Characterization, Recovery Opportunities, and Valuation of Metals in Municipal Sludges from U.S. Wastewater Treatment Plants Nationwide

Abstract

U.S. sewage sludges were analyzed for 58 regulated and nonregulated elements by ICP-MS and electron microscopy to explore opportunities for removal and recovery. Sludge/water distribution coefficients (KD, L/kg dry weight) spanned 5 orders of magnitude, indicating significant metal accumulation in biosolids. Rare-earth elements and minor metals (Y, La, Ce, Pr, Nd, Pm, Sm, Eu, Gd, Tb, Dy, Ho, Er, Tm, Yb, Lu) detected in sludges showed enrichment factors (EFs) near unity, suggesting dust or soils as likely dominant sources. In contrast, most platinum group elements (i.e., Ru, Rh, Pd, Pt) showed high EF and KD values, indicating anthropogenic sources. Numerous metallic and metal oxide colloids (<100-500 nm diameter) were detected; the morphology of abundant aggregates of primary particles measuring <100 nm provided clues to their origin. For a community of 1 million people, metals in biosolids were valued at up to US$13 million annually. A model incorporating a parameter (KD × EF × $Value) to capture the relative potential for economic value from biosolids revealed the identity of the 13 most lucrative elements (Ag, Cu, Au, P, Fe, Pd, Mn, Zn, Ir, Al, Cd, Ti, Ga, and Cr) with a combined value of US $280/ton of sludge.

Full text

Characterization, Recovery Opportunities, and Valuation of Metals in
Municipal Sludges from U.S. Wastewater Treatment Plants
Nationwide
Paul Westerhoff,*
,†
Sungyun Lee,
†
Yu Yang,
†
Gwyneth W. Gordon,
‡
Kiril Hristovski,
§
Rolf U. Halden,
†,∥
and Pierre Herckes
⊥
†
School of Sustainable Engineering and the Built Environment, Arizona State University, Tempe, Arizona 85287-3005, United States
‡
School of Earth and Space Exploration, Arizona State University, Tempe, Arizona 85287-1404, United States
§
The Polytechnic School, Ira A. Fulton Schools of Engineering, Arizona State University, Peralta Hall 330A, 7171 E. Sonoran Arroyo
Mall, Mesa, Arizona 85212-2180, United States
∥
Center for Environmental Security, The Biodesign Institute at Arizona State University, Security and Defense Systems Initiative, 781
E. Terrace Mall, Tempe, Arizona 85287-5904, United States
⊥
Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, United States
*
SSupporting Information
ABSTRACT: U.S. sewage sludges were analyzed for 58 regulated
and nonregulated elements by ICP-MS and electron microscopy
to explore opportunities for removal and recovery. Sludge/water
distribution coefficients (KD, L/kg dry weight) spanned 5 orders
of magnitude, indicating significant metal accumulation in
biosolids. Rare-earth elements and minor metals (Y, La, Ce, Pr,
Nd, Sm, Eu, Gd, Tb, Dy, Ho, Er, Tm, Yb, Lu) detected in sludges
showed enrichment factors (EFs) near unity, suggesting dust or
soils as likely dominant sources. In contrast, most platinum group
elements (i.e., Ru, Rh, Pd, Pt) showed high EF and KDvalues,
indicating anthropogenic sources. Numerous metallic and metal
oxide colloids (<100−500 nm diameter) were detected; the morphology of abundant aggregates of primary particles measuring
<100 nm provided clues to their origin. For a community of 1 million people, metals in biosolids were valued at up to US$13
million annually. A model incorporating a parameter (KD×EF ×$Value) to capture the relative potential for economic value from
biosolids revealed the identity of the 13 most lucrative elements (Ag, Cu, Au, P, Fe, Pd, Mn, Zn, Ir, Al, Cd, Ti, Ga, and Cr) with a
combined value of US $280/ton of sludge.
■INTRODUCTION
Nationally, 16 024 wastewater treatment plants (WWTPs) were
identified in 1996, and these facilities provided service to 190
million people, representing 73% of the total population (258
million); this number was expected to increase to 90% of the
U.S. population by 2016 as communities install sewers and as
population increases in urban areas.
1
Bacterial-based biological
treatment processes purify the wastewater by producing
biomass and transforming nutrients in wastewater as the
bacteria grow. Biomass produced at WWTPs comprise active
bacteria, inert or residual biomass, extracellular polymeric
substances, protozoa and other higher life forms, mineral
precipitates and influent refractory solids.
2
This biomass is
separated, during primary and secondary wastewater treatment,
from purified wastewater. The separated biomass, also referred
to as sewage sludge, can be further treated into Class A or B
biosolids prior to land application.
3
WWTPs produce more
than 8 million tons of municipal biosolids annually in the
U.S.,
4−6
and this amount is also increasing because of the
commissioning of new plants and upgrades to existing
facilities.
7
Approximately 60% of the sewage sludge in the
U.S. are land applied (grassland, forests, agricultural crop land),
22% are incinerated and the remainder are landfilled.
4
Recent
information also shows the presence of both regulated and
nonregulated organic substances in biosolids and tools
developed to estimate their accumulation.
8,9
Heavy metals
(Cu, Cd, Zn, Ag) and some trace organics (pesticides,
herbicides,surfactants,sterols,perfluoroalkyl substances,
pharmaceuticals, and personal care products) are well removed
from the liquid-phase during biological wastewater treatment
through association with biomass, which is processed into
biosolids,
10−17
while the remaining fraction is present in
Special Issue: Critical Materials Recovery from Solutions and Wastes
Received: October 31, 2014
Revised: January 6, 2015
Accepted: January 12, 2015
Published: January 12, 2015
Article
pubs.acs.org/est
© 2015 American Chemical Society 9479 DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488

WWTP effluent discharged to rivers or lakes.
18−21
There is
recent evidence that engineered nanomaterials may accumulate
in biosolids and be taken up by plants from soils amended with
biosolids.
22−30
Many metals are toxic to aquatic organisms and are regulated
in WWTP discharges and biosolids.
31−36
Several monitoring
programs document the levels of regulated, toxic metals (As,
Cd, Cu, Pb, Hg, Mo, Ni, Se, Zn) in biosolids,
35,37,38
but few
comprehensive studies exist on a broader range of unregulated
metals in biosolids or their physical-chemical form (e.g., ionic
versus particulate or colloidal forms). This paper aims to fill
existing knowledge gaps for nonregulated metals in biomass
and biosolids.
There has long been interest in recovering elements from
WWTPs, as both a move toward sustainable use of resources
and to offset the cost of wastewater treatment.
39−41
Potentially,
a large benefit of land applying biosolids is to add bioavailable
nutrients (nitrogen and phosphorus) and organic matter to
soils.
42
However, long-term application of biosolids containing
metals can affect the productivity of soils.
43−47
Most attention
of resource recovery has been on improved phosphorus
removal/extraction, and in particular using struvite-based
precipitation processes during anaerobic treatment of sewage
sludge.
48−53
Other strategies and technologies to recover metals
from biosolids include pyrolysis, electrolysis, biobleaching or
other means of lysing cellular matter to release ionic forms of
metals, which can be separated using chemical precipitation,
membranes, or other means.
54−58
Recovery of metals directly
from wastewater, and not only biosolids, has also been
suggested for dual benefits of reduced pollutant loading and
creating potential economic value.
59,60
Gold recovery from
WWTPs may prove to have economic value, as upward of 360
tons of gold worldwide may be accumulating annually in
biosolids.
61,62
Several platinum group elements (Pt, Pd, Rh, Ru,
Ir, Os) were present in biosolids in the United Kingdom,
including over 600 ppb of Pt and Pd, which were suggested to
be from automobile catalysts that drained from roadways into
sewers.
