Fertiliser prod-ucts from new sanitation systems: their potential values and risks, Bioresour.Technol. 100 (18) (2009) 4090–4096.

72] G. Ysart, P. Miller, H. Crews, P. Robb, M. Baxter, C.D. L’Argy, S. Lofthouse, C.Sargent, N. Harrison, Dietary exposure estimates of 30 elements from the UKtotal diet study, Food Addit. Contam. 16 (9) (1999) 391–403.

73] G. Zeeman, New Sanitation: Bridging Cities and Agriculture, Wageningen Uni-versity, 2012.

74] G. Zeeman, K. Kujawa-Roeleveld, Resource recovery from source separateddomestic waste (water) streams: full scale results, Water Sci. Technol. 64 (10)(2011) 1987–1992.