63
In order to recognize the economic value of
recovering metals from biosolids, additional information is
needed on their occurrence in biosolids and physical form (e.g.,
ionic versus particulate).
The goals of this paper are to provide quantitative data on
(1) distribution of metals between water and biomass phases
during activated sludge treatment; (2) presence of regulated
and nonregulated metals in previously prepared mega-
composites of wastewater biosolids from across the U.S.; (3)
electron microscopy characterization of colloidal metallic
present in biosolids; and (4) potential economic value of
metals in biosolids. To address these goals, liquid and biomass
samples were collected in 2013 from activated sludge WWTPs
in central Arizona, analyzed for a broad spectrum of elements,
and used to compute distribution coefficients for each element
between liquid phase (settled supernatant) and return activated
sludge (RAS) biomass phases. The U.S. EPA performed
national sewage sludge surveys in 1989, 2001 and 2006/7. After
completion of the 2001 survey, unused samples were released
to a nationwide repository of biosolids samples. Mega-
composite samples from this nationwide study were charac-
terized after digestion and analysis by inductively coupled
plasma mass spectrometry (ICP-MS) for a broad range of 58
elements, including 30 that have not been previously measured
on similar composite samples.
35,64
To our knowledge this is the
most intensive characterization of the size, morphology, and
inorganic elemental composition of biosolids that were
analyzed by scanning electron microscopy (SEM) with energy
dispersive X-ray spectroscopy (EDX). Based upon the
elemental composition in finished biosolids, an economic
analysis was performed using recent market values of purified
elemental prices to assess the maximum value that could be
recognized from recovering these elements, and the potential
value was compared against the current costs of treating
biosolids to prepare them for ultimate disposal using current
strategies (land application, incineration, landfilling).
■MATERIALS AND METHODS
Sample Description. Biosolids samples were obtained
from the National Biosolids Repository, maintained at Arizona
State University by Halden’s research group.
65
Complete details
on the EPA biosolids composite samples collection methods
and other characterization are provided elsewhere
14,15,17
and in
the Supporting Information (SI). Briefly, biosolids samples with
1−30% solid contents were obtained from 94 wastewater
treatment plants in 32 states and the District of Columbia for
the 2001 National Sewage Sludge Survey (NSSS). Sampling
locations were selected by the U.S. EPA to reflect a
representative estimate of theoccurrenceofchemical
contaminants in sewage sludge that are disposed of primarily
by land application.
Additional samples were collected in 2013 from two activated
sludge WWTPs in central Arizona, both of which achieve
partial denitrification. Sample locations included settled primary
supernatant, RAS biomass, and secondary settled supernatant;
for one plant that processes biomass into biosolids on-site,
additional samples across anaerobic digestion and dewatering
processes were also collected (see SI Figure S-4). Total
suspended solids (TSS) was determined following the standard
methods for water and wastewater analysis.
66
Sludge-water
distribution coefficients (KD) values (L/kg dry weight), which
could also be considered liquid-to-solid ratios, were calculated
by dividing the element content in the return activated sludge
biomass (μg/kg dry weight) by the element content of the
nonfiltered secondary effluent (μg/L).
Sample Digestion and Element Analysis. Using nitric
acid and hydrogen peroxide, samples were microwave digested
in Teflon vials, followed by additional digestion steps until all
solids were clear and free of precipitates. Samples were analyzed
by quadrupole ICP-MS (ThermoFisher Scientific iCAP Q, with
CCT option). The instrument passed the mass calibration,
cross calibration and daily performance reports for sensitivity,
stability, oxide production ratio and doubly charged production
ratio prior to sample measurement. Complete description of
digestion, vial cleaning procedures, ICP analysis and quality
control used are in SI.
Electron Microscopy Analysis. Biosolids were dried and
ground into powder with a mortar and pestle. 0.5 g of each
sample was suspended in 5 mL of DI water and sonicated in a
water bath for 1 h. 0.5 mL of solution were diluted with 25 mL
of methanol (99.8%, ACS grade, VWR International) and then
one or two drops of the resultant suspension were dripped on
carbon tape on an aluminum stub or TEM copper grid (Ted
Pella Inc., California). Samples were air-dried at room
temperature (22 °C) before analysis. Scanning electron
microscopy equipped with an energy dispersive X-ray micro-
analysis system (SEM/EDX) (FEG ESEM Philips XL30 with
EDAX system) was used to locate and characterize metallic
particles in biosolids. High-resolution transmission electron
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9480

microscopy (HR-TEM) coupled with energy dispersive X-ray
spectroscopy (EDX) (Philips CM200 FEG HR-TEM/STEM)
was used to characterize the colloids visually and determine the
chemical composition of the samples.
■RESULTS AND DISCUSSION
Distribution of Metals from Sewage into Activated
Sludge Biomass. Liquid and biomass samples were collected
from multiple locations across two WWTPs (see SI Figure S-4).
Tabular data for concentrations of all elements at multiple
locations with these two facilities are summarized in SI (Table
S-1). RAS solids concentration was 5.43 and 5.04 gTSS/L for
WWTP#1 and WWTP#2, respectively. Figure 1shows that
detectable metal concentrations in RAS ranged over 6 orders of
magnitude from ∼107μg/kg dry wt. (10 g/kg) for the major
elements (Na, Ca, P, K, Mg, Fe, Al) to 101−102μg/kg dry wt.
for others (Dy, Yb, Er, Eu, Ir, Tl, Ho, Re). For additional
reference, phosphorus accounted for ∼3% of the dry weight of
the biomass, which is consistent with the elemental
composition of cellular material.
52
Figure 2shows the range of sludge-water distribution
coefficients (KD) for metals across the biological treatment
process (activated sludge) in both samples. A few liquid effluent
samples had metal concentrations below the detection limit; KD
values were not calculated for these metals. KDvalues span a
range greater than 5 orders of magnitude, with KDvalues above
unity indicating a preference for the biomass phase over the
liquid phase. High KDvalues measured in this study
demonstrate a strong affinity for a wide range of metals toward
biomass. Even metals (e.g., V, W) that commonly occur as
anionic oxo-anions accumulate in biosolids. Metals with very
low solubility solids (e.g., Ti, Au, Pd) also exhibit high KD
values. Traditionally, distribution coefficient (KD), isotherm
(Freundlich, Langmuir) or multisurface (diffuse layer) models
for free and organically complexed metals (Cd, Cu, Zn) have
been used to describe relationships between metal accumu-
lation on wastewater biosolids and in soils amended with
biosolids.
67−73
Thus, it is possible that both ionic and colloidal
Figure 1. Elemental concentrations in biomass (return activated sludge) for two Arizona WWTPs. Some elements were below detection limits in
WWTP#1 (no bars shown), and other elements (Se, Rh, Te, Tb, Tm, Lu, Pt) were not detected above detection limits in either biomass samples.
Figure 2. Distribution coefficients (Log KD) for elements detected in both biomass and settled supernatants at two Arizona WWTPs.
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9481

or particulate forms of metals accumulated in the biosolids. To
explore this, we imaged submicron sized metals in biosolids
(presented later).
The calculated KDvalues are only for the activated sludge
unit process. Settled solids are further processed using
dewatering systems (e.g., belt filter presses, centrifuges; see SI
for a typical process flow diagram) and sometimes include
anaerobic digestion where the volume of biosolids is lowered to
reduce the cost of hauling and disposing biosolids off-site (i.e.,
transportation and tipping fees). Liquid waste streams from the
dewatering systems and anaerobic digestors are usually
returned to the front of the WWTP treatment train. To
understand these processes, we examined solids handling at
WWTPs that use anaerobic digestion followed by dewatering.
Across these processes, the total daily mass flux of one element
(Ti) into the biosolids processing facility was 5.6 ×103g Ti/
day. Titanium was selected to monitor because its aqueous
solubility is quite low in natural waters.
74
A large percentage
(84%) of the titanium entering the solids processing ended up
in finished biosolids, while 4.5%, 4.5%, and 7% of the titanium
was accounted for in gravity thickener liquid, belt filter press
thickener liquid and centrifugation liquid, respectively.
Although titanium likely occurs in mineral forms (anatase,
rutile, brookite, silicates) with low solubility, this analysis
indicates that metals are retained within biomass as they are
further processed into biosolids. For more soluble minerals and
elements, return of liquid flows containing these metals to the
front of the WWTP will again allow distribution onto biomass
during activated sludge treatment.
Elemental Composition of Biosolids from Local
WWTP and EPA Mega-Composite Biosolids Samples.
The concentrations of regulated metals (As, Cd, Cr, Cu, Pb,
Mo, Ni, Zn) in the WWTP#1 biosolids (10, 3.6, 36, 436, 24,
7.8, 28, 620 mg/kg, respectively) are roughly 10-fold below
ceiling concentration limits for biosolids intended for land
application based upon EPA Section 503.13 (75, 85, 3000,
4300, 8400, 75, 420, 7500 mg/kg, respectively); mercury (Hg)
was not analyzed and Se was below our detection limits. The
rank order from higher to lower concentrations (Zn > Cu > Cr
> Ni > Pb > Cd) of these regulated elements is consistent with
trends reported elsewhere for biosolids.
35
To fill data-gaps
where more information is needed for Ba, Mn and Ag,
75
their
concentrations in WWTP#1 biosolids were measured as 275,
1500, and 17 mg/kg, respectively. SI Table S-2 shows that
elemental concentrations in the biosolids from WWTP#1 are
similar to those for the five EPA mega-composites and the 50th
percentile concentrations for a subset of elements reported
35
in
biosolids collected from across the U.S. We observed relative
concentrations of trace elements similar to those recently
reported for sewer sludge ash after incineration.
76
To improve our understanding of element occurrence in
biosolids, a geochemical analysis strategy was employed that
normalizes observed element content to element content in the
upper continental crust.
77
Enrichment factors (EFs) are
obtained by comparing the abundance of a given trace element
in the biosolids relative to that same trace element in a
reference material. Specifically, the EF of an element (X) is
often calculated relative to the average composition of upper
continental crust (UCC)
78
using Al or Fe as the reference
element (R) where EF = [X/R]sample/[X/R]UCC. The EFs of
selected elements relative to UCC
77
using Al as the reference
element are shown in Figure 3, with the x-axis presenting
elements in order of atomic mass (low to high). An enrichment
value of unity suggests the ratio to aluminum of that element is
Figure 3. Enrichment factor of elements in biosolids from EPA biosolids mega-composite groups, two Arizona WWTPs and 50th percentile
occurrence data from a previous study on a subset of samples. EF calculated relative to Al. (error bars for “Stevens”data show 10th and 90th
percentile values for a prior study;
35
other error bars show two standard deviations around a mean from replicate digested and analyzed samples (n=
3 to 5)).
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9482

the same as in crustal material (e.g., soil, dust). Hence under
the assumption that the main aluminum source in wastewater is
crustal material, this means the element also comes mainly from
crustal sources like soil dust. Elements with EF > 10 suggest
that there are other sources (i.e., anthropogenic sources) for
that element. This approach is commonly used to apportion the
sources of trace metals in atmospheric aerosol studies.
79
No
element shows consistently an EF < 1, which tends to support
the premise that the main source of aluminum in WWTP
biosolids is crustal (soil dust). This is further supported by the
rare-earth elements (REE) and several minor metals (Y, La, Ce,
Pr, Nd, Pm, Sm, Eu, Tb, Dy, Ho, Er, Tm, Yb, Lu) showing a
ratio close to UCC. While REE and minor metals have
industrial applications, it appears that a substantial part of
crustal soil material is present in WWTPs (likely because of
urban runoff/stormwater or other sources) and implies the
industrial sources are small and nearly negligible. A few
exceptions occur, such as gadolinium, which is used as a
contrast agent in medical diagnostics and shows a slight
enrichment.
80−84
Phosphorus is highly enriched (EF > 100), suggesting its
noncrustal sources (e.g., anthropogenic sources such as foods,
industrial acids, etc.). Phosphorus has a high KD(Figure 1),
indicating that bacteria accumulate P present in wastewater.
Likewise, biosolids have long been recognized to concentrate
(i.e., higher KDvalues) toxic metals (e.g., Cu, Zn, Cd, Ag, Sn,
Pb), and EFs for these metals exceed unity due to their uses in
industry. Calculated EF values for biosolids collected in 2012 at
the two Arizona WWTPs and the five mega-composite samples
align well with values calculated using concentrations for a
subset of metals reported in the literature (e.g., ref 35 as labeled
in Figure 3). By expanding the suite of metals analyzed, we are
among the first to show significant EFs in biosolids of most
platinum group elements (i.e., Ru, Rh, Pd, Pt), which have
likely sources including catalytic converters in cars that
dominate their sources into the environment.
85
Some of the
elements for which we could calculate partition coefficients
onto biomass have KDvalues >100 (Figure 2). Despite having
EFs near unity, indicating they likely have origins in crustal
materials, several of these REEs and minor metals (Eu, Sm, Sr,
V, W, Cr, Gd, Mo, Mn, Sb, Ir) with detectable liquid phase and
biomass concentrations have KDvalues greater than unity. This
suggests that these elements accumulate in biosolids during
biological wastewater treatment. Some elements (e.g., Mo) may
be critical trace nutrients for bacteria, while other elements may
be present in ionic forms or insoluble particulates that
accumulate on the surface of suspended bacterial biofilms.
Electron Microscopy Analysis of Biosolids. To explore
possible sources of these elements into the wastewater system
from sources other than natural “dusts”or soil (i.e., EFs > 1)
and to consider potential biological, physical or chemical means
to recover the elements from biosolids, we analyzed the
morphology of metallic objects in the biosolids. After
conducting SEM-EDX analysis of dozens of samples, we
identified numerous metallic and metal oxide colloids ranging
in size from <100 to 500 nm (Figure 4;SI Table S-3). Several
objects were composed of aggregates containing primary
particle sizes <100 nm. Some objects appear to be incidental
nanomaterials (NMs). For example, particles containing tin
appear teardrop-shaped in Figure 4and may have been tin-
based solder hydraulically sheared from piping. Some colloids
occurred frequently in the biosolids samples (e.g., TiO2), while
Figure 4. SEM images showing morphology of colloidal and particulate-sized inorganic materials in EPA mega-composite biosolids samples.
Elemental composition was determined by EDX analysis during SEM.
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9483

colloids composed of other elements (e.g., Au) were only
observed in one or two samples. Titanium oxides were found
easily in nearly all samples, with morphologies and sizes ranging
from those similar to food grade TiO2found in toothpaste to
micron-size material found in paints.
86,87
Silica oxides were
found in forms representing both clays and zeolite structures,
where the latter is used in some foods and washing
detergents.
88−91
Lead and silver sulfides were far less frequently
observed than TiO2. Sulfide forms of metals can readily form
within activated sludge systems due to bacterial reduction of
sulfate and low solubility of many metal sulfide materi-
als.
22,92−95
Gold- or platinum-series containing particulates
were also observed and could result from discharges into sewers
from mining, electroplating industries, electronic and jewelry
manufacturing,
96
industrial catalysts, or automotive catalysts
present in stormwater that enters sewers.
97−99
Tantalates are
also widely used in electronics, in part to form protective oxide
layers on surfaces. Many elements with EF > 10 were visualized
as colloids within biosolids using electron microscopy.
Rather than hunting for individual colloidal-scale objects in
samples prepared on electron microscopy stubs/grids, we
attempted to employ elemental mapping across a grid area.
This works well to locate larger-sized or high-abundance
particulates in fairly clean samples but proved less useful in
“locating”nanoscale particles while processing our samples
because the latter contains so little elemental mass for the
existing EDX technology to identify and quantify. Elemental
mapping helped locate nanoscale TiO2(confirmed by atomic
ratios of titanium and oxygen from EDX) in or on what appears
to be clay that contains Si, Fe, Al, and traces of Ce (SI Figure S-
1 and S-2). Elemental scanning for rarer elements like silver
necessitates searching large areas; low signal intensity was
observed, indicating few concentrated regions of Ag, which
signify silver nanoparticles or suggest that Ag is distributed
across the biomass (i.e., ions sorbed to biosolids materials).
Emerging research debates the implications of nanosilver,
titanium dioxide, zinc and gold on plants receiving land applied
biosolids or runofffrom such lands; far less data or
identification exists for other nanoscale materials that may be
toxic or exhibit catalytic properties.
Despite decades of research on metals and biosolids, this
electron microscopy work is among the first, to our knowledge,
to present and discuss the morphology of colloidal-size inert
solids in biosolids. The morphology may be very important in
understanding why some elements accumulate in biosolids (i.e.,
KD> 1). The presence of submicron sized particles composed of
regulated, toxic metals in biosolids is not surprising but may be
important in understanding the mechanisms for removing
metals at WWTPs. The common explanation and models for
removal of toxic metals by biological processes at WWTPs view
metals as being present as mostly ions. Models exist for
speciation of metal ions into various aqueous species, and
surface sorption binding models exist for such species onto
wastewater biomass.
100−106
The presence of nonionic forms of
metals may help explain some of the variability in metal
removal at different WWTPs.
107
Thus, it is possible that
previous conceptual approaches for metal sorption to biomass
may have oversimplified distribution of metals with biomass by
only considering ionic species. It is likely that colloidal forms of
metals behave differently than ions where colloids are taken up
by cells or involved in aggregation with biological colloids and
cells.
Integration of ICP-MS Concentration and Electron
Microscopy Characterization of Elements in Biosolids.
Data from ICP-MS and SEM/TEM/EDX were interpreted
together to determine the probability of finding metal-based
nanomaterials in biosolids samples by electron microscopy. The
dry mass data (ppm; mg element/kg biosolids) can be useful in
estimating the probability of finding physical objects. For
example, we find many iron oxides and calcium phosphates
colloids in biosolids by electron microscopy because their metal
contents are very high in biosolids (e.g., 55 000 ppm Fe, 35 000
ppm of Ca). Titanium (1500 ppm) is readily found with
silicates or as TiO2in biosolids. Colloids containing copper
(400 ppm) and silver (15 ppm) are found less frequently.
While we periodically found colloids containing palladium (0.3
ppm) or gold (0.3 ppm), we rarely found colloids containing
yttrium (2 ppm), neodymium (1.9 ppm) or dysprosium (0.3
ppm), which are commercially available and used as oxide
nanopowders. Based upon mass concentrations it should be
more likely to image titanium- than silver- or gold-bearing
particulates when “prospecting”in biosolids using electron
microscopy. This premise was analyzed in detail (see SI) and
lead to an important conclusion. The likely occurrence for TiO2
or a metal-bearing particulate to be present in an electron
microscopy stub area of 1 μm2follows the following trend from
higher to lower probability of locating: TiO2>Ca>Fe>Zn>
Al > Ba > Cu > Pb > Ag > Sb > Au. The probability of finding a
silver or gold submicron particle is on the order of 105or 106
times lower than finding a TiO2nanoparticle, respectively. The
fact that we observed any in our SEM work is somewhat
fortuitous.
Economic Value of Metals in Biosolids. Approximately
60% of U.S. biosolids are recycled and applied to agricultural or
forest lands that benefit from the nitrogen and phosphorus
content, but the rate and long-term application amount to
individual fields can be limited by the presence of metals.
35,108
The other 40% of biosolids are disposed in landfills or
incinerated, with the ash deposited to landfills. Recycling
options for N and P from biosolids have been proposed,
52
where nutrients can be separated from metals and organics in
the biosolids. The question arises: what is the economic value
of these nutrients relative to other metals in wastewater
biosolids?
This question was investigated using the metal concen-
trations for the mega-composite biosolids samples (SI Table S-
2) and the spot market price of purified metals (SI Table S-4).
Prices are intended to be more comparative than absolute.
Annual per capita production of biosolids is on the order of 26
kg/person-year.
109,110
Analysis was performed for a community
with a population of 1 000 000 people (∼28 600 dry tons of
biosolids per year), and the resulting economic potential is
illustrated in SI (Figure S-3 and Table S-4). For this
community, the estimated value of metals in the biosolids
could approach $13,000,000 per year ($460/ton) with greater
than 20% of the value accounted ($2,600,000 per year) for by
gold and silver. These commodity prices represent high purity
elements, so it would take considerable energy and cost to
purify these biosolids. Gold ore grades range from 0.3 to 80 g
per metric ton (g/t), and the biosolids measured here contain
gold ranging from 0.3 to 0.6 g/t which is in the range of values
reported elsewhere of 0.2 to 7 g/t.
61
It is noteworthy that
phosphorus, which is the focus of many wastewater recovery
systems, has a relatively low economic value ($57,000/year).
Some of the elements may create misleading total values of
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9484

elements in biosolids. Prime examples are rubidium (Rb) or
lutetium (Lu), which are approximately five to six times more
expensive than gold and are among the most expensive of the
REEs. Rb and Lu concentrations in biosolids are quite low,
have an EF near unity, and because of the low Lu concentration
in wastewater, their KDcould not be determined; Rb has a log
KDof 3.0. Thus, the potential economic value of such
nonenriching metals may be misleading in that it cannot be
easily extracted in practice (SI Figure S-3).
The most promising elements to recover from biosolids
would have high potential economic value (based upon cost of
element in a purified form ($/kg), high concentration in
biosolids (mg/kg)), high EF values indicating the element is
used in anthropogenic products or processes, and a high KD
value indicating the ability of biological processes in WWTP to
accumulate the element. Thus, for each element we developed a
“relative potential for economic value from biosolids”
parameter (KD×EF ×$Value). Figure 5shows this parameter
for 30 elements having the highest values. This analysis may
help in prioritizing elements to obtain more information on
their occurrence in biosolids, assess potential chemical
processes to recover the elements, and assess market needs
for their purity. Given the observed presence of many metals in
the form of particles rather than ions in this study, this
speciation may play an important role in resource recovery.
Based on our analysis, the top 13 most attractive elements to
recover from biosolids are Ag, Cu, Au, P, Fe, Pd, Mn, Zn, Ir, Al,
Cd, Ti, Ga, and Cr. Several of these are part of identified energy-
critical-elements (Ga, Pd, Ag, Ir) or critical elements for food
systems (P).
111−113
For a community of 1 000 000 people, the
economic value of recovering these elements could be on the
order of $8,000,000 annually or less, depending on the recovery
yield. As can be seen from Figure 5(gray bars), recovering
elements with a high relative potential for economic value
would also address concerns over the toxicity of these biosolids
constituents. Thus, recovering metals could be an economic
and environmental win-win scenario.
The total cost of biosolids treatment is on the order of $300
per ton, which includes anaerobic treatment and thickening etc.
to reduce the water content to roughly 20% solids, plus
additional disposal costs for land application. The economic
value of biosolids if all the elements were recovered in adequate
purity is estimated to be on the order of $100 per dry ton. Per
capita wastewater production in the U.S. is declining due to
increased water conservation measures, but the per capita
pollutant loading is expected to remain stable, thereby resulting
in higher strength wastewaters. Consequently, the metal
concentrations in biosolids may increase in the future, which
would complicate land application but would work in favor of
resource recovery from biosolids. There may come a tipping
point when the costs to recover or sell biosolids based upon
their resource value will be a more economical and sustainable
avenue than land disposal. While it may appear tempting to
reverse industrial point-source discharges into sewers because
this could increase the value of recoverable metals in biosolids,
the authors believe that separation and recovery closest to the
point of use and discharge probably holds the most
environmental benefit and opportunities for reuse. It is possible
that regional differences may exist in the metal concentrations
that contribute to the relative potential for economic value from
sewage sludge or biosolids, and future research should
understand the existing spatial differences and consider how
these may change in the future. Added environmental benefits
would result as well because biosolids contain a suite of organic
pollutants that threaten the health and safety of soils receiving
land applications of biosolids (i.e., biosolids as soil amend-
ments).
13,17,114,115
■ASSOCIATED CONTENT
*
SSupporting Information
Details on mega-composite sampling, digestion and analysis is
provided. Additional particle imaging and number analysis is
provided. Economic value estimates are tabularized. This
material is available free of charge via the Internet at http://
pubs.acs.org/
Figure 5. Relative potential (y-axis) for economic value from biosolids for the top 30 elements based upon a community of 1 000 000 people
producing 26 kg/person-year of dry biosolids. Gray bars indicate elements considered potentially toxic for land application and have dry weight
concentration limits on their land application regulated by the Part 503 Biosolids Rule.
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9485

■AUTHOR INFORMATION
Corresponding Author
*Phone: 480-965-2885; fax: 480-965-0557; e-mail: p.
westerhoff@asu.edu.
Notes
The authors declare no competing financial interest.
■ACKNOWLEDGMENTS
This study was partially funded by the Water Environment
Research Foundation (RD831713), National Science Founda-
tion (CBET 1336542 and BCS-1026865, Central Arizona-
Phoenix Long-Term Ecological Research (CAP LTER)), and
USEPA (RD RD83558001) and by awards R01ES015445 and
1R01ES020889 from the National Institute of Environmental
Health Sciences (NIEHS).
■REFERENCES
(1) USEPA Clean Water Needs Survey; USEPA: Washington, DC,
1996.
(2) Rittmann, B. E.; McCarty, P. L. Environmental Biotechnology:
Principles and Applications; McGraw Hill: New York, 2001.
(3) USEPA A Guide to the Biosolids Risk Assessments for the EPA Part
503 Rule; U.S. Environmental Protection Agency: Washington, DC,
September, 1995; p 144.
(4) Peccia, J.; Paez-Rubio, T. Quantification of Airborne Biological
Contaminants Associated with Land Applied Biosolids; Water Environ-
ment Research Foundation, 2006; p 169.
(5) NEBRA A National Biosolids Regulation, Quality, End Use and
Disposal Survey (Final Report); North East Biosolids and Residuals
Association (NEBRA): Tamworth, NH, 2007; p 34.
(6) NRC. Biosolids Applied to Land: Advancing Standards and
Practices. National Academies Press: 2002; p 368.
(7) NRC. Biosolids Applied to Land: Advancing Standards and
Practices; National Academy Press: Washington, DC, 2002; p 284.
(8) Deo, R. P.; Halden, R. U. In silico screening for unmonitored,
potentially problematic high production volume (HPV) chemicals
prone to sequestration in biosolids. J. Environ. Monit. 2010,12 (10),
1840−1845.
(9) Chari, B. P.; Halden, R. U. Predicting the concentration range of
unmonitored chemicals in wastewater-dominated streams and in run-
off from biosolids-amended soils. Sci. Total Environ. 2012,440, 314−
320.
(10) Chanpiwat, P.; Sthiannopkao, S.; Kim, K. W. Metal content
variationinwastewaterandbiosludgefromBangkok’scentral
wastewater treatment plants. Microchem J. 2010,95 (2), 326−332.
(11) Karvelas, M.; Katsoyiannis, A.; Samara, C. Occurrence and fate
of heavy metals in the wastewater treatment process. Chemosphere
2003,53 (10), 1201−1210.
(12) Ustun, G. E. Occurrence and removal of metals in urban
wastewater treatment plants. J. Hazard. Mater. 2009,172 (2−3), 833−
838.
(13) Venkatesan, A. K.; Halden, R. U. National inventory of
perfluoroalkyl substances in archived US biosolids from the 2001 EPA
National Sewage Sludge Survey. J. Hazard. Mater. 2013,252, 413−
418.
(14) Chari, B. P.; Halden, R. U. Validation of mega composite
sampling and nationwide mass inventories for 26 previously
unmonitored contaminants in archived biosolids from the U.S
National Biosolids Repository. Water Res. 2012,46 (15), 4814−4824.
(15) Walters, E.; McClellan, K.; Halden, R. U. Occurrence and loss
over three years of 72 pharmaceuticals and personal care products
from biosolids-soil mixtures in outdoor mesocosms. Water Res. 2010,
44 (20), 6011−6020.
(16) Venkatesan, A. K.; Halden, R. U. National inventory of
alkylphenol ethoxylate compounds in U.S. sewage sludges and
chemical fate in outdoor soil mesocosms. Environ. Pollut. 2013,174,
189−193.
(17) McClellan, K.; Halden, R. U. Pharmaceuticals and personal care
products in archived US biosolids from the 2001 EPA national sewage
sludge survey. Water Res. 2010,44 (2), 658−668.
(18) Kolpin, D. W.; Furlong, E. T.; Meyer, M. T.; Thurman, E. M.;
Zaugg, S. D.; Barber, L. B.; Buxton, H. T. Pharmaceuticals, hormones,
and other organic wastewater contaminants in U.S.Stream, 1999−
2000: A national reconnaissance. Environ. Sci. Technol. 2002,36 (6),
1202−1211.
(19) Snyder, S. A.; Leising, J.; Westerhoff, P.; Yoon, Y.; Mash, H.;
Vanderford, B. Biological and physical attenuation of endocrine
pisruptors and pharmaceuticals: Implications for water reuse. Ground
Water Monitor R. 2004,24 (2), 108−118.
(20) Snyder, S. A.; Westerhoff, P.; Yoon, Y.; Sedlak, D. L.
Pharmaceuticals, personal care products, and endocrine disruptors in
water: Implications for the water industry. Environ. Eng. Sci. 2003,20
(5), 449−469.
(21) Westerhoff, P.; Yoon, Y.; Snyder, S.; Wert, E. Fate of endocrine-
disruptor, pharmaceutical, and personal care product chemicals during
simulated drinking water treatment processes. Environ. Sci. Technol.
2005,39 (17), 6649−6663.
(22) Kaegi, R.; Voegelin, A.; Sinnet, B.; Zuleeg, S.; Hagendorfer, H.;
Burkhardt, M.; Siegrist, H. Behavior of metallic silver nanoparticles in a
pilot wastewater treatment plant. Environ. Sci. Technol. 2011,45 (9),
3902−3908.
(23) Kiser, M. A.; Ladner, D.; Hristovski, K. D.; Westerhoff, P.
Nanomaterial transformation and association with fresh and freeze-
dried wastewater activated sludge: Implications for testing protocol
and environmental fate. Environ. Sci. Technol. 2012,46, 7046−7053.
(24) Wang, Y.; Westerhoff, P.; Hristovski, K. D. Fate and biological
effects of silver, titanium dioxide, and C60 (fullerene) nanomaterials
during simulated wastewater treatment processes. J. Hazard.Mater.
2012,201−202,16−22.
(25) Gottschalk, F.; Sonderer, T.; Scholz, R. W.; Nowack, B.
Modeled environmental concentrations of engineered nanomaterials
(TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ. Sci.
Technol. 2009,43 (24), 9216−9222.
(26) Lombi, E.; Nowack, B.; Baun, A.; McGrath, S. P. Evidence for
effects of manufactured nanomaterials on crops is inconclusive. Proc.
Natl. Acad. Sci. U. S. A. 2012,109 (49), E3336−E3336.
(27) Hernandez-Viezcas, J. A.; Castillo-Michel, H.; Andrews, J. C.;
Cotte, M.; Rico, C.; Peralta-Videa, J. R.; Ge, Y.; Priester, J. H.; Holden,
P. A.; Gardea-Torresdey, J. L. In situ synchrotron X-ray fluorescence
mapping and speciation of CeO2and ZnO Nanoparticles in soil
cultivated soybean (Glycine max). ACS Nano 2013,7(2), 1415−1423.
(28) Priester, J. H.; Ge, Y.; Mielke, R. E.; Horst, A. M.; Moritz, S. C.;
Espinosa, K.; Gelb, J.; Walker, S. L.; Nisbet, R. M.; An, Y. J.; Schimel, J.
P.; Palmer, R. G.; Hernandez-Viezcas, J. A.; Zhao, L. J.; Gardea-
Torresdey, J. L.; Holden, P. A. Soybean susceptibility to manufactured
nanomaterials with evidence for food quality and soil fertility
interruption. Proc. Natl. Acad. Sci. U. S. A. 2012,109 (37), E2451−
E2456.
(29) Colman, B. P.; Arnaout, C. L.; Anciaux, S.; Gunsch, C. K.;
Hochella, M. F.; Kim, B.; Lowry, G. V.; McGill, B. M.; Reinsch, B. C.;
Richardson, C. J.; Unrine, J. M.; Wright, J. P.; Yin, L. Y.; Bernhardt, E.
S., Low concentrations of silver nanoparticles in biosolids cause
adverse ecosystem responses under realistic field scenario. PLoS One
2013,8, (2).
(30) Judy, J. D.; Unrine, J. M.; Bertsch, P. M. Evidence for
biomagnification of gold nanoparticles within a terrestrial food chain.
Environ. Sci. Technol. 2011,45 (2), 776−781.
(31) Wu, F. C.; Mu, Y. S.; Chang, H.; Zhao, X. L.; Giesy, J. P.; Wu, K.
B. Predicting water quality criteria for protecting aquatic life from
physicochemical properties of metals or metalloids. Environ. Sci.
Technol. 2013,47 (1), 446−453.
(32) McLaughlin, M. J.; Whatmuff, M.; Warne, M.; Heemsbergen,
D.; Barry, G.; Bell, M.; Nash, D.; Pritchard, D. A field investigation of
solubility and food chain accumulation of biosolid-cadmium across
diverse soil types. Environ. Chem. 2006,3(6), 428−432.
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9486

(33) Oliver, I. W.; Hass, A.; Merrington, G.; Fine, P.; McLaughlin, M.
J. Copper availability in seven Israeli soils incubated with and without
biosolids. J. Environ. Qual. 2005,34 (2), 508−513.
(34) Mantovi, P.; Baldoni, G.; Toderi, G. Reuse of liquid, dewatered,
and composted sewage sludge on agricultural land: Effects of long-
term application on soil and crop. Water Res. 2005,39 (2−3), 289−
296.
(35) Stevens, R., U.S. EPA’s 2006−2007 Targeted National Sewage
Sludge Survey. In Contaminants of Emerging Concern in the Environ-
ment: Ecological and Human Health Considerations; Halden, R. U., Ed.;
American Chemical Society: Washington, DC, 2010; pp 173−198.
(36) Sanchez-Monedero, M. A.; Mondini, C.; de Nobili, M.; Leita, L.;
Roig, A. Land application of biosolids. Soil response to different
stabilization degree of the treated organic matter. Waste Manage 2004,
24 (4), 325−332.
(37) Park, J. H.; Lamb, D.; Paneerselvam, P.; Choppala, G.; Bolan,
N.; Chung, J. W. Role of organic amendments on enhanced
bioremediation of heavy metal(loid) contaminated soils. J. Hazard.
Mater. 2011,185 (2−3), 549−574.
(38) Furr, A. K.; Lawrence, A. W.; Tong, S. S. C.; Grandolfo, M. C.;
Hofstader, R. A.; Bache, C. A.; Gutenmann, W. H.; Lisk, D. J.
Multielement and chlorinated hydrocarbon analysis of municipal sewer
sludges of American cities. Environ. Sci. Technol. 1976,10 (7), 683−
687.
(39) Spinosa, L. From sludge to resources through biosolids. Water
Sci. Technol. 2004,50 (9), 1−8.
(40) Rittmann, B. E.; Lee, H. S.; Zhang, H. S.; Alder, J.; Banaszak, J.
E.; Lopez, R. Full-scale application of focused-pulsed pre-treatment for
improving biosolids digestion and conversion to methane. Water Sci.
Technol. 2008,58 (10), 1895−1901.
(41) Bridle, T. R.; Pritchard, D. Energy and nutrient recovery from
sewage sludge via pyrolysis. Water Sci. Technol. 2004,50 (9), 169−175.
(42) Cogger, C. G.; Sullivan, D. M.; Bary, A. I.; Kropf, J. A. Matching
plant-available nitrogen from biosolids with dryland wheat needs. J.
Prod. Agric. 1998,11 (1), 41−47.
(43) McBride, M. B. Toxic metal accumulation from agricultural use
of sludgeAre USEPA regulations protective. J. Environ. Qual. 1995,
24 (1), 5−18.
(44) Dowdy, R. H.; Latterell, J. J.; Hinesly, T. D.; Grossman, R. B.;
Sullivan, D. L. Trace-metal movement in an aeric ochraqualf following
14 years of annual sludge application. J. Environ. Qual. 1991,20 (1),
119−123.
(45) Chang, A. C.; Page, A. L.; Warneke, J. E.; Resketo, M. R.; Jones,
T. E. Accumulation of camium and zinc in barley grown on sludge-
treated soilsA long-term field study. J. Environ. Qual. 1983,12 (3),
391−397.
(46) Emmerich, W. E.; Lund, L. J.; Page, A. L.; Chang, A. C.
Movement of heavy-metals in sewage treated soils. J. Environ. Qual.
1982,11 (2), 174−178.
(47) Beckett, P. H. T.; Davis, R. D. Additivity of toxic effects of Cu,
Ni, and Zn in young barley. New Phytol. 1978,81 (1), 155−173.
(48) Le Corre, K. S.; Valsami-Jones, E.; Hobbs, P.; Parsons, S. A.
Phosphorus recovery from wastewater by struvite crystallization: A
review. Crit. Rev. Environ. Sci. Technol. 2009,39 (6), 433−477.
(49) Shu, L.; Schneider, P.; Jegatheesan, V.; Johnson, J. An economic
evaluation of phosphorus recovery as struvite from digester super-
natant. Bioresour. Technol. 2006,97 (17), 2211−2216.
(50) de-Bashan, L. E.; Bashan, Y. Recent advances in removing
phosphorus from wastewater and its future use as fertilizer (1997−
2003). Water Res. 2004,38 (19), 4222−4246.
(51) Doyle, J. D.; Parsons, S. A. Struvite formation, control and
recovery. Water Res. 2002,36 (16), 3925−3940.
(52) Rittmann, B. E.; Mayer, B.; Westerhoff, P.; Edwards, M.
Capturing the lost phosphorus. Chemosphere 2011,84 (6), 846−853.
(53) Driver, J.; Lijmbach, D.; Steen, I. Why recover phosphorus for
recycling, and how? Environ. Technol. 1999,20 (7), 651−662.
(54) Meunier, N.; Drogui, P.; Gourvenec, C.; Mercier, G.; Hausler,
R.; Blais, J. F. Removal of metals in leachate from sewage sludge using
electrochemical technology. Environ. Technol. 2004,25 (2), 235−245.
(55) Sloan, J. J.; Dowdy, R. H.; Dolan, M. S. Recovery of biosolids-
applied heavy metals sixteen years after application. J. Environ. Qual.
1998,27 (6), 1312−1317.
(56) Pathak, A.; Dastidar, M. G.; Sreekrishnan, T. R. Bioleaching of
heavy metals from sewage sludge: A review. J. Environ. Manage. 2009,
90 (8), 2343−2353.
(57) Meunier, N.; Blais, J. F.; Lounes, M.; Tyagi, R. D.; Sasseville, J.
L. Different options for metal recovery after sludge decontamination at
the Montreal Urban Community wastewater treatment plant. Water
Sci. Technol. 2002,46 (10), 33−41.
(58) Leung, W. C.; Wong, M. F.; Chua, H.; Lo, W.; Yu, P. H. F.;
Leung, C. K. Removal and recovery of heavy metals by bacteria
isolated from activated sludge treating industrial effluents and
municipal wastewater. Water Sci. Technol. 2000,41 (12), 233−240.
(59) Jainae, K.; Sanuwong, K.; Nuangjamnong, J.; Sukpirom, N.;
Unob, F. Extraction and recovery of precious metal ions in wastewater
by polystyrene-coated magnetic particles functionalized with 2-(3-(2-
aminoethylthio)propylthio)ethanamine. Chem. Eng. J. 2010,160 (2),
586−593.
(60) Al-Enezi, G.; Hamoda, M. F.; Fawzi, N. Ion exchange extraction
of heavy metals from wastewater sludges. J. Environ. Sci. Health, Part A:
Toxic/Hazard. Subst. Environ. Eng. 2004,39 (2), 455−464.
(61) Lottermoser, B. G. Nobel-metals in municipal sewage sludges of
southeastern Australia. Ambio 1995,24 (6), 354−357.
(62) Reeves, S. J.; Plimer, I. R. Exploitation of gold in a historic
sewage sludge stockpile, Werribee, Australia: Resource evaluation,
chemical extraction and subsequent utilisation sludgeReply. J.
Geochem. Explor. 2001,72 (1), 77−79.
(63) Jackson, M. T.; Prichard, H. M.; Sampson, J. Platinum-group
elements in sewage sludge and incinerator ash in the United Kingdom:
Assessment of PGE sources and mobility in cities. Sci. Total Environ.
2010,408 (6), 1276−1285.
(64) USEPA Targeted National Sewage Sludge Survey Statistical
Analysis Report; US Environmental Protection Agency, April 2009,
2009; p 58.
(65) Venkatesan, A. K.; Done, H.; Halden, R. U. United States
National Sewage Sludge Repository at Arizona State UniversityA
new resource and research tool for environmental scientists, engineers,
and epidemiologists. Environ. Sci. Pollut. Res. 2014,1−10.
(66) APHA; AWWA; WEF. Standard Methods for the Examination of
Water And Wastewater, 21st ed.; American Public Health Association:
Washington, DC, 2005.
(67) Burton, E. D.; Hawker, D. W.; Redding, M. R. Estimating sludge
loadings to land based on trace metal sorption in soil: Effect of
dissolved organo-metallic complexes. Water Res. 2003,37 (6), 1394−
1400.
(68) Khai, N. M.; Oborn, I.; Hillier, S.; Gustafsson, J. P. Modeling of
metal binding in tropical Fluvisols and Acrisols treated with biosolids
and wastewater. Chemosphere 2008,70 (8), 1338−1346.
(69) Oliver, I. W.; Merrington, G.; McLaughlin, M. J. Copper
partitioning among mineral and organic fractions in biosolids. Environ.
Chem. 2006,3(1), 48−52.
(70) Fard, R. F.; Azimi, A. A.; Bidhendi, G. R. N. Batch kinetics and
isotherms for biosorption of cadmium onto biosolids. Desali. and
Water Treat. 2011,28 (1−3), 69−74.
(71) Hammaini, A.; Gonzalez, F.; Ballester, A.; Blazquez, M. L.;
Munoz, J. A. Biosorption of heavy metals by activated sludge and their
desorption characteristics. J. Environ. Manage. 2007,84 (4), 419−426.
(72) Hawari, A. H.; Mulligan, C. N. Biosorption of lead(II),
cadmium(II), copper(II) and nickel(II) by anaerobic granular biomass.
Bioresour. Technol. 2006,97 (4), 692−700.
(73) Liu, Y.; Lam, M. C.; Fang, H. H. P. Adsorption of heavy metals
by EPS of activated sludge. Water Sci. Technol. 2001,43 (6), 59−66.
(74) Hem, J. D. Study and Interpretation of the Chemical Character-
istics of Natural Water; US Geological Survey: Washington, DC, 1992;
p 263.
(75) USEPA. Targeted National Sewage Sludge Survey Sampling and
Analysis Technical Report-Overview; U.S. Environmental Protection
Agency: Washington, DC, 2009; p 79.
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9487

(76) Krueger, O.; Grabner, A.; Adam, C. Complete survey of German
sewage sludge ash. Environ. Sci. Technol. 2014,48 (20), 11811−11818.
(77) Rudnick, R.; Gao, S. Composition of the continental crust.
Treatise Geochem. 2003,3,1−64.
(78) Taylor, S. R.; McLennan, S. M. The geochemical evolution of
the continental-crust. Rev. Geophys. 1995,33 (2), 241−265.
(79) Upadhyay, N.; Clements, A.; Fraser, M.; Herckes, P. Chemical
Speciation of PM2.5 and PM10 in South Phoenix, AZ. J. Air Waste
Manage. Assoc. 2011,61 (3), 302−310.
(80) Rabiet, M.; Brissaud, F.; Seidel, J. L.; Pistre, S.; Elbaz-Poulichet,
F. Positive gadolinium anomalies in wastewater treatment plant
effluents and aquatic environment in the Herault watershed (South
France). Chemosphere 2009,75 (8), 1057−1064.
(81) Verplanck, P. L.; Taylor, H. E.; Nordstrom, D. K.; Barber, L. B.
Aqueous stability of gadolinium in surface waters receiving sewage
treatment plant effluent, Boulder Creek, Colorado. Environ. Sci.
Technol. 2005,39 (18), 6923−6929.
(82) Kummerer, K. Drugs in the environment: Emission of drugs,
diagnostic aids and disinfectants into wastewater by hospitals in
relation to other sourcesA review. Chemosphere 2001,45 (6−7),
957−969.
(83) Hermann, P.; Kotek, J.; Kubicek, V.; Lukes, I. Gadolinium(III)
complexes as MRI contrast agents: Ligand design and properties of the
complexes. Dalton Transactions 2008,23, 3027−3047.
(84) Viswanathan, S.; Kovacs, Z.; Green, K. N.; Ratnakar, S. J.;
Sherry, A. D. Alternatives to gadolinium-based metal chelates for
magnetic resonance imaging. Chem. Rev. 2010,110 (5), 2960−3018.
(85) Ravindra, K.; Bencs, L.; Van Grieken, R. Platinum group
elements in the environment and their health risk. Sci. Total Environ.
2004,318 (1−3), 1−43.
(86) Weir, A.; Westerhoff, P.; Fabricius, L.; Hristovski, K.; von Goetz,
N. Titanium dioxide nanoparticles in food and personal care products.
Environ. Sci. Technol. 2012,46 (4), 2242−2250.
(87) Yang, Y.; Doudrick, K.; Bi, X. Y.; Hristovski, K.; Herckes, P.;
Westerhoff, P.; Kaegi, R. Characterization of food-grade titanium
dioxide: The presence of nanosized particles. Environ. Sci. Technol.
2014,48 (11), 6391−6400.
(88) Bauer, H.; Schimmel, G.; Jurges, P. The evolution of detergent
builders from phosphates to zeolites to silicates. Tenside, Surfactants,
Deterg. 1999,36 (4), 225−229.
(89) Fruijtier-Polloth, C. The safety of synthetic zeolites used in
detergents. Arch. Toxicol. 2009,83 (1), 23−35.
(90) Dickinson, E. Use of nanoparticles and microparticles in the
formation and stabilization of food emulsions. Trends Food Sci.
Technol. 2012,24 (1), 4−12.
(91) Szakal, C.; Roberts, S. M.; Westerhoff, P.; Bartholomaeus, A.;
Buck, N.; Illuminato, I.; Canady, R.; Rogers, M. Measurement of
nanomaterials in foods: Integrative consideration of challenges and
future prospects. ACS Nano 2014,8(4), 3128−3135.
(92) Kaegi, R.; Voegelin, A.; Ort, C.; Sinnet, B.; Thalmann, B.;
Krismer, J.; Hagendorfer, H.; Elumelu, M.; Mueller, E. Fate and
transformation of silver nanoparticles in urban wastewater systems.
Water Res. 2013,47 (12), 3866−3877.
(93) Song, Y.; Fitch, M.; Burken, J.; Nass, L.; Chilukiri, S.; Gale, N.;
Ross, C. Lead and zinc removal by laboratory-scale constructed
wetlands. Water Environ. Res. 2001,73 (1), 37−44.
(94) Thalmann, B.; Voegelin, A.; Sinnet, B.; Morgenroth, E.; Kaegi,
R. Sulfidation kinetics of silver nanoparticles reacted with metal
sulfides. Environ. Sci. Technol. 2014,48 (9), 4885−4892.
(95) Kaegi, R.; Voegelin, A.; Zuleeg, S.; Sinnet, B.; Eugster, J.;
Burkhardt, M.; Siegrist, H. Behavior of silver nanoparticles in a waste
water treatment plant. Geochim. Cosmochim. Acta 2010,74 (12),
A488−A488.
(96) Ebrahimzadeh, H.; Tavassoli, N.; Amini, M. M.; Fazaeli, Y.;
Abedi, H. Determination of very low levels of gold and palladium in
wastewater and soil samples by atomic absorption after preconcentra-
tion on modified MCM-48 and MCM-41 silica. Talanta 2010,81 (4−
5), 1183−1188.
(97) Ek, K. H.; Morrison, G. M.; Rauch, S. Environmental routes for
platinum group elements to biological materialsA review. Sci. Total
Environ. 2004,334,21−38.
(98) Rauch, S.; Morrison, G. M. Environmental relevance of the
platinum-group elements. Elements 2008,4(4), 259−263.
(99) Whiteley, J. D.; Murray, F. Autocatalyst-derived platinum,
palladium and rhodium (PGE) in infiltration basin and wetland
sediments receiving urban runoff. Sci. Total Environ. 2005,341 (1−3),
199−209.
(100) Arican, B.; Gokcay, C. F.; Yetis, U. Mechanistics of nickel
sorption by activated sludge. Process Biochem. 2002,37 (11), 1307−
1315.
(101) Kempton, S.; Sterritt, R. M.; Lester, J. N. Factors affecting the
fate and behavior of toxic elements in the activated sludge process.
Environ. Pollut., Ser. A 1983,32 (1), 51−78.
(102) Lawson, P. S.; Sterritt, R. M.; Lester, J. N. Adsorption and
Complexation Mechanisms of Heavy-Metal Uptake in Activated
Sludge. J. Chem. Technol. Biotechnol., Biotechnol. 1984,34 (4), 253−
262.
(103) Lawson, P. S.; Sterritt, R. M.; Lester, J. N. Factors affecting the
removal of metals during activated sludge wastewater treatment 1. The
role of soluble ligands. Arch. Environ. Contam. Toxicol. 1984,13 (4),
383−390.
(104) McKay, G.; Ho, Y. S.; Ng, J. C. Y. Biosorption of copper from
waste waters: A review. Sep. Purif. Methods 1999,28 (1), 87−125.
(105) Sterritt, R. M.; Lester, J. N. Significance and behavior of heavy-
metals in wastewater treatment processes 3. Speciation in waste-waters
and related complex matrices. Sci. Total Environ. 1984,34 (1−2),
117−141.
(106) Vaiopoulou, E.; Gikas, P. Effects of chromium on activated
sludge and on the performance of wastewater treatment plants: A
review. Water Res. 2012,46 (3), 549−570.
(107) Santos, A.; Judd, S. The fate of metals in wastewater treated by
the activated sludge process and membrane bioreactors: A brief review.
J. Environ. Monit. 2010,12 (1), 110−118.
(108) USEPA. Biosolids Generation, Use, and Disposal in the United
States; Washington DC, 1999.
(109) Gomez, A.; Zubizarreta, J.; Rodrigues, M.; Dopazo, C.; Fueyo,
N. Potential and cost of electricity generation from human and animal
waste in Spain. Renewable Energy 2010,35 (2), 498−505.
(110) Roy, M. M.; Dutta, A.; Corscadden, K.; Havard, P.; Dickie, L.
Review of biosolids management options and co-incineration of a
biosolid-derived fuel. Waste Manage 2011,31 (11), 2228−2235.
(111) USDOE. Critical Materials Strategy; U.S. Department of
Energy, 2011; p 196.
(112) Chen, W.-Q.; Graedel, T. E. Anthropogenic cycles of the
elements: A critical review. Environ. Sci. Technol. 2012,46 (16), 8574−
8586.
(113) Du, X.; Graedel, T. E., Uncovering the global life cycles of the
rare earth elements. Sci. Rep. 2011,1.
(114) Heidler, J.; Sapkota, A.; Halden, R. U. Partitioning, persistence,
and accumulation in digested sludge of the topical antiseptic
triclocarban during wastewater treatment. Environ. Sci. Technol. 2006,
40 (11), 3634−3639.
(115) Higgins, C. P.; Paesani, Z. J.; Chalew, T. E. A.; Halden, R. U.
Bioaccumulation of triclocarban in Lumbriculus variegatus.Environ.
Toxicol. Chem. 2009,28 (12), 2580−2586.
■NOTE ADDED AFTER ASAP PUBLICATION
This article published January 26, 2015 with errors throughout
the text. The corrected version published January 27, 2015.
Environmental Science & Technology Article
DOI: 10.1021/es505329q
Environ. Sci. Technol. 2015, 49, 9479−9488
9488